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Citation for Study 20145

Citation title: "Coevolution of paired receptors in Xenopus carcinoembryonic antigen-related cell adhesion molecule families suggests appropriation as pathogen receptors".

Study name: "Coevolution of paired receptors in Xenopus carcinoembryonic antigen-related cell adhesion molecule families suggests appropriation as pathogen receptors".

This study is part of submission 20145 (Status: Published).

Citation

Zimmermann W., & Kammerer R. 2016. Coevolution of paired receptors in Xenopus carcinoembryonic antigen-related cell adhesion molecule families suggests appropriation as pathogen receptors. BMC Genomics, 17: 928.

Authors

• Zimmermann W.
• Kammerer R. (submitter)

Abstract

Background In mammals, CEACAM1 and closely related members represent paired receptors with similar extracellular ligand-binding regions and cytoplasmic domains with opposing functions. Human CEACAM1 and CEACAM3 which have inhibitory ITIM/ITSM and activating ITAM-like motifs, respectively, in their cytoplasmic regions are such paired receptors. Various bacterial pathogens bind to CEACAM1 on epithelial and immune cells facilitating both entry into the host and down-regulation of the immune response whereas interaction with granulocyte-specific CEACAM3 leads to their uptake and destruction. It is unclear whether paired CEACAM receptors also exist in other vertebrate clades. Results We identified more than 80 ceacam genes in Xenopus tropicalis and X. laevis. They consist of two subgroups containing one or two putative paired receptor pairs each. Analysis of genomic sequences of paired receptors provide evidence that their highly similar ligand binding domains were adjusted by recent gene conversion events. In contrast, selection for diversification is observed among inhibitory receptor orthologs of the two frogs which split some 60 million years ago. The allotetraploid X. laevis arose later by hybridization of two closely related species. Interestingly, despite the conservation of the genomic landscape surrounding the homeologous ceacam loci only one locus resembles the one found in X. tropicalis. From the second X. laevis locus more than 80 % of the ceacam genes were lost including 5 of the 6 paired receptor genes. This suggests that once the gene for one of the paired receptors is lost the remaining gene cluster degrades rapidly probably due to lack of selection pressure exerted by pathogens. Conclusions The presence of paired receptors and selection for diversification suggests that also in amphibians CEACAM1-related inhibitory proteins are or were used as pathogen receptors.

Keywords

Carcinoembryonic antigen-related cell-cell adhesion molecule (CEACAM), Paired receptors, Positive selection, Allotetraploid, Xenopus, Amphibia, ITIM, ITAM, Immunoglobulin superfamily

External links

• DOI: 10.1186/s12864-016-3279-9
• Other URL: http://bmcgenomics.biomedcentral.com/articles/10.1186/s12864-016-3279-9

About this resource

• Canonical resource URI: http://purl.org/phylo/treebase/phylows/study/TB2:S20145
• Other versions: Nexus NeXML
• Show BibTeX reference

  		@ARTICLE{TreeBASE2Ref26529,
  	 author = {Wolfgang  Zimmermann and Robert  Kammerer},
  	 title = {Coevolution of paired receptors in Xenopus carcinoembryonic antigen-related cell adhesion molecule families suggests appropriation as pathogen receptors},
  	 year = {2016},
  	 keywords = {Carcinoembryonic antigen-related cell-cell adhesion molecule (CEACAM), Paired receptors, Positive selection, Allotetraploid, Xenopus, Amphibia, ITIM, ITAM, Immunoglobulin superfamily},
  	 doi = {10.1186/s12864-016-3279-9},
  	 url = {http://bmcgenomics.biomedcentral.com/articles/10.1186/s12864-016-3279-9},
  	 pmid = {},
  	 journal = {BMC Genomics},
  	 volume = {17},
  	 number = {},
  	 pages = {928},
  	 abstract = {Background
  
  In mammals, CEACAM1 and closely related members represent paired receptors with similar extracellular ligand-binding regions and cytoplasmic domains with opposing functions. Human CEACAM1 and CEACAM3 which have inhibitory ITIM/ITSM and activating ITAM-like motifs, respectively, in their cytoplasmic regions are such paired receptors. Various bacterial pathogens bind to CEACAM1 on epithelial and immune cells facilitating both entry into the host and down-regulation of the immune response whereas interaction with granulocyte-specific CEACAM3 leads to their uptake and destruction. It is unclear whether paired CEACAM receptors also exist in other vertebrate clades.
  
  Results
  
  We identified more than 80 ceacam genes in Xenopus tropicalis and X. laevis. They consist of two subgroups containing one or two putative paired receptor pairs each. Analysis of genomic sequences of paired receptors provide evidence that their highly similar ligand binding domains were adjusted by recent gene conversion events. In contrast, selection for diversification is observed among inhibitory receptor orthologs of the two frogs which split some 60 million years ago. The allotetraploid X. laevis arose later by hybridization of two closely related species. Interestingly, despite the conservation of the genomic landscape surrounding the homeologous ceacam loci only one locus resembles the one found in X. tropicalis. From the second X. laevis locus more than 80 % of the ceacam genes were lost including 5 of the 6 paired receptor genes. This suggests that once the gene for one of the paired receptors is lost the remaining gene cluster degrades rapidly probably due to lack of selection pressure exerted by pathogens.
  
  Conclusions
  
  The presence of paired receptors and selection for diversification suggests that also in amphibians CEACAM1-related inhibitory proteins are or were used as pathogen receptors.}
  }
  		

• Show RIS reference

  		TY  - JOUR
  ID  - 26529
  AU  - Zimmermann,Wolfgang 
  AU  - Kammerer,Robert 
  T1  - Coevolution of paired receptors in Xenopus carcinoembryonic antigen-related cell adhesion molecule families suggests appropriation as pathogen receptors
  PY  - 2016
  KW  - Carcinoembryonic antigen-related cell-cell adhesion molecule (CEACAM)
  KW  - Paired receptors
  KW  - Positive selection
  KW  - Allotetraploid
  KW  - Xenopus
  KW  - Amphibia
  KW  - ITIM
  KW  - ITAM
  KW  - Immunoglobulin superfamily
  UR  - http://bmcgenomics.biomedcentral.com/articles/10.1186/s12864-016-3279-9
  N2  - Background
  
  In mammals, CEACAM1 and closely related members represent paired receptors with similar extracellular ligand-binding regions and cytoplasmic domains with opposing functions. Human CEACAM1 and CEACAM3 which have inhibitory ITIM/ITSM and activating ITAM-like motifs, respectively, in their cytoplasmic regions are such paired receptors. Various bacterial pathogens bind to CEACAM1 on epithelial and immune cells facilitating both entry into the host and down-regulation of the immune response whereas interaction with granulocyte-specific CEACAM3 leads to their uptake and destruction. It is unclear whether paired CEACAM receptors also exist in other vertebrate clades.
  
  Results
  
  We identified more than 80 ceacam genes in Xenopus tropicalis and X. laevis. They consist of two subgroups containing one or two putative paired receptor pairs each. Analysis of genomic sequences of paired receptors provide evidence that their highly similar ligand binding domains were adjusted by recent gene conversion events. In contrast, selection for diversification is observed among inhibitory receptor orthologs of the two frogs which split some 60 million years ago. The allotetraploid X. laevis arose later by hybridization of two closely related species. Interestingly, despite the conservation of the genomic landscape surrounding the homeologous ceacam loci only one locus resembles the one found in X. tropicalis. From the second X. laevis locus more than 80 % of the ceacam genes were lost including 5 of the 6 paired receptor genes. This suggests that once the gene for one of the paired receptors is lost the remaining gene cluster degrades rapidly probably due to lack of selection pressure exerted by pathogens.
  
  Conclusions
  
  The presence of paired receptors and selection for diversification suggests that also in amphibians CEACAM1-related inhibitory proteins are or were used as pathogen receptors.
  L3  - 10.1186/s12864-016-3279-9
  JF  - BMC Genomics
  VL  - 17
  IS  - 
  ER  -