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Ca2+-modulated membrane guanylate cyclase in the testes

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Abstract

To date, the calcium-regulated membrane guanylate cyclase Rod Outer Segment Guanylate Cyclase type 1 (ROS-GC1) transduction system in addition to photoreceptors is known to be expressed in three other types of neuronal cells: in the pinealocytes, mitral cells of the olfactory bulb and the gustatory epithelium of tongue. Very recent studies from our laboratory show that expression of ROS-GC1 is not restricted to the neuronal cells; the male gonads and the spermatozoa also express ROS-GC1. In this presentation, the authors review the existing information on the localization and function of guanylate cyclase with special emphasis on Ca2+-modulated membrane guanylate cyclase, ROS-GC1, in the testes. The role of ROS-GC1 and its Ca2+-sensing modulators in the processes of spermatogenesis and fertilization are discussed.

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References

  1. Wedel BJ, Garbers DL (2001) The guanylate cyclase family at Y2 K. Annu Rev Physiol 63:215–233

    PubMed  CAS  Google Scholar 

  2. Kuhn M (2009) Function and dysfunction of mammalian membrane guanylyl cyclase receptors: lessons from genetic mouse models and implications for human diseases. Handb Exp Pharmacol 191:47–69

    PubMed  CAS  Google Scholar 

  3. Derbyshire ER, Marletta MA (2009) Biochemistry of soluble guanylate cyclase. Handb Exp Pharmacol 191:17–31

    PubMed  CAS  Google Scholar 

  4. Duda T, Sharma RK (2008) ONE-GC membrane guanylate cyclase, a trimodal odorant signal transducer. Biochem Biophys Res Commun 367:440–445

    PubMed  CAS  Google Scholar 

  5. Middendorff R, Davidoff MS, Behrends S, Mewe M, Miethens A, Muller D (2000) Multiple roles of the messenger molecule cGMP in testicular function. Andrologia 32:55–59

    PubMed  CAS  Google Scholar 

  6. Pascolini R, Spreca A, Lorvik S, Fagioli O, Fano G (1985) Ultracytochemical and biochemical evidence for guanylate cyclase in guinea pig testis. Anat Rec 212:277–281

    PubMed  CAS  Google Scholar 

  7. Marala RB, Sharma RK (1988) Characterization of atrial-natriuretic-factor-receptor-coupled membrane guanylate cyclase from rat and mouse testes. Biochem J 251:301–304

    PubMed  CAS  Google Scholar 

  8. Minamino N, Aburay M, Kojima M, Miyamoto K, Kangawa K, Matsuo H (1993) Distribution of C-type natriuertic peptide and its messenger RNA in rat central nervous system and peripheral tissue. Biochem Bipohys Res Commun 197:326–335

    CAS  Google Scholar 

  9. Middendorff R, Muller D, Paust HJ, Holstein AF, Davidoff MS (1997) New aspects of Leydig cell function. Adv Exp Med Biol 424:25–138

    Google Scholar 

  10. Middendorf R, Muller D, Wichers S, Holstein AF, Davidoff MS (1997) Evidence for production and functional activity of nitric oxide in seminiferous tubules and blood vessels of the human testes. J Clin Endocrinol Metab 82:4154–4161

    Google Scholar 

  11. Davidoff MS, Middendorff R, Mayer B, de Vente J, Koesling D, Holstein AF (1997) Nitric oxide/cGMP-pathway components in Leydig cells. Cell Tissue Res 287:61–170

    Google Scholar 

  12. Shi F, Perez E, Wang T, Peitz B, Lapolt PS (2005) Stage- and cell-specific expression of soluble guanylyl cyclase alpha and beta subunits, cGMP-dependent protein kinase I alpha and beta, and cyclic nucleotide-gated channel subunit 1 in the rat testis. J Androl 26:258–263

    PubMed  CAS  Google Scholar 

  13. Lee NP, Cheng CY (2008) Nitric oxide and cyclic nucleotides: their roles in junction dynamics and spermatogenesis. Oxid Med Cell Longev 1:25–32

    PubMed  Google Scholar 

  14. Lee NP, Cheng CY (2004) Nitric oxide/nitric oxide synthase, spermatogenesis, and tight junction dynamics. Biol Reprod 70:267–276

    PubMed  CAS  Google Scholar 

  15. Cheng CY, Mruk DD (2002) Cell junction dynamics in the testis: Sertoli-germ interaction and male contraceptive development. Physiol Rev 82:825–874

    PubMed  CAS  Google Scholar 

  16. Burnett AL (2006) Nitric oxide in the penis—science and therapeutic implications from erectile dysfunction to priapism. J Sex Med 3:578–582

    PubMed  CAS  Google Scholar 

  17. Champion HC, Bivalacqua TJ, Takimoto E, Kass DA, Burnett AL (2005) Phosphodiesterase-5A dysregulation in penile erectile tissue is a mechanism of priapism. Proc Natl Acad Sci USA 102:1661–1666

    PubMed  CAS  Google Scholar 

  18. Lefievre L, de Lamirande E, Gangon C (2000) The cyclic GMP-specific phosphodiesterase inhibitor, sidenafil, stimulates human sperm motility and capacitation but not acrosome reaction. J Androl 21:929–937

    PubMed  CAS  Google Scholar 

  19. Muller D, Mukhopadhyay AK, Speth RC, Guidone G, Potthast R, Potter LR, Middendorff R (2004) Spatiotemporal regulation of the two atrial natriuretic peptide receptors in testes. Endocrinology 145:1392–1401

    PubMed  Google Scholar 

  20. Mukhopadhyay AK, Bohnet HG, Leidenberger FA (1986) Testosterone production by mouse Leydig cells is stimulated in vitro by atrial natriuretic factor. FEBS Lett 202:111–116

    PubMed  CAS  Google Scholar 

  21. Pandey KN, Pavlou SN, Kovacs WJ, Inagami T (1986) Atrial natriuretic factor regulates steroidogenic responsiveness and cyclic nucleotide levels in mouse Leydig cells in vitro. Biochem Biophys Res Commun 138:399–404

    PubMed  CAS  Google Scholar 

  22. Mewe M, Bauer CK, Muller D, Middendorff R (2006) Regulation of spontaneous contractile activity in the bovine epididymal duct by the cyclic guanosine 5’-monophosphate-dependent pathway. Endocrinology 147:2051–2062

    PubMed  CAS  Google Scholar 

  23. Kim SZ, Kang SY, Lee SJ, Cho KW (2000) Localization of receptors for natriuretic peptide and endothelin in the duct of epididymis of the freshwater turtle. Gen Comp Endocrinol 118:26–38

    PubMed  CAS  Google Scholar 

  24. Jaleel M, London R, Eber SL, Forte LR, Visweswariah SS (2002) Expression of the receptor guanylate cyclase C and its ligands in reproductive tissue of rat: a potential role for novel signalling pathway in epididymis. Biol Reprod 67:1975–1980

    PubMed  CAS  Google Scholar 

  25. Kuhn M, Ng DCK, Su Y-H, Kilic A, Mitko D, Bien-Ly N, Komuves LG, Yang R-B (2004) Identification of an orphan guanylate cyclase receptor selectively expresses in mouse testis. Biochem J 379:385–393

    PubMed  CAS  Google Scholar 

  26. Huang YH, Wei CC, Su YH, Wu BT, Ciou YY, Tu CF, Cooper TG, Yeung CH, Chu ST, Tsai MT, Yang RB (2006) Localization and characterization of an orphan receptor, guanylyl cyclase-G, in mouse testis and sperm. Endocrinology 147:4792–4800

    PubMed  CAS  Google Scholar 

  27. Schultz S, Wedel BJ, Matthews A, Garbers DL (1998) The cloning and expression of new guanylyl cyclase orphan receptor. J Biol Chem 273:1032–1037

    Google Scholar 

  28. Fleischer J, Breer H, Strotmann J (2009) Mammalian olfactory receptors. Front Cell Neurosci 3:9

    PubMed  Google Scholar 

  29. Jankowska A, Burczynska B, Duda T, Warchol JB, Sharma RK (2007) Calcium-modulated rod outer segment membrane guanylate cyclase type 1 transduction machinery in the testes. J Androl 1:50–58

    Google Scholar 

  30. Jankowska A, Burczynska B, Duda T, Warchol JB (2008) Rod outer segment membrane guanylate cyclase type 1, ROS-GC1, calcium-modulated transduction system in the sperm. Fertil Steril 2008 Dec 24. Epub ahead of print

  31. Koch K-W (1991) Purification and identification of photoreceptor guanylate cyclase. J Biol Chem 266:8634–8637

    PubMed  CAS  Google Scholar 

  32. Stephen R, Filipek S, Palczewski K, Sousa MC (2008) Ca2+-dependent regulation of phototransduction. Photochem Photobiol 84:903–910

    PubMed  CAS  Google Scholar 

  33. Dizhoor AM, Olshevskaya EV, Henzel WJ, Wong SC, Stults JT, Ankoudinova I, Hurley JB (1995) Cloning, sequencing and expression of a 24-kDa Ca2+-binding protein activating photoreceptor guanylyl cyclase. J Biol Chem 270:25200–25206

    PubMed  CAS  Google Scholar 

  34. Frins S, Bonigk W, Muller F, Kellner R, Koch K-W (1996) Functional characterisation of guanylyl cyclase-activating protein from vertebrate rod. J Biol Chem 271:8022–8027

    PubMed  CAS  Google Scholar 

  35. Pozdnyakov N, Goraczniak R, Margulis A, Duda T, Sharma RK, Yoshida A, Sitaramayya A (1997) Structural and functional characterization of retinal calcium-dependent guanylate cyclase activator protein (CD-GCAP): identity with S100beta protein. Biochemistry 36:4159–14166

    Google Scholar 

  36. Haeseleer F, Sokal I, Li N, Pettenati M, Rao PN, Baehr W, Palczewski K (1999) Molecular characterisation of a third member of the guanylyl cyclase-activating protein subfamily. J Biol Chem 274:6526–6535

    PubMed  CAS  Google Scholar 

  37. Kumar VD, Vijay-Kumar S, Krishnan A, Duda T, Sharma RK (1999) A second calcium regulator of rod outer segment membrane guanylate cyclase, ROS-GC1: neurocalcin. Biochemistry 38:12614–12620

    PubMed  CAS  Google Scholar 

  38. Duda T, Goraczniak R, Surgucheva I, Rudnicka-Nawrot M, Gorczyca WA, Palczewski K, Sitaramayya A, Baehr W, Sharma RK (1996) Calcium modulation of bovine photoreceptor guanylate cyclase. Biochemistry 35:8478–8482

    PubMed  CAS  Google Scholar 

  39. Krishnan A, Goraczniak R, Duda T, Sharma RK (1998) Third calcium-modulated rod outer segment membrane guanylate cyclase transduction mechanism. Mol Cell Biochem 178:251–259

    PubMed  CAS  Google Scholar 

  40. Lange C, Duda T, Beyermann M, Koch K-W, Sharma RK (1999) Regions in vertebrate photoreceptor guanylyl cyclase ROS-GC1 involved in Ca2+-dependent regulation by guanylyl cyclase-activating protein GCAP-1. FEBS Lett 22:27–31

    Google Scholar 

  41. Sokal I, Haeseleer F, Arendt A, Adman ET, Hargrave PA, Palczewski K (1999) Identification of a guanylyl cyclase-activating protein-binding site within the catalytic domain of retinal guanylyl cyclase 1. Biochemistry 38:1387–1393

    PubMed  CAS  Google Scholar 

  42. Margulis A, Pozdnyakov N, Sitaramayya A (1996) Activation of bovine photoreceptor guanylate cyclase by S100 proteins. Biochem Biophys Res Commun 218:243–247

    PubMed  CAS  Google Scholar 

  43. Duda T, Krishnan A, Venkataraman V, Lange C, Koch K-W, Sharma RK (1999) Mutation in the rod outer segment membrane guanylate cyclase in a cone-rod dystrophy cause defects in calcium signaling. Biochemistry 38:13912–13919

    PubMed  CAS  Google Scholar 

  44. Venkataraman V, Duda T, Vardi N, Koch KW, Sharma RK (2003) Calcium-modulated guanylate cyclase transduction machinery in the photoreceptor-bipolar synaptic region. Biochemistry 40:5640–5648

    Google Scholar 

  45. Venkataraman V, Nagele R (2002) Calcium-sensitive ROS-GC1 signaling outside of photoreceptors: a common theme. Mol Cell Biochem 230:117–124

    PubMed  CAS  Google Scholar 

  46. Duda T, Venkataraman V, Krishnan A, Nagele RG, Sharma RK (2001) Negatively calcium-modulated membrane guanylate cyclase signaling system in the rat olfactory bulb. Biochemistry 40:4654–4662

    PubMed  CAS  Google Scholar 

  47. Duda T, Sharma RK (2004) S100B-modulated Ca2+-dependent ROS-GC1 transduction machinery in the gustatory epithelium: a new mechanism in gustatory transduction. FEBS Lett 577:393–398

    PubMed  CAS  Google Scholar 

  48. Goraczniak R, Duda T, Sharma RK (1998) Calcium modulated signaling in type 2 rod outer segment membrane guanylate cyclase (ROS-GC2). Biochem Biophys Res Commun 245:447–453

    PubMed  CAS  Google Scholar 

  49. Duda T, Jankowska A, Venkataraman V, Nagele R, Sharma RK (2001) A novel calcium-regulated guanylate cyclase transduction system in olfactory neuroepithelium. Biochemistry 40:12067–12077

    PubMed  CAS  Google Scholar 

  50. Koch K-W, Duda T, Sharma RK (2002) Photoreceptor specific guanylate cyclases in vertebrate phototransduction. Mol Cell Biochem 230:97–106

    PubMed  CAS  Google Scholar 

  51. Krishnan A, Venkataraman V, Fik-Rymarkiewicz E, Duda T, Sharma RK (2004) Structural, biochemical and functional characterization of the calcium sensor neurocalcin δ in the inner retinal neurons and its linkage with the rod outer segment membrane guanylate cyclase transudation system. Biochemistry 43:2708–2723

    PubMed  CAS  Google Scholar 

  52. Weyand IM, Goode S, Frings J, Weiner F, Muller W, Altenhofen H, Hatt H, Kaupp UB (1994) Cloning and functional expression of a cyclic-nucleotide-gated channels from mammalian sperm. Nature 368:859–863

    PubMed  CAS  Google Scholar 

  53. Frings SR, Seifert M, Godde M, Kaupp UB (1995) Profoundly different calcium permeation and blockage determinate the specific function of distinct cyclic nucleotide-gated channels. Neuron 15:169–179

    PubMed  CAS  Google Scholar 

  54. Wiesner B, Weiner J, Middendorff R, Hagen V, Kaupp UB, Weyand I (1998) Cyclic nucleotide-gated channels on the flagellum control Ca2+ entry into sperm. J Cell Biol 142:473–484

    PubMed  CAS  Google Scholar 

  55. Biel M, Zong X, Distler M, Bosse E, Klugbauer N, Murakami M, Flockerzi V, Hofmann F (1994) Another member of the cyclic nucleotide-gated channel family, expressed in testis, kidney and heart. Proc Natl Acad Sci USA 91:3505–3509

    PubMed  CAS  Google Scholar 

  56. Biel M, Zong X, Ludwig A, Sautter A, Hofmann F (1996) Molecular cloning and expression of the modulatory subunit of the cyclic nucleotide-gated channel. J Biol Chem 271:6349–6355

    PubMed  CAS  Google Scholar 

  57. Kaupp UB, Seifert R (2002) Cyclic nucleotide-gated ion channels. Physiol Rev 82:769–824

    PubMed  CAS  Google Scholar 

  58. Quill TA, Ren D, Clapham DE, Garbers DL (2001) A voltage-gated ion channel expressed specifically in spermatozoa. Prot Natl Acad Sci USA 98:12527–12531

    CAS  Google Scholar 

  59. Ren D, Navarro B, Perez G, Jackson AC, Hsu S, Shi Q, Tilly JL, Clapham DE (2001) A sperm ion channel required for sperm motility and male fertility. Nature 413:603–609

    PubMed  CAS  Google Scholar 

  60. Lobley A, Pierron V, Reynolds L, Allen L, Michalovich D (2003) Identification of human and mouse CatSper3 and CatSper4 genes: characterisation of a common interaction domain and evidence and evidence for expression in testis. Reprod Biol Endocrinol 1:53

    PubMed  Google Scholar 

  61. Nikpoor P, Mowla SJ, Movahedin M, Ziaee SA, Tiraihi T (2004) CatSper gene expression in postnatal development of mouse testes and in subfertile men with deficient sperm motility. Hum Reprod 19:124–128

    PubMed  Google Scholar 

  62. Quill TA, Sugden SA, Rossi KL, Doolittle LK, Hammer RE, Garbers DL (2003) Hyperactivated sperm motility driven by CatSper2 is required for fertilization. Prot Natl Acad Sci USA 100:14869–14874

    CAS  Google Scholar 

  63. Kobori H, Miyazaki S, Kuwabara Y (2000) Characterization of intracellular Ca2+ increase in response to progesterone and cyclic nucleotides in mouse spermatozoa. Biol Reprod 63:113–116

    PubMed  CAS  Google Scholar 

  64. Galindo BE, de la Vega-Beltran JL, Labarca P, Vacqueier VD, Darszon A (2007) Sp4tetraKCNG: a novel cyclic nucleotide gated K+-channel. Biochem Biophys Res Commun 354:668–675

    PubMed  CAS  Google Scholar 

  65. Strunker T, Weyand I, Bonigk W, Van Q, Loogen A, Brown JE, Kashikar N, Hagen V, Krause E, Kaupp UB (2006) A K+-selective cGMP-gated ion channel controls chemosensation of sperm. Nat Cell Biol 8:1149–1154

    PubMed  Google Scholar 

  66. Kaupp UB, Kashikar ND, Weyand I (2008) Mechanisms of sperm chemotaxis. Annu Rev Physiol 70:93–117

    PubMed  CAS  Google Scholar 

  67. Garbers DL (1989) Molecular basis of signalling in the spermatozoon. J Androl 10:99–107

    PubMed  CAS  Google Scholar 

  68. Repaske DR, Garbers DL (1983) A hydrogen ion flux mediates stimulation of respiratory activity by speract in sea urchin spermatozoa. J Biol Chem 258:1524–1529

    Google Scholar 

  69. Ward GE, Garbers DL, Vacqueir VD (1985) Effect of extracellular egg factors on sperm guanylate cyclase. Science 227:768–770

    PubMed  CAS  Google Scholar 

  70. Shapiro BM, Cook S, Quest AF, Oberdorf J, Wothe DJ (1990) Molecular mechanisms of sea-urchin sperm activation before fertilization. Reprod Fertil 42:3–8

    CAS  Google Scholar 

  71. Matsumoto M, Solzin J, Helbig A, Hagen V, Ueno S, Kawase O, Maruyama Y, Ogiso M, Godde M, Minakata H, Kaupp UB, Hoshi M, Weyand I (2003) A sperm-activating peptide controls a cGMP-signaling pathway in starfish sperm. Dev Biol 260:314–324

    PubMed  CAS  Google Scholar 

  72. Kaupp UB, Solzin J, Brown JE, Helbig A, Hagen V, Beyermann V, Hilderbrand M, Weyand I (2003) The signal flow controlling chemotaxis of sea urchin sperm. Nat Cell Biol 5:109–117

    PubMed  CAS  Google Scholar 

  73. Pacey AA, Hill CJ, Scudamore IW, Warren MA, Barratt CLR, Cooke ID (1993) The interaction in vitro of human spermatozoa with epithelial cells from the human uterine (Fallopian tube). Hum Reprod 10:360–366

    Google Scholar 

  74. Eisenbach M (2007) A hitchhiker’s guide trough advances and conceptual changes in chemotaxis. J Cell Physiol 213:574–580

    PubMed  CAS  Google Scholar 

  75. Williams M, Hill CJ, Scudamore IW, Dunphy B, Cooke ID, Barratt CLR (1993) Sperm numbers distribution within the human fallopian tube around ovulation. Hum Reprod 8:2019–2026

    PubMed  CAS  Google Scholar 

  76. Eisenbach M, Tur-Kaspa I (1999) Do human eggs attract spermatozoa? Bioessays 21:203–210

    PubMed  CAS  Google Scholar 

  77. Eisenbach M (2004) Towards understanding the molecular mechanism of sperm chemotaxis. J Gen Physiol 24:105–108

    Google Scholar 

  78. Bahat A, Eisenbach M (2006) Sperm chemotaxis. Mol Cell Endocrinol 252:115–119

    PubMed  CAS  Google Scholar 

  79. Steegers EAP, Hollanders JMG, Jongsma HW, Hein PR (1990) Atrial natriuretic peptide and progesterone in ovarian follicular fluid. Gynecol Obstet Invest 29:185–187

    Article  PubMed  CAS  Google Scholar 

  80. Zamir N, Riven-Kreitman R, Manor M, Makler S, Blumberg D, Ralt D, Eisenbach M (1993) Atrial natriuretic peptide attracts human spermatozoa in vitro. Biochem Biophys Res Commun 197:116–122

    PubMed  CAS  Google Scholar 

  81. Silvestroni L, Palleshi S, Guglielmi R, Tost-Croce C (1992) Identification and localisation of atrial natriuretic factor receptors in human spermatozoa. Arch Androl 28:75–82

    PubMed  CAS  Google Scholar 

  82. Spehr M, Gisselmann G, Poplawski A, Riffell JA, Wetzel CH, Zimmer RK, Hatt H (2003) Identification of a testicular odorant receptor mediating human sperm chemotaxis. Science 299:2054–2058

    PubMed  CAS  Google Scholar 

  83. Fukuda N, Yomogida K, Okabe M, Touhara K (2004) Functional characterization of a mouse testicular olfactory receptor and its role in chemosensing and in regulation of sperm motility. J Cell Sci 117:5835–5845

    PubMed  CAS  Google Scholar 

  84. Baldi E, Luconi M, Banaccorsi L, Forti GJ (2002) Signal transduction pathways in human spermatozoa. Reprod Immunol 53:121–131

    CAS  Google Scholar 

  85. Publicover S, Harper CV, Barrat C (2007) [Ca2+]i signalling in sperm—making the most of what you’ve got. Nat Cell Biol 9:235–242

    PubMed  CAS  Google Scholar 

  86. Lucas KA, Pitari GM, Kazerounian S, Ruiz-Stewart I, Park J, Schulz S, Chepenik KP, Weldman SA (2000) Guanylyl cyclases signalling by cyclic GMP. Pharm Rev 52:357–414

    Google Scholar 

  87. Spruill WA, Koide Y, Huang HL, Levine SN, Ong SH, Steiner AL, Beavo JA (1981) Immunocytochemical localization of cyclic guanosine monophosphate-dependent protein kinase in endocrine tissues. Endocrinology 109:2239–2248

    PubMed  CAS  Google Scholar 

  88. Pawson T, Scott JD (1997) Signaling through scaffold, anchoring, and adaptor proteins. Science 278:2075–2080

    PubMed  CAS  Google Scholar 

  89. Yuasa K, Omori K, Yanaka N (2000) Binding and phosphorylation of a novel male germ cell-specific cGMP-dependent protein kinase-anchoring protein by cGMP-dependent protein kinase Iα. J Biol Chem 275:4897–4905

    PubMed  CAS  Google Scholar 

  90. Zhang Q, Zhang F, Chen XH, Wang YQ, Wang WQ, Lin AA, Cavalli-Sforza LL, Jin L, Huo R, Sha JH, Li Z, Su B (2007) Rapid evolution, genetic variations, and functional association of the human spermatogenesis-related gene NYD-SP12. J Mol Evol 65:154–161

    PubMed  CAS  Google Scholar 

  91. Banu Y, Matsuda M, Yoshida M, Kondo M, Sutou S, Matsukuma S (2002) Golgi matrix protein gene, Golga3/Mea2, rearranged and reexpressed in pachytene spermatocytes restore spermatogenesis in the mouse. Mol Reprod Dev 61:288–301

    PubMed  CAS  Google Scholar 

  92. Bascom RA, Srinivascan S, Nussbaum RL (1999) Identification and characterization of Golgin-84, a novel Golgi integral membrane protein with a cytoplasmic coiled-coil domain. J Biol Chem 274:2953–2962

    PubMed  CAS  Google Scholar 

  93. Fan J, Graham M, Akabane H, Richardson LL, Zhu G-Z (2006) Identification of novel male germ-specific gene TESF-1 in mice. Biochem Biophys Res Commun 340:8–12

    PubMed  CAS  Google Scholar 

  94. Willipinski-Stapelfeld B, Lubberstedt J, Stelter S, Vogt K, Mukhopadyay AK, Muller D (2004) Comparative analysis between analysis between cyclic GMP and cyclic AMP signaling in human sperm. Mol Hum Reprod 10:543–552

    Google Scholar 

  95. Miraglia E, Rullo ML, Bosia A, Massobrio M, Revelli A, Ghigo D (2006) Stimulation of the nitric oxide/cyclic guanosine monophosphate signaling pathway elicits human sperm chemotaxis in vitro. Fertil Steril 87:1059–1063

    Google Scholar 

  96. Revelli A, Costamagna C, Moffa F, Aldieri E, Ochetti S, Bosia A, Massobrio M, Lindbloom B, Ghigio D (2001) Signaling pathways of nitric oxide-induced acrosome reaction in human sperm. Biol Reprod 64:1708–1712

    PubMed  CAS  Google Scholar 

  97. Zhang H, Hong H, Zhou B, Jin S, Wang Y, Fu M, Wang S, Xia G (2006) The expression of atrial natriuretic peptide in the oviduct and its function in pig spermatozoa. J Endocrinol 189:493–507

    PubMed  CAS  Google Scholar 

  98. Zhang H, Zhou Q, Li X, Zhao W, Wang Y, Liu H, Li N (2007) Ginsenoside RE promotes human sperm capacitation through nitric oxide-dependent pathway. Mol Reprod Dev 74:497–501

    PubMed  CAS  Google Scholar 

  99. Rotem R, Zamir N, Keynan N, Barkan D, Breitbarat H, Naor Z (1998) Atrial natriuretic peptide induces acrosomal exocytosis of human spermatozoa. Am J Physiol 274:218–223

    Google Scholar 

  100. Korschen HG, Beyerman M, Muller F, Heck M, Vantler M, Koch K-W, Kellner R, Wolfrum U, Bode C, Hofmann KP, Kaupp UB (1999) Interaction of glutamic-acid-rich proteins with cGMP signalling pathway in rod photoreceptors. Nature 400:761–766

    PubMed  CAS  Google Scholar 

  101. Rizzuto R, Pozzan T (2006) Microdomains of intracellular Ca2+: molecular determinants and functional consequences. Physiol Rev 86:369–408

    PubMed  CAS  Google Scholar 

  102. Clapham DE (2007) Calcium signaling. Cell 131:1047–1058

    PubMed  CAS  Google Scholar 

  103. Dupont G, Cambettes L, Leybaert L (2007) Calcium dynamics: spatio-temporal organization from the subcellular to organ level. Biol Reprod 77:551–559

    Google Scholar 

  104. Revelli A, Ghigo D, Moffa F, Massobrio M, Tur-Kaspa I (2002) Guanylate cyclase activity and sperm function. Endocr Rev 23:484–494

    PubMed  CAS  Google Scholar 

  105. Venkataraman V, Nagele R, Duda T, Sharma RK (2000) Rod outer segment membrane guanylate cyclase type 1-linked stimulatory and inhibitory calcium signaling systems in the pineal gland: biochemical, molecular, and immunohistochemical evidence. Biochemistry 39:6042–6052

    PubMed  CAS  Google Scholar 

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Acknowledgments

The author (A.J.) wishes to thank Dr. Teresa Duda for the cherished support in preparing this manuscript and for her continuous encouragement and Dr. Rameshwar K. Sharma for laying the groundwork and setting up the study.

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Jankowska, A., Warchol, J.B. Ca2+-modulated membrane guanylate cyclase in the testes. Mol Cell Biochem 334, 169–179 (2010). https://doi.org/10.1007/s11010-009-0329-5

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