Phylogenetic analysis of the tenascin gene family: evidence of origin early in the chordate lineage

<p>Abstract</p> <p>Background</p> <p>Tenascins are a family of glycoproteins found primarily in the extracellular matrix of embryos where they help to regulate cell proliferation, adhesion and migration. In order to learn more about their origins and relationships to ea...

Full description

Bibliographic Details
Main Authors: Tucker RP, Drabikowski K, Hess JF, Ferralli J, Chiquet-Ehrismann R, Adams JC
Format: Article
Language:English
Published: BMC 2006-08-01
Series:BMC Evolutionary Biology
Online Access:http://www.biomedcentral.com/1471-2148/6/60
_version_ 1831598917593071616
author Tucker RP
Drabikowski K
Hess JF
Ferralli J
Chiquet-Ehrismann R
Adams JC
author_facet Tucker RP
Drabikowski K
Hess JF
Ferralli J
Chiquet-Ehrismann R
Adams JC
author_sort Tucker RP
collection DOAJ
description <p>Abstract</p> <p>Background</p> <p>Tenascins are a family of glycoproteins found primarily in the extracellular matrix of embryos where they help to regulate cell proliferation, adhesion and migration. In order to learn more about their origins and relationships to each other, as well as to clarify the nomenclature used to describe them, the tenascin genes of the urochordate <it>Ciona intestinalis</it>, the pufferfish <it>Tetraodon nigroviridis </it>and <it>Takifugu rubripes </it>and the frog <it>Xenopus tropicalis </it>were identified and their gene organization and predicted protein products compared with the previously characterized tenascins of amniotes.</p> <p>Results</p> <p>A single tenascin gene was identified in the genome of <it>C. intestinalis </it>that encodes a polypeptide with domain features common to all vertebrate tenascins. Both pufferfish genomes encode five tenascin genes: two tenascin-C paralogs, a tenascin-R with domain organization identical to mammalian and avian tenascin-R, a small tenascin-X with previously undescribed GK repeats, and a tenascin-W. Four tenascin genes corresponding to tenascin-C, tenascin-R, tenascin-X and tenascin-W were also identified in the <it>X. tropicalis </it>genome. Multiple sequence alignment reveals that differences in the size of tenascin-W from various vertebrate classes can be explained by duplications of specific fibronectin type III domains. The duplicated domains are encoded on single exons and contain putative integrin-binding motifs. A phylogenetic tree based on the predicted amino acid sequences of the fibrinogen-related domains demonstrates that tenascin-C and tenascin-R are the most closely related vertebrate tenascins, with the most conserved repeat and domain organization. Taking all lines of evidence together, the data show that the tenascins referred to as tenascin-Y and tenascin-N are actually members of the tenascin-X and tenascin-W gene families, respectively.</p> <p>Conclusion</p> <p>The presence of a tenascin gene in urochordates but not other invertebrate phyla suggests that tenascins may be specific to chordates. Later genomic duplication events led to the appearance of four family members in vertebrates: tenascin-C, tenascin-R, tenascin-W and tenascin-X.</p>
first_indexed 2024-12-18T14:14:26Z
format Article
id doaj.art-3f22a4bf179f402197de7ab568c5e5f3
institution Directory Open Access Journal
issn 1471-2148
language English
last_indexed 2024-12-18T14:14:26Z
publishDate 2006-08-01
publisher BMC
record_format Article
series BMC Evolutionary Biology
spelling doaj.art-3f22a4bf179f402197de7ab568c5e5f32022-12-21T21:05:03ZengBMCBMC Evolutionary Biology1471-21482006-08-01616010.1186/1471-2148-6-60Phylogenetic analysis of the tenascin gene family: evidence of origin early in the chordate lineageTucker RPDrabikowski KHess JFFerralli JChiquet-Ehrismann RAdams JC<p>Abstract</p> <p>Background</p> <p>Tenascins are a family of glycoproteins found primarily in the extracellular matrix of embryos where they help to regulate cell proliferation, adhesion and migration. In order to learn more about their origins and relationships to each other, as well as to clarify the nomenclature used to describe them, the tenascin genes of the urochordate <it>Ciona intestinalis</it>, the pufferfish <it>Tetraodon nigroviridis </it>and <it>Takifugu rubripes </it>and the frog <it>Xenopus tropicalis </it>were identified and their gene organization and predicted protein products compared with the previously characterized tenascins of amniotes.</p> <p>Results</p> <p>A single tenascin gene was identified in the genome of <it>C. intestinalis </it>that encodes a polypeptide with domain features common to all vertebrate tenascins. Both pufferfish genomes encode five tenascin genes: two tenascin-C paralogs, a tenascin-R with domain organization identical to mammalian and avian tenascin-R, a small tenascin-X with previously undescribed GK repeats, and a tenascin-W. Four tenascin genes corresponding to tenascin-C, tenascin-R, tenascin-X and tenascin-W were also identified in the <it>X. tropicalis </it>genome. Multiple sequence alignment reveals that differences in the size of tenascin-W from various vertebrate classes can be explained by duplications of specific fibronectin type III domains. The duplicated domains are encoded on single exons and contain putative integrin-binding motifs. A phylogenetic tree based on the predicted amino acid sequences of the fibrinogen-related domains demonstrates that tenascin-C and tenascin-R are the most closely related vertebrate tenascins, with the most conserved repeat and domain organization. Taking all lines of evidence together, the data show that the tenascins referred to as tenascin-Y and tenascin-N are actually members of the tenascin-X and tenascin-W gene families, respectively.</p> <p>Conclusion</p> <p>The presence of a tenascin gene in urochordates but not other invertebrate phyla suggests that tenascins may be specific to chordates. Later genomic duplication events led to the appearance of four family members in vertebrates: tenascin-C, tenascin-R, tenascin-W and tenascin-X.</p>http://www.biomedcentral.com/1471-2148/6/60
spellingShingle Tucker RP
Drabikowski K
Hess JF
Ferralli J
Chiquet-Ehrismann R
Adams JC
Phylogenetic analysis of the tenascin gene family: evidence of origin early in the chordate lineage
BMC Evolutionary Biology
title Phylogenetic analysis of the tenascin gene family: evidence of origin early in the chordate lineage
title_full Phylogenetic analysis of the tenascin gene family: evidence of origin early in the chordate lineage
title_fullStr Phylogenetic analysis of the tenascin gene family: evidence of origin early in the chordate lineage
title_full_unstemmed Phylogenetic analysis of the tenascin gene family: evidence of origin early in the chordate lineage
title_short Phylogenetic analysis of the tenascin gene family: evidence of origin early in the chordate lineage
title_sort phylogenetic analysis of the tenascin gene family evidence of origin early in the chordate lineage
url http://www.biomedcentral.com/1471-2148/6/60
work_keys_str_mv AT tuckerrp phylogeneticanalysisofthetenascingenefamilyevidenceoforiginearlyinthechordatelineage
AT drabikowskik phylogeneticanalysisofthetenascingenefamilyevidenceoforiginearlyinthechordatelineage
AT hessjf phylogeneticanalysisofthetenascingenefamilyevidenceoforiginearlyinthechordatelineage
AT ferrallij phylogeneticanalysisofthetenascingenefamilyevidenceoforiginearlyinthechordatelineage
AT chiquetehrismannr phylogeneticanalysisofthetenascingenefamilyevidenceoforiginearlyinthechordatelineage
AT adamsjc phylogeneticanalysisofthetenascingenefamilyevidenceoforiginearlyinthechordatelineage