Sturgeon hatching enzyme and the mechanism of egg envelope digestion: Insight into changes in the mechanism of egg envelope digestion during the evolution of ray-finned fish

Journal of Experimental Zoology Part B: Molecular and Developmental Evolution

Volumn 324, Issue 8, 2015, Pages 720-732

  Nagasawa, Tatsuki ^a   Kawaguchi, Mari ^a   Sano, Kaori ^b   Yasumasu, Shigeki ^a  

^a SOPHIA UNIVERSITY   (Japan)

^b JOSAI UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ASTACIN; EGG PROTEIN; METALLOPROTEINASE;

ANIMAL; COMPARATIVE STUDY; EMBRYOLOGY; ENZYMOLOGY; EVOLUTION; FISH; GENETICS; HYBRIDIZATION; METABOLISM; NONMAMMALIAN EMBRYO; PHYLOGENY; PROTEIN DOMAIN; ZONA PELLUCIDA;

ANIMALS; BIOLOGICAL EVOLUTION; EGG PROTEINS; EMBRYO, NONMAMMALIAN; FISHES; HYBRIDIZATION, GENETIC; METALLOENDOPEPTIDASES; PHYLOGENY; PROTEIN DOMAINS; ZONA PELLUCIDA;

EID: 84983140545     PISSN: 15525007     EISSN: 15525015     Source Type: Journal    
DOI: 10.1002/jez.b.22660     Document Type: Article

References (44)

1. Canestro C, Albalat R, Irimia M, Garcia-Fernandez J. 2013. Impact of gene gains, losses and duplication modes on the origin and diversification of vertebrates. Semin Cell Dev Biol 24:83-94.
2. Chuang-Ju L, Qi-Wei W, Xi-Hua C, et al. 2011. Molecular characterization and expression pattern of three zona pellucida 3 genes in the Chinese sturgeon, Acipenser sinensis. Fish Pysiol Biochem 37:471-484.
3. Dettlaff TA, Ginsburg AS, Schmalhausen OI. 1993. Sturgeon fishes: developmental biology and aquaculture. Springer-Verlag 238-252.
4. Fan T, Katagiri C. 2001. Properties of the hatching enzyme from Xenopus laevis. Eur J Biochem 268:4892-4898.
5. Fujita T, Fukada H, Shimizu M, Hiramatsu N, Hara A. 2008. Molecular cloning and characterization of three distinct choriogenins in masu salmon, Oncorhynchus masou. Mol Reprod Dev 75:1217-1228.
6. Glasauer SMK, Neuhauss SCF. 2014. Whole-genome duplication in teleost fished and its evolutionary consequences. Mol Genet Genomics 289:1045-1060.
7. Goudet G, Mugnier S, Callebaut I, Monget P. 2008. Phylogenetic analysis and identification of pseudogenes reveal a progressive loss of Zona Pellucida genes during evolution of vertebrates. Biol Reprod 78:796-806.
8. Ha C, Iuchi I. 1998. 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.
9. Hiroi J, Maruyama K, Kawazu K, et al. 2004. Structure and developmental expression of hatching enzyme genes of the Japanese eel Anguilla japonica: an aspect of the evolution of fish hatching enzyme. Dev Genes Evol 214:176-184.
10. Hopkins DR, Keles S, Greenspan DS. 2007. The bone morphogenetic protein 1/tolloid-like metalloproteinases. Matrix Biol 26:508-523.
11. Inohaya K, Yasumasu S, Araki K, et al. 1997. Species-dependent migration of fish hatching gland cells that commonly express astacin-like proteases in common. Dev Growth Differ 39:191-197.
12. Inoue JG, Miya M, Tsukamoto K, Nishida M. 2003. Basal actinopterygian relationships: a mitogenomic perspective on the phylogeny of the "ancient fish." Mol Phylogenet Evol 26:110-120.
13. Institutional animal care and use committee; [http://iacuc.usc.edu/]
14. Law for the Humane Treatment and Management of Animals in Japan. 2013; https://www.env.go.jp/nature/dobutsu/aigo/2_data/laws/nt_h25_84.pdf
15. Kanamori A, Naruse K, Mitani H, Shima A, Hori H. 2003. Genomic organization of ZP domain containing egg envelope genes in medaka (Oryzias latipes). Gene 305:35-45.
16. Katagiri C, Maeda R, Yamasika C, et al. 1997. Molecular cloning of Xenopus hatching enzyme and its specific expression in hatching gland cells. Int J Dev Biol 41:19-25.
17. Kaushal GP, Haun RS, Herzog C, Shah SV. 2013. Meprin A metalloproteinase and its role in acute kidney injury. Am J Physiol Renal Physiol 304:F1150-F1158.
18. Kawaguchi M, Yasumasu S, Shimizu A, et al. 2005. Purification and gene cloning of Fundulus heteroclitus hatching enzyme. A hatching enzyme system composed of high choriolytic enzyme and low choriolytic enzyme is conserved between two different teleosts, Fundulus heteroclitus and medaka Oryzias latipes. FEBS J 272:4315-4326.
19. Kawaguchi M, Yasumasu S, Hiroi J, et al. 2006. Evolution of teleostean hatching enzyme genes and their paralogous genes. Dev Genes Evol 216:769-784.
20. Kawaguchi M, Yasumasu S, Hiroi J, et al. 2007. Analysis of the exon-intron 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.
21. Kawaguchi M, Fujita H, Yoshizaki N, et al. 2009. Different hatching strategies in embryos of two species, pacific herring Clupea pallasii and Japanese anchovy Engraulis japonicas, that belong to the same order clupeiformes, and their environmental adaptation. J Exp Zoolog B Mol Dev Evol 312B:95-107.
22. Kawaguchi M, Hiroi J, Miya M, et al. 2010. Intron-loss evolution of hatching enzyme genes in Teleostei. BMC Evol Biol 10:260.
23. Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
24. Lee K, Yasumasu S, Nomura K, 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 339:2812-2884.
25. Lindsay LL, Hedrick JL. 1995. Isolation and characterization of ovochymase, a chymotrypsin-like protease released during Xenopus laevis egg activation. Dev Biol 167:513-516.
26. Lindsay LL, Hedrick JL. 2004. Proteolysis of Xenopus laevis egg envelope ZPA triggers envelope hardening. Biochem Biophys Res Commun 324:648-654.
27. Lindsay LL, Wallace MA, Hedrick JL. 2001. A hatching enzyme substrate in the Xenopus laevis egg envelope is a high molecular weight ZPA homolog. Dev Growth Differ 43:305-313.
28. Lindsay LL, Yang JC, Hedrick JL. 2002. Identification and characterization of a unique Xenopus laevis egg envelope component, ZPD. Dev Growth Differ 44:205-212.
29. Muir A, Greenspan DS. 2011. Metalloproteinases in Drosophila to human that are central players in developmental processes. J Biol Chem 286:41905-41911.
30. Olivotto I, Yasumasu S, Gioacchini G, et al. 2004. Cloning and expression of high choriolytic enzyme, a component of the hatching enzyme system, during embryonic development of the marine ornamental fish Chrysiptera parasema. Marine Biol 145:1235-1241.
31. Oppen-berntsen DO, Helvik JV, Walther BT. 1990. The major structural proteins of cod (Gadus morhua) eggshells and protein crosslinking during teleost egg hardening. Dev Biol 137:258-265.
32. Sano K, Inohaya K, Kawaguchi M, et al. 2008. Purification and characterization of zebrafish hatching enzyme-an evolutionary aspect of the mechanism of egg envelope digestion. FEBS J 275:5934-5946.
33. Sano K, Kawaguchi M, Yoshikawa M, et al. 2011. Hatching enzyme of Japanese eel Anguilla japonica and the possible evolution of the egg envelope digestion mechanism. FEBS J 278:3711-3723.
34. Sano K, Kawaguchi M, Watanabe S, et al. 2013. Inferring the evolution of teleostean zp genes based on their sites of expression. J Exp Zoolog B Mol Dev Evol 320B:332-343.
35. Sano K, Kawaguchi M, Watanabe S, Yasumasu S. 2014. Neofunctionalization of a duplicate hatching enzyme gene during the evolution of teleost fishes. BMC Evol Biol 14:221.
36. 2. PloS ONE 5:1.
37. Stamatakis A. 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688-2690.
38. Sterchi EE, Stocker W, Bond JS. 2008. Meprins, membrane-bound and secreted astacin metalloproteinases. Mol Aspects Med 29:309-328.
39. Tao Z, Peng Y, Nolasco L, et al. 2005. Recombinant CUB-1 domain polypeptide inhibits the cleavage of ULVWF strings by ADAMTS13 under flow conditions. Blood 106:4139-4145.
40. Thomson JD, Gibson TJ, lewniak PF, Jeanmougin F, Higgins DG. 1997. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876-4882.
41. Yasumasu S, Mao KM, Sultana F, Sakaguchi H, 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.
42. Yasumasu S, Uzawa M, Iwasawa A, Yoshizaki N. 2010a. Hatching mechanism of the Chinese soft-shelled turtle Pelodiscus sinensis. Comp Biochem Physiol B 155:435-441.
43. Yasumasu S, Kawaguchi M, Ouchi S, et al. 2010b. Mechanism of egg envelope digestion by hatching enzymes, HCE and LCE in medaka, Oryzias latipes. J Biochem 148:439-448.
44. Yue HM, Cao H, Chen XH, et al. 2014. Molecular characterization of the cDNAs of two zona pellucida genes in the Chinese sturgeon, Acipencer sinenses Gray, 1835. J Appl Ichtyol 30:1273-1281.