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The evolutionary conservation of the A Disintegrin-like and Metalloproteinase domain with Thrombospondin-1 motif metzincins across vertebrate species and their expression in teleost zebrafish

Identifieur interne : 000A43 ( Pmc/Curation ); précédent : 000A42; suivant : 000A44

The evolutionary conservation of the A Disintegrin-like and Metalloproteinase domain with Thrombospondin-1 motif metzincins across vertebrate species and their expression in teleost zebrafish

Auteurs : Frédéric G. Brunet [France] ; Fiona W. Fraser ; Marley J. Binder ; Adam D. Smith ; Christopher Kintakas ; Carolyn M. Dancevic ; Alister C. Ward ; Daniel R. Mcculloch

Source :

RBID : PMC:4349717

Abstract

Background

The A Disintegrin-like and Metalloproteinase domain with Thrombospondin-1 motifs (ADAMTS) enzymes comprise 19 mammalian zinc-dependent metalloproteinases (metzincins) with homologues in a wide range of invertebrates. ADAMTS enzymes have a broad range of functions in development and diseases due to their extracellular matrix remodelling activity. Here, we report a detailed characterisation of their evolutionary conservation across vertebrates.

Results

Using bioinformatics complemented with de novo sequencing, gene sequences for ADAMTS enzymes were obtained from a variety of organisms. Detailed evolutionary analyses revealed a high level of conservation across vertebrates with evidence of ADAMTS gene expansion during two rounds of whole genome duplication (WGD) in vertebrates, while tandem duplication events and gene loss were also apparent. However, the additional round of teleost-specific WGD did not have a significant effect on ADAMTS gene family members suggesting their conserved roles have remained constant in teleost fish. Quantitative reverse-transcriptase polymerase chain reaction analysis revealed dynamic expression of adamts genes throughout zebrafish embryonic development reflecting the key conserved roles they play in vertebrate embryogenesis. Notably, several adamts mRNAs were maternally expressed with a dramatic increase in mRNA levels coinciding with zygotic expression and organogenesis. Broad adamts mRNA expression was also demonstrated in several adult organs indicating potential roles in adult homeostasis.

Conclusions

Our data highlight the evolution of the ADAMTS gene family through duplication processes across metazoans supplemented by a burst of amplification through vertebrate WGD events. It also strongly posits the zebrafish as a potential model species to further elucidate the function of ADAMTS enzymes during vertebrate development.

Electronic supplementary material

The online version of this article (doi:10.1186/s12862-015-0281-9) contains supplementary material, which is available to authorized users.


Url:
DOI: 10.1186/s12862-015-0281-9
PubMed: 25879701
PubMed Central: 4349717

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Fiona W. Fraser
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Marley J. Binder
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<wicri:noCountry code="subfield">VIC 3216 Australia</wicri:noCountry>
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Adam D. Smith
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Christopher Kintakas
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Carolyn M. Dancevic
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Alister C. Ward
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Alister C. Ward
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Daniel R. Mcculloch
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Daniel R. Mcculloch
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<title>Background</title>
<p>The
<italic>A D</italic>
isintegrin-like and
<italic>M</italic>
etalloproteinase domain with
<italic>T</italic>
hrombo
<italic>s</italic>
pondin-1 motifs (ADAMTS) enzymes comprise 19 mammalian zinc-dependent metalloproteinases (metzincins) with homologues in a wide range of invertebrates. ADAMTS enzymes have a broad range of functions in development and diseases due to their extracellular matrix remodelling activity. Here, we report a detailed characterisation of their evolutionary conservation across vertebrates.</p>
</sec>
<sec>
<title>Results</title>
<p>Using bioinformatics complemented with
<italic>de novo</italic>
sequencing, gene sequences for ADAMTS enzymes were obtained from a variety of organisms. Detailed evolutionary analyses revealed a high level of conservation across vertebrates with evidence of
<italic>ADAMTS</italic>
gene expansion during two rounds of whole genome duplication (WGD) in vertebrates, while tandem duplication events and gene loss were also apparent. However, the additional round of teleost-specific WGD did not have a significant effect on
<italic>ADAMTS</italic>
gene family members suggesting their conserved roles have remained constant in teleost fish. Quantitative reverse-transcriptase polymerase chain reaction analysis revealed dynamic expression of
<italic>adamts</italic>
genes throughout zebrafish embryonic development reflecting the key conserved roles they play in vertebrate embryogenesis. Notably, several
<italic>adamts</italic>
mRNAs were maternally expressed with a dramatic increase in mRNA levels coinciding with zygotic expression and organogenesis. Broad
<italic>adamts</italic>
mRNA expression was also demonstrated in several adult organs indicating potential roles in adult homeostasis.</p>
</sec>
<sec>
<title>Conclusions</title>
<p>Our data highlight the evolution of the
<italic>ADAMTS</italic>
gene family through duplication processes across metazoans supplemented by a burst of amplification through vertebrate WGD events. It also strongly posits the zebrafish as a potential model species to further elucidate the function of ADAMTS enzymes during vertebrate development.</p>
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<p>The online version of this article (doi:10.1186/s12862-015-0281-9) contains supplementary material, which is available to authorized users.</p>
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<journal-id journal-id-type="nlm-ta">BMC Evol Biol</journal-id>
<journal-id journal-id-type="iso-abbrev">BMC Evol. Biol</journal-id>
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<journal-title>BMC Evolutionary Biology</journal-title>
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<issn pub-type="epub">1471-2148</issn>
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<publisher-name>BioMed Central</publisher-name>
<publisher-loc>London</publisher-loc>
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<article-id pub-id-type="pmid">25879701</article-id>
<article-id pub-id-type="pmc">4349717</article-id>
<article-id pub-id-type="publisher-id">281</article-id>
<article-id pub-id-type="doi">10.1186/s12862-015-0281-9</article-id>
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<subject>Research Article</subject>
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</article-categories>
<title-group>
<article-title>The evolutionary conservation of the A Disintegrin-like and Metalloproteinase domain with Thrombospondin-1 motif metzincins across vertebrate species and their expression in teleost zebrafish</article-title>
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<email>mjbin@deakin.edu.au</email>
</address>
<xref ref-type="aff" rid="Aff2"></xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Smith</surname>
<given-names>Adam D</given-names>
</name>
<address>
<email>damnitsham@hotmail.com</email>
</address>
<xref ref-type="aff" rid="Aff2"></xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Kintakas</surname>
<given-names>Christopher</given-names>
</name>
<address>
<email>cki@deakin.edu.au</email>
</address>
<xref ref-type="aff" rid="Aff2"></xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Dancevic</surname>
<given-names>Carolyn M</given-names>
</name>
<address>
<email>cmdan@deakin.edu.au</email>
</address>
<xref ref-type="aff" rid="Aff2"></xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Ward</surname>
<given-names>Alister C</given-names>
</name>
<address>
<email>alister.ward@deakin.edu.au</email>
</address>
<xref ref-type="aff" rid="Aff2"></xref>
<xref ref-type="aff" rid="Aff3"></xref>
</contrib>
<contrib contrib-type="author" corresp="yes">
<name>
<surname>McCulloch</surname>
<given-names>Daniel R</given-names>
</name>
<address>
<email>daniel.mcculloch@deakin.edu.au</email>
</address>
<xref ref-type="aff" rid="Aff2"></xref>
<xref ref-type="aff" rid="Aff3"></xref>
</contrib>
<aff id="Aff1">
<label></label>
Institut de Génomique Fonctionnelle de Lyon, Université de Lyon, Université Lyon 1, CNRS, Ecole Normale Supérieure de Lyon, 46, allée d’Italie, 69364 Lyon cedex 07, France</aff>
<aff id="Aff2">
<label></label>
School of Medicine, Deakin University, Geelong, VIC 3216 Australia</aff>
<aff id="Aff3">
<label></label>
Molecular and Medical Research Strategic Research Centre, Deakin University, Geelong, VIC 3216 Australia</aff>
</contrib-group>
<pub-date pub-type="epub">
<day>15</day>
<month>2</month>
<year>2015</year>
</pub-date>
<pub-date pub-type="pmc-release">
<day>15</day>
<month>2</month>
<year>2015</year>
</pub-date>
<pub-date pub-type="collection">
<year>2015</year>
</pub-date>
<volume>15</volume>
<elocation-id>22</elocation-id>
<history>
<date date-type="received">
<day>14</day>
<month>7</month>
<year>2014</year>
</date>
<date date-type="accepted">
<day>5</day>
<month>1</month>
<year>2015</year>
</date>
</history>
<permissions>
<copyright-statement>© Brunet et al.; licensee BioMed Central. 2015</copyright-statement>
<license license-type="open-access">
<license-p>This is an Open Access article distributed under the terms of the Creative Commons Attribution License (
<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0">http://creativecommons.org/licenses/by/4.0</ext-link>
), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (
<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/publicdomain/zero/1.0/">http://creativecommons.org/publicdomain/zero/1.0/</ext-link>
) applies to the data made available in this article, unless otherwise stated.</license-p>
</license>
</permissions>
<abstract id="Abs1">
<sec>
<title>Background</title>
<p>The
<italic>A D</italic>
isintegrin-like and
<italic>M</italic>
etalloproteinase domain with
<italic>T</italic>
hrombo
<italic>s</italic>
pondin-1 motifs (ADAMTS) enzymes comprise 19 mammalian zinc-dependent metalloproteinases (metzincins) with homologues in a wide range of invertebrates. ADAMTS enzymes have a broad range of functions in development and diseases due to their extracellular matrix remodelling activity. Here, we report a detailed characterisation of their evolutionary conservation across vertebrates.</p>
</sec>
<sec>
<title>Results</title>
<p>Using bioinformatics complemented with
<italic>de novo</italic>
sequencing, gene sequences for ADAMTS enzymes were obtained from a variety of organisms. Detailed evolutionary analyses revealed a high level of conservation across vertebrates with evidence of
<italic>ADAMTS</italic>
gene expansion during two rounds of whole genome duplication (WGD) in vertebrates, while tandem duplication events and gene loss were also apparent. However, the additional round of teleost-specific WGD did not have a significant effect on
<italic>ADAMTS</italic>
gene family members suggesting their conserved roles have remained constant in teleost fish. Quantitative reverse-transcriptase polymerase chain reaction analysis revealed dynamic expression of
<italic>adamts</italic>
genes throughout zebrafish embryonic development reflecting the key conserved roles they play in vertebrate embryogenesis. Notably, several
<italic>adamts</italic>
mRNAs were maternally expressed with a dramatic increase in mRNA levels coinciding with zygotic expression and organogenesis. Broad
<italic>adamts</italic>
mRNA expression was also demonstrated in several adult organs indicating potential roles in adult homeostasis.</p>
</sec>
<sec>
<title>Conclusions</title>
<p>Our data highlight the evolution of the
<italic>ADAMTS</italic>
gene family through duplication processes across metazoans supplemented by a burst of amplification through vertebrate WGD events. It also strongly posits the zebrafish as a potential model species to further elucidate the function of ADAMTS enzymes during vertebrate development.</p>
</sec>
<sec>
<title>Electronic supplementary material</title>
<p>The online version of this article (doi:10.1186/s12862-015-0281-9) contains supplementary material, which is available to authorized users.</p>
</sec>
</abstract>
<kwd-group xml:lang="en">
<title>Keywords</title>
<kwd>ADAMTS</kwd>
<kwd>Evolution</kwd>
<kwd>Whole genome duplications</kwd>
<kwd>Vertebrata</kwd>
<kwd>Metazoa</kwd>
<kwd>Zebrafish</kwd>
<kwd>Development</kwd>
<kwd>Gene expression</kwd>
</kwd-group>
<custom-meta-group>
<custom-meta>
<meta-name>issue-copyright-statement</meta-name>
<meta-value>© The Author(s) 2015</meta-value>
</custom-meta>
</custom-meta-group>
</article-meta>
</front>
</pmc>
</record>

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