KIR2DL2 enhances protective and detrimental HLA class I-mediated immunity in chronic viral infection

PLoS Pathogens

Volumn 7, Issue 10, 2011, Pages

  Seich al Basatena, Nafisa Katrin ^a   MacNamara, Aidan ^a   Vine, Alison M ^a   Thio, Chloe L ^b   Astemborski, Jacquie ^b   Usuku, Koichiro ^c   Osame, Mitsuhiro ^d   Kirk, Gregory D ^b   Donfield, Sharyne M ^e   Goedert, James J ^f   Bangham, Charles R M ^a   Carrington, Mary ^g,h   Khakoo, Salim I ^a   Asquith, Becca ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c KUMAMOTO UNIVERSITY   (Japan)

^d KAGOSHIMA UNIVERSITY   (Japan)

^e Rho   (United States)

^f NATIONAL CANCER INSTITUTE   (United States)

^g SAIC FREDERICK INC   (United States)

^h MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HLA ANTIGEN CLASS 1; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 2DL1; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 2DL2; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 2DL3; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 2DL4; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR; KIR2DL2 PROTEIN, HUMAN;

ADAPTIVE IMMUNITY; ADULT; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; GENOTYPE; HAPLOTYPE; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; HUMAN T CELL LEUKEMIA VIRUS 1; MAJOR CLINICAL STUDY; MOLECULAR INTERACTION; PROTEIN ANALYSIS; PROTEIN FUNCTION; T LYMPHOCYTE; VIRAL CLEARANCE; VIRUS IMMUNITY; VIRUS LOAD; FEMALE; GENE; GENETICS; HUMAN T CELL LEUKEMIA VIRUS INFECTION; IMMUNOLOGY; MALE; METABOLISM; NATURAL KILLER CELL; PHYSIOLOGY; VIROLOGY;

HEPATITIS C VIRUS; HUMAN T-LYMPHOTROPIC VIRUS 1;

FEMALE; GENES, MHC CLASS I; HEPACIVIRUS; HEPATITIS C, CHRONIC; HISTOCOMPATIBILITY ANTIGENS CLASS I; HTLV-I INFECTIONS; HUMAN T-LYMPHOTROPIC VIRUS 1; HUMANS; KILLER CELLS, NATURAL; MALE; RECEPTORS, KIR; RECEPTORS, KIR2DL2; T-LYMPHOCYTES; VIRAL LOAD;

EID: 80055091825     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002270     Document Type: Article

References (52)

1. Mingari MC, Moretta A, Moretta L, (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. Speiser DE, Pittet MJ, Valmori D, Dunbar R, Rimoldi D, et al. (1999) In vivo expression of natural killer cell inhibitory receptors by human melanoma-specific cytolytic T lymphocytes. J Exp Med 190: 775-782.
3. Speiser DE, Valmori D, Rimoldi D, Pittet MJ, Lienard D, et al. (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. Long EO, Rajagopalan S, (2000) HLA class I recognition by killer cell Ig-like receptors. Semin Immunol 12: 101-108.
5. Gerosa F, Baldani-Guerra B, Nisii C, Marchesini V, Carra G, et al. (2002) Reciprocal Activating Interaction between Natural Killer Cells and Dendritic Cells. J Exp Med 195: 327-333.
6. Piccioli D, Sbrana S, Melandri E, Valiante NM, (2002) Contact-dependent Stimulation and Inhibition of Dendritic Cells by Natural Killer Cells. J Exp Med 195: 335-341.
7. Raulet DH, (2004) Interplay of natural killer cells and their receptors with the adaptive immune response. Nat Immunol 5: 996-1002.
8. Wagtmann N, Rajagopalan S, Winter CC, Peruzzi M, Long EO, (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. Moesta AK, Norman PJ, Yawata M, Yawata N, Gleimer M, et al. (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. 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.
11. 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.
12. Nagai M, Usuku K, Matsumoto W, Kodama D, Takenouchi N, et al. (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. Jeffery KJ, Siddiqui AA, Bunce M, Lloyd AL, Vine AM, et al. (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. Jeffery KJ, Usuku K, Hall SE, Matsumoto W, Taylor GP, et al. (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. Dustin LB, Rice CM, (2007) Flying Under the Radar: The Immunobiology of Hepatitis C. Annu Rev Immunol 25: 71-99.
16. Kim AY, Kuntzen T, Timm J, Nolan BE, Baca MA, et al. (2011) Spontaneous control of HCV is associated with the expression of HLA-B*57 and preservation of targeted epitopes. Gastroenterology 140: 686-696.
17. Kuniholm MH, Kovacs A, Gao X, Xue X, Marti D, et al. (2010) Specific human leukocyte antigen class I and II alleles associated with hepatitis C virus viremia. Hepatology 51: 1514-1522.
18. Thio CL, Gao X, Goedert JJ, Vlahov D, Nelson KE, et al. (2002) HLA-Cw*04 and Hepatitis C Virus Persistence. J Virol 76: 4792-4797.
19. Chuang WC-M, Sarkodie F, Brown CJ, Owusu-Ofori S, Brown J, et al. (2007) Protective effect of HLA-B57 on HCV genotype 2 infection in a West African population. J Med Virol 79: 724-733.
20. MacNamara, Rowan, Hilburn, Kadolsky, Fujiwara, et al. (2010) HLA class I binding of HBZ determines outcome in HTLV-1 infection. PLoS Pathog 6: e1001117.
21. MacNamara A, Kadolsky U, Bangham CR, Asquith B, (2009) T-cell epitope prediction: rescaling can mask biological variation between MHC molecules. PLoS Comput Biol 5: e1000327.
22. Norman PJ, Cook MA, Carey BS, Carrington CV, Verity DH, et al. (2004) SNP haplotypes and allele frequencies show evidence for disruptive and balancing selection in the human leukocyte receptor complex. Immunogenetics 56: 225-237.
23. Winter CC, Gumperz JE, Parham P, Long EO, Wagtmann N, (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'Connor GM, Guinan KJ, Cunningham RT, Middleton D, Parham P, et al. (2007) Functional polymorphism of the KIR3DL1/S1 receptor on human NK cells. J Immunol 178: 235-241.
25. Yawata M, Yawata N, Draghi M, Little AM, Partheniou F, et al. (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. Vilches C, Parham P, (2002) KIR: diverse, rapidly evolving receptors of innate and adaptive immunity. Annu Rev Immunol 20: 217-251.
27. Fadda L, Borhis G, Ahmed P, Cheent K, Pageon SV, et al. Peptide antagonism as a mechanism for NK cell activation. Proc Natl Acad Sci U S A 107: 10160-10165.
28. Ahlenstiel G, Martin MP, Gao X, Carrington M, Rehermann B, (2008) Distinct KIR/HLA compound genotypes affect the kinetics of human antiviral natural killer cell responses. J Clin Invest 118: 1017-1026.
29. Thomas DL, Thio CL, Martin MP, Qi Y, Ge D, et al. (2009) Genetic variation in IL28B and spontaneous clearance of hepatitis C virus. Nature 461: 798-801.
30. Ugolini S, Arpin C, Anfossi N, Walzer T, Cambiaggi A, et al. (2001) Involvement of inhibitory NKRs in the survival of a subset of memory-phenotype CD8+ T cells. Nat Immunol 2: 430-435.
31. Young NT, Uhrberg M, Phillips JH, Lanier LL, Parham P, (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. Gati A, Guerra N, Gaudin C, Da Rocha S, Escudier B, et al. (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. Young NT, Uhrberg M, (2002) KIR expression shapes cytotoxic repertoires: a developmental program of survival. Trends Immunol 23: 71-75.
34. Anfossi N, Pascal V, Vivier E, Ugolini S, (2001) Biology of T memory type 1 cells. Immunol Rev 181: 269-278.
35. Bieganowska K, Hollsberg P, Buckle GJ, Lim DG, Greten TF, et al. (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. Bonorino P, Leroy V, Dufeu-Duchesne T, Tongiani-Dashan S, Sturm N, et al. (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. Soderquest K, Walzer T, Zafirova B, Klavinskis LS, Polic B, et al. Cutting edge: CD8+ T cell priming in the absence of NK cells leads to enhanced memory responses. J Immunol 186: 3304-3308.
38. Takao S, Ishikawa T, Yamashita K, Uchiyama T, 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. Alter G, Rihn S, Streeck H, Teigen N, Piechocka-Trocha A, et al. (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. Poon K, Montamat-Sicotte D, Cumberbatch N, McMichael AJ, Callan MF, (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 Veken LT, Campelo MD, van der Hoorn MA, Hagedoorn RS, van Egmond HM, et al. (2009) Functional analysis of killer Ig-like receptor-expressing cytomegalovirus-specific CD8+ T cells. J Immunol 182: 92-101.
42. Vlahov D, Anthony JC, Munoz A, Margolick J, Nelson KE, et al. (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. Goedert JJ, Kessler CM, Aledort LM, Biggar RJ, Andes WA, et al. (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. Hilgartner MW, Donfield SM, Willoughby A, Contant CF, Evatt BL, et al. (1993) Hemophilia growth and development study. Design, methods, and entry data. Am J Pediatr Hematol Oncol 15: 208-218.
45. Bunce M, O'Neill CM, Barnardo MCNM, Krausa P, Browning MJ, et al. (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. Martin MP, Gao X, Lee J-H, Nelson GW, Detels R, et al. (2002) Epistatic interaction between KIR3DS1 and HLA-B delays the progression to AIDS. Nat Genet 31: 429-434.
47. Uhrberg M, Valiante NM, Shum BP, Shilling HG, Lienert-Weidenbach K, et al. (1997) Human diversity in killer cell inhibitory receptor genes. Immunity 7: 753-763.
48. Nagai M, Usuku K, Matsumoto W, Kodama D, Takenouchi N, et al. (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. Thio CL, Gao X, Goedert JJ, Vlahov D, Nelson KE, et al. (2002) HLA-Cw*04 and hepatitis C virus persistence. J Virol 76: 4792-4797.
50. Cohen J, (1988) Statistical Power Analysis for the Behavioral Sciences.
51. Yang X, Yu X, (2009) An introduction to epitope prediction methods and software. Rev Med Virol 19: 77-96.
52. Borghans JAM, Mølgaard A, de Boer RJ, Keşmir C, (2007) HLA Alleles Associated with Slow Progression to AIDS Truly Prefer to Present HIV-1 p24. PLoS ONE 2: e920-e920.