Breadth of HIV-1 Env-specific antibody-dependent cellular cytotoxicity: Relevance to global HIV vaccine design

AIDS

Volumn 28, Issue 13, 2014, Pages 1859-1870

  Madhavi, Vijaya ^a   Wren, Leia H ^a   Center, Rob J ^a   Gonelli, Christopher ^a   Winnall, Wendy R ^a   Parsons, Matthew S ^a   Kramski, Marit ^a   Kent, Stephen J ^a,b,c   Stratov, Ivan ^a,b,c  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b The Anxiety Clinic   (Australia)

^c ALFRED HOSPITAL   (Australia)

Author keywords

Antibody dependent cellular cytotoxicity; Env; Glycosylation; HIV controllers; HIV 1; Natural killer cells

Indexed keywords

GLYCOPROTEIN GP 140; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; VIRUS ENVELOPE PROTEIN; EPITOPE; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY;

ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ARTICLE; CELL ACTIVATION; CELL KILLING; CLINICAL ARTICLE; CONTROLLED STUDY; CROSS REACTION; DRUG DESIGN; GLYCOSYLATION; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNE RESPONSE; NATURAL KILLER CELL; PRIORITY JOURNAL; VIRUS TYPING; ADULT; CLASSIFICATION; CYTOTOXIC T LYMPHOCYTE; FEMALE; GENETICS; GENOTYPE; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOLOGY; MALE; MIDDLE AGED; YOUNG ADULT;

ADULT; AIDS VACCINES; ENV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; EPITOPES; FEMALE; GENOTYPE; HIV ANTIBODIES; HIV INFECTIONS; HIV-1; HUMANS; MALE; MIDDLE AGED; T-LYMPHOCYTES, CYTOTOXIC; YOUNG ADULT;

EID: 84906794353     PISSN: 02699370     EISSN: 14735571     Source Type: Journal    
DOI: 10.1097/QAD.0000000000000310     Document Type: Article

References (52)

1. Battegay M, Nuesch R, Hirschel B, Kaufmann GR. Immunological recovery and antiretroviral therapy in HIV-1 infection. Lancet Infect Dis 2006; 6:280-287.
2. Buchbinder SP, Mehrotra DV, Duerr A, Fitzgerald DW, Mogg R, Li D, et al. Efficacy assessment of a cell-mediated immunity HIV-1 vaccine (the Step Study): a double-blind, randomised, placebo-controlled, test-of-concept trial. Lancet 2008; 372: 1881-1893.
3. Pitisuttithum P. HIV-1 prophylactic vaccine trials in Thailand. Curr HIV Res 2005; 3:17-30.
4. Sanou MP, De Groot AS, Murphey-Corb M, Levy JA, Yamamoto JK. HIV-1 vaccine trials: evolving concepts and designs. Open AIDS J 2012; 6:274-288.
5. 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.
6. Haynes BF, Gilbert PB, McElrath MJ, Zolla-Pazner S, Tomaras GD, Alam SM, et al. Immune-correlates analysis of an HIV-1 vaccine efficacy trial. N Engl J Med 2012; 366:1275-1286.
7. Bonsignori M, Pollara J, Moody MA, Alpert MD, Chen X, Hwang KK, et al. Antibody-dependent cellular cytotoxicity-mediating antibodies from an HIV-1 vaccine efficacy trial target multiple epitopes and preferentially use the VH1 gene family. J Virol 2012; 86:11521-11532.
8. Tomaras GD, Ferrari G, Shen XY, Alam SM, Liao HX, 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.
9. Kamya P, Tallon B, Melendez-Pena C, Parsons MS, Migueles SA, Connors M, 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; 143:246-255.
10. Sáez-Cirión A, Bacchus C, Hocqueloux L, Avettand-Fenoel V, Girault I, Lecuroux C, et al. Post-treatment HIV-1 controllers with a long-term virological remission after the interruption of early initiated antiretroviral therapy ANRS VISCONTI study. PLoS Pathog 2013; 9:e1003211.
11. Mellors JW, Kingsley LA, Rinaldo CR Jr, Todd JA, Hoo BS, Kokka RP, et al. Quantitation of HIV-1 RNA in plasma predicts outcome after seroconversion. Ann Intern Med 1995; 122:573-579.
12. Deacon NJ, Tsykin A, Solomon A, Smith K, Ludford-Menting M, Hooker DJ, et al. Genomic structure of an attenuated quasi species of HIV-1 from a blood transfusion donor and recipients. Science 1995; 270:988-991.
13. Zaunders J, van Bockel D. Innate and adaptive immunity in long-term non-progression in HIV disease. Front Immunol 2013; 4:95.
14. Walker BD. Elite control of HIV infection: implications for vaccines and treatments. Top HIV Med 2007; 15:134-136.
15. 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.
16. Pereya 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.
17. Lambotte O, Ferrari G, Moog C, Yates NL, Liao HX, Parks RJ, et al. Heterogeneous neutralizing antibody and antibodydependent cell cytotoxicity responses in HIV-1 elite controllers. AIDS 2009; 23:897-906.
18. Doria-Rose NA, Klein RM, Daniels MG, O'Dell S, Nason M, Lapedes A, et al. Breadth of human immunodeficiency virusspecific neutralizing activity in sera: clustering analysis and association with clinical variables. J Virol 2010; 84:1631-1636.
19. 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.
20. 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.
21. Banks ND, Kinsey N, Clements J, Hildreth JE. Sustained antibody-dependent cell-mediated cytotoxicity (ADCC) in SIVinfected macaques correlates with delayed progression to AIDS. AIDS Res Hum Retroviruses 2002; 18:1197-1205.
22. Jia M, Li D, He X, Zhao Y, Peng H, MA P, et al. Impaired natural killer cell-induced antibody-dependent cell-mediated cytotoxicity is associated with human immunodefeciency virus-1 disease progression. Clin Exp Immunol 2013; 171:107-116.
23. 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.
24. Boutwell CL, Rolland MM, Herbeck JT, Mullins JI, Allen TM. Viral evolution and escape during acute HIV-1 infection. J Infect Dis 2010; 202:S309-S314.
25. Ndung'u T, Weiss RA. On HIV diversity. AIDS 2012; 26:1255-1260.
26. Santoro MM, Perno CF. HIV-1 genetic variability and clinical implications. ISRN Microbiol 2013; 2013:481314.
27. Hemelaar J, Gouws E, Ghys PD, Osmanov S. Global trends in molecular epidemiology of HIV-1 during 2000-2007. AIDS 2011; 25:679-689.
28. Koch M, Pancera M, Kwong PD, Kolchinsky P, Grundner C, Wang L, et al. Structure-based, targeted deglycosylation of HIV-1 gp120 and effects on neutralization sensitivity and antibody recognition. Virology 2003; 313:387-400.
29. Julien JP, Sok D, Khayat R, Lee JH, Doores KJ, Walker LM, et al. Broadly neutralizing antibody PGT121 allosterically modulates CD4 binding via recognition of the HIV-1 gp120 V3 base and multiple surrounding glycans. PLoS Pathog 2013; 9:e1003342.
30. Walker LM, Huber M, Doores KJ, Falkowska E, Pejchal R, Julien JP, et al. Broad neutralization coverage of HIV by multiple highly potent antibodies. Nature 2011; 477:466-470.
31. Kovacs JM, Nkolola JP, Peng H, Cheung A, Perry J, Miller CA, et al. HIV-1 envelope trimer elicits more potent neutralizing antibody responses than monomeric gp120. Proc Natl Acad Sci U S A 2012; 109:12111-12116.
32. Anderson DJ, Politch JA, Nadolski AM, Blaskewicz CD, Pudney J, Mayer KH. Targeting Trojan Horse leukocytes for HIV prevention. AIDS 2010; 24:163-187.
33. Mascola JR, Haynes BF. HIV-1 neutralizing antibodies: understanding nature's pathways. Immunol Rev 2013; 254:225-244.
34. Stephenson KE, SanMiguel A, Simmons NL, Smith K, Lewis MG, Szinger JJ, et al. Full-length HIV-1 immunogens induce greater magnitude and comparable breadth of T lymphocyte responses to conserved HIV-1 regions compared with conserved-regiononly HIV-1 immunogens in rhesus monkeys. J Virol 2012; 86:11434-11440.
35. Garber DA, Silverstri G, Feinberg MF. Review: prospects for an AIDS vaccine: three big questions, no easy answers. Lancet Infect Dis 2004; 4:397-413.
36. Center RJ, Wheatley AK, Campbell SM, Gaeguta AJ, Peut V, Alcantara S, 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; 27:6605-6612.
37. Reeves PJ, Callewaert N, Contreras R, Khorana HG. Structure and function in rhodopsin: High-level expression of rhodopsin with restricted and homogeneous N-glycosylation by a tetracycline-inducible N-acetylglucosaminyltransferase I-negative HEK293S stable mammalian cell line. Proc Natl Acad Sci U S A 2002; 99:13419-13424.
38. Chung AW, Rollman E, Center RJ, Kent SJ, Stratov I. Rapid degranulation of NK cells following activation by HIV-specific antibodies. J Immunol 2009; 182:1202-1210.
39. 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.
40. Wren L, Parsons MS, Isitman G, Center RJ, Kelleher AD, Stratov I, et al. Influence of cytokines on HIV-specific antibody-dependent cellular cytotoxicity activation profile of natural killer cells. PLoS One 2012; 7:e38580.
41. Kramski M, Schorcht A, Johnston AP, Lichtfuss GF, Jegaskanda S, De Rose R, et al. Role of monocytes in mediating HIVspecific antibody-dependent cellular cytotoxicity. J Immunol Methods 2012; 384:51-61.
42. Gomez-Roman VR, Florese RH, Patterson LJ, Peng B, Venzon D, Aldrich K, et al. A simplified method for the rapid fluorometric assessment of antibody-dependent cell-mediated cytotoxicity. J Immunol Methods 2006; 308:53-67.
43. Genovese L, Nebuloni M, Alfano M. Cell-mediated immunity in elite controllers naturally controlling HIV viral load. Front Immunol 2013; 4:86.
44. Mandalia S, Westrop SJ, Beck EJ, Nelson M, Gazzard BG, Imami N, et al. Are long-term non-progressors very slow progressors? Insights from the Chelsea and Westminster HIV cohort, 1998-2010. PLos One 2012; 7:e29844.
45. Pejchal R, Doores KJ, Walker LM, Khayat R, Huang PS, Wang SK, et al. A potent and broad neutralizing antibody recognizes and penetrates the HIV glycan shield. Science 2011; 334:1097-1103.
46. Wei X, Decker JM, Wang S, Hui H, Kappes JC, Wu X, et al. Antibody neutralization and escape by HIV-1. Nature 2003; 422:307-312.
47. Pitisuttithum P, Gilbert P, Gurwith M, Heyward W, Martin M, van Griensven F, et al. Randomized, double-blind, placebocontrolled efficacy trial of a bivalent recombinant glycoprotein 120 HIV-1 vaccine among injection drug users in Bangkok, Thailand. J Infect Dis 2006; 194:1661-1671.
48. Huber M, Trkola A. Humoral immunity to HIV-1: neutralization and beyond. J Intern Med 2007; 262:5-25.
49. Raska M, Takahashi K, Czernekova L, Zachova K, Hall S, Moldoveanu Z, et al. Glycosylation patterns of HIV-1 gp120 depend on the type of expressing cells and affect antibody recognition. J Biol Chem 2010; 285:20860-20869.
50. Bonomelli C, Doores KJ, Dunlop DC, Thaney V, Dwek RA, Burton DR, et al. The glycan shield of HIV is predominantly oligomannose independently of production system or viral clade. PLoS One 2011; 6:e23521.
51. Doores KJ, Bonomelli C, Harvey DJ, Vasiljevic S, Dwek RA, Burton DR, et al. Envelope glycans of immunodeficiency virions are almost entirely oligomannose antigens. Proc Natl Acad Sci U S A 2010; 107:13800-13805.
52. Willey RL, Shibata R, Freed EO, Cho MW, Martin MA. Differential glycosylation, virion incorporation, and sensitivity to neutralizing antibodies of human immunodeficiency virus type 1 envelope produced from infected primary T-lymphocyte and macrophage cultures. J Virol 1996; 70:6431-6436.