The role of HIV-specific antibody-dependent cellular cytotoxicity in HIV prevention and the influence of the HIV-1 Vpu protein

AIDS

Volumn 29, Issue 2, 2015, Pages 137-144

  Kramski, Marit ^a   Stratov, Ivan ^a   Kent, Stephen J ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Antibodies; Antibody dependent cellular cytotoxicity; HIV; Tetherin; Viral protein U

Indexed keywords

ERDOSTEINE; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; UNCLASSIFIED DRUG; VPU PROTEIN; BST2 PROTEIN, HUMAN; GLYCOSYLPHOSPHATIDYLINOSITOL ANCHORED PROTEIN; HUMAN IMMUNODEFICIENCY VIRUS PROTEIN; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; LEUKOCYTE ANTIGEN; VIRUS PROTEIN; VPU PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS 1;

ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; CELL MEDIATED CYTOTOXICITY; CELLULAR IMMUNITY; DISEASE COURSE; DISEASE TRANSMISSION; EFFECTOR CELL; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IN VITRO STUDY; INFECTION CONTROL; INFECTION PREVENTION; NATURAL KILLER CELL; NONHUMAN; OBSERVATIONAL STUDY; REVIEW; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; ACQUIRED IMMUNODEFICIENCY SYNDROME; ANIMAL; BIOSYNTHESIS; HIV INFECTIONS; IMMUNOLOGY; MOUSE; PASSIVE IMMUNIZATION; RHESUS MONKEY;

ACQUIRED IMMUNODEFICIENCY SYNDROME; AIDS VACCINES; ANIMALS; ANTIBODY-DEPENDENT CELL CYTOTOXICITY; ANTIGENS, CD; GPI-LINKED PROTEINS; HIV ANTIBODIES; HIV INFECTIONS; HUMAN IMMUNODEFICIENCY VIRUS PROTEINS; HUMANS; IMMUNIZATION, PASSIVE; KILLER CELLS, NATURAL; MACACA MULATTA; MICE; SIMIAN IMMUNODEFICIENCY VIRUS; VIRAL REGULATORY AND ACCESSORY PROTEINS;

EID: 84920274731     PISSN: 02699370     EISSN: 14735571     Source Type: Journal    
DOI: 10.1097/QAD.0000000000000523     Document Type: Review

References (66)

1. Kramski M, Schorcht A, Johnston APR, Lichtfuss GF, Jegaskanda S, De Rose R, et al. Role of monocytes in mediating HIV-specific antibody-dependent cellular cytotoxicity. J Immunol Methods 2012; 384:51-61.
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. Madhavi V, Navis M, Chung AW, Isitman G, Wren LH, De Rose R, et al. Activation of NK cells by HIV-specific ADCC antibodies: role for granulocytes in expressing HIV-1 peptide epitopes. Hum Vaccines Immunother 2013; 9:1011-1018.
4. Daëron M. Fc receptor biology. Annu Rev Immunol 1997; 15:203-234.
5. Baum LL, Cassutt KJ, Knigge K, Khattri R, Margolick J, Rinaldo C, et al. HIV-1 gp120-specific antibody-dependent cell-mediated cytotoxicity correlates with rate of disease progression. J Immunol 1996; 157:2168-2173.
6. Baum LL. Role of humoral immunity in host defense against HIV. Curr HIV/AIDS Rep 2010; 7:11-18.
7. Lambotte O, Ferrari G, Moog C, Yates NL, Liao H-X, Parks RJ, et al. Heterogeneous neutralizing antibody and antibody-dependent cell cytotoxicity responses in HIV-1 elite controllers. AIDS 2009; 23:897-906.
8. Lyerly HK, Reed DL, Matthews TJ, Langlois AJ, Ahearne PA, Petteway SR, et al. Anti-GP 120 antibodies from HIV seropositive individuals mediate broadly reactive anti-HIV ADCC. AIDS Res Hum Retroviruses 1987; 3:409-422.
9. Berger CT, Alter G. Natural killer cells in spontaneous control of HIV infection. Curr Opin HIV AIDS 2011; 6:208-213.
10. 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; 75:6953-6961.
11. Johansson SE, Rollman E, Chung AW, Center RJ, Hejdeman B, Stratov I, et al. NK cell function and antibodies mediating ADCC in HIV-1-infected viremic and controller patients. Viral Immunol 2011; 24:359-368.
12. Chung AW, Navis M, Isitman G, Wren L, Silvers J, Amin J, et al. Activation of NK cells by ADCC antibodies and HIV disease progression. J Acquir Immune Defic Syndr 2011; 58:127-131.
13. Wren LH, Chung AW, Isitman G, Kelleher AD, Parsons MS, Amin J, et al. Specific antibody-dependent cellular cytotoxicity responses associated with slow progression of HIV infection. Immunology 2013; 138:116-123.
14. Ahmad A, Menezes J. Antibody-dependent cellular cytotoxicity in HIV infections. FASEB J 1996; 10:258-266.
15. Ahmad R, Sindhu ST, Toma E, Morisset R, Vincelette J, Menezes J, et al. Evidence for a correlation between antibody-dependent cellular cytotoxicity-mediating anti-HIV-1 antibodies and prognostic predictors of HIV infection. J Clin Immunol 2001; 21:227-233.
16. Alter G, Altfeld M. NK cells in HIV-1 infection: evidence for their role in the control of HIV-1 infection. J Intern Med 2009; 265:29-42.
17. Alpert MD, Harvey JD, Lauer WA, Reeves RK, Piatak M, Carville A, et al. ADCC develops over time during persistent infection with live-attenuated SIV and is associated with complete protection against SIV(mac)251 challenge. PLoS Pathog 2012; 8:e1002890.
18. Huber M, Trkola A. Humoral immunity to HIV-1: neutralization and beyond. J Intern Med 2007; 262:5-25.
19. Stratov I, Chung A, Kent SJ. Robust NK cell-mediated human immunodeficiency virus (HIV)-specific antibody-dependent responses in HIV-infected subjects. J Virol 2008; 82:5450-5459.
20. Rerks-Ngarm S, Pitisuttithum P, Nitayaphan S, Kaewkungwal J, Chiu J, Paris R, et al. Vaccination with ALVAC and AIDSVAX to prevent HIV-1 infection in Thailand. N Engl J Med 2009; 361:2209-2220.
21. Cohen J. AIDS research. Novel antibody response may explain HIV vaccine success. Science 2011; 333:1560.
22. Haynes BFB, Gilbert PBP, McElrath MJM, Zolla-Pazner SS, Tomaras GDG, Alam SMS, et al. Immune-correlates analysis of an HIV-1 vaccine efficacy trial. N Engl J Med 2012; 366:1275-1286.
23. Rolland M, Edlefsen PT, Larsen BB, Tovanabutra S, Sanders-Buell E, Hertz T, et al. Increased HIV-1 vaccine efficacy against viruses with genetic signatures in Env V2. Nature 2012; 490:417-420.
24. Tomaras GD, Ferrari G, Shen X, Alam SM, Liao H-X, Pollara J, 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 U S A 2013; 110:9019-9024.
25. Bonsignori M, Montefiori DC, Wu X, Chen X, Hwang K-K, Tsao C-Y, et al. Two distinct broadly neutralizing antibody specificities of different clonal lineages in a single HIV-1-infected donor: implications for vaccine design. J Virol 2012; 86:4688-4692.
26. Yates NL, Liao H-X, Fong Y, DeCamp A, Vandergrift NA, Williams WT, et al. Vaccine-induced Env V1-V2 IgG3 correlates with lower HIV-1 infection risk and declines soon after vaccination. Sci Transl Med 2014; 6:228ra39.
27. Chung AW, Ghebremichael M, Robinson H, Brown E, Choi I, Lane S, et al. Polyfunctional Fc-effector profiles mediated by IgG subclass selection distinguish RV144 and VAX003 vaccines. Sci Transl Med 2014; 6:228ra38.
28. Gómez-Román VR, Patterson LJ, Venzon D, Liewehr D, Aldrich K, Florese R, et al. Vaccine-elicited antibodies mediate antibody-dependent cellular cytotoxicity correlated with significantly reduced acute viremia in rhesus macaques challenged with SIVmac251. J Immunol 2005; 174:2185-2189.
29. Hidajat R, Xiao P, Zhou Q, Venzon D, Summers LE, Kalyanaraman VS, et al. Correlation of vaccine-elicited systemic and mucosal nonneutralizing antibody activities with reduced acute viremia following intrarectal simian immunodeficiency virus SIVmac251 challenge of rhesus macaques. J Virol 2009; 83:791-801.
30. Xiao P, Zhao J, Patterson LJ, Brocca-Cofano E, Venzon D, Kozlowski PA, et al. Multiple vaccine-elicited nonneutralizing antienvelope antibody activities contribute to protective efficacy by reducing both acute and chronic viremia following simian/human immunodeficiency virus SHIV89.6P challenge in rhesus macaques. J Virol 2010; 84:7161-7173.
31. Florese RH, Demberg T, Xiao P, Kuller L, Larsen K, Summers LE, et al. Contribution of nonneutralizing vaccine-elicited antibody activities to improved protective efficacy in rhesus macaques immunized with Tat/Env compared with multigenic vaccines. J Immunol 2009; 182:3718-3727.
32. Brocca-Cofano E, McKinnon K, Demberg T, Venzon D, Hidajat R, Xiao P, et al. Vaccine-elicited SIV and HIV envelope-specific IgA and IgG memory B cells in rhesus macaque peripheral blood correlate with functional antibody responses and reduced viremia. Vaccine 2011; 29:3310-3319.
33. Ohkawa SS, Xu KK, Wilson LAL, Montelaro RR, Martin LNL, Murphey-Corb MM. Analysis of envelope glycoprotein-specific antibodies from SIV-infected and gp110-immunized monkeys in ACC and ADCC assays. AIDS Res Hum Retroviruses 1995; 11:395-403.
34. Bialuk I, Whitney S, Andresen V, Florese RH, Nacsa J, Cecchinato V, et al. Vaccine induced antibodies to the first variable loop of human immunodeficiency virus type 1 gp120, mediate antibody-dependent virus inhibition in macaques. Vaccine 2011; 30:78-94.
35. Barouch DH, Liu J, Li H, Maxfield LF, Abbink P, Lynch DM, et al. Vaccine protection against acquisition of neutralization-resistant SIV challenges in rhesus monkeys. Nature 2012; 482:89-93.
36. Hessell AJ, Hangartner L, Hunter M, Havenith CEG, Beurskens FJ, Bakker JM, et al. Fc receptor but not complement binding is important in antibody protection against HIV. Nature 2007; 449:101-104.
37. Hessell AJ, Rakasz EG, Poignard P, Hangartner L, Landucci G, Forthal DN, et al. Broadly neutralizing human anti-HIV antibody 2G12 is effective in protection against mucosal SHIV challenge even at low serum neutralizing titers. PLoS Pathog 2009; 5:e1000433.
38. Pietzsch J, Gruell H, Bournazos S, Donovan BM, Klein F, Diskin R, et al. A mouse model for HIV-1 entry. Proc Natl Acad Sci U S A 2012; 109:15859-15864.
39. Moldt B, Schultz N, Dunlop DC, Alpert MD, Harvey JD, Evans DT, et al. A panel of IgG1 b12 variants with selectively diminished or enhanced affinity for Fc( receptors to define the role of effector functions in protection against HIV. J Virol 2011; 85:10572-10581.
40. Moldt B, Shibata-Koyama M, Rakasz EG, Schultz N, Kanda Y, Dunlop DC, et al. A nonfucosylated variant of the anti-HIV-1 monoclonal antibody b12 has enhanced Fc(RIIIa-mediated antiviral activity in vitro but does not improve protection against mucosal SHIV challenge in macaques. J Virol 2012; 86:6189-6196.
41. Moldt B, Rakasz EG, Schultz N, Chan-Hui P-Y, Swiderek K, Weisgrau KL, et al. Highly potent HIV-specific antibody neutralization in vitro translates into effective protection against mucosal SHIV challenge in vivo. Proc Natl Acad Sci US A 2012; 109:18921-18925.
42. Burton DR, Hessell AJ, Keele BF, Klasse PJ, Ketas TA, Moldt B, et al. Limited or no protection by weakly or nonneutralizing antibodies against vaginal SHIV challenge of macaques compared with a strongly neutralizing antibody. Proc Natl Acad Sci U S A 2011; 108:11181-11186.
43. Dugast A-S, Chan Y, Hoffner M, Licht A, Nkolola J, Li H, et al. Lack of protection following passive transfer of polyclonal highly functional low-dose nonneutralizing antibodies. PLoS One 2014; 9:e97229-e97229.
44. Corti D, Voss J, Gamblin SJ, Codoni G, Macagno A, Jarrossay D, et al. A neutralizing antibody selected from plasma cells that binds to group 1 and group 2 influenza A hemagglutinins. Science 2011; 333:850-856.
45. DiLillo DJ, Tan GS, Palese P, Ravetch JV. Broadly neutralizing hemagglutinin stalk-specific antibodies require Fc(R interactions for protection against influenza virus in vivo. Nat Med 2014; 20:143-151.
46. Richman DD, Wrin T, Little SJ, Petropoulos CJ. Rapid evolution of the neutralizing antibody response to HIV type 1 infection. Proc Natl Acad Sci U S A 2003; 100:4144-4149.
47. Phillips RE, Rowland-Jones S, Nixon DF, Gotch FM, Edwards JP, Ogunlesi AO, et al. Human immunodeficiency virus genetic variation that can escape cytotoxic T cell recognition. Nature 1991; 354:453-459.
48. Chung AW, Isitman G, Navis M, Kramski M, Center RJ, Kent SJ, et al. Immune escape from HIV-specific antibody-dependent cellular cytotoxicity (ADCC) pressure. Proc Natl Acad Sci 2011; 108:7505-7510.
49. Acharya P, Tolbert WD, Gohain N, Wu X, Yu L, Liu T, et al. Structural definition of an antibody-dependent cellular cytotoxicity (ADCC) response implicated in reduced risk for HIV-1 infection. J Virol 2014; 88:12895-12906.
50. Sauter D, Specht A, Kirchhoff F. Tetherin: holding on and letting go. Cell 2009; 141:392-398.
51. Giese S, Marsh M. Tetherin can restrict cell-free and cell-cell transmission of HIV from primary macrophages to T cells. PLoS Pathog 2014; 10:e1004189.
52. Strebel K. HIV-1 Vpu - an ion channel in search of a job. Biochim Biophys Acta 2014; 1838:1074-1081.
53. Roy N, Pacini G, Berlioz-Torrent C, Janvier K. Mechanisms underlying HIV-1 Vpu-mediated viral egress. Front Microbiol 2014; 5:177.
54. Strebel K. HIV accessory proteins versus host restriction factors. Curr Opin Virol 2013; 3:692-699.
55. Alvarez RA, Hamlin RE, Monroe A, Moldt B, Hotta MT, Rodriguez Caprio G, et al. HIV-1 Vpu antagonism of tetherin inhibits antibody-dependent cellular cytotoxic responses by natural killer cells. J Virol 2014; 88:6031-6046.
56. Arias JF, Heyer LN, Bredow von B, Weisgrau KL, Moldt B, Burton DR, et al. Tetherin antagonism by Vpu protects HIV-infected cells from antibody-dependent cell-mediated cytotoxicity. Proc Natl Acad Sciences U S A 2014; 111:6425-6430.
57. Pham TNQ, Lukhele S, Hajjar F, Routy J-P, Cohen ÉA. HIV Nef and Vpu protect HIV-infected CD4+ T cells from antibody-mediated cell lysis through down-modulation of CD4 and BST2. Retrovirology 2014; 11:15.
58. Li SX, Barrett BS, Heilman KJ, Messer RJ, Liberatore RA, Bieniasz PD, et al. Tetherin promotes the innate and adaptive cell-mediated immune response against retrovirus infection in vivo. J Immunol 2014; 193:306-316.
59. Schubert U, Antón LC, Bacík I, Cox JH, Bour S, Bennink JR, et al. CD4 glycoprotein degradation induced by human immunodeficiency virus type 1 Vpu protein requires the function of proteasomes and the ubiquitin-conjugating pathway. J Virol 1998; 72:2280-2288.
60. Shah AH, Sowrirajan B, Davis ZB, Ward JP, Campbell EM, Planelles V, et al. Degranulation of natural killer cells following interaction with HIV-1-infected cells is hindered by downmodulation of NTB-A by Vpu. Cell Host Microbe 2010; 8:397-409.
61. Veillette M, Désormeaux A, Medjahed H, Gharsallah N-E, Coutu M, Baalwa J, et al. Interaction with cellular CD4 exposes HIV-1 envelope epitopes targeted by antibody-dependent cell-mediated cytotoxicity. J Virol 2014; 88:2633-2644.
62. Ka˚hrström CT. Viral pathogenesis: Vpu puts the brakes on ADCC. Nat Rev Micro 2014; 12:397.
63. Alter GG, Heckerman DD, Schneidewind AA, Fadda LL, Kadie CMC, Carlson JMJ, et al. HIV-1 adaptation to NK-cell-mediated immune pressure. Nature 2011; 476:96-100.
64. Addo MM, Yu XG, Rosenberg ES, Walker BD, Altfeld M. Cytotoxic T-lymphocyte (CTL) responses directed against regulatory and accessory proteins in HIV-1 infection. DNA Cell Biol 2002; 21:671-678.
65. Addo MM, Altfeld M, Rathod A, Yu M, Yu XG, Goulder PJR, et al. HIV-1 Vpu represents a minor target for cytotoxic T lymphocytes in HIV-1-infection. AIDS 2002; 16:1071-1073.
66. Yu XG, Lichterfeld M, Addo MM, Altfeld M. Regulatory and accessory HIV-1 proteins: potential targets for HIV-1 vaccines? Curr Med Chem 2005; 12:741-747.