ZP3-dependent activation of sperm cation channels regulates acrosomal secretion during mammalian fertilization

Journal of Cell Biology

Volumn 134, Issue 3, 1996, Pages 637-645

  Arnoult, Christophe ^a   Zeng, Yang ^b   Florman, Harvey M ^a  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACROSOME; ANIMAL CELL; ARTICLE; CALCIUM TRANSPORT; CATTLE; CHANNEL GATING; FERTILIZATION; ION TRANSPORT; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; ZONA PELLUCIDA;

ANIMALIA; BOS TAURUS; MAMMALIA;

EID: 0029775791     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.134.3.637     Document Type: Article

References (69)

1. Arnoult, C., and M. Villaz. 1994. Differential developmental fates of the two calcium currents in early embryos of the ascidian Ciona intestinalis. J. Membr. Biol. 137:127-135.
2. 2+] and pH of mammalian sperm by voltage-dependent and pH -sensitive mechanisms. J. Biol. Chem. 262:15041-15047.
3. Babcock, D.F., G.A. Rufo, and H.A. Lardy. 1983. Potassium-dependent increases in cytosolic pH stimulate metabolism and motility of mammalian sperm. Proc. Natl. Acad. Sci. USA. 80:1327-1331.
4. Bailey, J.L., and B.T. Storey. 1994. Calcium influx into mouse spermatozoa activated by solubilized mouse zona pellucida, monitored with the calcium fluorescent indicator, fluo-3. Inhibition of the influx by the influx by three inhibitors of the zona pellucida induced acrosome reaction: tyrphostin A48, pertussis toxin, and 3′-quinuclidinyl benzilate. Mol. Reprod. Dev. 39:297-308.
5. Beebe, S.J., L. Leyton, D. Burks, M. Ishikawa, T. Fuerst, J. Dean, and P. Saling. 1992. Recombinant mouse ZP3 inhibits sperm binding and induces the acrosome reaction. Dev. Biol. 151:48-54.
6. Benoff, S., G.W. Cooper, I. Hurley, F.S. Mandel, D.L. Rosenfeld, G.M. Scholl, B.R. Gilbert, and A. Hershlag. 1994. The effect of calcium ion channel blockers of sperm fertilization potential. Fertil. Steril. 62:606-617.
7. Blatz, A.L. 1991. Asymmetric proton block of inward rectifier K channels in skeletal muscle. Pfluegers Arch. Eur. J. Physiol. 401:402-407.
8. Bleil, J.D., and P.M. Wassarman. 1980. Mammalian sperm-egg interaction: identification of a glycoprotein in mouse egg zonae pellucidae possessing receptor activity for sperm. Cell. 20:873-882.
9. Bleil, J.D., and P.M. Wassarman. 1980. Structure and function of the zona pellucida: identification and characterization of the proteins of the mouse oocyte's zona pellucida. Dev. Biol. 76:185-202.
10. Bleil, J.D., and P.M. Wassarman. 1983. Sperm-egg interactions in the mouse: sequence of events and induction of the acrosome reaction by a zona pellucida glycoprotein. Dev. Biol. 95:317-324.
11. Bleil, J.D., and P.M. Wassarman. 1986. Autoradiographic visualization of the mouse egg's sperm receptor bound to sperm. J. Cell Biol. 102:1363-1371.
12. Bleil, J.D., and P.M. Wassarman. 1990. Identification of a ZP3-binding protein on acrosome-intact mouse sperm by photoaffinity crosslinking. Proc. Natl. Acad. Sci. USA. 87:5563-5567.
13. Christensen, B.N., and E. Hida. 1990. Protonation of histidine groups inhibits gating of the quisqualate/kainate channel protein in isolated catfish cone cells. Neuron. 5:471-478.
14. Clark, E.N., M.E. Corron, and H.M. Florman. 1993. Caltrin, the calcium transport regulatory peptide of spermatozoa, modulates acrosomal exocytosis in response to the egg's zona pellucida. J. Biol. Chem. 268:5309-5316.
15. + channels in pancreatic B-cells. Nature (Lond.). 311: 269-271.
16. Cox, T., P. Campbell, and R.N. Peterson. 1991. Ion channels in boar sperm plasma membranes: characterization of a cation selective channel. Mol. Reprod. Dev. 30:135-147.
17. Davies, N.W., N.B. Standen, and P.R. Stanfield. 1992. The effect of intracellular pH on ATP-dependent potassium channels of frog skeletal muscle. J. Physiol. (Camb.). 445:549-568.
18. Dixon, D.B., K.-I. Takahashi, and D.R. Copenhagen. 1993. L-Glutamate suppresses HVA calcium current in catfish horizontal cells by raising intracellular proton concentration. Neuron. 11:267-277.
19. Endo, Y., M.A. Lee, and G.S. Kopf. 1987. Evidence for a role of a guanine nucleotide-binding regulatory protein in the zona pellucida-induced mouse sperm acrosome reaction. Dev. Biol. 119:210-216.
20. Endo, Y., M.A. Lee, and G.S. Kopf. 1988. Characterization of an islet-activating protein sensitive site in mouse sperm that is involved in the zona pellucida-induced acrosome reaction. Dev. Biol. 129:12-24.
21. 2+ are initiated by the zona pellucida during acrosomal exocytosis. Dev. Biol. 165:152-164.
22. Florman, H.M., and D.F. Babcock. 1990. Progress toward understanding the molecular basis of capacitation. In Elements of Mammalian Fertilization. Basic Concepts. P.M. Wassarman, editor. CRC Press, Boca Raton, FL. 105-132.
23. Florman, H.M., and N.L. First. 1988. The regulation of acrosomal exocytosis. I. Sperm capacitation is required for the induction of acrosome reactions by the bovine zona pellucida in vitro. Dev. Biol. 128:453-463.
24. Florman, H.M., R.M. Tombes, N.L. First, and D.F. Babcock. 1989. An adhesion-associated agonist from the zona pellucida activates G protein-promoted elevations of internal Ca and pH that mediate mammalian sperm acrosomal exocytosis. Dev. Biol. 135:133-146.
25. Florman, H.M., M.E. Corron, T.D.-H. Kim, and D.F. Babcock. 1992. Activation of voltage-dependent calcium channels of mammalian sperm is required for zona pellucida-induced acrosomal exocytosis. Dev. Biol. 152: 304-314.
26. Foresta, C., M. Rossato, and F. Di Virgilio. 1993. Ion fluxes through the progesterone-activated channel of the sperm plasma membrane. Biochem. J. 294:279-283.
27. Gong, X., D.H. Dubois, D.J. Miller, and B.D. Shur. 1995. Activation of a G protein complex by aggregation of β-1,4-galactosyltransferase on the surface of sperm. Science (Wash. DC). 269:1718-1721.
28. +-currents in rat tectal neurons. Neurosci Lett. 89:198-203.
29. 2+ channels during the egg jelly-induced acrosome reaction of sea urchin sperm. J. Biol. Chem. 264:19593-19599.
30. Haynes, L.W. 1992. Block of the cyclic GMP-gated channel of vertebrate rod and cone photoreceptors by l-cis-diltiazem. J. Gen. Physiol. 100:783-801.
31. Hershlag, A., G.W. Cooper, and S. Benoff. 1995. Pregnancy following discontinuation of a calcium channel blocker in the male partner. Hum. Reprod. 10:599-606.
32. Hille, B. 1992. Ionic Channels of Excitable Membranes. Sinauer Associates. Inc., Sunderland. MA. 594 pp.
33. Hinton, B.T., and M.A. Palladino. 1995. Epididymal epithelium: its contribution to the formation of a luminal fluid microenvironment. Microscopy Research and Tecnhique. 30:67-81.
34. Kaibara, M., and M. Kameyama. 1988. Inhibition of the calcium channel by intracellular protons in single ventricular myocytes of the guinea pig. J. Physiol. (Camb.) 403:621-640.
35. Kinloch, R.A., S. Mortillo, C.L. Stewart, and P.M. Wassarman. 1991. Embryonal carcinoma cells transfected with ZP3 genes differentially glycosylate similar polypeptides and secrete active mouse sperm receptor. J. Cell Biol. 115:655-664.
36. 2+ channels. J. Gen. Physiol. 103:647-663.
37. + channel from rat skeletal muscle incorporated into planar bilayers. J. Gen. Physiol. 98:1025-1043.
38. 2+ permeability: population and single cell kinetics. Gamete Res. 24:303-326.
39. Leyton, L., and P. Saling. 1989. 95 kd sperm proteins bind ZP3 and serve as tyrosine kinase substrates in response to zona binding. Cell. 57:1123-1130.
40. Leyton, L., P. LeGuen, D. Bunch, and P.M. Saling. 1992. Regulation of mouse gamete interaction by a sperm tyrosine kinase. Proc. Natl. Acad. Sci. USA. 89:11692-11695.
41. McDonald, T.F., S. Pelzer, W. Trautwein, and D. J. Pelzer. 1994. Regulation and modulation of calcium channels in cardiac, skeletal, and smooth muscle cells. Physiol. Rev. 74:365-507.
42. Miller, D.J., M.B. Macek, and B.D. Shur. 1992. Complementarity between sperm surface β-1,4-galactosyltransferase and egg-coat ZP3 mediates sperm-egg binding. Nature (Lond.). 357:589-593.
43. Miller, D.J., X. Gong, and B.D. Shur. 1993. Sperm require β-N-acetylglucosaminidase to penetrate through the egg zona pellucida. Development (Camb.). 118:1279-1289.
44. Mohr, F.C., and C. Fewtrell. 1987. IgE receptor-mediated depolarization of rat basophilic leukemia cells measured with the fluorescent probe bis-oxonal. J. Immunol. 138:1564-1570.
45. Moller, C.C., J.D. Bleil, R.A. Kinloch, and P.M. Wassarman. 1990. Structural and functional relationships between mouse and hamster zona pellucida glycoproteins. Dev. Biol. 137:276-286.
46. + on the electrical properties of excitable cells. Annu. Rev. Neurosci. 7:257-278.
47. Mortillo, S., and P.M. Wassarman. 1991. Differential binding of gold-labeled zona pellucida glycoproteins mZP2 and mZP3 to mouse sperm membrane compartments. Development. 113:141-149.
48. Orlowski, J., R.A. Kandasamy, and G.E. Shull. 1992. Molecular cloning of putative members of the Na/H exchanger gene family. cDNA cloning, deduced amino acid sequence, and mRNA tissue expression of the rat Na/H exchanger NHE-1 and two structurally related proteins. J. Biol. Chem. 267:9331-9339.
49. Parkkila, S., H. Rajaniemi, and S. Kellokumpu. 1993. Polarized expression of a band 3-related protein in mammalian sperm cells. Biol. Reprod. 49: 326-331.
50. Parrish, J.J., J.L. Susko-Parrish, and N.L. First. 1989. Capacitation of bovine sperm by heparin: Inhibitory effect of glucose and role of intracellular pH. Biol. Reprod. 41:683-699.
51. + as permeant ions. J. Gen. Physiol. 94:1-21.
52. Roos, A., and W.F. Boron. 1981. Intracellular pH. Physiol. Rev. 61:296-434.
53. Schoff, P.K., and H.A. Lardy. 1987. The effects of fluoride and caffeine on the metabolism and motility of ejaculated bovine spermatozoa. Biol. Reprod. 37:1037-1046.
54. 31P-NMR study of the epididymis and epididymal sperm of the bovine and hamster. Biol. Reprod. 33:1029-1035.
55. + channel possessing two transmembrane segments. Nature (Lond.). 367:642-645.
56. 2+-selective channels in planar lipid bilayers. Am. J. Physiol. 268: C1284-C1294.
57. Tomes, C.N., C.R. McMaster, and P.M. Saling. 1996. Activation of mouse sperm phosphatidylinositol-4,5 bisphosphate-phospholipase C by zona pellucida is modulated by tyrosine phosphorylation. Mol. Reprod. Dev. 43:196-204.
58. Umbach, J.A. 1982. Changes in intracellular pH affect calcium currents in Paramecium caudatum. Proc. R. Soc. Lond. B. Biol. Sci. 216:209-224.
59. Vredenburgh, W.L., and J.J. Parrish. 1995. Intracellular pH of bovine sperm increases during capacitation. Mol. Reprod. Dev. 40:490-502.
60. Ward, C.R., and G.S. Kopf. 1993. Molecular events mediating gamete activation. Dev. Biol. 158:9-34.
61. Ward, C.R., and B.T. Storey. 1984. Determination of the time course of capacitation in mouse spermatozoa using a chlortetracycline fluorescence assay. Dev. Biol. 104:287-296.
62. i protein in mouse sperm membranes by solubilzed proteins of the zona pellucida, the egg's extracellular matrix. J. Biol. Chem. 267:14061-14067.
63. Wassarman, P.M. 1988. Zona pellucida glycoproteins. Ann. Rev. Biochem. 57:415-442.
64. Wassarman, P.M., and S. Mortillo. 1991. Structure of the mouse egg extracellular coat, the zona pellucida. Int. Rev. Cytol. 130:85-110.
65. Weyand, I., M. Godde, S. Frings, J. Weiner, F. Muller, W. Altenhofer, H. Hatt, and U.B. Kaupp. 1994. Cloning and functional expression of a cyclic-nucleotide-gated channel from mammalian sperm. Nature (Lond.). 368:859-863.
66. Wickman, K., and D.E. Clapham. 1995. Ion channel regulation by G proteins. Physiol. Rev. 75:865-885.
67. Yanagimachi, R. 1994. Mammalian fertilization. In The Physiology of Reproduction. E. Knobil and J.D. Neill, editors. Raven Press, Ltd., New York. 189-317.
68. Zeng, Y., E.N. Clark, and H.M. Florman. 1995. Sperm membrane potential: hyperpolarization during capacitation regulates zona pellucida-dependent acrosomal secretion. Dev. Biol. 171:554-563.
69. --dependent and arylaminobenzoate-dependent mechanisms in the control of internal pH in mouse sperm. Dev. Biol. 173:510-520.