Functional advantage of educated KIR2DL1+ natural killer cells for anti-HIV-1 antibody-dependent activation

Clinical and Experimental Immunology

Volumn 184, Issue 1, 2016, Pages 101-109

  Gooneratne, S L ^a   Center, R J ^b   Kent, S J ^a,c   Parsons, M S ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b BURNET INSTITUTE   (Australia)

^c MELBOURNE SEXUAL HEALTH CENTRE   (Australia)

Author keywords

AIDS; Killer immunoglobulin like receptors; Natural killer cells

Indexed keywords

CHEMOKINE RECEPTOR CCR5; GAMMA INTERFERON; GLYCOPROTEIN GP 140; HLA C ANTIGEN; HUMAN IMMUNODEFICIENCY VIRUS 1 ANTIBODY; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 2DL1; UNCLASSIFIED DRUG; CD57 ANTIGEN; GP140 ENVELOPE PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS 1; KIR2DL1 PROTEIN, HUMAN; RECOMBINANT PROTEIN; VIRUS ENVELOPE PROTEIN;

ANTIBODY DEPENDENT ENHANCEMENT; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; HUMAN; HUMAN CELL; LYMPHOCYTE ACTIVATION; LYMPHOCYTE DIFFERENTIATION; NATURAL KILLER CELL; PRIORITY JOURNAL; TARGET CELL; ALLELE; BIOSYNTHESIS; CD4+ T LYMPHOCYTE; CLASSIFICATION; DEFICIENCY; DRUG EFFECTS; GENE EXPRESSION; GENETICS; HISTOCOMPATIBILITY TEST; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; HUMORAL IMMUNITY; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; PRIMARY CELL CULTURE; VIROLOGY;

ALLELES; ANTIGENS, CD57; CD4-POSITIVE T-LYMPHOCYTES; ENV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; GENE EXPRESSION; HISTOCOMPATIBILITY TESTING; HIV ANTIBODIES; HIV INFECTIONS; HIV-1; HLA-C ANTIGENS; HUMANS; IMMUNITY, HUMORAL; IMMUNOLOGIC MEMORY; INTERFERON-GAMMA; KILLER CELLS, NATURAL; LYMPHOCYTE ACTIVATION; PRIMARY CELL CULTURE; RECEPTORS, KIR2DL1; RECOMBINANT PROTEINS;

EID: 84960247399     PISSN: 00099104     EISSN: 13652249     Source Type: Journal    
DOI: 10.1111/cei.12752     Document Type: Article

References (36)

1. Pollara J, Hart L, Brewer F et al. High-throughput quantitative analysis of HIV-1 and SIV-specific ADCC-mediating antibody responses. Cytometry A 2011; 79:603-12.
2. Smalls-Mantey A, Connors M, Sattentau QJ. Comparative efficiency of HIV-1-infected T cell killing by NK cells, monocytes and neutrophils. PLOS ONE 2013; 8:e74858
3. Veillette M, Desormeaux A, Medjahed H et al. Interaction with cellular CD4 exposes HIV-1 envelope epitopes targeted by antibody-dependent cell-mediated cytotoxicity. J Virol 2014; 88:2633-44.
4. Chung AW, Rollman E, Center RJ, Kent SJ, Stratov I. Rapid degranulation of NK cells following activation by HIV-specific antibodies. J Immunol 2009; 182:1202-10.
5. Fauriat C, Long EO, Ljunggren HG, Bryceson YT. Regulation of human NK-cell cytokine and chemokine production by target cell recognition. Blood 2010; 115:2167-76.
6. Song R, Lisovsky I, Lebouche B, Routy JP, Bruneau J, Bernard NF. HIV protective KIR3DL1/S1-HLA-B genotypes influence NK cell-mediated inhibition of HIV replication in autologous CD4 targets. PLOS Pathog 2014; 10:e1003867
7. Haynes BF, Gilbert PB, McElrath MJ et al. Immune-correlates analysis of an HIV-1 vaccine efficacy trial. N Engl J Med 2012; 366:1275-86.
8. Rerks-Ngarm S, Pitisuttithum P, Nitayaphan S et al. Vaccination with ALVAC and AIDSVAX to prevent HIV-1 infection in Thailand. N Engl J Med 2009; 361:2209-20.
9. Tomaras GD, Ferrari G, Shen X et al. Vaccine-induced plasma IgA specific for the C1 region of the HIV-1 envelope blocks binding and effector function of IgG. Proc Natl Acad Sci USA 2013; 110:9019-24.
10. Parsons MS, Loh L, Gooneratne S, Center RJ, Kent SJ. Role of education and differentiation in determining the potential of natural killer cells to respond to antibody-dependent stimulation. AIDS 2014; 28:2781-6.
11. Parsons MS, Wren L, Isitman G et al. HIV infection abrogates the functional advantage of natural killer cells educated through KIR3DL1/HLA-Bw4 interactions to mediate anti-HIV antibody-dependent cellular cytotoxicity. J Virol 2012; 86:4488-95.
12. Anfossi N, Andre P, Guia S et al. Human NK cell education by inhibitory receptors for MHC class I. Immunity 2006; 25:331-42.
13. Fauriat C, Ivarsson MA, Ljunggren HG, Malmberg KJ, Michaelsson J. Education of human natural killer cells by activating killer cell immunoglobulin-like receptors. Blood 2010; 115:1166-74.
14. Kim S, Sunwoo JB, Yang L et al. HLA alleles determine differences in human natural killer cell responsiveness and potency. Proc Natl Acad Sci USA 2008; 105:3053-8.
15. Solana R, Tarazona R, Gayoso I, Lesur O, Dupuis G, Fulop T. Innate immunosenescence: effect of aging on cells and receptors of the innate immune system in humans. Semin Immunol 2012; 24:331-41.
16. Lopez-Verges S, Milush JM, Pandey S et al. CD57 defines a functionally distinct population of mature NK cells in the human CD56dimCD16+ NK-cell subset. Blood 2010; 116:3865-74.
17. Gooneratne SL, Richard J, Lee WS, Finzi A, Kent SJ, Parsons MS. Slaying the Trojan horse: natural killer cells exhibit robust anti-HIV-1 antibody-dependent activation and cytolysis against allogeneic T cells. J Virol 2015; 89:97-109.
18. *57 is associated with a reduced risk of HIV infection. AIDS 2008; 22:1487-91.
19. Martin MP, Qi Y, Gao X et al. Innate partnership of HLA-B and KIR3DL1 subtypes against HIV-1. Nat Genet 2007; 39:733-40.
20. Williams AP, Bateman AR, Khakoo SI. Hanging in the balance. KIR and their role in disease. Mol Interv 2005; 5:226-40.
21. Jennes W, Verheyden S, Mertens JW et al. Inhibitory KIR/HLA incompatibility between sexual partners confers protection against HIV-1 transmission. Blood 2013; 121:1157-64.
22. Korner C, Granoff ME, Amero MA et al. Increased frequency and function of KIR2DL1-3(+) NK cells in primary HIV-1 infection are determined by HLA-C group haplotypes. Eur J Immunol 2014; 44:2938-48.
23. Eller MA, Eller LA, Ouma BJ et al. Elevated natural killer cell activity despite altered functional and phenotypic profile in Ugandans with HIV-1 clade A or clade D infection. J Acquir Immune Defic Syndr 2009; 51:380-9.
24. Wong AH, Williams K, Reddy S et al. Alterations in natural killer cell receptor profiles during HIV type 1 disease progression among chronically infected South African adults. AIDS Res Hum Retroviruses 2010; 26:459-69.
25. Kamya P, Tallon B, Melendez-Pena C et al. Inhibitory killer immunoglobulin-like receptors to self HLA-B and HLA-C ligands contribute differentially to natural killer cell functional potential in HIV infected slow progressors. Clin Immunol 2012; 143:246-55.
26. Parsons MS, Tang CC, Jegaskanda S et al. Anti-HIV antibody-dependent activation of NK cells impairs NKp46 expression. J Immunol 2014; 192:308-15.
27. Center RJ, Wheatley AK, Campbell SM et al. Induction of HIV-1 subtype B and AE-specific neutralizing antibodies in mice and macaques with DNA prime and recombinant gp140 protein boost regimens. Vaccine 2009; 27:6605-12.
28. Charoudeh HN, Schmied L, Gonzalez A et al. Quantity of HLA-C surface expression and licensing of KIR2DL+ natural killer cells. Immunogenetics 2012; 64:739-45.
29. Mabuka J, Nduati R, Odem-Davis K, Peterson D, Overbaugh J. HIV-specific antibodies capable of ADCC are common in breastmilk and are associated with reduced risk of transmission in women with high viral loads. PLOS Pathog 2012; 8:e1002739.
30. Batraville LA, Richard J, Veillette M et al. Short communication: anti-HIV-1 envelope immunoglobulin Gs in blood and cervicovaginal samples of Beninese commercial sex workers. AIDS Res Hum Retroviruses 2014; 30:1145-9.
31. Parsons MS, Madhavi V, Ana-Sosa-Batiz F et al. Seminal plasma anti-HIV antibodies trigger antibody-dependent cellular cytotoxicity: implications for HIV transmission. JAIDS 2016; 71:17-23.
32. Ward JP, Bonaparte MI, Barker E. HLA-C and HLA-E reduce antibody-dependent natural killer cell-mediated cytotoxicity of HIV-infected primary T cell blasts. AIDS 2004; 18:1769-79.
33. Lang P, Pfeiffer M, Handgretinger R et al. Clinical scale isolation of T cell-depleted CD56+ donor lymphocytes in children. Bone Marrow Transplant 2002; 29:497-502.
34. Terszowski G, Klein C, Stern M. KIR/HLA interactions negatively affect rituximab- but not GA101 (obinutuzumab)-induced antibody-dependent cellular cytotoxicity. J Immunol 2014; 192:5618-24.
35. Smalls-Mantey A, Doria-Rose N, Klein R et al. Antibody-dependent cellular cytotoxicity against primary HIV-infected CD4+ T cells is directly associated with the magnitude of surface IgG binding. J Virol 2012; 86:8672-80.
36. Forthal DN, Landucci G, Daar ES. Antibody from patients with acute human immunodeficiency virus (HIV) infection inhibits primary strains of HIV type 1 in the presence of natural-killer effector cells. J Virol 2001; 75:6953-61.