Skip to main content
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1997 Dec;179(23):7476–7487. doi: 10.1128/jb.179.23.7476-7487.1997

Negative regulation of mutS and mutH repair gene expression by the Hfq and RpoS global regulators of Escherichia coli K-12.

H C Tsui 1, G Feng 1, M E Winkler 1
PMCID: PMC179700  PMID: 9393714

Abstract

The MutS, MutL, and MutH proteins play major roles in several DNA repair pathways. We previously reported that the cellular amounts of MutS and MutH decreased by as much as 10-fold in stationary-phase cultures. Consequently, we tested whether the amounts of MutS, MutL, and MutH were regulated by two global regulators, RpoS (sigma38) and Hfq (HF-I [putative RNA chaperone]), which are involved in stationary-phase transition. We report here that mutations in hfq and rpoS reversed the stationary-phase down-regulation of the amounts of MutS and MutH. hfq regulation of the amount of MutS in stationary-phase cultures was mediated by RpoS-dependent and -independent mechanisms, whereas hfq regulation of the amount of MutH was mediated only through RpoS. Consistent with this interpretation, the amount of MutS but not MutH was regulated by Hfq, but not RpoS, in exponentially growing cells. The amount of MutL remained unchanged in rpoS, hfq-1, and rpoS+, hfq+ strains in exponentially growing and stationary-phase cultures and served as a control. The beta-galactosidase activities of single-copy mutS-lacZ operon and gene fusions suggested that hfq regulates mutS posttranscriptionally in exponentially growing cultures. RNase T2 protection assays revealed increased amounts of mutS transcript that are attributed to increased mutS transcript stability in hfq-1 mutants. Lack of Hfq also increased the amounts and stabilities of transcripts initiated from P(miaA) and P1hfqHS, two of the promoters for hfq, suggesting autoregulation, but did not change the half-life of bulk mRNA. These results suggest that the amounts of MutS and MutH may be adjusted in cells subjected to different stress conditions by an RpoS-dependent mechanism. In addition, Hfq directly or indirectly regulates several genes, including mutS, hfq, and miaA, by an RpoS-independent mechanism that destabilizes transcripts.

Full Text

The Full Text of this article is available as a PDF (624.0 KB).

Selected References

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

  1. Arps P. J., Winkler M. E. Structural analysis of the Escherichia coli K-12 hisT operon by using a kanamycin resistance cassette. J Bacteriol. 1987 Mar;169(3):1061–1070. doi: 10.1128/jb.169.3.1061-1070.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Babitzke P., Kushner S. R. The Ams (altered mRNA stability) protein and ribonuclease E are encoded by the same structural gene of Escherichia coli. Proc Natl Acad Sci U S A. 1991 Jan 1;88(1):1–5. doi: 10.1073/pnas.88.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Barrera I., Schuppli D., Sogo J. M., Weber H. Different mechanisms of recognition of bacteriophage Q beta plus and minus strand RNAs by Q beta replicase. J Mol Biol. 1993 Jul 20;232(2):512–521. doi: 10.1006/jmbi.1993.1407. [DOI] [PubMed] [Google Scholar]
  4. Boe L. Mechanism for induction of adaptive mutations in Escherichia coli. Mol Microbiol. 1990 Apr;4(4):597–601. doi: 10.1111/j.1365-2958.1990.tb00628.x. [DOI] [PubMed] [Google Scholar]
  5. Brown L., Elliott T. Efficient translation of the RpoS sigma factor in Salmonella typhimurium requires host factor I, an RNA-binding protein encoded by the hfq gene. J Bacteriol. 1996 Jul;178(13):3763–3770. doi: 10.1128/jb.178.13.3763-3770.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Brown L., Elliott T. Mutations that increase expression of the rpoS gene and decrease its dependence on hfq function in Salmonella typhimurium. J Bacteriol. 1997 Feb;179(3):656–662. doi: 10.1128/jb.179.3.656-662.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Carraway M., Marinus M. G. Repair of heteroduplex DNA molecules with multibase loops in Escherichia coli. J Bacteriol. 1993 Jul;175(13):3972–3980. doi: 10.1128/jb.175.13.3972-3980.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cole J. R., Nomura M. Changes in the half-life of ribosomal protein messenger RNA caused by translational repression. J Mol Biol. 1986 Apr 5;188(3):383–392. doi: 10.1016/0022-2836(86)90162-2. [DOI] [PubMed] [Google Scholar]
  9. Donovan W. P., Kushner S. R. Polynucleotide phosphorylase and ribonuclease II are required for cell viability and mRNA turnover in Escherichia coli K-12. Proc Natl Acad Sci U S A. 1986 Jan;83(1):120–124. doi: 10.1073/pnas.83.1.120. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Dove S. L., Smith S. G., Dorman C. J. Control of Escherichia coli type 1 fimbrial gene expression in stationary phase: a negative role for RpoS. Mol Gen Genet. 1997 Mar 18;254(1):13–20. doi: 10.1007/s004380050385. [DOI] [PubMed] [Google Scholar]
  11. Eisenstark A., Calcutt M. J., Becker-Hapak M., Ivanova A. Role of Escherichia coli rpoS and associated genes in defense against oxidative damage. Free Radic Biol Med. 1996;21(7):975–993. doi: 10.1016/s0891-5849(96)00154-2. [DOI] [PubMed] [Google Scholar]
  12. Feng G., Tsui H. C., Winkler M. E. Depletion of the cellular amounts of the MutS and MutH methyl-directed mismatch repair proteins in stationary-phase Escherichia coli K-12 cells. J Bacteriol. 1996 Apr;178(8):2388–2396. doi: 10.1128/jb.178.8.2388-2396.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Feng G., Winkler M. E. Single-step purifications of His6-MutH, His6-MutL and His6-MutS repair proteins of escherichia coli K-12. Biotechniques. 1995 Dec;19(6):956–965. [PubMed] [Google Scholar]
  14. Foster P. L., Cairns J. Mechanisms of directed mutation. Genetics. 1992 Aug;131(4):783–789. doi: 10.1093/genetics/131.4.783. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Franze de Fernandez M. T., Eoyang L., August J. T. Factor fraction required for the synthesis of bacteriophage Qbeta-RNA. Nature. 1968 Aug 10;219(5154):588–590. doi: 10.1038/219588a0. [DOI] [PubMed] [Google Scholar]
  16. Franze de Fernandez M. T., Hayward W. S., August J. T. Bacterial proteins required for replication of phage Q ribonucleic acid. Pruification and properties of host factor I, a ribonucleic acid-binding protein. J Biol Chem. 1972 Feb 10;247(3):824–831. [PubMed] [Google Scholar]
  17. Gentry D. R., Hernandez V. J., Nguyen L. H., Jensen D. B., Cashel M. Synthesis of the stationary-phase sigma factor sigma s is positively regulated by ppGpp. J Bacteriol. 1993 Dec;175(24):7982–7989. doi: 10.1128/jb.175.24.7982-7989.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Gottesman S., Clark W. P., de Crecy-Lagard V., Maurizi M. R. ClpX, an alternative subunit for the ATP-dependent Clp protease of Escherichia coli. Sequence and in vivo activities. J Biol Chem. 1993 Oct 25;268(30):22618–22626. [PubMed] [Google Scholar]
  19. Harris R. S., Feng G., Ross K. J., Sidhu R., Thulin C., Longerich S., Szigety S. K., Winkler M. E., Rosenberg S. M. Mismatch repair protein MutL becomes limiting during stationary-phase mutation. Genes Dev. 1997 Sep 15;11(18):2426–2437. doi: 10.1101/gad.11.18.2426. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Hengge-Aronis R. Back to log phase: sigma S as a global regulator in the osmotic control of gene expression in Escherichia coli. Mol Microbiol. 1996 Sep;21(5):887–893. doi: 10.1046/j.1365-2958.1996.511405.x. [DOI] [PubMed] [Google Scholar]
  21. Herman C., Ogura T., Tomoyasu T., Hiraga S., Akiyama Y., Ito K., Thomas R., D'Ari R., Bouloc P. Cell growth and lambda phage development controlled by the same essential Escherichia coli gene, ftsH/hflB. Proc Natl Acad Sci U S A. 1993 Nov 15;90(22):10861–10865. doi: 10.1073/pnas.90.22.10861. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Humbert O., Prudhomme M., Hakenbeck R., Dowson C. G., Claverys J. P. Homeologous recombination and mismatch repair during transformation in Streptococcus pneumoniae: saturation of the Hex mismatch repair system. Proc Natl Acad Sci U S A. 1995 Sep 26;92(20):9052–9056. doi: 10.1073/pnas.92.20.9052. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Jishage M., Ishihama A. Regulation of RNA polymerase sigma subunit synthesis in Escherichia coli: intracellular levels of sigma 70 and sigma 38. J Bacteriol. 1995 Dec;177(23):6832–6835. doi: 10.1128/jb.177.23.6832-6835.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Kajitani M., Kato A., Wada A., Inokuchi Y., Ishihama A. Regulation of the Escherichia coli hfq gene encoding the host factor for phage Q beta. J Bacteriol. 1994 Jan;176(2):531–534. doi: 10.1128/jb.176.2.531-534.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Kaminski P. A., Desnoues N., Elmerich C. The expression of nifA in Azorhizobium caulinodans requires a gene product homologous to Escherichia coli HF-I, an RNA-binding protein involved in the replication of phage Q beta RNA. Proc Natl Acad Sci U S A. 1994 May 24;91(11):4663–4667. doi: 10.1073/pnas.91.11.4663. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Katayama Y., Gottesman S., Pumphrey J., Rudikoff S., Clark W. P., Maurizi M. R. The two-component, ATP-dependent Clp protease of Escherichia coli. Purification, cloning, and mutational analysis of the ATP-binding component. J Biol Chem. 1988 Oct 15;263(29):15226–15236. [PubMed] [Google Scholar]
  27. Kolodner R. D. Mismatch repair: mechanisms and relationship to cancer susceptibility. Trends Biochem Sci. 1995 Oct;20(10):397–401. doi: 10.1016/s0968-0004(00)89087-8. [DOI] [PubMed] [Google Scholar]
  28. Kramer W., Fartmann B., Ringbeck E. C. Transcription of mutS and mutL-homologous genes in Saccharomyces cerevisiae during the cell cycle. Mol Gen Genet. 1996 Sep 13;252(3):275–283. doi: 10.1007/BF02173773. [DOI] [PubMed] [Google Scholar]
  29. Kushner S. R., Nagaishi H., Clark A. J. Indirect suppression of recB and recC mutations by exonuclease I deficiency. Proc Natl Acad Sci U S A. 1972 Jun;69(6):1366–1370. doi: 10.1073/pnas.69.6.1366. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Lange R., Hengge-Aronis R. Identification of a central regulator of stationary-phase gene expression in Escherichia coli. Mol Microbiol. 1991 Jan;5(1):49–59. doi: 10.1111/j.1365-2958.1991.tb01825.x. [DOI] [PubMed] [Google Scholar]
  31. Lange R., Hengge-Aronis R. The cellular concentration of the sigma S subunit of RNA polymerase in Escherichia coli is controlled at the levels of transcription, translation, and protein stability. Genes Dev. 1994 Jul 1;8(13):1600–1612. doi: 10.1101/gad.8.13.1600. [DOI] [PubMed] [Google Scholar]
  32. Lee I. S., Lin J., Hall H. K., Bearson B., Foster J. W. The stationary-phase sigma factor sigma S (RpoS) is required for a sustained acid tolerance response in virulent Salmonella typhimurium. Mol Microbiol. 1995 Jul;17(1):155–167. doi: 10.1111/j.1365-2958.1995.mmi_17010155.x. [DOI] [PubMed] [Google Scholar]
  33. Lieb M., Bhagwat A. S. Very short patch repair: reducing the cost of cytosine methylation. Mol Microbiol. 1996 May;20(3):467–473. doi: 10.1046/j.1365-2958.1996.5291066.x. [DOI] [PubMed] [Google Scholar]
  34. Lieb M., Rehmat S. 5-Methylcytosine is not a mutation hot spot in nondividing Escherichia coli. Proc Natl Acad Sci U S A. 1997 Feb 4;94(3):940–945. doi: 10.1073/pnas.94.3.940. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Lieb M., Rehmat S. Very short patch repair of T:G mismatches in vivo: importance of context and accessory proteins. J Bacteriol. 1995 Feb;177(3):660–666. doi: 10.1128/jb.177.3.660-666.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Loewen P. C., Hengge-Aronis R. The role of the sigma factor sigma S (KatF) in bacterial global regulation. Annu Rev Microbiol. 1994;48:53–80. doi: 10.1146/annurev.mi.48.100194.000413. [DOI] [PubMed] [Google Scholar]
  37. Man T. K., Pease A. J., Winkler M. E. Maximization of transcription of the serC (pdxF)-aroA multifunctional operon by antagonistic effects of the cyclic AMP (cAMP) receptor protein-cAMP complex and Lrp global regulators of Escherichia coli K-12. J Bacteriol. 1997 Jun;179(11):3458–3469. doi: 10.1128/jb.179.11.3458-3469.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Marra G., Chang C. L., Laghi L. A., Chauhan D. P., Young D., Boland C. R. Expression of human MutS homolog 2 (hMSH2) protein in resting and proliferating cells. Oncogene. 1996 Nov 21;13(10):2189–2196. [PubMed] [Google Scholar]
  39. Maurizi M. R., Clark W. P., Katayama Y., Rudikoff S., Pumphrey J., Bowers B., Gottesman S. Sequence and structure of Clp P, the proteolytic component of the ATP-dependent Clp protease of Escherichia coli. J Biol Chem. 1990 Jul 25;265(21):12536–12545. [PubMed] [Google Scholar]
  40. Maurizi M. R., Trisler P., Gottesman S. Insertional mutagenesis of the lon gene in Escherichia coli: lon is dispensable. J Bacteriol. 1985 Dec;164(3):1124–1135. doi: 10.1128/jb.164.3.1124-1135.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Mellon I., Rajpal D. K., Koi M., Boland C. R., Champe G. N. Transcription-coupled repair deficiency and mutations in human mismatch repair genes. Science. 1996 Apr 26;272(5261):557–560. doi: 10.1126/science.272.5261.557. [DOI] [PubMed] [Google Scholar]
  42. Membrillo-Hernández J., Kim S. O., Cook G. M., Poole R. K. Paraquat regulation of hmp (flavohemoglobin) gene expression in Escherichia coli K-12 is SoxRS independent but modulated by sigma S. J Bacteriol. 1997 May;179(10):3164–3170. doi: 10.1128/jb.179.10.3164-3170.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Modrich P., Lahue R. Mismatch repair in replication fidelity, genetic recombination, and cancer biology. Annu Rev Biochem. 1996;65:101–133. doi: 10.1146/annurev.bi.65.070196.000533. [DOI] [PubMed] [Google Scholar]
  44. Modrich P. Mechanisms and biological effects of mismatch repair. Annu Rev Genet. 1991;25:229–253. doi: 10.1146/annurev.ge.25.120191.001305. [DOI] [PubMed] [Google Scholar]
  45. Modrich P. Mismatch repair, genetic stability, and cancer. Science. 1994 Dec 23;266(5193):1959–1960. doi: 10.1126/science.7801122. [DOI] [PubMed] [Google Scholar]
  46. Muffler A., Fischer D., Hengge-Aronis R. The RNA-binding protein HF-I, known as a host factor for phage Qbeta RNA replication, is essential for rpoS translation in Escherichia coli. Genes Dev. 1996 May 1;10(9):1143–1151. doi: 10.1101/gad.10.9.1143. [DOI] [PubMed] [Google Scholar]
  47. Muffler A., Traulsen D. D., Fischer D., Lange R., Hengge-Aronis R. The RNA-binding protein HF-I plays a global regulatory role which is largely, but not exclusively, due to its role in expression of the sigmaS subunit of RNA polymerase in Escherichia coli. J Bacteriol. 1997 Jan;179(1):297–300. doi: 10.1128/jb.179.1.297-300.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Mulvey M. R., Loewen P. C. Nucleotide sequence of katF of Escherichia coli suggests KatF protein is a novel sigma transcription factor. Nucleic Acids Res. 1989 Dec 11;17(23):9979–9991. doi: 10.1093/nar/17.23.9979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Nakao H., Watanabe H., Nakayama S., Takeda T. yst gene expression in Yersinia enterocolitica is positively regulated by a chromosomal region that is highly homologous to Escherichia coli host factor 1 gene (hfq). Mol Microbiol. 1995 Dec;18(5):859–865. doi: 10.1111/j.1365-2958.1995.18050859.x. [DOI] [PubMed] [Google Scholar]
  50. Noble J. A., Innis M. A., Koonin E. V., Rudd K. E., Banuett F., Herskowitz I. The Escherichia coli hflA locus encodes a putative GTP-binding protein and two membrane proteins, one of which contains a protease-like domain. Proc Natl Acad Sci U S A. 1993 Nov 15;90(22):10866–10870. doi: 10.1073/pnas.90.22.10866. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. O'Neal C. R., Gabriel W. M., Turk A. K., Libby S. J., Fang F. C., Spector M. P. RpoS is necessary for both the positive and negative regulation of starvation survival genes during phosphate, carbon, and nitrogen starvation in Salmonella typhimurium. J Bacteriol. 1994 Aug;176(15):4610–4616. doi: 10.1128/jb.176.15.4610-4616.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Parker B. O., Marinus M. G. Repair of DNA heteroduplexes containing small heterologous sequences in Escherichia coli. Proc Natl Acad Sci U S A. 1992 Mar 1;89(5):1730–1734. doi: 10.1073/pnas.89.5.1730. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Radman M., Matic I., Halliday J. A., Taddei F. Editing DNA replication and recombination by mismatch repair: from bacterial genetics to mechanisms of predisposition to cancer in humans. Philos Trans R Soc Lond B Biol Sci. 1995 Jan 30;347(1319):97–103. doi: 10.1098/rstb.1995.0015. [DOI] [PubMed] [Google Scholar]
  54. Rayssiguier C., Thaler D. S., Radman M. The barrier to recombination between Escherichia coli and Salmonella typhimurium is disrupted in mismatch-repair mutants. Nature. 1989 Nov 23;342(6248):396–401. doi: 10.1038/342396a0. [DOI] [PubMed] [Google Scholar]
  55. Richards B., Zhang H., Phear G., Meuth M. Conditional mutator phenotypes in hMSH2-deficient tumor cell lines. Science. 1997 Sep 5;277(5331):1523–1526. doi: 10.1126/science.277.5331.1523. [DOI] [PubMed] [Google Scholar]
  56. Rudd K. E., Miller W., Ostell J., Benson D. A. Alignment of Escherichia coli K12 DNA sequences to a genomic restriction map. Nucleic Acids Res. 1990 Jan 25;18(2):313–321. doi: 10.1093/nar/18.2.313. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Sancar A., Hearst J. E. Molecular matchmakers. Science. 1993 Mar 5;259(5100):1415–1420. doi: 10.1126/science.8451638. [DOI] [PubMed] [Google Scholar]
  58. Schaaper R. M., Radman M. The extreme mutator effect of Escherichia coli mutD5 results from saturation of mismatch repair by excessive DNA replication errors. EMBO J. 1989 Nov;8(11):3511–3516. doi: 10.1002/j.1460-2075.1989.tb08516.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Schuppli D., Miranda G., Tsui H. C., Winkler M. E., Sogo J. M., Weber H. Altered 3'-terminal RNA structure in phage Qbeta adapted to host factor-less Escherichia coli. Proc Natl Acad Sci U S A. 1997 Sep 16;94(19):10239–10242. doi: 10.1073/pnas.94.19.10239. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Schweder T., Lee K. H., Lomovskaya O., Matin A. Regulation of Escherichia coli starvation sigma factor (sigma s) by ClpXP protease. J Bacteriol. 1996 Jan;178(2):470–476. doi: 10.1128/jb.178.2.470-476.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Senear A. W., Steitz J. A. Site-specific interaction of Qbeta host factor and ribosomal protein S1 with Qbeta and R17 bacteriophage RNAs. J Biol Chem. 1976 Apr 10;251(7):1902–1912. [PubMed] [Google Scholar]
  62. Simons R. W., Houman F., Kleckner N. Improved single and multicopy lac-based cloning vectors for protein and operon fusions. Gene. 1987;53(1):85–96. doi: 10.1016/0378-1119(87)90095-3. [DOI] [PubMed] [Google Scholar]
  63. Singer M., Baker T. A., Schnitzler G., Deischel S. M., Goel M., Dove W., Jaacks K. J., Grossman A. D., Erickson J. W., Gross C. A. A collection of strains containing genetically linked alternating antibiotic resistance elements for genetic mapping of Escherichia coli. Microbiol Rev. 1989 Mar;53(1):1–24. doi: 10.1128/mr.53.1.1-24.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Squires C. L., Pedersen S., Ross B. M., Squires C. ClpB is the Escherichia coli heat shock protein F84.1. J Bacteriol. 1991 Jul;173(14):4254–4262. doi: 10.1128/jb.173.14.4254-4262.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Su Q., Schuppli D., Tsui HcT, Winkler M. E., Weber H. Strongly reduced phage Qbeta replication, but normal phage MS2 replication in an Escherichia coli K12 mutant with inactivated Qbeta host factor (hfq) gene. Virology. 1997 Jan 6;227(1):211–214. doi: 10.1006/viro.1996.8302. [DOI] [PubMed] [Google Scholar]
  66. Su S. S., Lahue R. S., Au K. G., Modrich P. Mispair specificity of methyl-directed DNA mismatch correction in vitro. J Biol Chem. 1988 May 15;263(14):6829–6835. [PubMed] [Google Scholar]
  67. Su S. S., Modrich P. Escherichia coli mutS-encoded protein binds to mismatched DNA base pairs. Proc Natl Acad Sci U S A. 1986 Jul;83(14):5057–5061. doi: 10.1073/pnas.83.14.5057. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Tanaka K., Takayanagi Y., Fujita N., Ishihama A., Takahashi H. Heterogeneity of the principal sigma factor in Escherichia coli: the rpoS gene product, sigma 38, is a second principal sigma factor of RNA polymerase in stationary-phase Escherichia coli. Proc Natl Acad Sci U S A. 1993 Apr 15;90(8):3511–3515. doi: 10.1073/pnas.90.8.3511. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Tsui H. C., Feng G., Winkler M. E. Transcription of the mutL repair, miaA tRNA modification, hfq pleiotropic regulator, and hflA region protease genes of Escherichia coli K-12 from clustered Esigma32-specific promoters during heat shock. J Bacteriol. 1996 Oct;178(19):5719–5731. doi: 10.1128/jb.178.19.5719-5731.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Tsui H. C., Leung H. C., Winkler M. E. Characterization of broadly pleiotropic phenotypes caused by an hfq insertion mutation in Escherichia coli K-12. Mol Microbiol. 1994 Jul;13(1):35–49. doi: 10.1111/j.1365-2958.1994.tb00400.x. [DOI] [PubMed] [Google Scholar]
  71. Tsui H. C., Winkler M. E. Transcriptional patterns of the mutL-miaA superoperon of Escherichia coli K-12 suggest a model for posttranscriptional regulation. Biochimie. 1994;76(12):1168–1177. doi: 10.1016/0300-9084(94)90046-9. [DOI] [PubMed] [Google Scholar]
  72. Tsui H. C., Zhao G., Feng G., Leung H. C., Winkler M. E. The mutL repair gene of Escherichia coli K-12 forms a superoperon with a gene encoding a new cell-wall amidase. Mol Microbiol. 1994 Jan;11(1):189–202. doi: 10.1111/j.1365-2958.1994.tb00300.x. [DOI] [PubMed] [Google Scholar]
  73. Welsh K. M., Lu A. L., Clark S., Modrich P. Isolation and characterization of the Escherichia coli mutH gene product. J Biol Chem. 1987 Nov 15;262(32):15624–15629. [PubMed] [Google Scholar]
  74. Wu T. H., Marinus M. G. Dominant negative mutator mutations in the mutS gene of Escherichia coli. J Bacteriol. 1994 Sep;176(17):5393–5400. doi: 10.1128/jb.176.17.5393-5400.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Xu J., Johnson R. C. Identification of genes negatively regulated by Fis: Fis and RpoS comodulate growth-phase-dependent gene expression in Escherichia coli. J Bacteriol. 1995 Feb;177(4):938–947. doi: 10.1128/jb.177.4.938-947.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Yang Y., Zhao G., Winkler M. E. Identification of the pdxK gene that encodes pyridoxine (vitamin B6) kinase in Escherichia coli K-12. FEMS Microbiol Lett. 1996 Jul 15;141(1):89–95. doi: 10.1111/j.1574-6968.1996.tb08368.x. [DOI] [PubMed] [Google Scholar]

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

RESOURCES