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Environmental Regulation of Shigella Virulence

  • Chapter
Pathogenesis of Shigellosis

Part of the book series: Current Topics in Microbiology and Immunology ((CT MICROBIOLOGY,volume 180))

Abstract

Bacterial pathogens frequently find themselves exposed to a variety of diverse, frequently hostile conditions during their infectious cycle. The journey from the external environment to the host, where the bacteria may ultimately cause disease, is an adventurous one and involves exposure of the organism to a multitude of growth conditions. Successful pathogens have evolved the means for survival within the varied growth conditions encountered both inside and outside their respective hosts. The ability to synthesize proteins which facilitate survival under different growth conditions is part of an organism’s adaptive response. The adaptive response also involves mechanisms for sensing environmental changes and, in turn, regulating gene expression. Many examples exist of nonpathogenic bacteria which regulate genes in response to changes in their surroundings. Nutrient limitation, a shift in growth from one carbon source to another, a change from aerobic to anaerobic growth conditions, and changes in osmolarity and temperature are all signals to which bacteria respond by altering gene expression (reviewed by Gottesman 1984; Stock et al. 1989).

The opinion or assertions of A.T.M. and A.E.H. contained herein are the private ones of the authors and or not be construed as official or reflecting the views of te Department of Defense or the Uniformed Services University of Health Sciences

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References

  • Abeles AL, Freidman SA, Austin SJ (1985) Partition of unit-copy miniplasmids to daughter cells. III. The DNA sequence and functional organization of the P1 partition region. J Mol Biol 185: 261–272

    Article  Google Scholar 

  • Adler B, Sasakawa C, Tobe T, Makino S, Komatsu K, Yoshikawa M (1989) A dual transcriptional activation system for the 230 kb plasmid genes coding for virulence-associated antigens of Shigella flexneri. Mol Microbiol 3: 627–635

    Article  PubMed  CAS  Google Scholar 

  • Aliabadi Z, Park YK, Slonczewski JL, Foster JW (1988) Novel regulatory loci controlling oxygen- and pH-regulated gene expression in Salmonella typhimurium. J Bacteriol 170: 842–851

    PubMed  CAS  Google Scholar 

  • Andrews GP, Hromockyj AE, Coker C, Maurelli AT (1991) Two novel virulence loci, mxiA and mxiB, in Shigella flexneri 2a facilitate excretion of invasion plasmid antigens. Infect Immun 59: 1997–2005

    PubMed  CAS  Google Scholar 

  • Arico B, Miller FJ, Craig R, Stibitz S, Monack D, Falkow S, Gross R, Rappuoli R (1989) Sequences required for expression of Bordetella pertussis virulence factor share homology with prokaryotic signal transduction proteins. Proc Natl Acäd Sei USA 86: 6671–6675

    Article  CAS  Google Scholar 

  • Baudry B, Kaczorek M, Sansonetti PJ (1988) Nucleotide sequence of the invasion plasmid antigen B and C genes (ipaB andipaC). Microb Pathog 4: 345–357

    Article  PubMed  CAS  Google Scholar 

  • Bernardini ML, Fontaine A, Sansonetti PJ (1990) The two-component regulatory system OmpR-EnvZ controls the virulence of Shigella flexneri. J Bacteriol 172: 6274–6281

    PubMed  CAS  Google Scholar 

  • Bernardini ML, Mounier J, d’Hauteville H, Coquis-Rondon M, Sansonetti PJ (1989) 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: 3867–3871

    Article  PubMed  CAS  Google Scholar 

  • Braun G, Cole ST (1982) The nucleotide sequence coding for major outer membrane protein OmpA of Shigella dysenteriae. Nucleic Acids Res 10: 2367–2378

    Article  PubMed  CAS  Google Scholar 

  • Brenner DJ, Fanning GR, Sherman FJ, Falkow S (1972) Polynucleotide divergence among strains of Escherichia coli and closely related organisms. J Bacteriol 109: 953–965

    PubMed  CAS  Google Scholar 

  • Buysse JM, Venkatesan M, Mills JA, Oaks EV (1990) Molecular characterization of a trans-acting, positive effector (ipaR) of invasion plasmid antigen synthesis in Shigella flexneri serotype 5. Microb Pathog 8: 197–211

    Article  PubMed  CAS  Google Scholar 

  • Comeau DEK, Ikenaka K, Tsung K, Inouye M (1985) Primary characterization of the protein products of the Escherichia coli ompB locus: structure and regulation of synthesis of the OmpR and EnvZ proteins. J Bacteriol 164: 578–584

    PubMed  CAS  Google Scholar 

  • Cossart P, Groisman EA, Serre M, Casadaban MJ, Gicquel-Sanzey B (1986) crp genes of Shigella flexneri, Salmonella typhimurium, and Escherichia coli. J Bacteriol 167: 639–646

    PubMed  CAS  Google Scholar 

  • Csonka LN (1989) Physiological and genetic responses of bacteria to osmotic stress. Microbiol Rev 56: 121–147

    Google Scholar 

  • Daskaleros PA, Payne SM (1987) Congo red binding phenotype is associated with hemin binding and increased infectivity of Shigella flexneri in the HeLa cell model. Infect Immun 55: 1393–1398

    PubMed  CAS  Google Scholar 

  • Deretic V, Dikshit R, Konyescni WM, Chakrabarty AM, Misra TK (1989) The algR gene, which regulates mucoidy in Pseudomonas aeruginosa, belongs to a class of environmentally responsive genes. J Bacteriol 171: 1278–1283

    PubMed  CAS  Google Scholar 

  • DiRita JV, Mekalanos JJ (1989) Genetic regulation of bacterial virulence. Annu Rev Genet 23: 455–482

    Article  PubMed  CAS  Google Scholar 

  • Dorman CJ, NiBhriain N, Higgins CF (1990) DNA supercoiling and environmental regulation of virulence gene expression in Shigella flexneri. Nature 344: 789–792

    Article  PubMed  CAS  Google Scholar 

  • Drlica K, Rouviere-Yaniv J (1987) Histone like proteins of bacteria. Microbiol Rev 51: 301–319

    PubMed  CAS  Google Scholar 

  • DuPont HL, Levine MM, Hornick RB, Formal SB (1989) Inoculum size in shigellosis and implications for expected mode of transmission. J Infect Dis 159: 1126–1128

    Article  PubMed  CAS  Google Scholar 

  • Ernst RK, Dombroski DM, Merrick JM (1990) Anaerobiosis, type 1 fimbriae, and growth phase are factors that affect invasion of HEp-2 cells by Salmonella typhimurium. Infect Immun 58: 2014–2016

    PubMed  CAS  Google Scholar 

  • Falconi M, Gualtieri MT, LaTeana A, Lasso MA, Pon CL (1988) Proteins from the prokaryotic nucleoid: primary and quaternary structure of the 15 kDEscherichia coli DNA binding protein H-NS. Mol Microbiol 2: 323–329

    Article  PubMed  CAS  Google Scholar 

  • Formal SB, Gemski P Jr, Baron LS, LaBrec EH (1971) A chromosomal locus which controls the ability of Shigella flexneri to evoke keratoconjunctivitis. Infect Immun 3: 73–79

    PubMed  CAS  Google Scholar 

  • Forst S, Comeau D, Shigemi D, Inouye M (1987) Localization and membrane topology of EnvZ, a protein involved in osmoregulation of OmpF and OmpC inEscherichia coli. J Biol Chem 262: 16433–16438

    PubMed  CAS  Google Scholar 

  • Forst S, Delgado J, Inouye M (1989) Phosphorylation of OmpR by the osmosensor EnvZ modulates expression of the ompF andompC genes in Escherichia coli. Proc Natl Acad Sci USA 86: 6052–6056

    Article  PubMed  CAS  Google Scholar 

  • Friedrich K, Gualerzi CO, Lammi M, Pon CL (1988) Proteins from the prokaryotic nucleoid: interaction of nucleic acids with the 15 kDa Escherichia coli histone-like protein H-NS. FEBS Lett 229: 197–202

    Article  PubMed  CAS  Google Scholar 

  • Galan JE, Curtiss R III (1990) Expression of Salmonella typhimurium genes required for invasion is regulated by changes in DNA supercoiling. Infect Immun 58: 1879–1885

    PubMed  CAS  Google Scholar 

  • Goodman HM, Abelson J, Landy A, Brenner S, Smith JD (1968) Amber suppression: a nucleotide change in the anticodon of a tyrosine transfer RNA. Nature 217:1019–1024

    Article  PubMed  CAS  Google Scholar 

  • Göransson M, Uhlin BE (1984) Environmental temperature regulates transcription of a virulence pili operon in E. coli. EMBO J 3: 2885–2888

    PubMed  Google Scholar 

  • Göransson M, Sonden B, Nilsson P, Dagberg B, Forsman K, Emanuelson K, Uhlin BE (1990) Transcriptional silencing and thermoregulation of gene expression in Escherichia coli. Nature 344: 682–685

    Article  PubMed  Google Scholar 

  • Görden J, Small P (1990) Quantitative analysis of the effects of variable pH on the growth of Shigella flexneri, Salmonella typhimurium, and enteroinvasive Escherichia coli. Abstracts of the 90th annual meeting of the American Society for Microbiology, Washington, p 64

    Google Scholar 

  • Gottesman S (1984) Bacterial regulation: global regulatory networks. Annu Rev Genet 18: 415–441

    Article  PubMed  CAS  Google Scholar 

  • Gualerzi CO, Losso MA, Lammi M, Friedrich K, Pawlik RT, Canonaco MA, Gianfranceschi G, Pingoud A, Pon CJ (1986) Proteins from the prokaryotic nucleoid. Structural and function characterization of the Escherichia coli DNA-binding proteins NS (HU) and H-NS. In: Gualerzi CO, Pon CL (eds) Bacterial chromatin. Springer, Berlin Heidelberg New York, pp 101–134

    Chapter  Google Scholar 

  • Hancock REW (1987) Role of porins in other membrane permeability. J Bacteriol 163: 929–933

    Google Scholar 

  • Headley VL, Payne SM (1990) Differential protein expression by Shigella flexneri in intracellular and extracellular environments. Proc Natl Acad Sci USA 87: 4179–4183

    Article  PubMed  CAS  Google Scholar 

  • Higgins CF, Dorman CJ, NiBhriain N (1990) Environmental influences on DNA supercoiling: a novel mechanism for the regulation of gene expression. In: Drlica K, Riley M (eds) The bacterial chromosome. American Society for Microbiology, Washington, D.C., pp 421–434

    Google Scholar 

  • Hromockyj AE, Maurelli AT (1989a) Identification of Shigella invasion genes by isolation of temperature-regulatedinv:: lacZ operon fusions. Infect Immun 57: 2963–2970

    PubMed  CAS  Google Scholar 

  • Hromockyj AE, Maurelli AT (1989b) Identification of an Escherichia coli gene homologous to virR, a regulator of Shigella virulence. J Bacteriol 171: 2879–2881

    PubMed  CAS  Google Scholar 

  • Hulton CSJ, Seirafi A, Hinton JCD, Sidebotham JM, Waddell L, Pavitt GD, Owen-Hughes T, Spassky A, Buc H, Higgins CF (1990) Histone-like protein HI (H-NS), DNA supercoiling, and gene expression in bacteria. Cell 63: 631–642

    Article  PubMed  CAS  Google Scholar 

  • Jones PG, VanBogelen RA, Neidhardt FC (1987) Induction of proteins in response to low temperature in Escherichia coli. J Bacteriol 169: 2092–2095

    PubMed  CAS  Google Scholar 

  • Kato J-I, Ito K-I, Nakamura A, Watanabe H (1989) 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 57:1391–1398

    PubMed  CAS  Google Scholar 

  • Kawula T, Orndorff P (1991) Rapid site specific DNA inversion in Escherichia coli mutants lacking the histone-like protein H-NS. J Bacteriol 173: 4116–4123

    PubMed  CAS  Google Scholar 

  • LaTeana A, Falconi M, Scarlato V, Lammi M, Pon CL (1989) Characterization of the structural genes for the DNA-binding protein H-NS in Enterobacteriaceae. FEBS Lett 244: 34–38

    Article  CAS  Google Scholar 

  • Lee CA, Falkow S (1990) The ability of Salmonella to enter mammalian cells is affected by bacterial growth state. Proc Natl Acad Sci USA 87: 4304–4308

    Article  PubMed  CAS  Google Scholar 

  • Leroux B, Yanofsky MF, Winas SC, Ward JE, Ziegler SF, Nester EW (1987) Characterization of the virA locus of Agrobacterium tumefaciens: a transcriptional regulator and host range determinant. EMBO J 6: 849–856

    PubMed  CAS  Google Scholar 

  • Lugtenberg B, Peters R, Bernheimer M, Berendson W (1976) Influence of cultural conditions and mutations on the composition of the outer membrane proteins of Escherichia coli. Mol Gen Genet 147:251–262

    Article  PubMed  CAS  Google Scholar 

  • Makino S, Sasakawa C, Kamata K, Kurata T, Yoshikawa M (1986) A genetic determinant required for continuous reinfection of adjacent cells on large plasmid in S. flexneri2a. Cell 46: 551–555

    Article  PubMed  CAS  Google Scholar 

  • Marsh M, Hillyard DR (1990) Nucleotide sequence of hns encoding the DNA-binding protein H-NS of Salmonella typhimurium. Nucleic Acids Res 18: 3397

    Article  PubMed  CAS  Google Scholar 

  • Maurelli AT (1989a) Regulation of virulence genes in Shigella. Mol Biol Med 6: 425–432

    PubMed  CAS  Google Scholar 

  • Maurelli AT (1989b) Temperature regulation of virulence genes in pathogenic bacteria: a global strategy for human pathogens. Microb Pathog 7:1–10

    Article  PubMed  CAS  Google Scholar 

  • Maurelli AT, Curtiss R III (1984) Bacteriophage Mudl (Apr lac) generates vir-lac operon fusions inShigella flexneri 2a. Infect Immun 45: 642–648

    PubMed  CAS  Google Scholar 

  • Maurelli AT, Sansonetti PJ (1988) Identification of a chromosomal gene controlling temperature-regulated expression ofShigella virulence. Proc Natl Acad Sei USA 85: 2820–2824

    Article  PubMed  CAS  Google Scholar 

  • Maurelli AT, Blackmon B, Curtiss R III (1984a) Temperature-dependent expression of virulence genes in Shigella species. Infect Immun 43: 195–201

    PubMed  CAS  Google Scholar 

  • Maurelli AT, Blackmon B, Curtiss R III (1984b) Loss of pigmentation in Shigella flexneri 2a is correlated with loss of virulence and virulence-associated plasmid. Infect Immun 43: 397–401

    PubMed  CAS  Google Scholar 

  • May G, Dersch P, Haardt M, Middendorf A, Bremer E (1990) The osmZ (bglY) gene encodes the DNA-binding protein H-NS (Hla), a component of the Escherichia coli K12 nucleoid. Mol Gen Genet 224: 81–90

    Article  PubMed  CAS  Google Scholar 

  • Miller JF, Mekalanos JJ, Falkow S (1989) Coordinate regulation and sensory transduction in the control of bacterial virulence. Science 243: 916–922

    Article  PubMed  CAS  Google Scholar 

  • Miller SI, Kukral AM, Mekalanos JJ (1989) A two-component regulatory system (phoP-phoQ) controls Salmonella typhimurium virulence. Proc Natl Acad Sci USA 86: 5054–5058

    Article  PubMed  CAS  Google Scholar 

  • Mori H, Kondo A, Oshima T, Hiraga S (1986) Structure and function of the F plasmid genes essential for partitioning. J Mol Biol 192:1–15

    Article  PubMed  CAS  Google Scholar 

  • Neidhardt FC, VanBogelen RA (1987) Heat shock response. In: Neidhardt FC (ed)Escherichia coli and Salmonella typhimurium cellular and molecular biology. American Society for Microbiology, Washington, D C, pp 1334–1345

    Google Scholar 

  • Nikaido H, Vaara M (1985) Molecular basis of bacterial outer membrane permeability. Microbiol Rev 49: 1–32

    PubMed  CAS  Google Scholar 

  • Norioka S, Ramakrishnan R, Ikenaka K, Inouye M (1986) Interaction of a transcriptional activator, OmpR, with reciprocally osmoregulated genes ompF and ompC ofEscherichia coli. J Biol Chem 257: 13692–13698

    Google Scholar 

  • Ochman H. Whittam TS, Caugant DA, Seiander RK (1983) Enzyme polymorphism and genetic population structure in Escherichia coli andShigella. J Gen Microbiol 129: 2715–2726

    PubMed  CAS  Google Scholar 

  • Pal T, Newland JW, Tall BD, Formal SB, Hale TL (1989) Intracellular spread of Shigella flexneri associated with the kcpA locus and a 140-kilodalton protein. Infect Immun 57: 477–486

    PubMed  CAS  Google Scholar 

  • Payne SM, Finkelstein RA (1977) Detection and differentiation of iron-responsive avirulent mutants on Congo red agar. Infect Immun 18: 94–98

    PubMed  CAS  Google Scholar 

  • Pon CL, Calogero RA, Gualerzi CO (1988) Identification, cloning, nucleotide sequence and chromosomal map location of hns, the structural gene for Escherichia coli DNA-binding protein H-NS. Mol Gen Genet 212: 199–202

    Article  PubMed  CAS  Google Scholar 

  • Ronson CW, Nixon BT, Ausubel FM (1987) Conserved domains in bacterial regulatory proteins that respond to environmental stimuli. Cell 49: 579–581

    Article  PubMed  CAS  Google Scholar 

  • Sakai T, Sasakawa C, Makino C, Kamata K, Yoshikawa M (1986a) Molecular cloning of a genetic determinant for Congo red binding ability which is essential for the virulence of Shigella flexneri. Infect Immun 51: 476–482

    PubMed  CAS  Google Scholar 

  • Sakai T, Sasakawa C, Makino C, Yoshikawa M (1986b) DNA sequence and product analysis of the virF locus responsible for Congo red binding and cell invasion in S. flexneri 2a. Infect Immun 54: 395–402

    PubMed  CAS  Google Scholar 

  • Sakai T, Sasakawa C, Yoshikawa M (1988) Expression of four virulence antigens of Shigella flexneri is positively regulated at the transcriptional level by the 30 kilodalton virF protein. Mol Microbiol 2: 589–597

    Article  PubMed  CAS  Google Scholar 

  • Sankaran K, Ramachandran V, Subrahmanyam YVBK, Rajarathnam S, Elango S, Roy RK (1989) Congo red-mediated regulation of levels of Shigella flexneri2a membrane proteins. Infect Immun 57: 2364–2371

    PubMed  CAS  Google Scholar 

  • Sansonetti PJ, Hale TL, Dammin GJ, Kapfer C, Collins HH Jr, Formal SB (1983) Alterations in the pathogenicity of Escherichia coli K-12 after transfer of plasmid and chromosomal genes from Shigella flexneri. Infect Immun 39: 1392–1402

    PubMed  CAS  Google Scholar 

  • Sasakawa C, Makino S, Kamata K, Yoshikawa M (1986) Isolation, characterization, and mapping of Tn5 insertions in the 140 megadalton invasion plasmid defective in the mouse Sereny test in Shigella flexneri 2a. Infect Immun 54: 32–36116

    PubMed  CAS  Google Scholar 

  • Schiemann DA, Shope SR (1991) Anaerobic growth of Salmonella typhimurium results in increased uptake by Henle 407 epithelial and mouse peritoneal cells in vitro and repression of a major outer membrane protein. Infect immun 59: 437–440

    PubMed  CAS  Google Scholar 

  • Sekiya T, Gait MJ, Noris K, Ramamoorthy B, Khorana HG (1976) The nucleotide sequence in the promoter region of the gene for an Escherichia coli tyrosine transfer ribonucleic acid. J Biol Chem 251:5124–5140

    CAS  Google Scholar 

  • Slonczewski JL, Gonzalez TN, Bartholomew FM, Holt NJ (1987) Mu d-directed lacZ fusions regulated by low pH inEscherichia coli. J Bacterid 169: 3001–3006

    CAS  Google Scholar 

  • Spassky A, Buc HD (1977) Physio-chemical properties of a DNA binding protein: Escherichia coli factor Hv Eur J Biochem 81: 79–90

    Article  PubMed  CAS  Google Scholar 

  • Spassky A, Timsky S, Garreau H, Buc H (1984) Hla, an E. coli DNA-binding protein which accumulates in stationary phase, strongly compacts DNA in vitro. Nucleic Acids Res 12: 5321–5340

    Article  PubMed  CAS  Google Scholar 

  • Straley SC, Bowmer WS (1986) Virulence genes regulated at the transcriptional level by Ca2+ in Yersinia pestis include structural genes for outer membrane proteins. Infect Immun 51: 445–454

    PubMed  CAS  Google Scholar 

  • Stock JB, Ninfa AJ, Stock A (1989) Protein phosphorylation and regulation of adaptive responses in bacteria. Microbiol Rev 53: 450–490

    PubMed  CAS  Google Scholar 

  • Stugard CE, Daskaleros PA, Payne SM (1989) A 101-kilodalton heme-binding protein associated with Congo red binding virulence of Shigella flexneri and enteroinvasive Escherichia coli strains. Infect Immun 57: 3534–3539

    PubMed  CAS  Google Scholar 

  • Tobe T, Nagai S, Okada N, Adler B, Yoshikawa M, Sasakawa C (1991) Temperature-regulated expression of invasion genes in Shigella flexneri is controlled through the transcriptional activation of the virB gene on the large plasmid. Mol Microbiol 5: 887–893

    Article  PubMed  CAS  Google Scholar 

  • VanBogelen RA, Neidhardt FC (1990) Ribosomes as sensors of heat and cold shock in Escherichia coli. Proc Natl Acad Sei USA 87: 5589–5593

    Article  Google Scholar 

  • VanBogelen RA, Hutton ME, Neidhardt FC (1990) Gene-protein database of Escherichia coli K-12: edition 3. Electrophoresis 11:1131–1166

    Article  Google Scholar 

  • Watanabe H, Arakawa E, Ito K-l, Kato J-l, Nakamura A (1990) 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 172: 619–629

    PubMed  CAS  Google Scholar 

  • Yamada M, Sasakawa C, Okada N, Makino S-l, Yoshikawa M (1989) Molecular cloning and characterization of chromosomal virulence region kcpA ofShigella flexneri, Mol Microbiol 3: 207–213

    Article  PubMed  CAS  Google Scholar 

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Maurelli, A.T., Hromockyj, A.E., Bernardini, M.L. (1992). Environmental Regulation of Shigella Virulence. In: Sansonetti, P.J. (eds) Pathogenesis of Shigellosis. Current Topics in Microbiology and Immunology, vol 180. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-77238-2_5

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