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Identification of an atypical form of 30 kDa SOD—a possible virulence factor in clinical isolates of Shigella spp.

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Abstract

Reviews on the pathogenic mechanisms of Shigella species show a lacunae in the understanding of the bacterial antioxidant defense system and its regulations. This study was done to investigate the regulation of expression of antioxidant enzymes in clinical isolates of Shigella species, under various growth conditions. The in vitro expression of superoxide dismutase in the clinical isolates of Shigella spp., is modulated by both endogenous and exogenous factors. During aerobic and iron repleted growth conditions, the expression of the MnSOD and FeSOD enzymes were higher, and an atypical SOD was also expressed. However, under anaerobic growth conditions and in plasmid-cured strains, the antioxidant enzyme activities were decreased and the atypical SOD was not expressed. Absence of the atypical form of SOD may be due to the low oxygen environment. Plasmid-encoded factors may also play a role in the expression of this SOD, which had a molecular weight of ∼30 kDa. In the rat ileal loop ligation assay, mild lesions were observed only in the intestinal microvilli of rats injected with plasmid-cured strains of Shigella spp., suggesting that plasmid-encoded factors, including those that regulate the expression of the atypical SOD, are essential for the virulence of Shigella spp. (Mol Cell Biochem 267: 91–98, 2004)

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References

  1. Beyer W, Imaly J, Fridovich I: Superoxide dismutases. Prog Nucleic Acid Res 40: 221–253, 1991

    Google Scholar 

  2. Touati D: The molecular genetics of superoxide dismutase in E. coli. An approach to understanding the biological role and regulation of SODs in relation to other elements of the defense system against oxygen toxicity. Free Radic Res Commun 8: 1–9, 1989

    PubMed  Google Scholar 

  3. Hassan HM, Fridovich I: Regulation of the synthesis of superoxide dismutase in Escherichia coli. J Biol Chem 252: 7667–7672, 1977

    PubMed  Google Scholar 

  4. Mims CA: The encounter of the microbe with the phagocytic cell. In: The Pathogenesis of Infectious Disease. Academic Press, Inc., London, 1987, pp 63–91

    Google Scholar 

  5. Touati D: Regulation and protective role of the microbial superoxide dismutases. In: Molecular Biology of Free Radical Scavenging Systems. Cold Springer Harbour Laboratory Press, New York, 1992, pp 231–236

    Google Scholar 

  6. Demple B: Regulation of bacterial oxidative stress genes. Ann Rev Genet 25: 315–337, 1991

    PubMed  Google Scholar 

  7. Hopkin KA, Papazian MA, Steinman HM: Functional differences between manganese and iron superoxide dismutase in Escherichia coli K-12. J Bacteriol 267: 24253–24258, 1992

    Google Scholar 

  8. Benov LT, Fridovich I: Escherichia coli expresses a Copper and Zinc-containing superoxide dismutase. J Biol Chem 269: 25310–25314, 1994

    PubMed  Google Scholar 

  9. Imaly KR, Imaly JA: Cloning and analysis of sodC, encoding the copper-zinc superoxide dismutase of Escherichia coli. J Bacteriol 178: 2564–2571, 1996

    PubMed  Google Scholar 

  10. Kim EJ, Such CB, Hah YC, Roe JH: Transcriptional and post transcriptional regulation by nickel of sodN gene encoding nickel-containing superoxide dismutase from Streptomyces coelicolor Muller. Mol Microbiol 27: 187–195, 1998

    PubMed  Google Scholar 

  11. Buysee 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 169: 2561–2569, 1987

    PubMed  Google Scholar 

  12. Knutton S, Baldini M, Kaper JB, McNeish AS: Role of Plasmid-encoded adherence factors in adhesion of enteropathogenic Escherichia coli to Hep-2 cells. Infect Immun 55: 78–85, 1987

    PubMed  Google Scholar 

  13. Pal T, Hale TL: Plasmid-associated adherence of Shigella flexneri in a HeLa cell model. Infect Immun 57: 2580–2582, 1989

    PubMed  Google Scholar 

  14. Franzon VL, Aronde J, Sansonetti PJ: Contribution of superoxide dismutase and catalase activities to Shigella flexneri pathogenesis. Infect Immun 58: 529–535,1990

    PubMed  Google Scholar 

  15. Sambrook I, Fritsch EF, Maniatis T: Molecular Cloning: A Laboratory Manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, 1989

    Google Scholar 

  16. Williams PH, Sedgwick MI, Evans N, Turner PJ, George RH, McNeish AS: Adherence of enteropathogenic strain of Escherichia coli to human ntestinal mucosa is mediated by a colicinogenic conjugative plasmid. Infec Immun 22: 393–402, 1978

    Google Scholar 

  17. Guhathakurta B, Sasmal D, Datta A: Adhesion of Shigella dysenteriae type 1 and Shigella flexneri to Guinea-pig Colonic epithelial cells in vitro. J Med Microbiol 36: 403–405, 1992

    PubMed  Google Scholar 

  18. Guhathakurta B, Sasmal D, Ghosh AN, Kumar R, Saha P, Biswas D, Khetawat D, Datta A: Adhesion and invasion of a mutant Shigella flexneri to an eukaryotic cell line in absence of the 220-kb virulence plasmid. FEMS Microbiol Lett 181: 267–275, 1999

    PubMed  Google Scholar 

  19. Knapp HR, Ann Melly M: Bacterial effects of polyunsaturated fatty acids. J Inf Dis 154: 84–94, 1986

    Google Scholar 

  20. Beauchamp CO, Fridovich I: Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44: 276–287, 1971

    PubMed  Google Scholar 

  21. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ: Protein measurement with the Folin phenol reagent. J Biol Chem 193: 265–275, 1951

    PubMed  Google Scholar 

  22. Sun Y, Elwell JH, Oberley LW: A simultaneous visualization of the antioxidant enzymes glutathione peroxidase and catalase on polyacry-lamide gels. Free Radic Res Commun 5: 67–75, 1988

    PubMed  Google Scholar 

  23. Misra HP, Fridovich I: The role of superoxide in the auto oxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem 247: 3170–3175, 1972

    PubMed  Google Scholar 

  24. Laemmli UK: Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680–685, 1970

    PubMed  Google Scholar 

  25. Hassan HM, Fridovich I: Enzymatic defences against the toxicity of oxygen and streptonigrin in Escherichia coli. J Bacteriol 129: 1574–1583, 1977

    PubMed  Google Scholar 

  26. Britigan BE, Miller RA, Hassett DJ, Pfaller MA, Mccormick ML, Ramsmussen GT: Antioxidant enzyme expression in clinical isolates of Pseudomonas aeruginosa an atypical form of manganese superoxide dismutase. Infect Immun 69: 7396–7401, 2001

    PubMed  Google Scholar 

  27. Hassett DJ, Howell ML, Ochsner UA, Vasil ML, Johnson Z, Dean GE: An operon containing fumC and sodA encoding fumarase C and manganese superoxide dismutase is controlled by ferric uptake regulator in Pseudomonas aeruginosa: fur mutants produce elevated alginate levels. J Bacteriol 179: 1452–1459, 1997

    PubMed  Google Scholar 

  28. Hassett DJ, Schweizer HP, Ohman DE: Pseudomonas aeruginosa sodA and sodB mutants defective in manganese and iron co-factors superoxide dismutase activity demonstrate the importance of the iron co-factored form in aerobic metabolism. J Bacteriol 177: 6330–6337, 1995

    PubMed  Google Scholar 

  29. Benov L, Sage H, Fridovich I: The copper-and zinc-containing superoxide dismutase from Escherichia coli: Molecular weight and stability. Arch Biochem Biophys 340: 305–310, 1997

    PubMed  Google Scholar 

  30. Bourne Y, Reford SM, Steinman HM, Lepock JR, Tainer JA, Getzoff ED: Novel dimeric interface and electrostatic recognition in bacterial Cu, Zn superoxide dismutase. Proc Natl Acad Sci USA 93: 12774–12779, 1996

    PubMed  Google Scholar 

  31. Kim TS, Jung Y, Na BK, Kim KS, Chaung PR: Molecular cloning and expression of Cu/Zn containing superoxide dismutase from Faciola hepatica. Infect Immun 68: 3941–3948, 2000

    PubMed  Google Scholar 

  32. Herbert Wu CH, Tsai-wu JJ, Huang YT, Lin CY, Lioua GG, Lee FJS: Identification and Subcellular localization of a novel Cu, Zn superoxide dismutase of Mycobacterium tuberculosis. FEBS Lett 49: 192–196, 1998

    Google Scholar 

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Authors and Affiliations

  1. Department of Biochemistry, University of Madras, Guindy Campus, Chennai, India

    Radhakrishnan Prakash & S. Niranjali Devaraj

  2. Department of Zoology (Unit of Biochemistry), University of Madras, Guindy Campus, Chennai, India

    Halagowder Devaraj

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  1. Radhakrishnan Prakash
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  2. Halagowder Devaraj
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  3. S. Niranjali Devaraj
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Prakash, R., Devaraj, H. & Devaraj, S.N. Identification of an atypical form of 30 kDa SOD—a possible virulence factor in clinical isolates of Shigella spp.. Mol Cell Biochem 267, 91–98 (2004). https://doi.org/10.1023/B:MCBI.0000049369.78195.b1

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