Association of activating KIR copy number variation of NK cells with containment of SIV replication in rhesus monkeys

PLoS Pathogens

Volumn 7, Issue 12, 2011, Pages

  Hellmann, Ina ^a   Lim, So Yon ^a   Gelman, Rebecca S ^b   Letvin, Norman L ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR; TRIPARTITE MOTIF PROTEIN 5; CYTOKINE;

ALLELE; ANIMAL EXPERIMENT; ARTICLE; COPY NUMBER VARIATION; GENETIC ASSOCIATION; NATURAL KILLER CELL; NONHUMAN; PROTEIN EXPRESSION; RHESUS MONKEY; SIMIAN IMMUNODEFICIENCY VIRUS; VIRUS INFECTION; VIRUS REPLICATION; ANIMAL; BIOSYNTHESIS; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; GENETICS; IMMUNOLOGY; MACACA MULATTA; METABOLISM; PHYSIOLOGY; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; VIROLOGY;

HUMAN IMMUNODEFICIENCY VIRUS 1; MACACA MULATTA; SIMIAN IMMUNODEFICIENCY VIRUS;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CYTOKINES; DNA COPY NUMBER VARIATIONS; KILLER CELLS, NATURAL; MACACA MULATTA; RECEPTORS, KIR; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; VIRUS REPLICATION;

EID: 84855295985     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002436     Document Type: Article

References (54)

1. Biron CA, (1999) Initial and innate responses to viral infections-pattern setting in immunity or disease. Curr Opin Microbiol 2: 374-381.
2. Cerwenka A, Lanier LL, (2001) Natural killer cells, viruses and cancer. Nat Rev Immunol 1: 41-49.
3. Orange JS, (2002) Human natural killer cell deficiencies and susceptibility to infection. Microbes Infect 4: 1545-1558.
4. Lanier LL, (2005) NK cell recognition. Annu Rev Immunol 23: 225-274.
5. Trinchieri G, (1989) Biology of natural killer cells. Adv Immunol 47: 187-376.
6. Moretta A, Bottino C, Mingari MC, Biassoni R, Moretta L, (2002) What is a natural killer cell? Nat Immunol 3: 6-8.
7. Vivier E, Nunes JA, Vely F, (2004) Natural killer cell signaling pathways. Science 306: 1517-1519.
8. Moretta A, Sivori S, Vitale M, Pende D, Morelli L, et al. (1995) Existence of both inhibitory (p58) and activatory (p50) receptors for HLA-C molecules in human natural killer cells. J Exp Med 182: 875-884.
9. 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: 505-518.
10. Parham P, (2005) MHC class I molecules and KIRs in human history, health and survival. Nat Rev Immunol 5: 201-214.
11. Martin MP, Carrington M, (2005) Immunogenetics of viral infections. Curr Opin Immunol 17: 510-516.
12. 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: 429-434.
13. Alter G, Martin MP, Teigen N, Carr WH, Suscovich TJ, et al. (2007) Differential natural killer cell-mediated inhibition of HIV-1 replication based on distinct KIR/HLA subtypes. J Exp Med 204: 3027-3036.
14. Alter G, Rihn S, Walter K, Nolting A, Martin M, et al. (2009) HLA class I subtype-dependent expansion of KIR3DS1+ and KIR3DL1+ NK cells during acute human immunodeficiency virus type 1 infection. J Virol 83: 6798-6805.
15. Martin MP, Pascal V, Yeager M, Phair J, Kirk GD, et al. (2007) A mutation in KIR3DS1 that results in truncation and lack of cell surface expression. Immunogenetics 59: 823-829.
16. Haigwood NL, (2004) Predictive value of primate models for AIDS. AIDS Rev 6: 187-198.
17. 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.
18. Blokhuis JH, Doxiadis GG, Bontrop RE, (2009) A splice site mutation converts an inhibitory killer cell Ig-like receptor into an activating one. Mol Immunol 46: 640-648.
19. Blokhuis JH, van der Wiel MK, Doxiadis GG, Bontrop RE, (2010) The mosaic of KIR haplotypes in rhesus macaques. Immunogenetics 62: 295-306.
20. Chaichompoo P, Bostik P, Stephenson S, Udompunturuk S, Kobkitjaroen J, et al. (2010) Multiple KIR gene polymorphisms are associated with plasma viral loads in SIV-infected rhesus macaques. Cell Immunol 263: 176-187.
21. Kruse PH, Rosner C, Walter L, (2010) Characterization of rhesus macaque KIR genotypes and haplotypes. Immunogenetics 62: 281-293.
22. Degenhardt JD, de Candia P, Chabot A, Schwartz S, Henderson L, et al. (2009) Copy number variation of CCL3-like genes affects rate of progression to simian-AIDS in Rhesus Macaques (Macaca mulatta). PLoS Genet 5: e1000346.
23. Yasutomi Y, Reimann KA, Lord CI, Miller MD, Letvin NL, (1993) Simian immunodeficiency virus-specific CD8+ lymphocyte response in acutely infected rhesus monkeys. J Virol 67: 1707-1711.
24. Pal R, Venzon D, Letvin NL, Santra S, Montefiori DC, et al. (2002) ALVAC-SIV-gag-pol-env-based vaccination and macaque major histocompatibility complex class I (A*01) delay simian immunodeficiency virus SIVmac-induced immunodeficiency. J Virol 76: 292-302.
25. Mothe BR, Weinfurter J, Wang C, Rehrauer W, Wilson N, et al. (2003) Expression of the major histocompatibility complex class I molecule Mamu-A*01 is associated with control of simian immunodeficiency virus SIVmac239 replication. J Virol 77: 2736-2740.
26. Loffredo JT, Maxwell J, Qi Y, Glidden CE, Borchardt GJ, et al. (2007) Mamu-B*08-positive macaques control simian immunodeficiency virus replication. J Virol 81: 8827-8832.
27. Yant LJ, Friedrich TC, Johnson RC, May GE, Maness NJ, et al. (2006) The high-frequency major histocompatibility complex class I allele Mamu-B*17 is associated with control of simian immunodeficiency virus SIVmac239 replication. J Virol 80: 5074-5077.
28. Lim SY, Rogers T, Chan T, Whitney JB, Kim J, et al. (2010) TRIM5alpha Modulates Immunodeficiency Virus Control in Rhesus Monkeys. PLoS Pathog 6: e1000738.
29. Lim SY, Chan T, Gelman RS, Whitney JB, O'Brien KL, et al. (2010) Contributions of Mamu-A*01 status and TRIM5 allele expression, but not CCL3L copy number variation, to the control of SIVmac251 replication in Indian-origin rhesus monkeys. PLoS Genet 6: e1000997.
30. Lifson JD, Nowak MA, Goldstein S, Rossio JL, Kinter A, et al. (1997) The extent of early viral replication is a critical determinant of the natural history of simian immunodeficiency virus infection. J Virol 71: 9508-9514.
31. Letvin NL, Mascola JR, Sun Y, Gorgone DA, Buzby AP, et al. (2006) Preserved CD4+ central memory T cells and survival in vaccinated SIV-challenged monkeys. Science 312: 1530-1533.
32. 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: 739-751.
33. Bostik P, Kobkitjaroen J, Tang W, Villinger F, Pereira LE, et al. (2009) Decreased NK cell frequency and function is associated with increased risk of KIR3DL allele polymorphism in simian immunodeficiency virus-infected rhesus macaques with high viral loads. J Immunol 182: 3638-3649.
34. Reeves RK, Gillis J, Wong FE, Yu Y, Connole M, et al. (2010) CD16- natural killer cells: enrichment in mucosal and secondary lymphoid tissues and altered function during chronic SIV infection. Blood 115: 4439-4446.
35. Martin MP, Qi Y, Gao X, Yamada E, Martin JN, et al. (2007) Innate partnership of HLA-B and KIR3DL1 subtypes against HIV-1. Nat Genet 39: 733-740.
36. Qi Y, Martin MP, Gao X, Jacobson L, Goedert JJ, et al. (2006) KIR/HLA pleiotropism: protection against both HIV and opportunistic infections. PLoS Pathog 2: e79.
37. Boulet S, Sharafi S, Simic N, Bruneau J, Routy JP, et al. (2008) Increased proportion of KIR3DS1 homozygotes in HIV-exposed uninfected individuals. Aids 22: 595-599.
38. Gaudieri S, DeSantis D, McKinnon E, Moore C, Nolan D, et al. (2005) Killer immunoglobulin-like receptors and HLA act both independently and synergistically to modify HIV disease progression. Genes Immun 6: 683-690.
39. Jennes W, Verheyden S, Demanet C, Adje-Toure CA, Vuylsteke B, et al. (2006) Cutting edge: resistance to HIV-1 infection among African female sex workers is associated with inhibitory KIR in the absence of their HLA ligands. J Immunol 177: 6588-6592.
40. Ravet S, Scott-Algara D, Bonnet E, Tran HK, Tran T, et al. (2007) Distinctive NK-cell receptor repertoires sustain high-level constitutive NK-cell activation in HIV-exposed uninfected individuals. Blood 109: 4296-4305.
41. Middleton D, Gonzalez A, Gilmore PM, (2007) Studies on the expression of the deleted KIR2DS4*003 gene product and distribution of KIR2DS4 deleted and nondeleted versions in different populations. Hum Immunol 68: 128-134.
42. Goodridge JP, Lathbury LJ, Steiner NK, Shulse CN, Pullikotil P, et al. (2007) Three common alleles of KIR2DL4 (CD158d) encode constitutively expressed, inducible and secreted receptors in NK cells. Eur J Immunol 37: 199-211.
43. Sauermann U, Siddiqui R, Suh YS, Platzer M, Leuchte N, et al. (2008) Mhc class I haplotypes associated with survival time in simian immunodeficiency virus (SIV)-infected rhesus macaques. Genes Immun 9: 69-80.
44. Borrow P, Lewicki H, Hahn BH, Shaw GM, Oldstone MB, (1994) Virus-specific CD8+ cytotoxic T-lymphocyte activity associated with control of viremia in primary human immunodeficiency virus type 1 infection. J Virol 68: 6103-6110.
45. Koup RA, (1994) Virus escape from CTL recognition. J Exp Med 180: 779-782.
46. Matano T, Shibata R, Siemon C, Connors M, Lane HC, et al. (1998) Administration of an anti-CD8 monoclonal antibody interferes with the clearance of chimeric simian/human immunodeficiency virus during primary infections of rhesus macaques. J Virol 72: 164-169.
47. Jin X, Bauer DE, Tuttleton SE, Lewin S, Gettie A, et al. (1999) Dramatic rise in plasma viremia after CD8(+) T cell depletion in simian immunodeficiency virus-infected macaques. J Exp Med 189: 991-998.
48. Schmitz JE, Kuroda MJ, Santra S, Sasseville VG, Simon MA, et al. (1999) Control of viremia in simian immunodeficiency virus infection by CD8+ lymphocytes. Science 283: 857-860.
49. Mavilio D, Lombardo G, Kinter A, Fogli M, La Sala A, et al. (2006) Characterization of the defective interaction between a subset of natural killer cells and dendritic cells in HIV-1 infection. J Exp Med 203: 2339-2350.
50. Alter G, Teigen N, Davis BT, Addo MM, Suscovich TJ, et al. (2005) Sequential deregulation of NK cell subset distribution and function starting in acute HIV-1 infection. Blood 106: 3366-3369.
51. Mavilio D, Benjamin J, Daucher M, Lombardo G, Kottilil S, et al. (2003) Natural killer cells in HIV-1 infection: dichotomous effects of viremia on inhibitory and activating receptors and their functional correlates. Proc Natl Acad Sci USA 100: 15011-15016.
52. Sun Y, Permar SR, Buzby AP, Letvin NL, (2007) Memory CD4+ T-lymphocyte loss and dysfunction during primary simian immunodeficiency virus infection. J Virol 81: 8009-8015.
53. Kozlowski P, Lin M, Meikle L, Kwiatkowski DJ, (2007) Robust method for distinguishing heterozygous from homozygous transgenic alleles by multiplex ligation-dependent probe assay. Biotechniques 42: 584, 586, 588.
54. Chenna R, Sugawara H, Koike T, Lopez R, Gibson TJ, et al. (2003) Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res 31: 3497-3500.