Comparative genomics of natural killer cell receptor gene clusters

PLoS Genetics

Volumn 1, Issue 2, 2005, Pages 0129-0139

  Kelley, James ^a   Walter, Lutz ^b   Trowsdale, John ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b GERMAN PRIMATE CENTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 33646942320     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.0010027     Document Type: Review

References (123)

1. Trowsdale J (2001) Genetic and functional relationships between MHC and NK receptor genes. Immunity 15: 363-374.
2. Kasahara M, Suzuki T, Du Pasquier L (2004) On the origins of the adaptive immune system: Novel insights from invertebrates and cold-blooded vertebrates. Trends Immunol 25: 105-111.
3. Kelley J, Walter L, Trowsdale J (2005) Comparative genomics of major histocompatibility complexes. Immunogenetics 56: 683-695.
4. Parham P (2005) MHC class I molecules and KIRs in human history, health and survival. Nat Rev Immunol 5: 201-214.
5. Kelley JM, Trowsdale J (2005) Features of MHC and NK gene clusters. Transpl Immunol. In press.
6. Long EO (1999) Regulation of immune responses through inhibitory receptors. Ann Rev Immunol 17: 875-904.
7. Natarajan K, Dimasi N, Wang J, Mariuzza RA, Margulies DH (2002) Structure and function of natural killer cell receptors: Multiple molecular solutions to self, nonself discrimination. Ann Rev Immunol 20: 853-885.
8. Vely F, Vivier E (1997) Conservation of structural features reveals the existence of a large family of inhibitory cell surface receptors and noninhibitory/activatory counterparts. J Immunol 159: 2075-2077.
9. Stebbins CC, Watzl C, Billadeau DD, Leibson PJ, Burshtyn DN, et al. (2003) Vav1 dephosphorylation by the tyrosine phosphatase SHP-1 as a mechanism for inhibition of cellular cytotoxicity. Mol Cell Biol 23: 6291-6299.
10. Lanier LL (2001) On Guard-Activating NK cell receptors. Nat Immunol 2: 23-27.
11. Vivier E, Nunes JA, Vely F (2004) Natural killer cell signaling pathways. Science 306: 1517-1519.
12. 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: 3415-3425.
13. Trowsdale J, Barten R, Haude A, Stewart CA, Beck S, et al. (2001) The genomic context of natural killer receptor extended gene families. Immunol Rev 181: 20-38.
14. Wende H, Colonna M, Ziegler A, Volz A (1999) Organization of the leukocyte receptor cluster (LRC) on human chromosome 19q13.4. Mamm Genome 10: 154-160.
15. Martin AM, Kulski JK, Witt C, Pontarotti P, Christiansen FT (2002) Leukocyte Ig-like receptor complex (LRC) in mice and men. Trends Immunol 23: 81-88.
16. 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 U S A 97: 4778-4783.
17. 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: 268-280.
18. Vilches C, Parham P (2002) KIR: Diverse, rapidly evolving receptors of innate and adaptive immunity. Ann Rev Immunol 20: 217-251.
19. 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: 2192-2195.
20. 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: 3859-3863.
21. Torkar M, Haude A, Milne S, Beck S, Trowsdale J, et al. (2000) Arrangement of the ILT gene cluster: A common null allele of the ILT6 gene results from a 6.7-kbp deletion. Eur J Immunol 30: 3655-3662.
22. Kandil E, Egashira M, Miyoshi O, Niikawa N, Ishibashi T, et al. (1996) The human gene encoding the heavy chain of the major histocompatibility complex class I-like Fc receptor (FCGRT) maps to 19q13.3. Cytogenet Cell Genet 73: 97-98.
23. Munday J, Floyd H, Crocker PR (1999) Sialic acid binding receptors (Siglecs) expressed by macrophages. J Leukoc Biol 66: 705-711.
24. Hammarstrom S (1999) The carcinoembryonic antigen (CEA) family: Structures, suggested functions and expression in normal and malignant tissues. Semin Cancer Biol 9: 67-81.
25. Renedo M, Arce I, Rodriguez A, Carretero M, Lanier LL, et al. (1997) The human natural killer gene complex is located on chromosome 12p12-p13. Immunogenetics 46: 307-311.
26. Yokoyama WM, Plougastel BF (2003) Immune functions encoded by the natural killer gene complex. Nat Rev Immunol 3: 304-316.
27. Westgaard IH, Berg SF, Orstavik S, Fossum S, Dissen E (1998) Identification of a human member of the Ly-49 multigene family. Eur J Immunol 28: 1839-1846.
28. Lanier LL, Chang C, Phillips JH (1994) Human NKR-P1A. A disulfidelinked homodimer of the C-type lectin superfamily expressed by a subset of NK and T lymphocytes. J Immunol 153: 2417-2428.
29. Lazetic S, Chang C, Houchins JP, Lanier LL, Phillips JH (1996) Human natural killer cell receptors involved in MHC class I recognition are disulfide-linked heterodimers of CD94 and NKG2 Subunits. J Immunol 157: 4741-4745.
30. Braud VM, Allan DS, O'Callaghan CA, Soderstrom K, D'Andrea A, et al. (1998) HLA-E binds to natural killer cell receptors CD94/NKG2A, B and C. Nature 391: 795-799.
31. Vales-Gomez M, Reyburn HT, Erskine RA, Lopez-Botet M, Strominger JL (1999) Kinetics and peptide dependency of the binding of the inhibitory NK receptor CD94/NKG2-A and the activating receptor CD94/NKG2-C to HLA-E. EMBOJ 18: 4250-4260.
32. Plougastel B, TrowsdaleJ (1997) Cloning of NKG2-F, a new member of the NKG2 family of human natural killer cell receptor genes. Eur J Immunol 27: 2835-2839.
33. Wu J, Song Y, Bakker AB, Bauer S, Spies T, et al. (1999) An activating immunoreceptor complex formed by NKG2D and DAP10. Science 285: 730-732.
34. Billadeau DD, Upshaw JL, Schoon RA, Dick CJ, Leibson PJ (2003) NKG2D-DAP10 triggers human NK cell-mediated killing via a Syk-independent regulatory pathway. Nat Immunol 4: 557-564.
35. Cosman D, Mullberg J, Sutherland CL, Chin W, Armitage R, et al. (2001) ULBPs, novel MHC class I- related molecules, bind to CMV glycoprotein UL16 and stimulate NK cytotoxicity through the NKG2D receptor. Immunity 14: 123-133.
36. Guthmann MD, Tal M, Pecht I (1995) A new member of the C-type lectin family is a modulator of the mast cell secretory response. Int ArchAllergy Immunol 107: 82-86.
37. Hamann J, Montgomery KT, Lau S, Kucherlapati R, van Lier RA (1997) AICL: A new activation-induced antigen encoded by the human NK gene complex. Immunogenetics 45: 295-300.
38. Boles KS, Barten R, Kumaresan PR, Trowsdale J, Mathew PA (1999) Cloning of a new lectin-like receptor expressed on human NK cells. Immunogenetics 50: 1-7.
39. Bull C, Sobanov Y, Rohrdanz B, O'Brien J, Lehrach H, et al. (2000) The centromeric part of the human NK gene complex: Linkage of LOX-1 and LY49L with the CD94/NKG2 region. Genes Immun 1: 280-287.
40. Sobanov Y, Bernreiter A, Derdak S, Mechtcheriakova D, Schweighofer B, et al. (2001) A novel cluster of lectin-like receptor genes expressed in monocytic, dendritic and endothelial cells maps close to the NK receptor genes in the human NK gene complex. Eur J Immunol 31: 3493-3503.
41. 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.
42. 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: 687-698.
43. 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: 356-369.
44. 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: 220-229.
45. LaBonte ML, Hershberger KL, Korber B, Letvin NL (2001) The KIR and CD94/NKG2 families of molecules in the rhesus monkey. Immunol Rev 183: 25-40.
46. Hershberger KL, Shyam R, Miura A, Letvin NL (2001) Diversity of the killer cell Ig-like receptors of rhesus monkeys. J Immunol 166: 4380-4390.
47. 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: 922-935.
48. Adams EJ, Parham P (2001) Species-specific evolution of MHC class I genes in the higher primates. Immunol Rev 183: 41-64.
49. Adams EJ, Thomson G, Parham P (1999) Evidence for an HLA-C-like locus in the orangutan Pongo pygmaeus. Immunogenetics 49: 865-871.
50. 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. Procs Nat Acad Sci U S A 90: 12000-12004.
51. 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: 872-874.
52. 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: 2818-2822.
53. van der Slik AR, Koeleman BP, Verduijn W, Bruining GJ, Roep BO, et al. (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: 2639-2642.
54. 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: 1159-1167.
55. Cook MA, Milligan DW, Fegan CD, Darbyshire PJ, Mahendra P, et al. (2004) The impact of donor KIR and patient HLA-C genotypes on outcome following HLA-identical sibling hematopoietic stem cell transplantation for myeloid leukemia. Blood 103: 1521-1526.
56. King A, Hiby SE, Gardner L, Joseph S, Bowen JM, et al. (2000) Recognition of trophoblast HLA class I molecules by decidual NK cell receptors - A review. Placenta 2: S81-S85.
57. Canavez F, Young NT, Guethlein LA, Rajalingam R, Khakoo SI, et al. (2001) Comparison of chimpanzee and human leukocyte Ig-like receptor genes reveals framework and rapidly evolving genes. J Immunol 167: 5786-5794.
58. Shum BP, Flodin LR, Muir DG, Rajalingam R, Khakoo SI, et al. (2002) Conservation and variation in human and common chimpanzee CD94 and NKG2 genes. J Immunol 168: 240-252.
59. Barten R, Trowsdale J (1999) The human Ly-49L gene. Immunogenetics 49: 731-734.
60. 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: 626-630.
61. 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: 782-790.
62. 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: 2259-2263.
63. Bryceson YT, Foster JA, Kuppusamy SP, Herkenham M, Long EO (2005) Expression of a killer cell receptor-like gene in plastic regions of the central nervous system. J Neuroimmunol 161: 177-182.
64. Kubagawa H, Cooper MD, Chen CC, Ho LH, Alley TL, et al. (1999) Paired immunoglobulin-like receptors of activating and inhibitory types. Curr Top Microbiol Immunol 244: 137-149.
65. Liang S, Baibakov B, Horuzsko A (2002) HLA-G inhibits the functions of murine dendritic cells via the PIR-B immune inhibitory receptor. Eur J Immunol 32: 2418-2426.
66. Maruoka T, Nagata T, Kasahara M (2004) Identification of the rat IgA Fc receptor encoded in the leukocyte receptor complex. Immunogenetics 55: 712-716.
67. Iizuka K, Naidenko OV, Plougastel BF, Fremont DH, Yokoyama WM (2003) Genetically linked C-type lectin-related ligands for the NKRP1 family of natural killer cell receptors. Nature Immunology 4: 801-807.
68. Chambers WH, Vujanovic NL, DeLeo AB, Olszowy MW, Herberman RB, et al. (1989) Monoclonal antibody to a triggering structure expressed on rat natural killer cells and adherent lymphokine-activated killer cells. J Exp Med 169: 1373-1389.
69. Giorda R, Rudert WA, Vavassori C, Chambers WH, Hiserodt JC, et al. (1990) NKRP1, a signal transduction molecule on natural killer cells. Science 249: 1298-1300.
70. Barten R, Torkar M, Haude A, Trowsdale J, Wilson MJ (2001) Divergent and convergent evolution of NK-cell receptors. Trends Immunol 22: 52-57.
71. Wilhelm BT, Gagnier L, Mager DL (2002) Sequence analysis of the Ly49 cluster in C57BL/6 mice: A rapidly evolving multigene family in the immune system. Genomics 80: 646-661.
72. Proteau MF, Rousselle E, Makrigiannis AP (2004) Mapping of the BALB/c Ly49 cluster defines a minimal natural killer cell receptor gene repertoire. Genomics 84: 669-677.
73. Kamogawa-Schifter Y, Ohkawa J, Namiki S, Arai N, Arai KI, et al. (2004) Ly49Q defines two pDC subsets in mice. Blood 105: 2787-2792.
74. Toyama-Sorimachi N, Tsujimura Y, Maruya M, Onoda A, Kubota T, et al. (2004) Ly49Q, a member of the Ly49 family that is selectively expressed on myeloid lineage cells and involved in regulation of cytoskeletal architecture. Proc Natl Acad Sci U S A 101: 1016-1021.
75. Nylenna O, Naper C, Vaage JT, Woon PY, Gauguier D, et al. (2005) The genes and gene organization of the Ly49 region of the rat natural killer cell gene complex. Eur J Immunol 35: 261-272.
76. Hao L, Nei M (2004) Genomic organization and evolutionary analysis of Ly49 genes encoding the rodent natural killer cell receptors: Rapid evolution by repeated gene duplication. Immunogenetics 56: 343-354.
77. Hurt P, Walter L, Sudbrak R, Klages S, Müller I, et al. (2004) The genomic sequence and comparative analysis of the rat major histocompatibility complex. Genome Res 14: 631-639.
78. Hamerman JA, Ogasawara K, Lanier LL (2005) NK cells in innate immunity. Curr Opin Immunol 17: 29-35.
79. Scalzo AA, Lyons PA, Fitzgerald NA, Forbes CA, Yokoyama WM, et al. (1995) Genetic mapping of Cmv1 in the region of mouse chromosome 6 encoding the NK gene complex-associated loci Ly49 and musNKR-P1. Genomics 27: 435-441.
80. Brown MG, Dokun AO, Heusel JW, Smith HR, Beckman DL, et al. (2001) Vital involvement of a natural killer cell activation receptor in resistance to viral infection. Science 292: 934-937.
81. Daniels KA, Devora G, Lai WC, O'Donnell CL, Bennett M, et al. (2001) Murine cytomegalovirus is regulated by a discrete subset of natural killer cells reactive with monoclonal antibody to Ly49h. J Exp Med 194: 29-44.
82. Lee SH, Girard S, Macina D, Busa M, Zafer A, et al. (2001) Susceptibility to mouse cytomegalovirus is associated with deletion of an activating natural killer cell receptor of the C-type lectin superfamily. Nat Genetics 28: 42-45.
83. Sjolin H, Tomasello E, Mousavi-Jazi M, Bartolazzi A, Karre K, et al. (2002) Pivotal role of KARAP/DAP12 adaptor molecule in the natural killer cell-mediated resistance to murine cytomegalovirus infection. J Expl Med 195: 825-834.
84. Arase H, Mocarski ES, Campbell AE, Hill AB, Lanier LL (2002) Direct recognition of cytomegalovirus by activating and inhibitory NK cell receptors. Science 296: 1323-1326.
85. Lopez-Botet M, Angulo A, Guma M (2004) Natural killer cell receptors for major histocompatibility complex class I and related molecules in cytomegalovirus infection. Tissue Antigens 63: 195-203.
86. Vance RE, Kraft JR, Altman JD, Jensen PE, Raulet DH (1998) Mouse CD94/ NKG2A is a natural killer cell receptor for the nonclassical major histocompatibility complex (MHC) Class I molecule Qa-1(b). J Exp Med 188: 1841-1848.
87. Watanabe Y, Maruoka T, Walter L, Kasahara M (2004) Comparative genomics of the mill family: A rapidly evolving MHC class I gene family. Eur J Immunol 34: 1597-1607.
88. Ehrlich LI, Ogasawara K, Hamerman JA, Takaki R, Zingoni A, et al. (2005) Engagement of NKG2D by cognate ligand or antibody alone is insufficient to mediate costimulation of human and mouse CD8+ T cells. J Immunol 174: 1922-1931.
89. Rosen DB, Araki M, Hamerman JA, Chen T, Yamamura T, et al. (2004) A structural basis for the association of DAP12 with mouse, but not human, NKG2D. J Immunol 173: 2470-2478.
90. Storset AK, Kulberg S, Berg I, Boysen P, Hope JC, et al. (2004) NKp46 defines a subset of bovine leukocytes with natural killer cell characteristics. Eur J Immunol 34: 669-676.
91. 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: 980-990.
92. Govaerts MM, Goddeeris BM (2001) Homologues of natural killer cell receptors NKG2-D and NKR-P1 expressed in cattle. Vet Immunol Immunopathol 80: 339-344.
93. McQueen KL, Freeman JD, Takei F, Mager DL (1998) Localization of five new Ly49 genes, including three closely related to Ly49c. Immunogenetics 48: 174-183.
94. Ahn JS, Hamilton MJ, Davis WC, Park YH (2002) Cloning of bovine CD69. Vet Immunol Immunopathol 88: 43-48.
95. Gagnier L, Wilhelm BT, Mager DL (2003) Ly49 genes in non-rodent mammals. Immunogenetics 55: 109-115.
96. 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: 773-784.
97. Yim D, Sotiriadis J, Kim KS, Shin SC, Jie HB, et al. (2002) Molecular cloning, expression pattern and chromosomal mapping of Pig CD69. Immunogenetics 54: 276-281.
98. Kaufman J, Milne S, Gobel TWF, Walker BA, Jacob JP, et al. (1999) The chicken B locus is a minimal major histocompatibility complex. Nature 401: 923-925.
99. Viertlboeck BC, Crooijmans RP, Groenen MA, Gobel TW (2004) Chicken Ig-like receptor B2, a member of a multigene family, is mainly expressed on B lymphocytes, recruits both Src homology 2 domain containing protein tyrosine phosphatase (SHP)-1 and SHP-2, and inhibits proliferation. J Immunol 173: 7385-7393.
100. Nikolaidis N, Makalowska I, Chalkia D, Makalowski W, Klein J, et al. (2005) Origin and evolution of the chicken leukocyte receptor complex. Proc Natl Acad Sci U S A 102: 4057-4062.
101. Nikolaidis N, Klein J, Nei M (2005) 〉 Origin and evolution of the Ig-like domains present in mammalian leukocyte receptors: Insights from chicken, frog, and fish homologues. Immunogenetics. Epub 2005 March 7.
102. Rogers SL, Gobel TW, Viertlboeck BC, Milne S, Beck S, et al. (2005) Characterization of the chicken C-type lectin-like receptors B-NK and B-lec suggests that the NK complex and the MHC share a common ancestral region. J Immunol 174: 3475-3483.
103. Yoder JA, Mueller MG, Wei S, Corliss BC, Prather DM, et al. (2001) Immune-type receptor genes in zebrafish share genetic and functional properties with genes encoded by the mammalian leukocyte receptor cluster. Proc Natl Acad Sci U S A 98: 6771-6776.
104. Yoder JA, Litman RT, Mueller MG, Desai S, Dobrinski KP, et al. (2004) Resolution of the novel immune-type receptor gene cluster in zebrafish. Proc Natl Acad Sci U S A 101: 15706-15711.
105. Kikuno R, Sato A, Mayer WE, Shintani S, Aoki T, et al. (2004) Clustering of C-type lectin natural killer receptor-like loci in the bony fish Oreochromis niloticus. Scand J Immunol 59: 133-142.
106. Sato A, Mayer WE, Overath P, Klein J (2003) Genes encoding putative natural killer cell C-type lectin receptors in teleostean fishes. Proc Natl Acad Sci U S A 100: 7779-7784.
107. Zimmerman AM, Evenhuis JP, Thorgaard GH, Ristow SS (2004) A single major chromosomal region controls natural killer cell-like activity in rainbow trout. Immunogenetics 55: 825-835.
108. Wilhelm BT, Mager DL (2004) Rapid expansion of the Ly49 gene cluster in rat. Genomics 84: 218-221.
109. Trowsdale J, Parham P (2004) Defense strategies and immune-related genes. Eur J Immunol 34: 7-17.
110. Lynch M, Conery JS (2003) The evolutionary demography of duplicate genes. J Struct Funct Genomics 3: 35-44.
111. 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: 1319-1332.
112. Desrosiers MP, Kielczewska A, Loredo-Osti JC, Adam SG, Makrigiannis AP, et al. (2005) Epistasis between mouse Klra and major histocompatibility complex class I loci is associated with a new mechanism of natural killer cell-mediated innate resistance to cytomegalovirus infection. Nat Genetics 37: 593-599.
113. Dam J, Guan R, Natarajan K, Dimasi N, Chlewicki LK, et al. (2003) Variable MHC class I engagement by Ly49 natural killer cell receptors demonstrated by the crystal structure of Ly49C bound to H-2K(b). Nat Immunol 4: 1213-1222.
114. 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 U S A. In press.
115. Springer MS, Murphy WJ, Eizirik E, O'Brien SJ (2003) Placental mammal diversification and the cretaceous-tertiary boundary. Proc Natl Acad Sci USA 100: 1056-1061.
116. Biron CA, Nguyen KB, Pien GC, Cousens LP, Salazar-Mather TP (1999) Natural killer cells in antiviral defense: Function and regulation by innate cytokines. Ann Rev Immunol 17: 189-220.
117. Ludwig B, Kraus FB, Allwinn R, Doerr HW, Preiser W (2003) Viral zoonoses - A threat under control? Intervirology 46: 71-78.
118. Parham P, Ohta T (1996) Population Biology of Antigen Presentation by MHC Class I Molecules. Science 272: 67-74.
119. Hill AV (1999) Immunogenetics. Defence by diversity. Nature 398: 668-669.
120. 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: 957-965.
121. Henry J, Miller MM, Pontarotti P (1999) Structure and evolution of the extended B7 family. Immunol Today 20: 285-288.
122. Kelley J, de Bono B, Trowsdale J (2005) IRIS: A database surveying known human immune system genes. Genomics 85: 803-833.
123. Wheeler DL, Barren T, Benson DA, Bryant SH, Canese K, et al. (2005) Database resources of the national center for biotechnology information. Nucleic Acids Res 33: D39-D45.