Ontogeny of Purinergic Neurotransmission

  • Geoffrey Burnstock
  • Alexei Verkhratsky


Changes in the timing of expression of P1 and P2 purinoceptor subtypes occur during embryonic and postnatal development in both the peripheral and central nervous systems, as well as in the retina and inner ear. Purinergic signaling to embryonic stem cells is also considered.


Dorsal Root Ganglion Neuron Contractile Response Purinergic Signalling Postnatal Development Mesencephalic Trigeminal Nucleus 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Abe Y, Sorimachi M, Itoyama Y, Furukawa K, Akaike N (1995) ATP responses in the embryo chick ciliary ganglion cells. Neuroscience 64:547–551PubMedCrossRefGoogle Scholar
  2. Afework M, Burnstock G (2005) Changes in P2Y2 receptor localization on adrenaline- and noradrenaline containing chromaffin cells in the rat adrenal gland during development and ageing. Int J Dev Neurosci 23:567–573PubMedCrossRefGoogle Scholar
  3. Allgaier C, Wellmann H, Schobert A, von Kügelgen I (1995) Cultured chick sympathetic neurons: modulation of electrically evoked noradrenaline release by P2-purinoceptors. Naunyn Schmiedebergs Arch. Pharmacol. 352:17–24PubMedGoogle Scholar
  4. Anikina TA, Sitdikov FG, Khamzina EY, Bilalova GA (2005) Role of purinoceptors in cardiac function in rats during ontogeny. Bull Exp Biol Med 140:483–485PubMedCrossRefGoogle Scholar
  5. Baker OJ, Camden JM, Ratchford AM, Seye CI, Erb L, Weisman GA (2006) Differential coupling of the P2Y1 receptor to Gα14 and Gαq/11 proteins during the development of the rat salivary gland. Arch Oral Biol 51:359–370PubMedCrossRefGoogle Scholar
  6. Bao JX, Eriksson IE, Stjärne L (1989) Age-related variations in the relative importance of noradrenaline and ATP as mediators of the contractile response of rat tail artery to sympathetic nerve stimulation. Acta Physiol Scand 136:287–288PubMedCrossRefGoogle Scholar
  7. Bardoni R (2001) Excitatory synaptic transmission in neonatal dorsal horn: NMDA and ATP receptors. News Physiol Sci 16:95–100PubMedGoogle Scholar
  8. Bauman LA, Mahle CD, Boissard CG, Gribkoff VK (1992) Age-dependence of effects of A1 adenosine receptor antagonism in rat hippocampal slices. J Neurophysiol 68:629–638PubMedGoogle Scholar
  9. Bogdanov Y, Rubino A, Burnstock G (1998) Characerisation of subtypes of the P2X and P2Y families of receptors in the foetal human heart. Life Sci 62:697–703PubMedCrossRefGoogle Scholar
  10. Bogdanov YD, Dale L, King BF, Whittock N, Burnstock G (1997) Early expression of a novel nucleotide receptor in the neural plate of Xenopus embryos. J Biol Chem 272:12583–12590PubMedCrossRefGoogle Scholar
  11. Boldogköi Z, Schütz B, Sallach J, Zimmer A (2002) P2X3 receptor expression at early stage of mouse embryogenesis. Mech Dev 118:255–260PubMedCrossRefGoogle Scholar
  12. Braganhol E, Bruno AN, Bavaresco L, Barreto-Chaves ML, Sarkis JJ, Battastini AM (2006) Neonatal hypothyroidism affects the adenine nucleotides metabolism in astrocyte cultures from rat brain. Neurochem Res 31:449–454PubMedCrossRefGoogle Scholar
  13. Braun N, Sevigny J, Mishra SK, Robson SC, Barth SW, Gerstberger R, Hammer K, Zimmermann H (2003) Expression of the ecto-ATPase NTPDase2 in the germinal zones of the developing and adult rat brain. Eur J Neurosci 17:1355–1364PubMedCrossRefGoogle Scholar
  14. Brändle U, Kohler K, Wheeler-Schilling TH (1998) Expression of the P2X7-receptor subunit in neurons of the rat retina. Brain Res Mol Brain Res 62:106–109PubMedCrossRefGoogle Scholar
  15. Brosenitsch TA, Adachi T, Lipski J, Housley GD, Funk GD (2005) Developmental downregulation of P2X3 receptors in motoneurons of the compact formation of the nucleus ambiguus. Eur J Neurosci 22:809–824PubMedCrossRefGoogle Scholar
  16. Brouns I, Van Genechten J, Hayashi H, Gajda M, Gomi T, Burnstock G, Timmermans J-P, Adriaensen D (2003) Dual sensory innervation of pulmonary neuroepithelial bodies. Am J Respir Cell Mol Biol 28:275–285PubMedCrossRefGoogle Scholar
  17. Bruno AN, Ricachenevsky FK, Pochmann D, Bonan CD, Battastini AM, Barreto-Chaves ML, Sarkis JJ (2005) Hypothyroidism changes adenine nucleotide hydrolysis in synaptosomes from hippocampus and cerebral cortex of rats in different phases of development. Int J Dev Neurosci 23:37–44PubMedCrossRefGoogle Scholar
  18. Burnstock G (2001a) Purinergic signalling in lower urinary tract. In: Abbracchio MP, Williams M (eds) Handbook of experimental pharmacology, volume 151/I. Purinergic and pyrimidinergic signalling I—molecular, nervous and urinogenitary system function. Springer, Berlin, pp 423–515Google Scholar
  19. Burnstock G (2001b) Purinergic signalling in development. In: Abbracchio MP, Williams M (eds) Handbook of experimental pharmacology, volume 151/I. Purinergic and pyrimidinergic signalling I—molecular, nervous and urinogenitary system function. Springer, Berlin, pp 89–127Google Scholar
  20. Burnstock G, Ulrich H (2011) Purinergic signalling in embryonic and stem cell development. Cell Mol Life Sci 68:1369–1394Google Scholar
  21. Burnstock G, Wood JN (1996) Purinergic receptors: their role in nociception and primary afferent neurotransmission. Curr Opin Neurobiol 6:526–532PubMedCrossRefGoogle Scholar
  22. Casel D, Brockhaus J, Deitmer JW (2005) Enhancement of spontaneous synaptic activity in rat Purkinje neurons by ATP during development. J Physiol 568:111–122PubMedCrossRefGoogle Scholar
  23. Cheng J-T, Liu I-M, Juang S-W, Jou S-B (2000) Decrease of adenosine A-1 receptor gene expression in cerebral cortex of aged rats. Neurosci Lett 283:227–229PubMedCrossRefGoogle Scholar
  24. Cheung K–K, Burnstock G (2002) Localisation of P2X3 and co-expression with P2X2 receptors during rat embryonic neurogenesis. J Comp Neurol 443:368–382PubMedCrossRefGoogle Scholar
  25. Cheung K–K, Ryten M, Burnstock G (2003) Abundant and dynamic expression of G protein-coupled P2Y receptors in mammalian development. Dev Dyn 228:254–266PubMedCrossRefGoogle Scholar
  26. Cheung K–K, Chan WY, Burnstock G (2005) Expression of P2X receptors during rat brain development and their inhibitory role on motor axon outgrowth in neural tube explant cultures. Neuroscience 133:937–945PubMedCrossRefGoogle Scholar
  27. Choi RC, Siow NL, Cheng AW, Ling KK, Tung EK, Simon J, Barnard EA, Tsim KW (2003) ATP acts via P2Y1 receptors to stimulate acetylcholinesterase and acetylcholine receptor expression: transduction and transcription control. J Neurosci 23:4445–4456PubMedGoogle Scholar
  28. Collet C, Strube C, Csernoch L, Mallouk N, Ojeda C, Allard B, Jacquemond V (2002) Effects of extracellular ATP on freshly isolated mouse skeletal muscle cells during pre-natal and post-natal development. Pflugers Arch 443:771–778PubMedCrossRefGoogle Scholar
  29. Collo G, Neidhart S, Kawashima E, Kosco-Vilbois M, North RA, Buell G (1997) Tissue distribution of the P2X7 receptor. Neuropharmacology 36:1277–1283PubMedCrossRefGoogle Scholar
  30. Corsi C, Melani A, Bianchi L, Pepeu G, Pedata F (1999a) Striatal A2A adenosine receptors differentially regulate spontaneous and K+-evoked glutamate release in vivo in young and aged rats. NeuroReport 10:687–691PubMedCrossRefGoogle Scholar
  31. Corsi C, Melani A, Bianchi L, Pepeu G, Pedata F (1999b) Effect of adenosine A2A receptor stimulation on GABA release from the striatum of young and aged rats in vivo. Neuroreport 10:3933–3937PubMedCrossRefGoogle Scholar
  32. Costenla AR, de Mendonça A, Ribeiro JA (1999) Adenosine modulates synaptic plasticity in hippocampal slices from aged rats. Brain Res 851:228–234PubMedCrossRefGoogle Scholar
  33. Coutinho-Silva R, Parsons M, Robson T, Burnstock G (2001) Changes in expression of P2 receptors in rat and mouse pancreas during development and aging. Cell Tissue Res 306:373–383PubMedCrossRefGoogle Scholar
  34. Crowe R, Burnstock G (1981) Perinatal development of quinacrine-positive neurons in the rabbit gastrointestinal tract. J Auton Nerv Syst 4:217–230PubMedCrossRefGoogle Scholar
  35. Cunha RA, Constantino MC, Sebastiao AM, Ribeiro JA (1995) Modification of A1 and A2a adenosine receptor binding in aged striatum, hippocampus and cortex of the rat. Neuroreport 6:1583–1588PubMedCrossRefGoogle Scholar
  36. da Silva RL, Resende RR, Ulrich H (2007) Alternative splicing of P2X6 receptors in developing mouse brain and during in vitro neuronal differentiation. Exp Physiol 92:139–145PubMedCrossRefGoogle Scholar
  37. Dale N (2002) Resetting intrinsic purinergic modulation of neural activity: an associative mechanism? J Neurosci 22:10461–10469PubMedGoogle Scholar
  38. Delic J, Zimmermann H (2010) Nucleotides affect neurogenesis and dopaminergic differentiation of mouse fetal midbrain-derived neural precursor cells. Purinergic Signal 6:417–428PubMedCrossRefGoogle Scholar
  39. Devader C, Webb RJ, Thomas GM, Dale L (2006) Xenopus apyrase (xapy), a secreted nucleotidase that is expressed during early development. Gene 367:135–141PubMedCrossRefGoogle Scholar
  40. Dowling P, Ranson RN, Santer RM (2006) Age-associated changes in distribution of the P2X2 receptor in the major pelvic ganglion of the male rat. Neurosci Lett 404:320–323PubMedCrossRefGoogle Scholar
  41. Dunn PM, Gever J, Ruan H-Z, Burnstock G (2005) Developmental changes in heteromeric P2X2/3 receptor expression in rat sympathetic ganglion neurons. Dev Dyn 234:505–511PubMedCrossRefGoogle Scholar
  42. Dutton JL, Hansen MA, Balcar VJ, Barden JA, Bennett MR (1999) Development of P2X receptor clusters on smooth muscle cells in relation to nerve varicosities in the rat urinary bladder. J Neurocytol 28:4–16PubMedCrossRefGoogle Scholar
  43. Ekman M, Andersson KE, Arner A (2006) Developmental regulation of nerve and receptor mediated contractions of mammalian urinary bladder smooth muscle. Eur J Pharmacol 532:99–106PubMedCrossRefGoogle Scholar
  44. Evans MJ, Kaufman MH (1981) Establishment in culture of pluripotential cells from mouse embryos. Nature 292:154–156PubMedCrossRefGoogle Scholar
  45. Fu WM (1995) Regulatory role of ATP at developing neuromuscular junctions. Prog Neurobiol 47:31–44Google Scholar
  46. Fu WM, Chen YH, Lee KF, Liou JC (1997) Regulation of quantal transmitter secretion by ATP and protein kinases at developing neuromuscular synapses. Eur J Neurosci 9:676–685PubMedCrossRefGoogle Scholar
  47. Furness JB, Campbell GR, Gillard SM, Malmfors T, Cobb JL, Burnstock G (1970) Cellular studies of sympathetic denervation produced by 6-hydroxydopamine in the vas deferens. J Pharmacol Exp Ther 174:111–122PubMedGoogle Scholar
  48. Gage FH (2000) Mammalian neural stem cells. Science 287:1433–1438Google Scholar
  49. García-Lecea M, Sen RP, Soto F, Miras-Portugal MT, Castro E (2001) P2 receptors in cerebellar neurons: molecular diversity of ionotropic ATP receptors in Purkinje cells. Drug Dev Res 52:104–113Google Scholar
  50. Gauda EB, Northington FJ, Linden J, Rosin DL (2000) Differential expression of A2a, A1-adenosine and D2-dopamine receptor genes in rat peripheral arterial chemoreceptors during postnatal development. Brain Res 872:1–10PubMedCrossRefGoogle Scholar
  51. Gaytan SP, Saadani-Makki F, Bodineau L, Frugière A, Larnicol N, Pásaro R (2006) Effect of postnatal exposure to caffeine on the pattern of adenosine A1 receptor distribution in respiration-related nuclei of the rat brainstem. Auton. Neurosci. 126–127:339–346PubMedCrossRefGoogle Scholar
  52. Gershon MD, Thompson EB (1973) The maturation of neuromuscular function in a multiply innervated structure: development of the longitudinal smooth muscle of the foetal mammalian gut and its cholinergic excitatory, adrenergic inhibitory, and non-adrenergic inhibitory innervation. J Physiol 234:257–277PubMedGoogle Scholar
  53. Giaroni C, Knight GE, Zanetti E, Chiarelli RA, Lecchini S, Frigo G, Burnstock G (2006) Postnatal development of P2 receptors in the murine gastrointestinal tract. Neuropharmacology 50:690–704PubMedCrossRefGoogle Scholar
  54. Giovannelli L, Giovannini MG, Pedata F, Pepeu G (1988) Purinergic modulation of cortical acetylcholine release is decreased in aging rats. Exp Gerontol 23:175–181PubMedCrossRefGoogle Scholar
  55. Grimm I, Messemer N, Stanke M, Gachet C, Zimmermann H (2009) Coordinate pathways for nucleotide and EGF signaling in cultured adult neural progenitor cells. J Cell Sci 122:2524–2533PubMedCrossRefGoogle Scholar
  56. Grimm I, Ullsperger SN, Zimmermann H (2010) Nucleotides and epidermal growth factor induce parallel cytoskeletal rearrangements and migration in cultured adult murine neural stem cells. Acta Physiol (Oxf) 199:181–189CrossRefGoogle Scholar
  57. Hanahisa Y, Yamaguchi M (1998) Increase of Ca 2+-ATPase activity in the brain microsomes of rats with increasing ages: involvement of protein kinase C. Brain Res Bull 46:329–332PubMedCrossRefGoogle Scholar
  58. Heine C, Heimrich B, Vogt J, Wegner A, Illes P, Franke H (2006) P2 receptor-stimulation influences axonal outgrowth in the developing hippocampus in vitro. Neuroscience 138:303–311PubMedCrossRefGoogle Scholar
  59. Henning RH (1997) Purinoceptors in neuromuscular transmission. Pharmacol Ther 74:115–128PubMedCrossRefGoogle Scholar
  60. Heo JS, Han HJ (2006) ATP stimulates mouse embryonic stem cell proliferation via protein kinase C, phosphatidylinositol 3-kinase/Akt, and mitogen-activated protein kinase signaling pathways. Stem Cells 24:2637–2648PubMedCrossRefGoogle Scholar
  61. Hill CE, Phillips JK, Sandow SL (1999) Development of peripheral autonomic synapses: neurotransmitter receptors, neuroeffector associations and neural influences. Clin Exp Pharmacol Physiol 26:581–590PubMedCrossRefGoogle Scholar
  62. Hourani SMO (1999) Postnatal development of purinoceptors in rat visceral smooth muscle preparations. Gen Pharmacol 32:3–7PubMedCrossRefGoogle Scholar
  63. Housley GD, Luo L, Ryan AF (1998) Localization of mRNA encoding the P2X2 receptor subunit of the adenosine 5′-triphosphate-gated ion channel in the adult and developing rat inner ear by in situ hybridization. J Comp Neurol 393:403–414Google Scholar
  64. Huang H, Wu X, Nicol GD, Meller S, Vasko MR (2003) ATP augments peptide release from rat sensory neurons in culture through activation of P2Y receptors. J Pharmacol Exp Ther 306:1137–1144PubMedCrossRefGoogle Scholar
  65. Huang LC, Greenwood D, Thorne PR, Housley GD (2005) Developmental regulation of neuron-specific P2X3 receptor expression in the rat cochlea. J Comp Neurol 484:133–143PubMedCrossRefGoogle Scholar
  66. Huang LC, Ryan AF, Cockayne DA, Housley GD (2006) Developmentally regulated expression of the P2X3 receptor in the mouse cochlea. Histochem Cell Biol 125:681–692PubMedCrossRefGoogle Scholar
  67. Jang IS, Rhee JS, Kubota H, Akaike N, Akaike N (2001) Developmental changes in P2X purinoceptors on glycinergic presynaptic nerve terminals projecting to rat substantia gelatinosa neurons. J Physiol 536:505–519PubMedCrossRefGoogle Scholar
  68. Jo YH, Role LW (2002) Cholinergic modulation of purinergic and GABAergic co-transmission at in vitro hypothalamic synapses. J Neurophysiol 88:2501–2508PubMedCrossRefGoogle Scholar
  69. Johansson B, Georgiev V, Fredholm BB (1997) Distribution and postnatal ontogeny of adenosine A2A receptors in rat brain: comparison with dopamine receptors. Neuroscience 80:1187–1207PubMedCrossRefGoogle Scholar
  70. Kageyama S, Fujita K, Suzuki K, Shinbo H, Masuda N, Uchida W (2000) Effect of age on the responses of rat bladder detrusor strips to adenosine triphosphate. BJU Int 85:899–904PubMedCrossRefGoogle Scholar
  71. Khakh BS, Smith WB, Chiu CS, Ju D, Davidson N, Lester HA (2001) Activation-dependent changes in receptor distribution and dendritic morphology in hippocampal neurons expressing P2X2-green fluorescent protein receptors. Proc Natl Acad Sci U S A 98:5288–5293PubMedCrossRefGoogle Scholar
  72. Kidd EJ, Miller KJ, Sansum AJ, Humphrey PPA (1998) Evidence for P2X3 receptors in the developing rat brain. Neuroscience 87:533–539PubMedCrossRefGoogle Scholar
  73. Kolb HA, Wakelam MJO (1983) Transmitter-like action of ATP on patched membranes of cultured myoblasts and myotubes. Nature 303:621–623PubMedCrossRefGoogle Scholar
  74. Konduri GG, Forman K, Mital S (2000) Characterization of purine receptors in fetal lamb pulmonary circulation. Pediatr Res 47:114–120PubMedCrossRefGoogle Scholar
  75. Konishi C, Naito Y, Ohara N (1999) Age-related changes in adenosine 5′-triphosphate-induced constriction of isolated, perfused mesenteric arteries of rats. Life Sci 64:1265–1273PubMedCrossRefGoogle Scholar
  76. Laasberg T (1990) Ca2+-mobilizing receptors of gastrulating chick embryo. Comp Biochem Physiol C 97:9–12PubMedCrossRefGoogle Scholar
  77. Labrakakis C, Gerstner E, MacDermott AB (2000) Adenosine triphosphate-evoked currents in cultured dorsal root ganglion neurons obtained from rat embryos: desensitization kinetics and modulation of glutamate release. Neuroscience 101:1117–1126PubMedCrossRefGoogle Scholar
  78. León D, Albasanz JL, Ruiz MA, Fernandez M, Martin M (2002) Adenosine A1 receptor down-regulation in mothers and fetal brain after caffeine and theophylline treatments to pregnant rats. J Neurochem 82:625–634PubMedCrossRefGoogle Scholar
  79. Ling KK, Siow NL, Choi RC, Tsim KW (2005) ATP potentiates the formation of AChR aggregate in the co-culture of NG108-15 cells with C2C12 myotubes. FEBS Lett 579:2469–2474PubMedCrossRefGoogle Scholar
  80. Lopes LV, Cunha RA, Ribeiro JA (1999) Cross talk between A1 and A2A adenosine receptors in the hippocampus and cortex of young adult and old rats. J Neurophysiol 82:3196–3203PubMedGoogle Scholar
  81. MacDonald A, McGrath JC (1984) Post-natal development of functional neurotransmission in rat vas deferens. Br J Pharmacol 82:25–34PubMedCrossRefGoogle Scholar
  82. Majumder P, Trujillo CA, Lopes CG, Resende RR, Gomes KN, Yuahasi KK, Britto LR, Ulrich H (2007) New insights into purinergic receptor signaling in neuronal differentiation, neuroprotection, and brain disorders. Purinergic Signal. 3:317–331PubMedCrossRefGoogle Scholar
  83. Maric D, Maric I, Chang YH, Barker JL (2000) Stereotypical physiological properties emerge during early neuronal and glial lineage development in the embryonic rat neocortex. Cereb Cortex 10:729–747PubMedCrossRefGoogle Scholar
  84. Martin GR (1981) Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc Natl Acad Sci U S A 78:7634–7638PubMedCrossRefGoogle Scholar
  85. Martins AH, Alves JM, Trujillo CA, Schwindt TT, Barnabé GF, Motta FL, Guimarães AO, Casarini DE, Mello LE, Pesquero JB, Ulrich H (2008) Kinin-B2 receptor expression and activity during differentiation of embryonic rat neurospheres. Cytometry A 73:361–368PubMedGoogle Scholar
  86. Martins AH, Resende RR, Majumder P, Faria M, Casarini DE, Tarnok A, Colli W, Pesquero JB, Ulrich H (2005) Neuronal differentiation of P19 embryonal carcinoma cells modulates kinin B2 receptor gene expression and function. J Biol Chem 280:19576–19586PubMedCrossRefGoogle Scholar
  87. May C, Weigl L, Karel A, Hohenegger M (2006) Extracellular ATP activates ERK1/ERK2 via a metabotropic P2Y1 receptor in a Ca2+ independent manner in differentiated human skeletal muscle cells. Biochem Pharmacol 71:1497–1509PubMedCrossRefGoogle Scholar
  88. McBurney MW (1993) P19 embryonal carcinoma cells. Int J Dev Biol 37:135–140PubMedGoogle Scholar
  89. Meerlo P, Roman V, Farkas E, Keijser JN, Nyakas C, Luiten PG (2004) Ageing-related decline in adenosine A1 receptor binding in the rat brain: an autoradiographic study. J Neurosci Res 78:742–748PubMedCrossRefGoogle Scholar
  90. Meyer MP, Gröschel-Stewart U, Robson T, Burnstock G (1999) Expression of two ATP-gated ion channels, P2X5 and P2X6, in developing chick skeletal muscle. Dev Dyn 216:442–449PubMedCrossRefGoogle Scholar
  91. Miao LY, Tang JP, Esposito DP, Zhang JH (2001) Age-related changes in P2 receptor mRNA of rat cerebral arteries. Exp Gerontol 37:67–79PubMedCrossRefGoogle Scholar
  92. Molliver DC, Wright DE, Leitner ML, Parsadanian AS, Doster K, Wen D, Yan Q, Snider WD (1997) IB4-binding DRG neurons switch from NGF to GDNF dependence in early postnatal life. Neuron 19:849–861PubMedCrossRefGoogle Scholar
  93. Mooradian AD, Grabau G, Bastani B (1994) Adenosine triphosphatases of rat cerebral microvessels. Effect of age and diabetes mellitus. Life Sci 55:1261–1265PubMedCrossRefGoogle Scholar
  94. Moores TS, Hasdemir B, Vega-Riveroll L, Deuchars J, Parson SH (2005) Properties of presynaptic P2X7-like receptors at the neuromuscular junction. Brain Res 1034:40–50PubMedCrossRefGoogle Scholar
  95. Nakatsuka T, Mena N, Ling J, Gu JG (2001) Depletion of substance P from rat primary sensory neurons by ATP, an implication of P2X receptor-mediated release of substance P. Neuroscience 107:293–300PubMedCrossRefGoogle Scholar
  96. Narcisse L, Scemes E, Zhao Y, Lee SC, Brosnan CF (2005) The cytokine IL-1β transiently enhances P2X7 receptor expression and function in human astrocytes. Glia 49:245–258PubMedCrossRefGoogle Scholar
  97. Nedeljkovic N, Banjac A, Horvat A, Stojiljkovic M, Nikezic G (2005) Developmental profile of NTPDase activity in synaptic plasma membranes isolated from rat cerebral cortex. Int J Dev Neurosci 23:45–51PubMedCrossRefGoogle Scholar
  98. Nikolic P, Housley GD, Luo L, Ryan AF, Thorne PR (2001) Transient expression of P2X1 receptor subunits of ATP-gated ion channels in the developing rat cochlea. Brain Res Dev Brain Res 126:173–182PubMedCrossRefGoogle Scholar
  99. Nörenberg W, Gobel I, Meyer A, Cox SL, Starke K, Trendelenburg AU (2001) Stimulation of mouse cultured sympathetic neurons by uracil but not adenine nucleotides. Neuroscience 103:227–236PubMedCrossRefGoogle Scholar
  100. Norton WHJ, Rohr KB, Burnstock G (2000) Embryonic expression of a P2X3 receptor encoding gene in zebrafish. Mech Dev 99:149–152PubMedCrossRefGoogle Scholar
  101. Nunes PH, Calaza kDa C, Albuquerque LM, Fragel-Madeira L, Sholl-Franco A, Ventura AL (2007) Signal transduction pathways associated with ATP-induced proliferation of cell progenitors in the intact embryonic retina. Int J Dev Neurosci 25:499–508PubMedCrossRefGoogle Scholar
  102. O’Reilly BA, Kosaka AH, Chang TK, Ford AP, Popert R, Rymer JM, McMahon SB (2001) A quantitative analysis of purinoceptor expression in human fetal and adult bladders. J Urol 165:1730–1734PubMedCrossRefGoogle Scholar
  103. Paes de Carvalho R, Braas KM, Alder R, Snyder SH (1992) Developmental regulation of adenosine A1 receptors, uptake sites and endogenous adenosine in the chick retina. Brain Res Dev Brain Res 70:87–95CrossRefGoogle Scholar
  104. Pazzagli M, Corsi C, Fratti S, Pedata F, Pepeu G (1995) Regulation of extracellular adenosine levels in the striatum of aging rats. Brain Res 684:103–106PubMedCrossRefGoogle Scholar
  105. Pham TM, Morris JB, Arthur JF, Post GR, Brown JH, Woodcock EA (2003) UTP but not ATP causes hypertrophic growth in neonatal rat cardiomyocytes. J Mol Cell Cardiol 35:287–292PubMedCrossRefGoogle Scholar
  106. Phillips JK, Hill CE (1999) Neuroreceptor mRNA expression in the rat mesenteric artery develops independently of innervation. Int J Dev Neurosci 17:377–386PubMedCrossRefGoogle Scholar
  107. 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 122:1411–1416PubMedCrossRefGoogle Scholar
  108. Popoli P, Reggio R, Pezzola A, Fuxe K, Ferre S (1998) Adenosine A1 and A2A receptor antagonists stimulate motor activity: evidence for an increased effectiveness in aged rats. Neurosci Lett 251:201–204PubMedCrossRefGoogle Scholar
  109. Prediger RD, Batista LC, Takahashi RN (2005) Caffeine reverses age-related deficits in olfactory discrimination and social recognition memory in rats. Involvement of adenosine A1 and A2A receptors. Neurobiol Aging 26:957–964PubMedCrossRefGoogle Scholar
  110. Resende RR, Britto LR, Ulrich H (2008) Pharmacological properties of purinergic receptors and their effects on proliferation and induction of neuronal differentiation of P19 embryonal carcinoma cells. Int J Dev Neurosci 26:763–777PubMedCrossRefGoogle Scholar
  111. Resende RR, Majumder P, Gomes KN, Britto LR, Ulrich H (2007) P19 embryonal carcinoma cells as in vitro model for studying purinergic receptor expression and modulation of N-methyl-D-aspartate-glutamate and acetylcholine receptors during neuronal differentiation. Neuroscience 146:1169–1181PubMedCrossRefGoogle Scholar
  112. Ruan H-Z, Moules E, Burnstock G (2004) Changes in P2X purinoceptors in sensory ganglia of the mouse during embryonic and postnatal development. Histochem Cell Biol 122:539–551PubMedCrossRefGoogle Scholar
  113. Ruppelt A, Liang BT, Soto F (1999) Cloning, functional characterization and developmental expression of a P2X receptor from chick embryo. Prog Brain Res 120:81–90PubMedCrossRefGoogle Scholar
  114. Ruppelt A, Ma W, Borchardt K, Silberberg SD, Soto F (2001) Genomic structure, developmental distribution and functional properties of the chicken P2X5 receptor. J Neurochem 77:1256–1265PubMedCrossRefGoogle Scholar
  115. Ryten M, Hoebertz A, Burnstock G (2001) Sequential expression of three receptor subtypes for extracellular ATP in developing rat skeletal muscle. Dev Dyn 221:331–341PubMedCrossRefGoogle Scholar
  116. Ryten M, Dunn PM, Neary JT, Burnstock G (2002) ATP regulates the differentiation of mammalian skeletal muscle by activation of a P2X5 receptor on satellite cells. J Cell Biol 158:345–355PubMedCrossRefGoogle Scholar
  117. Ryten M, Koshi R, Knight GE, Turmaine M, Dunn PM, Cockayne DA, Ford APDW, Burnstock G (2007) Abnormalities in neuromuscular junction structure and skeletal muscle function in mice lacking the P2X2 nucleotide receptor. Neuroscience 148:700–711PubMedCrossRefGoogle Scholar
  118. Ryu JK, Choi HB, Hatori K, Heisel RL, Pelech SL, McLarnon JG, Kim SU (2003) Adenosine triphosphate induces proliferation of human neural stem cells: Role of calcium and p70 ribosomal protein S6 kinase. J Neurosci Res 72:352–362PubMedCrossRefGoogle Scholar
  119. Safiulina VF, Kasyanov AM, Sokolova E, Cherubini E, Giniatullin R (2005) ATP contributes to the generation of network-driven giant depolarizing potentials in the neonatal rat hippocampus. J Physiol 565:981–992PubMedCrossRefGoogle Scholar
  120. Safiulina VF, Afzalov R, Khiroug L, Cherubini E, Giniatullin R (2006) Reactive oxygen species mediate the potentiating effects of ATP on GABAergic synaptic transmission in the immature hippocampus. J Biol Chem 281:23464–23470PubMedCrossRefGoogle Scholar
  121. Saito M, Gotoh M, Kato K, Kondo A (1991) Influence of aging on the rat urinary bladder function. Urol Int 47:39–42PubMedCrossRefGoogle Scholar
  122. Sanches G, de Alencar LS, Ventura AL (2002) ATP induces proliferation of retinal cells in culture via activation of PKC and extracellular signal-regulated kinase cascade. Int J Dev Neurosci 20:21–27PubMedCrossRefGoogle Scholar
  123. Schiffmann SN, Vanderhaeghen JJ (1993) Age-related loss of mRNA encoding adenosine A2 receptor in the rat striatum. Neurosci Lett 158:121–124PubMedCrossRefGoogle Scholar
  124. Schwindt TT, Trujillo CA, Negraes PD, Lameu C, Ulrich H (2011) Directed differentiation of neural progenitors into neurons is accompanied by altered expression of P2X purinergic receptors. J Mol Neurosci 44:141–146PubMedCrossRefGoogle Scholar
  125. Sebastiao AM, Cunha RA, de MA, Ribeiro JA (2000) Modification of adenosine modulation of synaptic transmission in the hippocampus of aged rats. Br J Pharmacol 131:1629–1634PubMedCrossRefGoogle Scholar
  126. Shukla V, Zimmermann H, Wang L, Kettenmann H, Raab S, Hammer K, Sevigny J, Robson SC, Braun N (2005) Functional expression of the ecto-ATPase NTPDase2 and of nucleotide receptors by neuronal progenitor cells in the adult murine hippocampus. J Neurosci Res 80:600–610PubMedCrossRefGoogle Scholar
  127. Soto F, Krause U, Borchardt K, Ruppelt A (2003) Cloning, tissue distribution and functional characterization of the chicken P2X1 receptor. FEBS Lett 533:54–58PubMedCrossRefGoogle Scholar
  128. Sperlágh B, Zsilla G, Baranyi M, Kekes-Szabo A, Vizi ES (1997) Age-dependent changes of presynaptic neuromodulation via A1-adenosine receptors in rat hippocampal slices. Int J Dev Neurosci 15:739–747PubMedCrossRefGoogle Scholar
  129. Stellwagen D, Shatz CJ (2002) An instructive role for retinal waves in the development of retinogeniculate connectivity. Neuron 33:357–367PubMedCrossRefGoogle Scholar
  130. Sugioka M, Zhou WL, Hofmann HD, Yamashita M (1999) Involvement of P2 purinoceptors in the regulation of DNA synthesis in the neural retina of chick embryo. Int J Dev Neurosci 17:135–144PubMedCrossRefGoogle Scholar
  131. Sugioka M, Fukuda Y, Yamashita M (1996) Ca2+ responses to ATP via purinoceptors in the early embryonic chick retina. J Physiol 493:855–863PubMedGoogle Scholar
  132. Syed MM, Lee S, Zheng J, Zhou ZJ (2004) Stage-dependent dynamics and modulation of spontaneous waves in the developing rabbit retina. J Physiol 560:533–549PubMedCrossRefGoogle Scholar
  133. Tarnok A, Ulrich H (2001) Characterization of pressure-induced calcium response in neuronal cell lines. Cytometry 43:175–181Google Scholar
  134. Thiruchelvam N, Wu C, David A, Woolf AS, Cuckow PM, Fry CH (2003) Neurotransmission and viscoelasticity in the ovine fetal bladder after in utero bladder outflow obstruction. Am J Physiol Regul Integr Comp Physiol 284:R1296–R1305PubMedGoogle Scholar
  135. Thompson CS, Kenney WL (2004) Altered neurotransmitter control of reflex vasoconstriction in aged human skin. J Physiol 558:697–704PubMedCrossRefGoogle Scholar
  136. Torres IL, Battastini AM, Buffon A, Furstenau CR, Siqueira I, Sarkis JJ, Dalmaz C, Ferreira MB (2003) Ecto-nucleotidase activities in spinal cord of rats changes as function of age. Int J Dev Neurosci 21:425–429PubMedCrossRefGoogle Scholar
  137. Trujillo CA, Schwindt TT, Martins AH, Alves JM, Mello LE, Ulrich H (2009) Novel perspectives of neural stem cell differentiation: from neurotransmitters to therapeutics. Cytom A 75:38–53CrossRefGoogle Scholar
  138. Tugay M, Yildiz F, Utkan T, Gacar N, Ulak G, Erden F (2003) Age-related smooth muscle reactivity changes in the rat bladder: an in vitro study. Pharmacol Res 48:329–334PubMedCrossRefGoogle Scholar
  139. Ulrich H, Majumder P (2006) Neurotransmitter receptor expression and activity during neuronal differentiation of embryonal carcinoma and stem cells: from basic research towards clinical applications. Cell Prolif 39:281–300Google Scholar
  140. Virus RM, Baglajewski T, Radulovacki M (1984) [3H]N6-(L-Phenylisopropyl) adenosine binding in brains from young and old rats. Neurobiol Aging 5:61–62PubMedCrossRefGoogle Scholar
  141. Wakade TD, Palmer KC, McCauley R, Przywara DA, Wakade AR (1995) Adenosine-induced apoptosis in chick embryonic sympathetic neurons: a new physiological role for adenosine. J Physiol 488:123–138PubMedGoogle Scholar
  142. Wallace A, Knight GE, Cowen T, Burnstock G (2006) Changes in function and expression of P2X and P2Y receptors in the rat tail and mesenteric arteries during maturation and aging. Neuropharmacology 50:191–208PubMedCrossRefGoogle Scholar
  143. Weissman TA, Riquelme PA, Ivic L, Flint AC, Kriegstein AR (2004) Calcium waves propagate through radial glial cells and modulate proliferation in the developing neocortex. Neuron 43:647–661PubMedCrossRefGoogle Scholar
  144. Wells DG, Zawisa MJ, Hume RI (1995) Changes in responsiveness to extracellular ATP in chick skeletal muscle during development and upon dennervation. Dev Biol 172:585–590PubMedCrossRefGoogle Scholar
  145. Wuest M, Morgenstern K, Graf EM, Braeter M, Hakenberg OW, Wirth MP, Ravens U (2005) Cholinergic and purinergic responses in isolated human detrusor in relation to age. J Urol 173:2182–2189PubMedCrossRefGoogle Scholar
  146. Xiang Z, Burnstock G (2004) Development of nerves expressing P2X3 receptors in the myenteric plexus of rat stomach. Histochem Cell Biol 122:111–119PubMedCrossRefGoogle Scholar
  147. Xiang Z, Burnstock G (2005) Changes in expression of P2X purinoceptors in rat cerebellum during postnatal development. Dev Brain Res 156:147–157CrossRefGoogle Scholar
  148. Yoshida M, Miyamae K, Iwashita H, Otani M, Inadome A (2004) Management of detrusor dysfunction in the elderly: changes in acetylcholine and adenosine triphosphate release during aging. Urology 63:17–23PubMedCrossRefGoogle Scholar
  149. Zagorodnyuk V, Hoyle CHV, Burnstock G (1993) An electrophysiological study of developmental changes in the innervation of the guinea-pig taenia coli. Pflugers Arch 423:427–433PubMedCrossRefGoogle Scholar
  150. Zhu Y, Kimelberg HK (2001) Developmental expression of metabotropic P2Y1 and P2Y2 receptors in freshly isolated astrocytes from rat hippocampus. J Neurochem 77:530–541PubMedCrossRefGoogle Scholar
  151. Zimmermann H (2006) Nucleotide signaling in nervous system development. Pflugers Arch 452:573–588PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  1. 1.Autonomic Neuroscience CentreUniversity College Medical SchoolLondonUK
  2. 2.Faculty of Life SciencesUniversity of ManchesterManchesterUK

Personalised recommendations