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. 2001 May;158(1):41–64. doi: 10.1093/genetics/158.1.41

Comparative gene expression profiles following UV exposure in wild-type and SOS-deficient Escherichia coli.

J Courcelle 1, A Khodursky 1, B Peter 1, P O Brown 1, P C Hanawalt 1
PMCID: PMC1461638  PMID: 11333217

Abstract

The SOS response in UV-irradiated Escherichia coli includes the upregulation of several dozen genes that are negatively regulated by the LexA repressor. Using DNA microarrays containing amplified DNA fragments from 95.5% of all open reading frames identified on the E. coli chromosome, we have examined the changes in gene expression following UV exposure in both wild-type cells and lexA1 mutants, which are unable to induce genes under LexA control. We report here the time courses of expression of the genes surrounding the 26 documented lexA-regulated regions on the E. coli chromosome. We observed 17 additional sites that responded in a lexA-dependent manner and a large number of genes that were upregulated in a lexA-independent manner although upregulation in this manner was generally not more than twofold. In addition, several transcripts were either downregulated or degraded following UV irradiation. These newly identified UV-responsive genes are discussed with respect to their possible roles in cellular recovery following exposure to UV irradiation.

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Selected References

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  1. Arthur H. M., Eastlake P. B. Transcriptional control of the uvrD gene of Escherichia coli. Gene. 1983 Nov;25(2-3):309–316. doi: 10.1016/0378-1119(83)90235-4. [DOI] [PubMed] [Google Scholar]
  2. Bagg A., Kenyon C. J., Walker G. C. Inducibility of a gene product required for UV and chemical mutagenesis in Escherichia coli. Proc Natl Acad Sci U S A. 1981 Sep;78(9):5749–5753. doi: 10.1073/pnas.78.9.5749. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Barondess J. J., Beckwith J. A bacterial virulence determinant encoded by lysogenic coliphage lambda. Nature. 1990 Aug 30;346(6287):871–874. doi: 10.1038/346871a0. [DOI] [PubMed] [Google Scholar]
  4. Barondess J. J., Beckwith J. bor gene of phage lambda, involved in serum resistance, encodes a widely conserved outer membrane lipoprotein. J Bacteriol. 1995 Mar;177(5):1247–1253. doi: 10.1128/jb.177.5.1247-1253.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Berg O. G., von Hippel P. H. Selection of DNA binding sites by regulatory proteins. II. The binding specificity of cyclic AMP receptor protein to recognition sites. J Mol Biol. 1988 Apr 20;200(4):709–723. doi: 10.1016/0022-2836(88)90482-2. [DOI] [PubMed] [Google Scholar]
  6. Blattner F. R., Plunkett G., 3rd, Bloch C. A., Perna N. T., Burland V., Riley M., Collado-Vides J., Glasner J. D., Rode C. K., Mayhew G. F. The complete genome sequence of Escherichia coli K-12. Science. 1997 Sep 5;277(5331):1453–1462. doi: 10.1126/science.277.5331.1453. [DOI] [PubMed] [Google Scholar]
  7. Bonner C. A., Hays S., McEntee K., Goodman M. F. DNA polymerase II is encoded by the DNA damage-inducible dinA gene of Escherichia coli. Proc Natl Acad Sci U S A. 1990 Oct;87(19):7663–7667. doi: 10.1073/pnas.87.19.7663. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Brandsma J. A., Bosch D., Backendorf C., van de Putte P. A common regulatory region shared by divergently transcribed genes of the Escherichia coli SOS system. Nature. 1983 Sep 15;305(5931):243–245. doi: 10.1038/305243a0. [DOI] [PubMed] [Google Scholar]
  9. Brent R., Ptashne M. Mechanism of action of the lexA gene product. Proc Natl Acad Sci U S A. 1981 Jul;78(7):4204–4208. doi: 10.1073/pnas.78.7.4204. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Casaregola S., D'Ari R., Huisman O. Quantitative evaluation of recA gene expression in Escherichia coli. Mol Gen Genet. 1982;185(3):430–439. doi: 10.1007/BF00334135. [DOI] [PubMed] [Google Scholar]
  11. Courcelle J., Carswell-Crumpton C., Hanawalt P. C. recF and recR are required for the resumption of replication at DNA replication forks in Escherichia coli. Proc Natl Acad Sci U S A. 1997 Apr 15;94(8):3714–3719. doi: 10.1073/pnas.94.8.3714. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Courcelle J., Crowley D. J., Hanawalt P. C. Recovery of DNA replication in UV-irradiated Escherichia coli requires both excision repair and recF protein function. J Bacteriol. 1999 Feb;181(3):916–922. doi: 10.1128/jb.181.3.916-922.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Crowley D. J., Hanawalt P. C. Induction of the SOS response increases the efficiency of global nucleotide excision repair of cyclobutane pyrimidine dimers, but not 6-4 photoproducts, in UV-irradiated Escherichia coli. J Bacteriol. 1998 Jul;180(13):3345–3352. doi: 10.1128/jb.180.13.3345-3352.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Fernández De Henestrosa A. R., Ogi T., Aoyagi S., Chafin D., Hayes J. J., Ohmori H., Woodgate R. Identification of additional genes belonging to the LexA regulon in Escherichia coli. Mol Microbiol. 2000 Mar;35(6):1560–1572. doi: 10.1046/j.1365-2958.2000.01826.x. [DOI] [PubMed] [Google Scholar]
  15. Fogliano M., Schendel P. F. Evidence for the inducibility of the uvrB operon. Nature. 1981 Jan 15;289(5794):196–198. doi: 10.1038/289196a0. [DOI] [PubMed] [Google Scholar]
  16. Georgiou T., Yu Y. N., Ekunwe S., Buttner M. J., Zuurmond A., Kraal B., Kleanthous C., Snyder L. Specific peptide-activated proteolytic cleavage of Escherichia coli elongation factor Tu. Proc Natl Acad Sci U S A. 1998 Mar 17;95(6):2891–2895. doi: 10.1073/pnas.95.6.2891. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Huisman O., D'Ari R. An inducible DNA replication-cell division coupling mechanism in E. coli. Nature. 1981 Apr 30;290(5809):797–799. doi: 10.1038/290797a0. [DOI] [PubMed] [Google Scholar]
  18. Iwasaki H., Nakata A., Walker G. C., Shinagawa H. The Escherichia coli polB gene, which encodes DNA polymerase II, is regulated by the SOS system. J Bacteriol. 1990 Nov;172(11):6268–6273. doi: 10.1128/jb.172.11.6268-6273.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Jin S., Chen Y., Christie G. E., Benedik M. J. Regulation of the Serratia marcescens extracellular nuclease: positive control by a homolog of P2 Ogr encoded by a cryptic prophage. J Mol Biol. 1996 Feb 23;256(2):264–278. doi: 10.1006/jmbi.1996.0084. [DOI] [PubMed] [Google Scholar]
  20. Kenyon C. J., Walker G. C. Expression of the E. coli uvrA gene is inducible. Nature. 1981 Feb 26;289(5800):808–810. doi: 10.1038/289808a0. [DOI] [PubMed] [Google Scholar]
  21. Khodursky A. B., Peter B. J., Schmid M. B., DeRisi J., Botstein D., Brown P. O., Cozzarelli N. R. Analysis of topoisomerase function in bacterial replication fork movement: use of DNA microarrays. Proc Natl Acad Sci U S A. 2000 Aug 15;97(17):9419–9424. doi: 10.1073/pnas.97.17.9419. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Lewis L. K., Harlow G. R., Gregg-Jolly L. A., Mount D. W. Identification of high affinity binding sites for LexA which define new DNA damage-inducible genes in Escherichia coli. J Mol Biol. 1994 Aug 26;241(4):507–523. doi: 10.1006/jmbi.1994.1528. [DOI] [PubMed] [Google Scholar]
  23. Little J. W. Autodigestion of lexA and phage lambda repressors. Proc Natl Acad Sci U S A. 1984 Mar;81(5):1375–1379. doi: 10.1073/pnas.81.5.1375. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Little J. W., Mount D. W., Yanisch-Perron C. R. Purified lexA protein is a repressor of the recA and lexA genes. Proc Natl Acad Sci U S A. 1981 Jul;78(7):4199–4203. doi: 10.1073/pnas.78.7.4199. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Lloyd R. G., Picksley S. M., Prescott C. Inducible expression of a gene specific to the RecF pathway for recombination in Escherichia coli K12. Mol Gen Genet. 1983;190(1):162–167. doi: 10.1007/BF00330340. [DOI] [PubMed] [Google Scholar]
  26. Mellon I., Hanawalt P. C. Induction of the Escherichia coli lactose operon selectively increases repair of its transcribed DNA strand. Nature. 1989 Nov 2;342(6245):95–98. doi: 10.1038/342095a0. [DOI] [PubMed] [Google Scholar]
  27. Ohmori H., Saito M., Yasuda T., Nagata T., Fujii T., Wachi M., Nagai K. The pcsA gene is identical to dinD in Escherichia coli. J Bacteriol. 1995 Jan;177(1):156–165. doi: 10.1128/jb.177.1.156-165.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Perrino F. W., Rein D. C., Bobst A. M., Meyer R. R. The relative rate of synthesis and levels of single-stranded DNA binding protein during induction of SOS repair in Escherichia coli. Mol Gen Genet. 1987 Oct;209(3):612–614. doi: 10.1007/BF00331171. [DOI] [PubMed] [Google Scholar]
  29. Perry K. L., Elledge S. J., Mitchell B. B., Marsh L., Walker G. C. umuDC and mucAB operons whose products are required for UV light- and chemical-induced mutagenesis: UmuD, MucA, and LexA proteins share homology. Proc Natl Acad Sci U S A. 1985 Jul;82(13):4331–4335. doi: 10.1073/pnas.82.13.4331. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Prieto-Alamo M. J., Jurado J., Gallardo-Madueno R., Monje-Casas F., Holmgren A., Pueyo C. Transcriptional regulation of glutaredoxin and thioredoxin pathways and related enzymes in response to oxidative stress. J Biol Chem. 2000 May 5;275(18):13398–13405. doi: 10.1074/jbc.275.18.13398. [DOI] [PubMed] [Google Scholar]
  31. Rudd K. E. EcoGene: a genome sequence database for Escherichia coli K-12. Nucleic Acids Res. 2000 Jan 1;28(1):60–64. doi: 10.1093/nar/28.1.60. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Salles B., Paoletti C. Control of UV induction of recA protein. Proc Natl Acad Sci U S A. 1983 Jan;80(1):65–69. doi: 10.1073/pnas.80.1.65. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Sassanfar M., Roberts J. W. Nature of the SOS-inducing signal in Escherichia coli. The involvement of DNA replication. J Mol Biol. 1990 Mar 5;212(1):79–96. doi: 10.1016/0022-2836(90)90306-7. [DOI] [PubMed] [Google Scholar]
  34. Slilaty S. N., Little J. W. Lysine-156 and serine-119 are required for LexA repressor cleavage: a possible mechanism. Proc Natl Acad Sci U S A. 1987 Jun;84(12):3987–3991. doi: 10.1073/pnas.84.12.3987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Taddei F., Matic I., Radman M. cAMP-dependent SOS induction and mutagenesis in resting bacterial populations. Proc Natl Acad Sci U S A. 1995 Dec 5;92(25):11736–11740. doi: 10.1073/pnas.92.25.11736. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Walker G. C. Mutagenesis and inducible responses to deoxyribonucleic acid damage in Escherichia coli. Microbiol Rev. 1984 Mar;48(1):60–93. doi: 10.1128/mr.48.1.60-93.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]

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