Shigella flexneri infection: Pathogenesis and vaccine development

FEMS Microbiology Reviews

Volumn 28, Issue 1, 2004, Pages 43-58

  Jennison, Amy V ^a   Verma, Naresh K ^a  

^a AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

Author keywords

Pathogenesis; Shigella flexneri; Vaccine development

Indexed keywords

ANTIBIOTIC AGENT; INACTIVATED VACCINE; LIVE VACCINE; SUBUNIT VACCINE; VACCINE; VIRULENCE FACTOR;

APOPTOSIS; BACTERIAL INFECTION; BACTERIUM ADHERENCE; CELLULAR IMMUNITY; CLINICAL TRIAL; COLON MUCOSA; COLONY FORMING UNIT; DEVELOPING COUNTRY; DIARRHEA; DOSE RESPONSE; EPITHELIUM CELL; EXPERIMENTAL MODEL; FEVER; HOST; HUMAN; HUMORAL IMMUNITY; IMMUNE RESPONSE; INFLAMMATION; MACROPHAGE; MOLECULAR MECHANICS; NONHUMAN; PATHOGENESIS; REVIEW; SEROTYPE; SHIGELLA FLEXNERI; SHIGELLOSIS; VACCINATION;

BACTERIA (MICROORGANISMS); NEGIBACTERIA; SHIGELLA FLEXNERI;

EID: 1242306203     PISSN: 01686445     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.femsre.2003.07.002     Document Type: Review

References (164)

1. Wei J., Goldberg M.B., Burland V., Venkatesan M.M., Deng W., Fournier G., Mayhew G., Plunkett G. III, Rose D., Darling A., Mau B., Perna N.T., Payne S.M., Runyen-Janecky L., Zhou S., Schwartz D.C., Blattner F.R. Complete genomic sequence and comparative genomics of Shigella flexneri serotype 2a strain 2457T. Infect. Immun. 71:2003;2775-2786.
2. Jin Q., Yuan Z., Xu J., Wang Y., Shen Y., Lu W., Wang J., Liu H., Yang J., Yang F., Zhang X., Zhang J., Yang G., Wu H., Qu D., Dong J., Sun L., Xue Y., Zhao A., Gao Y., Zhu J., Kan B., Ding K., Chen S., Cheng H., Yao Z., He B., Chen R., Ma D., Qiang B., Wen Y., Hou Y., Yu J. Genome sequence of Shigella flexneri 2a: insights into pathogenicity through comparison with genomes of Escherichia coli K12 and O157. Nucleic Acids Res. 30:2002;4432-4441.
3. Bennish M.L. Potentially lethal complications of shigellosis. Rev. Infect. Dis. 13:1991;S319-S324.
4. Kotloff K.L., Winickoff J.P., Ivanoff B., Clemens J.D., Swedlow D.L., Sansonetti P.J., Adak G.K., Levine M.M.M. Global burden of Shigella infections: implications for vaccine development and implementation of control strategies. Bull. World Health Organ. 77:1999;651.
5. Bennish M.L., Wojtyniak B.J. Mortality due to shigellosis: community and hospital data. Rev. Infect. Dis. 13:1991;S245-S251.
6. Ashkenazi S., Levy I., Kazaronovski V., Samra Z. Growing antimicrobial resistance of Shigella isolates. J. Antimicrob. Chemother. 51:2003;427-429.
7. Moss J.E., Cardozo T.J., Zychlinsky A., Groisman E.A. The SelC-associated SHI-2 pathogenicity island of Shigella flexneri. Mol. Microbiol. 33:1999;74-83.
8. Rajakumar K., Sasakawa C., Adler B. Use of a novel approach, termed island probing, identifies the Shigella flexneri she pathogenicity island which encodes a homolog of the immunoglobulin A protease-like family of proteins. Infect. Immun. 65:1997;4606-4614.
9. Turner S.A., Luck S.N., Sakellaris H., Rajakumar K., Adler B. Nested deletions of the SRL pathogenicity island of Shigella flexneri 2a. J. Bacteriol. 183:2001;5535-5543.
10. Walker J.C., Verma N.K. Identification of a putative pathogenicity island in Shigella flexneri using subtractive hybridisation of the S. flexneri and Escherichia coli genomes. FEMS Microbiol. Lett. 10580:2002;1-8.
11. Allison G.E., Verma N.K. Serotype-converting bacteriophages and O-antigen modification in Shigella flexneri. Trends Microbiol. 8:2000;17-23.
12. Mallet C.P., VanDeVerg L.L., Collins H.H., Hale T.L. Evaluation of Shigella vaccine safety and efficacy in an intranasally challenged mouse model. Vaccine. 11:1993;190-196.
13. Oaks E.V., Wingfield M.E., Formal S.B. Plaque formation by virulent Shigella flexneri. Infect. Immun. 48:1985;124-129.
14. Sereny B. Experimental keratoconjunctivitis Shigellosa. Acta Microbiol. Acad. Sci. Hung. 1957;4.
15. Wassef J.S., Keren D.F., Mailloux J.L. Role of M cells in initial antigen uptake and in ulcer formation in the rabbit intestinal loop model of shigellosis. Infect. Immun. 57:1989;858-863.
16. DuPont H.L., Levine M.M., Hornick R.B., Formal S.B. Inoculum size in shigellosis and implications for expected mode of transmission. J. Infect. Dis. 159:1989;1126-1127.
17. Small P., Blankenhorn D., Welty D., Zinser E., Slonczewski J.L. Acid and base resistance in Escherichia coli and Shigella flexneri: role of rpoS and growth pH. J. Bacteriol. 176:1994;1729-1737.
18. Philpott D.J., Edgeworth J.D., Sansonetti P.J. The pathogenesis of Shigella flexneri infection: lessons from in vitro and in vivo studies. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 355:2000;575-586.
19. Mounier J., Vasselon T., Hellio R., Lesourd M., Sansonetti P.J. Shigella flexneri enters the human colonic Caco-2 epithelial cells through the basolateral pole. Infect. Immun. 60:1992;237-248.
20. Neutra M.R., Pringault E., Kraehenbuhl J.P. Antigen sampling across epithelial barriers and induction of mucosal immune responses. Annu. Rev. Immunol. 14:1996.
21. Sansonetti P.J., Phalipon A. M cells as ports of entry for enteroinvasive pathogens: mechanisms of interaction, consequences for the disease process. Semin. Immunol. 11:1999;193-203.
22. Beatty W.L., Sansonetti P.J. Role of lipopolysaccharide in signaling to subepithelial polymorphonuclear leukocytes. Infect. Immun. 65:1997;4395-4404.
23. Perdomo J.J., Gounon P., Sansonetti P.J. Polymorphonuclear leukocyte transmigration promotes invasion of colonic epithelial monolayer by Shigella flexneri. J. Clin. Invest. 93:1994;633-643.
24. Sansonetti P.J., Arondel J., Cavaillon J.M., Huerre M. Role of interleukin-1 in the pathogenesis of experimental shigellosis. J. Clin. Invest. 96:1995;884-892.
25. Sansonetti P.J., 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. 67:1999;1471-1480.
26. Perdomo O.J., Cavaillon J.M., Huerre M., Ohayon H., Gounon P., Sansonetti P.J. Acute inflammation causes epithelial invasion and mucosal destruction in experimental shigellosis. J. Exp. Med. 180:1994;1307-1319.
27. Sakaguchi T., Kohler H., Gu X., McCormick B.A., Reinecker H. Shigella flexneri regulates the tight junction-associated proteins in human intestinal epithelial cells. Cell. Microbiol. 4:2002;367-381.
28. Kuwae A., Yoshida S., Tamano K., Mimuro H., Suzuki T., Sasakawa C. Shigella invasion of macrophage requires the insertion of IpaC into the host plasma membrane. J. Biol. Chem. 276:2001;32230-32239.
29. High N., Mounier J., Prevost M.C., Sansonetti P.J. IpaB of Shigella flexneri causes entry into epithelial cells and escape from the phagocytic vacuole. EMBO J. 11:1992;1991-1999.
30. Chen R., Smith M.R., Thirumalai K., Zychlinsky A. A bacterial invasin induces macrophage apoptosis by binding directly to ICE. EMBO J. 15:1996;3853-3860.
31. Dinarello C.A. Interleukin-. 1β , Interleukin-18 and the Interleukin- 1β converting enzyme Ann. N.Y. Acad. Sci. 856:1998;1-11.
32. Zychlinsky A., Thirumalai K., Arondel J., Cantey J.R., Aliprantis A.O., Sansonetti P.J. In vivo apoptosis in Shigella flexneri infections. Infect. Immun. 64:1996;5357-5365.
33. Nutten A., Sansonetti P.J., Huet G., Bourdon-Bisiaux C., Meresse B., Colombel J., Desreumaux P. Epithelial inflammation response induced by Shigella flexneri depends on mucin gene expression. Microbes Infect. 4:2002;1121-1124.
34. Menard R., Sansonetti P.J., Parsot C. The secretion of the Shigella flexneri Ipa invasions is activated by epithelial cells and controlled by IpaB and IpaD. EMBO J. 13:1994;5293-5302.
35. Watarai M., Funato S., Sasakawa C. Interaction of Ipa proteins of Shigella flexneri with alpha5beta1 integrin promotes entry of the bacteria into mammalian cells. J. Exp. Med. 183:1996;991-999.
36. Alho A.M., Underhill C.B. The hyaluronate receptor is preferentially expressed on proliferating epithelial cells. J. Cell Biol. 108:1989;1557-1565.
37. Skoudy A., Mounier J., Aruffo A., Ohayon H., Gounon P., Sansonetti P.J., Tran Van Nhieu G. CD44 binds to the Shigella IpaB protein and participates in bacterial invasion of epithelial cells. Cell. Microbiol. 2:2000;19-33.
38. Tran Van Nhieu G., Sansonetti P.J. Mechanism of Shigella entry into epithelial cells. Curr. Opin. Microbiol. 2:1999;51-55.
39. Kohler H., Rodrigues S.P., McCormick B.A. S. flexneri interactions with the basolateral membrane domain of polarised model intestinal epithelium: role of LPS in cell invasion and in activation of the mitogen activated protein kinase ERK. Infect. Immun. 70:2002;1150-1158.
40. Aderem A., Ulevitch R.J. Toll-like receptors in the induction of the Innate Immune Response. Science. 406:2000;782-787.
41. Ingalls R.R., Monks B.G., Savedra R., Christ W.J., Delude R.L., Medvedev A.E., Espevik T., Golenbock D.T. CD11/CD18 and CD14 share a common lipid A signalling pathway. J. Immunol. 161:1998;5413-5420.
42. Hueck C.J. Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol. Mol. Biol. Rev. 62:1998;379-433.
43. Menard R., Sansonetti P.J., Parsot C. Non-polar mutagenesis of the ipa genes defines IpaB, IpaC and IpaD as effectors of Shigella entry into epithelial cells. J. Bacteriol. 175:1993;5899-5906.
44. Sasakawa C., Kamata K., Sakai T., Makino S., Yamada M., Okada N., Yoshikawa M. Virulence-associated genetic regions comprising 31 kilobases of the 230-kilobase plasmid in Shigella flexneri 2a. J. Bacteriol. 170:1988;2480-2484.
45. Menard R., Sansonetti P.J., Parsot C., Vasselon T. Extracellular association and cytoplasmic partitioning of the IpaB and IpaC invasins of Shigella flexneri. Cell. 79:1994;515-525.
46. Page A.L., Sansonetti P.J., Parsot C. Spa15 of Shigella flexneri, a third type of chaperone in the type III secretion pathway. Mol. Microbiol. 43:2002;1533-1542.
47. Harrington A.T., Hearn P.D., Picking W.L., Barker J.R., Wessel A., Picking W.D. Structural characterization of the N terminus of IpaC from Shigella flexneri. Infect. Immun. 71:2003;1255-1264.
48. Blocker A., Gounon P., Larquet E., Niebuhr K., Cabiaux V., Parsot C., Sansonetti P.J. The tripartite type III secretion of Shigella flexneri inserts IpaB and IpaC into hosts membranes. J. Cell Biol. 147:1999;683-693.
49. Tran Van Nhieu G., Caron E., Hall A., Sansonetti P.J. IpaC induces actin polymerization and filopodia formation during Shigella entry into epithelial cells. EMBO J. 18:1999;3249-3262.
50. Bourdet-Sicard R., Rudiger M., Jockusch B.M., Gounon P., Sansonetti P.J., Tran Van Nhieu G. Binding of the Shigella protein IpaA to vinculin induces F-actin depolymerization. EMBO J. 18:1999;5853-5862.
51. Tran Van Nhieu G., Ben-Ze'ev A., Sansonetti P.J. Modulation of bacterial entry into epithelial cells by association between vinculin and the Shigella IpaA invasin. EMBO J. 16:1997;2717-2729.
52. 2 into PtdIns(5)P by the S. flexneri effector IpgD reorganizes host cell morphology. EMBO J. 21:2002;5069-5078.
53. Yoshida S., Katayama E., Kuwae A., Mimuro H., Suzuki T., Sasakawa C. Shigella deliver an effector protein to trigger host microtubule destabilization, which promotes Rac1 activity and efficient bacterial internalization. EMBO J. 21:2002;2923-2935.
54. De Geyter C., Vogt B., Benjelloun-Touimi Z., Sansonetti P.J., Ruysschaert J.M., Cabiaux V. Purification of IpaC, a protein involved in entry of Shigella flexneri into epithelial cells and characterization of its interaction with lipid membranes. FEBS Lett. 400:1997;149-154.
55. Kueltzo L.A., Osiecki J., Barker J., Picking W.L., Ersoy B., Picking W.D., Middaugh C.R. Structure-function analysis of Invasion Plasmid Antigen C (IpaC) from Shigella flexneri. J. Biol. Chem. 278:2003;2792-2798.
56. Mantis N., Prevost M.C., Sansonetti P.J. Analysis of epithelial cell stress response during infection by Shigella flexneri. Infect. Immun. 64:1996;2474-2482.
57. Kane C.D., Schuch R., Day W.A., Maurelli A.T. MxiE regulates intracellular expression of factors secreted by the Shigella flexneri 2a type III secretion system. Infect. Immun. 184:2002;4409-4419.
58. Bernardini M.L., Mounier J., d'Hauteville H., Coquis-Rondon M., Sansonetti P.J. Identification of icsA, a plasmid locus of Shigella flexneri that governs bacterial intra- and intercellular spread through interaction with F-actin. Proc. Natl. Acad. Sci. USA. 86:1989;3867-3871.
59. Lett M., Sasakawa C., Okada N., Sakai T., Makino S., Yamada M., Komatsu K., Yoshikawa M. irG, a plasmid-coded virulence gene of Shigella flexneri: identification of the virG protein and determination of the complete coding sequence. J. Bacteriol. 171:1989;353-359.
60. Sansonetti P.J., Arondel J., Fontaine A., d'Hauteville H., Bernardini M.L. OmpB (osmo-regulation) and IcsA (cell-cell spread) mutants of Shigella flexneri; vaccine candidates and probes to study the pathogenesis of shigellosis. Vaccine. 9:1991;416-422.
61. Goldberg M.B., Barzu O., Parsot C., Sansonetti P.J. Unipolar localization and ATPase activity of IcsA, a Shigella flexneri protein involved in intracellular movement. J. Bacteriol. 175:1993;2189-2196.
62. Steinhauer J., Agha R., Pham T., Varga A.W., Goldberg M.B. The unipolar Shigella surface protein IcsA is targeted directly to the bacterial old pole: IcsP cleavage of IcsA occurs over the entire bacterial surface. Mol. Microbiol. 32:1999;367-377.
63. Charles M., Perez M., Kobil J.H., Goldberg M.B. Polar targeting of Shigella virulence factor IcsA in Enterobacteriacae and Vibrio. Proc. Natl. Acad. Sci. USA. 98:2001;9871-9876.
64. Sandlin R.C., Goldberg M.B., Maurelli A.T. Effect of O side-chain length and composition on the virulence of Shigella flexneri 2a. Mol. Microbiol. 22:1996;63-73.
65. Sandlin R.C., Lampel K.A., Keasler S.P., Goldberg M.B., Stolzer A.L., Maurelli A.T. Avirulence of rough mutants of Shigella flexneri: requirement of O antigen for correct unipolar localisation of IcsA in the bacterial outer membrane. Infect. Immun. 63:1995;229-237.
66. Van Den Bosch L., Manning P.A., Morona R. Regulation of O-antigen chain length is required for Shigella flexneri virulence. Mol. Microbiol. 23:1997;765-775.
67. Robbins J.R., Monack D.M., McCallum S.J., Vegas A., Pham E., Goldberg M.B., Theriot J.A. The making of a gradient: IcsA (VirG) polarity in Shigella flexneri. Mol. Microbiol. 41:2001;861-872.
68. Morona R., Daniels C., Van Den Bosch L. Genetic modulation of Shigella flexneri 2a lipopolysaccharide O antigen modal chain length reveals that it has been optimized for virulence. Microbiology. 149:2003;925-939.
69. Purdy G.E., Hong M., Panyne S. Shigella flexneri DegP facilitates IcsA surface expression and is required for efficient intercellular spread. Infect. Immun. 70:2002;6355-6364.
70. Suzuki T., Miki H., Takenawa T., Sasakawa C. Neural Wiskott-Aldrich syndrome protein is implicated in the actin based motility of Shigella flexneri. EMBO J. 17:1998;2767-2776.
71. Goldberg M.B. Shigella actin-based motility in the absence of vinculin. Cell Motil. Cytoskeleton. 37:1997;44-53.
72. Suzuki T., Saga S., Sasakawa C. Functional analysis of Shigella VirG domains essential for interaction with vinculin and actin-based motility. J. Biol. Chem. 271:1996.
73. Egile C., Loisel T.P., Laurent V., Li R., Pantaloni D., Sansonetti P.J., Carlier M.F. Activation of the CDC42 effector N-WASP by the Shigella flexneri IcsA protein promotes actin nucleation by Arp2/3 complex and bacterial actin-based motility. J. Cell Biol. 146:1999;1319-1332.
74. Suzuki T., Mimuro H., Suetsugu S., Miki H., Takenawa T., Sasakawa C. Neural Wiskott-Aldrich syndrome protein (N-WASP) is the specific ligand for Shigella VirG among the WASP family and determines the host cell type allowing actin-based spreading. Cell. Microbiol. 4:2002;223-233.
75. Monack D.M., Theriot J.A. Actin-based motility is sufficient for bacterial membrane protrusion formation and host cell uptake. Cell. Microbiol. 2:2001;633-647.
76. Rathman M., de Lanerolle P., Ohayon H., Gounon P., Sansonetti P.J. Myosin light chain kinase plays an essential role in S. flexneri dissemination. J. Cell Sci. 113:2000;3375-3386.
77. Sansonetti P.J., Mounier J., Prevost M.C., Mege R.M. Cadherin expression is required for the spread of Shigella flexneri between epithelial cells. Cell. 76:1994;829-839.
78. Page A.L., Ohayon H., Sansonetti P.J., Parsot C. The secreted IpaB and IpaC invasins and their cytoplasmic chaperone IpgC are required for intercellular dissemination of Shigella flexneri. Cell. Microbiol. 1:1999;183-193.
79. Suzuki T., Murai T., Fukuda T., Tobe T., Yoshikawa M., Sasakawa C. Identification and characterization of a chromosomal virulence gene, vacJ, required for intercellular spreading of Shigella flexneri. Mol. Microbiol. 11:1994;31-41.
80. Raqib R., Lindberg A.A., Wretlind B., Bardhan P.K., Andersson U., Andersson J. Persistence of local cytokine production in shigellosis in acute and convalescent stages. Infect. Immun. 63:1995;289-296.
81. Hathaway L.J., Griffin G.E., Sansonetti P.J., Edgeworth J.D. Human monocytes kill Shigella flexneri but then die by apoptosis associated with suppression of proinflammatory cytokine production. Infect. Immun. 70:2002;3833-3842.
82. Zychlinsky A., Prevost M.C., Sansonetti P.J. Shigella flexneri induces apoptosis in infected macrophages. Nature. 358:1992;167-169.
83. Biet F., Locht C., Kremer L. Immunoregulatory functions of interleukin 18 and its role in defense against bacterial pathogens. J. Mol. Med. 80:2002;147-162.
84. Way S.S., Borczuk A.C., Dominitz R., Goldberg M.B. An essential role for gamma interferon in innate resistance to Shigella flexneri infection. Infect. Immun. 66:1998;1342-1348.
85. Mandic-Mulec I., Weiss J., Zychlinsky A. Shigella flexneri is trapped in polymorphonuclear leukocyte vacuoles and efficiently killed. Infect. Immun. 65:1997;110-115.
86. Weinrauch Y., Drujan D., Shapiro S.D., Weiss J., Zychlinsky A. Neutrophil elastase targets virulence factors of enterobacteria. Nature. 417:2002;91-94.
87. Zhang J., Jin L., Champion G., Seydel K.B., Stanley S.L. Shigella infection in a SCID mouse-human intestinal xenograft model: role for neutrophils in containing bacterial dissemination in human intestine. Infect. Immun. 69:2001;3240-3247.
88. Gomez H.F., Ochoa T.J., Carlin L.G., Cleary T.G. Human lactoferrin impairs virulence of Shigella flexneri. J. Infect. Dis. 187:2003;87-95.
89. Salzman N.H., Ghosh D., Huttner K.M., Paterson Y., Bevins C.L. Protection against enteric salmonellosis in transgenic mice expressing a human intestinal defensin. Nature. 422:2003;522-526.
90. Islam D., Christensson B. Disease dependant changes in T-cell populations in patients with shigellosis. APMIS. 108:2000;251-260.
91. Islam D., Bardhan P.K., Lindberg A.A., 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. 63:1995;2941-2949.
92. Islam D., Wretlind B., Lindberg A.A., Christensson B. Changes in the peripheral blood T-cell receptor. Vβ repertoire in vivo and in vitro during shigellosis Infect. Immun. 64:1996;1391-1399.
93. Zwillich S.H., Duby A.D., Lipsky P.E. T-lymphocyte clones responsive to Shigella flexneri. J. Clin. Microbiol. 27:1989;417-421.
94. Kotloff K.L., Noriega F.R., Samandari T., Sztein M.B., Losonsky G.A., Nataro J.P., Picking W.D., Barry E.M., Levine M.M. Shigella flexneri 2a strain CVD 1207, with specific deletions in virG, sen, set and guaBA, is highly attenuated in humans. Infect. Immun. 68:2000;1034-1039.
95. van de Verg L.L., Mallet C.P., Collins H.H., Larsen T., Hammack C., Hale T.L. Antibody and cytokine responses in a mouse pulmonary model of Shigella flexneri serotype 2a infection. Infect. Immun. 63:1995;1947-1954.
96. Nelson M.R., Shanson D.C., Hawkins D.A., Gazzard B.G. Salmonella, Campylobacter and Shigella in HIV-seropositive patients. AIDS. 6:1992;1495-1498.
97. Way S.S., Borczuk A.C., Goldberg M.B. Thymic independance of adaptive immunity to the intracellular pathogen Shigella flexneri serotype 2a. Infect. Immun. 67:1999;3970-3979.
98. DuPont H.L., Hornick R.B., Synder M.J., Libonati J.P., Formal S.B., Gangarosa E.J. Immunity in shigellosis. II. Protection induced by oral live vaccine or primary infection. J. Infect. Dis. 125:1972;12-16.
99. Formal S.B., Oaks E.V., Olsen R.E., Wingfield M.E., Snoy P.J., Cogan J.P. Effect of prior infection with virulent Shigella flexneri 2a on the resistance of monkeys to subsequent infection with Shigella sonnei. J. Infect. Dis. 164:1991;533-537.
100. Mel D.M., Bogoljub L.A., Nikolic B.D., Radovanic M.L. Studies on vaccination against bacillary dysentery. 4. Oral immunization with live monotypic and combined vaccines. Bull. World Health Organ. 39:1968;375-380.
101. Van De Verg L.L., Bendiuk N.O., Kotloff K., Marsh M.M., Ruckert J.L., Puryear J.L., Taylor D.N., Hartman A.B. Cross-reactivity of Shigella flexneri serotype 2a O antigen antibodies following immunization or infection. Vaccine. 14:1996;1062-1068.
102. Raqib R., Qadri F., Sarker P., Mia S.M., Sansonetti P.J., Albert M.J., Andersson J. Delayed and reduced adaptive humoral immune responses in children with shigellosis compared with in adults. Scand. J. Immunol. 55:2002;414-423.
103. Phalipon A., Cardona A., Kraehenbuhl J.P., Edelman L., Sansonetti P.J., Corthesy B. Secretory component: a new role in secretory IgA-mediated immune exclusion in vivo. Immunity. 17:2002;107-115.
104. Iijima H., Takahashi I., Kiyono H. Mucosal immune network in the gut for the control of infectious diseases. Rev. Med. Virol. 11:2001;117-133.
105. Cohen D., Block C., Green M.S., Lowell G.H., Ofek I. Immunoglobulin M, A and G antibody response to lipopolysaccharide O antigen in symptomatic and asymptomatic Shigella infections. J. Clin. Microbiol. 27:1989;162-167.
106. Islam D., Veress B., Bardhan P.K., Lindberg A.A., Christensson B. Quantitative assessment of IgG and IgA subclass producing cells in rectal mucosa during shigellosis. J. Clin. Pathol. 50:1997;513-520.
107. Oberhelman R.A., Kopecko D.J., Salazar-Lindo E., Gotuzzo E., Buysse J.M., Venkatesan M.M., Fernandez-Prada C., Guzman M., Leon-Barua R. Prospective study of systemic and mucosal immune responses in dysenteric patients to specific Shigella invasion plasmid antigens and lipopolysaccharides. Infect. Immun. 59:1991;2341-2350.
108. Rasolofo-Razanamparany V., Cassel-Beraud A.M., Roux J., Sansonetti P.J., Phalipon A. Predominance of serotype-specific mucosal antibody response in Shigella flexneri -infected humans living in an area of endemicity. Infect. Immun. 69:2001;5230-5234.
109. Schultsz C., Qadri F., Hossain S.A., Ahmed F., Ciznar I. Shigella-specific IgA in saliva of children with bacillary dysentery. FEMS Microbiol. Immunol. 4:1992;65-72.
110. Clemens J.D., Stanton B., Stoll B., Shahid N.S., Banu H., Chowdhury A.K. Breastfeeding as a determinant of severity in shigellosis: evidence for protection throughout the first three years of life in Bangladesh children. Am. J. Epidemiol. 123:1986;710-720.
111. Phalipon A., Kaufman M., Michetti P., Cavaillon J.M., Huerre M., Sansonetti P.J., Kraehenbuhl J.P. Monoclonal immunoglobulin A antibody directed against serotype-specific epitope of Shigella flexneri lipopolysaccharide protects against murine experimental shigellosis. J. Exp. Med. 182:1995;769-778.
112. Oaks E.V., Hale T.L., Formal S.B. Serum immune response to Shigella protein antigens in Rhesus monkeys and humans infected with Shigella species. Infect. Immun. 53:1986;57-63.
113. van de Verg L.L., Herrington D.A., Boslego J., Lindberg A.A., Levine M.M. 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. 166:1992;158-161.
114. Way S.S., Borczuk A.C., Goldberg M.B. Adaptive immune response to Shigella flexneri 2a cydC in immunocompetent mice and mice lacking immunoglobulin A. Infect. Immun. 67:1999;2001-2004.
115. Cohen D., Green M.S., 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. 29:1991;386-389.
116. Lowell G.H., MacDermott R.P., Summers P.L., Reeder A.A., Bertovich M.J., Formal S.B. Antibody-dependant cell-mediated antibacterial activity: K lymphocytes, monocytes and granulocytes are effective against Shigella. J. Immunol. 125:1980.
117. Reed W.P., Albright E.L. Serum factors responsible for killing of Shigella. Immunology. 26:1974;205-215.
118. Barnes L.A., Cooper M.L., Jerome E.A., Durant R.C., Smith A.B. Field trial of Shigella flexneri III vaccine. VI. Mouse protective studies. J. Immunol. 66:1951;515-525.
119. Bennett I.L., Gordon R.S., Barnes L.A. A field trial of Shigella flexneri III vaccine. II. Serum agglutination studies. J. Infect. Dis. 85:1949;180-194.
120. Cooper M.L., Tepper J., Keller H.M. Studies in dysentery vaccination. IV. Primary vaccination of children with monovalent vaccines of Shigella. J. Immunol. 60:1948;189-203.
121. Higgins A., Floyd T., Kader M. Studies in shigellosis. III. A controlled evaluation of monovalent Shigella vaccine in a highly endemic environment. Am. J. Trop. Med. Hyg. 4:1955;281-288.
122. Fries L.F., Montemarano A.D., Mallet C.P., Taylor D.N., Hale T.L., Lowell G.H. Safety and immunogenicity of a proteosome-Shigella flexneri 2a lipopolysaccharide vaccine administered intranasally to healthy adults. Infect. Immun. 69:2001;4545-4553.
123. Ashkenazi S., Passwell J.H., Harlev E., Miron D., Dagan R., Farzan N., Ramon R., Majadly F., Bryla D.A., Karpas A.B., Robbins J.R., Schneerson R. Safety and immunogenicity of Shigella sonnei and Shigella flexneri 2a O-specific polysaccharide conjugates in children. J. Infect. Dis. 179:1999;1565-1568.
124. Cohen D., Ashkenazi S., Green M.S., Lerman Y., Slepon R., Robin G., Orr N., Taylor D.N., Sadoff J.C., Chu C., Shiloach J., Schneerson R., Robbins J.R. Safety and immunogenicity of investigational Shigella conjugate vaccines in Israeli volunteers. Infect. Immun. 64:1996;4074-4077.
125. Passwell J.H., Harlev E., Ashkenazi S., Chu C., Miron D., Ramon R., Farzan N., Shiloach J., Bryla D.A., Majadly F., Roberson R., Robbins J.R., Schneerson R. Safety and immunogenicity of improved Shigella O-specific polysaccharide-protein conjugate vaccines in adults in Israel. Infect. Immun. 69:2001;1351-1357.
126. Taylor D.N., Trofa A.C., Sadoff J.C., Chu C., Bryla D.A., Shiloach J., Cohen D., Ashkenazi S., Lerman Y., Egan W. 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. 61:1993;3678-3687.
127. Turbyfill K.R., Hartman A.B., Oaks E.V. Isolation and characterization of a Shigella flexneri invasin complex subunit vaccine. Infect. Immun. 68:2000;6624-6632.
128. Levenson V.I., Chernokhvostova E.V., Lyubinskaya M.M., Salamatova S.A., Dzhikidze E., Stasilevitch Z.K. Parental immunization with Shigella ribosomal vaccine elicits local IgA response and primes for mucosal memory. Int. Arch. Allergy Immunol. 87:1988;25-31.
129. Levenson V.I., Egorova T.P. Polysaccharide nature of O-antigen in protective ribosomal preparations from Shigella: experimental evidence and implications from the ribosomal vaccine concept. Res. Microbiol. 141:1990;707-720.
130. Formal S.B., LaBrec E., Palmer A., Falkow S. Protection of monkeys against experimental shigellosis with attenuated vaccines. J. Bacteriol. 90:1965;63-68.
131. Chakrabarti M.K., Bhattacharya J., Bhattacharya M.K., Nair G.B., Bhattacharya S.K., Mahalanabis D. Killed oral Shigella vaccine made from Shigella flexneri 2a protects against challenge in the rabbit model of shigellosis. Acta Paediatr. 88:1999;161-165.
132. 32-ISTRATI). Arch. Roum. Pathol. Exp. Microbiol. 43:1984;251-278.
133. Karnell A., Li A., Zhao C.R., Karlsson K., Nguyen B.M., Lindberg A.A. Safety and immunogenicity study of the auxotrophic Shigella flexneri 2a vaccine SFL1070 with a deleted aroD gene in adult Swedish volunteers. Vaccine. 13:1995;88-99.
134. Kotloff K.L., Noriega F.R., Losonsky G.A., Sztein M.B., Wasserman S.S., Nataro J.P., Levine M.M. Safety, immunogenicity, and transmissibility in humans of CVD1203, a live oral Shigella flexneri 2a vaccine candidate attenuated by deletions in aroA and virG. Infect. Immun. 64:1996;4542-4548.
135. Li A., Pal T., Forsum U., Lindberg A.A. Safety and immunogenicity of the live oral auxotrophic Shigella flexneri SFL124 in volunteers. Vaccine. 10:1992;395-404.
136. Coster T.S., Hoge C.W., van de Verg L.L., Hartman A.B., Oaks E.V., Venkatesan M.M., Cohen D., Robin G., Fontaine-Thompson A., Sansonetti P.J., Hale T.L. Vaccination against shigellosis with attenuated Shigella flexneri 2a strain SC602. Infect. Immun. 67:1999;3437-3443.
137. Falkow S., Schneider H., Baron L.S., Formal S.B. Virulence of Escherichia-Shigella genetic hybrids for the guinea pig. J. Bacteriol. 86:1963;1251-1258.
138. Levine M.M., Woodward D., Formal S.B., Gemski P., DuPont H.L., Hornick R.B., Snyder M. Studies with a new generation of oral attenuated Shigella vaccine: Escherichia coli bearing surface antigens of Shigella flexneri. J. Infect. Dis. 136:1977;577-582.
139. Kotloff K.L., Herrington D.A., Hale T.L., Newland J.W., van de Verg L.L., Cogan J.P., Snoy P.J., Sadoff J.C., Formal S.B., Levine M.M. Safety, immunogenicity and efficacy in monkeys and humans of invasive Escherichia coli K-12 vaccine candidates expressing Shigella flexneri 2a somatic antigen. Infect. Immun. 60:1992;2218-2224.
140. Kotloff K.L., Losonsky G.A., Nataro J.P., Wasserman S.S., Hale T.L., Taylor D.N., Newland J.W., Sadoff J.C., Formal S.B., Levine M.M. Evaluation of the safety, immunogenicity and efficacy in healthy adults of four doses of live oral hybrid Escherichia coli-Shigella flexneri 2a vaccine strain EcSf2a-2. Vaccine. 13:1995;495-502.
141. Rui X., Xu Y., Wan H., Su G., Huang C. Construction of a stable and non-resistant bivalent vaccine candidate strain against Shigella flexneri 2a and Shigella sonnei. Chin. J. Biotechnol. 12:1996;89-97.
142. Klee S.R., Tzscgaschel B.D., Singh M., Falt I., Lindberg A.A., Timmis K.N., Guzman C.A. Construction and characterization of genetically-marked bivalent anti-Shigella dysenteriae and anti-Shigella flexneri Y live vaccine candidates. Microb. Pathogenesis. 22:1997;363-376.
143. Carlin N.I.A., Lindberg A.A. Monoclonal antibodies specific for Shigella flexneri lipopolysaccharides: clones binding to type IV, V and VI antigens, group 3,4 antigen and an epitope common to all Shigella flexneri and Shigella dysenteriae type 1 strains. Infect. Immun. 55:1987;1412-1420.
144. Noriega F.R., Liao F.M., Maneval D.R., Ren S., Formal S.B., Levine M.M. Strategy for cross-protection among Shigella flexneri serotypes. Infect. Immun. 67:1999;782-788.
145. Guan S., Verma N.K. Serotype conversion of a Shigella flexneri candidate vaccine strain via a novel site specific chromosome-integration system. FEMS Microbiol. Lett. 166:1998;79-87.
146. DuPont H.L., Hornick R.B., Snyder M., Libonati J.P., Formal S.B., Gangarosa E.J. Immunity in shigellosis. I. Response of man to attenuated strains of Shigella. J. Infect. Dis. 125:1972;5-11.
147. Mills J.A., Venkatesan M.M., Baron L.S., Buysse J.M. Spontaneous insertion of an IS1-like element into the virF gene is responsible for avirulence in opaque colonial variants of Shigella flexneri 2a. Infect. Immun. 60:1992;175-182.
148. Levine M.M., Gangarosa E.J., Werner M., Morris G.K. Shigellosis in custodial institutions. III. Prospective clinical and bacteriologic surveillance of children vaccinated with oral attenuated Shigella vaccines. J. Pediatr. 84:1974;803-806.
149. Mel D.M., Terzin A.L., Vuksic L. Studies on vaccination against bacillary dysentery. 3. Effective oral immunization against Shigella flexneri 2a in a field trial. Bull. World Health Organ. 32:1965;647-655.
150. 32-ISTRATI Shigella flexneri 2a vaccine strain. Vaccine. 9:1991;358-363.
151. Sansonetti P.J., Arondel J. Construction and evaluation of a double mutant of S. flexneri as a candidate for oral vaccination against shigellosis. Vaccine. 7:1989;443-450.
152. Dentchev V., Marinova S., Vassilev T., Bratoyeva M., Linde K. Live Shigella flexneri 2a and Shigella sonnei I vaccine candidate strains with two attenuating markers. II. Preliminary results of vaccination of adult volunteers and children aged 2-17 years. Vaccine. 8:1990;30-34.
153. Linde K., Dentchev V., Bondarenko V., Marinova S., Randhagen B., Bratoyeva M., Tsvetanov Y., Romanova Y. Live Shigella flexneri and Shigella sonnei I vaccine candidate strains with two attenuating markers. I. Construction of vaccine candidate strains with retained invasiveness but reduced intracellular multiplication. Vaccine. 8:1990;25-29.
154. Linde K., Randhagen B., Beer J., Dentchev V., Marinova S., Vassilev T., Bratoyeva M. Shigella flexneri 2a and sonnei I vaccine with two attenuating markers: construction, tolerability and immunogenicity in 143 children aged 3-17 years. Vaccine. 11:1993;197-199.
155. Ahmed Z.U., Sarker M.R., Sack D.A. Protection of adult rabbits and monkeys from lethal shigellosis by oral immunization with a thymine-requiring and temperature-sensitive mutant of Shigella flexneri Y. Vaccine. 8:1990;153-158.
156. Ashraf M.M., Giri D.K., Batra H.V., Khandekar P., Ahmed Z.U., Talwar G.P. Potentials of Shigella flexneri Y strain TSF21 as a candidate vaccine against shigellosis: safety, immunogenicity and protective efficacy in Bonnet monkeys. FEMS Microbiol. Immunol. 3:1991;165-170.
157. Karnell A., Sweiha H., Lindberg A.A. Auxotrophic live oral Shigella flexneri vaccine protects against challenge with S. flexneri of different serotypes. Vaccine. 10:1992;167-174.
158. Karnell A., Stocker B.A., Katakura S., Reinholt F.P., Lindberg A.A. Live oral auxotrophic Shigella flexneri SFL124 vaccine with a deleted aroD gene: characterisation and monkey protection studies. Vaccine. 10:1992;389-394.
159. Li A., Cam P.D., Islam D., Minh N.B., Huan P.T., Rong Z.C., Karlsson K., Lindberg A.A., Lindberg G. Immune response in vietnamese children after a single dose of the auxotrophic, live Shigella flexneri Y vaccine strain SFL124. J. Infect. 28:1994;11-23.
160. Li A., Karnell A., Huan P.T., Cam P.D., Minh N.B., Tram L.N., Quy N.P., Trach D.D., Karlsson K., Lindberg G. Safety and immunogenicity of the live oral auxotrophic Shigella flexneri SFL124 in adult vietnamese volunteers. Vaccine. 11:1993;180-189.
161. Karnell A., Cam P.D., Verma N.K., Lindberg A.A. AroD deletion attenuates Shigella flexneri strain 2457T and makes it a safe and efficacious oral vaccine in monkeys. Vaccine. 11:1993;830-836.
162. Noregia F., Wang J., Losonsky G., Maneval D., Hone D., Levine M. Construction and characterization of attenuated delta aroA delta virG Shigella flexneri 2a strain CVD 1203, a prototype live oral vaccine. Infect. Immun. 62:1994;5168-5172.
163. Noriega F.R., Losonsky G.A., Wang J.Y., Formal S.B., Levine M.M. Further characterisation of aroA virG Shigella flexneri 2a strain CVD 1203 as a mucosal Shigella vaccine and as a live-vector vaccine for delivering antigens of enterotoxigenic Escherichia coli. Infect. Immun. 64:1996;23-27.
164. Barzu S., Fontaine A., Sansonetti P.J., Phalipon A. Induction of a local anti-IpaC antibody response in mice by use of a Shigella flexneri 2a vaccine candidate: implications for use of IpaC as a protein carrier. Infect. Immun. 64:1996;1190-1196.