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PMID: 8698507 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Virulence properties of Pseudomonas aeruginosa lacking the extreme-stress sigma factor AlgU (sigmaE).

Infection and immunity ·Vol. 64 ·No. 7 ·1996-07-00 ·Pages 2774-81

Yu H, Boucher JC, Hibler NS, Deretic V

Abstract

A discerning feature of Pseudomonas aeruginosa strains causing chronic endobronchial infections in cystic fibrosis is their conversion into the mucoid, exopolysaccharide alginate-overproducing phenotype. This morphologically prominent change is caused by mutations which upregulate AlgU (sigma(E)), a novel extreme-stress sigma factor with functional equivalents in gram-negative organisms. In this work, we investigated the role of algU in P. aeruginosa sensitivity to reactive oxygen intermediates, killing by phagocytic cells, and systemic virulence of this bacterium. Inactivation of algU in P. aeruginosa PA01 increased its susceptibility to killing by chemically or enzymatically generated halogenated reactive oxygen intermediates and reduced its survival in bactericidal assays with J774 murine macrophages and human neutrophils. Surprisingly, inactivation of algU caused increased systemic virulence of P. aeruginosa in mouse models of acute infection. The increased lethality of the algU-deficient strain was also observed in the endotoxin-resistant C3H/HeJ mice. Only minor differences between algU+ and algU mutant cells in their sensitivity to human serum were observed, and no differences in their lipopolysaccharide profiles were detected. Intriguingly, while inactivation of algU downregulated five polypeptides it also upregulated the expression of seven polypeptides as determined by two-dimensional gel analyses, suggesting that algU plays both a positive and a negative role in gene expression in P. aeruginosa. While the observation that algU inactivation increases systemic virulence in P. aeruginosa requires further explanation, this phenomenon contrasts with the apparent selection for strains with upregulated AlgU during colonization of the cystic fibrosis lung and suggests opposing roles for this system in chronic and acute infections.

MeSH Terms
Animals Bacterial Proteins/genetics,physiology Blood Bactericidal Activity Cystic Fibrosis/complications Disease Models, Animal Humans Hypochlorous Acid/pharmacology In Vitro Techniques Mice Mice, Inbred C3H Mice, Inbred C57BL Mutation Opportunistic Infections/complications,etiology Pseudomonas Infections/complications,etiology Pseudomonas aeruginosa/genetics,pathogenicity,physiology Sepsis/etiology,microbiology Sigma Factor/genetics,physiology Virulence/genetics,physiology
Chemicals
AlgU protein, Pseudomonas aeruginosa Bacterial Proteins Sigma Factor Hypochlorous Acid
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Yu H
Department of Microbiology, University of Texas Health Science Center at San Antonio, Texas 78284-7758, USA.
Boucher J C
Hibler N S
Deretic V
References (46)
46 references, click to expand
  1. Microbiology of lung infection in cystic fibrosis.
    Br Med Bull. 1992 Oct;48(4):912-30 PMID: 1281036
  2. Two distinct loci affecting conversion to mucoidy in Pseudomonas aeruginosa in cystic fibrosis encode homologs of the serine protease HtrA.
    J Bacteriol. 1996 Jan;178(2):511-23 PMID: 8550474
  3. A mutation in algN permits trans activation of alginate production by algT in Pseudomonas species.
    J Bacteriol. 1993 Mar;175(5):1303-8 PMID: 8444793
  4. Pathogenesis of cystic fibrosis.
    Lancet. 1993 Apr 24;341(8852):1065-9 PMID: 7682274
  5. Mechanism of conversion to mucoidy in Pseudomonas aeruginosa infecting cystic fibrosis patients.
    Proc Natl Acad Sci U S A. 1993 Sep 15;90(18):8377-81 PMID: 8378309
  6. Differentiation of Pseudomonas aeruginosa into the alginate-producing form: inactivation of mucB causes conversion to mucoidy.
    Mol Microbiol. 1993 Aug;9(3):497-506 PMID: 8412698
  7. Alginate may accumulate in cystic fibrosis lung because the enzymatic and free radical capacities of phagocytic cells are inadequate for its degradation.
    Biochem Mol Biol Int. 1993 Aug;30(6):1021-34 PMID: 8220249
  8. Conversion of Pseudomonas aeruginosa to mucoidy in cystic fibrosis: environmental stress and regulation of bacterial virulence by alternative sigma factors.
    J Bacteriol. 1994 May;176(10):2773-80 PMID: 8188579
  9. Mycobacterium marinum persists in cultured mammalian cells in a temperature-restricted fashion.
    Infect Immun. 1994 Aug;62(8):3222-9 PMID: 8039892
  10. 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
  11. Determination of median lethal and infectious doses in animal model systems.
    Methods Enzymol. 1994;235:29-39 PMID: 8057901
  12. Bactericidal activity of aerobic and anaerobic polymorphonuclear neutrophils.
    Infect Immun. 1974 Feb;9(2):337-41 PMID: 4361295
  13. Intracellular and extracellular degranulation of human polymorphonuclear azurophil and specific granules induced by immune complexes.
    Infect Immun. 1974 Dec;10(6):1241-9 PMID: 4215759
  14. Inflammatory reaction and airway damage in cystic fibrosis.
    J Lab Clin Med. 1976 Sep;88(3):423-6 PMID: 8575
  15. Alginate synthesis in mucoid Pseudomonas aeruginosa: a chromosomal locus involved in control.
    J Gen Microbiol. 1980 Aug;119(2):443-50 PMID: 6785378
  16. Simple model for the study of Pseudomonas aeruginosa infections in leukopenic mice.
    Infect Immun. 1983 Mar;39(3):1067-71 PMID: 6404816
  17. Infections caused by Pseudomonas aeruginosa.
    Rev Infect Dis. 1983 Mar-Apr;5(2):279-313 PMID: 6405475
  18. Pseudomonas aeruginosa isolates from patients with cystic fibrosis: a class of serum-sensitive, nontypable strains deficient in lipopolysaccharide O side chains.
    Infect Immun. 1983 Oct;42(1):170-7 PMID: 6413410
  19. Bacteremic pneumonia due to gram-negative bacilli.
    Arch Intern Med. 1983 Nov;143(11):2147-9 PMID: 6639235
  20. Avirulence and altered physiological properties of cystic fibrosis strains of Pseudomonas aeruginosa.
    Infect Immun. 1985 Nov;50(2):572-6 PMID: 3932213
  21. Flagella and motility alterations in Pseudomonas aeruginosa strains from patients with cystic fibrosis: relationship to patient clinical condition.
    Infect Immun. 1985 Nov;50(2):577-82 PMID: 3932214
  22. Hypochlorite scavenging by Pseudomonas aeruginosa alginate.
    Infect Immun. 1987 Aug;55(8):1813-8 PMID: 3038752
  23. Alginate inhibition of the uptake of Pseudomonas aeruginosa by macrophages.
    J Gen Microbiol. 1988 Jan;134(1):29-36 PMID: 3141564
  24. Identification, characterization, and mapping of the Escherichia coli htrA gene, whose product is essential for bacterial growth only at elevated temperatures.
    J Bacteriol. 1989 Mar;171(3):1574-84 PMID: 2537822
  25. Scavenging by alginate of free radicals released by macrophages.
    Free Radic Biol Med. 1989;6(4):347-53 PMID: 2540067
  26. Increased phagocytic cell chemiluminescence in patients with cystic fibrosis.
    Am J Dis Child. 1989 Aug;143(8):944-50 PMID: 2502909
  27. 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
  28. Differential inactivation of Escherichia coli membrane dehydrogenases by a myeloperoxidase-mediated antimicrobial system.
    Biochemistry. 1990 Jan 30;29(4):1075-80 PMID: 1692736
  29. Microbiology of airway disease in patients with cystic fibrosis.
    Clin Microbiol Rev. 1991 Jan;4(1):35-51 PMID: 1900735
  30. The role of a stress-response protein in Salmonella typhimurium virulence.
    Mol Microbiol. 1991 Feb;5(2):401-7 PMID: 1645840
  31. Seasonal onset of initial colonisation and chronic infection with Pseudomonas aeruginosa in patients with cystic fibrosis in Denmark.
    Thorax. 1992 Feb;47(2):109-11 PMID: 1549817
  32. Lung infection with alginate-producing, mucoid Pseudomonas aeruginosa in cystic fibrosis.
    APMIS Suppl. 1992;28:1-79 PMID: 1449848
  33. Mucoid-to-nonmucoid conversion in alginate-producing Pseudomonas aeruginosa often results from spontaneous mutations in algT, encoding a putative alternate sigma factor, and shows evidence for autoregulation.
    J Bacteriol. 1994 Nov;176(21):6677-87 PMID: 7961421
  34. 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
  35. Infection with Pseudomonas cepacia in chronic granulomatous disease: role of nonoxidative killing by neutrophils in host defense.
    J Infect Dis. 1994 Dec;170(6):1524-31 PMID: 7527826
  36. Biologic activities of antibodies to the neutral-polysaccharide component of the Pseudomonas aeruginosa lipopolysaccharide are blocked by O side chains and mucoid exopolysaccharide (alginate).
    Infect Immun. 1995 Jan;63(1):21-6 PMID: 7528730
  37. 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
  38. 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
  39. Functional equivalence of Escherichia coli sigma E and Pseudomonas aeruginosa AlgU: E. coli rpoE restores mucoidy and reduces sensitivity to reactive oxygen intermediates in algU mutants of P. aeruginosa.
    J Bacteriol. 1995 Jun;177(11):3259-68 PMID: 7768826
  40. Reactive oxygen species in the killing of Pseudomonas aeruginosa by human leukocytes.
    Curr Microbiol. 1995 Aug;31(2):124-8 PMID: 7606187
  41. Whole-genome random sequencing and assembly of Haemophilus influenzae Rd.
    Science. 1995 Jul 28;269(5223):496-512 PMID: 7542800
  42. Avirulence of a Pseudomonas aeruginosa algC mutant in a burned-mouse model of infection.
    Infect Immun. 1995 Oct;63(10):4166-9 PMID: 7558335
  43. Multiple promoters and induction by heat shock of the gene encoding the alternative sigma factor AlgU (sigma E) which controls mucoidy in cystic fibrosis isolates of Pseudomonas aeruginosa.
    J Bacteriol. 1995 Oct;177(19):5670-9 PMID: 7559357
  44. Pseudomonas aeruginosa sodA and sodB mutants defective in manganese- and iron-cofactored superoxide dismutase activity demonstrate the importance of the iron-cofactored form in aerobic metabolism.
    J Bacteriol. 1995 Nov;177(22):6330-7 PMID: 7592406
  45. Pseudomonas aeruginosa, mucoidy and the chronic infection phenotype in cystic fibrosis.
    Trends Microbiol. 1995 Sep;3(9):351-6 PMID: 8520888
  46. 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
Article Info
Journal
Infection and immunity
Abbr.
Infect Immun
ISSN
0019-9567
Published
1996-07-00
Pages
2774-81
Language
English
Region
United States
NLM ID
0246127
PMCID
PMC174138
Subset
IM
Grants
NIAID NIH HHS · AI31139 · United States
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