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. 1995 Aug 2;130(4):857–869. doi: 10.1083/jcb.130.4.857

Inositol 1,4,5-trisphosphate receptors selectively localized to the acrosomes of mammalian sperm

PMCID: PMC2199962  PMID: 7642703

Abstract

Calcium flux is required for the mammalian sperm acrosome reaction, an exocytotic event triggered by egg binding, which results in a dramatic rise in sperm intracellular calcium. Calcium-dependent membrane fusion results in the release of enzymes that facilitate sperm penetration through the zona pellucida during fertilization. We have characterized inositol 1,4,5-trisphosphate (IP3)-gated calcium channels and upstream components of the phosphoinositide signaling system in mammalian sperm. Peptide antibodies colocalized G alpha q/11 and the beta 1 isoform of phospholipase C (PLC beta 1) to the anterior acrosomal region of mouse sperm. Western blotting using a polyclonal antibody directed against purified brain IP3 receptor (IP3R) identified a specific 260 kD band in 1% Triton X-100 extracts of rat, hamster, mouse and dog sperm. In each species, IP3R immunostaining localized to the acrosome cap. Scatchard analysis of [3H]IP3 binding to rat sperm sonicates revealed a curvilinear plot with high affinity (Kd = 26 nM, Bmax = 30 pmol/mg) and low affinity (Kd = 1.6 microM, Bmax = 550 pmol/mg) binding sites, reflecting among the highest receptor densities in mammalian tissue. Immunoelectron microscopy confirmed the acrosomal localization in rat sperm. The IP3R fractionated with acrosomes by discontinuous sucrose gradient centrifugation and was enriched in the medium of acrosome- reacted sperm. ATP-dependent 45Ca2+ loading of digitonin permeabilized rat sperm was decreased by 45% in the presence of 10 microM IP3. The IP3-mediated release of calcium was blocked by heparin. Thapsigargin, a sequiterpene lactone inhibitor of the microsomal Ca(2+)-ATPase, stimulated the acrosome reaction of mouse sperm to the same extent as the Ca2+ ionophore, A23187. The failure of caffeine and ryanodine to affect calcium accumulation suggested that thapsigargin acted through an IP3-sensitive store. The presence of G alpha q/11, PLC beta 1 and a functional IP3R in the anterior acrosomal region of mammalian sperm, as well as thapsigargin's induction of the acrosome reaction, implicate IP3-gated calcium release in the mammalian acrosome reaction.

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Selected References

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  1. Abrahamsson H., Gylfe E., Hellman B. Influence of external calcium ions on labelled calcium efflux from pancreatic beta-cells and insulin granules in mice. J Physiol. 1981 Feb;311:541–550. doi: 10.1113/jphysiol.1981.sp013603. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Baffy G., Yang L., Wolf B. A., Williamson J. R. G-protein specificity in signaling pathways that mobilize calcium in insulin-secreting beta-TC3 cells. Diabetes. 1993 Dec;42(12):1878–1882. doi: 10.2337/diab.42.12.1878. [DOI] [PubMed] [Google Scholar]
  3. Berridge M. J., Irvine R. F. Inositol phosphates and cell signalling. Nature. 1989 Sep 21;341(6239):197–205. doi: 10.1038/341197a0. [DOI] [PubMed] [Google Scholar]
  4. Berryman M. A., Porter W. R., Rodewald R. D., Hubbard A. L. Effects of tannic acid on antigenicity and membrane contrast in ultrastructural immunocytochemistry. J Histochem Cytochem. 1992 Jun;40(6):845–857. doi: 10.1177/40.6.1350287. [DOI] [PubMed] [Google Scholar]
  5. Bird G. S., Rossier M. F., Hughes A. R., Shears S. B., Armstrong D. L., Putney J. W., Jr Activation of Ca2+ entry into acinar cells by a non-phosphorylatable inositol trisphosphate. Nature. 1991 Jul 11;352(6331):162–165. doi: 10.1038/352162a0. [DOI] [PubMed] [Google Scholar]
  6. Blackmore P. F., Beebe S. J., Danforth D. R., Alexander N. Progesterone and 17 alpha-hydroxyprogesterone. Novel stimulators of calcium influx in human sperm. J Biol Chem. 1990 Jan 25;265(3):1376–1380. [PubMed] [Google Scholar]
  7. Blackmore P. F., Neulen J., Lattanzio F., Beebe S. J. Cell surface-binding sites for progesterone mediate calcium uptake in human sperm. J Biol Chem. 1991 Oct 5;266(28):18655–18659. [PubMed] [Google Scholar]
  8. Bleil J. D., Wassarman P. M. Mammalian sperm-egg interaction: identification of a glycoprotein in mouse egg zonae pellucidae possessing receptor activity for sperm. Cell. 1980 Jul;20(3):873–882. doi: 10.1016/0092-8674(80)90334-7. [DOI] [PubMed] [Google Scholar]
  9. Bleil J. D., Wassarman P. M. Sperm-egg interactions in the mouse: sequence of events and induction of the acrosome reaction by a zona pellucida glycoprotein. Dev Biol. 1983 Feb;95(2):317–324. doi: 10.1016/0012-1606(83)90032-5. [DOI] [PubMed] [Google Scholar]
  10. Blondel O., Moody M. M., Depaoli A. M., Sharp A. H., Ross C. A., Swift H., Bell G. I. Localization of inositol trisphosphate receptor subtype 3 to insulin and somatostatin secretory granules and regulation of expression in islets and insulinoma cells. Proc Natl Acad Sci U S A. 1994 Aug 2;91(16):7777–7781. doi: 10.1073/pnas.91.16.7777. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Borgese F., Sardet C., Cappadoro M., Pouyssegur J., Motais R. Cloning and expression of a cAMP-activated Na+/H+ exchanger: evidence that the cytoplasmic domain mediates hormonal regulation. Proc Natl Acad Sci U S A. 1992 Aug 1;89(15):6765–6769. doi: 10.1073/pnas.89.15.6765. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Brass L. F., Joseph S. K. A role for inositol triphosphate in intracellular Ca2+ mobilization and granule secretion in platelets. J Biol Chem. 1985 Dec 5;260(28):15172–15179. [PubMed] [Google Scholar]
  13. Cheek T. R., Barry V. A. Stimulus-secretion coupling in excitable cells: a central role for calcium. J Exp Biol. 1993 Nov;184:183–196. doi: 10.1242/jeb.184.1.183. [DOI] [PubMed] [Google Scholar]
  14. Cheng A., Le T., Palacios M., Bookbinder L. H., Wassarman P. M., Suzuki F., Bleil J. D. Sperm-egg recognition in the mouse: characterization of sp56, a sperm protein having specific affinity for ZP3. J Cell Biol. 1994 May;125(4):867–878. doi: 10.1083/jcb.125.4.867. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Domino S. E., Garbers D. L. The fucose-sulfate glycoconjugate that induces an acrosome reaction in spermatozoa stimulates inositol 1,4,5-trisphosphate accumulation. J Biol Chem. 1988 Jan 15;263(2):690–695. [PubMed] [Google Scholar]
  16. Ehrlich B. E., Kaftan E., Bezprozvannaya S., Bezprozvanny I. The pharmacology of intracellular Ca(2+)-release channels. Trends Pharmacol Sci. 1994 May;15(5):145–149. doi: 10.1016/0165-6147(94)90074-4. [DOI] [PubMed] [Google Scholar]
  17. Endo Y., Lee M. A., Kopf G. S. Evidence for the role of a guanine nucleotide-binding regulatory protein in the zona pellucida-induced mouse sperm acrosome reaction. Dev Biol. 1987 Jan;119(1):210–216. doi: 10.1016/0012-1606(87)90222-3. [DOI] [PubMed] [Google Scholar]
  18. Ferris C. D., Huganir R. L., Supattapone S., Snyder S. H. Purified inositol 1,4,5-trisphosphate receptor mediates calcium flux in reconstituted lipid vesicles. Nature. 1989 Nov 2;342(6245):87–89. doi: 10.1038/342087a0. [DOI] [PubMed] [Google Scholar]
  19. Florman H. M., Corron M. E., Kim T. D., Babcock D. F. Activation of voltage-dependent calcium channels of mammalian sperm is required for zona pellucida-induced acrosomal exocytosis. Dev Biol. 1992 Aug;152(2):304–314. doi: 10.1016/0012-1606(92)90137-6. [DOI] [PubMed] [Google Scholar]
  20. Florman H. M. Sequential focal and global elevations of sperm intracellular Ca2+ are initiated by the zona pellucida during acrosomal exocytosis. Dev Biol. 1994 Sep;165(1):152–164. doi: 10.1006/dbio.1994.1242. [DOI] [PubMed] [Google Scholar]
  21. Florman H. M., Tombes R. M., First N. L., Babcock D. F. An adhesion-associated agonist from the zona pellucida activates G protein-promoted elevations of internal Ca2+ and pH that mediate mammalian sperm acrosomal exocytosis. Dev Biol. 1989 Sep;135(1):133–146. doi: 10.1016/0012-1606(89)90164-4. [DOI] [PubMed] [Google Scholar]
  22. Fraser L. R. Calcium channels play a pivotal role in the sequence of ionic changes involved in initiation of mouse sperm acrosomal exocytosis. Mol Reprod Dev. 1993 Nov;36(3):368–376. doi: 10.1002/mrd.1080360313. [DOI] [PubMed] [Google Scholar]
  23. Fraser L. R. Na+ requirements for capacitation and acrosomal exocytosis in mammalian sperm. Int Rev Cytol. 1994;149:1–46. [PubMed] [Google Scholar]
  24. Fraser L. R., Umar G., Sayed S. Na(+)-requiring mechanisms modulate capacitation and acrosomal exocytosis in mouse spermatozoa. J Reprod Fertil. 1993 Mar;97(2):539–549. doi: 10.1530/jrf.0.0970539. [DOI] [PubMed] [Google Scholar]
  25. Giannini G., Conti A., Mammarella S., Scrobogna M., Sorrentino V. The ryanodine receptor/calcium channel genes are widely and differentially expressed in murine brain and peripheral tissues. J Cell Biol. 1995 Mar;128(5):893–904. doi: 10.1083/jcb.128.5.893. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Glassner M., Jones J., Kligman I., Woolkalis M. J., Gerton G. L., Kopf G. S. Immunocytochemical and biochemical characterization of guanine nucleotide-binding regulatory proteins in mammalian spermatozoa. Dev Biol. 1991 Aug;146(2):438–450. doi: 10.1016/0012-1606(91)90245-x. [DOI] [PubMed] [Google Scholar]
  27. Gordon M., Dandekar P. V., Eager P. R. Identification of phosphates on the membranes of guinea pig sperm. Anat Rec. 1978 May;191(1):123–133. doi: 10.1002/ar.1091910111. [DOI] [PubMed] [Google Scholar]
  28. Gordon M. Localization of phosphatase activity on the membranes of the mammalian sperm head. J Exp Zool. 1973 Jul;185(1):111–120. doi: 10.1002/jez.1401850111. [DOI] [PubMed] [Google Scholar]
  29. Grinstein S., Rothstein A. Mechanisms of regulation of the Na+/H+ exchanger. J Membr Biol. 1986;90(1):1–12. doi: 10.1007/BF01869680. [DOI] [PubMed] [Google Scholar]
  30. Grinstein S., Rotin D., Mason M. J. Na+/H+ exchange and growth factor-induced cytosolic pH changes. Role in cellular proliferation. Biochim Biophys Acta. 1989 Jan 18;988(1):73–97. doi: 10.1016/0304-4157(89)90004-x. [DOI] [PubMed] [Google Scholar]
  31. Khan A. A., Steiner J. P., Klein M. G., Schneider M. F., Snyder S. H. IP3 receptor: localization to plasma membrane of T cells and cocapping with the T cell receptor. Science. 1992 Aug 7;257(5071):815–818. doi: 10.1126/science.1323146. [DOI] [PubMed] [Google Scholar]
  32. Khan A. A., Steiner J. P., Snyder S. H. Plasma membrane inositol 1,4,5-trisphosphate receptor of lymphocytes: selective enrichment in sialic acid and unique binding specificity. Proc Natl Acad Sci U S A. 1992 Apr 1;89(7):2849–2853. doi: 10.1073/pnas.89.7.2849. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Kinloch R. A., Mortillo S., Stewart C. L., Wassarman P. M. Embryonal carcinoma cells transfected with ZP3 genes differentially glycosylate similar polypeptides and secrete active mouse sperm receptor. J Cell Biol. 1991 Nov;115(3):655–664. doi: 10.1083/jcb.115.3.655. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Lee C. H., Park D., Wu D., Rhee S. G., Simon M. I. Members of the Gq alpha subunit gene family activate phospholipase C beta isozymes. J Biol Chem. 1992 Aug 15;267(23):16044–16047. [PubMed] [Google Scholar]
  35. Lee M. A., Storey B. T. 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 Nov;24(3):303–326. doi: 10.1002/mrd.1120240307. [DOI] [PubMed] [Google Scholar]
  36. Leyton L., LeGuen P., Bunch D., Saling P. M. Regulation of mouse gamete interaction by a sperm tyrosine kinase. Proc Natl Acad Sci U S A. 1992 Dec 15;89(24):11692–11695. doi: 10.1073/pnas.89.24.11692. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Leyton L., Saling P. 95 kd sperm proteins bind ZP3 and serve as tyrosine kinase substrates in response to zona binding. Cell. 1989 Jun 30;57(7):1123–1130. doi: 10.1016/0092-8674(89)90049-4. [DOI] [PubMed] [Google Scholar]
  38. Llopis J., Chow S. B., Kass G. E., Gahm A., Orrenius S. Comparison between the effects of the microsomal Ca(2+)-translocase inhibitors thapsigargin and 2,5-di-(t-butyl)-1,4-benzohydroquinone on cellular calcium fluxes. Biochem J. 1991 Jul 15;277(Pt 2):553–556. doi: 10.1042/bj2770553. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Lytton J., Westlin M., Hanley M. R. Thapsigargin inhibits the sarcoplasmic or endoplasmic reticulum Ca-ATPase family of calcium pumps. J Biol Chem. 1991 Sep 15;266(26):17067–17071. [PubMed] [Google Scholar]
  40. MacGlashan D., Jr, Botana L. M. Biphasic Ca2+ responses in human basophils. Evidence that the initial transient elevation associated with the mobilization of intracellular calcium is an insufficient signal for degranulation. J Immunol. 1993 Feb 1;150(3):980–991. [PubMed] [Google Scholar]
  41. Malviya A. N., Rogue P., Vincendon G. Stereospecific inositol 1,4,5-[32P]trisphosphate binding to isolated rat liver nuclei: evidence for inositol trisphosphate receptor-mediated calcium release from the nucleus. Proc Natl Acad Sci U S A. 1990 Dec;87(23):9270–9274. doi: 10.1073/pnas.87.23.9270. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Manganel M., Turner R. J. Agonist-induced activation of Na+/H+ exchange in rat parotid acinar cells. J Membr Biol. 1989 Oct;111(2):191–198. doi: 10.1007/BF01871782. [DOI] [PubMed] [Google Scholar]
  43. Manganel M., Turner R. J. Rapid secretagogue-induced activation of Na+H+ exchange in rat parotid acinar cells. Possible interrelationship between volume regulation and stimulus-secretion coupling. J Biol Chem. 1991 Jun 5;266(16):10182–10188. [PubMed] [Google Scholar]
  44. Marty A. Calcium release and internal calcium regulation in acinar cells of exocrine glands. J Membr Biol. 1991 Dec;124(3):189–197. doi: 10.1007/BF01994353. [DOI] [PubMed] [Google Scholar]
  45. Meizel S., Turner K. O. Initiation of the human sperm acrosome reaction by thapsigargin. J Exp Zool. 1993 Nov 1;267(3):350–355. doi: 10.1002/jez.1402670312. [DOI] [PubMed] [Google Scholar]
  46. Mendoza C., Tesarik J. A plasma-membrane progesterone receptor in human sperm is switched on by increasing intracellular free calcium. FEBS Lett. 1993 Sep 6;330(1):57–60. doi: 10.1016/0014-5793(93)80919-l. [DOI] [PubMed] [Google Scholar]
  47. Metz D. C., Patto R. J., Mrozinski J. E., Jr, Jensen R. T., Turner R. J., Gardner J. D. Thapsigargin defines the roles of cellular calcium in secretagogue-stimulated enzyme secretion from pancreatic acini. J Biol Chem. 1992 Oct 15;267(29):20620–20629. [PubMed] [Google Scholar]
  48. Miller D. J., Macek M. B., Shur B. D. Complementarity between sperm surface beta-1,4-galactosyltransferase and egg-coat ZP3 mediates sperm-egg binding. Nature. 1992 Jun 18;357(6379):589–593. doi: 10.1038/357589a0. [DOI] [PubMed] [Google Scholar]
  49. Miyazaki S., Yuzaki M., Nakada K., Shirakawa H., Nakanishi S., Nakade S., Mikoshiba K. Block of Ca2+ wave and Ca2+ oscillation by antibody to the inositol 1,4,5-trisphosphate receptor in fertilized hamster eggs. Science. 1992 Jul 10;257(5067):251–255. doi: 10.1126/science.1321497. [DOI] [PubMed] [Google Scholar]
  50. Mourey R. J., Verma A., Supattapone S., Snyder S. H. Purification and characterization of the inositol 1,4,5- trisphosphate receptor protein from rat vas deferens. Biochem J. 1990 Dec 1;272(2):383–389. doi: 10.1042/bj2720383. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Nakamura M., Moriya M., Baba T., Michikawa Y., Yamanobe T., Arai K., Okinaga S., Kobayashi T. An endoplasmic reticulum protein, calreticulin, is transported into the acrosome of rat sperm. Exp Cell Res. 1993 Mar;205(1):101–110. doi: 10.1006/excr.1993.1063. [DOI] [PubMed] [Google Scholar]
  52. Nicaise G., Maggio K., Thirion S., Horoyan M., Keicher E. The calcium loading of secretory granules. A possible key event in stimulus-secretion coupling. Biol Cell. 1992;75(2):89–99. doi: 10.1016/0248-4900(92)90128-n. [DOI] [PubMed] [Google Scholar]
  53. Osman R. A., Andria M. L., Jones A. D., Meizel S. Steroid induced exocytosis: the human sperm acrosome reaction. Biochem Biophys Res Commun. 1989 Apr 28;160(2):828–833. doi: 10.1016/0006-291x(89)92508-4. [DOI] [PubMed] [Google Scholar]
  54. Peng Y. W., Sharp A. H., Snyder S. H., Yau K. W. Localization of the inositol 1,4,5-trisphosphate receptor in synaptic terminals in the vertebrate retina. Neuron. 1991 Apr;6(4):525–531. doi: 10.1016/0896-6273(91)90055-5. [DOI] [PubMed] [Google Scholar]
  55. Purvis K., Cusan L., Attramadal H., Ege A., Hansson V. Rat sperm enzymes during epididymal transit. J Reprod Fertil. 1982 Jul;65(2):381–387. doi: 10.1530/jrf.0.0650381. [DOI] [PubMed] [Google Scholar]
  56. Putney J. W., Jr Capacitative calcium entry revisited. Cell Calcium. 1990 Nov-Dec;11(10):611–624. doi: 10.1016/0143-4160(90)90016-n. [DOI] [PubMed] [Google Scholar]
  57. Roldan E. R., Harrison R. A. Diacylglycerol in the exocytosis of the mammalian sperm acrosome. Biochem Soc Trans. 1993 May;21(2):284–289. doi: 10.1042/bst0210284. [DOI] [PubMed] [Google Scholar]
  58. Roldan E. R., Murase T., Shi Q. X. Exocytosis in spermatozoa in response to progesterone and zona pellucida. Science. 1994 Dec 2;266(5190):1578–1581. doi: 10.1126/science.7985030. [DOI] [PubMed] [Google Scholar]
  59. Saling P. M. How the egg regulates sperm function during gamete interaction: facts and fantasies. Biol Reprod. 1991 Feb;44(2):246–251. doi: 10.1095/biolreprod44.2.246. [DOI] [PubMed] [Google Scholar]
  60. Schilling W. P., Cabello O. A., Rajan L. Depletion of the inositol 1,4,5-trisphosphate-sensitive intracellular Ca2+ store in vascular endothelial cells activates the agonist-sensitive Ca(2+)-influx pathway. Biochem J. 1992 Jun 1;284(Pt 2):521–530. doi: 10.1042/bj2840521. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Sharp A. H., McPherson P. S., Dawson T. M., Aoki C., Campbell K. P., Snyder S. H. Differential immunohistochemical localization of inositol 1,4,5-trisphosphate- and ryanodine-sensitive Ca2+ release channels in rat brain. J Neurosci. 1993 Jul;13(7):3051–3063. doi: 10.1523/JNEUROSCI.13-07-03051.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Storey B. T., Hourani C. L., Kim J. B. A transient rise in intracellular Ca2+ is a precursor reaction to the zona pellucida-induced acrosome reaction in mouse sperm and is blocked by the induced acrosome reaction inhibitor 3-quinuclidinyl benzilate. Mol Reprod Dev. 1992 May;32(1):41–50. doi: 10.1002/mrd.1080320108. [DOI] [PubMed] [Google Scholar]
  63. Sullivan K. M., Busa W. B., Wilson K. L. Calcium mobilization is required for nuclear vesicle fusion in vitro: implications for membrane traffic and IP3 receptor function. Cell. 1993 Jul 2;73(7):1411–1422. doi: 10.1016/0092-8674(93)90366-x. [DOI] [PubMed] [Google Scholar]
  64. Supattapone S., Worley P. F., Baraban J. M., Snyder S. H. Solubilization, purification, and characterization of an inositol trisphosphate receptor. J Biol Chem. 1988 Jan 25;263(3):1530–1534. [PubMed] [Google Scholar]
  65. Tesarik J., Carreras A., Mendoza C. Differential sensitivity of progesterone- and zona pellucida-induced acrosome reactions to pertussis toxin. Mol Reprod Dev. 1993 Feb;34(2):183–189. doi: 10.1002/mrd.1080340210. [DOI] [PubMed] [Google Scholar]
  66. Thastrup O., Cullen P. J., Drøbak B. K., Hanley M. R., Dawson A. P. Thapsigargin, a tumor promoter, discharges intracellular Ca2+ stores by specific inhibition of the endoplasmic reticulum Ca2(+)-ATPase. Proc Natl Acad Sci U S A. 1990 Apr;87(7):2466–2470. doi: 10.1073/pnas.87.7.2466. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Thomas P., Meizel S. Phosphatidylinositol 4,5-bisphosphate hydrolysis in human sperm stimulated with follicular fluid or progesterone is dependent upon Ca2+ influx. Biochem J. 1989 Dec 1;264(2):539–546. doi: 10.1042/bj2640539. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Thorn P. Spatial aspects of Ca2+ signalling in pancreatic acinar cells. J Exp Biol. 1993 Nov;184:129–144. doi: 10.1242/jeb.184.1.129. [DOI] [PubMed] [Google Scholar]
  69. Verma A., Hirsch D. J., Hanley M. R., Thastrup O., Christensen S. B., Snyder S. H. Inositol trisphosphate and thapsigargin discriminate endoplasmic reticulum stores of calcium in rat brain. Biochem Biophys Res Commun. 1990 Oct 30;172(2):811–816. doi: 10.1016/0006-291x(90)90747-b. [DOI] [PubMed] [Google Scholar]
  70. Verma A., Hirsch D. J., Snyder S. H. Calcium pools mobilized by calcium or inositol 1,4,5-trisphosphate are differentially localized in rat heart and brain. Mol Biol Cell. 1992 Jun;3(6):621–631. doi: 10.1091/mbc.3.6.621. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Walensky L. D., Roskams A. J., Lefkowitz R. J., Snyder S. H., Ronnett G. V. Odorant receptors and desensitization proteins colocalize in mammalian sperm. Mol Med. 1995 Jan;1(2):130–141. [PMC free article] [PubMed] [Google Scholar]
  72. Ward C. R., Storey B. T., Kopf G. S. Selective activation of Gi1 and Gi2 in mouse sperm by the zona pellucida, the egg's extracellular matrix. J Biol Chem. 1994 May 6;269(18):13254–13258. [PubMed] [Google Scholar]
  73. 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 Oct;159(2):679–690. doi: 10.1006/dbio.1993.1274. [DOI] [PubMed] [Google Scholar]
  74. Worley P. F., Baraban J. M., Supattapone S., Wilson V. S., Snyder S. H. Characterization of inositol trisphosphate receptor binding in brain. Regulation by pH and calcium. J Biol Chem. 1987 Sep 5;262(25):12132–12136. [PubMed] [Google Scholar]
  75. Xu Z., Kopf G. S., Schultz R. M. Involvement of inositol 1,4,5-trisphosphate-mediated Ca2+ release in early and late events of mouse egg activation. Development. 1994 Jul;120(7):1851–1859. doi: 10.1242/dev.120.7.1851. [DOI] [PubMed] [Google Scholar]
  76. Yanagimachi R., Usui N. Calcium dependence of the acrosome reaction and activation of guinea pig spermatozoa. Exp Cell Res. 1974 Nov;89(1):161–174. doi: 10.1016/0014-4827(74)90199-2. [DOI] [PubMed] [Google Scholar]
  77. Yoo S. H., Albanesi J. P. Inositol 1,4,5-trisphosphate-triggered Ca2+ release from bovine adrenal medullary secretory vesicles. J Biol Chem. 1990 Aug 15;265(23):13446–13448. [PubMed] [Google Scholar]
  78. Zahler W. L., Doak G. A. Isolation of the outer acrosomal membrane from bull sperm. Biochim Biophys Acta. 1975 Nov 3;406(4):479–488. doi: 10.1016/0005-2736(75)90026-7. [DOI] [PubMed] [Google Scholar]
  79. von Tscharner V., Prod'hom B., Baggiolini M., Reuter H. Ion channels in human neutrophils activated by a rise in free cytosolic calcium concentration. 1986 Nov 27-Dec 3Nature. 324(6095):369–372. doi: 10.1038/324369a0. [DOI] [PubMed] [Google Scholar]

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