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Current Immunology Reviews (Discontinued)

Editor-in-Chief

ISSN (Print): 1573-3955
ISSN (Online): 1875-631X

Review Article

Mucosal Vaccine Approaches for Prevention of HIV and SIV Transmission

Author(s): Pamela A. Kozlowski and Anna Aldovini*

Volume 15, Issue 1, 2019

Page: [102 - 122] Pages: 21

DOI: 10.2174/1573395514666180605092054

Abstract

Optimal protective immunity to HIV will likely require that plasma cells, memory B cells and memory T cells be stationed in mucosal tissues at portals of viral entry. Mucosal vaccine administration is more effective than parenteral vaccine delivery for this purpose. The challenge has been to achieve efficient vaccine uptake at mucosal surfaces, and to identify safe and effective adjuvants, especially for mucosally administered HIV envelope protein immunogens. Here, we discuss strategies used to deliver potential HIV vaccine candidates in the intestine, respiratory tract, and male and female genital tract of humans and nonhuman primates. We also review mucosal adjuvants, including Toll-like receptor agonists, which may adjuvant both mucosal humoral and cellular immune responses to HIV protein immunogens.

Keywords: HIV, SIV, nonhuman primates, mucosal adjuvants, rectal, vaginal, oral, nasal immunization TLR agonists, vaccine vectors, delivery vehicles.

[1]
Brenchley JM, Schacker TW, Ruff LE, et al. CD4+ T cell depletion during all stages of HIV disease occurs predominantly in the gastrointestinal tract. J Exp Med 2004; 200(6): 749-59.
[2]
Li Q, Duan L, Estes JD, et al. Peak SIV replication in resting memory CD4+ T cells depletes gut lamina propria CD4+ T cells. Nature 2005; 434(7037): 1148-52.
[3]
Mehandru S, Poles MA, Tenner-Racz K, et al. Primary HIV-1 infection is associated with preferential depletion of CD4+ T lymphocytes from effector sites in the gastrointestinal tract. J Exp Med 2004; 200(6): 761-70.
[4]
Santangelo PJ, Rogers KA, Zurla C, et al. Whole-body immunoPET reveals active SIV dynamics in viremic and antiretroviral therapy-treated macaques. Nat Methods 2015; 12(5): 427-32.
[5]
Xu H, Wang X, Veazey RS. Mucosal immunology of HIV infection. Immunol Rev 2013; 254(1): 10-33.
[6]
Chenine AL, Siddappa NB, Kramer VG, et al. Relative transmissibility of an R5 clade C simian-human immunodeficiency virus across different mucosae in macaques parallels the relative risks of sexual HIV-1 transmission in humans via different routes. J Infect Dis 2010; 201(8): 1155-63.
[7]
Keele BF, Estes JD. Barriers to mucosal transmission of immunodeficiency viruses. Blood 2011; 118(4): 839-46.
[8]
Haase AT. Early events in sexual transmission of HIV and SIV and opportunities for interventions. Annu Rev Med 2011; 62: 127-39.
[9]
Miller CJ, Li Q, Abel K, et al. Propagation and dissemination of infection after vaginal transmission of simian immunodeficiency virus. J Virol 2005; 79(14): 9217-27.
[10]
Adnan S, Reeves RK, Gillis J, et al. Persistent low-level replication of SIV Delta nef drives maturation of antibody and CD8 T cell responses to induce protective immunity against vaginal SIV infection. PLoS Pathog 2016; 12(12): e1006104.
[11]
Neutra MR, Kozlowski PA. Mucosal vaccines: The promise and the challenge. Nat Rev Immunol 2006; 6(2): 148-58.
[12]
Kutzler MA, Weiner DB. DNA vaccines: Ready for prime time? Nat Rev Genet 2008; 9(10): 776-88.
[13]
Lin IY, Van TT, Smooker PM. Live-attenuated bacterial vectors: Tools for vaccine and therapeutic agent delivery. Vaccines (Basel) 2015; 3(4): 940-72.
[14]
Unnikrishnan M, Rappuoli R, Serruto D. Recombinant bacterial vaccines. Curr Opin Immunol 2012; 24(3): 337-42.
[15]
Parks CL, Picker LJ, King CR. Development of replication-competent viral vectors for HIV vaccine delivery. Curr Opin HIV AIDS 2013; 8(5): 402-11.
[16]
Cao X. Self-regulation and cross-regulation of pattern-recognition receptor signalling in health and disease. Nat Rev Immunol 2016; 16(1): 35-50.
[17]
O’Neill LA, Golenbock D, Bowie AG. The history of Toll-like receptors-redefining innate immunity. Nat Rev Immunol 2013; 13(6): 453-60.
[18]
Kumar H, Kawai T, Akira S. Pathogen recognition by the innate immune system. Int Rev Immunol 2011; 30(1): 16-34.
[19]
Fukata M, Abreu MT. TLR4 signalling in the intestine in health and disease. Biochem Soc Trans 2007; 35(Pt 6): 1473-8.
[20]
Oh JZ, Ravindran R, Chassaing B, et al. TLR5-mediated sensing of gut microbiota is necessary for antibody responses to seasonal influenza vaccination. Immunity 2014; 41(3): 478-92.
[21]
Bauer S, Pigisch S, Hangel D, Kaufmann A, Hamm S. Recognition of nucleic acid and nucleic acid analogs by Toll-like receptors 7, 8 and 9. Immunobiology 2008; 213(3-4): 315-28.
[22]
Kotton CN, Hohmann EL. Enteric pathogens as vaccine vectors for foreign antigen delivery. Infect Immun 2004; 72(10): 5535-47.
[23]
Binet R, Letoffe S, Ghigo JM, Delepelaire P, Wandersman C. Protein secretion by Gram-negative bacterial ABC exporters--a review. Gene 1997; 192(1): 7-11.
[24]
Hahn HP, von Specht BU. Secretory delivery of recombinant proteins in attenuated Salmonella strains: Potential and limitations of Type I protein transporters. FEMS Immunol Med Microbiol 2003; 37(2-3): 87-98.
[25]
Chin’ombe N, Bourn WR, Williamson AL, Shephard EG. Oral vaccination with a recombinant Salmonella vaccine vector provokes systemic HIV-1 subtype C Gag-specific CD4+ Th1 and Th2 cell immune responses in mice. Virol J 2009; 6: 87-96.
[26]
Evans DT, Chen LM, Gillis J, et al. Mucosal priming of simian immunodeficiency virus-specific cytotoxic T-lymphocyte responses in rhesus macaques by the Salmonella type III secretion antigen delivery system. J Virol 2003; 77(4): 2400-9.
[27]
Fouts TR, Tuskan RG, Chada S, Hone DM, Lewis GK. Construction and immunogenicity of Salmonella typhimurium vaccine vectors that express HIV-1 gp120. Vaccine 1995; 13(17): 1697-705.
[28]
Franchini G, Robert-Guroff M, Tartaglia J, et al. Highly attenuated HIV type 2 recombinant poxviruses, but not HIV-2 recombinant Salmonella vaccines, induce long-lasting protection in rhesus macaques. AIDS Res Hum Retroviruses 1995; 11(8): 909-20.
[29]
Shata MT, Reitz MS Jr, DeVico AL, Lewis GK, Hone DM. Mucosal and systemic HIV-1 Env-specific CD8(+) T-cells develop after intragastric vaccination with a Salmonella Env DNA vaccine vector. Vaccine 2001; 20(3-4): 623-9.
[30]
Vecino WH, Morin PM, Agha R, Jacobs WR Jr, Fennelly GJ. Mucosal DNA vaccination with highly attenuated Shigella is superior to attenuated Salmonella and comparable to intramuscular DNA vaccination for T cells against HIV. Immunol Lett 2002; 82(3): 197-204.
[31]
Brichacek B, Lagenaur LA, Lee PP, Venzon D, Hamer DH. In vivo evaluation of safety and toxicity of a Lactobacillus jensenii producing modified cyanovirin-N in a rhesus macaque vaginal challenge model. PLoS One 2013; 8(11): e78817.
[32]
Lagenaur LA, Sanders-Beer BE, et al. Prevention of vaginal SHIV transmission in macaques by a live recombinant Lactobacillus. Mucosal Immunol 2011; 4(6): 648-57.
[33]
Aldovini A, Young RA. Development of a BCG recombinant vehicle for candidate AIDS vaccines. Int Rev Immunol 1990; 7(1): 79-83.
[34]
Aldovini A, Young RA. Humoral and cell-mediated immune responses to live recombinant BCG-HIV vaccines. Nature 1991; 351(6326): 479-82.
[35]
Jensen K, Pena MG, Wilson RL, et al. A neonatal oral Mycobacterium tuberculosis-SIV prime / intramuscular MVA-SIV boost combination vaccine induces both SIV and Mtb-specific immune responses in infant macaques. Trials Vaccinol 2013; 2: 53-63.
[36]
Jensen K, Nabi R, Van Rompay KK Jr, et al. Vaccine-elicited mucosal and systemic antibody responses are associated with reduced simian immunodeficiency viremia in infant rhesus macaques. J Virol 2016; 90(16): 7285-302.
[37]
Gasper MA, Hesseling AC, Mohar I, et al. BCG vaccination induces HIV target cell activation in HIV-exposed infants in a randomized trial. J Clin Invest Insight 2017; 2(7): e91963.
[38]
Jensen K, Dela Pena-Ponce MG, Piatak M Jr, et al. Balancing trained immunity with persistent immune activation and the risk of simian immunodeficiency virus infection in infant macaques vaccinated with attenuated Mycobacterium tuberculosis or Mycobacterium bovis BCG vaccine. Clin Vaccine Immunol 2017; 24(1): e00360.
[39]
Schnell MJ. Viral vectors as potential HIV-1 vaccines. FEMS Microbiol Lett 2001; 200(2): 123-9.
[40]
Pegu P, Vaccari M, Gordon S, et al. Antibodies with high avidity to the gp120 envelope protein in protection from simian immunode
ficiency virus SIV(mac251) acquisition in an immunization regimen that mimics the RV-144 Thai trial. J Virol 2013; 87(3): 1708-19.
[41]
Price PJ, Torres-Dominguez LE, Brandmuller C, Sutter G, Lehmann MH. Modified vaccinia virus Ankara: innate immune activation and induction of cellular signalling. Vaccine 2013; 31(39): 4231-4.
[42]
Rerks-Ngarm S, Pitisuttithum P, Nitayaphan S, et al. Vaccination with ALVAC and AIDSVAX to prevent HIV-1 infection in Thailand. N Engl J Med 2009; 361(23): 2209-20.
[43]
Teigler JE, Phogat S, Franchini G, Hirsch VM, Michael NL, Barouch DH. The canarypox virus vector ALVAC induces distinct cytokine responses compared to the vaccinia virus-based vectors MVA and NYVAC in rhesus monkeys. J Virol 2014; 88(3): 1809-14.
[44]
Kent SJ, Dale CJ, Ranasinghe C, et al. Mucosally-administered human-simian immunodeficiency virus DNA and fowlpoxvirus-based recombinant vaccines reduce acute phase viral replication in macaques following vaginal challenge with CCR5-tropic SHIVSF162P3. Vaccine 2005; 23(42): 5009-21.
[45]
Lai L, Kwa SF, Kozlowski PA, et al. SIVmac239 MVA vaccine with and without a DNA prime, similar prevention of infection by a repeated dose SIVsmE660 challenge despite different immune responses. Vaccine 2012; 30(9): 1737-45.
[46]
Manrique M, Kozlowski PA, Cobo-Molinos A, et al. Resistance to infection, early and persistent suppression of simian immunode
ficiency virus SIVmac251 viremia, and significant reduction of tissue viral burden after mucosal vaccination in female rhesus macaques. J Virol 2014; 88(1): 212-24.
[47]
Manrique M, Kozlowski PA, Wang SW, et al. Nasal DNA-MVA SIV vaccination provides more significant protection from progression to AIDS than a similar intramuscular vaccination. Mucosal Immunol 2009; 2(6): 536-50.
[48]
Munseri PJ, Kroidl A, Nilsson C, et al. Priming with a simplified intradermal HIV-1 DNA vaccine regimen followed by boosting with recombinant HIV-1 MVA vaccine is safe and immunogenic: A phase IIa randomized clinical trial. PLoS One 2015; 10(4): e0119629.
[49]
Bertley FM, Kozlowski PA, Wang SW, et al. Control of simian/human immunodeficiency virus viremia and disease progression after IL-2-augmented DNA-modified vaccinia virus Ankara nasal vaccination in nonhuman primates. J Immunol 2004; 172(6): 3745-57.
[50]
Manrique M, Kozlowski PA, Cobo-Molinos A, et al. Immunogenicity of a vaccine regimen composed of simian immunodeficiency virus DNA, rMVA, and viral particles administered to female rhesus macaques via four different mucosal routes. J Virol 2013; 87(8): 4738-50.
[51]
Manrique M, Kozlowski PA, Cobo-Molinos A, et al. Long-term control of simian immunodeficiency virus mac251 viremia to undetectable levels in half of infected female rhesus macaques nasally vaccinated with simian immunodeficiency virus DNA/recombinant modified vaccinia virus Ankara. J Immunol 2011; 186(6): 3581-93.
[52]
Manrique M, Micewicz E, Kozlowski PA, et al. DNA-MVA vaccine protection after X4 SHIV challenge in macaques correlates with day-of-challenge antiviral CD4+ cell-mediated immunity levels and postchallenge preservation of CD4+ T cell memory. AIDS Res Hum Retroviruses 2008; 24(3): 505-19.
[53]
Emmer KL, Wieczorek L, Tuyishime S, Molnar S, Polonis VR, Ertl HC. Antibody responses to prime-boost vaccination with an HIV-1 gp145 envelope protein and chimpanzee adenovirus vectors expressing HIV-1 gp140. AIDS 2016; 30(16): 2405-14.
[54]
Cheng C, Wang L, Ko SY, et al. Combination recombinant simian or chimpanzee adenoviral vectors for vaccine development. Vaccine 2015; 33(51): 7344-51.
[55]
Brocca-Cofano E, McKinnon K, Demberg T, et al. Vaccine-elicited SIV and HIV envelope-specific IgA and IgG memory B cells in rhesus macaque peripheral blood correlate with functional antibody responses and reduced viremia. Vaccine 2011; 29(17): 3310-9.
[56]
Demberg T, Florese RH, Heath MJ, et al. A replication-competent adenovirus-human immunodeficiency virus (Ad-HIV) tat and Ad-HIV env priming/Tat and envelope protein boosting regimen elicits enhanced protective efficacy against simian/human immunodeficiency virus SHIV89.6P challenge in rhesus macaques. J Virol 2007; 81(7): 3414-27.
[57]
Hidajat R, Xiao P, Zhou Q, et al. Correlation of vaccine-elicited systemic and mucosal nonneutralizing antibody activities with reduced acute viremia following intrarectal simian immunodeficiency virus SIVmac251 challenge of rhesus macaques. J Virol 2009; 83(2): 791-801.
[58]
Lakhashe SK, Velu V, Sciaranghella G, et al. Prime-boost vaccination with heterologous live vectors encoding SIV gag and multimeric HIV-1 gp160 protein: Efficacy against repeated mucosal R5 clade C SHIV challenges. Vaccine 2011; 29(34): 5611-22.
[59]
Patterson LJ, Robert-Guroff M. Replicating adenovirus vector prime/protein boost strategies for HIV vaccine development. Expert Opin Biol Ther 2008; 8(9): 1347-63.
[60]
Xiao P, Zhao J, Patterson LJ, et al. Multiple vaccine-elicited nonneutralizing antienvelope antibody activities contribute to protective efficacy by reducing both acute and chronic viremia following simian/human immunodeficiency virus SHIV89.6P challenge in rhesus macaques. J Virol 2011; 84(14): 7161-73.
[61]
Xiao P, Patterson LJ, Kuate S, et al. Replicating adenovirus-simian immunodeficiency virus (SIV) recombinant priming and envelope protein boosting elicits localized, mucosal IgA immunity in rhesus macaques correlated with delayed acquisition following a repeated low-dose rectal SIV(mac251) challenge. J Virol 2012; 86(8): 4644-57.
[62]
Valentin A, McKinnon K, Li J, et al. Comparative analysis of SIV-specific cellular immune responses induced by different vaccine platforms in rhesus macaques. Clin Immunol 2014; 155(1): 91-107.
[63]
Hansen SG, Ford JC, Lewis MS, et al. Profound early control of highly pathogenic SIV by an effector memory T-cell vaccine. Nature 2011; 473(7348): 523-7.
[64]
Hansen SG, Jr MP, Ventura AB, Hughes CM, et al. Immune clearance of highly pathogenic SIV infection. Nature 2013; 502(7469): 100-4.
[65]
Hansen SG, Sacha JB, Hughes CM, et al. Cytomegalovirus vectors violate CD8+ T cell epitope recognition paradigms. Science 2013; 340(6135): e1237874.
[66]
Traina-Dorge V, Pahar B, Marx P, et al. Recombinant varicella vaccines induce neutralizing antibodies and cellular immune responses to SIV and reduce viral loads in immunized rhesus macaques. Vaccine 2010; 28(39): 6483-90.
[67]
Crotty S, Lohman BL, Lu FX, Tang S, Miller CJ, Andino R. Mucosal immunization of cynomolgus macaques with two serotypes of live poliovirus vectors expressing simian immunodeficiency virus antigens: stimulation of humoral, mucosal, and cellular immunity. J Virol 1999; 73(11): 9485-95.
[68]
Crotty S, Miller CJ, Lohman BL, et al. Protection against simian immunodeficiency virus vaginal challenge by using Sabin poliovirus vectors. J Virol 2001; 75(16): 7435-52.
[69]
Marthas ML, Van Rompay KK, Abbott Z, et al. Partial efficacy of a VSV-SIV/MVA-SIV vaccine regimen against oral SIV challenge in infant macaques. Vaccine 2011; 29(17): 3124-37.
[70]
Schell JB, Bahl K, Folta-Stogniew E, et al. Antigenic requirement for Gag in a vaccine that protects against high-dose mucosal challenge with simian immunodeficiency virus. Virology 2015; 476: 405-12.
[71]
Sharpe S, Polyanskaya N, Dennis M, et al. Induction of Simian Immunodeficiency Virus (SIV)-specific CTL in rhesus macaques by vaccination with modified vaccinia virus Ankara expressing SIV transgenes: Influence of pre-existing anti-vector immunity. J Gen Virol 2001; 82(Pt 9): 2215-23.
[72]
Kannanganat S, Nigam P, Velu V, et al. Preexisting vaccinia virus immunity decreases SIV-specific cellular immunity but does not diminish humoral immunity and efficacy of a DNA/MVA vaccine. J Immunol 2010; 185(12): 7262-73.
[73]
Priddy FH, Brown D, Kublin J, et al. Safety and immunogenicity of a replication-incompetent adenovirus type 5 HIV-1 clade B gag/pol/nef vaccine in healthy adults. Clin Infect Dis 2008; 46(11): 1769-81.
[74]
Frey SE, Lottenbach KR, Hill H, et al. A Phase I, dose-escalation trial in adults of three recombinant attenuated Salmonella Typhi vaccine vectors producing Streptococcus pneumoniae surface protein antigen PspA. Vaccine 2013; 31(42): 4874-80.
[75]
Kantele A, Kantele JM, Arvilommi H, Makela PH. Active immunity is seen as a reduction in the cell response to oral live vaccine. Vaccine 1991; 9(6): 428-31.
[76]
Bolton DL, Santra S, Swett-Tapia C, et al. Priming T-cell responses with recombinant measles vaccine vector in a heterologous prime-boost setting in non-human primates. Vaccine 2012; 30(41): 5991-8.
[77]
Tatsis N, Lasaro MO, Lin SW, et al. Adenovirus vector-induced immune responses in nonhuman primates: responses to prime boost regimens. J Immunol 2009; 182(10): 6587-99.
[78]
Sauermann U, Radaelli A, Stolte-Leeb N, et al. Vector order determines protection against pathogenic simian immunodeficiency virus infection in a triple component vaccine by balancing CD4(+) and CD8(+) T-cell responses. J Virol 2017; pii: JVI.01120-17.
[79]
Koup RA, Roederer M, Lamoreaux L, et al. Priming immunization with DNA augments immunogenicity of recombinant adenoviral vectors for both HIV-1 specific antibody and T-cell responses. PLoS One 2010; 5(2): e9015.
[80]
Clarke DK, Hendry RM, Singh V, et al. Live virus vaccines based on a Vesicular Stomatitis Virus (VSV) backbone: Standardized template with key considerations for a risk/benefit assessment. Vaccine 2016; 34(51): 6597-609.
[81]
Liu MA. DNA vaccines: A review. J Intern Med 2003; 253(4): 402-10.
[82]
Boyer JD, Chattergoon MA, Ugen KE, et al. Enhancement of cellular immune response in HIV-1 seropositive individuals: A DNA-based trial. Clin Immunol 1999; 90(1): 100-7.
[83]
Calarota S, Bratt G, Nordlund S, et al. Cellular cytotoxic response induced by DNA vaccination in HIV-1-infected patients. Lancet 1998; 351(9112): 1320-5.
[84]
MacGregor RR, Boyer JD, Ugen KE, et al. First human trial of a DNA-based vaccine for treatment of human immunodeficiency virus type 1 infection: Safety and host response. J Infect Dis 1998; 178(1): 92-100.
[85]
Haigwood NL, Pierce CC, Robertson MN, et al. Protection from pathogenic SIV challenge using multigenic DNA vaccines. Immunol Lett 1999; 66(1-3): 183-8.
[86]
Lu S, Arthos J, Montefiori DC, et al. Simian immunodeficiency virus DNA vaccine trial in macaques. J Virol 1996; 70(6): 3978-91.
[87]
Robinson HL, Montefiori DC, Johnson RP, et al. Neutralizing antibody-independent containment of immunodeficiency virus challenges by DNA priming and recombinant pox virus booster immunizations. Nat Med 1999; 5(5): 526-34.
[88]
Wang SW, Kozlowski PA, Schmelz G, et al. Effective induction of simian immunodeficiency virus-specific systemic and mucosal immune responses in primates by vaccination with proviral DNA producing intact but noninfectious virions. J Virol 2000; 74(22): 10514-22.
[89]
Felber BK, Valentin A, Rosati M, Bergamaschi C, Pavlakis GN. HIV DNA vaccine: stepwise improvements make a difference. Vaccines (Basel) 2014; 2(2): 354-79.
[90]
Iyer SS, Amara RR. DNA/MVA Vaccines for HIV/AIDS. Vaccines (Basel) 2014; 2(1): 160-78.
[91]
Kulkarni V, Rosati M, Bear J, et al. Comparison of intradermal and intramuscular delivery followed by in vivo electroporation of SIV Env DNA in macaques. Hum Vaccin Immunother 2013; 9(10): 2081-94.
[92]
Kulkarni V, Rosati M, Jalah R, et al. DNA vaccination by intradermal electroporation induces long-lasting immune responses in Rhesus macaques. J Med Primatol 2014; 43(5): 329-40.
[93]
Li J, Valentin A, Kulkarni V, et al. HIV/SIV DNA vaccine combined with protein in a co-immunization protocol elicits highest humoral responses to envelope in mice and macaques. Vaccine 2013; 31(36): 3747-55.
[94]
Lindsay RW, Ouellette I, Arendt HE, et al. SIV antigen-specific effects on immune responses induced by vaccination with DNA electroporation and plasmid IL-12. Vaccine 2013; 31(42): 4749-58.
[95]
Muthumani K, Bagarazzi M, Conway D, et al. A Gag-Pol/Env-Rev SIV239 DNA vaccine improves CD4 counts, and reduce viral loads after pathogenic intrarectal SIV(mac)251 challenge in Rhesus macaques. Vaccine 2003; 21(7-8): 629-37.
[96]
Muthumani K, Kudchodkar S, Zhang D, et al. Issues for improving multiplasmid DNA vaccines for HIV-1. Vaccine 2002; 20(15): 1999-2003.
[97]
Patel V, Jalah R, Kulkarni V, et al. DNA and virus particle vaccination protects against acquisition and confers control of viremia upon heterologous simian immunodeficiency virus challenge. Proc Natl Acad Sci USA 2013; 110(8): 2975-80.
[98]
Rosati M, Bergamaschi C, et al. DNA vaccination in rhesus macaques induces potent immune responses and decreases acute and chronic viremia after SIVmac251 challenge. Proc Natl Acad Sci USA 2009; 106(37): 15831-6.
[99]
Boyer JD, Robinson TM, Maciag PC, et al. DNA prime Listeria boost induces a cellular immune response to SIV antigens in the rhesus macaque model that is capable of limited suppression of SIV239 viral replication. Virology 2005; 333(1): 88-101.
[100]
Kwissa M, Amara RR, Robinson HL, et al. Adjuvanting a DNA vaccine with a TLR9 ligand plus FLT3 ligand results in enhanced cellular immunity against the simian immunodeficiency virus. J Exp Med 2007; 204(11): 2733-46.
[101]
Lai L, Kwa S, Kozlowski PA, et al. Prevention of infection by a granulocyte-macrophage colony-stimulating factor co-expressing DNA/modified vaccinia Ankara simian immunodeficiency virus vaccine. J Infect Dis 2011; 204(1): 164-73.
[102]
Lai L, Vodros D, Kozlowski PA, et al. GM-CSF DNA: An adjuvant for higher avidity IgG, rectal IgA, and increased protection against the acute phase of a SHIV-89.6P challenge by a DNA/MVA immunodeficiency virus vaccine. Virology 2007; 369(1): 153-67.
[103]
Liu J, Kjeken R, Mathiesen I, Barouch DH. Recruitment of antigen-presenting cells to the site of inoculation and augmentation of human immunodeficiency virus type 1 DNA vaccine immunogenicity by in vivo electroporation. J Virol 2008; 82(11): 5643-9.
[104]
Rosati M, Valentin A, Jalah R, et al. Increased immune responses in rhesus macaques by DNA vaccination combined with electroporation. Vaccine 2008; 26(40): 5223-9.
[105]
Kichaev G, Mendoza JM, Amante D, et al. Electroporation mediated DNA vaccination directly to a mucosal surface results in improved immune responses. Hum Vaccin Immunother 2013; 9(10): 2041-8.
[106]
Mestecky J, Russell MW, Elson CO. Perspectives on mucosal vaccines: is mucosal tolerance a barrier? J Immunol 2007; 179(9): 5633-8.
[107]
Coquet JM, Rausch L, Borst J. The importance of co-stimulation in the orchestration of T helper cell differentiation. Immunol Cell Biol 2015; 93(9): 780-8.
[108]
Schmitt N, Ueno H. Regulation of human helper T cell subset differentiation by cytokines. Curr Opin Immunol 2015; 34: 130-6.
[109]
Coffman RL, Sher A, Seder RA. Vaccine adjuvants: Putting innate immunity to work. Immunity 2010; 33(4): 492-503.
[110]
Hirota K, Turner JE, Villa M, et al. Plasticity of Th17 cells in Peyer’s patches is responsible for the induction of T cell-dependent IgA responses. Nat Immunol 2013; 14(4): 372-9.
[111]
Cao AT, Yao S, Gong B, Nurieva RI, Elson CO, Cong Y. Interleukin (IL)-21 promotes intestinal IgA response to microbiota. Mucosal Immunol 2015; 8(5): 1072-82.
[112]
Dann SM, Manthey CF, Le C, et al. IL-17A promotes protective IgA responses and expression of other potential effectors against the lumen-dwelling enteric parasite Giardia. Exp Parasitol 2015; 156: 68-78.
[113]
Christensen D, Mortensen R, Rosenkrands I, Dietrich J, Andersen P. Vaccine-induced Th17 cells are established as resident memory cells in the lung and promote local IgA responses. Mucosal Immunol 2017; 10(1): 260-70.
[114]
Smith PD, Smythies LE, Shen R, Greenwell-Wild T, Gliozzi M, Wahl SM. Intestinal macrophages and response to microbial encroachment. Mucosal Immunol 2011; 4(1): 31-42.
[115]
Moens L, Tangye SG. Cytokine-mediated regulation of plasma cell generation: IL-21 takes center stage. Front Immunol 2014; 5(article 65): 1-13.
[116]
DePaolo RW, Kamdar K, Khakpour S, Sugiura Y, Wang W, Jabri B. A specific role for TLR1 in protective T(H)17 immunity during mucosal infection. J Exp Med 2012; 209(8): 1437-44.
[117]
Gallorini S, Taccone M, Bonci A, et al. Sublingual immunization with a subunit influenza vaccine elicits comparable systemic immune response as intramuscular immunization, but also induces local IgA and TH17 responses. Vaccine 2014; 32(20): 2382-8.
[118]
Orr MT, Beebe EA, Hudson TE, et al. Mucosal delivery switches the response to an adjuvanted tuberculosis vaccine from systemic TH1 to tissue-resident TH17 responses without impacting the protective efficacy. Vaccine 2015; 33(48): 6570-8.
[119]
Douagi I, Gujer C, Sundling C, et al. Human B cell responses to TLR ligands are differentially modulated by myeloid and plasmacytoid dendritic cells. J Immunol 2009; 182(4): 1991-2001.
[120]
Soloff AC, Barratt-Boyes SM. Enemy at the gates: Dendritic cells and immunity to mucosal pathogens. Cell Res 2010; 20(8): 872-85.
[121]
McClure R, Massari P. TLR-dependent human mucosal epithelial cell responses to microbial pathogens. Front Immunol 2014; 5: 386-99.
[122]
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(6): 1584-95.
[123]
Dennis EA, Robinson TO, Smythies LE, Smith PD. Characterization of human blood monocytes and intestinal macrophages Curr Protoc Immunol 2017; 118(143): 1-14
[124]
Wira CR, Fahey JV, Sentman CL, Pioli PA, Shen L. Innate and adaptive immunity in female genital tract: Cellular responses and interactions. Immunol Rev 2005; 206: 306-35.
[125]
Herbst-Kralovetz MM, Quayle AJ, Ficarra M, et al. Quantification and comparison of toll-like receptor expression and responsiveness in primary and immortalized human female lower genital tract epithelia. Am J Reprod Immunol 2008; 59(3): 212-24.
[126]
Joachim A, Bauer A, Joseph S, et al. Boosting with subtype C CN54rgp140 protein adjuvanted with glucopyranosyl lipid adjuvant after priming with HIV-DNA and HIV-MVA Is safe and enhances immune responses: a phase I trial. PLoS One 2016; 11(5): e0155702.
[127]
Kasturi SP, Kozlowski PA, Nakaya HI, et al. Adjuvanting a simian immunodeficiency virus vaccine with Toll-like receptor ligands encapsulated in nanoparticles induces persistent antibody responses and enhanced protection in TRIM5alpha restrictive macaques. J Virol 2017; 91(4): e01844.
[128]
Moody MA, Santra S, Vandergrift NA, et al. Toll-like receptor 7/8 (TLR7/8) and TLR9 agonists cooperate to enhance HIV-1 envelope antibody responses in rhesus macaques. J Virol 2014; 88(6): 3329-39.
[129]
Wille-Reece U, Flynn BJ, Lore K, et al. HIV Gag protein conjugated to a Toll-like receptor 7/8 agonist improves the magnitude and quality of Th1 and CD8+ T cell responses in nonhuman primates. Proc Natl Acad Sci USA 2005; 102(42): 15190-4.
[130]
Wille-Reece U, Flynn BJ, Lore K, et al. Toll-like receptor agonists influence the magnitude and quality of memory T cell responses after prime-boost immunization in nonhuman primates. J Exp Med 2006; 203(5): 1249-58.
[131]
Park H, Adamson L, Ha T, et al. Polyinosinic-polycytidylic acid is the most effective TLR adjuvant for SIV Gag protein-induced T cell responses in nonhuman primates. J Immunol 2013; 190(8): 4103-15.
[132]
Bekeredjian-Ding I, Jego G. Toll-like receptors: Sentries in the B-cell response. Immunology 2009; 128(3): 311-23.
[133]
Kabelitz D. Expression and function of Toll-like receptors in T lymphocytes. Curr Opin Immunol 2007; 19(1): 39-45.
[134]
Manicassamy S, Pulendran B. Modulation of adaptive immunity with Toll-like receptors. Semin Immunol 2009; 21(4): 185-93.
[135]
Gujer C, Sundling C, Seder RA, Karlsson Hedestam GB, Lore K. Human and rhesus plasmacytoid dendritic cell and B-cell responses to Toll-like receptor stimulation. Immunology 2011; 134(3): 257-69.
[136]
Jesudason S, Collins MG, Rogers NM, Kireta S, Coates PT. Non-human primate dendritic cells. J Leukoc Biol 2012; 91(2): 217-28.
[137]
Ketloy C, Engering A, Srichairatanakul U, et al. Expression and function of Toll-like receptors on dendritic cells and other antigen presenting cells from non-human primates. Vet Immunol Immunopathol 2008; 125(1-2): 18-30.
[138]
Thompson EA, Lore K. Non-human primates as a model for understanding the mechanism of action of toll-like receptor-based vaccine adjuvants. Curr Opin Immunol 2017; 47: 1-7.
[139]
Kwissa M, Nakaya HI, Oluoch H, Pulendran B. Distinct TLR adjuvants differentially stimulate systemic and local innate immune responses in nonhuman primates. Blood 2012; 119(9): 2044-55.
[140]
Basto AP, Leitao A. Targeting TLR2 for vaccine development. J Immunol Res 2014; 2014(article 619410): 1-22.
[141]
Veazey RS, Siddiqui A, Klein K, et al. Evaluation of mucosal adjuvants and immunization routes for the induction of systemic and mucosal humoral immune responses in macaques. Hum Vaccin Immunother 2015; 11(12): 2913-22.
[142]
Buffa V, Klein K, Fischetti L, Shattock RJ. Evaluation of TLR agonists as potential mucosal adjuvants for HIV gp140 and tetanus toxoid in mice. PLoS One 2012; 7(12): e50529.
[143]
Morgan ME, Koelink PJ, Zheng B, et al. Toll-like receptor 6 stimulation promotes T-helper 1 and 17 responses in gastrointestinal-associated lymphoid tissue and modulates murine experimental colitis. Mucosal Immunol 2014; 7(5): 1266-77.
[144]
Moreira AP, Cavassani KA, Ismailoglu UB, et al. The protective role of TLR6 in a mouse model of asthma is mediated by IL-23 and IL-17A. J Clin Invest 2011; 121(11): 4420-32.
[145]
Zhang X, Chentoufi AA, Dasgupta G, et al. A genital tract peptide epitope vaccine targeting TLR-2 efficiently induces local and systemic CD8+ T cells and protects against herpes simplex virus type 2 challenge. Mucosal Immunol 2009; 2(2): 129-43.
[146]
De Smet R, Demoor T, Verschuere S, et al. Beta-Glucan microparticles are good candidates for mucosal antigen delivery in oral vaccination. J Control Release 2013; 172(3): 671-8.
[147]
Kraehenbuhl JP, Neutra MR. Epithelial M cells: differentiation and function. Annu Rev Cell Dev Biol 2000; 16: 301-32.
[148]
Chabot S, Wagner JS, Farrant S, Neutra MR. TLRs regulate the gatekeeping functions of the intestinal follicle-associated epithelium. J Immunol 2006; 176(7): 4275-83.
[149]
Chabot SM, Chernin TS, Shawi M, et al. TLR2 activation by proteosomes promotes uptake of particulate vaccines at mucosal surfaces. Vaccine 2007; 25(29): 5348-58.
[150]
Liang Y, Hasturk H, Elliot J, et al. Toll-like receptor 2 induces mucosal homing receptor expression and IgA production by human B cells. Clin Immunol 2011; 138(1): 33-40.
[151]
Lazarus NH, Kunkel EJ, Johnston B, Wilson E, Youngman KR, Butcher EC. A common mucosal chemokine (mucosae-associated epithelial chemokine/CCL28) selectively attracts IgA plasmablasts. J Immunol 2003; 170(7): 3799-805.
[152]
Kunkel EJ, Kim CH, Lazarus NH, et al. CCR10 expression is a common feature of circulating and mucosal epithelial tissue IgA Ab-secreting cells. J Clin Invest 2003; 111(7): 1001-10.
[153]
Hieshima K, Kawasaki Y, Hanamoto H, et al. CC chemokine ligands 25 and 28 play essential roles in intestinal extravasation of IgA antibody-secreting cells. J Immunol 2004; 173(6): 3668-75.
[154]
Wang S, Villablanca EJ, De Calisto J, et al. MyD88-dependent TLR1/2 signals educate dendritic cells with gut-specific imprinting properties. J Immunol 2011; 187(1): 141-50.
[155]
Caron G, Duluc D, Fremaux I, et al. Direct stimulation of human T cells via TLR5 and TLR7/8: flagellin and R-848 up-regulate proliferation and IFN-gamma production by memory CD4+ T cells. J Immunol 2005; 175(3): 1551-7.
[156]
Komai-Koma M, Jones L, Ogg GS, Xu D, Liew FY. TLR2 is expressed on activated T cells as a costimulatory receptor. Proc Natl Acad Sci USA 2004; 101(9): 3029-34.
[157]
Henrick BM, Yao XD, Rosenthal KL. team Is. HIV-1 structural proteins serve as PAMPs for TLR2 heterodimers significantly Increasing Infection and innate immune activation. Front Immunol 2015; 6(article 426): 1-15
[158]
Thibault S, Tardif MR, Barat C, Tremblay MJ. TLR2 signaling renders quiescent naive and memory CD4+ T cells more susceptible to productive infection with X4 and R5 HIV-type 1. J Immunol 2007; 179(7): 4357-66.
[159]
Bolduc JF, Ouellet M, Hany L, Tremblay MJ. Toll-like receptor 2 ligation enhances HIV-1 replication in activated CCR6+ CD4+ T cells by increasing virus entry and establishing a more permissive environment to infection. J Virol 2017; 91(4): e01402-16.
[160]
Zhang SY, Herman M, Ciancanelli MJ, et al. TLR3 immunity to infection in mice and humans. Curr Opin Immunol 2013; 25(1): 19-33.
[161]
Toussi DN, Massari P. Immune adjuvant effect of molecularly-defined Toll-like receptor ligands. Vaccines (Basel) 2014; 2(2): 323-53.
[162]
Le Bon A, Etchart N, Rossmann C, et al. Cross-priming of CD8+ T cells stimulated by virus-induced type I interferon. Nat Immunol 2003; 4(10): 1009-15.
[163]
Stahl-Hennig C, Eisenblatter M, Jasny E, et al. Synthetic double-stranded RNAs are adjuvants for the induction of T helper 1 and humoral immune responses to human papillomavirus in rhesus macaques. PLoS Pathog 2009; 5(4): e1000373.
[164]
Ichinohe T, Ainai A, Ami Y, et al. Intranasal administration of adjuvant-combined vaccine protects monkeys from challenge with the highly pathogenic influenza A H5N1 virus. J Med Virol 2010; 82(10): 1754-61.
[165]
Saito S, Ainai A, Suzuki T, et al. The effect of mucoadhesive excipient on the nasal retention time of and the antibody responses induced by an intranasal influenza vaccine. Vaccine 2016; 34(9): 1201-7.
[166]
Overton ET, Goepfert PA, Cunningham P, et al. Intranasal seasonal influenza vaccine and a TLR-3 agonist, rintatolimod, induced cross-reactive IgA antibody formation against avian H5N1 and H7N9 influenza HA in humans. Vaccine 2014; 32(42): 5490-5.
[167]
Aravantinou M, Frank I, Hallor M, et al. PolyICLC exerts pro- and anti-HIV effects on the DC-T cell milieu in vitro and in vivo. PLoS One 2016; 11(9): e0161730.
[168]
Vagenas P, Aravantinou M, Williams VG, et al. A tonsillar PolyICLC/AT-2 SIV therapeutic vaccine maintains low viremia following antiretroviral therapy cessation. PLoS One 2010; 5(9): e12891.
[169]
Andersen JM, Al-Khairy D, Ingalls RR. Innate immunity at the mucosal surface: role of Toll-like receptor 3 and Toll-like receptor 9 in cervical epithelial cell responses to microbial pathogens. Biol Reprod 2006; 74(5): 824-31.
[170]
Veazey RS, Pilch-Cooper HA, Hope TJ, et al. Prevention of SHIV transmission by topical IFN beta treatment. Mucosal Immunol 2016; 9(6): 1528-36.
[171]
Reed SG, Hsu FC, Carter D, Orr MT. The science of vaccine adjuvants: Advances in TLR4 ligand adjuvants. Curr Opin Immunol 2016; 41: 85-90.
[172]
Gwinn WM, Johnson BT, Kirwan SM, et al. A comparison of non-toxin vaccine adjuvants for their ability to enhance the immunogenicity of nasally-administered anthrax recombinant protective antigen. Vaccine 2013; 31(11): 1480-9.
[173]
Arias MA, Van Roey GA, Tregoning JS, et al. Glucopyranosyl Lipid Adjuvant (GLA), a synthetic TLR4 agonist, promotes potent systemic and mucosal responses to intranasal immunization with HIVgp140. PLoS One 2012; 7(7): e41144.
[174]
McKay PF, King DF, Mann JF, Barinaga G, Carter D, Shattock RJ. TLR4 and TLR7/8 adjuvant combinations generate different vaccine antigen-specific immune outcomes in minipigs when administered via the ID or IN routes. PLoS One 2016; 11(2): e0148984.
[175]
Yang J, Dai L, Yu Q, Yang Q. Histological and anatomical structure of the nasal cavity of Bama minipigs. PLoS One 2017; 12(3): e0173902.
[176]
Vijay-Kumar M, Gewirtz AT. Flagellin: key target of mucosal innate immunity. Mucosal Immunol 2009; 2(3): 197-205.
[177]
Taylor DN, Treanor JJ, Strout C, et al. Induction of a potent immune response in the elderly using the TLR-5 agonist, flagellin, with a recombinant hemagglutinin influenza-flagellin fusion vaccine (VAX125, STF2.HA1 SI). Vaccine 2011; 29(31): 4897-902.
[178]
Honko AN, Sriranganathan N, Lees CJ, Mizel SB. Flagellin is an effective adjuvant for immunization against lethal respiratory challenge with Yersinia pestis. Infect Immun 2006; 74(2): 1113-20.
[179]
Vassilieva EV, Wang BZ, Vzorov AN, et al. Enhanced mucosal immune responses to HIV virus-like particles containing a membrane-anchored adjuvant. MBio 2011; 2(1): e00328-10.
[180]
Lee SE, Hong SH, Verma V, et al. Flagellin is a strong vaginal adjuvant of a therapeutic vaccine for genital cancer. OncoImmunology 2016; 5(2): e1081328.
[181]
Chabot SM, Shawi M, Eaves-Pyles T, Neutra MR. Effects of flagellin on the functions of follicle-associated epithelium. J Infect Dis 2008; 198(6): 907-10.
[182]
Vasilakos JP, Tomai MA. The use of Toll-like receptor 7/8 agonists as vaccine adjuvants. Expert Rev Vaccines 2013; 12(7): 809-19.
[183]
McKay PF, Mann JF, Pattani A, et al. Intravaginal immunisation using a novel antigen-releasing ring device elicits robust vaccine antigen-specific systemic and mucosal humoral immune responses. J Control Release 2017; 249: 74-83.
[184]
Iho S, Maeyama J, Suzuki F. CpG oligodeoxynucleotides as mucosal adjuvants. Hum Vaccin Immunother 2015; 11(3): 755-60.
[185]
Wang Y, Blozis SA, Lederman M, Krieg A, Landay A, Miller CJ. Enhanced antibody responses elicited by a CpG adjuvant do not improve the protective effect of an aldrithiol-2-inactivated simian immunodeficiency virus therapeutic AIDS vaccine. Clin Vaccine Immunol 2009; 16(4): 499-505.
[186]
Newsted D, Fallahi F, Golshani A, Azizi A. Advances and challenges in mucosal adjuvant technology. Vaccine 2015; 33(21): 2399-405.
[187]
Bode C, Zhao G, Steinhagen F, Kinjo T, Klinman DM. CpG DNA as a vaccine adjuvant. Expert Rev Vaccines 2011; 10(4): 499-511.
[188]
Abel K, Wang Y, Fritts L, et al. Deoxycytidyl-deoxyguanosine oligonucleotide classes A, B, and C induce distinct cytokine gene expression patterns in rhesus monkey peripheral blood mononuclear cells and distinct alpha interferon responses in TLR9-expressing rhesus monkey plasmacytoid dendritic cells. Clin Diagn Lab Immunol 2005; 12(5): 606-21.
[189]
Vollmer J, Weeratna R, Payette P, et al. Characterization of three CpG oligodeoxynucleotide classes with distinct immunostimulatory activities. Eur J Immunol 2004; 34(1): 251-62.
[190]
Teleshova N, Kenney J, Jones J, et al. CpG-C immunostimulatory oligodeoxyribonucleotide activation of plasmacytoid dendritic cells in rhesus macaques to augment the activation of IFN-gamma-secreting simian immunodeficiency virus-specific T cells. J Immunol 2004; 173(3): 1647-57.
[191]
Wang Y, Abel K, Lantz K, Krieg AM, McChesney MB, Miller CJ. The Toll-like receptor 7 (TLR7) agonist, imiquimod, and the TLR9 agonist, CpG ODN, induce antiviral cytokines and chemokines but do not prevent vaginal transmission of simian immunodeficiency virus when applied intravaginally to rhesus macaques. J Virol 2005; 79(22): 14355-70.
[192]
Vagenas P, Williams VG, Piatak M Jr, et al. Tonsillar application of AT-2 SIV affords partial protection against rectal challenge with SIVmac239. J Acquir Immune Defic Syndr 2009; 52(4): 433-42.
[193]
Mansson A, Bachar O, Adner M, Cardell LO. Nasal CpG oligodeoxynucleotide administration induces a local inflammatory response in nonallergic individuals. Allergy 2009; 64(9): 1292-300.
[194]
Barouch DH, Craiu A, Kuroda MJ, et al. Augmentation of immune responses to HIV-1 and simian immunodeficiency virus DNA vaccines by IL-2/Ig plasmid administration in rhesus monkeys. Proc Natl Acad Sci USA 2000; 97(8): 4192-7.
[195]
Barouch DH, Santra S, Schmitz JE, et al. Control of viremia and prevention of clinical AIDS in rhesus monkeys by cytokine-augmented DNA vaccination. Science 2000; 290(5491): 486-92.
[196]
Demberg T, Boyer JD, Malkevich N, et al. Sequential priming with simian immunodeficiency virus (SIV) DNA vaccines, with or without encoded cytokines, and a replicating adenovirus-SIV recombinant followed by protein boosting does not control a pathogenic SIVmac251 mucosal challenge. J Virol 2008; 82(21): 10911-21.
[197]
Hirao LA, Wu L, Khan AS, et al. Combined effects of IL-12 and electroporation enhances the potency of DNA vaccination in macaques. Vaccine 2008; 26(25): 3112-20.
[198]
Jalah R, Patel V, Kulkarni V, et al. IL-12 DNA as molecular vaccine adjuvant increases the cytotoxic T cell responses and breadth of humoral immune responses in SIV DNA vaccinated macaques. Hum Vaccin Immunother 2012; 8(11): 1620-9.
[199]
Winstone N, Wilson AJ, Morrow G, et al. Enhanced control of pathogenic Simian immunodeficiency virus SIVmac239 replication in macaques immunized with an interleukin-12 plasmid and a DNA prime-viral vector boost vaccine regimen. J Virol 2011; 85(18): 9578-87.
[200]
Boyer JD, Robinson TM, Kutzler MA, et al. Protection against simian/human immunodeficiency virus (SHIV) 89.6P in macaques after coimmunization with SHIV antigen and IL-15 plasmid. Proc Natl Acad Sci USA 2007; 104(47): 18648-53.
[201]
Dubie RA, Maksaereekul S, Shacklett BL, et al. Co-immunization with IL-15 enhances cellular immune responses induced by a vif-deleted simian immunodeficiency virus proviral DNA vaccine and confers partial protection against vaginal challenge with SIVmac251. Virology 2009; 386(1): 109-21.
[202]
Sui Y, Zhu Q, Gagnon S, et al. Innate and adaptive immune correlates of vaccine and adjuvant-induced control of mucosal transmission of SIV in macaques. Proc Natl Acad Sci USA 2010; 107(21): 9843-8.
[203]
Yin J, Dai A, Laddy DJ, et al. High dose of plasmid IL-15 inhibits immune responses in an influenza non-human primates immunogenicity model. Virology 2009; 393(1): 49-55.
[204]
Van Roey GA, Arias MA, Tregoning JS, Rowe G, Shattock RJ. Thymic stromal lymphopoietin (TSLP) acts as a potent mucosal adjuvant for HIV-1 gp140 vaccination in mice. Eur J Immunol 2012; 42(2): 353-63.
[205]
Egan MA, Chong SY, Hagen M, et al. A comparative evaluation of nasal and parenteral vaccine adjuvants to elicit systemic and mucosal HIV-1 peptide-specific humoral immune responses in cynomolgus macaques. Vaccine 2004; 22(27-28): 3774-88.
[206]
Bradney CP, Sempowski GD, Liao HX, Haynes BF, Staats HF. Cytokines as adjuvants for the induction of anti-human immunodeficiency virus peptide immunoglobulin G (IgG) and IgA antibodies in serum and mucosal secretions after nasal immunization. J Virol 2002; 76(2): 517-24.
[207]
Schell JB, Bahl K, Rose NF, et al. Viral vectored granulocyte-macrophage colony stimulating factor inhibits vaccine protection in an SIV challenge model: protection correlates with neutralizing antibody. Vaccine 2012; 30(28): 4233-9.
[208]
Kannanganat S, Wyatt LS, Gangadhara S, et al. High doses of GM-CSF inhibit antibody responses in rectal secretions and diminish modified vaccinia Ankara/Simian immunodeficiency virus vaccine protection in TRIM5alpha-restrictive macaques. J Immunol 2016; 197(9): 3586-96.
[209]
Rainone V, Dubois G, Temchura V, et al. CCL28 induces mucosal homing of HIV-1-specific IgA-secreting plasma cells in mice immunized with HIV-1 virus-like particles. PLoS One 2011; 6(10): e26979.
[210]
Hu K, Luo S, Tong L, et al. CCL19 and CCL28 augment mucosal and systemic immune responses to HIV-1 gp140 by mobilizing responsive immunocytes into secondary lymph nodes and mucosal tissue. J Immunol 2013; 191(4): 1935-47.
[211]
Cha HR, Ko HJ, Kim ED, et al. Mucosa-associated epithelial chemokine/CCL28 expression in the uterus attracts CCR10+ IgA plasma cells following mucosal vaccination via estrogen control. J Immunol 2011; 187(6): 3044-52.
[212]
Kutzler MA, Wise MC, Hutnick NA, et al. Chemokine-adjuvanted electroporated DNA vaccine induces substantial protection from simian immunodeficiency virus vaginal challenge. Mucosal Immunol 2016; 9(1): 13-23.
[213]
Clements JD, Freytag LC. Parenteral vaccination can be an effective means of inducing protective mucosal responses. Clin Vaccine Immunol 2016; 23(6): 438-41.
[214]
Lycke N. Recent progress in mucosal vaccine development: potential and limitations. Nat Rev Immunol 2012; 12(8): 592-605.
[215]
Lebens M, Terrinoni M, Karlsson SL, et al. Construction and preclinical evaluation of mmCT, a novel mutant cholera toxin adjuvant that can be efficiently produced in genetically manipulated Vibrio cholerae. Vaccine 2016; 34(18): 2121-8.
[216]
Norton EB, Lawson LB, Freytag LC, Clements JD. Characterization of a mutant Escherichia coli heat-labile toxin, LT(R192G/L211A), as a safe and effective oral adjuvant. Clin Vaccine Immunol 2011; 18(4): 546-51.
[217]
Marks E, Helgeby A, Andersson JO, Schon K, Lycke NY. CD4(+) T-cell immunity in the female genital tract is critically dependent on local mucosal immunization. Eur J Immunol 2011; 41(9): 2642-53.
[218]
Larena M, Holmgren J, Lebens M, Terrinoni M, Lundgren A. Cholera toxin, and the related nontoxic adjuvants mmCT and dmLT, promote human Th17 responses via cyclic AMP-protein kinase A and inflammasome-dependent IL-1 signaling. J Immunol 2015; 194(8): 3829-39.
[219]
van Ginkel FW, Jackson RJ, Yoshino N, et al. Enterotoxin-based mucosal adjuvants alter antigen trafficking and induce inflammatory responses in the nasal tract. Infect Immun 2005; 73(10): 6892-902.
[220]
Lewis DJ, Huo Z, Barnett S, et al. Transient facial nerve paralysis (Bell’s palsy) following intranasal delivery of a genetically detoxified mutant of Escherichia coli heat labile toxin. PLoS One 2009; 4(9): e6999.
[221]
Lundgren A, Bourgeois L, Carlin N, et al. Safety and immunogenicity of an improved oral inactivated multivalent enterotoxigenic Escherichia coli (ETEC) vaccine administered alone and together with dmLT adjuvant in a double-blind, randomized, placebo-controlled Phase I study. Vaccine 2014; 32(52): 7077-84.
[222]
Belyakov IM, Hel Z, Kelsall B, et al. Mucosal AIDS vaccine reduces disease and viral load in gut reservoir and blood after mucosal infection of macaques. Nat Med 2001; 7(12): 1320-6.
[223]
Fuller DH, Rajakumar P, Che JW, et al. Therapeutic DNA vaccine induces broad T cell responses in the gut and sustained protection from viral rebound and AIDS in SIV-infected rhesus macaques. PLoS One 2012; 7(3): e33715.
[224]
Frederick DR, Goggins JA, Sabbagh LM, Freytag LC, Clements JD, McLachlan JB. Adjuvant selection regulates gut migration and phenotypic diversity of antigen-specific CD4+ T cells following parenteral immunization. Mucosal Immunol 2018; 11(2): 549-61.
[225]
Norton EB, Bauer DL, Weldon WC, Oberste MS, Lawson LB, Clements JD. The novel adjuvant dmLT promotes dose sparing, mucosal immunity and longevity of antibody responses to the inactivated polio vaccine in a murine model. Vaccine 2015; 33(16): 1909-15.
[226]
Lawson LB, Norton EB, Clements JD. Defending the mucosa: Adjuvant and carrier formulations for mucosal immunity. Curr Opin Immunol 2011; 23(3): 414-20.
[227]
Smith A, Perelman M, Hinchcliffe M. Chitosan: A promising safe and immune-enhancing adjuvant for intranasal vaccines. Hum Vaccin Immunother 2014; 10(3): 797-807.
[228]
Deli MA. Potential use of tight junction modulators to reversibly open membranous barriers and improve drug delivery. Biochim Biophys Acta 2009; 1788(4): 892-910.
[229]
McNeela EA, Jabbal-Gill I, Illum L, Pizza M, et al. Intranasal immunization with genetically detoxified diphtheria toxin induces T cell responses in humans: enhancement of Th2 responses and toxin-neutralizing antibodies by formulation with chitosan. Vaccine 2004; 22(8): 909-14.
[230]
Sigsgaard T, Thorne PS, Schlunssen V, et al. The change in nasal inflammatory markers after intranasal challenges with particulate chitin and lipopolysaccharide: a randomized, double-blind, placebo-controlled, crossover study with a positive control. Int Forum Allergy Rhinol 2015; 5(8): 716-23.
[231]
Cosgrove CA, Lacey CJ, Cope AV, et al. Comparative Immunogenicity of HIV-1 gp140 vaccine delivered by parenteral, and mucosal routes in female volunteers; MUCOVAC2, a randomized two centre study. PLoS One 2016; 11(5): e0152038.
[232]
Hayashi M, Aoshi T, Ozasa K, et al. RNA is an adjuvanticity mediator for the lipid-based mucosal adjuvant, Endocine. Sci Rep 2016; 6: e29165.
[233]
Brekke K, Lind A, Holm-Hansen C, et al. Intranasal administration of a therapeutic HIV vaccine (Vacc-4x) induces dose-dependent systemic and mucosal immune responses in a randomized controlled trial. PLoS One 2014; 9(11): e112556.
[234]
Buonaguro L, Devito C, Tornesello ML, et al. DNA-VLP prime-boost intra-nasal immunization induces cellular and humoral anti-HIV-1 systemic and mucosal immunity with cross-clade neutralizing activity. Vaccine 2007; 25(32): 5968-77.
[235]
Buonaguro L, Tagliamonte M, Visciano ML, et al. Immunogenicity of HIV virus-like particles in rhesus macaques by intranasal administration. Clin Vaccine Immunol 2012; 19(6): 970-3.
[236]
Quinn KM, Yamamoto A, Costa A, et al. Coadministration of polyinosinic: Polycytidylic acid and immunostimulatory complexes modifies antigen processing in dendritic cell subsets and enhances HIV gag-specific T cell immunity. J Immunol 2013; 191(10): 5085-96.
[237]
Helgeby A, Robson NC, Donachie AM, et al. The combined CTA1-DD/ISCOM adjuvant vector promotes priming of mucosal and systemic immunity to incorporated antigens by specific targeting of B cells. J Immunol 2006; 176(6): 3697-706.
[238]
Eliasson DG, Helgeby A, Schon K, et al. A novel non-toxic combined CTA1-DD and ISCOMS adjuvant vector for effective mucosal immunization against influenza virus. Vaccine 2011; 29(23): 3951-61.
[239]
McEntee C, Lavelle EC, O’Hagan DT. Antigen delivery systems I: Nonliving microparticles, liposomes, and immune-stimulating complexes (ISCOMs).In: Mestecky J, Strober W, Russell MW, Kelsall BL, Cheroutre H, Lambrecht BN, editors. Mucosal Immunology. 4th ed. Boston: Elsevier; 2015. p. 1211-31.
[240]
Rodriguez-Garcia M, Patel MV, Wira CR. Innate and adaptive anti-HIV immune responses in the female reproductive tract. J Reprod Immunol 2013; 97(1): 74-84.
[241]
Mukherjee S, Hooper LV. Antimicrobial defense of the intestine. Immunity 2015; 42(1): 28-39.
[242]
Ghosh M. Secreted mucosal antimicrobials in the female reproductive tract that are important to consider for HIV prevention. Am J Reprod Immunol 2014; 71(6): 575-88.
[243]
Zhang P, Summer WR, Bagby GJ, Nelson S. Innate immunity and pulmonary host defense. Immunol Rev 2000; 173: 39-51.
[244]
Akhtar M, Qadri F, Bhuiyan TR, et al. Kinetics of antibody-secreting cell and fecal IgA responses after oral cholera vaccination in different age groups in a cholera endemic country. Vaccine 2017; 35(2): 321-8.
[245]
Levine MM, Ferreccio C, Abrego P, Martin OS, Ortiz E, Cryz S. Duration of efficacy of Ty21a, attenuated Salmonella typhi live oral vaccine. Vaccine 1999; 17(Suppl. 2): S22-7.
[246]
Maroni A, Moutaharrik S, Zema L, Gazzaniga A. Enteric coatings for colonic drug delivery: State of the art. Expert Opin Drug Deliv 2017; 14(9): 1027-9.
[247]
Mercier GT, Nehete PN, Passeri MF, et al. Oral immunization of rhesus macaques with adenoviral HIV vaccines using enteric-coated capsules. Vaccine 2007; 25(52): 8687-701.
[248]
Zhu Q, Talton J, Zhang G, et al. Large intestine-targeted, nanoparticle-releasing oral vaccine to control genitorectal viral infection. Nat Med 2012; 18(8): 1291-6.
[249]
Hara H, Ono F, Nakamura S, et al. An oral abeta vaccine using a recombinant adeno-ssociated virus vector in aged monkeys: Reduction in plaque amyloid and increase in abeta oligomers. J Alzheimers Dis 2016; 54(3): 1047-59.
[250]
Mabbott NA, Donaldson DS, Ohno H, Williams IR, Mahajan A. Microfold (M) cells: Important immunosurveillance posts in the intestinal epithelium. Mucosal Immunol 2013; 6(4): 666-77.
[251]
McNeela EA, Lavelle EC. Recent advances in microparticle and nanoparticle delivery vehicles for mucosal vaccination. Curr Top Microbiol Immunol 2012; 354: 75-99.
[252]
Ogasawara N, Kojima T, Go M, et al. Epithelial barrier and antigen uptake in lymphoepithelium of human adenoids. Acta Otolaryngol 2011; 131(2): 116-23.
[253]
Ensign LM, Cone R, Hanes J. Nanoparticle-based drug delivery to the vagina: A review. J Control Release 2014; 190: 500-14.
[254]
Mohideen M, Quijano E, Song E, et al. Degradable bioadhesive nanoparticles for prolonged intravaginal delivery and retention of elvitegravir. Biomaterials 2017; 144: 144-54.
[255]
Howe SE, Konjufca VH. Protein-coated nanoparticles are internalized by the epithelial cells of the female reproductive tract and induce systemic and mucosal immune responses. PLoS One 2014; 9(12): e114601.
[256]
Kasturi SP, Skountzou I, Albrecht RA, et al. Programming the magnitude and persistence of antibody responses with innate immunity. Nature 2011; 470(7335): 543-7.
[257]
Singh M, Chesko J, Kazzaz J, et al. Adsorption of a novel recombinant glycoprotein from HIV (Env gp120dV2 SF162) to anionic PLG microparticles retains the structural integrity of the protein, whereas encapsulation in PLG microparticles does not. Pharm Res 2004; 21(12): 2148-52.
[258]
Lambert JS, Keefer M, Mulligan MJ, et al. A Phase I safety and immunogenicity trial of UBI microparticulate monovalent HIV-1 MN oral peptide immunogen with parenteral boost in HIV-1 seronegative human subjects. Vaccine 2001; 19(23-24): 3033-42.
[259]
Singh M, Kazzaz J, Ugozzoli M, Malyala P, Chesko J, O’Hagan DT. Polylactide-co-glycolide microparticles with surface adsorbed antigens as vaccine delivery systems. Curr Drug Deliv 2006; 3(1): 115-20.
[260]
Bernasconi V, Norling K, Bally M, Hook F, Lycke NY. Mucosal vaccine development based on liposome technology. J Immunol Res 2016; 2016: 5482087.
[261]
Childers NK, Zhang SS, Michalek SM. Oral immunization of humans with dehydrated liposomes containing Streptococcus mutans glucosyltransferase induces salivary immunoglobulin A2 antibody responses. Oral Microbiol Immunol 1994; 9(3): 146-53.
[262]
Nguyen HH, Boyaka PN, Moldoveanu Z, et al. Influenza virus-infected epithelial cells present viral antigens to antigen-specific CD8+ cytotoxic T lymphocytes. J Virol 1998; 72(5): 4534-6.
[263]
Hatano R, Yamada K, Iwamoto T, et al. Antigen presentation by small intestinal epithelial cells uniquely enhances IFN-gamma secretion from CD4+ intestinal intraepithelial lymphocytes. Biochem Biophys Res Commun 2013; 435(4): 592-6.
[264]
Ochiel DO, Rossoll RM, Schaefer TM, Wira CR. Effect of oestradiol and pathogen-associated molecular patterns on class II-mediated antigen presentation and immunomodulatory molecule expression in the mouse female reproductive tract. Immunology 2012; 135(1): 51-62.
[265]
Morelli AB, Becher D, Koernig S, Silva A, Drane D, Maraskovsky E. ISCOMATRIX: A novel adjuvant for use in prophylactic and therapeutic vaccines against infectious diseases. J Med Microbiol 2012; 61(Pt 7): 935-43.
[266]
Lycke N, Bemark M. Mucosal adjuvants and long-term memory development with special focus on CTA1-DD and other ADP-ribosylating toxins. Mucosal Immunol 2010; 3(6): 556-66.
[267]
Furrie E, Smith RE, Turner MW, Strobel S, Mowat AM. Induction of local innate immune responses and modulation of antigen uptake as mechanisms underlying the mucosal adjuvant properties of immune stimulating complexes (ISCOMS). Vaccine 2002; 20(17-18): 2254-62.
[268]
Pahar B, Cantu MA, Zhao W, et al. Single epitope mucosal vaccine delivered via immuno-stimulating complexes induces low level of immunity against simian-HIV. Vaccine 2006; 24(47-48): 6839-49.
[269]
Wee JL, Scheerlinck JP, Snibson KJ, et al. Pulmonary delivery of ISCOMATRIX influenza vaccine induces both systemic and mucosal immunity with antigen dose sparing. Mucosal Immunol 2008; 1(6): 489-96.
[270]
Cusi MG. Applications of influenza virosomes as a delivery system. Hum Vaccin 2006; 2(1): 1-7.
[271]
Moser C, Muller M, Kaeser MD, Weydemann U, Amacker M. Influenza virosomes as vaccine adjuvant and carrier system. Expert Rev Vaccines 2013; 12(7): 779-91.
[272]
Garcia-Sastre A. Influenza virus receptor specificity: Disease and transmission. Am J Pathol 2010; 176(4): 1584-5.
[273]
Gargett T, Grubor-Bauk B, Miller D, et al. Increase in DNA vaccine efficacy by virosome delivery and co-expression of a cytolytic protein. Clin Transl Immunology 2014; 3(6): e18.
[274]
Blom RAM, Amacker M, van Dijk RM, et al. Pulmonary delivery of virosome-bound antigen enhances antigen-specific CD4(+) T cell proliferation compared to liposome-bound or soluble antigen. Front Immunol 2017; 8(article 359): 1-17.
[275]
Pedersen GK, Ebensen T, Gjeraker IH, et al. Evaluation of the sublingual route for administration of influenza H5N1 virosomes in combination with the bacterial second messenger c-di-GMP. PLoS One 2011; 6(11): e26973.
[276]
De Bernardis F, Arancia S, Sandini S, Graziani S, Norelli S. Studies of Immune Responses in Candida vaginitis. Pathogens 2015; 4(4): 697-707.
[277]
Koopman G, Bogers WM, van Gils M, et al. Comparison of intranasal with targeted lymph node immunization using PR8-Flu ISCOM adjuvanted HIV antigens in macaques. J Med Virol 2007; 79(5): 474-82.
[278]
Zhou M, Ruprecht RM. Are anti-HIV IgAs good guys or bad guys? Retrovirology 2014; 11(article 109): 1-11
[279]
Bomsel M, Tudor D, Drillet AS, et al. Immunization with HIV-1 gp41 subunit virosomes induces mucosal antibodies protecting nonhuman primates against vaginal SHIV challenges. Immunity 2011; 34(2): 269-80.
[280]
Leroux-Roels G, Maes C, Clement F, et al. Randomized Phase I: Safety, Immunogenicity and Mucosal Antiviral Activity in Young Healthy Women Vaccinated with HIV-1 Gp41 P1 Peptide on Virosomes. PLoS One 2013; 8(2): e55438.
[281]
Berger CT, Greiff V, Mehling M, et al. Influenza vaccine response profiles are affected by vaccine preparation and preexisting immunity, but not HIV infection. Hum Vaccin Immunother 2015; 11(2): 391-6.
[282]
Cech PG, Aebi T, Abdallah MS, et al. Virosome-formulated Plasmodium falciparum AMA-1 & CSP derived peptides as malaria vaccine: randomized phase 1b trial in semi-immune adults & children. PLoS One 2011; 6(7): e22273.
[283]
Chappuis F, Farinelli T, Deckx H, et al. Immunogenicity and estimation of antibody persistence following vaccination with an inactivated virosomal hepatitis A vaccine in adults: A 20-year follow-up study. Vaccine 2017; 35(10): 1448-54.
[284]
Grimaldi N, Andrade F, Segovia N, et al. Lipid-based nanovesicles for nanomedicine. Chem Soc Rev 2016; 45(23): 6520-45.
[285]
Levine MM. Immunogenicity and efficacy of oral vaccines in developing countries: lessons from a live cholera vaccineBMC Biol 2010; 8(article 129): 1-10
[286]
Loehr BI, Rankin R, Pontarollo R, et al. Suppository-mediated DNA immunization induces mucosal immunity against bovine herpesvirus-1 in cattle. Virology 2001; 289(2): 327-33.
[287]
Eriksson K, Quiding-Jarbrink M, Osek J, et al. Specific-antibody-secreting cells in the rectums and genital tracts of nonhuman primates following vaccination. Infect Immun 1998; 66(12): 5889-96.
[288]
Eriksson K, Quiding-Jarbrink M, Osek J, et al. Anatomic segmentation of the intestinal immune response in nonhuman primates: differential distribution of B cells after oral and rectal immunizations to sites defined by their source of vascularization. Infect Immun 1999; 67(11): 6210-2.
[289]
Kozlowski PA, Cu-Uvin S, Neutra MR, Flanigan TP. Comparison of the oral, rectal, and vaginal immunization routes for induction of antibodies in rectal and genital tract secretions of women. Infect Immun 1997; 65(4): 1387-94.
[290]
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(1): 566-74.
[291]
Wassen L, Schon K, Holmgren J, Jertborn M, Lycke N. Local intravaginal vaccination of the female genital tract. Scand J Immunol 1996; 44(4): 408-14.
[292]
Rudin A, Riise GC, Holmgren J. Antibody responses in the lower respiratory tract and male urogenital tract in humans after nasal and oral vaccination with cholera toxin B subunit. Infect Immun 1999; 67(6): 2884-90.
[293]
Demberg T, Robert-Guroff M. Mucosal immunity and protection against HIV/SIV infection: strategies and challenges for vaccine design. Int Rev Immunol 2009; 28(1): 20-48.
[294]
McMichael AJ. HIV vaccines. Annu Rev Immunol 2006; 24: 227-55.
[295]
Haynes BF, Gilbert PB, McElrath MJ, et al. Immune-correlates analysis of an HIV-1 vaccine efficacy trial. N Engl J Med 2012; 366(14): 1275-86.
[296]
Ruiz MJ, Salido J, Abusamra L, et al. Evaluation of Different Parameters of Humoral and Cellular Immune Responses in HIV Serodiscordant Heterosexual Couples: Humoral Response Potentially Implicated in Modulating Transmission Rates. EBioMedicine 2017; 26: 25-37.
[297]
Fenizia C, Rossignol JF, Clerici M, Biasin M. Genetic and immune determinants of immune activation in HIV-exposed seronegative individuals and their role in protection against HIV infection. Infect Genet Evol 2017; pii: S1567-1348(17)30439-2.
[298]
Hirbod T, Kong X, Kigozi G, et al. HIV acquisition is associated with increased antimicrobial peptides and reduced HIV neutralizing IgA in the foreskin prepuce of uncircumcised men. PLoS Pathog 2014; 10(10): e1004416.
[299]
Pantophlet R, Burton DR. GP120: Target for neutralizing HIV-1 antibodies. Annu Rev Immunol 2006; 24: 739-69.
[300]
Hendricks EE, Ludlage E, Bussell S, George K, Wegner FH, Mansfield KG. Wasting syndrome and disruption of the somatotropic axis in simian immunodeficiency virus-infected macaques with Mycobacterium avium complex infection. J Infect Dis 2004; 190(12): 2187-94.
[301]
Letvin NL. Progress toward an HIV vaccine. Annu Rev Med 2005; 56: 213-23.
[302]
Gottardo R, Bailer RT, Korber BT, et al. Plasma IgG to linear epitopes in the V2 and V3 regions of HIV-1 gp120 correlate with a reduced risk of infection in the RV144 vaccine efficacy trial. PLoS One 2013; 8(9): e75665.
[303]
Zolla-Pazner S, deCamp AC, Cardozo T, et al. Analysis of V2 antibody responses induced in vaccinees in the ALVAC/AIDSVAX HIV-1 vaccine efficacy trial. PLoS One 2013; 8(1): e53629.
[304]
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. Chiang Mai HEPS Working Group. J Infect Dis 1999; 179(1): 59-67.
[305]
Plummer FA, Ball TB, Kimani J, Fowke KR. Resistance to HIV-1 infection among highly exposed sex workers in Nairobi: what mediates protection and why does it develop? Immunol Lett 1999; 66(1-3): 27-34.
[306]
Clerici M, Salvi A, Trabattoni D, et al. A role for mucosal immunity in resistance to HIV infection. Immunol Lett 1999; 66(1-3): 21-5.
[307]
Clerici M, Barassi C, Devito C, et al. Serum IgA of HIV-exposed uninfected individuals inhibit HIV through recognition of a region within the alpha-helix of gp41. AIDS 2002; 16(13): 1731-41.
[308]
Lo Caputo S, Trabattoni D, Vichi F, et al. Mucosal and systemic HIV-1-specific immunity in HIV-1-exposed but uninfected heterosexual men. AIDS 2003; 17(4): 531-9.
[309]
Wang SW, Bertley FM, Kozlowski PA, et al. An SHIV DNA/MVA rectal vaccination in macaques provides systemic and mucosal virus-specific responses and protection against AIDS. AIDS Res Hum Retroviruses 2004; 20(8): 846-59.
[310]
Stahl-Hennig C, Kuate S, Franz M, et al. Atraumatic oral spray immunization with replication-deficient viral vector vaccines. J Virol 2007; 81(23): 13180-90.
[311]
Feinberg MB, Moore JP. AIDS vaccine models: Challenging challenge viruses. Nat Med 2002; 8(3): 207-10.
[312]
Belyakov IM, Kuznetsov VA, Kelsall B, et al. Impact of vaccine-induced mucosal high-avidity CD8+ CTLs in delay of AIDS viral dissemination from mucosa. Blood 2006; 107(8): 3258-64.
[313]
Chin’ombe N, Ruhanya V. Recombinant Salmonella bacteria vectoring HIV/AIDS vaccines. Open Virol J 2013; 7: 121-6.
[314]
Ambrose Z, Larsen K, Thompson J, et al. Evidence for early local viral replication and local production of antiviral immunity upon mucosal simian-human immunodeficiency virus SHIV (89.6) infection in Macaca nemestrina. J Virol 2001; 75(18): 8589-96.
[315]
Genesca M, McChesney MB, Miller CJ. Antiviral CD8+ T cells in the genital tract control viral replication and delay progression to AIDS after vaginal SIV challenge in rhesus macaques immunized with virulence attenuated SHIV 89.6. J Intern Med 2009; 265(1): 67-77.
[316]
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(6): 3113-25.
[317]
Barnett SW, Srivastava IK, Kan E, et al. Protection of macaques against vaginal SHIV challenge by systemic or mucosal and systemic vaccinations with HIV-envelope. AIDS 2008; 22(3): 339-48.
[318]
Alpert MD, Harvey JD, Lauer WA, et al. ADCC develops over time during persistent infection with live-attenuated SIV and is associated with complete protection against SIV(mac)251 challenge. PLoS Pathog 2012; 8(8): e1002890.
[319]
Stevceva L, Alvarez X, Lackner AA, et al. Both mucosal and systemic routes of immunization with the live, attenuated NYVAC/simian immunodeficiency virus SIV(gpe) recombinant vaccine result in gag-specific CD8(+) T-cell responses in mucosal tissues of macaques. J Virol 2002; 76(22): 11659-76.
[320]
Cuburu N, Graham BS, Buck CB, et al. Intravaginal immunization with HPV vectors induces tissue-resident CD8+ T cell responses. J Clin Invest 2012; 122(12): 4606-20.
[321]
Belyakov IM, Ahlers JD. Mucosal immunity and HIV-1 infection: Applications for mucosal AIDS vaccine development. Curr Top Microbiol Immunol 2012; 354: 157-79.
[322]
Vajdy M, Gardner J, Neidleman J, et al. Human immunodeficiency virus type 1 Gag-specific vaginal immunity and protection after local immunizations with sindbis virus-based replicon particles. J Infect Dis 2001; 184(12): 1613-6.
[323]
Gupta S, Janani R, Bin Q, et al. Characterization of human immunodeficiency virus Gag-specific gamma interferon-expressing cells following protective mucosal immunization with alphavirus replicon particles. J Virol 2005; 79(11): 7135-45.
[324]
Schautteet K, De Clercq E, Jonsson Y, et al. Protection of pigs against genital Chlamydia trachomatis challenge by parenteral or mucosal DNA immunization. Vaccine 2012; 30(18): 2869-81.
[325]
Mall AS, Habte H, Mthembu Y, Peacocke J, de Beer C. Mucus and Mucins: do they have a role in the inhibition of the human immunodeficiency virus? Virol J 2017; 14(1): e192.
[326]
Carias AM, McCoombe S, McRaven M, et al. Defining the interaction of HIV-1 with the mucosal barriers of the female reproductive tract. J Virol 2013; 87(21): 11388-400.
[327]
King BF. The permeability of nonhuman primate vaginal epithelium: a freeze-fracture and tracer-perfusion study. J Ultrastruct Res 1983; 83(1): 99-110.
[328]
Parr MB, Parr EL. Antigen recognition in the female reproductive tract: I. Uptake of intraluminal protein tracers in the mouse vagina. J Reprod Immunol 1990; 17(2): 101-14.
[329]
Pialoux G, Hocini H, Perusat S, et al. Phase I study of a candidate vaccine based on recombinant HIV-1 gp160 (MN/LAI) administered by the mucosal route to HIV-seronegative volunteers: The ANRS VAC14 study. Vaccine 2008; 26(21): 2657-66.
[330]
Lewis DJ, Fraser CA, Mahmoud AN, et al. Phase I randomised clinical trial of an HIV-1(CN54), clade C, trimeric envelope vaccine candidate delivered vaginally. PLoS One 2011; 6(9): e25165.
[331]
Cranage MP, Fraser CA, Cope A, et al. Antibody responses after intravaginal immunisation with trimeric HIV-1 CN54 clade C gp140 in Carbopol gel are augmented by systemic priming or boosting with an adjuvanted formulation. Vaccine 2011; 29(7): 1421-30.
[332]
Wright PF, Mestecky J, McElrath MJ, 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(7): 1221-31.
[333]
Gordon SN, Doster MN, Kines RC, et al. Antibody to the gp120 V1/V2 loops and CD4+ and CD8+ T cell responses in protection from SIVmac251 vaginal acquisition and persistent viremia. J Immunol 2014; 193(12): 6172-83.
[334]
Lewis DJ, Wang Y, Huo Z, et al. Effect of vaginal immunization with HIVgp140 and HSP70 on HIV-1 replication and innate and T cell adaptive immunity in women. J Virol 2014; 88(20): 11648-57.
[335]
Weaver EA, Nehete PN, Nehete BP, et al. Comparison of systemic and mucosal immunization with helper-dependent adenoviruses for vaccination against mucosal challenge with SHIV. PLoS One 2013; 8(7): e67574.
[336]
Abel K, Compton L, Rourke T, et al. Simian-human immunodeficiency virus SHIV89.6-induced protection against intravaginal challenge with pathogenic SIVmac239 is independent of the route of immunization and is associated with a combination of cytotoxic T-lymphocyte and alpha interferon responses. J Virol 2003; 77(5): 3099-118.
[337]
Genesca M, Ma ZM, Wang Y, et al. Live-attenuated lentivirus immunization modulates innate immunity and inflammation while protecting rhesus macaques from vaginal simian immunodeficiency virus challenge. J Virol 2012; 86(17): 9188-200.
[338]
Ganor Y, Zhou Z, Bodo J, et al. The adult penile urethra is a novel entry site for HIV-1 that preferentially targets resident urethral macrophages. Mucosal Immunol 2013; 6(4): 776-86.
[339]
Zhou Z, Barry de Longchamps N, Schmitt A, et al. HIV-1 efficient entry in inner foreskin is mediated by elevated CCL5/RANTES that recruits T cells and fuels conjugate formation with Langerhans cells. PLoS Pathog 2011; 7(6): e1002100.
[340]
Prodger JL, Gray R, Kigozi G, et al. Foreskin T-cell subsets differ substantially from blood with respect to HIV co-receptor expression, inflammatory profile, and memory status. Mucosal Immunol 2012; 5(2): 121-8.
[341]
Dinh MH, Anderson MR, McRaven MD, et al. Visualization of HIV-1 interactions with penile and foreskin epithelia: clues for female-to-male HIV transmission. PLoS Pathog 2015; 11(3): e1004729.
[342]
Anderson D, Politch JA, Pudney J. HIV infection and immune defense of the penis. Am J Reprod Immunol 2011; 65(3): 220-9.
[343]
Sennepin A, Real F, Duvivier M, et al. The human penis is a genuine immunological effector siteFront Immunol 2017; 8(article 1732): 1- 18
[344]
Rothaeusler K, Ma ZM, Qureshi H, et al. Antiviral antibodies and T cells are present in the foreskin of simian immunodeficiency virus-infected rhesus macaques. J Virol 2012; 86(13): 7098-106.
[345]
Pudney J, Anderson DJ. Immunobiology of the human penile urethra. Am J Pathol 1995; 147(1): 155-65.
[346]
Mestecky J, Alexander RC, Wei Q, Moldoveanu Z. Methods for evaluation of humoral immune responses in human genital tract secretions. Am J Reprod Immunol 2011; 65(3): 361-7.
[347]
Moldoveanu Z, Huang WQ, 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(6): 4127-36.
[348]
Prodger JL, Hirbod T, Kigozi G, et al. Immune correlates of HIV exposure without infection in foreskins of men from Rakai, Uganda. Mucosal Immunol 2014; 7(3): 634-44.
[349]
Adams SE, Dawson KM, Gull K, Kingsman SM, Kingsman AJ. The expression of hybrid HIV: Ty virus-like particles in yeast. Nature 1987; 329(6134): 68-70.
[350]
Lehner T, Tao L, Panagiotidi C, et al. Mucosal model of genital immunization in male rhesus macaques with a recombinant simian immunodeficiency virus p27 antigen. J Virol 1994; 68(3): 1624-32.
[351]
Balandya E, Miller AD, Beck M, et al. Adenovirus serotype 26 and 35 vectors induce simian immunodeficiency virus-specific T lymphocyte responses in foreskin in rhesus monkeys. J Virol 2014; 88(7): 3756-65.
[352]
Quiding-Jarbrink M, Granstrom G, Nordstrom I, Holmgren J, Czerkinsky C. Induction of compartmentalized B-cell responses in human tonsils. Infect Immun 1995; 63(3): 853-7.
[353]
Mills KH, Cosgrove C, McNeela EA, et al. Protective levels of diphtheria-neutralizing antibody induced in healthy volunteers by unilateral priming-boosting intranasal immunization associated with restricted ipsilateral mucosal secretory immunoglobulin A. Infect Immun 2003; 71(2): 726-32.
[354]
Huo Z, Sinha R, McNeela EA, et al. Induction of protective serum meningococcal bactericidal and diphtheria-neutralizing antibodies and mucosal immunoglobulin A in volunteers by nasal insufflations of the Neisseria meningitidis serogroup C polysaccharide-CRM197 conjugate vaccine mixed with chitosan. Infect Immun 2005; 73(12): 8256-65.
[355]
Anjuere F, Bekri S, Bihl F, et al. B cell and T cell immunity in the female genital tract: Potential of distinct mucosal routes of vaccination and role of tissue-associated dendritic cells and natural killer cells. Clin Microbiol Infect 2012; 18(Suppl. 5): 117-22.
[356]
Davila SJ, Olive AJ, Starnbach MN. Integrin alpha4beta1 is necessary for CD4+ T cell-mediated protection against genital Chlamydia trachomatis infection. J Immunol 2014; 192(9): 4284-93.
[357]
Nardelli-Haefliger D, Kraehenbuhl JP, Curtiss R III, et al. Oral and rectal immunization of adult female volunteers with a recombinant attenuated Salmonella typhi vaccine strain. Infect Immun 1996; 64(12): 5219-24.
[358]
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 1998; 66(12): 5630-5.
[359]
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 Ty 21a vaccine. J Reprod Immunol 2001; 52(1-2): 61-75.
[360]
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(5): 370-9.
[361]
Kubota M, Miller CJ, Imaoka K, et al. Oral immunization with simian immunodeficiency virus p55gag and cholera toxin elicits both mucosal IgA and systemic IgG immune responses in nonhuman primates. J Immunol 1997; 158(11): 5321-9.
[362]
Wu HY, Russell MW. Induction of mucosal immunity by intranasal application of a streptococcal surface protein antigen with the cholera toxin B subunit. Infect Immun 1993; 61(1): 314-22.
[363]
Gallichan WS, Rosenthal KL. Long-lived cytotoxic T lymphocyte memory in mucosal tissues after mucosal but not systemic immunization. J Exp Med 1996; 184(5): 1879-90.
[364]
Gallichan WS, Rosenthal KL. Long-term immunity and protection against herpes simplex virus type 2 in the murine female genital tract after mucosal but not systemic immunization. J Infect Dis 1998; 177(5): 1155-61.
[365]
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 the cholera toxin B subunit. Infect Immun 1996; 64(4): 1272-83.
[366]
Rudin A, Johansson EL, Bergquist C, Holmgren J. Differential kinetics and distribution of antibodies in serum and nasal and vaginal secretions after nasal and oral vaccination of humans. Infect Immun 1998; 66(7): 3390-6.
[367]
Green CA, Scarselli E, Sande CJ, et al. Chimpanzee adenovirus- and MVA-vectored respiratory syncytial virus vaccine is safe and immunogenic in adults. Sci Transl Med 2015; 7(300): e126.
[368]
Adderson E, Branum K, Sealy RE, et al. Safety and immunogenicity of an intranasal Sendai virus-based human parainfluenza virus type 1 vaccine in 3- to 6-year-old children. Clin Vaccine Immunol 2015; 22(3): 298-303.
[369]
Lambkin-Williams R, Gelder C, Broughton R, et al. An intranasal proteosome-adjuvanted trivalent influenza vaccine Is safe, immunogenic & efficacious in the human viral influenza challenge model. Serum IgG and Mucosal IgA are important correlates of protection against illness associated with infection. PLoS One 2016; 11(12): e0163089.
[370]
Madan A, Segall N, Ferguson M, et al. Immunogenicity and safety of an AS03-adjuvanted H7N9 pandemic influenza vaccine in a randomized trial in healthy adults. J Infect Dis 2016; 214(11): 1717-27.
[371]
Riddle MS, Kaminski RW, Williams C, et al. Safety and immunogenicity of an intranasal Shigella flexneri 2a Invaplex 50 vaccine. Vaccine 2011; 29(40): 7009-19.
[372]
Malkin E, Yogev R, Abughali N, et al. Safety and immunogenicity of a live attenuated RSV vaccine in healthy RSV-seronegative children 5 to 24 months of age. PLoS One 2013; 8(10): e77104.
[373]
Thorstensson R, Trollfors B, Al-Tawil N, et al. A phase I clinical study of a live attenuated Bordetella pertussis vaccine--BPZE1; a single centre, double-blind, placebo-controlled, dose-escalating study of BPZE1 given intranasally to healthy adult male volunteers. PLoS One 2014; 9(1): e83449.
[374]
Rudenko L, Kiseleva I, Stukova M, et al. Clinical testing of pre-pandemic live attenuated A/H5N2 influenza candidate vaccine in adult volunteers: results from a placebo-controlled, randomized double-blind phase I study. Vaccine 2015; 33(39): 5110-7.
[375]
Enose Y, Ui M, Miyake A, et al. Protection by intranasal immunization of a nef-deleted, nonpathogenic SHIV against intravaginal challenge with a heterologous pathogenic SHIV. Virology 2002; 298(2): 306-16.
[376]
Bolton DL, Song K, Wilson RL, et al. Comparison of systemic and mucosal vaccination: impact on intravenous and rectal SIV challenge. Mucosal Immunol 2012; 5(1): 41-52.
[377]
Egan MA, Chong SY, Rose NF, et al. Immunogenicity of attenuated vesicular stomatitis virus vectors expressing HIV type 1 Env and SIV Gag proteins: comparison of intranasal and intramuscular vaccination routes. AIDS Res Hum Retroviruses 2004; 20(9): 989-1004.
[378]
Egan MA, Chong SY, Megati S, et al. Priming with plasmid DNAs expressing interleukin-12 and simian immunodeficiency virus gag enhances the immunogenicity and efficacy of an experimental AIDS vaccine based on recombinant vesicular stomatitis virus. AIDS Res Hum Retroviruses 2005; 21(7): 629-43.
[379]
Fouda GG, Amos JD, Wilks AB, et al. Mucosal immunization of lactating female rhesus monkeys with a transmitted/founder HIV-1 envelope induces strong Env-specific IgA antibody responses in breast milk. J Virol 2013; 87(12): 6986-99.
[380]
Watkins JD, Sholukh AM, Mukhtar MM, 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(9): F13-20.
[381]
Sholukh AM, Watkins JD, Vyas HK, 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(17): 2086-95.
[382]
Pauthner M, Havenar-Daughton C, Sok D, et al. Elicitation of robust tier 2 neutralizing antibody responses in nonhuman primates by HIV envelope trimer immunization using optimized approaches. Immunity 2017; 46(6): 1073-88.

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