A Novel System of Polymorphic and Diverse NK Cell Receptors in Primates

Averdam, Anne; Petersen, Beatrix; Rosner, Cornelia; Neff, Jennifer; Roos, Christian; Eberle, M.; Aujard, Fabienne; Münch, Claudia; Schempp, Werner; Carrington, Mary; Shiina, Takashi; Inoko, Hidetoshi; Knaust, Florian; Coggill, Penny; Sehra, Harminder; Beck, Stephan; Abi-Rached, Laurent; Reinhardt, Richard; Walter, Lutz

doi:10.1371/journal.pgen.1000688

Cited by 72 publications

(106 citation statements)

References 44 publications

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“…The loss of MHC-A and its function as a classical MHC class I gene of MHC-G either happened in the lineage leading to platyrrhine primates (New World monkeys) or, alternatively, the specialized function of MHC-G and the classical function of MHC-A genes evolved in the lineage leading to catarrhine primates (Old World monkeys, apes, and humans). Unfortunately, strepsirrhine primates, such as lemurs, are not informative because the MHC class I genes of these species do not show a particularly close relationship with any of the simian MHC class I lineages (27).…”

Section: Discussionmentioning

confidence: 99%

Genomic Sequence Analysis of the MHC Class I G/F Segment in Common Marmoset (Callithrix jacchus)

Kono

Brameier

Roos

et al. 2014

The Journal of Immunology

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The common marmoset (Callithrix jacchus) is a New World monkey that is used frequently as a model for various human diseases. However, detailed knowledge about the MHC is still lacking. In this study, we sequenced and annotated a total of 854 kb of the common marmoset MHC region that corresponds to the HLA-A/G/F segment (Caja-G/F) between the Caja-G1 and RNF39 genes. The sequenced region contains 19 MHC class I genes, of which 14 are of the MHC-G (Caja-G) type, and 5 are of the MHC-F (Caja-F) type. Six putatively functional Caja-G and Caja-F genes (Caja-G1, Caja-G3, Caja-G7, Caja-G12, Caja-G13, and Caja-F4), 13 pseudogenes related either to Caja-G or Caja-F, three non-MHC genes (ZNRD1, PPPIR11, and RNF39), two miscRNA genes (ZNRD1-AS1 and HCG8), and one non-MHC pseudogene (ETF1P1) were identified. Phylogenetic analysis suggests segmental duplications of units consisting of basically five (four Caja-G and one Caja-F) MHC class I genes, with subsequent expansion/deletion of genes. A similar genomic organization of the Caja-G/F segment has not been observed in catarrhine primates, indicating that this genomic segment was formed in New World monkeys after the split of New World and Old World monkeys.

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Section: Discussionmentioning

confidence: 99%

Genomic Sequence Analysis of the MHC Class I G/F Segment in Common Marmoset (Callithrix jacchus)

Kono

Brameier

Roos

et al. 2014

The Journal of Immunology

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“…Some non‐human simian species show a comparable level of diversity and complexity in KIR haplotypes to humans 214. However, there are extensive differences in size and organization between the KIR loci of higher primate species 215. It is evident in primates that different lineages of KIR genes have been expanded concomitantly with species‐specific evolution of MHC class I genes 216.…”

Section: Kir Model Systemsmentioning

confidence: 99%

Deciphering the killer‐cell immunoglobulin‐like receptor system at super‐resolution for natural killer and T‐cell biology

et al. 2016

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SummaryKiller‐cell immunoglobulin‐like receptors (KIRs) are components of two fundamental biological systems essential for human health and survival. First, they contribute to host immune responses, both innate and adaptive, through their expression by natural killer cells and T cells. Second, KIR play a key role in regulating placentation, and hence reproductive success. Analogous to the diversity of their human leucocyte antigen class I ligands, KIR are extremely polymorphic. In this review, we describe recent developments, fuelled by methodological advances, that are helping to decipher the KIR system in terms of haplotypes, polymorphisms, expression patterns and their ligand interactions. These developments are delivering deeper insight into the relevance of KIR in immune system function, evolution and disease.

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“…Although cattle and simian primates both have diverse KIR gene families, they are clearly the products of independent expansions [34]. Further emphasizing the restriction of diverse KIR3DL to the simian primates, prosimian primates have expanded and diversified the CD94 and NKG2 families of NKC genes in the context of their non-functional KIR [20]. Particularly extreme in their divergence from the human situation are rodents (for example mouse and rat), who use diverse families of NKC-encoded Ly49 receptors as their variable NK-cell receptors for MHC class I [36,37].…”

Section: Counterparts To the Human Killer Cell Immunoglobulin-like Rementioning

confidence: 99%

Human-specific evolution of killer cell immunoglobulin-like receptor recognition of major histocompatibility complex class I molecules

Parham

Norman

Abi-Rached

et al. 2012

Phil. Trans. R. Soc. B

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In placental mammals, natural killer (NK) cells are a population of lymphocytes that make unique contributions to immune defence and reproduction, functions essential for survival of individuals, populations and species. Modulating these functions are conserved and variable NK-cell receptors that recognize epitopes of major histocompatibility complex (MHC) class I molecules. In humans, for example, recognition of human leucocyte antigen (HLA)-E by the CD94:NKG2A receptor is conserved, whereas recognition of HLA-A, B and C by the killer cell immunoglobulin-like receptors (KIRs) is diversified. Competing demands of the immune and reproductive systems, and of T-cell and NK-cell immunity-combined with the segregation on different chromosomes of variable NK-cell receptors and their MHC class I ligands-drive an unusually rapid evolution that has resulted in unprecedented levels of species specificity, as first appreciated from comparison of mice and humans. Counterparts to human KIR are present only in simian primates. Observed in these species is the coevolution of KIR and the four MHC class I epitopes to which human KIR recognition is restricted. Unique to hominids is the emergence of the MHC-C locus as a supplier of specialized and superior ligands for KIR. This evolutionary trend is most highly elaborated in the chimpanzee. Unique to the human KIR locus are two groups of KIR haplotypes that are present in all human populations and subject to balancing selection. Group A KIR haplotypes resemble chimpanzee KIR haplotypes and are enriched for genes encoding KIR that bind HLA class I, whereas group B KIR haplotypes are enriched for genes encoding receptors with diminished capacity to bind HLA class I. Correlating with their balance in human populations, B haplotypes favour reproductive success, whereas A haplotypes favour successful immune defence. Evolution of the B KIR haplotypes is thus unique to the human species.

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A Novel System of Polymorphic and Diverse NK Cell Receptors in Primates

Cited by 72 publications

References 44 publications

Genomic Sequence Analysis of the MHC Class I G/F Segment in Common Marmoset (Callithrix jacchus)

Genomic Sequence Analysis of the MHC Class I G/F Segment in Common Marmoset (Callithrix jacchus)

Deciphering the killer‐cell immunoglobulin‐like receptor system at super‐resolution for natural killer and T‐cell biology

Human-specific evolution of killer cell immunoglobulin-like receptor recognition of major histocompatibility complex class I molecules

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