Induction of intestinal immunity by mucosal vaccines as a means of controlling HIV infection

AIDS Research and Human Retroviruses

Volumn 30, Issue 11, 2014, Pages 1027-1040

  Poles, Jordan ^a   Alvarez, Yelina ^a   Hioe, Catarina E ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HUMAN IMMUNODEFICIENCY VIRUS VACCINE;

CD4+ T LYMPHOCYTE; CYTOTOXIC T LYMPHOCYTE; DRUG ADMINISTRATION ROUTE; EPIDEMIC; GASTROINTESTINAL MUCOSA; GASTROINTESTINAL TRACT; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNIZATION; INFECTION CONTROL; INTERMETHOD COMPARISON; MUCOSAL IMMUNITY; NONHUMAN; PRIORITY JOURNAL; REVIEW; T CELL DEPLETION; HIV INFECTIONS; IMMUNOLOGY; INTESTINE MUCOSA; INTRANASAL DRUG ADMINISTRATION; MUCOSAL DRUG ADMINISTRATION; ORAL DRUG ADMINISTRATION; RECTAL DRUG ADMINISTRATION;

ADMINISTRATION, INTRANASAL; ADMINISTRATION, MUCOSAL; ADMINISTRATION, ORAL; ADMINISTRATION, RECTAL; AIDS VACCINES; HIV INFECTIONS; HUMANS; IMMUNITY, MUCOSAL; INTESTINAL MUCOSA;

EID: 84931464215     PISSN: 08892229     EISSN: 19318405     Source Type: Journal    
DOI: 10.1089/aid.2014.0233     Document Type: Review

References (129)

1. WHO, UNICEF, and UNAIDS: Progress report 2011: Global HIV/AIDS response. World Health Organization, Geneva, 2011.
2. Prejean J, Song R, Hernandez A, et al.: Estimated HIV incidence in the United States, 2006-2009. PLoS One 2011;6:e17502.
3. Palella, FJ, Delaney, KM, Moorman, AC, et al.: Declining morbidity and mortality among patients with advanced human immunodeficiency virus infection. N Engl J Med 1998;338:853-860.
4. Ho DD and Zhang L: HIV-1 rebound after anti-retroviral therapy. Nature Med 2000;6:736-737.
5. Summers T and Kates J: Trends in U.S. government funding for HIV/AIDS-fiscal years 1981 to 2004. Henry J. Kaiser Family Foundation. Available at http://kaiserfamilyfoundation.files.wordpress.com/2013/01/issue-brief-trends-in-u-s-government-funding-for-hiv-aids-fiscal-years-1981-to-2004.pdf.
6. Schackman BR, Gebo KA, Walensky RP, et al.: The lifetime cost of current human immunodeficiency virus care in the United States. Med Care 2006;44:990-997.
7. Mahy M, Tassie J-M, Ghys PD, et al.: Estimation of an-tiretroviral therapy coverage: Methodology and trends. Curr Opin HIV AIDS 2010;5:97-102.
8. Celum C and Baeten JM: Antiretroviral-based HIV-1 prevention: Antiretroviral treatment and pre-exposure prophylaxis. Antiviral Ther 2012;17:1483-1493.
9. Alistar SS, Grant PM, and Bendavid E: Comparative effectiveness and cost-effectiveness of antiretroviral therapy and pre-exposure prophylaxis for HIV prevention in South Africa. BMC Med 2014;12:46.
10. Cohen MS, Chen YQ, McCauley M, et al.: Prevention of HIV-1 infection with early antiretroviral therapy. N Engl J Med 2011;365:493-505.
11. Grant RM, Lama JR, Anderson PL, et al.: Preexposure chemoprophylaxis for HIV prevention in men who have sex with men. N Engl J Med 2010;363:2587-2599.
12. Thigpen MC, Kebaabetswe PM, Paxton LA, et al.: Anti-retroviral preexposure prophylaxis for heterosexual HIV transmission in Botswana N Engl J Med 2012;367: 423-434.
13. Baeten JM, Donnell D, Ndase P, et al.: Antiretroviral prophylaxis for HIV prevention in heterosexual men and women. N Engl J Med 2012;367:399-410.
14. Choopanya K, Martin M, Suntharasama P, et al.: Anti-retroviral prophylaxis for HIV infection in injecting drug users in Bangkok, Thailand (the Bangkok Tenofovir Study): A randomised, double-blind, placebo-controlled phase 3 trial. Lancet 2013;381:2083-2090.
15. Mellors JW, Rinaldo CRJ, Gupta P, et al.: Prognosis in HIV-1 infection predicted by the quantity of virus in plasma. Science 1996;272:1167-1170.
16. Whitney JB, Hill AL, Sanisetty S, et al.: Rapid seeding of the viral reservoir prior to SIV viraemia in rhesus monkeys. Nature 2014;512:74-77.
17. Pitisuttithum P, Gilbert P, Gurwith M, et al.: Randomized, double-blind, placebo-controlled efficacy trial of a bivalent recombinant glycoprotein 120 HIV-1 vaccine among injection drug users in Bangkok, Thailand. J Infect Dis 2006;194:1661-1671.
18. Flynn NM, Forthal DN, Harro CD, et al.: Placebo-controlled phase 3 trial of a recombinant glycoprotein 120 vaccine to prevent HIV-1 infection. J Infect Dis 2005;191: 654-665.
19. Buchbinder SP, Mehrotra DV, Duerr A, et al.: Efficacy assessment of a cell-mediated immunity HIV-1 vaccine (the Step Study): A double-blind, randomised, placebo-controlled, test-of-concept trial. Lancet 2008;372:1881-1893.
20. 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;361:2209-2220.
21. Barouch DH and Deeks SG: Immunologic strategies for HIV-1 remission and eradication. Science 2014;345: 169-174.
22. Nitayaphan S, Pitisuttithum P, Karnasuta C, et al.: Safety and immunogenicity of an HIV subtype B and E prime-boost vaccine combination in HIV-negative Thai adults. J Infect Dis 2004;190:702-706.
23. De Souza MS, Ratto-Kim S, Chuenarom W, et al.: The Thai phase III trial (RV144) vaccine regimen induces T cell responses that preferentially target epitopes within the V2 region of HIV-1 envelope. J Immunol 2012;188: 5166-5176.
24. Haynes BF, Gilbert PB, McElrath MJ, et al.: Immune-correlates analysis of an HIV-1 vaccine efficacy trial. N Engl J Med 2012;366:1275-1286.
25. Arthos J, Cicala C, Martinelli E, et al.: HIV-1 envelope protein binds to and signals through integrin a4b7, the gut mucosal homing receptor for peripheral T cells. Nat Immunol 2008;9:301-309.
26. Cicala C, Martinelli E, McNally JP, et al.: The integrin alpha4beta7 forms a complex with cell-surface CD4 and defines a T-cell subset that is highly susceptible to infection by HIV-1. Proc Natl Acad Sci USA 2009;106: 20877-20882.
27. Ansari AA, Reimann KA, Mayne AE, et al.: Blocking of a4b7 gut-homing integrin during acute infection leads to decreased plasma and gastrointestinal tissue viral loads in simian immunodeficiency virus-infected rhesus macaques. J Immunol 2011;186(2):1044-1059.
28. Burgess MJ and Kasten MJ: Human immunodeficiency virus: What primary care clinicians need to know. Mayo Clinic Proc 2013;88:1468-1474.
29. 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;200:749-759.
30. 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;200:761-770.
31. Veazey RS, DeMaria M, Chalifoux LV, et al.: Gastrointestinal tract as a major site of CD4 + T cell depletion and viral replication in SIV infection. Science 1998;280: 427-431.
32. Bolton DL, Song K, Wilson RL, et al.: Comparison of systemic and mucosal vaccination: Impact on intravenous and rectal SIV challenge. Mucosal Immunol 2012;5:41-52.
33. Moir S, Chun T-W, and Fauci AS: Pathogenic mechanisms of HIV disease. Annu Rev Pathol 2011;6:223-248.
34. Brenchley JM, Paiardini M, Knox KS, et al.: Differential Th17 CD4 T-cell depletion in pathogenic and nonpatho-genic lentiviral infections. Blood 2008;112:2826-2835.
35. Cecchinato V, Trindade CJ, Laurence A, et al.: Altered balance between Th17 and Th1 cells at mucosal sites predicts AIDS progression in simian immunodeficiency virus-infected macaques. Mucosal Immunol 2008;1: 279-288.
36. Kader M, Wang X, Piatak M, et al.: Alpha4(+) beta7(hi)CD4(+) memory T cells harbor most Th-17 cells and are preferentially infected during acute SIV infection. Mucosal Immunol 2009;2:439-449.
37. Favre D, Lederer S, Kanwar B, et al.: Critical loss of the balance between Th17 and T regulatory cell populations in pathogenic SIV infection. PLoS Pathog 2009;5: e1000295.
38. Macal M, Sankaran S, Chun T-W, et al.: Effective CD4 + T-cell restoration in gut-associated lymphoid tissue of HIV-infected patients is associated with enhanced Th17 cells and polyfunctional HIV-specific T-cell responses. Mucosal Immunol 2008;1:475-48
39. El Hed A, Khaitan A, Kozhaya L, et al.: Susceptibility of human Th17 cells to human immunodeficiency virus and their perturbation during infection. J Infect Dis 2010;201: 843-854.
40. Kim CJ, McKinnon LR, Kovacs C, et al.: Mucosal Th17 cell function is altered during HIV infection and is an independent predictor of systemic immune activation. J Immunol 2013;191:2164-2173.
41. Alvarez Y, Tuen M, Shen G, et al.: Preferential HIV infection of CCR6 + Th17 cells is associated with higher levels of virus receptor expression and lack of CCR5 li-gands. J Virol 2013;87:10843-10854.
42. Alvarez Y, Tuen M, Nadas A. and Hioe CE: In vitro restoration of Th17 response during HIV infection with an antiretroviral drug and Th17 differentiation cytokines. AIDS Res Hum Retroviruses 2012;28:823-834.
43. Wolk K, Witte E, Wallace E, et al.: IL-22 regulates the expression of genes responsible for antimicrobial defense, cellular differentiation, and mobility in keratinocytes: A potential role in psoriasis. Eur J Immunol 2006;36: 1309-1323.
44. Li Q, Estes JD, Duan L, et al.: Simian immunodeficiency virus-induced intestinal cell apoptosis is the underlying mechanism of the regenerative enteropathy of early infection. J Infect Dis 2008;197:420-429.
45. Kim CJ, Nazli A, Rojas OL, et al.: A role for mucosal IL-22 production and Th22 cells in HIV-associated mu-cosal immunopathogenesis. Mucosal Immunol 2012;5: 670-680.
46. Brenchley JM, Price DA, Schacker TW, et al.: Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat Med 2006;12:1365-1371.
47. Kristoff J, Haret-Richter G, Ma D, et al.: Early microbial translocation blockade reduces SIV-mediated inflammation and viral replication. J Clin Invest 2014;124: 2802-2806.
48. Quiñones-Mateu. ME, Lederman. MM, Feng. Z, et al.: Human epithelial beta-defensins 2 and 3 inhibit HIV-1 replication. AIDS (London, England) 2003;17:F39-48.
49. Lafferty MK, Sun L, DeMasi L, Lu W, and Garzino-Demo A: CCR6 ligands inhibit HIV by inducing APOBEC3G. Blood 2010;115:1564-1571.
50. Bienenstock J and McDermott M: A common mucosal immunologic system involving the bronchus, breast and bowel. Adv Exp Med Biol 1978;107:53-59.
51. Holmgren J and Czerkinsky C: Mucosal immunity and vaccines. Nat Med 2005;11:S45-S53.
52. Czerkinsky C and Holmgren J: Topical immunization strategies. Mucosal Immunol 2010;3(6):545-555.
53. Ciabattini A, Pettin E, Arsenijevic S, Pozzi G, and Me-daglini D: Intranasal immunization with vaccine vector Streptococcus gordonii elicits primed CD4 + and CD8 + T cells in the genital and intestinal tracts. Vaccine 2010; 28:1226-1233.
54. Liu X, Yang T, Sun QM, and Sun MS: Efficient intranasal immunization of newborn mice with recombinant adeno-virus expressing rotavirus protein VP4 against oral rota-virus infection. Acta Virol 2005;49:17-22.
55. Mora, JR, Iwata, M, Eksteen, B, et al.: Generation of gut-homing IgA-secreting B cells by intestinal dendritic cells. Science 2006;314:1157-1160.
56. Iwata M, Hirakiyama A, Eshima Y, et al.: Retinoic acid imprints gut-homing specificity on T cells. Immunity 2004;21:527-538.
57. Ranasinghe C and Ramshaw I: Immunisation route-dependent expression of IL-4/IL-13 can modulate HIV-specific CD8(+) CTL avidity. Eur J Immunol 2009;39: 1819-1830.
58. 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;107:3258-3264.
59. Xiao P, Patterson LJ, Kuate S, et al.: Replicating adeno-virus-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) ch. J Virol 2012;86:4644-4657.
60. Chin'ombe N, Bourn WR, Williamson A-L, and 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.
61. Fouts TR, Tuskan RG, Chada S, Hone DM, and Lewis GK: Construction and immunogenicity of Salmonella typhimurium vaccine vectors that express HIV-1 gp120. Vaccine 1995;13:1697-1705.
62. 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;11:909-920.
63. Shata MT, Reitz MS, DeVico AL, Lewis GK, and 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;20:623-629.
64. Kaneko H, Bednarek I, Wierzbicki A, et al.: Oral DNA vaccination promotes mucosal and systemic immune responses to HIV envelope glycoprotein. Virology 2000; 267:8-16.
65. Peng B, Wang LR, Gómez-Román VR, et al.: Replicating rather than nonreplicating adenovirus-human immunodeficiency virus recombinant vaccines are better at eliciting potent cellular immunity and priming high-titer antibodies. J Virol 2005;79:10200-10209.
66. Zhou Q, Hidajat R, Peng B, and Venzon D: Comparative evaluation of oral and intranasal priming with replication-competent adenovirus 5 host range mutant (Ad5hr)-simian immunodeficiency virus (SIV) recombinant vaccines on immunogenicity and protective efficacy against SIV(-mac251). Vaccine 2007;25:8021-8035.
67. 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;83:791-801.
68. Bukh I, Calcedo R, Roy S, et al.: Increased mucosal CD4+ T cell activation in rhesus macaques following vaccination with an adenoviral vector. J Virol 2014; 88(15):8468-8478.
69. Benlahrech A, Harris J, Meiser A, et al.: Adenovirus vector vaccination induces expansion of memory CD4 T cells with a mucosal homing phenotype that are readily susceptible to HIV-1. Proc Natl Acad Sci USA 2009; 106(47):19940-19945.
70. Masek-Hammerman K, Li H, Liu J, et al.: Mucosal trafficking of vector-specific CD4 + T lymphocytes following vaccination of rhesus monkeys with adenovirus serotype 5. J Virol 2010;88:9810-9816.
71. O'Brien KL, Liu J, King SL, et al.: Adenovirus-specific immunity after immunization with an Ad5 HIV-1 vaccine candidate in humans. Nat Med 2009;15.8: 873-875.
72. Nwanegbo E, Vardas E, Gao W, et al.: Prevalence of neutralizing antibodies to adenoviral serotypes 5 and 35 in the adult populations of The Gambia, South Africa, and the United States. Clin Diagnos Lab Immunol 2004;11: 351-357.
73. Takamura S, Niikura M, Li T.C, et al.: DNA vaccine-encapsulated virus-like particles derived from an orally transmissible virus stimulate mucosal and systemic immune responses by oral administration. Gene Ther 2004; 11:628-635.
74. Jensen K, dela 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.
75. Lin SW, Cun AS, Harris-McCoy K, and Ertl HC: Intramuscular rather than oral administration of replication-defective adenoviral vaccine vector induces specific CD8+ T cell responses in the gut. Vaccine 2007;25: 2187-2193.
76. Wang L, Cheng C, Ko S-Y, et al.: Delivery of human immunodeficiency virus vaccine vectors to the intestine induces enhanced mucosal cellular immunity. J Virol 2009;83:7166-7175.
77. Cuburu N, Kweon M-N, Song J-H, et al.: Sublingual immunization induces broad-based systemic and mucosal immune responses in mice. Vaccine 2007;25:8598-8610.
78. Mercier G, Nehete P, and Passeri M: Oral immunization of rhesus macaques with adenoviral HIV vaccines using enteric-coated capsules. Vaccine 2007;25:8687-8701.
79. Mestecky J, Russell MW, and Elson CO: Perspectives on mucosal vaccines: Is mucosal tolerance a barrier? J Immunol 2007;179:5633-5638.
80. Guetard D, Greco R, Cervantes Gonzalez M, et al.: Im-munogenicity and tolerance following HIV-1/HBV plant-based oral vaccine administration. Vaccine 2008;26: 4477-4485.
81. Shim B-S, Choi Y, Cheon IS, and Song MK: Sublingual delivery of vaccines for the induction of mucosal immunity. Immune Network 2013;13:81-85.
82. Cuburu N, Kweon MN, Hervouet C, et al.: Sublingual immunization with nonreplicating antigens induces antibody-forming cells and cytotoxic T cells in the female genital tract mucosa and protects against genital papillo-mavirus infection. J Immunol 2009;183:7851-7859.
83. Hervouet C, Luci C, Cuburu N, et al.: Sublingual immunization with an HIV subunit vaccine induces antibodies and cytotoxic T cells in the mouse female genital tract. Vaccine 2010;28:5582-5590.
84. 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;87:4738-4750.
85. Manrique M, Kozlowski PA, Cobo-Molinos A, et al.: Resistance to infection, early and persistent suppression of simian immunodeficiency virus SIVmac251 viremia, and significant reduction of tissue viral burden after mucosal vaccination in female rhesus macaques. J Virol 2014;88: 212-224.
86. Song J-H, Nguyen HH, Cuburu N, et al.: Sublingual vaccination with influenza virus protects mice against lethal viral infection. Proc Natl Acad Sci USA 2008;105: 1644-1649.
87. Appledorn DM, Aldhamen YA, Godbehere S, Seregin SS, and Amalfitano A: Sublingual administration of an ade-novirus serotype 5 (Ad5)-based vaccine confirms Toll-like receptor agonist activity in the oral cavity and elicits improved mucosal and systemic cell-mediated responses against HIV antigens despite preexisting Ad5 immunity. Clin Vaccine Immunol: CVI 2011;18:150-160.
88. Vagenas P, Williams VG, Piatak M, et al.: Tonsillar application of AT-2 SIV affords partial protection against rectal challenge with SIVmac239. J Acquir Immune Defic Syndr 2009;52:433-442.
89. Stahl-Hennig C, Kuate S, Franz M, et al.: Atraumatic oral spray immunization with replication-deficient viral vector vaccines. J Virol 2007;81:13180-13190.
90. Earl PL, Americo JL, Wyatt LS, et al.: Recombinant modified vaccinia virus Ankara provides durable protection against disease caused by an immunodeficiency virus as well as long-term immunity to an orthopoxvirus in a non-human primate. Virology 2007;366:84-97.
91. Shiver JW, Fu TM, Chen L, et al.: Replication-incompetent adenoviral vaccine vector elicits effective anti-immunodeficiency-virus immunity. Nature 2002;415.6869: 331-335.
92. Kraan H, Vrieling H, Czerkinsky C, et al.: Buccal and sublingual vaccine delivery. J Control Rel 2014;190(28): 580-592.
93. Shapiro SZ: Clinical development of candidate HIV vaccines: Different problems for different vaccines. AIDS Res Hum Retroviruses 2014;30.4:325-329.
94. Ruane D, Brane L, Reis BS, et al.: Lung dendritic cells induce migration of protective T cells to the gastrointestinal tract. J Exp Med 2013;210:1871-1888.
95. Goldoni AL, Maciel M Jr, Rigato PO, et al.: Mucosal and systemic anti-GAG immunity induced by neonatal immunization with HIV LAMP/gag DNA vaccine in mice. Immunobiology 2011;216:505-512.
96. Kaufman DR, Liu J, Carville A, et al.: Trafficking of antigen-specific CD8 + T lymphocytes to mucosal surfaces following intramuscular vaccination. J Immunol 2008;181(6):4188-4198.
97. Liu J, O'Brien KL, Lynch DM, et al.: Immune control of an SIV challenge by a T-cell-based vaccine in rhesus monkeys. Nature 2008;457(7225):87-91.
98. Ranasinghe C, Medveczky JC, Woltring D, et al.: Evaluation of fowlpox-vaccinia virus prime-boost vaccine strategies for high-level mucosal and systemic immunity against HIV-1. Vaccine 2006;24:5881-5895.
99. Ranasinghe C, Turner SJ, McArthur C, et al.: Mucosal HIV-1 pox virus prime-boost immunization induces high-avidity CD8 + T cells with regime-dependent cytokine/granzyme B profiles. J Immunol 2007;178: 2370-2379.
100. Manrique M, Kozlowski PA, Wang S.W, et al.: Nasal DNA-MVA SIV vaccination provides more significant protection from progression to AIDS than a similar intramuscular vaccination. Mucosal Immunol 2009;2:536-550.
101. Mothe BR, Weinfurter J, Wang C, et al.: Expression of the major histocompatibility complex class I molecule Mamu-A∗01 is associated with control of simian immunodeficiency virus SIVmac239 replication. J Virol 2003; 77(4):2736-2740.
102. Muhl T, Krawczak M, Ten Haaft P, et al.: MHC class I alleles influence set-point viral load and survival time in simian immunodeficiency virus-infected rhesus monkeys. J Immunol 2002;169(6):3438-3446.
103. Bertley FMN, Kozlowski PA, Wang S-W, 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;172:3745-3757.
104. Lemiale F, Kong W, Akyu LM, et al.: Enhanced mucosal immunoglobulin A response of intranasal adenoviral vector human immunodeficiency virus vaccine and localization in the central nervous system. J Virol 2003;77: 10078-10087.
105. Croyle MA, Patel A, Tran KN, et al.: Nasal delivery of an adenovirus-based vaccine bypasses pre-existing immunity to the vaccine carrier and improves the immune response in mice. PloS One 2008;3:e3548.
106. Cristillo A and Ferrari M: Induction of mucosal and systemic antibody and T-cell responses following prime-boost immunization with novel adjuvanted human immunodeficiency virus-1-vaccine formulations. J Gen Virol 2011;92:128-140.
107. Lewis DJM, 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:e6999.
108. Couch RB: Nasal vaccination, Escherichia coli entero-toxin, and Bell's palsy. N Engl J Med 2004;350:860-861.
109. Armstrong ME, Lavelle EC, Loscher CE, Lynch Ma, and Mills KHG: Proinflammatory responses in the murine brain after intranasal delivery of cholera toxin: Implications for the use of AB toxins as adjuvants in intranasal vaccines. J Infect Dis 2005;192:1628-1633.
110. Ginkel FW van, Jackson RJ, Yoshino N, et al.: En-terotoxin-based mucosal adjuvants alter antigen trafficking induce inflammatory responses in the nasal tract. Infect Immun 2005;73:6892-6902.
111. Ginkel FW van, Jackson RJ, Yuki Y, and McGhee JR: Cutting edge: The mucosal adjuvant cholera toxin redirects vaccine proteins into olfactory tissues. J Immunol 2000;165:4778-4782.
112. Smith A, Perelma M, and Hinchcliffe M: Chitosan: A promising safe and immune-enhancing adjuvant for in-tranasal vaccines. Hum Vaccines Immunother 2014;10(3): 797-807.
113. Kobayashi T, Fukushima K, Sannan T, et al.: Evaluation of the effectiveness and safety of chitosan derivatives as adjuvants for intranasal vaccines. Viral Immunol 2013;26: 133-142.
114. Belyakov IM, Isakov D, Zhu Q, Dzutsev A, and Berzofsky JA: A novel functional CTL avidity/activity compart-mentalization to the site of mucosal immunization contributes to protection of macaques against simian/human immunodeficiency viral depletion of mucosal CD4 + T cells. J Immunol 2007;178:7211-7221.
115. 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;7:1320-1326.
116. Belyakov IM, Derby MA, Ahlers JD, et al.: Mucosal immunization with HIV-1 peptide vaccine induces mu-cosal and systemic cytotoxic T lymphocytes and protective immunity in mice against intrarectal recombinant HIV-vaccinia challenge. Proc Natl Acad Sci USA 1998; 95:1709-1714.
117. Murph JR, Grose C, McAndrew P, et al.: Sabin inactivated trivalent poliovirus vaccine: First clinical trial and ser-oimmunity survey. Pediatr Infect Dis J1988;7:760-765.
118. Cáceres VM and Sutter RW: Sabin monovalent oral polio vaccines: Review of past experiences and their potential use after polio eradication. Clin Infect Dis 2001;33:531-541.
119. Yen C, Tate JE, Hyde TB, et al.: Rotavirus vaccines: Current status and future considerations. Hum Vaccines Immunotherapeut 2014;10(6):1436-1448.
120. Cortes JE, Curns AT, Tate JE, et al.: Rotavirus vaccine and health care utilization for diarrhea in U.S. children. N Engl J Med 2011;365:1108-1117.
121. Ciarlet M and Schödel F: Development of a rotavirus vaccine: Clinical safety, immunogenicity, and efficacy of the pentavalent rotavirus vaccine, RotaTeq. Vaccine 2009; Suppl 6:G72-81.
122. Kabir S: The compositions and protective efficacies of the oral killed cholera vaccines: A critical analysis. Clin Vaccine Immunol: CVI 2014;21(9):1195-1205.
123. Gabutti G, Aquilina M, Cova M, et al.: Prevention of fecal-orally transmitted diseases in travelers through an oral anticholeric vaccine (WC/rBS). J Prevent Med Hyg 2012;53:199-203.
124. Charles RC, Hilaire IJ, Mayo-Smith LM, et al.: Im-munogenicity of a killed bivalent (O1 and O139) whole cell oral cholera vaccine, Shanchol, in Haiti. PLoS Negl Trop Dis 2014;8:e2828.
125. Pastor M, Pedraz JL, and Esquisabel A: The state-of-the-art of approved and under-development cholera vaccines. Vaccine 2013;31:4069-4078.
126. Bhuiyan TR, Choudhury FK, Khanam F, et al.: Evaluation of immune responses to an oral typhoid vaccine, Ty21a, in children from 2 to 5 years of age in Bangladesh. Vaccine 2014;32:1055-1060.
127. Levine MM, Ferreccio C, Black RE, and Germanier R: Large-scale field trial of Ty21a live oral typhoid vaccine in enteric-coated capsule formulation. Lancet 1987;1:1049-1052.
128. Levine MM, Ferreccio C, Abrego P, et al.: Duration of efficacy of Ty21a, attenuated Salmonella typhi live oral vaccine. Vaccine 1999;17(Suppl 2):S22-27.
129. Esposito S, Montinaro V, Groppali E, et al.: Live attenuated intranasal influenza vaccine. Hum Vaccines Im-munother 2012;8:76-80.