Abstract
We isolated seven cDNA clones from embryos of the Japanese eel Anguilla japonica. Each deduced amino acid sequence consisted of a signal peptide, a propeptide and a mature enzyme portion belonging to the astacin protease family. A phylogenetic analysis showed that the eel enzymes resembled the high choriolytic enzyme (HCE) of medaka Oryzias latipes, and the hatching enzymes of the zebra fish Danio rerio and masu salmon Oncorhynchus masou. Hatching enzymes of these teleosts belonged to the group of the medaka HCE, and not the medaka low choriolytic enzyme (LCE), another hatching enzyme of medaka. Southern blot analysis showed that the genes of the eel hatching enzymes were multicopy genes like the medaka HCE genes. However, one of the eel hatching enzyme genes comprised eight exons and seven introns, and the exon-intron organization was similar to the medaka LCE gene, which is a single-copy gene. The molecular evolution of the fish hatching enzyme genes is discussed. In addition, whole-mount in situ hybridization and immunocytochemistry showed that the eel hatching enzyme was first expressed in the pillow anterior to the forebrain of early neurula, and finally in the cell mass on the yolk sac of later stage embryos. The early differentiation profile of eel hatching gland cells was similar to that of medaka, masu salmon and zebrafish, whereas the final location of the gland cells was different among fishes.
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References
Ballard WW (1982) Morphogenetic movements and fate map of the cypriniform teleost, Catostomus commersoni (Lacepede). J Exp Zool 219:301–321
Bond JS, Beynon RJ (1995) The astacin family of metalloendopeptidases. Protein Sci 4:1247–1261
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791
Geier G, Jacob E, Stocker W, Zwilling R (1997) Genomic organization of the zinc-endopeptidase astacin. In: Zwilling R, Stocker W (eds) The Astacins—structure and function of a new protein family. Dr. Kovac, Hamburg, pp 259–274
Hiroi J, Kaneko T, Tanaka M (1999) In vivo sequential changes in chloride cell morphology in the yolk-sac membrane of Mozambique tilapia (Oreochromis mossambicus) embryos and larvae during seawater adaptation. J Exp Biol 202:3485–3495
Inohaya K, Yasumasu S, Ishimaru M, Ohyama A, Iuchi I, Yamagami K (1995) Temporal and spatial patterns of gene expression for the hatching enzyme in the teleost embryo, Oryzias latipes. Dev Biol 171:374–385
Inohaya K, Yasumasu S, Araki K, Naruse K, Yamazaki K, Yasumasu I, Iuchi I, Yamagami K (1997) Species-dependent migration of fish hatching gland cells that express astacin-like proteases in common. Dev Growth Differ 39:191–197
Kimmel CB, Warga RM, Schilling TF (1990) Origin and organization of the zebrafish fate map. Development 108:581–594
Lambowitz AM, Belfort M (1993) Introns as mobile genetic elements. Annu Rev Biochem 62:587–622
Lauder GV, Liem KF (1983) The evolution and interrelationships of the actinopterygian fishes. Bull Mus Comp Zool 150:95–197
Long M, Rosenberg C, Gilbert W (1995) Intron phase correlations and the evolution of the intron/exon structure of genes. Proc Natl Acad Sci USA 92:12495–12499
Nelson G (1989) Phylogeny of major fish groups. In: Fernholm B, Bremer K, Jornvall H (eds) The hierarchy of life. Excerpta Medica, Amsterdam, pp 325–336
Rosen DE (1973) Interrelationships of higher teleostean fishes. In: Greenwood PH, Miles RS, Patterson C (eds) Interrelationships of fishes. Academic, London, pp 397–513
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Sasaki H, Hogan BL (1993) Differential expression of multiple fork head related genes during gastrulation and axial pattern formation in the mouse embryo. Development 118:47–59
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
Vanin EF (1985) Processed pseudogenes: characteristics and evolution. Annu Rev Genet 19:253–272
Weiner AM, Deininger PL, Efstratiadis A (1986) Nonviral retroposons: genes, pseudogenes, and transposable elements generated by the reverse flow of genetic information. Annu Rev Biochem 55:631–661
Yamamoto M (1963) Electron microscopy of fish development. I. Fine structure of the hatching glands of the teleost, Oryzias latipes. J Fac Sci Univ Tokyo Sect IV 10:115–121
Yasumasu S, Katow S, Hamazaki TS, Iuchi I, Yamagami K (1992a) Two constituent proteases of a teleostean hatching enzyme: concurrent syntheses and packaging in the same secretory granules in discrete arrangement. Dev Biol 149:349–356
Yasumasu S, Yamada K, Akasaka K, Mitsunaga K, Iuchi I, Shimada H, Yamagami K (1992b) 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
Yasumasu S, Iuchi I, Yamagami K (1994) cDNAs and the genes of HCE and LCE, two constituents of the medaka hatching enzyme. Dev Growth Differ 36:241–250
Yasumasu S, Shimada H, Inohaya K, Yamazaki K, Iuchi I, Yasumasu I, Yamagami K (1996) Different exon-intron organizations of the genes for two astacin-like proteases, high choriolytic enzyme (choriolysin H) and low choriolytic enzyme (choriolysin L), the constituents of the fish hatching enzyme. Eur J Biochem 237:752–758
Acknowledgements
We express our gratitude to Professor Ichiro Iuchi, of Sophia University, for his encouragement and helpful advice during the course of this study. This study was supported in part by a Grant-in-Aid for Scientific Research from the Ministry of Education, Science and Culture, Japan. J.H. was supported by Research Fellowships of the Japan Society for the Promotion of Science for Young Scientists.
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Hiroi, J., Maruyama, K., Kawazu, K. et al. Structure and developmental expression of hatching enzyme genes of the Japanese eel Anguilla japonica: an aspect of the evolution of fish hatching enzyme gene. Dev Genes Evol 214, 176–184 (2004). https://doi.org/10.1007/s00427-004-0397-1
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DOI: https://doi.org/10.1007/s00427-004-0397-1