Association of Activating KIR Copy Number Variation of NK Cells with Containment of SIV Replication in Rhesus Monkeys

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While the contribution of CD8⁺ cytotoxic T lymphocytes to early containment of HIV-1 spread is well established, a role for NK cells in controlling HIV-1 replication during primary infection has been uncertain. The highly polymorphic family of KIR molecules expressed on NK cells can inhibit or activate these effector cells and might therefore modulate their activity against HIV-1-infected cells. In the present study, we investigated copy number variation in KIR3DH loci encoding the only activating KIR receptor family in rhesus monkeys and its effect on simian immunodeficiency virus (SIV) replication during primary infection in rhesus monkeys. We observed an association between copy numbers of KIR3DH genes and control of SIV replication in Mamu-A*01^– rhesus monkeys that express restrictive TRIM5 alleles. These findings provide further evidence for an association between NK cells and the early containment of SIV replication, and underscore the potential importance of activating KIRs in stimulating NK cell responses to control SIV spread.

Vyšlo v časopise: Association of Activating KIR Copy Number Variation of NK Cells with Containment of SIV Replication in Rhesus Monkeys. PLoS Pathog 7(12): e32767. doi:10.1371/journal.ppat.1002436
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1002436

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1. BironCA 1999 Initial and innate responses to viral infections--pattern setting in immunity or disease. Curr Opin Microbiol 2 374 381

2. CerwenkaALanierLL 2001 Natural killer cells, viruses and cancer. Nat Rev Immunol 1 41 49

3. OrangeJS 2002 Human natural killer cell deficiencies and susceptibility to infection. Microbes Infect 4 1545 1558

4. LanierLL 2005 NK cell recognition. Annu Rev Immunol 23 225 274

5. TrinchieriG 1989 Biology of natural killer cells. Adv Immunol 47 187 376

6. MorettaABottinoCMingariMCBiassoniRMorettaL 2002 What is a natural killer cell? Nat Immunol 3 6 8

7. VivierENunesJAVelyF 2004 Natural killer cell signaling pathways. Science 306 1517 1519

8. MorettaASivoriSVitaleMPendeDMorelliL 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. PendeDBiassoniRCantoniCVerdianiSFalcoM 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. ParhamP 2005 MHC class I molecules and KIRs in human history, health and survival. Nat Rev Immunol 5 201 214

11. MartinMPCarringtonM 2005 Immunogenetics of viral infections. Curr Opin Immunol 17 510 516

12. MartinMPGaoXLeeJHNelsonGWDetelsR 2002 Epistatic interaction between KIR3DS1 and HLA-B delays the progression to AIDS. Nat Genet 31 429 434

13. AlterGMartinMPTeigenNCarrWHSuscovichTJ 2007 Differential natural killer cell-mediated inhibition of HIV-1 replication based on distinct KIR/HLA subtypes. J Exp Med 204 3027 3036

14. AlterGRihnSWalterKNoltingAMartinM 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. MartinMPPascalVYeagerMPhairJKirkGD 2007 A mutation in KIR3DS1 that results in truncation and lack of cell surface expression. Immunogenetics 59 823 829

16. HaigwoodNL 2004 Predictive value of primate models for AIDS. AIDS Rev 6 187 198

17. HershbergerKLShyamRMiuraALetvinNL 2001 Diversity of the killer cell Ig-like receptors of rhesus monkeys. J Immunol 166 4380 4390

18. BlokhuisJHDoxiadisGGBontropRE 2009 A splice site mutation converts an inhibitory killer cell Ig-like receptor into an activating one. Mol Immunol 46 640 648

19. BlokhuisJHvan der WielMKDoxiadisGGBontropRE 2010 The mosaic of KIR haplotypes in rhesus macaques. Immunogenetics 62 295 306

20. ChaichompooPBostikPStephensonSUdompunturukSKobkitjaroenJ 2010 Multiple KIR gene polymorphisms are associated with plasma viral loads in SIV-infected rhesus macaques. Cell Immunol 263 176 187

21. KrusePHRosnerCWalterL 2010 Characterization of rhesus macaque KIR genotypes and haplotypes. Immunogenetics 62 281 293

22. DegenhardtJDde CandiaPChabotASchwartzSHendersonL 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. YasutomiYReimannKALordCIMillerMDLetvinNL 1993 Simian immunodeficiency virus-specific CD8+ lymphocyte response in acutely infected rhesus monkeys. J Virol 67 1707 1711

24. PalRVenzonDLetvinNLSantraSMontefioriDC 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. MotheBRWeinfurterJWangCRehrauerWWilsonN 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. LoffredoJTMaxwellJQiYGliddenCEBorchardtGJ 2007 Mamu-B*08-positive macaques control simian immunodeficiency virus replication. J Virol 81 8827 8832

27. YantLJFriedrichTCJohnsonRCMayGEManessNJ 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. LimSYRogersTChanTWhitneyJBKimJ 2010 TRIM5alpha Modulates Immunodeficiency Virus Control in Rhesus Monkeys. PLoS Pathog 6 e1000738

29. LimSYChanTGelmanRSWhitneyJBO'BrienKL 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. LifsonJDNowakMAGoldsteinSRossioJLKinterA 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. LetvinNLMascolaJRSunYGorgoneDABuzbyAP 2006 Preserved CD4+ central memory T cells and survival in vaccinated SIV-challenged monkeys. Science 312 1530 1533

32. ValianteNMUhrbergMShillingHGLienert-WeidenbachKArnettKL 1997 Functionally and structurally distinct NK cell receptor repertoires in the peripheral blood of two human donors. Immunity 7 739 751

33. BostikPKobkitjaroenJTangWVillingerFPereiraLE 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. ReevesRKGillisJWongFEYuYConnoleM 2010 CD16- natural killer cells: enrichment in mucosal and secondary lymphoid tissues and altered function during chronic SIV infection. Blood 115 4439 4446

35. MartinMPQiYGaoXYamadaEMartinJN 2007 Innate partnership of HLA-B and KIR3DL1 subtypes against HIV-1. Nat Genet 39 733 740

36. QiYMartinMPGaoXJacobsonLGoedertJJ 2006 KIR/HLA pleiotropism: protection against both HIV and opportunistic infections. PLoS Pathog 2 e79

37. BouletSSharafiSSimicNBruneauJRoutyJP 2008 Increased proportion of KIR3DS1 homozygotes in HIV-exposed uninfected individuals. Aids 22 595 599

38. GaudieriSDeSantisDMcKinnonEMooreCNolanD 2005 Killer immunoglobulin-like receptors and HLA act both independently and synergistically to modify HIV disease progression. Genes Immun 6 683 690

39. JennesWVerheydenSDemanetCAdje-ToureCAVuylstekeB 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. RavetSScott-AlgaraDBonnetETranHKTranT 2007 Distinctive NK-cell receptor repertoires sustain high-level constitutive NK-cell activation in HIV-exposed uninfected individuals. Blood 109 4296 4305

41. MiddletonDGonzalezAGilmorePM 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. GoodridgeJPLathburyLJSteinerNKShulseCNPullikotilP 2007 Three common alleles of KIR2DL4 (CD158d) encode constitutively expressed, inducible and secreted receptors in NK cells. Eur J Immunol 37 199 211

43. SauermannUSiddiquiRSuhYSPlatzerMLeuchteN 2008 Mhc class I haplotypes associated with survival time in simian immunodeficiency virus (SIV)-infected rhesus macaques. Genes Immun 9 69 80

44. BorrowPLewickiHHahnBHShawGMOldstoneMB 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. KoupRA 1994 Virus escape from CTL recognition. J Exp Med 180 779 782

46. MatanoTShibataRSiemonCConnorsMLaneHC 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. JinXBauerDETuttletonSELewinSGettieA 1999 Dramatic rise in plasma viremia after CD8(+) T cell depletion in simian immunodeficiency virus-infected macaques. J Exp Med 189 991 998

48. SchmitzJEKurodaMJSantraSSassevilleVGSimonMA 1999 Control of viremia in simian immunodeficiency virus infection by CD8+ lymphocytes. Science 283 857 860

49. MavilioDLombardoGKinterAFogliMLa SalaA 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. AlterGTeigenNDavisBTAddoMMSuscovichTJ 2005 Sequential deregulation of NK cell subset distribution and function starting in acute HIV-1 infection. Blood 106 3366 3369

51. MavilioDBenjaminJDaucherMLombardoGKottililS 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 U S A 100 15011 15016

52. SunYPermarSRBuzbyAPLetvinNL 2007 Memory CD4+ T-lymphocyte loss and dysfunction during primary simian immunodeficiency virus infection. J Virol 81 8009 8015

53. KozlowskiPLinMMeikleLKwiatkowskiDJ 2007 Robust method for distinguishing heterozygous from homozygous transgenic alleles by multiplex ligation-dependent probe assay. Biotechniques 42 584, 586, 588

54. ChennaRSugawaraHKoikeTLopezRGibsonTJ 2003 Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res 31 3497 3500