Portal de Periódicos da CAPES

Zona Pellucida and Progesterone‐Induced Ca 2+ Signaling and Acrosome Reaction in Human Spermatozoa

2002; Wiley; Volume: 23; Issue: 3 Linguagem: Inglês

10.1002/j.1939-4640.2002.tb02232.x

2047-2927

Jackson Kirkman‐Brown, Emma L. Punt, Christopher L. R. Barratt, Stephen J. Publicover,

Insect and Pesticide Research

Journal of AndrologyVolume 23, Issue 3 p. 306-315 Free Access Zona Pellucida and Progesterone-Induced Ca2+ Signaling and Acrosome Reaction in Human Spermatozoa JACKSON C. KIRKMAN-BROWN, Corresponding Author JACKSON C. KIRKMAN-BROWN School of Biosciences, University of Birmingham Assisted Conception Unit, Birmingham Women's Hospital, Birmingham, United Kingdom.School of Biosciences, University of Birmingham, Birmingham, B15 2TT, United Kingdom (e-mail: [email protected]).Search for more papers by this authorEMMA L. PUNT, EMMA L. PUNT School of Biosciences, University of Birmingham Assisted Conception Unit, Birmingham Women's Hospital, Birmingham, United Kingdom.Search for more papers by this authorCHRISTOPHER L. R. BARRATT, CHRISTOPHER L. R. BARRATT Reproductive Biology and Genetics Research Group, The Medical School, University of Birmingham Assisted Conception Unit, Birmingham Women's Hospital, Birmingham, United Kingdom.Search for more papers by this authorSTEPHEN J. PUBLICOVER, STEPHEN J. PUBLICOVER School of Biosciences, University of Birmingham Assisted Conception Unit, Birmingham Women's Hospital, Birmingham, United Kingdom.Search for more papers by this author JACKSON C. KIRKMAN-BROWN, Corresponding Author JACKSON C. KIRKMAN-BROWN School of Biosciences, University of Birmingham Assisted Conception Unit, Birmingham Women's Hospital, Birmingham, United Kingdom.School of Biosciences, University of Birmingham, Birmingham, B15 2TT, United Kingdom (e-mail: [email protected]).Search for more papers by this authorEMMA L. PUNT, EMMA L. PUNT School of Biosciences, University of Birmingham Assisted Conception Unit, Birmingham Women's Hospital, Birmingham, United Kingdom.Search for more papers by this authorCHRISTOPHER L. R. BARRATT, CHRISTOPHER L. R. BARRATT Reproductive Biology and Genetics Research Group, The Medical School, University of Birmingham Assisted Conception Unit, Birmingham Women's Hospital, Birmingham, United Kingdom.Search for more papers by this authorSTEPHEN J. PUBLICOVER, STEPHEN J. PUBLICOVER School of Biosciences, University of Birmingham Assisted Conception Unit, Birmingham Women's Hospital, Birmingham, United Kingdom.Search for more papers by this author First published: 02 January 2013 https://doi.org/10.1002/j.1939-4640.2002.tb02232.xCitations: 8AboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onEmailFacebookTwitterLinkedInRedditWechat References Aitken RJ. Molecular mechanisms regulating human sperm function. Mol Hum Reprod 1997; 3: 169–173. Aitken RJ, Buckingham DW, Irvine DS. The extragenomic action of progesterone on human spermatozoa: evidence for a ubiquitous response that is rapidly down-regulated. Endocrinology 1996; 137: 3999–4009. Arnoult C., Cardullo RA, Lemos JR, Florman HM. Activation of mouse sperm T-type Ca2+ channels by adhesion to the egg zona pellucida. Proc Natl Acad Sci USA 1996a; 93: 13004–13009. Arnoult C., Kazam IG, Visconti PE, Kopf GS, Villaz M., Florman HM. Control of the low voltage-activated calcium channel of mouse sperm by egg ZP3 and by membrane hyperpolarization during capacitation. Proc Natl Acad Sci USA 1999; 96: 6757–6762. Arnoult C., Villaz M., Florman HM. Pharmacological properties of the T-type Ca2+ current of mouse spermatogenic cells. Mol Pharmacol 1998; 53: 1104–1111. Arnoult C., Zeng Y., Florman HM. ZP3-dependent activation of sperm cation channels regulates acrosomal secretion during mammalian fertilization. J Cell Biol 1996b; 134: 637–645. Baba T., Azuma S., Kashiwabara S., Toyoda Y. Sperm from mice carrying a targeted mutation of the acrosin gene can penetrate the oocyte zona pellucida and effect fertilization. J Biol Chem 1994; 269: 31845–31849. Baldi E., Casano R., Falsetti C., Krausz C., Maggi M., Forti G. Intracellular calcium accumulation and responsiveness to progesterone in capacitating human spermatozoa. J Androl 1991; 12: 323–330. Baldi E., Luconi M., Muratori M., Forti G. A novel functional estrogen receptor on human sperm membrane interferes with progesterone effects. Mol Cell Endocrinol 2000; 161: 31–35. Bedford JM. Mammalian fertilization misread? Sperm penetration of the eutherian zona pellucida is unlikely to be a lytic event. Biol Reprod 1998; 59: 1275–1287. Beebe SJ, Leyton L., Burks D., Ishikawa M., Fuerst T., Dean J., Saling P. Recombinant mouse ZP3 inhibits sperm binding and induces the acrosome reaction. Dev Biol 1992; 151: 48–54. Benoff S. Voltage dependent calcium channels in mammalian spermatozoa. Front Biosci 1998; 3: D1220–D1240. Berridge MJ. Capacitative calcium entry. Biochem J 1995; 312: 1–11. Bielfeld P., Anderson RA, Mack SR, De Jonge CJ, Zaneveld LJ. Are capacitation or calcium ion influx required for the human sperm acrosome reaction Fertil Steril 1994a; 62: 1255–1261. Bielfeld P., Faridi A., Zaneveld LJ, De Jonge CJ. The zona pellucida-induced acrosome reaction of human spermatozoa is mediated by protein kinases. Fertil Steril 1994b; 61: 536–541. Blackmore PF. Thapsigargin elevates and potentiates the ability of progesterone to increase intracellular free calcium in human sperm: possible role of perinuclear calcium. Cell Calcium 1993; 14: 53–60. Blackmore PF, Beebe SJ, Danforth DR, Alexander N. Progesterone and 17-hydroxyprogesterone: novel stimulators of calcium influx in human sperm. J Biol Chem 1990; 265: 1376–1380. Blackmore PF, Eisoldt S. The neoglycoprotein mannose-bovine serum albumin, but not progesterone, activates T-type calcium channels in human spermatozoa. Mol Hum Reprod 1999; 5: 498–506. Blackmore PF, Im WB, Bleasdale JE. The cell surface progesterone receptor which stimulates calcium influx in human sperm is unlike the A-ring reduced steroid site on the GABAA receptor/chloride channel. Mol Cell Endocrinol 1994; 104: 237–243. Blackmore PF, Neulen J., Lattanzio FA, Beebe SJ. Cell surface receptors for progesterone mediate calcium uptake in human sperm. J Biol Chem 1991; 266: 18655–18659. Bootman MD, Collins TJ, Peppiatt CM, et al. Calcium signalling—an overview. Semin Cell Dev Biol 2001; 12: 3–10. Brandelli A., Miranda PV, Anon-Vazquez MG, Marin-Briggiler CI, Sanjurjo C., Gonzalez-Echeverria F., Blaquier JA, Tezon JG. A new predictive test for in-vitro fertilization based on the induction of sperm acrosome reaction by N-acetylglucosamine-neoglycoprotein. Hum Reprod 1995; 10: 1751–1756. Brandelli A., Miranda PV, Tezon JG. Voltage-dependent calcium channels and Gi regulatory protein mediate the human sperm acrosomal exo-cytosis induced by N-acetylglucosaminyl/mannosyl neoglycoproteins. J Androl 1996; 17: 522–529. Bray C., Brown JCK, Publicover SJ, Barratt CL. Progesterone interaction with sperm plasma membrane, calcium influx and induction of the acrosome reaction. Rep Med Rev 1999; 7: 81–93. Breitbart H., Spungin B. The biochemistry of the acrosome reaction. Mol Hum Reprod 1997; 3: 195–202. Brewis IA, Clayton R., Barratt CL, Hornby DP, Moore HD. Recombinant human zona pellucida glycoprotein 3 induces calcium influx and acrosome reaction in human spermatozoa. Mol Hum Reprod 1996; 2: 583–589. Calogero AE, Burrello N., Ferrara E., Hall J., Fishel S., D'Agata R. Gammaaminobutyric acid (GABA) A and B receptors mediate the stimulatory effects of GABA on the human sperm acrosome reaction: interaction with progesterone. Fertil Steril 1999; 71: 930–936. Carrell DT, Middleton RG, Peterson CM, Jones KP, Urry RL. Role of the cumulus in the selection of morphologically normal sperm and induction of the acrosome reaction during human in vitro fertilization. Arch Androl 1993; 31: 133–137. Chen C., Sathananthan AH. Early penetration of human sperm through the vestments of human eggs in vitro. Arch Androl 1986; 16: 183–197. Cross NL, Morales P., Overstreet JW, Hanson FW. Induction of acrosome reactions by the human zona pellucida. Biol Reprod 1988; 38: 235–244. Darszon A., Labarca P., Nishigaki T., Espinosa F. Ion channels in sperm physiology. Phys Rev 1999; 79: 481–510. De Jonge C. The cAMP-dependent kinase pathway and human sperm acrosomal exocytosis. Front Biosci 1996; 1: d234–d240. De Jonge CJ, Barratt CLR, Radwanska E., Cooke ID. The acrosome reaction-inducing effect of human follicular and oviductal fluid. J Androl 1993; 14: 359–365. De Jonge CJ, Rawlins RG, Zaneveld LJ. Induction of the human sperm acrosome reaction by human oocytes. Fertil Steril 1988; 50: 949–953. Dragileva E., Rubinstein S., Breitbart H. Intracellular Ca2+-Mg2+-ATPase regulates calcium influx and acrosomal exocytosis in bull and ram spermatozoa. Biol Reprod 1999; 61: 1226–1234. Espinosa F., Lopez-Gonzalez I., Munoz-Garay C., Felix R., De la Vega-Beltran JL, Kopf GS, Visconti PE, Darszon A. Dual regulation of the T-type Ca2+ current by serum albumin and beta-estradiol in mammalian spermatogenic cells. FEBS Lett 2000; 475: 251–256. Florman HM. Sequential focal and global elevations of sperm intracellular calcium are initiated by the zona pellucida during acrosomal exocytosis. Dev Biol 1994; 165: 152–164. Florman HM, Arnoult C., Kazam IG, Li C., O'Toole CMB. A perspective on the control of mammalian fertilisation by egg-activated ion channels in sperm: a tale of two channels. Biol Reprod 1998; 59: 12–16. Foresta C., Rossato M., Di Virgilio F. Ion fluxes through the progesterone-activated channel of the sperm plasma membrane. Biochem J 1993; 294: 279–283. Fukami K., Nakao K., Inoue T., et al. Requirement of phospholipase Cdelta4 for the zona pellucida-induced acrosome reaction. Science 2001; 292: 920–923. Garcia MA, Meizel S. Progesterone-mediated calcium influx and acrosome reaction of human spermatozoa: pharmacological investigation of T-type calcium channels. Biol Reprod 1999; 60: 102–109. Goodwin LO, Leeds NB, Hurley I., Cooper GW, Pergolizzi RG, Benoff S. Alternative splicing of exons in the alphal subunit of the rat testis L-type voltage-dependent calcium channel generates line-specific dihydropyridine binding sites. Mol Hum Reprod 1998; 4: 215–226. Goodwin LO, Leeds NB, Hurley I., Mandel FS, Pergolizzi RG, Benoff S. Isolation and characterization of the primary structure of testis-specific L-type calcium channel: implications for contraception. Mol Hum Reprod 1997; 3: 255–268. Gregory L., Booth AD, Wells C., Walker SM. A study of the cumuluscorona cell complex in in-vitro fertilization and embryo transfer; a prognostic indicator of the failure of implantation. Hum Reprod 1994; 9: 1308–1317. Hartshorne GM. Steroid production by the cumulus: relationship to fertilization in vitro. Hum Reprod 1989; 4: 742–745. Henkel R., Franken DR, Habenicht UF. Zona pellucida as physiological trigger for the induction of acrosome reaction. Andrologia 1998; 30: 275–280. Hofmann T., Obukhov AG, Schaefer M., Harteneck C., Gudermann T., Schultz G. Direct activation of human TRPC6 and TRPC3 channels by diacylglycerol. Nature 1999; 397: 259–263. Hughes DC, Barratt CL. Identification of the true human orthologue of the mouse Zp1 gene: evidence for greater complexity in the mammalian zona pellucida Biochim Biophys Acta 1999; 1447: 303–306. Jagannathan S., Barratt CLR, Publicover SJ. Characterisation of alpha 1H, a T-type calcium ion channel from human germ cells. Eur J Neurosci 2000a; 12(suppl): 383. Jagannathan S., Punt EL, Ivic A., Zamponi GW, Hamid J., Barratt CLR, Publicover SJ. Evidence for the expression of alpha 1G (T-type) voltage operated Ca2+ channels in human male germ cells. J Androl 2000b; 108(suppl): 61. Jungnickel MK, Marrero H., Birnbaumer L., Lemos JR, Florman HM. Trp2 regulates entry of Ca2+ into mouse sperm triggered by egg ZP3. Nat Cell Biol 2001; 3: 499–502. Kirkman-Brown JC, Bray C., Stewart PM, Barratt CL, Publicover SJ. Biphasic elevation of [Ca2+]i in individual human spermatozoa exposed to progesterone. Dev Biol 2000; 222: 326–335. Kiselyov K., Xu X., Mozhayeva G., Kuo T., Pessah I., Mignery G., Zhu X., Birnbaumer L., Muallem S. Functional interaction between InsP3 receptors and store-operated hTrp3 channels. Nature 1998; 396: 478–482. Kobori H., Miyazaki S., Kuwabara Y. Characterization of intracellular Ca2+ increase in response to progesterone and cyclic nucleotides in mouse spermatozoa. Biol Reprod 2000; 63: 113–120. Krausz C., Bonaccorsi L., Luconi M., Fuzzi B., Criscuoli L., Pellegrini S., Forti G., Baldi E. Intracellular calcium increase and acrosome reaction in response to progesterone in human spermatozoa are correlated with in-vitro fertilization. Hum Reprod 1995; 10: 120–124. Krausz C., Bonaccorsi L., Maggio P., et al. Two functional assays of sperm responsiveness to progesterone and their predictive values in in vitro fertilisation. Hum Reprod 1996; 11: 1661–1667. Kuroda Y., Kaneko S., Yoshimura Y., Nozawa S., Mikoshiba K. Are there inositol 1,4,5-triphosphate (IP3) receptors in human sperm Life Sci 1999; 65: 135–143. Laufer N., DeCherney AH, Haseltine FP, Behrman HR. Steroid secretion by the human egg-corona-cumulus complex in culture. J Clin Endocrinol Metab 1984; 58: 1153–1157. Lee MA, Storey BT. Endpoint of first stage of zona pellucida-induced acrosome reaction in mouse spermatozoa characterized by acrosomal H+ and Ca2+ permeability: population and single cell kinetics. Gamete Res 1989; 24: 303–326. Lee MA, Trucco GS, Bechtol KB, Wummer N., Kopf GS, Blasco L., Storey BT. Capacitation and acrosome reactions in human spermatozoa monitored by a chlortetracycline fluorescence assay. Fertil Steril 1987; 48: 649–658. Lenz RW, Ball GD, Lohse JK, First NL, Ax RL. Chondroitin sulfate facilitates an acrosome reaction in bovine spermatozoa as evidenced by light microscopy, electron microscopy and in vitro fertilization. Biol Reprod 1983; 28: 683–690. Lievano A., Santi CM, Serrano CJ, Trevino CL, Bellve AR, Hernandez-Cruz A., Darszon A. T-type channels and alpha1E expression in spermatogenic cells, and their possible relevance to the sperm acrosome reaction. FEBS Lett 1996; 388: 150–154. Liu DY, Baker HW. Relationship between the zona pellucida (ZP) and ionophore A23187-induced acrosome reaction and the ability of sperm to penetrate the ZP in men with normal sperm-ZP binding. Fertil Steril 1996; 66: 312–315. Llanos MN, Ronco AM, Aguirre MC, Meizel S. Hamster sperm glycine receptor: evidence for its presence and involvement in the acrosome reaction. Mol Reprod Dev 2001; 58: 205–215. Luconi M., Bonaccorsi L., Maggi M., Pecchioli P., Krausz C., Forti G., Baldi E. Identification and characterisation of functional nongenomic progesterone receptors on human sperm membrane. J Clin Endocrinol Metab 1998; 83: 877–855. Luconi M., Muratori M., Forti G., Baldi E. Identification and characterization of a novel functional estrogen receptor on human sperm membrane that interferes with progesterone effects. JClin Endocrinol Metab 1999; 84: 1670–1678. Mattioli M., Barboni B. Signal transduction mechanism for LH in the cumulus-oocyte complex. Mol Cell Endocrinol 2000; 161: 19–23. Meizel S., Turner KO. Initiation of the human sperm acrosome reaction by thapsigargin. J Exp Zool 1993; 267: 350–355. Meizel S., Turner KO, Nuccitelli R. Progesterone triggers a wave of increased free calcium during the human sperm acrosome reaction. Dev Biol 1997; 182: 67–75. Melendrez CS, 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. Mendoza C., Tesarik J. Effect of follicular fluid on sperm movement characteristics. Fertil Steril 1990; 54: 1135–1139. Mendoza C., Tesarik J. A plasma-membrane progesterone receptor in human sperm is switched on by increasing intracellular free calcium. FEBS Lett 1993; 330: 57–60. Morales P., Pizarro E., Kong M., Kerr B., Ceric F., Vigil P. Gonadotropin-releasing hormone-stimulated sperm binding to the human zona is mediated by a calcium influx. Biol Reprod 2000; 63: 635–642. Morales P., Vigil P., Franken DR, Kaskar K., Coetzee K., Kruger TF. Spermoocyte interaction: studies on the kinetics of zona pellucida binding and acrosome reaction of human spermatozoa. Andrologia 1994; 26: 131–137. Motta PM, Makabe S., Naguro T., Correr S. Oocyte follicle cells association during development of human ovarian follicle. A study by high resolution scanning and transmission electron microscopy. Arch Histol Cytol 1994; 57: 369–394. Motta PM, Nottola SA, Pereda J., Croxatto HB, Familiari G. Ultrastructure of human cumulus oophorus: a transmission electron microscopic study on oviductal oocytes and fertilized eggs. Hum Reprod 1995; 10: 2361–2367. Myles DG, Primakoff P. Why did the sperm cross the cumulus? To get to the oocyte. Functions of the sperm surface proteins PH-20 and fertilin in arriving at, and fusing with, the egg. Biol Reprod 1997; 56: 320–327. Nagae T., Yanagimachi R., Srivastava PN, Yanagimachi H. Acrosome reaction in human spermatozoa. Fertil Steril 1986; 45: 701–707. Nottola SA, Macchiarelli G., Familiari G., Stallone T., Sathananthan AH, Motta PM. Egg-sperm interactions in humans: ultrastructural aspects. Ital J Anat Embryol 1998; 103(4 suppl 1): 85–101. Oehninger S., Blackmore P., Morshedi M., Sueldo C., Acosta AA, Alexander NJ. Defective calcium influx and acrosome reaction (spontaneous and progesterone-induced) in spermatozoa of infertile men with severe teratozoospermia. Fertil Steril 1994a; 61: 349–354. Oehninger S., Sueldo C., Lanzendorf S., Mahony M., Burkman LJ, Alexander NJ, Hodgen GD. A sequential analysis of the effect of progesterone on specific sperm functions crucial to fertilization in vitro in infertile patients. Hum Reprod 1994b; 9: 1322–1327. Osman RA, Andria ML, Jones AD, Meizel S. Steroid induced exocytosis: the human sperm acrosome reaction. Biochem Biophys Res Commun 1989; 160: 828–833. O'Toole CM, Arnoult C., Darszon A., Steinhardt RA, Florman HM. Ca2+ entry through store-operated channels in mouse sperm is initiated by egg ZP3 and drives the acrosome reaction. Mol Biol Cell 2000; 11: 1571–1584. O'Toole CMB, Roldan ERS, Fraser LR. Role for Ca2+ channels in the signal transduction pathway leading to acrosomal exocytosis in human spermatozoa. Mol Reprod Dev 1996a; 45: 204–211. O'Toole CMB, Roldan ERS, Hampton P., Fraser LR. A role for diacylglycerol in human sperm acrosomal exocytosis. Mol Hum Reprod 1996b; 2: 317–326. Patrat C., Serres C., Jouannet P. Induction of a sodium ion influx by progesterone in human spermatozoa. Biol Reprod 2000a; 62: 1380–1386. Patrat, C., Serres S., Jouannet P. The acrosome reaction in human spermatozoa. Biol Cell 2000b; 92: 255–266. Pereda J., Coppo M. An electron microscopic study of sperm penetration into the human egg investments. Anat Embryol (Berl) 1985; 173: 247–252. Plant A., McLaughlin EA, Ford WCL. Intracellular calcium measurements in individual human sperm demonstrate that the majority can respond to progesterone. Fertil Steril 1995; 64: 1213–1215. Publicover SJ, Barratt CLR. Voltage operated Ca2+ channels and the acrosome reaction: which channels are present and what do they do Hum Reprod 1999; 14: 873–879. Punt EL, Barratt CLR, Publicover SJ. Involvement of store operated channels in the sustained component of the progesterone-induced [Ca2+]i signal in human spermatozoa. J Androl Suppl MayJune 2001: 90. Putney JW Jr. TRP, inositol 1,4,5-trisphosphate receptors, and capacitative calcium entry. Proc Natl Acad Sci USA 1999; 96: 14669–14671. Putney JW Jr, McKay RR. Capacitative calcium entry channels. Bioessays 1999; 21: 38–46. Ren D., Navarro B., Perez G., Jackson AC, Hsu S., Shi Q., Tilly JL, Clapham D. A sperm ion channel required for sperm motility and male fertility. Nature 2001; 413: 603–609. Rockwell PL, Storey BT. Kinetics of onset of mouse sperm acrosome reaction induced by solubilized zona pellucida: fluorimetric determination of loss of pH gradient between acrosomal lumen and medium monitored by dapoxyl (2-aminoethyl) sulfonamide and of intracellular Ca2+ changes monitored by fluo-3. Mol Reprod Dev 2000; 55: 335–349. Roldan ER, Murase T., Shi QT. Exocytosis in spermatozoa in response to progesterone and zona-pellucida. Science 1994; 266: 1578–1581. Rossato M., Di Virgilio F., Rizzuto R., Galeazzi C., Foresta C. Intracellular calcium store depletion and acrosome reaction in human spermatozoa: role of calcium and plasma membrane potential. Mol Hum Reprod 2001; 7: 119–128. Sabeur K., Cherr GN, Yudin AI, Overstreet JW. Hyaluronic acid enhances induction of the acrosome reaction of human sperm through interaction with the PH-20 protein. Zygote 1998; 6: 103–111. Santi CM, Darszon A., Hernandez-Cruz A. A dihydropyridine-sensitive T-type Ca2+ current is the man Ca2+ current carrier in mouse primary spermatocytes. Am J Physiol 1996; 271: C1583–C1593. Sato Y., Son JH, Tucker RP, Meizel S. The zona pellucida-initiated acrosome reaction: defect due to mutations in the sperm glycine receptor/Cl− channel. Dev Biol 2000; 227: 211–218. Schaefer M., Hofmann T., Schultz G., Gudermann T. A new prostaglandin E receptor mediates calcium influx and acrosome reaction in human spermatozoa. Proc Natl Acad Sci USA 1998; 95: 3008–3013. Serrano CJ, Trevino CL, Felix R., Darszon A. Voltage-dependent Ca2+ channel subunit expression and immunolocalization in mouse spermatogenic cells and sperm. FEBS Lett 1999; 462: 171–176. Shi QX, Roldan ERS. Evidence that a GABAA like receptor is involved in progesterone-induced acrosomal exocytosis in mouse spermatozoa. Biol Reprod 1995; 52: 373–381. Shirakawa H., Miyazaki S. Spatiotemporal characterization of intracellular Ca2+ rise during the acrosome reaction of mammalian spermatozoa induced by zona pellucida. Dev Biol 1999; 208: 70–78. Snell WJ, White JM. The molecules of mammalian fertilisation. Cell 1996; 85: 629–637. Son WY, Lee JH, Lee JH, Han CT. Acrosome reaction of human spermatozoa is mainly mediated by 1H T-type calcium channels. Mol Hum Reprod 2000; 6: 893–897. Spungin B., Breitbart H. Calcium mobilization and influx during sperm exocytosis. J Cell Sci 1996; 109: 1947–1955. Sueldo CE, Oehninger S., Subias E., Mahony M., Alexander NJ, Burkman LJ, Acosta AA. Effect of progesterone on human zona pellucida sperm binding and oocyte penetrating capacity. Fertil Steril 1993; 60: 137–140. Talbot P. Sperm penetration through oocyte investments in mammals. Am J Anat 1985; 174: 331–346. Tanghe S., Van Soom A., Nauwynck H., Coryn M., De Kruif A. Functions of the cumulus oophorus during oocyte maturation, ovulation, and fertilization. Mol Reprod Dev 2002; 61: 414–424. Tesarik J., Carreras A., Mendoza C. Single cell analysis of tyrosine kinase dependent and independent Ca2+ fluxes in progesterone induced acrosome reaction. Mol Hum Reprod 1996; 2: 225–232. Tesarik J., Oltras Mendoza C., Testart J. Effect of the human cumulus oophorus on movement characteristics of human capacitated spermatozoa. J Reprod Fertil 1990; 88: 665–675. Tesarik J., Moos J., Mendoza C. Stimulation of protein tyrosine phosphorylation by a progesterone receptor on the cell surface of human sperm. Endocrinology 1993; 133: 328–335. Tesarik J., Pilka L., Drahorad J., Cechova D., Veselsky L. The role of cumulus cell-secreted proteins in the development of human sperm fertilizing ability: implication in IVF. Hum Reprod 1988; 3: 129–132. Thastrup O., Cullen PJ, Drobak BK, Hanley MR, Dawson AP. Thapsigargin, a tumor promoter, discharges intracellular Ca2+ stores by specific inhibition of the endoplasmic reticulum Ca2+-ATPase. Proc Natl Acad Sci USA 1990; 87: 2466–2470. Thomas P., Meizel S. Phosphatidylinositol-4,5-bisphosphate hydrolysis in human sperm stimulated with follicular fluid or progesterone is dependent on Ca2+ influx. Biochem J 1989; 264: 539–546. Tosti E., Di Cosmo A., Cuomo A., Di Cristo C., Gragnaniello G. Progesterone induces activation in Octopus vulgaris spermatozoa. Mol Reprod Dev 2001; 59: 97–105. Tovey SC, Godfrey RE, Hughes PJ, Mezna M., Minchin SD, Mikoshiba K., Michelangeli F. Identification and characterization of inositol 1,4,5-trisphosphate receptors in rat testis. Cell Calcium 1997; 21: 311–319. Treiman M., Caspersen C., Christensen SB. A tool coming of age: thapsigargin as an inhibitor of sarco-endoplasmic reticulum Ca2+-ATPases. Tips 1998; 19: 131–135. Tulsiani DR, Yoshida-Komiya H., Araki Y. Mammalian fertilization: a carbohydrate-mediated event. Biol Reprod 1997; 57: 487–494. Turner K., Meizel S. Progesterone-mediated efflux of cytosolic chloride during the human sperm acrosome reaction. Biochem Biophys Res Commun 1995; 212: 774–780. Turner KO, Syvanen M., Meizel S. The human acrosome reaction is highly sensitive to inhibition by cyclodiene insecticides. J Androl 1997; 18: 571–575. Vannier B., Peyton M., Boulay G., Brown D., Qin N., Jiang M., Zhu X., Birnbaumer L. Mouse trp2, the homologue of the human trpc2 pseudogene, encodes mTrp2, a store depletion-activated capacitative Ca2+ entry channel. Proc Natl Acad Sci USA 1999; 96: 2060–2064. Walensky LD, Snyder SH. Inositol 1,4,5-trisphosphate receptors selectively localized to the acrosomes of mammalian sperm. J Cell Biol 1995; 130: 857–869. Ward CR, Kopf GS. Molecular events mediating sperm activation. Dev Biol 1993; 158: 9–34. Wennemuth G., Westenbroek RE, Xu T., Hille B., Babcock DF. CaV2.2 and CaV2.3 (N- and R-type) Ca2+ channels in depolarization-evoked entry of Ca2+ into mouse sperm. J Biol Chem 2000; 275: 21210–21217. Wes PD, Chevesich J., Jeromin A., Rosenberg C., Stetten G., Montell C. TRPC1, a human homolog of a Drosophila store-operated channel. Proc Natl Acad Sci USA 1995; 92: 9652–9656. Westenbroek RE, Babcock DF. Discrete regional distributions suggest diverse functional roles of calcium channel alpha1 subunits in sperm. Dev Biol 1999; 207: 457–469. Wistrom CA, 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. Yanagimachi R. Fertility of mammalian spermatozoa: its development and relativity. Zygote 1994; 2: 371–372. Zaneveld LJ, De Jonge CJ, Anderson RA, Mack SR. Human sperm capacitation and the acrosome reaction. Hum Reprod 1991; 6: 1265–1274. Zitt C., Zobel A., Obukhov AG, Harteneck C., Kalkbrenner F., Luckhoff A., Schultz G. Cloning and functional expression of a human Ca2+-permeable cation channel activated by calcium store depletion. Neuron 1996; 16: 1189–1196. Citing Literature Volume23, Issue3May‐June 2002Pages 306-315 ReferencesRelatedInformation