A splice site mutation converts an inhibitory killer cell Ig-like receptor into an activating one

Molecular Immunology

Volumn 46, Issue 4, 2009, Pages 640-648

  Blokhuis, Jeroen H ^a   Doxiadis, Gaby G M ^a   Bontrop, Ronald E ^a  

^a BIOMEDICAL PRIMATE RESEARCH CENTRE   (Netherlands)

Author keywords

Evolution; KIR; Natural killer cells; Primates; Splicing

Indexed keywords

KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR;

ANIMAL CELL; ARTICLE; CONVERGENT EVOLUTION; EXON; GENE; GENE MUTATION; GENETIC POLYMORPHISM; GENETIC TRANSCRIPTION; GENOMICS; INTRON; MMKIR3DH GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIMATE; PRIORITY JOURNAL; PROTEIN FUNCTION; RHESUS MONKEY;

ALLELES; ALTERNATIVE SPLICING; AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; EXONS; INTRONS; KILLER CELLS, NATURAL; MACACA MULATTA; MOLECULAR SEQUENCE DATA; MUTATION; PHYLOGENY; POLYMORPHISM, GENETIC; RECEPTORS, KIR; RNA SPLICE SITES; SEQUENCE ALIGNMENT;

ANIMALIA; MACACA MULATTA; PRIMATES;

EID: 58249102944     PISSN: 01615890     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molimm.2008.08.270     Document Type: Article

References (65)

1. Abi-Rached L., and Parham P. Natural selection drives recurrent formation of activating killer cell immunoglobulin-like receptor and Ly49 from inhibitory homologues. J. Exp. Med. 201 (2005) 1319-1332
2. Alter G., Martin M.P., Teigen N., Carr W.H., Suscovich T.J., Schneidewind A., Streeck H., Waring M., Meier A., Brander C., Lifson J.D., Allen T.M., Carrington M., and Altfeld M. Differential natural killer cell-mediated inhibition of HIV-1 replication based on distinct KIR/HLA subtypes. J. Exp. Med. 204 (2007) 3027-3036
3. Andersen H., Rossio J.L., Coalter V., Poore B., Martin M.P., Carrington M., and Lifson J.D. Characterization of rhesus macaque natural killer activity against a rhesus-derived target cell line at the single-cell level. Cell Immunol. 231 (2004) 85-95
4. Artavanis-Tsakonas K., Eleme K., McQueen K.L., Cheng N.W., Parham P., Davis D.M., and Riley E.M. Activation of a subset of human NK cells upon contact with Plasmodium falciparum-infected erythrocytes. J. Immunol. 171 (2003) 5396-5405
5. Bontrop R.E. Non-human primates: essential partners in biomedical research. Immunol. Rev. 183 (2001) 5-9
6. Bontrop R.E., Otting N., de Groot N.G., and Doxiadis G.G. Major histocompatibility complex class II polymorphisms in primates. Immunol. Rev. 167 (1999) 339-350
7. Canavez F., Young N.T., Guethlein L.A., Rajalingam R., Khakoo S.I., Shum B.P., and Parham P. Comparison of chimpanzee and human leukocyte Ig-like receptor genes reveals framework and rapidly evolving genes. J. Immunol. 167 (2001) 5786-5794
8. Colonna M., and Samaridis J. Cloning of immunoglobulin-superfamily members associated with HLA-C and HLA-B recognition by human natural killer cells. Science 268 (1995) 405-408
9. Doxiadis G.G., de Groot N., Claas F.H., Doxiadis I.I., van Rood J.J., and Bontrop R.E. A highly divergent microsatellite facilitating fast and accurate DRB haplotyping in humans and rhesus macaques. Proc. Natl. Acad. Sci. U.S.A. 104 (2007) 8907-8912
10. Doxiadis G.G., Rouweler A.J., de Groot N.G., Louwerse A., Otting N., Verschoor E.J., and Bontrop R.E. Extensive sharing of MHC class II alleles between rhesus and cynomolgus macaques. Immunogenetics 58 (2006) 259-268
11. Draghi M., Yawata N., Gleimer M., Yawata M., Valiante N.M., and Parham P. Single-cell analysis of the human NK cell response to missing self and its inhibition by HLA class I. Blood 105 (2005) 2028-2035
12. Faure M., and Long E.O. KIR2DL4 (CD158d), an NK cell-activating receptor with inhibitory potential. J. Immunol. 168 (2002) 6208-6214
13. Feng J., Call M.E., and Wucherpfennig K.W. The assembly of diverse immune receptors is focused on a polar membrane-embedded interaction site. PLoS Biol. 4 (2006) e142
14. Ferrini S., Cambiaggi A., Meazza R., Sforzini S., Marciano S., Mingari M.C., and Moretta L. T cell clones expressing the natural killer cell-related p58 receptor molecule display heterogeneity in phenotypic properties and p58 function. Eur. J. Immunol. 24 (1994) 2294-2298
15. Gardiner C.M., Guethlein L.A., Shilling H.G., Pando M., Carr W.H., Rajalingam R., Vilches C., and Parham P. Different NK cell surface phenotypes defined by the DX9 antibody are due to KIR3DL1 gene polymorphism. J. Immunol. 166 (2001) 2992-3001
16. Gedil M.A., Steiner N.K., and Hurley C.K. Genomic characterization of KIR2DL4 in families and unrelated individuals reveals extensive diversity in exon and intron sequences including a common frameshift variation occurring in several alleles. Tissue Antigens 65 (2005) 402-418
17. Goodridge J.P., Lathbury L.J., Steiner N.K., Shulse C.N., Pullikotil P., Seidah N.G., Hurley C.K., Christiansen F.T., and Witt C.S. Three common alleles of KIR2DL4 (CD158d) encode constitutively expressed, inducible and secreted receptors in NK cells. Eur. J. Immunol. 37 (2007) 199-211
18. Grendell R.L., Hughes A.L., and Golos T.G. Cloning of rhesus monkey killer-cell Ig-like receptors (KIRs) from early pregnancy decidua. Tissue Antigens 58 (2001) 329-334
19. Guethlein L.A., Flodin L.R., Adams E.J., and Parham P. NK cell receptors of the orangutan (Pongo pygmaeus): a pivotal species for tracking the coevolution of killer cell Ig-like receptors with MHC-C. J. Immunol. 169 (2002) 220-229
20. Guethlein L.A., Older Aguilar A.M., Abi-Rached L., and Parham P. Evolution of killer cell Ig-like receptor (KIR) genes: definition of an orangutan KIR haplotype reveals expansion of lineage III KIR associated with the emergence of MHC-C. J. Immunol. 179 (2007) 491-504
21. Hershberger K.L., Kurian J., Korber B.T., and Letvin N.L. Killer cell immunoglobulin-like receptors (KIR) of the African-origin sabaeus monkey: evidence for recombination events in the evolution of KIR. Eur. J. Immunol. 35 (2005) 922-935
22. Hershberger K.L., Shyam R., Miura A., and Letvin N.L. Diversity of the killer cell Ig-like receptors of rhesus monkeys. J. Immunol. 166 (2001) 4380-4390
23. Hiby S.E., Walker J.J., O'Shaughnessy K.M., Redman C.W., Carrington M., Trowsdale J., and Moffett A. Combinations of maternal KIR and fetal HLA-C genes influence the risk of preeclampsia and reproductive success. J. Exp. Med. 200 (2004) 957-965
24. Hsu K.C., Gooley T., Malkki M., Pinto-Agnello C., Dupont B., Bignon J.D., Bornhauser M., Christiansen F., Gratwohl A., Morishima Y., Oudshoorn M., Ringden O., van Rood J.J., and Petersdorf E. KIR ligands and prediction of relapse after unrelated donor hematopoietic cell transplantation for hematologic malignancy. Biol. Blood Marrow Transplant. 12 (2006) 828-836
25. Khakoo S.I., Rajalingam R., Shum B.P., Weidenbach K., Flodin L., Muir D.G., Canavez F., Cooper S.L., Valiante N.M., Lanier L.L., and Parham P. Rapid evolution of NK cell receptor systems demonstrated by comparison of chimpanzees and humans. Immunity 12 (2000) 687-698
26. LaBonte M.L., Hershberger K.L., Korber B., and Letvin N.L. The KIR and CD94/NKG2 families of molecules in the rhesus monkey. Immunol. Rev. 183 (2001) 25-40
27. Lanier L.L. NK cell receptors. Annu. Rev. Immunol. 16 (1998) 359-393
28. Lanier L.L., Corliss B.C., Wu J., Leong C., and Phillips J.H. Immunoreceptor DAP12 bearing a tyrosine-based activation motif is involved in activating NK cells. Nature 391 (1998) 703-707
29. Litwin V., Gumperz J., Parham P., Phillips J.H., and Lanier L.L. NKB1: a natural killer cell receptor involved in the recognition of polymorphic HLA-B molecules. J. Exp. Med. 180 (1994) 537-543
30. Marsh S.G., Parham P., Dupont B., Geraghty D.E., Trowsdale J., Middleton D., Vilches C., Carrington M., Witt C., Guethlein L.A., Shilling H., Garcia C.A., Hsu K.C., and Wain H. Killer-cell immunoglobulin-like receptor (KIR) nomenclature report, 2002. Immunogenetics 55 (2003) 220-226
31. Martin M.P., Bashirova A., Traherne J., Trowsdale J., and Carrington M. Cutting edge: expansion of the KIR locus by unequal crossing over. J. Immunol. 171 (2003) 2192-2195
32. Martin M.P., Pascal V., Yeager M., Phair J., Kirk G.D., Hoots K., O'Brien S.J., Anderson S.K., and Carrington M. A mutation in KIR3DS1 that results in truncation and lack of cell surface expression. Immunogenetics 59 (2007) 823-829
33. Middleton D., Meenagh A., and Gourraud P.A. KIR haplotype content at the allele level in 77 Northern Irish families. Immunogenetics 59 (2007) 145-158
34. Middleton D., Meenagh A., Moscoso J., and Arnaiz-Villena A. Killer immunoglobulin receptor gene and allele frequencies in Caucasoid, Oriental and Black populations from different continents. Tissue Antigens (2007)
35. Miller J.S., Cooley S., Parham P., Farag S.S., Verneris M.R., McQueen K.L., Guethlein L.A., Trachtenberg E.A., Haagenson M., Horowitz M.M., Klein J.P., and Weisdorf D.J. Missing KIR ligands are associated with less relapse and increased graft-versus-host disease (GVHD) following unrelated donor allogeneic HCT. Blood 109 (2007) 5058-5061
36. Moretta A., Sivori S., Vitale M., Pende D., Morelli L., Augugliaro R., Bottino C., and Moretta L. Existence of both inhibitory (p58) and activatory (p50) receptors for HLA-C molecules in human natural killer cells. J. Exp. Med. 182 (1995) 875-884
37. Nelson G.W., Martin M.P., Gladman D., Wade J., Trowsdale J., and Carrington M. Cutting edge: heterozygote advantage in autoimmune disease: hierarchy of protection/susceptibility conferred by HLA and killer Ig-like receptor combinations in psoriatic arthritis. J. Immunol. 173 (2004) 4273-4276
38. Otting N., de Vos-Rouweler A.J., Heijmans C.M., de Groot N.G., Doxiadis G.G., and Bontrop R.E. MHC class I A region diversity and polymorphism in macaque species. Immunogenetics 59 (2007) 367-375
39. Otting N., Heijmans C.M., Noort R.C., de Groot N.G., Doxiadis G.G., van Rood J.J., Watkins D.I., and Bontrop R.E. Unparalleled complexity of the MHC class I region in rhesus macaques. Proc. Natl. Acad. Sci. U.S.A. 102 (2005) 1626-1631
40. Parham P. Immunogenetics of killer cell immunoglobulin-like receptors. Mol. Immunol. 42 (2005) 459-462
41. Pende D., Biassoni R., Cantoni C., Verdiani S., Falco M., di Donato C., Accame L., Bottino C., Moretta A., and Moretta L. The natural killer cell receptor specific for HLA-A allotypes: a novel member of the p58/p70 family of inhibitory receptors that is characterized by three immunoglobulin-like domains and is expressed as a 140-kD disulphide-linked dimer. J. Exp. Med. 184 (1996) 505-518
42. Penedo M.C., Bontrop R.E., Heijmans C.M., Otting N., Noort R., Rouweler A.J., de Groot N., de Groot N.G., Ward T., and Doxiadis G.G. Microsatellite typing of the rhesus macaque MHC region. Immunogenetics 57 (2005) 198-209
43. Pertea M., Lin X., and Salzberg S.L. GeneSplicer: a new computational method for splice site prediction. Nucleic Acids Res. 29 (2001) 1185-1190
44. Rajagopalan S., Bryceson Y.T., Kuppusamy S.P., Geraghty D.E., van der Meer A., Joosten I., and Long E.O. Activation of NK cells by an endocytosed receptor for soluble HLA-G. PLoS Biol. 4 (2006) e9
45. Rajalingam R., Hong M., Adams E.J., Shum B.P., Guethlein L.A., and Parham P. Short KIR haplotypes in pygmy chimpanzee (Bonobo) resemble the conserved framework of diverse human KIR haplotypes. J. Exp. Med. 193 (2001) 135-146
46. Rajalingam R., Parham P., and Abi-Rached L. Domain shuffling has been the main mechanism forming new hominoid killer cell Ig-like receptors. J. Immunol. 172 (2004) 356-369
47. Roberts C.H., Madrigal J.A., and Marsh S.G. Cloning and sequencing alleles of the KIR2DL4 gene from genomic DNA samples. Tissue Antigens 69 (2007) 88-91
48. Roberts C.H., Turino C., Madrigal J.A., and Marsh S.G. Enrichment of individual KIR2DL4 sequences from genomic DNA using long-template PCR and allele-specific hybridization to magnetic bead-bound oligonucleotide probes. Tissue Antigens 69 (2007) 597-601
49. Sambrook J.G., Bashirova A., Andersen H., Piatak M., Vernikos G.S., Coggill P., Lifson J.D., Carrington M., and Beck S. Identification of the ancestral killer immunoglobulin-like receptor gene in primates. BMC Genomics 7 (2006) 209
50. Sambrook J.G., Bashirova A., Palmer S., Sims S., Trowsdale J., Abi-Rached L., Parham P., Carrington M., and Beck S. Single haplotype analysis demonstrates rapid evolution of the killer immunoglobulin-like receptor (KIR) loci in primates. Genome Res. 15 (2005) 25-35
51. Schellekens J., Rozemuller E.H., Petersen E.J., van den Tweel J.G., Verdonck L.F., and Tilanus M.G. Activating KIRs exert a crucial role on relapse and overall survival after HLA-identical sibling transplantation. Mol. Immunol. 45 (2008) 2255-2261
52. Schellekens J., Tilanus M.G., and Rozemuller E.H. The elucidation of KIR2DL4 gene polymorphism. Mol. Immunol. (2007)
53. Shahjahan Miah S.M., Hughes T.L., and Campbell K.S. KIR2DL4 differentially signals downstream functions in human NK cells through distinct structural modules. J. Immunol. 180 (2008) 2922-2932
54. Slierendregt B.L., van Noort J.T., Bakas R.M., Otting N., Jonker M., and Bontrop R.E. Evolutionary stability of transspecies major histocompatibility complex class II DRB lineages in humans and rhesus monkeys. Hum. Immunol. 35 (1992) 29-39
55. Swofford, D.L., 2003, PAUP*: Phylogenetic Analysis Using Parsimony (*and other methods), Version 4. Sinauer Associates, Sunderland.
56. Thananchai H., Gillespie G., Martin M.P., Bashirova A., Yawata N., Yawata M., Easterbrook P., McVicar D.W., Maenaka K., Parham P., Carrington M., Dong T., and Rowland-Jones S. Cutting edge: allele-specific and peptide-dependent interactions between KIR3DL1 and HLA-A and HLA-B. J. Immunol. 178 (2007) 33-37
57. Uhrberg M., Valiante N.M., Shum B.P., Shilling H.G., Lienert-Weidenbach K., Corliss B., Tyan D., Lanier L.L., and Parham P. Human diversity in killer cell inhibitory receptor genes. Immunity 7 (1997) 753-763
58. Uhrberg M., Valiante N.M., Young N.T., Lanier L.L., Phillips J.H., and Parham P. The repertoire of killer cell Ig-like receptor and CD94:NKG2A receptors in T cells: clones sharing identical alpha beta TCR rearrangement express highly diverse killer cell Ig-like receptor patterns. J. Immunol. 166 (2001) 3923-3932
59. Valiante N.M., Lienert K., Shilling H.G., Smits B.J., and Parham P. Killer cell receptors: keeping pace with MHC class I evolution. Immunol. Rev. 155 (1997) 155-164
60. VandenBussche C.J., Dakshanamurthy S., Posch P.E., and Hurley C.K. A single polymorphism disrupts the killer Ig-like receptor 2DL2/2DL3 D1 domain. J. Immunol. 177 (2006) 5347-5357
61. Vierboom M.P., Jonker M., Bontrop R.E., and t Hart B. Modeling human arthritic diseases in nonhuman primates. Arthhritis Res. Ther. 7 (2005) 145-154
62. Vilches C., and Parham P. KIR: diverse, rapidly evolving receptors of innate and adaptive immunity. Annu. Rev. Immunol. 20 (2002) 217-251
63. Wagtmann N., Biassoni R., Cantoni C., Verdiani S., Malnati M.S., Vitale M., Bottino C., Moretta L., Moretta A., and Long E.O. Molecular clones of the p58 NK cell receptor reveal immunoglobulin-related molecules with diversity in both the extra- and intracellular domains. Immunity 2 (1995) 439-449
64. Wende H., Volz A., and Ziegler A. Extensive gene duplications and a large inversion characterize the human leukocyte receptor cluster. Immunogenetics 51 (2000) 703-713
65. Wilson M.J., Torkar M., Haude A., Milne S., Jones T., Sheer D., Beck S., and Trowsdale J. Plasticity in the organization and sequences of human KIR/ILT gene families. Proc. Natl. Acad. Sci. U.S.A. 97 (2000) 4778-4783