• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of jbacterPermissionsJournals.ASM.orgJournalJB ArticleJournal InfoAuthorsReviewers
J Bacteriol. Mar 1997; 179(6): 1931–1939.
PMCID: PMC178916

sfi-independent filamentation in Escherichia coli Is lexA dependent and requires DNA damage for induction.

Abstract

In Escherichia coli, damage to DNA induces the expression of a set of genes known collectively as the SOS response. Part of the SOS response includes genes that repair DNA damage, but another part of the response coordinates DNA replication and septation to prevent untimely cell division. The classic SOS gene product that inhibits cell division is SfiA (or SulA), which binds to FtsZ and prevents septum formation until the DNA damage has been repaired. However, another pathway acts to coordinate DNA replication and cell division when sfiA, or the sfi-dependent pathway, is inoperative. Until recently, little was known of this alternative pathway, which is called the sfi-independent pathway. We report here that sfi-independent filamentation is suppressed by lexA(Ind-) mutations, suggesting that derepression of the LexA regulon is necessary for sfi-independent induction. However, expression of LexA-controlled genes is not sufficient; DNA damage is also required to induce this secondary pathway of cell division inhibition. Furthermore, we postulate that loss of the common regulatory circuitry of the sfi-dependent and sfi-independent pathways by recA or lexA mutants uncouples cell division and DNA replication.

Full Text

The Full Text of this article is available as a PDF (1.6M).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Burton P, Holland IB. Two pathways of division inhibition in UV-irradiated E. coli. Mol Gen Genet. 1983;190(2):309–314. [PubMed]
  • Castellazzi M, George J, Buttin G. Prophage induction and cell division in E. coli. I. Further characterization of the thermosensitive mutation tif-1 whose expression mimics the effect of UV irradiation. Mol Gen Genet. 1972;119(2):139–152. [PubMed]
  • Capaldo FN, Barbour SD. DNA content, synthesis and integrity in dividing and non-dividing cells of rec- strains of Escherichia coli K12. J Mol Biol. 1975 Jan 5;91(1):53–66. [PubMed]
  • Cayrol C, Petit C, Raynaud B, Capdevielle J, Guillemot JC, Defais M. Recovery of respiration following the SOS response of Escherichia coli requires RecA-mediated induction of 2-keto-4-hydroxyglutarate aldolase. Proc Natl Acad Sci U S A. 1995 Dec 5;92(25):11806–11809. [PMC free article] [PubMed]
  • Cooper S, Helmstetter CE. Chromosome replication and the division cycle of Escherichia coli B/r. J Mol Biol. 1968 Feb 14;31(3):519–540. [PubMed]
  • D'Ari R, Huisman O. Novel mechanism of cell division inhibition associated with the SOS response in Escherichia coli. J Bacteriol. 1983 Oct;156(1):243–250. [PMC free article] [PubMed]
  • de Boer PA, Cook WR, Rothfield LI. Bacterial cell division. Annu Rev Genet. 1990;24:249–274. [PubMed]
  • George J, Castellazzi M, Buttin G. Prophage induction and cell division in E. coli. III. Mutations sfiA and sfiB restore division in tif and lon strains and permit the expression of mutator properties of tif. Mol Gen Genet. 1975 Oct 22;140(4):309–332. [PubMed]
  • Gottesman S, Halpern E, Trisler P. Role of sulA and sulB in filamentation by lon mutants of Escherichia coli K-12. J Bacteriol. 1981 Oct;148(1):265–273. [PMC free article] [PubMed]
  • Hegde S, Sandler SJ, Clark AJ, Madiraju MV. recO and recR mutations delay induction of the SOS response in Escherichia coli. Mol Gen Genet. 1995 Jan 20;246(2):254–258. [PubMed]
  • Higashitani A, Higashitani N, Horiuchi K. A cell division inhibitor SulA of Escherichia coli directly interacts with FtsZ through GTP hydrolysis. Biochem Biophys Res Commun. 1995 Apr 6;209(1):198–204. [PubMed]
  • Hiraga S, Niki H, Ogura T, Ichinose C, Mori H, Ezaki B, Jaffé A. Chromosome partitioning in Escherichia coli: novel mutants producing anucleate cells. J Bacteriol. 1989 Mar;171(3):1496–1505. [PMC free article] [PubMed]
  • Howe WE, Mount DW. Production of cells without deoxyribonucleic acid during thymidine starvation of lexA- cultures of Escherichia coli K-12. J Bacteriol. 1975 Dec;124(3):1113–1121. [PMC free article] [PubMed]
  • Huisman O, D'Ari R. An inducible DNA replication-cell division coupling mechanism in E. coli. Nature. 1981 Apr 30;290(5809):797–799. [PubMed]
  • Huisman O, D'Ari R, George J. Inducible sfi dependent division inhibition in Escherichia coli. Mol Gen Genet. 1980;177(4):629–636. [PubMed]
  • Huisman O, Jacques M, D'ari R, Caro L. Role of the sfiA-dependent cell division regulation system in Escherichia coli. J Bacteriol. 1983 Feb;153(2):1072–1074. [PMC free article] [PubMed]
  • Huisman O, D'Ari R, Gottesman S. Cell-division control in Escherichia coli: specific induction of the SOS function SfiA protein is sufficient to block septation. Proc Natl Acad Sci U S A. 1984 Jul;81(14):4490–4494. [PMC free article] [PubMed]
  • Inouye M. Pleiotropic effect of the rec A gene of Escherichia coli: uncoupling of cell division from deoxyribonucleic acid replication. J Bacteriol. 1971 May;106(2):539–542. [PMC free article] [PubMed]
  • Jaffé A, D'Ari R, Norris V. SOS-independent coupling between DNA replication and cell division in Escherichia coli. J Bacteriol. 1986 Jan;165(1):66–71. [PMC free article] [PubMed]
  • Jones C, Holland IB. Role of the SulB (FtsZ) protein in division inhibition during the SOS response in Escherichia coli: FtsZ stabilizes the inhibitor SulA in maxicells. Proc Natl Acad Sci U S A. 1985 Sep;82(18):6045–6049. [PMC free article] [PubMed]
  • Kato J, Nishimura Y, Yamada M, Suzuki H, Hirota Y. Gene organization in the region containing a new gene involved in chromosome partition in Escherichia coli. J Bacteriol. 1988 Sep;170(9):3967–3977. [PMC free article] [PubMed]
  • Kenyon CJ, Walker GC. DNA-damaging agents stimulate gene expression at specific loci in Escherichia coli. Proc Natl Acad Sci U S A. 1980 May;77(5):2819–2823. [PMC free article] [PubMed]
  • Krueger JH, Walker GC. Mud(Ap, lac)-generated fusions in studies of gene expression. Methods Enzymol. 1983;100:501–509. [PubMed]
  • Kuempel PL, Henson JM, Dircks L, Tecklenburg M, Lim DF. dif, a recA-independent recombination site in the terminus region of the chromosome of Escherichia coli. New Biol. 1991 Aug;3(8):799–811. [PubMed]
  • Lesca C, Petit C, Defais M. UV induction of LexA independent proteins which could be involved in SOS repair. Biochimie. 1991 Apr;73(4):407–409. [PubMed]
  • Lewis LK, Jenkins ME, Mount DW. Isolation of DNA damage-inducible promoters in Escherichia coli: regulation of polB (dinA), dinG, and dinH by LexA repressor. J Bacteriol. 1992 May;174(10):3377–3385. [PMC free article] [PubMed]
  • Lewis LK, Harlow GR, Gregg-Jolly LA, Mount DW. 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. [PubMed]
  • Little JW, Edmiston SH, Pacelli LZ, Mount DW. Cleavage of the Escherichia coli lexA protein by the recA protease. Proc Natl Acad Sci U S A. 1980 Jun;77(6):3225–3229. [PMC free article] [PubMed]
  • Little JW. LexA cleavage and other self-processing reactions. J Bacteriol. 1993 Aug;175(16):4943–4950. [PMC free article] [PubMed]
  • Ma C, Rupert CS. Promoters of the phr gene in Escherichia coli K-12. Mol Gen Genet. 1995 Jul 22;248(1):52–58. [PubMed]
  • Maguin E, Brody H, Hill CW, D'Ari R. SOS-associated division inhibition gene sfiC is part of excisable element e14 in Escherichia coli. J Bacteriol. 1986 Oct;168(1):464–466. [PMC free article] [PubMed]
  • Mizusawa S, Gottesman S. Protein degradation in Escherichia coli: the lon gene controls the stability of sulA protein. Proc Natl Acad Sci U S A. 1983 Jan;80(2):358–362. [PMC free article] [PubMed]
  • Niki H, Jaffé A, Imamura R, Ogura T, Hiraga S. The new gene mukB codes for a 177 kd protein with coiled-coil domains involved in chromosome partitioning of E. coli. EMBO J. 1991 Jan;10(1):183–193. [PMC free article] [PubMed]
  • Nordström K, Bernander R, Dasgupta S. The Escherichia coli cell cycle: one cycle or multiple independent processes that are co-ordinated? Mol Microbiol. 1991 Apr;5(4):769–774. [PubMed]
  • 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. [PMC free article] [PubMed]
  • Petit C, Cayrol C, Lesca C, Kaiser P, Thompson C, Defais M. Characterization of dinY, a new Escherichia coli DNA repair gene whose products are damage inducible even in a lexA(Def) background. J Bacteriol. 1993 Feb;175(3):642–646. [PMC free article] [PubMed]
  • Sassanfar M, Roberts JW. Nature of the SOS-inducing signal in Escherichia coli. The involvement of DNA replication. J Mol Biol. 1990 Mar 5;212(1):79–96. [PubMed]
  • Satta G, Pardee AB. Inhibition of Escherichia coli division by protein X. J Bacteriol. 1978 Mar;133(3):1492–1500. [PMC free article] [PubMed]
  • Schmid MB. A locus affecting nucleoid segregation in Salmonella typhimurium. J Bacteriol. 1990 Sep;172(9):5416–5424. [PMC free article] [PubMed]
  • Sharma B, Hill TM. Insertion of inverted Ter sites into the terminus region of the Escherichia coli chromosome delays completion of DNA replication and disrupts the cell cycle. Mol Microbiol. 1995 Oct;18(1):45–61. [PubMed]
  • Skarstad K, Boye E. Degradation of individual chromosomes in recA mutants of Escherichia coli. J Bacteriol. 1993 Sep;175(17):5505–5509. [PMC free article] [PubMed]
  • Wu LJ, Franks AH, Wake RG. Replication through the terminus region of the Bacillus subtilis chromosome is not essential for the formation of a division septum that partitions the DNA. J Bacteriol. 1995 Oct;177(19):5711–5715. [PMC free article] [PubMed]
  • Zyskind JW, Svitil AL, Stine WB, Biery MC, Smith DW. RecA protein of Escherichia coli and chromosome partitioning. Mol Microbiol. 1992 Sep;6(17):2525–2537. [PubMed]

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

Formats:

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...

Links

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...