Recent expansion and adaptive evolution of the carcinoembryonic antigen family in bats of the Yangochiroptera subgroup
Abstract Background Expansions of gene families are predictive for ongoing genetic adaptation to environmental cues. We describe such an expansion of the carcinoembryonic antigen (CEA) gene family in certain bat families. Members of the CEA family in humans and mice are exploited as cellular recepto...
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| Format: | Article |
| Language: | English |
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BMC
2017-09-01
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| Series: | BMC Genomics |
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| Online Access: | http://link.springer.com/article/10.1186/s12864-017-4106-7 |
| _version_ | 1819243080475213824 |
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| author | Robert Kammerer Martin Mansfeld Jana Hänske Sophie Mißbach Xiaocui He Bernd Köllner Susan Mouchantat Wolfgang Zimmermann |
| author_facet | Robert Kammerer Martin Mansfeld Jana Hänske Sophie Mißbach Xiaocui He Bernd Köllner Susan Mouchantat Wolfgang Zimmermann |
| author_sort | Robert Kammerer |
| collection | DOAJ |
| description | Abstract Background Expansions of gene families are predictive for ongoing genetic adaptation to environmental cues. We describe such an expansion of the carcinoembryonic antigen (CEA) 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. Results 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. Conclusions 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. |
| first_indexed | 2024-12-23T14:50:01Z |
| format | Article |
| id | doaj.art-e1925070498d4e31b8628fe8a6499a07 |
| institution | Directory Open Access Journal |
| issn | 1471-2164 |
| language | English |
| last_indexed | 2024-12-23T14:50:01Z |
| publishDate | 2017-09-01 |
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| series | BMC Genomics |
| spelling | doaj.art-e1925070498d4e31b8628fe8a6499a072022-12-21T17:42:58ZengBMCBMC Genomics1471-21642017-09-0118111410.1186/s12864-017-4106-7Recent expansion and adaptive evolution of the carcinoembryonic antigen family in bats of the Yangochiroptera subgroupRobert Kammerer0Martin Mansfeld1Jana Hänske2Sophie Mißbach3Xiaocui He4Bernd Köllner5Susan Mouchantat6Wolfgang Zimmermann7Institute of Immunology, Friedrich-Loeffler InstituteInstitute of Immunology, Friedrich-Loeffler InstituteInstitute of Immunology, Friedrich-Loeffler InstituteInstitute of Immunology, Friedrich-Loeffler InstituteInstitute of Immunology, Friedrich-Loeffler InstituteInstitute of Immunology, Friedrich-Loeffler InstituteJunior Research Group Wildlife Diseases, Friedrich-Loeffler-InstituteTumor Immunology Laboratory, LIFE Center, University Clinic, Ludwig-Maximilians-UniversityAbstract Background Expansions of gene families are predictive for ongoing genetic adaptation to environmental cues. We describe such an expansion of the carcinoembryonic antigen (CEA) 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. Results 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. Conclusions 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.http://link.springer.com/article/10.1186/s12864-017-4106-7Carcinoembryonic antigen gene familyPregnancy-specific glycoproteinsPositive selectionChiropteraImmunoglobulin superfamilyBats |
| spellingShingle | Robert Kammerer Martin Mansfeld Jana Hänske Sophie Mißbach Xiaocui He Bernd Köllner Susan Mouchantat Wolfgang Zimmermann Recent expansion and adaptive evolution of the carcinoembryonic antigen family in bats of the Yangochiroptera subgroup BMC Genomics Carcinoembryonic antigen gene family Pregnancy-specific glycoproteins Positive selection Chiroptera Immunoglobulin superfamily Bats |
| title | Recent expansion and adaptive evolution of the carcinoembryonic antigen family in bats of the Yangochiroptera subgroup |
| title_full | Recent expansion and adaptive evolution of the carcinoembryonic antigen family in bats of the Yangochiroptera subgroup |
| title_fullStr | Recent expansion and adaptive evolution of the carcinoembryonic antigen family in bats of the Yangochiroptera subgroup |
| title_full_unstemmed | Recent expansion and adaptive evolution of the carcinoembryonic antigen family in bats of the Yangochiroptera subgroup |
| title_short | Recent expansion and adaptive evolution of the carcinoembryonic antigen family in bats of the Yangochiroptera subgroup |
| title_sort | recent expansion and adaptive evolution of the carcinoembryonic antigen family in bats of the yangochiroptera subgroup |
| topic | Carcinoembryonic antigen gene family Pregnancy-specific glycoproteins Positive selection Chiroptera Immunoglobulin superfamily Bats |
| url | http://link.springer.com/article/10.1186/s12864-017-4106-7 |
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