Abstract
The protective function of mucosal HIV-1- or SIV-specific antibodies against viral infection has stimulated extensive studies of their Ig isotype association with differences in specificity and in effector functions. In contrast to many mucosally acquired microbial infections in which the humoral responses are dominated by induction of secretory IgA (S-IgA), HIV-1/SIV infections stimulate vigorous IgG responses in sera as well as in external secretions but low IgA virus-specific antibodies although the total levels of IgA in these fluids remain unaltered. The diminished or even absent IgA responses to HIV-1/SIV and to other mucosal antigens in external secretions and their replacement with IgG is likely to influence the functionality of mucosal barriers and eliminate antiinflammatory effector functions of IgA antibodies. Furthermore, the polymeric character of S-IgA with 4-8 antigen-binding sites, exquisite resistance to proteolysis and anti-inflammatory potential are of great advantage in mucosal protection. The markedly different effector functions of mucosal antibodies of IgG and IgA isotypes must be considered in the design of HIV-1 vaccines to stimulate S-IgA responses at sites of virus entry and IgG responses in the systemic compartment.
Keywords: HIV-1, SIV, IgG, IgA, Secretory IgA, Genital tract, Intestinal tract.
[1]
Artenstein A, VanCott TC, Sitz KV, et al. Mucosal immune responses in four distinct compartments of women infected with human immunodeficiency virus type 1: A comparison by site and correlation with clinical information. J Infect Dis 1997; 175: 265-71.
[2]
Brenchley JM, Douek DC. The mucosal barrier and immune activation in HIV-1 pathogenesis. Curr Opin HIV-1 AIDS 2008; 3:
356-61..
[3]
Haase AT. Perils at mucosal front lines for HIV-1 and SIV and their hosts. Nat Rev Immunol 2005; 5: 783-92.
[4]
Mestecky J, Moldoveanu Z, Russell MW. Immunological uniqueness of the genital tract: Challenge for vaccine development. Am J Reprod Immunol 2005; 53: 208-14.
[5]
Mestecky J, Raska M, Novak J, Alexander RC, Moldoveanu Z. Antibody-mediated protection and the mucosal immune system of the genital tract: Relevance to vaccine design. J Reprod Immunol 2010; 85: 81-5.
[6]
Wira CR, Fahey JV. A new strategy to understand how HIV-1 infects women: Identification of a window of vulnerability during the menstrual cycle. AIDS 2008; 22: 1909-17.
[7]
Veazey RS, Marx PA, Lackner AA. The mucosal immune system: primary target for HIV-1 infection and AIDS. Trends Immunol 2001; 22: 626-33.
[8]
Baba TW, Liska V, Hofmann-Lehmann R, et al. Human neutralizing monoclonal antibodies of the IgG1 subtype protect against mucosal simian-human immunodeficiency virus infection. Nat Med 2000; 6: 200-6.
[9]
Fouda GG, Eudailey J, Kunz EL, et al. Systemic administration of an HIV-1 broadly neutralizing dimeric IgA yields mucosal secretory IgA and virus neutralization. Mucosal Immunol 2017; 10: 228-37.
[10]
Hessell AJ. Rakasz Eg, Tehrani DM, et al. Broadly neutralizing monoclonal antibodies 2F5 and 4E10 directed against the human immunodeficiency virus type 1 gp41 membrane-proximal external region protect against mucosal challenge by simian-human immunodeficiency virus SHIV-1Ba-L. J Virol 2010; 84: 1302-13.
[11]
Li Q, Zeng M, Duan L, et al. Live simian immunodeficiency virus vaccine correlate of protection: local antibody production and concentration on the path of virus entry. J Immunol 2014; 193: 3113-25.
[12]
Mantis NJ, Palaia J, Hessell AJ, et al. Inhibition of HIV-1infectivity and epithelial cell transfer by human monoclonal IgG and IgA antibodies carrying the b12 V region. J Immunol 2007; 179: 3144-52.
[13]
Mascola JR, Stiegler G, VanCott TC, et al. Protection of macaques against vaginal transmission of a pathogenic HIV-1/SIV chimeric virus by passive infusion of neutralizing antibodies. Nat Med 2000; 6: 207-10.
[14]
Mascola JR. Passive transfer studies to elucidate the role of antibody-mediated protection against HIV-1. Vaccine 2002; 20: 1922-5.
[15]
Moldt B, Rakasz EG, Schultz N, et al. Highly potent HIV-1-specific antibody neutralization in vitro translates into effective protection against mucosal SHIV-1 challenge in vivo. Proc Natl Acad Sci USA 2012; 109: 18921-5.
[16]
Moog C, Dereuddre-Bosquet N, Teillaud JL, et al. Protective effect of vaginal application of neutralizing and nonneutralizing inhibitory antibodies against vaginal SHIV-1 challenge in macaques. Mucosal Immunol 2014; 7: 46-56.
[17]
Overbaugh J, Morris L. The antibody response against HIV-1. Cold Spring Harb Perspect Med 2012; 2(1): 0007039.
[18]
Sholukh AM, Watkins JD, Hemant KV, et al. Defense-in-depth by mucosally administered anti- HIV-1 dimeric IgA2 and systemic IgG1 mAbs: Complete protection of rhesus monkeys from mucosal SHIV-1 challenge. Vaccine 2015; 33: 2086-95.
[19]
Veazey RS, Shattock RJ, Pope M, et al. Prevention of virus transmission to macaque monkeys by a vaginally applied monoclonal antibody to HIV-1 gp120. Nat Med 2003; 9: 343-6.
[20]
Watkins JD, Sholukh AM, Mukhtar MM, et al. Anti-HIV-1 IgA isotypes: Differential virion capture and inhibition of transcytosis are linked to prevention of mucosal R5 SHIV-1 transmission. AIDS 2013; 27: F13-20.
[21]
Jackson S, Moldoveanu Z, Mestecky J. Appendix I: Collection and
processing of human mucosal secretions. In: Mucosal Immunology,
4th Edition (Eds. J. Mestecky, W. Strober, M.W., Russell, B. L.
Kelsall, H. Cheroute, B. N. Lambrecht) pp.2345-54;
Elsevier/Academic Press, Amsterdam (2015)..
[22]
Boskey ER, Moench TR, Hees PS, Cone RA. A self-sampling method to obtain large volumes of undiluted cervicovaginal secretions. Sex Transm Dis 2003; 30: 107-9.
[23]
Archary D, Seaton KE, Passmore JS, et al. Distinct genital tract HIV-specific antibody profiles associated with tenofovir gel. Mucosal Immunol 2016; 9: 821-33.
[24]
Kutteh WH, Prince SJ, Hammond KR, Kutteh CC, Mestecky J. Variations in immunoglobulins and IgA subclasses of human uterine cervical secretions around the time of ovulation. Clin Exp Immunol 1996; 104: 538-42.
[25]
Kutteh WH, Moldoveanu Z, Mestecky J. 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 1998; 14: S51-.
[26]
Moldoveanu Z, Mestecky J. Mucosal antibody responses to HIV-1. Methods Mol Biol 2009; 485: 333-45.
[27]
Moldoveanu Z, Huang W-Q, Kulhavy R, Pate MS, Mestecky J. Human male genital tract secretions: Both mucosal and systemic immune compartments contribute to the humoral immunity. J Immunol 2005; 175: 4127-36.
[28]
Raux M, Finkielsztejn L, Salmon-Ceron D, et al. Comparison of the distribution of IgG and IgA antibodies in serum and various mucosal fluids of HIV type 1-infected subjects. AIDS Res Hum Retroviruses 1999; 15: 1365-76.
[29]
Raux M, Finkielsztejn L, Salmon-Ceron D, et al. IgG subclass distribution in serum and various mucosal fluids of HIV type 1-infected subjects. AIDS Res Hum Retroviruses 2000; 16: 583-94.
[30]
Donadoni C, Bisighini C, Scotti L, et al. Setting of methods for analysis of mucosal antibodies in seminal and vaginal fluids of HIV seropositive subjects from Cambodian and Italian cohorts. PLoS One 2010; 5(3): e9920.
[31]
McNeely TB, Dealy M, Dripps DJ, Orenstein JM, Eisenberg SP, Wahl SM. Secretory leukocyte protease inhibitor: A human saliva protein exhibiting anti-human immunodeficiency virus 1 activity in vivo. J Clin Invest 1995; 96: 456-64.
[32]
Orsi N. The antimicrobial activity of lactoferrin: Current status and perspectives. Biometals 2004; 17: 189-96.
[33]
Harmsen MC, Swart PJ, de Bethune MP, et al. Antiviral effects of plasma and milk proteins: Lactoferrin shows potent activity against both human immunodeficiency virus and human cytomegalovirus replication in vitro. J Infect Dis 1995; 172: 380-8.
[34]
Kazmi SH, Naglik JR, Sweet SP, et al. Comparison of human immunodeficiency virus type 1-specific inhibitory activities in saliva and other human mucosal fluids. Clin Vaccine Immunol 2006; 13: 1111-8.
[35]
Lee-Huang S, Huang PL, Sun Y, et al. Lysozyme and RNases as anti-HIV components in beta-core preparations of human chorionic gonadotropin. Proc Natl Acad Sci USA 1999; 96: 2678-81.
[36]
Nagashunmugam T, Malamud D, Davis C, Abrams WR, Friedman HM. Human submandibular saliva inhibits human immunodeficiency virus type 1 infection by displacing envelope glycoprotein gp120 from the virus. J Infect Dis 1998; 178: 1635-41.
[37]
Veazey RS, Pilch-Cooper HA, Hope TJ, et al. Prevention of SHIV-1 transmission by topical IFN-β treatment. Mucosal Immunol 2016; 9: 1528-36.
[38]
Wahl SM, McNeely TB, Janoff EN, et al. Secretory Leukocyte Protease Inhibitor (SLPI) in mucosal fluids inhibits HIV-1. Oral Dis 1997; 3: 64-9.
[39]
Jackson S, Prince S, Kulhavy R, Mestecky J. False positivity of enzyme-linked immunosorbent assay for measurement of secretory IgA antibodies directed at HIV-1 antigens. AIDS Res Hum Retroviruses 2000; 16: 595-602.
[40]
Mestecky J, Wright PF, Lopalco L, et al. Sparcity 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 2011; 27: 469-86.
[41]
Santra S, Tomaras GD, Warrier R, et al. Human non-neutralizing HIV-1 envelope monoclonal antibodies limit the number of founder viruses during SHIV mucosal infection in Rhesus Macaques. PLoS Pathog 2015; 11(8): e1005042.
[42]
Moir S, Fauci AS. Pathogenic mechanisms of B-lymphocyte dysfunction in HIV disease. J Allergy Clin Immunol 2008; 122: 12-9.
[43]
Wright PF, Kozlowski PA, Rybczyk GK, et al. Detection of mucosal antibodies in HIV-1 type 1-infected individuals. AIDS Res Hum Retroviruses 2002; 18: 1291-300.
[44]
Mestecky J, Jackson S, Moldoveanu Z, et al. Paucity of antigen-specific IgA responses in sera and external secretions of HIV-1-infected individuals. AIDS Res Hum Retroviruses 2004; 20: 972-88.
[45]
Mestecky J, Wei Q, Alexander R, Raska M, Novak J, Moldoveanu Z. Humoral immune responses to HIV-1 in the mucosal secretions and sera of HIV-1-infected women. Am J Reprod Immunol 2014; 71: 600-7.
[46]
Mestecky J. Humoral immune responses to the Human Immunodeficiency Virus Type-1 (HIV-1) in the genital tract as compared to other mucosal sites. J Reprod Immunol 2007; 73: 86-97.
[47]
Veazey RS, DeMaria M, Chalifoux LV, et al. Gastrointestinal tract as a major site of CD4+ T cell depletion and viral replication in SIV infection. Science 1998; 280: 427-31.
[48]
Brenchley JM, Schacker TW, Ruff LE, et al. CD4+ T cells depletion during all stages of HIV-1 disease occurs predominantly in the gastrointestinal tract. J Exp Med 2004; 200: 749-59.
[50]
Fagarasan S, Kawamoto S, Kanagawa O, Suzuki K. Adaptive immune regulation in the gut: T cell-dependent and T cell-independent IgA synthesis. Annu Rev Immunol 2010; 28: 243-73.
[51]
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: 3931-41.
[52]
He B, Xu W, Santini PA, et al. Intestinal bacteria trigger T cell-independent immunoglobulin A2 class switching by inducing epithelial-cell secretion of the cytokine APRIL. Immunity 2007; 26: 812-26.
[53]
McGhee JR, Mestecky J, Elson CO, Kiyono H. Regulation of IgA synthesis and immune responses by T cells and interleukins. J Clin Immunol 1989; 9: 175-99.
[54]
Schultheiss T, Schulte R, Sauermann U, Ibing W, Stahl-Henning C. Strong mucosal immune responses in SIV infected macaques contribute to viral control and preserved CD4+ T-cell levels in blood and mucosal tissues. Retrovirology 2011; 8: 24.
[55]
Landsverk OJB, Snir O, Bartolome R, et al. Antibody-secreting plasma cells persist for decades in human intestine. J Exp Med 2017; 214: 309-17.
[57]
Woof JM, Mestecky J. Mucosal Immunoglobulins. In: Mucosal
Immunology, 4th Edition (Eds. J. Mestecky, W. Strober, M.W.,
Russell, B. L. Kelsall, H. Cheroute, B. N. Lambrecht), Chapter 17,
pp. 287-324; Elsevier/Academic Press, Amsterdam (2015).
[58]
Pakkanen SH, Kantele JM, Moldoveanu Z, et al. Expression of homing receptors on IgA1 and IgA2 plasmablasts in blood reflects differential distribution of IgA1 and IgA2 in various body fluids. Clin Vaccine Immunol 2010; 17: 393-401.
[59]
Baker K, Blumberg RS, Kaetzel CS. Immunoglobulin transport and immunoglobulin receptors. In: Mucosal Immunology, 4th Edition
(Eds. J. Mestecky, W. Strober, M.W., Russell, B. L. Kelsall, H.
Cheroute, B. N. Lambrecht), Chapter 19, pp. 349-408;
Elsevier/Academic Press, Amsterdam (2015).
[60]
Radl J, Swart ACW, Mestecky J. The nature of the polymeric serum IgA in man. Proc Soc Exp Biol Med 1975; 150: 482-4.
[61]
Jonard PP, Rambaud JC, Vaerman JP, Galian A, Delaroix DL. Secretion of immunoglobulins and plasma proteins from the jejunal mucosa. Transport rate and origin of polymeric immunoglobulin A. J Clin Invest 1984; 74: 525-35.
[62]
Kubagawa H, Bertoli LF, Barton JC, Koopman WJ, Mestecky J, Cooper MD. Analysis of paraprotein transport into the saliva by using anti-idiotype antibodies. J Immunol 1987; 138: 435-9.
[63]
Mestecky J, Russell MW. IgA subclasses. In: Basic and Clinical
Aspects of IgG Subclasses (Ed. Shakib, F.) S. Karger, Basel.
Monogr. Allergy 1986; 19: 277-301.
[64]
Mestecky J, Russell MW, Jackson S, Brown TA. The human IgA system: A reassessment. Clin Immunol Immunopathol 1986; 40: 105-14.
[65]
Kutteh WH, Hatch KD, Blackwell RE, Mestecky J. Secretory immune system of the female reproductive tract: I. Immunoglobulin and secretory component-containing cells. Obstet Gynecol 1988; 71: 56-60.
[66]
Kutteh W, Hammond K, Prince S, Wester R, Mestecky J. Production of immunoglobulin A by the cervix of the human female genital tract.In: Reproductive Immunology (Eds. Dondero,
F., and Johnson, P.M.), Raven Press, New York 1993; 97: 151-8
[67]
Crowley-Nowick PA, Bell M, Edwards RP, et al. Normal uterine cervix: characterization of isolated lymphocyte phenotypes and immunoglobulin secretion. Am J Reprod Immunol 1995; 34: 241-7.
[68]
Brandtzaeg P. The mucosal B cell system. In: Mucosal
Immunology, 4th Edition (Eds. Mestecky J, Strober W, Russell
MW, Kelsall BL, Cheroute H, Lambrecht BN), Chapter 31, pp.
623-69; Elsevier/Academic Press, Amsterdam (2015)
[69]
Jalanti R, Isliker H. Immunoglobulins in human cervico-vaginal secretions. Int Arch Allergy Appl Immunol 1977; 53: 402-8.
[70]
Pudney J, Anderson DJ. Immunobiology of the human penile urethra. Am J Pathol 1995; 147: 155-65.
[71]
Lemos MP, Karuna ST, Mize GJ, et al. In men at risk of HIV infection, IgM, IgG1, IgG3, and IgA reach the human foreskin epidermis. Mucosal Immunol 2016; 9: 798-808.
[72]
Auvert B, Taljaard D, Lagarde E, et al. Randomized, controlled intervention trial of male circumcision for reduction of HIV infection risk: the ANRS 1265 Trial. PLoS Med 2005; 2: e298.
[73]
Bailey RC, Moses S, Parker CB, et al. Male circumcision for HIV prevention in young men in Kisumu, Kenya: A randomized controlled trial. Lancet 2007; 369: 643-56.
[74]
Gray RH, Kigozi G, Serwadda D, et al. Male circumcision for HIV prevention in men in Rakai, Uganda: A randomized trial. Lancet 2007; 369: 657-66.
[75]
Haynes BF, Gilbert PB, McElrath MJ, et al. Immune-correlates analysis of an HIV-1 vaccine efficacy trial. N Engl J Med 2012; 366: 1275-86.
[76]
Tomaras GD, Ferrari G, Shen X, 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 USA 2013; 110: 9019-24.
[77]
Yates NL, Liao HX, Fong Y, 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: 228ra239.
[78]
Chung AW, Ghebremichael M, Robinson H, et al. Polyfunctional Fc-effector profiles mediated by IgG subclass selection distinguish RV144 and VAX003 vaccines. Sci Transl Med 2014; 6: 228ra238.
[79]
Zolla-Pazner S, deCamp A, Gilbert PB, et al. Vaccine-induced IgG antibodies to V1V2 regions of multiple HIV-1 subtypes correlate with decreased risk of HIV-1 infections. PLoS One 2014; 9(2): e87572.
[80]
Nimmerjahn F, Ravetch JV. Fc gamma receptors as regulators of immune responses. Nat Rev Immunol 2008; 8: 34-47.
[81]
Cheeseman HM, Carias AM, Evans AB, et al. Expression profile of human Fc receptors in mucosal tissue: Implication for antibody-dependent cellular effector functions targeting HIV-1 transmission. PLoS One 2016; 11(5): e54656.
[82]
Sips M, Krykbaeva M, Diefenbach TJ, et al. Fc receptor-mediated phagocytosis in tissues as a potent mechanism for preventive and therapeutic HIV vaccine strategies. Mucosal Immunol 2016; 9: 1584-95.
[83]
Fahrbach KM, Malykhina O, Stieh DJ, Hope TJ. Differential binding of IgG and IgA to mucus of the female reproductive tract. PLoS One 2013; 8: e76176.
[84]
Shukair SA, Allen SA, Cianci GC, et al. Human cervicovaginal mucus contains an activity that hinders HIV-1 movement. Mucosal Immunol 2013; 6: 427-34.
[85]
Gunn B, Schneider J, Shansab M, et al. Enhanced binding of antibodies generated during chronic HIV infection to mucus component MUC16. Mucosal Immunol 2016; 9: 1549-58.
[86]
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 anti-gp41 antibodies with ineffective control of initial viremia. J Virol 2008; 82: 12449-63.
[87]
Liao HX, Chen X, Munshaw S, et al. Initial antibodies binding to HIV-1 gp41 in acutely infected subjects are polyreactive and highly mutated. J Exp Med 2011; 208: 2237-49.
[88]
Trama AM, Moody MA, Alam SM, et al. HIV-1 envelope gp41 antibodies can originate from terminal ileum B cells that share cross-reactivity with commensal bacteria. Cell Host Microbe 2014; 16: 215-26.
[89]
Williams WB, Liao HX, Moody MA, et al. HIV-1 VACCINES. Diversion of HIV-1 vaccine-induced immunity by gp41-microbiota cross-reactive antibodies. Science 2015; 349: 705-16.
[90]
Gosmann C, Anahtar MN, Handley SA, et al. Lactobacillus-deficient cervicovaginal bacterial communities are associated with increased HIV acquisition in young South African women. Immunity 2017; 46: 29-37.
[91]
Klatt NR, Cheu R, Birse K, et al. Vaginal bacteria modify HIV tenofovir microbicide efficacy in African women. Science 2017; 356: 938-45.
[92]
Hel Z, Xu J, Denning WL, et al. Dysregulation of systemic and mucosal humoral responses to microbial and food antigens in HIV-1-infected individuals. PLoS Pathog 2017; 13(1): e1006087.
[93]
Brandtzaeg P, Tolo K. Mucosal penetrability enhanced by serum-derived antibodies. Nature 1977; 266(5599): 262-3.
[94]
Russell MW, Sibley DA, Nikolova EB, Tomana M, Mestecky J. IgA antibody as a non-inflammatory regulator of immunity. Biochem Soc Trans 1997; 25: 466-70.
[95]
Afsen 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: 6257-65.
[96]
Alter G, Moody MA. The humoral response to HIV-1: New insights, renewed focus. J Infect Dis 2010; 202(S2): S315-22.
[97]
Battle-Miller K, Eby CA, Landay AL, Cohen MH, Sha BE, Baum LL. Antibody-dependent cell-mediated cytotoxicity in cervical lavage fluids of human immunodeficiency virus type-1infected women. J Infect Dis 2002; 185: 439-47.
[98]
Bomsel M, Tudor D, Drillet AS, et al. Immunization with HIV-1 gp41 subunit virosomes induces mucosal antibodies protecting nonhuman primates against vaginal SHIV-1 challenges. Immunity 2011; 34: 269-80.
[99]
Burton DR, Hessell AJ, Keele BF, et al. Limited or no protection by weakly or nonneutralizing antibodies against vaginal SHIV-1 challenge of macaques compared with a strongly neutralizing antibody. Proc Natl Acad Sci USA 2011; 108: 11181-6. l
[100]
Burton DR, Stanfield RL, Wilson IA. Antibody vs. HIV-1 in a clash of evolutionary titans. Proc Natl Acad Sci USA 2005; 102: 14943-8.
[101]
Gorlani A, Forthal DN. Antibody-dependent enhancement and the
risk of HIV-1 infection. Curr HIV-1 Res 2013; 11: 421-6.
[102]
Gupta S, Gasch JS, Becerra JC, et al. The neonatal Fc receptor (FcRn) enhances Human immunodeficiency virus type 1 (HIV-1-1) transcytosis across epithelial cells. PLoS Pathog 2013; 9(11): e1003776.
[103]
Hocini H, Belec L, Iscaki S, et al. High-level ability of Secretory IgA to block HIV-1 type 1 transcytosis: Contrasting secretory IgA and IgG responses to glycoprotein 160. J AIDS Res Hum Retroviruses 1997; 13: 1179-85.
[104]
Belec L, Tevi-Benissan C, Lu XS, Prazuck T, Pillot J. Local synthesis of IgG antibodies to HIV within the female and male genital tracts during asymptomatic and pre-AIDS stages of HIV infection. AIDS Res Hum Retroviruses 1995; 11: 719-29.
[105]
Kozlowski PA, Black KP, Shen L, Jackson S. High prevalence of serum IgA HIV-1 infection-enhancing antibodies in HIV-1-infected persons: Masking by IgG. J Immunol 1995; 154: 6163-73.
[106]
Lamm ME. Protection of mucosal epithelia by IgA: Intracellular neutralization and excretion of antigens. In: Mucosal Immune
Defense: Immunoglobulin A, CS Kaetzel (ed). New York, Springer Science Business Media, LLC. 2007; pp 173-82
[107]
Nag P, Kim J, Sapiega V, et al. Women with cervicovaginal antibody- dependent cell-mediated cytotoxicity have lower genital HIV-1 RNA loads. J Infect Dis 2004; 190: 1970-80.
[108]
Robinson WE, Montefiori DC, Mitchell WM. Antibody-dependent enhancement of human immunodeficiency virus type 1 infection. Lancet 1988; 331: 790-4.
[109]
Rochereau N, Pavot V, Verrier B, et al. Secretory IgA as a vaccine carrier for delivery of HIV-1 antigen to M cells. Eur J Immunol 2015; 45: 773-9.
[110]
Ruane D, Do Y, Brane L, et al. A dendritic cell targeted vaccine induces long-term HIV-1-specific immunity within the gastrointestinal tract. Mucosal Immunol 2016; 9: 1341-52.
[111]
Alexander R, Mestecky J. Neutralizing antibodies in mucosal secretions: IgG or IgA? Curr HIV-1 Research 2007; 5: 588-93
[112]
Astronomo RD, Santra S, Ballweber-Fleming L, et al. Neutralization takes precedence over IgG or IgA isotype-related functions in mucosal HIV-1 antibody-mediated protection. EBioMedicine 2016; 14: 97-111.
[113]
Bidgood SR, Tam JCH, McEwan WA, Mallery DL, James LC. Translocalized IgA mediates neutralization and stimulates innate immunity inside infected cells. Proc Natl Acad Sci USA 2014; 111: 13463-8.
[114]
Burnett PR, Van Cott TC, Polonis VR, Redfield RR, Birx DL. Serum IgA-mediated neutralization of HIV-1 type 1. J Immunol 1994; 152: 4642-8.
[115]
Escolani A, Dosenovic P, Nussenzweig MC. Progress toward active or passive HIV-1 vaccination. J Exp Med 2017; 214(1): 3-16.
[116]
Friedman J, Alam SM, Shen X, et al. Isolation of HIV-1-neutralizing mucosal monoclonal antibodies from human colostrum. PLoS One 2012; 7: e37648.
[117]
Hasselrot K, Saberg P, Hirbod T, et al. Oral HIV-1-exposure elicits mucosal HIV-1-neutralizing antibodies in uninfected men who have sex with men. AIDS 2009; 23: 329-33.
[118]
Hessell AJ, Epson E, Moldt B, et al. Bio-distribution of neutralizing monoclonal antibodies IgG1 b12 and LALA in mucosal and lymphatic tissues of rhesus macaques. Retrovirology 2012; 9: 204.
[http://dx.doi.org/10.1186/1742-4690-9-S2P204]
[http://dx.doi.org/10.1186/1742-4690-9-S2P204]
[119]
Hirbod T, Kaul R, Reichard C, et al. HIV-1-neutralizing immunoglobulin A and HIV-1-specific proliferation are independently associated with reduced HIV-1 acquisition in Kenyan sex workers. AIDS 2008; 22: 727-35.
[120]
Kozlowski PA, Chen D, Eldridge JH, Jackson S. Contrasting IgA and IgG neutralization capacities and responses to HIV-1 type 1 gp120 V3 loop in HIV-1-infected individuals. AIDS Res Hum Retroviruses 1994; 10: 813-22.
[121]
Lorin V, Malbec M, Eden C, et al. Broadly neutralizing antibodies suppress post-transcytosis HIV-1 infectivity. Mucosal Immunol 2017; 10: 814-26.
[122]
McKinley SA, Chen A, Shi F, et al. Modeling neutralization kinetics of HIV-1 by broadly neutralizing monoclonal antibodies in genital secretions coating the cervicovaginal mucosa. PLoS One 2014; 9: e100598.
[123]
Mkhize NN, Durgiah R, Ashley V, et al. Broadly neutralizing antibody specificities detected in the genital tract of HIV-1 infected women. AIDS 2016; 30: 1005-14.
[124]
Scharf O, Golding H, King LR, et al. Immunoglobulin G3 from polyclonal human immunodeficiency virus (HIV-1) immune globulin is more potent than other subclasses in neutralizing HIV-1 type 1. J Virol 2001; 75: 6558-65.
[125]
Scott YM, Park SY, Dezzutti CS. Broadly neutralizing anti-HIV antibodies prevent HIV infection of mucosal tissue ex vivo. Antimicrob Agents Chemother 2016; 60: 904-12.
[126]
Söderlund J, Hirbod T, Goh LE, Andersson J, Broliden K. Presence of HIV-1 neutralizing IgA antibodies in primary HIV-1-1 infected patients. Scand J Infect Dis 2004; 36: 663-9.
[127]
Stamatatos L, Morris L, Burton DR, Mascola JR. Neutralizing antibodies generated during natural HIV-1infection: Good news for an HIV-1 vaccine? Nat Med 2009; 15: 866-70.
[128]
Su B, Moog C. Which antibody functions are important for an HIV-1 vaccine? Front Immunol 2014; 5: 1-12.
[129]
Tudor D, Derrien M, Diomede L, et al. 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 2009; 2: 412-26.
[130]
Tudor D, Yu H, Maupetit J, et al. Isotype modulates epitope specificity, affinity, and antiviral activities of anti-HIV-1 human broadly neutralizing 2F5 antibody. Proc Natl Acad Sci USA 2012; 109: 12680-5.
[131]
Wei Q, Moldoveanu Z, Huang WQ, Alexander RC, Goepfert PA, Mestecky J. Comparative evaluation of HIV-1 neutralization in external secretions and sera of HIV-1-infected women. Open AIDS J 2012; 6: 293-302.
[132]
Zhou M, Ruprecht RM. Are anti-HIV-1 IgAs good guys or bad guys? Retrovirology 2014; 11: 109-20.
[133]
Belec L, Dupre T, Prazuck T, et al. Cervicovaginal overproduction of specific IgG to Human Immunodeficiency Virus (HIV-1) contrasts with normal or impaired IgA local response in HIV-1 infection. J Infect Dis 1995; 172: 691-7.
[134]
Belec L, Meillet D, Gaillard O, et al. Decreased cervicovaginal production of both IgA1 and IgA2 subclasses in women with AIDS. Clin Exp Immunol 1995; 101: 100-6.
[135]
Berneman A, Belec L, Fischetti VA, Bouvet JP. The specificity patterns of human immunoglobulin G antibodies in serum differ from those in autologous secretions. Infect Immun 1998; 66: 4163-8.
[136]
Chaoul N, Burelout C, Peruchon S, et al. Default in plasma and intestinal IgA responses during acute infection by simian immunodeficiency virus. Retrovirology 2012; 9: 43-56.
[137]
Fouda GG, Yates NL, Pollara J, et al. HIV-1-specific functional antibody responses in breast milk mirror those in plasma and are primarily mediated by IgG antibodies. J Virol 2011; 85: 9555-67.
[138]
Haimovici F, Mayer KH, Anderson DJ. Quantitation of HIV-1 specific IgG, IgA, and IgM antibodies in human genital tract secretions. J AIDS Retrovirol 1997; 15: 185-91.
[139]
Israel ZR, Marx PA. Nonclassical mucosal antibodies predominate in genital secretions of HIV-1 infected chimpanzees. J Med Primatol 1995; 24: 53-60.
[140]
Jackson S, Moldoveanu Z, Mestecky J, et al. Decreased IgA-producing cells in the gut of SIV-infected rhesus monkeys. Adv Exp Med Biol 1995; 371B: 1035-8.
[141]
Janoff EN, Jackson S, Wahl SM, Thomas K, Peterman JH, Smith PD. Intestinal mucosal immunoglobulins during Human Immunodeficiency Virus type 1 infection. J Infect Dis 1994; 170: 299-307.
[142]
Letvin NL, Rao SS, Dang V, et al. No evidence for consistent virus-specific immunity in simian immunodeficiency virus-exposed, uninfected Rhesus monkeys. J Virol 2007; 81: 12368-74.
[143]
Lu F. Predominate HIV-1 specific IgG activity in various mucosal compartments of HIV-1-infected individuals. Clin Immunol 2000; 97: 59-68.
[144]
Schafer F, Kewenig S, Stolte N, et al. Lack of Simian Immunodeficiency Virus (SIV) specific IgA response in the intestine of SIV-infected rhesus macaques. Gut 2002; 50: 608-14.
[145]
Tay MZ, Liu P, Williams LD, et al. Antibody-mediated internalization of infectious HIV-1 virions differs among antibody isotypes and subclasses. PLoS Pathog 2016; 12: e1005817.
[146]
Ngo-Giang-Huong N, Candotti D, Goubar A, et al. HIV-1 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: 1435-46.
[147]
van de Perre P, Hitimana DG, Lepage P. Human immunodeficiency virus antibodies of IgG, IgA, and IgM subclasses in milk of seropositive mothers. J Pediatr 1988; 113: 1039-41.
[148]
Xu W, Santini PA, Sullivan JS, et al. 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: 1008-19.
[149]
Yates NL, Lucas JT, Nolen TL, et al. Multiple HIV-1 specific IgG3 responses decline during acute HIV-1-1: implications for detection of incident HIV-1 infection. AIDS 2011; 25: 2089-97.
[150]
Yates NL, Liao HX, Fong Y. Fo. Vaccine-induced Env V1-V2 IgG3 correlates with lower HIV-1 infection risk and declines soon after vaccination. Sci Transl Med 2014; 6: 228-39.
[151]
Vidarsson G, Dekkers G, Rispens T. IgG subclasses and allotypes: from structure to effector functions. Front Immunol 2014; 5: 520.
[152]
Arnold JN, Wormald MR, Sim RB, Rudd PM, Dwek RA. The impact of glycosylation on the biological function and structure of human immunoglobulins. Annu Rev Immunol 2007; 25: 21-50.
[153]
Forthal DN, Gach JS, Landucci G, et al. Fc-glycosylation influences Fcγ receptor binding and cell-mediated anti-HIV-1 activity of monoclonal antibody 2G12. J Immunol 2010; 185: 6876-82.
[154]
Forthal DN, Hope TJ, Alter G. New paradigms for functional HIV- 1-specific non-neutralizing antibodies. Curr Opin HIV-1 AIDS 2013; 8: 392-400
[155]
Li T, DiLillo DJ, Bournazos S, Giddens JP, Ravetch JV, Wang L-X. Modulating IgG effector function by Fc glycan engineering. Proc Natl Acad Sci USA 2017; 114: 3485-90.
[156]
Mestecky J, Russell MW. Specific antibody activity, glycan heterogeneity and polyreactivity contribute to the protective activity of S-IgA at mucosal surfaces. Immunol Lett 2009; 124: 57-62.
[157]
Miranda LR, Duval M, Doherty H, Seaman MS, Posner MR, Cavacini LA. The neutralization properties of a HIV-1-specific antibody are markedly altered by glycosylation events outside the antigen-binding domain. J Immunol 2007; 178: 7132-8.
[158]
Moore JS, Wu X, Kulhavy R, et al. Increased levels of galactose-deficient IgG in sera of HIV-1-1-infected individuals. AIDS 2005; 19: 381-9.
[159]
Raju TS. Terminal sugars of Fc glycan influence antibody effector functions of IgGs. Curr Opin Immunol 2008; 20: 471-8.
[160]
Scallon BJ, Tam SH, McCarthy SG, Cai AN, Raju TS. Higher levels of sialylated Fc glycans in immunoglobulin G molecules can adversely impact functionality. Mol Immunol 2007; 44: 1524-34.
[161]
Huang YT, Wright A, Gao X, Kulick L, Yan H, Lamm M. Intraepithelial cell neutralization of HIV-1 replication. J Immunol 2005; 174: 4828-35.
[162]
Li Z, Palaniyandi S, Zeng R, Tuo W, Roopenian DC, Zhu X. Transfer of IgG in the female genital tract by MHC class I-related neonatal Fc Receptor (FcRn) confers protective immunity to vaginal infection. Proc Natl Acad Sci USA 2011; 108: 4388-93.
[163]
Wright A, Lamm ME, Huang YT. Excretion of human immunodeficiency virus type 1 through polarized epithelium by immunoglobulin A. J Virol 2008; 82: 11526-35.
[164]
Berger CT, Alter G. Natural killer cells in spontaneous control of
HIV-1 infection. Curr Opin HIV-1 AIDS 2011; 6: 208-13.
[165]
Musich T, Li L, Liu L, et al. Monoclonal antibodies specific for the V2, V3, CD4-binding site, and gp41 of HIV-1 mediate phagocytosis in a dose-dependent manner. J Virol 2017; 91(8): pii: e02325-.
[166]
Qiao X, He B, Chiu A, Knowles DM, Chadburn A, Cerutti A. Human immunodeficiency virus 1 Nef suppresses CD40-dependent immunoglobulin class switching in bystander B cells. Nat Immunol 2005; 7: 302-10.
[167]
Cartry O, Moja P, Quesnel A, Pozzetto B, Lucht FR, Genin C. Quantification of IgA and IgG and specificities of antibodies to viral proteins in parotid saliva at different stages of HIV-1 infection. Clin Exp Immunol 1997; 109: 47-53.
[168]
Matsuda S, Oka S, Honda M, Takebe Y, Takemori T. Characteristics of IgA antibodies against HIV-1 in sera and saliva from HIV-1-seropositive individuals in different clinical stages. Scand J Immunol 1993; 38: 428-34.
[169]
Franklin RD, Kutteh WH. Characterization of immunoglobulins and cytokines in human cervical mucus: Influence of exogenous and endogenous hormones. J Reprod Immunol 1999; 42: 93-106.
[170]
Hel Z, Stringer E, Mestecky J. Sex steroid hormones, hormonal contraception, and the Immunobiology of human immunodeficiency virus-1 infection. Endocr Rev 2010; 31: 79-97.
[171]
Menge AC, Mestecky J. Surface expression of secretory component and HLA class II DR antigen on glandular epithelial cells from human endometrium and two endometrial adenocarcinoma cell lines. J Clin Immunol 1993; 13: 259-64.
[172]
Yates NL, Stacy AR, Nolen TL, et al. HIV-1 gp41 envelope IgA is frequently elicited after transmission but has an initial short response half-life. Mucosal Immunol 2013; 6: 692-703.
[173]
Nabi R, Moldoveanu Z, Wei Q. Differences in serum IgA responses to HIV-1 gp41 in elite controllers compared to viral suppressors on highly active antiretroviral therapy. PLoS One 2017; 12(7): e0180245.
[174]
Armstrong SJ, Dimmock NJ. Neutralization of influenza virus by low concentrations of hemagglutinin-specific polymeric immunoglobulin A inhibits viral fusion activity, but activation of the ribonucleoprotein is also inhibited. J Virol 1992; 66: 3823-32.
[175]
Balazs AB, Ouyang Y, Hong CM, et al. Vectored immunoprophylaxis protects humanized mice from mucosal HIV-1 transmission. Nat Med 2014; 20: 296-300.
[176]
Williams IR, Owen RL. M cells: Specialized antigen sampling cells
in the follicle-associated epithelium. In: Mucosal Immunology, 4th
Edition (Eds. J. Mestecky W. Strober MW, Russell BL, Kelsall H.
Cheroute BN. Lambrecht), Chapter 21, pp.429-454;
Elsevier/Academic Press, Amsterdam (2015)
[177]
Renegar KB, Jackson GDF, Mestecky J. In vitro comparison of the biologic activities of monoclonal monomeric IgA, polymeric IgA and secretory IgA. J Immunol 1998; 160: 1219-23.
[178]
Taylor HP, Dimmock NJ. Mechanism of neutralization of influenza virus by secretory IgA is different from that of monomeric IgA or IgG. J Exp Med 1985; 161: 198-209.
[179]
Kilian M, Mestecky J, Russell MW. Defense mechanisms involving Fc-dependent functions of immunoglobulin A and their subversion by bacterial immunoglobulin A protease. Microbiol Rev 1988; 52: 296-303.
[180]
Kaetzel CS, Russell MW. Phylogeny and comparative physiology of mucosal immunoglobulins.. In: Mucosal Immunology, 4th
Edition (Eds. J. Mestecky, W. Strober, M.W., Russell, B. L.
Kelsall, H. Cheroute, B. N. Lambrecht), Chapter 18, pp.325-47;
Elsevier/Academic Press, Amsterdam (2015)
[181]
Russell MW, Kilian M, Mantis NJ, Corthesy B. Biological activities of IgA. In: Mucosal Immunology, 4th Edition (Eds. J.
Mestecky, W. Strober, M.W., Russell, B. L. Kelsall, H. Cheroute,
B. N. Lambrecht), Chapter 21, pp.429-54; Elsevier/Academic
Press, Amsterdam (2015)
[182]
Russell MW, Lue C, van den Wall Bake AWL, Moldoveanu Z, Mestecky J. Molecular heterogeneity of human IgA antibodies during an immune response. Clin Exp Immunol 1992; 87: 1-6.
[183]
Kozlowski PA, Jackson S. Serum IgA subclasses and molecular forms in HIV-1 infection: Selective increases in monomer and apparent restriction of the antibody response to IgA1 antibodies mainly directed at ENV glycoproteins. AIDS Res Hum Retroviruses 1992; 8: 1773-80.
[184]
Corti D, Langedijk JP, Hinz A, et al. Analysis of memory B cell responses and isolation of novel monoclonal antibodies with neutralizing breadth from HIV-1-infected individuals. PLoS One 2010; 5: e8805.
[185]
Kulkarni V, Ruprecht RM. Mucosal IgA responses: Damaged in
established HIV infection - yet, effective weapon against HIV
transmission. Front Immunol 2017; 8: 01581.doi: 10.3389.
[186]
Mallery DL, McEwan WA, Bidgood SR, Towers GJ, Johnson CM, James LC. Antibodies mediate intracellular immunity through tripartite motif-containing 21 (TRIM21). Proc Natl Acad Sci USA 2010; 107: 19985-90.
[187]
McEwan WA, Mallery DL, Rhodes DA, Trowsdale J, James LC. Intracellular antibody-mediated immunity and the role of TRIM21. BioEssays 2011; 33: 803-9.
[188]
Vaysburd M, Watkinson RE, Cooper H, et al. Intracellular antibody receptor TRIM21 prevents fatal viral infection. Proc Natl Acad Sci USA 2013; 110: 12397-401.
[189]
Stieh DJ, King DF, Klein K, et al. Aggregate complexes of HIV-1 induced by multimeric antibodies. Retrovirology 2014; 11: 78-94.
[190]
Liu P, Yates NL, Shen X, et al. Infectious virion capture by HIV-1 gp120-specific IgG from RV144 vaccinees. J Virol 2013; 87: 7828-36.
[191]
Liu P, Williams LD, Shen X, et al. Capacity for infectious HIV-1 virion capture differs by envelope antibody specificity. J Virol 2014; 88: 5165-70.
[192]
Beyrer C, Artenstein AW, Rugpao S, et al. Epidemiologic and biologic characterization of a cohort of human Immunodeficiency virus type 1 highly exposed, persistently seronegative female sex workers in Northern Thailand. J Infect Dis 1999; 179: 59-67.
[193]
Broliden K, Hinkula J, Devito C, et al. Functional HIV-1 specific IgA antibodies in HIV-1- exposed, persistently IgG seronegative female sex workers. Immunol Lett 2001; 79: 29-36.
[194]
Buchacz K, Parekh BS, Padian NS, et al. HIV-1-specific IgG in cervicovaginal secretions of exposed HIV-1-uninfected female sexual partners of HIV-1-infected men. AIDS Res Hum Retroviruses 2001; 17: 1689-93.
[195]
Choi RY, Levinson P, Guthrie BL, et al. Cervicovaginal HIV-1-neutralizing immunoglobulin A detected among HIV-1-exposed seronegative female partners in HIV-1-discordant couples. AIDS 2012; 26: 2155-63.
[196]
Clerici M, Barassi C, Devito C, et al. Serum IgA of HIV-1-exposed uninfected individuals inhibit HIV-1 through recognition of a region within the alpha-helix of gp41. AIDS 2002; 16: 1731-41.
[197]
Devito C, Broliden K, Kaul R, et al. Mucosal and plasma IgA from HIV-1-exposed uninfected individuals inhibit HIV-1 transcytosis across human epithelial cells. J Immunol 2000; 165: 5170-6.
[198]
Devito C, Hinkula J, Kaul R, et al. Cross-clade HIV-1-specific neutralizing IgA in mucosal and systemic compartments of HIV-1-exposed, persistently seronegative subjects. J Acquir Immune Defic Syndr 2005; 30: 413-20.
[199]
Devito C, Hinkula J, Kaul R, et al. Mucosal and plasma IgA from HIV-1-exposed seronegative individuals neutralize a primary HIV-1 isolate. AIDS 2000; 8: 1917-20.
[200]
Dorrell L, Hessell AJ, Wang M, et al. Absence of specific mucosal antibody responses in HIV-1-exposed uninfected sex workers from the Gambia. AIDS 2000; 14: 1117-22.
[201]
Fiore JR, Laddago V, Lepera A, Angarano G. Limited secretory-IgA response in cervicovaginal secretions from HIV-1-infected, but not high risk seronegative women: Lack of correlation to genital viral shedding. New Microbiol 2000; 23: 85-92.
[202]
Hirbod T, Broliden K. Mucosal immune responses in the genital tract of HIV-1-exposed uninfected women. J Intern Med 2007; 262: 44-58.
[203]
Horton RE, Ball TB, Wachichi C, et al. Cervical HIV-1-specific IgA in a population of commercial sex workers correlates with repeated exposure but not resistance to HIV-1. AIDS Res Hum Retroviruses 2009; 25: 83-92.
[204]
Kaul R, Trabattoni D, Bwayo JJ, et al. HIV-1-specific mucosal IgA in a cohort of HIV-1-resistant Kenyan sex workers. AIDS 1999; 13: 23-9.
[205]
Kaul R, Plummer F, Clerici M, Bomsel M, Lopalco L, Broliden K. Mucosal IgA in exposed, uninfected subjects: Evidence for a role in protection against HIV infection. AIDS 2001; 15: 431-2.
[206]
Lo CS, Trabattoni D, Vichi F, et al. Mucosal and systemic HIV-1-specific immunity in HIV-1-exposed but uninfected heterosexual men. AIDS 2003; 17: 531-9.
[207]
Lund JM, Broliden K, Pyra MN, et al. HIV-1 neutralizing IgA detected in genital secretions of highly HIV-1-exposed seronegative women on oral preexposure prophylaxis. J Virol 2016; 90(21): 9855-61.
[208]
Mazzoli S, Lopalco L, Salvi A, et al. Human Immunodeficiency Virus (HIV-1)-specific IgA and HIV-1 neutralizing activity in the serum of exposed seronegative partners of HIV-1-seropositive persons. J Infect Dis 1999; 180: 871-5.
[209]
Mazzoli S, Trabaironi D, Lo Caputo S, et al. HIV-1-specific mucosal and cellular immunity in HIV-1-seronegative partners of HIV-1-seropositive individuals. Nat Med 1997; 3: 1250-7.
[210]
Seaton KE, Ballweber L, Lan A, et al. HIV-1-specific IgA detected in vaginal secretions of HIV-1 uninfected women participating in a microbicide trail in Southern Africa are primarily directed toward gp120 and gp140 specificities. PLoS One 2014; 9: e101863.
[211]
Schneider JA, Alam SA, Ackers M, et al. Mucosal HIV-binding antibody and neutralizing activity in high-risk HIV-uninfected female participants in a trial of HIV-vaccine efficacy. J Infect Dis 2007; 196: 1637-44.
[212]
Skurnick JH, Palumbo P, DeVico A, et al. Correlates of nontransmission in US women at high risk of human immunodeficiency virus type 1 infection through sexual exposure. J Infect Dis 2002; 185: 428-38.
[213]
Abdulhaqq SA, Zorrilla C, Kang G, et al. HIV-1-negative female sex workers sustain high cervical IFNε, low immune activation, and low expression of HIV-1-required host genes. Mucosal Immunol 2016; 9: 1027-38.
[214]
Kutteh WH, Edwards RP, Menge AC, Mestecky J. IgA immunity in female reproductive tract secretions. In: Local
Immunity in Reproductive Tract Tissues. (Eds. Griffin PD. and
Johnson PM). Chapter 13, pp. 229-243. Oxford University Press,
Delhi (1993)
[215]
Russell MW, Mestecky J. Humoral immune responses to microbial infections in the genital tract. Microbes Infect 2002; 4: 667-77.
[216]
Russell MW, Mestecky J. Tolerance and protection against infection in the genital tract. Immunol Invest 2010; 39: 500-25.
[217]
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 anti-gp41 antibodies with ineffective control of initial viremia. J Virol 2008; 82: 12449-63.
[218]
Archary D, Seaton KE, Passmore JS, et al. Distinct genital tract HIV-specific antibody profiles associated with tenofovir gel. Mucosal Immunol 2016; 9: 821-33.
[219]
Bouvet JP, Belec L, Pires R, Pillot J. Immunoglobulin G antibodies in human vaginal secretions after parenteral vaccination. Infect Immun 1994; 62: 3957-61.
[220]
Pavot V, Rochereau N, Lawrence P, et al. Recent progress in HIV-1 vaccines inducing mucosal immune responses. AIDS 2014; 28: 1701-18.
[221]
Underdown BJ, Strober W. Parenteral immunization and protection from mucosal infection. In: Mucosal Immunology, 4th Edition
(Eds. J. Mestecky, W. Strober, M.W., Russell, B. L. Kelsall, H.
Cheroute, B. N. Lambrecht), Chapter 70, pp.1391-403;
Elsevier/Academic Press, Amsterdam (2015).
[222]
Mestecky J. The common mucosal immune system and current strategies for induction of immune responses in external secretions. J Clin Immunol 1987; 7: 265-76.
[223]
Russell MW, Mestecky J. Mucosal Vaccines: An Overview.
In: Mucosal Immunology, 4th Edition (Eds. J. Mestecky, W.
Strober, M.W., Russell, B. L. Kelsall, H. Cheroute, B. N.
Lambrecht), Chapter 55, pp.1039-46; Elsevier/Academic Press,
Amsterdam (2015)
[224]
McElrath MJ. Mucosal immunity and vaccines against simian immunodeficiency virus and human immunodeficiency virus.. In:
Mucosal Immunology, 4th Edition (Eds. J. Mestecky, W. Strober,
M.W., Russell, B. L. Kelsall, H. Cheroute, B. N. Lambrecht),
Chapter 60, pp.1171-81; Elsevier/Academic Press, Amsterdam
(2015).
[225]
Wright PF, Mestecky J, McElrath MJ. Keefer et al. Comparison of systemic and mucosal delivery of 2 canarypox virus vaccines expressing either HIV-1 genes or the gene for rabies virus G protein. J Infect Dis 2004; 189: 1221-31.
[226]
Agnello D, Denimal D, Lavaux A, et al. Intrarectal immunization and IgA antibody-secreting cell homing to the small intestine. J Immunol 2013; 190: 4836-47.
[227]
Crowley-Nowick PA, Bell MC, Brockwell R, et al. Rectal immunization for induction of specific antibody in the genital tract of women. J Clin Immunol 1997; 17: 370-9.
[228]
Crowley-Nowick PA, Edwards RP, Moldoveanu Z, Kutteh W, Mestecky J. Menstrual cycle: Effects on vaccine-induced antibodies in genital tract secretions.. In: Mucosal Solutions.
Advances in Mucosal Immunology. (Eds. Husband, A.J., Beagley,
K.W., Clancy, R.L., Collins, A.M., Cripps, A.W., and Emery, D.L.)
The University of Sydney, Australia 1: 393-401 (1997)
[229]
Kantele A, Hakkinen M, Moldoveanu Z, et al. Differences in immune responses induced by oral and rectal immunizations with Salmonella typhi Ty21a: Evidence for compartmentalization within the common mucosal immune system in humans. Infect Immun 1988; 66: 5630-5.
[230]
Kutteh WH, Kantele A, Moldoveanu Z, Crowley-Nowick PA, Mestecky J. Induction of specific immune responses in the genital tract of women after oral or rectal immunization and rectal boosting with Salmonella typhi Type 21a vaccine. J Reprod Immunol 2001; 61-75.
[231]
Kozlowski PA, Williams SB, Lynch RM, et al. Differential induction of mucosal and systemic antibody responses in women after nasal, rectal, or vaginal immunization: Influence of the menstrual cycle. J Immunol 2002; 169: 566-74.
[232]
Wassen L, Schon K, Holmgren J, Jertborn M, Lycke N. Local intravaginal vaccination of the female genital tract. Scand J Immunol 1996; 44: 408-14.
[233]
Johansson E-L, Wassen L, Holmgren J, Jertborn M, Rudin A. Nasal and vaginal vaccinations have differential effects on antibody responses in vaginal and cervical secretions in humans. Infect Immun 2001; 69(12): 7481-6.
[234]
Lehner T, Panagiotidi C, Bergmeier LA, Ping T, Brookes R, Adams SE. A comparison of the immune responses following oral, vaginal or rectal route of immunization with SIV antigens in nonhuman primates. Vaccine Rep 1992; 3: 319-30.
[235]
Miller CJ, Kang DW, Marthas M, et al. Genital secretory immune response to chronic Simian Immunodeficiency Virus (SIV) infection: A comparison between intravenously and genitally inoculated rhesus macaques. Clin Exp Immunol 1992; 88: 520-6.
[236]
Russell MW, Moldoveanu Z, White PL, Sibert GJ, Mestecky J, Michalek SM. Salivary, nasal, genital and systemic antibody responses in monkeys immunized intranasally with a bacterial protein antigen and cholera toxin B subunit. Infect Immun 1996; 64: 1272-83.
[237]
Brown TA, Mestecky J. Immunoglobulin A subclass distribution of naturally occurring salivary antibodies to microbial antigens. Infect Immun 1985; 49: 459-62.
[238]
Brown WR, Newcomb RW, Ishizaka K. Proteolytic degradation of exocrine and serum immunoglobulins. J Clin Invest 1970; 49: 1374-80.
[239]
Conley ME, Delacroix DL. Intravascular and mucosal immunoglobulin A: Two separate but related systems of immune defense? Ann Intern Med 1987; 106: 892-9.
[240]
Endo T, Mestecky J, Kulhavy R, Kobata A. Carbohydrate heterogeneity of human myeloma proteins of the IgA1 and IgA2 subclasses. Mol Immunol 1994; 33: 1415-22.
[241]
Hammarström L, Smith CIE. IgG subclass changes in response to vaccination. Monogr Allergy 1986; 19: 241-52.
[242]
Ladjeva I, Peterman JH, Mestecky J. IgA subclasses of human colostral antibodies specific for microbial and food antigens. Clin Exp Immunol 1989; 78: 85-90.
[243]
Mestecky J, McGhee JR, Immunoglobulin A. IgA): Molecular and cellular interactions involved in IgA biosynthesis and immune response. Adv Immunol 1987; 40: 153-245.
Article Metrics
79
3