Ly49h-deficient C57BL/6 mice: A new mouse cytomegalovirus-susceptible model remains resistant to unrelated pathogens controlled by the NK gene complex

Journal of Immunology

Volumn 181, Issue 9, 2008, Pages 6394-6405

  Fodil Cornu, Nassima ^a   Lee, Seung Hwan ^b   Belanger, Simon ^c   Makrigiannis, Andrew P ^c   Biron, Christine A ^b   Buller, R Mark ^d   Vidal, Silvia M ^a  

^a MCGILL UNIVERSITY   (Canada)

^b BROWN UNIVERSITY   (United States)

^c CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

^d SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN; PROTEIN LY49H; UNCLASSIFIED DRUG; CYTOKINE; KLRA8 PROTEIN, MOUSE; NATURAL KILLER CELL LECTIN LIKE RECEPTOR SUBFAMILY A; NATURAL KILLER CELL RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOARCHITECTURE; CYTOKINE PRODUCTION; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTION; ECTROMELIA VIRUS; HISTOLOGY; HOST PATHOGEN INTERACTION; LEISHMANIA MAJOR; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; SPLEEN; SPLEEN CELL; VIRUS REPLICATION; ANIMAL; BAGG ALBINO MOUSE; BETAHERPESVIRINAE; BIOSYNTHESIS; C57BL MOUSE; CHO CELL; CRICETULUS; CYTOLOGY; DISEASE MODEL; GENETIC PREDISPOSITION; GENETICS; HAMSTER; HERPES VIRUS INFECTION; IMMUNOLOGY; INNATE IMMUNITY; METABOLISM; MOLECULAR GENETICS; MOUSE MUTANT; MOUSE STRAIN; NUCLEOTIDE SEQUENCE; PATHOGENICITY; PATHOLOGY; PHYSIOLOGY;

ANIMALS; BASE SEQUENCE; CHO CELLS; CRICETINAE; CRICETULUS; CYTOKINES; DISEASE MODELS, ANIMAL; ECTROMELIA VIRUS; GENETIC PREDISPOSITION TO DISEASE; HERPESVIRIDAE INFECTIONS; IMMUNITY, INNATE; LEISHMANIA MAJOR; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, INBRED STRAINS; MICE, KNOCKOUT; MOLECULAR SEQUENCE DATA; MUROMEGALOVIRUS; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY A; RECEPTORS, NATURAL KILLER CELL; SPLEEN;

EID: 58049214053     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.181.9.6394     Document Type: Article

References (86)

1. Sinclair, J., and P. Sissons. 2006. Latency and reactivation of human cytomegalovirus. J. Gen. Virol. 87: 1763-1779.
2. Mocarski, E. S., Jr. 2002. Immunomodulation by cytomegaloviruses: manipulative strategies beyond evasion. Trends Microbiol. 10: 332-339.
3. Tay, C. H., and R. M. Welsh. 1997. Distinct organ-dependent mechanisms for the control of murine cytomegalovirus infection by natural killer cells. J. Virol. 71: 267-275.
4. Orange, J. S., and C. A. Biron. 1996. An absolute and restricted requirement for IL-12 in natural killer cell IFN-γ production and antiviral defense: studies of natural killer and T cell responses in contrasting viral infections. J. Immunol. 156: 1138-1142. (Pubitemid 26048109)
5. Biron, C. A., K. S. Byron, and J. L. Sullivan. 1989. Severe herpesvirus infections in an adolescent without natural killer cells. N. Engl. J. Med. 320: 1731-1735. (Pubitemid 19163129)
6. Shellam, G. R., J. E. Allan, J. M. Papadimitriou, and G. J. Bancroft. 1981. Increased susceptibility to cytomegalovirus infection in beige mutant mice. Proc. Natl. Acad. Sci. USA 78: 5104-5108. (Pubitemid 12229681)
7. Bukowski, J. F., B. A. Woda, S. Habu, K. Okumura, and R. M. Welsh. 1983. Natural killer cell depletion enhances virus synthesis and virus-induced hepatitis in vivo. J. Immunol. 131: 1531-1538.
8. Welsh, R. M., P. L. Dundon, E. E. Eynon, J. O. Brubaker, G. C. Koo, and C. L. O'Donnell. 1990. Demonstration of the antiviral role of natural killer cells in vivo with a natural killer cell-specific monoclonal antibody (NK 1.1). Nat. Immun. Cell Growth Regul. 9: 112-120. (Pubitemid 20141713)
9. Dalod, M., T. P. Salazar-Mather, L. Malmgaard, C. Lewis, C. Asselin-Paturel, F. Briere, G. Trinchieri, and C. A. Biron. 2002. Interferon α/β and interleukin 12 responses to viral infections: pathways regulating dendritic cell cytokine expression in vivo. J. Exp. Med. 195: 517-528. (Pubitemid 34461304)
10. Scalzo, A. A., N. A. Fitzgerald, A. Simmons, A. B. La Vista, and G. R. Shellam. 1990. Cmv-1, a genetic locus that controls murine cytomegalovirus replication in the spleen. J. Exp. Med. 171: 1469-1483.
11. Scalzo, A. A., N. A. Fitzgerald, C. R. Wallace, A. E. Gibbons, Y. C. Smart, R. C. Burton, and G. R. Shellam. 1992. The effect of the Cmv-1 resistance gene, which is linked to the natural killer cell gene complex, is mediated by natural killer cells. J. Immunol. 149: 581-589.
12. Brown, M. G., A. O. Dokun, J. W. Heusel, H. R. Smith, D. L. Beckman, E. A. Blattenberger, C. E. Dubbelde, L. R. Stone, A. A. Scalzo, and W. M. Yokoyama. 2001. Vital involvement of a natural killer cell activation receptor in resistance to viral infection. Science 292: 934-937.
13. Lee, S. H., S. Girard, D. Macina, M. Busa, A. Zafer, A. Belouchi, P. Gros, and S. M. Vidal. 2001. Susceptibility to mouse cytomegalovirus is associated with deletion of an activating natural killer cell receptor of the C-type lectin superfamily. Nat. Genet. 28: 42-45.
14. Daniels, K. A., G. Devora, W. C. Lai, C. L. O'Donnell, M. Bennett, and R. M. Welsh. 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.
15. Lee, S. H., A. Zafer, Y. de Repentigny, R. Kothary, M. L. Tremblay, P. Gros, P. Duplay, J. R. Webb, and S. M. Vidal. 2003. Transgenic expression of the activating natural killer receptor Ly49H confers resistance to cytomegalovirus in genetically susceptible mice. J. Exp. Med. 197: 515-526.
16. Scalzo, A. A., M. G. Brown, D. T. Chu, J. W. Heusel, W. M. Yokoyama, and C. A. Forbes. 1999. Development of intra-natural killer complex (NKC) recombinant and congenic mouse strains for mapping and functional analysis of NK cell regulatory loci. Immunogenetics 49: 238-241.
17. Sjolin, H., E. Tomasello, M. Mousavi-Jazi, A. Bartolazzi, K. Karre, E. Vivier, and C. Cerboni. 2002. Pivotal role of KARAP/DAP12 adaptor molecule in the natural killer cell-mediated resistance to murine cytomegalovirus infection. J. Exp. Med. 195: 825-834. (Pubitemid 34286754)
18. Arase, H., E. S. Mocarski, A. E. Campbell, A. B. Hill, and L. L. Lanier. 2002. Direct recognition of cytomegalovirus by activating and inhibitory NK cell receptors. Science 296: 1323-1326. (Pubitemid 34522789)
19. Smith, H. R., J. W. Heusel, I. K. Mehta, S. Kim, B. G. Dorner, O. V. Naidenko, K. Iizuka, H. Furukawa, D. L. Beckman, J. T. Pingel, et al. 2002. Recognition of a virus-encoded ligand by a natural killer cell activation receptor. Proc. Natl. Acad. Sci. USA 99: 8826-8831. (Pubitemid 34693643)
20. Dorner, B. G., H. R. Smith, A. R. French, S. Kim, J. Poursine-Laurent, D. L. Beckman, J. T. Pingel, R. A. Kroczek, and W. M. Yokoyama. 2004. Coordinate expression of cytokines and chemokines by NK cells during murine cytomegalovirus infection. J. Immunol. 172: 3119-3131. (Pubitemid 38263702)
21. Dokun, A. O., S. Kim, H. R. Smith, H. S. Kang, D. T. Chu, and W. M. Yokoyama. 2001. Specific and nonspecific NK cell activation during virus infection. Nat. Immunol. 2: 951-956. (Pubitemid 32976168)
22. Bubic, I., M. Wagner, A. Krmpotic, T. Saulig, S. Kim, W. M. Yokoyama, S. Jonjic, and U. H. Koszinowski. 2004. Gain of virulence caused by loss of a gene in murine cytomegalovirus. J. Virol. 78: 7536-7544. (Pubitemid 38915900)
23. Yokoyama, W. M., and B. F. Plougastel. 2003. Immune functions encoded by the natural killer gene complex. Nat. Rev. Immunol. 3: 304-316.
24. Pereira, R. A., A. Scalzo, and A. Simmons. 2001. Cutting edge: a NK complex-linked locus governs acute versus latent herpes simplex virus infection of neurons. J. Immunol. 166: 5869-5873.
25. Delano, M. L., and D. G. Brownstein. 1995. Innate resistance to lethal mousepox is genetically linked to the NK gene complex on chromosome 6 and correlates with early restriction of virus replication by cells with an NK phenotype. J. Virol. 69: 5875-5877.
26. Hansen, D. S., K. J. Evans, M. C. D'Ombrain, N. J. Bernard, A. C. Sexton, L. Buckingham, A. A. Scalzo, and L. Schofield. 2005. The natural killer complex regulates severe malarial pathogenesis and influences acquired immune responses to Plasmodium berghei ANKA. Infect. Immun. 73: 2288-2297.
27. Beebe, A. M., S. Mauze, N. J. Schork, and R. L. Coffman. 1997. Serial backcross mapping of multiple loci associated with resistance to Leishmania major in mice. Immunity 6: 551-557.
28. Hansen, D. S., M. A. Siomos, L. Buckingham, A. A. Scalzo, and L. Schofield. 2003. Regulation of murine cerebral malaria pathogenesis by CD1d-restricted NKT cells and the natural killer complex. Immunity 18: 391-402.
29. Parker, A. K., S. Parker, W. M. Yokoyama, J. A. Corbett, and R. M. Buller. 2007. Induction of natural killer cell responses by ectromelia virus controls infection. J. Virol. 81: 4070-4079.
30. + T cell subsets and induces early resistance to Leishmania major in mice. J. Exp. Med. 178: 567-577.
31. Depatie, C., E. Muise, P. Lepage, P. Gros, and S. M. Vidal. 1997. High-resolution linkage map in the proximity of the host resistance locus Cmv1. Genomics 39: 154-163. (Pubitemid 27069213)
32. Zhang, W. W., and G. Matlashewski. 2004. In vivo selection for Leishmania donovani miniexon genes that increase virulence in Leishmania major. Mol. Microbiol. 54: 1051-1062.
33. Karupiah, G., T. N. Fredrickson, K. L. Holmes, L. H. Khairallah, and R. M. Buller. 1993. Importance of interferons in recovery from mousepox. J. Virol. 67: 4214-4226.
34. Adam, S. G., A. Caraux, N. Fodil-Cornu, J. C. Loredo-Osti, S. Lesjean-Pottier, J. Jaubert, I. Bubic, S. Jonjic, J. L. Guenet, S. M. Vidal, and F. Colucci. 2006. Cmv4, a new locus linked to the NK cell gene complex, controls innate resistance to cytomegalovirus in wild-derived mice. J. Immunol. 176: 5478-5485.
35. Salazar-Mather, T. P., J. S. Orange, and C. A. Biron. 1998. Early murine cytomegalovirus (MCMV) infection induces liver natural killer (NK) cell inflammation and protection through macrophage inflammatory protein 1α (MIP-1α)-dependent pathways. J. Exp. Med. 187: 1-14.
36. Biron, C. A., H. C. Su, and J. S. Orange. 1996. Function and regulation of natural killer (NK) cells during viral infections: characterization of responses in vivo. Methods 9: 379-393.
37. Ruzek, M. C., A. H. Miller, S. M. Opal, B. D. Pearce, and C. A. Biron. 1997. Characterization of early cytokine responses and an interleukin (IL)-6-dependent pathway of endogenous glucocorticoid induction during murine cytomegalovirus infection. J. Exp. Med. 185: 1185-1192.
38. Delale, T., A. Paquin, C. Asselin-Paturel, M. Dalod, G. Brizard, E. E. Bates, P. Kastner, S. Chan, S. Akira, A. Vicari, et al. 2005. MyD88-dependent and -independent murine cytomegalovirus sensing for IFN-α release and initiation of immune responses in vivo. J. Immunol. 175: 6723-6732. (Pubitemid 41598916)
39. Ljunggren, H. G., C. Ohlen, P. Hoglund, L. Franksson, and K. Karre. 1991. The RMA-S lymphoma mutant; consequences of a peptide loading defect on immunological recognition and graft rejection. Int. J. Cancer 6: 38-44.
40. Idris, A. H., H. R. Smith, L. H. Mason, J. R. Ortaldo, A. A. Scalzo, and W. M. Yokoyama. 1999. The natural killer gene complex genetic locus Chok encodes Ly-49D, a target recognition receptor that activates natural killing. Proc. Natl. Acad. Sci. USA 96: 6330-6335.
41. Elsner, L., V. Muppala, M. Gehrmann, J. Lozano, D. Malzahn, H. Bickeboller, E. Brunner, M. Zientkowska, T. Herrmann, L. Walter, et al. 2007. The heat shock protein HSP70 promotes mouse NK cell activity against tumors that express inducible NKG2D ligands. J. Immunol. 179: 5523-5533.
42. Orange, J. S., B. Wang, C. Terhorst, and C. A. Biron. 1995. Requirement for natural killer cell-produced interferon γ in defense against murine cytomegalovirus infection and enhancement of this defense pathway by interleukin 12 administration. J. Exp. Med. 182: 1045-1056.
43. Orange, J. S., T. P. Salazar-Mather, S. M. Opal, and C. A. Biron. 1997. Mechanisms for virus-induced liver disease: tumor necrosis factor-mediated pathology independent of natural killer and T cells during murine cytomegalovirus infection. J. Virol. 71: 9248-9258.
44. Bukowski, J. F., B. A. Woda, and R. M. Welsh. 1984. Pathogenesis of murine cytomegalovirus infection in natural killer cell-depleted mice. J. Virol. 52: 119-128. (Pubitemid 14000479)
45. Bukowski, J. F., C. A. Biron, and R. M. Welsh. 1983. Elevated natural killer cell-mediated cytotoxicity, plasma interferon, and tumor cell rejection in mice persistently infected with lymphocytic choriomeningitis virus. J. Immunol. 131: 991-996.
46. Benedict, C. A., C. De Trez, K. Schneider, S. Ha, G. Patterson, and C. F. 2006. Ware. Specific remodeling of splenic architecture by cytomegalovirus. PLoS Pathog. 2: e16.
47. Sjolin, H., S. H. Robbins, G. Bessou, A. Hidmark, E. Tomasello, M. Johansson, H. Hall, F. Charifi, G. B. Karlsson Hedestam, C. A. Biron, et al. 2006. DAP12 signaling regulates plasmacytoid dendritic cell homeostasis and down-modulates their function during viral infection. J. Immunol. 177: 2908-2916. (Pubitemid 44277806)
48. Sell, M. S., J. F. Bale, Jr., and R. H. Giller. 1985. T-lymphocyte subpopulations and function during murine cytomegalovirus infection. Pediatr. Res. 19: 583-587. (Pubitemid 15093323)
49. + NK cells migrate to and protect splenic white pulp stroma from murine cytomegalovirus infection. J. Immunol. 180: 6768-6776.
50. Lucin, P., S. Jonjic, M. Messerle, B. Polic, H. Hengel, and U. H. Koszinowski. 1994. Late phase inhibition of murine cytomegalovirus replication by synergistic action of interferon-γ and tumour necrosis factor. J. Gen. Virol. 75: 101-110. (Pubitemid 24033985)
51. Heise, M. T., and H. W. t. Virgin. 1995. The T-cell-independent role of γ interferon and tumor necrosis factor α in macrophage activation during murine cytomegalovirus and herpes simplex virus infections. J. Virol. 69: 904-909.
52. Presti, R. M., J. L. Pollock, A. J. Dal Canto, A. K. O'Guin, and H. W. t. Virgin. 1998. Interferon γ regulates acute and latent murine cytomegalovirus infection and chronic disease of the great vessels. J. Exp. Med. 188: 577-588.
53. Beebe, A. M., D. J. Cua, and R. L. Coffman. 1999. Genetic control of T helper subset differentiation in Leishmania major infection of mice. Microbes Infect. 1: 89-94. (Pubitemid 29364917)
54. Taylor, B. A., C. Wnek, B. S. Kotlus, N. Roemer, T. MacTaggart, and S. J. Phillips. 1999. Genotyping new BXD recombinant inbred mouse strains and comparison of BXD and consensus maps. Mamm. Genome 10: 335-348.
55. Long, M. 2001. Evolution of novel genes. Curr. Opin. Genet. Dev. 11: 673-680.
56. Henthorn, P. S., O. Smithies, and D. L. Mager. 1990. Molecular analysis of deletions in the human β-globin gene cluster: deletion junctions and locations of breakpoints. Genomics 6: 226-237.
57. Venturin, M., C. Gervasini, F. Orzan, A. Bentivegna, L. Corrado, P. Colapietro, A. Friso, R. Tenconi, M. Upadhyaya, L. Larizza, and P. Riva. 2004. Evidence for non-homologous end joining and non-allelic homologous recombination in atypical NF1 microdeletions. Hum. Genet. 115: 69-80. (Pubitemid 38787218)
58. Wilhelm, B. T., L. Gagnier, and D. L. Mager. 2002. Sequence analysis of the Ly49 cluster in C57BL/6 mice: a rapidly evolving multigene family in the immune system. Genomics 80: 646-661.
59. Abi-Rached, L., and P. Parham. 2005. Natural selection drives recurrent formation of activating killer cell immunoglobulin-like receptor and Ly49 from inhibitory homologues. J. Exp. Med. 201: 1319-1332. (Pubitemid 40629074)
60. Crozat, K., K. Hoebe, S. Ugolini, N. A. Hong, E. Janssen, S. Rutschmann, S. Mudd, S. Sovath, E. Vivier, and B. Beutler. 2007. Jinx, an MCMV susceptibility phenotype caused by disruption of Unc13d: a mouse model of type 3 familial hemophagocytic lymphohistiocytosis. J. Exp. Med. 204: 853-863. (Pubitemid 46631614)
61. Loh, J., D. T. Chu, A. K. O'Guin, W. M. Yokoyama, and H. W. t. Virgin. 2005. Natural killer cells utilize both perforin and γ interferon to regulate murine cytomegalovirus infection in the spleen and liver. J. Virol. 79: 661-667.
62. van Dommelen, S. L., N. Sumaria, R. D. Schreiber, A. A. Scalzo, M. J. Smyth, and M. A. Degli-Esposti. 2006. Perforin and granzymes have distinct roles in defensive immunity and immunopathology. Immunity 25: 835-848. (Pubitemid 46107286)
63. + cells and murine cytomegalovirus infection: what happens in situ? J. Immunol. 166: 1796-1802.
64. Gregoire, C., C. Cognet, L. Chasson, C. A. Coupet, M. Dalod, A. Reboldi, J. Marvel, F. Sallusto, E. Vivier, and T. Walzer. 2008. Intrasplenic trafficking of natural killer cells is redirected by chemokines upon inflammation. Eur. J. Immunol. 38: 2076-2084.
65. Salazar-Mather, T. P., and K. L. Hokeness. 2003. Calling in the troops: regulation of inflammatory cell trafficking through innate cytokine/chemokine networks. Viral Immunol. 16: 291-306.
66. Dalod, M., T. Hamilton, R. Salomon, T. P. Salazar-Mather, S. C. Henry, J. D. Hamilton, and C. A. Biron. 2003. Dendritic cell responses to early murine cytomegalovirus infection: subset functional specialization and differential regulation by interferon α/β. J. Exp. Med. 197: 885-898. (Pubitemid 36437865)
67. Robbins, S. H., G. Bessou, A. Cornillon, N. Zucchini, B. Rupp, Z. Ruzsics, T. Sacher, E. Tomasello, E. Vivier, U. H. Koszinowski, and M. Dalod. 2007. Natural killer cells promote early CD8 T cell responses against cytomegalovirus. PLoS Pathog. 3: e123.
68. Banks, T. A., S. Rickert, C. A. Benedict, L. Ma, M. Ko, J. Meier, W. Ha, K. Schneider, S. W. Granger, O. Turovskaya, et al. 2005. A lymphotoxin-IFN- β axis essential for lymphocyte survival revealed during cytomegalovirus infection. J. Immunol. 174: 7217-7225.
69. + T-cell memory. Curr. Opin. Immunol. 16: 271-276.
70. Carrero, J. A., B. Calderon, and E. R. Unanue. 2004. Type I interferon sensitizes lymphocytes to apoptosis and reduces resistance to Listeria infection. J. Exp. Med. 200: 535-540.
71. O'Connell, R. M., S. K. Saha, S. A. Vaidya, K. W. Bruhn, G. A. Miranda, B. Zarnegar, A. K. Perry, B. O. Nguyen, T. F. Lane, T. Taniguchi, et al. 2004. Type I interferon production enhances susceptibility to Listeria monocytogenes infection. J. Exp. Med. 200: 437-445. (Pubitemid 39121901)
72. Zucchini, N., G. Bessou, S. H. Robbins, L. Chasson, A. Raper, P. R. Crocker, and M. Dalod. 2008. Individual plasmacytoid dendritic cells are major contributors to the production of multiple innate cytokines in an organ-specific manner during viral infection. Int. Immunol. 20: 45-56.
73. Zucchini, N., G. Bessou, S. Traub, S. H. Robbins, S. Uematsu, S. Akira, L. Alexopoulou, and M. Dalod. 2008. Cutting edge: overlapping functions of TLR7 and TLR9 for innate defense against a herpesvirus infection. J. Immunol. 180: 5799-5803.
74. Krug, A., A. R. French, W. Barchet, J. A. Fischer, A. Dzionek, J. T. Pingel, M. M. Orihuela, S. Akira, W. M. Yokoyama, and M. Colonna. 2004. TLR9-dependent recognition of MCMV by IPC and DC generates coordinated cytokine responses that activate antiviral NK cell function. Immunity 21: 107-119. (Pubitemid 38925271)
75. Lipoldova, M., and P. Demant. 2006. Genetic susceptibility to infectious disease: lessons from mouse models of leishmaniasis. Nat. Rev. Genet. 7: 294-305.
76. Roberts, L. J., T. M. Baldwin, J. M. Curtis, E. Handman, and S. J. Foote. 1997. Resistance to Leishmania major is linked to the H2 region on chromosome 17 and to chromosome 9. J. Exp. Med. 185: 1705-1710. (Pubitemid 27203266)
77. Fang, M., L. L. Lanier, and L. J. Sigal. 2008. A role for NKG2D in NK cell-mediated resistance to poxvirus disease. PLoS Pathog. 4: e30. (Pubitemid 351340717)
78. Vercammen, E., J. Staal, and R. Beyaert. 2008. Sensing of viral infection and activation of innate immunity by Toll-like receptor 3. Clin. Microbiol. Rev. 21: 13-25. (Pubitemid 351160008)
79. Carrington, M., S. Wang, M. P. Martin, X. Gao, M. Schiffman, J. Cheng, R. Herrero, A. C. Rodriguez, R. Kurman, R. Mortel, 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: 1069-1075. (Pubitemid 40524675)
80. Williams, F., A. Meenagh, C. Sleator, D. Cook, M. Fernandez-Vina, A. M. Bowcock, and D. Middleton. 2005. Activating killer cell immunoglobulin-like receptor gene KIR2DS1 is associated with psoriatic arthritis. Hum. Immunol. 66: 836-841. (Pubitemid 41169774)
81. Martin, M. P., G. Nelson, J. H. Lee, F. Pellett, X. Gao, J. Wade, M. J. Wilson, J. Trowsdale, D. Gladman, and M. Carrington. 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.
82. Suzuki, Y., Y. Hamamoto, Y. Ogasawara, K. Ishikawa, Y. Yoshikawa, T. Sasazuki, and M. Muto. 2004. Genetic polymorphisms of killer cell immunoglobulin-like receptors are associated with susceptibility to psoriasis vulgaris. J. Invest. Dermatol. 122: 1133-1136. (Pubitemid 38651087)
83. Seet, B. T., and G. McFadden. 2002. Viral chemokine-binding proteins. J. Leukocyte Biol. 72: 24-34.
84. Reading, P. C., J. A. Symons, and G. L. Smith. 2003. A soluble chemokine-binding protein from vaccinia virus reduces virus virulence and the inflammatory response to infection. J. Immunol. 170: 1435-1442.
85. Smith, H. R., H. H. Chuang, L. L. Wang, M. Salcedo, J. W. Heusel, and W. M. Yokoyama. 2000. Nonstochastic coexpression of activation receptors on murine natural killer cells. J. Exp. Med. 191: 1341-1354. (Pubitemid 30227122)
86. Cheng, T. P., A. R. French, B. F. Plougastel, J. T. Pingel, M. M. Orihuela, M. L. Buller, and W. M. Yokoyama. 2008. Ly49h is necessary for genetic resistance to murine cytomegalovirus. Immunogenetics 60: 565-573.