Bimodal evolution of the killer cell Ig-like receptor (KIR) family in New World primates
- 192 Downloads
The immunoglobulin-like receptor (KIR) gene family in New World primates (Platyrrhini) has been characterized only in the owl monkey (Aotus sp.). To gain a better understanding of the KIR system in Platyrrhini, we analyzed a KIR haplotype in Ateles geoffroyi, and sequenced KIR complementary DNAs (cDNAs) from other three Atelidae species, Ateles hybridus, Ateles belzebuth, and Lagothrix lagotricha. Atelidae expressed a variable set of activating and inhibitory KIRs that diversified independently from their Catarrhini counterparts. They had a unique mechanism to generate activating receptors from inhibitory ones, involving a single nucleotide deletion in exon 7 and a change in the donor splice site of intron 7. The A. geoffroyi haplotype contained at least six gene models including a pseudogene, two coding inhibitory receptors, and three coding activating receptors. The centromeric region was in a tail-to-tail orientation with respect to the telomeric region. The owl monkey KIR haplotype shared this organization, and in phylogenetic trees, the centromeric genes clustered together with those of A. geoffroyi, whereas their telomeric genes clustered independently. KIR cDNAs from the other Atelidae species conformed to this pattern. Signatures of positive selection were found in residues predicted to interact with the major histocompatibility complex. Such signatures, however, primarily explained variability between paralogous genes but not between alleles in a locus. Atelidae, therefore, has expanded the KIR family in a bimodal fashion, where an inverted centromeric region has remained relatively conserved and the telomeric region has diversified by a rapid process of gene duplication and divergence, likely favored by positive selection for ligand binding.
KeywordsKIR Killer cell Ig-like receptor New World primates Atelidae
This work was supported by a grant from the Universidad Nacional de Colombia’s Research Division to LFC. We thank Marcela Fuquen and Alejandro Cerón for technical support. Colombia’s Ministry of the Environment and Sustainable Development authorized the access to genetic resources for scientific research without commercial interests (contract no. 1 of 2012).
- Averdam A, Petersen B, Rosner C, Neff J, Roos C, Eberle M, Aujard F, Munch C, Schempp W, Carrington M, Shiina T, Inoko H, Knaust F, Coggill P, Sehra H, Beck S, Abi-Rached L, Reinhardt R, Walter L (2009) A novel system of polymorphic and diverse NK cell receptors in primates. PLoS Genet 5(10):e1000688PubMedCrossRefGoogle Scholar
- Hershkovitz P (1977) Living New World monkeys (Platyrrhini) with an introduction to primates, vol 1. University of Chicago Press, ChicagoGoogle Scholar
- Vivian JP, Duncan RC, Berry R, O'Connor GM, Reid HH, Beddoe T, Gras S, Saunders PM, Olshina MA, Widjaja JM, Harpur CM, Lin J, Maloveste SM, Price DA, Lafont BA, McVicar DW, Clements CS, Brooks AG, Rossjohn J (2011) Killer cell immunoglobulin-like receptor 3DL1-mediated recognition of human leukocyte antigen B. Nature 479(7373):401–405PubMedCrossRefGoogle Scholar