Widespread divergence of the CEACAM/PSG genes in vertebrates and humans suggests sensitivity to selection
In mammals, carcinoembryonic antigen cell adhesion molecules (CEACAMs) and pregnancy-specific glycoproteins (PSGs) play important roles in the regulation of pathogen transmission, tumorigenesis, insulin signaling turnover, and fetal-maternal interactions. However, how these genes evolved and to what...
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| creator | Chang, Chia Lin Semyonov, Jenia Cheng, Po Jen Huang, Shang Yu Park, Jae Il Tsai, Huai-Jen Lin, Cheng-Yung Grützner, Frank Soong, Yung Kuei Cai, James J Hsu, Sheau Yu Teddy |
| description | In mammals, carcinoembryonic antigen cell adhesion molecules (CEACAMs) and pregnancy-specific glycoproteins (PSGs) play important roles in the regulation of pathogen transmission, tumorigenesis, insulin signaling turnover, and fetal-maternal interactions. However, how these genes evolved and to what extent they diverged in humans remain to be investigated specifically. Based on syntenic mapping of chordate genomes, we reveal that diverging homologs with a prototypic CEACAM architecture-including an extracellular domain with immunoglobulin variable and constant domain-like regions, and an intracellular domain containing ITAM motif-are present from cartilaginous fish to humans, but are absent in sea lamprey, cephalochordate or urochordate. Interestingly, the CEACAM/PSG gene inventory underwent radical divergence in various vertebrate lineages: from zero in avian species to dozens in therian mammals. In addition, analyses of genetic variations in human populations showed the presence of various types of copy number variations (CNVs) at the CEACAM/PSG locus. These copy number polymorphisms have 3-80% frequency in select populations, and encompass single to more than six PSG genes. Furthermore, we found that CEACAM/PSG genes contain a significantly higher density of nonsynonymous single nucleotide polymorphism (SNP) compared to the chromosome average, and many CEACAM/PSG SNPs exhibit high population differentiation. Taken together, our study suggested that CEACAM/PSG genes have had a more dynamic evolutionary history in vertebrates than previously thought. Given that CEACAM/PSGs play important roles in maternal-fetal interaction and pathogen recognition, these data have laid the groundwork for future analysis of adaptive CEACAM/PSG genotype-phenotypic relationships in normal and complicated pregnancies as well as other etiologies. |
| doi_str_mv | 10.1371/journal.pone.0061701 |
| format | Article |
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However, how these genes evolved and to what extent they diverged in humans remain to be investigated specifically. Based on syntenic mapping of chordate genomes, we reveal that diverging homologs with a prototypic CEACAM architecture-including an extracellular domain with immunoglobulin variable and constant domain-like regions, and an intracellular domain containing ITAM motif-are present from cartilaginous fish to humans, but are absent in sea lamprey, cephalochordate or urochordate. Interestingly, the CEACAM/PSG gene inventory underwent radical divergence in various vertebrate lineages: from zero in avian species to dozens in therian mammals. In addition, analyses of genetic variations in human populations showed the presence of various types of copy number variations (CNVs) at the CEACAM/PSG locus. These copy number polymorphisms have 3-80% frequency in select populations, and encompass single to more than six PSG genes. Furthermore, we found that CEACAM/PSG genes contain a significantly higher density of nonsynonymous single nucleotide polymorphism (SNP) compared to the chromosome average, and many CEACAM/PSG SNPs exhibit high population differentiation. Taken together, our study suggested that CEACAM/PSG genes have had a more dynamic evolutionary history in vertebrates than previously thought. Given that CEACAM/PSGs play important roles in maternal-fetal interaction and pathogen recognition, these data have laid the groundwork for future analysis of adaptive CEACAM/PSG genotype-phenotypic relationships in normal and complicated pregnancies as well as other etiologies.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0061701</identifier><identifier>PMID: 23613906</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Analysis ; Animals ; Antigens ; Antigens, CD - genetics ; Biological evolution ; Biology ; Carcinoembryonic antigen ; Cell adhesion ; Cell adhesion & migration ; Cell adhesion molecules ; Cell Adhesion Molecules - genetics ; Cellular biology ; Copy number ; Divergence ; Ethics ; Etiology ; Evolution ; Evolution, Molecular ; Fetuses ; Gene mapping ; Gene polymorphism ; Genes ; Genetic diversity ; Genomes ; Genomics ; Glycoproteins ; Gynecology ; Homology ; Hospitals ; Human populations ; Humans ; Immunoglobulins ; Insulin ; Laboratory animals ; Mammals ; Medical research ; Medicine ; Mutation ; Obstetrics ; Pathogens ; Polymorphism ; Polymorphism, Single Nucleotide - genetics ; Population differentiation ; Population genetics ; Populations ; Pregnancy ; Pregnancy Proteins - genetics ; Proteins ; Selection, Genetic - genetics ; Signaling ; Single nucleotide polymorphisms ; Single-nucleotide polymorphism ; Stem cells ; Synteny ; Tumorigenesis ; Vertebrates ; Zebrafish</subject><ispartof>PloS one, 2013-04, Vol.8 (4), p.e61701-e61701</ispartof><rights>COPYRIGHT 2013 Public Library of Science</rights><rights>2013 Chang et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://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>2013 Chang et al 2013 Chang et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c758t-d1d240d8e97032146d2f965f1da9c84a5684438bca7f85db0dcde654fcf2f96e3</citedby><cites>FETCH-LOGICAL-c758t-d1d240d8e97032146d2f965f1da9c84a5684438bca7f85db0dcde654fcf2f96e3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3628338/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3628338/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,724,777,781,861,882,2096,2915,23847,27905,27906,53772,53774,79349,79350</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23613906$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Laudet, Vincent</contributor><creatorcontrib>Chang, Chia Lin</creatorcontrib><creatorcontrib>Semyonov, Jenia</creatorcontrib><creatorcontrib>Cheng, Po Jen</creatorcontrib><creatorcontrib>Huang, Shang Yu</creatorcontrib><creatorcontrib>Park, Jae Il</creatorcontrib><creatorcontrib>Tsai, Huai-Jen</creatorcontrib><creatorcontrib>Lin, Cheng-Yung</creatorcontrib><creatorcontrib>Grützner, Frank</creatorcontrib><creatorcontrib>Soong, Yung Kuei</creatorcontrib><creatorcontrib>Cai, James J</creatorcontrib><creatorcontrib>Hsu, Sheau Yu Teddy</creatorcontrib><title>Widespread divergence of the CEACAM/PSG genes in vertebrates and humans suggests sensitivity to selection</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>In mammals, carcinoembryonic antigen cell adhesion molecules (CEACAMs) and pregnancy-specific glycoproteins (PSGs) play important roles in the regulation of pathogen transmission, tumorigenesis, insulin signaling turnover, and fetal-maternal interactions. However, how these genes evolved and to what extent they diverged in humans remain to be investigated specifically. Based on syntenic mapping of chordate genomes, we reveal that diverging homologs with a prototypic CEACAM architecture-including an extracellular domain with immunoglobulin variable and constant domain-like regions, and an intracellular domain containing ITAM motif-are present from cartilaginous fish to humans, but are absent in sea lamprey, cephalochordate or urochordate. Interestingly, the CEACAM/PSG gene inventory underwent radical divergence in various vertebrate lineages: from zero in avian species to dozens in therian mammals. In addition, analyses of genetic variations in human populations showed the presence of various types of copy number variations (CNVs) at the CEACAM/PSG locus. These copy number polymorphisms have 3-80% frequency in select populations, and encompass single to more than six PSG genes. Furthermore, we found that CEACAM/PSG genes contain a significantly higher density of nonsynonymous single nucleotide polymorphism (SNP) compared to the chromosome average, and many CEACAM/PSG SNPs exhibit high population differentiation. Taken together, our study suggested that CEACAM/PSG genes have had a more dynamic evolutionary history in vertebrates than previously thought. Given that CEACAM/PSGs play important roles in maternal-fetal interaction and pathogen recognition, these data have laid the groundwork for future analysis of adaptive CEACAM/PSG genotype-phenotypic relationships in normal and complicated pregnancies as well as other etiologies.</description><subject>Analysis</subject><subject>Animals</subject><subject>Antigens</subject><subject>Antigens, CD - genetics</subject><subject>Biological evolution</subject><subject>Biology</subject><subject>Carcinoembryonic antigen</subject><subject>Cell adhesion</subject><subject>Cell adhesion & migration</subject><subject>Cell adhesion molecules</subject><subject>Cell Adhesion Molecules - genetics</subject><subject>Cellular biology</subject><subject>Copy number</subject><subject>Divergence</subject><subject>Ethics</subject><subject>Etiology</subject><subject>Evolution</subject><subject>Evolution, Molecular</subject><subject>Fetuses</subject><subject>Gene mapping</subject><subject>Gene polymorphism</subject><subject>Genes</subject><subject>Genetic diversity</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Glycoproteins</subject><subject>Gynecology</subject><subject>Homology</subject><subject>Hospitals</subject><subject>Human populations</subject><subject>Humans</subject><subject>Immunoglobulins</subject><subject>Insulin</subject><subject>Laboratory animals</subject><subject>Mammals</subject><subject>Medical research</subject><subject>Medicine</subject><subject>Mutation</subject><subject>Obstetrics</subject><subject>Pathogens</subject><subject>Polymorphism</subject><subject>Polymorphism, Single Nucleotide - genetics</subject><subject>Population differentiation</subject><subject>Population genetics</subject><subject>Populations</subject><subject>Pregnancy</subject><subject>Pregnancy Proteins - genetics</subject><subject>Proteins</subject><subject>Selection, Genetic - genetics</subject><subject>Signaling</subject><subject>Single nucleotide polymorphisms</subject><subject>Single-nucleotide polymorphism</subject><subject>Stem cells</subject><subject>Synteny</subject><subject>Tumorigenesis</subject><subject>Vertebrates</subject><subject>Zebrafish</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><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>eNqNk99v0zAQxyMEYmPwHyCIhITgoZ0dO7bzglRVY1QaGmL8eLQc-5J6SuMudir23-Os2dSgPSA_2Hf-3Pfssy9JXmM0x4Tj02vXd61q5lvXwhwhhjnCT5JjXJBsxjJEnh6sj5IX3l8jlBPB2PPkKCMMkwKx48T-tgb8tgNlUmN30NXQakhdlYY1pMuzxXLx9fTb1Xka_eBT26aRCVB2KkRTtSZd9xvV-tT3dQ0-xAW03ga7s-E2DS6aDehgXfsyeVapxsOrcT5Jfn4--7H8Mru4PF8tFxczzXMRZgabjCIjoOCIZJgyk1UFyytsVKEFVTkTlBJRasUrkZsSGW2A5bTS1QACOUne7nW3jfNyrJKXmFCKeMZFEYnVnjBOXcttZzequ5VOWXnncF0tVResbkDmlaACM4ILCpTzvCSVANCUGFHiDAatT2O2vtyA0dCGTjUT0elOa9eydjtJWCYIEVHgwyjQuZs-VlBurNfQNKoF19-dm2HMc04j-u4f9PHbjVSt4gVsW7mYVw-ickG5yHIRU0dq_ggVh4GN1fFLVTb6JwEfJwGRCfAn1Kr3Xq6uvv8_e_lryr4_YNegmrD2rumHL-OnIN2DunPed1A9FBkjOXTEfTXk0BFy7IgY9ubwgR6C7luA_AWURAYV</recordid><startdate>20130416</startdate><enddate>20130416</enddate><creator>Chang, Chia Lin</creator><creator>Semyonov, Jenia</creator><creator>Cheng, Po Jen</creator><creator>Huang, Shang Yu</creator><creator>Park, Jae Il</creator><creator>Tsai, Huai-Jen</creator><creator>Lin, Cheng-Yung</creator><creator>Grützner, Frank</creator><creator>Soong, Yung Kuei</creator><creator>Cai, James J</creator><creator>Hsu, Sheau Yu Teddy</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><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>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>COVID</scope><scope>D1I</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>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20130416</creationdate><title>Widespread divergence of the CEACAM/PSG genes in vertebrates and humans suggests sensitivity to selection</title><author>Chang, Chia Lin ; Semyonov, Jenia ; Cheng, Po Jen ; Huang, Shang Yu ; Park, Jae Il ; Tsai, Huai-Jen ; Lin, Cheng-Yung ; Grützner, Frank ; Soong, Yung Kuei ; Cai, James J ; Hsu, Sheau Yu Teddy</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c758t-d1d240d8e97032146d2f965f1da9c84a5684438bca7f85db0dcde654fcf2f96e3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Analysis</topic><topic>Animals</topic><topic>Antigens</topic><topic>Antigens, CD - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Chang, Chia Lin</au><au>Semyonov, Jenia</au><au>Cheng, Po Jen</au><au>Huang, Shang Yu</au><au>Park, Jae Il</au><au>Tsai, Huai-Jen</au><au>Lin, Cheng-Yung</au><au>Grützner, Frank</au><au>Soong, Yung Kuei</au><au>Cai, James J</au><au>Hsu, Sheau Yu Teddy</au><au>Laudet, Vincent</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Widespread divergence of the CEACAM/PSG genes in vertebrates and humans suggests sensitivity to selection</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2013-04-16</date><risdate>2013</risdate><volume>8</volume><issue>4</issue><spage>e61701</spage><epage>e61701</epage><pages>e61701-e61701</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>In mammals, carcinoembryonic antigen cell adhesion molecules (CEACAMs) and pregnancy-specific glycoproteins (PSGs) play important roles in the regulation of pathogen transmission, tumorigenesis, insulin signaling turnover, and fetal-maternal interactions. However, how these genes evolved and to what extent they diverged in humans remain to be investigated specifically. Based on syntenic mapping of chordate genomes, we reveal that diverging homologs with a prototypic CEACAM architecture-including an extracellular domain with immunoglobulin variable and constant domain-like regions, and an intracellular domain containing ITAM motif-are present from cartilaginous fish to humans, but are absent in sea lamprey, cephalochordate or urochordate. Interestingly, the CEACAM/PSG gene inventory underwent radical divergence in various vertebrate lineages: from zero in avian species to dozens in therian mammals. In addition, analyses of genetic variations in human populations showed the presence of various types of copy number variations (CNVs) at the CEACAM/PSG locus. These copy number polymorphisms have 3-80% frequency in select populations, and encompass single to more than six PSG genes. Furthermore, we found that CEACAM/PSG genes contain a significantly higher density of nonsynonymous single nucleotide polymorphism (SNP) compared to the chromosome average, and many CEACAM/PSG SNPs exhibit high population differentiation. Taken together, our study suggested that CEACAM/PSG genes have had a more dynamic evolutionary history in vertebrates than previously thought. Given that CEACAM/PSGs play important roles in maternal-fetal interaction and pathogen recognition, these data have laid the groundwork for future analysis of adaptive CEACAM/PSG genotype-phenotypic relationships in normal and complicated pregnancies as well as other etiologies.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>23613906</pmid><doi>10.1371/journal.pone.0061701</doi><tpages>e61701</tpages><oa>free_for_read</oa></addata></record> |
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| ispartof | PloS one, 2013-04, Vol.8 (4), p.e61701-e61701 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_1344072789 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Public Library of Science (PLoS); EZB-FREE-00999 freely available EZB journals; PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | Analysis Animals Antigens Antigens, CD - genetics Biological evolution Biology Carcinoembryonic antigen Cell adhesion Cell adhesion & migration Cell adhesion molecules Cell Adhesion Molecules - genetics Cellular biology Copy number Divergence Ethics Etiology Evolution Evolution, Molecular Fetuses Gene mapping Gene polymorphism Genes Genetic diversity Genomes Genomics Glycoproteins Gynecology Homology Hospitals Human populations Humans Immunoglobulins Insulin Laboratory animals Mammals Medical research Medicine Mutation Obstetrics Pathogens Polymorphism Polymorphism, Single Nucleotide - genetics Population differentiation Population genetics Populations Pregnancy Pregnancy Proteins - genetics Proteins Selection, Genetic - genetics Signaling Single nucleotide polymorphisms Single-nucleotide polymorphism Stem cells Synteny Tumorigenesis Vertebrates Zebrafish |
| title | Widespread divergence of the CEACAM/PSG genes in vertebrates and humans suggests sensitivity to selection |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-21T00%3A14%3A24IST&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=Widespread%20divergence%20of%20the%20CEACAM/PSG%20genes%20in%20vertebrates%20and%20humans%20suggests%20sensitivity%20to%20selection&rft.jtitle=PloS%20one&rft.au=Chang,%20Chia%20Lin&rft.date=2013-04-16&rft.volume=8&rft.issue=4&rft.spage=e61701&rft.epage=e61701&rft.pages=e61701-e61701&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0061701&rft_dat=%3Cgale_plos_%3EA478258362%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=1344072789&rft_id=info:pmid/23613906&rft_galeid=A478258362&rft_doaj_id=oai_doaj_org_article_5f848163194e4775b3f8eec43d8b12e9&rfr_iscdi=true |