T-type Ca2+ channels in sperm function

Cell Calcium

Volumn 40, Issue 2, 2006, Pages 241-252

  Darszon, Alberto ^a   López Martínez, Pablo ^a   Acevedo, Juan José ^b   Hernández Cruz, Arturo ^c   Treviño, Claudia L ^a  

^a INSTITUTO DE BIOTECNOLOGÍA   (Mexico)

^b UNIVERSIDAD AUTÓNOMA DEL ESTADO DE MORELOS   (Mexico)

^c INSTITUTO DE FISIOLOGÍA CELULAR   (Mexico)

Author keywords

Capacitation; Motility; Sperm acrosome reaction; Voltage dependent Ca2+ channels

Indexed keywords

CALCIUM CHANNEL T TYPE; CALCIUM ION; VOLTAGE GATED CALCIUM CHANNEL; MESSENGER RNA;

ACROSOME; ACROSOME REACTION; ARTICLE; CALCIUM CELL LEVEL; CELL FUNCTION; CELL MEMBRANE; CELL VACUOLE; ELECTROPHYSIOLOGY; EXOCYTOSIS; FERTILIZATION; HUMAN; MEMBRANE FUSION; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; SPERM; SPERMATOZOON; SPERMATOZOON CAPACITATION; SPERMATOZOON MATURATION; SPERMATOZOON MOTILITY; ANIMAL; CYTOLOGY; GENETICS; MALE; METABOLISM; PHYSIOLOGY; REVIEW;

ANIMALS; CALCIUM CHANNELS, T-TYPE; HUMANS; MALE; RNA, MESSENGER; SPERMATOZOA;

EID: 33745672742     PISSN: 01434160     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ceca.2006.04.028     Document Type: Article

References (103)

1. Yanagimachi R. Mammalian fertilization. In: Knobile E., and Neill J.D. (Eds). The Physiology of Reproduction vol. 1 (1994), Raven Press, New York 189-317
2. Jungnickel M.K., Sutton K.A., and Florman H.M. In the beginning: lessons from fertilization in mice and worms. Cell 114 (2003) 401-404
3. Ho H.C., and Suarez S.S. Characterization of the intracellular calcium store at the base of the sperm flagellum that regulates hyperactivated motility. Biol. Reprod. 68 (2003) 1590-1596
4. Carafoli E. Calcium-a universal carrier of biological signals. Delivered on 3 July 2003 at the Special FEBS Meeting in Brussels. FEBS J. 272 (2005) 1073-1089
5. Fox A.P., Nowycky M.C., and Tsien R.W. Single-channel recordings of three types of calcium channels in chick sensory neurones. J. Physiol. 394 (1987) 173-200
6. Perez-Reyes E. Molecular physiology of low-voltage-activated t-type calcium channels. Physiol. Rev. 83 (2003) 117-161
7. 2+ fluctuations in sperm physiology. Int. Rev. Cytol. 243 (2005) 79-172
8. 2+ channel. Nature 439 (2006) 737-740
9. Gur Y., and Breitbart H. Mammalian sperm translate nuclear-encoded proteins by mitochondrial-type ribosomes. Genes Dev. 20 (2006) 411-416
10. Florman H.M., Arnoult C., Kazam I.G., Li C., and O'Toole C.M. A perspective on the control of mammalian fertilization by egg-activated ion channels in sperm: a tale of two channels. Biol. Reprod. 59 (1998) 12-16
11. Jimenez-Gonzalez C., Michelangeli F., Harper C.V., Barratt C.L., and Publicover S.J. Calcium signalling in human spermatozoa: a specialized 'toolkit' of channels, transporters and stores. Hum. Reprod. Update 12 3 (2005) 253-267
12. 2+ channels and alpha1E expression in spermatogenic cells, and their possible relevance to the sperm acrosome reaction. FEBS Lett. 388 (1996) 150-154
13. Espinosa F., Lopez-Gonzalez I., Serrano C.J., Gasque G., de la Vega-Beltran J.L., Trevino C.L., and Darszon A. Anion channel blockers differentially affect T-type Ca(2+) currents of mouse spermatogenic cells, alpha1E currents expressed in Xenopus oocytes and the sperm acrosome reaction. Dev. Genet. 25 (1999) 103-114
14. 2+ channels during spermatogenesis and organogenesis in mice. Dev. Growth Differ. 44 (2002) 181-190
15. 2+ channels in human sperm. Exp. Mol. Med. 35 (2003) 285-292
16. Goodwin L.O., Karabinus D.S., Pergolizzi R.G., and Benoff S. L-type voltage-dependent calcium channel alpha-1C subunit mRNA is present in ejaculated human spermatozoa. Mol. Hum. Reprod. 6 (2000) 127-136
17. Westenbroek R.E., and Babcock D.F. Discrete regional distributions suggest diverse functional roles of calcium channel alpha1 subunits in sperm. Dev. Biol. 207 (1999) 457-469
18. 2+ into mouse sperm. J. Biol. Chem. 275 (2000) 21210-21217
19. Trevino C.L., Felix R., Castellano L.E., Gutierrez C., Rodriguez D., Pacheco J., Lopez-Gonzalez I., Gomora J.C., Tsutsumi V., Hernandez-Cruz A., Fiordelisio T., Scaling A.L., and Darszon A. Expression and differential cell distribution of low-threshold Ca(2+) channels in mammalian male germ cells and sperm. FEBS Lett. 563 (2004) 87-92
20. Goodwin L.O., Leeds N.B., Hurley I., Mandel F.S., Pergolizzi R.G., and Benoff S. Isolation and characterization of the primary structure of testis-specific L-type calcium channel: implications for contraception. Mol. Hum. Reprod. 3 (1997) 255-268
21. Benoff S. Voltage dependent calcium channels in mammalian spermatozoa. Front. Biosci. 3 (1998) D1220-D1240
22. 2+ current carrier in mouse primary spermatocytes. Am. J. Physiol. 271 (1996) C1583-C1593
23. 2+ channels by adhesion to the egg zona pellucida. Proc. Natl. Acad. Sci. USA 93 (1996) 13004-13009
24. Bai J.P., and Shi Y.L. Inhibition of Ca(2+) channels in mouse spermatogenic cells by male antifertility compounds from Tripterygium wilfordii Hook. f. Contraception 65 (2002) 441-445
25. Jagannathan S., Punt E.L., Gu Y., Arnoult C., Sakkas D., Barratt C.L., and Publicover S.J. Identification and localization of T-type voltage-operated calcium channel subunits in human male germ cells. Expression of multiple isoforms. J. Biol. Chem. 277 (2002) 8449-8456
26. Catterall W.A., Striessnig J., Snutch T.P., and Perez-Reyes E. International union of pharmacology. XL. Compendium of voltage-gated ion channels: calcium channels. Pharmacol. Rev. 55 (2003) 579-581
27. Serrano C.J., Trevino C.L., Felix R., and Darszon A. Voltage-dependent Ca(2+) channel subunit expression and immunolocalization in mouse spermatogenic cells and sperm. FEBS Lett. 462 (1999) 171-176
28. Hagiwara S., and Kawa K. Calcium and potassium currents in spermatogenic cells dissociated from rat seminiferous tubules. J. Physiol. 356 (1984) 135-149
29. Lievano A., Bolden A., and Horn R. Calcium channels in excitable cells: divergent genotypic and phenotypic expression of alpha 1-subunits. Am. J. Physiol. 267 (1994) C411-C424
30. 2+ current of mouse spermatogenic cells. Mol. Pharmacol. 53 (1998) 1104-1111
31. Perez-Reyes E., Cribbs L.L., Daud A., Lacerda A.E., Barclay J., Williamson M.P., Fox M., Rees M., and Lee J.H. Molecular characterization of a neuronal low-voltage-activated T-type calcium channel. Nature 391 (1998) 896-900
32. Cribbs L.L., Gomora J.C., Daud A.N., Lee J.H., and Perez-Reyes E. Molecular cloning and functional expression of Ca(v)3.1c, a T-type calcium channel from human brain. FEBS Lett. 466 (2000) 54-58
33. Klugbauer N., Marais E., Lacinova L., and Hofmann F. A T-type calcium channel from mouse brain. Pflugers Arch. 437 (1999) 710-715
34. Sakata Y., Saegusa H., Zong S., Osanai M., Murakoshi T., Shimizu Y., Noda T., Aso T., and Tanabe T. Analysis of Ca(2+) currents in spermatocytes from mice lacking Ca(v)2.3 (alpha(1E)) Ca(2+) channel. Biochem. Biophys. Res. Commun. 288 (2001) 1032-1036
35. Lee J.H., Gomora J.C., Cribbs L.L., and Perez-Reyes E. Nickel block of three cloned T-type calcium channels: low concentrations selectively block alpha1H. Biophys. J. 77 (1999) 3034-3042
36. Stamboulian S., Kim D., Shin H.S., Ronjat M., De Waard M., and Arnoult C. Biophysical and pharmacological characterization of spermatogenic T-type calcium current in mice lacking the CaV3.1 (alpha1G) calcium channel: CaV3.2 (alpha1H) is the main functional calcium channel in wild-type spermatogenic cells. J. Cell Physiol. 200 (2004) 116-124
37. Benoff S.J.A., Silye A., Centola G.M., and Hurley I.R. Characterization of Low Voltage-Activated T-type Calcium Channels Expressed in Rat Testis and Sperm (2000), Cold Spring Harbor Meeting on Germ Cells, USA pp. 28
38. 2+ channels. Science 302 (2003) 1416-1418
39. Son W.Y., Lee J.H., and Han C.T. Acrosome reaction of human spermatozoa is mainly mediated by alpha1H T-type calcium channels. Mol. Hum. Reprod. 6 (2000) 893-897
40. Miller R.L. Sperm chemo-orientation in the metazoa. In: Metz C.B., and Monroy A. (Eds). Biology of Fertilization (1985), Academic Press, New York 275-337
41. Morisawa M. Cell signaling mechanisms for sperm motility. Zool. Sci. 11 (1994) 647-662
42. Ward G.E., Brokaw C.J., Garbers D.L., and Vacquier V.D. Chemotaxis of Arbacia punctulata spermatozoa to resact, a peptide from the egg jelly layer. Int. J. Cell Biol. 101 (1985) 2324-2329
43. Brokaw C.J. Calcium-induced asymmetrical beating of triton-demembranated sea urchin sperm flagella. J. Cell Biol. 82 (1979) 401-411
44. Brokaw C.J. Calcium sensors in sea urchin sperm flagella. Cell Motil. Cytoskeleton 18 (1991) 123-130
45. Ren D., Navarro B., Perez G., Jackson A.C., Hsu S., Shi Q., Tilly J.L., and Clapham D.E. A sperm ion channel required for sperm motility and male fertility. Nature 413 (2001) 603-609
46. Quill T.A., Ren D., Clapham D.E., and Garbers D.L. A voltage-gated ion channel expressed specifically in spermatozoa. Proc. Natl. Acad. Sci. USA 98 (2001) 12527-12531
47. 2+ entry and control of flagellar function in sperm. Proc. Natl. Acad. Sci. USA 100 (2003) 14864-14868
48. Suarez S.S., Varosi S.M., and Dai X. Intracellular calcium increases with hyperactivation in intact, moving hamster sperm and oscillates with the flagellar beat cycle. Proc. Natl. Acad. Sci. USA 90 (1993) 4660-4664
49. Wood C.D., Nishigaki T., Furuta T., Baba S.A., and Darszon A. Real-time analysis of the role of Ca(2+) in flagellar movement and motility in single sea urchin sperm. J. Cell Biol. 169 (2005) 725-731
50. 2+ channels in sea urchin sperm. FEBS Lett. 579 (2005) 6667-6672
51. Yoshida M. Mechanism of chemotaxis of the ascidian spermatozoa. Zool. Sci. 20 (2003) 1499-1500
52. Visconti P.E., Westbrook V.A., Chertihin O., Demarco I., Sleight S., and Diekman A.B. Novel signaling pathways involved in sperm acquisition of fertilizing capacity. J. Reprod. Immunol. 53 (2002) 133-150
53. Visconti P.E., and Kopf G.S. Regulation of protein phosphorylation during sperm capacitation. Biol. Reprod. 59 (1998) 1-6
54. Flesch F.M., and Gadella B.M. Dynamics of the mammalian sperm plasma membrane in the process of fertilization. Biochim. Biophys. Acta 1469 (2000) 197-235
55. Arnoult C., Kazam I.G., Visconti P.E., Kopf G.S., Villaz M., and Florman H.M. 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 96 (1999) 6757-6762
56. Munoz-Garay C., De la Vega-Beltran J.L., Delgado R., Labarca P., Felix R., and Darszon A. Inwardly rectifying K(+) channels in spermatogenic cells: functional expression and implication in sperm capacitation. Dev. Biol. 234 (2001) 261-274
57. Espinosa F., Lopez-Gonzalez I., Munoz-Garay C., Felix R., De la Vega-Beltran J.L., Kopf G.S., Visconti P.E., and Darszon A. Dual regulation of the T-type Ca(2+) current by serum albumin and beta-estradiol in mammalian spermatogenic cells. FEBS Lett. 475 (2000) 251-256
58. Vacquier V.D. Evolution of gamete recognition proteins. Science 281 (1998) 1995-1998
59. 2+ channels during the egg jelly-induced acrosome reaction of sea urchin sperm. J. Biol. Chem. 264 (1989) 19593-19599
60. Schackmann R.W. Ionic regulation of the sea urchin sperm acrosome reaction and stimulation by egg-derived peptides. In: Schatte H., and Schatten G. (Eds). The Cell Biology of Fertilization (1989), Academic Press, San Diego 3-28
61. Guerrero A., and Darszon A. Egg jelly triggers a calcium influx which inactivates and is inhibited by calmodulin antagonists in the sea urchin sperm. Biochim. Biophys. Acta 980 (1989) 109-116
62. Gonzalez-Martinez M.T., Galindo B.E., de De La Torre L., Zapata O., Rodriguez E., Florman H.M., and Darszon A. A sustained increase in intracellular Ca(2+) is required for the acrosome reaction in sea urchin sperm. Dev. Biol. 236 (2001) 220-229
63. Domino S.E., and Garbers D.L. Stimulation of phospholipid turnover in isolated sea urchin sperm heads by the fucose-sulfate glycoconjugate that induces an acrosome reaction. Biol. Reprod. 41 (1989) 133-141
64. Zapata O., Ralston J., Beltran C., Parys J.B., Chen J.L., Longo F.J., and Darszon A. Inositol triphosphate receptors in sea urchin sperm. Zygote 5 (1997) 355-364
65. Gonzalez-Martinez M., and Darszon A. A fast transient hyperpolarization occurs during the sea urchin sperm acrosome reaction induced by egg jelly. FEBS Lett. 218 (1987) 247-250
66. Tao J., Wu Y., Chen J., Zhu H., and Li S. Effects of urocortin on T-type calcium currents in mouse spermatogenic cells. Biochem. Biophys. Res. Commun. 329 (2005) 743-748
67. 2+ channels in mouse spermatogenic cells. Reprod. Toxicol. 21 (2006) 48-53
68. Linares-Hernandez L., Guzman-Grenfell A.M., Hicks-Gomez J.J., and Gonzalez-Martinez M.T. Voltage-dependent calcium influx in human sperm assessed by simultaneous optical detection of intracellular calcium and membrane potential. Biochim. Biophys. Acta 1372 (1998) 1-12
69. Brandelli A., Miranda P.V., and Tezon J.G. Voltage-dependent calcium channels and Gi regulatory protein mediate the human sperm acrosomal exocytosis induced by N-acetylglucosaminyl/mannosyl neoglycoproteins. J. Androl. 17 (1996) 522-529
70. Blackmore P.F., and Eisoldt S. The neoglycoprotein mannose-bovine serum albumin, but not progesterone, activates T-type calcium channels in human spermatozoa. Mol. Hum. Reprod. 5 (1999) 498-506
71. Harper C.V., and Publicover S.J. Reassessing the role of progesterone in fertilization-compartmentalized calcium signalling in human spermatozoa?. Hum. Reprod. 20 (2005) 2675-2680
72. Meizel S., Turner K.O., and Nuccitelli R. Progesterone triggers a wave of increased free calcium during the human sperm acrosome reaction. Dev. Biol. 182 (1997) 67-75
73. Kirkman-Brown J.C., Barratt C.L., and Publicover S.J. Slow calcium oscillations in human spermatozoa. Biochem. J. 378 (2004) 827-832
74. Harper C.V., Barratt C.L., and Publicover S.J. Stimulation of human spermatozoa with progesterone gradients to simulate approach to the oocyte. Induction of [Ca(2+)](i) oscillations and cyclical transitions in flagellar beating. J. Biol. Chem. 279 (2004) 46315-46325
75. Baldi E., Casano R., Falsetti C., Krausz C., Maggi M., and Forti G. Intracellular calcium accumulation and responsiveness to progesterone in capacitating human spermatozoa. J. Androl. 12 (1991) 323-330
76. Foresta C., Rossato M., Mioni R., and Zorzi M. Progesterone induces capacitation in human spermatozoa. Andrologia 24 (1992) 33-35
77. de Lamirande E., Harakat A., and Gagnon C. Human sperm capacitation induced by biological fluids and progesterone, but not by NADH or NADPH, is associated with the production of superoxide anion. J. Androl. 19 (1998) 215-225
78. Roldan E.R., Murase T., and Shi Q.X. Exocytosis in spermatozoa in response to progesterone and zona pellucida. Science 266 (1994) 1578-1581
79. Fukami K., Nakao K., Inoue T., Kataoka Y., Kurokawa M., Fissore R.A., Nakamura K., Katsuki M., Mikoshiba K., Yoshida N., and Takenawa T. Requirement of phospholipase Cdelta4 for the zona pellucida-induced acrosome reaction. Science 292 (2001) 920-923
80. 2+]i transient in human spermatozoa. Dev. Biol. 259 (2003) 71-82
81. Guzman-Grenfell A.M., and Gonzalez-Martinez M.T. Lack of voltage-dependent calcium channel opening during the calcium influx induced by progesterone in human sperm. Effect of calcium channel deactivation and inactivation. J. Androl. 25 (2004) 117-122
82. Pietrobon E.O., Soria M., Dominguez L.A., Monclus Mde L., and Fornes M.W. Simultaneous activation of PLA2 and PLC are required to promote acrosomal reaction stimulated by progesterone via G-proteins. Mol. Reprod. Dev. 70 (2005) 58-63
83. 2+ influx. Biochem. J. 264 (1989) 539-546
84. Arnoult C., Lemos J.R., and Florman H.M. Voltage-dependent modulation of T-type calcium channels by protein tyrosine phosphorylation. EMBO J. 16 (1997) 1593-1599
85. Wolfe J.T., Wang H., Perez-Reyes E., and Barrett P.Q. Stimulation of recombinant Ca(v)3.2, T-type, Ca(2+) channel currents by CaMKIIgamma(C). J. Physiol. 538 (2002) 343-355
86. Lopez-Gonzalez I., De La Vega-Beltran J.L., Santi C.M., Florman H.M., Felix R., and Darszon A. Calmodulin antagonists inhibit T-type Ca(2+) currents in mouse spermatogenic cells and the zona pellucida-induced sperm acrosome reaction. Dev. Biol. 236 (2001) 210-219
87. 2+ channel currents in cultured rat bone marrow cells. J. Physiol. 489 Pt 3 (1995) 649-661
88. Alvarez J.L., Rubio L.S., and Vassort G. Facilitation of T-type calcium current in bullfrog atrial cells: voltage-dependent relief of a G protein inhibitory tone. J. Physiol. 491 Pt 2 (1996) 321-334
89. Gomora J.C., Murbartian J., Arias J.M., Lee J.H., and Perez-Reyes E. Cloning and expression of the human T-type channel Ca(v)3.3: insights into prepulse facilitation. Biophys. J. 83 (2002) 229-241
90. Sanchez D., Labarca P., and Darszon A. Sea urchin sperm cation-selective channels directly modulated by cAMP. FEBS Lett. 503 (2001) 111-115
91. Gorelik J., Gu Y., Spohr H.A., Shevchuk A.I., Lab M.J., Harding S.E., Edwards C.R., Whitaker M., Moss G.W., Benton D.C., Sanchez D., Darszon A., Vodyanoy I., Klenerman D., and Korchev Y.E. Ion channels in small cells and subcellular structures can be studied with a smart patch-clamp system. Biophys. J. 83 (2002) 3296-3303
92. Gu Y., Kirkman-Brown J.C., Korchev Y., Barratt C.L., and Publicover S.J. Multi-state, 4-aminopyridine-sensitive ion channels in human spermatozoa. Dev. Biol. 274 (2004) 308-317
93. Korchev Y.E., Gorelik J., Lab M.J., Sviderskaya E.V., Johnston C.L., Coombes C.R., Vodyanoy I., and Edwards C.R. Cell volume measurement using scanning ion conductance microscopy. Biophys. J. 78 (2000) 451-457
94. 2+ channels from the sea urchin sperm plasma membrane. J. Gen. Physiol. 95 (1990) 273-296
95. Guerrero A., Sanchez J.A., and Darszon A. Single-channel activity in sea urchin sperm revealed by the patch-clamp technique. FEBS Lett. 220 (1987) 295-298
96. 2+ channel found in sea urchin and mouse spermatozoa. FEBS Lett. 338 (1994) 23-26
97. Shevchuk A.I., Frolenkov G.I., Sanchez D., James P.S., Freedman N., Lab M.J., Jones R., Klenerman D., and Korchev Y.E. Imaging proteins in membranes of living cells by high-resolution scanning ion conductance microscopy. Angew. Chem. Int. Ed. Engl. (2006)
98. Parvinen M. The chromatoid body in spermatogenesis. Int. J. Androl. 28 (2005) 189-201
99. Miller D., Ostermeier G.C., and Krawetz S.A. The controversy, potential and roles of spermatozoal RNA. Trends Mol. Med. 11 (2005) 156-163
100. Kumar G., Patel D., and Naz R.K. c-MYC mRNA is present in human sperm cells. Cell Mol. Biol. Res. 39 (1993) 111-117
101. Ostermeier G.C., Miller D., Huntriss J.D., Diamond M.P., and Krawetz S.A. Reproductive biology: delivering spermatozoan RNA to the oocyte. Nature 429 (2004) 154
102. 2+ spikes in the flagellum control chemotactic behavior of sperm. Embo. J. 24 (2005) 2741-2752
103. Kaupp U.B., Solzin J., Hildebrand E., Brown J.E., Helbig A., Hagen V., Beyermann M., Pampaloni F., and Weyand I. The signal flow and motor response controlling chemotaxis of sea urchin sperm. Nat. Cell Biol. 5 (2003) 109-117