Activation of GABA_A Receptor/Cl⁻ Channel and Capacitation in Rat Spermatozoa: HCO₃⁻ and Cl⁻ are Essential

References

• Ashcroft, F. M. Ion Channels and Disease. Acadermic Press, LondonUK 2000
   Google Scholar
• Austin C. R. The “capacitation” of the mammalian sperm. Nature 1952; 170: 326
   PubMed Web of Science ®Google Scholar
• Barboni B., Mattioli M., Seren E. Influence of progesterone on boar sperm capacitation. J Endocrinol 1995; 144: 13–18
   Google Scholar
• Burkman L. J., Overstreet J. M., Katz D. F. A possible role for potassium and pyruvate in the modulation of sperm motility in the rabbit oviductal isthmus. J Reprod Fertil 1984; 71: 367–376
   Google Scholar
• Calogero A. E., Burerello N., Ferrara E., Hall J., Fishei S., D'agata R. γ-Aminobutyric acid (GABA) A and B receptor mediate the stimulatory effects of GABA on the human sperm acrosome reaction: interaction with progesterone. Fertil Steril 1999; 71: 930–936
   PubMed Web of Science ®Google Scholar
• Calogero A. E., Hall J., Fishel S., Green S., Hunter A., D'Agata R. Effects of gamma-aminobutyric acid on human sperm motility and hyperactivation. Mol Hum Reprod 1996; 2: 733–738
   PubMedGoogle Scholar
• Cancel A. M., Lobdell D., Mendola P., Perreault S. D. Objective evaluation of hyperactivated motility in rat spermatozoa using computer-assisted sperm analysis. Hum Reprod 2000; 6: 1322–1328
   Google Scholar
• Cann M. Bicarbonate stimulated adenylyl cyclases. IUBMB Life 2004; 56: 529–534
   Google Scholar
• Celotti F., Apud J. A., Rovescalli A. C., Metcangi R. C., Negri-Cesi P., Racagni G. The GABAergic extrinsic innervation of the rat fallopian tubes; biochemical evidence and endocrine modulation. Adv Biochem Psychopharmacol 1986; 42: 251–264
   Google Scholar
• Chan H. C., Shi Q. X., Zhou C. X., Wang X. F., Xu W. M., Chen W. Y., Chen A. J., Ni Y., Yuan Y. Y. Critical role of CFTR in uterine bicarbonate secretion and the fertilizing capacity of sperm. Mol Endocrinol 2006; 250: 106–113
   Google Scholar
• Chan H. C., Zhou T. S., Fu W. O., Wang W. P., Shi Y. L., Wang P. Y. D. Cation and anion channels in rat and human spermatozoa. Biochim Biophys Acta 1997; 1323: 117–129
   Google Scholar
• Chang M. C. Fertilizing capacity of spermatozoa deposited in fallopian tubes. Nature 1951; 168: 997–998
   Google Scholar
• Chen Y., Cann M. J., Litvin T. N., Iourgenko V., Sinclair M. L., Levin L. R., Buck J. Soluble adenyl cyclase as an evolutionarily conserved bicarbonate sensor. Science 2000; 289: 625–628
   PubMed Web of Science ®Google Scholar
• DasGupta S., O'Toole C., Mills C. L., Frasser L. R. Effect of pentoxifylline and progesterone on human sperm capacitation and acrosomal exocytosis. Hum Reprod 1994; 9: 2103–2109
   Google Scholar
• De las Heras M. A., Valcarcel A., Perez L. J. In vitro capacitating effect of gamma-aminobutyric acid in ram spermatozoa. Biol Reprod 1997; 56: 964–968
   Google Scholar
• Espinosa F., De la Vega-Beltran J. L., Lopez-Gonzalez I., Delgado R., Labarca P., Darszon A. Mouse sperm patch-clamp recordings reveal single Cl− channels sensitive to niflumic acid, a blocker of the sperm acrosome reaction. FEBS Letters 1998; 426: 47–51
   Google Scholar
• Erdo S. L., Rosdy B., Szporny L. Higheer GABA concentrations in fallopian tube than in brain of the rat. J Neurochem 1982; 38: 1174–1176
   PubMed Web of Science ®Google Scholar
• Erdo S. L., Wekerle L. GABAA type binding sites on membranes of spermatozoa. Life Sci 1990; 47: 1147–1151
   Google Scholar
• Ewert M., Shivers B. D., Luddens H., Mohler H., Seeburg P. H. Subunit selectivity and epitope characterization of mAbs directed against the GABAA/benzodiazepine receptor. J Cell Biol 1990; 110: 2043–2048
   Google Scholar
• Falkenstein E., Heck M., Gerdes D., Grube D., Christ M., Weigel M., Buddhikot M., Meizel S., Wehling M. Specific progesterone binding to a membrane protein and related nongenomic effects on Ca2+-fluxes in sperm. Endocrinol 1999; 140: 5999–6002
   PubMed Web of Science ®Google Scholar
• Fassio A., Rossi F., Bonanno G., Raiteri M. GABA induces norepinephrine exocytosis from hippocampal noradrenergic axon terminals by a dual mechanism involving different voltage-sensitive calcium channels. J Neurosci Res 1999; 57: 324–331
   Google Scholar
• Florman, H. M. and Babcock, D. F. (1991) Progress toward understanding the molecular basis of capacitation. In: Wassarman, P. M. (Ed.), Elements of Mammalian Fertilization, vol. 1. Boca Raton: CRC Press; pp. 105–132
   Google Scholar
• Fraser L. R. Potassium ions modulate expression of mouse sperm fertilizing ability, acrosome reaction and Hyperactivated motility in vitro. J Reprod Fertil 1983; 69: 539–353
   PubMedGoogle Scholar
• Hernandez-Gonzalez E. O., Trevino C. L., Castellano L. E., Vega-Beltran J. L., Ocampo A. Y., Visconti P. E., Darszon A. Involvement of Cystic Fibrosis Transmembrane Conductance Regulator in mouse sperm capacitation. J. Biol. Chem 2007; 232: 24397–24406
   Google Scholar
• Hoger P. U., French A. S., Torkkeli P. H. Contributions of Voltage-and Ca2+-activated conductances to GABA-induced depolarization in spider mechanosory neurons. J Neurophysiol 2008; 99: 1596–1606
   Google Scholar
• Hu J. H., He X. B., Wu Q., Yan Y. C., Koide S. S. Biphasic effect of GABA on rat sperm acrosome reaction: involvement of GABA (A) and GABA (B) receptors. Arch Androl 2002a; 48: 369–378
   PubMed Web of Science ®Google Scholar
• Hu J. H., He X. B., Wu Q., Yan Y. C., Koide S. S. Subunit composition and function of GABAA receptors of rat spermatozoa. Neurochem Res 2002b; 27: 195–199
   Google Scholar
• Hyne R. V., Edwards K. P., Lopata A., Smith J. D. Changes in guinea pig sperm intracellular sodium and potassium content during capacitation and treatment with monovalent ionophores. Gamete Res 1985; 12: 65–73
   Google Scholar
• Isomura Y., Sugimoto M., Fujiwara-Tsukamoto Y., Yamamoto-Muraki S., Yamada J., Fukuda A. Synaptically activated Cl− accumulation responsible for depolarizing GABAergic responses in mature hippocampal neurons. J Neurophysiol 2003; 90(4)2752–2756
   Google Scholar
• Jaiswal B. S., Eisenbach M. Capacitation. Fertilization, D. M. Hardy. Academic Press, San Diego 2002; 57–117
   Google Scholar
• Kaila K. Ionic basis of GABAA receptor channel function in the nervous system. Progress in Neurobiology 1994; 42: 489–537
   PubMed Web of Science ®Google Scholar
• Kanbara K., Okamoto K., Nomura S., Kaneko T., Shigemoto R., Azuma H., Katsuoka Y., Watanabe M. Cellular localization of GABA and GABAB receptor subunit proteins during spermiogenesis in rat testis. J Andro 2005; 26: 485–493
   Google Scholar
• Lee M. A., Storey B. T. Bicarbonate is essential for fertilization of mouse eggs: mouse sperm require it to undergo the acrosome reaction. Biol Reprod 1986; 34: 349–356
   PubMedGoogle Scholar
• Meizel S. The sperm, a neuron with a tail: ‘neuronal’ receptors in mammalian sperm. Biol Rev 2004; 79: 713–732
   PubMed Web of Science ®Google Scholar
• Melendrez C. S., Meizel S. Studies of porcine and human sperm suggesting a role for a sperm glycine receptor/Cl− channel in the zona pellucida-initiated acrosome reaction. Biol Reprod 1995; 53: 676–683
   Google Scholar
• Murashima Y. L., Kato T. Distribution of gamma-aminobutyric acid and glutamate decarboxylase in the layers of rat oviduct. J Neurochem 1986; 46: 166–172
   PubMed Web of Science ®Google Scholar
• Neill J. M., Olds-Clarke P. A computer-assisted assay for mouse sperm hyperactivation demonstrates that bicarbonate but not bovine serum albumin is required. Gamete Res 1987; 18: 121–140
   PubMedGoogle Scholar
• Oberlander G., Yeung C. H., Cooper T. G. Influence of oral administration of ornidazole on capacitation and the activity of some glycolytic enzymes of rat spermatozoa. J Reprod Fertil 1996; 106: 231–239
   PubMedGoogle Scholar
• Poulsen J. H., Fischer H., Illek B., Machen T. E. Bicarbonate conductance and pH regulatory capability of cystic fibrosis transmembrane conductance regulator. Proc Natl Acad Sci USA 1994; 91: 5340–5344
   PubMed Web of Science ®Google Scholar
• Reddy M. M., Quinton P. M. Selective activation of cystic fibrosis transmembrane conductance regulator Cl− and HCO3− conductance. J Pancreas 2001; 2: 212–218
   Google Scholar
• Ritta M. N., Calamera J. C., Bas D. E. Occurrence of GABA and GABA receptors in human spermatozoa. Mol Hum Reprod 1998; 4: 769–773
   PubMed Web of Science ®Google Scholar
• Roldan E. R. S., Murase T., Shi Q. X. Exocytosis in spermatozoa in response to progesterone and zona pellicida. Science 1994; 266: 1578–1581
   PubMedGoogle Scholar
• Shalgi R. A Comparative Overview of mammalian Fertilization. Fertilization in Rat, B. S. Dunbar, M. G. O'Rand. Plenum Press, New York 1991; 245–255
   Google Scholar
• Shalgi R., Phillips D. M. Motility of rat spermatozoa at the site of fertilization. Biol Reprod 1988; 39: 1207–1213
   Google Scholar
• Shi Q. X., Roldan E. R. S. Bicarbonate/CO2 is not required for zona pellucida- or progesterone-induced acrosomal exocytosis of mouse spermatozoa but is essential for capacitation. Biol Reprod 1995a; 52: 540–546
   PubMedGoogle Scholar
• Shi Q. X., Roldan E. R. S. Evidence that a GABAA-like receptor is involved in progesterone-induced acrosomal exocytosis in mouse spermatozoa. Biol Reprod 1995b; 52: 373–381
   PubMed Web of Science ®Google Scholar
• Shi Q. X., Yuan Y. Y., Roldan E. R. S. gamma-Aminobutyric acid (GABA) induces the acrosome reaction in human spermatozoa. Mol Hum Reprod 1997; 3: 677–683
   PubMed Web of Science ®Google Scholar
• Sieghart W. Structure, pharmacology and function of GABAA receptor subtypes. Adv Pharmacol 2006; 54: 231–263
   PubMedGoogle Scholar
• Staley K. J., Proctor W. R. Modulation of mammalian dendritic GABA(A) receptor function by the kinetics of Cl− and HCO3− transport. J Physiol 1999; 519.3: 693–712
   Google Scholar
• Suarez S. S. Hyperactivated motility in sperm. J Androl 1996; 17: 331–335
   PubMedGoogle Scholar
• Suarez S. S., Dai X. Hyperactivation enhances mouse sperm capacity for penetrating viscoelastic media. Biology of Reproduction 1992; 46: 686–691
   PubMed Web of Science ®Google Scholar
• Turner K. O., Garcia M. A., Meizel S. Progesterone initiation of the human sperm acrosome reaction: the obligatory increase in intracellular calcium is independent of the chloride requirement. Mol Cell Endocrinol 1994; 101: 221–225
   Google Scholar
• Uhler M. L., Leung A., Ghan S. Y., Wang G. Direct effects of progesterone and antiprogesterone on human sperm hyperactivated motility and acrosome reaction. Fertil. Steril. 1992; 58: 1191–1198
   PubMed Web of Science ®Google Scholar
• Visconti P. E., Bailey J. L., Moore G. D., Pan D., Olds-Clarke P., Kopf G. S. Capacitation of mouse spermatozoa. I. Correlation between the capacitation state and protein tyrosine phosphorylation. Development 1995; 121: 1129–1137
   PubMed Web of Science ®Google Scholar
• Visconti P. E., Galantinohomer H., Moore G. D., Bailey J. L., Ning X. P., Fornes M., Kopf G. S. The molecular basis of sperm capacitation. J Androl 1998; 19: 242–248
   PubMedGoogle Scholar
• Visconti P. E., Westbrook V. A., Chertithin O., Demarco I., Sleight S., Diekman A. B. Novel signaling pathways involved in sperm acquisition of fertilizing capacity. J Reprod Immunol 2002; 53: 133–150
   PubMed Web of Science ®Google Scholar
• Wang X. F., Zhou C. X., Shi Q. X., Yuan Y. Y., Yu M. K., Ajonuma L. C., Ho L. S., Lo P. S., Tsang L. L., Liu Y., et al. Involvement of CFTR in uterine bicarbonate secretion and the fertilizing capacity of sperm. Nat Cell Biol 2003; 5: 902–906
   PubMed Web of Science ®Google Scholar
• Williams B., Bence M., Evert H., Forrest-Owen W., Lightman S. L., Mcardle C. A. GABAA receptor mediated elevation of Ca2+ and modulation of gonadotropin-release hormone action in alpha T3-1 gonadotropin. J Neroendocrinol 2000; 12: 159–166
   Google Scholar
• Wistrom C. A., Meizel S. Evidence suggesting involvement of a unique human sperm steroid receptor/Cl− channel complex in the progesterone-initiated acrosome reaction. Dev Biol 1993; 159: 679–690
   Google Scholar
• Xu W. M., Shi Q. X., Chen W. Y., Zhou C. X., Ni Y., Rowlands D. K., Lui G. Y., Zhu H., Ma Z. G., Wang X. F., et al. Cystic fibrosis transmembrane conductance regulator is vital to sperm fertilizing capacity and male fertility. Proc Natl Acad Sci 2007; 104: 9816–9821
   PubMed Web of Science ®Google Scholar
• Yanagimachi R. Mammalian fertilization. Physiology of Reproduction, E. Knobil, J. Neill. Raven Press, New York 1994; 189–317
   Google Scholar
• Yashimatsu N., Yanagimachi R. Effects of cations and other medium components on the zona-induced acrosome reaction of hamster spermatozoa. Dev Growth Differ 1988; 30: 51–659
   Google Scholar
• Yeung C. H., Barfield J. P., Anapolski M., Cooper T. G. Volume regulation of mature and immature spermatozoa in a primate model, and possible ion channels involved. Hum. Reprod 2004; 19: 2587–2593
   Google Scholar
• Yeung C. H., Oberländer G., Cooper T. G. The effects of the male antifertility agent ornidazole on sperm function in vitro and in the female genital tract. J Reprod Fertil 1995; 103(2)257–264
   Google Scholar
• Yuan Y. Y., Zhang Z. H., Shi Q. X. Initiation of the acrosome reaction in Chinese Hamster sperm by cumulus oophorus and matrix. Acta Anat Sin 1998; 29: 404–409
   Google Scholar
• Zeng Y., Oberdorf J. A., Florman H. M. PH regulation in mouse sperm: identification of Na+-, Cl−-, HCO3−-dependent and arylaminobenzoate-dependent regulatory mechanisms and characterization of their roles in sperm capacitation. Dev Biol 1996; 173: 510–520
   PubMed Web of Science ®Google Scholar
• Zhang G. P., Shi Y. L. Progress in the studies of background chloride channels. Progress in Biochem Biophys 1998; 25: 324–328
   Google Scholar
• Zhang Z. H., Chen W. Y., Shi Q. X., Yuan Y. Y., Lou Y. C. Capacitating action of GABA and progesterone in spermatozoa of human and guinea pig in vitro. Acta Physiol Sin 2000; 52: 179–184
   Google Scholar