Recent expansion and adaptive evolution of the carcinoembryonic antigen family in bats of the Yangochiroptera subgroup.

Publisher: BioMed Central Country of Publication: England NLM ID: 100965258 Publication Model: Electronic Cited Medium: Internet ISSN: 1471-2164 (Electronic) Linking ISSN: 14712164 NLM ISO Abbreviation: BMC Genomics Subsets: MEDLINE

Original Publication: London : BioMed Central, [2000-

Absorption, Physiological* ; Evolution, Molecular* ; Gene Expression Regulation*; Carcinoembryonic Antigen/*genetics ; Carcinoembryonic Antigen/*metabolism ; Chiroptera/*genetics ; Chiroptera/*physiology; Amino Acid Sequence ; Animals ; Base Sequence ; Carcinoembryonic Antigen/chemistry ; Phylogeny ; Sequence Homology, Nucleic Acid

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.

J Reprod Fertil. 1979 May;56(1):417-29. (PMID: 381657)
Nat Microbiol. 2016 Oct 17;2:16189. (PMID: 27748768)
Viruses. 2014 Dec;6(12):4880-901. (PMID: 25494448)
PLoS Curr. 2011 Feb 04;3:RRN1212. (PMID: 21327164)
Mol Phylogenet Evol. 2003 Aug;28(2):297-307. (PMID: 12878466)
Mol Microbiol. 2001 Feb;39(4):850-62. (PMID: 11251807)
Braz J Infect Dis. 2008 Dec;12(6):466-8. (PMID: 19287830)
Reproduction. 2016 Sep;152(3):171-84. (PMID: 27280409)
Sci Rep. 2016 Jun 13;6:27726. (PMID: 27291671)
Trends Ecol Evol. 2009 Jul;24(7):351-4. (PMID: 19482373)
Bioinformatics. 2005 Sep 15;21(18):3674-6. (PMID: 16081474)
Nat Immunol. 2008 Nov;9(11):1270-8. (PMID: 18836450)
J Exp Zool B Mol Dev Evol. 2008 Jul 15;310(5):428-49. (PMID: 18481267)
BMC Evol Biol. 2010 Jun 15;10:181. (PMID: 20550670)
Gene. 2004 Sep 15;339:99-109. (PMID: 15363850)
PLoS One. 2014 Apr 17;9(4):e94106. (PMID: 24743304)
Science. 2005 Jan 28;307(5709):580-4. (PMID: 15681385)
Nature. 2015 Jan 15;517(7534):386-90. (PMID: 25363763)
BMC Evol Biol. 2007 Oct 18;7:196. (PMID: 17945019)
Nat Biotechnol. 2011 May 15;29(7):644-52. (PMID: 21572440)
Int J Dev Biol. 2014;58(2-4):273-80. (PMID: 25023693)
Nucleic Acids Res. 2006 Jul 1;34(Web Server issue):W293-7. (PMID: 16845012)
Eur J Immunol. 1998 Nov;28(11):3664-74. (PMID: 9842909)
BMC Genomics. 2012 Jun 20;13:261. (PMID: 22716473)
Mol Biol Evol. 2015 May;32(5):1365-71. (PMID: 25701167)
BMC Biol. 2010 Feb 04;8:12. (PMID: 20132533)
Science. 2013 Jan 25;339(6118):456-60. (PMID: 23258410)
Zoonoses Public Health. 2013 Feb;60(1):104-16. (PMID: 23302292)
J Immunol. 2001 Jun 1;166(11):6537-44. (PMID: 11359805)
J Virol. 1991 Dec;65(12):6881-91. (PMID: 1719235)
Mol Microbiol. 2004 May;52(4):963-83. (PMID: 15130118)
Bioinformatics. 2006 Dec 15;22(24):3096-8. (PMID: 17110367)
Mol Biol Evol. 2007 Jul;24(7):1553-61. (PMID: 17449895)
PLoS Genet. 2012;8(7):e1002764. (PMID: 22807683)
Science. 2010 Sep 3;329(5996):1197-201. (PMID: 20813953)
BMC Genomics. 2016 Nov 16;17(1):928. (PMID: 27852220)
Infect Immun. 2015 Apr;83(4):1372-83. (PMID: 25605771)
Nat Microbiol. 2016 Oct 17;2:16188. (PMID: 27748756)
Mol Biol Evol. 2010 Jun;27(6):1221-5. (PMID: 20123797)
Genome Biol Evol. 2014 May 23;6(6):1314-26. (PMID: 24858421)
Front Microbiol. 2012 Feb 24;3:68. (PMID: 22375141)
Cell Commun Signal. 2014 Apr 15;12:27. (PMID: 24735478)
Mob DNA. 2016 Jul 22;7:12. (PMID: 27489570)

Keywords: Bats; Carcinoembryonic antigen gene family; Chiroptera; Immunoglobulin superfamily; Positive selection; Pregnancy-specific glycoproteins

0 (Carcinoembryonic Antigen)

Date Created: 20170913 Date Completed: 20180430 Latest Revision: 20240326

20240326

PMC5594555

10.1186/s12864-017-4106-7

28893191