The killer immunoglobulin-like receptor gene cluster: Tuning the genome for defense

Annual Review of Genomics and Human Genetics

Volumn 7, Issue , 2006, Pages 277-300

  Bashirova, Arman A ^a   Martin, Maureen P ^b   McVicar, Daniel W ^c   Carrington, Mary ^b  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b SAIC FREDERICK INC   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Immune genes; Immune receptors; Innate immunity; NK cell

Indexed keywords

IMMUNOGLOBULIN RECEPTOR; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR; LIGAND; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; NATURAL KILLER CELL RECEPTOR;

ALLOTYPE; CHROMOSOME 19Q; GENE CLUSTER; GENE LOCUS; GENE STRUCTURE; GENETIC ORGANIZATION; GENETIC POLYMORPHISM; GENETIC VARIABILITY; GENOME; HAPLOTYPE; INNATE IMMUNITY; NATURAL KILLER CELL; NUCLEOTIDE SEQUENCE; RECEPTOR GENE; REVIEW; SEQUENCE HOMOLOGY;

GENOME, HUMAN; HUMANS; MULTIGENE FAMILY; POLYMORPHISM, GENETIC; RECEPTORS, KIR;

EID: 33750356775     PISSN: 15278204     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.genom.7.080505.115726     Document Type: Review

References (158)

1. Abi-Rached L, Parham P. 2005. Natural selection drives recurrent formation of activating killer cell immunoglobulin-like receptor and Ly49 from inhibitory homologues. J. Exp. Med. 201:1319-32
2. Arnheim L, Dillner J, Sanjeevi CB. 2005. A population-based cohort study of KIR genes and genotypes in relation to cervical intraepithelial neoplasia. Tissue Antigens 65:252-59
3. Arnon TI, Achdout H, Lieberman N, Gazit R, Gonen-Gross T, et al. 2004. The mechanisms controlling the recognition of tumor- and virus-infected cells by NKp46. Blood 103:664-72
4. Artavanis-Tsakonas K, Eleme K, McQueen KL, Cheng NW, Parham P, et al. 2003. Activation of a subset of human NK cells upon contact with Plasmodium falciparum-infected erythrocytes. J. Immunol. 171:5396-405
5. Bagot M, Moretta A, Sivori S, Biassoni R, Cantoni C, et al. 2001. CD4(+) cutaneous T-cell lymphoma cells express the p140-killer cell immunoglobulin-like receptor. Blood 97:1388-91
6. Biassoni R, Falco M, Cambiaggi A, Costa P, Verdiani S, et al. 1995. Amino acid substitutions can influence the natural killer (NK)-mediated recognition of HLA-C molecules. Role of serine-77 and lysine-80 in the target cell protection from lysis mediated by "group 2" or "group 1" NK clones. J. Exp. Med. 182:605-9
7. Biassoni R, Pessino A, Malaspina A, Cantoni C, Bottino C, et al. 1997. Role of amino acid position 70 in the binding affinity of p50.1 and p58.1 receptors for HLA-Cw4 molecules. Eur. J. Immunol. 27:3095-99
8. Boyington JC, Motyka SA, Schuck P, Brooks AG, Sun PD. 2000. Crystal structure of an NK cell immunoglobulin-like receptor in complex with its class I MHC ligand. Nature 405:537-43
9. Boyington JC, Sun PD. 2002. A structural perspective on MHC class I recognition by killer cell immunoglobulin-like receptors. Mol. Immunol. 38:1007-21
10. Boyton RJ, Smith J, Ward R, Jones M, Ozerovitch L, et al. 2006. HLA-C and killer cell immunoglobulin-like receptor (KIR) genes in idiopathic bronchiectasis. Am. J. Respir. Crit. Care Med. 173:327-33
11. Butsch Kovacic M, Martin M, Gao X, Fuksenko T, Chen CJ, et al. 2005. Variation of the killer cell immunoglobulin-like receptors and HLA-C genes in nasopharyngeal carcinoma. Cancer Epidemiol. Biomarkers Prev. 14:2673-77
12. Carosella ED, Moreau P, Le Maoult J, Le Discorde M, Dausset J, Rouas-Freiss N. 2003. HLA-G molecules: from maternal-fetal tolerance to tissue acceptance. Adv. Immunol. 81:199-252
13. Carr WH, Pando MJ, Parham P. 2005. KIR3DL1 polymorphisms that affect NK cell inhibition by HLA-Bw4 ligand. J. Immunol. 175:5222-29
14. Carrington M, Martin MP. 2006. The impact of variation at the KIR gene cluster on human disease. Curr. Top Microbiol. Immunol. 298:225-57
15. Carrington M, Norman P. 2003. The KIR Gene Cluster: U.S. Natl. Library Med., National Center for Biotechnology Information, Bethesda, MD. http://www. ncbi.nlm.nih.gov/entrez/query.fcgi?db=Books
16. Carrington M, Wang S, Martin MP, Gao X, Schiffman M, et al. 2005. Hierarchy of resistance to cervical neoplasia mediated by combinations of killer immunoglobulin-like receptor and human leukocyte antigen loci. J. Exp. Med. 201:1069-75
17. Cella M, Longo A, Ferrara GB, Strominger JL, Colonna M. 1994. NK3-specific natural killer cells are selectively inhibited by Bw4-positive HLA alleles with isoleucine 80. J. Exp. Med. 180:1235-42
18. Chan AT, Kollnberger SD, Wedderburn LR, Bowness P. 2005. Expansion and enhanced survival of natural killer cells expressing the killer immunoglobulin-like receptor KIR3DL2 in spondylarthritis. Arthritis Rheum. 52:3586-95
19. Chan HW, Kurago ZB, Stewart CA, Wilson MJ, Martin MP, et al. 2003. DNA methylation maintains allele-specific KIR gene expression in human natural killer cells. J. Exp. Med. 197:245-55
20. Chan HW, Miller JS, Moore MB, Lutz CT. 2005. Epigenetic control of highly homologous killer Ig-like receptor gene alleles. J. Immunol. 175:5966-74
21. Colonna M, Borsellino G, Falco M, Ferrara GB, Strominger JL. 1993. HLA-C is the inhibitory ligand that determines dominant resistance to lysis by NK1- and NK2-specific natural killer cells. Proc. Natl. Acad. Sci. USA 90:12000-4
22. Cook M, Briggs D, Craddock C, Mahendra P, Milligan D, et al. 2006. Donor KIR genotype has a major influence on the rate of cytomegalovirus reactivation following T-cell replete stem cell transplantation. Blood 107:1230-32
23. Crum KA, Logue SE, Curran MD, Middleton D. 2000. Development of a PCR-SSOP approach capable of defining the natural killer cell inhibitory receptor (KIR) gene sequence repertoires. Tissue Antigens 56:313-26
24. Daza-Vamenta R, Glusman G, Rowen L, Guthrie B, Geraghty DE. 2004. Genetic divergence of the rhesus macaque major histocompatibility complex. Genome Res. 14:1501-15
25. Dohring C, Scheidegger D, Samaridis J, Cella M, Colonna M. 1996. A human killer inhibitory receptor specific for HLA-A1,2. J. Immunol. 156:3098-101
26. Epling-Burnette PK, Painter JS, Chaurasia P, Bai F, Wei S, et al. 2004. Dysregulated NK receptor expression in patients with lymphoproliferative disease of granular lymphocytes. Blood 103:3431-39
27. Fan QR, Long EO, Wiley DC. 2001. Crystal structure of the human natural killer cell inhibitory receptor KIR2DL1-HLA-Cw4 complex. Nat. Immunol. 2:452-60
28. Fernandez NC, Treiner E, Vance KE, Jamieson AM, Lemieux S, Raulet DH. 2005. A subset of natural killer cells achieves self-tolerance without expressing inhibitory receptors specific for self-MHC molecules. Blood 105:4416-23
29. Franco EL. 1995. Cancer causes revisited: human papillomavirus and cervical neoplasia. J. Natl. Cancer Inst. 87:779-80
30. Frohn C, Schlenke P, Kirchner H. 1997. The repertoire of HLA-Cw-specific NK cell receptors CD158 a/b (EB6 and GL183) in individuals with different HLA phenotypes. Immunology 92:567-70
31. Gagnier L, Wilhelm BT, Mager DL. 2003. Ly49 genes in non-rodent mammals. Immunogenetics 55:109-15
32. Gardiner CM, Guethlein LA, Shilling HG, Pando M, Carr WH, et al. 2001. Different NK cell surface phenotypes defined by the DX9 antibody are due to KIR3DL1 gene polymorphism. J. Immunol. 166:2992-3001
33. Gardiner CM, Guethlein LA, Shilling HG, Pando M, Carr WH, et al. 2001. Different NK cell surface phenotypes defined by the DX9 antibody are due to KIR3DL1 gene polymorphism. J. Immunol. 166:2992-3001
34. Gomez-Lozano N, Estefania E, Williams F, Halfpenny I, Middleton D, et al. 2005. The silent KIR3DP1 gene (CD158c) is transcribed and might encode a secreted receptor in a minority of humans, in whom the KIR3DP1, KIR2DL4 and KIR3DL1/KIR3DS1 genes are duplicated. Eur. J. Immunol. 35:16-24
35. Goodridge JP, Witt CS, Christiansen FT, Warren HS. 2003. KIR2DL4(CD158d) genotype influences expression and function in NK cells. J. Immunol. 171:1768-74
36. Grendell RL, Hughes AL, Golos TG. 2001. Cloning of rhesus monkey killer-cell Ig-like receptors (KIRs) from early pregnancy decidua. Tissue Antigens 58:329-34
37. Guethlein LA, Flodin LR, Adams EJ, Parham P. 2002. 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. 169:220-29
38. Gumperz JE, Litwin V, Phillips JH, Lanier LL, Parham P. 1995. The Bw4 public epitope of HLA-B molecules confers reactivity with natural killer cell clones that express NKB1, a putative HLA receptor. J. Exp. Med. 181:1133-44
39. Gumperz JE, Valiante NM, Parham P, Lanier LL, Tyan D. 1996. Heterogeneous phenotypes of expression of the NKB1 natural killer cell class I receptor among individuals of different human histocompatibility leukocyte antigens types appear genetically regulated, but not linked to major histocompatibililty complex haplotype. J. Exp. Med. 183:1817-27
40. Hansasuta P, Dong T, Thananchai H, Weekes M, Willberg C, et al. 2004. Recognition of HLA-A3 and HLA-A11 by KIR3DL2 is peptide-specific. Eur. J. Immunol. 34:1673-79
41. Hershberger KL, Kurian J, Korber BT, Letvin NL. 2005. Killer cell immunoglobulin-like receptors (KIR) of the African-origin sabaeus monkey: evidence for recombination events in the evolution of KIR. Eur. J. Immunol. 35:922-35
42. Hershberger KL, Shyam R, Miura A, Letvin NL. 2001. Diversity of the killer cell Ig-like receptors of rhesus monkeys. J. Immunol. 166:4380-90
43. Hiby SE, Walker JJ, O'Shaughnessy KM, Redman CW, Carrington M, et al. 2004. Combinations of maternal KIR and fetal HLA-C genes influence the risk of preeclampsia and reproductive success. J. Exp. Med. 200:957-65
44. Hoelsbrekken SE, Nylenna O, Saether PC, Slettedal IO, Ryan JC, et al. 2003. Cutting edge: molecular cloning of a killer cell Ig-like receptor in the mouse and rat. J. Immunol. 170:2259-63
45. Holm SJ, Sakuraba K, Mallbris L, Wolk K, Stahle M, Sanchez FO. 2005. Distinct HLA-C/KIR genotype profile associates with guttate psoriasis. J. Invest. Dermatol. 125:721-30
46. Hsu KC, Chida S, Geraghty DE, Dupont B. 2002. The killer cell immunoglobulin-like receptor (KIR) genomic region: gene-order, haplotypes and allelic polymorphism. Immunol. Rev. 190:40-52
47. Hsu KC, Liu XR, Selvakumar A, Mickelson E, O'Reilly RJ, Dupont B. 2002. Killer Ig-like receptor haplotype analysis by gene content: evidence for genomic diversity with a minimum of six basic framework haplotypes, each with multiple subsets. J. Immunol. 169:5118-29
48. Jiang K, Zhu FM, Lv QF, Yan LX. 2005. Distribution of killer cell immunoglobulin-like receptor genes in the Chinese Han population. Tissue Antigens 65:556-63
49. Karlhofer FM, Ribaudo RK, Yokoyama WM. 1992. MHC class I alloantigen specificity of Ly-49+ IL-2-activated natural killer cells. Nature 358:66-70
50. Kärre K, Ljunggren HG, Piontek G, Kiessling R. 1986. Selective rejection of H-2-deficient lymphoma variants suggests alternative immune defence strategy. Nature 319:675-78
51. Katz G, Gazit R, Arnon TI, Gonen-Gross T, Tarcic G, et al. 2004. MHC class I-independent recognition of NK-activating receptor KIR2DS4. J. Immunol. 173:1819-25
52. Katz G, Markel G, Mizrahi S, Arnon TI, Mandelboim O. 2001. Recognition of HLA-Cw4 but not HLA-Cw6 by the NK cell receptor killer cell Ig-like receptor two-domain short tail number 4. J. Immunol. 166:7260-67
53. Khakoo SI, Rajalingam R, Shum BP, Weidenbach K, Flodin L, et al. 2000. Rapid evolution of NK cell receptor systems demonstrated by comparison of chimpanzees and humans. Immunity 12:687-98
54. Khakoo SI, Thio CL, Martin MP, Brooks CR, Gao X, et al. 2004. HLA and NK cell inhibitory receptor genes in resolving hepatitis C virus infection. Science 305:872-74
55. Kiepiela P, Leslie AJ, Honeyborne I, Ramduth D, Thobakgale C, et al. 2004. Dominant influence of HLA-B in mediating the potential co-evolution of HIV and HLA. Nature 432:769-75
56. Kikuchi-Maki A, Catina TL, Campbell KS. 2005. Cutting edge: KIR2DL4 transduces signals into human NK cells through association with the Fc receptor gamma protein. J. Immunol. 174:3859-63
57. Kikuchi-Maki A, Yusa S, Catina TL, Campbell KS. 2003. KIR2DL4 is an IL-2-regulated NK cell receptor that exhibits limited expression in humans but triggers strong IFN-gamma production. J. Immunol. 171:3415-25
58. Kim S, Poursine-Laurent J, Truscott SM, Lybarger L, Song YJ, et al. 2005. Licensing of natural killer cells by host major histocompatibility complex class I molecules. Nature 436:709-13
59. Lanier LL. 2005. NK cell recognition. Annu. Rev. Immunol. 23:225-74
60. Lanier LL, Corliss BC, Wu J, Leong C, Phillips JH. 1998. Immunoreceptor DAP12 bearing a tyrosine-based activation motif is involved in activating NK cells. Nature 391:703-7
61. Ljunggren HG, Karre K. 1990. In search of the "missing self": MHC molecules and NK cell recognition. Immunol. Today 11:237-44
62. Lopez-Vazquez A, Mina-Blanco A, Martinez-Borra J, Njobvu PD, Suarez-Alvarez B, et al. 2005. Interaction between KIR3DL1 and HLA-B*57 supertype alleles influences the progression of HIV-1 infection in a Zambian population. Hum. Immunol. 66:285-89
63. Lopez-Vazquez A, Rodrigo L, Martinez-Borra J, Perez R, Rodriguez M, et al. 2005. Protective effect of the HLA-Bw4I80 epitope and the killer cell immunoglobulin-like receptor 3DS1 gene against the development of hepatocellular carcinoma in patients with hepatitis C virus infection. J. Infect. Dis. 192:162-65
64. Luszczek W, Manczak M, Cislo M, Nockowski P, Wisniewski A, et al. 2004. Gene for the activating natural killer cell receptor, KIR2DS1, is associated with susceptibility to psoriasis vulgaris. Hum. Immunol. 65:758-66
65. Maeda N, Izumiya C, Oguri H, Kusume T, Yamamoto Y, Fukaya T. 2002. Aberrant expression of intercellular adhesion molecule-1 and killer inhibitory receptors induces immune tolerance in women with pelvic endometriosis. Fertil. Steril. 77:679-83
66. Maeda N, Izumiya C, Yamamoto Y, Oguri H, Kusume T, Fukaya T. 2002. Increased killer inhibitory receptor KIR2DL1 expression among natural killer cells in women with pelvic endometriosis. Fertil. Steril. 77:297-302
67. Maenaka K, Juji T, Nakayama T, Wyer JR, Gao GF, et al. 1999. Killer cell immunoglobulin receptors and T cell receptors bind peptide-major histocompatibility complex class I with distinct thermodynamic and kinetic properties. J. Biol. Chem. 274:28329-34
68. Mager DL, McQueen KL, Wee V, Freeman JD. 2001. Evolution of natural killer cell receptors: coexistence of functional Ly49 and KIR genes in baboons. Curr. Biol 11:626-30
69. Malnati MS, Peruzzi M, Parker KC, Biddison WE, Ciccone E, et al. 1995. Peptide specificity in the recognition of MHC class I by natural killer cell clones. Science 267:1016-18
70. Mandelboim O, Wilson SB, Vales-Gomez M, Reyburn HT, Strominger JL. 1997. Self and viral peptides can initiate lysis by autologous natural killer cells. Proc. Natl. Acad. Sci. USA 94:4604-9
71. Martin AM, Freitas EM, Witt CS, Christiansen FT. 2000. The genomic organization and evolution of the natural killer immunoglobulin-like receptor (KIR) gene cluster. Immunogenetics 51:268-80
72. Martin AM, Kulski JK, Gaudieri S, Witt CS, Freitas EM, et al. 2004. Comparative genomic analysis, diversity and evolution of two KIR haplotypes A and B. Gene 335:121-31
73. Martin MP, Bashirova A, Traherne J, Trowsdale J, Carrington M. 2003. Cutting edge: expansion of the KIR locus by unequal crossing over. J. Immunol. 171:2192-95
74. Martin MP, Gao X, Lee JH, Nelson GW, Detels R, et al. 2002. Epistatic interaction between KIR3DS1 and HLA-B delays the progression to AIDS. Nat. Genet. 31:429-34
75. Martin MP, Nelson G, Lee JH, Pellett F, Gao X, et al. 2002. Cutting edge: susceptibility to psoriatic arthritis: influence of activating killer Ig-like receptor genes in the absence of specific HLA-C alleles. J. Immunol. 169:2818-22
76. McQueen KL, Wilhelm BT, Harden KD, Mager DL. 2002. Evolution of NK receptors: a single Ly49 and multiple KIR genes in the cow. Eur. J. Immunol. 32:810-17
77. Miller JS, McCullar V. 2001. Human natural killer cells with polyclonal lectin and immunoglobulinlike receptors develop from single hematopoietic stem cells with preferential expression of NKG2A and KIR2DL2/L3/S2. Blood 98:705-13
78. Moffett-King A. 2002. Natural killer cells and pregnancy. Nat. Rev. Immunol. 2:656-63
79. Momot T, Koch S, Hunzelmann N, Krieg T, Ulbricht K, et al. 2004. Association of killer cell immunoglobulin-like receptors with scleroderma. Arthritis Rheum. 50:1561-65
80. Moretta A, Tambussi G, Bottino C, Tripodi G, Merli A, et al. 1990. A novel surface antigen expressed by a subset of human CD3-CD16+ natural killer cells. Role in cell activation and regulation of cytolytic function. J. Exp. Med. 171:695-714
81. Moretta A, Vitale M, Bottino C, Orengo AM, Morelli L, et al. 1993. P58 molecules as putative receptors for major histocompatibility complex (MHC) class I molecules in human natural killer (NK) cells. Anti-p58 antibodies reconstitute lysis of MHC class I-protected cells in NK clones displaying different specificities. J. Exp. Med. 178:597-604
82. Morice WG, Kurtin PJ, Leibson PJ, Tefferi A, Hanson CA. 2003. Demonstration of aberrant T-cell and natural killer-cell antigen expression in all cases of granular lymphocytic leukaemia. Br. J. Haematol. 120:1026-36
83. Nakajima T, Goek O, Zhang X, Kopecky SL, Frye RL, et al. 2003. De novo expression of killer immunoglobulin-like receptors and signaling proteins regulates the cytotoxic function of CD4 T cells in acute coronary syndromes. Circ. Res. 93:106-13
84. Naumova E, Mihaylova A, Stoitchkov K, Ivanova M, Quin L, Toneva M. 2005. Genetic polymorphism of NK receptors and their ligands in melanoma patients: prevalence of inhibitory over activating signals. Cancer Immunol. Immunother. 54:172-78
85. Nelson GW, Martin MP, Gladman D, Wade J, Trowsdale J, Carrington M. 2004. 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. 173:4273-76
86. Nikitina-Zake L, Rajalingham R, Rumba I, Sanjeevi CB. 2004. Killer cell immunoglobulin-like receptor genes in Latvian patients with type 1 diabetes mellitus and healthy controls. Ann. N. Y. Acad. Sci. 1037:161-69
87. Norman PJ, Carrington CV, Byng M, Maxwell LD, Curran MD, et al. 2002. Natural killer cell immunoglobulin-like receptor (KIR) locus profiles in African and South Asian populations. Genes Immun. 3:86-95
88. Nowakowski GS, Morice WG, Phyliky RL, Li CY, Tefferi A. 2005. Human leucocyte antigen class I and killer immunoglobulin-like receptor expression patterns in T-cell large granular lymphocyte leukaemia. Br. J. Haematol. 128:490-92
89. Olcese L, Cambiaggi A, Semenzato G, Bottino C, Moretta A, Vivier E. 1997. Human killer cell activatory receptors for MHC class I molecules are included in a multimeric complex expressed by natural killer cells. J. Immunol. 158:5083-86
90. Pando MJ, Gardiner CM, Gleimer M, McQueen KL, Parham P. 2003. The protein made from a common allele of KIR3DL1 (3DL1*004) is poorly expressed at cell surfaces due to substitution at positions 86 in Ig domain 0 and 182 in Ig domain 1. J. Immunol. 171:6640-49
91. Parham P. 2005. MHC class I molecules and KIRs in human history, health and survival. Nat. Rev. Immunol. 5:201-14
92. Pascal V, Schleinitz N, Brunet C, Ravet S, Bonnet E, et al. 2004. Comparative analysis of NK cell subset distribution in normal and lymphoproliferative disease of granular lymphocyte conditions. Eur. J. Immunol. 34:2930-40
93. Pende D, Biassoni R, Cantoni C, Verdiani S, Falco M, et al. 1996. 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. 184:505-18
94. Peruzzi M, Parker KC, Long EO, Malnati MS. 1996. Peptide sequence requirements for the recognition of HLA-B*2705 by specific natural killer cells. J. Immunol. 157:3350-56
95. Ponte M, Cantoni C, Biassoni R, Tradori-Cappai A, Bentivoglio G, et al. 1999. Inhibitory receptors sensing HLA-G1 molecules in pregnancy: decidua-associated natural killer cells express LIR-1 and CD94/NKG2A and acquire p49, an HLA-G1-specific receptor. Proc. Natl. Acad. Sci. USA 96:5674-79
96. Poszepczynska-Guigne E, Schiavon V, D'Incan M, Echchakir H, Musette P, et al. 2004. CD158k/KIR3 DL2 is a new phenotypic marker of Sezary cells: relevance for the diagnosis and follow-up of Sezary syndrome. J. Invest. Dermatol. 122:820-23
97. Rajagopalan S, Bryceson YT, Kuppusamy SP, Geraghty DE, van der Meer A, et al. 2006. Activation of NK cells by an endocytosed receptor for soluble HLA-G. PLoS Biol. 1:70-86
98. Rajagopalan S, Fu J, Long EO. 2001. Cutting edge: induction of IFN-gamma production but not cytotoxicity by the killer cell Ig-like receptor KIR2DL4 (CD158d) in resting NK cells. J. Immunol. 167:1877-81
99. Rajagopalan S, Long EO. 1997. The direct binding of a p58 killer cell inhibitory receptor to human histocompatibility leukocyte antigen (HLA)-Cw4 exhibits peptide selectivity. J. Exp. Med. 185:1523-28
100. Rajagopalan S, Long EO. 1999. A human histocompatibility leukocyte antigen (HLA)-G-specific receptor expressed on all natural killer cells. J. Exp. Med. 189:1093-100
101. Rajalingam R, Hong M, Adams EJ, Shum BP, Guethlein LA, Parham P. 2001. Short KIR haplotypes in pygmy chimpanzee (Bonobo) resemble the conserved framework of diverse human KIR haplotypes. J. Exp. Med. 193:135-46
102. Rajalingam R, Parham P, Abi-Rached L. 2004. Domain shuffling has been the main mechanism forming new hominoid killer cell Ig-like receptors. J. Immunol. 172:356-69
103. Richardson J, Reyburn HT, Luque I, Vales-Gomez M, Strominger JL. 2000. Definition of polymorphic residues on killer Ig-like receptor proteins which contribute to the HLA-C binding site. Eur. J. Immunol. 30:1480-85
104. Roberts JM. 2003. Pre-eclampsia: a two-stage disorder. In Pre-eclampsia, ed. H Critchley, A MacLean, L Poston, J Walker, pp. 66-78. London: RCOG Press
105. Ruggeri L, Capanni M, Mancusi A, Aversa F, Martelli MF, Velardi A. 2004. Natural killer cells as a therapeutic tool in mismatched transplantation. Best Pract. Res. Clin. Haematol. 17:427-38
106. Ruggeri L, Capanni M, Mancusi A, Martelli MF, Velardi A. 2005. The impact of donor natural killer cell alloreactivity on allogeneic hematopoietic transplantation. Transpl. Immunol. 14:203-6
107. Ruggeri L, Capanni M, Mancusi A, Perruccio K, Burchielli E, et al. 2005. Natural killer cell alloreactivity in haploidentical hematopoietic stem cell transplantation. Int. J. Hematol. 81:13-17
108. Ruggeri L, Mancusi A, Perruccio K, Burchielli E, Martelli MF, Velardi A. 2005. Natural killer cell alloreactivity for leukemia therapy. J. Immunother. 28:175-82
109. Saleh A, Davies GE, Pascal V, Wright PW, Hodge DL, et al. 2004. Identification of probabilistic transcriptional switches in the Ly49 gene cluster: a eukaryotic mechanism for selective gene activation. Immunity. 21:55-66
110. Sambrook JG, Bashirova A, Palmer S, Sims S, Trowsdale J, et al. 2005. Single haplotype analysis demonstrates rapid evolution of the killer immunoglobulin-like receptor (KIR) loci in primates. Genome. Res. 15:25-35
111. Sambrook JG, Bashirova AA, Andersen H, Piatak M, Vernikos G, et al. 2005. Comparative Mapping of the KIR Regions in Primates. Presented at KIR Polymorphism Workshop, Cambridge, UK
112. Santourlidis S, Trompeter HI, Weinhold S, Eisermann B, Meyer KL, et al. 2002. Crucial role of DNA methylation in determination of clonally distributed killer cell Ig-like receptor expression patterns in NK cells. J. Immunol. 169:4253-61
113. Saulquin X, Gastinel LN, Vivier E. 2003. Crystal structure of the human natural killer cell activating receptor KIR2DS2 (CD158j). J. Exp. Med. 197:933-38
114. Shilling HG, Guethlein LA, Cheng NW, Gardiner CM, Rodriguez R, et al. 2002. Allelic polymorphism synergizes with variable gene content to individualize human KIR genotype. J. Immunol. 168:2307-15
115. Shilling HG, Young N, Guethlein LA, Cheng NW, Gardiner CM, et al. 2002. Genetic control of human NK cell repertoire. J. Immunol. 169:239-47
116. Stewart CA, Laugier-Anfossi F, Vely F, Saulquin X, Riedmuller J, et al. 2005. Recognition of peptide-MHC class I complexes by activating killer immunoglobulin-like receptors. Proc. Natl. Acad. Sci. USA 102:13224-29
117. Stewart CA, Van Bergen J, Trowsdale J. 2003. Different and divergent regulation of the KIR2DL4 and KIR3DL1 promoters. J. Immunol. 170:6073-81
118. Stewart-Jones GB, di Gleria K, Kollnberger S, McMichael AJ, Jones EY, Bowness P. 2005. Crystal structures and KIR3DL1 recognition of three immunodominant viral peptides complexed to HLA-B*2705. Eur. J. Immunol. 35:341-51
119. Storset AK, Slettedal IO, Williams JL, Law A, Dissen E. 2003. Natural killer cell receptors in cattle: a bovine killer cell immunoglobulin-like receptor multigene family contains members with divergent signaling motifs. Eur. J. Immunol. 33:980-90
120. Suzuki Y, Hamamoto Y, Ogasawara Y, Ishikawa K, Yoshikawa Y, et al. 2004. Genetic polymorphisms of killer cell immunoglobulin-like receptors are associated with susceptibility to psoriasis vulgaris. J. Invest. Dermatol. 122:1133-36
121. Takahashi T, Yawata M, Raudsepp T, Lear TL, Chowdhary BP, et al. 2004. Natural killer cell receptors in the horse: evidence for the existence of multiple transcribed LY49 genes. Eur. J. Immunol. 34:773-84
122. Takeno M, Shimoyama Y, Kashiwakura J, Nagafuchi H, Sakane T, Suzuki N. 2004. Abnormal killer inhibitory receptor expression on natural killer cells in patients with Behcet's disease. Rheumatol. Int. 24:212-16
123. Toneva M, Lepage V, Lafay G, Dulphy N, Busson M, et al. 2001. Genomic diversity of natural killer cell receptor genes in three populations. Tissue Antigens 57:358-62
124. Trinchieri G. 1989. Biology of natural killer cells. Adv. Immunol. 47:187-376
125. Trompeter HI, Gomez-Lozano N, Santourlidis S, Eisermann B, Wernet P, et al. 2005. Three structurally and functionally divergent kinds of promoters regulate expression of clonally distributed killer cell Ig-like receptors (KIR), of KIR2DL4, and of KIR3DL3. J. Immunol. 174:4135-43
126. Uhrberg M, Parham P, Wernet P. 2002. Definition of gene content for nine common group B haplotypes of the Caucasoid population: KIR haplotypes contain between seven and eleven KIR genes. Immunogenetics 54:221-29
127. Uhrberg M, Valiante NM, Shum BP, Shilling HG, Lienert-Weidenbach K, et al. 1997. Human diversity in killer cell inhibitory receptor genes. Immunity 7:753-63
128. Uhrberg M, Valiante NM, Young NT, Lanier LL, Phillips JH, Parham P. 2001. The repertoire of killer cell Ig-like receptor and CD94:NKG2 A receptors in T cells: clones sharing identical alpha beta TCR rearrangement express highly diverse killer cell Ig-like receptor patterns. J. Immunol. 166:3923-32
129. Vales-Gomez M, Reyburn H, Strominger J. 2000. Molecular analyses of the interactions between human NK receptors and their HLA ligands. Hum. Immunol. 61:28-38
130. Vales-Gomez M, Reyburn HT, Erskine RA, Strominger J. 1998. Differential binding to HLA-C of p50-activating and p58-inhibitory natural killer cell receptors. Proc. Natl. Acad. Sci. USA 95:14326-31
131. Valiante NM, Uhrberg M, Shilling HG, Lienert-Weidenbach K, Arnett KL, et al. 1997. Functionally and structurally distinct NK cell receptor repertoires in the peripheral blood of two human donors. Immunity 7:739-51
132. van Bergen J, Stewart CA, van den Elsen PJ, Trowsdale J. 2005. Structural and functional differences between the promoters of independently expressed killer cell Ig-like receptors. Eur. J. Immunol. 35:2191-99
133. van der Slik AR, Koeleman BP, Verduijn W, Bruining GJ, Roep BO, Giphart MJ. 2003. KIR in type 1 diabetes: disparate distribution of activating and inhibitory natural killer cell receptors in patients versus HLA-matched control subjects. Diabetes 52:2639-42
134. Varla-Leftherioti M. 2004. Role of a KIR/HLA-C allorecognition system in pregnancy. J. Reprod. Immunol. 62:19-27
135. Varla-Leftherioti M, Spyropoulou-Vlachou M, Keramitsoglou T, Papadimitropoulos M, Tsekoura C, et al. 2005. Lack of the appropriate natural killer cell inhibitory receptors in women with spontaneous abortion. Hum. Immunol. 66:65-71
136. Varla-Leftherioti M, Spyropoulou-Vlachou M, Niokou D, Keramitsoglou T, Darlamitsou A, et al. 2003. Natural killer (NK) cell receptors' repertoire in couples with recurrent spontaneous abortions. Am. J. Reprod. Immunol. 49:183-91
137. Verheyden S, Bernier M, Demanet C. 2004. Identification of natural killer cell receptor phenotypes associated with leukemia. Leukemia 18:2002-7
138. Volz A, Wende H, Laun K, Ziegler A. 2001. Genesis of the ILT/LIR/MIR clusters within the human leukocyte receptor complex. Immunol. Rev. 181:39-51
139. Wagtmann N, Rajagopalan S, Winter CC, Peruzzi M, Long EO. 1995. Killer cell inhibitory receptors specific for HLA-C and HLA-B identified by direct binding and by functional transfer. Immunity 3:801-9
140. Warren HS, Christiansen FT, Witt CS. 2003. Functional inhibitory human leucocyte antigen class I receptors on natural killer (NK) cells in patients with chronic NK lymphocytosis. Br. J. Haematol. 121:793-804
141. Wechsler J, Bagot M, Nikolova M, Parolini S, Martin-Garcia N, et al. 2003. Killer cell immunoglobulin-like receptor expression delineates in situ Sezary syndrome lymphocytes. J. Pathol. 199:77-83
142. Welch AY, Kasahara M, Spain LM. 2003. Identification of the mouse killer immunoglobulin-like receptor-like (Kirl) gene family mapping to chromosome X. Immunogenetics 54:782-90
143. Whang DH, Park H, Yoon JA, Park MH. 2005. Haplotype analysis of killer cell immunoglobulin-like receptor genes in 77 Korean families. Hum. Immunol. 66:146-54
144. Williams AP, Bateman AR, Khakoo SI. 2005. Hanging in the balance. KIR and their role in disease. Mol. Interv. 5:226-40
145. Williams F, Maxwell LD, Halfpenny IA, Meenagh A, Sleator C, et al. 2003. Multiple copies of KIR 3DL/S1 and KIR 2DL4 genes identified in a number of individuals. Hum. Immunol. 64:729-32
146. Wilson MJ, Torkar M, Haude A, Milne S, Jones T, et al. 2000. Plasticity in the organization and sequences of human KIR/ILT gene families. Proc. Natl. Acad. Sci. USA 97:4778-83
147. Winter CC, Gumperz JE, Parham P, Long EO, Wagtmann N. 1998. Direct binding and functional transfer of NK cell inhibitory receptors reveal novel patterns of HLA-C allotype recognition. J. Immunol. 161:571-77
148. Witt CS, Dewing C, Sayer DC, Uhrberg M, Parham P, Christiansen FT. 1999. Population frequencies and putative haplotypes of the killer cell immunoglobulin-like receptor sequences and evidence for recombination. Transplantation 68:1784-89
149. Witt CS, Whiteway JM, Warren HS, Barden A, Rogers M, et al. 2002. Alleles of the KIR2DL4 receptor and their lack of association with pre-eclampsia. Eur. J. Immunol. 32:18-29
150. Wu MY, Yang JH, Chao KH, Hwang JL, Yang YS, Ho HN. 2000. Increase in the expression of killer cell inhibitory receptors on peritoneal natural killer cells in women with endometriosis. Fertil. Steril. 74:1187-91
151. Yang JH, Chen MJ, Chen HF, Lee TH, Ho HN, Yang YS. 2004. Decreased expression of killer cell inhibitory receptors on natural killer cells in eutopic endometrium in women with adenomyosis. Hum. Reprod. 19:1974-78
152. Yawata M, Yawata N, Abi-Rached L, Parham P. 2002. Variation within the human killer cell immunoglobulin-like receptor (KIR) gene family. Crit. Rev. Immunol. 22:463-82
153. Yawata M, Yawata N, McQueen KL, Cheng NW, Guethlein LA, et al. 2002. Predominance of group A KIR haplotypes in Japanese associated with diverse NK cell repertoires of KIR expression. Immunogenetics 54:543-50
154. Yawata M, Yawata N, Draghi M, Little AM, Partheniou F, Parham P. 2006. Roles for HLA and KIR polymorphisms in natural killer cell repertoire selection and modulation of effector function. J. Exp. Med. 203:633-45
155. Yen JH, Moore BE, Nakajima T, Scholl D, Schaid DJ, et al. 2001. Major histocompatibility complex class I-recognizing receptors are disease risk genes in rheumatoid arthritis. J. Exp. Med. 193:1159-67
156. Zambello R, Falco M, Della Chiesa M, Trentin L, Carollo D, et al. 2003. Expression and function of KIR and natural cytotoxicity receptors in NK-type lymphoproliferative diseases of granular lymphocytes. Blood 102:1797-805
157. Zambello R, Semenzato G. 2003. Natural killer receptors in patients with lymphoproliferative diseases of granular lymphocytes. Semin. Hematol. 40:201-12
158. Zappacosta F, Borrego F, Brooks AG, Parker KC, Coligan JE. 1997. Peptides isolated from HLA-Cw*0304 confer different degrees of protection from natural killer cell-mediated lysis. Proc. Natl. Acad. Sci. USA 94:6313-18