Functional-genomic analysis reveals intraspecies diversification of antiviral receptor transporter proteins in Xenopus laevis
The Receptor Transporter Protein (RTP) family is present in most, if not all jawed vertebrates. Most of our knowledge of this protein family comes from studies on mammalian RTPs, which are multi-function proteins that regulate cell-surface G-protein coupled receptor levels, influence olfactory syste...
Gespeichert in:
| Veröffentlicht in: | PLoS genetics 2021-05, Vol.17 (5), p.e1009578-e1009578 |
|---|---|
| Hauptverfasser: | , , |
| Format: | Artikel |
| Sprache: | eng |
| Schlagworte: | |
| Online-Zugang: | Volltext |
| Tags: |
Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
|
| container_end_page | e1009578 |
|---|---|
| container_issue | 5 |
| container_start_page | e1009578 |
| container_title | PLoS genetics |
| container_volume | 17 |
| creator | Boys, Ian N Mar, Katrina B Schoggins, John W |
| description | The Receptor Transporter Protein (RTP) family is present in most, if not all jawed vertebrates. Most of our knowledge of this protein family comes from studies on mammalian RTPs, which are multi-function proteins that regulate cell-surface G-protein coupled receptor levels, influence olfactory system development, regulate immune signaling, and directly inhibit viral infection. However, mammals comprise less than one-tenth of extant vertebrate species, and our knowledge about the expression, function, and evolution of non-mammalian RTPs is limited. Here, we explore the evolutionary history of RTPs in vertebrates. We identify signatures of positive selection in many vertebrate RTP clades and characterize multiple, independent expansions of the RTP family outside of what has been described in mammals. We find a striking expansion of RTPs in the African clawed frog, Xenopus laevis, with 11 RTPs in this species as opposed to 1 to 4 in most other species. RNA sequencing revealed that most X. laevis RTPs are upregulated following immune stimulation. In functional assays, we demonstrate that at least three of these X. laevis RTPs inhibit infection by RNA viruses, suggesting that RTP homologs may serve as antiviral effectors outside of Mammalia. |
| doi_str_mv | 10.1371/journal.pgen.1009578 |
| format | Article |
| fullrecord | <record><control><sourceid>gale_plos_</sourceid><recordid>TN_cdi_plos_journals_2541857500</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><galeid>A663949196</galeid><doaj_id>oai_doaj_org_article_309332d5739d4b7e85809bea8e8c4852</doaj_id><sourcerecordid>A663949196</sourcerecordid><originalsourceid>FETCH-LOGICAL-c726t-e8b0d66966095355b899ce4e5ee4eda49ad9198b224d54be601b6dd3edf674a43</originalsourceid><addsrcrecordid>eNqVk12L1DAUhoso7jr6D0QLgujFjEnz0eRGWBZXBxYX_MK7kCanMxk6TU3awb3wv5s63WVG9kIptGn6vO_pOTkny55itMCkxG82fgitbhbdCtoFRkiyUtzLTjFjZF5SRO8frE-yRzFuECJMyPJhdkIowlQW7DT7dTG0pnc-Oc2Tkd86k-v0ch1dzAPsQDcxd20fdOzAOIi5dTsI0dXO6FGX-zoJerdzQTdJYaDrfciToI2dDz2EvAu-B9eOPvn3FKMbYt5o2Ln4OHtQpwDwZHrOsq8X776cf5hfXr1fnp9dzk1Z8H4OokKWc8l5ypIwVgkpDVBgkG5WU6mtxFJURUEtoxVwhCtuLQFb85JqSmbZ871v1_iopspFVTCKBStZKswsW-4J6_VGdcFtdbhWXjv1Z8OHldKhd6YBRZAkpLCsJNLSqgTBBJIVaAHCUMGK5PV2ijZUW7AGxvI1R6bHX1q3Viu_UwKXBeIsGbyaDIL_MUDs1dZFA02jW_DD-N8EFwSXYoz14i_07uwmaqVTAq6tfYprRlN1xjmRNJWPJ2pxB5UuC6ktfAu1S_tHgtdHgsT08LNf6SFGtfz86T_Yj__OXn07Zl8esOvUr_06-mYYezMeg3QPmuBjDFDfHghGapyom8qpcaLUNFFJ9uzwMG9FNyNEfgOvcR24</addsrcrecordid><sourcetype>Open Website</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2541857500</pqid></control><display><type>article</type><title>Functional-genomic analysis reveals intraspecies diversification of antiviral receptor transporter proteins in Xenopus laevis</title><source>DOAJ Directory of Open Access Journals</source><source>Public Library of Science (PLoS) Journals Open Access</source><source>EZB-FREE-00999 freely available EZB journals</source><source>PubMed Central</source><creator>Boys, Ian N ; Mar, Katrina B ; Schoggins, John W</creator><contributor>Gojobori, Takashi</contributor><creatorcontrib>Boys, Ian N ; Mar, Katrina B ; Schoggins, John W ; Gojobori, Takashi</creatorcontrib><description>The Receptor Transporter Protein (RTP) family is present in most, if not all jawed vertebrates. Most of our knowledge of this protein family comes from studies on mammalian RTPs, which are multi-function proteins that regulate cell-surface G-protein coupled receptor levels, influence olfactory system development, regulate immune signaling, and directly inhibit viral infection. However, mammals comprise less than one-tenth of extant vertebrate species, and our knowledge about the expression, function, and evolution of non-mammalian RTPs is limited. Here, we explore the evolutionary history of RTPs in vertebrates. We identify signatures of positive selection in many vertebrate RTP clades and characterize multiple, independent expansions of the RTP family outside of what has been described in mammals. We find a striking expansion of RTPs in the African clawed frog, Xenopus laevis, with 11 RTPs in this species as opposed to 1 to 4 in most other species. RNA sequencing revealed that most X. laevis RTPs are upregulated following immune stimulation. In functional assays, we demonstrate that at least three of these X. laevis RTPs inhibit infection by RNA viruses, suggesting that RTP homologs may serve as antiviral effectors outside of Mammalia.</description><identifier>ISSN: 1553-7404</identifier><identifier>ISSN: 1553-7390</identifier><identifier>EISSN: 1553-7404</identifier><identifier>DOI: 10.1371/journal.pgen.1009578</identifier><identifier>PMID: 34014925</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Analysis ; Biology and Life Sciences ; Chromosomes ; Computer and Information Sciences ; Evolutionary biology ; Gene conversion ; Genes ; Genetic aspects ; Genomes ; Genomic analysis ; Genomics ; Hybridization ; Identification and classification ; Maximum likelihood method ; Medicine and Health Sciences ; Protein transport ; Proteins ; Recombination ; Reptiles & amphibians ; Research and Analysis Methods ; RNA sequencing ; Vertebrates ; Viral infections ; Viruses ; Xenopus laevis</subject><ispartof>PLoS genetics, 2021-05, Vol.17 (5), p.e1009578-e1009578</ispartof><rights>COPYRIGHT 2021 Public Library of Science</rights><rights>2021 Boys et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2021 Boys et al 2021 Boys et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c726t-e8b0d66966095355b899ce4e5ee4eda49ad9198b224d54be601b6dd3edf674a43</citedby><cites>FETCH-LOGICAL-c726t-e8b0d66966095355b899ce4e5ee4eda49ad9198b224d54be601b6dd3edf674a43</cites><orcidid>0000-0002-0854-207X ; 0000-0002-7944-6800 ; 0000-0003-3640-2418</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8172065/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8172065/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2102,2928,23866,27924,27925,53791,53793,79600,79601</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34014925$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Gojobori, Takashi</contributor><creatorcontrib>Boys, Ian N</creatorcontrib><creatorcontrib>Mar, Katrina B</creatorcontrib><creatorcontrib>Schoggins, John W</creatorcontrib><title>Functional-genomic analysis reveals intraspecies diversification of antiviral receptor transporter proteins in Xenopus laevis</title><title>PLoS genetics</title><addtitle>PLoS Genet</addtitle><description>The Receptor Transporter Protein (RTP) family is present in most, if not all jawed vertebrates. Most of our knowledge of this protein family comes from studies on mammalian RTPs, which are multi-function proteins that regulate cell-surface G-protein coupled receptor levels, influence olfactory system development, regulate immune signaling, and directly inhibit viral infection. However, mammals comprise less than one-tenth of extant vertebrate species, and our knowledge about the expression, function, and evolution of non-mammalian RTPs is limited. Here, we explore the evolutionary history of RTPs in vertebrates. We identify signatures of positive selection in many vertebrate RTP clades and characterize multiple, independent expansions of the RTP family outside of what has been described in mammals. We find a striking expansion of RTPs in the African clawed frog, Xenopus laevis, with 11 RTPs in this species as opposed to 1 to 4 in most other species. RNA sequencing revealed that most X. laevis RTPs are upregulated following immune stimulation. In functional assays, we demonstrate that at least three of these X. laevis RTPs inhibit infection by RNA viruses, suggesting that RTP homologs may serve as antiviral effectors outside of Mammalia.</description><subject>Analysis</subject><subject>Biology and Life Sciences</subject><subject>Chromosomes</subject><subject>Computer and Information Sciences</subject><subject>Evolutionary biology</subject><subject>Gene conversion</subject><subject>Genes</subject><subject>Genetic aspects</subject><subject>Genomes</subject><subject>Genomic analysis</subject><subject>Genomics</subject><subject>Hybridization</subject><subject>Identification and classification</subject><subject>Maximum likelihood method</subject><subject>Medicine and Health Sciences</subject><subject>Protein transport</subject><subject>Proteins</subject><subject>Recombination</subject><subject>Reptiles & amphibians</subject><subject>Research and Analysis Methods</subject><subject>RNA sequencing</subject><subject>Vertebrates</subject><subject>Viral infections</subject><subject>Viruses</subject><subject>Xenopus laevis</subject><issn>1553-7404</issn><issn>1553-7390</issn><issn>1553-7404</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNqVk12L1DAUhoso7jr6D0QLgujFjEnz0eRGWBZXBxYX_MK7kCanMxk6TU3awb3wv5s63WVG9kIptGn6vO_pOTkny55itMCkxG82fgitbhbdCtoFRkiyUtzLTjFjZF5SRO8frE-yRzFuECJMyPJhdkIowlQW7DT7dTG0pnc-Oc2Tkd86k-v0ch1dzAPsQDcxd20fdOzAOIi5dTsI0dXO6FGX-zoJerdzQTdJYaDrfciToI2dDz2EvAu-B9eOPvn3FKMbYt5o2Ln4OHtQpwDwZHrOsq8X776cf5hfXr1fnp9dzk1Z8H4OokKWc8l5ypIwVgkpDVBgkG5WU6mtxFJURUEtoxVwhCtuLQFb85JqSmbZ871v1_iopspFVTCKBStZKswsW-4J6_VGdcFtdbhWXjv1Z8OHldKhd6YBRZAkpLCsJNLSqgTBBJIVaAHCUMGK5PV2ijZUW7AGxvI1R6bHX1q3Viu_UwKXBeIsGbyaDIL_MUDs1dZFA02jW_DD-N8EFwSXYoz14i_07uwmaqVTAq6tfYprRlN1xjmRNJWPJ2pxB5UuC6ktfAu1S_tHgtdHgsT08LNf6SFGtfz86T_Yj__OXn07Zl8esOvUr_06-mYYezMeg3QPmuBjDFDfHghGapyom8qpcaLUNFFJ9uzwMG9FNyNEfgOvcR24</recordid><startdate>20210520</startdate><enddate>20210520</enddate><creator>Boys, Ian N</creator><creator>Mar, Katrina B</creator><creator>Schoggins, John W</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>IOV</scope><scope>ISN</scope><scope>ISR</scope><scope>3V.</scope><scope>7QP</scope><scope>7QR</scope><scope>7SS</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>COVID</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7P</scope><scope>P64</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0002-0854-207X</orcidid><orcidid>https://orcid.org/0000-0002-7944-6800</orcidid><orcidid>https://orcid.org/0000-0003-3640-2418</orcidid></search><sort><creationdate>20210520</creationdate><title>Functional-genomic analysis reveals intraspecies diversification of antiviral receptor transporter proteins in Xenopus laevis</title><author>Boys, Ian N ; Mar, Katrina B ; Schoggins, John W</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c726t-e8b0d66966095355b899ce4e5ee4eda49ad9198b224d54be601b6dd3edf674a43</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Analysis</topic><topic>Biology and Life Sciences</topic><topic>Chromosomes</topic><topic>Computer and Information Sciences</topic><topic>Evolutionary biology</topic><topic>Gene conversion</topic><topic>Genes</topic><topic>Genetic aspects</topic><topic>Genomes</topic><topic>Genomic analysis</topic><topic>Genomics</topic><topic>Hybridization</topic><topic>Identification and classification</topic><topic>Maximum likelihood method</topic><topic>Medicine and Health Sciences</topic><topic>Protein transport</topic><topic>Proteins</topic><topic>Recombination</topic><topic>Reptiles & amphibians</topic><topic>Research and Analysis Methods</topic><topic>RNA sequencing</topic><topic>Vertebrates</topic><topic>Viral infections</topic><topic>Viruses</topic><topic>Xenopus laevis</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Boys, Ian N</creatorcontrib><creatorcontrib>Mar, Katrina B</creatorcontrib><creatorcontrib>Schoggins, John W</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Opposing Viewpoints</collection><collection>Gale In Context: Canada</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>Coronavirus Research Database</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Access via ProQuest (Open Access)</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PLoS genetics</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Boys, Ian N</au><au>Mar, Katrina B</au><au>Schoggins, John W</au><au>Gojobori, Takashi</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Functional-genomic analysis reveals intraspecies diversification of antiviral receptor transporter proteins in Xenopus laevis</atitle><jtitle>PLoS genetics</jtitle><addtitle>PLoS Genet</addtitle><date>2021-05-20</date><risdate>2021</risdate><volume>17</volume><issue>5</issue><spage>e1009578</spage><epage>e1009578</epage><pages>e1009578-e1009578</pages><issn>1553-7404</issn><issn>1553-7390</issn><eissn>1553-7404</eissn><abstract>The Receptor Transporter Protein (RTP) family is present in most, if not all jawed vertebrates. Most of our knowledge of this protein family comes from studies on mammalian RTPs, which are multi-function proteins that regulate cell-surface G-protein coupled receptor levels, influence olfactory system development, regulate immune signaling, and directly inhibit viral infection. However, mammals comprise less than one-tenth of extant vertebrate species, and our knowledge about the expression, function, and evolution of non-mammalian RTPs is limited. Here, we explore the evolutionary history of RTPs in vertebrates. We identify signatures of positive selection in many vertebrate RTP clades and characterize multiple, independent expansions of the RTP family outside of what has been described in mammals. We find a striking expansion of RTPs in the African clawed frog, Xenopus laevis, with 11 RTPs in this species as opposed to 1 to 4 in most other species. RNA sequencing revealed that most X. laevis RTPs are upregulated following immune stimulation. In functional assays, we demonstrate that at least three of these X. laevis RTPs inhibit infection by RNA viruses, suggesting that RTP homologs may serve as antiviral effectors outside of Mammalia.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>34014925</pmid><doi>10.1371/journal.pgen.1009578</doi><orcidid>https://orcid.org/0000-0002-0854-207X</orcidid><orcidid>https://orcid.org/0000-0002-7944-6800</orcidid><orcidid>https://orcid.org/0000-0003-3640-2418</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1553-7404 |
| ispartof | PLoS genetics, 2021-05, Vol.17 (5), p.e1009578-e1009578 |
| issn | 1553-7404 1553-7390 1553-7404 |
| language | eng |
| recordid | cdi_plos_journals_2541857500 |
| source | DOAJ Directory of Open Access Journals; Public Library of Science (PLoS) Journals Open Access; EZB-FREE-00999 freely available EZB journals; PubMed Central |
| subjects | Analysis Biology and Life Sciences Chromosomes Computer and Information Sciences Evolutionary biology Gene conversion Genes Genetic aspects Genomes Genomic analysis Genomics Hybridization Identification and classification Maximum likelihood method Medicine and Health Sciences Protein transport Proteins Recombination Reptiles & amphibians Research and Analysis Methods RNA sequencing Vertebrates Viral infections Viruses Xenopus laevis |
| title | Functional-genomic analysis reveals intraspecies diversification of antiviral receptor transporter proteins in Xenopus laevis |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-26T02%3A34%3A31IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Functional-genomic%20analysis%20reveals%20intraspecies%20diversification%20of%20antiviral%20receptor%20transporter%20proteins%20in%20Xenopus%20laevis&rft.jtitle=PLoS%20genetics&rft.au=Boys,%20Ian%20N&rft.date=2021-05-20&rft.volume=17&rft.issue=5&rft.spage=e1009578&rft.epage=e1009578&rft.pages=e1009578-e1009578&rft.issn=1553-7404&rft.eissn=1553-7404&rft_id=info:doi/10.1371/journal.pgen.1009578&rft_dat=%3Cgale_plos_%3EA663949196%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2541857500&rft_id=info:pmid/34014925&rft_galeid=A663949196&rft_doaj_id=oai_doaj_org_article_309332d5739d4b7e85809bea8e8c4852&rfr_iscdi=true |