Skip to main content
PMC home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1986 Jun;166(3):756–762. doi: 10.1128/jb.166.3.756-762.1986

Overproduction of FtsZ suppresses sensitivity of lon mutants to division inhibition.

J Lutkenhaus, B Sanjanwala, M Lowe
PMCID: PMC215191  PMID: 3011743

Abstract

Escherichia coli lon mutants are sensitive to UV light and other DNA-damaging agents. This sensitivity is due to the loss of the lon-encoded ATP-dependent proteolytic activity which results in increased stability of the cell division inhibitor SulA. Introduction of the multicopy plasmid pZAQ containing the ftsZ gene, which is known to increase the level of FtsZ, suppressed the sensitivity of lon mutants to the DNA-damaging agents UV and nitrofurantoin. Alterations of pZAQ which reduced the expression of ftsZ reduced the ability of this plasmid to suppress the UV sensitivity. Examination of the kinetics of cell division revealed that pZAQ did not suppress the transient filamentation seen after exposure to UV, but did suppress the long-term inhibition that is normally observed. lon strains carrying pZAQ could stably maintain a multicopy plasmid carrying sulA (pBS2), which cannot otherwise be introduced into lon mutants. In addition, the increased temperature sensitivity of lexA(Ts) strains containing pBS2 was suppressed by pZAQ. These results suggest that SulA inhibits cell division by inhibiting FtsZ and that this interaction is stoichiometric.

Full text

PDF
756

Images in this article

761Image
on p.761

Selected References

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

  1. Beck E., Bremer E. Nucleotide sequence of the gene ompA coding the outer membrane protein II of Escherichia coli K-12. Nucleic Acids Res. 1980 Jul 11;8(13):3011–3027. doi: 10.1093/nar/8.13.3011. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Burnette W. N. "Western blotting": electrophoretic transfer of proteins from sodium dodecyl sulfate--polyacrylamide gels to unmodified nitrocellulose and radiographic detection with antibody and radioiodinated protein A. Anal Biochem. 1981 Apr;112(2):195–203. doi: 10.1016/0003-2697(81)90281-5. [DOI] [PubMed] [Google Scholar]
  3. Burton P., Holland I. B. Two pathways of division inhibition in UV-irradiated E. coli. Mol Gen Genet. 1983;190(1):128–132. doi: 10.1007/BF00330334. [DOI] [PubMed] [Google Scholar]
  4. Charette M. F., Henderson G. W., Markovitz A. ATP hydrolysis-dependent protease activity of the lon (capR) protein of Escherichia coli K-12. Proc Natl Acad Sci U S A. 1981 Aug;78(8):4728–4732. doi: 10.1073/pnas.78.8.4728. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Chung C. H., Goldberg A. L. The product of the lon (capR) gene in Escherichia coli is the ATP-dependent protease, protease La. Proc Natl Acad Sci U S A. 1981 Aug;78(8):4931–4935. doi: 10.1073/pnas.78.8.4931. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. 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. doi: 10.1128/jb.156.1.243-250.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Gayda R. C., Yamamoto L. T., Markovitz A. Second-site mutations in capR (lon) strains of Escherichia coli K-12 that prevent radiation sensitivity and allow bacteriophage lambda to lysogenize. J Bacteriol. 1976 Sep;127(3):1208–1216. doi: 10.1128/jb.127.3.1208-1216.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. 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] [Google Scholar]
  9. 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. doi: 10.1128/jb.148.1.265-273.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Gottesman S., Zipser D. Deg phenotype of Escherichia coli lon mutants. J Bacteriol. 1978 Feb;133(2):844–851. doi: 10.1128/jb.133.2.844-851.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. HOWARD-FLANDERS P., SIMSON E., THERIOT L. A LOCUS THAT CONTROLS FILAMENT FORMATION AND SENSITIVITY TO RADIATION IN ESCHERICHIA COLI K-12. Genetics. 1964 Feb;49:237–246. doi: 10.1093/genetics/49.2.237. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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]
  13. Huisman O., D'Ari R., George J. Inducible sfi dependent division inhibition in Escherichia coli. Mol Gen Genet. 1980;177(4):629–636. doi: 10.1007/BF00272673. [DOI] [PubMed] [Google Scholar]
  14. 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. doi: 10.1073/pnas.81.14.4490. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Jones C. A., Holland I. B. Inactivation of essential division genes, ftsA, ftsZ, suppresses mutations at sfiB, a locus mediating division inhibition during the SOS response in E. coli. EMBO J. 1984 May;3(5):1181–1186. doi: 10.1002/j.1460-2075.1984.tb01948.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Jones C., Holland I. B. 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. doi: 10.1073/pnas.82.18.6045. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Little J. W., Mount D. W. The SOS regulatory system of Escherichia coli. Cell. 1982 May;29(1):11–22. doi: 10.1016/0092-8674(82)90085-x. [DOI] [PubMed] [Google Scholar]
  18. Lutkenhaus J. F. Coupling of DNA replication and cell division: sulB is an allele of ftsZ. J Bacteriol. 1983 Jun;154(3):1339–1346. doi: 10.1128/jb.154.3.1339-1346.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Lutkenhaus J. F., Wolf-Watz H., Donachie W. D. Organization of genes in the ftsA-envA region of the Escherichia coli genetic map and identification of a new fts locus (ftsZ). J Bacteriol. 1980 May;142(2):615–620. doi: 10.1128/jb.142.2.615-620.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Mizusawa S., Court D., Gottesman S. Transcription of the sulA gene and repression by LexA. J Mol Biol. 1983 Dec 15;171(3):337–343. doi: 10.1016/0022-2836(83)90097-9. [DOI] [PubMed] [Google Scholar]
  21. 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. doi: 10.1073/pnas.80.2.358. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Mound D. W., Walker A. C., Kosel C. Suppression of lex mutations affecting deoxyribonucleic acid repair in Escherichia coli K-12 by closely linked thermosensitive mutations. J Bacteriol. 1973 Nov;116(2):950–956. doi: 10.1128/jb.116.2.950-956.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Schoemaker J. M., Gayda R. C., Markovitz A. Regulation of cell division in Escherichia coli: SOS induction and cellular location of the sulA protein, a key to lon-associated filamentation and death. J Bacteriol. 1984 May;158(2):551–561. doi: 10.1128/jb.158.2.551-561.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Takano T. Bacterial mutants defective in plasmid formation: requirement for the lon + allele. Proc Natl Acad Sci U S A. 1971 Jul;68(7):1469–1473. doi: 10.1073/pnas.68.7.1469. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. 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]
  26. Walker J. R., Ussery C. L., Allen J. S. Bacterial cell division regulation: lysogenization of conditional cell division lon - mutants of Escherichia coli by bacteriophage. J Bacteriol. 1973 Mar;113(3):1326–1332. doi: 10.1128/jb.113.3.1326-1332.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Ward J. E., Jr, Lutkenhaus J. F. A lacZ-ftsZ gene fusion is an analog of the cell division inhibitor sulA. J Bacteriol. 1984 Mar;157(3):815–820. doi: 10.1128/jb.157.3.815-820.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Ward J. E., Jr, Lutkenhaus J. Overproduction of FtsZ induces minicell formation in E. coli. Cell. 1985 Oct;42(3):941–949. doi: 10.1016/0092-8674(85)90290-9. [DOI] [PubMed] [Google Scholar]
  29. Yi Q. M., Lutkenhaus J. The nucleotide sequence of the essential cell-division gene ftsZ of Escherichia coli. Gene. 1985;36(3):241–247. doi: 10.1016/0378-1119(85)90179-9. [DOI] [PubMed] [Google Scholar]
  30. Yi Q. M., Rockenbach S., Ward J. E., Jr, Lutkenhaus J. Structure and expression of the cell division genes ftsQ, ftsA and ftsZ. J Mol Biol. 1985 Aug 5;184(3):399–412. doi: 10.1016/0022-2836(85)90290-6. [DOI] [PubMed] [Google Scholar]
  31. de Bruijn F. J., Lupski J. R. The use of transposon Tn5 mutagenesis in the rapid generation of correlated physical and genetic maps of DNA segments cloned into multicopy plasmids--a review. Gene. 1984 Feb;27(2):131–149. doi: 10.1016/0378-1119(84)90135-5. [DOI] [PubMed] [Google Scholar]

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

RESOURCES