Ovastacin, a cortical granule protease, cleaves ZP2 in the zona pellucida to prevent polyspermy

Journal of Cell Biology

Volumn 197, Issue 1, 2012, Pages 37-44

  Burkart, Anna D ^a   Xiong, Bo ^a   Baibakov, Boris ^a   Jiménez Movilla, Maria ^a   Dean, Jurrien ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

ANTISERUM; GLYCOPROTEIN; OVASTACIN; PROTEINASE; UNCLASSIFIED DRUG; ZP2 PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; FEMALE; FERTILIZATION; MOUSE; NONHUMAN; NULL ALLELE; OOCYTE; OOCYTE CORTEX; POLYSPERMY; PRIORITY JOURNAL; PROTEIN CLEAVAGE; SPERM; ZONA PELLUCIDA;

ANIMALS; EGG PROTEINS; FEMALE; FERTILIZATION; MALE; MEMBRANE GLYCOPROTEINS; METALLOPROTEASES; MICE; RECEPTORS, CELL SURFACE; SPERMATOZOA;

MUS;

EID: 84860301985     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201112094     Document Type: Article

References (42)

1. Baibakov, B., L. Gauthier, P. Talbot, T.L. Rankin, and J. Dean. 2007. Sperm binding to the zona pellucida is not sufficient to induce acrosome exocytosis. Development. 134:933-943. http://dx.doi.org/10.1242/dev.02752
2. Barros, C., and R. Yanagimachi. 1971. Induction of zona reaction in golden hamster eggs by cortical granule material. Nature. 233:268-269. http://dx.doi.org/10.1038/233268a0
3. Bauskin, A.R., D.R. Franken, U. Eberspaecher, and P. Donner. 1999. Characterization of human zona pellucida glycoproteins. Mol. Hum. Reprod. 5:534-540. http://dx.doi.org/10.1093/molehr/5.6.534
4. 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. http://dx.doi.org/10.1016/0012-1606(80)90371-1
5. Bleil, J.D., C.F. Beall, and P.M. Wassarman. 1981. Mammalian sperm-egg interaction: Fertilization of mouse eggs triggers modification of the major zona pellucida glycoprotein, ZP2. Dev. Biol. 86:189-197. http://dx.doi.org/101016/0012-1606(81)90329-8
6. Boja, E.S., T. Hoodbhoy, H.M. Fales, and J. Dean. 2003. Structural characterization of native mouse zona pellucida proteins using mass spectrometry. J. Biol. Chem. 278:34189-34202. http://dx.doi.org/10.1074/jbc.M304026200
7. Bond, J.S., and R.J. Beynon. 1995. The astacin family of metalloendopeptidases. Protein Sci. 4:1247-1261. http://dx.doi.org/10.1002/pro.5560040701
8. Bronson, R.A., and A. McLaren. 1970. Transfer to the mouse oviduct of eggs with and without the zona pellucida. J. Reprod. Fertil. 22:129-137. http://dx.doi.org/10.1530/jrf.0.0220129
9. Cummins, J.M., and R. Yanagimachi. 1982. Sperm-egg ratios and the site of the acrosome reaction during in vivo fertilization in the hamster. Gamete Res. 5:239-256. http://dx.doi.org/10.1002/mrd.1120050304
10. Deng, M., H. Kishikawa, R. Yanagimachi, G.S. Kopf, R.M. Schultz, and C.J. Williams. 2003. Chromatin-mediated cortical granule redistribution is responsible for the formation of the cortical granule-free domain in mouse eggs. Dev. Biol. 257:166-176. http://dx.doi.org/10.1016/S0012-1606(03)00045-9
11. Ducibella, T., S. Rangarajan, and E. Anderson. 1988a. The development of mouse oocyte cortical reaction competence is accompanied by major changes in cortical vesicles and not cortical granule depth. Dev. Biol. 130:789-792. http://dx.doi.org/10.1016/0012-1606(88)90368-5
12. Ducibella, T., E. Anderson, D.F. Albertini, J. Aalberg, and S. Rangarajan. 1988b. Quantitative studies of changes in cortical granule number and distribution in the mouse oocyte during meiotic maturation. Dev. Biol. 130:184-197. http://dx.doi.org/10.1016/0012-1606(88)90425-3
13. Ducibella, T., P. Duffy, and J. Buetow. 1994. Quantification and localization of cortical granules during oogenesis in the mouse. Biol. Reprod. 50:467-473. http://dx.doi.org/10.1095/biolreprod50.3.467
14. Ducibella, T., D. Huneau, E. Angelichio, Z. Xu, R.M. Schultz, G.S. Kopf, R. Fissore, S. Madoux, and J.P. Ozil. 2002. Egg-to-embryo transition is driven by differential responses to Ca(2+) oscillation number. Dev. Biol. 250:280-291. http://dx.doi.org/10.1006/dbio.2002.0788
15. Dumermuth, E., E.E. Sterchi, W.P. Jiang, R.L. Wolz, J.S. Bond, A.V. Flannery, and R.J. Beynon. 1991. The astacin family of metalloendopeptidases. J. Biol. Chem. 266:21381-21385.
16. East, I.J., and J. Dean. 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. http://dx.doi.org/10.1083/jcb.98.3.795
17. Gahlay, G., L. Gauthier, B. Baibakov, O. Epifano, and J. Dean. 2010. Gamete recognition in mice depends on the cleavage status of an egg's zona pellucida protein. Science. 329:216-219. http://dx.doi.org/10.1126/science.1188178
18. Greenhouse, S., P.E. Castle, and J. Dean. 1999. Antibodies to human ZP3 induce reversible contraception in transgenic mice with 'humanized' zonae pellucidae. Hum. Reprod. 14:593-600. http://dx.doi.org/10.1093/humrep/14.3.593
19. Hasegawa, A., K. Koyama, Y. Okazaki, M. Sugimoto, and S. Isojima. 1994. Amino acid sequence of a porcine zona pellucida glycoprotein ZP4 determined by peptide mapping and cDNA cloning. J. Reprod. Fertil. 100:245-255. http://dx.doi.org/10.1530/jrf.0.1000245
20. Horvath, P.M., T. Kellom, J. Caulfield, and J. Boldt. 1993. Mechanistic studies of the plasma membrane block to polyspermy in mouse eggs. Mol. Reprod. Dev. 34:65-72. http://dx.doi.org/10.1002/mrd.1080340111
21. Inoue, M., and D.P. Wolf. 1975. Sperm binding characteristics of the murine zona pellucida. Biol. Reprod. 13:340-346. http://dx.doi.org/10.1095/biolreprod13.3.340
22. Jaffe, L.A., A.P. Sharp, and D.P. Wolf. 1983. Absence of an electrical polyspermy block in the mouse. Dev. Biol. 96:317-323. http://dx.doi.org/10.1016/0012-1606(83)90168-9
23. Jiménez-Movilla, M., M. Avilés, M.J. Gómez-Torres, P.J. Fernández-Colom, M.T. Castells, J. de Juan, A. Romeu, and J. Ballesta. 2004. Carbohydrate analysis of the zona pellucida and cortical granules of human oocytes by means of ultrastructural cytochemistry. Hum. Reprod. 19:1842-1855. http://dx.doi.org/10.1093/humrep/deh311
24. Li, L., P. Zheng, and J. Dean. 2010. Maternal control of early mouse development. Development. 137:859-870. http://dx.doi.org/10.1242/dev.039487
25. Lindsay, L.L., and J.L. Hedrick. 2004. Proteolysis of Xenopus laevis egg envelope ZPA triggers envelope hardening. Biochem. Biophys. Res. Commun. 324:648-654. http://dx.doi.org/10.1016/j.bbrc.2004.09.099
26. Liu, M. 2011. The biology and dynamics of mammalian cortical granules. Reprod. Biol. Endocrinol. 9:149. http://dx.doi.org/10.1186/1477-7827-9-149
27. Liu, M., D. Sims, P. Calarco, and P. Talbot. 2003a. Biochemical heterogeneity, migration, and pre-fertilization release of mouse oocyte cortical granules. Reprod. Biol. Endocrinol. 1:77. http://dx.doi.org/10.1186/1477-7827-1-77
28. Liu, P., N.A. Jenkins, and N.G. Copeland. 2003b. A highly efficient recombineering-based method for generating conditional knockout mutations. Genome Res. 13:476-484. http://dx.doi.org/10.1101/gr.749203
29. Maleszewski, M., Y. Kimura, and R. Yanagimachi. 1996. Sperm membrane incorporation into oolemma contributes to the oolemma block to sperm penetration: Evidence based on intracytoplasmic sperm injection experiments in the mouse. Mol. Reprod. Dev. 44:256-259. http://dx.doi.org/10.1002/(SICI)1098-2795(199606)44:2<256::AID-MRD16>3.0.CO;2-0
30. Modliński, J.A. 1970. The role of the zona pellucida in the development of mouse eggs in vivo. J. Embryol. Exp. Morphol. 23:539-547.
31. Nicosia, S.V., D.P. Wolf, and M. Inoue. 1977. Cortical granule distribution and cell surface characteristics in mouse eggs. Dev. Biol. 57:56-74. http://dx.doi.org/10.1016/0012-1606(77)90354-2
32. Quesada, V., L.M. Sánchez, J. Alvarez, and C. López-Otín. 2004. Identification and characterization of human and mouse ovastacin: A novel metalloproteinase similar to hatching enzymes from arthropods, birds, amphibians, and fish. J. Biol. Chem. 279:26627-26634. http://dx.doi.org/10.1074/jbc.M401588200
33. Rankin, T.L., M. O'Brien, E. Lee, K.E.J.J. Wigglesworth, J. Eppig, and J. Dean. 2001. Defective zonae pellucidae in Zp2-null mice disrupt folliculogenesis, fertility and development. Development. 128:1119-1126.
34. 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 homologs. Dev. Cell. 5:33-43. http://dx.doi.org/10.1016/S1534-5807(03)00195-3
35. Sato, K. 1979. Polyspermy-preventing mechanisms in mouse eggs fertilized in vitro. J. Exp. Zool. 210:353-359. http://dx.doi.org/10.1002/jez.1402100219
36. Stewart-Savage, J., and B.D. Bavister. 1988. A cell surface block to polyspermy occurs in golden hamster eggs. Dev. Biol. 128:150-157. http://dx.doi.org/10.1016/0012-1606(88)90277-1
37. Suarez, S.S., and A.A. Pacey. 2006. Sperm transport in the female reproductive tract. Hum. Reprod. Update. 12:23-37. http://dx.doi.org/10.1093/humupd/dmi047
38. Sun, W., Y.H. Lou, J. Dean, and K.S. Tung. 1999. A contraceptive peptide vaccine targeting sulfated glycoprotein ZP2 of the mouse zona pellucida. Biol. Reprod. 60:900-907. http://dx.doi.org/10.1095/biolreprod60.4.900
39. Tian, J., H. Gong, and W.J. Lennarz. 1999. Xenopus laevis sperm receptor gp69/64 glycoprotein is a homolog of the mammalian sperm receptor ZP2. Proc. Natl. Acad. Sci. USA. 96:829-834. http://dx.doi.org/10.1073/pnas.96.3.829
40. Wessel, G.M., J.M. Brooks, E. Green, S. Haley, E. Voronina, J. Wong, V. Zaydfudim, and S. Conner. 2001. The biology of cortical granules. Int. Rev. Cytol. 209:117-206. http://dx.doi.org/10.1016/S0074-7696(01)09012-X
41. Zamboni, L. 1970. Ultrastructure of mammalian oocytes and ova. Biol. Reprod. 2:44-63. http://dx.doi.org/10.1095/biolreprod2.Supplement_2.44
42. Zheng, P., and J. Dean. 2009. Role of Filia, a maternal effect gene, in maintaining euploidy during cleavage-stage mouse embryogenesis. Proc. Natl. Acad. Sci. USA. 106:7473-7478. http://dx.doi.org/10.1073/pnas.0900519106