Human ZP3 restores fertility in Zp3 null mice without affecting order-specific sperm binding

Development

Volumn 125, Issue 13, 1998, Pages 2415-2424

  Rankin, Tracy L ^a   Tong, Zhi Bin ^a   Castle, Philip E ^a   Lee, Eric ^b   Gore Langton, Robert ^a   Nelson, Lawrence M ^a   Dean, Jurrien ^a  

^a SUBURBAN HOSPITAL   (United States)

^b EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

Author keywords

Human fertilization; Mouse; Mouse fertility; Order specific sperm binding; Sperm egg interaction; Transgene; Zona pellucida

Indexed keywords

PROTEIN;

ACROSOME REACTION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; FEMALE FERTILITY; GENE EXPRESSION; HUMAN; MOUSE; NONHUMAN; OOCYTE; OVIDUCT; PHENOTYPE; POLYSPERMY; PRIORITY JOURNAL; SPERM; TRANSGENE; ZONA PELLUCIDA;

ANIMALS; CHIMERA; EGG PROTEINS; FEMALE; FERTILITY; FERTILIZATION; HUMANS; INFERTILITY, FEMALE; MALE; MEMBRANE GLYCOPROTEINS; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; RECEPTORS, CELL SURFACE; SPERM-OVUM INTERACTIONS; SPERMATOZOA; ZONA PELLUCIDA;

EID: 0031927829     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (65)

1. Amanze, D. and Iyengar, A. (1990). The micropyle: a sperm guidance system in teleost fertilization. Development 109, 495-500.
2. Bedford, J. M. (1977). Sperm/egg interaction: The specificity of human spermatozoa. Anat. Rec. 188, 477-488.
3. Bleil, J. D., Greve, J. M. and Wassarman, P. M. (1988). Identification of a secondary sperm receptor in the mouse egg zona pellucida: Role in maintenance of binding of acrosome-reacted sperm to eggs. Dev. Biol. 128, 376-385.
4. Bleil, J. D. and Wassarman, P. M. (1980a). Structure and function of the zona pellucida: Identification and characterization of the proteins of the mouse oocyte's zona pellucida. Dev. Biol. 76, 185-202.
5. Bleil, J. D. and Wassarman, P. M. (1980b). Mammalian sperm-egg interaction: Identification of a glycoprotein in mouse egg zonae pellucidae possessing receptor activity for sperm. Cell 20, 873-882.
6. Bleil, J. D. and Wassarman, P. M. (1983). Sperm-egg interactions in the mouse: Sequence of events and induction of the acrosome reaction by a zona pellucida glycoprotein. Dev. Biol. 95, 317-324.
7. Bleil, J. D. and Wassarman, P. M. (1988). Galactose at the nonreducing terminus of O-linked oligosaccharides of mouse egg zona pellucida glycoprotein ZP3 is essential for the glycoprotein's sperm receptor activity. Proc. Natl. Acad. Sci. USA 85, 6778-6782.
8. Burnette, W. N. (1981). 'Western blotting': Electrophoretic transfer of proteins from sodium dodecyl sulfate-polyacrylamide gels to unmodified nitrocellulose and radiographic detection with antibody and radioiodinated protein A. Analyt. Biochem. 112, 195-203.
9. Chamberlin, M. E. and Dean, J. (1989). Genomic organization of a sex specific gene: The primary sperm receptor of the mouse zona pellucida. Dev. Biol. 131, 207-214.
10. Chamberlin, M. E. and Dean, J. (1990). Human homolog of the mouse sperm receptor. Proc. Natl. Acad. Sci. USA 87, 6014-6018.
11. Chang, Y. S., Wang, S. C., Tsao, C. C. and Huang, F. L. (1996). Molecular cloning, structural analysis, and expression of carp ZP3 gene. Mol. Reprod. Dev. 44, 295-304.
12. Chang, Y. S., Hsu, C. C., Wang, S. C., Tsao, C. C. and Huang, F. L. (1997). Molecular cloning, structural analysis, and expression of carp ZP2 gene. Mol. Reprod. Dev. 46, 258-267.
13. Coyne, J. A. (1992). Genetics and speciation. Nature 355, 511-515.
14. East, I. J., Gulyas, B. J. and Dean, J. (1985). Monoclonal antibodies to the murine zona pellucida protein with sperm receptor activity: Effects on fertilization and early development. Dev. Biol. 109, 268-273.
15. East, I. J. and Dean, J. (1984). Monoclonal antibodies as probes of the distribution of ZP-2, the major sulfated glycoprotein of the murine zona pellucida. J. Cell Biol. 98, 795-800.
16. Epifano, O., Liang, L. and Dean, J. (1995a). Mouse Zp1 encodes a zona pellucida protein homologous to egg envelope proteins in mammals and fish. J. Biol. Chem. 270, 27254-27258.
17. Epifano, O., Liang, L., Familari, M., Moos, M. C., Jr. and Dean, J. (1995b). Coordinate expression of the three zona pellucida genes during mouse oogenesis. Development 121, 1947-1956.
18. Florman, H. M. and Storey, B. T. (1982). Mouse gamete interactions: The zona pellucida is the site of the acrosome reaction leading to fertilization in vitro. Dev. Biol. 91, 121-130.
19. Florman, H. M. and Wassarman, P. M. (1985). O-linked oligosaccharides of mouse egg ZP3 account for its sperm receptor activity. Cell 41, 313-324.
20. Greve, J. M. and Wassarman, P. M. (1985). Mouse egg extracellular coat is a matrix of interconnected filaments possessing a structural repeat. J. Mol. Biol. 181, 253-264.
21. Harris, J. D., Hibler, D. W., Fontenot, G. K., Hsu, K. T., Yurewicz, E. C. and Sacco, A. G. (1994). Cloning and characterization of zona pellucida genes and cDNAs from a variety of mammalian species: ZPA, ZPB, and ZPC gene families. DNA Seq 4, 361-393.
22. Hedrick, J. L. (1996). Comparative structural and antigenic properties of zona pellucida glycoproteins. J. Reprod. Fertil. S50, 9-17.
23. Hildreth, J. E., Holt, V., August, J. T. and Pescovitz, M. D. (1989) Monoclonal antibodies against porcine LFA-1: Species cross-reactivity and functional effects of beta-subunit-specific antibodies. Mol. Immunol. 26, 883-895.
24. Ho, Y., Wigglesworth, K., Eppig, J. J. and Schultz, R. M. (1995). Preimplantation development of mouse embryos in KSOM: Augmentation by amino acids and analysis of gene expression. Mol. Reprod. Dev. 41, 232-238.
25. Hogan, B., Beddington, R., Costantini, F. and Lacy, E. (1994). Manipulating the Mouse Embryo. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory.
26. Kinloch, R. A., Mortillo, S. and Wassarman, P. M. (1992). Transgenic mouse eggs with functional hamster sperm receptors in their zona pellucida. Development 115, 937-946.
27. Kubo, H., Kawano, T., Tsubuki, S., Kawashima, S., Katagiri, C. and Suzuki, A. (1997). A major glycoprotein of Xenopus egg vitelline envelope, gp41, is a frog homolog of mammalian ZP3. Dev. Growth Differ. 39, 405-417.
28. Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
29. Liang, L., Chamow, S. M. and Dean, J. (1990). Oocyte-specific expression of mouse Zp-2: Developmental regulation of the zona pellucida genes. Mol. Cell. Biol. 10, 1507-1515.
30. Liang, L. and Dean, J. (1993). Conservation of the mammalian secondary sperm receptor genes results in promoter function of the human homologue in heterologous mouse oocytes. Dev. Biol. 156, 399-408.
31. Liu, C., Litscher, E. S., Mortillo, S., Sakai, Y., Kinloch, R. A., Stewart, C. L. and Wassarman, P. M. (1996). Targeted disruption of the mZP3 gene results in production of eggs lacking a zona pellucida and infertility in female mice. Proc. Natl. Acad. Sci. USA 93, 5431-5436.
32. Lu, Q. and Shur, B. D. (1997). Sperm from β1,4-galactosyltransferase-null mice are refractory to ZP3-induced acrosome reactions and penetrate the zona pellucida poorly. Development 124, 4121-4131.
33. Lunsford, R. D., Jenkins, N. A., Kozak, C. A., Liang, L., Silan, C. M., Copeland, N. G. and Dean, J. (1990). Genomic mapping of murine Zp-2 and Zp-3, two oocyte-specific loci encoding zona pellucida proteins. Genomics 6, 184-187.
34. Lyons, C. E., Payette, K. L., Price, J. L. and Huang, R. C. C. (1993) Expression and structural analysis of a teleost homolog of a mammalian zona pellucida gene. J. Biol. Chem. 268, 21351-21358.
35. Metz, E. C. and Palumbi, S. R. (1996). Positive selection and sequence rearrangements generate extensive polymorphism in the gamete recognition protein bindin. Mol. Biol. Evol. 13, 397-406.
36. Miller, D. J., Macek, M. B. and Shur, B. D. (1992). Complementarity between sperm surface beta-1,4-galactosyltransferase and egg-coat ZP3 mediates sperm-egg binding. Nature 357, 589-593.
37. Murata, K., Sasaki, T., Yasumasu, S., Iuchi, I., Yasumasu, I. and Yamagami, K. (1995). Cloning of cDNA for precursor protein of a low moleclar weight subunit of the inner layer of the egg envelope (chorion) of the fish. Oryzias latipes. Dev. Biol. 167, 9-17.
38. Murata, K., Sugiyama, H., Yasumasu, S., Iuchi, I., Yasumasu, I. and Yamagami, K. (1997). Cloning of cDNA and estrogen-induced hepaticgene expression for choriogenin H, a precursor protein of the fish egg envelope (chorion). Proc. Natl. Acad. Sci. U. S. A. 94, 2050-2055.
39. O'Rand, M. G. (1988). Sperm-egg recognition and barriers to interspecies fertilization. Gamete Res. 19, 315-328.
40. Prasad, S. V., Wilkins, B., Skinner, S. M. and Dunbar, B. S. (1996). Evaluating zona-pellucida structure and function using antibodies to rabbit 55 kDa ZP protein expressed in baculovirus expression system. Mol. Reprod. Dev. 43, 519-529.
41. Rankin, T., Familari, M., Lee, E., Ginsberg, A. M., Dwyer, N., Blanchette-Mackie, J., Drago, J., Westphal, H. and Dean, J. (1996). Mice homozygous for an insertional mutation in the Zp3 gene lack a zona pellucida and are infertile. Development 122, 2903-2910.
42. Ringuette, M. J., Chamberlin, M. E., Baur, A. W., Sobieski, D. A. and Dean, J. (1988). Molecular analysis of cDNA coding for ZP3, a sperm binding protein of the mouse zona pellucida. Dev. Biol. 127, 287-295.
43. Roldan, E. R. and Yanagimachi, R. (1989). Cross-fertilization between Syrian and Chinese hamsters. J. Exp. Zool. 250, 321-328.
44. Russell, L. D. and Rogers, B. J. (1987). Improvement in the quality and fertilization potential of a human sperm population using the rise technique. J. Androl. 8, 25-33.
45. Sacco, A. G., Yurewicz, E. C., Subramanian, M. G. and DeMayo, F. (1981). Zona pellucida composition: Species cross reactivity and contraceptive potential of antiserum to a purified pig zona pellucida antigen (PPZA). Biol. Reprod. 25, 997-1008.
46. Sacco, A. G., Yurewicz, E. C., Subramanian, M. G. and Matzat, P. D. (1989). Porcine zona pellucida: Association of sperm receptor activity with the alpha-glycoprotein component of the Mr = 55,000 family. Biol. Reprod. 41, 523-532.
47. Saling, P. M., Sowinski, J. and Storey, B. T. (1979). An ultrastructural study of epididymal mouse spermatozoa binding to zonae pellucidae in vitro: Sequential relationship to the acrosome reaction. J. Exp. Zool. 209, 229-238.
48. Schliewen, U. K., Tautz, D. and Paabo, S. (1994). Sympatric speciation suggested by monophyly of crater lake cichlids. Nature 368, 629-632.
49. Schwoebel, E., Prasad, S., Timmons, T. M., Cook, R., Kimura, H., Niu, E., Cheung, P., Skinner, S., Avery, S. E., Wilkins, B. and Dunbar, B. S. (1991). Isolation and characterization of a full-length cDNA encoding the 55 kDa rabbit zona pellucida protein. J. Biol. Chem. 266, 7214-7219.
50. Shabanowitz, R. B. and O'Rand, M. G. (1988). Characterization of the human zona pellucida from fertilized and unfertilized eggs. J. Reprod. Fertil. 82, 151-161.
51. Shimizu, S., Ito, M. and Dean, J. (1982). Glycoproteins of mouse zona pellucida: analysis of their reactivity to lectins. Biochem. Biophys. Res. Commun. 109, 449-454.
52. Shimizu, S., Tsuji, M. and Dean, J. (1983). In vitro biosynthesis of three sulfated glycoproteins of murine zonae pellucidae by oocytes grown in follicle culture. J. Biol. Chem. 258, 5858-5863.
53. Shoemaker, D. D. and Ross, K. G. (1996). Effects of social organization on gene flow in the fire ant Solenopsis invicta. Nature 383, 613-616.
54. Snell, W. J. and White, J. M. (1996). The molecules of mammalian fertilization. Cell 85, 629-637.
55. Storey, B. T., Lee, M. A., Muller, C., Ward, C. R. and Wirtshafter, D. G. (1984). Binding of mouse spermatozoa to the zonae pellucidae of mouse eggs in cumulus: Evidence that the acrosomes remain substantially intact. Biol. Reprod. 31, 1119-1128.
56. Thall, A. D., Maly, P. and Lowe, J. B. (1995). Oocyte galγ1.3gal epitopes implicated in sperm adhesion to the zona pellucida glycoprotein ZP3 are not required for fertilization in the mouse. J. Biol. Chem. 270, 21437-21440.
57. Tian, J., Gong, H., Thomsen, G. H. and Lennarz, W. J. (1997). Gamete interactions in Xenopus laevis: Identification of sperm binding glycoproteins in the egg vitelline envelope. J. Cell Biol. 136, 1099-1108.
58. Tong, Z., Nelson, L. M. and Dean, J. (1995). Inhibition of zona pellucida gene expression by antisense oligonucleotides injected into mouse oocytes. J. Biol. Chem. 270, 849-853.
59. van Duin, M., Polman, J. E. M., De Breet, I. T. M., van Ginneken, K., Bunschoten, H., Grootenhuis, A., Brindle, J. and Aitken, R. J. (1994). Recombinant human zona pellucida protein ZP3 produced by Chinese hamster ovary cells induces the human sperm acrosome reaction and promotes sperm-egg fusion. Biol. Reprod. 51, 607-617.
60. Wolf, D. P. and Hamada, M. (1979). Sperm binding to the mouse egg plasmalemma. Biol. Reprod. 21, 205-211.
61. Yamagami, K., Hamazaki, T. S., Yasumasu, S., Masuda, K. and Iuchi, I. (1992). Molecular and cellular basis of formation, hardening, and breakdown of the egg envelope in fish. Int. Rev. Cytol. 136, 51-92.
62. Yanagimachi, R. (1994). Mammalian fertilization. In The Physiology of Reproduction, (ed. E. Knobil and J. Neil), pp. 189-317. New York: Raven Press.
63. Yang, J. C. and Hedrick, J. L. (1997). cDNA cloning and sequence analysis of the Xenopus laevis egg envelope glycoprotein gp43. Dev. Growth Differ. 39, 457-467.
64. Yonezawa, N., Aoki, H., Hatanaka, Y. and Nakano, M. (1995). Involvement of N-linked carbohydrate chains of pig zona pellucida in sperm-egg binding. Eur: J. Biochem. 233, 35-41.
65. Yurewicz, E. C., Sacco, A. G., Gupta, S. K., Xu, N. and Gage, D. A. (1998) Hetero-oligomerization-dependent binding of pig oocyte zona pellucida glycoproteins ZPB and ZPC to boar sperm membrane vesicles. J. Biol. Chem. 273, 7488-7494.