HIV-1-specific antibody responses during acute and chronic HIV-1 infection

Current Opinion in HIV and AIDS

Volumn 4, Issue 5, 2009, Pages 373-379

  Tomaras, Georgia D ^a   Haynes, Barton F ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Antibody; Humoral responses; Isotype; Mucosal

Indexed keywords

CD8 ANTIGEN; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY; IMMUNOGLOBULIN G;

ANTIBODY RESPONSE; ANTIBODY SPECIFICITY; B LYMPHOCYTE; BINDING AFFINITY; CD8+ T LYMPHOCYTE; CHRONIC DISEASE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; HUMORAL IMMUNITY; LATENT PERIOD; MICROENVIRONMENT; NONHUMAN; PRIORITY JOURNAL; REVIEW; VIRUS INHIBITION; VIRUS REPLICATION; VIRUS TRANSMISSION;

HIV ANTIBODIES; HIV INFECTIONS; HIV-1; HUMANS;

EID: 69549097604     PISSN: 1746630X     EISSN: 17466318     Source Type: Journal    
DOI: 10.1097/COH.0b013e32832f00c0     Document Type: Review

References (74)

1. Raghavan M, Bjorkman PJ. Fc receptors and their interactions with immunoglobulins. Annu Rev Cell Dev Biol 1996; 12:181-220.
2. Binley JM, Klasse PJ, Cao Y, et al. Differential regulation of the antibody responses to Gag and Env proteins of human immunodeficiency virus type 1. J Virol 1997; 71:2799-2809. (Pubitemid 27119919)
3. Keele BF, Giorgi EE, Salazar-Gonzalez JF, et al. Identification and characterization of transmitted and early founder virus envelopes in primary HIV-1 infection. Proc Natl Acad Sci U S A 2008; 105:7552-7557.
4. Abrahams MR, Anderson JA, Giorgi EE, et al. Quantitating the multiplicity of infection with human immunodeficiency virus type 1 subtype C reveals a non-Poisson distribution of transmitted variants. J Virol 2009; 83:3556-3567.
5. Fiebig EW, Wright DJ, Rawal BD, et al. Dynamics of HIV viremia and antibody seroconversion in plasma donors: implications for diagnosis and staging of primary HIV infection. AIDS 2003; 17:1871-1879.
6. Tomaras GD, Yates NL, Liu P, et al. Initial B-cell responses to transmitted human immunodeficiency virus type 1: virion-binding immunoglobulin M (IgM) and IgG antibodies followed by plasma antigp41 antibodies with ineffective control of initial viremia. J Virol 2008; 82:12449-12463.
7. Wei X, Decker JM, Wang S, et al. Antibody neutralization and escape by HIV-1. Nature 2003; 422:307-312.
8. 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. (Pubitemid 36418171)
9. Stacey AR, Norris PJ, Qin L, et al. Induction of a striking systemic cytokine cascade prior to peak viremia in acute human immunodeficiency virus type 1 infection, in contrast to more modest and delayed responses in acute hepatitis B and C virus infections. J Virol 2009; 83:3719-3733.
10. Davis KL, Gray ES, Moore PL, et al. High titer HIV-1 V3-specific antibodies with broad reactivity but low neutralizing potency in acute infection and following vaccination. Virology 2009; 387:414-426. This elegant study details the early development of V3-specific neutralizing antibody responses in acute infection (clades B and C) and in vaccines (clade B) using HIV-2/HIV-1 V3 Env scaffolds.
11. Moore PL, Gray ES, Choge IA, et al. The c3-v4 region is a major target of autologous neutralizing antibodies in human immunodeficiency virus type 1 subtype C infection. J Virol 2008; 82:1860-1869.
12. Honnen WJ, Krachmarov C, Kayman SC, et al. Type-specific epitopes targeted by monoclonal antibodies with exceptionally potent neutralizing activities for selected strains of human immunodeficiency virus type 1 map to a common region of the V2 domain of gp120 and differ only at single positions from the clade B consensus sequence. J Virol 2007; 81:1424-1432. (Pubitemid 46167863)
13. Rong R, Bibollet-Ruche F, Mulenga J, et al. Role of V1V2 and other human immunodeficiency virus type 1 envelope domains in resistance to autologous neutralization during clade C infection. J Virol 2007; 81:1350-1359. (Pubitemid 46167856)
14. Pinter A. Roles of HIV-1 Env variable regions in viral neutralization and vaccine development. Curr HIV Res 2007; 5:542-553. (Pubitemid 351210988)
15. Peacock DB, Jones JV, Gough M. The immune response to thetaX 174 in man. I. Primary and secondary antibody production in normal adults. Clin Exp Immunol 1973; 13:497-513.
16. Fehr T, Naim HY, Bachmann MF, et al. T-cell independent IgM and enduring protective IgG antibodies induced by chimeric measles viruses. Nat Med 1998; 4:945-948. (Pubitemid 28364035)
17. Levesque MC, Moody MA, Hwang K, et al. Polyclonal B cell differentiation and loss of gastrointestinal tract germinal centers in the earliest stages of HIV-1 infection. PLoS Med 2009 (in press). This study addresses the effect of HIV-1 transmission on the B cell subsets in the blood and terminal ileum GALTs in acute and early HIV-1 infection.
18. Binley JM, Lybarger EA, Crooks ET, et al. Profiling the specificity of neutralizing antibodies in a large panel of plasmas from patients chronically infected with human immunodeficiency virus type 1 subtypes B and C. J Virol 2008; 82:11651-11668. A comprehensive analysis of neutralizing antibody specificities and antibody isotypes in plasma from patients with HIV-1 neutralization breadth.
19. Shen X, Parks RJ, Montefiori DC, et al. In vivo gp41 antibodies targeting the 2F5 monoclonal antibody epitope mediate human immunodeficiency virus type 1 neutralization breadth. J Virol 2009; 83:3617-3625.
20. Cerutti A. The regulation of IgA class switching. Nat Rev Immunol 2008; 8:421-434. An excellent review of recent studies on innate immune recognition of pathogens and the critical role this plays in mucosal IgA class switching.
21. He B, Qiao X, Klasse PJ, et al. HIV-1 envelope triggers polyclonal Ig class switch recombination through a CD40-independent mechanism involving BAFF and C-type lectin receptors. J Immunol 2006; 176:3931-3941. (Pubitemid 44264370)
22. Shan M, Klasse PJ, Banerjee K, et al. HIV-1 gp120 mannoses induce immunosuppressive responses from dendritic cells. PLoS Pathog 2007; 3:e169. (Pubitemid 350291601)
23. Klasse J, Blomberg J. Patterns of antibodies to human immunodeficiency virus proteins in different subclasses of IgG. J Infect Dis 1987; 156:1026-1030. (Pubitemid 18017087)
24. McDougal JS, Kennedy MS, Nicholson JK, et al. Antibody response to human immunodeficiency virus in homosexual men. Relation of antibody specificity, titer, and isotype to clinical status, severity of immunodeficiency, and disease progression. J Clin Invest 1987; 80:316-324.
25. Khalife J, Guy B, Capron M, et al. Isotypic restriction of the antibody response to human immunodeficiency virus. AIDS Res Hum Retroviruses 1988; 4:3-9. (Pubitemid 18094601)
26. Mathiesen T, Chiodi F, Broliden PA, et al. Analysis of a subclass-restricted HIV-1 gp41 epitope by omission peptides. Immunology 1989; 67:1-7. (Pubitemid 19153121)
27. Mergener K, Enzensberger W, Rubsamen-Waigmann H, et al. Immunoglobulin class- and subclass-specific HIV antibody detection in serum and CSF specimens by ELISA and Western blot. Infection 1987; 15:317-322. (Pubitemid 17156101)
28. Sundqvist VA, Linde A, Kurth R, et al. Restricted IgG subclass responses to HTLV-III/LAV and to cytomegalovirus in patients with AIDS and lymphadenopathy syndrome. J Infect Dis 1986; 153:970-973. (Pubitemid 16114876)
29. Wilson KM, Johnson EI, Croom HA, et al. Incidence immunoassay for distinguishing recent from established HIV-1 infection in therapy-naive populations. AIDS 2004; 18:2253-2259.
30. Ljunggren K, Broliden PA, Morfeldt-Manson L, et al. IgG subclass response to HIV in relation to antibody-dependent cellular cytotoxicity at different clinical stages. Clin Exp Immunol 1988; 73:343-347. (Pubitemid 18228133)
31. Perez LG, Costa MR, Todd CA, et al. Utilization of IgG Fc receptors by human immunodeficiency virus type 1: a specific role for antibodies against the membrane proximal external region of gp41. J Virol 2009; 83:7397-7410. This study details the role of FcgRI and FcgRIIb with IgG subclass and antibody specificity in antibody-mediated neutralization of HIV-1.
32. Marcelino JM, Nilsson C, Barroso H, et al. Envelope-specific antibody response in HIV-2 infection: C2V3C3-specific IgG response is associated with disease progression. AIDS 2008; 22:2257-2265.
33. Chiodi F, Mathiesen T, Albert J, et al. IgG subclass responses to a transmembrane protein (gp41) peptide in HIV infection. J Immunol 1989; 142:3809-3814. (Pubitemid 19164407)
34. Lambotte O, Ferrari G, Moog C, et al. Heterogeneous neutralizing antibody and antibody-dependent cell cytotoxicity responses in HIV-1 elite controllers. AIDS 2009; 23:897-906. A comprehensive analysis of the binding and neutralizing antibody responses in a virus controller cohort that found that ADCC was higher in the virus controllers than in chronics. Among the binding antibody responses studied, anti-immunodominant and anti-MPER IgG1 and IgG2 were detected in this study, with IgG1-immunodominant antibodies found in lower concentrations in the virus controller group.
35. Trkola A, Purtscher M, Muster T, et al. Human monoclonal antibody 2G12 defines a distinctive neutralization epitope on the gp120 glycoprotein of human immunodeficiency virus type 1. J Virol 1996; 70:1100-1108. (Pubitemid 26029030)
36. Haynes BF, Montefiori DC. Aiming to induce broadly reactive neutralizing antibody responses with HIV-1 vaccine candidates. Expert Rev Vaccines 2006; 5:347-363. (Pubitemid 44167156)
37. Lal RB, Heiba IM, Dhawan RR, et al. IgG subclass responses to human immunodeficiency virus-1 antigens: lack of IgG2 response to gp41 correlates with clinical manifestation of disease. Clin Immunol Immunopathol 1991; 58:267-277.
38. Ngo-Giang-Huong N, Candotti D, Goubar A, et al. HIV type 1-specific IgG2 antibodies: markers of helper T cell type 1 response and prognostic marker of long-term nonprogression. AIDS Res Hum Retroviruses 2001; 17:1435-1446. (Pubitemid 33042811)
39. Broliden PA, Morfeldt-Mansson L, Rosen J, et al. Fine specificity of IgG subclass response to group antigens in HIV-1-infected patients. Clin Exp Immunol 1989; 76:216-221. (Pubitemid 19150391)
40. Scharf O, Golding H, King LR, et al. Immunoglobulin G3 from polyclonal human immunodeficiency virus (HIV) immune globulin is more potent than other subclasses in neutralizing HIV type 1. J Virol 2001; 75:6558-6565. (Pubitemid 32578175)
41. Beniguel L, Begaud E, Peruchon S, et al. Isotype profiles of antigp160 antibodies from HIV-infected patients in plasma and culture supernatants. Immunol Lett 2004; 93:57-62. (Pubitemid 38591521)
42. Kovacsovics-Bankowski M, Carini C, Kashala O, Essex M. Isotypic distribution of HIV-1-specific antibodies in individuals from central Africa. Viral Immunol 1992; 5:243-248. (Pubitemid 23054085)
43. Klasse PJ, Berntorp E, Hansson BG. An aberrant subclass pattern of HIV-specific immunoglobulin G in sera from haemophiliacs. AIDS 1988; 2:311-313. (Pubitemid 18230845)
44. Haynes BF, Shattock RJ. Critical issues in mucosal immunity for HIV-1 vaccine development. J Allergy Clin Immunol 2008; 122:3-9; quiz 10-11.
45. Bomsel M, Heyman M, Hocini H, et al. Intracellular neutralization of HIV transcytosis across tight epithelial barriers by anti-HIV envelope protein dIgA or IgM. Immunity 1998; 9:277-287. (Pubitemid 28400041)
46. Alfsen A, Iniguez P, Bouguyon E, Bomsel M. Secretory IgA specific for a conserved epitope on gp41 envelope glycoprotein inhibits epithelial transcytosis of HIV-1. J Immunol 2001; 166:6257-6265. (Pubitemid 32440758)
47. Battle-Miller K, Eby CA, Landay AL, et al. Antibody-dependent cell-mediated cytotoxicity in cervical lavage fluids of human immunodeficiency virus type 1-infected women. J Infect Dis 2002; 185:439-447. (Pubitemid 34142805)
48. Rowland-Jones S. Dimers are a girl's best friend. Nat Med 1997; 3:1199-1200. (Pubitemid 27508817)
49. Hirbod T, Broliden K, Kaul R. Genital immunoglobulin A and HIV-1 protection: virus neutralization versus specificity. AIDS 2008; 22:2401-2402.
50. Hirbod T, Kaul R, Reichard C, et al. HIV-neutralizing immunoglobulin A and HIV-specific proliferation are independently associated with reduced HIV acquisition in Kenyan sex workers. AIDS 2008; 22:727-735. Several studies have reported potentially protective immune responses in highly exposed, persistently HIV-1-seronegative (HEPS) individuals. This recent study found neutralizing IgA antibodies in the lower genital tract that was associated with reduced rates of HIV-1 acquisition. Of note, these IgA antibodies were not HIV-1-specific and the specificity of these neutralizing IgA antibodies remains unknown.
51. Horton RE, Ball TB, Wachichi C, et al. Cervical HIV-specific IgA in a population of commercial sex workers correlates with repeated exposure but not resistance to HIV. AIDS Res Hum Retroviruses 2009; 25:83-92.
52. Granados-Gonzalez V, Piedrahita LD, Martinez M, et al. Neutralizing interclade cross-reactivity of HIV-1 V1/V2-specific immunoglobulin A in Colombian and French cohorts. AIDS 2009; 23:in press.
53. Ravetch JV, Bolland S. IgG Fc receptors. Annu Rev Immunol 2001; 19:275-290.
54. Walker MR, Lund J, Thompson KM, Jefferis R. Aglycosylation of human IgG1 and IgG3 monoclonal antibodies can eliminate recognition by human cells expressing Fc gamma RI and/or Fc gamma RII receptors. Biochem J 1989; 259:347-353. (Pubitemid 19111668)
55. Burton DR. Antibodies, viruses and vaccines. Nat Rev Immunol 2002; 2:706-713.
56. Stoiber H, Speth C, Dierich MP. Role of complement in the control of HIV dynamics and pathogenesis. Vaccine 2003; 21 (Suppl 2):S77-S82. (Pubitemid 36588652)
57. Moir S, Fauci AS. B cells in HIV infection and disease. Nat Rev Immunol 2009; 9:235-245. A recent expert review on the mechanisms of B cell dysfunction in HIV-1 with accompanying time line of research highlights since 1983.
58. Forthal DN, Landucci G, Bream J, et al. FcgammaRIIa genotype predicts progression of HIV infection. J Immunol 2007; 179:7916-7923.
59. Hessell AJ, Hangartner L, Hunter M, et al. Fc receptor but not complement binding is important in antibody protection against HIV. Nature 2007; 449:101-104. (Pubitemid 47373775)
60. Martinez V, Costagliola D, Bonduelle O, et al. Combination of HIV-1-specific CD4 Th1 cell responses and IgG2 antibodies is the best predictor for persistence of long-term nonprogression. J Infect Dis 2005; 191:2053-2063. (Pubitemid 40800576)
61. Toptygina AP, Pukhalsky AL, Alioshkin VA. Immunoglobulin G subclass profile of antimeasles response in vaccinated children and in adults with measles history. Clin Diagn Lab Immunol 2005; 12:845-847.
62. Lange JM, Coutinho RA, Krone WJ, et al. Distinct IgG recognition patterns during progression of subclinical and clinical infection with lymphadenopathy associated virus/human T lymphotropic virus. Br Med J (Clin Res Ed) 1986; 292:228-230.
63. Lange JM, de Wolf F, Goudsmit J. Markers for progression in HIV infection. AIDS 1989; 3 (Suppl 1):S153-160.
64. Lange JM, Paul DA, Huisman HG, et al. Persistent HIV antigenaemia and decline of HIV core antibodies associated with transition to AIDS. Br Med J (Clin Res Ed) 1986; 293:1459-1462.
65. Cheingsong-Popov R, Panagiotidi C, Bowcock S, et al. Relation between humoral responses to HIV gag and env proteins at seroconversion and clinical outcome of HIV infection. Br Med J 1991; 302:23-26.
66. Weber JN, Clapham PR, Weiss RA, et al. Human immunodeficiency virus infection in two cohorts of homosexual men: neutralising sera and association of antigag antibody with prognosis. Lancet 1987; 1:119-122.
67. Chargelegue D, Stanley CM, O'Toole CM, et al. The affinity of IgG antibodies to gag p24 and p17 in HIV-1-infected patients correlates with disease progression. Clin Exp Immunol 1995; 99:175-181.
68. Forster SM, Osborne LM, Cheingsong-Popov R, et al. Decline of antip24 antibody precedes antigenaemia as correlate of prognosis in HIV-1 infection. AIDS 1987; 1:235-240. (Pubitemid 18017396)
69. Spira TJ, Kaplan JE, Holman RC, et al. Deterioration in immunologic status of human immunodeficiency virus (HIV)-infected homosexual men with lymphadenopathy: prognostic implications. J Clin Immunol 1989; 9:132-138.
70. Scheid JF, Mouquet H, Feldhahn N, et al. Broad diversity of neutralizing antibodies isolated from memory B cells in HIV-infected individuals. Nature 2009; 458:636-640. Using HIV-1 gp140 protein as bait, this study isolated HIV-1-neutralizing antibodies from HIV-1-specific memory B cells from the blood of HIV-1 elite controllers. Of interest to the work covered in this review, upon examination of the antibody repertoire, they found skewing toward kappa (k) antibody light chain.
71. Simek MD, Rida W, Priddy FH, et al. HIV-1 elite neutralizers: individuals with broad and potent neutralizing activity identified using a high throughput neutralization assay together with an analytical selection algorithm. J Virol 2009; 83:7337-7348.
72. Sather DN, Armann J, Ching LK, et al. Factors associated with the development of cross-reactive neutralizing antibodies during human immunodeficiency virus type 1 infection. J Virol 2009; 83:757-769.
73. Stamatatos L, Morris L, Burton DR, Mascola JR. Neutralizing antibodies generated during natural HIV-1 infection: good news for an HIV-1 vaccine? Nat Med 2009. Epub ahead of print doi: 10.1038/nm.1949.
74. Scheid JF, Mouquet H, Feldhahn N, et al. A method for identification of HIV gp140 binding memory B cells in human blood. J Immunol Methods 2009; 343:65-67.