Amino acid sequence of a unique protease from the crayfish Astacus fluviatilis

Titani, Koiti; Torff, Hans Joachim; Hormel, Scott; Kumar, Santosh; Walsh, Kenneth A.; Rödl, Josef; Neurath, Hans; Zwilling, Robert

doi:10.1021/bi00375a029

Cited by 105 publications

(71 citation statements)

References 16 publications

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“…Recent studies have characterized multiple tissue-specific astacin proteins in a variety of organisms from crayfish to mammals. The astacin gene family includes digestive enzymes (18), hatching enzymes (19,20), bone morphogenic proteins (21), meprins (22), and the recently discovered proteins cimp1 (23) and nephrosin (24), which are expressed in the gills and kidney of bony fishes. We obtained the complete coding sequence of patristacin from the brood pouches of pregnant male S. scovelli, Syngnathus rostellatus, and Syngnathus acus, as well as representative sequences from the kidney and liver of several syngnathids and other fishes ( Table 1, which is published as supporting information on the PNAS web site).…”

Section: Resultsmentioning

confidence: 99%

Gene cooption without duplication during the evolution of a male-pregnancy gene in pipefish

Harlin-Cognato

Hoffman

Jones

2006

Proc. Natl. Acad. Sci. U.S.A.

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Comparative studies of developmental processes suggest that novel traits usually evolve through the cooption of preexisting genes and proteins, mainly via gene duplication and functional specialization of paralogs. However, an alternative hypothesis is that novel protein function can evolve without gene duplication, through changes in the spatiotemporal patterns of gene expression (e.g., via cis-regulatory elements), or functional modifications (e.g., addition of functional domains) of the proteins they encode, or both. Here we present an astacin metalloprotease, dubbed patristacin, which has been coopted without duplication, via alteration in the expression of a preexisting gene from the kidney and liver of bony fishes, for a novel role in the brood pouch of pregnant male pipefish. We examined the molecular evolution of patristacin and found conservation of astacin-specific motifs but also several positively selected amino acids that may represent functional modifications for male pregnancy. Overall, our results pinpoint a clear case in which gene cooption occurred without gene duplication during the genesis of an evolutionarily significant novel structure, the male brood pouch. These findings contribute to a growing understanding of morphological innovation, a critically important but poorly understood process in evolutionary biology.novel trait evolution ͉ patristacin ͉ Syngnathidae E volutionary innovation has been defined as ''the origin of a novel body part which may serve a novel function or specialize in a function that was already performed in the ancestral lineage but without a dedicated organ' ' (ref. 1, p. 581). In seahorses and pipefishes (family Syngnathidae) males carry their embryos on their ventral surface, either exposed to the environment or enclosed in a fleshy brood pouch (Fig. 1). The brood pouch is a clear example of an evolutionary innovation: syngnathids are the only lineage to have evolved a morphological structure that allows males to become pregnant. In many species of syngnathid fishes, the brood pouch is a complex organ composed of highly vascularized epithelial tissue that forms a honeycomb matrix encapsulating individual eggs during gestation ( Fig. 1) (2). This placenta-like tissue apparently supplies nutrients to developing embryos (3) in a manner analogous to the placenta of female mammals. The pouch is lined with cells rich in mitochondria (CRMs) (Fig. 1) (2, 4) that transfer ions between the brood pouch fluid and the male bloodstream, maintaining an osmotically neutral environment during the early stages of gestation (4-6). A phylogeny of the Syngnathidae suggests two independent origins of the brood pouch based on its location on either the abdomen (Gastrophori) or the tail (Urophori) of the male (7), and within these two lineages there is considerable variation in the degree to which the pouch encloses developing embryos, the complexity of the ''pseudoplacenta,'' and the structure of brood pouch folds (7).Clearly, the evolution of a structure as complex as a brood pouch req...

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Section: Resultsmentioning

confidence: 99%

Gene cooption without duplication during the evolution of a male-pregnancy gene in pipefish

Harlin-Cognato

Hoffman

Jones

2006

Proc. Natl. Acad. Sci. U.S.A.

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“…were deduced from cDNA sequences except for astacin in which the protease domain sequence was determined from the mature protein and the prepro sequence deduced from the cDNA. References: astacin, Titani et al (1987); HCEI, HCE2, and LCE, Yasumasu et al (1994); QuCAM-I, Elaroussi and DeLuca (1994); HMPI, Sarras (pers. comm.…”

Section: Js Bond and R J Beynonmentioning

confidence: 99%

“…The original members of the family identified were: the crayfish digestive enzyme astacin, bone morphogenetic protein-I (BMP-1) from human bone, meprins from mouse kidney and human intestine (the latter was originally designated as N-benzoyl-L-tyrosyl-p-aminobenzoic acid hydrolase or PPH), and UVS.2, a partial sequence from Xenopus laevis embryos. The family was named the "astacin family" because a protease from the crayfish Astacus astacus L., the enzyme now called astacin (EC 3.4.24.21), was the first to be sequenced and biochemically characterized (Titani et al, 1987). It has subsequently been crystallized and the three-dimensional structure solved, adding a new dimension to our understanding and exploration of these metalloendopeptidases (Bode et al, 1992).…”

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confidence: 99%

The astacin family of metalloendopeptidases

1995

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The astacin family of metalloendopeptidases was recognized as a novel family of proteases in the 1990s. The crayfish enzyme astacin was the first characterized and is one of the smallest members of the family. More than 20 members of the family have now been identified. They have been detected in species ranging from hydra to humans, in mature and in developmental systems. Proposed functions of these proteases include activation of growth factors, degradation of polypeptides, and processing of extracellular proteins. Astacin family proteases are synthesized with NH,-terminal signal and proenzyme sequences, and many (such as meprins, BMP-1, folloid) contain multiple domains COOH-terminal to the protease domain. They are either secreted from cells or are plasma membrane-associated enzymes. They have some distinguishing features in addition to the signature sequence in the protease domain: HEXXHXXGFXHEXXRXDR. They have a unique type of zinc binding, with pentacoordination, and a protease domain tertiary structure that contains common attributes with serralysins, matrix metalloendopeptidases, and snake venom proteases; they cleave peptide bonds in polypeptides such as insulin B chain and bradykinin and in proteins such as casein and gelatin; and they have arylamidase activity. Meprins are unique proteases in the astacin family, and indeed in the animal kingdom, in their oligomeric structure; they are dimers of disulfide-linked dimers and are highly glycosylated, type I integral membrane proteins that have many attributes of receptors or integrins with adhesion, epidermal growth factor-like, and transmembrane domains. The 01 and /3 subunits are differentially expressed and processed to yield latent and active proteases as well as membraneassociated and secreted forms. Meprins represent excellent models of hetero-and homo-oligomeric enzymes that are regulated at the transcriptional and posttranslational levels.

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“…Matrixins: collagenase n, collagenase from human neutrophil granulocytes (Hasty et al, 1990); matrilysin, human punctuated (or putative) matrix metalloproteinase, PUMP1 (Muller et al, 1988;Quantin et al, 1989); stromelysin, human stromelysin 1 (Whitham et al, 1986). Astacins: astacin from crayfish (Titani et al, 1987); meprin a from mouse kidney ; BMPl, human bone morphogenetic protein 1 (Wozney et al, 1988). Alignments were established by the program CLUSTAL (implemented in the software package HUSAR at the German Cancer Research Center Biocomputing Facility, Heidelberg) and corrected on the basis of topological similarity using the program OVRLAP (Rossmann & Argos, 1975 …”

Section: The Northern Wall Of the Active Site Cleftmentioning

confidence: 99%

The metzincins — Topological and sequential relations between the astacins, adamalysins, serralysins, and matrixins (collagenases) define a super family of zinc‐peptidases

et al. 1995

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The three-dimensional structures of the zinc endopeptidases human neutrophil collagenase, adamalysin I1 from rattle snake venom, alkaline proteinase from Pseudomonas aeruginosa, and astacin from crayfish are topologically similar, with respect to a five-stranded 0-sheet and three a-helices arranged in typical sequential order. The four proteins exhibit the characteristic consensus motif HEXXHXXGXXH, whose three histidine residues are involved in binding of the catalytically essential zinc ion. Moreover, they all share a conserved methionine residue beneath the active site metal as part of a superimposable "Met-turn.'' This structural relationship is supported by a sequence alignment performed on the basis of topological equivalence showing faint but distinct sequential similarity. The alkaline proteinase is about equally distant (26% sequence identity) to both human neutrophil collagenase and astacin and a little further away from adamalysin I1 (17% identity). The pairs astacin/adamalysin 11, astacidhuman neutrophil collagenase, and adamalysin Whuman neutrophil collagenase exhibit sequence identities of 16%, 14%, and 13%, respectively. Therefore, the corresponding four distinct families of zinc peptidases, the astacins, the matrix metalloproteinases (matrixins, collagenases), the adamalysins/reprolysins (snake venom proteinases/reproductive tract proteins), and the serralysins (large bacterial proteases from Serratia, Erwinia, and Pseudomonas) appear to have originated by divergent evolution from a common ancestor and form a superfamily of proteolytic enzymes for which the designation "metzincins" has been proposed. There is also a faint but significant structural relationship of the metzincins to the thermolysin-like enzymes, which share the truncated zincbinding motif HEXXH and, moreover, similar topologies in their N-terminal domains.Keywords: crystal structure; metalloproteinase; molecular evolution; protein family; sequence alignment; topology is involved in metal binding (McKerrow, 1987;

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Amino acid sequence of a unique protease from the crayfish Astacus fluviatilis

Cited by 105 publications

References 16 publications

Gene cooption without duplication during the evolution of a male-pregnancy gene in pipefish

Gene cooption without duplication during the evolution of a male-pregnancy gene in pipefish

The astacin family of metalloendopeptidases

The metzincins — Topological and sequential relations between the astacins, adamalysins, serralysins, and matrixins (collagenases) define a super family of zinc‐peptidases

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