HIV-1 specific IgA detected in vaginal secretions of HIV uninfected women participating in a microbicide trial in Southern Africa are primarily directed toward gp120 and gp140 specificities

PLoS ONE

Volumn 9, Issue 7, 2014, Pages

  Seaton, Kelly E ^a   Ballweber, Lamar ^b   Lan, Audrey ^a   Donathan, Michele ^a   Hughes, Sean ^b   Vojtech, Lucia ^b   Moody, M Anthony ^a   Liao, Hua Xin ^a   Haynes, Barton F ^a   Galloway, Christine G ^c   Richardson, Barbra A ^c,d   Karim, Salim Abdool ^e,f   Dezzutti, Charlene S ^g   McElrath, M Juliana ^c,d   Tomaras, Georgia D ^a   Hladik, Florian ^b,c,d  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^c Fred Hutchinson Cancer Research Center   (United States)

^d UNIVERSITY OF WASHINGTON   (United States)

^e UNIVERSITY OF KWAZULU NATAL   (South Africa)

^f Och Spine at New York Presbyterian Hospitals   (United States)

^g UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN GP 120; GLYCOPROTEIN GP 140; GLYCOPROTEIN GP 41; IMMUNOGLOBULIN A ANTIBODY; IMMUNOGLOBULIN G ANTIBODY; POLYESTER; ANTIINFECTIVE AGENT; GP140 ENVELOPE PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; VIRUS ENVELOPE PROTEIN;

AFRICAN; ANTIBODY DETECTION; ANTIBODY RESPONSE; ANTIBODY SPECIFICITY; ANTIBODY TITER; ANTIGEN ANTIBODY REACTION; ARTICLE; COHORT ANALYSIS; COMPARATIVE STUDY; CONTROLLED STUDY; ETHNIC GROUP; FEMALE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOGLOBULIN BLOOD LEVEL; MAJOR CLINICAL STUDY; PILOT STUDY; SAMPLER; SOUTH AFRICA; VAGINAL SECRETION; VAGINITIS; ANALYSIS OF VARIANCE; BODILY SECRETIONS; DEVICES; DRUG EFFECTS; HIV INFECTIONS; IMMUNOLOGY; LABORATORY DIAGNOSIS; MUCOSAL IMMUNITY; PROCEDURES; SERODIAGNOSIS; VAGINA; VIROLOGY;

ANALYSIS OF VARIANCE; ANTI-INFECTIVE AGENTS; BODILY SECRETIONS; COHORT STUDIES; ENV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; FEMALE; HIV ANTIBODIES; HIV ENVELOPE PROTEIN GP120; HIV INFECTIONS; HIV SERONEGATIVITY; HIV SEROPOSITIVITY; HIV-1; HUMANS; IMMUNITY, MUCOSAL; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; PILOT PROJECTS; SOUTH AFRICA; SPECIMEN HANDLING; VAGINA;

EID: 84904688744     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0101863     Document Type: Article

References (65)

1. Hladik F, McElrath MJ (2008) Setting the stage: host invasion by HIV. Nat Rev Immunol 8: 447-457. (Pubitemid 351735878)
2. Royce RA, Sena A, Cates W Jr, Cohen MS (1997) Sexual transmission of HIV. N Engl J Med 336: 1072-1078. (Pubitemid 27163861)
3. Shacklett BL (2006) Understanding the "lucky few": the conundrum of HIV-exposed, seronegative individuals. Curr HIV/AIDS Rep 3: 26-31.
4. Alimonti JB, Kimani J, Matu L, Wachihi C, Kaul R, et al. (2006) Characterization of CD8 T-cell responses in HIV-1-exposed seronegative commercial sex workers from Nairobi, Kenya. Immunol Cell Biol 84: 482-485. (Pubitemid 44286043)
5. Hladik F, Desbien A, Lang J, Wang L, Ding Y, et al. (2003) Most highly exposed seronegative men lack HIV-1-specific, IFN-gamma-secreting T cells. J Immunol 171: 2671-2683. (Pubitemid 37025581)
6. Mazzoli S, Trabattoni D, Lo Caputo S, Piconi S, Ble C, et al. (1997) HIV-specific mucosal and cellular immunity in HIV-seronegative partners of HIV-seropositive individuals. Nat Med 3: 1250-1257. (Pubitemid 27508826)
7. Bernard NF, Yannakis CM, Lee JS, Tsoukas CM (1999) Human immunodeficiency virus (HIV)-specific cytotoxic T lymphocyte activity in HIV-exposed seronegative persons. J Infect Dis 179: 538-547. (Pubitemid 30016136)
8. Rowland-Jones S, Sutton J, Ariyoshi K, Dong T, Gotch F, et al. (1995) HIV-specific cytotoxic T-cells in HIV-exposed but uninfected Gambian women. Nat Med 1: 59-64.
9. Rowland-Jones SL, Dong T, Fowke KR, Kimani J, Krausa P, et al. (1998) Cytotoxic T cell responses to multiple conserved HIV epitopes in HIV- resistant prostitutes in Nairobi. J Clin Invest 102: 1758-1765. (Pubitemid 28516261)
10. Erickson AL, Willberg CB, McMahan V, Liu A, Buchbinder SP, et al. (2008) Potentially exposed but uninfected individuals produce cytotoxic and polyfunctional human immunodeficiency virus type 1-specific CD8(+) T-cell responses which can be defined to the epitope level. Clin Vaccine Immunol 15: 1745-1748.
11. Lo Caputo S, Trabattoni D, Vichi F, Piconi S, Lopalco L, et al. (2003) Mucosal and systemic HIV-1-specific immunity in HIV-1-exposed but uninfected heterosexual men. AIDS 17: 531-539. (Pubitemid 36293106)
12. Pinto LA, Sullivan J, Berzofsky JA, Clerici M, Kessler HA, et al. (1995) ENV-specific cytotoxic T lymphocyte responses in HIV seronegative health care workers occupationally exposed to HIV-contaminated body fluids. J Clin Invest 96: 867-876.
13. Kaul R, Plummer FA, Kimani J, Dong T, Kiama P, et al. (2000) HIV-1-specific mucosal CD8+ lymphocyte responses in the cervix of HIV-1- resistant prostitutes in Nairobi. J Immunol 164: 1602-1611. (Pubitemid 30067280)
14. Choi RY, Levinson P, Guthrie BL, Payne B, Bosire R, et al. (2012) Cervicovaginal HIV-1-neutralizing IgA detected among HIV-1-exposed seronegative female partners in HIV-1-discordant Kenyan couples. AIDS.
15. Belec L, Ghys PD, Hocini H, Nkengasong JN, Tranchot-Diallo J, et al. (2001) Cervicovaginal secretory antibodies to human immunodeficiency virus type 1 (HIV-1) that block viral transcytosis through tight epithelial barriers in highly exposed HIV-1-seronegative African women. J Infect Dis 184: 1412-1422. (Pubitemid 33108855)
16. Kaul R, Plummer F, Clerici M, Bomsel M, Lopalco L, et al. (2001) Mucosal IgA in exposed, uninfected subjects: evidence for a role in protection against HIV infection. Aids 15: 431-432. (Pubitemid 32163839)
17. Devito C, Hinkula J, Kaul R, Lopalco L, Bwayo JJ, et al. (2000) Mucosal and plasma IgA from HIV-exposed seronegative individuals neutralize a primary HIV-1 isolate. Aids 14: 1917-1920.
18. Kaul R, Rowland-Jones SL, Kimani J, Dong T, Yang HB, et al. (2001) Late seroconversion in HIV-resistant Nairobi prostitutes despite pre- existing HIV-specific CD8+ responses. J Clin Invest 107: 341-349. (Pubitemid 32157966)
19. Dezzutti CS, Hendrix CW, Marrazzo JM, Pan Z, Wang L, et al. (2011) Performance of swabs, lavage, and diluents to quantify biomarkers of female genital tract soluble mucosal mediators. PLoS One 6: e23136.
20. Belec L, Meillet D, Levy M, Georges A, Tevi-Benissan C, et al. (1995) Dilution assessment of cervicovaginal secretions obtained by vaginal washing for immunological assays. Clin Diagn Lab Immunol 2: 57-61.
21. Mitchell C, Paul K, Agnew K, Gaussman R, Coombs RW, et al. (2011) Estimating volume of cervicovaginal secretions in cervicovaginal lavage fluid collected for measurement of genital HIV-1 RNA levels in women. J Clin Microbiol 49: 735-736.
22. Tomaras GD, Binley JM, Gray ES, Crooks ET, Osawa K, et al. (2011) Polyclonal B cell responses to conserved neutralization epitopes in a subset of HIV-1-infected individuals. J Virol 85: 11502-11519.
23. Tomaras GD, Yates NL, Liu P, Qin L, Fouda GG, et al. (2008) 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 82: 12449-12463.
24. Yates NL, Lucas JT, Nolen TL, Vandergrift NA, Soderberg KA, et al. (2011) Multiple HIV-1-specific IgG3 responses decline during acute HIV-1: implications for detection of incident HIV infection. AIDS 25: 2089-2097.
25. Yates NL, Stacey AR, Nolen TL, Vandergrift NA, Moody MA, et al. (2013) HIV-1 gp41 envelope IgA is frequently elicited after transmission but has an initial short response half-life. Mucosal Immunol 6: 692-703.
26. Abdool Karim SS, Richardson BA, Ramjee G, Hoffman IF, Chirenje ZM, et al. (2011) Safety and effectiveness of BufferGel and 0.5% PRO2000 gel for the prevention of HIV infection in women. AIDS 25: 957-966.
27. Dezzutti CS, Richardson BA, Marrazzo JM, Tugetman J, Ramjee G, et al. (2012) Mucosal Escherichia coli bactericidal activity and immune mediators are associated with HIV-1 seroconversion in women participating in the HPTN 035 trial. J Infect Dis 206: 1931-1935.
28. Fouda GG, Yates NL, Pollara J, Shen X, Overman GR, et al. (2011) HIV-specific functional antibody responses in breast milk mirror those in plasma and are primarily mediated by IgG antibodies. J Virol 85: 9555-9567.
29. Liu P, Overman RG, Yates NL, Alam SM, Vandergrift N, et al. (2011) Dynamic antibody specificities and virion concentrations in circulating immune complexes in acute to chronic HIV-1 infection. J Virol 85: 11196-11207.
30. Liu P, Yates NL, Shen X, Bonsignori M, Moody MA, et al. (2013) Infectious Virion Capture by HIV-1 gp120-Specific IgG from RV144 Vaccinees. J Virol 87: 7828-7836.
31. Morris L, Chen X, Alam M, Tomaras G, Zhang R, et al. (2011) Isolation of a human anti-HIV gp41 membrane proximal region neutralizing antibody by antigen-specific single B cell sorting. PLoS One 6: e23532.
32. Alam SM, Scearce RM, Parks RJ, Plonk K, Plonk SG, et al. (2008) Human immunodeficiency virus type 1 gp41 antibodies that mask membrane proximal region epitopes: antibody binding kinetics, induction, and potential for regulation in acute infection. J Virol 82: 115-125. (Pubitemid 350309129)
33. Liao HX, Tsao CY, Alam SM, Muldoon M, Vandergrift N, et al. (2013) Antigenicity and immunogenicity of transmitted/founder, consensus, and chronic envelope glycoproteins of human immunodeficiency virus type 1. J Virol 87: 4185-4201.
34. Gaschen B, Taylor J, Yusim K, Foley B, Gao F, et al. (2002) Diversity considerations in HIV-1 vaccine selection. Science 296: 2354-2360. (Pubitemid 34734202)
35. Liao HX, Sutherland LL, Xia SM, Brock ME, Scearce RM, et al. (2006) A group M consensus envelope glycoprotein induces antibodies that neutralize subsets of subtype B and C HIV-1 primary viruses. Virology 353: 268-282. (Pubitemid 44404137)
36. Gao F, Weaver EA, Lu Z, Li Y, Liao HX, et al. (2005) Antigenicity and immunogenicity of a synthetic human immunodeficiency virus type 1 group m consensus envelope glycoprotein. J Virol 79: 1154-1163. (Pubitemid 40053898)
37. UNAIDS report on the global AIDS epidemic (2013). Geneva: UNAIDS/WHO.
38. Global AIDS Response Progress Report (2012). Republic of South Africa.
39. Devito C, Broliden K, Kaul R, Svensson L, Johansen K, et al. (2000) Mucosal and plasma IgA from HIV-1-exposed uninfected individuals inhibit HIV-1 transcytosis across human epithelial cells. J Immunol 165: 5170-5176.
40. Tudor D, Derrien M, Diomede L, Drillet AS, Houimel M, et al. (2009) HIV-1 gp41-specific monoclonal mucosal IgAs derived from highly exposed but IgG-seronegative individuals block HIV-1 epithelial transcytosis and neutralize CD4(+) cell infection: an IgA gene and functional analysis. Mucosal Immunol 2: 412-426.
41. Beyrer C, Artenstein AW, Rugpao S, Stephens H, VanCott TC, et al. (1999) Epidemiologic and biologic characterization of a cohort of human immunodeficiency virus type 1 highly exposed, persistently seronegative female sex workers in northern Thailand. Chiang Mai HEPS Working Group. J Infect Dis 179: 59-67. (Pubitemid 29028339)
42. Kaul R, Trabattoni D, Bwayo JJ, Arienti D, Zagliani A, et al. (1999) HIV-1-specific mucosal IgA in a cohort of HIV-1-resistant Kenyan sex workers. AIDS 13: 23-29. (Pubitemid 29078060)
43. Dorrell L, Hessell AJ, Wang M, Whittle H, Sabally S, et al. (2000) Absence of specific mucosal antibody responses in HIV-exposed uninfected sex workers from the Gambia. AIDS 14: 1117-1122. (Pubitemid 30420654)
44. Young JM, Turpin JA, Musib R, Sharma OK (2011) Outcomes of a National Institute of Allergy and Infectious Diseases Workshop on understanding HIV-exposed but seronegative individuals. AIDS Res Hum Retroviruses 27: 737-743.
45. Mazzoli S, Trabattoni D, Lo Caputo S, Piconi S, Ble C, et al. (1997) HIV-specific mucosal and cellular immunity in HIV-seronegative partners of HIV-seropositive individuals. Nat Med 3: 1250-1257. (Pubitemid 27508826)
46. Franklin RD, Kutteh WH (1999) Characterization of immunoglobulins and cytokines in human cervical mucus: influence of exogenous and endogenous hormones. J Reprod Immunol 42: 93-106. (Pubitemid 29148262)
47. Kutteh WH, Moldoveanu Z, Mestecky J (1998) Mucosal immunity in the female reproductive tract: correlation of immunoglobulins, cytokines, and reproductive hormones in human cervical mucus around the time of ovulation. AIDS Res Hum Retroviruses 14 Suppl 1: S51-55. (Pubitemid 28208889)
48. Mackelprang RD, Baeten JM, Donnell D, Celum C, Farquhar C, et al. (2012) Quantifying Ongoing HIV-1 Exposure in HIV-1-Serodiscordant Couples to Identify Individuals With Potential Host Resistance to HIV-1. J Infect Dis.
49. Cranage M, Sharpe S, Herrera C, Cope A, Dennis M, et al. (2008) Prevention of SIV rectal transmission and priming of T cell responses in macaques after local pre-exposure application of tenofovir gel. PLoS Med 5: e157; discussion e157.
50. Mestecky J, Wright PF, Lopalco L, Staats HF, Kozlowski PA, et al. (2011) Scarcity or absence of humoral immune responses in the plasma and cervicovaginal lavage fluids of heavily HIV-1-exposed but persistently seronegative women. AIDS Res Hum Retroviruses 27: 469-486.
51. Mestecky J, Jackson S, Moldoveanu Z, Nesbit LR, Kulhavy R, et al. (2004) Paucity of antigen-specific IgA responses in sera and external secretions of HIV-type 1-infected individuals. AIDS Res Hum Retroviruses 20: 972-988. (Pubitemid 39369704)
52. Donadoni C, Bisighini C, Scotti L, Diomede L, Ngyen M, et al. (2010) Setting of methods for analysis of mucosal antibodies in seminal and vaginal fluids of HIV seropositive subjects from Cambodian and Italian cohorts. PLoS One 5: e9920.
53. Liu P, Williams LD, Shen X, Bonsignori M, Vandergrift NA, et al. (2014) Capacity for infectious HIV-1 virion capture differs by envelope antibody specificity. J Virol 88: 5165-5170.
54. Jain S, Rosenthal KL (2011) The gp41 epitope, QARVLAVERY, is highly conserved and a potent inducer of IgA that neutralizes HIV-1 and inhibits viral transcytosis. Mucosal Immunol 4: 539-553.
55. Shen R, Drelichman ER, Bimczok D, Ochsenbauer C, Kappes JC, et al. (2010) GP41-specific antibody blocks cell-free HIV type 1 transcytosis through human rectal mucosa and model colonic epithelium. J Immunol 184: 3648-3655.
56. Moog C, Dereuddre-Bosquet N, Teillaud JL, Biedma ME, Holl V, et al. (2014) Protective effect of vaginal application of neutralizing and nonneutralizing inhibitory antibodies against vaginal SHIV challenge in macaques. Mucosal Immunol 7: 46-56.
57. Burton DR, Hessell AJ, Keele BF, Klasse PJ, Ketas TA, et al. (2011) 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 108: 11181-11186.
58. Shukair SA, Allen SA, Cianci GC, Stieh DJ, Anderson MR, et al. (2013) Human cervicovaginal mucus contains an activity that hinders HIV-1 movement. Mucosal Immunol 6: 427-434.
59. Watkins JD, Sholukh AM, Mukhtar MM, Siddappa NB, Lakhashe SK, et al. (2013) Anti-HIV IgA isotypes: differential virion capture and inhibition of transcytosis are linked to prevention of mucosal R5 SHIV transmission. AIDS 27: F13-20.
60. Buchbinder SP, Mehrotra DV, Duerr A, Fitzgerald DW, Mogg R, et al. (2008) Efficacy assessment of a cell-mediated immunity HIV-1 vaccine (the Step Study): a double-blind, randomised, placebo-controlled, test-of-concept trial. Lancet 372: 1881-1893.
61. McElrath MJ, De Rosa SC, Moodie Z, Dubey S, Kierstead L, et al. (2008) HIV-1 vaccine-induced immunity in the test-of-concept Step Study: a case-cohort analysis. Lancet 372: 1894-1905.
62. Cohen J (2013) AIDS RESEARCH More Woes for Struggling HIV Vaccine Field. Science 340: 667-667.
63. Hammer SM, Sobieszczyk ME, Janes H, Karuna ST, Mulligan MJ, et al. (2013) Efficacy trial of a DNA/rAd5 HIV-1 preventive vaccine. N Engl J Med 369: 2083-2092.
64. Rerks-Ngarm S, Pitisuttithum P, Nitayaphan S, Kaewkungwal J, Chiu J, et al. (2009) Vaccination with ALVAC and AIDSVAX to prevent HIV-1 infection in Thailand. N Engl J Med 361: 2209-2220.
65. Haynes BF, Gilbert PB, McElrath MJ, Zolla-Pazner S, Tomaras GD, et al. (2012) Immune-correlates analysis of an HIV-1 vaccine efficacy trial. N Engl J Med 366: 1275-1286.