Skip to main content
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1984 Nov 1;99(5):1634–1641. doi: 10.1083/jcb.99.5.1634

Localized surface antigens of guinea pig sperm migrate to new regions prior to fertilization

PMCID: PMC2113358  PMID: 6436252

Abstract

We have previously defined distinct localizations of antigens on the surface of the guinea pig sperm using monoclonal antibodies. In the present study we have demonstrated that these antigen localizations are dynamic and can be altered during changes in the functional state of the sperm. Before the sperm is capable of fertilizing the egg, it must undergo capacitation and an exocytic event, the acrosome reaction. Prior to capacitation, the antigen recognized by the monoclonal antibody, PT-1, was restricted to the posterior tail region (principle piece and end piece). After incubation in capacitating media at 37 degrees C for 1 h, 100% of the sperm population showed migration of the PT-1 antigen onto the anterior tail. This redistribution of surface antigen resulted from a migration of the surface molecules originally present on the posterior tail. It did not occur in the presence of metabolic poisons or when tail-beating was prevented. It was temperature-dependent, and did not require exogenous Ca2+. Since the PT- 1 antigen is freely diffusing on the posterior tail before migration, the mechanism of redistribution could involve the alteration of a presumptive membrane barrier. In addition, we observed the redistribution of a second surface antigen after the acrosome reaction. The antigen recognized by the monoclonal antibody, PH-20, was localized exclusively in the posterior head region of acrosome-intact sperm. Within 7-10 min of induction of the acrosome reaction with Ca2+ and A23187, 90-100% of the acrosome-reacted sperm population no longer demonstrated binding of the PH-20 antibody on the posterior head, but showed binding instead on the inner acrosomal membrane. This redistribution of the PH-20 antigen also resulted from the migration of pre-existing surface molecules, but did not appear to require energy. The migration of PH-20 antigen was a selective process; other antigens localized to the posterior head region did not leave the posterior head after the acrosome reaction. These rearrangements of cell surface molecules may act to regulate cell surface function during fertilization.

Full Text

The Full Text of this article is available as a PDF (912.3 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Anderson R. G., Brown M. S., Beisiegel U., Goldstein J. L. Surface distribution and recycling of the low density lipoprotein receptor as visualized with antireceptor antibodies. J Cell Biol. 1982 Jun;93(3):523–531. doi: 10.1083/jcb.93.3.523. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bouchard P., Penningroth S. M., Cheung A., Gagnon C., Bardin C. W. erythro-9-[3-(2-Hydroxynonyl)]adenine is an inhibitor of sperm motility that blocks dynein ATPase and protein carboxylmethylase activities. Proc Natl Acad Sci U S A. 1981 Feb;78(2):1033–1036. doi: 10.1073/pnas.78.2.1033. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Chow I., Poo M. M. Redistribution of cell surface receptors induced by cell-cell contact. J Cell Biol. 1982 Nov;95(2 Pt 1):510–518. doi: 10.1083/jcb.95.2.510. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Dragsten P. R., Blumenthal R., Handler J. S. Membrane asymmetry in epithelia: is the tight junction a barrier to diffusion in the plasma membrane? Nature. 1981 Dec 24;294(5843):718–722. doi: 10.1038/294718a0. [DOI] [PubMed] [Google Scholar]
  5. Fraser S. E., Poo M. Development, maintenance, and modulation of patterned membrane topography: models based on the acetylcholine receptor. Curr Top Dev Biol. 1982;17(Pt 3):77–100. doi: 10.1016/s0070-2153(08)60519-0. [DOI] [PubMed] [Google Scholar]
  6. Friend D. S., Orci L., Perrelet A., Yanagimachi R. Membrane particle changes attending the acrosome reaction in guinea pig spermatozoa. J Cell Biol. 1977 Aug;74(2):561–577. doi: 10.1083/jcb.74.2.561. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Friend D. S. Plasma-membrane diversity in a highly polarized cell. J Cell Biol. 1982 May;93(2):243–249. doi: 10.1083/jcb.93.2.243. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Friend D. S., Rudolf I. Acrosomal disruption in sperm. Freeze-fracture of altered membranes. J Cell Biol. 1974 Nov;63(2 Pt 1):466–479. doi: 10.1083/jcb.63.2.466. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Fujita M., Ota H., Kawai K., Matsui H., Nakao M. Differential isolation of microvillous and basolateral plasma membranes from intestinal mucosa: mutually exclusive distribution of digestive enzymes and ouabain-sensitive ATPase. Biochim Biophys Acta. 1972 Aug 9;274(2):336–347. doi: 10.1016/0005-2736(72)90181-2. [DOI] [PubMed] [Google Scholar]
  10. Geiduschek J. B., Singer S. J. Molecular changes in the membranes of mouse erythroid cells accompanying differentiation. Cell. 1979 Jan;16(1):149–163. doi: 10.1016/0092-8674(79)90196-x. [DOI] [PubMed] [Google Scholar]
  11. Green D. P. The induction of the acrosome reaction in guinea-pig sperm by the divalent metal cation ionophore A23187. J Cell Sci. 1978 Aug;32:137–151. doi: 10.1242/jcs.32.1.137. [DOI] [PubMed] [Google Scholar]
  12. Hyne R. V., Garbers D. L. Calcium-dependent increase in adenosine 3',5'-monophosphate and induction of the acrosome reaction in guinea pig spermatozoa. Proc Natl Acad Sci U S A. 1979 Nov;76(11):5699–5703. doi: 10.1073/pnas.76.11.5699. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Koehler J. K., Gaddum-Rosse P. Media induced alterations of the membrane associated particles of the guinea pig sperm tail. J Ultrastruct Res. 1975 Apr;51(1):106–118. doi: 10.1016/s0022-5320(75)80012-8. [DOI] [PubMed] [Google Scholar]
  14. Koehler J. K. The mammalian sperm surface: studies with specific labeling techniques. Int Rev Cytol. 1978;54:73–108. doi: 10.1016/s0074-7696(08)60165-5. [DOI] [PubMed] [Google Scholar]
  15. Koppel D. E., Oliver J. M., Berlin R. D. Surface functions during mitosis. III. Quantitative analysis of ligand-receptor movement into the cleavage furrow: diffusion vs. flow. J Cell Biol. 1982 Jun;93(3):950–960. doi: 10.1083/jcb.93.3.950. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. McCaig C. D., Robinson K. R. The distribution of lectin receptors on the plasma membrane of the fertilized sea urchin egg during first and second cleavage. Dev Biol. 1982 Jul;92(1):197–202. doi: 10.1016/0012-1606(82)90163-4. [DOI] [PubMed] [Google Scholar]
  17. Myles D. G., Primakoff P., Bellvé A. R. Surface domains of the guinea pig sperm defined with monoclonal antibodies. Cell. 1981 Feb;23(2):433–439. doi: 10.1016/0092-8674(81)90138-0. [DOI] [PubMed] [Google Scholar]
  18. Myles D. G., Primakoff P., Koppel D. E. A localized surface protein of guinea pig sperm exhibits free diffusion in its domain. J Cell Biol. 1984 May;98(5):1905–1909. doi: 10.1083/jcb.98.5.1905. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Oliver J. M., Berlin R. D. Mechanisms that regulate the structural and functional architecture of cell surfaces. Int Rev Cytol. 1982;74:55–94. doi: 10.1016/s0074-7696(08)61169-9. [DOI] [PubMed] [Google Scholar]
  20. Pastan I. H., Willingham M. C. Journey to the center of the cell: role of the receptosome. Science. 1981 Oct 30;214(4520):504–509. doi: 10.1126/science.6170111. [DOI] [PubMed] [Google Scholar]
  21. Penningroth S. M., Cheung A., Bouchard P., Gagnon C., Bardin C. W. Dynein ATPase is inhibited selectively in vitro by erythro-9-[3-2-(hydroxynonyl)]adenine. Biochem Biophys Res Commun. 1982 Jan 15;104(1):234–240. doi: 10.1016/0006-291x(82)91964-7. [DOI] [PubMed] [Google Scholar]
  22. Primakoff P., Myles D. G. A map of the guinea pig sperm surface constructed with monoclonal antibodies. Dev Biol. 1983 Aug;98(2):417–428. doi: 10.1016/0012-1606(83)90371-8. [DOI] [PubMed] [Google Scholar]
  23. Rogalski A. A., Bouck G. B. Flagellar surface antigens in Euglena: immunological evidence for an external glycoprotein pool and its transfer to the regenerating flagellum. J Cell Biol. 1982 Jun;93(3):758–766. doi: 10.1083/jcb.93.3.758. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Rogers B. J., Ueno M., Yanagimachi R. Fertilization by guinea pig spermatozoa requires potassium ions. Biol Reprod. 1981 Oct;25(3):639–648. doi: 10.1095/biolreprod25.3.639. [DOI] [PubMed] [Google Scholar]
  25. Springer T. A. Quantitation of hybridoma immunoglobulins and selection of light-chain loss variants. Methods Enzymol. 1983;92:147–160. doi: 10.1016/0076-6879(83)92014-1. [DOI] [PubMed] [Google Scholar]
  26. Stya M., Axelrod D. Diffusely distributed acetylcholine receptors can participate in cluster formation on cultured rat myotubes. Proc Natl Acad Sci U S A. 1983 Jan;80(2):449–453. doi: 10.1073/pnas.80.2.449. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Talbot P., Franklin L. E. Surface modification of guinea pig sperm during in vitro capacitation: an assessment using lectin-induced agglutination of living sperm. J Exp Zool. 1978 Jan;203(1):1–14. doi: 10.1002/jez.1402030102. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES