Hostname: page-component-76fb5796d-45l2p Total loading time: 0 Render date: 2024-04-27T13:16:48.769Z Has data issue: false hasContentIssue false
  • English
  • Français

Molecular structure and function of CD4 on murine egg plasma membrane

Published online by Cambridge University Press:  26 September 2008

Mao Wu Guo ,
Toshiki Watanabe ,
Etsuko Mori  and
Tsuneatsu Mori
Mao Wu Guo
Affiliation:
Department of Immunology and Pathology, Institute of Medical Science, University of Tokyo, Tokyo, Japan.
Toshiki Watanabe
Affiliation:
Department of Immunology and Pathology, Institute of Medical Science, University of Tokyo, Tokyo, Japan.
Etsuko Mori
Affiliation:
Department of Immunology and Pathology, Institute of Medical Science, University of Tokyo, Tokyo, Japan.
Tsuneatsu Mori*
Affiliation:
Department of Immunology and Pathology, Institute of Medical Science, University of Tokyo, Tokyo, Japan.
*
T.Mori, Department of Immunology, Institute of Medical science, University of Tokyo, 4-6-1, Shirokanedai Minatoku, Tokyo 108, Japan. Telephone: +81-3-5449-5261. Fax: +8-3-3443-3893.
Get access Rights & Permissions [Opens in a new window]

Summary

In the present study, the expression of the CD4 molecule on murine egg plasma membrane was confirmed by the indirect immunofluorescence (IIF) method. The full-length CD4 cDNA from murine eggs was synthesised by the reverse transcriptase-polymerase chain reaction (RT-PCR) method and its authenticity verified by Southern blot hybridisation using an end-labelled internal oligonucleotide. The results of DNA sequencing showed that the nucleotide sequence of the cDNA of CD4 from murine egg mRNA was identical to that of immune T cells. To demonstrate the direct interaction of CD4 from murine egg with murine sperm cells bearing MHC (major histocompatibility complex) class II molecule, we employed a baculovirus expression system to generate CD4 on the surface of Spodoptera frugiperda (Sf9) cells. Expression of CD4 on Sf9 cells infected with autographa californica nuclear polyhedrosis virus (AcNPV)-CD4 was demonstrated by IIF and immunoblotting. The CD4-expressing Sf9 cells adhered to MHC class II-bearing sperm cells since the adhension was specifically blocked by anti-CD4 monoclonal antibody (mAb) or anti-monomorphic region of MHC class II mAb. Taking our previous and present experimental results together, they strongly suggest that intercellular membrane adhesion between two gametes at the fusion step in fertilisation is mediated by the MHC class II molecule located on the posterior region of the sperm head and the CD4 molecule on egg plasma membrane.

Keywords

CD4EggMHC class IISf9Sperm
Type
Article
Information
Zygote , Volume 3 , Issue 1 , February 1995 , pp. 65 - 73
Copyright
Copyright © Cambridge University Press 1995

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

1Department of Immunology, Institute of Medical Science, University of Tokyo, Tokyo, Japan.
1Department of Pathology, Institute of Medical science, University of Tokyo, Tokyo, Japan.

References

Barros, C., & Franklin, L.E.. (1968). Behavior of the gamete membranes during sperm entry into the mammalian egg. J. Cell Biol. 37, C13.CrossRefGoogle ScholarPubMed
Benacerraf, B.. (1981). Role of MHC gene products in immune regulation. Science 212, 1229–38.CrossRefGoogle ScholarPubMed
Bhattacharya, A., Dorf, M.E., & Springer, T.A.. (1981). A shared alloantigenic determinant on Ia antigens encoded by the I-A and I-E subregions: evidence for I region gene duplication. J. Immunol. 127, 2488–95.CrossRefGoogle Scholar
Bishara, A., Okesenberg, J.R., Frankel, G., Margalioth, E.I., Persitz, E., Nelken, D., Friedmann, A., & Brautbar, C.. (1987). Human leukocyte antigens (HLA) class I and class II on sperm cells studied at the serological, cellular, and genomic levels. Am. J. Reprod. Immunol. Microbiol. 13, 97–103.CrossRefGoogle Scholar
Blobel, C.P., Wolfsberg, T.G., Turck, C.W., Myles, D.G., Primakoff, P., & White, J.M.. (1992). A potential fusion peptide and an integrin ligand domain in a protein active in sperm-egg fusion [see comments]. Nature 356, 248–52.CrossRefGoogle Scholar
Bronson, R.A., & Fusi, F.. (1990a). Evidence that an Arg-Gly-Asp adhesion sequence plays a role in mammalian fertilization. Biol. Reprod. 43, 1019–25.CrossRefGoogle Scholar
Bronson, R.A., & Fusi, F.. (1990b). Sperm–oolemmal interaction: role of the Arg-Gly-Asp (RGD) adhesion peptide. Fertil. Steril. 54, 527–9.CrossRefGoogle ScholarPubMed
Burnet, F.M.. (1971). ‘Self-recognition’ in colonial marine forms and flowering plants in relation to the evolution of immunity. Nature 232, 230–5.CrossRefGoogle Scholar
Cammarota, G., Scheirle, A., Takacs, B., Doran, D.M., Bannwarth, W., Guardiola, J., & Singaglia, F.. (1992). Identification of a CD4 binding site on the β2 domain of HLA-DR molecules. Nature 356, 799–801.CrossRefGoogle Scholar
Clayton, L.K., Sieh, M., Pious, D.A., & Reinherz, E.L.. (1989). Identification of human CD4 residues affecting class II MHC versus HIV-1 gp120 binding. Nature 339, 548–51.CrossRefGoogle ScholarPubMed
Dalgleish, A.G., Beverley, P.C., Clapham, P.R., Crawford, D.H., Greaves, M.F., & Weiss, R.A.. (1984). The CD4 (T4) antigen is an essential component of the receptor for the AIDS retrovirus. Nature 312, 763–7.CrossRefGoogle ScholarPubMed
Doyle, C., & Strominger, J.L.. (1987). Interaction between CD4 and class II MHC molecules mediates cell adhesion. Nature 330, 256–9.CrossRefGoogle ScholarPubMed
Fellous, M., & Dausset, J.. (1970). Probable haploid expression of HL-A antigens on human spermatozoon. Nature 225, 191–3.CrossRefGoogle ScholarPubMed
Gosgrove, D., Gray, D., Dierich, A., Kaufman, J., Lemeur, M., Benoist, C., & Mathis, D.. (1991). Mice lacking MHC class II molecules. cell 66, 1051–66.CrossRefGoogle Scholar
Guo, M.W., Nose, K., Mori, E., & Mori, T.. (1990). Binding of foreign DNA to mouse sperm mediated by its MHC class II structure. Am. J Reprod. Immunol. 24, 120–6.Google Scholar
Henson, J.H., Begg, D.A., Beaulieu, S.M., Fishkind, D.J., Bonder, E.M., Terasaki, M., Lebeche, D., & Kaminer, B.. (1989). A calsequestrim-like protein in the endoplasmic reticulum of the sea urchin: localization and dynamics in the egg and first cell cycle embryo. J. Cell Biol. 109, 149–61.CrossRefGoogle ScholarPubMed
Hogan, H., Costantini, F., & Lacy, E.. (1986). Chemicals, supplies and solution. In Manipulating the Mouse Embryo, pp. 270–7. New York: Cold Spring Harbor Laboratory.Google Scholar
Kawasaki, E.S., & Wang, A.M.. (1989). PCR Technology, ed. Erlich, H.A., pp. 89–97. New York: M. Stockton press.CrossRefGoogle Scholar
Klatzmann, D., Champagne, E., Chamaret, S., Gruest, J., Guetard, D., Hercend, T., Gluckman, J.C., & Montagnier, L.. (1984). T-lymphocyte T4 molecule behaves as the receptor for human retrovirus LAV. Nature 312, 767–8.CrossRefGoogle ScholarPubMed
Kruisbeek, A.M., Mond, J.J., Fowlkes, B.J., Carmen, J.A., Bridges, S., & Longo, D.L. (1985). Absence of the Lyt-2−, L3T4+ lineage of T cells in mice treated neonatally with anti-I-A correlates with absence of intrathymic I-A-bearing antigen-presenting cell function. J. Exp. Med. 161, 1029–47.CrossRefGoogle ScholarPubMed
Kuhlmann, D., Dohr, G., Pusch, H.H., Scherbaum, W., Schieferstein, G., Uchanska, Z.B., & Ziegler, A.. (1986). Absence of HLA class I and class II antigens as well as beta 2-microglobulin from normal and pathological human spermatozoa. Tissue Antigens 27, 179–84.CrossRefGoogle Scholar
Littman, D.R., & Gettner, S.N.. (1987). Unusual intron in the immunoglobulin domain of the newly isolated murine CD4 (L3T4) gene. Nature 325, 453–5.CrossRefGoogle ScholarPubMed
Maddon, P.J., Dalgleish, A.G., McDougal, J.S., Clapham, P.R., Weiss, R.A., & Axel, R.. (1986). The T4 gene encodes the AIDS virus receptor and is expressed in the immune system and the brain. Cell 47, 333–48.CrossRefGoogle ScholarPubMed
McDougal, J.S., Mawle, A., Cort, S.P., Nicholson, J.K., Cross, G.D., Scheppler, C.J., Hicks, D., & Sligh, J. (1985). Cellular tropism of the human retrovirus HTLV-III/LAV. I. Role of T cell activation and expression of the T4 antigen. J. Immunol. 135, 3151–62.CrossRefGoogle ScholarPubMed
Miller, D.J., Macek, M.B., & Shur, B.D.. (1992). Complementarity between sperm surface beta-1,4-galactosyltransferase and egg-coat ZP3 mediates sperm–egg binding. Nature 357, 589–93.CrossRefGoogle ScholarPubMed
Moebius, U., Clayton, L.K., Abraham, S., Diener, A., Yunis, J.J., Harrison, S.C., & Reinherz, E.L. (1992). Human immunodeficiency virus gp120 binding C'C″ ridge of CD4 domain 1 is also involved in interaction with class II major histocompatibility complex molecules. Proc. Natl. Acad. Sci. USA 89, 12008–12.CrossRefGoogle Scholar
Mori, E., Takasaki, S., Hedrick, J.L., Wardrip, N.J., Mori, T. & Kobata, A.. (1991). Neutral oligosaccharide structures linked to asparagines of porcine zona pellucida glycoproteins. Biochemistry 30, 2078–87.CrossRefGoogle ScholarPubMed
Mori, T., Guo, M.W., Mori, E., Shindo, Y., Mori, N., Fukuda, A., & Mori, T.. (1990). Expression of class II major historcompatibility complex antigen on mouse sperm and its roles in fertilization. Am. J. Reprod. Immunol. 24, 9–14.CrossRefGoogle ScholarPubMed
Mori, T., Guo, M.W., & Mori, E.. (1991). Expression of CD4-like structure on murine egg vitelline membrane and its signal transductive roles through p56lck in fertilization. Am. J. Reprod. Immunol. 26, 97–103.CrossRefGoogle ScholarPubMed
Mori, T., Guo, M.W., Yoshida, H., Saito, S., & Mori, T. (1992). Expression of the signal transducing regions of CD4-like and lck genes in murine egg. Biochem. Biophys. Res. Commun. 182, 527–33.CrossRefGoogle ScholarPubMed
Oka, H., & Watanabe, H.. (1957). Colony-specificity in compound acidians as tested by fusion experiments. Proc. Jpn. Acad. Sci. 33, 657–9.CrossRefGoogle Scholar
Pierres, A., Naquet, P., Van, A.A., Bekkhoucha, F., Denizot, F., Mishal, Z., Schmitt, V.A., & Pierres, M.. (1984). A rat anti-mouse T4 monoclonal antibody (H129.19) inhibits the proliferation of Ia-reactive T cell clones and delineates two phenotypically distinct (T4+, Lyt-2,3− and T4−, Lyt-2,3+) subsets among anti-Ia cytolytic T cell clones. J. Immunol. 132, 2775–82.CrossRefGoogle ScholarPubMed
Primakoff, P., & Hyatt, H.. (1986). An antisperm monoclonal antibody inhibits sperm fusion with zona-free hamster eggs but not homologous eggs. Fertil. Steril. 46, 489–93.CrossRefGoogle Scholar
Reinherz, E.L., Kung, P.C., Goldstein, G., Levey, R.H., & Schlossman, S.F.. (1979). Separation of functional subsets of human T cells by a monoclonal antibody. Proc. Natl. Acad. Sci. USA 76, 4061–5.CrossRefGoogle Scholar
Reinherz, E.L., Kung, P.C., Goldstein, G., Levey, R.H., & Schlossman, S.F.. (1980a). Discrete stages of human intrathymic differentiation: analysis of normal thymocytes and leukemic lymphoblasts of T-cell lineage. Proc. Natl. Acad. Sci. USA 77, 1588–92.CrossRefGoogle ScholarPubMed
Reinherz, E.L., Morimoto, C., Penta, A.C., & Schlossman, S.F..(1980b). Regulation of B cell immunoglobulin secretion by functional subsets of T lymphocytes in man. Eur. J. Immunol. 10, 570–2.CrossRefGoogle ScholarPubMed
Robey, E., & Axel, R. (1990). CD4: collaborator in immune recognition and HIV infection. Cell 60, 697–700.CrossRefGoogle ScholarPubMed
Rodriguez, C.S., & Arnaiz, V.A. (1985). HLA-A and -B (but not -C, -Bw4, Bw6 or -DR antigens) are expressed on purified spermatozoa. Tissue Antigens 25, 11–18.CrossRefGoogle Scholar
Rudd, C.E., Trevillyan, J.M., Dasgupta, J.D., Wong, L.L., & Schlossman, S.F. (1988). The CD4 receptor is complexed in detergent lysates to a protein-tyrosine kinase (pp58) from human T lymphocytes. Proc. Natl. Acad. Sci. USA 85, 5190–4.CrossRefGoogle ScholarPubMed
Saiki, R.K., Gelfand, D.H., Stoffel, S., Scharf, S.J., Higuchi, R., Horn, G.T., Mullis, K.B., & Ehrlich, H.A.. (1988). Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science 239, 487–91.CrossRefGoogle ScholarPubMed
Sanger, F., Nicklen, S., & Coulson, A.R.. (1977). DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA 74, 5463–7.CrossRefGoogle ScholarPubMed
Scofield, V.L., Schlumpberger, J.M., West, L.A., & Weissman, I.L.. (1982). Protochordate allorecognition is controlled by a MHC-like gene system. Nature 295, 499–502.CrossRefGoogle ScholarPubMed
Shur, B.D., & Neely, C.A. (1988). Plasma membrane association, purification, and partial characterization of mouse sperm beta 1,4-galactosyltransferase [published erraturm appears in J. Biol. Chem. (1989) 264, 4264]. J. Biol. Chem. 263, 17706–14.CrossRefGoogle Scholar
Snell, G.D.. (1981). Studies in histocompatibility. Science 213, 172–8.CrossRefGoogle ScholarPubMed
Summers, M.D., & Smith, G.E.. (1987). A Manual of methods for Baculovirus Vectors and Insect Cell Culture Procedures. Texas Agriculture Experiment Station Bulletin no. 1555.Google Scholar
Swain, S.L.. (1983). T cell subsets and the recognition of MHC class. Immunol. Rev. 74, 129–42.CrossRefGoogle ScholarPubMed
Tourvieille, B., Gorman, S.D., Field, E.H., Hunkapiller, T., & Parnes, J.R.. (1986). Isolation and sequence of L3T4 complementary DNA clones: expression in T cells and brain. Science 234, 610–14.CrossRefGoogle Scholar
Veillette, A.. Bookman, M.A., Horak, E.M., & Bolen, J.B.. (1988). The CD4 and CD8 T cell surface antigens are associated with the internal membrane tyrosine-protein kinase p56lck. Cell 55, 301–8.CrossRefGoogle ScholarPubMed
Vojtiskova, M.. (1969). H-2d antigens on mouse spermatozoa. Nature 222, 1293–4.CrossRefGoogle ScholarPubMed
Wassarman, P.M.. (1987). The biology and chemistry of fertilization. Science 235, 553–60.CrossRefGoogle ScholarPubMed
Whitten, W.K., & Biggers, J.D. (1968). Complete development in vitro of the pre-implantation stages of the mouse in a simple chemically defined medium. J. Reprod. Fert. 17, 399–401.CrossRefGoogle Scholar
Williams, A.F., Davis, S.J., He, Q., & Barclay, A.N. (1989). Structural diversity in domains of the immunoglobulin superfamily. Cold Spring Harbor Symp. Quant. Biol. 2, 637–47.CrossRefGoogle Scholar
Yanagimachi, R. (1984). Zona-free hamster eggs: their use in assessing fertilization capacity and examining chromosomes of human spermatoazoa. Gamete Res. 7, 145–54.CrossRefGoogle Scholar
Yanagimachi, R.. (1988). Sperm–egg fusion. In current Topics in Membranes and Transport, vol. 32, ed. Duzgunes, N., & Bronner, F., pp 3–33. San Diego CA: Academic Press.Google Scholar
Zuniga, P.J., McCarthy, S.A., Weston, M., Longo, D.L., Singer, A., & Kruisbeek, A.M.. (1989). Role of CD4 in thymocyte selection and maturation. J. Exp. Med. 169, 2085–96.CrossRefGoogle Scholar