Mechanism of egg envelope digestion by hatching enzymes, HCE and LCE in medaka, Oryzias latipes

Journal of Biochemistry

Volumn 148, Issue 4, 2010, Pages 439-448

  Yasumasu, Shigeki ^a   Kawaguchi, Mari ^a,b   Ouchi, Satoshi ^a   Sano, Kaori ^a   Murata, Kenji ^c   Sugiyama, Hitoshi ^d   Akema, Tatsuo ^d   Iuchi, Ichiro ^a  

^a SOPHIA UNIVERSITY   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d ST MARIANNA UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

astacin metalloprotease family; egg envelope; hatching enzyme; medaka; ZP domain

Indexed keywords

HEXAPEPTIDE; TREFOIL PEPTIDE;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; CELL DIVISION; EGG; EMBRYO; ENZYME ACTIVITY; HATCHING; NONHUMAN; ORYZIAS; ZONA PELLUCIDA;

AMINO ACID SEQUENCE; ANIMALS; EGG PROTEINS; EMBRYO, NONMAMMALIAN; ENZYMES; FISH PROTEINS; MOLECULAR SEQUENCE DATA; ORYZIAS; OVUM; PROTEIN PRECURSORS; SUBSTRATE SPECIFICITY;

LOTUS; ORYZIAS LATIPES; ORYZIINAE;

EID: 77958035208     PISSN: 0021924X     EISSN: 17562651     Source Type: Journal    
DOI: 10.1093/jb/mvq086     Document Type: Article

References (37)

1. Ishida, J. (1944) Hatching enzyme in the freshwater fish, Oryzias latipes. Annot. Zool. Jpn. 22, 137-164
2. Ishida, J. (1985) Hatching enzyme: past, present and future. Zool. Sci. 2, 1-10
3. Katagiri, C., Maeda, R., Yamashika, C., Mita, K., Sargent, T.D., and Yasumasu, S. (1997) Molecular cloning of Xenopus hatching enzyme and its specific expression in hatching gland cells. Int. J. Dev. Biol. 41, 19-25
4. Yasumasu, S., Mao, K.M., Sultana, F., Sakaguchi, H., and Yoshizaki, N. (2005) Cloning of a quail homologue of hatching enzyme: its conserved function and additional function in egg envelope digestion. Dev. Genes Evol. 215, 489-498
5. Bond, J.S. and Beynon, R.J. (1995) The astacin family of metalloendopeptidases. Protein Sci. 4, 1247-1261
6. Quesada, V., Sanchez, L.M., Alvarez, J., and Lopez- Otin, C. (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
7. Wassarman, P.M. and Mortillo, S. (1991) Structure of the mouse egg extracellular coat, the zona pellucida. Int. Rev. Cytol. 130, 85-110
8. Spargo, S.C. and Hope, R.M. (2003) Evolution and nomenclature of the zona pellucida gene family. Biol. Reprod. 68, 358-362
9. Aagaard, J.E., Yi, X., MacCoss, M.J., and Swanson, W.J. (2006) Rapidly evolving zona pellucida domain proteins are a major component of the vitelline envelope of abalone eggs. Proc. Natl Acad. Sci. USA 103, 17302-17307
10. Jovine, L., Darie, C.C., Litscher, E.S., and Wassarman, P.M. (2005) Zona pellucida domain proteins. Annu. Rev. Biochem. 74, 83-114
11. Structural model of human endoglin, a transmembrane receptor responsible for hereditary hemorrhagic telangiectasia. J. Mol. Biol. 365, 694-705
12. Monné , M., Han, L., Schwend, T., Burendahl, S., and Jovine, L. (2008) Crystal structure of the ZP-N domain of ZP3 reveals the core fold of animal egg coats. Nature.456, 653-657.
13. 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
14. Yasumasu, S., Iuchi, I., and Yamagami, K. (1988) Medaka hatching enzyme consists of two kinds of proteases which act cooperatively. Zool. Sci. 5, 191-195
15. Yasumasu, S., Iuchi, I., and Yamagami, K. (1989) Purification and partial characterization of high choriolytic enzyme (HCE), a component of the hatching enzyme of the teleost, Oryzias latipes. J. Biochem. 105, 204-211
16. Yasumasu, S., Iuchi, I., and Yamagami, K. (1989) Isolation and some properties of low choriolytic enzyme (LCE), a component of the hatching enzyme of the teleost, Oryzias latipes. J. Biochem. 105, 212-218
17. Yasumasu, S., Yamada, K., Akasaka, K., Mitsunaga, K., Iuchi, I., Shimada, H., and Yamagami, K. (1992) Isolation of cDNAs for LCE and HCE, two constituent proteases of the hatching enzyme of Oryzias latipes, and concurrent expression of their mRNAs during development. Dev. Biol. 153, 250-258
18. Yamamoto, T. and Yamagami, K. (1975) Electron microscopic studies on choriolysis by the hatching enzyme (chorionase) of the teleost, Oryzias latipes. Dev. Biol. 43, 313-321
19. Lee, K.S., Yasumasu, S., Nomura, K., and Iuchi, I. (1994) HCE, a constituent of the hatching enzymes of Oryzias latipes embryos, releases unique proline-rich polypeptides from its natural substrate, the hardened chorion. FEBS Lett. 339, 281-284
20. Hamazaki, T.S., Iuchi, I., and Yamagami, K. (1987) Isolation and partial characterization of a spawning female-specific substance in the teleost, Oryzias latipes. J. Exp. Zool. 242, 343-349
21. Hamazaki, T.S., Nagahama, Y., Iuchi, I., and Yamagami, K. (1989) A glycoprotein from the liver constitutes the inner layer of the egg envelope (zona pullucida interna) of fish, Oryzias latipes. Dev. Biol. 133, 101-110
22. 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
23. 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
24. Murata, K., Sasaki, T., Yasumasu, S., Iuchi, I., Enami, J., Yasumasu, I., and Yamagami, K. (1995) Cloning of cDNAs for the precursor protein of a low-molecularweight subunit of the inner layer of the egg envelope (chorion) of the fish Oryzias latipes. Dev. Biol. 167, 9-17
25. Sugiyama, H., Murata, K., Iuchi, I., Nomura, K., and Yamagami, K. (1999) Formation of mature egg envelope subunit proteins from their precursors (choriogenins) in the fish, Oryzias latipes: loss of partial C-terminal sequences of the choriogenins. J. Biochem. 125, 469-475.
26. Sugiyama, H. and Iuchi, I. (2000) Molecular structure and hardening of egg envelope in fish. Recent Res. Dev. Comp. Biochem. Physiol. 1, 139-161.
27. Ha, C.R. and Iuchi, I. (1988) Enzyme responsible for egg envelope (chorion) hardening in fish: purification and partial characterization of two transglutaminases associated with their substrate, unfertilized egg chorion, of the rainbow trout, Oncorhynchus mykiss. J. Biochem. 124, 917-926
28. Masuda, K., Iuchi, I., and Yamagami, K. (1991) Analysis of hardening of the egg envelope (chorion) of the fish, Oryzias latipes. Dev. Growth Differ. 33, 75-83
29. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685
30. Boja, E.S., Hoodbhoy, T., Fales, H.M., and Dean, J. (2003) Structural characterization of native mouse zona pellucida proteins using mass spectrometry. J. Biol. Chem. 278, 34189-34202
31. Darie, C.C., Biniossek, M.L., Jovine, L., Litscher, E.S., and Wassarman, P.M. (2004) Structural characterization of fish egg vitelline envelope proteins by mass spectrometry. Biochemistry 43, 7459-7478
32. Darie, C.C., Janssen, W.G., Litscher, E.S., and Wassarman, P.M. (2008) Purified trout egg vitelline envelope proteins VEβ and VEγ polymerize into homomeric fibrils from dimers in vitro. Biochim. Biophys. Acta 1784, 385-392
33. Litscher, E.S., Janssen, W.G., Darie, C.C., and Wassarman, P.M. (2008) Purified mouse egg zona pellucida glycoproteins polymerize into homomeric fibrils under non-denaturing conditions. J. Cell. Physiol. 214, 153-157
34. Qi, H., Williams, Z., and Wassarman, P.M. (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
35. Jovine, L., Qi, H., Williams, Z., Litscher, E., and Wassarman, P.M. (2002) The ZP domain is a conserved module for polymerization of extracellular proteins. Nature Cell. Biol. 4, 457-461
36. Kawaguchi, M., Yasumasu, S., Hiroi, J., Naruse, K., Suzuki, T., and Iuchi, I. (2007) Analysis of the exonintron structures of fish, amphibian, bird and mammalian hatching enzyme genes, with special reference to the intron loss evolution of hatching enzyme genes in Teleostei. Gene. 392, 77-88
37. Sano, K., Inohaya, K., Kawaguchi, K., Yoshizaki, N., Iuchi, N., and Yasumasu, S. (2008) Purification and characterization of zebrafish hatching enzyme - an evolutionary aspect of the mechanism of egg envelope digestion. FEBS J. 275, 5934-5946