Skip to main content
NCBI home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1989 Mar;171(3):1476–1484. doi: 10.1128/jb.171.3.1476-1484.1989

Escherichia coli proteins inducible by oxidative stress mediated by the superoxide radical.

L K Walkup 1, T Kogoma 1
PMCID: PMC209769  PMID: 2537820

Abstract

Two-dimensional gel analyses were made of proteins synthesized in Escherichia coli during various O2- -generating conditions. Nine proteins were constitutively synthesized over wild-type levels in superoxide dismutase (sodA sodB) double mutants. Addition of redox cycling agents such as paraquat and plumbagin at various concentrations induced up to 13 proteins in wild-type cells. Among these 13 were 5 of the 9 constitutively synthesized in the sodA sodB double mutants. Addition of these agents to the superoxide dismutase mutants in low micromolar concentrations induced an additional set of 14 proteins. The proteins induced included only five proteins that have been previously associated with stress responses, consisting of endonuclease IV (Nfo), three oxyR-regulated proteins, and one heat shock protein. O2- -mediated induction of the superoxide inducible (Soi) proteins in the wild type was independent of the oxyR+ gene for all but the three oxyR-regulated proteins. Analyses of proteins from three soi::lacZ gene fusions previously isolated (T. Kogoma, S. B. Farr, K. M. Joyce, and D. O. Natvig, Proc. Natl. Acad. Sci. USA 85:4799-4803, 1988) indicated the specific loss of one of these induced proteins in each fusion strain and the constitutive expression of some Soi proteins.

Full text

PDF
1476

Images in this article

1478Image
on p.1478
1479Image
on p.1479
1480Image
on p.1480
1481Image
on p.1481

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Ananthaswamy H. N., Eisenstark A. Repair of hydrogen peroxide-induced single-strand breaks in Escherichia coli deoxyribonucleic acid. J Bacteriol. 1977 Apr;130(1):187–191. doi: 10.1128/jb.130.1.187-191.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bielski B. H., Shiue G. G. Reaction rates of superoxide radicals with the essential amino acids. Ciba Found Symp. 1978 Jun 6;(65):43–56. doi: 10.1002/9780470715413.ch4. [DOI] [PubMed] [Google Scholar]
  3. Brawn K., Fridovich I. DNA strand scission by enzymically generated oxygen radicals. Arch Biochem Biophys. 1981 Feb;206(2):414–419. doi: 10.1016/0003-9861(81)90108-9. [DOI] [PubMed] [Google Scholar]
  4. Brawn M. K., Fridovich I. Increased superoxide radical production evokes inducible DNA repair in Escherichia coli. J Biol Chem. 1985 Jan 25;260(2):922–925. [PubMed] [Google Scholar]
  5. Brunori M., Rotilio G. Biochemistry of oxygen radical species. Methods Enzymol. 1984;105:22–35. doi: 10.1016/s0076-6879(84)05005-9. [DOI] [PubMed] [Google Scholar]
  6. Carlioz A., Touati D. Isolation of superoxide dismutase mutants in Escherichia coli: is superoxide dismutase necessary for aerobic life? EMBO J. 1986 Mar;5(3):623–630. doi: 10.1002/j.1460-2075.1986.tb04256.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Carlsson J., Carpenter V. S. The recA+ gene product is more important than catalase and superoxide dismutase in protecting Escherichia coli against hydrogen peroxide toxicity. J Bacteriol. 1980 Apr;142(1):319–321. doi: 10.1128/jb.142.1.319-321.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Chan E., Weiss B. Endonuclease IV of Escherichia coli is induced by paraquat. Proc Natl Acad Sci U S A. 1987 May;84(10):3189–3193. doi: 10.1073/pnas.84.10.3189. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Christman M. F., Morgan R. W., Jacobson F. S., Ames B. N. Positive control of a regulon for defenses against oxidative stress and some heat-shock proteins in Salmonella typhimurium. Cell. 1985 Jul;41(3):753–762. doi: 10.1016/s0092-8674(85)80056-8. [DOI] [PubMed] [Google Scholar]
  10. Cunningham R. P., Saporito S. M., Spitzer S. G., Weiss B. Endonuclease IV (nfo) mutant of Escherichia coli. J Bacteriol. 1986 Dec;168(3):1120–1127. doi: 10.1128/jb.168.3.1120-1127.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Demple B., Halbrook J., Linn S. Escherichia coli xth mutants are hypersensitive to hydrogen peroxide. J Bacteriol. 1983 Feb;153(2):1079–1082. doi: 10.1128/jb.153.2.1079-1082.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Ewing D. Synergistic damage from H2O2 and OH radicals in irradiated cells. Radiat Res. 1983 Apr;94(1):171–189. [PubMed] [Google Scholar]
  13. Farr S. B., D'Ari R., Touati D. Oxygen-dependent mutagenesis in Escherichia coli lacking superoxide dismutase. Proc Natl Acad Sci U S A. 1986 Nov;83(21):8268–8272. doi: 10.1073/pnas.83.21.8268. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Farr S. B., Natvig D. O., Kogoma T. Toxicity and mutagenicity of plumbagin and the induction of a possible new DNA repair pathway in Escherichia coli. J Bacteriol. 1985 Dec;164(3):1309–1316. doi: 10.1128/jb.164.3.1309-1316.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Farr S. B., Touati D., Kogoma T. Effects of oxygen stress on membrane functions in Escherichia coli: role of HPI catalase. J Bacteriol. 1988 Apr;170(4):1837–1842. doi: 10.1128/jb.170.4.1837-1842.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Fridovich I. Superoxide dismutases: regularities and irregularities. Harvey Lect. 1983 1984;79:51–75. [PubMed] [Google Scholar]
  17. Goff S. A., Goldberg A. L. Production of abnormal proteins in E. coli stimulates transcription of lon and other heat shock genes. Cell. 1985 Jun;41(2):587–595. doi: 10.1016/s0092-8674(85)80031-3. [DOI] [PubMed] [Google Scholar]
  18. Greenberg J. T., Demple B. Overproduction of peroxide-scavenging enzymes in Escherichia coli suppresses spontaneous mutagenesis and sensitivity to redox-cycling agents in oxyR-mutants. EMBO J. 1988 Aug;7(8):2611–2617. doi: 10.1002/j.1460-2075.1988.tb03111.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hagensee M. E., Bryan S. K., Moses R. E. DNA polymerase III requirement for repair of DNA damage caused by methyl methanesulfonate and hydrogen peroxide. J Bacteriol. 1987 Oct;169(10):4608–4613. doi: 10.1128/jb.169.10.4608-4613.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Hagensee M. E., Moses R. E. Repair response of Escherichia coli to hydrogen peroxide DNA damage. J Bacteriol. 1986 Dec;168(3):1059–1065. doi: 10.1128/jb.168.3.1059-1065.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Halliwell B., Gutteridge J. M. Oxygen toxicity, oxygen radicals, transition metals and disease. Biochem J. 1984 Apr 1;219(1):1–14. doi: 10.1042/bj2190001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Hassan H. M., Fridovich I. Intracellular production of superoxide radical and of hydrogen peroxide by redox active compounds. Arch Biochem Biophys. 1979 Sep;196(2):385–395. doi: 10.1016/0003-9861(79)90289-3. [DOI] [PubMed] [Google Scholar]
  23. Hassan H. M., Fridovich I. Regulation of the synthesis of superoxide dismutase in Escherichia coli. Induction by methyl viologen. J Biol Chem. 1977 Nov 10;252(21):7667–7672. [PubMed] [Google Scholar]
  24. Howard C. A., Baker T. I. Identification of DNA repair and damage induced proteins from Neurospora crassa. Mol Gen Genet. 1986 Jun;203(3):462–467. doi: 10.1007/BF00422071. [DOI] [PubMed] [Google Scholar]
  25. Imlay J. A., Linn S. Mutagenesis and stress responses induced in Escherichia coli by hydrogen peroxide. J Bacteriol. 1987 Jul;169(7):2967–2976. doi: 10.1128/jb.169.7.2967-2976.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Kogoma T., Farr S. B., Joyce K. M., Natvig D. O. Isolation of gene fusions (soi::lacZ) inducible by oxidative stress in Escherichia coli. Proc Natl Acad Sci U S A. 1988 Jul;85(13):4799–4803. doi: 10.1073/pnas.85.13.4799. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Loewen P. C. Isolation of catalase-deficient Escherichia coli mutants and genetic mapping of katE, a locus that affects catalase activity. J Bacteriol. 1984 Feb;157(2):622–626. doi: 10.1128/jb.157.2.622-626.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Loewen P. C., Triggs B. L., George C. S., Hrabarchuk B. E. Genetic mapping of katG, a locus that affects synthesis of the bifunctional catalase-peroxidase hydroperoxidase I in Escherichia coli. J Bacteriol. 1985 May;162(2):661–667. doi: 10.1128/jb.162.2.661-667.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Lutkenhaus J. F. Role of a major outer membrane protein in Escherichia coli. J Bacteriol. 1977 Aug;131(2):631–637. doi: 10.1128/jb.131.2.631-637.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Morgan R. W., Christman M. F., Jacobson F. S., Storz G., Ames B. N. Hydrogen peroxide-inducible proteins in Salmonella typhimurium overlap with heat shock and other stress proteins. Proc Natl Acad Sci U S A. 1986 Nov;83(21):8059–8063. doi: 10.1073/pnas.83.21.8059. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Morimyo M. Isolation and characterization of methyl viologen-sensitive mutants of Escherichia coli K-12. J Bacteriol. 1988 May;170(5):2136–2142. doi: 10.1128/jb.170.5.2136-2142.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Morrissey J. H. Silver stain for proteins in polyacrylamide gels: a modified procedure with enhanced uniform sensitivity. Anal Biochem. 1981 Nov 1;117(2):307–310. doi: 10.1016/0003-2697(81)90783-1. [DOI] [PubMed] [Google Scholar]
  33. Neidhardt F. C., Phillips T. A., VanBogelen R. A., Smith M. W., Georgalis Y., Subramanian A. R. Identity of the B56.5 protein, the A-protein, and the groE gene product of Escherichia coli. J Bacteriol. 1981 Jan;145(1):513–520. doi: 10.1128/jb.145.1.513-520.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. O'Farrell P. H. High resolution two-dimensional electrophoresis of proteins. J Biol Chem. 1975 May 25;250(10):4007–4021. [PMC free article] [PubMed] [Google Scholar]
  35. Pedersen S., Bloch P. L., Reeh S., Neidhardt F. C. Patterns of protein synthesis in E. coli: a catalog of the amount of 140 individual proteins at different growth rates. Cell. 1978 May;14(1):179–190. doi: 10.1016/0092-8674(78)90312-4. [DOI] [PubMed] [Google Scholar]
  36. Pelham H. R. Speculations on the functions of the major heat shock and glucose-regulated proteins. Cell. 1986 Sep 26;46(7):959–961. doi: 10.1016/0092-8674(86)90693-8. [DOI] [PubMed] [Google Scholar]
  37. Phillips T. A., VanBogelen R. A., Neidhardt F. C. lon gene product of Escherichia coli is a heat-shock protein. J Bacteriol. 1984 Jul;159(1):283–287. doi: 10.1128/jb.159.1.283-287.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Sakamoto H., Touati D. Cloning of the iron superoxide dismutase gene (sodB) in Escherichia coli K-12. J Bacteriol. 1984 Jul;159(1):418–420. doi: 10.1128/jb.159.1.418-420.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Saporito S. M., Cunningham R. P. Nucleotide sequence of the nfo gene of Escherichia coli K-12. J Bacteriol. 1988 Nov;170(11):5141–5145. doi: 10.1128/jb.170.11.5141-5145.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Schellhorn H. E., Hassan H. M. Transcriptional regulation of katE in Escherichia coli K-12. J Bacteriol. 1988 Sep;170(9):4286–4292. doi: 10.1128/jb.170.9.4286-4292.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Smith M. W., Neidhardt F. C. Proteins induced by aerobiosis in Escherichia coli. J Bacteriol. 1983 Apr;154(1):344–350. doi: 10.1128/jb.154.1.344-350.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Storz G., Christman M. F., Sies H., Ames B. N. Spontaneous mutagenesis and oxidative damage to DNA in Salmonella typhimurium. Proc Natl Acad Sci U S A. 1987 Dec;84(24):8917–8921. doi: 10.1073/pnas.84.24.8917. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Tilly K., VanBogelen R. A., Georgopoulos C., Neidhardt F. C. Identification of the heat-inducible protein C15.4 as the groES gene product in Escherichia coli. J Bacteriol. 1983 Jun;154(3):1505–1507. doi: 10.1128/jb.154.3.1505-1507.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Touati D. Cloning and mapping of the manganese superoxide dismutase gene (sodA) of Escherichia coli K-12. J Bacteriol. 1983 Sep;155(3):1078–1087. doi: 10.1128/jb.155.3.1078-1087.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Touati D. Transcriptional and posttranscriptional regulation of manganese superoxide dismutase biosynthesis in Escherichia coli, studied with operon and protein fusions. J Bacteriol. 1988 Jun;170(6):2511–2520. doi: 10.1128/jb.170.6.2511-2520.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. VanBogelen R. A., Kelley P. M., Neidhardt F. C. Differential induction of heat shock, SOS, and oxidation stress regulons and accumulation of nucleotides in Escherichia coli. J Bacteriol. 1987 Jan;169(1):26–32. doi: 10.1128/jb.169.1.26-32.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES