Impact of protective killer inhibitory receptor/human leukocyte antigen genotypes on natural killer cell and T-cell function in HIV-1-infected controllers

AIDS

Volumn 26, Issue 15, 2012, Pages 1869-1878

  Tomescu, Costin ^a   Duh, Fuh Mei ^b,c   Hoh, Rebecca ^d   Viviani, Anne ^d   Harvill, Kara ^d   Martin, Maureen P ^b,c   Carrington, Mary ^b,c   Deeks, Steven G ^d   Montaner, Luis J ^a  

^a WISTAR INSTITUTE   (United States)

^b SAIC FREDERICK INC   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

AIDS; elite controllers; HIV 1; human leukocyte antigen; killer inhibitory receptor; natural killer cells; T cells

Indexed keywords

ALPHA INTERFERON; HLA B57 ANTIGEN; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 3DL1;

ADAPTIVE IMMUNITY; ADULT; ARTICLE; CD8+ T LYMPHOCYTE; GENOTYPE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; INNATE IMMUNITY; NATURAL KILLER CELL; PRIORITY JOURNAL; T LYMPHOCYTE; VIRUS CELL INTERACTION; VIRUS REPLICATION;

ACQUIRED IMMUNODEFICIENCY SYNDROME; ADAPTIVE IMMUNITY; ADULT; CALIFORNIA; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; DISEASE PROGRESSION; FEMALE; GENOTYPE; HIV SEROPOSITIVITY; HIV-1; HUMANS; IMMUNITY, INNATE; KILLER CELLS, NATURAL; MALE; RECEPTORS, KIR; RECEPTORS, KIR3DL1; RNA, VIRAL; VIRUS REPLICATION;

EID: 84866735381     PISSN: 02699370     EISSN: 14735571     Source Type: Journal    
DOI: 10.1097/QAD.0b013e32835861b0     Document Type: Article

References (48)

1. Grabar S, Selinger-Leneman H, Abgrall S, Pialoux G, Weiss L, Costagliola D. Prevalence and comparative characteristics of long-Term nonprogressors and HIV controller patients in the French Hospital Database on HIV. AIDS 2009; 23:1163-1169.
2. Hubert JB, Burgard M, Dussaix E, Tamalet C, Deveau C, Le Chenadec J, et al. Natural history of serum HIV-1 RNA levels in 330 patients with a known date of infection. The SEROCO Study Group. AIDS 2000; 14:123-131. (Pubitemid 30116437)
3. Deeks SG, Walker BD. Human immunodeficiency virus controllers: mechanisms of durable virus control in the absence of antiretroviral therapy. Immunity 2007; 27:406-416. (Pubitemid 47418678)
4. Buzon MJ, Seiss K, Weiss R, Brass AL, Rosenberg ES, Pereyra F, et al. Inhibition of HIV-1 integration in ex vivo-infected CD4 T cells from elite controllers. J Virol 2011; 85:9646-9650.
5. Chen H, Li C, Huang J, Cung T, Seiss K, Beamon J, et al. CD4RT cells from elite controllers resist HIV-1 infection by selective upregulation of p21. J Clin Invest 2011; 121:1549-1560.
6. Brumme ZL, Li C, Miura T, Sela J, Rosato PC, Brumme CJ, et al. Reduced replication capacity of NL4-3 recombinant viruses encoding reverse transcriptase-integrase sequences from HIV-1 elite controllers. J Acquir Immune Defic Syndr 2011; 56:100-108.
7. Miura T, Brockman MA, Brumme ZL, Brumme CJ, Pereyra F, Trocha A, et al. HLA-Associated alterations in replication capacity of chimeric NL4-3 viruses carrying gag-protease from elite controllers of human immunodeficiency virus type 1. J Virol 2009; 83:140-149.
8. Miura T, Brumme CJ, Brockman MA, Brumme ZL, Pereyra F, Block BL, et al. HLA-Associated viral mutations are common in human immunodeficiency virus type 1 elite controllers. J Virol 2009; 83:3407-3412.
9. Miura T, Brumme ZL, Brockman MA, Rosato P, Sela J, Brumme CJ, et al. Impaired replication capacity of acute/early viruses in persons who become HIV controllers. J Virol 2010; 84:7581-7591.
10. Emu B, Sinclair E, Hatano H, Ferre A, Shacklett B, Martin JN, et al. HLA class I-restricted T cell responses may contribute to the control of HIV infection, but such responses are not always necessary for long-Term virus control. J Virol 2008; 82:5398-5407. (Pubitemid 351705247)
11. Mothe B, Llano A, Ibarrondo J, Zamarreno J, Schiaulini M, Miranda C, et al. CTL responses of high functional avidity and broad variant cross-reactivity are associated with HIV control. PLoS One 2012; 7:e29717.
12. Pereyra F, Addo MM, Kaufmann DE, Liu Y, Miura T, Rathod A, et al. Genetic and immunologic heterogeneity among persons who control HIV infection in the absence of therapy. J Infect Dis 2008; 197:563-571. (Pubitemid 351321534)
13. Hersperger AR, Martin JN, Shin LY, Sheth PM, Kovacs CM, Cosma GL, et al. Increased HIV-specific CD8RT-cell cytotoxic potential in HIV elite controllers is associated with T-bet expression. Blood 2012; 117:3799-3808.
14. Hersperger AR, Pereyra F, Nason M, Demers K, Sheth P, Shin LY, et al. Perforin expression directly ex vivo by HIV-specific CD8 T-cells is a correlate of HIV elite control. PLoS Pathog 2010; 6:e1000917.
15. Costello C, Tang J, Rivers C, Karita E, Meizen-Derr J, Allen S, Kaslow RA. HLA-BM5703 independently associated with slower HIV-1 disease progression in Rwandan women. AIDS 1999; 13:1990-1991. (Pubitemid 29509568)
16. McNeil AJ, Yap PL, Gore SM, Brettle RP, McColl M, Wyld R, et al. Association of HLA types A1-B8-DR3 and B27 with rapid and slow progression of HIV disease. QJM 1996; 89:177-185. (Pubitemid 26086136)
17. den Uyl D, van der Horst-Bruinsma IE, van Agtmael M. Progression of HIV to AIDS: a protective role for HLA-B27? AIDS Rev 2004; 6:89-96.
18. Migueles SA, Laborico AC, Imamichi H, Shupert WL, Royce C, McLaughlin M, et al. The differential ability of HLA BM5701R long-Term nonprogressors and progressors to restrict human immunodeficiency virus replication is not caused by loss of recognition of autologous viral gag sequences. J Virol 2003; 77:6889-6898. (Pubitemid 36666882)
19. Kamya P, Boulet S, Tsoukas CM, Routy JP, Thomas R, Cote P, et al. Receptor-ligand requirements for increased NK cell polyfunctional potential in slow progressors infected with HIV-1 coexpressing KIR3DL1Mh/My and HLA-BM57. J Virol 2011; 85:5949-5960.
20. Lopez-Vazquez A, Mina-Blanco A, Martinez-Borra J, Njobvu PD, Suarez-Alvarez B, Blanco-Gelaz MA, et al. Interaction between KIR3DL1 and HLA-BM57 supertype alleles influences the progression of HIV-1 infection in a Zambian population. Hum Immunol 2005; 66:285-289. (Pubitemid 40395248)
21. Martin MP, Qi Y, Gao X, Yamada E, Martin JN, Pereyra F, et al. Innate partnership of HLA-B and KIR3DL1 subtypes against HIV-1. Nat Genet 2007; 39:733-740. (Pubitemid 46848586)
22. Martin MP, Gao X, Lee JH, Nelson GW, Detels R, Goedert JJ, et al. Epistatic interaction between KIR3DS1 and HLA-B delays the progression to AIDS. Nat Genet 2002; 31:429-434. (Pubitemid 35154456)
23. Yawata M, Yawata N, Draghi M, Little AM, Partheniou F, Parham P. Roles for HLA and KIR polymorphisms in natural killer cell repertoire selection and modulation of effector function. J Exp Med 2006; 203:633-645.
24. Long BR, Ndhlovu LC, Oksenberg JR, Lanier LL, Hecht FM, Nixon DF, Barbour JD. KIR3DS1 conferral of enhanced natural killer cell function in early HIV-1 infection. J Virol 2008; 82:4785-4592.
25. Alter G, Martin MP, Teigen N, Carr WH, Suscovich TJ, Schneidewind A, et al. Differential natural killer cell-mediated inhibition of HIV-1 replication based on distinct KIR/HLA subtypes. J Exp Med 2007; 204:3027-3036. (Pubitemid 350179568)
26. Boulet S, Kleyman M, Kim JY, Kamya P, Sharafi S, Simic N, et al. A combined genotype of KIR3DL1 high expressing alleles and HLA-BM57 is associated with a reduced risk of HIV infection. AIDS 2008; 22:1487-1491.
27. Naranbhai V, Bartman P, Ndlovu D, Ramkalawon P, Ndung'u T, Wilson D, et al. Impact of blood processing variations on natural killer cell frequency, activation, chemokine receptor expression and function. J Immunol Methods 2011; 366:28-35.
28. Martin MP, Carrington M. KIR locus polymorphisms: genotyping and disease association analysis. Methods Mol Biol 2008; 415:49-64.
29. Thomas R, Yamada E, Alter G, Martin MP, Bashirova AA, Norman PJ, et al. Novel KIR3DL1 alleles and their expression levels on NK cells: convergent evolution of KIR3DL1 phenotype variation? J Immunol 2008; 180:6743-6750.
30. Stern M, Ruggeri L, Capanni M, Mancusi A, Velardi A. Human leukocyte antigens A23, A24, and A32 but not A25 are ligands for KIR3DL1. Blood 2008; 112:708-710.
31. Tomescu C, Chehimi J, Maino VC, Montaner LJ. NK cell lysis of HIV-1-infected autologous CD4 primary T cells: requirement for IFN-mediated NK activation by plasmacytoid dendritic cells. J Immunol 2007; 179:2097-2104.
32. De Maria A, Fogli M, Costa P, Murdaca G, Puppo F, Mavilio D, et al. The impaired NK cell cytolytic function in viremic HIV-1 infection is associated with a reduced surface expression of natural cytotoxicity receptors (NKp46, NKp30 and NKp44). Eur J Immunol 2003; 33:2410-2418. (Pubitemid 37138973)
33. Mavilio D, Benjamin J, Daucher M, Lombardo G, Kottilil S, Planta MA, et al. 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 2003; 100:15011-15016. (Pubitemid 37518008)
34. Sirianni MC, Mezzaroma I, Aiuti F, Moretta A. Analysis of the cytolytic activity mediated by natural killer cells from acquired immunodeficiency syndrome patients in response to phytohemagglutinin or anti-CD16 monoclonal antibody. Eur J Immunol 1994; 24:1874-1878. (Pubitemid 24237561)
35. Julg B, Williams KL, Reddy S, Bishop K, Qi Y, Carrington M, et al. Enhanced anti-HIV functional activity associated with Gag-specific CD8 T-cell responses. J Virol 2010; 84:5540-5549.
36. Kiepiela P, Ngumbela K, Thobakgale C, Ramduth D, Honeyborne I, Moodley E, et al. CD8R T-cell responses to different HIV proteins have discordant associations with viral load. Nat Med 2007; 13:46-53. (Pubitemid 46067385)
37. Waggoner SN, Cornberg M, Selin LK, Welsh RM. Natural killer cells act as rheostats modulating antiviral T cells. Nature 2011; 481:394-410.
38. Bandyopadhyay S, Perussia B, Trinchieri G, Miller DS, Starr SE. Requirement for HLA-DRR accessory cells in natural killing of cytomegalovirus-infected fibroblasts. J Exp Med 1986; 164: 180-195. (Pubitemid 16069231)
39. Feldman M, Howell D, Fitzgerald-Bocarsly P. Interferon-Alphadependent and -independent participation of accessory cells in natural killer cell-mediated lysis of HSV-1-infected fibroblasts. J Leukoc Biol 1992; 52:473-482.
40. Fitzgerald-Bocarsly P, Feldman M, Curl S, Schnell J, Denny T. Positively selected Leu-11a (CD16R) cells require the presence of accessory cells or factors for the lysis of herpes simplex virusinfected fibroblasts but not herpes simplex virus-infected Raji. J Immunol 1989; 143:1318-1326. (Pubitemid 19211367)
41. Oh SH, Bandyopadhyay S, Miller DS, Starr SE. Cooperation between CD16(Leu-11b)R NK cells and HLA-DRR cells in natural killing of herpesvirus-infected fibroblasts. J Immunol 1987; 139:2799-2802. (Pubitemid 17153963)
42. Perussia B, Fanning V, Trinchieri G. A leukocyte subset bearing HLA-DR antigens is responsible for in vitro alpha interferon production in response to viruses. Nat Immun Cell Growth Regul 1985; 4:120-137. (Pubitemid 15228688)
43. Boulet S, Song R, Kamya P, Bruneau J, Shoukry NH, Tsoukas CM, Bernard NF. HIV protective KIR3DL1 and HLA-B genotypes influence NK cell function following stimulation with HLA-devoid cells. J Immunol 2010; 184:2057-2064.
44. Machmach K, Leal M, Gras C, Viciana P, Genebat M, Franco E, et al. Plasmacytoid dendritic cells reduce HIV production in elite controllers. J Virol 2012; 86:4245-4252.
45. Martinez-Picado J, Prado JG, Fry EE, Pfafferott K, Leslie A, Chetty S, et al. Fitness cost of escape mutations in p24 Gag in association with control of human immunodeficiency virus type 1. J Virol 2006; 80:3617-3623.
46. Fadda L, O'Connor GM, Kumar S, Piechocka-Trocha A, Gardiner CM, Carrington M, et al. Common HIV-1 peptide variants mediate differential binding of KIR3DL1 to HLA-Bw4 molecules. J Virol 2011; 85:5970-5974.
47. Alter G, Heckerman D, Schneidewind A, Fadda L, Kadie CM, Carlson JM, et al. HIV-1 adaptation to NK-cell-mediated immune pressure. Nature 2011; 476:96-100.
48. Autran B, Descours B, Avettand-Fenoel V, Rouzioux C. Elite controllers as a model of functional cure. Curr Opin HIV AIDS 2011; 6:181-187.