Inactivated and subunit vaccines to prevent shigellosis

Expert Review of Vaccines

Volumn 8, Issue 12, 2009, Pages 1693-1704

  Kaminski, Robert W ^a   Oaks, Edwin V ^a  

^a WALTER REED ARMY INSTITUTE OF RESEARCH   (United States)

Author keywords

Ipa; Lipopolysaccharide; LPS; Shigella; Subunit vaccines

Indexed keywords

ALUMINUM POTASSIUM SULFATE; IMMUNOGLOBULIN A; INACTIVATED VACCINE; INVAPLEX; INVASIN; LIPOPOLYSACCHARIDE; OLIGOSACCHARIDE; PROTEASOME; SHIGELLA VACCINE; SUBUNIT VACCINE; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; ANTIBODY RESPONSE; BACTERIAL VIRULENCE; CHILD; COLOSTRUM; CROSS REACTION; CYTOTOXICITY; DRUG BLOOD LEVEL; DRUG MEGADOSE; DRUG TOLERABILITY; FOOD CONTAMINATION; HEADACHE; HUMAN; IMMUNOGENICITY; INJECTION SITE REACTION; INJECTION SITE SWELLING; INJECTION SITE TENDERNESS; INNATE IMMUNITY; KERATOCONJUNCTIVITIS; LOW DRUG DOSE; LYMPHOCYTE; MALAISE; MUCOSAL IMMUNITY; MYALGIA; NATURAL KILLER T CELL; NEISSERIA MENINGITIDIS; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; REVIEW; RHINORRHEA; SALMONELLA TYPHIMURIUM; SEROCONVERSION; SHIGELLA BOYDII; SHIGELLA DYSENTERIAE; SHIGELLA FLEXNERI; SHIGELLA SONNEI; SHIGELLOSIS; TYPE III SECRETION SYSTEM;

BACTERIAL PROTEINS; DYSENTERY, BACILLARY; HUMANS; LIPOPOLYSACCHARIDES; SHIGELLA DYSENTERIAE; SHIGELLA FLEXNERI; SHIGELLA SONNEI; SHIGELLA VACCINES; VACCINES, INACTIVATED; VACCINES, SUBUNIT;

EID: 73849133281     PISSN: 14760584     EISSN: 17448395     Source Type: Journal    
DOI: 10.1586/erv.09.127     Document Type: Review

References (132)

1. 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).
2. 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).
3. Venkatesan MM, Ranallo RT. Liveattenuated Shigella vaccines. Expert Rev. Vaccines 5(5), 669-686 (2006). • Excellent review of live-attenuated Shigella vaccines.
4. 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).
5. Molbak K, Jensen H, Ingholt L, Aaby P. Risk factors for diarrheal disease incidence in early childhood: a community cohort study from Guinea-Bissau. Am. J. Epidemiol. 146(3), 273-282 (1997).
6. Guerrant DI, Moore SR, Lima AA, Patrick PD, Schorling JB, Guerrant RL. Association of early childhood diarrhea and cryptosporidiosis with impaired physical fitness and cognitive function four-seven years later in a poor urban community in northeast Brazil. Am. J. Trop. Med. Hyg. 61(5), 707-713 (1999).
7. Niehaus MD, Moore SR, Patrick PD et al. Early childhood diarrhea is associated with diminished cognitive function 4 to 7 years later in children in a northeast Brazilian shantytown. Am. J. Trop. Med. Hyg. 66(5), 590-593 (2002).
8. Watarai M, Funato S, Sasakawa C. Interaction of Ipa proteins of Shigella flexneri with a5b1 integrin promotes entry of the bacteria into mammalian cells. J. Exp. Med. 183(3), 991-999 (1996).
9. Tyrer P, Foxwell AR, Cripps AW, Apicella MA, Kyd JM. Microbial pattern recognition receptors mediate M-cell uptake of a Gram-negative bacterium. Infect. Immun. 74(1), 625-631 (2006).
10. Zychlinsky A, Prevost MC, Sansonetti PJ. Shigella flexneri induces apoptosis in infected macrophages. Nature 358(6382), 167-169 (1992).
11. Zychlinsky A, Kenny B, Menard R, Prevost MC, Holland IB, Sansonetti PJ. IpaB mediates macrophage apoptosis induced by Shigella flexneri. Mol. Microbiol. 11(4), 619-627 (1994).
12. Hilbi H, Zychlinsky A, Sansonetti PJ. Macrophage apoptosis in microbial infections. Parasitology 115(Suppl.), S79-S87 (1997).
13. Hilbi H, Moss JE, Hersh D et al. Shigella-induced apoptosis is dependent on caspase-1 which binds to IpaB. J. Biol. Chem. 273(49), 32895-32900 (1998).
14. Edgeworth JD, Spencer J, Phalipon A, Griffin GE, Sansonetti PJ. Cytotoxicity and interleukin-1b processing following Shigella flexneri infection of human monocyte-derived dendritic cells. Eur. J. Immunol. 32(5), 1464-1471 (2002).
15. Hathaway LJ, Griffin GE, Sansonetti PJ, Edgeworth JD. Human monocytes kill Shigella flexneri but then die by apoptosis associated with suppression of proinflammatory cytokine production. Infect. Immun. 70(7), 3833-3842 (2002).
16. Suzuki T, Nakanishi K, Tsutsui H et al. A novel caspase-1/Toll-like receptor 4-independent pathway of cell death induced by cytosolic Shigella in infected macrophages. J. Biol. Chem. 280(14), 14042-14050 (2005).
17. Schroeder GN, Jann NJ, Hilbi H. Intracellular type III secretion by cytoplasmic Shigella flexneri promotes caspase-1-dependent macrophage cell death. Microbiology 153(Pt 9), 2862-2876 (2007).
18. Suzuki T, Franchi L, Toma C et al. Differential regulation of caspase-1 activation, pyroptosis, and autophagy via Ipaf and ASC in Shigella-infected macrophages. PLoS Pathog. 3(8), e111 (2007).
19. 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).
20. Rallabhandi P, Awomoyi A, Thomas KE et al. Differential activation of human TLR4 by Escherichia coli and Shigella flexneri 2a lipopolysaccharide: combined effects of lipid A acylation state and TLR4 polymorphisms on signaling. J. Immunol. 180(2), 1139-1147 (2008).
21. Tamano K, Aizawa S, Katayama E et al. Supramolecular structure of the Shigella type III secretion machinery: the needle part is changeable in length and essential for delivery of effectors. EMBO J. 19(15), 3876-3887 (2000).
22. Espina M, Olive AJ, Kenjale R et al. IpaD localizes to the tip of the type III secretion system needle of Shigella flexneri. Infect. Immun. 74(8), 4391-4400 (2006).
23. Stensrud KF, Adam PR, La Mar CD et al. Deoxycholate interacts with IpaD of Shigella flexneri in inducing the recruitment of IpaB to the type III secretion apparatus needle tip. J. Biol. Chem. 283(27), 18646-18654 (2008).
24. Epler CR, Dickenson NE, Olive AJ, Picking WL, Picking WD. Liposomes recruit IpaC to the Shigella flexneri type III secretion apparatus needle as a final step in secretion induction. Infect. Immun. 77(7), 2754-2761 (2009).
25. West NP, Sansonetti P, Mounier J et al. Optimization of virulence functions through glucosylation of Shigella LPS. Science 307(5713), 1313-1317 (2005).
26. Blocker A, Gounon P, Larquet E et al. The tripartite type III secreton of Shigella flexneri inserts IpaB and IpaC into host membranes. J. Cell Biol. 147(3), 683-693 (1999).
27. High N, Mounier J, Prevost MC, Sansonetti PJ. IpaB of Shigella flexneri causes entry into epithelial cells and escape from the phagocytic vacuole. EMBO J. 11(5), 1991-1999 (1992).
28. Barzu S, Benjelloun-Touimi Z, Phalipon A, Sansonetti P, Parsot C. Functional analysis of the Shigella flexneri IpaC invasin by insertional mutagenesis. Infect. Immun. 65(5), 1599-1605 (1997).
29. Suzuki T, Nunez G. A role for Nod-like receptors in autophagy induced by Shigella infection. Autophagy 4(1), 73-75 (2008).
30. Sansonetti PJ, Arondel J, Huerre M, Harada A, Matsushima K. Interleukin-8 controls bacterial transepithelial translocation at the cost of epithelial destruction in experimental shigellosis. Infect. Immun. 67(3), 1471-1480 (1999).
31. Raqib R, Lindberg AA, Wretlind B, Bardhan PK, Andersson U, Andersson J. Persistence of local cytokine production in shigellosis in acute and convalescent stages. Infect. Immun. 63(1), 289-296 (1995).
32. Okuda J, Toyotome T, Kataoka N et al. Shigella effector IpaH9.8 binds to a splicing factor U2AF(35) to modulate host immune responses. Biochem. Biophys. Res. Commun. 333(2), 531-539 (2005).
33. Ingersoll MA, Zychlinsky A. ShiA abrogates the innate T-cell response to Shigella flexneri infection. Infect. Immun. 74(4), 2317-2327 (2006).
34. Ingersoll MA, Moss JE, Weinrauch Y, Fisher PE, Groisman EA, Zychlinsky A. The ShiA protein encoded by the Shigella flexneri SHI-2 pathogenicity island attenuates inflammation. Cell Microbiol. 5(11), 797-807 (2003).
35. Zurawski DV, Mumy KL, Faherty CS, McCormick BA, Maurelli AT. Shigella flexneri type III secretion system effectors OspB and OspF target the nucleus to downregulate the host inflammatory response via interactions with retinoblastoma protein. Mol. Microbiol. 71(2), 350-368 (2009).
36. Kim DW, Lenzen G, Page AL, Legrain P, Sansonetti PJ, Parsot C. The Shigella flexneri effector OspG interferes with innate immune responses by targeting ubiquitin-conjugating enzymes. Proc. Natl Acad. Sci. USA 102(39), 14046-14051 (2005).
37. Le-Barillec K, Magalhaes JG, Corcuff E et al. Roles for T and NK cells in the innate immune response to Shigella flexneri. J. Immunol. 175(3), 1735-1740 (2005).
38. Ferreccio C, Prado V, Ojeda A et al. Epidemiologic patterns of acute diarrhea and endemic Shigella infections in children in a poor periurban setting in Santiago, Chile. Am. J. Epidemiol. 134(6), 614-627 (1991).
39. Islam D, Wretlind B, Hammarstrom L, Christensson B, Lindberg AA. Semiquantitative estimation of Shigella antigen-specific antibodies: correlation with disease severity during shigellosis. APMIS 104(7-8), 563-574 (1996).
40. Andrews GP, Hromockyj AE, Coker C, Maurelli AT. Two novel virulence loci, mxiA and mxiB, in Shigella flexneri 2a facilitate excretion of invasion plasmid antigens. Infect. Immun. 59(6), 1997-2005 (1991).
41. Islam D, Bardhan PK, Lindberg AA, Christensson B. Shigella infection induces cellular activation of T and B cells and distinct species-related changes in peripheral blood lymphocyte subsets during the course of the disease. Infect. Immun. 63(8), 2941-2949 (1995).
42. Runyen-Janecky LJ, Payne SM. Identification of chromosomal Shigella flexneri genes induced by the eukaryotic intracellular environment. Infect. Immun. 70(8), 4379-4388 (2002).
43. Purdy GE, Fisher CR, Payne SM. IcsA surface presentation in Shigella flexneri requires the periplasmic chaperones DegP, Skp, and SurA. J. Bacteriol. 189(15), 5566-5573 (2007).
44. 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).
45. Fasano A, Noriega FR, Liao FM, Wang W, Levine MM. Effect of Shigella enterotoxin 1 (ShET1) on rabbit intestine in vitro and in vivo. Gut 40(4), 505-511 (1997).
46. 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).
47. Raqib R, Qadri F, SarkEr P et al. Delayed and reduced adaptive humoral immune responses in children with shigellosis compared with in adults. Scand. J. Immunol. 55(4), 414-423 (2002).
48. 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).
49. 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).
50. 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).
51. Chowers Y, Kirschner J, Keller N et al. O-specific [corrected] polysaccharide conjugate vaccine-induced [corrected] antibodies prevent invasion of Shigella into Caco-2 cells and may be curative. Proc. Natl Acad. Sci. USA 104(7), 2396-2401 (2007).
52. Mills JA, Buysse JM, Oaks EV. Shigella flexneri invasion plasmid antigens B and C: epitope location and characterization with monoclonal antibodies. Infect. Immun. 56(11), 2933-2941 (1988).
53. Sani M, Allaoui A, Fusetti F, Oostergetel GT, Keegstra W, Boekema EJ. Structural organization of the needle complex of the type III secretion apparatus of Shigella flexneri. Micron 38(3), 291-301 (2007).
54. Lowell GH, MacDermott RP, Summers PL, Reeder AA, Bertovich MJ, Formal SB. Antibody-dependent cellmediated antibacterial activity: K lymphocytes, monocytes, and granulocytes are effective against Shigella. J. Immunol. 125(6), 2778-2784 (1980).
55. Cleary TG, Winsor DK, Reich D, Ruiz-Palacios G, Calva JJ. Human milk immunoglobulin A antibodies to Shigella virulence determinants. Infect. Immun. 57(6), 1675-1679 (1989).
56. Cohen D, Orr N, Robin G et al. Detection of antibodies to Shigella lipopolysaccharide in urine after natural Shigella infection or vaccination. Clin. Diagn. Lab. Immunol. 3(4), 451-455 (1996).
57. Islam D, Wretlind B, Ryd M, Lindberg AA, Christensson B. Immunoglobulin subclass distribution and dynamics of Shigellaspecific antibody responses in serum and stool samples in shigellosis. Infect. Immun. 63(5), 2054-2061 (1995).
58. Schultsz C, Qadri F, Hossain SA, Ahmed F, Ciznar I. Shigella-specific IgA in saliva of children with bacillary dysentery. FEMS Microbiol. Immunol. 4(2), 65-72 (1992).
59. Islam D, Veress B, Bardhan PK, Lindberg AA, Christensson B. In situ characterization of inflammatory responses in the rectal mucosae of patients with shigellosis. Infect. Immun. 65(2), 739-749 (1997).
60. 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).
61. Ashkenazi S, Passwell JH, Harlev E et al. Safety and immunogenicity of Shigella sonnei and Shigella flexneri 2a O-specific polysaccharide conjugates in children. J. Infect. Dis. 179(6), 1565-1568 (1999).
62. Robbins JB, Schneerson R. Future vaccine development at NICHD. Ann NY Acad. Sci. 1038, 49-59 (2004).
63. 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).
64. Hayani KC, Guerrero ML, Morrow AL et al. Concentration of milk secretory immunoglobulin A against Shigella virulence plasmid-associated antigens as a predictor of symptom status in Shigellainfected breast-fed infants. J. Pediatr. 121(6), 852-856 (1992).
65. Tacket CO, Binion SB, Bostwick E, Losonsky G, Roy MJ, Edelman R. Efficacy of bovine milk immunoglobulin concentrate in preventing illness after Shigella flexneri challenge. Am. J. Trop. Med. Hyg. 47(3), 276-283 (1992).
66. 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).
67. 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).
68. Turbyfill KR, Joseph SW, Oaks EV. Recognition of three epitopic regions on invasion plasmid antigen C by immune sera of rhesus monkeys infected with Shigella flexneri 2a. Infect. Immun. 63(10), 3927-3935 (1995).
69. Kweon MN. Shigellosis: the current status of vaccine development. Curr. Opin. Infect. Dis. 21(3), 313-318 (2008).
70. Trofa AF, Ueno-Olsen H, Oiwa R, Yoshikawa M. Dr. Kiyoshi Shiga: discoverer of the dysentery bacillus. Clin. Infect. Dis. 29(5), 1303-1306 (1999).
71. Osorio M, Bray MD, Walker RI. Vaccine potential for inactivated Shigellae. Vaccine 25(9), 1581-1592 (2007).
72. 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). • Recent work outlining a Shigella killed, whole-cell vaccine approach.
73. Mukhopadhaya A, Mahalanabis D, Khanam J, Chakrabarti MK. Protective efficacy of oral immunization with heat-killed Shigella flexneri 2a in animal model: study of cross protection, immune response and antigenic recognition. Vaccine 21(21-22), 3043-3050 (2003).
74. Chakrabarti MK, Bhattacharya J, Bhattacharya MK, Nair GB, Bhattacharya SK, Mahalanabis D. Killed oral Shigella vaccine made from Shigella flexneri 2a protects against challenge in the rabbit model of shigellosis. Acta Paediatr. 88(2), 161-165 (1999).
75. Formal SB, Labrec EH, Palmer A, Falkow S. Protection of monkeys against experimental shigellosis with attenuated vaccines. J. Bacteriol. 90(1), 63-68 (1965).
76. Tabrizi CA, Walcher P, Mayr UB et al. Bacterial ghosts - biological particles as delivery systems for antigens, nucleic acids and drugs. Curr. Opin. Biotechnol. 15(6), 530-537 (2004).
77. Higgins AR, Floyd TM, Kader MA. Studies in shigellosis. III. A controlled evaluation of a monovalent Shigella vaccine in a highly endemic environment. Am. J. Trop. Med. Hyg. 4(2), 281-288 (1955).
78. Formal SB, LaBrec EH, Kent TH, May HC, Lowenthal JP, Berman S. Biological properties of freeze-dried attenuated Shigella vaccines. Proc. Soc. Exp. Biol. Med. 124(1), 284-289 (1967).
79. Shaughnessy HJ, OLsson RC, Bass K, Friewer F, Levinson SO. Experimental human bacillary dysentery: polyvalent dysentery vaccine in its prevention. J. Am. Med. Assoc. 132(7), 362-371 (1946).
80. 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).
81. Pope LM, Reed KE, Payne SM. Increased protein secretion and adherence to HeLa cells by Shigella spp. following growth in the presence of bile salts. Infect. Immun. 63(9), 3642-3648 (1995).
82. Payne SM. Iron and virulence in Shigella. Mol. Microbiol. 3(9), 1301-1306 (1989).
83. Sen A, Leon MA, Palchaudhuri S. Environmental signals induce major changes in virulence of Shigella spp. FEMS Microbiol. Lett. 68(2), 231-236 (1991).
84. Boulette ML, Payne SM. Anaerobic regulation of Shigella flexneri virulence: ArcA regulates Fur and iron acquisition genes. J. Bacteriol. 189(19), 6957-6967 (2007).
85. Black RE, Levine MM, Clements ML, Young CR, Svennerholm AM, Holmgren J. Protective efficacy in humans of killed whole-vibrio oral cholera vaccine with and without the B subunit of cholera toxin. Infect. Immun. 55(5), 1116-1120 (1987).
86. Trach DD, Clemens JD, Ke NT et al. Field trial of a locally produced, killed, oral cholera vaccine in Vietnam. Lancet 349(9047), 231-235 (1997).
87. Walker RI. Considerations for development of whole cell bacterial vaccines to prevent diarrheal diseases in children in developing countries. Vaccine 23(26), 3369-3385 (2005).
88. Taylor DN, Trofa AC, Sadoff J et al. Synthesis, characterization, and clinical evaluation of conjugate vaccines composed of the O-specific polysaccharides of Shigella dysenteriae type 1, Shigella flexneri type 2a, and Shigella sonnei (Plesiomonas shigelloides) bound to bacterial toxoids. Infect. Immun. 61(9), 3678-3687 (1993).
89. Pavliakova D, Chu C, Bystricky S et al. Treatment with succinic anhydride improves the immunogenicity of Shigella flexneri type 2a O-specific polysaccharide-protein conjugates in mice. Infect. Immun. 67(10), 5526-5529 (1999).
90. 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).
91. Cohen D, Ashkenazi S, Green MS et al. Double-blind vaccine-controlled randomised efficacy trial of an investigational Shigella sonnei conjugate vaccine in young adults. Lancet 349(9046), 155-159 (1997).
92. Wright K, Guerreiro C, Laurent I, Baleux F, Mulard LA. Preparation of synthetic glycoconjugates as potential vaccines against Shigella flexneri serotype 2a disease. Org. Biomol. Chem. 2(10), 1518-1527 (2004).
93. Pavliakova D, Moncrief JS, Lyerly DM et al. Clostridium difficile recombinant toxin A repeating units as a carrier protein for conjugate vaccines: studies of pneumococcal type 14, Escherichia coli K1, and Shigella flexneri type 2a polysaccharides in mice. Infect. Immun. 68(4), 2161-2166 (2000).
94. Robbins JB, Schneerson R. Evaluating the Haemophilus influenzae type b conjugate vaccine PRP-D. N. Engl. J. Med. 323(20), 1415-1416 (1990).
95. Anderson PW Jr, Stein EC, Insel RA. Background and indications for Haemophilus influenzae type b vaccines consisting of capsular antigen coupled to protein carriers. Contrib. Microbiol. Immunol. 10, 115-124 (1989).
96. 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).
97. Pozsgay V, Kubler-Kielb J, Schneerson R, Robbins JB. Effect of the nonreducing end of Shigella dysenteriae type 1 O-specific oligosaccharides on their immunogenicity as conjugates in mice. Proc. Natl Acad. Sci. USA 104(36), 14478-14482 (2007).
98. Phalipon A, Mulard LA, Sansonetti PJ. Vaccination against shigellosis: is it the path that is difficult or is it the difficult that is the path? Microbes Infect. 10(9), 1057-1062 (2008).
99. Chu CY, Liu BK, Watson D et al. Preparation, characterization, and immunogenicity of conjugates composed of the O-specific polysaccharide of Shigella dysenteriae type 1 (Shiga's bacillus) bound to tetanus toxoid. Infect. Immun. 59(12), 4450-4458 (1991).
100. Kopecko DJ, Washington O, Formal SB. Genetic and physical evidence for plasmid control of Shigella sonnei form I cell surface antigen. Infect. Immun. 29(1), 207-214 (1980).
101. Kubler-Kielb J, Schneerson R, Mocca C, Vinogradov E. The elucidation of the structure of the core part of the LPS from Plesiomonas shigelloides serotype O17 expressing O-polysaccharide chain identical to the Shigella sonnei O-chain. Carbohydr. Res. 343(18), 3123-3127 (2008).
102. Pozsgay V, Chu C, Pannell L, Wolfe J, Robbins JB, Schneerson R. Protein conjugates of synthetic saccharides elicit higher levels of serum IgG lipopolysaccharide antibodies in mice than do those of the O-specific polysaccharide from Shigella dysenteriae type 1. Proc. Natl Acad. Sci. USA 96(9), 5194-5197 (1999).
103. Robbins JB, Kubler-Kielb J, Vinogradov E et al. Synthesis, characterization, and immunogenicity in mice of Shigella sonnei O-specific oligosaccharide-core-protein conjugates. Proc. Natl Acad. Sci. USA 106(19), 7974-7978 (2009).
104. Ahmed A, Li J, Shiloach Y, Robbins JB, Szu SC. Safety and immunogenicity of Escherichia coli O157 O-specific polysaccharide conjugate vaccine in 2-5-year-old children. J. Infect. Dis. 193(4), 515-521 (2006).
105. Cohen D, Ashkenazi S, Green M et al. Safety and immunogenicity of investigational Shigella conjugate vaccines in Israeli volunteers. Infect. Immun. 64(10), 4074-4077 (1996).
106. Passwell JH, Ashkenazi S, Harlev E et al. 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).
107. Klein Klouwenberg P, Bont L. Neonatal and infantile immune responses to encapsulated bacteria and conjugate vaccines. Clin. Dev. Immunol. 2008, 628963 (2008).
108. 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).
109. Phalipon A, Costachel C, Grandjean C et al. Characterization of functional oligosaccharide mimics of the Shigella flexneri serotype 2a O-antigen: implications for the development of a chemically defined glycoconjugate vaccine. J. Immunol. 176(3), 1686-1694 (2006).
110. Robbins JB, Kubler-Kielb J, Vinogradov E et al. Synthesis, characterization, and immunogenicity in mice of Shigella sonnei O-specific oligosaccharide-core-protein conjugates. Proc. Natl Acad. Sci. USA 106(19), 7974-7978 (2009). • Recent update on Shigella lipopolysaccharide conjugate vaccine approach.
111. 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).
112. Phalipon A, Folgori A, Arondel J et al. Induction of anti-carbohydrate antibodies by phage library-selected peptide mimics. Eur. J. Immunol. 27(10), 2620-2625 (1997).
113. 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).
114. Clement MJ, Fortune A, Phalipon A et al. Toward a better understanding of the basis of the molecular mimicry of polysaccharide antigens by peptides: the example of Shigella flexneri 5a. J. Biol. Chem. 281(4), 2317-2332 (2006).
115. 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).
116. Lieberman MM, McKissock DC, Wright GL. Passive immunization against Pseudomonas with a ribosomal vaccineinduced immune serum and immunoglobulin fractions. Infect. Immun. 23(2), 509-521 (1979).
117. Angerman CR, Eisenstein TK. Comparative efficacy and toxicity of a ribosomal vaccine, acetone-killed cells, lipopolysaccharide, and a live cell vaccine prepared from Salmonella typhhimurium. Infect. Immun. 19(2), 575-582 (1978).
118. Chernokhvostova EV, Lyubinskaya MM, Belkin ZP, Levenson VI. Protective milk O antibodies induced in guinea pigs by parenteral Shigella ribosomal vaccine. Int. Arch. Allergy Appl. Immunol. 92(3), 265-267 (1990).
119. Levenson VI, Egorova TP, Belkin ZP et al. Protective ribosomal preparation from Shigella sonnei as a parenteral candidate vaccine. Infect. Immun. 59(10), 3610-3618 (1991).
120. Levenson VI, Dzhikidze EK, Stasilevich ZK, Kavtaradze KN, Subbotina Iu L. Trial of the protective activity of ribosomal Sonne vaccine in monkeys. Vestn. Akad. Med. Nauk. SSSR 3, 69-72 (1986).
121. Levenson VJ, Mallett CP, Hale TL. Protection against local Shigella sonnei infection in mice by parenteral immunization with a nucleoprotein subcellular vaccine. Infect. Immun. 63(7), 2762-2765 (1995).
122. 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).
123. 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).
124. 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).
125. 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).
126. 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).
127. Turbyfill KR, Hartman AB, Oaks EV. Isolation and characterization of a Shigella flexneri invasin complex subunit vaccine. Infect. Immun. 68(12), 6624-6632 (2000).
128. Kaminski RW, Turbyfill KR, Oaks EV. Mucosal adjuvant properties of the Shigella invasin complex. Infect. Immun. 74(5), 2856-2866 (2006).
129. 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).
130. Kaminski RW, Riddle MS, Williams C et al. Dose-finding, safety, and immunogenicity Phase 1 trial of an intranasal Shigella flexneri 2a Invaplex 50 vaccine in North American, adult volunteers. In: Eleventh Annual Conference on Vaccine Research. National Foundation for Infectious Diseases, Baltimore, MD, USA, 79 (2008).
131. Turbyfill KR, Kaminski RW, Oaks EV. Immunogenicity and efficacy of highly purified invasin complex vaccine from Shigella flexneri 2a. Vaccine 26(10), 1353-1364 (2008).
132. 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).