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PMID: 10084987 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

The alternative sigma factor, sigmaE, is critically important for the virulence of Salmonella typhimurium.

Infection and immunity ·Vol. 67 ·No. 4 ·1999-04-00 ·Pages 1560-8

Humphreys S, Stevenson A, Bacon A, Weinhardt AB, Roberts M

Abstract

In Escherichia coli, extracytoplasmic stress is partially controlled by the alternative sigma factor, RpoE (sigmaE). In response to environmental stress or alteration in the protein content of the cell envelope, sigmaE upregulates the expression of a number of genes, including htrA. It has been shown that htrA is required for intramacrophage survival and virulence in Salmonella typhimurium. To investigate whether sigmaE-regulated genes other than htrA are involved in salmonella virulence, we inactivated the rpoE gene of S. typhimurium SL1344 by allelic exchange and compared the phenotype of the mutant (GVB311) in vitro and in vivo with its parent and an isogenic htrA mutant (BRD915). Unlike E. coli, sigmaE is not required for the growth and survival of S. typhimurium at high temperatures. However, GVB311 did display a defect in its ability to utilize carbon sources other than glucose. GVB311 was more sensitive to hydrogen peroxide, superoxide, and antimicrobial peptides than SL1344 and BRD915. Although able to invade both macrophage and epithelial cell lines normally, the rpoE mutant was defective in its ability to survive and proliferate in both cell lines. The effect of the rpoE mutation on the intracellular behavior of S. typhimurium was greater than that of the htrA mutation. Both GVB311 and BRD915 were highly attenuated in mice. Neither strain was able to kill mice via the oral route, and the 50% lethal dose (LD50) for both strains via the intravenous (i.v.) route was very high. The i.v. LD50s for SL1344, BRD915, and GVB311 were <10, 5.5 x 10(5), and 1.24 x 10(7) CFU, respectively. Growth in murine tissues after oral and i.v. inoculation was impaired for both the htrA and rpoE mutant, with the latter mutant being more severely affected. Neither mutant was able to translocate successfully from the Peyer's patches to other organs after oral infection or to proliferate in the liver and spleen after i.v. inoculation. However, the htrA mutant efficiently colonized the livers and spleens of mice infected i.v., but the rpoE mutant did not. Previous studies have shown that salmonella htrA mutants are excellent live vaccines. In contrast, oral immunization of mice with GVB311 was unable to protect any of the mice from oral challenge with SL1344. Furthermore, i.v. immunization with a large dose ( approximately 10(6) CFU) of GVB311 protected less than half of the orally challenged mice. Thus, our results indicate that genes in the sigmaE regulon other than htrA play a critical role in the virulence and immunogenicity of S. typhimurium.

MeSH Terms
Animals Anti-Bacterial Agents/pharmacology Bacterial Proteins/genetics,physiology Humans Hydrogen Peroxide/pharmacology Intracellular Fluid Macrophages/microbiology Mice Mutagenesis Paraquat/pharmacology Polymyxin B/pharmacology Salmonella typhimurium/drug effects,genetics,growth & development,pathogenicity Sigma Factor/genetics,physiology Transcription Factors/genetics,physiology Tumor Cells, Cultured Virulence
Chemicals
Anti-Bacterial Agents Bacterial Proteins Sigma Factor Transcription Factors sporulation-specific sigma factors Hydrogen Peroxide Polymyxin B Paraquat
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Humphreys S
Department of Veterinary Pathology, Glasgow University Veterinary School, Glasgow G61 1QH, United Kingdom.
Stevenson A
Bacon A
Weinhardt A B
Roberts M
References (54)
54 references, click to expand
  1. How bacteria resist killing by host-defense peptides.
    Trends Microbiol. 1994 Nov;2(11):444-9 PMID: 7866702
  2. Identification of the sigma E subunit of Escherichia coli RNA polymerase: a second alternate sigma factor involved in high-temperature gene expression.
    Genes Dev. 1989 Sep;3(9):1462-71 PMID: 2691330
  3. rpoE, the gene encoding the second heat-shock sigma factor, sigma E, in Escherichia coli.
    EMBO J. 1995 Mar 1;14(5):1032-42 PMID: 7889934
  4. The rpoE gene encoding the sigma E (sigma 24) heat shock sigma factor of Escherichia coli.
    EMBO J. 1995 Mar 1;14(5):1043-55 PMID: 7889935
  5. Expression of LacZ from the htrA, nirB and groE promoters in a Salmonella vaccine strain: influence of growth in mammalian cells.
    FEMS Microbiol Lett. 1995 Feb 1;126(1):97-101 PMID: 7896085
  6. The rpoE gene of Escherichia coli, which encodes sigma E, is essential for bacterial growth at high temperature.
    J Bacteriol. 1995 May;177(10):2918-22 PMID: 7751307
  7. Macrophage killing is an essential virulence mechanism of Salmonella typhimurium.
    Proc Natl Acad Sci U S A. 1996 Apr 30;93(9):4197-201 PMID: 8633040
  8. Construction and characterization of a Yersinia enterocolitica O:8 high-temperature requirement (htrA) isogenic mutant.
    Infect Immun. 1996 Jun;64(6):2088-94 PMID: 8675311
  9. Bacterial responses to host-defense peptides.
    Trends Microbiol. 1996 Apr;4(4):127-8; discussion 128-9 PMID: 8728603
  10. Virulence properties of Pseudomonas aeruginosa lacking the extreme-stress sigma factor AlgU (sigmaE).
    Infect Immun. 1996 Jul;64(7):2774-81 PMID: 8698507
  11. Identification and characterization of the Yersinia enterocolitica gsrA gene, which protectively responds to intracellular stress induced by macrophage phagocytosis and to extracellular environmental stress.
    Infect Immun. 1996 Aug;64(8):2980-7 PMID: 8757824
  12. Salmonella typhimurium invasion induces apoptosis in infected macrophages.
    Proc Natl Acad Sci U S A. 1996 Sep 3;93(18):9833-8 PMID: 8790417
  13. New components of protein folding in extracytoplasmic compartments of Escherichia coli SurA, FkpA and Skp/OmpH.
    Mol Microbiol. 1996 Aug;21(4):871-84 PMID: 8878048
  14. Salmonella spp. are cytotoxic for cultured macrophages.
    Mol Microbiol. 1996 Sep;21(5):1101-15 PMID: 8885278
  15. PhoP-PhoQ activates transcription of pmrAB, encoding a two-component regulatory system involved in Salmonella typhimurium antimicrobial peptide resistance.
    J Bacteriol. 1996 Dec;178(23):6857-64 PMID: 8955307
  16. Role of oxidants in microbial pathophysiology.
    Clin Microbiol Rev. 1997 Jan;10(1):1-18 PMID: 8993856
  17. Safety of live oral Salmonella typhi vaccine strains with deletions in htrA and aroC aroD and immune response in humans.
    Infect Immun. 1997 Feb;65(2):452-6 PMID: 9009296
  18. Decreased intracellular survival of an fkpA mutant of Salmonella typhimurium Copenhagen.
    Infect Immun. 1997 Feb;65(2):806-10 PMID: 9009347
  19. The sigma(E) and the Cpx signal transduction systems control the synthesis of periplasmic protein-folding enzymes in Escherichia coli.
    Genes Dev. 1997 May 1;11(9):1183-93 PMID: 9159399
  20. Modulation of the Escherichia coli sigmaE (RpoE) heat-shock transcription-factor activity by the RseA, RseB and RseC proteins.
    Mol Microbiol. 1997 Apr;24(2):355-71 PMID: 9159522
  21. The sigmaE-mediated response to extracytoplasmic stress in Escherichia coli is transduced by RseA and RseB, two negative regulators of sigmaE.
    Mol Microbiol. 1997 Apr;24(2):373-85 PMID: 9159523
  22. The Yersinia enterocolitica GsrA stress protein, involved in intracellular survival, is induced by macrophage phagocytosis.
    Infect Immun. 1997 Jun;65(6):2190-6 PMID: 9169750
  23. SlyA, a transcriptional regulator of Salmonella typhimurium, is required for resistance to oxidative stress and is expressed in the intracellular environment of macrophages.
    Infect Immun. 1997 Sep;65(9):3725-30 PMID: 9284144
  24. Bacterial copper- and zinc-cofactored superoxide dismutase contributes to the pathogenesis of systemic salmonellosis.
    Mol Microbiol. 1997 Aug;25(4):785-96 PMID: 9379906
  25. The HtrA family of serine proteases.
    Mol Microbiol. 1997 Oct;26(2):209-21 PMID: 9383148
  26. The transcriptional regulator SoxS is required for resistance of Salmonella typhimurium to paraquat but not for virulence in mice.
    Infect Immun. 1997 Dec;65(12):5371-5 PMID: 9393844
  27. Periplasmic superoxide dismutase protects Salmonella from products of phagocyte NADPH-oxidase and nitric oxide synthase.
    Proc Natl Acad Sci U S A. 1997 Dec 9;94(25):13997-4001 PMID: 9391141
  28. Comparison of the abilities of different attenuated Salmonella typhimurium strains to elicit humoral immune responses against a heterologous antigen.
    Infect Immun. 1998 Feb;66(2):732-40 PMID: 9453634
  29. Balance between endogenous superoxide stress and antioxidant defenses.
    J Bacteriol. 1998 Mar;180(6):1402-10 PMID: 9515906
  30. PmrA-PmrB-regulated genes necessary for 4-aminoarabinose lipid A modification and polymyxin resistance.
    Mol Microbiol. 1998 Mar;27(6):1171-82 PMID: 9570402
  31. Characterization of a Salmonella typhimurium aro vaccine strain expressing the P.69 antigen of Bordetella pertussis.
    Infect Immun. 1992 Oct;60(10):3994-4002 PMID: 1398911
  32. Purification and characterization of a potent bactericidal and membrane active protein from the granules of human polymorphonuclear leukocytes.
    J Biol Chem. 1978 Apr 25;253(8):2664-72 PMID: 344320
  33. Trans-complementation-dependent replication of a low molecular weight origin fragment from plasmid R6K.
    Cell. 1978 Dec;15(4):1199-208 PMID: 728998
  34. Constitutive expression of the phoP regulon attenuates Salmonella virulence and survival within macrophages.
    J Bacteriol. 1990 May;172(5):2485-90 PMID: 2185222
  35. The role of a stress-response protein in Salmonella typhimurium virulence.
    Mol Microbiol. 1991 Feb;5(2):401-7 PMID: 1645840
  36. Construction of versatile low-copy-number vectors for cloning, sequencing and gene expression in Escherichia coli.
    Gene. 1991 Apr;100:195-9 PMID: 2055470
  37. Construction of an eae deletion mutant of enteropathogenic Escherichia coli by using a positive-selection suicide vector.
    Infect Immun. 1991 Dec;59(12):4310-7 PMID: 1937792
  38. Oxidative stress responses in Escherichia coli and Salmonella typhimurium.
    Microbiol Rev. 1991 Dec;55(4):561-85 PMID: 1779927
  39. Evaluation of Salmonella typhimurium strains harbouring defined mutations in htrA and aroA in the murine salmonellosis model.
    Microb Pathog. 1992 Feb;12(2):145-51 PMID: 1584006
  40. Characterization of a locus determining the mucoid status of Pseudomonas aeruginosa: AlgU shows sequence similarities with a Bacillus sigma factor.
    J Bacteriol. 1993 Feb;175(4):1153-64 PMID: 8432708
  41. Identification of an immunoreactive Brucella abortus HtrA stress response protein homolog.
    Infect Immun. 1994 Mar;62(3):1000-7 PMID: 8112833
  42. Salmonella typhimurium loci involved in survival within macrophages.
    Infect Immun. 1994 May;62(5):1623-30 PMID: 8168923
  43. Analysis of the Streptomyces coelicolor sigE gene reveals the existence of a subfamily of eubacterial RNA polymerase sigma factors involved in the regulation of extracytoplasmic functions.
    Proc Natl Acad Sci U S A. 1994 Aug 2;91(16):7573-7 PMID: 8052622
  44. Analysis of promoters controlled by the putative sigma factor AlgU regulating conversion to mucoidy in Pseudomonas aeruginosa: relationship to sigma E and stress response.
    J Bacteriol. 1994 Nov;176(21):6688-96 PMID: 7961422
  45. Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines.
    Nature. 1981 May 21;291(5812):238-9 PMID: 7015147
  46. Nucleotide sequence of the kanamycin resistance transposon Tn903.
    J Mol Biol. 1981 Apr 5;147(2):217-26 PMID: 6270337
  47. Isolation of superoxide dismutase mutants in Escherichia coli: is superoxide dismutase necessary for aerobic life?
    EMBO J. 1986 Mar;5(3):623-30 PMID: 3011417
  48. Mutants of Salmonella typhimurium that cannot survive within the macrophage are avirulent.
    Proc Natl Acad Sci U S A. 1986 Jul;83(14):5189-93 PMID: 3523484
  49. Regulation of the promoters and transcripts of rpoH, the Escherichia coli heat shock regulatory gene.
    Genes Dev. 1987 Jul;1(5):419-32 PMID: 3315851
  50. Sequence analysis and regulation of the htrA gene of Escherichia coli: a sigma 32-independent mechanism of heat-inducible transcription.
    Nucleic Acids Res. 1988 Nov 11;16(21):10053-67 PMID: 3057437
  51. Characterization of degP, a gene required for proteolysis in the cell envelope and essential for growth of Escherichia coli at high temperature.
    J Bacteriol. 1989 May;171(5):2689-96 PMID: 2540154
  52. Direct clone characterization from plaques and colonies by the polymerase chain reaction.
    Nucleic Acids Res. 1989 May 25;17(10):4000 PMID: 2734114
  53. A two-component regulatory system (phoP phoQ) controls Salmonella typhimurium virulence.
    Proc Natl Acad Sci U S A. 1989 Jul;86(13):5054-8 PMID: 2544889
  54. DNA repair is more important than catalase for Salmonella virulence in mice.
    J Clin Invest. 1995 Mar;95(3):1047-53 PMID: 7883952
Article Info
Journal
Infection and immunity
Abbr.
Infect Immun
ISSN
0019-9567
Published
1999-04-00
Pages
1560-8
Language
English
Region
United States
NLM ID
0246127
PMCID
PMC96497
Subset
IM
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