Recent progress towards development of a Shigella vaccine

References

• UNICEF/WHO. Diarrhea: why children are still dying and what can be done (2009).
   Google Scholar
• Ahs W, Tao W, Löfgren J, Forsberg BC. Diarrheal diseases in low- and middle-income countries: incidence, prevention and management. Open Infect. Dis. J. 4, 113–124 (2010).
   Google Scholar
• Lorntz B, Soares AM, Moore SR et al. Early childhood diarrhea predicts impaired school performance. Pediatr. Infect. Dis. J. 25(6), 513–520 (2006).
   PubMed Web of Science ®Google Scholar
• Moore SR, Lima AA, Conaway MR, Schorling JB, Soares AM, Guerrant RL. Early childhood diarrhoea and helminthiases associate with long-term linear growth faltering. Int. J. Epidemiol. 30(6), 1457–1464 (2001).
   PubMed Web of Science ®Google Scholar
• Kotloff KL, Winickoff JP, Ivanoff B et al. Global burden of Shigella infections: implications for vaccine development and implementation of control strategies. Bull. World Health Organ. 77(8), 651–666 (1999).
   PubMed Web of Science ®Google Scholar
• Bardhan P, Faruque AS, Naheed A, Sack DA. Decrease in shigellosis-related deaths without Shigella spp.-specific interventions, Asia. Emerging Infect. Dis. 16(11), 1718–1723 (2010).
   PubMed Web of Science ®Google Scholar
• Levine MM, Kotloff KL, Barry EM, Pasetti MF, Sztein MB. Clinical trials of Shigella vaccines: two steps forward and one step back on a long, hard road. Nat. Rev. Microbiol. 5(7), 540–553 (2007).
   PubMed Web of Science ®Google Scholar
• Ashkenazi S, Levy I, Kazaronovski V, Samra Z. Growing antimicrobial resistance of Shigella isolates. J. Antimicrob. Chemother. 51(2), 427–429 (2003).
   PubMed Web of Science ®Google Scholar
• DuPont HL, Levine MM, Hornick RB, Formal SB. Inoculum size in shigellosis and implications for expected mode of transmission. J. Infect. Dis. 159(6), 1126–1128 (1989).
   PubMed Web of Science ®Google Scholar
• Levine MM, DuPont HL, Formal SB et al. Pathogenesis of Shigella dysenteriae 1 (Shiga) dysentery. J. Infect. Dis. 127(3), 261–270 (1973).
   PubMed Web of Science ®Google Scholar
• Niyogi SK. Shigellosis. J. Microbiol. 43(2), 133–143 (2005).
   PubMed Web of Science ®Google Scholar
• Greco KM, McDonough MA, Butterton JR. Variation in the Shiga toxin region of 20th-century epidemic and endemic Shigella dysenteriae 1 strains. J. Infect. Dis. 190(2), 330–334 (2004).
   PubMedGoogle Scholar
• von Seidlein L, Kim DR, Ali M et al. A multicentre study of Shigella diarrhoea in six Asian countries: disease burden, clinical manifestations, and microbiology. PLoS Med. 3(9), e353 (2006).
   PubMed Web of Science ®Google Scholar
• Niyogi SK. Increasing antimicrobial resistance–an emerging problem in the treatment of shigellosis. Clin. Microbiol. Infect. 13(12), 1141–1143 (2007).
   PubMed Web of Science ®Google Scholar
• Schroeder GN, Hilbi H. Molecular pathogenesis of Shigella spp.: controlling host cell signaling, invasion, and death by type III secretion. Clin. Microbiol. Rev. 21(1), 134–156 (2008).
   PubMed Web of Science ®Google Scholar
• Sansonetti PJ. Shigellosis: an old disease in new clothes? PLoS Med. 3(9), e354 (2006).
   PubMedGoogle Scholar
• Sansonetti PJ. War and peace at mucosal surfaces. Nat. Rev. Immunol. 4(12), 953–964 (2004).
   PubMed Web of Science ®Google Scholar
• Sansonetti PJ. To be or not to be a pathogen: that is the mucosally relevant question. Mucosal Immunol. 4(1), 8–14 (2011).
   PubMed Web of Science ®Google Scholar
• Phalipon A, Sansonetti PJ. Shigella’s ways of manipulating the host intestinal innate and adaptive immune system: a tool box for survival? Immunol. Cell Biol. 85(2), 119–129 (2007).
   PubMed Web of Science ®Google Scholar
• Sansonetti PJ. The bacterial weaponry: lessons from Shigella. Ann. N. Y. Acad. Sci. 1072, 307–312 (2006).
   PubMedGoogle Scholar
• Van Gijsegem F, Genin S, Boucher C. Conservation of secretion pathways for pathogenicity determinants of plant and animal bacteria. Trends Microbiol. 1(5), 175–180 (1993).
   PubMedGoogle Scholar
• Formal SB, Oaks EV, Olsen RE, Wingfield-Eggleston M, Snoy PJ, Cogan JP. Effect of prior infection with virulent Shigella flexneri 2a on the resistance of monkeys to subsequent infection with Shigella sonnei. J. Infect. Dis. 164(3), 533–537 (1991).
   PubMed Web of Science ®Google Scholar
• Robbins JB, Chu C, Schneerson R. Hypothesis for vaccine development: protective immunity to enteric diseases caused by nontyphoidal salmonellae and shigellae may be conferred by serum IgG antibodies to the O-specific polysaccharide of their lipopolysaccharides. Clin. Infect. Dis. 15(2), 346–361 (1992).
   PubMed Web of Science ®Google Scholar
• Noriega FR, Liao FM, Maneval DR, Ren S, Formal SB, Levine MM. Strategy for cross-protection among Shigella flexneri serotypes. Infect. Immun. 67(2), 782–788 (1999).
   PubMed Web of Science ®Google Scholar
• Kotloff KL, Nataro JP, Losonsky GA et al. A modified Shigella volunteer challenge model in which the inoculum is administered with bicarbonate buffer: clinical experience and implications for Shigella infectivity. Vaccine 13(16), 1488–1494 (1995).
   PubMed Web of Science ®Google Scholar
• Cohen D, Green MS, Block C, Slepon R, Lerman Y. Natural immunity to shigellosis in two groups with different previous risks of exposure to Shigella is only partly expressed by serum antibodies to lipopolysaccharide. J. Infect. Dis. 165(4), 785–787 (1992).
   PubMedGoogle Scholar
• Cohen D, Green MS, Block C, Slepon R, Ofek I. Prospective study of the association between serum antibodies to lipopolysaccharide O antigen and the attack rate of shigellosis. J. Clin. Microbiol. 29(2), 386–389 (1991).
   PubMed Web of Science ®Google Scholar
• Oberhelman RA, Kopecko DJ, Salazar-Lindo E et al. Prospective study of systemic and mucosal immune responses in dysenteric patients to specific Shigella invasion plasmid antigens and lipopolysaccharides. Infect. Immun. 59(7), 2341–2350 (1991).
   PubMed Web of Science ®Google Scholar
• Islam D, Wretlind B, Ryd M, Lindberg AA, Christensson B. Immunoglobulin subclass distribution and dynamics of Shigella-specific antibody responses in serum and stool samples in shigellosis. Infect. Immun. 63(5), 2054–2061 (1995).
   PubMed Web of Science ®Google Scholar
• Orr N, Robin G, Lowell G, Cohen D. Presence of specific immunoglobulin A-secreting cells in peripheral blood after natural infection with Shigella sonnei. J. Clin. Microbiol. 30(8), 2165–2168 (1992).
   PubMed Web of Science ®Google Scholar
• Li A, Rong ZC, Ekwall E, Forsum U, Lindberg AA. Serum antibody responses against Shigella lipopolysaccharides and invasion plasmid-coded antigens in Shigella infected Swedish patients. Scand. J. Infect. Dis. 25(5), 569–577 (1993).
   PubMed Web of Science ®Google Scholar
• Orr N, Robin G, Cohen D, Arnon R, Lowell GH. Immunogenicity and efficacy of oral or intranasal Shigella flexneri 2a and Shigella sonnei proteosome-lipopolysaccharide vaccines in animal models. Infect. Immun. 61(6), 2390–2395 (1993).
   PubMed Web of Science ®Google Scholar
• Al-Hasani K, Navarro-Garcia F, Huerta J, Sakellaris H, Adler B. The immunogenic SigA enterotoxin of Shigella flexneri 2a binds to HEp-2 cells and induces fodrin redistribution in intoxicated epithelial cells. PLoS ONE 4(12), e8223 (2009).
   PubMed Web of Science ®Google Scholar
• Oaks EV, Hale TL, Formal SB. Serum immune response to Shigella protein antigens in rhesus monkeys and humans infected with Shigella spp. Infect. Immun. 53(1), 57–63 (1986).
   PubMed Web of Science ®Google Scholar
• Van de Verg LL, Herrington DA, Boslego J, Lindberg AA, Levine MM. Age-specific prevalence of serum antibodies to the invasion plasmid and lipopolysaccharide antigens of Shigella species in Chilean and North American populations. J. Infect. Dis. 166(1), 158–161 (1992).
   PubMedGoogle Scholar
• Mukhopadhaya A, Mahalanabis D, Chakrabarti MK. Role of Shigella flexneri 2a 34 kDa outer membrane protein in induction of protective immune response. Vaccine 24(33–34), 6028–6036 (2006).
   PubMedGoogle Scholar
• Kaminski RW, Oaks EV. Inactivated and subunit vaccines to prevent shigellosis. Expert Rev. Vaccines 8(12), 1693–1704 (2009).
   PubMed Web of Science ®Google Scholar
• Biswas A, Banerjee P, Mukherjee G, Biswas T. Porin of Shigella dysenteriae activates mouse peritoneal macrophage through Toll-like receptors 2 and 6 to induce polarized type I response. Mol. Immunol. 44(5), 812–820 (2007).
   PubMedGoogle Scholar
• Bagchi AK, Sinha AK. Role of 57 kDa major antigenic component of Shigella dysenteriae outer membrane proteins in induction of major histocompatibility complex II-restricted T-cell response. Arch. Med. Res. 35(5), 427–434 (2004).
   PubMedGoogle Scholar
• Pore D, Mahata N, Pal A, Chakrabarti MK. Outer membrane protein A (OmpA) of Shigella flexneri 2a, induces protective immune response in a mouse model. PLoS ONE 6(7), e22663 (2011).
   PubMedGoogle Scholar
• Fasano A, Noriega FR, Maneval DR Jr et al. Shigella enterotoxin 1: an enterotoxin of Shigella flexneri 2a active in rabbit small intestine in vivo and in vitro. J. Clin. Invest. 95(6), 2853–2861 (1995).
   PubMed Web of Science ®Google Scholar
• Wu T, Grassel C, Levine MM, Barry EM. Live attenuated Shigella dysenteriae type 1 vaccine strains overexpressing shiga toxin B subunit. Infect. Immun. 79(12), 4912–4922 (2011).
   PubMed Web of Science ®Google Scholar
• Venkatesan MM, Hartman AB, Newland JW et al. Construction, characterization, and animal testing of WRSd1, a Shigella dysenteriae 1 vaccine. Infect. Immun. 70(6), 2950–2958 (2002).
   PubMedGoogle Scholar
• Launay O, Sadorge C, Jolly N et al. Safety and immunogenicity of SC599, an oral live attenuated Shigella dysenteriae type-1 vaccine in healthy volunteers: results of a Phase 2, randomized, double-blind placebo-controlled trial. Vaccine 27(8), 1184–1191 (2009).
   PubMedGoogle Scholar
• Neutra MR, Kozlowski PA. Mucosal vaccines: the promise and the challenge. Nat. Rev. Immunol. 6(2), 148–158 (2006).
   PubMed Web of Science ®Google Scholar
• Levine MM. Immunization against bacterial diseases of the intestine. J. Pediatr. Gastroenterol. Nutr. 31(4), 336–355 (2000).
   PubMedGoogle Scholar
• Lamm ME. Interaction of antigens and antibodies at mucosal surfaces. Annu. Rev. Microbiol. 51, 311–340 (1997).
   PubMed Web of Science ®Google Scholar
• Levine MM. Immunogenicity and efficacy of oral vaccines in developing countries: lessons from a live cholera vaccine. BMC Biol. 8, 129 (2010).
   PubMed Web of Science ®Google Scholar
• Sutter RW, Maher C. Mass vaccination campaigns for polio eradication: an essential strategy for success. Curr. Top. Microbiol. Immunol. 304, 195–220 (2006).
   PubMed Web of Science ®Google Scholar
• Andrianarivelo MR, Boisier P, Rabarijaona L, Ratsitorahina M, Migliani R, Zeller H. Mass vaccination campaigns to eradicate poliomyelitis in Madagascar: oral poliovirus vaccine increased immunity of children who missed routine programme. Trop. Med. Int. Health 6(12), 1032–1039 (2001).
   PubMedGoogle Scholar
• Mitragotri S. Immunization without needles. Nat. Rev. Immunol. 5(12), 905–916 (2005).
   PubMed Web of Science ®Google Scholar
• Kersten G, Hirschberg H. Needle-free vaccine delivery. Expert Opin. Drug Deliv. 4(5), 459–474 (2007).
   PubMed Web of Science ®Google Scholar
• Pavot V, Rochereau N, Genin C, Verrier B, Paul S. New insights in mucosal vaccine development. Vaccine 30(2), 142–154 (2012).
   PubMed Web of Science ®Google Scholar
• Clemens J. Evaluation of vaccines against enteric infections: a clinical and public health research agenda for developing countries. Philos. Trans. R. Soc. Lond. B Biol. Sci. 366(1579), 2799–2805 (2011).
   PubMedGoogle Scholar
• Patriarca PA, Wright PF, John TJ. Factors affecting the immunogenicity of oral poliovirus vaccine in developing countries: review. Rev. Infect. Dis. 13(5), 926–939 (1991).
   PubMedGoogle Scholar
• Hallander HO, Paniagua M, Espinoza F et al. Calibrated serological techniques demonstrate significant different serum response rates to an oral killed cholera vaccine between Swedish and Nicaraguan children. Vaccine 21(1–2), 138–145 (2002).
   PubMed Web of Science ®Google Scholar
• Future needs and directions for Shigella vaccines. Wkly Epidemiol. Rec. 81(6), 51–58 (2006).
   Google Scholar
• Serazin AC, Shackelton LA, Wilson C, Bhan MK. Improving the performance of enteric vaccines in the developing world. Nat. Immunol. 11(9), 769–773 (2010).
   PubMedGoogle Scholar
• Baqui AH, Black RE, El Arifeen S et al. Effect of zinc supplementation started during diarrhoea on morbidity and mortality in Bangladeshi children: community randomised trial. BMJ 325(7372), 1059 (2002).
   PubMed Web of Science ®Google Scholar
• Albert MJ, Qadri F, Wahed MA et al. Supplementation with zinc, but not vitamin A, improves seroconversion to vibriocidal antibody in children given an oral cholera vaccine. J. Infect. Dis. 187(6), 909–913 (2003).
   PubMed Web of Science ®Google Scholar
• Santosham M, Chandran A, Fitzwater S, Fischer-Walker C, Baqui AH, Black R. Progress and barriers for the control of diarrhoeal disease. Lancet 376(9734), 63–67 (2010).
   PubMed Web of Science ®Google Scholar
• Ahmed T, Svennerholm AM, Al Tarique A, Sultana GN, Qadri F. Enhanced immunogenicity of an oral inactivated cholera vaccine in infants in Bangladesh obtained by zinc supplementation and by temporary withholding breast-feeding. Vaccine 27(9), 1433–1439 (2009).
   PubMed Web of Science ®Google Scholar
• Ovsyannikova IG, Poland GA. Vaccinomics: current findings, challenges and novel approaches for vaccine development. AAPS J. 13(3), 438–444 (2011).
   PubMed Web of Science ®Google Scholar
• Venkatesan MM, Ranallo RT. Live-attenuated Shigella vaccines. Expert Rev. Vaccines 5(5), 669–686 (2006).
   PubMed Web of Science ®Google Scholar
• Kweon MN. Shigellosis: the current status of vaccine development. Curr. Opin. Infect. Dis. 21(3), 313–318 (2008).
   PubMed Web of Science ®Google Scholar
• Phalipon A, Sansonetti PJ. Shigellosis: innate mechanisms of inflammatory destruction of the intestinal epithelium, adaptive immune response, and vaccine development. Crit. Rev. Immunol. 23(5-6), 371–401 (2003).
   PubMedGoogle Scholar
• Goldblatt D. Conjugate vaccines. Clin. Exp. Immunol. 119(1), 1–3 (2000).
   PubMed Web of Science ®Google Scholar
• González-Fernández A, Faro J, Fernández C. Immune responses to polysaccharides: lessons from humans and mice. Vaccine 26(3), 292–300 (2008).
   PubMed Web of Science ®Google Scholar
• Passwell JH, Ashkenazi S, Harlev E et al.; Israel Shigella Study Group. Safety and immunogenicity of Shigella sonnei-CRM9 and Shigella flexneri type 2a-rEPAsucc conjugate vaccines in one- to four-year-old children. Pediatr. Infect. Dis. J. 22(8), 701–706 (2003).
   PubMed Web of Science ®Google Scholar
• Passwell JH, Harlev E, Ashkenazi S et al. Safety and immunogenicity of improved Shigella O-specific polysaccharide-protein conjugate vaccines in adults in Israel. Infect. Immun. 69(3), 1351–1357 (2001).
   PubMed Web of Science ®Google Scholar
• Passwell JH, Ashkenzi S, Banet-Levi Y et al.; Israeli Shigella Study Group. Age-related efficacy of Shigella O-specific polysaccharide conjugates in 1–4-year-old Israeli children. Vaccine 28(10), 2231–2235 (2010).
   PubMed Web of Science ®Google Scholar
• Szu SC, Li XR, Schneerson R, Vickers JH, Bryla D, Robbins JB. Comparative immunogenicities of Vi polysaccharide-protein conjugates composed of cholera toxin or its B subunit as a carrier bound to high- or lower-molecular-weight Vi. Infect. Immun. 57(12), 3823–3827 (1989).
   PubMed Web of Science ®Google Scholar
• Acosta CJ, Galindo CM, Deen JL et al. Vaccines against cholera, typhoid fever and shigellosis for developing countries. Expert Opin. Biol. Ther. 4(12), 1939–1951 (2004).
   PubMed Web of Science ®Google Scholar
• Levenson VI, Chernokhvostova EV, Lyubinskaya MM, Salamatova SA, Dzhikidze EK, Stasilevitch ZK. Parenteral immunization with Shigella ribosomal vaccine elicits local IgA response and primes for mucosal memory. Int. Arch. Allergy Appl. Immunol. 87(1), 25–31 (1988).
   PubMedGoogle Scholar
• Shim DH, Chang SY, Park SM et al. Immunogenicity and protective efficacy offered by a ribosomal-based vaccine from Shigella flexneri 2a. Vaccine 25(25), 4828–4836 (2007).
   PubMed Web of Science ®Google Scholar
• Phalipon A, Tanguy M, Grandjean C et al. A synthetic carbohydrate-protein conjugate vaccine candidate against Shigella flexneri 2a infection. J. Immunol. 182(4), 2241–2247 (2009).
   PubMed Web of Science ®Google Scholar
• Borrelli S, Hossany RB, Pinto BM. Immunological evidence for functional rather than structural mimicry by a Shigella flexneri Y polysaccharide-mimetic peptide. Clin. Vaccine Immunol. 15(7), 1106–1114 (2008).
   PubMed Web of Science ®Google Scholar
• Turbyfill KR, Hartman AB, Oaks EV. Isolation and characterization of a Shigella flexneri invasin complex subunit vaccine. Infect. Immun. 68(12), 6624–6632 (2000).
   PubMed Web of Science ®Google Scholar
• Oaks EV, Turbyfill KR. Development and evaluation of a Shigella flexneri 2a and S. sonnei bivalent invasin complex (Invaplex) vaccine. Vaccine 24(13), 2290–2301 (2006).
   PubMed Web of Science ®Google Scholar
• Mallett CP, Hale TL, Kaminski RW et al. Intransal or intragastric immunization with proteosome-Shigella lipopolysaccharide vaccines protects against lethal pneumonia in a murine model of Shigella infection. Infect. Immun. 63(6), 2382–2386 (1995).
   PubMed Web of Science ®Google Scholar
• Riddle MS, Kaminski RW, Williams C et al. Safety and immunogenicity of an intranasal Shigella flexneri 2a Invaplex 50 vaccine. Vaccine 29(40), 7009–7019 (2011).
   PubMed Web of Science ®Google Scholar
• Kaminski RW, Turbyfill KR, Chao C, Ching WM, Oaks EV. Mucosal adjuvanticity of a Shigella invasin complex with DNA-based vaccines. Clin. Vaccine Immunol. 16(4), 574–586 (2009).
   PubMedGoogle Scholar
• Martinez-Becerra FJ, Kissmann JM, Diaz-McNair J et al. Broadly protective Shigella vaccine based on type III secretion apparatus proteins. Infect. Immun. 80(3), 1222–1231 (2012).
   PubMed Web of Science ®Google Scholar
• Collins BS. Gram-negative outer membrane vesicles in vaccine development. Discov. Med. 12(62), 7–15 (2011).
   PubMed Web of Science ®Google Scholar
• Lewis S, Sadarangani M, Hoe JC, Pollard AJ. Challenges and progress in the development of a serogroup B meningococcal vaccine. Expert Rev. Vaccines 8(6), 729–745 (2009).
   PubMed Web of Science ®Google Scholar
• Ellis TN, Leiman SA, Kuehn MJ. Naturally produced outer membrane vesicles from Pseudomonas aeruginosa elicit a potent innate immune response via combined sensing of both lipopolysaccharide and protein components. Infect. Immun. 78(9), 3822–3831 (2010).
   PubMed Web of Science ®Google Scholar
• Schild S, Nelson EJ, Bishop AL, Camilli A. Characterization of Vibrio cholerae outer membrane vesicles as a candidate vaccine for cholera. Infect. Immun. 77(1), 472–484 (2009).
   PubMed Web of Science ®Google Scholar
• Alaniz RC, Deatherage BL, Lara JC, Cookson BT. Membrane vesicles are immunogenic facsimiles of Salmonella typhimurium that potently activate dendritic cells, prime B and T cell responses, and stimulate protective immunity in vivo. J. Immunol. 179(11), 7692–7701 (2007).
   PubMed Web of Science ®Google Scholar
• McConnell MJ, Rumbo C, Bou G, Pachón J. Outer membrane vesicles as an acellular vaccine against Acinetobacter baumannii. Vaccine 29(34), 5705–5710 (2011).
   PubMed Web of Science ®Google Scholar
• Kadurugamuwa JL, Beveridge TJ. Delivery of the non-membrane-permeative antibiotic gentamicin into mammalian cells by using Shigella flexneri membrane vesicles. Antimicrob. Agents Chemother. 42(6), 1476–1483 (1998).
   PubMed Web of Science ®Google Scholar
• Camacho AI, de Souza J, Sánchez-Gómez S, Pardo-Ros M, Irache JM, Gamazo C. Mucosal immunization with Shigella flexneri outer membrane vesicles induced protection in mice. Vaccine 29(46), 8222–8229 (2011).
   PubMed Web of Science ®Google Scholar
• Biswas A, Banerjee P, Biswas T. Porin of Shigella dysenteriae directly promotes toll-like receptor 2-mediated CD4+ T cell survival and effector function. Mol. Immunol. 46(15), 3076–3085 (2009).
   PubMedGoogle Scholar
• Berlanda Scorza F, Colucci AM, Maggiore L et al. High yield production process for Shigella outer membrane particles. PLoS ONE 7(6), e35616 (2012).
   PubMed Web of Science ®Google Scholar
• Belyakov IM, Ahlers JD. What role does the route of immunization play in the generation of protective immunity against mucosal pathogens? J. Immunol. 183(11), 6883–6892 (2009).
   PubMed Web of Science ®Google Scholar
• Lawson LB, Norton EB, Clements JD. Defending the mucosa: adjuvant and carrier formulations for mucosal immunity. Curr. Opin. Immunol. 23(3), 414–420 (2011).
   PubMed Web of Science ®Google Scholar
• Freytag LC, Clements JD. Mucosal adjuvants. Vaccine 23(15), 1804–1813 (2005).
   PubMed Web of Science ®Google Scholar
• Schijns VE, Lavelle EC. Trends in vaccine adjuvants. Expert Rev. Vaccines 10(4), 539–550 (2011).
   PubMed Web of Science ®Google Scholar
• Pulendran B, Ahmed R. Immunological mechanisms of vaccination. Nat. Immunol. 12(6), 509–517 (2011).
   PubMed Web of Science ®Google Scholar
• Mosca F, Tritto E, Muzzi A et al. Molecular and cellular signatures of human vaccine adjuvants. Proc. Natl Acad. Sci. USA 105(30), 10501–10506 (2008).
   PubMed Web of Science ®Google Scholar
• Schwarz TF. Clinical update of the AS04-adjuvanted human papillomavirus-16/18 cervical cancer vaccine, Cervarix. Adv. Ther. 26(11), 983–998 (2009).
   PubMed Web of Science ®Google Scholar
• 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. 18(4), 546–551 (2011).
   PubMed Web of Science ®Google Scholar
• Pizza M, Giuliani MM, Fontana MR et al. Mucosal vaccines: non toxic derivatives of LT and CT as mucosal adjuvants. Vaccine 19(17–19), 2534–2541 (2001).
   PubMed Web of Science ®Google Scholar
• Hartman AB, Van De Verg LL, Venkatesan MM. Native and mutant forms of cholera toxin and heat-labile enterotoxin effectively enhance protective efficacy of live attenuated and heat-killed Shigella vaccines. Infect. Immun. 67(11), 5841–5847 (1999).
   PubMed Web of Science ®Google Scholar
• Orr N, Arnon R, Rubin G, Cohen D, Bercovier H, Lowell GH. Enhancement of anti-Shigella lipopolysaccharide (LPS) response by addition of the cholera toxin B subunit to oral and intranasal proteosome-Shigella flexneri 2a LPS vaccines. Infect. Immun. 62(11), 5198–5200 (1994).
   PubMed Web of Science ®Google Scholar
• Fries LF, Montemarano AD, Mallett CP, Taylor DN, Hale TL, Lowell GH. Safety and immunogenicity of a proteosome-Shigella flexneri 2a lipopolysaccharide vaccine administered intranasally to healthy adults. Infect. Immun. 69(7), 4545–4553 (2001).
   PubMed Web of Science ®Google Scholar
• Katz DE, DeLorimier AJ, Wolf MK et al. Oral immunization of adult volunteers with microencapsulated enterotoxigenic Escherichia coli (ETEC) CS6 antigen. Vaccine 21(5-6), 341–346 (2003).
   PubMed Web of Science ®Google Scholar
• Ochoa J, Irache JM, Tamayo I, Walz A, DelVecchio VG, Gamazo C. Protective immunity of biodegradable nanoparticle-based vaccine against an experimental challenge with Salmonella Enteritidis in mice. Vaccine 25(22), 4410–4419 (2007).
   PubMed Web of Science ®Google Scholar
• Huang JL, Yin YX, Pan ZM et al. Intranasal immunization with chitosan/pCAGGS-flaA nanoparticles inhibits Campylobacter jejuni in a White Leghorn model. J. Biomed. Biotechnol. 2010, pii: 589476 (2010).
   Google Scholar
• De Temmerman ML, Rejman J, Demeester J, Irvine DJ, Gander B, De Smedt SC. Particulate vaccines: on the quest for optimal delivery and immune response. Drug Discov. Today 16(13-14), 569–582 (2011).
   PubMed Web of Science ®Google Scholar
• De Koker S, Lambrecht BN, Willart MA et al. Designing polymeric particles for antigen delivery. Chem. Soc. Rev. 40(1), 320–339 (2011).
   PubMed Web of Science ®Google Scholar
• Burgdorf S, Kurts C. Endocytosis mechanisms and the cell biology of antigen presentation. Curr. Opin. Immunol. 20(1), 89–95 (2008).
   PubMed Web of Science ®Google Scholar
• Shen H, Ackerman AL, Cody V et al. Enhanced and prolonged cross-presentation following endosomal escape of exogenous antigens encapsulated in biodegradable nanoparticles. Immunology 117(1), 78–88 (2006).
   PubMed Web of Science ®Google Scholar
• Chadwick S, Kriegel C, Amiji M. Nanotechnology solutions for mucosal immunization. Adv. Drug Deliv. Rev. 62(4-5), 394–407 (2010).
   PubMed Web of Science ®Google Scholar
• Gupta RK, Singh M, O’Hagan DT. Poly(lactide-co-glycolide) microparticles for the development of single-dose controlled-release vaccines. Adv. Drug Deliv. Rev. 32(3), 225–246 (1998).
   PubMed Web of Science ®Google Scholar
• Jain S, O’Hagan DT, Singh M. The long-term potential of biodegradable poly(lactide-co-glycolide) microparticles as the next-generation vaccine adjuvant. Expert Rev. Vaccines 10(12), 1731–1742 (2011).
   PubMed Web of Science ®Google Scholar
• Ahmed R, Gray D. Immunological memory and protective immunity: understanding their relation. Science 272(5258), 54–60 (1996).
   PubMed Web of Science ®Google Scholar
• Demento SL, Cui W, Criscione JM et al. Role of sustained antigen release from nanoparticle vaccines in shaping the T cell memory phenotype. Biomaterials 33(19), 4957–4964 (2012).
   PubMed Web of Science ®Google Scholar
• Moon JJ, Suh H, Li AV, Ockenhouse CF, Yadava A, Irvine DJ. Enhancing humoral responses to a malaria antigen with nanoparticle vaccines that expand Tfh cells and promote germinal center induction. Proc. Natl Acad. Sci. USA 109(4), 1080–1085 (2012).
   PubMed Web of Science ®Google Scholar
• Cox E, Verdonck F, Vanrompay D, Goddeeris B. Adjuvants modulating mucosal immune responses or directing systemic responses towards the mucosa. Vet. Res. 37(3), 511–539 (2006).
   PubMed Web of Science ®Google Scholar
• Sharp FA, Ruane D, Claass B et al. Uptake of particulate vaccine adjuvants by dendritic cells activates the NALP3 inflammasome. Proc. Natl Acad. Sci. USA 106(3), 870–875 (2009).
   PubMed Web of Science ®Google Scholar
• Bal SM, Slütter B, Verheul R, Bouwstra JA, Jiskoot W. Adjuvanted, antigen loaded N-trimethyl chitosan nanoparticles for nasal and intradermal vaccination: adjuvant- and site-dependent immunogenicity in mice. Eur. J. Pharm. Sci. 45(4), 475–481 (2012).
   PubMed Web of Science ®Google Scholar
• Malyala P, Chesko J, Ugozzoli M et al. The potency of the adjuvant, CpG oligos, is enhanced by encapsulation in PLG microparticles. J. Pharm. Sci. 97(3), 1155–1164 (2008).
   PubMed Web of Science ®Google Scholar
• Agren LC, Ekman L, Löwenadler B, Lycke NY. Genetically engineered nontoxic vaccine adjuvant that combines B cell targeting with immunomodulation by cholera toxin A1 subunit. J. Immunol. 158(8), 3936–3946 (1997).
   PubMed Web of Science ®Google Scholar
• Kotturi MF, Botten J, Sidney J et al. A multivalent and cross-protective vaccine strategy against arenaviruses associated with human disease. PLoS Pathog. 5(12), e1000695 (2009).
   PubMed Web of Science ®Google Scholar
• Ma W, Chen M, Kaushal S et al. PLGA nanoparticle-mediated delivery of tumor antigenic peptides elicits effective immune responses. Int. J. Nanomedicine 7, 1475–1487 (2012).
   PubMed Web of Science ®Google Scholar
• Afrin F, Rajesh R, Anam K, Gopinath M, Pal S, Ali N. Characterization of Leishmania donovani antigens encapsulated in liposomes that induce protective immunity in BALB/c mice. Infect. Immun. 70(12), 6697–6706 (2002).
   PubMed Web of Science ®Google Scholar
• Prasad S, Cody V, Saucier-Sawyer JK et al. Optimization of stability, encapsulation, release, and cross-priming of tumor antigen-containing PLGA nanoparticles. Pharm. Res. 29(9), 2565–2577 (2012).
   PubMed Web of Science ®Google Scholar
• Hall MA, Stroop SD, Hu MC et al. Intranasal immunization with multivalent group A streptococcal vaccines protects mice against intranasal challenge infections. Infect. Immun. 72(5), 2507–2512 (2004).
   PubMed Web of Science ®Google Scholar
• Mel D, Gangarosa EJ, Radovanovic ML, Arsic BL, Litvinjenko S. Studies on vaccination against bacillary dysentery. 6. Protection of children by oral immunization with streptomycin-dependent Shigella strains. Bull. World Health Organ. 45(4), 457–464 (1971).
   PubMed Web of Science ®Google Scholar
• Levine MM, Gangarosa EJ, Barrow WB, Weiss CF. Shigellosis in custodial institutions. V. Effect of intervention with streptomycin-dependent Shigella sonnei vaccine in an institution with endemic disease. Am. J. Epidemiol. 104(1), 88–92 (1976).
   PubMedGoogle Scholar
• Venkatesan M, Fernandez-Prada C, Buysse JM, Formal SB, Hale TL. Virulence phenotype and genetic characteristics of the T32-ISTRATI Shigella flexneri 2a vaccine strain. Vaccine 9(5), 358–363 (1991).
   PubMedGoogle Scholar
• Kotloff KL, Pasetti MF, Barry EM et al. Deletion in the Shigella enterotoxin genes further attenuates Shigella flexneri 2a bearing guanine auxotrophy in a Phase 1 trial of CVD 1204 and CVD 1208. J. Infect. Dis. 190(10), 1745–1754 (2004).
   PubMed Web of Science ®Google Scholar
• Kotloff KL, Simon JK, Pasetti MF et al. Safety and immunogenicity of CVD 1208S, a live, oral DeltaguaBA Deltasen Deltaset Shigella flexneri 2a vaccine grown on animal-free media. Hum. Vaccin. 3(6), 268–275 (2007).
   PubMed Web of Science ®Google Scholar
• Simon JK, Maciel M Jr, Weld ED et al. Antigen-specific IgA B memory cell responses to Shigella antigens elicited in volunteers immunized with live attenuated Shigella flexneri 2a oral vaccine candidates. Clin. Immunol. 139(2), 185–192 (2011).
   PubMedGoogle Scholar
• Orr N, Katz DE, Atsmon J et al. Community-based safety, immunogenicity, and transmissibility study of the Shigella sonnei WRSS1 vaccine in Israeli volunteers. Infect. Immun. 73(12), 8027–8032 (2005).
   PubMedGoogle Scholar
• Barnoy S, Baqar S, Kaminski RW et al. Shigella sonnei vaccine candidates WRSs2 and WRSs3 are as immunogenic as WRSS1, a clinically tested vaccine candidate, in a primate model of infection. Vaccine 29(37), 6371–6378 (2011).
   PubMedGoogle Scholar
• Barnoy S, Jeong KI, Helm RF et al. Characterization of WRSs2 and WRSs3, new second-generation virG(icsA)-based Shigella sonnei vaccine candidates with the potential for reduced reactogenicity. Vaccine 28(6), 1642–1654 (2010).
   PubMedGoogle Scholar
• Sadorge C, Ndiaye A, Beveridge N et al. Phase 1 clinical trial of live attenuated Shigella dysenteriae type-1 DeltaicsA Deltaent Deltafep DeltastxA:HgR oral vaccine SC599 in healthy human adult volunteers. Vaccine 26(7), 978–987 (2008).
   PubMedGoogle Scholar
• Coster TS, Hoge CW, VanDeVerg LL et al. Vaccination against shigellosis with attenuated Shigella flexneri 2a strain SC602. Infect. Immun. 67(7), 3437–3443 (1999).
   PubMed Web of Science ®Google Scholar
• Katz DE, Coster TS, Wolf MK et al. Two studies evaluating the safety and immunogenicity of a live, attenuated Shigella flexneri 2a vaccine (SC602) and excretion of vaccine organisms in North American volunteers. Infect. Immun. 72(2), 923–930 (2004).
   PubMed Web of Science ®Google Scholar
• Ranallo RT, Thakkar S, Chen Q, Venkatesan MM. Immunogenicity and characterization of WRSF2G11: a second generation live attenuated Shigella flexneri 2a vaccine strain. Vaccine 25(12), 2269–2278 (2007).
   PubMedGoogle Scholar
• Rahman KM, Arifeen SE, Zaman K et al. Safety, dose, immunogenicity, and transmissibility of an oral live attenuated Shigella flexneri 2a vaccine candidate (SC602) among healthy adults and school children in Matlab, Bangladesh. Vaccine 29(6), 1347–1354 (2011).
   PubMedGoogle Scholar
• McKenzie R, Walker RI, Nabors GS et al. Safety and immunogenicity of an oral, inactivated, whole-cell vaccine for Shigella sonnei: preclinical studies and a Phase I trial. Vaccine 24(18), 3735–3745 (2006).
   PubMed Web of Science ®Google Scholar
• Summerton NA, Welch RW, Bondoc L et al. Toward the development of a stable, freeze-dried formulation of Helicobacter pylori killed whole cell vaccine adjuvanted with a novel mutant of Escherichia coli heat-labile toxin. Vaccine 28(5), 1404–1411 (2010).
   PubMed Web of Science ®Google Scholar
• Hagiwara Y, Kawamura YI, Kataoka K et al. A second generation of double mutant cholera toxin adjuvants: enhanced immunity without intracellular trafficking. J. Immunol. 177(5), 3045–3054 (2006).
   PubMedGoogle Scholar
• Mizel SB, Bates JT. Flagellin as an adjuvant: cellular mechanisms and potential. J. Immunol. 185(10), 5677–5682 (2010).
   PubMed Web of Science ®Google Scholar
• Harandi AM, Medaglini D. Mucosal adjuvants. Curr. HIV Res. 8(4), 330–335 (2010).
   PubMed Web of Science ®Google Scholar
• Blaas SH, Stieber-Gunckel M, Falk W, Obermeier F, Rogler G. CpG-oligodeoxynucleotides stimulate immunoglobulin A secretion in intestinal mucosal B cells. Clin. Exp. Immunol. 155(3), 534–540 (2009).
   PubMedGoogle Scholar
• Uematsu S, Fujimoto K, Jang MH et al. Regulation of humoral and cellular gut immunity by lamina propria dendritic cells expressing Toll-like receptor 5. Nat. Immunol. 9(7), 769–776 (2008).
   PubMed Web of Science ®Google Scholar
• Warshakoon HJ, Hood JD, Kimbrell MR et al. Potential adjuvantic properties of innate immune stimuli. Hum. Vaccin. 5(6), 381–394 (2009).
   PubMed Web of Science ®Google Scholar
• 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. 85(18), 9578–9587 (2011).
   PubMedGoogle Scholar
• Muhammad A, Champeimont J, Mayr UB, Lubitz W, Kudela P. Bacterial ghosts as carriers of protein subunit and DNA-encoded antigens for vaccine applications. Expert Rev. Vaccines 11(1), 97–116 (2012).
   PubMed Web of Science ®Google Scholar
• Peek LJ, Middaugh CR, Berkland C. Nanotechnology in vaccine delivery. Adv. Drug Deliv. Rev. 60(8), 915–928 (2008).
   PubMed Web of Science ®Google Scholar
• McNeela EA, Lavelle EC. Recent advances in microparticle and nanoparticle delivery vehicles for mucosal vaccination. Curr. Top. Microbiol. Immunol. 354, 75–99 (2012).
   PubMedGoogle Scholar
• van der Lubben IM, Verhoef JC, Borchard G, Junginger HE. Chitosan for mucosal vaccination. Adv. Drug Deliv. Rev. 52(2), 139–144 (2001).
   PubMed Web of Science ®Google Scholar
• Irache JM, Salman HH, Gomez S, Espuelas S, Gamazo C. Poly(anhydride) nanoparticles as adjuvants for mucosal vaccination. Front. Biosci. (Schol. Ed). 2, 876–890 (2010).
   PubMedGoogle Scholar