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Evolution of teleostean hatching enzyme genes and their paralogous genes

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Abstract

We isolated genes for hatching enzymes and their paralogs having two cysteine residues at their N-terminal regions in addition to four cysteines conserved in all the astacin family proteases. Genes for such six-cysteine-containing astacin proteases (C6AST) were searched out in the medaka genome database. Five genes for MC6AST1 to 5 were found in addition to embryo-specific hatching enzyme genes. RT-PCR and whole-mount in situ hybridization evidenced that MC6AST1 was expressed in embryos and epidermis of almost all adult tissues examined, while MC6AST2 and 3 were in mesenterium, intestine, and testis. MC6AST4 and 5 were specifically expressed in jaw. In addition, we cloned C6AST cDNA homologs from zebrafish, ayu, and fugu. The MC6AST1 to 5 genes were classified into three groups in the phylogenetic positions, and the expression patterns and hatching enzymes were clearly discriminated from other C6ASTs. Analysis of the exon–intron structures clarified that genes for hatching enzymes MHCE and MAHCE were intron-less, while other MC6AST genes were basically the same as the gene for another hatching enzyme MLCE. In the basal Teleost, the C6AST genes having the ancestral exon–intron structure (nine exon/eight intron structure) first appeared by duplication and chromosomal translocation. Thereafter, maintaining such ancestral exon–intron structure, the LCE gene was newly diversified in Euteleostei, and the MC6AST1 to 5 gene orthologs were duplicated and diversified independently in respective fish lineages. The HCE gene lost all introns in Euteleostei, whereas in the lineage to zebrafish, it was translocated from chromosome to chromosome and lost some of its introns.

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Abbreviations

MHCE:

medaka high choriolytic enzyme

MAHCE:

medaka acidic high choriolytic enzyme

MLCE:

medaka low choriolytic enzyme

MC6AST:

medaka six-cysteine-containing astacin family protease

AyHCE:

ayu high choriolytic enzyme

AyLCE:

ayu low choriolytic enzyme

AyNep:

ayu nephrosin

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Acknowledgements

We express our cordial thanks to Dr. K. Yamagami, former Professor of Developmental Biology, Life Science Institute, Sophia University, Tokyo, for giving us valuable advice and for reading the present manuscript. The present study was supported in part by a Grant-in-aid for Scientific Research (C) from J.S.P.S. to I. I. (No. 17570189) and S. Y. (No. 15570102).

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Authors and Affiliations

  1. Life Science Institute, Sophia University, 7-1 Kioi-cho, Chiyoda-ku, Tokyo, 102-8554, Japan

    Mari Kawaguchi, Shigeki Yasumasu & Ichiro Iuchi

  2. Department of Anatomy, St. Marianna University School of Medicine, 2-16-1 Sugao, Miyamae-ku, Kawasaki, 216-8511, Japan

    Junya Hiroi

  3. Department of Biological Sciences, Graduate School of Science, The University of Tokyo, Bunkyo-ku, Tokyo, 113-0033, Japan

    Kiyoshi Naruse

  4. Chiba Prefectural Fisheries Research Center Fresh-Water Station, Sakura, Chiba, 285-0866, Japan

    Masayuki Inoue

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  1. Mari Kawaguchi
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  2. Shigeki Yasumasu
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  4. Kiyoshi Naruse
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  5. Masayuki Inoue
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  6. Ichiro Iuchi
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Corresponding author

Correspondence to Ichiro Iuchi.

Additional information

Communicated by M. Hammerschmidt

The nucleotide sequence data reported in the present paper will appear in the DDBJ/EMBL/GenBank nucleotide sequence databases with accession numbers from AB256940 to AB256952.

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Fig. S1

A multiple alignment of amino acid sequences deduced from C6AST cDNAs of medaka (MHCE, MAHCE, MLCE and MC6AST1 to 5) and ayu (AyHCE, AyLCE1, AyLCE2 and AyNep). White and black triangles indicate the putative signal sequence cleavage sites and the N-terminals of mature enzymes, respectively. Arrows indicate the intron insertion sites for MLCE (intron 1-7), AyLCE1 (intron 1-8), AyLCE2 (intron 2-8), MC6AST1 and MC6AST4 and 5 (intron 1-8), MC6AST2 (intron 1, 3-8) and MC6AST3 (intron 1, 3-7). Identical residues are boxed. Dashes and asterisks represent gaps and stop codons, respectively. Two active site consensus sequences of the astacin family proteases are indicated in dark and light gray boxes, and conserved cysteine residues are in black boxes. Accession numbers: MHCE, M96170; MAHCE, AB256944; MLCE, M96169; MC6AST1, AB256945; MC6AST2, AB256946; MC6AST3, AB256947; MC6AST4, AB256948; MC6AST5, AB256949; AyHCE, AB256940; AyLCE1, AB256941 (3734 kb)

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Kawaguchi, M., Yasumasu, S., Hiroi, J. et al. Evolution of teleostean hatching enzyme genes and their paralogous genes. Dev Genes Evol 216, 769–784 (2006). https://doi.org/10.1007/s00427-006-0104-5

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