Hatching mechanism of the Chinese soft-shelled turtle Pelodiscus sinensis

Yasumasu, Shigeki; Uzawa, Moeko; Iwasawa, Atsushi; Yoshizaki, Norio

doi:10.1016/j.cbpb.2010.01.009

Cited by 18 publications

(11 citation statements)

References 39 publications

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“…The K m value for purified EHE toward the best synthetic peptide substrate, RPTFG↓RPGIT, was 232.6 μ m . This value was smaller than that of medaka hatching enzyme (HCE) toward the best substrate (480 μ m , NPQVPQ↓YPSKPQ) [8]. The k cat value was 15.8 s −1 .…”

Section: Resultsmentioning

confidence: 91%

“…Hatching enzyme is an enzyme that digests the egg envelope at the time of embryo hatching. Hatching enzyme orthologs, which belong to the astacin metalloproteinase family [1,2], are found in amphibians, birds, reptiles, mammals and fishes [3–8]. The egg envelopes of vertebrate embryos, as the substrates of hatching enzymes, are constructed of several homologous glycoproteins that possess a characteristic zona pellucida (ZP) domain consisting of ∼ 260 amino acids [9–14].…”

Section: Introductionmentioning

confidence: 99%

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Hatching enzyme of Japanese eel Anguilla japonica and the possible evolution of the egg envelope digestion mechanism

et al. 2011

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We purified eel hatching enzyme (EHE) from the hatching liquid of Japanese eel Anguilla japonica belonging to Elopomorpha to a single band on SDS ⁄ PAGE. TOF-MS analysis revealed that the purified EHE contained several isozymes with similar molecular masses. Comparison of the egg envelope digestion specificities of the purified EHE and of recombinant EHE4, one of the EHE isozymes, suggested that the isozymes contained in the purified EHE were functionally the same in terms of egg envelope digestion. By electron microscopy, the egg envelope became swollen after treatment with the purified EHE. The EHE cleavage sites on the zona pellucida (ZP) protein of the egg envelope were located in the N-terminal repeat regions. In previous phylogenetic analysis, we suggested that fishes included in Elopomorpha, as basal teleosts, possess a single type of hatching enzyme genes, and that fishes in Otocephala and Euteleostei gain two types of hatching enzyme genes called clade I and II genes by duplication. Further, the clade I enzymes, zebrafish hatching enzyme (ZHE1) and medaka high choriolytic enzyme (HCE), swell the egg envelope by cleaving the N-terminal regions of ZP proteins, while the clade II enzyme, medaka low choriolytic enzyme (LCE), solubilizes the swollen envelope by cleaving the site at the middle region on the ZP domain. In this evolutionary scenario, our findings support that hatching of Japanese eel conserves the ancestral mechanism of fish egg envelope digestion. The clade I enzymes inherit the ancestral enzyme function, and the clade II enzymes gain a new function during evolution to Otocephala and Euteleostei.

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Section: Resultsmentioning

confidence: 91%

Section: Introductionmentioning

confidence: 99%

Hatching enzyme of Japanese eel Anguilla japonica and the possible evolution of the egg envelope digestion mechanism

et al. 2011

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“…The enzyme belongs to the astacin metallo-protease family [14] as do BMP1 (bone morphogenetic protein 1) and meprin (metallo-endopeptidase from renal tissue). Hatching enzyme orthologs are also found in other vertebrates [15-18]. Those of tetrapods are multi-domain proteins consisting of astacin protease domain and additional C-terminal domain(s).…”

Section: Introductionmentioning

confidence: 99%

Intron-loss evolution of hatching enzyme genes in Teleostei

et al. 2010

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BackgroundHatching enzyme, belonging to the astacin metallo-protease family, digests egg envelope at embryo hatching. Orthologous genes of the enzyme are found in all vertebrate genomes. Recently, we found that exon-intron structures of the genes were conserved among tetrapods, while the genes of teleosts frequently lost their introns. Occurrence of such intron losses in teleostean hatching enzyme genes is an uncommon evolutionary event, as most eukaryotic genes are generally known to be interrupted by introns and the intron insertion sites are conserved from species to species. Here, we report on extensive studies of the exon-intron structures of teleostean hatching enzyme genes for insight into how and why introns were lost during evolution.ResultsWe investigated the evolutionary pathway of intron-losses in hatching enzyme genes of 27 species of Teleostei. Hatching enzyme genes of basal teleosts are of only one type, which conserves the 9-exon-8-intron structure of an assumed ancestor. On the other hand, otocephalans and euteleosts possess two types of hatching enzyme genes, suggesting a gene duplication event in the common ancestor of otocephalans and euteleosts. The duplicated genes were classified into two clades, clades I and II, based on phylogenetic analysis. In otocephalans and euteleosts, clade I genes developed a phylogeny-specific structure, such as an 8-exon-7-intron, 5-exon-4-intron, 4-exon-3-intron or intron-less structure. In contrast to the clade I genes, the structures of clade II genes were relatively stable in their configuration, and were similar to that of the ancestral genes. Expression analyses revealed that hatching enzyme genes were high-expression genes, when compared to that of housekeeping genes. When expression levels were compared between clade I and II genes, clade I genes tends to be expressed more highly than clade II genes.ConclusionsHatching enzyme genes evolved to lose their introns, and the intron-loss events occurred at the specific points of teleostean phylogeny. We propose that the high-expression hatching enzyme genes frequently lost their introns during the evolution of teleosts, while the low-expression genes maintained the exon-intron structure of the ancestral gene.

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“…At hatching, a proteolytic enzyme called hatching enzyme is secreted by the embryo into the perivitelline space and digests the egg envelope. The hatching enzyme cDNAs have been isolated from many vertebrates, including teleostei (masu salmon, Oncorhynchus masou (Inohaya et al, ); yellow‐tailed damsel, Chrysiptera parasema (Olivotto et al, ); Japanese eel, Anguilla japonica (Hiroi et al, ); and mummichog Fundulus heteroclitus (Kawaguchi et al, )), amphibians (frog, Xenopus laevis (Katagiri et al, )), birds (Japanese quail, Coturnix japonica (Yasumasu et al, )), and reptiles (turtle, Pelodiscus sinensis (Yasumasu et al, )). All the previously cloned vertebrate hatching enzymes belong to the astacin metalloprotease family, which comprises about 200 amino acids (with two active site consensus motifs, HExxHxxGFxHExxRxDR and SxMHY).…”

mentioning

confidence: 99%

“…eel, Anguilla japonica (Hiroi et al, 2004); and mummichog Fundulus heteroclitus (Kawaguchi et al, 2005)), amphibians (frog, Xenopus laevis (Katagiri et al,'97)), birds (Japanese quail, Coturnix japonica ), and reptiles (turtle, Pelodiscus sinensis (Yasumasu et al, 2010a)). All the previously cloned vertebrate hatching enzymes belong to the astacin metalloprotease family, which comprises about 200 amino acids (with two active site consensus motifs, HExxHxxGFxHExxRxDR and SxMHY).…”

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confidence: 99%

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

et al. 2015

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We investigated the evolution of the hatching enzyme gene using bester sturgeon (hybrid of Acipencer ruthenus and Huso huso), a basal member of ray-finned fishes. We purified the bester hatching enzyme from hatching liquid, yielding a single band on SDS-PAGE, then isolated its cDNA from embryos by PCR. The sturgeon hatching enzyme consists of an astacin family protease domain and a CUB domain. The CUB domains are present in frog and bird hatching enzymes, but not in teleostei, suggesting that the domain structure of sturgeon hatching enzyme is the tetrapod type. The purified hatching enzyme swelled the egg envelope, and selectively cleaved one of five egg envelope proteins, ZPAX. Xenopus hatching enzyme preferentially digests ZPAX, thus, the egg envelope digestion process is conserved between amphibians and basal ray-finned fish. Teleostei hatching enzymes cleave the repeat sequences at the N-terminal region of ZPB and ZPC, suggesting that the targets of the teleostei hatching enzymes differ from those of amphibians and sturgeons. Such repeat sequences were not found in the N-terminal region of ZPB and ZPC of amphibians and sturgeons. Our results suggest that the change in substrates of the hatching enzymes was accompanied by the mutation of the amino acid sequence of N-terminal regions of ZPB and ZPC. We conclude that the changes in the mechanism of egg envelope digestion, including the change in the domain structure of the hatching enzymes and the switch in substrate, occurred during the evolution of teleostei, likely triggered by the teleost-specific third whole genome duplication. J. Exp. Zool. (Mol. Dev. Evol.) 324B: 720-732, 2015. © 2015 Wiley Periodicals, Inc.

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Hatching mechanism of the Chinese soft-shelled turtle Pelodiscus sinensis

Cited by 18 publications

References 39 publications

Hatching enzyme of Japanese eel Anguilla japonica and the possible evolution of the egg envelope digestion mechanism

Hatching enzyme of Japanese eel Anguilla japonica and the possible evolution of the egg envelope digestion mechanism

Intron-loss evolution of hatching enzyme genes in Teleostei

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

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