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Microbiol Rev. Jun 1991; 55(2): 206–224.
PMCID: PMC372811

Genetic basis of virulence in Shigella species.


Shigella species and enteroinvasive strains of Escherichia coli cause disease by invasion of the colonic epithelium, and this invasive phenotype is mediated by genes carried on 180- to 240-kb plasmids. In addition, at least eight loci on the Shigella chromosome are necessary for full expression of virulence. The products of these genes can be classified as (i) virulence determinants that directly affect the ability of shigellae to survive in the intestinal tissues, e.g., the aerobactin siderophore (iucABCD and iutA), superoxide dismutase (sodB), and somatic antigen expression (rfa and rfb); (ii) cytotoxins that contribute to the severity of disease, e.g., the Shiga toxin (stx) and a putative analog of this toxin (flu); and (iii) regulatory loci that affect the expression of plasmid genes, e.g., ompR-envZ, which mediates response to changes in osmolarity, virR (osmZ), which mediates response to changes in temperature, and kcpA, which affects the translation of the plasmid virG (icsA) gene which is associated with intracellular bacterial mobility and intracellular bacterial spread. A single plasmid regulatory gene (virF) controls a virulence-associated plasmid regulon including virG (icsA) and two invasion-related loci, i.e., (i) ipaABCD, encoding invasion plasmid antigens that may be structural components of the Shigella invasion determinant; and (ii) invAKJH (mxi), which is necessary for insertion of invasion plasmid antigens into the outer membrane.

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  • Adler B, Sasakawa C, Tobe T, Makino S, Komatsu K, Yoshikawa M. A dual transcriptional activation system for the 230 kb plasmid genes coding for virulence-associated antigens of Shigella flexneri. Mol Microbiol. 1989 May;3(5):627–635. [PubMed]
  • Ashkenazi S, Cleary KR, Pickering LK, Murray BE, Cleary TG. The association of Shiga toxin and other cytotoxins with the neurologic manifestations of shigellosis. J Infect Dis. 1990 May;161(5):961–965. [PubMed]
  • Bachmann BJ. Linkage map of Escherichia coli K-12, edition 8. Microbiol Rev. 1990 Jun;54(2):130–197. [PMC free article] [PubMed]
  • Baudry B, Kaczorek M, Sansonetti PJ. Nucleotide sequence of the invasion plasmid antigen B and C genes (ipaB and ipaC) of Shigella flexneri. Microb Pathog. 1988 May;4(5):345–357. [PubMed]
  • Baudry B, Maurelli AT, Clerc P, Sadoff JC, Sansonetti PJ. Localization of plasmid loci necessary for the entry of Shigella flexneri into HeLa cells, and characterization of one locus encoding four immunogenic polypeptides. J Gen Microbiol. 1987 Dec;133(12):3403–3413. [PubMed]
  • Bennish ML, Harris JR, Wojtyniak BJ, Struelens M. Death in shigellosis: incidence and risk factors in hospitalized patients. J Infect Dis. 1990 Mar;161(3):500–506. [PubMed]
  • Bernardini ML, Fontaine A, Sansonetti PJ. The two-component regulatory system ompR-envZ controls the virulence of Shigella flexneri. J Bacteriol. 1990 Nov;172(11):6274–6281. [PMC free article] [PubMed]
  • Black RE, Craun GF, Blake PA. Epidemiology of common-source outbreaks of shigellosis in the United States, 1961-1975. Am J Epidemiol. 1978 Jul;108(1):47–52. [PubMed]
  • Blaser MJ, Hale TL, Formal SB. Recurrent shigellosis complicating human immunodeficiency virus infection: failure of pre-existing antibodies to confer protection. Am J Med. 1989 Jan;86(1):105–107. [PubMed]
  • Bunning VK, Raybourne RB, Archer DL. Foodborne enterobacterial pathogens and rheumatoid disease. Soc Appl Bacteriol Symp Ser. 1988;17:87S–107S. [PubMed]
  • Butler T, Speelman P, Kabir I, Banwell J. Colonic dysfunction during shigellosis. J Infect Dis. 1986 Nov;154(5):817–824. [PubMed]
  • Buysse JM, Stover CK, Oaks EV, Venkatesan M, Kopecko DJ. Molecular cloning of invasion plasmid antigen (ipa) genes from Shigella flexneri: analysis of ipa gene products and genetic mapping. J Bacteriol. 1987 Jun;169(6):2561–2569. [PMC free article] [PubMed]
  • Buysse JM, Venkatesan M, Mills JA, Oaks EV. Molecular characterization of a trans-acting, positive effector (ipaR) of invasion plasmid antigen synthesis in Shigella flexneri serotype 5. Microb Pathog. 1990 Mar;8(3):197–211. [PubMed]
  • Clerc PL, Berthon B, Claret M, Sansonetti PJ. Internalization of Shigella flexneri into HeLa cells occurs without an increase in cytosolic Ca2+ concentration. Infect Immun. 1989 Sep;57(9):2919–2922. [PMC free article] [PubMed]
  • Clerc PL, Ryter A, Mounier J, Sansonetti PJ. Plasmid-mediated early killing of eucaryotic cells by Shigella flexneri as studied by infection of J774 macrophages. Infect Immun. 1987 Mar;55(3):521–527. [PMC free article] [PubMed]
  • Clerc P, Sansonetti PJ. Entry of Shigella flexneri into HeLa cells: evidence for directed phagocytosis involving actin polymerization and myosin accumulation. Infect Immun. 1987 Nov;55(11):2681–2688. [PMC free article] [PubMed]
  • Clerc PL, Sansonetti PJ. Evidence for clathrin mobilization during directed phagocytosis of Shigella flexneri by HEp2 cells. Microb Pathog. 1989 Nov;7(5):329–336. [PubMed]
  • Csonka LN. Physiological and genetic responses of bacteria to osmotic stress. Microbiol Rev. 1989 Mar;53(1):121–147. [PMC free article] [PubMed]
  • Daskaleros PA, Payne SM. Cloning the gene for Congo red binding in Shigella flexneri. Infect Immun. 1985 Apr;48(1):165–168. [PMC free article] [PubMed]
  • Daskaleros PA, Payne SM. Characterization of Shigella flexneri sequences encoding congo red binding (crb): conservation of multiple crb sequences and role of IS1 in loss of the Crb+ phenotype. Infect Immun. 1986 Nov;54(2):435–443. [PMC free article] [PubMed]
  • Daskaleros PA, Payne SM. Congo red binding phenotype is associated with hemin binding and increased infectivity of Shigella flexneri in the HeLa cell model. Infect Immun. 1987 Jun;55(6):1393–1398. [PMC free article] [PubMed]
  • de Lorenzo V, Herrero M, Neilands JB. IS1-mediated mobility of the aerobactin system of pColV-K30 in Escherichia coli. Mol Gen Genet. 1988 Aug;213(2-3):487–490. [PubMed]
  • Derbyshire P, Baldwin T, Stevenson P, Griffiths E, Roberts M, Williams P, Hale TL, Formal SB. Expression in Escherichia coli K-12 of the 76,000-dalton iron-regulated outer membrane protein of Shigella flexneri confers sensitivity to cloacin DF13 in the absence of Shigella O antigen. Infect Immun. 1989 Sep;57(9):2794–2798. [PMC free article] [PubMed]
  • Dorman CJ, Ni Bhriain N, Higgins CF. DNA supercoiling and environmental regulation of virulence gene expression in Shigella flexneri. Nature. 1990 Apr 19;344(6268):789–792. [PubMed]
  • DuPont HL, Levine MM, Hornick RB, Formal SB. Inoculum size in shigellosis and implications for expected mode of transmission. J Infect Dis. 1989 Jun;159(6):1126–1128. [PubMed]
  • Eiklid K, Olsnes S. Animal toxicity of Shigella dysenteriae cytotoxin: evidence that the neurotoxic, enterotoxic, and cytotoxic activities are due to one toxin. J Immunol. 1983 Jan;130(1):380–384. [PubMed]
  • Endo Y, Tsurugi K, Yutsudo T, Takeda Y, Ogasawara T, Igarashi K. Site of action of a Vero toxin (VT2) from Escherichia coli O157:H7 and of Shiga toxin on eukaryotic ribosomes. RNA N-glycosidase activity of the toxins. Eur J Biochem. 1988 Jan 15;171(1-2):45–50. [PubMed]
  • Fasano A, Kay BA, Russell RG, Maneval DR, Jr, Levin MM. Enterotoxin and cytotoxin production by enteroinvasive Escherichia coli. Infect Immun. 1990 Nov;58(11):3717–3723. [PMC free article] [PubMed]
  • Fontaine A, Arondel J, Sansonetti PJ. Role of Shiga toxin in the pathogenesis of bacillary dysentery, studied by using a Tox- mutant of Shigella dysenteriae 1. Infect Immun. 1988 Dec;56(12):3099–3109. [PMC free article] [PubMed]
  • Formal SB, Gemski P, Baron LS, Labrec EH. Genetic Transfer of Shigella flexneri Antigens to Escherichia coli K-12. Infect Immun. 1970 Mar;1(3):279–287. [PMC free article] [PubMed]
  • Formal SB, Gemski P, Baron LS, Labrec EH. A Chromosomal Locus Which Controls the Ability of Shigella flexneri to Evoke Keratoconjunctivitis. Infect Immun. 1971 Jan;3(1):73–79. [PMC free article] [PubMed]
  • Formal SB, Labrec EH, Palmer A, Falkow S. Protection of Monkeys Against Experimental Shigellosis with Attenuated Vaccines. J Bacteriol. 1965 Jul;90(1):63–68. [PMC free article] [PubMed]
  • Franzon VL, Arondel J, Sansonetti PJ. Contribution of superoxide dismutase and catalase activities to Shigella flexneri pathogenesis. Infect Immun. 1990 Feb;58(2):529–535. [PMC free article] [PubMed]
  • Gemski P, Jr, Koeltzow DE, Formal SB. Phage conversion of Shigella flexneri group antigens. Infect Immun. 1975 Apr;11(4):685–691. [PMC free article] [PubMed]
  • Gemski P, Jr, Sheahan DG, Washington O, Formal SB. Virulence of Shigella flexneri hybrids expressing Escherichia coli somatic antigens. Infect Immun. 1972 Aug;6(2):104–111. [PMC free article] [PubMed]
  • GERBER DF, WATKINS HM. Growth of shigellae in monolayer tissue cultures. J Bacteriol. 1961 Dec;82:815–822. [PMC free article] [PubMed]
  • Göransson M, Sondén B, Nilsson P, Dagberg B, Forsman K, Emanuelsson K, Uhlin BE. Transcriptional silencing and thermoregulation of gene expression in Escherichia coli. Nature. 1990 Apr 12;344(6267):682–685. [PubMed]
  • Gots RE, Formal SB, Giannella RA. Indomethacin inhibition of Salmonella typhimurium, Shigella flexneri, and cholera-mediated rabbit ileal secretion. J Infect Dis. 1974 Sep;130(3):280–284. [PubMed]
  • Griffiths E, Stevenson P, Hale TL, Formal SB. Synthesis of aerobactin and a 76,000-dalton iron-regulated outer membrane protein by Escherichia coli K-12-Shigella flexneri hybrids and by enteroinvasive strains of Escherichia coli. Infect Immun. 1985 Jul;49(1):67–71. [PMC free article] [PubMed]
  • Hale TL, Bonventre PF. Shigella infection of Henle intestinal epithelial cells: role of the bacterium. Infect Immun. 1979 Jun;24(3):879–886. [PMC free article] [PubMed]
  • Hale TL, Formal SB. Protein synthesis in HeLa or Henle 407 cells infected with Shigella dysenteriae 1, Shigella flexneri 2a, or Salmonella typhimurium W118. Infect Immun. 1981 Apr;32(1):137–144. [PMC free article] [PubMed]
  • Hale TL, Guerry P, Seid RC, Jr, Kapfer C, Wingfield ME, Reaves CB, Baron LS, Formal SB. Expression of lipopolysaccharide O antigen in Escherichia coli K-12 hybrids containing plasmid and chromosomal genes from Shigella dysenteriae 1. Infect Immun. 1984 Nov;46(2):470–475. [PMC free article] [PubMed]
  • Hale TL, Morris RE, Bonventre PF. Shigella infection of henle intestinal epithelial cells: role of the host cell. Infect Immun. 1979 Jun;24(3):887–894. [PMC free article] [PubMed]
  • Hale TL, Oaks EV, Formal SB. Identification and antigenic characterization of virulence-associated, plasmid-coded proteins of Shigella spp. and enteroinvasive Escherichia coli. Infect Immun. 1985 Dec;50(3):620–629. [PMC free article] [PubMed]
  • Hale TL, Sansonetti PJ, Schad PA, Austin S, Formal SB. Characterization of virulence plasmids and plasmid-associated outer membrane proteins in Shigella flexneri, Shigella sonnei, and Escherichia coli. Infect Immun. 1983 Apr;40(1):340–350. [PMC free article] [PubMed]
  • Hartman AB, Venkatesan M, Oaks EV, Buysse JM. Sequence and molecular characterization of a multicopy invasion plasmid antigen gene, ipaH, of Shigella flexneri. J Bacteriol. 1990 Apr;172(4):1905–1915. [PMC free article] [PubMed]
  • Headley VL, Payne SM. Differential protein expression by Shigella flexneri in intracellular and extracellular environments. Proc Natl Acad Sci U S A. 1990 Jun;87(11):4179–4183. [PMC free article] [PubMed]
  • Higgins CF, Dorman CJ, Stirling DA, Waddell L, Booth IR, May G, Bremer E. A physiological role for DNA supercoiling in the osmotic regulation of gene expression in S. typhimurium and E. coli. Cell. 1988 Feb 26;52(4):569–584. [PubMed]
  • Hromockyj AE, Maurelli AT. Identification of an Escherichia coli gene homologous to virR, a regulator of Shigella virulence. J Bacteriol. 1989 May;171(5):2879–2881. [PMC free article] [PubMed]
  • Hromockyj AE, Maurelli AT. Identification of Shigella invasion genes by isolation of temperature-regulated inv::lacZ operon fusions. Infect Immun. 1989 Oct;57(10):2963–2970. [PMC free article] [PubMed]
  • Hulton CS, Seirafi A, Hinton JC, Sidebotham JM, Waddell L, Pavitt GD, Owen-Hughes T, Spassky A, Buc H, Higgins CF. Histone-like protein H1 (H-NS), DNA supercoiling, and gene expression in bacteria. Cell. 1990 Nov 2;63(3):631–642. [PubMed]
  • Isberg RR, Leong JM. Cultured mammalian cells attach to the invasin protein of Yersinia pseudotuberculosis. Proc Natl Acad Sci U S A. 1988 Sep;85(18):6682–6686. [PMC free article] [PubMed]
  • Isberg RR, Leong JM. Multiple beta 1 chain integrins are receptors for invasin, a protein that promotes bacterial penetration into mammalian cells. Cell. 1990 Mar 9;60(5):861–871. [PubMed]
  • Isberg RR, Voorhis DL, Falkow S. Identification of invasin: a protein that allows enteric bacteria to penetrate cultured mammalian cells. Cell. 1987 Aug 28;50(5):769–778. [PubMed]
  • Izhar M, Nuchamowitz Y, Mirelman D. Adherence of Shigella flexneri to guinea pig intestinal cells is mediated by a mucosal adhesion. Infect Immun. 1982 Mar;35(3):1110–1118. [PMC free article] [PubMed]
  • Jackson MP. Structure-function analyses of Shiga toxin and the Shiga-like toxins. Microb Pathog. 1990 Apr;8(4):235–242. [PubMed]
  • Katakura S, Reinholt FP, Kärnell A, Huan PT, Trach DD, Lindberg AA. The pathology of Shigella flexneri infection in rhesus monkeys: an endoscopic and histopathological study of colonic lesions. APMIS. 1990 Apr;98(4):313–319. [PubMed]
  • Kato J, Ito K, Nakamura A, Watanabe H. Cloning of regions required for contact hemolysis and entry into LLC-MK2 cells from Shigella sonnei form I plasmid: virF is a positive regulator gene for these phenotypes. Infect Immun. 1989 May;57(5):1391–1398. [PMC free article] [PubMed]
  • Keusch GT, Grady GF, Mata LJ, McIver J. The pathogenesis of Shigella diarrhea. I. Enterotoxin production by Shigella dysenteriae I. J Clin Invest. 1972 May;51(5):1212–1218. [PMC free article] [PubMed]
  • Kim R, Corwin LM. Mutation in Shigella flexneri resulting in loss of ability to penetrate HeLa cells and loss of glycerol kinase activity. Infect Immun. 1974 May;9(5):916–923. [PMC free article] [PubMed]
  • Kopecko DJ, Holcombe J, Formal SB. Molecular characterization of plasmids from virulent and spontaneously occurring avirulent colonial variants of Shigella flexneri. Infect Immun. 1979 May;24(2):580–582. [PMC free article] [PubMed]
  • Kopecko DJ, Washington O, Formal SB. Genetic and physical evidence for plasmid control of Shigella sonnei form I cell surface antigen. Infect Immun. 1980 Jul;29(1):207–214. [PMC free article] [PubMed]
  • Koster F, Levin J, Walker L, Tung KS, Gilman RH, Rahaman MM, Majid MA, Islam S, Williams RC., Jr Hemolytic-uremic syndrome after shigellosis. Relation to endotoxemia and circulating immune complexes. N Engl J Med. 1978 Apr 27;298(17):927–933. [PubMed]
  • Kozlov YuV, Kabishev AA, Lukyanov EV, Bayev AA. The primary structure of the operons coding for Shigella dysenteriae toxin and temperature phage H30 shiga-like toxin. Gene. 1988 Jul 30;67(2):213–221. [PubMed]
  • Labrec EH, Schneider H, Magnani TJ, Formal SB. EPITHELIAL CELL PENETRATION AS AN ESSENTIAL STEP IN THE PATHOGENESIS OF BACILLARY DYSENTERY. J Bacteriol. 1964 Nov;88(5):1503–1518. [PMC free article] [PubMed]
  • Lawlor KM, Payne SM. Aerobactin genes in Shigella spp. J Bacteriol. 1984 Oct;160(1):266–272. [PMC free article] [PubMed]
  • Lawlor KM, Daskaleros PA, Robinson RE, Payne SM. Virulence of iron transport mutants of Shigella flexneri and utilization of host iron compounds. Infect Immun. 1987 Mar;55(3):594–599. [PMC free article] [PubMed]
  • Lett MC, Sasakawa C, Okada N, Sakai T, Makino S, Yamada M, Komatsu K, Yoshikawa M. virG, a plasmid-coded virulence gene of Shigella flexneri: identification of the virG protein and determination of the complete coding sequence. J Bacteriol. 1989 Jan;171(1):353–359. [PMC free article] [PubMed]
  • Leong JM, Fournier RS, Isberg RR. Identification of the integrin binding domain of the Yersinia pseudotuberculosis invasin protein. EMBO J. 1990 Jun;9(6):1979–1989. [PMC free article] [PubMed]
  • Leung KY, Reisner BS, Straley SC. YopM inhibits platelet aggregation and is necessary for virulence of Yersinia pestis in mice. Infect Immun. 1990 Oct;58(10):3262–3271. [PMC free article] [PubMed]
  • Leung KY, Straley SC. The yopM gene of Yersinia pestis encodes a released protein having homology with the human platelet surface protein GPIb alpha. J Bacteriol. 1989 Sep;171(9):4623–4632. [PMC free article] [PubMed]
  • Levine MM, DuPont HL, Formal SB, Hornick RB, Takeuchi A, Gangarosa EJ, Snyder MJ, Libonati JP. Pathogenesis of Shigella dysenteriae 1 (Shiga) dysentery. J Infect Dis. 1973 Mar;127(3):261–270. [PubMed]
  • Lindberg AA, Brown JE, Strömberg N, Westling-Ryd M, Schultz JE, Karlsson KA. Identification of the carbohydrate receptor for Shiga toxin produced by Shigella dysenteriae type 1. J Biol Chem. 1987 Feb 5;262(4):1779–1785. [PubMed]
  • Lopez EL, Diaz M, Grinstein S, Devoto S, Mendilaharzu F, Murray BE, Ashkenazi S, Rubeglio E, Woloj M, Vasquez M, et al. Hemolytic uremic syndrome and diarrhea in Argentine children: the role of Shiga-like toxins. J Infect Dis. 1989 Sep;160(3):469–475. [PubMed]
  • LURIA SE, BURROUS JW. Hybridization between Escherichia coli and Shigella. J Bacteriol. 1957 Oct;74(4):461–476. [PMC free article] [PubMed]
  • Makino S, Sasakawa C, Kamata K, Kurata T, Yoshikawa M. A genetic determinant required for continuous reinfection of adjacent cells on large plasmid in S. flexneri 2a. Cell. 1986 Aug 15;46(4):551–555. [PubMed]
  • Makino S, Sasakawa C, Yoshikawa M. Genetic relatedness of the basic replicon of the virulence plasmid in shigellae and enteroinvasive Escherichia coli. Microb Pathog. 1988 Oct;5(4):267–274. [PubMed]
  • Maurelli AT. Regulation of virulence genes in Shigella. Mol Biol Med. 1989 Oct;6(5):425–432. [PubMed]
  • Maurelli AT, Baudry B, d'Hauteville H, Hale TL, Sansonetti PJ. Cloning of plasmid DNA sequences involved in invasion of HeLa cells by Shigella flexneri. Infect Immun. 1985 Jul;49(1):164–171. [PMC free article] [PubMed]
  • Maurelli AT, Sansonetti PJ. Identification of a chromosomal gene controlling temperature-regulated expression of Shigella virulence. Proc Natl Acad Sci U S A. 1988 Apr;85(8):2820–2824. [PMC free article] [PubMed]
  • Mills JA, Buysse JM, Oaks EV. Shigella flexneri invasion plasmid antigens B and C: epitope location and characterization with monoclonal antibodies. Infect Immun. 1988 Nov;56(11):2933–2941. [PMC free article] [PubMed]
  • Moulder JW. Intracellular parasitism: life in an extreme environment. J Infect Dis. 1974 Sep;130(3):300–306. [PubMed]
  • Mounier J, Ryter A, Coquis-Rondon M, Sansonetti PJ. Intracellular and cell-to-cell spread of Listeria monocytogenes involves interaction with F-actin in the enterocytelike cell line Caco-2. Infect Immun. 1990 Apr;58(4):1048–1058. [PMC free article] [PubMed]
  • Nassif X, Mazert MC, Mounier J, Sansonetti PJ. Evaluation with an iuc::Tn10 mutant of the role of aerobactin production in the virulence of Shigella flexneri. Infect Immun. 1987 Sep;55(9):1963–1969. [PMC free article] [PubMed]
  • Neill RJ, Gemski P, Formal SB, Newland JW. Deletion of the Shiga toxin gene in a chlorate-resistant derivative of Shigella dysenteriae type 1 that retains virulence. J Infect Dis. 1988 Oct;158(4):737–741. [PubMed]
  • Newland JW, Neill RJ. DNA probes for Shiga-like toxins I and II and for toxin-converting bacteriophages. J Clin Microbiol. 1988 Jul;26(7):1292–1297. [PMC free article] [PubMed]
  • Oaks EV, Hale TL, Formal SB. Serum immune response to Shigella protein antigens in rhesus monkeys and humans infected with Shigella spp. Infect Immun. 1986 Jul;53(1):57–63. [PMC free article] [PubMed]
  • Oaks EV, Wingfield ME, Formal SB. Plaque formation by virulent Shigella flexneri. Infect Immun. 1985 Apr;48(1):124–129. [PMC free article] [PubMed]
  • O'Brien AD, LaVeck GD, Thompson MR, Formal SB. Production of Shigella dysenteriae type 1-like cytotoxin by Escherichia coli. J Infect Dis. 1982 Dec;146(6):763–769. [PubMed]
  • Obrig TG, Del Vecchio PJ, Brown JE, Moran TP, Rowland BM, Judge TK, Rothman SW. Direct cytotoxic action of Shiga toxin on human vascular endothelial cells. Infect Immun. 1988 Sep;56(9):2373–2378. [PMC free article] [PubMed]
  • Ogawa H, Nakamura A, Nakaya R. Cinemicrographic study of tissue cell cultures infected with Shigella flexneri. Jpn J Med Sci Biol. 1968 Aug;21(4):259–273. [PubMed]
  • Okada N, Sasakawa C, Tobe T, Yamada M, Nagai S, Talukder KA, Komatsu K, Kanegasaki S, Yoshikawa M. Virulence-associated chromosomal loci of Shigella flexneri identified by random Tn5 insertion mutagenesis. Mol Microbiol. 1991 Jan;5(1):187–195. [PubMed]
  • Okamura N, Nagai T, Nakaya R, Kondo S, Murakami M, Hisatsune K. HeLa cell invasiveness and O antigen of Shigella flexneri as separate and prerequisite attributes of virulence to evoke keratoconjunctivitis in guinea pigs. Infect Immun. 1983 Feb;39(2):505–513. [PMC free article] [PubMed]
  • Pál T, Hale TL. Plasmid-associated adherence of Shigella flexneri in a HeLa cell model. Infect Immun. 1989 Aug;57(8):2580–2582. [PMC free article] [PubMed]
  • Pál T, Newland JW, Tall BD, Formal SB, Hale TL. Intracellular spread of Shigella flexneri associated with the kcpA locus and a 140-kilodalton protein. Infect Immun. 1989 Feb;57(2):477–486. [PMC free article] [PubMed]
  • Payne SM. Iron and virulence in Shigella. Mol Microbiol. 1989 Sep;3(9):1301–1306. [PubMed]
  • Prado D, Cleary TG, Pickering LK, Ericsson CD, Bartlett AV, 3rd, DuPont HL, Johnson PC. The relation between production of cytotoxin and clinical features in shigellosis. J Infect Dis. 1986 Jul;154(1):149–155. [PubMed]
  • Ried G, Hindennach I, Henning U. Role of lipopolysaccharide in assembly of Escherichia coli outer membrane proteins OmpA, OmpC, and OmpF. J Bacteriol. 1990 Oct;172(10):6048–6053. [PMC free article] [PubMed]
  • Rohde JE. Selective primary health care: strategies for control of disease in the developing world. XV. Acute diarrhea. Rev Infect Dis. 1984 Nov-Dec;6(6):840–854. [PubMed]
  • Rout WR, Formal SB, Giannella RA, Dammin GJ. Pathophysiology of Shigella diarrhea in the rhesus monkey: intestinal transport, morphological, and bacteriological studies. Gastroenterology. 1975 Feb;68(2):270–278. [PubMed]
  • Sakai T, Sasakawa C, Makino S, Kamata K, Yoshikawa M. Molecular cloning of a genetic determinant for Congo red binding ability which is essential for the virulence of Shigella flexneri. Infect Immun. 1986 Feb;51(2):476–482. [PMC free article] [PubMed]
  • Sakai T, Sasakawa C, Makino S, Yoshikawa M. DNA sequence and product analysis of the virF locus responsible for congo red binding and cell invasion in Shigella flexneri 2a. Infect Immun. 1986 Nov;54(2):395–402. [PMC free article] [PubMed]
  • Sakai T, Sasakawa C, Yoshikawa M. Expression of four virulence antigens of Shigella flexneri is positively regulated at the transcriptional level by the 30 kiloDalton virF protein. Mol Microbiol. 1988 Sep;2(5):589–597. [PubMed]
  • Sankaran K, Ramachandran V, Subrahmanyam YV, Rajarathnam S, Elango S, Roy RK. Congo red-mediated regulation of levels of Shigella flexneri 2a membrane proteins. Infect Immun. 1989 Aug;57(8):2364–2371. [PMC free article] [PubMed]
  • Sansonetti PJ, d'Hauteville H, Ecobichon C, Pourcel C. Molecular comparison of virulence plasmids in Shigella and enteroinvasive Escherichia coli. Ann Microbiol (Paris) 1983 May-Jun;134A(3):295–318. [PubMed]
  • Sansonetti PJ, Hale TL, Dammin GJ, Kapfer C, Collins HH, Jr, Formal SB. Alterations in the pathogenicity of Escherichia coli K-12 after transfer of plasmid and chromosomal genes from Shigella flexneri. Infect Immun. 1983 Mar;39(3):1392–1402. [PMC free article] [PubMed]
  • Sansonetti PJ, Kopecko DJ, Formal SB. Shigella sonnei plasmids: evidence that a large plasmid is necessary for virulence. Infect Immun. 1981 Oct;34(1):75–83. [PMC free article] [PubMed]
  • Sansonetti PJ, Kopecko DJ, Formal SB. Involvement of a plasmid in the invasive ability of Shigella flexneri. Infect Immun. 1982 Mar;35(3):852–860. [PMC free article] [PubMed]
  • Sansonetti PJ, Mounier J. Metabolic events mediating early killing of host cells infected by Shigella flexneri. Microb Pathog. 1987 Jul;3(1):53–61. [PubMed]
  • Sansonetti PJ, Ryter A, Clerc P, Maurelli AT, Mounier J. Multiplication of Shigella flexneri within HeLa cells: lysis of the phagocytic vacuole and plasmid-mediated contact hemolysis. Infect Immun. 1986 Feb;51(2):461–469. [PMC free article] [PubMed]
  • Sasakawa C, Adler B, Tobe T, Okada N, Nagai S, Komatsu K, Yoshikawa M. Functional organization and nucleotide sequence of virulence Region-2 on the large virulence plasmid in Shigella flexneri 2a. Mol Microbiol. 1989 Sep;3(9):1191–1201. [PubMed]
  • 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. 1988 Jun;170(6):2480–2484. [PMC free article] [PubMed]
  • Sasakawa C, Kamata K, Sakai T, Murayama SY, Makino S, Yoshikawa M. Molecular alteration of the 140-megadalton plasmid associated with loss of virulence and Congo red binding activity in Shigella flexneri. Infect Immun. 1986 Feb;51(2):470–475. [PMC free article] [PubMed]
  • Sasakawa C, Makino S, Kamata K, Yoshikawa M. Isolation, characterization, and mapping of Tn5 insertions into the 140-megadalton invasion plasmid defective in the mouse Sereny test in Shigella flexneri 2a. Infect Immun. 1986 Oct;54(1):32–36. [PMC free article] [PubMed]
  • Schmitt MP, Payne SM. Genetics and regulation of enterobactin genes in Shigella flexneri. J Bacteriol. 1988 Dec;170(12):5579–5587. [PMC free article] [PubMed]
  • Sekizaki T, Harayama S, Brazil GM, Timmis KN. Localization of stx, a determinant essential for high-level production of shiga toxin by Shigella dysenteriae serotype 1, near pyrF and generation of stx transposon mutants. Infect Immun. 1987 Sep;55(9):2208–2214. [PMC free article] [PubMed]
  • Seltmann G, Pál T, Tschäpe H. Surface hydrophobicity of plasmid-carrying virulent Shigella flexneri and their avirulent variants. J Basic Microbiol. 1986;26(5):283–287. [PubMed]
  • Sharon P, Ligumsky M, Rachmilewitz D, Zor U. Role of prostaglandins in ulcerative colitis. Enhanced production during active disease and inhibition by sulfasalazine. Gastroenterology. 1978 Oct;75(4):638–640. [PubMed]
  • Silva RM, Saadi S, Maas WK. A basic replicon of virulence-associated plasmids of Shigella spp. and enteroinvasive Escherichia coli is homologous with a basic replicon in plasmids of IncF groups. Infect Immun. 1988 Apr;56(4):836–842. [PMC free article] [PubMed]
  • Simmons DA. Immunochemistry of Shigella flexneri O-antigens: a study of structural and genetic aspects of the biosynthesis of cell-surface antigens. Bacteriol Rev. 1971 Jun;35(2):117–148. [PMC free article] [PubMed]
  • Simmons DA, Romanowska E. Structure and biology of Shigella flexneri O antigens. J Med Microbiol. 1987 Jun;23(4):289–302. [PubMed]
  • Speelman P, Kabir I, Islam M. Distribution and spread of colonic lesions in shigellosis: a colonoscopic study. J Infect Dis. 1984 Dec;150(6):899–903. [PubMed]
  • Stieglitz H, Fosmire S, Lipsky P. Identification of a 2-Md plasmid from Shigella flexneri associated with reactive arthritis. Arthritis Rheum. 1989 Aug;32(8):937–946. [PubMed]
  • Stoll BJ, Glass RI, Huq MI, Khan MU, Banu H, Holt J. Epidemiologic and clinical features of patients infected with Shigella who attended a diarrheal disease hospital in Bangladesh. J Infect Dis. 1982 Aug;146(2):177–183. [PubMed]
  • Strockbine NA, Jackson MP, Sung LM, Holmes RK, O'Brien AD. Cloning and sequencing of the genes for Shiga toxin from Shigella dysenteriae type 1. J Bacteriol. 1988 Mar;170(3):1116–1122. [PMC free article] [PubMed]
  • Stugard CE, Daskaleros PA, Payne SM. A 101-kilodalton heme-binding protein associated with congo red binding and virulence of Shigella flexneri and enteroinvasive Escherichia coli strains. Infect Immun. 1989 Nov;57(11):3534–3539. [PMC free article] [PubMed]
  • Takeuchi A, Formal SB, Sprinz H. Exerimental acute colitis in the Rhesus monkey following peroral infection with Shigella flexneri. An electron microscope study. Am J Pathol. 1968 Mar;52(3):503–529. [PMC free article] [PubMed]
  • Tilney LG, Portnoy DA. Actin filaments and the growth, movement, and spread of the intracellular bacterial parasite, Listeria monocytogenes. J Cell Biol. 1989 Oct;109(4 Pt 1):1597–1608. [PMC free article] [PubMed]
  • Timakov VD, Petrovskaya VG, Bondarenko VM. Studies on the genetic control of shigella sub-group B type specific antigens. I. Behaviour of Shigella flexneri type specific antigens in sexual recombination of Shigella x E. coli. Ann Inst Pasteur (Paris) 1970 Jan;118(1):3–9. [PubMed]
  • Tobias PS, Soldau K, Ulevitch RJ. Identification of a lipid A binding site in the acute phase reactant lipopolysaccharide binding protein. J Biol Chem. 1989 Jun 25;264(18):10867–10871. [PubMed]
  • Venkatesan MM, Buysse JM. Nucleotide sequence of invasion plasmid antigen gene ipaA from Shigella flexneri 5. Nucleic Acids Res. 1990 Mar 25;18(6):1648–1648. [PMC free article] [PubMed]
  • Venkatesan MM, Buysse JM, Kopecko DJ. Characterization of invasion plasmid antigen genes (ipaBCD) from Shigella flexneri. Proc Natl Acad Sci U S A. 1988 Dec;85(23):9317–9321. [PMC free article] [PubMed]
  • Venkatesan MM, Buysse JM, Kopecko DJ. Use of Shigella flexneri ipaC and ipaH gene sequences for the general identification of Shigella spp. and enteroinvasive Escherichia coli. J Clin Microbiol. 1989 Dec;27(12):2687–2691. [PMC free article] [PubMed]
  • Venkatesan M, Buysse JM, Vandendries E, Kopecko DJ. Development and testing of invasion-associated DNA probes for detection of Shigella spp. and enteroinvasive Escherichia coli. J Clin Microbiol. 1988 Feb;26(2):261–266. [PMC free article] [PubMed]
  • Wassef JS, Keren DF, Mailloux JL. Role of M cells in initial antigen uptake and in ulcer formation in the rabbit intestinal loop model of shigellosis. Infect Immun. 1989 Mar;57(3):858–863. [PMC free article] [PubMed]
  • Watanabe H. Genetics of virulence of Shigella species. Microbiol Sci. 1988 Oct;5(10):307–310. [PubMed]
  • Watanabe H, Arakawa E, Ito K, Kato J, Nakamura A. Genetic analysis of an invasion region by use of a Tn3-lac transposon and identification of a second positive regulator gene, invE, for cell invasion of Shigella sonnei: significant homology of invE with ParB of plasmid P1. J Bacteriol. 1990 Feb;172(2):619–629. [PMC free article] [PubMed]
  • Watanabe H, Nakamura A. Large plasmids associated with virulence in Shigella species have a common function necessary for epithelial cell penetration. Infect Immun. 1985 Apr;48(1):260–262. [PMC free article] [PubMed]
  • Watanabe H, Nakamura A. Identification of Shigella sonnei form I plasmid genes necessary for cell invasion and their conservation among Shigella species and enteroinvasive Escherichia coli. Infect Immun. 1986 Aug;53(2):352–358. [PMC free article] [PubMed]
  • Watanabe H, Nakamura A, Timmis KN. Small virulence plasmid of Shigella dysenteriae 1 strain W30864 encodes a 41,000-dalton protein involved in formation of specific lipopolysaccharide side chains of serotype 1 isolates. Infect Immun. 1984 Oct;46(1):55–63. [PMC free article] [PubMed]
  • Watanabe H, Timmis KN. A small plasmid in Shigella dysenteriae 1 specifies one or more functions essential for O antigen production and bacterial virulence. Infect Immun. 1984 Jan;43(1):391–396. [PMC free article] [PubMed]
  • WATKINS HM. Some attributes of virulence in Shigella. Ann N Y Acad Sci. 1960 Nov 21;88:1167–1186. [PubMed]
  • Wharton M, Spiegel RA, Horan JM, Tauxe RV, Wells JG, Barg N, Herndon J, Meriwether RA, MacCormack JN, Levine RH. A large outbreak of antibiotic-resistant shigellosis at a mass gathering. J Infect Dis. 1990 Dec;162(6):1324–1328. [PubMed]
  • Williams KM, Raybourne RB. Demonstration of cross-reactivity between bacterial antigens and class I human leukocyte antigens by using monoclonal antibodies to Shigella flexneri. Infect Immun. 1990 Jun;58(6):1774–1781. [PMC free article] [PubMed]
  • Yamada M, Sasakawa C, Okada N, Makino SI, Yoshikawa M. Molecular cloning and characterization of chromosomal virulence region kcpA of Shigella flexneri. Mol Microbiol. 1989 Feb;3(2):207–213. [PubMed]
  • Yoshikawa M, Sasakawa C, Makino S, Okada N, Lett MC, Sakai T, Yamada M, Komatsu K, Kamata K, Kurata T, et al. Molecular genetic approaches to the pathogenesis of bacillary dysentery. Microbiol Sci. 1988 Nov;5(11):333–339. [PubMed]

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