IgG subclass profiles in infected HIV type 1 controllers and chronic progressors and in uninfected recipients of env vaccines

AIDS Research and Human Retroviruses

Volumn 26, Issue 4, 2010, Pages 445-458

  Banerjee, Kaustuv ^a   Klasse, P J ^a   Sanders, Rogier W ^a,b   Pereyra, Florencia ^c   Michael, Elizabeth ^a   Lu, Min ^a   Walker, Bruce D ^c   Moore, John P ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b ACADEMIC MEDICAL CENTER   (Netherlands)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAG PROTEIN; GLYCOPROTEIN GP 120; GLYCOPROTEIN GP 41; HUMAN IMMUNODEFICIENCY VIRUS ANTIGEN; IMMUNOGLOBULIN ANTIBODY; IMMUNOGLOBULIN G; IMMUNOGLOBULIN G1 ANTIBODY; IMMUNOGLOBULIN G2 ANTIBODY; IMMUNOGLOBULIN G24 ANTIBODY; IMMUNOGLOBULIN G3 ANTIBODY; PLACEBO; TRANSACTIVATOR PROTEIN; UNCLASSIFIED DRUG;

ANTIBODY RESPONSE; ANTIBODY TITER; ANTIGEN ANTIBODY REACTION; ARTICLE; CELL POLARITY; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE COURSE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; HUMORAL IMMUNITY; IMMUNE RESPONSE; INFECTION CONTROL; NONHUMAN; PRIORITY JOURNAL; TH1 CELL; TH2 CELL; VACCINATION;

AIDS VACCINES; ANTIBODIES, VIRAL; ANTIBODY SPECIFICITY; DISEASE PROGRESSION; HIV CORE PROTEIN P24; HIV ENVELOPE PROTEIN GP120; HIV ENVELOPE PROTEIN GP41; HIV INFECTIONS; HIV-1; HUMANS; IMMUNITY, HUMORAL; IMMUNOGLOBULIN G; TAT GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS;

EID: 77951817919     PISSN: 08892229     EISSN: None     Source Type: Journal    
DOI: 10.1089/aid.2009.0223     Document Type: Article

References (71)

1. Deeks SG and Walker BD: Human immunodeficiency virus controllers: Mechanisms of durable virus control in the absence of antiretroviral therapy. Immunity 2007;27:406-416.
2. Pereyra F, Addo MM, Kaufmann DE, Liu Y, Miura T, Rathod A, Baker B, Trocha A, Rosenberg R, Mackey E, Ueda P, Lu Z, Cohen D, Wrin T, Petropoulos CJ, Rosenberg ES, and Walker BD: Genetic and immunologic heterogeneity among persons who control HIV infection in the absence of therapy. J Infect Dis 2008;197:563-571.
3. Baker BM, Block BL, Rothchild AC, and Walker BD: Elite control of HIV infection: Implications for vaccine design. Expert Opin Biol Ther 2009;9:55-69.
4. Edwards BH, Bansal A, Sabbaj S, Bakari J, Mulligan MJ, and Goepfert PA: Magnitude of functional CD8+ T-cell responses to the gag protein of human immunodeficiency virus type 1 correlates inversely with viral load in plasma. J Virol 2002;76:2298-2305.
5. Geldmacher C, Currier JR, Herrmann E, Haule A, Kuta E, McCutchan F, Njovu L, Geis S, Hoffmann O, Maboko L, Williamson C, Birx D, Meyerhans A, Cox J, and Hoelscher M: CD8 T-cell recognition of multiple epitopes within specific Gag regions is associated with maintenance of a low steady-state viremia in human immunodeficiency virus type 1-seropositive patients. J Virol 2007;81:2440-2448.
6. Honeyborne I, Prendergast A, Pereyra F, Leslie A, Crawford H, Payne R, Reddy S, Bishop K, Moodley E, Nair K, van der Stok M, McCarthy N, Rousseau CM, Addo M, Mullins JI, Brander C, Kiepiela P, Walker BD, and Goulder PJ: Control of human immunodeficiency virus type 1 is associated with HLA-B*13 and targeting of multiple gag-specific CD8+ T-cell epitopes. J Virol 2007;81:3667-3672.
7. Kiepiela P, Ngumbela K, Thobakgale C, Ramduth D, Honeyborne I, Moodley E, Reddy S, de Pierres C, Mncube Z, Mkhwanazi N, Bishop K, van der Stok M, Nair K, Khan N, Crawford H, Payne R, Leslie A, Prado J, Prendergast A, Frater J, McCarthy N, Brander C, Learn GH, Nickle D, Rousseau C, Coovadia H, Mullins JI, Heckerman D, Walker BD, and Goulder P: CD8+ T-cell responses to different HIV proteins have discordant associations with viral load. Nat Med 2007;13:46-53.
8. Streeck H, Lichterfeld M, Alter G, Meier A, Teigen N, Yassine-Diab B, Sidhu HK, Little S, Kelleher A, Routy JP, Rosenberg ES, Sekaly RP, Walker BD, and Altfeld M: Recognition of a defined region within p24 gag by CD8+ T cells during primary human immunodeficiency virus type 1 infection in individuals expressing protective HLA class I alleles. J Virol 2007;81:7725-7731.
9. Cleghorn F, Pape JW, Schechter M, Bartholomew C, Sanchez J, Jack N, Metch BJ, Hansen M, Allen M, Cao H, Montefiori DC, Tomaras GD, Gurunathan S, Eastman DJ, do Lago RF, Jean S, Lama JR, Lawrence DN, and Wright PF: Lessons from a multisite international trial in the Caribbean and South America of an HIV-1 Canarypox vaccine (ALVACHIV vCP1452) with or without boosting with MN rgp120. J Acquir Immune Defic Syndr 2007;46:222-230.
10. Flynn NM, Forthal DN, Harro CD, Judson FN, Mayer KH, and Para MF: Placebo-controlled phase 3 trial of a recombinant glycoprotein 120 vaccine to prevent HIV-1 infection. J Infect Dis 2005;191:654-665.
11. Mascola JR, Snyder SW, Weislow OS, Belay SM, Belshe RB, Schwartz DH, Clements ML, Dolin R, Graham BS, Gorse GJ, Keefer MC, McElrath MJ, Walker MC, Wagner KF, McNeil JG, McCutchan FE, and Burke DS: Immunization with envelope subunit vaccine products elicits neutralizing antibodies against laboratory-adapted but not primary isolates of human immunodeficiency virus type 1. The National Institute of Allergy and Infectious Diseases AIDS Vaccine Evaluation Group. J Infect Dis 1996;173:340-348.
12. Pitisuttithum P, Gilbert P, Gurwith M, Heyward W, Martin M, van Griensven F, Hu D, Tappero JW, and Choopanya K: Randomized, double-blind, placebo-controlled 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.
13. Moore JP, Klasse PJ, Dolan MJ, and Ahuja SK: AIDS/HIV: A STEP into darkness or light? Science 2008;320:753-755.
14. Buchacher A, Predl R, Strutzenberger K, Steinfellner W, Trkola A, Purtscher M, Gruber G, Tauer C, Steindl F, Jungbauer A, et al.: Generation of human monoclonal antibodies against HIV-1 proteins; electrofusion and Epstein-Barr virus transformation for peripheral blood lymphocyte immortalization. AIDS Res Hum Retroviruses 1994;10:359-369. (Pubitemid 24141210)
15. Scanlan CN, Pantophlet R, Wormald MR, Ollmann Saphire E, Stanfield R, Wilson IA, Katinger H, Dwek RA, Rudd PM, and Burton DR: The broadly neutralizing anti-human immunodeficiency virus type 1 antibody 2G12 recognizes a cluster of alpha1 → 2 mannose residues on the outer face of gp120. J Virol 2002;76:7306-7321.
16. Trkola A, Purtscher M, Muster T, Ballaun C, Buchacher A, Sullivan N, Srinivasan K, Sodroski J, Moore JP, and Katinger H: 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)
17. Cardoso RM, Zwick MB, Stanfield RL, Kunert R, Binley JM, Katinger H, Burton DR, and Wilson IA: Broadly neutralizing anti-HIV antibody 4E10 recognizes a helical conformation of a highly conserved fusion-associated motif in gp41. Immunity 2005;22:163-173.
18. Parker CE, Deterding LJ, Hager-Braun C, Binley JM, Schulke N, Katinger H, Moore JP, and Tomer KB: Fine definition of the epitope on the gp41 glycoprotein of human immunodeficiency virus type 1 for the neutralizing monoclonal antibody 2F5. J Virol 2001;75:10906-10911. (Pubitemid 33031557)
19. Cavacini L, Duval M, Song L, Sangster R, Xiang SH, Sodroski J, and Posner M: Conformational changes in env oligomer induced by an antibody dependent on the V3 loop base. AIDS 2003;17:685-689.
20. Gorny MK, Conley AJ, Karwowska S, Buchbinder A, Xu JY, Emini EA, Koenig S, and Zolla-Pazner S: Neutralization of diverse human immunodeficiency virus type 1 variants by an anti-V3 human monoclonal antibody. J Virol 1992;66:7538-7542.
21. Tomaras GD, Yates NL, Liu P, Qin L, Fouda GG, Chavez LL, Decamp AC, Parks RJ, Ashley VC, Lucas JT, Cohen M, Eron J, Hicks CB, Liao HX, Self SG, Landucci G, Forthal DN, Weinhold KJ, Keele BF, Hahn BH, Greenberg ML, Morris L, Karim SS, Blattner WA, Montefiori DC, Shaw GM, Perelson AS, and Haynes BF: Initial B-cell responses to transmitted human immunodeficiency virus type 1: Virion-binding immunoglobulin M (IgM) and IgG antibodies followed by plasma anti-gp41 antibodies with ineffective control of initial viremia. J Virol 2008;82:12449-12463.
22. Moore JP and Jarrett RF: Sensitive ELISA for the gp120 and gp160 surface glycoproteins of HIV-1. AIDS Res Hum Retroviruses 1988;4:369-379.
23. Moore JP and Sodroski J: Antibody cross-competition analysis of the human immunodeficiency virus type 1 gp120 exterior envelope glycoprotein. J Virol 1996;70:1863-1872. (Pubitemid 26062950)
24. Burton DR, Barbas CF, 3rd, Persson MA, Koenig S, Chanock RM, and Lerner RA: A large array of human monoclonal antibodies to type 1 human immunodeficiency virus from combinatorial libraries of asymptomatic seropositive individuals. Proc Natl Acad Sci USA 1991;88:10134-10137.
25. Perneger TV: What's wrong with Bonferroni adjustments. BMJ 1998;316:1236-1238.
26. Binley JM, Klasse PJ, Cao Y, Jones I, Markowitz M, Ho DD, and Moore JP: Differential regulation of the antibody responses to Gag and Env proteins of human immunodeficiency virus type 1. J Virol 1997;71:2799-2809.
27. Groopman JE, Benz PM, Ferriani R, Mayer K, Allan JD, and Weymouth LA: Characterization of serum neutralization response to the human immunodeficiency virus (HIV). AIDS Res Hum Retroviruses 1987;3:71-85.
28. Bailey JR, Lassen KG, Yang HC, Quinn TC, Ray SC, Blankson JN, and Siliciano RF: Neutralizing antibodies do not mediate suppression of human immunodeficiency virus type 1 in elite suppressors or selection of plasma virus variants in patients on highly active antiretroviral therapy. J Virol 2006;80:4758-4770.
29. Cheingsong-Popov R, Panagiotidi C, Bowcock S, Aronstam A, Wadsworth J, and Weber J: Relation between humoral responses to HIV gag and env proteins at seroconversion and clinical outcome of HIV infection. BMJ 1991;302:23-26.
30. Brown AE, Vahey MT, Zhou SY, Chung RC, Ruiz NM, Hofheinz D, Lane JR, and Mayers DL: Quantitative relationship of circulating p24 antigen with human immunodeficiency virus (HIV) RNA and specific antibody in HIV-infected subjects receiving antiretroviral therapy. The RV43 Study Group. J Infect Dis 1995;172:1091-1095.
31. Hogervorst E, Jurriaans S, de Wolf F, van Wijk A, Wiersma A, Valk M, Roos M, van Gemen B, Coutinho R, Miedema F, et al.: Predictors for non- and slow progression in human immunodeficiency virus (HIV) type 1 infection: Low viral RNA copy numbers in serum and maintenance of high HIV-1 p24-specific but not V3-specific antibody levels. J Infect Dis 1995;171:811-821.
32. Chargelegue D, Stanley CM, O'Toole CM, Colvin BT, and Steward MW: 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.
33. Zagury JF, Sill A, Blattner W, Lachgar A, Le Buanec H, Richardson M, Rappaport J, Hendel H, Bizzini B, Gringeri A, Carcagno M, Criscuolo M, Burny A, Gallo RC, and Zagury D: Antibodies to the HIV-1 Tat protein correlated with nonprogression to AIDS: A rationale for the use of Tat toxoid as an HIV-1 vaccine. J Hum Virol 1998;1: 282-292.
34. Zwart G, van der Hoek L, Valk M, Cornelissen MT, Baan E, Dekker J, Koot M, Kuiken CL, and Goudsmit J: Antibody responses to HIV-1 envelope and gag epitopes in HIV-1 seroconverters with rapid versus slow disease progression. Virology 1994;201:285-293.
35. Klasse PJ and Moore JP: Is there enough gp120 in the body fluids of HIV-1-infected individuals to have biologically significant effects? Virology 2004;323:1-8.
36. Lambotte O, Ferrari G, Moog C, Yates NL, Liao HX, Parks RJ, Hicks CB, Owzar K, Tomaras GD, Montefiori DC, Haynes BF, and Delfraissy JF: Heterogeneous neutralizing antibody and antibody-dependent cell cytotoxicity responses in HIV-1 elite controllers. AIDS 2009;23:897-906.
37. Re MC, Furlini G, Vignoli M, Ramazzotti E, Zauli G, and La Placa M: Antibody against human immunodeficiency virus type 1 (HIV-1) Tat protein may have influenced the progression of AIDS in HIV-1-infected hemophiliac patients. Clin Diagn Lab Immunol 1996;3:230-232.
38. Re MC, Vignoli M, Furlini G, Gibellini D, Colangeli V, Vitone F, and La Placa M: Antibodies against full-length Tat protein and some low-molecular-weight Tat-peptides correlate with low or undetectable viral load in HIV-1 seropositive patients. J Clin Virol 2001;21:81-89.
39. Richardson MW, Mirchandani J, Duong J, Grimaldo S, Kocieda V, Hendel H, Khalili K, Zagury JF, Rappaport J: Antibodies to Tat and Vpr in the GRIV cohort: Differential association with maintenance of long-term non-progression status in HIV-1 infection. Biomed Pharmacother 2003;57: 4-14.
40. Senkaali D, Kebba A, Shafer LA, Campbell GR, Loret EP, Van Der Paal L, Grosskurth H, Yirrell D, and Kaleebu P: Tatspecific binding IgG and disease progression in HIV type 1- infected Ugandans. AIDS Res Hum Retroviruses 2008; 24:587-594.
41. Binley JM, Jin X, Huang Y, Zhang L, Cao Y, Ho DD, and Moore JP: Persistent antibody responses but declining cytotoxic T-lymphocyte responses to multiple human immunodeficiency virus type 1 antigens in a long-term nonprogressing individual with a defective p17 proviral sequence and no detectable viral RNA expression. J Virol 1998;72:3472-3474.
42. Butto S, Fiorelli V, Tripiciano A, Ruiz-Alvarez MJ, Scoglio A, Ensoli F, Ciccozzi M, Collacchi B, Sabbatucci M, Cafaro A, Guzman CA, Borsetti A, Caputo A, Vardas E, Colvin M, Lukwiya M, Rezza G, and Ensoli B: Sequence conservation and antibody cross-recognition of clade B human immunodeficiency virus (HIV) type 1 Tat protein in HIV-1-infected Italians, Ugandans, and South Africans. J Infect Dis 2003; 188:1171-1180.
43. Krone WJ, Debouck C, Epstein LG, Heutink P, Meloen R, and Goudsmit J: Natural antibodies to HIV-tat epitopes and expression of HIV-1 genes in vivo. J Med Virol 1988;26: 261-270.
44. Reiss P, de Wolf F, Kuiken CL, de Ronde A, Dekker J, Boucher CA, Debouck C, Lange JM, and Goudsmit J: Contribution of antibody response to recombinant HIV-1 geneencoded products nef, rev, tat, and protease in predicting development of AIDS in HIV-1-infected individuals. J Acquir Immune Defic Syndr 1991;4:165-172.
45. Gorry PR, McPhee DA, Verity E, Dyer WB, Wesselingh SL, Learmont J, Sullivan JS, Roche M, Zaunders JJ, Gabuzda D, Crowe SM, Mills J, Lewin SR, Brew BJ, Cunningham AL, and Churchill MJ: Pathogenicity and immunogenicity of attenuated, nef-deleted HIV-1 strains in vivo. Retrovirology 2007;4:66.
46. Verity EE, Zotos D, Wilson K, Chatfield C, Lawson VA, Dwyer DE, Cunningham A, Learmont J, Dyer W, Sullivan J, Churchill M, Wesselingh SL, Gabuzda D, Gorry PR, and McPhee DA: Viral phenotypes and antibody responses in long-term survivors infected with attenuated human immunodeficiency virus type 1 containing deletions in the nef and long terminal repeat regions. J Virol 2007;81:9268-9278.
47. Ngo-Giang-Huong N, Candotti D, Goubar A, Autran B, Maynart M, Sicard D, Clauvel JP, Agut H, Costagliola D, and Rouzioux C: 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.
48. Martinez V, Costagliola D, Bonduelle O, N'go N, Schnuriger A, Theodorou I, Clauvel JP, Sicard D, Agut H, Debre P, Rouzioux C, and Autran B: 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.
49. Jabara HH, Loh R, Ramesh N, Vercelli D, and Geha RS: Sequential switching from mu to epsilon via gamma 4 in human B cells stimulated with IL-4 and hydrocortisone. J Immunol 1993;151:4528-4533.
50. Punnonen J, Aversa G, Cocks BG, McKenzie AN, Menon S, Zurawski G, de Waal Malefyt R, and de Vries JE: Interleukin 13 induces interleukin 4-independent IgG4 and IgE synthesis and CD23 expression by human B cells. Proc Natl Acad Sci USA 1993;90:3730-3734.
51. Al-Darmaki S, Knightshead K, Ishihara Y, Best A, Schenkein HA, Tew JG, and Barbour SE: Delineation of the role of platelet-activating factor in the immunoglobulin G2 antibody response. Clin Diagn Lab Immunol 2004;11:720-728.
52. Kawano Y, Noma T, and Yata J: Regulation of human IgG subclass production by cytokines. IFN-gamma and IL-6 act antagonistically in the induction of human IgG1 but additively in the induction of IgG2. J Immunol 1994;153: 4948-4958.
53. Kitani A and Strober W: Regulation of C gamma subclass germ-line transcripts in human peripheral blood B cells. J Immunol 1993;151:3478-3488.
54. Kilpinen S, Laine S, Hulkkonen J, and Hurme M: Immunoglobulin G3 and immunoglobulin M isotype plasma levels are influenced by interleukin-1alpha genotype. Scand J Immunol 2003;57:296-302.
55. Kotowicz K and Callard RE: Human immunoglobulin class and IgG subclass regulation: Dual action of interleukin-4. Eur J Immunol 1993;23:2250-2256.
56. Aalberse RC, Stapel SO, Schuurman J, and Rispens T: Immunoglobulin G4: An odd antibody. Clin Exp Allergy 2009; 39:469-477.
57. Connor RI, Korber BT, Graham BS, Hahn BH, Ho DD, Walker BD, Neumann AU, Vermund SH, Mestecky J, Jackson S, Fenamore E, Cao Y, Gao F, Kalams S, Kunstman KJ, McDonald D, McWilliams N, Trkola A, Moore JP, and Wolinsky SM: Immunological and virological analyses of persons infected by human immunodeficiency virus type 1 while participating in trials of recombinant gp120 subunit vaccines. J Virol 1998;72:1552-1576.
58. Gorse GJ, Corey L, Patel GB, Mandava M, Hsieh RH, Matthews TJ, Walker MC, McElrath MJ, Berman PW, Eibl MM, and Belshe RB: HIV-1MN recombinant glycoprotein 160 vaccine-induced cellular and humoral immunity boosted by HIV-1MN recombinant glycoprotein 120 vaccine. National Institute of Allergy and Infectious Diseases AIDS Vaccine Evaluation Group. AIDS Res Hum Retroviruses 1999;15: 115-132.
59. Gilbert PB, Peterson ML, Follmann D, Hudgens MG, Francis DP, Gurwith M, Heyward WL, Jobes DV, Popovic V, Self SG, Sinangil F, Burke D, and Berman PW: Correlation between immunologic responses to a recombinant glycoprotein 120 vaccine and incidence of HIV-1 infection in a phase 3 HIV-1 preventive vaccine trial. J Infect Dis 2005;191:666-677. (Pubitemid 40271053)
60. Binley JM, Lybarger EA, Crooks ET, Seaman MS, Gray E, Davis KL, Decker JM, Wycuff D, Harris L, Hawkins N, Wood B, Nathe C, Richman D, Tomaras GD, Bibollet-Ruche F, Robinson JE, Morris L, Shaw GM, Montefiori DC, and Mascola JR: 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.
61. Klasse J and Blomberg J: Patterns of antibodies to human immunodeficiency virus proteins in different subclasses of IgG. J Infect Dis 1987;156:1026-1030.
62. Raux M, Finkielsztejn L, Salmon-Ceron D, Bouchez H, Excler JL, Dulioust E, Grouin JM, Sicard D, and Blondeau C: IgG subclass distribution in serum and various mucosal fluids of HIV type 1-infected subjects. AIDS Res Hum Retroviruses 2000;16:583-594.
63. Daly LM, Johnson PA, Donnelly G, Nicolson C, Robertson J, and Mills KH: Innate IL-10 promotes the induction of Th2 responses with plasmid DNA expressing HIV gp120. Vaccine 2005;23:963-974.
64. Banerjee K, Andjelic S, Klasse PJ, Kang Y, Sanders RW, Michael E, Durso RJ, Ketas TJ, Olson WC, and Moore JP: Enzymatic removal of mannose moieties can increase the immune response to HIV-1 gp120 in vivo. Virology 2009; 389:108-121.
65. Shan M, Klasse PJ, Banerjee K, Dey AK, Iyer SP, Dionisio R, Charles D, Campbell-Gardener L, Olson WC, Sanders RW, and Moore JP: HIV-1 gp120 mannoses induce immunosuppressive responses from dendritic cells. PLoS Pathog 2007; 3:e169.
66. Klasse PJ, Berntorp E, and Hansson BG: An aberrant subclass pattern of HIV-specific immunoglobulin G in sera from haemophiliacs. AIDS 1988;2:311-313.
67. Khalife J, Guy B, Capron M, Kieny MP, Ameisen JC, Montagnier L, Lecocq JP, and Capron A: Isotypic restriction of the antibody response to human immunodeficiency virus. AIDS Res Hum Retroviruses 1988;4:3-9.
68. Jankovic D, Caspar P, Zweig M, Garcia-Moll M, Showalter SD, Vogel FR, and Sher A: Adsorption to aluminum hydroxide promotes the activity of IL-12 as an adjuvant for antibody as well as type 1 cytokine responses to HIV-1 gp120. J Immunol 1997;159:2409-2417.
69. Geeraedts F, Goutagny N, Hornung V, Severa M, de Haan A, Pool J, Wilschut J, Fitzgerald KA, and Huckriede A: Superior immunogenicity of inactivated whole virus H5N1 influenza vaccine is primarily controlled by Toll-like receptor signalling. PLoS Pathog 2008;4:e1000138.
70. Xu W, Santini PA, Sullivan JS, He B, Shan M, Ball SC, Dyer WB, Ketas TJ, Chadburn A, Cohen-Gould L, Knowles DM, Chiu A, Sanders RW, Chen K, and Cerutti A: HIV-1 evades virus-specific IgG2 and IgA responses by targeting systemic and intestinal B cells via long-range intercellular conduits. Nat Immunol 2009;10:1008-1017.
71. Mestecky J, Jackson S, Moldoveanu Z, Nesbit LR, Kulhavy R, Prince SJ, Sabbaj S, Mulligan MJ, and Goepfert PA: Paucity of antigen-specific IgA responses in sera and external secretions of HIV-type 1-infected individuals. AIDS Res Hum Retroviruses 2004;20:972-988.