Natural Immunity to HIV: A Template for Vaccine Strategies
Abstract
:1. Introduction
2. Immunology of the Female Genital Tract
3. The Female Genital Tract in the Context of HIV
4. Natural Immunity to HIV in the FGT of HESNs
5. Immunoregulatory Cell Populations in HESNs
6. The Importance of HIV ENV Reactive Immunoglobulins: Lessons from Vaccination Trials
7. HIV ENV Reactive Immunoglobulins in HESNs
8. Innate B-Cells and BLyS/BAFF in Natural Immunity to HIV
9. Concluding Remarks
Acknowledgments
Conflicts of Interest
References
- UNAIDS Unaids Data 2017. Available online: http://www.unaids.org/en/resources/documents/2017/2017_data_book (accessed on 20 March 2018).
- Poudrier, J.; Thibodeau, V.; Roger, M. Natural immunity to HIV: A delicate balance between strength and control. Clin. Dev. Immunol. 2012, 2012, 875821. [Google Scholar] [CrossRef] [PubMed]
- Fowke, K.R.; Nagelkerke, N.J.; Kimani, J.; Simonsen, J.N.; Anzala, A.O.; Bwayo, J.J.; MacDonald, K.S.; Ngugi, E.N.; Plummer, F.A. Resistance to HIV-1 infection among persistently seronegative prostitutes in Nairobi, Kenya. Lancet 1996, 348, 1347–1351. [Google Scholar] [CrossRef]
- Yao, X.D.; Omange, R.W.; Henrick, B.M.; Lester, R.T.; Kimani, J.; Ball, T.B.; Plummer, F.A.; Rosenthal, K.L. Acting locally: Innate mucosal immunity in resistance to HIV-1 infection in Kenyan commercial sex workers. Mucosal Immunol. 2014, 7, 268–279. [Google Scholar] [CrossRef] [PubMed]
- Wira, C.R.; Fahey, J.V.; Sentman, C.L.; Pioli, P.A.; Shen, L. Innate and adaptive immunity in female genital tract: Cellular responses and interactions. Immunol. Rev. 2005, 206, 306–335. [Google Scholar] [CrossRef] [PubMed]
- Shacklett, B.L. Cell-mediated immunity to hiv in the female reproductive tract. J. Reprod. Immunol. 2009, 83, 190–195. [Google Scholar] [CrossRef] [PubMed]
- Wira, C.R.; Fahey, J.V. A new strategy to understand how HIV infects women: Identification of a window of vulnerability during the menstrual cycle. Aids 2008, 22, 1909–1917. [Google Scholar] [CrossRef] [PubMed]
- Wira, C.R.; Rodriguez-Garcia, M.; Patel, M.V. The role of sex hormones in immune protection of the female reproductive tract. Nat. Rev. Immunol. 2015, 15, 217–230. [Google Scholar] [CrossRef] [PubMed]
- Hickey, D.K.; Patel, M.V.; Fahey, J.V.; Wira, C.R. Innate and adaptive immunity at mucosal surfaces of the female reproductive tract: Stratification and integration of immune protection against the transmission of sexually transmitted infections. J. Reprod. Immunol. 2011, 88, 185–194. [Google Scholar] [CrossRef] [PubMed]
- Iwasaki, A.; Medzhitov, R. Toll-like receptor control of the adaptive immune responses. Nat. Immunol. 2004, 5, 987–995. [Google Scholar] [CrossRef] [PubMed]
- Poudrier, J.; Chagnon-Choquet, J.; Roger, M. Influence of dendritic cells on b-cell responses during hiv infection. Clin. Dev. Immunol. 2012, 2012, 592187. [Google Scholar] [CrossRef] [PubMed]
- Nazli, A.; Chan, O.; Dobson-Belaire, W.N.; Ouellet, M.; Tremblay, M.J.; Gray-Owen, S.D.; Arsenault, A.L.; Kaushic, C. Exposure to HIV-1 directly impairs mucosal epithelial barrier integrity allowing microbial translocation. PLoS Pathog. 2010, 6, e1000852. [Google Scholar] [CrossRef] [PubMed]
- Grant-Tschudy, K.S.; Wira, C.R. Paracrine mediators of mouse uterine epithelial cell transepithelial resistance in culture. J. Reprod. Immunol. 2005, 67, 1–12. [Google Scholar] [CrossRef] [PubMed]
- Cleret-Buhot, A.; Zhang, Y.; Planas, D.; Goulet, J.P.; Monteiro, P.; Gosselin, A.; Wacleche, V.S.; Tremblay, C.L.; Jenabian, M.A.; Routy, J.P.; et al. Identification of novel HIV-1 dependency factors in primary CCR4+CCR6+Th17 cells via a genome-wide transcriptional approach. Retrovirology 2015, 12, 102. [Google Scholar] [CrossRef] [PubMed]
- Gringhuis, S.I.; van der Vlist, M.; van den Berg, L.M.; den Dunnen, J.; Litjens, M.; Geijtenbeek, T.B. HIV-1 exploits innate signaling by TLR8 and DC-SIGN for productive infection of dendritic cells. Nat. Immunol. 2010, 11, 419–426. [Google Scholar] [CrossRef] [PubMed]
- Haase, A.T. Targeting early infection to prevent HIV-1 mucosal transmission. Nature 2010, 464, 217–223. [Google Scholar] [CrossRef] [PubMed]
- Magerus-Chatinet, A.; Yu, H.; Garcia, S.; Ducloux, E.; Terris, B.; Bomsel, M. Galactosyl ceramide expressed on dendritic cells can mediate HIV-1 transfer from monocyte derived dendritic cells to autologous T cells. Virology 2007, 362, 67–74. [Google Scholar] [CrossRef] [PubMed]
- Bomsel, M. Transcytosis of infectious human immunodeficiency virus across a tight human epithelial cell line barrier. Nat. Med. 1997, 3, 42–47. [Google Scholar] [CrossRef] [PubMed]
- Shang, L.; Duan, L.; Perkey, K.E.; Wietgrefe, S.; Zupancic, M.; Smith, A.J.; Southern, P.J.; Johnson, R.P.; Haase, A.T. Epithelium-innate immune cell axis in mucosal responses to siv. Mucosal Immunol. 2017, 10, 508–519. [Google Scholar] [CrossRef] [PubMed]
- Geijtenbeek, T.B.; Kwon, D.S.; Torensma, R.; van Vliet, S.J.; van Duijnhoven, G.C.; Middel, J.; Cornelissen, I.L.; Nottet, H.S.; KewalRamani, V.N.; Littman, D.R.; et al. DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells. Cell 2000, 100, 587–597. [Google Scholar] [CrossRef]
- Fontenot, D.; He, H.; Hanabuchi, S.; Nehete, P.N.; Zhang, M.; Chang, M.; Nehete, B.; Wang, Y.H.; Wang, Y.H.; Ma, Z.M.; et al. TSLP production by epithelial cells exposed to immunodeficiency virus triggers DC-mediated mucosal infection of CD4+ T cells. Proc. Natl. Acad. Sci. USA 2009, 106, 16776–16781. [Google Scholar] [CrossRef] [PubMed]
- Malim, M.H.; Bieniasz, P.D. HIV restriction factors and mechanisms of evasion. Cold Spring Harb. Perspect. Med. 2012, 2, a006940. [Google Scholar] [CrossRef] [PubMed]
- Haase, A.T. Early events in sexual transmission of HIV and SIV and opportunities for interventions. Annu. Rev. Med. 2011, 62, 127–139. [Google Scholar] [CrossRef] [PubMed]
- Gringhuis, S.I.; den Dunnen, J.; Litjens, M.; van der Vlist, M.; Geijtenbeek, T.B. Carbohydrate-specific signaling through the DC-SIGN signalosome tailors immunity to Mycobacterium tuberculosis, HIV-1 and Helicobacter pylori. Nat. Immunol. 2009, 10, 1081–1088. [Google Scholar] [CrossRef] [PubMed]
- Teijeira, A.; Russo, E.; Halin, C. Taking the lymphatic route: Dendritic cell migration to draining lymph nodes. Semin. Immunopathol. 2014, 36, 261–274. [Google Scholar] [CrossRef] [PubMed]
- Miller, C.J.; Li, Q.; Abel, K.; Kim, E.Y.; Ma, Z.M.; Wietgrefe, S.; La Franco-Scheuch, L.; Compton, L.; Duan, L.; Shore, M.D.; et al. Propagation and dissemination of infection after vaginal transmission of simian immunodeficiency virus. J. Virol. 2005, 79, 9217–9227. [Google Scholar] [CrossRef] [PubMed]
- Stieh, D.J.; Matias, E.; Xu, H.; Fought, A.J.; Blanchard, J.L.; Marx, P.A.; Veazey, R.S.; Hope, T.J. Th17 cells are preferentially infected very early after vaginal transmission of SIV in macaques. Cell Host Microbe 2016, 19, 529–540. [Google Scholar] [CrossRef] [PubMed]
- Ivanov, I.I.; McKenzie, B.S.; Zhou, L.; Tadokoro, C.E.; Lepelley, A.; Lafaille, J.J.; Cua, D.J.; Littman, D.R. The orphan nuclear receptor rorgammat directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell 2006, 126, 1121–1133. [Google Scholar] [CrossRef] [PubMed]
- Manel, N.; Unutmaz, D.; Littman, D.R. The differentiation of human T(H)-17 cells requires transforming growth factor-beta and induction of the nuclear receptor RORgammat. Nat. Immunol. 2008, 9, 641–649. [Google Scholar] [CrossRef] [PubMed]
- Kader, M.; Wang, X.; Piatak, M.; Lifson, J.; Roederer, M.; Veazey, R.; Mattapallil, J.J. α4+β7hiCD4+ memory T cells harbor most Th-17 cells and are preferentially infected during acute SIV infection. Mucosal Immunol. 2009, 2, 439–449. [Google Scholar] [CrossRef] [PubMed]
- Cremel, M.; Berlier, W.; Hamzeh, H.; Cognasse, F.; Lawrence, P.; Genin, C.; Bernengo, J.C.; Lambert, C.; Dieu-Nosjean, M.C.; Delezay, O. Characterization of CCL20 secretion by human epithelial vaginal cells: Involvement in langerhans cell precursor attraction. J. Leukoc. Biol. 2005, 78, 158–166. [Google Scholar] [CrossRef] [PubMed]
- Schutyser, E.; Struyf, S.; Van Damme, J. The CC chemokine CCL20 and its receptor CCR6. Cytokine Growth Factor Rev. 2003, 14, 409–426. [Google Scholar] [CrossRef]
- Li, Q.; Estes, J.D.; Schlievert, P.M.; Duan, L.; Brosnahan, A.J.; Southern, P.J.; Reilly, C.S.; Peterson, M.L.; Schultz-Darken, N.; Brunner, K.G.; et al. Glycerol monolaurate prevents mucosal SIV transmission. Nature 2009, 458, 1034–1038. [Google Scholar] [CrossRef] [PubMed]
- Schellenberg, J.J.; Plummer, F.A. The microbiological context of HIV resistance: Vaginal microbiota and mucosal inflammation at the viral point of entry. Int. J. Inflam. 2012, 2012, 131243. [Google Scholar] [CrossRef] [PubMed]
- Lajoie, J.; Juno, J.; Burgener, A.; Rahman, S.; Mogk, K.; Wachihi, C.; Mwanjewe, J.; Plummer, F.A.; Kimani, J.; Ball, T.B.; et al. A distinct cytokine and chemokine profile at the genital mucosa is associated with HIV-1 protection among HIV-exposed seronegative commercial sex workers. Mucosal Immunol. 2012, 5, 277–287. [Google Scholar] [CrossRef] [PubMed]
- Lajoie, J.; Poudrier, J.; Massinga Loembe, M.; Guedou, F.; Leblond, F.; Labbe, A.C.; Alary, M.; Roger, M. Chemokine expression patterns in the systemic and genital tract compartments are associated with HIV-1 infection in women from Benin. J. Clin. Immunol. 2010, 30, 90–98. [Google Scholar] [CrossRef] [PubMed]
- Lajoie, J.; Poudrier, J.; Massinga-Loembe, M.; Guedou, F.; Agossa-Gbenafa, C.; Labbe, A.C.; Alary, M.; Roger, M. Differences in immunoregulatory cytokine expression patterns in the systemic and genital tract compartments of HIV-1-infected commercial sex workers in Benin. Mucosal Immunol. 2008, 1, 309–316. [Google Scholar] [CrossRef] [PubMed]
- Ball, T.B.; Ji, H.; Kimani, J.; McLaren, P.; Marlin, C.; Hill, A.V.; Plummer, F.A. Polymorphisms in IRF-1 associated with resistance to HIV-1 infection in highly exposed uninfected kenyan sex workers. Aids 2007, 21, 1091–1101. [Google Scholar] [CrossRef] [PubMed]
- Ji, H.; Ball, T.B.; Ao, Z.; Kimani, J.; Yao, X.; Plummer, F.A. Reduced HIV-1 long terminal repeat transcription in subjects with protective interferon regulatory factor-1 genotype: A potential mechanism mediating resistance to infection by HIV-1. Scand. J. Infect. Dis. 2010, 42, 389–394. [Google Scholar] [CrossRef] [PubMed]
- Fowke, K.R.; Kaul, R.; Rosenthal, K.L.; Oyugi, J.; Kimani, J.; Rutherford, W.J.; Nagelkerke, N.J.; Ball, T.B.; Bwayo, J.J.; Simonsen, J.N.; et al. HIV-1-specific cellular immune responses among HIV-1-resistant sex workers. Immunol. Cell Biol. 2000, 78, 586–595. [Google Scholar] [CrossRef] [PubMed]
- Kaul, R.; Plummer, F.A.; Kimani, J.; Dong, T.; Kiama, P.; Rostron, T.; Njagi, E.; MacDonald, K.S.; Bwayo, J.J.; McMichael, A.J.; et al. HIV-1-specific mucosal CD8+ lymphocyte responses in the cervix of HIV-1-resistant prostitutes in Nairobi. J. Immunol. 2000, 164, 1602–1611. [Google Scholar] [CrossRef] [PubMed]
- McKinnon, L.R.; Nyanga, B.; Chege, D.; Izulla, P.; Kimani, M.; Huibner, S.; Gelmon, L.; Block, K.E.; Cicala, C.; Anzala, A.O.; et al. Characterization of a human cervical CD4+ T cell subset coexpressing multiple markers of HIV susceptibility. J. Immunol. 2011, 187, 6032–6042. [Google Scholar] [CrossRef] [PubMed]
- McLaren, P.J.; Ball, T.B.; Wachihi, C.; Jaoko, W.; Kelvin, D.J.; Danesh, A.; Kimani, J.; Plummer, F.A.; Fowke, K.R. HIV-exposed seronegative commercial sex workers show a quiescent phenotype in the CD4+ T cell compartment and reduced expression of HIV-dependent host factors. J. Infect. Dis. 2010, 202, S339–S344. [Google Scholar] [CrossRef] [PubMed]
- Alimonti, J.B.; Koesters, S.A.; Kimani, J.; Matu, L.; Wachihi, C.; Plummer, F.A.; Fowke, K.R. CD4+ T cell responses in HIV-exposed seronegative women are qualitatively distinct from those in HIV-infected women. J. Infect. Dis. 2005, 191, 20–24. [Google Scholar] [CrossRef] [PubMed]
- Thibodeau, V.; Fourcade, L.; Labbe, A.C.; Alary, M.; Guedou, F.; Poudrier, J.; Roger, M. Highly-exposed HIV-1 seronegative female commercial sex workers sustain in their genital mucosa increased frequencies of tolerogenic myeloid and regulatory T-cells. Sci. Rep. 2017, 7, 43857. [Google Scholar] [CrossRef] [PubMed]
- Saitoh, S.I.; Abe, F.; Kanno, A.; Tanimura, N.; Mori Saitoh, Y.; Fukui, R.; Shibata, T.; Sato, K.; Ichinohe, T.; Hayashi, M.; et al. TLR7 mediated viral recognition results in focal type I interferon secretion by dendritic cells. Nat. Commun. 2017, 8, 1592. [Google Scholar] [CrossRef] [PubMed]
- Doyle, T.; Goujon, C.; Malim, M.H. HIV-1 and interferons: Who’s interfering with whom? Nat. Rev. Microbiol. 2015, 13, 403–413. [Google Scholar] [CrossRef] [PubMed]
- Kawai, T.; Akira, S. The role of pattern-recognition receptors in innate immunity: Update on toll-like receptors. Nat. Immunol. 2010, 11, 373–384. [Google Scholar] [CrossRef] [PubMed]
- Siewe, B.; Stapleton, J.T.; Martinson, J.; Keshavarzian, A.; Kazmi, N.; Demarais, P.M.; French, A.L.; Landay, A. Regulatory B cell frequency correlates with markers of HIV disease progression and attenuates anti-HIV CD8+ T cell function in vitro. J. Leukoc. Biol. 2013, 93, 811–818. [Google Scholar] [CrossRef] [PubMed]
- Chagnon-Choquet, J.; Fontaine, J.; Poudrier, J.; Roger, M. IL-10 and lymphotoxin-alpha expression profiles within marginal zone-like B-cell populations are associated with control of HIV-1 disease progression. PLoS ONE 2014, 9, e101949. [Google Scholar] [CrossRef] [PubMed]
- Das, A.; Ellis, G.; Pallant, C.; Lopes, A.R.; Khanna, P.; Peppa, D.; Chen, A.; Blair, P.; Dusheiko, G.; Gill, U.; et al. IL-10-producing regulatory B cells in the pathogenesis of chronic hepatitis B virus infection. J. Immunol. 2012, 189, 3925–3935. [Google Scholar] [CrossRef] [PubMed]
- De Waal Malefyt, R.; Haanen, J.; Spits, H.; Roncarolo, M.G.; te Velde, A.; Figdor, C.; Johnson, K.; Kastelein, R.; Yssel, H.; de Vries, J.E. Interleukin 10 (IL-10) and viral IL-10 strongly reduce antigen-specific human T cell proliferation by diminishing the antigen-presenting capacity of monocytes via downregulation of class II major histocompatibility complex expression. J. Exp. Med. 1991, 174, 915–924. [Google Scholar] [CrossRef] [PubMed]
- Amodio, G.; Gregori, S. Human tolerogenic DC-10: Perspectives for clinical applications. Transplant. Res. 2012, 1, 14. [Google Scholar] [CrossRef] [PubMed]
- Amodio, G.; Comi, M.; Tomasoni, D.; Gianolini, M.E.; Rizzo, R.; LeMaoult, J.; Roncarolo, M.G.; Gregori, S. HLA-G expression levels influence the tolerogenic activity of human DC-10. Haematologica 2015, 100, 548–557. [Google Scholar] [CrossRef] [PubMed]
- Card, C.M.; McLaren, P.J.; Wachihi, C.; Kimani, J.; Plummer, F.A.; Fowke, K.R. Decreased immune activation in resistance to HIV-1 infection is associated with an elevated frequency of CD4+CD25+FOXP3+ regulatory T cells. J. Infect. Dis. 2009, 199, 1318–1322. [Google Scholar] [CrossRef] [PubMed]
- Gagliani, N.; Magnani, C.F.; Huber, S.; Gianolini, M.E.; Pala, M.; Licona-Limon, P.; Guo, B.; Herbert, D.R.; Bulfone, A.; Trentini, F.; et al. Coexpression of CD49B and LAG-3 identifies human and mouse t regulatory type 1 cells. Nat. Med. 2013, 19, 739–746. [Google Scholar] [CrossRef] [PubMed]
- Attanasio, J.; Wherry, E.J. Costimulatory and coinhibitory receptor pathways in infectious disease. Immunity 2016, 44, 1052–1068. [Google Scholar] [CrossRef] [PubMed]
- Day, T.A.; Kublin, J.G. Lessons learned from HIV vaccine clinical efficacy trials. Curr. HIV Res. 2013, 11, 441–449. [Google Scholar] [CrossRef] [PubMed]
- Wills, S.; Hwang, K.K.; Liu, P.; Dennison, S.M.; Tay, M.Z.; Shen, X.; Pollara, J.; Lucas, J.T.; Parks, R.; Rerks-Ngarm, S.; et al. HIV-1-specific iga monoclonal antibodies from an HIV-1 vaccinee mediate galactosylceramide blocking and phagocytosis. J. Virol. 2018, 92. [Google Scholar] [CrossRef] [PubMed]
- Kim, J.H.; Excler, J.L.; Michael, N.L. Lessons from the RV144 Thai phase III HIV-1 vaccine trial and the search for correlates of protection. Annu. Rev. Med. 2015, 66, 423–437. [Google Scholar] [CrossRef] [PubMed]
- Williams, W.B.; Liao, H.X.; Moody, M.A.; Kepler, T.B.; Alam, S.M.; Gao, F.; Wiehe, K.; Trama, A.M.; Jones, K.; Zhang, R.; et al. HIV-1 vaccines. Diversion of HIV-1 vaccine-induced immunity by GP41-microbiota cross-reactive antibodies. Science 2015, 349, aab1253. [Google Scholar] [CrossRef] [PubMed]
- Kulkarni, V.; Ruprecht, R.M. Mucosal iga responses: Damaged in established HIV infection-yet, effective weapon against HIV transmission. Front. Immunol. 2017, 8, 1581. [Google Scholar] [CrossRef] [PubMed]
- Bomsel, M.; Tudor, D.; Drillet, A.S.; Alfsen, A.; Ganor, Y.; Roger, M.G.; Mouz, N.; Amacker, M.; Chalifour, A.; Diomede, L.; et al. Immunization with HIV-1 GP41 subunit virosomes induces mucosal antibodies protecting nonhuman primates against vaginal shiv challenges. Immunity 2011, 34, 269–280. [Google Scholar] [CrossRef] [PubMed]
- Sholukh, A.M.; Watkins, J.D.; Vyas, H.K.; Gupta, S.; Lakhashe, S.K.; Thorat, S.; Zhou, M.; Hemashettar, G.; Bachler, B.C.; Forthal, D.N.; et al. Defense-in-depth by mucosally administered anti-HIV dimeric IgA2 and systemic IgG1 mabs: Complete protection of rhesus monkeys from mucosal SHIV challenge. Vaccine 2015, 33, 2086–2095. [Google Scholar] [CrossRef] [PubMed]
- Watkins, J.D.; Sholukh, A.M.; Mukhtar, M.M.; Siddappa, N.B.; Lakhashe, S.K.; Kim, M.; Reinherz, E.L.; Gupta, S.; Forthal, D.N.; Sattentau, Q.J.; et al. Anti-HIV iga isotypes: Differential virion capture and inhibition of transcytosis are linked to prevention of mucosal R5 SHIV transmission. Aids 2013, 27, F13–F20. [Google Scholar] [CrossRef] [PubMed]
- Batraville, L.A.; Richard, J.; Veillette, M.; Labbe, A.C.; Alary, M.; Guedou, F.; Kaufmann, D.E.; Poudrier, J.; Finzi, A.; Roger, M. Short communication: Anti-HIV-1 envelope immunoglobulin Gs in blood and cervicovaginal samples of beninese commercial sex workers. AIDS Res. Hum. Retroviruses 2014, 30, 1145–1149. [Google Scholar] [CrossRef] [PubMed]
- Choi, R.Y.; Levinson, P.; Guthrie, B.L.; Lohman-Payne, B.; Bosire, R.; Liu, A.Y.; Hirbod, T.; Kiarie, J.; Overbaugh, J.; John-Stewart, G.; et al. Cervicovaginal HIV-1-neutralizing immunoglobulin a detected among HIV-1-exposed seronegative female partners in HIV-1-discordant couples. Aids 2012, 26, 2155–2163. [Google Scholar] [CrossRef] [PubMed]
- Seaton, K.E.; Ballweber, L.; Lan, A.; Donathan, M.; Hughes, S.; Vojtech, L.; Moody, M.A.; Liao, H.X.; Haynes, B.F.; Galloway, C.G.; et al. 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 2014, 9, e101863. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kaul, R.; Trabattoni, D.; Bwayo, J.J.; Arienti, D.; Zagliani, A.; Mwangi, F.M.; Kariuki, C.; Ngugi, E.N.; MacDonald, K.S.; Ball, T.B.; et al. HIV-1-specific mucosal iga in a cohort of HIV-1-resistant kenyan sex workers. Aids 1999, 13, 23–29. [Google Scholar] [CrossRef] [PubMed]
- Broliden, K.; Hinkula, J.; Devito, C.; Kiama, P.; Kimani, J.; Trabbatoni, D.; Bwayo, J.J.; Clerici, M.; Plummer, F.; Kaul, R. Functional HIV-1 specific iga antibodies in HIV-1 exposed, persistently igg seronegative female sex workers. Immunol. Lett. 2001, 79, 29–36. [Google Scholar] [CrossRef]
- 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, 431–432. [Google Scholar] [CrossRef] [PubMed]
- Belec, L.; Ghys, P.D.; Hocini, H.; Nkengasong, J.N.; Tranchot-Diallo, J.; Diallo, M.O.; Ettiegne-Traore, V.; Maurice, C.; Becquart, P.; Matta, M.; et al. 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. 2001, 184, 1412–1422. [Google Scholar] [CrossRef] [PubMed]
- Hocini, H.; Bomsel, M. Infectious human immunodeficiency virus can rapidly penetrate a tight human epithelial barrier by transcytosis in a process impaired by mucosal immunoglobulins. J. Infect. Dis. 1999, 179, S448–S453. [Google Scholar] [CrossRef] [PubMed]
- Kaul, R.; Rowland-Jones, S.L.; Kimani, J.; Dong, T.; Yang, H.B.; Kiama, P.; Rostron, T.; Njagi, E.; Bwayo, J.J.; MacDonald, K.S.; et al. Late seroconversion in HIV-resistant nairobi prostitutes despite pre-existing HIV-specific CD8+ responses. J. Clin. Investig. 2001, 107, 341–349. [Google Scholar] [CrossRef] [PubMed]
- Slack, E.; Balmer, M.L.; Macpherson, A.J. B cells as a critical node in the microbiota-host immune system network. Immunol. Rev. 2014, 260, 50–66. [Google Scholar] [CrossRef] [PubMed]
- Gaudet, R.G.; Breden, F.; Plummer, F.; Berry, J.D. Molecular characterization of the cervical and systemic B-cell repertoire: Unique, yet overlapping, immune compartments of an HIV-1 resistant individual. MAbs 2011, 3, 181–191. [Google Scholar] [CrossRef] [PubMed]
- Cerutti, A.; Cols, M.; Puga, I. Marginal zone B cells: Virtues of innate-like antibody-producing lymphocytes. Nat. Rev. Immunol. 2013, 13, 118–132. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Victora, G.D.; Nussenzweig, M.C. Germinal centers. Annu. Rev. Immunol. 2012, 30, 429–457. [Google Scholar] [CrossRef] [PubMed]
- Bikos, V.; Karypidou, M.; Stalika, E.; Baliakas, P.; Xochelli, A.; Sutton, L.A.; Papadopoulos, G.; Agathangelidis, A.; Papadopoulou, E.; Davis, Z.; et al. An immunogenetic signature of ongoing antigen interactions in splenic marginal zone lymphoma expressing IGHV1-2*04 receptors. Clin. Cancer Res. 2016, 22, 2032–2040. [Google Scholar] [CrossRef] [PubMed]
- Zhou, T.; Georgiev, I.; Wu, X.; Yang, Z.Y.; Dai, K.; Finzi, A.; Kwon, Y.D.; Scheid, J.F.; Shi, W.; Xu, L.; et al. Structural basis for broad and potent neutralization of HIV-1 by antibody VRC01. Science 2010, 329, 811–817. [Google Scholar] [CrossRef] [PubMed]
- He, B.; Qiao, X.; Klasse, P.J.; Chiu, A.; Chadburn, A.; Knowles, D.M.; Moore, J.P.; Cerutti, A. 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. [Google Scholar] [CrossRef] [PubMed]
- Weill, J.C.; Weller, S.; Reynaud, C.A. Human marginal zone B cells. Annu. Rev. Immunol. 2009, 27, 267–285. [Google Scholar] [CrossRef] [PubMed]
- Dosenovic, P.; Soldemo, M.; Scholz, J.L.; O’Dell, S.; Grasset, E.K.; Pelletier, N.; Karlsson, M.C.; Mascola, J.R.; Wyatt, R.T.; Cancro, M.P.; et al. Blys-mediated modulation of naive B cell subsets impacts HIV env-induced antibody responses. J. Immunol. 2012, 188, 6018–6026. [Google Scholar] [CrossRef] [PubMed]
- Moir, S.; Lapointe, R.; Malaspina, A.; Ostrowski, M.; Cole, C.E.; Chun, T.W.; Adelsberger, J.; Baseler, M.; Hwu, P.; Fauci, A.S. CD40-mediated induction of CD4 and CXCR4 on B lymphocytes correlates with restricted susceptibility to human immunodeficiency virus type 1 infection: Potential role of b lymphocytes as a viral reservoir. J. Virol. 1999, 73, 7972–7980. [Google Scholar] [PubMed]
- Moir, S.; Fauci, A.S. Insights into B cells and HIV-specific B-cell responses in HIV-infected individuals. Immunol. Rev. 2013, 254, 207–224. [Google Scholar] [CrossRef] [PubMed]
- Fontaine, J.; Chagnon-Choquet, J.; Valcke, H.S.; Poudrier, J.; Roger, M. High expression levels of B lymphocyte stimulator (blys) by dendritic cells correlate with hiv-related B-cell disease progression in humans. Blood 2011, 117, 145–155. [Google Scholar] [CrossRef] [PubMed]
- Wada, N.I.; Jacobson, L.P.; Margolick, J.B.; Breen, E.C.; Macatangay, B.; Penugonda, S.; Martinez-Maza, O.; Bream, J.H. The effect of HAART-induced HIV suppression on circulating markers of inflammation and immune activation. Aids 2015, 29, 463–471. [Google Scholar] [CrossRef] [PubMed]
- Chagnon-Choquet, J.; Gauvin, J.; Roger, J.; Fontaine, J.; Poudrier, J.; Roger, M. HIV nef promotes expression of B-lymphocyte stimulator by blood dendritic cells during HIV infection in humans. J. Infect. Dis. 2015, 211, 1229–1240. [Google Scholar] [CrossRef] [PubMed]
- Gomez, A.M.; Ouellet, M.; Tremblay, M.J. HIV-1-triggered release of type I IFN by plasmacytoid dendritic cells induces BAFF production in monocytes. J. Immunol. 2015, 194, 2300–2308. [Google Scholar] [CrossRef] [PubMed]
- Sjostrand, M.; Johansson, A.; Aqrawi, L.; Olsson, T.; Wahren-Herlenius, M.; Espinosa, A. The expression of baff is controlled by irf transcription factors. J. Immunol. 2016, 196, 91–96. [Google Scholar] [CrossRef] [PubMed]
- Chu, V.T.; Enghard, P.; Riemekasten, G.; Berek, C. In vitro and in vivo activation induces BAFF and april expression in B cells. J. Immunol. 2007, 179, 5947–5957. [Google Scholar] [CrossRef] [PubMed]
- Sabourin-Poirier, C.; Fourcade, L.; Chagnon-Choquet, J.; Labbe, A.C.; Alary, M.; Guedou, F.; Poudrier, J.; Roger, M. Blood B lymphocyte stimulator (BLYS)/BAFF levels may reflect natural immunity to HIV in highly exposed uninfected Beninese commercial sex workers. Sci. Rep. 2016, 6, 32318. [Google Scholar] [CrossRef] [PubMed]
- Varin, M.M.; Le Pottier, L.; Youinou, P.; Saulep, D.; Mackay, F.; Pers, J.O. B-cell tolerance breakdown in Sjogren’s syndrome: Focus on BAFF. Autoimmun. Rev. 2010, 9, 604–608. [Google Scholar] [CrossRef] [PubMed]
- Borhis, G.; Richard, Y. Subversion of the B-cell compartment during parasitic, bacterial, and viral infections. BMC Immunol. 2015, 16, 15. [Google Scholar] [CrossRef] [PubMed]
- Gauvin, J.; Chagnon-Choquet, J.; Poudrier, J.; Roger, M. Fluctuations in blood marginal zone B-cell frequencies may reflect migratory patterns associated with HIV-1 disease progression status. PLoS ONE 2016, 11, e0155868. [Google Scholar] [CrossRef] [PubMed]
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Fourcade, L.; Poudrier, J.; Roger, M. Natural Immunity to HIV: A Template for Vaccine Strategies. Viruses 2018, 10, 215. https://doi.org/10.3390/v10040215
Fourcade L, Poudrier J, Roger M. Natural Immunity to HIV: A Template for Vaccine Strategies. Viruses. 2018; 10(4):215. https://doi.org/10.3390/v10040215
Chicago/Turabian StyleFourcade, Lyvia, Johanne Poudrier, and Michel Roger. 2018. "Natural Immunity to HIV: A Template for Vaccine Strategies" Viruses 10, no. 4: 215. https://doi.org/10.3390/v10040215