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. 1997 Jan;179(1):163–169. doi: 10.1128/jb.179.1.163-169.1997

Gene transcription and chromosome replication in Escherichia coli.

P Zhou 1, J A Bogan 1, K Welch 1, S R Pickett 1, H J Wang 1, A Zaritsky 1, C E Helmstetter 1
PMCID: PMC178675  PMID: 8981994

Abstract

Transcript levels of several Escherichia coli genes involved in chromosome replication and cell division were measured in dnaC2(Ts) mutants synchronized for chromosome replication by temperature shifts. Levels of transcripts from four of the genes, dam, nrdA, mukB, and seqA, were reduced at a certain stage during chromosome replication. The magnitudes of the decreases were similar to those reported previously ftsQ and ftsZ (P. Zhou and C. E. Helmstetter, J. Bacteriol. 176:6100-6106, 1994) but considerably less than those seen with dnaA, gidA, and mioC (P. W. Theisen, J. E. Grimwade, A. C. Leonard, J. A. Bogan, and C. E. Helmstetter, Mol. Microbiol. 10:575-584, 1993). The decreases in transcripts appeared to correlate with the estimated time at which the genes replicated. This same conclusion was reached in studies with synchronous cultures obtained with the baby machine in those instances in which periodicities in transcript levels were clearly evident. The transcriptional levels for two genes, minE and tus, did not fluctuate significantly, whereas the transcripts for one gene, iciA, appeared to increase transiently. The results support the idea that cell cycle timing in E. coli is not governed by timed bursts of gene expression, since the overall findings summarized in this report are generally consistent with cell cycle-dependent transient inhibitions of transcription rather than stimulations.

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Selected References

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  1. Andrews B. J., Herskowitz I. Regulation of cell cycle-dependent gene expression in yeast. J Biol Chem. 1990 Aug 25;265(24):14057–14060. [PubMed] [Google Scholar]
  2. Bogan J. A., Helmstetter C. E. mioC transcription, initiation of replication, and the eclipse in Escherichia coli. J Bacteriol. 1996 Jun;178(11):3201–3206. doi: 10.1128/jb.178.11.3201-3206.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bramhill D., Kornberg A. Duplex opening by dnaA protein at novel sequences in initiation of replication at the origin of the E. coli chromosome. Cell. 1988 Mar 11;52(5):743–755. doi: 10.1016/0092-8674(88)90412-6. [DOI] [PubMed] [Google Scholar]
  4. Brun Y. V., Marczynski G., Shapiro L. The expression of asymmetry during Caulobacter cell differentiation. Annu Rev Biochem. 1994;63:419–450. doi: 10.1146/annurev.bi.63.070194.002223. [DOI] [PubMed] [Google Scholar]
  5. Campbell J. L., Kleckner N. E. coli oriC and the dnaA gene promoter are sequestered from dam methyltransferase following the passage of the chromosomal replication fork. Cell. 1990 Sep 7;62(5):967–979. doi: 10.1016/0092-8674(90)90271-f. [DOI] [PubMed] [Google Scholar]
  6. Carl P. L. Escherichia coli mutants with temperature-sensitive synthesis of DNA. Mol Gen Genet. 1970;109(2):107–122. doi: 10.1007/BF00269647. [DOI] [PubMed] [Google Scholar]
  7. Carlson J., Fuchs J. A., Messing J. Primary structure of the Escherichia coli ribonucleoside diphosphate reductase operon. Proc Natl Acad Sci U S A. 1984 Jul;81(14):4294–4297. doi: 10.1073/pnas.81.14.4294. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Eberle H., Forrest N., Hrynyszyn J., Van Knapp J. Regulation of DNA synthesis and capacity for initiation in DNA temperature sensitive mutants of Escherichia coli I. Reinitiation and chain elongation. Mol Gen Genet. 1982;186(1):57–65. doi: 10.1007/BF00422912. [DOI] [PubMed] [Google Scholar]
  9. Evans I. M., Eberle H. Accumulation of the capacity of initiation of deoxyribonucleic acid replication in Escherichia coli. J Bacteriol. 1975 Mar;121(3):883–891. doi: 10.1128/jb.121.3.883-891.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. French S. Consequences of replication fork movement through transcription units in vivo. Science. 1992 Nov 20;258(5086):1362–1365. doi: 10.1126/science.1455232. [DOI] [PubMed] [Google Scholar]
  11. Garrido T., Sánchez M., Palacios P., Aldea M., Vicente M. Transcription of ftsZ oscillates during the cell cycle of Escherichia coli. EMBO J. 1993 Oct;12(10):3957–3965. doi: 10.1002/j.1460-2075.1993.tb06073.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Grover N. B., Helmstetter C. E. Characterization of cell-cycle-specific events in synchronous cultures of Escherichia coli: a theoretical evaluation. Microbiology. 1995 Jan;141(Pt 1):59–62. doi: 10.1099/00221287-141-1-59. [DOI] [PubMed] [Google Scholar]
  13. Hanna M. H., Carl P. L. Reinitiation of deoxyribonucleic acid synthesis by deoxyribonucleic acid initiation mutants of Escherichia coli: role of ribonucleic acid synthesis, protein synthesis, and cell division. J Bacteriol. 1975 Jan;121(1):219–226. doi: 10.1128/jb.121.1.219-226.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hansen F. G., Christensen B. B., Atlung T. The initiator titration model: computer simulation of chromosome and minichromosome control. Res Microbiol. 1991 Feb-Apr;142(2-3):161–167. doi: 10.1016/0923-2508(91)90025-6. [DOI] [PubMed] [Google Scholar]
  15. Hattman S., Brooks J. E., Masurekar M. Sequence specificity of the P1 modification methylase (M.Eco P1) and the DNA methylase (M.Eco dam) controlled by the Escherichia coli dam gene. J Mol Biol. 1978 Dec 15;126(3):367–380. doi: 10.1016/0022-2836(78)90046-3. [DOI] [PubMed] [Google Scholar]
  16. Helmstetter C. E., Krajewski C. A. Initiation of chromosome replication in dnaA and dnaC mutants of Escherichia coli B/r F. J Bacteriol. 1982 Feb;149(2):685–693. doi: 10.1128/jb.149.2.685-693.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hwang D. S., Thöny B., Kornberg A. IciA protein, a specific inhibitor of initiation of Escherichia coli chromosomal replication. J Biol Chem. 1992 Feb 5;267(4):2209–2213. [PubMed] [Google Scholar]
  18. Lacks S., Greenberg B. Complementary specificity of restriction endonucleases of Diplococcus pneumoniae with respect to DNA methylation. J Mol Biol. 1977 Jul;114(1):153–168. doi: 10.1016/0022-2836(77)90289-3. [DOI] [PubMed] [Google Scholar]
  19. Li Z., Clarke A. J., Beveridge T. J. A major autolysin of Pseudomonas aeruginosa: subcellular distribution, potential role in cell growth and division and secretion in surface membrane vesicles. J Bacteriol. 1996 May;178(9):2479–2488. doi: 10.1128/jb.178.9.2479-2488.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Liu B., Wong M. L., Tinker R. L., Geiduschek E. P., Alberts B. M. The DNA replication fork can pass RNA polymerase without displacing the nascent transcript. Nature. 1993 Nov 4;366(6450):33–39. doi: 10.1038/366033a0. [DOI] [PubMed] [Google Scholar]
  21. Lu M., Campbell J. L., Boye E., Kleckner N. SeqA: a negative modulator of replication initiation in E. coli. Cell. 1994 May 6;77(3):413–426. doi: 10.1016/0092-8674(94)90156-2. [DOI] [PubMed] [Google Scholar]
  22. Lutkenhaus J. F., Moore B. A., Masters M., Donachie W. D. Individual proteins are synthesized continuously throughout the Escherichia coli cell cycle. J Bacteriol. 1979 May;138(2):352–360. doi: 10.1128/jb.138.2.352-360.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Lutkenhaus J. FtsZ ring in bacterial cytokinesis. Mol Microbiol. 1993 Aug;9(3):403–409. doi: 10.1111/j.1365-2958.1993.tb01701.x. [DOI] [PubMed] [Google Scholar]
  24. Løbner-Olesen A., Skarstad K., Hansen F. G., von Meyenburg K., Boye E. The DnaA protein determines the initiation mass of Escherichia coli K-12. Cell. 1989 Jun 2;57(5):881–889. doi: 10.1016/0092-8674(89)90802-7. [DOI] [PubMed] [Google Scholar]
  25. 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. doi: 10.1002/j.1460-2075.1991.tb07935.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Ogawa T., Okazaki T. Cell cycle-dependent transcription from the gid and mioC promoters of Escherichia coli. J Bacteriol. 1994 Mar;176(6):1609–1615. doi: 10.1128/jb.176.6.1609-1615.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Roecklein B. A., Kuempel P. L. In vivo characterization of tus gene expression in Escherichia coli. Mol Microbiol. 1992 Jun;6(12):1655–1661. doi: 10.1111/j.1365-2958.1992.tb00890.x. [DOI] [PubMed] [Google Scholar]
  28. Schubach W. H., Whitmer J. D., Davern C. I. Genetic control of DNA initiation in Escherichia coli. J Mol Biol. 1973 Feb 25;74(2):205–221. doi: 10.1016/0022-2836(73)90107-1. [DOI] [PubMed] [Google Scholar]
  29. Skarstad K., Boye E. The initiator protein DnaA: evolution, properties and function. Biochim Biophys Acta. 1994 Mar 1;1217(2):111–130. doi: 10.1016/0167-4781(94)90025-6. [DOI] [PubMed] [Google Scholar]
  30. Sun L., Fuchs J. A. Escherichia coli ribonucleotide reductase expression is cell cycle regulated. Mol Biol Cell. 1992 Oct;3(10):1095–1105. doi: 10.1091/mbc.3.10.1095. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Sun L., Jacobson B. A., Dien B. S., Srienc F., Fuchs J. A. Cell cycle regulation of the Escherichia coli nrd operon: requirement for a cis-acting upstream AT-rich sequence. J Bacteriol. 1994 Apr;176(8):2415–2426. doi: 10.1128/jb.176.8.2415-2426.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Theisen P. W., Grimwade J. E., Leonard A. C., Bogan J. A., Helmstetter C. E. Correlation of gene transcription with the time of initiation of chromosome replication in Escherichia coli. Mol Microbiol. 1993 Nov;10(3):575–584. doi: 10.1111/j.1365-2958.1993.tb00929.x. [DOI] [PubMed] [Google Scholar]
  33. Zhou P., Helmstetter C. E. Relationship between ftsZ gene expression and chromosome replication in Escherichia coli. J Bacteriol. 1994 Oct;176(19):6100–6106. doi: 10.1128/jb.176.19.6100-6106.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. de Boer P. A., Crossley R. E., Rothfield L. I. Isolation and properties of minB, a complex genetic locus involved in correct placement of the division site in Escherichia coli. J Bacteriol. 1988 May;170(5):2106–2112. doi: 10.1128/jb.170.5.2106-2112.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. von Freiesleben U., Rasmussen K. V., Schaechter M. SeqA limits DnaA activity in replication from oriC in Escherichia coli. Mol Microbiol. 1994 Nov;14(4):763–772. doi: 10.1111/j.1365-2958.1994.tb01313.x. [DOI] [PubMed] [Google Scholar]

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