Abstract
Evidence has been presented that the PH-20 protein functions in sperm adhesion to the egg zona pellucida (Primakoff, P., H. Hyatt, and D. G. Myles, 1985, J. Cell Biol., 101:2239-2244). The PH-20 protein migrates from its original surface domain to a new surface domain after the acrosome reaction (Myles, D. G., and P. Primakoff, 1984, J. Cell Biol., 99:1634-1641). The acrosome reaction is an exocytotic event that results in insertion of a region of the secretory granule membrane, the inner acrosomal membrane (IAM), into the plasma membrane. After the acrosome reaction, PH-20 protein migrates to the IAM from its initial domain on the posterior head surface. We have now found a new dynamic feature of the regulation of PH-20 protein on the sperm surface; exocytosis increases the surface expression of PH-20 protein. After the acrosome reaction there is an approximately threefold increase in the number of PH-20 antigenic sites on the sperm surface. These new antigenic sites are revealed on the surface by insertion of the IAM into the plasma membrane. Our evidence indicates that before the acrosome reaction an intracellular population of PH-20 antigen is localized to the IAM. When migration of the surface population of the PH-20 protein is prevented, PH-20 protein can still be detected on the IAM of acrosome-reacted sperm. Also, PH-20 protein can be detected on the IAM of permeabilized acrosome-intact sperm by indirect immunofluorescence. Thus, the sperm cell regulates the amount of PH-20 protein on its surface by sequestering about two-thirds of the protein on an intracellular membrane and subsequently exposing this population on the cell surface by an exocytotic event. This may be a general mechanism for regulating cell surface composition where a rapid increase in the amount of a cell surface protein is required.
Full Text
The Full Text of this article is available as a PDF (2.0 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Andersson B., Anderson J. M. Lateral heterogeneity in the distribution of chlorophyll-protein complexes of the thylakoid membranes of spinach chloroplasts. Biochim Biophys Acta. 1980 Dec 3;593(2):427–440. doi: 10.1016/0005-2728(80)90078-x. [DOI] [PubMed] [Google Scholar]
- BURGOS M. H., FAWCETT D. W. Studies on the fine structure of the mammalian testis. I. Differentiation of the spermatids in the cat (Felis domestica). J Biophys Biochem Cytol. 1955 Jul 25;1(4):287–300. doi: 10.1083/jcb.1.4.287. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Borregaard N., Heiple J. M., Simons E. R., Clark R. A. Subcellular localization of the b-cytochrome component of the human neutrophil microbicidal oxidase: translocation during activation. J Cell Biol. 1983 Jul;97(1):52–61. doi: 10.1083/jcb.97.1.52. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brown W. R., Barclay A. N., Sunderland C. A., Williams A. F. Identification of a glycophorin-like molecule at the cell surface of rat thymocytes. Nature. 1981 Feb 5;289(5797):456–460. doi: 10.1038/289456a0. [DOI] [PubMed] [Google Scholar]
- Dudkiewicz A. B., Srivastava P. N., Yang C. H., Williams W. L. Extraction of human and rabbit acrosomes: a comparison of sequential and sonication methods. Andrologia. 1979 Sep-Oct;11(5):355–366. doi: 10.1111/j.1439-0272.1979.tb02218.x. [DOI] [PubMed] [Google Scholar]
- Fearon D. T., Collins L. A. Increased expression of C3b receptors on polymorphonuclear leukocytes induced by chemotactic factors and by purification procedures. J Immunol. 1983 Jan;130(1):370–375. [PubMed] [Google Scholar]
- Fletcher M. P., Gallin J. I. Degranulating stimuli increase the availability of receptors on human neutrophils for the chemoattractant f-met-leu-phe. J Immunol. 1980 Apr;124(4):1585–1588. [PubMed] [Google Scholar]
- Fletcher M. P., Gallin J. I. Human neutrophils contain an intracellular pool of putative receptors for the chemoattractant N-formyl-methionyl-leucyl-phenylalanine. Blood. 1983 Oct;62(4):792–799. [PubMed] [Google Scholar]
- Fletcher M. P., Seligmann B. E., Gallin J. I. Correlation of human neutrophil secretion, chemoattractant receptor mobilization, and enhanced functional capacity. J Immunol. 1982 Feb;128(2):941–948. [PubMed] [Google Scholar]
- Garoff H. Using recombinant DNA techniques to study protein targeting in the eucaryotic cell. Annu Rev Cell Biol. 1985;1:403–445. doi: 10.1146/annurev.cb.01.110185.002155. [DOI] [PubMed] [Google Scholar]
- 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]
- Holt W. V. Membrane heterogeneity in the mammalian spermatozoon. Int Rev Cytol. 1984;87:159–194. doi: 10.1016/s0074-7696(08)62442-0. [DOI] [PubMed] [Google Scholar]
- Mason D. W., Williams A. F. The kinetics of antibody binding to membrane antigens in solution and at the cell surface. Biochem J. 1980 Apr 1;187(1):1–20. doi: 10.1042/bj1870001. [DOI] [PMC free article] [PubMed] [Google Scholar]
- McRorie R. A., Williams W. L. Biochemistry of mammalian fertilization. Annu Rev Biochem. 1974;43(0):777–803. doi: 10.1146/annurev.bi.43.070174.004021. [DOI] [PubMed] [Google Scholar]
- 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]
- Myles D. G., Primakoff P. Localized surface antigens of guinea pig sperm migrate to new regions prior to fertilization. J Cell Biol. 1984 Nov;99(5):1634–1641. doi: 10.1083/jcb.99.5.1634. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Olson G. E., Winfrey V. P. Structure of membrane domains and matrix components of the bovine acrosome. J Ultrastruct Res. 1985 Jan;90(1):9–25. doi: 10.1016/0889-1605(85)90113-2. [DOI] [PubMed] [Google Scholar]
- Parham P. On the fragmentation of monoclonal IgG1, IgG2a, and IgG2b from BALB/c mice. J Immunol. 1983 Dec;131(6):2895–2902. [PubMed] [Google Scholar]
- Primakoff P., Hyatt H., Myles D. G. A role for the migrating sperm surface antigen PH-20 in guinea pig sperm binding to the egg zona pellucida. J Cell Biol. 1985 Dec;101(6):2239–2244. doi: 10.1083/jcb.101.6.2239. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Primakoff P., Myles D. G., Bellvé A. R. Biochemical analysis of the released products of the mammalian acrosome reaction. Dev Biol. 1980 Dec;80(2):324–331. doi: 10.1016/0012-1606(80)90408-x. [DOI] [PubMed] [Google Scholar]
- Sabatini D. D., Kreibich G., Morimoto T., Adesnik M. Mechanisms for the incorporation of proteins in membranes and organelles. J Cell Biol. 1982 Jan;92(1):1–22. doi: 10.1083/jcb.92.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Staehelin L. A. Reversible particle movements associated with unstacking and restacking of chloroplast membranes in vitro. J Cell Biol. 1976 Oct;71(1):136–158. doi: 10.1083/jcb.71.1.136. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wooding F. B. The effect of Triton X-100 on the ultrastructure of ejaculated bovine sperm. J Ultrastruct Res. 1973 Mar;42(5):502–516. doi: 10.1016/s0022-5320(73)80023-1. [DOI] [PubMed] [Google Scholar]
