Enhances Protective and Detrimental HLA Class I-Mediated Immunity in Chronic Viral Infection
Killer cell immunoglobulin-like receptors (KIRs) influence both innate and adaptive immunity. But while the role of KIRs in NK-mediated innate immunity is well-documented, the impact of KIRs on the T cell response in human disease is not known. Here we test the hypothesis that an individual's KIR genotype affects the efficiency of their HLA class I-mediated antiviral immune response and the outcome of viral infection. We show that, in two unrelated viral infections, hepatitis C virus and human T lymphotropic virus type 1, possession of the KIR2DL2 gene enhanced both protective and detrimental HLA class I-restricted anti-viral immunity. These results reveal a novel role for inhibitory KIRs. We conclude that inhibitory KIRs, in synergy with T cells, are a major determinant of the outcome of persistent viral infection.
Vyšlo v časopise:
Enhances Protective and Detrimental HLA Class I-Mediated Immunity in Chronic Viral Infection. PLoS Pathog 7(10): e32767. doi:10.1371/journal.ppat.1002270
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1002270
Souhrn
Killer cell immunoglobulin-like receptors (KIRs) influence both innate and adaptive immunity. But while the role of KIRs in NK-mediated innate immunity is well-documented, the impact of KIRs on the T cell response in human disease is not known. Here we test the hypothesis that an individual's KIR genotype affects the efficiency of their HLA class I-mediated antiviral immune response and the outcome of viral infection. We show that, in two unrelated viral infections, hepatitis C virus and human T lymphotropic virus type 1, possession of the KIR2DL2 gene enhanced both protective and detrimental HLA class I-restricted anti-viral immunity. These results reveal a novel role for inhibitory KIRs. We conclude that inhibitory KIRs, in synergy with T cells, are a major determinant of the outcome of persistent viral infection.
Zdroje
1. MingariMCMorettaAMorettaL 1998 Regulation of KIR expression in human T cells: a safety mechanism that may impair protective T-cell responses. Immunol Today 19 153 157
2. SpeiserDEPittetMJValmoriDDunbarRRimoldiD 1999 In vivo expression of natural killer cell inhibitory receptors by human melanoma-specific cytolytic T lymphocytes. J Exp Med 190 775 782
3. SpeiserDEValmoriDRimoldiDPittetMJLienardD 1999 CD28-negative cytolytic effector T cells frequently express NK receptors and are present at variable proportions in circulating lymphocytes from healthy donors and melanoma patients. Eur J Immunol 29 1990 1999
4. LongEORajagopalanS 2000 HLA class I recognition by killer cell Ig-like receptors. Semin Immunol 12 101 108
5. GerosaFBaldani-GuerraBNisiiCMarchesiniVCarraG 2002 Reciprocal Activating Interaction between Natural Killer Cells and Dendritic Cells. J Exp Med 195 327 333
6. PiccioliDSbranaSMelandriEValianteNM 2002 Contact-dependent Stimulation and Inhibition of Dendritic Cells by Natural Killer Cells. J Exp Med 195 335 341
7. RauletDH 2004 Interplay of natural killer cells and their receptors with the adaptive immune response. Nat Immunol 5 996 1002
8. WagtmannNRajagopalanSWinterCCPeruzziMLongEO 1995 Killer cell inhibitory receptors specific for HLA-C and HLA-B identified by direct binding and by functional transfer. Immunity 3 801 809
9. MoestaAKNormanPJYawataMYawataNGleimerM 2008 Synergistic polymorphism at two positions distal to the ligand-binding site makes KIR2DL2 a stronger receptor for HLA-C than KIR2DL3. J Immunol 180 3969 3979
10. KhakooSIThioCLMartinMPBrooksCRGaoX 2004 HLA and NK cell inhibitory receptor genes in resolving hepatitis C virus infection. Science 305 872 874
11. MartinMPQiYGaoXYamadaEMartinJN 2007 Innate partnership of HLA-B and KIR3DL1 subtypes against HIV-1. Nat Genet 39 733 740
12. NagaiMUsukuKMatsumotoWKodamaDTakenouchiN 1998 Analysis of HTLV-I proviral load in 202 HAM/TSP patients and 243 asymptomatic HTLV-I carriers: high proviral load strongly predisposes to HAM/TSP. J Neurovirol 4 586 593
13. JefferyKJSiddiquiAABunceMLloydALVineAM 2000 The influence of HLA class I alleles and heterozygosity on the outcome of human T cell lymphotropic virus type I infection. J Immunol 165 7278 7284
14. JefferyKJUsukuKHallSEMatsumotoWTaylorGP 1999 HLA alleles determine human T-lymphotropic virus-I (HTLV-I) proviral load and the risk of HTLV-I-associated myelopathy. Proc Natl Acad Sci U S A 96 3848 3853
15. DustinLBRiceCM 2007 Flying Under the Radar: The Immunobiology of Hepatitis C. Annu Rev Immunol 25 71 99
16. KimAYKuntzenTTimmJNolanBEBacaMA 2011 Spontaneous control of HCV is associated with the expression of HLA-B*57 and preservation of targeted epitopes. Gastroenterology 140 686 696
17. KuniholmMHKovacsAGaoXXueXMartiD 2010 Specific human leukocyte antigen class I and II alleles associated with hepatitis C virus viremia. Hepatology 51 1514 1522
18. ThioCLGaoXGoedertJJVlahovDNelsonKE 2002 HLA-Cw*04 and Hepatitis C Virus Persistence. J Virol 76 4792 4797
19. ChuangWC-MSarkodieFBrownCJOwusu-OforiSBrownJ 2007 Protective effect of HLA-B57 on HCV genotype 2 infection in a West African population. J Med Virol 79 724 733
20. MacNamaraRowanHilburnKadolskyFujiwara 2010 HLA class I binding of HBZ determines outcome in HTLV-1 infection. PLoS Pathog 6 e1001117
21. MacNamaraAKadolskyUBanghamCRAsquithB 2009 T-cell epitope prediction: rescaling can mask biological variation between MHC molecules. PLoS Comput Biol 5 e1000327
22. NormanPJCookMACareyBSCarringtonCVVerityDH 2004 SNP haplotypes and allele frequencies show evidence for disruptive and balancing selection in the human leukocyte receptor complex. Immunogenetics 56 225 237
23. WinterCCGumperzJEParhamPLongEOWagtmannN 1998 Direct binding and functional transfer of NK cell inhibitory receptors reveal novel patterns of HLA-C allotype recognition. J Immunol 161 571 577
24. O'ConnorGMGuinanKJCunninghamRTMiddletonDParhamP 2007 Functional polymorphism of the KIR3DL1/S1 receptor on human NK cells. J Immunol 178 235 241
25. YawataMYawataNDraghiMLittleAMPartheniouF 2006 Roles for HLA and KIR polymorphisms in natural killer cell repertoire selection and modulation of effector function. J Exp Med 203 633 645
26. VilchesCParhamP 2002 KIR: diverse, rapidly evolving receptors of innate and adaptive immunity. Annu Rev Immunol 20 217 251
27. FaddaLBorhisGAhmedPCheentKPageonSV Peptide antagonism as a mechanism for NK cell activation. Proc Natl Acad Sci U S A 107 10160 10165
28. AhlenstielGMartinMPGaoXCarringtonMRehermannB 2008 Distinct KIR/HLA compound genotypes affect the kinetics of human antiviral natural killer cell responses. J Clin Invest 118 1017 1026
29. ThomasDLThioCLMartinMPQiYGeD 2009 Genetic variation in IL28B and spontaneous clearance of hepatitis C virus. Nature 461 798 801
30. UgoliniSArpinCAnfossiNWalzerTCambiaggiA 2001 Involvement of inhibitory NKRs in the survival of a subset of memory-phenotype CD8+ T cells. Nat Immunol 2 430 435
31. YoungNTUhrbergMPhillipsJHLanierLLParhamP 2001 Differential expression of leukocyte receptor complex-encoded Ig-like receptors correlates with the transition from effector to memory CTL. J Immunol 166 3933 3941
32. GatiAGuerraNGaudinCDa RochaSEscudierB 2003 CD158 Receptor Controls Cytotoxic T-Lymphocyte Susceptibility to Tumor-Mediated Activation-Induced Cell Death by Interfering with Fas Signaling. Cancer Res 63 7475 7482
33. YoungNTUhrbergM 2002 KIR expression shapes cytotoxic repertoires: a developmental program of survival. Trends Immunol 23 71 75
34. AnfossiNPascalVVivierEUgoliniS 2001 Biology of T memory type 1 cells. Immunol Rev 181 269 278
35. BieganowskaKHollsbergPBuckleGJLimDGGretenTF 1999 Direct analysis of viral-specific CD8+ T cells with soluble HLA-A2/Tax11-19 tetramer complexes in patients with human T cell lymphotropic virus-associated myelopathy. J Immunol 162 1765 1771
36. BonorinoPLeroyVDufeu-DuchesneTTongiani-DashanSSturmN 2007 Features and distribution of CD8 T cells with human leukocyte antigen class I-specific receptor expression in chronic hepatitis C. Hepatology 46 1375 1386
37. SoderquestKWalzerTZafirovaBKlavinskisLSPolicB Cutting edge: CD8+ T cell priming in the absence of NK cells leads to enhanced memory responses. J Immunol 186 3304 3308
38. TakaoSIshikawaTYamashitaKUchiyamaT The rapid induction of HLA-E is essential for the survival of antigen-activated naive CD4 T cells from attack by NK cells. J Immunol 185 6031 6040
39. AlterGRihnSStreeckHTeigenNPiechocka-TrochaA 2008 Ligand-independent exhaustion of killer immunoglobulin-like receptor-positive CD8+ T cells in human immunodeficiency virus type 1 infection. J Virol 82 9668 9677
40. PoonKMontamat-SicotteDCumberbatchNMcMichaelAJCallanMF 2005 Expression of leukocyte immunoglobulin-like receptors and natural killer receptors on virus-specific CD8+ T cells during the evolution of Epstein-Barr virus-specific immune responses in vivo. Viral Immunol 18 513 522
41. van der VekenLTCampeloMDvan der HoornMAHagedoornRSvan EgmondHM 2009 Functional analysis of killer Ig-like receptor-expressing cytomegalovirus-specific CD8+ T cells. J Immunol 182 92 101
42. VlahovDAnthonyJCMunozAMargolickJNelsonKE 1991 The ALIVE study, a longitudinal study of HIV-1 infection in intravenous drug users: description of methods and characteristics of participants. NIDA Res Monogr 109 75 100
43. GoedertJJKesslerCMAledortLMBiggarRJAndesWA 1989 A prospective study of human immunodeficiency virus type 1 infection and the development of AIDS in subjects with hemophilia. N Engl J Med 321 1141 1148
44. HilgartnerMWDonfieldSMWilloughbyAContantCFEvattBL 1993 Hemophilia growth and development study. Design, methods, and entry data. Am J Pediatr Hematol Oncol 15 208 218
45. BunceMO'NeillCMBarnardoMCNMKrausaPBrowningMJ 1995 Phototyping: comprehensive DNA typing for HLA-A, B, C, DRB1, DRB3, DRB4, DRB5 & DQB1 by PCR with 144 primer mixes utilizing sequence-specific primers (PCR-SSP). Tissue Antigens 46 355 367
46. MartinMPGaoXLeeJ-HNelsonGWDetelsR 2002 Epistatic interaction between KIR3DS1 and HLA-B delays the progression to AIDS. Nat Genet 31 429 434
47. UhrbergMValianteNMShumBPShillingHGLienert-WeidenbachK 1997 Human diversity in killer cell inhibitory receptor genes. Immunity 7 753 763
48. NagaiMUsukuKMatsumotoWKodamaDTakenouchiN 1998 Analysis of HTLV-I proviral load in 202 HAM/TSP patients and 243 asymptomatic HTLV-I carriers: high proviral load strongly predisposes to HAM/TSP. J Virol 4 586 593
49. ThioCLGaoXGoedertJJVlahovDNelsonKE 2002 HLA-Cw*04 and hepatitis C virus persistence. J Virol 76 4792 4797
50. CohenJ 1988 Statistical Power Analysis for the Behavioral Sciences
51. YangXYuX 2009 An introduction to epitope prediction methods and software. Rev Med Virol 19 77 96
52. BorghansJAMMølgaardAde BoerRJKeşmirC 2007 HLA Alleles Associated with Slow Progression to AIDS Truly Prefer to Present HIV-1 p24. PLoS ONE 2 e920 e920
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Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
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