Recent expansion and adaptive evolution of the carcinoembryonic antigen family in bats of the Yangochiroptera subgroup
Identifieur interne : 000759 ( Main/Exploration ); précédent : 000758; suivant : 000760Recent expansion and adaptive evolution of the carcinoembryonic antigen family in bats of the Yangochiroptera subgroup
Auteurs : Robert Kammerer [Allemagne] ; Martin Mansfeld [Allemagne] ; Jana H Nske [Allemagne] ; Sophie Mi Bach [Allemagne] ; Xiaocui He [Allemagne] ; Bernd Köllner [Allemagne] ; Susan Mouchantat [Allemagne] ; Wolfgang Zimmermann [Allemagne]Source :
- BMC Genomics [ 1471-2164 ] ; 2017.
Abstract
Expansions of gene families are predictive for ongoing genetic adaptation to environmental cues. We describe such an expansion of the
Analysis of the CEA gene family in bats revealed that in certain bat families, belonging to the subgroup Yangochiroptera but not the Yinpterochiroptera subgroup an expansion of the CEA gene family took place, resulting in approximately one hundred CEA family genes in some species of the Vespertilionidae. The majority of these genes encode secreted PSG-like proteins (further referred to as PSG). Remarkably, we found strong evidence that the ligand-binding domain (IgV-like domain) of PSG is under diversifying positive selection indicating that bat PSGs may interact with structurally highly variable ligands. Such ligands might represent bacterial or viral pathogen adhesins. We have identified two distinct clusters of PSGs in three Myotis species. The two PSG cluster differ in the amino acids under positive selection. One cluster was only expanded in members of the Vespertilionidae while the other was found to be expanded in addition in members of the Miniopteridae and Mormoopidae. Thus one round of PSG expansion may have occurred in an ancestry of all three families and a second only in Vespertilionidae. Although maternal ligands of PSGs may exist selective challenges by two distinct pathogens seem to be likely responsible for the expansion of PSGs in Vespertilionidae.
The rapid expansion of PSGs in certain bat species together with selection for diversification suggest that bat PSGs could be part of a pathogen defense system by serving as decoy receptors and/or regulators of feto-maternal interactions.
The online version of this article (10.1186/s12864-017-4106-7) contains supplementary material, which is available to authorized users.
Url:
DOI: 10.1186/s12864-017-4106-7
PubMed: 28893191
PubMed Central: 5594555
Affiliations:
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family in bats of the Yangochiroptera subgroup</title><author><name sortKey="Kammerer, Robert" sort="Kammerer, Robert" uniqKey="Kammerer R" first="Robert" last="Kammerer">Robert Kammerer</name><affiliation wicri:level="1"><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="GRID">grid.417834.d</institution-id><institution>Institute of Immunology, Friedrich-Loeffler Institute,</institution></institution-wrap>-Insel Riems, Greifswald, Germany</nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea>-Insel Riems, Greifswald</wicri:regionArea><wicri:noRegion>Greifswald</wicri:noRegion><wicri:noRegion>Greifswald</wicri:noRegion><wicri:noRegion>Greifswald</wicri:noRegion></affiliation></author><author><name sortKey="Mansfeld, Martin" sort="Mansfeld, Martin" uniqKey="Mansfeld M" first="Martin" last="Mansfeld">Martin Mansfeld</name><affiliation wicri:level="1"><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="GRID">grid.417834.d</institution-id><institution>Institute of Immunology, Friedrich-Loeffler Institute,</institution></institution-wrap>-Insel Riems, Greifswald, Germany</nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea>-Insel Riems, Greifswald</wicri:regionArea><wicri:noRegion>Greifswald</wicri:noRegion><wicri:noRegion>Greifswald</wicri:noRegion><wicri:noRegion>Greifswald</wicri:noRegion></affiliation></author><author><name sortKey="H Nske, Jana" sort="H Nske, Jana" uniqKey="H Nske J" first="Jana" last="H Nske">Jana H Nske</name><affiliation wicri:level="1"><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="GRID">grid.417834.d</institution-id><institution>Institute of Immunology, Friedrich-Loeffler Institute,</institution></institution-wrap>-Insel Riems, Greifswald, Germany</nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea>-Insel Riems, 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7018</institution-id><institution-id institution-id-type="GRID">grid.418215.b</institution-id><institution>Plattform Degenerative Erkrankungen, Deutsches Primatenzentrum GmbH,</institution></institution-wrap>Goettingen, Germany</nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea>Goettingen</wicri:regionArea></affiliation></author><author><name sortKey="He, Xiaocui" sort="He, Xiaocui" uniqKey="He X" first="Xiaocui" last="He">Xiaocui He</name><affiliation wicri:level="1"><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="GRID">grid.417834.d</institution-id><institution>Institute of Immunology, Friedrich-Loeffler Institute,</institution></institution-wrap>-Insel Riems, Greifswald, Germany</nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea>-Insel Riems, Greifswald</wicri:regionArea><wicri:noRegion>Greifswald</wicri:noRegion><wicri:noRegion>Greifswald</wicri:noRegion><wicri:noRegion>Greifswald</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="Aff3"><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 0491 4256</institution-id><institution-id institution-id-type="GRID">grid.429509.3</institution-id><institution>Department of Molecular Immunology,</institution><institution>Max-Planck-Institute of Immunobiology and Epigenetics,</institution></institution-wrap>Freiburg, Germany</nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea>Freiburg</wicri:regionArea></affiliation></author><author><name sortKey="Kollner, Bernd" sort="Kollner, Bernd" uniqKey="Kollner B" first="Bernd" last="Köllner">Bernd Köllner</name><affiliation wicri:level="1"><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="GRID">grid.417834.d</institution-id><institution>Institute of Immunology, Friedrich-Loeffler Institute,</institution></institution-wrap>-Insel Riems, Greifswald, Germany</nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea>-Insel Riems, Greifswald</wicri:regionArea><wicri:noRegion>Greifswald</wicri:noRegion><wicri:noRegion>Greifswald</wicri:noRegion><wicri:noRegion>Greifswald</wicri:noRegion></affiliation></author><author><name sortKey="Mouchantat, Susan" sort="Mouchantat, Susan" uniqKey="Mouchantat S" first="Susan" last="Mouchantat">Susan Mouchantat</name><affiliation wicri:level="1"><nlm:aff id="Aff4"><institution-wrap><institution-id institution-id-type="GRID">grid.417834.d</institution-id><institution>Junior Research Group Wildlife Diseases, Friedrich-Loeffler-Institute,</institution></institution-wrap>-Insel Riems, Greifswald, Germany</nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea>-Insel Riems, Greifswald</wicri:regionArea><wicri:noRegion>Greifswald</wicri:noRegion><wicri:noRegion>Greifswald</wicri:noRegion><wicri:noRegion>Greifswald</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="Aff5"><institution-wrap><institution-id institution-id-type="GRID">grid.5603.0</institution-id><institution>Institute of Diagnostic Radiology and Neuroradiology,</institution><institution>University Medicine Greifswald,</institution></institution-wrap>Greifswald, Germany</nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea>Greifswald</wicri:regionArea></affiliation></author><author><name sortKey="Zimmermann, Wolfgang" sort="Zimmermann, Wolfgang" uniqKey="Zimmermann W" first="Wolfgang" last="Zimmermann">Wolfgang Zimmermann</name><affiliation wicri:level="1"><nlm:aff id="Aff6"><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 1936 973X</institution-id><institution-id institution-id-type="GRID">grid.5252.0</institution-id><institution>Tumor Immunology Laboratory, LIFE Center, University Clinic,</institution><institution>Ludwig-Maximilians-University,</institution></institution-wrap>Munich, Germany</nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea>Munich</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="Aff7"><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 1936 973X</institution-id><institution-id institution-id-type="GRID">grid.5252.0</institution-id><institution>Department of Urology, University Clinic,</institution><institution>Ludwig-Maximilians-University,</institution></institution-wrap>Munich, Germany</nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea>Munich</wicri:regionArea></affiliation></author></analytic><series><title level="j">BMC Genomics</title><idno type="eISSN">1471-2164</idno><imprint><date when="2017">2017</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><sec><title>Background</title><p id="Par1">Expansions of gene families are predictive for ongoing genetic adaptation to environmental cues. We describe such an expansion of the <italic>carcinoembryonic antigen</italic> (<italic>CEA</italic>) gene family in certain bat families. Members of the CEA family in humans and mice are exploited as cellular receptors by a number of pathogens, possibly due to their function in immunity and reproduction. The CEA family is composed of CEA-related cell adhesion molecules (CEACAMs) and secreted pregnancy-specific glycoproteins (PSGs). PSGs are almost exclusively expressed by trophoblast cells at the maternal-fetal interface. The reason why PSGs exist only in a minority of mammals is still unknown.</p></sec><sec><title>Results</title><p id="Par2">Analysis of the CEA gene family in bats revealed that in certain bat families, belonging to the subgroup Yangochiroptera but not the Yinpterochiroptera subgroup an expansion of the CEA gene family took place, resulting in approximately one hundred CEA family genes in some species of the Vespertilionidae. The majority of these genes encode secreted PSG-like proteins (further referred to as PSG). Remarkably, we found strong evidence that the ligand-binding domain (IgV-like domain) of PSG is under diversifying positive selection indicating that bat PSGs may interact with structurally highly variable ligands. Such ligands might represent bacterial or viral pathogen adhesins. We have identified two distinct clusters of PSGs in three Myotis species. The two PSG cluster differ in the amino acids under positive selection. One cluster was only expanded in members of the Vespertilionidae while the other was found to be expanded in addition in members of the Miniopteridae and Mormoopidae. Thus one round of PSG expansion may have occurred in an ancestry of all three families and a second only in Vespertilionidae. Although maternal ligands of PSGs may exist selective challenges by two distinct pathogens seem to be likely responsible for the expansion of PSGs in Vespertilionidae.</p></sec><sec><title>Conclusions</title><p id="Par3">The rapid expansion of PSGs in certain bat species together with selection for diversification suggest that bat PSGs could be part of a pathogen defense system by serving as decoy receptors and/or regulators of feto-maternal interactions.</p></sec><sec><title>Electronic supplementary material</title><p>The online version of this article (10.1186/s12864-017-4106-7) contains supplementary material, which is available to authorized users.</p></sec></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Herzig, Ct" uniqKey="Herzig C">CT Herzig</name></author><author><name sortKey="Waters, Rw" uniqKey="Waters R">RW Waters</name></author><author><name sortKey="Baldwin, Cl" uniqKey="Baldwin C">CL Baldwin</name></author><author><name sortKey="Telfer, Jc" uniqKey="Telfer J">JC Telfer</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Chuong, Eb" uniqKey="Chuong E">EB Chuong</name></author><author><name sortKey="Tong, W" uniqKey="Tong W">W Tong</name></author><author><name sortKey="Hoekstra, He" uniqKey="Hoekstra H">HE Hoekstra</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Tchoupa, Ak" uniqKey="Tchoupa A">AK Tchoupa</name></author><author><name sortKey="Schuhmacher, T" uniqKey="Schuhmacher T">T Schuhmacher</name></author><author><name sortKey="Hauck, Cr" uniqKey="Hauck C">CR Hauck</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Singer, Bb" uniqKey="Singer B">BB Singer</name></author><author><name sortKey="Opp, L" uniqKey="Opp L">L Opp</name></author><author><name sortKey="Heinrich, A" uniqKey="Heinrich A">A Heinrich</name></author><author><name sortKey="Schreiber, F" 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Terol</name></author><author><name sortKey="Talon, M" uniqKey="Talon M">M Talon</name></author><author><name sortKey="Robles, M" uniqKey="Robles M">M Robles</name></author></analytic></biblStruct><biblStruct></biblStruct></listBibl></div1></back></TEI><affiliations><list><country><li>Allemagne</li></country></list><tree><country name="Allemagne"><noRegion><name sortKey="Kammerer, Robert" sort="Kammerer, Robert" uniqKey="Kammerer R" first="Robert" last="Kammerer">Robert Kammerer</name></noRegion><name sortKey="H Nske, Jana" sort="H Nske, Jana" uniqKey="H Nske J" first="Jana" last="H Nske">Jana H Nske</name><name sortKey="He, Xiaocui" sort="He, Xiaocui" uniqKey="He X" first="Xiaocui" last="He">Xiaocui He</name><name sortKey="He, Xiaocui" sort="He, Xiaocui" uniqKey="He X" first="Xiaocui" last="He">Xiaocui He</name><name sortKey="Kollner, Bernd" sort="Kollner, Bernd" uniqKey="Kollner B" first="Bernd" last="Köllner">Bernd Köllner</name><name sortKey="Mansfeld, Martin" sort="Mansfeld, Martin" uniqKey="Mansfeld M" first="Martin" last="Mansfeld">Martin Mansfeld</name><name sortKey="Mi Bach, Sophie" sort="Mi Bach, Sophie" uniqKey="Mi Bach S" first="Sophie" last="Mi Bach">Sophie Mi Bach</name><name sortKey="Mi Bach, Sophie" sort="Mi Bach, Sophie" uniqKey="Mi Bach S" first="Sophie" last="Mi Bach">Sophie Mi Bach</name><name sortKey="Mouchantat, Susan" sort="Mouchantat, Susan" uniqKey="Mouchantat S" first="Susan" last="Mouchantat">Susan Mouchantat</name><name sortKey="Mouchantat, Susan" sort="Mouchantat, Susan" uniqKey="Mouchantat S" first="Susan" last="Mouchantat">Susan Mouchantat</name><name sortKey="Zimmermann, Wolfgang" sort="Zimmermann, Wolfgang" uniqKey="Zimmermann W" first="Wolfgang" last="Zimmermann">Wolfgang Zimmermann</name><name sortKey="Zimmermann, Wolfgang" sort="Zimmermann, Wolfgang" uniqKey="Zimmermann W" first="Wolfgang" last="Zimmermann">Wolfgang Zimmermann</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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