Mutation of a Conserved Hydrophobic Patch Prevents Incorporation of ZP3 into the Zona Pellucida Surrounding Mouse Eggs

Molecular and Cellular Biology

Volumn 23, Issue 24, 2003, Pages 8982-8991

  Zhao, Ming ^a   Gold, Lyn ^a   Dorward, Heidi ^a   Liang, Li Fang ^a   Hoodbhoy, Tanya ^a   Boja, Emily S ^b   Fales, Henry M ^c   Dean, Jurrien ^a  

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

^b NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^c NONE

Author keywords

[No Author keywords available]

Indexed keywords

FURIN; GLYCOPROTEIN; GREEN FLUORESCENT PROTEIN; PROTEIN ZP1; PROTEIN ZP2; PROTEIN ZP3; SIGNAL PEPTIDE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; FERTILIZATION; GENE MUTATION; GENETIC CONSERVATION; HYDROPHOBICITY; MASS SPECTROMETRY; MOUSE; NONHUMAN; OOCYTE; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN SECRETION; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; TRANSGENIC MOUSE; ZONA PELLUCIDA;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CONSERVED SEQUENCE; EGG PROTEINS; FEMALE; GREEN FLUORESCENT PROTEINS; HYDROPHOBICITY; LUMINESCENT PROTEINS; MEMBRANE GLYCOPROTEINS; MICE; MICE, TRANSGENIC; MOLECULAR SEQUENCE DATA; MUTATION; OOGENESIS; PROTEIN SORTING SIGNALS; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, CELL SURFACE; RECOMBINANT FUSION PROTEINS; ZONA PELLUCIDA;

ANIMALIA; MAMMALIA; MUS MUSCULUS;

EID: 0344629667     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.23.24.8982-8991.2003     Document Type: Article

References (42)

1. Arribas, J., and A. Borroto. 2002. Protein ectodomain shedding. Chem. Rev. 102:4627-4638.
2. Bleil, J. D., and P. M. Wassarman. 1980. 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.
3. Bleil, J. D., and P. M. Wassarman. 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.
4. Blobel, C. P. 2000. Remarkable roles of proteolysis on and beyond the cell surface. Curr. Opin. Cell Biol. 12:606-612.
5. Boja, E., T. Hoodbhoy, H. Fales, and J. Dean. 2003. Structural characterization of native mouse zona pellucida proteins using mass spectrometry. J. Biol. Chem. 278:34189-34202.
6. Bork, P., and C. Sander. 1992. A large domain common to sperm receptors (Zp2 and Zp3) and TGF-β type III receptor. FEBS Lett. 300:237-240.
7. 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. Anal. Biochem. 112:195-203.
8. Chiquoine, A. D. 1960. The development of the zona pellucida of the mammalian ovum. Am. J. Anat. 106:149-169.
9. Dietl, J. 1989. Ultrastructural aspects of the developing mammalian zona pellucida, p. 49-60. In J. Dietl (ed.), The mammalian egg coat. Springer-Verlag, Berlin, Germany.
10. Donaldson, J. G., and J. Lippincott-Schwartz. 2000. Sorting and signaling at the Golgi complex. Cell 101:693-696.
11. East, I. J., B. J. Gulyas, and J. Dean. 1985. Monoclonal antibodies to the murine zona pellucida protein with sperm receptor activity: effects on fertilization and early development. Dev. Biol. 109:268-273.
12. Hadek, R. 1965. The structure of the mammalian egg. Int. Rev. Cytol. 18:29-68.
13. Hospital, V., V. Chesneau, A. Balogh, C. Joulie, N. G. Seidah, P. Cohen, and A. Prat. 2000. N-arginine dibasic convertase (nardilysin) isoforms are soluble dibasic-specific metalloendopeptidases that localize in the cytoplasm and at the cell surface. Biochem. J. 349:587-597.
14. Jovine, L., H. Qi, Z. Williams, E. Litscher, and P. M. Wassarman. 2002. The ZP domain is a conserved module for polymerization of extracellular proteins. Nat. Cell Biol. 4:457-461.
15. Kang, Y.-H. 1974. Development of the zona pellucida in the rat oocyte. Am. J. Anat. 139:535-566.
16. Kiefer, S. M., and P. Saling. 2002. Proteolytic processing of human zona pellucida proteins. Biol. Reprod. 66:407-414.
17. Klein, P., M. Kanehisa, and C. Delisi. 1985. The detection and classification of membrane-spanning proteins. Biochim. Biophys. Acta 815:468-476.
18. Kubo, H., M. Matsushita, M. Kotani, H. Kawasaki, T. C. Saido, S. Kawashima, C. Katagiri, and A. Suzuki. 1999. Molecular basis for oviductin-mediated processing from gp43 to gp41, the predominant glycoproteins of Xenopus egg envelopes. Dev. Genet. 25:123-129.
19. Litscher, E. S., H. Qi, and P. M. Wassarman. 1999. Mouse zona pellucida glycoproteins mZP2 and mZP3 undergo carboxy-terminal proteolytic processing in growing oocytes. Biochemistry 38:12280-12287.
20. Liu, C., E. S. Litscher, S. Mortillo, Y. Sakai, R. A. Kinloch, C. L. Stewart, and P. M. Wassarman. 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.
21. Marsh, B. J., and K. E. Howell. 2002. The mammalian Golgi-complex debates. Nat. Rev. Mol. Cell. Biol. 3:789-795.
22. Millar, S. E., S. M. Chamow, A. W. Baur, C. Oliver, F. Robey, and J. Dean. 1989. Vaccination with a synthetic zona pellucida peptide produces long-term contraception in female mice. Science 246:935-938.
23. Millar, S. E., E. Lader, L.-F. Liang, and J. Dean. 1991. Oocyte-specific factors bind a conserved upstream sequence required for mouse zona pellucida promoter activity. Mol. Cell. Biol. 12:6197-6204.
24. Qi, H., Z. Williams, and P. M. Wassarman. 2002. Secretion and assembly of zona pellucida glycoproteins by growing mouse oocytes microinjected with epitope-tagged cDNAs for mZP2 and mZP3. Mol. Biol. Cell 13:530-541.
25. Rankin, T., and J. Dean. 2000. The zona pellucida: using molecular genetics to study the mammalian egg coat. Rev. Reprod. 5:114-121.
26. Rankin, T., M. Familari, E. Lee, A. M. Ginsberg, N. Dwyer, J. Blanchette-Mackie, J. Drago, H. Westphal, and J. Dean. 1996. Mice homozygous for an insertional mutation in the Zp3 gene lack a zona pellucida and are infertile. Development 122:2903-2910.
27. Rankin, T., P. Talbot, E. Lee, and J. Dean. 1999. Abnormal zonae pellucidae in mice lacking ZP1 result in early embryonic loss. Development 126:3847-3855.
28. Rankin, T. L., J. S. Coleman, O. Epifano, T. Hoodbhoy, S. G. Turner, P. E. Castle, E. Lee, R. Gore-Langton, and J. Dean. 2003. Fertility and taxon-specific sperm binding persist after replacement of mouse "sperm receptors" with human homologues. Dev. Cell 5:33-43.
29. Rankin, T. L., M. O'Brien, E. Lee, K. E. J. J. Wigglesworth, and J. Dean. 2001. Defective zonae pellucidae in Zp2 null mice disrupt folliculogenesis, fertility and development. Development 128:1119-1126.
30. Rankin, T. L., Z.-B. Tong, P. E. Castle, E. Lee, R. Gore-Langton, L. M. Nelson, and J. Dean. 1998. Human ZP3 restores fertility in Zp3 null mice without affecting order-specific sperm binding. Development 125:2415-2424.
31. Ringuette, M. J., M. E. Chamberlin, A. W. Baur, D. A. Sobieski, and J. Dean. 1988. Molecular analysis of cDNA coding for ZP3, a sperm binding protein of the mouse zona pellucida. Dev. Biol. 127:287-295.
32. Sasanami, T., J. Pan, Y. Doi, M. Hisada, T. Kohsaka, and M. Toriyama. 2002. Secretion of egg envelope protein ZPC after C-terminal proteolytic processing in quail granulosa cells. Eur. J. Biochem. 269:2223-2231.
33. Schlondorff, J., L. Lum, and C. P. Blobel. 2001. Biochemical and pharmacological criteria define two shedding activities for TRANCE/OPGL that are distinct from the tumor necrosis factor alpha convertase. J. Biol. Chem. 276:14665-14674.
34. Schwager, S. L., A. J. Chubb, Z. L. Woodman, L. Yan, R. Mentele, M. R. Ehlers, and E. D. Sturrock. 2001. Cleavage of disulfide-bridged stalk domains during shedding of angiotensin-converting enzyme occurs at multiple juxtamembrane sites. Biochemistry 40:15624-15630.
35. Seto, D. 1990. An improved method for sequencing double stranded plasmid DNA from minipreps using DMSO and modified template preparation. Nucleic Acids Res. 18:5905-5906.
36. Shimizu, S., M. Tsuji, and J. Dean. 1983. In vitro biosynthesis of three sulfated glycoproteins of murine zonae pellucidae by oocytes grown in follicle culture. J. Biol. Chem. 258:5858-5863.
37. Thomas, G. 2002. Furin at the cutting edge: from protein traffic to embryogenesis and disease. Nat. Rev. Mol. Cell. Biol. 3:753-766.
38. Von Heijne, G. 1986. A new method for predicting signal sequence cleavage sites. Nucleic Acids Res. 14:4683-4690.
39. Williams, Z., and P. M. Wassarman. 2001. Secretion of mouse ZP3, the sperm receptor, requires cleavage of its polypeptide at a consensus furin cleavage-site. Biochemistry 40:929-937.
40. Yanagimachi, R. 1994. Mammalian fertilization, p. 189-317. In E. Knobil and J. Neil (ed.), The physiology of reproduction. Raven Press, New York, N.Y.
41. r = 55, 000 antigen (ZP3) of porcine oocyte zona pellucida. Purification and characterization of α- and β-glycoproteins following digestion of lactosaminoglycan with endo-β-galactosidase. J. Biol. Chem. 262:564-571.
42. Zhao, M., L. Gold, A. M. Ginsberg, L.-F. Liang, and J. Dean. 2002. Conserved furin cleavage site not essential for secretion and integration of ZP3 into the extracellular egg coat of transgenic mice. Mol. Cell. Biol. 22:3111-3120.