Expression, localization and functions in acrosome reaction and sperm motility of Cav3.1 and Cav3.2 channels in sperm cells: An evaluation from Cav3.1 and Cav3.2 deficient mice

Journal of Cellular Physiology

Volumn 212, Issue 3, 2007, Pages 753-763

  Escoffier, Jessica ^a   Boisseau, Sylvie ^a   Serres, Catherine ^b   Chen, Chien Chang ^c   Kim, Daesoo ^d   Stamboulian, Séverine ^a   Shin, Hee Sup ^d   Campbell, Kevin P ^c   De Waard, Michel ^a   Arnoult, Christophe ^a,e  

^a GRENOBLE INSTITUT DES NEUROSCIENCES   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c UNIVERSITY OF IOWA   (United States)

^d Korea Institute of Science and Technology   (South Korea)

^e CEA GRENOBLE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CHANNEL; POTASSIUM CHLORIDE; VOLTAGE GATED CALCIUM CHANNEL;

ACROSOME REACTION; AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CALCIUM CURRENT; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL FUNCTION; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SPERMATOCYTE; SPERMATOGENESIS; SPERMATOZOON MOTILITY; WESTERN BLOTTING; ZONA PELLUCIDA;

ACROSOME REACTION; ANIMALS; CALCIUM CHANNELS, T-TYPE; CALCIUM SIGNALING; CELLS, CULTURED; FEMALE; GENOTYPE; LITTER SIZE; MALE; MEMBRANE POTENTIALS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PHENOTYPE; POTASSIUM; SPERM MOTILITY; SPERMATOZOA; TIME FACTORS; TRANSFECTION;

MUS;

EID: 34547940325     PISSN: 00219541     EISSN: None     Source Type: Journal    
DOI: 10.1002/jcp.21075     Document Type: Article

References (40)

1. Arnoult C, Cardullo RA, Lemos JR, Florman HM. 1996. Activation of mouse sperm T-type Ca2+ channels by adhesion to the egg zona pellucida. Proc Natl Acad Sci U S A 93:13004-13009.
2. Arnoult C, Villaz M, Florman HM. 1998. Pharmacological properties of the T-type Ca2+ current of mouse spermatogenic cells. Mol Pharmacol 53:1104-1111.
3. Arnoult C, Kazam IG, Visconti PE, Kopf GS, Villaz M, Florman HM. 1999. Control of the low voltage-activated calcium channel of mouse sperm by egg ZP3 and by membrane hyperpolarization during capacitation. Proc Natl Acad Sci U S A 96:6757-6762.
4. Castellano LE, Trevino CL, Rodriguez D, Serrano CJ, Pacheco J, Tsutsumi V, Felix R, Darszon A. 2003. Transient receptor potential (TRPC) channels in human sperm: expression, cellular localization and involvement in the regulation of flagellar motility. FEBS Lett 541:69-74.
5. Chen CC, Lamping KG, Nuno DW, Barresi R, Prouty SJ, Lavoie JL, Cribbs LL, England SK, Sigmund CD, Weiss RM, Williamson RA, Hill JA, Campbell KP. 2003. Abnormal coronary function in mice deficient in alpha1H T-type Ca2+ channels. Science 302:1416-1418.
6. De Blas G, Michaut M, Trevino CL, Tomes CN, Yunes R, Darszon A, Mayorga LS. 2002. The intraacrosomal calcium pool plays a direct role in acrosomal exocytosis. J Biol Chem 277:49326-49331.
7. Espinosa F, Lopez-Gonzalez I, Serrano CJ, Gasque G, De La Vega-Beltran JL, Trevino CL, Darszon A. 1999. Anion channel blockers differentially affect T-type Ca(2+) currents of mouse spermatogenic cells, alphaIE currents expressed in Xenopus oocytes and the sperm acrosome reaction. Dev Genet 25:103-114.
8. Florman HM, Arnoult C, Kazam IG, Li C, O'Toole CM. 1998. A perspective on the control of mammalian fertilization by egg-activated ion channels in sperm: a tale of two channels. Biol Reprod S9:12-16.
9. Fukami K, Yoshida M, Inoue T, Kurokawa M, Fissore RA, Yoshida N, Mikoshiba K, Takenawa T. 2003. Phospholipase Cdelta4 is required for Ca2+ mobilization essential for acrosome reaction in sperm. J Cell Biol 161:79-88.
10. Goodwin LO, Leeds NB, Hurley I, Mandel FS, Pergolizzi RG, Benoff S. 1997. Isolation and characterization of the primary structure of testis- specific L-type calcium channel: Implications for contraception. Mol Hum Reprod 3:255-268.
11. Goodwin LO, Leeds NB, Hurley I, Cooper GW, Pergolizzi RG, Benoff S. 1998. Alternative splicing of exons in the alpha1 subunit of the rat testis L- type voltage-dependent calcium channel generates germ line-specific dihydropyridine binding sites. Mol Hum Reprod 4:215-226.
12. Goodwin LO, Leeds NB, Guzowski D, Hurley IR, Pergolizzi RG, Benoff S. 1999. Identification of structural elements of the testis-specific voltage dependent calcium channel that potentially regulate its biophysical properties. Mol Hum Reprod 5:311-322.
13. Hagiwara S, Kawa K. 1984. Calcium and potassium currents in spermatogenic cells dissociated from rat seminiferous tubules. J Physiol 356:135-149.
14. Hanna WF, Kerr CL, Shaper JH, Wright WW. 2004. Lewis X-containing neoglycoproteins mimic the intrinsic ability of zona pellucida glycoprotein ZP3 to induce the acrosome reaction in capacitated mouse sperm. Biol Reprod 71:778-789.
15. Herrick SB, Schweissinger DL, Kim SW, Bayan KR, Mann S, Cardullo RA. 2004. The acrosomal vesicle of mouse sperm is a calcium store. J Cell Physiol 202:663-671.
16. Inoue N, Ikawa M, Isotani A, Okabe M. 2005. The immunoglobulin superfamily protein Izumo is required for sperm to fuse with eggs. Nature 434:234-238.
17. Jagannathan S, Punt EL, Gu Y, Arnoult C, Sakkas D, Barratt CL, Publicover SJ. 2002. Identification and localization of T-type voltage operated calcium channel subunits in human male germ cells - expression of multiple isoforms. J Biol Chem 277:8449-8456.
18. Jun K, Piedras-Renteria ES, Smith SM, Wheeler DB, Lee SB, Lee TG, Chin H, Adams ME, Scheller RH, Tsien RW, Shin HS. 1999. Ablation of P/Q-type Ca(2+) channel currents, altered synaptic transmission, and progressive ataxia in mice lacking the alpha(1A)-subunit. Proc Natl Acad Sci U S A 96:15245-15250.
19. Jungnickel MK, Marrero H, Birnbaumer L, Lemos JR, Florman HM. 2001. Trp2 regulates entry of Ca2+ into mouse sperm triggered by egg ZP3. Nat Cell Biol 3:499-502.
20. Kim DK, Catterall WA. 1997. Ca2+-dependent and -independent interactions of the isoforms of the alpha1A subunit of brain Ca2+ channels with presynaptic SNARE proteins. Proc Natl Acad Sci U S A 94:14782-14786.
21. Kim C, Jun K, Lee T, Kim SS, McEnery MW, Chin H, Kim HL, Park JM, Kim DK, Jung SJ. Kim J, Shin HS. 2001a. Altered nociceptive response in mice deficient in the alpha(1B) subunit of the voltage-dependent calcium channel. Mol Cell Neurosci 18:235-245.
22. Kim D, Song I, Keum S, Lee T, Jeong MJ, Kim SS, McEnery MW, Shin HS. 2001b. Lack of the burst firing of thalamocortical relay neurons and resistance to absence seizures in mice lacking alpha(1G) T-type Ca(2+) channels. Neuron 31:35-45.
23. Kirkman-Brown JC, Bray C, Stewart PM, Barratt CL, Publicover SJ. 2000. Biphasic elevation of [Ca(2+)](i) in individual human spermatozoa exposed to progesterone. Dev Biol 222:326-335.
24. Lievano A, Santi CM, Serrano CJ, Trevino CL, Bellve AR, Hernandez-Cruz A, Darszon A. 1996. T-type Ca2+ channels and alpha1E expression in spermatogenic cells, and their possible relevance to the sperm acrosome reaction. FEBS Lett 388:150-154.
25. O'Toole CM, Arnoult C, Darszon A, Steinhardt RA, Florman HM. 2000. Ca(2+) entry through store-operated channels in mouse sperm is initiated by egg ZP3 and drives the acrosome reaction. Mol Biol Cell 11:1571-1584.
26. Rockwell PL, Storey BT. 2000. 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 Ca(2+) changes monitored by fluo-3. Mol Reprod Dev 55:335-349.
27. Romrell LJ, Bellve AR, Fawcett DW. 1976. Separation of mouse spermatogenic cells by sedimentation velocity. A morphological characterization. Dev Biol 49:119-131.
28. Saegusa H, Kurihara T, Zong S, Minowa O, Kazuno A, Han W, Matsuda Y, Yamanaka H, Osanai M, Noda T, Tanabe T. 2000. Altered pain responses in mice lacking alpha1E subunit of the voltage-dependent Ca2+ channel. Proc Natl Acad Sci U S A 97:6132-6137.
29. Sakata Y, Saegusa H, Zong S, Osanai M, Murakoshi T, Shimizu Y, Noda T, Aso T, Tanabe T. 2001. Analysis of Ca(2+) currents in spermatocytes from mice lacking Ca(v)2.3 (alpha(1E)) Ca(2+) channel. Biochem Biophys Res Commun 288:1032-1036.
30. Santi CM, Darszon A, Hernandez-Cruz A. 1996. A dihydropyridine-sensitive T-type Ca2+ current is the main Ca2+ current carrier in mouse primary spermatocytes. Am J Physiol 271:C1583-. CI593.
31. Serrano CJ, Trevino CL, Felix R, Darszon A. 1999. Voltage-dependent Ca(2+) channel subunit expression and immunolocalization in mouse spermatogenic cells and sperm. FEBS Lett 462:171-176.
32. Shirakawa H, Miyazaki S. 1999. Spatiotemporal characterization of intracellular Ca2+ rise during the acrosome reaction of mammalian spermatozoa induced by zona pellucida. Dev Biol 208:70-78.
33. Stamboulian S, Kim D, Shin HS, Ronjat M, De Waard M, Arnoult C. 2004. Biophysical and pharmacological characterization of spermatogenic T-type calcium current in mice lacking the Ca V3.1 (alpha1G) calcium channel: CaV3.2 (alpha1H) is the main functional calcium channel in wild-type spermatogenic cells. J Cell Physiol 200:116-124.
34. Sutton KA, Jungnickel MK, Wang Y, Cullen K, Lambert S, Florman HM. 2004. Enkurin is a novel calmodulin and TRPC channel binding protein in sperm. Dev Biol 274:426-435.
35. Trevino CL, Serrano CJ, Beltran C, Felix R, Darszon A. 2001. Identification of mouse trp homologs and lipid rafts from spermatogenic cells and sperm. FEBS Lett 509:119-125.
36. Trevino CL, Felix R, Castellano LE, Gutierrez C, Rodriguez D, Pacheco J, Lopez-Gonzalez I, Gomora JC, Tsutsumi V, Hernandez-Cruz A, Fiordelisio T, Scaling AL, Darszon A. 2004. Expression and differential cell distribution of low-threshold Ca(2+) channels in mammalian male germ cells and sperm. FEBS Lett 563:87-92.
37. Walensky LD, Snyder SH. 1995. Inositol 1,4,5-trisphosphate receptors selectively localized to the acrosomes of mammalian sperm. J Cell Biol 130:857-869.
38. Wennemuth G, Westenbroek RE, Xu T, Hille B, Babcock DF. 2000. Ca V2.2 and CaV2.3 (N-and R-type) Ca2+ channels in depolarization-evoked entry of Ca2+ into mouse sperm. J Biol Chem 275:21210-21217.
39. Westenbroek RE, Babcock DF. 1999. Discrete regional distributions suggest diverse functional roles of calcium channel alpha1 subunits in sperm. Dev Biol 207:457-469.
40. Zhang D, Chen J, Saraf A, Cassar S, Han P, Rogers JC, Brioni JD, Sullivan JP, Gopalakrishnan M. 2006. Association of CatSper1 or 2 with Cav3.3 leads to suppression of T-type calcium channel activity. J Biol Chem 281:22332-22341.