Retention of duplicated ITAM-containing transmembrane signaling subunits in the tetraploid amphibian species Xenopus laevis
The ITAM-bearing transmembrane signaling subunits (TSS) are indispensable components of activating leukocyte receptor complexes. The TSS-encoding genes map to paralogous chromosomal regions, which are thought to arise from ancient genome tetraploidization(s). To assess a possible role of tetraploidi...
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Veröffentlicht in: | Developmental and comparative immunology 2015-11, Vol.53 (1), p.158-168 |
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creator | Guselnikov, S.V. Grayfer, L. De Jesús Andino, F. Rogozin, I.B. Robert, J. Taranin, A.V. |
description | The ITAM-bearing transmembrane signaling subunits (TSS) are indispensable components of activating leukocyte receptor complexes. The TSS-encoding genes map to paralogous chromosomal regions, which are thought to arise from ancient genome tetraploidization(s). To assess a possible role of tetraploidization in the TSS evolution, we studied TSS and other functionally linked genes in the amphibian species Xenopus laevis whose genome was duplicated about 40 MYR ago. We found that X. laevis has retained a duplicated set of sixteen TSS genes, all except one being transcribed. Furthermore, duplicated TCRα loci and genes encoding TSS-coupling protein kinases have also been retained. No clear evidence for functional divergence of the TSS paralogs was obtained from gene expression and sequence analyses. We suggest that the main factor of maintenance of duplicated TSS genes in X. laevis was a protein dosage effect and that this effect might have facilitated the TSS set expansion in early vertebrates.
•Duplicated genes for ITAM-bearing subunits are retained in tetraploid X. laevis.•The retention is suggested to be due to a protein dosage effect.•There are two functional TCRa loci in the X. laevis genome.•Ancient WGDs might have contributed to the evolution of ITAM-bearing subunits. |
doi_str_mv | 10.1016/j.dci.2015.07.002 |
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•Duplicated genes for ITAM-bearing subunits are retained in tetraploid X. laevis.•The retention is suggested to be due to a protein dosage effect.•There are two functional TCRa loci in the X. laevis genome.•Ancient WGDs might have contributed to the evolution of ITAM-bearing subunits.</description><identifier>ISSN: 0145-305X</identifier><identifier>EISSN: 1879-0089</identifier><identifier>DOI: 10.1016/j.dci.2015.07.002</identifier><identifier>PMID: 26170006</identifier><language>eng</language><publisher>United States: Elsevier Ltd</publisher><subject>Activating receptor complexes ; Amino Acid Sequence ; Animals ; Base Sequence ; Cell Line ; Evolution, Molecular ; Genome mining ; HEK293 Cells ; Humans ; Immunogenetics ; Immunoreceptor Tyrosine-Based Activation Motif - genetics ; Molecular Sequence Data ; Protein dosage effect ; Receptors, Antigen, T-Cell, alpha-beta - genetics ; Receptors, Antigen, T-Cell, alpha-beta - immunology ; Receptors, IgG - genetics ; Receptors, IgG - immunology ; Sequence Alignment ; Signal Transduction - genetics ; Signal Transduction - immunology ; TCR ; Tetraploidization ; Tetraploidy ; Xenopus ; Xenopus laevis</subject><ispartof>Developmental and comparative immunology, 2015-11, Vol.53 (1), p.158-168</ispartof><rights>2015</rights><rights>Published by Elsevier Ltd.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c403t-d1e80764e60b31ac4c73b4bf5a498e3726c2a756b065a8fb4451ae5b30d23f9e3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.dci.2015.07.002$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>230,314,780,784,885,3550,27924,27925,45995</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26170006$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Guselnikov, S.V.</creatorcontrib><creatorcontrib>Grayfer, L.</creatorcontrib><creatorcontrib>De Jesús Andino, F.</creatorcontrib><creatorcontrib>Rogozin, I.B.</creatorcontrib><creatorcontrib>Robert, J.</creatorcontrib><creatorcontrib>Taranin, A.V.</creatorcontrib><title>Retention of duplicated ITAM-containing transmembrane signaling subunits in the tetraploid amphibian species Xenopus laevis</title><title>Developmental and comparative immunology</title><addtitle>Dev Comp Immunol</addtitle><description>The ITAM-bearing transmembrane signaling subunits (TSS) are indispensable components of activating leukocyte receptor complexes. The TSS-encoding genes map to paralogous chromosomal regions, which are thought to arise from ancient genome tetraploidization(s). To assess a possible role of tetraploidization in the TSS evolution, we studied TSS and other functionally linked genes in the amphibian species Xenopus laevis whose genome was duplicated about 40 MYR ago. We found that X. laevis has retained a duplicated set of sixteen TSS genes, all except one being transcribed. Furthermore, duplicated TCRα loci and genes encoding TSS-coupling protein kinases have also been retained. No clear evidence for functional divergence of the TSS paralogs was obtained from gene expression and sequence analyses. We suggest that the main factor of maintenance of duplicated TSS genes in X. laevis was a protein dosage effect and that this effect might have facilitated the TSS set expansion in early vertebrates.
•Duplicated genes for ITAM-bearing subunits are retained in tetraploid X. laevis.•The retention is suggested to be due to a protein dosage effect.•There are two functional TCRa loci in the X. laevis genome.•Ancient WGDs might have contributed to the evolution of ITAM-bearing subunits.</description><subject>Activating receptor complexes</subject><subject>Amino Acid Sequence</subject><subject>Animals</subject><subject>Base Sequence</subject><subject>Cell Line</subject><subject>Evolution, Molecular</subject><subject>Genome mining</subject><subject>HEK293 Cells</subject><subject>Humans</subject><subject>Immunogenetics</subject><subject>Immunoreceptor Tyrosine-Based Activation Motif - genetics</subject><subject>Molecular Sequence Data</subject><subject>Protein dosage effect</subject><subject>Receptors, Antigen, T-Cell, alpha-beta - genetics</subject><subject>Receptors, Antigen, T-Cell, alpha-beta - immunology</subject><subject>Receptors, IgG - genetics</subject><subject>Receptors, IgG - immunology</subject><subject>Sequence Alignment</subject><subject>Signal Transduction - genetics</subject><subject>Signal Transduction - immunology</subject><subject>TCR</subject><subject>Tetraploidization</subject><subject>Tetraploidy</subject><subject>Xenopus</subject><subject>Xenopus laevis</subject><issn>0145-305X</issn><issn>1879-0089</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kV9rFDEUxYModq1-AF8kj77MejP5M7MIQilqCxVBKvQtJJk7u1lmknGSWSh-ebNsW_TFvFyS_O65yTmEvGWwZsDUh_26c35dA5NraNYA9TOyYm2zqQDazXOyAiZkxUHenZFXKe2hrJbBS3JWK9aUjVqR3z8wY8g-Bhp72i3T4J3J2NHr24tvlYshGx982NI8m5BGHG2pSJPfBjMcz9Nil-Bzoj7QvEOasZDTEH1HzTjtvPUm0DSh85joHYY4LYkOBg8-vSYvejMkfPNQz8nPL59vL6-qm-9fry8vbiongOeqY9hCowQqsJwZJ1zDrbC9NGLTIm9q5WrTSGVBSdP2VgjJDErLoat5v0F-Tj6ddKfFjti58t_ZDHqa_Wjmex2N1__eBL_T23jQQnLFalYE3j8IzPHXginr0SeHw1CsiEvSxUzBhQIJBWUn1M0xpRn7pzEM9DE0vdclNH0MTUOjS2il593f73vqeEypAB9PABaXDh5nnYqdwWHnZ3RZd9H_R_4P7BCrZQ</recordid><startdate>20151101</startdate><enddate>20151101</enddate><creator>Guselnikov, S.V.</creator><creator>Grayfer, L.</creator><creator>De Jesús Andino, F.</creator><creator>Rogozin, I.B.</creator><creator>Robert, J.</creator><creator>Taranin, A.V.</creator><general>Elsevier Ltd</general><scope>6I.</scope><scope>AAFTH</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20151101</creationdate><title>Retention of duplicated ITAM-containing transmembrane signaling subunits in the tetraploid amphibian species Xenopus laevis</title><author>Guselnikov, S.V. ; Grayfer, L. ; De Jesús Andino, F. ; Rogozin, I.B. ; Robert, J. ; Taranin, A.V.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c403t-d1e80764e60b31ac4c73b4bf5a498e3726c2a756b065a8fb4451ae5b30d23f9e3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Activating receptor complexes</topic><topic>Amino Acid Sequence</topic><topic>Animals</topic><topic>Base Sequence</topic><topic>Cell Line</topic><topic>Evolution, Molecular</topic><topic>Genome mining</topic><topic>HEK293 Cells</topic><topic>Humans</topic><topic>Immunogenetics</topic><topic>Immunoreceptor Tyrosine-Based Activation Motif - genetics</topic><topic>Molecular Sequence Data</topic><topic>Protein dosage effect</topic><topic>Receptors, Antigen, T-Cell, alpha-beta - genetics</topic><topic>Receptors, Antigen, T-Cell, alpha-beta - immunology</topic><topic>Receptors, IgG - genetics</topic><topic>Receptors, IgG - immunology</topic><topic>Sequence Alignment</topic><topic>Signal Transduction - genetics</topic><topic>Signal Transduction - immunology</topic><topic>TCR</topic><topic>Tetraploidization</topic><topic>Tetraploidy</topic><topic>Xenopus</topic><topic>Xenopus laevis</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Guselnikov, S.V.</creatorcontrib><creatorcontrib>Grayfer, L.</creatorcontrib><creatorcontrib>De Jesús Andino, F.</creatorcontrib><creatorcontrib>Rogozin, I.B.</creatorcontrib><creatorcontrib>Robert, J.</creatorcontrib><creatorcontrib>Taranin, A.V.</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Developmental and comparative immunology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Guselnikov, S.V.</au><au>Grayfer, L.</au><au>De Jesús Andino, F.</au><au>Rogozin, I.B.</au><au>Robert, J.</au><au>Taranin, A.V.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Retention of duplicated ITAM-containing transmembrane signaling subunits in the tetraploid amphibian species Xenopus laevis</atitle><jtitle>Developmental and comparative immunology</jtitle><addtitle>Dev Comp Immunol</addtitle><date>2015-11-01</date><risdate>2015</risdate><volume>53</volume><issue>1</issue><spage>158</spage><epage>168</epage><pages>158-168</pages><issn>0145-305X</issn><eissn>1879-0089</eissn><abstract>The ITAM-bearing transmembrane signaling subunits (TSS) are indispensable components of activating leukocyte receptor complexes. The TSS-encoding genes map to paralogous chromosomal regions, which are thought to arise from ancient genome tetraploidization(s). To assess a possible role of tetraploidization in the TSS evolution, we studied TSS and other functionally linked genes in the amphibian species Xenopus laevis whose genome was duplicated about 40 MYR ago. We found that X. laevis has retained a duplicated set of sixteen TSS genes, all except one being transcribed. Furthermore, duplicated TCRα loci and genes encoding TSS-coupling protein kinases have also been retained. No clear evidence for functional divergence of the TSS paralogs was obtained from gene expression and sequence analyses. We suggest that the main factor of maintenance of duplicated TSS genes in X. laevis was a protein dosage effect and that this effect might have facilitated the TSS set expansion in early vertebrates.
•Duplicated genes for ITAM-bearing subunits are retained in tetraploid X. laevis.•The retention is suggested to be due to a protein dosage effect.•There are two functional TCRa loci in the X. laevis genome.•Ancient WGDs might have contributed to the evolution of ITAM-bearing subunits.</abstract><cop>United States</cop><pub>Elsevier Ltd</pub><pmid>26170006</pmid><doi>10.1016/j.dci.2015.07.002</doi><tpages>11</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Activating receptor complexes Amino Acid Sequence Animals Base Sequence Cell Line Evolution, Molecular Genome mining HEK293 Cells Humans Immunogenetics Immunoreceptor Tyrosine-Based Activation Motif - genetics Molecular Sequence Data Protein dosage effect Receptors, Antigen, T-Cell, alpha-beta - genetics Receptors, Antigen, T-Cell, alpha-beta - immunology Receptors, IgG - genetics Receptors, IgG - immunology Sequence Alignment Signal Transduction - genetics Signal Transduction - immunology TCR Tetraploidization Tetraploidy Xenopus Xenopus laevis |
title | Retention of duplicated ITAM-containing transmembrane signaling subunits in the tetraploid amphibian species Xenopus laevis |
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