Abnormal zonae pellucidae in mice lacking ZP1 result in early embryonic loss

Development

Volumn 126, Issue 17, 1999, Pages 3847-3855

  Rankin, Tracy ^a   Talbot, Prue ^a   Lee, Eric ^b   Dean, Jurrien ^a  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

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

Author keywords

Embryonic loss; Fertility; Pre implantation development; Zona pellucida; Zp1 null mutant mice

Indexed keywords

GLYCOPROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; EMBRYO DEATH; EMBRYO DEVELOPMENT; FEMALE; FERTILIZATION; GRANULOSA CELL; HORMONAL REGULATION; MOUSE; NONHUMAN; OOCYTE DEVELOPMENT; OVARY FOLLICLE DEVELOPMENT; OVULATION; PRIORITY JOURNAL; STEM CELL; ZONA PELLUCIDA;

ANIMALS; EGG PROTEINS; EMBRYONIC AND FETAL DEVELOPMENT; FEMALE; FERTILITY; FETAL DEATH; IN SITU HYBRIDIZATION; MALE; MEMBRANE GLYCOPROTEINS; MICE; MICE, KNOCKOUT; MICROSCOPY, ELECTRON, SCANNING; OVARY; PREGNANCY; RECEPTORS, CELL SURFACE; ZONA PELLUCIDA;

EID: 0032821285     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (59)

1. Amanze, D. and Iyengar, A. (1990). The micropyle: A sperm guidance system in teleost fertilization. Development 109, 495-500.
2. Beebe, S. J., Leyton, L., Burks, D., Fuerst, T., Dean, J. and Saling, P. M. (1992). Recombinant ZP3 inhibits sperm binding and induces the acrosome reaction. Dev. Biol. 151, 48-54.
3. Bleil, J. D. and Wassarman, P. M. (1980). Mammalian sperm-egg interaction: Identification of a glycoprotein in mouse egg zonae pellucidae possessing receptor activity for sperm. Cell 20, 873-882.
4. Bleil, J. D. and Wassarman, P. M. (1986). Autoradiographic visualization of the mouse egg's sperm receptor bound to sperm. J. Cell Biol. 102, 1363-1371.
5. 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. U. S. A. 85, 6778-6782.
6. Bleil, J. D., Beall, C. F. and Wassarman, P. M. (1981). Mammalian sperm-egg interaction: Fertilization of mouse eggs triggers modification of the major zona pellucida glycoprotein, ZP2. Dev. Biol. 86, 189-197.
7. 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.
8. Bork, P. and Sander, C. (1992). A large domain common to sperm receptors (Zp2 and Zp3) and TGF-beta type III receptor. FEBS Lett. 300, 237-240.
9. Bronson, R. A. and McLaren, A. (1970). Transfer to the mouse oviduct of eggs with and without the zona pellucida. J. Reprod. Fertil. 22, 129-137.
10. 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.
11. 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.
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. 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.
14. Del Giacco, L., Vanoni, C., Bonsignorio, D., Duga, S., Mosconi, G., Santucci, A. and Cotelli, F. (1998). Identification and spatial distribution of the mRNA encoding the gp49 component of the gilthead sea bream, Sparus aurata, egg envelope. Mol. Reprod. Dev. 49, 58-69.
15. Dietl, J. (1989). Ultrastructural aspects of the developing mammalian zona pellucida. In The Mammalian Egg Coat (ed. J. Dietl.), pp. 49-60. Berlin: Springer-Verlag.
16. 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.
17. 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.
18. Epifano, O., Liang, L.-F. and Dean, J. (1995b). Mouse Zp1 encodes a zona pellucida protein homologous to egg envelope proteins in mammals and fish. J. Biol. Chem. 270, 27254-27258.
19. Epifano, O., Liang, L.-F., Familari, M., Moos, M. C., Jr. and Dean, J. (1995a). Coordinate expression of the three zona pellucida genes during mouse oogenesis. Development 121, 1947-1956.
20. Eppig, J. J. (1991). Intercommunication between mammalian oocytes and companion somatic cells. BioEssays 13, 569-574.
21. 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.
22. Green, D. P. (1997). Three-dimensional structure of the zona pellucida. Rev. Reprod. 2, 147-156.
23. 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.
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. Killick, R., Legan, P. K., Malenczak, C. and Richardson, G. P. (1995). Molecular cloning of chick beta-tectorin, an extracellular matrix molecule of the inner ear. J. Cell Biol. 129, 535-547.
26. Kinloch, R. A., Mortillo, S., Stewart, C. L. and Wassarman, P. M. (1991). Embryonal carcinoma cells transfected with ZP3 genes differentially glycosylate similar polypeptides and secrete active mouse sperm receptor. J. Cell Biol. 115, 655-664.
27. Kinloch, R. A., Roller, R. J., Fimiani, C. M., Wassarman, D. A. and Wassarman, P. M. (1988). Primary structure of the mouse sperm receptor polypeptide determined by genomic cloning. Proc. Natl. Acad. Sci. USA 85, 6409-6413.
28. Kumar, S. and Hedges, S. B. (1998). A molecular timescale for vertebrate evolution. Nature 392, 917-920.
29. Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
30. Legan, P. K., Rau, A., Keen, J. N. and Richardson, G. P. (1997). The mouse tectorins. Modular matrix proteins of the inner ear homologous to components of the sperm-egg adhesion system. J. Biol. Chem. 272, 8791-8801.
31. Liang, L.-F., 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.
32. 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.
33. Lu, Q. and Shur, B. D. (1997). Sperm from b1,4-galactosyltransferase-null mice are refractory to ZP3-induced acrosome reactions and penetrate the zona pellucida poorly. Development 124, 4121-4131.
34. Lunsford, R. D., Jenkins, N. A., Kozak, C. A., Liang, L.-F., 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.
35. 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.
36. Miller, D. J., Gong, X., Decker, G. and Shur, B. D. (1993). Egg cortical granule N-acetylglucosaminidase is required for the mouse zona block to polyspermy. J. Cell Biol. 123, 1431-1440.
37. Modlinski, J. A. (1970). The role of the zona pellucida in the development of mouse eggs in vivo. J. Embryol. Exp. Morphol. 23, 539-547.
38. 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.
39. Murata, K., Sugiyama, H., Yasumasu, S., Iuchi, I., Yasumasu, I. and Yamagami, K. (1997). Cloning of cDNA and estrogen-induced hepatic-gene expression for choriogenin H, a precursor protein of the fish egg envelope (chorion). Proc. Natl. Acad. Sci. USA 94, 2050-2055.
40. Nagy, A., Rossant, J., Nagy, R., Abramow-Newerly, W. and Roder, J. C. (1993). Derivation of completely cell culture-derived mice from early-passage embryonic stem cells. Proc. Natl. Acad. Sci. USA 90, 8424-8428.
41. O'Rand, M. G. (1988). Sperm-egg recognition and barriers to interspecies fertilization. Gamete Res. 19, 315-328.
42. Phillips, D. M. and Shalgi, R. (1980). Surface architecture of the mouse and hamster zona pellucida and oocyte. J. Ultrastruct. Res. 72, 1-12.
43. 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.
44. 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.
45. Rankin, T., Tong, Z.-B., Castle, P. E., Lee, E., Gore-Langton, R., Nelson, L. M. and Dean, J. (1998). Human ZP3 restores fertility in Zp3 null mice without affecting order-specific sperm binding. Development 125, 2415-2424.
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. Sugiyama, H., Yasumasu, S., Murata, K., Iuchi, I. and Yamagami, K. (1998). The third egg envelope subunit in fish: cDNA cloning and analysis, and gene expression. Dev. Growth Differ. 40, 35-45.
49. Talbot, P. and DiCarlantonio, G. (1984). Ultrastructure of opossum oocyte investing coats and their sensitivity to trypsin and hyaluronidase. Dev. Biol. 103, 159-167.
50. Thomas, K. R. and Capecchi, M. R. (1987). Site-directed mutagenesis by gene targeting in mouse embryo-derived stem cells. Cell 51, 503-512.
51. Tian, J., Gong, H. and Lennarz, W. J. (1999). Xenopus laevix sperm receptor gp69/64 glycoprotein is a homolog of the mammalian sperm receptor ZP2. Proc. Natl. Acad. Sci. USA 96, 829-834.
52. Tian, J., Gong, H., Thomsen, G. H. and Lennarz, W. J. (1997a). Gamete interactions in Xenopus laevis: Identification of sperm binding glycoproteins in the egg vitelline envelope. J. Cell Biol. 136, 1099-1108.
53. Tian, J., Gong, H., Thomsen, G. H. and Lennarz, W. J. (1997b). Xenopus laevis sperm-egg adhesion is regulated by modifications in the sperm receptor and the egg vitelline envelope. Dev. Biol. 187, 143-153.
54. Tybulewicz, V. L. J., Crawford, C. E., Jackson, P. K., Bronson, R. T. and Mulligan, R. C. (1991). Neonatal lethality and lymphopenia in mice with a homozygous disruption of the c-abl proto-oncogene. Cell 65, 1153-1163.
55. 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.
56. Yamasaki, N., Richardson, R. T. and O'Rand, M. G. (1995). Expression of the rabbit sperm protein Sp17 in COS cells and interaction of recombinant Sp17 with the rabbit zona pellucida. Mol. Reprod. Dev. 40, 48-55.
57. 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.
58. Yurewicz, E. C., Hibler, D., Fontenot, G. K., Sacco, A. G. and Harris, J. (1993). Nucleotide sequence of cDNA encoding ZP3 alpha, a sperm-binding glycoprotein from zona pellucida of pig oocyte. Biochim. Biophys. Acta 1174, 211-214.
59. 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.