Abstract
Hydrolysis of the phospholipid phosphatidylinositol 4,5-bisphosphate is thought to be intimately involved in agonist-induced changes in intracellular Ca2+ levels. Recently we have shown that human preovulatory follicular fluid, which induces exocytosis in human sperm, can stimulate a rapid, transient increase in sperm cytosolic [Ca2+] [Thomas & Meizel (1988) Gamete Res. 20, 397-411]. We report here that both a Sephadex G-75 column fraction, derived from follicular fluid, and progesterone (a component of both the G-75 fraction and whole follicular fluid) stimulate rapid hydrolysis of PtdIns(4,5)P2 and PtdIns4P in human sperm. We also report that progesterone stimulates a rapid influx of Ca2+ in human sperm. Human spermatozoa were labelled for 24 h with myo-[3H]inositol and then treated with either the G-75 fraction or progesterone. A 30-65% loss of label was detected in PtdIns(4,5)P2 and PtdIns4P within 15 s of stimulus addition; no changes were observed in PtdIns during 2 min of treatment. The loss of label from both lipids was accompanied by an increase in water-soluble inositol phosphates. Production of both InsP3 and InsP2 was seen within 10 s; however, InsP3 was rapidly removed and had reached control levels by 1 min. Similarly, formation of InsP2 reached a peak by 30 s and then began a decline accompanied by a corresponding increase in InsP. No increases in InsP4 were seen in sperm treated in this fashion. Stimulated hydrolysis of the phosphoinositides and release of inositol phosphates were both blocked by the Ca2+ antagonist La3+. Likewise, the progesterone-induced increase in intracellular Ca2+ was inhibited by La3+, and phosphoinositide hydrolysis stimulated by this hormone was dependent upon the presence of extracellular Ca2+.
Full text
PDF







Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Bennet P. J., Moatti J. P., Mansat A., Ribbes H., Cayrac J. C., Pontonnier F., Chap H., Douste-Blazy L. Evidence for the activation of phospholipases during acrosome reaction of human sperm elicited by calcium ionophore A23187. Biochim Biophys Acta. 1987 Jun 23;919(3):255–265. doi: 10.1016/0005-2760(87)90265-7. [DOI] [PubMed] [Google Scholar]
- Berridge M. J., Downes C. P., Hanley M. R. Lithium amplifies agonist-dependent phosphatidylinositol responses in brain and salivary glands. Biochem J. 1982 Sep 15;206(3):587–595. doi: 10.1042/bj2060587. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Berruti G., Franchi E. Calcium and polyphosphoinositides: their distribution in relation to the membrane changes occurring in the head of boar spermatozoa. Eur J Cell Biol. 1986 Aug;41(2):238–245. [PubMed] [Google Scholar]
- Cicirelli M. F., Smith L. D. Do calcium and calmodulin trigger maturation in amphibian oocytes? Dev Biol. 1987 May;121(1):48–57. doi: 10.1016/0012-1606(87)90137-0. [DOI] [PubMed] [Google Scholar]
- Crossley I., Swann K., Chambers E., Whitaker M. Activation of sea urchin eggs by inositol phosphates is independent of external calcium. Biochem J. 1988 May 15;252(1):257–262. doi: 10.1042/bj2520257. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Deliconstantinos G. Structure activity relationship of cholesterol and steroid hormones with respect to their effects on the Ca2+-stimulated ATPase and lipid fluidity of synaptosomal plasma membranes from dog and rabbit brain. Comp Biochem Physiol B. 1988;89(3):585–594. doi: 10.1016/0305-0491(88)90178-2. [DOI] [PubMed] [Google Scholar]
- 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]
- Duval D., Durant S., Homo-Delarche F. Non-genomic effects of steroids. Interactions of steroid molecules with membrane structures and functions. Biochim Biophys Acta. 1983 Aug 11;737(3-4):409–442. doi: 10.1016/0304-4157(83)90008-4. [DOI] [PubMed] [Google Scholar]
- Eberhard D. A., Holz R. W. Intracellular Ca2+ activates phospholipase C. Trends Neurosci. 1988 Dec;11(12):517–520. doi: 10.1016/0166-2236(88)90174-9. [DOI] [PubMed] [Google Scholar]
- Fewtrell C. M., Gomperts B. D. Quercetin: a novel inhibitor of Ca2+ influx and exocytosis in rat peritoneal mast cells. Biochim Biophys Acta. 1977 Aug 15;469(1):52–60. doi: 10.1016/0005-2736(77)90325-x. [DOI] [PubMed] [Google Scholar]
- Fraser L. R., McIntyre K. Calcium channel antagonists modulate the acrosome reaction but not capacitation in mouse spermatozoa. J Reprod Fertil. 1989 May;86(1):223–233. doi: 10.1530/jrf.0.0860223. [DOI] [PubMed] [Google Scholar]
- Irvine R. F., Anggård E. E., Letcher A. J., Downes C. P. Metabolism of inositol 1,4,5-trisphosphate and inositol 1,3,4-trisphosphate in rat parotid glands. Biochem J. 1985 Jul 15;229(2):505–511. doi: 10.1042/bj2290505. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Irvine R. F., Moor R. M. Micro-injection of inositol 1,3,4,5-tetrakisphosphate activates sea urchin eggs by a mechanism dependent on external Ca2+. Biochem J. 1986 Dec 15;240(3):917–920. doi: 10.1042/bj2400917. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kuno M., Gardner P. Ion channels activated by inositol 1,4,5-trisphosphate in plasma membrane of human T-lymphocytes. Nature. 1987 Mar 19;326(6110):301–304. doi: 10.1038/326301a0. [DOI] [PubMed] [Google Scholar]
- Meizel S. Molecules that initiate or help stimulate the acrosome reaction by their interaction with the mammalian sperm surface. Am J Anat. 1985 Nov;174(3):285–302. doi: 10.1002/aja.1001740309. [DOI] [PubMed] [Google Scholar]
- Meldolesi J., Pozzan T. Pathways of Ca2+ influx at the plasma membrane: voltage-, receptor-, and second messenger-operated channels. Exp Cell Res. 1987 Aug;171(2):271–283. doi: 10.1016/0014-4827(87)90161-3. [DOI] [PubMed] [Google Scholar]
- Moreau M., Vilain J. P., Guerrier P. Free calcium changes associated with hormone action in amphibian oocytes. Dev Biol. 1980 Jul;78(1):201–214. doi: 10.1016/0012-1606(80)90329-2. [DOI] [PubMed] [Google Scholar]
- Morris A. P., Gallacher D. V., Irvine R. F., Petersen O. H. Synergism of inositol trisphosphate and tetrakisphosphate in activating Ca2+-dependent K+ channels. Nature. 1987 Dec 17;330(6149):653–655. doi: 10.1038/330653a0. [DOI] [PubMed] [Google Scholar]
- Nikolopoulou M., Soucek D. A., Vary J. C. Modulation of the lipid composition of boar sperm plasma membranes during an acrosome reaction in vitro. Arch Biochem Biophys. 1986 Oct;250(1):30–37. doi: 10.1016/0003-9861(86)90698-3. [DOI] [PubMed] [Google Scholar]
- Nishizuka Y. The role of protein kinase C in cell surface signal transduction and tumour promotion. Nature. 1984 Apr 19;308(5961):693–698. doi: 10.1038/308693a0. [DOI] [PubMed] [Google Scholar]
- 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]
- Penner R., Matthews G., Neher E. Regulation of calcium influx by second messengers in rat mast cells. Nature. 1988 Aug 11;334(6182):499–504. doi: 10.1038/334499a0. [DOI] [PubMed] [Google Scholar]
- Pollock W. K., Rink T. J., Irvine R. F. Liberation of [3H]arachidonic acid and changes in cytosolic free calcium in fura-2-loaded human platelets stimulated by ionomycin and collagen. Biochem J. 1986 May 1;235(3):869–877. doi: 10.1042/bj2350869. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rhodes D., Prpić V., Exton J. H., Blackmore P. F. Stimulation of phosphatidylinositol 4,5-bisphosphate hydrolysis in hepatocytes by vasopressin. J Biol Chem. 1983 Mar 10;258(5):2770–2773. [PubMed] [Google Scholar]
- Ribbes H., Plantavid M., Bennet P. J., Chap H., Douste-Blazy L. Phospholipase C from human sperm specific for phosphoinositides. Biochim Biophys Acta. 1987 Jun 23;919(3):245–254. doi: 10.1016/0005-2760(87)90264-5. [DOI] [PubMed] [Google Scholar]
- Rink T. J. Membrane potential of guinea-pig spermatozoa. J Reprod Fertil. 1977 Sep;51(1):155–157. doi: 10.1530/jrf.0.0510155. [DOI] [PubMed] [Google Scholar]
- Roldan E. R., Fleming A. D. Is a Ca2+ -ATPase involved in Ca2+ regulation during capacitation and the acrosome reaction of guinea-pig spermatozoa? J Reprod Fertil. 1989 Jan;85(1):297–308. doi: 10.1530/jrf.0.0850297. [DOI] [PubMed] [Google Scholar]
- Roldan E. R., Harrison R. A. Absence of active protein kinase C in ram spermatozoa. Biochem Biophys Res Commun. 1988 Sep 15;155(2):901–906. doi: 10.1016/s0006-291x(88)80581-3. [DOI] [PubMed] [Google Scholar]
- Roldan E. R., Harrison R. A. Polyphosphoinositide breakdown and subsequent exocytosis in the Ca2+/ionophore-induced acrosome reaction of mammalian spermatozoa. Biochem J. 1989 Apr 15;259(2):397–406. doi: 10.1042/bj2590397. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schackmann R. W., Christen R., Shapiro B. M. Membrane potential depolarization and increased intracellular pH accompany the acrosome reaction of sea urchin sperm. Proc Natl Acad Sci U S A. 1981 Oct;78(10):6066–6070. doi: 10.1073/pnas.78.10.6066. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schackmann R. W., Eddy E. M., Shapiro B. M. The acrosome reaction of Strongylocentrotus purpuratus sperm. Ion requirements and movements. Dev Biol. 1978 Aug;65(2):483–495. doi: 10.1016/0012-1606(78)90043-x. [DOI] [PubMed] [Google Scholar]
- SeGall G. K., Lennarz W. J. Chemical characterization of the component of the jelly coat from sea urchin eggs responsible for induction of the acrosome reaction. Dev Biol. 1979 Jul;71(1):33–48. doi: 10.1016/0012-1606(79)90080-0. [DOI] [PubMed] [Google Scholar]
- Shaikh N. A., Palmer F. B. Phosphoinositide kinases in chick brain and sciatic nerve, a developmental study. J Neurochem. 1977 Feb;28(2):395–402. doi: 10.1111/j.1471-4159.1977.tb07760.x. [DOI] [PubMed] [Google Scholar]
- Shapiro B. M. Molecular aspects of sperm-egg fusion. Ciba Found Symp. 1984;103:86–99. doi: 10.1002/9780470720844.ch6. [DOI] [PubMed] [Google Scholar]
- Siiteri J. E., Dandekar P., Meizel S. Human sperm acrosome reaction-initiating activity associated with the human cumulus oophorus and mural granulosa cells. J Exp Zool. 1988 Apr;246(1):71–80. doi: 10.1002/jez.1402460110. [DOI] [PubMed] [Google Scholar]
- Siiteri J. E., Gottlieb W., Meizel S. Partial characterization of a fraction from human follicular fluid that initiates the human sperm acrosome reaction in vitro. Gamete Res. 1988 May;20(1):25–42. doi: 10.1002/mrd.1120200104. [DOI] [PubMed] [Google Scholar]
- Singh J. P., Babcock D. F., Lardy H. A. Induction of accelerated acrosome reaction in guinea pig sperm. Biol Reprod. 1980 Apr;22(3):566–570. doi: 10.1093/biolreprod/22.3.566. [DOI] [PubMed] [Google Scholar]
- Singh J. P., Babcock D. F., Lardy H. A. Motility activation, respiratory stimulation, and alteration of Ca2+ transport in bovine sperm treated with amine local anesthetics and calcium transport antagonists. Arch Biochem Biophys. 1983 Feb 15;221(1):291–303. doi: 10.1016/0003-9861(83)90146-7. [DOI] [PubMed] [Google Scholar]
- Snyder P. M., Krause K. H., Welsh M. J. Inositol trisphosphate isomers, but not inositol 1,3,4,5-tetrakisphosphate, induce calcium influx in Xenopus laevis oocytes. J Biol Chem. 1988 Aug 15;263(23):11048–11051. [PubMed] [Google Scholar]
- Tesarík J. Comparison of acrosome reaction-inducing activities of human cumulus oophorus, follicular fluid and ionophore A23187 in human sperm populations of proven fertilizing ability in vitro. J Reprod Fertil. 1985 Jul;74(2):383–388. doi: 10.1530/jrf.0.0740383. [DOI] [PubMed] [Google Scholar]
- Thomas P., Meizel S. An influx of extracellular calcium is required for initiation of the human sperm acrosome reaction induced by human follicular fluid. Gamete Res. 1988 Aug;20(4):397–411. doi: 10.1002/mrd.1120200402. [DOI] [PubMed] [Google Scholar]
- Tsien R. W., Lipscombe D., Madison D. V., Bley K. R., Fox A. P. Multiple types of neuronal calcium channels and their selective modulation. Trends Neurosci. 1988 Oct;11(10):431–438. doi: 10.1016/0166-2236(88)90194-4. [DOI] [PubMed] [Google Scholar]
- Wasserman W. J., Pinto L. H., O'Connor C. M., Smith L. D. Progesterone induces a rapid increase in [Ca2+]in of Xenopus laevis oocytes. Proc Natl Acad Sci U S A. 1980 Mar;77(3):1534–1536. doi: 10.1073/pnas.77.3.1534. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Watson S. P., McConnell R. T., Lapetina E. G. The rapid formation of inositol phosphates in human platelets by thrombin is inhibited by prostacyclin. J Biol Chem. 1984 Nov 10;259(21):13199–13203. [PubMed] [Google Scholar]
- Wreggett K. A., Irvine R. F. A rapid separation method for inositol phosphates and their isomers. Biochem J. 1987 Aug 1;245(3):655–660. doi: 10.1042/bj2450655. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yamamoto K. R., Alberts B. M. Steroid receptors: elements for modulation of eukaryotic transcription. Annu Rev Biochem. 1976;45:721–746. doi: 10.1146/annurev.bi.45.070176.003445. [DOI] [PubMed] [Google Scholar]
- 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]
