Purinergic Signalling

, Volume 10, Issue 1, pp 157–187 | Cite as

Purinergic signalling in the reproductive system in health and disease

Review Article

Abstract

There are multiple roles for purinergic signalling in both male and female reproductive organs. ATP, released as a cotransmitter with noradrenaline from sympathetic nerves, contracts smooth muscle via P2X1 receptors in vas deferens, seminal vesicles, prostate and uterus, as well as in blood vessels. Male infertility occurs in P2X1 receptor knockout mice. Both short- and long-term trophic purinergic signalling occurs in reproductive organs. Purinergic signalling is involved in hormone secretion, penile erection, sperm motility and capacitation, and mucous production. Changes in purinoceptor expression occur in pathophysiological conditions, including pre-eclampsia, cancer and pain.

Keywords

Vas deferens Testes Penile erection Ovary Uterus Placenta 

References

  1. 1.
    Abdel-Hamid IA, Jannini EA, Andersson KE (2009) Premature ejaculation: focus on therapeutic targets. Expert Opin Ther Targets 13:175–193PubMedGoogle Scholar
  2. 2.
    Acevedo CG, Rojas S, Ramirez M, Bravo I (1995) Transport and metabolism of adenosine in the perfused human placenta. Placenta 16:611–622PubMedGoogle Scholar
  3. 3.
    Acevedo CG, Huambachano A, Perez E, Rojas S, Bravo I, Contreras E (1997) Effect of ethanol on human placental transport and metabolism of adenosine. Placenta 18:387–392PubMedGoogle Scholar
  4. 4.
    Aitken H, Poyser NL, Hollingsworth M (2001) The effects of P2Y receptor agonists and adenosine on prostaglandin production by the guinea-pig uterus. Br J Pharmacol 132:709–721PubMedCentralPubMedGoogle Scholar
  5. 5.
    Aleu J, Martin-Satue M, Navarro P, Perez dL I, Bahima L, Marsal J, Solsona C (2003) Release of ATP induced by hypertonic solutions in Xenopus oocytes. J Physiol 547:209–219PubMedCentralPubMedGoogle Scholar
  6. 6.
    Alexander SP, Cooper J, Shine J, Hill SJ (1996) Characterization of the human brain putative A2B adenosine receptor expressed in Chinese hamster ovary (CHO.A2B4) cells. Br J Pharmacol 119:1286–1290PubMedCentralPubMedGoogle Scholar
  7. 7.
    Aliagas E, Torrejón-Escribano B, Lavoie EG, Gómez de Aranda I, Sévigny J, Solsona C, Martín-Satué M (2010) Changes in expression and activity levels of ecto-5′-nucleotidase/CD73 along the mouse female estrous cycle. Acta Physiol (Oxf) 199:191–197Google Scholar
  8. 8.
    Aliagas E, Vidal A, Torrejón-Escribano B, Taco MR, Ponce J, de Aranda I, Sévigny J, Condom E, Martín-Satué M (2013) Ecto-nucleotidases distribution in human cyclic and postmenopausic endometrium. Purinergic Signal 9:227–237PubMedCentralPubMedGoogle Scholar
  9. 9.
    Allcorn RJ, Cunnane TC, Kirkpatrick K (1986) Actions of α, β-methylene ATP and 6-hydroxydopamine on sympathetic neurotransmission in the vas deferens of the guinea-pig, rat and mouse: support for cotransmission. Br J Pharmacol 89:647–659PubMedCentralPubMedGoogle Scholar
  10. 10.
    Allegrucci C, Liguori L, Mezzasoma I, Minelli A (2000) A1 adenosine receptor in human spermatozoa: its role in the fertilization process. Mol Genet Metab 71:381–386PubMedGoogle Scholar
  11. 11.
    Alm P (1982) On the autonomic innervation of the human vas deferens. Brain Res Bull 9:673–677PubMedGoogle Scholar
  12. 12.
    Amobi N, Smith IC (1987) Effects of α, β-methylene ATP on biphasic responses of rat vas deferens. Eur J Pharmacol 133:75–82PubMedGoogle Scholar
  13. 13.
    Amobi NI, Guillebaud J, Smith IC (2012) Perspective on the role of P2X-purinoceptor activation in human vas deferens contractility. Exp Physiol 97:583–602PubMedGoogle Scholar
  14. 14.
    Andersson KE, Wagner G (1995) Physiology of penile erection. Physiol Rev 75:191–236PubMedGoogle Scholar
  15. 15.
    Andersson KE, Chapple CR, Höfner K (2002) Future drugs for the treatment of benign prostatic hyperplasia. World J Urol 19:436–442PubMedGoogle Scholar
  16. 16.
    Anton PG, McGrath JC (1977) Further evidence for adrenergic transmission in the human vas deferens. J Physiol 273:45–55PubMedCentralPubMedGoogle Scholar
  17. 17.
    Antonio LS, Costa RR, Gomes MD, Varanda WA (2009) Mouse Leydig cells express multiple P2X receptor subunits. Purinergic Signal 5:277–287PubMedCentralPubMedGoogle Scholar
  18. 18.
    Arase T, Uchida H, Kajitani T, Ono M, Tamaki K, Oda H, Nishikawa S, Kagami M, Nagashima T, Masuda H, Asada H, Yoshimura Y, Maruyama T (2009) The UDP-glucose receptor P2RY14 triggers innate mucosal immunity in the female reproductive tract by inducing IL-8. J Immunol 182:7074–7084PubMedGoogle Scholar
  19. 19.
    Arellano RO, Garay E, Vázquez-Cuevas F (2009) Functional interaction between native G protein-coupled purinergic receptors in Xenopus follicles. Proc Natl Acad Sci U S A 106:16680–16685PubMedCentralPubMedGoogle Scholar
  20. 20.
    Auzanneau C, Norez C, Noel S, Jougla C, Becq F, Vandebrouck C (2006) Pharmacological profile of inhibition of the chloride channels activated by extracellular acid in cultured rat Sertoli cells. Reprod Nutr Dev 46:241–255PubMedGoogle Scholar
  21. 21.
    Azevedo I, Osswald W (1992) Does adenosine malfunction play a role in hypertension? Pharmacol Res 25:227–236PubMedGoogle Scholar
  22. 22.
    Banks F, Knight G, Calvert RC, Thompson CS, Mikhailidis DP, Morgan R, Burnstock G (2006) The purinergic component of human vas deferens contraction. Fertil Steril 85:932–939PubMedGoogle Scholar
  23. 23.
    Banks FCL, Knight GE, Calvert RC, Turmaine M, Thompson CS, Mikhailidis DP, Morgan RJ, Burnstock G (2006) Smooth muscle and purinergic contraction of the human, rabbit, rat, and mouse testicular capsule. Biol Reprod 74:473–480PubMedGoogle Scholar
  24. 24.
    Banks FCL, Calvert RC, Burnstock G (2010) Changing P2X receptor expression on maturing sperm in the epididymides of mice, hamsters, rats and man. Fertil Steril 93:1415–1420PubMedGoogle Scholar
  25. 25.
    Bar J, Orvieto R, Lahav J, Hod M, Kaplan B, Fisch B (2004) Effect of urinary versus recombinant follicle-stimulating hormone on platelet function and other hemostatic variables in controlled ovarian hyperstimulation. Fertil Steril 82:1564–1569PubMedGoogle Scholar
  26. 26.
    Barbacci E, Filippini A, De Cesaris P, Ziparo E (1996) Identification and characterization of an ecto-ATPase activity in rat Sertoli cells. Biochem Biophys Res Commun 222:273–279PubMedGoogle Scholar
  27. 27.
    Barden JA, Cottee LJ, Bennett MR (1999) Vesicle-associated proteins and P2X receptor clusters at single sympathetic varicosities in mouse vas deferens. J Neurocytol 28:469–480PubMedGoogle Scholar
  28. 28.
    Bardini M, Lee HY, Burnstock G (2000) Distribution of P2X receptor subtypes in the rat female reproductive tract at late pro-oestrus/early oestrus. Cell Tissue Res 299:105–113PubMedGoogle Scholar
  29. 29.
    Barrera NP, Morales B, Villalón M (2004) Plasma and intracellular membrane inositol 1,4,5-trisphosphate receptors mediate the Ca2+ increase associated with the ATP-induced increase in ciliary beat frequency. Am J Physiol Cell Physiol 287:C1114–C1124PubMedGoogle Scholar
  30. 30.
    Barrera NP, Morales B, Villalón M (2007) ATP and adenosine trigger the interaction of plasma membrane IP3 receptors with protein kinase A in oviductal ciliated cells. Biochem Biophys Res Commun 364:815–821PubMedGoogle Scholar
  31. 31.
    Behrman HR, Hall AK, Preston SL, Gore SD (1982) Antagonistic interactions of adenosine and prostaglandin F modulate acute responses of luteal cells to luteinizing hormone. Endocrinology 110:38–46PubMedGoogle Scholar
  32. 32.
    Behrman HR, Polan ML, Ohkawa R, Laufer N, Luborsky JL, Williams AT, Gore SD (1983) Purine modulation of LH action in gonadal cells. J Steroid Biochem 19:789–793PubMedGoogle Scholar
  33. 33.
    Belleannée C, Da Silva N, Shum WW, Brown D, Breton S (2010) Role of purinergic signaling pathways in V-ATPase recruitment to apical membrane of acidifying epididymal clear cells. Am J Physiol Cell Physiol 298:C817–C830PubMedCentralPubMedGoogle Scholar
  34. 34.
    Bennett MR, Gibson WG (1995) On the contribution of quantal secretion from close-contact and loose-contact varicosities to the synaptic potentials in the vas deferens. Philos Trans R Soc Lond B Biol Sci 347:187–204PubMedGoogle Scholar
  35. 35.
    Bevan JA (1984) The γ-connection’: are we ready to throw out the α-adrenoceptor in sympathetic vasoconstriction? Trends Pharmacol Sci 5:53–55Google Scholar
  36. 36.
    Billig H, Rosberg S (1986) Gonadotropin depression of adenosine triphosphate levels and interaction with adenosine in rat granulosa cells. Endocrinology 118:645–652PubMedGoogle Scholar
  37. 37.
    Billig H, Thelander H, Rosberg S (1988) Adenosine receptor-mediated effects by nonmetabolizable adenosine analogs in preovulatory rat granulosa cells: a putative local regulatory role of adenosine in the ovary. Endocrinology 122:52–61PubMedGoogle Scholar
  38. 38.
    Birmingham AT (1968) The human isolated vas deferens: its response to electrical stimulation and to drugs. Br J Pharmacol 34:692P–693PPubMedCentralPubMedGoogle Scholar
  39. 39.
    Blackburn MR, Wakamiya M, Caskey CT, Kellems RE (1995) Tissue-specific rescue suggests that placental adenosine deaminase is important for fetal development in mice. J Biol Chem 270:23891–23894PubMedGoogle Scholar
  40. 40.
    Blackburn MR, Wubah JA, Chunn JL, Thompson LF, Knudsen TB (1999) Transitory expression of the A2b adenosine receptor during implantation chamber development. Dev Dyn 216:127–136PubMedGoogle Scholar
  41. 41.
    Blakeley AG, Cunnane TC (1979) The packeted release of transmitter from the sympathetic nerves of the guinea-pig vas deferens: an electrophysiological study. J Physiol 296:85–96PubMedCentralPubMedGoogle Scholar
  42. 42.
    Blanco JM, Long JA, Gee G, Wildt DE, Donoghue AM (2012) Comparative cryopreservation of avian spermatozoa: effects of freezing and thawing rates on turkey and sandhill crane sperm cryosurvival. Anim Reprod Sci 131:1–8PubMedGoogle Scholar
  43. 43.
    Blaug S, Rymer J, Jalickee S, Miller SS (2003) P2 purinoceptors regulate calcium-activated chloride and fluid transport in 31EG4 mammary epithelia. Am J Physiol Cell Physiol 284:C897–C909PubMedGoogle Scholar
  44. 44.
    Bo X, Zhang Y, Nassar M, Burnstock G, Schoepfer R (1995) A P2X purinoceptor cDNA conferring a novel pharmacological profile. FEBS Lett 375:129–133PubMedGoogle Scholar
  45. 45.
    Bo X, Sexton A, Xiang Z, Nori SL, Burnstock G (1998) Pharmacological and histochemical evidence for P2X receptors in human umbilical vessels. Eur J Pharmacol 353:59–65PubMedGoogle Scholar
  46. 46.
    Bodas E, Aleu J, Pujol G, Martin-Satue M, Marsal J, Solsona C (2000) ATP crossing the cell plasma membrane generates an ionic current in Xenopus oocytes. J Biol Chem 275:20268–20273PubMedGoogle Scholar
  47. 47.
    Boland B, Himpens B, Vincent MF, Gillis JM, Casteels R (1992) ATP activates P2x-contracting and P2y-relaxing purinoceptors in the smooth muscle of mouse vas deferens. Br J Pharmacol 107:1152–1158PubMedCentralPubMedGoogle Scholar
  48. 48.
    Boryshpolets S, Dzyuba B, Rodina M, Li P, Hulak M, Gela D, Linhart O (2009) Freeze-thawing as the factor of spontaneous activation of spermatozoa motility in common carp (Cyprinus carpio L.). Cryobiology 59:291–296PubMedGoogle Scholar
  49. 49.
    Boselli C, Govoni S (2000) Alcohol differentially affects noradrenergic and purinergic responses in the bisected rat vas deferens. Alcohol 22:91–96PubMedGoogle Scholar
  50. 50.
    Bowman A, Gillespie JS (1983) Neurogenic vasodilatation in isolated bovine and canine penile arteries. J Physiol 341:603–616PubMedCentralPubMedGoogle Scholar
  51. 51.
    Brain KL, Trout SJ, Jackson VM, Dass N, Cunnane TC (2001) Nicotine induces calcium spikes in single nerve terminal varicosities: a role for intracellular calcium stores. Neuroscience 106:395–403PubMedGoogle Scholar
  52. 52.
    Breton S, Smith PJS, Lui B, Brown D (1996) Acidification of the male reproductive tract by a proton pumping (H+)-ATPase. Nat Med 2:470–472PubMedGoogle Scholar
  53. 53.
    Brock JA, Cunnane TC (1987) Relationship between the nerve action potential and transmitter release from sympathetic postganglionic nerve terminals. Nature 326:605–607PubMedGoogle Scholar
  54. 54.
    Brunette MG, Bastani B, Leclerc M, Narbaitz R (1995) Detection of different adenosine triphosphatases in human placental brush border membranes. J Membr Biol 145:285–293PubMedGoogle Scholar
  55. 55.
    Bülbring E, Casteels R, Kuriyama H (1968) Membrane potential and ion content in cat and guinea-pig myometrium and the response to adrenaline and noradrenaline. Br J Pharmacol 34:388–407PubMedCentralPubMedGoogle Scholar
  56. 56.
    Buljubasich R, Ventura S (2004) Adenosine 5′-triphosphate and noradrenaline are excitatory cotransmitters to the fibromuscular stroma of the guinea pig prostate gland. Eur J Pharmacol 499:335–344PubMedGoogle Scholar
  57. 57.
    Bulloch JM, McGrath JC (1988) Blockade of vasopressor and vas deferens responses by α, β-methylene ATP in the pithed rat. Br J Pharmacol 94:103–108PubMedCentralPubMedGoogle Scholar
  58. 58.
    Bültmann R, Klebroff W, Starke K (1999) A contraction-mediating receptor for UTP, presumably P2Y2, in rat vas deferens. Naunyn Schmiedebergs Arch Pharmacol 360:196–201PubMedGoogle Scholar
  59. 59.
    Burns JK (1987) Relation between elevated serum 5-nucleotidase in late human pregnancy and duration of labour. Proc Physiol Soc Suppl:57PGoogle Scholar
  60. 60.
    Burnstock G (1997) Commentary on paper by S. Hukovic (1961) entitled “Responses of the isolated sympathetic nerve-ductus deferens preparation of the guinea-pig”. In: Birmingham AT, Brown DA (eds) Landmarks in pharmacology. Br. J. Pharmacol. (Golden Jubilee 1946–1996), pp 192–201Google Scholar
  61. 61.
    Burnstock G (1999) Release of vasoactive substances from endothelial cells by shear stress and purinergic mechanosensory transduction. J Anat 194:335–342PubMedCentralPubMedGoogle Scholar
  62. 62.
    Burnstock G, Di Virgilio F (2013) Purinergic signalling in cancer. Purinergic Signal [Epub ahead of print 25/6/13]Google Scholar
  63. 63.
    Burnstock G, Holman ME (1960) Autonomic nerve-smooth muscle transmission. Nature 187:951–952PubMedGoogle Scholar
  64. 64.
    Burnstock G, Holman ME (1961) The transmission of excitation from autonomic nerve to smooth muscle. J Physiol 155:115–133PubMedCentralPubMedGoogle Scholar
  65. 65.
    Burnstock G, Holman ME (1962) Spontaneous potentials at sympathetic nerve endings in smooth muscle. J Physiol 160:446–460PubMedCentralPubMedGoogle Scholar
  66. 66.
    Burnstock G, Novak I (2013) Purinergic signalling and diabetes. Purinergic Signal 9:307–324PubMedCentralPubMedGoogle Scholar
  67. 67.
    Burnstock G, Verkhratsky A (2010) Vas deferens — a model used to establish sympathetic cotransmission. Trends Pharmacol Sci 31:131–139PubMedGoogle Scholar
  68. 68.
    Burton LD, Housley GD, Salih SG, Järlebark L, Christie DL, Greenwood D (2000) P2X2 receptor expression by interstitial cells of Cajal in vas deferens implicated in semen emission. Auton Neurosci 84:147–161PubMedGoogle Scholar
  69. 69.
    Buvinic S, Poblete MI, Donoso MV, Delpiano AM, Briones R, Miranda R, Huidobro-Toro JP (2006) P2Y1 and P2Y2 receptor distribution varies along the human placental vascular tree: role of nucleotides in vascular tone regulation. J Physiol 573:427–443PubMedCentralPubMedGoogle Scholar
  70. 70.
    Calamera JC, Quirós MC, Brugo S, Nicholson RF, Vilar O (1986) Adenosine 5′-triphosphate (ATP) activity in normal and pathological human semen. Relationship with round cells of the ejaculate. Andrologia 18:214–219PubMedGoogle Scholar
  71. 71.
    Calamera JC, Buffone MG, Doncel GF, Brugo-Olmedo S, de Vincentiis S, Calamera MM, Storey BT, Alvarez JG (2010) Effect of thawing temperature on the motility recovery of cryopreserved human spermatozoa. Fertil Steril 93:789–794PubMedGoogle Scholar
  72. 72.
    Calvert RC, Khan MA, Thompson CS, Mikhailidis DP, Burnstock G (2008) A functional study of purinergic signalling in the normal and pathological rabbit corpus cavernosum. BJU Int 101:1043–1047PubMedGoogle Scholar
  73. 73.
    Casali EA, da Silva TR, Gelain DP, Kaiser GR, Battastini AM, Sarkis JJ, Bernard EA (2001) Ectonucleotidase activities in Sertoli cells from immature rats. Braz J Med Biol Res 34:1247–1256PubMedGoogle Scholar
  74. 74.
    Chan HC, Fu WO, Chung YW, Chan PS, Wong PY (1995) An ATP-activated cation conductance in human epididymal cells. Biol Reprod 52:645–652PubMedGoogle Scholar
  75. 75.
    Chan HC, Zhou WL, Wong PY (1995) Extracellular ATP activates both Ca2+- and cAMP-dependent Cl conductances in rat epididymal cells. J Membr Biol 147:185–193PubMedGoogle Scholar
  76. 76.
    Chang SJ, Wang TY, Lee YH, Tai CJ (2007) Extracellular ATP activates nuclear translocation of ERK1/2 leading to the induction of matrix metalloproteinases expression in human endometrial stromal cells. J Endocrinol 193:393–404PubMedGoogle Scholar
  77. 77.
    Chang SJ, Tzeng CR, Lee YH, Tai CJ (2008) Extracellular ATP activates the PLC/PKC/ERK signaling pathway through the P2Y2 purinergic receptor leading to the induction of early growth response 1 expression and the inhibition of viability in human endometrial stromal cells. Cell Signal 20:1248–1255PubMedGoogle Scholar
  78. 78.
    Chen L, He HY, Li HM, Zheng J, Heng WJ, You JF, Fang WG (2004) ERK1/2 and p38 pathways are required for P2Y receptor-mediated prostate cancer invasion. Cancer Lett 215:239–247PubMedGoogle Scholar
  79. 79.
    Chiang PH, Wu SN, Tsai EM, Wu CC, Shen MR, Huang CH, Chiang CP (1994) Adenosine modulation of neurotransmission in penile erection. Br J Clin Pharmacol 38:357–362PubMedCentralPubMedGoogle Scholar
  80. 80.
    Choi KC, Tai CJ, Tzeng CR, Auersperg N, Leung PC (2003) Adenosine triphosphate activates mitogen-activated protein kinase in pre-neoplastic and neoplastic ovarian surface epithelial cells. Biol Reprod 68:309–315PubMedGoogle Scholar
  81. 81.
    Christoforidis S, Papamarcaki T, Galaris D, Kellner R, Tsolas O (1995) Purification and properties of human placental ATP diphosphohydrolase. Eur J Biochem 234:66–74PubMedGoogle Scholar
  82. 82.
    Chuang YC, Chancellor MB (2006) The application of botulinum toxin in the prostate. J Urol 176:2375–2382PubMedGoogle Scholar
  83. 83.
    Cordeaux Y, Middleton RJ, Myatt A, Kellam B, Hill SJ (2003) ABEA-BY630 is a fluorescent agonist at A2B adenosine receptors in human prostatic stromal cells. Br J Pharmacol 14:16PGoogle Scholar
  84. 84.
    Cox CI, Leese HJ (1994) Characterization of a functional purinergic receptor in primary cultures of bovine oviduct epithelia. J Reprod Fertil 13:5Google Scholar
  85. 85.
    Cox CI, Leese HJ (1995) Effect of purinergic stimulation on intracellular calcium concentration and transepithelial potential difference in cultured bovine oviduct cells. Biol Reprod 52:1244–1249PubMedGoogle Scholar
  86. 86.
    Dai Y, Zhang Y, Phatarpekar P, Mi T, Zhang H, Blackburn MR, Xia Y (2009) Adenosine signaling, priapism and novel therapies. J Sex Med 6(Suppl 3):292–301PubMedGoogle Scholar
  87. 87.
    Darville T, Welter-Stahl L, Cruz C, Sater AA, Andrews CW Jr, Ojcius DM (2007) Effect of the purinergic receptor P2X7 on Chlamydia infection in cervical epithelial cells and vaginally infected mice. J Immunol 179:3707–3714PubMedGoogle Scholar
  88. 88.
    De Lamirande E, Gagnon C (1992) Reactive oxygen species and human spermatozoa: II. Depletion of adenosine triphosphate plays an important role in the inhibition of sperm motility. J Androl 13:379–386PubMedGoogle Scholar
  89. 89.
    de Souza LF, Gelain DP, Jardim FR, Ribeiro GR, Zim M, Bernard EA (2006) Extracellular inosine participates in tumor necrosis factor-alpha induced nitric oxide production in cultured Sertoli cells. Mol Cell Biochem 281:123–128PubMedGoogle Scholar
  90. 90.
    Di Iulio JL, Gude NM, Brennecke SP, King RG (1997) Effects of ATP, ADP, thrombin, vasopressin and U46619 on human placental nitric oxide synthase activity. Methods Find Exp Clin Pharmacol 19:509–514PubMedGoogle Scholar
  91. 91.
    Diaz JW, Gonzalez MA, Avedo F, Mallea L, Rodriguez N (1992) Use of an ATP-supplemented medium for the conservation of human semen and the effect of caffeine on the motility of preserved sperm. Results in artificial insemination. Andrologia 24:131–133PubMedGoogle Scholar
  92. 92.
    Dickens CJ, Comer MT, Southgate J, Leese HJ (1996) Human Fallopian tubal epithelial cells in vitro: establishment of polarity and potential role of intracellular calcium and extracellular ATP in fluid secretion. Hum Reprod 11:212–217PubMedGoogle Scholar
  93. 93.
    Divald A, Karl PI, Fisher SE (2002) Regulation of phospholipase D in human placental trophoblasts by the P2 purinergic receptor. Placenta 23:584–593PubMedGoogle Scholar
  94. 94.
    Dobronyi I, Gontero E, Maguire MH (1992) Vascular actions of ATP, α,β-methylene-ATP and β,γ-methylene-ATP in the perfused human placenta cotyledon. FASEB J Supplement:A1007Google Scholar
  95. 95.
    Dobronyi I, Hung KS, Satchell DG, Maguire MH (1997) Evidence for a novel P2X purinoceptor in human placental chorionic surface arteries. Eur J Pharmacol 320:61–64PubMedGoogle Scholar
  96. 96.
    Donoso MV, Montes CG, Lewin J, Fournier A, Calixto JB, Huidobro-Toro JP (1992) Endothelin-1 (ET)-induced mobilization of intracellular Ca2+ stores from the smooth muscle facilitates sympathetic cotransmission by potentiation of adenosine 5′-triphosphate (ATP) motor activity: studies in the rat vas deferens. Peptides 13:831–840PubMedGoogle Scholar
  97. 97.
    Donoso MV, Bates F, Montiel J, Huidobro-Toro JP (1994) Adenosine 5′-triphosphate (ATP), the neurotransmitter in the prostatic portion of the longitudinal muscle layer of the rat vas deferens. Neurosci Lett 169:59–62PubMedGoogle Scholar
  98. 98.
    Donoso MV, Lopez R, Miranda R, Briones R, Huidobro-Toro JP (2005) A2B adenosine receptor mediates human chorionic vasoconstriction and signals through arachidonic acid cascade. Am J Physiol Heart Circ Physiol 288:H2439–H2449PubMedGoogle Scholar
  99. 99.
    Donoso MV, Hermosilla D, Navarrete C, Álvarez P, Lillo JG, Huidobro-Toro JP (2012) Reciprocal sympatho-sensory control: functional role of nucleotides and calcitonin gene-related peptide in a peripheral neuroeffector junction. Neuroscience 203:216–229PubMedGoogle Scholar
  100. 100.
    Dozi-Vassiliades J, Tsiamitas C, Kokolis N (1976) The effect of PGE2 and PGF on the response of guinea pig myometrium to adenine nucleotides in vitro. Prostaglandins 12:515–524PubMedGoogle Scholar
  101. 101.
    Dunn PM (2000) Fertility: purinergic receptors and the male contraceptive pill. Curr Biol 10:R305–R307PubMedGoogle Scholar
  102. 102.
    Dunn PM, Blakeley AGH (1988) Suramin: a reversible P2-purinceptor antagonist in the mouse vas deferens. Br J Pharmacol 93:243–245PubMedCentralPubMedGoogle Scholar
  103. 103.
    Edwards SE, Buffone MG, Knee GR, Rossato M, Bonanni G, Masiero S, Ferasin S, Gerton GL, Moss SB, Williams CJ (2007) Effects of extracellular adenosine 5′-triphosphate on human sperm motility. Reprod Sci 14:655–666PubMedGoogle Scholar
  104. 104.
    Ellis JL, Burnstock G (1989) Modulation of neurotransmission in the guinea-pig vas deferens by capsaicin: involvement of calcitonin gene-related peptide and substance P. Br J Pharmacol 98:707–713PubMedCentralPubMedGoogle Scholar
  105. 105.
    Ennion SJ, Evans RJ (2001) Agonist-stimulated internalisation of the ligand-gated ion channel P2X1 in rat vas deferens. FEBS Lett 489:154–158PubMedGoogle Scholar
  106. 106.
    Erkkila K, Kyttanen S, Wikstrom M, Taari K, Hikim AP, Swerdloff RS, Dunkel L (2006) Regulation of human male germ cell death by modulators of ATP production. Am J Physiol Endocrinol Metab 290:E1145–E1154PubMedGoogle Scholar
  107. 107.
    Escudero C, Sobrevia L (2008) A hypothesis for preeclampsia: adenosine and inducible nitric oxide synthase in human placental microvascular endothelium. Placenta 29:469–483PubMedGoogle Scholar
  108. 108.
    Escudero C, Casanello P, Sobrevia L (2008) Human equilibrative nucleoside transporters 1 and 2 may be differentially modulated by A2B adenosine receptors in placenta microvascular endothelial cells from pre-eclampsia. Placenta 29:816–825PubMedGoogle Scholar
  109. 109.
    Fabiani R, Ronquist G (1995) Abundance of guanine, guanosine, inosine and adenosine in human seminal plasma. Int J Clin Lab Res 25:47–51PubMedGoogle Scholar
  110. 110.
    Faria M, Magalhães-Cardoso T, Lafuente-de-Carvalho JM, Correia-de-Sá P (2006) Corpus cavernosum from men with vasculogenic impotence is partially resistant to adenosine relaxation due to endothelial A2B receptor dysfunction. J Pharmacol Exp Ther 319:405–413PubMedGoogle Scholar
  111. 111.
    Faria M, Magalhães-Cardoso T, Lafuente-de-Carvalho JM, Correia-de Sá P (2008) Decreased ecto-NTPDase1/CD39 activity leads to desensitization of P2 purinoceptors regulating tonus of corpora cavernosa in impotent men with endothelial dysfunction. Nucleosides Nucleotides Nucleic Acids 27:761–768PubMedGoogle Scholar
  112. 112.
    Faria M, Valente MJ, Magalhães-Cardoso T, Lafuente-de-Carvalho JM, Correia-de Sá P (2008) Dual regulation of human penile smooth muscle tone by P2 purinoceptors: possible implications in erectile dysfunction. Purinergic Signal 4:S4Google Scholar
  113. 113.
    Faria M, Timóteo MA, Lafuente-de-Carvalho M, Correia-de-Sá P (2010) P2 purinoceptor subtype changes in patients with vasculogenic erectile dysfunction. Purinergic Signal 6:S115Google Scholar
  114. 114.
    Fedan JS, Hogaboom GK, O'Donnell JP, Colby J, Westfall DP (1981) Contributions by purines to the neurogenic response of the vas deferens of the guinea-pig. Eur J Pharmacol 69:41–53PubMedGoogle Scholar
  115. 115.
    Fedan JS, Hogaboom GK, Westfall DP, O'Donnell JP (1982) Comparison of the effects of arylazido aminopropionyl ATP (ANAPP3), an ATP antagonist, on responses of the smooth muscle of the guinea-pig vas deferens to ATP and related nucleotides. Eur J Pharmacol 85:277–290PubMedGoogle Scholar
  116. 116.
    Felder CC, Williams HL, Axelrod J (1991) A transduction pathway associated with receptors coupled to the inhibitory guanine nucleotide binding protein Gi that amplifies ATP-mediated arachidonic acid release. Proc Natl Acad Sci U S A 88:6477–6480PubMedCentralPubMedGoogle Scholar
  117. 117.
    Feng YH, Wang L, Wang Q, Li X, Zeng R, Gorodeski GI (2005) ATP stimulates GRK-3 – phosphorylation and β-arrestin-2-dependent internalization of P2X7-receptor. Am J Physiol 288:C1342–C1356Google Scholar
  118. 118.
    Feng YH, Li X, Wang L, Zhou L, Gorodeski GI (2006) A truncated P2X7 receptor variant (P2X7-j) endogenously expressed in cervical cancer cells antagonizes the full-length P2X7 receptor through hetero-oligomerization. J Biol Chem 281:17228–17237PubMedCentralPubMedGoogle Scholar
  119. 119.
    Fénichel P, Gharib A, Emiliozzi C, Donzeau M, Ménézo Y (1996) Stimulation of human sperm during capacitation in vitro by an adenosine agonist with specificity for A2 receptors. Biol Reprod 54:1405–1411PubMedGoogle Scholar
  120. 120.
    Ferguson SE, Pallikaros Z, Michael AE, Cooke BA (1999) The effects of different culture media, glucose, pyridine nucleotides and adenosine on the activity of 11β-hydroxysteroid dehydrogenase in rat Leydig cells. Mol Cell Endocrinol 158:37–44PubMedGoogle Scholar
  121. 121.
    Figenschau Y, Bertheussen K (1999) Enzymatic treatment of spermatozoa with a trypsin solution, SpermSolute: improved motility and enhanced ATP concentration. Int J Androl 22:342–344PubMedGoogle Scholar
  122. 122.
    Filippi S, Amerini S, Maggi M, Natali A, Ledda F (1999) Studies on the mechanisms involved in the ATP-induced relaxation in human and rabbit corpus cavernosum. J Urol 161:326–331PubMedGoogle Scholar
  123. 123.
    Filippini A, Riccioli A, De Cesaris P, Paniccia R, Teti A, Stefanini M, Conti M, Ziparo E (1994) Activation of inositol phospholipid turnover and calcium signaling in rat Sertoli cells by P2-purinergic receptors: modulation of follicle-stimulating hormone responses. Endocrinology 134:1537–1545PubMedGoogle Scholar
  124. 124.
    Fleet IR, Heap RB (1982) Uterine blood flow, myometrial activity and their response to adenosine during the peri-implantation period in sheep. J Reprod Fertil 65:195–205PubMedGoogle Scholar
  125. 125.
    Foresta C, Rossato M, Di Virgilio F (1992) Extracellular ATP is a trigger for the acrosome reaction in human spermatozoa. J Biol Chem 267:19443–19447PubMedGoogle Scholar
  126. 126.
    Foresta C, Rossato M, Bordon P, Di Virgilio F (1995) Extracellular ATP activates different signalling pathways in rat Sertoli cells. Biochem J 311:269–274PubMedCentralPubMedGoogle Scholar
  127. 127.
    Foresta C, Rossato M, Chiozzi P, Di Virgilio F (1996) Mechanism of human sperm activation by extracellular ATP. Am J Physiol 270:C1709–C1714PubMedGoogle Scholar
  128. 128.
    Foresta C, Rossato M, Nogara A, Gottardello F, Bordon P, Di Virgilio F (1996) Role of P2-purinergic receptors in rat Leydig cell steroidogenesis. Biochem J 320:499–504PubMedCentralPubMedGoogle Scholar
  129. 129.
    Fourie MH, du Toit D, Bornman MS, van der Merwe MP, du Plessis DJ (1991) α-Glucosidase, sperm ATP concentrations, and epididymal function. Arch Androl 26:139–141PubMedGoogle Scholar
  130. 130.
    Fox IH, Kurpis L (1983) Binding characteristics of an adenosine receptor in human placenta. J Biol Chem 258:6952–6955PubMedGoogle Scholar
  131. 131.
    Francavilla S, Moscardelli S, Properzi G, De Matteis MA, Scorza BP, Natali PG, De MC (1987) Postnatal development of epididymis and ductus deferens in the rat. A correlation between the ultrastructure of the epithelium and tubule wall, and the fluorescence-microscopic distribution of actin, myosin, fibronectin, and basement membrane. Cell Tissue Res 249:257–265PubMedGoogle Scholar
  132. 132.
    Fraser LR (1990) Adenosine and its analogues, possibly acting at A2 receptors, stimulate mouse sperm fertilizing ability during early stages of capacitation. J Reprod Fertil 89:467–476PubMedGoogle Scholar
  133. 133.
    Fraser LR (2010) The “switching on” of mammalian spermatozoa: molecular events involved in promotion and regulation of capacitation. Mol Reprod Dev 77:197–208PubMedGoogle Scholar
  134. 134.
    Fraser LR, Duncan AE (1993) Adenosine analogues with specificity for A2 receptors bind to mouse spermatozoa and stimulate adenylate cyclase activity in uncapacitated suspensions. J Reprod Fertil 98:187–194PubMedGoogle Scholar
  135. 135.
    Fu W, McCormick T, Qi X, Zhou L, Li X, Wang BC, Gibbons HE, Abdul-Karim FW, Gorodeski GI (2009) Activation of P2X7-mediated apoptosis Inhibits DMBA/TPA-induced formation of skin papillomas and cancer in mice. BMC Cancer 9:114PubMedCentralPubMedGoogle Scholar
  136. 136.
    Fujita R, Kimura S, Kawasaki S, Takashima K, Matsumoto M, Hirano H, Sasaki K (2001) ATP suppresses the K+ current responses to FSH and adenosine in the follicular cells of Xenopus oocyte. Jpn J Physiol 51:491–500PubMedGoogle Scholar
  137. 137.
    Funahashi H, Romar R (2004) Reduction of the incidence of polyspermic penetration into porcine oocytes by pretreatment of fresh spermatozoa with adenosine and a transient co-incubation of the gametes with caffeine. Reproduction 128:789–800PubMedGoogle Scholar
  138. 138.
    Funahashi H, Asano A, Fujiwara T, Nagai T, Niwa K, Fraser LR (2000) Both fertilization promoting peptide and adenosine stimulate capacitation but inhibit spontaneous acrosome loss in ejaculated boar spermatozoa in vitro. Mol Reprod Dev 55:117–124PubMedGoogle Scholar
  139. 139.
    Furness JB, McLean JR, Burnstock G (1970) Distribution of adrenergic nerves and changes in neuromuscular transmission in the mouse vas deferens during postnatal development. Dev Biol 21:491–505PubMedGoogle Scholar
  140. 140.
    Furuya K, Nakano H, Enomoto K, Okuda A, Ichikawa J (2000) Mechanically induced calcium waves mediating purinergic coupling between myo- and secretory epithelial cells in mammary gland. Drug Dev Res 50:54Google Scholar
  141. 141.
    Gelain DP, de Souza LF, Bernard EA (2003) Extracellular purines from cells of seminiferous tubules. Mol Cell Biochem 245:1–9PubMedGoogle Scholar
  142. 142.
    Gessi S, Merighi S, Stefanelli A, Mirandola P, Bonfatti A, Fini S, Sensi A, Marci R, Varani K, Borea PA, Vesce F (2012) Downregulation of A1 and A2B adenosine receptors in human trisomy 21 mesenchymal cells from first-trimester chorionic villi. Biochim Biophys Acta 1822:1660–1670PubMedGoogle Scholar
  143. 143.
    Ghildyal P, Palani D, Manchanda R (2006) Post- and prejunctional consequences of ecto-ATPase inhibition: electrical and contractile studies in guinea-pig vas deferens. J Physiol 575:469–480PubMedCentralPubMedGoogle Scholar
  144. 144.
    Gillman TA, Pennefather JN (1998) Evidence for the presence of both P1 and P2 purinoceptors in the rat myometrium. Clin Exp Pharmacol Physiol 25:592–599PubMedGoogle Scholar
  145. 145.
    Glass R, Bardini M, Robson T, Burnstock G (2001) Expression of nucleotide P2X receptor subtypes during spermatogenesis in the adult rat testis. Cells Tissues Org 169:377–387Google Scholar
  146. 146.
    Gorodeski GI (2002) Regulation of transcervical permeability by two distinct P2 purinergic receptor mechanisms. Am J Physiol Cell Physiol 282:C75–C83PubMedGoogle Scholar
  147. 147.
    Gorodeski GI (2002) Expression, regulation, and function of P2X4 purinergic receptor in human cervical epithelial cells. Am J Physiol Cell Physiol 282:C84–C93PubMedGoogle Scholar
  148. 148.
    Gorodeski GI (2008) Regulation of paracellular permeability in low-resistance human vaginal–cervical epithelia. In: Ehrhardt C, Kim KJ (eds) Biotechnology, pharmaceutical aspects, drug absorption studies in situ, in vitro, and in silico Models. Springer, Berlin, pp 339–367Google Scholar
  149. 149.
    Gorodeski GI (2009) P2X7-mediated chemoprevention of epithelial cancers. Exp Opin Therap Targ 13:1313–1332Google Scholar
  150. 150.
    Gorodeski GI (2012) P2X7 receptors and epithelial cancers: focus article. WIREs Membr Transp Signal 1:349–371Google Scholar
  151. 151.
    Gorodeski GI, Goldfarb J (1997) Extracellular ATP regulates transcervical permeability by modulating two distinct paracellular pathways. Am J Physiol 272:C1602–C1610PubMedGoogle Scholar
  152. 152.
    Gorodeski GI, Goldfarb J (1998) Seminal fluid factor increases the resistance of the tight junctional complex of the cultured human cervical epithelium CaSki. Fertil Steril 69:309–317PubMedGoogle Scholar
  153. 153.
    Gorodeski GI, Peterson DE, De Santis BJ, Hopfer U (1996) Nucleotide receptor-mediated decrease of tight-junctional permeability in cultured human cervical epithelium. Am J Physiol 270:C1715–C1725PubMedGoogle Scholar
  154. 154.
    Gorodeski GI, Hopfer U, Liu CC, Margles E (2005) Estrogen acidifies vaginal pH by upregulation of proton secretion via the apical membrane of vaginal–ectocervical epithelial cells. Endocrinology 146:816–824PubMedCentralPubMedGoogle Scholar
  155. 155.
    Gray KT, Short JL, Ledent C, Ventura S (2008) Targeted disruption of the A2A adenosine receptor reduces in-vitro prostate contractility in mature mice. Eur J Pharmacol 592:151–157PubMedGoogle Scholar
  156. 156.
    Gröschel-Stewart U, Bardini M, Robson T, Burnstock G (1999) Localisation of P2X5 and P2X7 receptors by immunohistochemistry in rat stratified squamous epithelia. Cell Tissue Res 296:599–605PubMedGoogle Scholar
  157. 157.
    Gür S, Kadowitz PJ, Hellstrom WJ (2007) Purinergic (P2) receptor control of lower genitourinary tract function and new avenues for drug action: an overview. Curr Pharm Des 13:3236–3244PubMedGoogle Scholar
  158. 158.
    Gür S, Kadowitz PJ, Abdel-Mageed AS, Kendirci M, Sikka SC, Burnstock G, Hellstrom WJG (2009) Management of erectile function by purinergic P2 receptors in diabetic rat penis. J Urol 181:2382Google Scholar
  159. 159.
    Hall AK, Preston SL, Behrman HR (1981) Purine amplification of luteinizing hormone action in ovarian luteal cells. J Biol Chem 256:10390–10398PubMedGoogle Scholar
  160. 160.
    Hammami S, Willumsen NJ, Meinild AK, Klaerke DA, Novak I (2013) Purinergic signalling — a possible mechanism for KCNQ1 channel response to cell volume challenges. Acta Physiol (Oxf) 207:503–515Google Scholar
  161. 161.
    Hashitani H (2000) Neuroeffector transmission to different layers of smooth muscle in the rat penile bulb. J Physiol 524(Pt 2):549–563PubMedCentralPubMedGoogle Scholar
  162. 162.
    Haynes JM, Alexander SP, Hill SJ (1998) A1 and A2 adenosine receptor modulation of contractility in the cauda epididymis of the guinea-pig. Br J Pharmacol 125:570–576PubMedCentralPubMedGoogle Scholar
  163. 163.
    Hedlund H, Andersson KE, Larsson B (1985) Effect of drugs interacting with adrenoreceptors and muscarinic receptors in the epididymal and prostatic parts of the human isolated vas deferens. J Auton Pharmacol 5:261–270PubMedGoogle Scholar
  164. 164.
    Henry D, Ferino F, Tomova S, Ferry N, Stengel D, Hanoune J (1986) Inhibition of the catalytic subunit of ram sperm adenylate cyclase by adenosine. Biochem Biophys Res Commun 137:970–977PubMedGoogle Scholar
  165. 165.
    Holck MI, Marks BH (1978) Purine nucleoside and nucleotide interactions on normal and subsensitive alpha adrenoreceptor responsiveness in guinea-pig vas deferens. J Pharmacol Exp Ther 205:104–117PubMedGoogle Scholar
  166. 166.
    Holman ME (1987) The gamma controversy. Clin Exp Pharmacol Physiol 14:415–422PubMedGoogle Scholar
  167. 167.
    Honoré E, Martin C, Mironneau C, Mironneau J (1989) An ATP-sensitive conductance in cultured smooth muscle cells from pregnant rat myometrium. Am J Physiol 257:C297–C305PubMedGoogle Scholar
  168. 168.
    Hourani SM (1999) Postnatal development of purinoceptors in rat visceral smooth muscle preparations. Gen Pharmacol 32:3–7PubMedGoogle Scholar
  169. 169.
    Hourani SMO, Nicholls J, Lee BS, Halfhide EJ, Kitchen I (1993) Characterization and ontogeny of P1-purinoceptors on rat vas deferens. Br J Pharmacol 108:754–758PubMedCentralPubMedGoogle Scholar
  170. 170.
    Huidobro-Toro JP, Briones R, Buvinic S, Valdecantos P, Germain A (2002) Nucleotide receptor subtypes regulate flow in the human placenta. Vascular Neuroeffector Mechanisms, Lake Tahoe, July 12–15, 2002Google Scholar
  171. 171.
    Hukovic S (1961) Responses of the isolated sympathetic nerveductus deferens preparation of the guinea-pig. Br J Pharmacol Chemother 16:188–194PubMedCentralPubMedGoogle Scholar
  172. 172.
    Hupertan V, Neuzillet Y, Stücker O, Pons C, Leammel E, Lebret T (2012) Effects of nucleotides adenosine monophosphate and adenosine triphosphate in combination with l-arginine on male rabbit corpus cavernosum tissue. Int J Androl 35:860–866PubMedGoogle Scholar
  173. 173.
    Hutchings G, Gevaert T, Deprest J, Nilius B, Williams O, De Ridder D (2009) The effect of extracellular adenosine triphosphate on the spontaneous contractility of human myometrial strips. Eur J Obstet Gynecol Reprod Biol 143:79–83PubMedGoogle Scholar
  174. 174.
    Hutchings G, Williams O, Cretoiu D, Ciontea SM (2009) Myometrial interstitial cells and the coordination of myometrial contractility. J Cell Mol Med 13:4268–4282PubMedGoogle Scholar
  175. 175.
    Hutton RA, Chow FP, Craft IL, Dandona P (1980) Inhibitors of platelet aggregation in the fetoplacental unit and myometrium with particular reference to the ADP-degrading property of placenta. Placenta 1:125–130PubMedGoogle Scholar
  176. 176.
    Illes P, Rickmann H, Brod I, Bucher B, Stoclet J-C (1989) Subsensitivity of presynaptic adenosine A1-receptors in caudal arteries of spontaneously hypertensive rats. Eur J Pharmacol 174:237–251PubMedGoogle Scholar
  177. 177.
    Insler V, Glazerman M, Zeidel L, Bernstein D, Misgav N (1980) Sperm storage in the human cervix. Fertil Steril 33:288–229PubMedGoogle Scholar
  178. 178.
    Iredale PA, Hill SJ (1993) Increases in intracellular calcium via activation of an endogenous P2-purinoceptor in cultured CHO-K1 cells. Br J Pharmacol 110:1305–1310PubMedCentralPubMedGoogle Scholar
  179. 179.
    Iwata H, Goto H, Tanaka H, Sakaguchi Y, Kimura K, Kuwayama T, Monji Y (2011) Effect of maternal age on mitochondrial DNA copy number, ATP content and IVF outcome of bovine oocytes. Reprod Fertil Dev 23:424–432PubMedGoogle Scholar
  180. 180.
    Janssens R, Boeynaems JM (2001) Effects of extracellular nucleotides and nucleosides on prostate carcinoma cells. Br J Pharmacol 132:536–546PubMedCentralPubMedGoogle Scholar
  181. 181.
    Janssens R, Communi D, Pirotton S, Samson M, Parmentier M, Boeynaems JM (1996) Cloning and tissue distribution of the human P2Y1 receptor. Biochem Biophys Res Commun 221:588–593PubMedGoogle Scholar
  182. 182.
    Jeulin C, Soufir JC (1992) Reversible intracellular ATP changes in intact rat spermatozoa and effects on flagellar sperm movement. Cell Motil Cytoskeleton 21:210–222PubMedGoogle Scholar
  183. 183.
    Jiang L, Bardini M, Keogh A, dos Remedios CG, Burnstock G (2005) P2X1 receptors are closely associated with connexin 43 in human ventricular myocardium. Int J Cardiol 98:291–297PubMedGoogle Scholar
  184. 184.
    Kamada S, Blackmore PF, Oehninger S, Gordon K, Hodgen GD (1994) Existence of P2-purinoceptors on human and porcine granulosa cells. J Clin Endocrinol Metab 78:650–656PubMedGoogle Scholar
  185. 185.
    Kangasniemi M (1993) Effects of adenosine analog PIA (n-phenylisopropyladenosine) on FSH-stimulated cyclic AMP (cAMP) production in the rat seminiferous epithelium. Mol Cell Endocrinol 96:141–146PubMedGoogle Scholar
  186. 186.
    Karunanithi S, Lavidis NA, Bennett MR (1993) Evidence that each nerve varicosity on the surface of the mouse vas deferens secretes ATP. Neurosci Lett 161:157–160PubMedGoogle Scholar
  187. 187.
    Kasakov L, Ellis J, Kirkpatrick K, Milner P, Burnstock G (1988) Direct evidence for concomitant release of noradrenaline, adenosine 5′-triphosphate and neuropeptide Y from sympathetic nerve supplying the guinea-pig vas deferens. J Auton Nerv Syst 22:75–82PubMedGoogle Scholar
  188. 188.
    Kaschube M, Möller-Hartmann H, Zetler G (1989) The field-stimulated vas deferens of the streptozotocin-diabetic mouse: effects of prazosin, α, β-methylene ATP, and variation of stimulation parameters. J Neural Transm 77:171–180PubMedGoogle Scholar
  189. 189.
    Kataoka K, Furukawa K, Nagao K, Ishii N, Tsuru H (2007) The participation of adenosine receptors in the adenosine 5′-triphosphate-induced relaxation in the isolated rabbit corpus cavernosum penis. Int J Urol 14:764–768PubMedGoogle Scholar
  190. 190.
    Katoh K, Komatsu T, Yonekura S, Ishiwata H, Hagino A, Obara Y (2001) Effects of adenosine 5′-triphosphate and growth hormone on cellular H+ transport and calcium ion concentrations in cloned bovine mammary epithelial cells. J Endocrinol 169:381–388PubMedGoogle Scholar
  191. 191.
    Katugampola H, Burnstock G (2004) Purinergic signalling to rat ovarian smooth muscle: changes in P2X receptor expression during pregnancy. Cells Tissues Org 178:33–47Google Scholar
  192. 192.
    Kaya T, Sarioglu Y, Göksu OC, Yildirim S, Yildirim K (1998) Effect of additional testosterone on purinergic responses in isolated rabbit corpus cavernosum strips. Pharmacol Res 37:227–232PubMedGoogle Scholar
  193. 193.
    Keating N, Quinlan LR (2008) Effect of basolateral adenosine triphosphate on chloride secretion by bovine oviductal epithelium. Biol Reprod 78:1119–1126PubMedGoogle Scholar
  194. 194.
    Keating N, Quinlan LR (2012) Small conductance potassium channels drive ATP-activated chloride secretion in the oviduct. Am J Physiol Cell Physiol 302:C100–C109PubMedGoogle Scholar
  195. 195.
    Kempinas WD, Suarez JD, Roberts NL, Strader L, Ferrell J, Goldman JM, Klinefelter GR (1998) Rat epididymal sperm quantity, quality, and transit time after guanethidine-induced sympathectomy. Biol Reprod 59:890–896PubMedGoogle Scholar
  196. 196.
    Kerr KP (2006) The effect of histamine on field-stimulated contractions of the guinea-pig prostate. Naunyn Schmiedebergs Arch Pharmacol 373:237–244PubMedGoogle Scholar
  197. 197.
    Kesim M, Kadioglu M, Yaris E, Kalyoncu NI, Ozyavuz R, Ulku C (2004) Paroxetine alters KCl- or ATP-induced contractile responses of isolated vas deferens in rats chronically treated with ethanol. Pharmacol Res 49:51–57PubMedGoogle Scholar
  198. 198.
    Kettlun AM, Alvarez A, Quintar R, Valenzuela MA, Collados L, Aranda E, Banda A, Chayet L, Chiong M, Mancilla M (1994) Human placental ATP-diphosphohydrolase: biochemical characterization, regulation and function. Int J Biochem 26:437–448PubMedGoogle Scholar
  199. 199.
    Khanam T, Burnstock G (2007) Changes in expression of P2X1 receptor and connexin 43 in the rat myometrium during pregnancy. Fertil Steril 88:1174–1179PubMedGoogle Scholar
  200. 200.
    Khanum A, Buczko E, Dufau ML (1997) Essential role of adenosine triphosphate in activation of 17β-hydroxysteroid dehydrogenase in the rat Leydig cell. Endocrinology 138:1612–1620PubMedGoogle Scholar
  201. 201.
    Khattab MM, Al-Rawi MB, Aleisa AM (2007) Postjunctional synergism of norepinephrine with ATP and diadenosine tetraphosphate in guinea pig vas deferens. Role of protein kinase C and Myosin light chain phosphatase. Pharmacology 80:27–32PubMedGoogle Scholar
  202. 202.
    Khera M, Mohamed O, Avila D, Ekeruo W, Gangitano DA, Lipshultz LI, Somogyi GT (2008) ATP release from cavernosal tissue is greater in patients following prostatectomy as compared to patients with organic ED. J Urol 179:232Google Scholar
  203. 203.
    Kilicarslan H, Yildirim S, Bagcivan I, Ayan S, Sarac B, Sarioglu Y (2002) Effect of chronic renal failure on the purinergic responses of corpus cavernosal smooth muscle in rabbits. BJU Int 90:596–600PubMedGoogle Scholar
  204. 204.
    Kim JH, Hong EK, Choi HS, Oh SJ, Kim KM, Uhm DY, Kim SJ (2002) K+ channel currents in rat ventral prostate epithelial cells. Prostate 51:201–210PubMedGoogle Scholar
  205. 205.
    Kim JH, Nam JH, Kim MH, Koh DS, Choi SJ, Kim SJ, Lee JE, Min KM, Uhm DY, Kim SJ (2004) Purinergic receptors coupled to intracellular Ca2+ signals and exocytosis in rat prostate neuroendocrine cells. J Biol Chem 279:27345–27356PubMedGoogle Scholar
  206. 206.
    Kimoto Y, Ito Y (1987) Autonomic innervation of the canine penile artery and vein in relation to neural mechanisms involved in erection. Br J Urol 59:463–472PubMedGoogle Scholar
  207. 207.
    King BF, Wang S, Burnstock G (1996) P2 purinoceptor-activated inward currents in folliculated oocytes of Xenopus laevis. J Physiol 494:17–28PubMedCentralPubMedGoogle Scholar
  208. 208.
    Kirkpatrick K, Burnstock G (1987) Sympathetic nerve-mediated release of ATP from the guinea-pig vas deferens is unaffected by reserpine. Eur J Pharmacol 138:207–214PubMedGoogle Scholar
  209. 209.
    Klinge E, Sjöstrand NO (1977) Comparative study of some isolated mammalian smooth muscle effectors of penile erection. Acta Physiol Scand 100:354–367PubMedGoogle Scholar
  210. 210.
    Knecht M, Darbon JM, Ranta T, Baukal A, Catt KJ (1984) Inhibitory actions of adenosine on follicle-stimulating hormone-induced differentiation of cultured rat granulosa cells. Biol Reprod 30:1082–1090PubMedGoogle Scholar
  211. 211.
    Knight D, D'Arbe M, Liang S, Phillips WD, Lavidis NA (2003) Regional differences in sympathetic purinergic transmission along the length of the mouse vas deferens. Synapse 47:225–235PubMedGoogle Scholar
  212. 212.
    Knight GE, Bodin P, de Groat WC, Burnstock G (2002) ATP is released from guinea pig ureter epithelium on distension. Am J Physiol Renal Physiol 282:F281–F288PubMedGoogle Scholar
  213. 213.
    Knudsen TB, Blackburn MR, Chinsky JM, Airhart MJ, Kellems RE (1991) Ontogeny of adenosine deaminase in the mouse decidua and placenta: immunolocalization and embryo transfer studies. Biol Reprod 44:171–184PubMedGoogle Scholar
  214. 214.
    Ko WH, Au CL, Yip CY (2003) Multiple purinergic receptors lead to intracellular calcium increases in cultured rat Sertoli cells. Life Sci 72:1519–1535PubMedGoogle Scholar
  215. 215.
    Konrad L, Schiemann P, Renneberg H, Wennemuth G, Fini C, Aumuller G (1998) Expression and enzymic activity of ecto 5′-nucleotidase in the human male genital tract. Biol Reprod 59:190–196PubMedGoogle Scholar
  216. 216.
    Koshi R, Coutinho-Silva R, Cascabulho CM, Henrique-Pons A, Knight GE, Loesch A, Burnstock G (2005) Presence of the P2X7 purinergic receptor on immune cells that invade the rat endometrium during oestrus. J Reprod Immunol 66:127–140PubMedGoogle Scholar
  217. 217.
    Kumcu EK, Büyüknacar HS, Göçmen C, Evrüke IC, Önder S (2009) Differential effect of neocuproine, a copper(I) chelator, on contractile activity in isolated ovariectomized non-pregnant rat, pregnant rat and pregnant human uterus. Eur J Pharmacol 605:158–163PubMedGoogle Scholar
  218. 218.
    Kupitz Y, Atlas D (1993) A putative ATP-activated Na+ channel involved in sperm-induced fertilization. Science 261:484–486PubMedGoogle Scholar
  219. 219.
    Kwan CY, Ramlal T (1985) 5′-Nucleotidase activity in smooth muscle membranes of rat vas deferens. Mol Physiolo 8:277–292Google Scholar
  220. 220.
    Lahooti H, Thorsen T, Aakvaag A (1990) Effect of ATP on the regulation of the steroid binding activity of the oestradiol receptor. J Steroid Biochem 36:333–343PubMedGoogle Scholar
  221. 221.
    Lalevee N, Rogier C, Becq F, Joffre M (1999) Acute effects of adenosine triphosphates, cyclic 3′,5′-adenosine monophosphates, and follicle-stimulating hormone on cytosolic calcium level in cultured immature rat Ssertoli cells. Biol Reprod 61:343–352PubMedGoogle Scholar
  222. 222.
    Lara HE, Belmar J (1991) Release of norepinephrine from the cat ovary: changes after ovulation. Biol Reprod 44:752–759PubMedGoogle Scholar
  223. 223.
    Larriba S, Bassas L, Egozcue S, Giménez J, Ramos MD, Briceño O, Estivill X, Casals T (2001) Adenosine triphosphate-binding cassette superfamily transporter gene expression in severe male infertility. Biol Reprod 65:394–400PubMedGoogle Scholar
  224. 224.
    Lau DH, Metcalfe MJ, Mumtaz FH, Mikhailidis DP, Thompson CS (2009) Purinergic modulation of human corpus cavernosum relaxation. Int J Androl 32:149–155PubMedGoogle Scholar
  225. 225.
    Lau WA, Ventura S, Pennefather JN (1998) Pharmacology of neurotransmission to the smooth muscle of the rat and the guinea-pig prostate glands. J Auton Pharmacol 18:349–356PubMedGoogle Scholar
  226. 226.
    Lavidis NA, Bennett MR (1992) Probabilistic secretion of quanta from visualized sympathetic nerve varicosities in mouse vas deferens. J Physiol 454:9–26PubMedCentralPubMedGoogle Scholar
  227. 227.
    Lee HY, Bardini M, Burnstock G (2000) P2X receptor immunoreactivity in the male genital organs of the rat. Cell Tissue Res 300:321–330PubMedGoogle Scholar
  228. 228.
    Lee PS, Squires PE, Buchan AM, Yuen BH, Leung PC (1996) P2-purinoreceptor evoked changes in intracellular calcium oscillations in single isolated human granulosa-lutein cells. Endocrinology 137:3756–3761PubMedGoogle Scholar
  229. 229.
    Lee SY, Palmer ML, Maniak PJ, Jang SH, Ryu PD, O'Grady SM (2007) P2Y receptor regulation of sodium transport in human mammary epithelial cells. Am J Physiol Cell Physiol 293:C1472–C1480PubMedGoogle Scholar
  230. 230.
    León D, Albasanz JL, Ruíz MA, Martín M (2005) Chronic caffeine or theophylline intake during pregnancy inhibits A1 receptor function in the rat brain. Neuroscience 131:481–489PubMedGoogle Scholar
  231. 231.
    Leung AY, Tai HL, Wong PY (1993) ATP stimulates Ca 2+ release from a rapidly exchanging pool in cultured rat epididymal cells. Am J Physiol 264:C1388–C1394PubMedGoogle Scholar
  232. 232.
    Levin RM, Hypolite JA, Broderick GA (1995) Comparison of the pharmacological response of human corpus cavernosal tissue with the response of rabbit cavernosal tissue. Gen Pharmacol 26:1107–1111PubMedGoogle Scholar
  233. 233.
    Levine RF, Derks R, Beaman K (2005) Regeneration and tolerance factor. A vacuolar ATPase with consequences. Chem Immunol Allergy 89:126–134PubMedGoogle Scholar
  234. 234.
    Levitt B, Head RJ, Westfall DP (1984) High-pressure liquid chromatographic–fluorometric detection of adenosine and adenine nucleotides: application to endogenous content and electrically induced release of adenyl purines in guinea pig vas deferens. Anal Biochem 137:93–100PubMedGoogle Scholar
  235. 235.
    Lew MJ, White TD (1987) Release of endogenous ATP during sympathetic nerve stimulation. Br J Pharmacol 92:349–355PubMedCentralPubMedGoogle Scholar
  236. 236.
    Li X, Qi X, Zhou L, Catera D, Rote NS, Potashkin J, Abdul-Karim FW, Gorodeski GI (2007) Decreased expression of P2X7 in endometrial epithelial pre-cancerous and cancer cells. Gynecol Oncol 106:233–243PubMedCentralPubMedGoogle Scholar
  237. 237.
    Li X, Qi X, Zhou L, Fu W, Abdul-Karim FW, MacLennan G, Gorodeski GI (2009) P2X7 receptor expression is decreased in epithelial cancer cells of ectodermal, uro-genital sinus, and distal paramesonephric-duct origin. Purinergic Signal 5:351–368PubMedCentralPubMedGoogle Scholar
  238. 238.
    Liang SX, Phillips WD, Lavidis N (1998) Development of fast purinergic transmission in the mouse vas deferens. Proc Aust Neurosci Soc 9:119Google Scholar
  239. 239.
    Liang SX, D'Arbe M, Phillips WD, Lavidis NA (2000) Development of fast purinergic transmission in the mouse vas deferens. Synapse 37:283–291PubMedGoogle Scholar
  240. 240.
    Lin WY, Mannikarottu A, Chichester P, Neuman P, Johnson A, Pérez-Martínez FC, Levin RM (2008) The effect of chronic partial bladder outlet obstruction on corpus cavernosum smooth muscle and Rho-kinase in rabbits. Neurourol Urodyn 27:826–831PubMedGoogle Scholar
  241. 241.
    Lishko PV, Kirichok Y, Ren D, Navarro B, Chung JJ, Clapham DE (2012) The control of male fertility by spermatozoan ion channels. Annu Rev Physiol 74:453–475PubMedCentralPubMedGoogle Scholar
  242. 242.
    Liu DY, Jennings MG, Baker HW (1987) Correlation between defective motility (asthenospermia) and ATP reactivation of demembranated human spermatozoa. J Androl 8:349–353PubMedGoogle Scholar
  243. 243.
    Loir M (1999) Spermatogonia of rainbow trout: III. In vitro study of the proliferative response to extracellular ATP and adenosine. Mol Reprod Dev 53:443–450PubMedGoogle Scholar
  244. 244.
    Longhurst PA, Schwegel T, Folander K, Swanson R (1996) The human P2X1 receptor: molecular cloning, tissue distribution, and localization to chromosome 17. Biochim Biophys Acta 1308:185–188PubMedGoogle Scholar
  245. 245.
    Losier AJ, Armstrong RW, Younglai EV (1980) Adenosine triphosphate inhibits LH stimulated testosterone accumulation by isolated rabbit ovarian follicles. IRCS Med Sci 8:322Google Scholar
  246. 246.
    Luciano LG, Orleans-Juste P, Calixto JB, Rae GA (1995) Endothelin-1 contracts and increases motor responses to ATP in rat seminal vesicle. J Cardiovasc Pharmacol 26(Suppl 3):S91–S94PubMedGoogle Scholar
  247. 247.
    Luria A, Rubinstein S, Lax Y, Breitbart H (2002) Extracellular adenosine triphosphate stimulates acrosomal exocytosis in bovine spermatozoa via P2 purinoceptor. Biol Reprod 66:429–437PubMedGoogle Scholar
  248. 248.
    MacDonald A, McGrath JC (1984) Post-natal development of functional neurotransmission in rat vas deferens. Br J Pharmacol 82:25–34PubMedCentralPubMedGoogle Scholar
  249. 249.
    Mackenzie I, Burnstock G, Dolly JO (1982) The effects of purified botulinum neurotoxin type A on cholinergic, adrenergic and non-adrenergic, atropine-resistant autonomic neuromuscular transmission. Neuroscience 7:997–1006PubMedGoogle Scholar
  250. 250.
    Mackenzie I, Manzini S, Burnstock G (1988) Regulation of voltage-dependent excitatory responses to α, β-methylene ATP, ATP and non-adrenergic nerve stimulation by dihydropyridines in the guinea-pig vas deferens. Neuroscience 27:317–332PubMedGoogle Scholar
  251. 251.
    Macleod GT, Lavidis NA, Bennett MR (1994) Calcium dependence of quantal secretion from visualized sympathetic nerve varicosities on the mouse vas deferens. J Physiol 480(Pt 1):61–70PubMedCentralPubMedGoogle Scholar
  252. 252.
    Magocsi M, Penniston JT (1991) Ca2+ or Mg2+ nucleotide phosphohydrolases in myometrium: two ecto-enzymes. Biochim Biophys Acta 1070:163–172PubMedGoogle Scholar
  253. 253.
    Maguire MH, Kitagawa H, Hosokawa T, Howard RB (1990) ATP and adenosine. Ann N Y Acad Sci 603:443–444Google Scholar
  254. 254.
    Maguire MH, Szabo I, Slegel P, King CR (1992) Determination of concentrations of adenosine and other purines in human term placenta by reversed-phase high-performance liquid chromatography with photodiode-array detection: evidence for pathways of purine metabolism in the placenta. J Chromatogr 575:243–253PubMedGoogle Scholar
  255. 255.
    Major TC, Weishaar RE, Taylor DG (1989) Two phases of contractile response in rat isolated vas deferens and their regulation by adenosine and α-receptors. Eur J Pharmacol 167:323–331PubMedGoogle Scholar
  256. 256.
    Majumder GC, Biswas R (1979) Evidence for the occurrence of an ecto-(adenosine triphosphatase) in rat epididymal spermatozoa. Biochem J 183:737–743PubMedCentralPubMedGoogle Scholar
  257. 257.
    Malek A, Miller RK, Mattison DR, Ceckler T, Panigel M, di Sant'Agnese PA, Jessee LN (1995) Continuous measurement of ATP by 31P-NMR in term human dually perfused placenta in vitro: response to ischemia. J Appl Physiol 78:1778–1786PubMedGoogle Scholar
  258. 258.
    Mallard N, Marshall R, Sithers A, Spriggs B (1992) Suramin: a selective inhibitor of purinergic neurotransmission in the rat isolated vas deferens. Eur J Pharmacol 220:1–10PubMedGoogle Scholar
  259. 259.
    Maroto R, Hamill OP (2001) Brefeldin A block of integrin-dependent mechanosensitive ATP release from Xenopus oocytes reveals a novel mechanism of mechanotransduction. J Biol Chem 276:23867–23872PubMedGoogle Scholar
  260. 260.
    Martín-Satué M, Lavoie ÉG, Pelletier J, Fausther M, Csizmadia E, Guckelberger O, Robson SC, Sévigny J (2009) Localization of plasma membrane bound NTPDases in the murine reproductive tract. Histochem Cell Biol 131:615–628PubMedGoogle Scholar
  261. 261.
    Martín-Satué M, Lavoie EG, Fausther M, Lecka J, Aliagas E, Kukulski F, Sévigny J (2010) High expression and activity of ecto-5′-nucleotidase/CD73 in the male murine reproductive tract. Histochem Cell Biol 133:659–668PubMedGoogle Scholar
  262. 262.
    Matsubara S, Tamada T, Kurahashi K, Saito T (1987) Ultracytochemical localizations of adenosine nucleotidase activities in the human term placenta, with special reference to 5′-nucleotidase activity. Acta Histochem Cytochem 20:409–419Google Scholar
  263. 263.
    Matsumoto M, Sakurai Y, Kokubo T, Yagi H, Makita K, Matsui T, Titani K, Fujimura Y, Narita N (1999) The cDNA cloning of human placental ecto-ATP diphosphohydrolases I and II. FEBS Lett 453:335–340PubMedGoogle Scholar
  264. 264.
    Matsuoka I, Ohkubo S, Kimura J, Uezono Y (2002) Adenine nucleotide-induced activation of adenosine A2B receptors expressed in Xenopus laevis oocytes: involvement of a rapid and localized adenosine formation by ectonucleotidases. Mol Pharmacol 61:606–613PubMedGoogle Scholar
  265. 265.
    Mazzoni MR, Buffoni RS, Giusti L, Lucacchini A (1995) Characterization of a low affinity binding site for N 6-substituted adenosine derivatives in rat testis membranes. J Recept Signal Transduct Res 15:905–929PubMedGoogle Scholar
  266. 266.
    McLaren GJ, Lambrecht G, Mutschler E, Bäumert HG, Sneddon P, Kennedy C (1994) Investigation of the actions of PPADS, a novel P2x-purinoceptor antagonist, in the guinea-pig isolated vas deferens. Br J Pharmacol 111:913–917PubMedCentralPubMedGoogle Scholar
  267. 267.
    Megory E, Shoham Z, Madgar I, Lunenfeld B, Modan M, Weissenberg R (1987) ATP content in human semen and sperm quality. Arch Androl 19:243–247PubMedGoogle Scholar
  268. 268.
    Meldrum LA, Burnstock G (1983) Evidence that ATP acts as a co-transmitter with noradrenaline in sympathetic nerves supplying the guinea-pig vas deferens. Eur J Pharmacol 92:161–163PubMedGoogle Scholar
  269. 269.
    Meldrum LA, Burnstock G (1985) Evidence that ATP is involved as a co-transmitter in the hypogastric nerve supplying the seminal vesicle of the guinea-pig. Eur J Pharmacol 110:363–366PubMedGoogle Scholar
  270. 270.
    Menzies JRW, Kennedy C (2002) Perinuclear P2X7-like immunoreactivity in the guinea-pig vas deferens. Br J Pharmacol 135:50PGoogle Scholar
  271. 271.
    Meroni SB, Canepa DF, Pellizzari EH, Schteingart HF, Cigorraga SB (1998) Effects of purinergic agonists on aromatase and gamma-glutamyl transpeptidase activities and on transferrin secretion in cultured Sertoli cells. J Endocrinol 157:275–283PubMedGoogle Scholar
  272. 272.
    Mi T, Abbasi S, Zhang H, Uray K, Chunn JL, Xia LW, Molina JG, Weisbrodt NW, Kellems RE, Blackburn MR, Xia Y (2008) Excess adenosine in murine penile erectile tissues contributes to priapism via A2B adenosine receptor signaling. J Clin Invest 118:1491–1501PubMedCentralPubMedGoogle Scholar
  273. 273.
    Mieusset R, Parinaud J, Chap H, Pontonnier G (1989) Absence of correlation between the levels of ATP and other seminal compounds in semen and the results of human in-vitro fertilization. Int J Androl 12:346–353PubMedGoogle Scholar
  274. 274.
    Mihaylova-Todorova ST, Todorov LD, Westfall DP (2002) Enzyme kinetics and pharmacological characterization of nucleotidases released from the guinea pig isolated vas deferens during nerve stimulation: evidence for a soluble ecto-nucleoside triphosphate diphosphohydrolase-like ATPase and a soluble ecto-5′-nucleotidase-like AMPase. J Pharmacol Exp Ther 302:992–1001PubMedGoogle Scholar
  275. 275.
    Milošević M, Petrović S, Veličković N, Grković I, Ignjatović M, Horvat A (2012) ATP and ADP hydrolysis in cell membranes from rat myometrium. Mol Cell Biochem 371:199–208PubMedGoogle Scholar
  276. 276.
    Min K, Munarriz R, Yerxa BR, Goldstein I, Shaver SR, Cowlen MS, Traish AM (2003) Selective P2Y2 receptor agonists stimulate vaginal moisture in ovariectomized rabbits. Fertil Steril 79:393–398PubMedGoogle Scholar
  277. 277.
    Minelli A, Miscetti P, Allegrucci C, Mezzasoma I (1995) Evidence of A1 adenosine receptor on epidydimal bovine spermatozoa. Arch Biochem Biophys 322:272–276PubMedGoogle Scholar
  278. 278.
    Minelli A, Allegrucci C, Mezzasoma I (1997) [3H]-(R)-N 6-Phenylisopropyladenosine agonist binding to the solubilized A1 adenosine receptor from bovine epididymal spermatozoa. Arch Biochem Biophys 337:54–61PubMedGoogle Scholar
  279. 279.
    Minelli A, Allegrucci C, Piomboni P, Mannucci R, Lluis C, Franco R (2000) Immunolocalization of A1 adenosine receptors in mammalian spermatozoa. J Histochem Cytochem 48:1163–1171PubMedGoogle Scholar
  280. 280.
    Minelli A, Liguori L, Bellazza I, Mannucci R, Johansson B, Fredholm BB (2004) Involvement of A1 adenosine receptors in the acquisition of fertilizing capacity. J Androl 25:286–292PubMedGoogle Scholar
  281. 281.
    Minelli A, Bellezza I, Collodel G, Fredholm BB (2008) Promiscuous coupling and involvement of protein kinase C and extracellular signal-regulated kinase 1/2 in the adenosine A1 receptor signalling in mammalian spermatozoa. Biochem Pharmacol 75:931–941PubMedGoogle Scholar
  282. 282.
    Miyoshi H, Yamaoka K, Urabe S, Kodama M, Kudo Y (2010) Functional expression of purinergic P2X7 receptors in pregnant rat myometrium. Am J Physiol Regul Integr Comp Physiol 298:R1117–R1124PubMedGoogle Scholar
  283. 283.
    Miyoshi H, Yamaoka K, Urabe S, Kudo Y (2012) ATP-induced currents carried through P2X7 receptor in rat myometrial cells. Reprod Sci 19:1285–1291PubMedGoogle Scholar
  284. 284.
    Monaco L, Conti M (1986) Localization of adenosine receptors in rat testicular cells. Biol Reprod 35:258–266PubMedGoogle Scholar
  285. 285.
    Monaco L, DeManno DA, Martin MW, Conti M (1988) Adenosine inhibition of the hormonal response in the Sertoli cell is reversed by pertussis toxin. Endocrinology 122:2692–2698PubMedGoogle Scholar
  286. 286.
    Montiel-Herrera M, Zaske AM, Garcia-Colunga J, Martínez-Torres A, Miledi R (2011) Ion currents induced by ATP and angiotensin II in cultured follicular cells of Xenopus laevis. Mol Cells 32:397–404PubMedCentralPubMedGoogle Scholar
  287. 287.
    Morales B, Barrera N, Uribe P, Mora C, Villalon M (2000) Functional cross talk after activation of P2 and P1 receptors in oviductal ciliated cells. Am J Physiol Cell Physiol 279:C658–C669PubMedGoogle Scholar
  288. 288.
    Morales-Tlalpan V, Arellano RO, Diíz-Muñoz M (2005) Interplay between ryanodine and IP3 receptors in ATP-stimulated mouse luteinized-granulosa cells. Cell Calcium 37:203–213PubMedGoogle Scholar
  289. 289.
    Morikawa T, Tanaka N, Kubota Y, Mizuno H, Nakamura K, Kunitomo M, Shinozuka K (2007) ATP modulates the release of noradrenaline through two different prejunctional receptors on the adrenergic nerves of rat prostate. Clin Exp Pharmacol Physiol 34:601–605PubMedGoogle Scholar
  290. 290.
    Morishita H, Katsuragi T (1999) Existence and pharmacological properties of dopamine D4 receptors in guinea pig vas deferens. Eur J Pharmacol 374:255–261PubMedGoogle Scholar
  291. 291.
    Moritoki H, Takei M, Kasai T, Matsumura Y, Ishida Y (1979) Possible involvement of prostaglandins in the action of ATP on guinea-pig uterus. J Pharmacol Exp Ther 211:104–111PubMedGoogle Scholar
  292. 292.
    Morley P, Vanderhyden BC, Tremblay R, Mealing GAR, Durkin JP, Whitfield JF (1994) Purinergic receptor-mediated intracellular Ca2+ oscillations in chicken granulosa cells. Endocrinology 134:1269–1276PubMedGoogle Scholar
  293. 293.
    Movahed E, Sadrkhanlou R, Ahmadi K, Nejati V, Zamani Z (2013) Effect of purine nucleoside analogue-acyclovir on the sperm parameters and testosterone production in rats. Int J Fertil Steril 7:49–56PubMedCentralPubMedGoogle Scholar
  294. 294.
    Mulryan K, Gitterman DP, Lewis CJ, Vial C, Leckie BJ, Cobb AL, Brown JE, Conley EC, Buell G, Pritchard CA, Evans RJ (2000) Reduced vas deferens contraction and male infertility in mice lacking P2X1 receptors. Nature 403:86–89PubMedGoogle Scholar
  295. 295.
    Munch E, Munoz A, Boone TB, Smith CP, Somogyi GT (2009) Release of ATP and NO from rat prostate: an in vitro and in vivo assessment of adrenergic receptor stimulation. J Urol 181:503Google Scholar
  296. 296.
    Murphy KM, Snyder SH (1981) Adenosine receptors in rat testes: labeling with 3H-cyclohexyladenosine. Life Sci 28:917–920PubMedGoogle Scholar
  297. 297.
    Nakanishi H, Takeda H (1973) The possible role of adenosine triphosphate in chemical transmission between the hypogastric nerve terminal and seminal vesicle in the guinea-pig. Jpn J Pharmacol 23:479–490PubMedGoogle Scholar
  298. 298.
    Nakano H, Furuya K, Furuya S, Yamagishi S (1997) Involvement of P2-purinergic receptors in intracellular Ca2+ responses and the contraction of mammary myoepithelial cells. Pflugers Arch 435:1–8PubMedGoogle Scholar
  299. 299.
    Nakano H, Furuya K, Yamagishi S (2001) Synergistic effects of ATP on oxytocin-induced intracellular Ca2+ response in mouse mammary myoepithelial cells. Pflugers Arch 442:57–63PubMedGoogle Scholar
  300. 300.
    Navarro B, Miki K, Clapham DE (2011) ATP-activated P2X2 current in mouse spermatozoa. Proc Natl Acad Sci U S A 108:14342–14347PubMedCentralPubMedGoogle Scholar
  301. 301.
    Neild TO, Hirst GDS (1984) The γ-connection': a reply. Trends Pharmacol Sci 5:56–57Google Scholar
  302. 302.
    Nelson L, Olsson T, Emanuelson U, Holmberg O, Sandholm M, Åstrom G (1985) Adenosine-triphosphate (ATP) as a detection method of mastitis. Presented at IDF Seminar ‘Progress in the Control of Bovine Mastitis’, 21–24 May, 1985Google Scholar
  303. 303.
    Ning C, Qi L, Wen J, Zhang Y, Zhang W, Wang W, Blackburn M, Kellems R, Xia Y (2012) Excessive penile norepinephrine level underlies impaired erectile function in adenosine A1 receptor deficient mice. J Sex Med 9:2552–2561PubMedGoogle Scholar
  304. 304.
    Ning C, Wen J, Zhang Y, Blackburn M, Kellems R, Xia Y (2012) Impaired adenosine signaling contributes to erectile dysfunction. J Sex Med 9:228Google Scholar
  305. 305.
    Ning C, Zhang Y, Wen J, Blackburn M, Kellems R, Xia Y (2012) Adenosine signaling in priapism and novel therapies. J Sex Med 9:223Google Scholar
  306. 306.
    Ninomiya JG, Suzuki H (1983) Electrical responses of smooth muscle cells of the mouse uterus to adenosine triphosphate. J Physiol 342:499–515PubMedCentralPubMedGoogle Scholar
  307. 307.
    Noto T, Inoue H, Mochida H, Kikkawa K (2001) Role of adenosine and P2 receptors in the penile tumescence in anesthetized dogs. Eur J Pharmacol 425:51–55PubMedGoogle Scholar
  308. 308.
    Obara K, Lepor H, Walden PD (1998) Localization of P 2Y1 purinoceptor transcripts in the rat penis and urinary bladder. J Urol 160:587–591PubMedGoogle Scholar
  309. 309.
    Ohkawa H (1982) Excitatory junction potentials recorded from the circular smooth muscles of the guinea-pig seminal vesicle. Tohoku J Exp Med 136:89–102PubMedGoogle Scholar
  310. 310.
    Okada Y, Taniguchi T, Akagi Y, Muramatsu I (2002) Two-phase response of acid extrusion triggered by purinoceptor in Chinese hamster ovary cells. Eur J Pharmacol 455:19–25PubMedGoogle Scholar
  311. 311.
    Osa T, Maruta K (1987) The mechanical response of the isolated longitudinal muscle of pregnant rat myometrium to adenosine triphosphate in the Ca-free solution containing various polyvalent cations. Jpn J Physiol 37:821–836PubMedGoogle Scholar
  312. 312.
    Page KR, Abramovich DR, Bush P, Clarke S, Dacke CG, Pereira J, Willoughby D (1993) ATP action on calcium uptake by human placental microvillous border vesicles. J Physiol 459:495PGoogle Scholar
  313. 313.
    Palmer ML, Lee SY, Carlson D, Fahrenkrug S, O'Grady SM (2006) Stable knockdown of CFTR establishes a role for the channel in P2Y receptor-stimulated anion secretion. J Cell Physiol 206:759–770PubMedGoogle Scholar
  314. 314.
    Palmer ML, Schiller KR, O'Grady SM (2007) Estrogen and progesterone differentially regulate UTP-stimulated anion secretion in endometrial epithelial cells by altering expression of P2Y receptors and basolateral K+ channels. FASEB J 21:A956Google Scholar
  315. 315.
    Palmer ML, Peitzman ER, Maniak PJ, Sieck GC, Prakash YS, O'Grady SM (2011) KCa3.1 channels facilitate K+ secretion or Na+ absorption depending on apical or basolateral P2Y receptor stimulation. J Physiol 589:3483–3494PubMedCentralPubMedGoogle Scholar
  316. 316.
    Papamarcaki T, Tsolas O (1990) Identification of ATP diphosphohydrolase activity in human term placenta using a novel assay for AMP. Mol Cell Biochem 97:1–8PubMedGoogle Scholar
  317. 317.
    Papka RE, Hafemeister J, Storey-Workley M (2005) P2X receptors in the rat uterine cervix, lumbosacral dorsal root ganglia, and spinal cord during pregnancy. Cell Tissue Res 321:35–44PubMedGoogle Scholar
  318. 318.
    Peachey JA, Brownhill VR, Hourani SMO, Kitchen I (1996) The ontogenetic profiles of the pre- and postjunctional adenosine receptors in the rat vas deferens. Br J Pharmacol 117:1105–1110PubMedCentralPubMedGoogle Scholar
  319. 319.
    Petit A, Bélisle S (1995) Stimulation of intracellular calcium concentration by adenosine triphosphate and uridine 5′-triphosphate in human term placental cells: evidence for purinergic receptors. J Clin Endocrinol Metab 80:1809–1815PubMedGoogle Scholar
  320. 320.
    Pinna C, Rubino A, Burnstock G (1997) Age-related changes in purinergic and adrenergic components of sympathetic neurotransmission in guinea-pig seminal vesicles. Br J Pharmacol 122:1411–1416PubMedCentralPubMedGoogle Scholar
  321. 321.
    Piper AS, Hollingsworth M (1996) P2-purinoceptors mediating spasm of the isolated uterus of the non-pregnant guinea-pig. Br J Pharmacol 117:1721–1729PubMedCentralPubMedGoogle Scholar
  322. 322.
    Pochmann D, Rucker B, Battastini AM, Sarkis JJ (2004) Ovariectomy and estradiol replacement therapy alters the adenine nucleotide hydrolysis in rat blood serum. Thromb Res 114:275–281PubMedGoogle Scholar
  323. 323.
    Polan ML, DeCherney AH, Haseltine FP, Mezer HC, Behrman HR (1983) Adenosine amplifies follicle-stimulating hormone action in granulosa cells and luteinizing hormone action in luteal cells of rat and human ovaries. J Clin Endocrinol Metab 56:288–294PubMedGoogle Scholar
  324. 324.
    Poletto Chaves LA, Pontelli EP, Varanda WA (2006) P2X receptors in mouse Leydig cells. Am J Physiol Cell Physiol 290:C1009–C1017PubMedGoogle Scholar
  325. 325.
    Pousette Å, Åkerlöf E, Lundin A, Rosenborg L, Fredricsson B (1986) On the use of adenosine triphosphate for estimation of motility and energy status in human spermatozoa. Int J Androl 9:331–340PubMedGoogle Scholar
  326. 326.
    Prapong S, Reinhardt TA, Goff JP, Horst RL (2005) Short communication: Ca2+-adenosine triphosphatase protein expression in the mammary gland of periparturient cows. J Dairy Sci 88:1741–1744PubMedGoogle Scholar
  327. 327.
    Preston A, Lau WA, Pennefather JN, Ventura S (2000) Effects of adenine nucleosides and nucleotides on neuromuscular transmission to the prostatic stroma of the rat. Br J Pharmacol 131:1073–1080PubMedCentralPubMedGoogle Scholar
  328. 328.
    Preston A, Frydenberg M, Haynes JM (2004) A1 and A2A adenosine receptor modulation of α1-adrenoceptor-mediated contractility in human cultured prostatic stromal cells. Br J Pharmacol 141:302–310PubMedCentralPubMedGoogle Scholar
  329. 329.
    Preston SL, Parmer TG, Behrman HR (1987) Adenosine reverses calcium-dependent inhibition of follicle-stimulating hormone action and induction of maturation in cumulus-enclosed rat oocytes. Endocrinology 120:1346–1353PubMedGoogle Scholar
  330. 330.
    Queiroz G, Talaia C, Gonçalves J (2003) ATP modulates noradrenaline release by activation of inhibitory P2Y receptors and facilitatory P2X receptors in the rat vas deferens. J Pharmacol Exp Ther 307:809–815PubMedGoogle Scholar
  331. 331.
    Quintas LE, Noël F (2009) Mechanisms of adaptive supersensitivity in vas deferens. Auton Neurosci 146:38–46PubMedGoogle Scholar
  332. 332.
    Ragazzi E, Chinellato A, Italiano G, Pagano F, Calabrò A (1996) Characterization of in vitro relaxant mechanisms in erectile tissue from rabbits of different ages. Urol Res 24:317–322PubMedGoogle Scholar
  333. 333.
    Ralevic V, Burnstock G (1998) Receptors for purines and pyrimidines. Pharmacol Rev 50:413–492PubMedGoogle Scholar
  334. 334.
    Ralevic V, Burrell S, Kingdom J, Burnstock G (1997) Characterization of P2 receptors for purine and pyrimidine nucleotides in human placental cotyledons. Br J Pharmacol 121:1121–1126PubMedCentralPubMedGoogle Scholar
  335. 335.
    Ratnasooriya WD (1993) Intra-epidiymal administration of α, β-methylene ATP impairs fertility of male rats. Med Sci Res 21:417–419Google Scholar
  336. 336.
    Read MA, Boura AL, Walters WA (1993) Vascular actions of purines in the foetal circulation of the human placenta. Br J Pharmacol 110:454–460PubMedCentralPubMedGoogle Scholar
  337. 337.
    Reid DL, Davidson SR, Phernetton TM, Rankin JH (1990) Adenosine causes a biphasic response in the ovine fetal placental vasculature. J Dev Physiol 13:237–240PubMedGoogle Scholar
  338. 338.
    Ren LM, Hoyle CH, Burnstock G (1996) Developmental changes in sympathetic contraction of the circular muscle layer in the guinea-pig vas deferens. Eur J Pharmacol 318:411–417PubMedGoogle Scholar
  339. 339.
    Reviriego J, Alonso MJ, Ibañez C, Marín J (1990) Action of adenosine and characterization of adenosine receptors in human placental vasculature. Gen Pharmacol 21:227–233PubMedGoogle Scholar
  340. 340.
    Roberts VH, Clarson LH (2002) Expression of the P2X receptor family in human placental tissue and trophoblast cells in culture. J Physiol 539:125PGoogle Scholar
  341. 341.
    Roberts VH, Greenwood SL, Elliott AC, Sibley CP, Waters LH (2006) Purinergic receptors in human placenta: evidence for functionally active P2X4, P2X7, P2Y2, and P2Y6. Am J Physiol Regul Integr Comp Physiol 290:R1374–R1386PubMedGoogle Scholar
  342. 342.
    Roberts VH, Waters LH, Powell T (2007) Purinergic receptor expression and activation in first trimester and term human placenta. Placenta 28:339–347PubMedGoogle Scholar
  343. 343.
    Roberts VH, Webster RP, Brockman DE, Pitzer BA, Myatt L (2007) Post-translational modifications of the P2X4 purinergic receptor subtype in the human placenta are altered in preeclampsia. Placenta 28:270–277PubMedGoogle Scholar
  344. 344.
    Rodríguez-Miranda E, Buffone MG, Edwards SE, Ord TS, Lin K, Sammel MD, Gerton GL, Moss SB, Williams CJ (2008) Extracellular adenosine 5′-triphosphate alters motility and improves the fertilizing capability of mouse sperm. Biol Reprod 79:164–171PubMedGoogle Scholar
  345. 345.
    Rohde GC, Venezian E, Huidobro-Toro JP (1986) Asymmetric distribution of purinergic and adrenergic neurotransmission cooperates in the motor activity along the rat vas deferens. Neurosci Lett 71:197–202PubMedGoogle Scholar
  346. 346.
    Romac P, Zanic Grubisic T, Jezek D, Vucic M, Culic O (2008) Hydrolysis of extracellular adenine nucleotides by human permatozoa: regulatory role of ectonucleotidases in sperm function. Croat Chem Acta 81:169–176Google Scholar
  347. 347.
    Rommerts FF, Molenaar R, Hoogerbrugge JW, van der Molen HJ (1984) Development of adenosine responsiveness after isolation of Leydig cells. Biol Reprod 30:842–847PubMedGoogle Scholar
  348. 348.
    Ronca-Testoni S, Galbani P, Gambacciani M (1984) Some properties of a purinergic receptor solubilized from human uterus membranes. FEBS Lett 172:335–338PubMedGoogle Scholar
  349. 349.
    Ronquist KG, Ek B, Stavreus-Evers A, Larsson A, Ronquist G (2013) Human prostasomes express glycolytic enzymes with capacity for ATP production. Am J Physiol Endocrinol Metab 304:E576–E582PubMedGoogle Scholar
  350. 350.
    Rossato M, La Sala GB, Balasini M, Taricco F, Galeazzi C, Ferlin A, Foresta C (1999) Sperm treatment with extracellular ATP increases fertilization rates in in-vitro fertilization for male factor infertility. Hum Reprod 14:694–697PubMedGoogle Scholar
  351. 351.
    Rossato M, Merico M, Bettella A, Bordon P, Foresta C (2001) Extracellular ATP stimulates estradiol secretion in rat Sertoli cells in vitro: modulation by external sodium. Mol Cell Endocrinol 178:181–187PubMedGoogle Scholar
  352. 352.
    Rossato M, Ferigo M, Galeazzi C, Foresta C (2005) Estradiol inhibits the effects of extracellular ATP in human sperm by a non genomic mechanism of action. Purinergic Signal 1:369–375PubMedCentralPubMedGoogle Scholar
  353. 353.
    Ruan YC, Wang Z, Du JY, Zuo WL, Guo JH, Zhang J, Wu ZL, Wong HY, Chung YW, Chan HC, Zhou WL (2008) Regulation of smooth muscle contractility by the epithelium in rat vas deferens: role of ATP-induced release of PGE2. J Physiol 586:4843–4857PubMedCentralPubMedGoogle Scholar
  354. 354.
    Ruan YC, Shum WW, Belleannée C, Da Silva N, Breton S (2012) ATP secretion in the male reproductive tract: essential role of CFTR. J Physiol 590:4209–4222PubMedCentralPubMedGoogle Scholar
  355. 355.
    Rudge SA, Hughes PJ, Brown GR, Michell RH, Kirk CJ (1995) Inositol lipid-mediated signalling in response to endothelin and ATP in the mammalian testis. Mol Cell Biochem 149–150:161–174PubMedGoogle Scholar
  356. 356.
    Saldaña C, Vázquez-Cuevas F, Garay E, Arellano RO (2005) Epithelium and/or theca are required for ATP-elicited K+ current in follicle-enclosed Xenopus oocytes. J Cell Physiol 202:814–821PubMedGoogle Scholar
  357. 357.
    Salvetti NR, Panzani CG, Gimeno EJ, Neme LG, Alfaro NS, Ortega HH (2009) An imbalance between apoptosis and proliferation contributes to follicular persistence in polycystic ovaries in rats. Reprod Biol Endocrinol 7:68PubMedCentralPubMedGoogle Scholar
  358. 358.
    Samuelson UE, Wiklund NP, Gustafsson LE (1985) Dual effects of adenosine and adenosine analogues on motor activity of the human fallopian tube. Acta Physiol Scand 125:369–376PubMedGoogle Scholar
  359. 359.
    Sasseville M, Albuz FK, Côté N, Guillemette C, Gilchrist RB, Richard FJ (2009) Characterization of novel phosphodiesterases in the bovine ovarian follicle. Biol Reprod 81:415–425PubMedCentralPubMedGoogle Scholar
  360. 360.
    Sawa R, Asakura H, Power GG (1991) Changes in plasma adenosine during simulated birth of fetal sheep. J Appl Physiol 70:1524–1528PubMedGoogle Scholar
  361. 361.
    Schiemann WP, Westfall DP, Buxton IL (1991) Smooth muscle adenosine A1 receptors couple to disparate effectors by distinct G proteins in pregnant myometrium. Am J Physiol 261:E141–E150PubMedGoogle Scholar
  362. 362.
    Shaban M, Smith RA, Stone TW (1995) Purine suppression of proliferation of Sertoli-like TM4 cells in culture. Cell Prolif 28:673–682PubMedGoogle Scholar
  363. 363.
    Shabbir M, Ryten M, Thompson CS, Mikhailidis DP, Burnstock G (2008) Characterisation of calcium-independent purinergic receptor-mediated apoptosis in hormone refractory prostate cancer. BJU Int 101:352–359PubMedGoogle Scholar
  364. 364.
    Shalev M, Staerman F, Allain H, Lobel B, Saïag B (1999) Stimulation of P2y purinoceptors induces, via nitric oxide production, endothelium-dependent relaxation of human isolated corpus cavernosum. J Urol 161:955–959PubMedGoogle Scholar
  365. 365.
    Shariatmadari R, Sipila P, Vierula M, Tornquist K, Huhtaniemi I, Poutanen M (2003) Adenosine triphosphate induces Ca2+ signal in epithelial cells of the mouse caput epididymis through activation of P2X and P2Y purinergic receptors. Biol Reprod 68:1185–1192PubMedGoogle Scholar
  366. 366.
    Shen MR, Linden J, Chen SS, Wu SN (1993) Identification of adenosine receptors in human spermatozoa. Clin Exp Pharmacol Physiol 20:527–534PubMedGoogle Scholar
  367. 367.
    Shi D, Winston JH, Blackburn MR, Datta SK, Hanten G, Kellems RE (1997) Diverse genetic regulatory motifs required for murine adenosine deaminase gene expression in the placenta. J Biol Chem 272:2334–2341PubMedGoogle Scholar
  368. 368.
    Slater M, Barden JA, Murphy CR (2000) Distributional changes in purinergic receptor subtypes (P2X1-7) in uterine epithelial cells during pregnancy. Histochem J 32:365–372PubMedGoogle Scholar
  369. 369.
    Slater M, Barden JA, Murphy CR (2000) The purinergic calcium channels P2X1,2,5,7 are down-regulated while P2X3,4,6 are up-regulated during apoptosis in the ageing rat prostate. Histochem J 32:571–580PubMedGoogle Scholar
  370. 370.
    Slater M, Murphy CR, Barden JA (2002) Purinergic receptor expression in the apical plasma membrane of rat uterine epithelial cells during implantation. Cell Calcium 31:201–207PubMedGoogle Scholar
  371. 371.
    Slater M, Danieletto S, Barden JA (2005) Expression of the apoptotic calcium channel P2X7 in the glandular epithelium. J Mol Histol 36:159–165PubMedGoogle Scholar
  372. 372.
    Smith MA, Buxton IL, Westfall DP (1988) Pharmacological classification of receptors for adenyl purines in guinea pig myometrium. J Pharmacol Exp Ther 247:1059–1063PubMedGoogle Scholar
  373. 373.
    Smith NCE, Burnstock G (2004) Mechanism underlying postjunctional synergism between responses of the vas deferens to noradrenaline and ATP. Eur J Pharmacol 498:241–248PubMedGoogle Scholar
  374. 374.
    Sneddon P (1992) Suramin inhibits excitatory junction potentials in guinea-pig isolated vas deferens. Br J Pharmacol 107:101–103PubMedCentralPubMedGoogle Scholar
  375. 375.
    Sneddon P, Burnstock G (1984) Inhibition of excitatory junction potentials in guinea-pig vas deferens by α, β-methylene-ATP: further evidence for ATP and noradrenaline as cotransmitters. Eur J Pharmacol 100:85–90PubMedGoogle Scholar
  376. 376.
    Sneddon P, Burnstock G (1984) Do we need γ-receptors? Trends Pharmacol Sci 5:264–265Google Scholar
  377. 377.
    Sneddon P, Westfall DP (1984) Pharmacological evidence that adenosine triphosphate and noradrenaline are co-transmitters in the guinea-pig vas deferens. J Physiol Lond 347:561–580PubMedCentralPubMedGoogle Scholar
  378. 378.
    Sneddon P, Westfall TD, Todorov LD, Todorova SM, Westfall DP, Nickel P, Kennedy C (2000) The effect of P2 receptor antagonists and ATPase inhibition on sympathetic purinergic neurotransmission in the guinea-pig isolated vas deferens. Br J Pharmacol 129:1089–1094PubMedCentralPubMedGoogle Scholar
  379. 379.
    Söderquist L (1991) ATP content and sperm motility of extended bovine semen under different storage conditions. Acta Vet Scand 32:511–518PubMedGoogle Scholar
  380. 380.
    Söderquist L, Stålhammar EM (1991) Relationship between ATP content and motility in bovine spermatozoa with reference to the effects of the bull and the A.I. centre. Acta Vet Scand 32:353–359PubMedGoogle Scholar
  381. 381.
    Somers GR, Bradbury R, Trute L, Conigrave A, Venter DJ (1999) Expression of the human P2Y6 nucleotide receptor in normal placenta and gestational trophoblastic disease. Lab Invest 79:131–139PubMedGoogle Scholar
  382. 382.
    Soodak LK, MacDonald GJ, Behrman HR (1988) Luteolysis is linked to luteinizing hormone-induced depletion of adenosine triphosphate in vivo. Endocrinology 122:187–193PubMedGoogle Scholar
  383. 383.
    Souza LF, Horn AP, Gelain DP, Jardim FR, Lenz G, Bernard EA (2005) Extracellular inosine modulates ERK 1/2 and p38 phosphorylation in cultured Sertoli cells: possible participation in TNF-alpha modulation of ERK 1/2. Life Sci 77:3117–3126PubMedGoogle Scholar
  384. 384.
    Squires PE, Hill CJ, Pacey AA, Li TC, Cooke ID, Warren MA, Dunne MJ (1995) Purinergic receptor-mediated increases in intracellular Ca2+ in single isolated epithelial cells of the human uterine tube. Proc Physiol Soc 482P:PC57Google Scholar
  385. 385.
    Squires PE, Lee PSN, Ho Yuen B, Leung PCK, Buchan AMJ (1997) Mechanisms involved in ATP-evoked Ca2+ oscillations in isolated human granulosa-luteal cells. Cell Calcium 21:365–374PubMedGoogle Scholar
  386. 386.
    Stein DM, Fraser LR, Monks NJ (1986) Adenosine and Gpp(NH)p modulate mouse sperm adenylate cyclase. Gamete Res 13:151–158Google Scholar
  387. 387.
    Stiles GL, Pierson G, Sunay S, Parsons WJ (1986) The rat testicular A1 adenosine receptor-adenylate cyclase system. Endocrinology 119:1845–1851PubMedGoogle Scholar
  388. 388.
    Stjärne L (2001) Novel dual ‘small’ vesicle model of ATP- and noradrenaline-mediated sympathetic neuromuscular transmission. Auton Neurosci 87:16–36PubMedGoogle Scholar
  389. 389.
    Stone TW (1981) Differential blockade of ATP, noradrenaline and electrically evoked contractions of the rat vas deferens by nifedipine. Eur J Pharmacol 74:373–376PubMedGoogle Scholar
  390. 390.
    Suzuki Y (1991) Contraction and prostaglandin biosynthesis by myometrium from non-pregnant and pregnant rabbits in response to adenosine 5′-triphosphate. Eur J Pharmacol 195:93–99PubMedGoogle Scholar
  391. 391.
    Tai CJ, Kang SK, Cheng KW, Choi KC, Nathwani PS, Leung PC (2000) Expression and regulation of P2U-purinergic receptor in human granulosa-luteal cells. J Clin Endocrinol Metab 85:1591–1597PubMedGoogle Scholar
  392. 392.
    Tai CJ, Kang SK, Choi KC, Tzeng CR, Leung PC (2001) Antigonadotropic action of adenosine triphosphate in human granulosa-luteal cells: involvement of protein kinase Cα. J Clin Endocrinol Metab 86:3237–3242PubMedGoogle Scholar
  393. 393.
    Tai CJ, Chang SJ, Leung PC, Tzeng CR (2004) Adenosine 5′-triphosphate activates nuclear translocation of mitogen-activated protein kinases leading to the induction of early growth response 1 and raf expression in human granulosa-luteal cells. J Clin Endocrinol Metab 89:5189–5195PubMedGoogle Scholar
  394. 394.
    Takahashi Y, Ishii N, Lue TF, Tanagho EA (1991) Pharmacological effects of adenosine on canine penile erection. Tohoku J Exp Med 165:49–58PubMedGoogle Scholar
  395. 395.
    Takahashi Y, Ishii N, Lue TF, Tanagho EA (1992) Effects of adenosine on canine penile erection. J Urol 148:1323–1325PubMedGoogle Scholar
  396. 396.
    Tassell W, Slater M, Barden JA, Murphy CR (2000) Endometrial cell death during early pregnancy in the rat. Histochem J 32:373–379PubMedGoogle Scholar
  397. 397.
    Tiemann U, Neels P, Küchenmeister U, Walzel H, Spitschak M (1996) Effect of ATP and platelet-activating factor on intracellular calcium concentrations of cultured oviductal cells from cows. J Reprod Fertil 108:1–9PubMedGoogle Scholar
  398. 398.
    Todorov L, Tashiro K, Hakoda H, Ito Y (1991) Possible role of the α1-adrenoceptor in the modulation of adrenergic co-transmission in the guinea-pig vas deferens. Biomed Res 12:365–376Google Scholar
  399. 399.
    Todorov LD, Mihaylova Todorova S, Westfall TD, Sneddon P, Kennedy C, Bjur RA, Westfall DP (1997) Neuronal release of soluble nucleotidases and their role in neurotransmitter inactivation. Nature 387:76–79PubMedGoogle Scholar
  400. 400.
    Todorov LD, Mihaylova-Todorova ST, Bjur RA, Westfall DP (1999) Differential cotransmission in sympathetic nerves: role of frequency of stimulation and prejunctional autoreceptors. J Pharmacol Exp Ther 290:241–246PubMedGoogle Scholar
  401. 401.
    Tomiyama T, Ohashi K, Tsutsui T, Saji F, Tanizawa O (1995) Acrosome reaction induced in a limited population of human spermatozoa by progesterone (Ca2+-dependent) and ATP (Ca2+-independent). Hum Reprod 10:2052–2055PubMedGoogle Scholar
  402. 402.
    Tong YC, Broderick G, Hypolite J, Levin RM (1992) Correlations of purinergic, cholinergic and adrenergic functions in rabbit corporal cavernosal tissue. Pharmacology 45:241–249PubMedGoogle Scholar
  403. 403.
    Tosca L, Froment P, Solnais P, Ferre P, Foufelle F, Dupont J (2005) Adenosine 5′-monophosphate-activated protein kinase regulates progesterone secretion in rat granulosa cells. Endocrinology 146:4500–4513PubMedGoogle Scholar
  404. 404.
    Tostes RC, Giachini FR, Carneiro FS, Leite R, Inscho EW, Webb RC (2007) Determination of adenosine effects and adenosine receptors in murine corpus cavernosum. J Pharmacol Exp Ther 322:678–685PubMedGoogle Scholar
  405. 405.
    Turmel P, Dufresne J, Hermo L, Smith CE, Penuela S, Laird DW, Cyr DG (2011) Characterization of pannexin1 and pannexin3 and their regulation by androgens in the male reproductive tract of the adult rat. Mol Reprod Dev 78:124–138PubMedGoogle Scholar
  406. 406.
    Urabe S, Miyoshi H, Fujiwara H, Yamaoka K, Kudo Y (2009) Enhanced expression of P2X4 and P2X7 purinergic receptors in the myometrium of pregnant rats in preterm delivery models. Reprod Sci 16:1186–1192PubMedGoogle Scholar
  407. 407.
    Urbach V, Harvey BJ (1999) Regulation of intracellular Ca2+ by CFTR in Chinese hamster ovary cells. J Membr Biol 171:255–265PubMedGoogle Scholar
  408. 408.
    Valdecantos P, Briones R, Moya P, Germain A, Huidobro-Toro JP (2003) Pharmacological identification of P2X1, P2X4 and P2X7 nucleotide receptors in the smooth muscles of human umbilical cord and chorionic blood vessels. Placenta 24:17–26PubMedGoogle Scholar
  409. 409.
    Valenzuela MA, Collados L, Kettlun AM, Mancilla M, Lara H, Puente J, Aranda E, Chayet L, Alvarez A, Traverso-Cori A (1992) Changes in apyrase activity in uterus and mammary gland during the lactogenic cycle. Comp Biochem Physiol B 103:113–118PubMedGoogle Scholar
  410. 410.
    Vander Kooy D, Dubyak GR, Moore RM, Moore JJ (1989) Adenosine triphosphate activates the phospholipase-C cascade system in human amnion cells without increasing prostaglandin production. Endocrinology 124:2005–2012PubMedGoogle Scholar
  411. 411.
    Vasudevan K, Sztein JM (2011) Treatment of sperm with extracellular adenosine 5′-triphosphate improves the in vitro fertility rate of inbred and genetically modified mice with low fertility. Theriogenology 76:729–736PubMedCentralPubMedGoogle Scholar
  412. 412.
    Vázquez-Cuevas FG, Juárez B, Garay E, Arellano RO (2006) ATP-induced apoptotic cell death in porcine ovarian theca cells through P2X7 receptor activation. Mol Reprod Dev 73:745–755PubMedGoogle Scholar
  413. 413.
    Vázquez-Cuevas FG, Zárate-Diaz EP, Garay E, Arellano RO (2010) Functional expression and intracellular signaling of UTP-sensitive P2Y receptors in theca-interstitial cells. Reprod Biol Endocrinol 8:88PubMedCentralPubMedGoogle Scholar
  414. 414.
    Veitinger S, Veitinger T, Cainarca S, Fluegge D, Engelhardt CH, Lohmer S, Hatt H, Corazza S, Spehr J, Neuhaus EM, Spehr M (2011) Purinergic signalling mobilizes mitochondrial Ca2+ in mouse Sertoli cells. J Physiol 589:5033–5055PubMedCentralPubMedGoogle Scholar
  415. 415.
    Venkova KM, Radomirov R, Petkov V (1985) Contractile responses of vas deferens from spontaneously hypertensive rats to electrical stimulation. C R Acad Bulg Sci 38:277Google Scholar
  416. 416.
    Ventura S, Pennefather JN (1991) Sympathetic co-transmission to the cauda epididymis of the rat: characterization of postjunctional adrenoceptors and purinoceptors. Br J Pharmacol 102:540–544PubMedCentralPubMedGoogle Scholar
  417. 417.
    Ventura S, Pennefather JN (1992) Inhibition of field stimulation-induced contractions of rat cauda epididymis by purinoceptor agonists but not by adrenoceptor agonists. J Auton Pharmacol 12:299–309PubMedGoogle Scholar
  418. 418.
    Ventura S, Dewalagama RK, Lau LC (2003) Adenosine 5′-triphosphate (ATP) is an excitatory cotransmitter with noradrenaline to the smooth muscle of the rat prostate gland. Br J Pharmacol 138:1277–1284PubMedCentralPubMedGoogle Scholar
  419. 419.
    Vigue C, Vigue L, Huszar G (1992) Adenosine triphosphate (ATP) concentrations and ATP/adenosine diphosphate ratios in human sperm of normospermic, oligospermic, and asthenospermic specimens and in their swim-up fractions: lack of correlation between ATP parameters and sperm creatine kinase concentrations. J Androl 13:305–311PubMedGoogle Scholar
  420. 420.
    Villalon MJ, Carolina Danovaro M, Hinds TR (1995) Intracellular calcium concentration increases in monkey oviductal ciliated cells after stimulation with extracellular ATP. Biol Reprod 52:145Google Scholar
  421. 421.
    Vlaskovska M, Kasakov L, Rong W, Bodin P, Bardini M, Cockayne DA, Ford APDW, Burnstock G (2001) P2X3 knockout mice reveal a major sensory role for urothelially released ATP. J Neurosci 21:5670–5677PubMedGoogle Scholar
  422. 422.
    von Kügelgen I, Bültmann R, Starke K (1989) Effects of suramin and α, β-methylene ATP indicate noradrenaline–ATP co-transmission in the response of the mouse vas deferens to single and low frequency pulses. Naunyn Schmiedebergs Arch Pharmacol 340:760–763Google Scholar
  423. 423.
    von Versen-Höynck F, Rajakumar A, Bainbridge SA, Gallaher MJ, Roberts JM, Powers RW (2009) Human placental adenosine receptor expression is elevated in preeclampsia and hypoxia increases expression of the A2A receptor. Placenta 30:434–442Google Scholar
  424. 424.
    Wali FA, Greenidge E (1989) Evidence that ATP and noradrenaline are released during electrical field stimulation of the rat isolated seminal vesicle. Pharmacol Res 21:397–404PubMedGoogle Scholar
  425. 425.
    Wang XF, Chan HC (2000) Adenosine triphosphate induces inhibition of Na+ absorption in mouse endometrial epithelium: a Ca2+-dependent mechanism. Biol Reprod 63:1918–1924PubMedGoogle Scholar
  426. 426.
    Wang XF, Tsang LL, So SC, Chan HC (2001) Suppression of ATP-induced Cl secretion by enhanced expression of epithelial Na+ channels in mouse endometrial epithelium. Cell Biol Int 25:1017–1020PubMedGoogle Scholar
  427. 427.
    Wang YT, Takiguchi Y, Uematsu T, Nakashima M (1991) Augmented responsiveness to sympathetic nerve stimulation of isolated vas deferens of diabetic rats. Arch Int Pharmacodyn Ther 309:160–169PubMedGoogle Scholar
  428. 428.
    Wasilenko WJ, Cooper J, Palad AJ, Somers KD, Blackmore PF, Rhim JS, Wright GL Jr, Schellhammer PF (1997) Calcium signaling in prostate cancer cells: evidence for multiple receptors and enhanced sensitivity to bombesin/GRP. Prostate 30:167–173PubMedGoogle Scholar
  429. 429.
    Welter-Stahl L, da Silva CM, Schachter J, Persechini PM, Souza HS, Ojcius DM, Coutinho-Silva R (2009) Expression of purinergic receptors and modulation of P2X7 function by the inflammatory cytokine IFNγ in human epithelial cells. Biochim Biophys Acta 1788:1176–1187PubMedGoogle Scholar
  430. 430.
    Wen J, Xia Y (2012) Adenosine signaling: good or bad in erectile function? Arterioscler Thromb Vasc Biol 32:845–850PubMedGoogle Scholar
  431. 431.
    Wen J, Dai Y, Zhang Y, Zhang W, Kellems RE, Xia Y (2011) Impaired erectile function in CD73-deficient mice with reduced endogenous penile adenosine production. J Sex Med 8:2172–2180PubMedCentralPubMedGoogle Scholar
  432. 432.
    Wen J, Grenz A, Zhang Y, Dai Y, Kellems RE, Blackburn MR, Eltzschig HK, Xia Y (2011) A2B adenosine receptor contributes to penile erection via PI3K/AKT signaling cascade-mediated eNOS activation. FASEB J 25:2823–2830PubMedCentralPubMedGoogle Scholar
  433. 433.
    Wen X, Perrett D, Jones N, Tozer AJ, Docherty SM, Iles RK (2010) High follicular fluid adenosine levels may be pivotal in the metabolism and recycling of adenosine nucleotides in the human follicle. Metabolism 59:1145–1155PubMedGoogle Scholar
  434. 434.
    Westfall DP, Stitzel RE, Rowe JN (1978) The postjunctional effects and neural release of purine compounds in the guinea-pig vas deferens. Eur J Pharmacol 50:27–38PubMedGoogle Scholar
  435. 435.
    Westfall TD, Westfall DP (2001) Pharmacological techniques for the in vitro study of the vas deferens. J Pharmacol Toxicol Methods 45:109–122PubMedGoogle Scholar
  436. 436.
    Westfall TD, Kennedy C, Sneddon P (1996) Enhancement of sympathetic purinergic neurotransmission in the guinea-pig isolated vas deferens by the novel ecto-ATPase inhibitor ARL 67156. Br J Pharmacol 117:867–872PubMedCentralPubMedGoogle Scholar
  437. 437.
    Westfall TD, Menzies JR, Liberman R, Waterston S, Ramphir N, Westfall DP, Sneddon P, Kennedy C (2000) Release of a soluble ATPase from the rabbit isolated vas deferens during nerve stimulation. Br J Pharmacol 131:909–914PubMedCentralPubMedGoogle Scholar
  438. 438.
    Wheeler CP, Yudilevich DL (1988) Transport and metabolism of adenosine in the perfused guinea-pig placenta. J Physiol 405:511–526PubMedCentralPubMedGoogle Scholar
  439. 439.
    White DR, Aitken RJ (1989) Relationship between calcium, cyclic AMP, ATP, and intracellular pH and the capacity of hamster spermatozoa to express hyperactivated motility. Gamete Res 22:163–177PubMedGoogle Scholar
  440. 440.
    Wiklund NP, Samuelson UE, Brundin J (1986) Adenosine modulation of adrenergic neurotransmission in the human fallopian tube. Eur J Pharmacol 123:11–18PubMedGoogle Scholar
  441. 441.
    Wong PY (1988) Control of anion and fluid secretion by apical P2-purinoceptors in the rat epididymis. Br J Pharmacol 95:1315–1321PubMedCentralPubMedGoogle Scholar
  442. 442.
    World Health Organization Task Force on the Prevention and Management of Infertility (1992) Adenosine triphosphate in semen and other sperm characteristics: their relevance for fertility prediction in men with normal sperm concentration. Fertil Steril 57:877–881Google Scholar
  443. 443.
    Wu HY, Broderick GA, Suh JK, Hypolite JA, Levin RM (1993) Effects of purines on rabbit corpus cavernosum contractile activity. Int J Impot Res 5:161–167PubMedGoogle Scholar
  444. 444.
    Xue J, Ruddock NT, Tecirlioglu RT, French AJ (2004) Effect of exogenous ATP on the development of parthenogenetically activated bovine oocytes. Biol Reprod SP ISS:217Google Scholar
  445. 445.
    Yamashiro H, Toyomizu M, Toyama N, Aono N, Sakurai M, Hiradate Y, Yokoo M, Moisyadi S, Sato E (2010) Extracellular ATP and dibutyryl cAMP enhance the freezability of rat epididymal sperm. J Am Assoc Lab Anim Sci 49:167–172PubMedCentralPubMedGoogle Scholar
  446. 446.
    Yang K, Hardy DB, Doumouras MA, van Beek JP, Rocha E (2002) ATP stimulates human placental 11beta-hydroxysteroid dehydrogenase type 2 activity by a novel mechanism independent of phosphorylation. J Cell Biochem 84:295–300PubMedGoogle Scholar
  447. 447.
    Yeung CH (1986) Temporary inhibition of the initiation of motility of demembranated hamster sperm by high concentrations of ATP. Int J Androl 9:359–370PubMedGoogle Scholar
  448. 448.
    Yildirim MK, Bagcivan I, Sarac B, Kilicarslan H, Yildirim S, Kaya T (2008) Effect of hypothyroidism on the purinergic responses of corpus cavernosal smooth muscle in rabbits. Int Urol Nephrol 40:691–699PubMedGoogle Scholar
  449. 449.
    Yoneyama Y, Sawa R, Suzuki S, Shin S, Power GG, Araki T (1996) The relationship between uterine artery Doppler velocimetry and umbilical venous adenosine levels in pregnancies complicated by preeclampsia. Am J Obstet Gynecol 174:267–271PubMedGoogle Scholar
  450. 450.
    Yoneyama Y, Suzuki S, Sawa R, Otsubo Y, Power GG, Araki T (2000) Plasma adenosine levels increase in women with normal pregnancies. Am J Obstet Gynecol 182:1200–1203PubMedGoogle Scholar
  451. 451.
    Yoneyama Y, Suzuki S, Sawa R, Araki T (2004) Plasma adenosine concentrations increase in women with hyperemesis gravidarum. Clin Chim Acta 342:99–103PubMedGoogle Scholar
  452. 452.
    Young JS, Brain KL, Cunnane TC (2007) Electrical and optical study of nerve impulse-evoked ATP-induced, P2X-receptor-mediated sympathetic neurotransmission at single smooth muscle cells in mouse isolated vas deferens. Neuroscience 148:82–91PubMedCentralPubMedGoogle Scholar
  453. 453.
    Yu Y, Dumollard R, Rossbach A, Lai FA, Swann K (2010) Redistribution of mitochondria leads to bursts of ATP production during spontaneous mouse oocyte maturation. J Cell Physiol 224:672–680PubMedCentralPubMedGoogle Scholar
  454. 454.
    Yuh IS, Jang BB, Hong BJ (1998) Effects of adenosine and epidermal growth factor on the growth of mouse mammary epithelial cells. Cell Biol Int 22:131–135PubMedGoogle Scholar
  455. 455.
    Zamoner A, Bruno AN, Casali EA, Corbelini PF, Diniz GP, Barreto-Chaves ML, Silva FR, Sarkis JJ, Pessoa-Pureur R (2006) Genomic-independent action of thyroid hormones on NTPDase activities in Sertoli cell cultures from congenital hypothyroid rats. Life Sci 80:51–58PubMedGoogle Scholar
  456. 456.
    Zhou L, Qi X, Potashkin JA, Abdul-Karim FW, Gorodeski GI (2008) Micro-RNAs miR-186 and miR-150 downregulate expression of the pro-apoptotic purinergic P2X7 receptor by activation of instability sites at the 3′-untranslated region of the gene that decrease steady-state levels of the transcript. J Biol Chem 283:28274–28286PubMedCentralPubMedGoogle Scholar
  457. 457.
    Zhou L, Luo L, Qi X, Li X, Gorodeski GI (2009) Regulation of P2X7 gene transcription. Purinergic Signal 5:409–426PubMedCentralPubMedGoogle Scholar
  458. 458.
    Zhu L, Li X, Zeng R, Gorodeski GI (2006) Changes in tight junctional resistance of the cervical epithelium are associated with modulation of content and phosphorylation of occludin 65-kilodalton and 50- kilodalton forms. Endocrinology 147:977–989PubMedCentralPubMedGoogle Scholar
  459. 459.
    Ziessen T, Cellek S (2002) Purines and pyrimidines are not involved in NANC relaxant responses in the rabbit vaginal wall. Br J Pharmacol 137:513–521PubMedCentralPubMedGoogle Scholar
  460. 460.
    Ziessen T, Moncada S, Cellek S (2002) Characterization of the non-nitrergic NANC relaxation responses in the rabbit vaginal wall. Br J Pharmacol 135:546–554PubMedCentralPubMedGoogle Scholar
  461. 461.
    Ziganshin AU, Zaitsev AP, Shamsutdinov AF (2002) Pharmacological characteristics of P2 receptors in human uterus. Bull Exp Biol Med 133:255–257PubMedGoogle Scholar
  462. 462.
    Ziganshin AU, Zaitzev AP, Khasanov AA, Shamsutdinov AF, Burnstock G (2006) Term-dependency of P2 receptor-mediated contractile responses of isolated human pregnant uterus. Eur J Obstet Gynecol Reprod Biol 129:128–134PubMedGoogle Scholar
  463. 463.
    Ziganshin AU, Vafina ZR, Fatkullin IF (2008) Contrasting effects of P2 receptor agonists on spontaneous contractility of human fallopian tubes with and without acute inflammation. Pharmacol Res 57:56–59PubMedGoogle Scholar
  464. 464.
    Zimon A, Erat A, Von Wald T, Bissell B, Koulova A, Choi CH, Bachvarov D, Reindollar RH, Usheva A (2006) Genes invoked in the ovarian transition to menopause. Nucleic Acids Res 34:3279–3287PubMedCentralPubMedGoogle Scholar

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© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  1. 1.Autonomic Neuroscience CentreUniversity College Medical SchoolLondonUK
  2. 2.Department of PharmacologyUniversity of MelbourneMelbourneAustralia

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