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Immunogenetics

, Volume 65, Issue 10, pp 725–736 | Cite as

Bimodal evolution of the killer cell Ig-like receptor (KIR) family in New World primates

  • Luis F. Cadavid
  • Catalina Palacios
  • Juan S. Lugo
Original Paper

Abstract

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.

Keywords

KIR Killer cell Ig-like receptor New World primates Atelidae 

Notes

Acknowledgments

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).

Supplementary material

251_2013_719_MOESM1_ESM.doc (103 kb)
Supplementary Fig. 1 Deduced amino acid sequence alignment of Platyrrhini KIRs. Atge, A. geoffroyi; Athy, A. hybridus; Atbe, A. belzebuth; Lala, L. lagotricha; Om, owl monkey. (DOC 103 kb)
251_2013_719_Fig5_ESM.jpg (656 kb)
Supplementary Fig. 2

Homology modeling of Platyrrhini predicted KIR3DL proteins. a QMEAN4 values and root mean square deviation (RMSD) for representative structure models from the four Platyrrhini clades showed in Fig. 3b. Structure models were constructed using as template the crystallized structure of KIR3DL1*001 (PDB 3VH8). The allele KIR3DL1*031 was also modeled to be used as a baseline comparison. b Superposition analysis between KIR3DL1*001 (gray) and the structural model with the highest RMSD value, Atge-KIR3DL2 (blue), showing a nearly exact match. (JPEG 655 kb)

251_2013_719_MOESM2_ESM.eps (7.6 mb)
High resolution image (EPS 7778 kb)
251_2013_719_Fig6_ESM.jpg (7.6 mb)
Supplementary Fig. 3

Atelidae KIR3DL sequences are divided into three classes according the length and presence of functional motifs in the cytoplasmic domain. (JPEG 7771 kb)

251_2013_719_MOESM3_ESM.eps (1.3 mb)
High resolution image (EPS 1380 kb)

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Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Luis F. Cadavid
    • 1
  • Catalina Palacios
    • 1
    • 2
  • Juan S. Lugo
    • 1
  1. 1.Department of Biology and Institute of GeneticsUniversidad Nacional de ColombiaBogotáColombia
  2. 2.Department of Biological SciencesUniversidad de los AndesBogotáColombia

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