Skip to main content
PMC home page
Biophysical Journal logoLink to Biophysical Journal
. 1996 Jan;70(1):135–145. doi: 10.1016/S0006-3495(96)79555-3

Hypothesis: hypersensitive plasmid copy number control for ColE1.

M Ehrenberg 1
PMCID: PMC1224915  PMID: 8770193

Abstract

Initiation of replication of the plasmid ColE1 is primed by the cis-acting RNA II. Copy numbers are regulated by inhibition of RNA II by the antisense RNA I, whose concentration is proportional to the plasmid concentration. This inhibition is enhanced by a protein. Rom, and takes place during a time set by the transcription of 250 bases of the gene for RNA II. When this transcription is dominated by several steps of about equal duration, the probability for RNA II to prime DNA replication is approximately determined by e-constant[RNA I]. For large values of the "constant" small changes in [RNA I] give large variations in the priming probability. It is shown, first, that this type of mechanism can reduce the rate of plasmid loss and enable single copies of ColE1 to duplicate at a well-defined time in the cell cycle; second, that when the rate of initiation of transcription of RNA II increases, plasmid losses decrease and the distribution of single copy duplication times becomes narrower; third, that the action of Rom may further reduce plasmid losses and further narrow the distribution of duplication times in the single-copy case.

Full text

PDF
142

Selected References

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

  1. Brantl S., Birch-Hirschfeld E., Behnke D. RepR protein expression on plasmid pIP501 is controlled by an antisense RNA-mediated transcription attenuation mechanism. J Bacteriol. 1993 Jul;175(13):4052–4061. doi: 10.1128/jb.175.13.4052-4061.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Brantl S., Wagner E. G. Antisense RNA-mediated transcriptional attenuation occurs faster than stable antisense/target RNA pairing: an in vitro study of plasmid pIP501. EMBO J. 1994 Aug 1;13(15):3599–3607. doi: 10.1002/j.1460-2075.1994.tb06667.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bremer H., Lin-Chao S. Analysis of the physiological control of replication of ColE1-type plasmids. J Theor Biol. 1986 Dec 21;123(4):453–470. doi: 10.1016/s0022-5193(86)80213-2. [DOI] [PubMed] [Google Scholar]
  4. Brendel V., Perelson A. S. Quantitative model of ColE1 plasmid copy number control. J Mol Biol. 1993 Feb 20;229(4):860–872. doi: 10.1006/jmbi.1993.1092. [DOI] [PubMed] [Google Scholar]
  5. Brenner M., Tomizawa J. Quantitation of ColE1-encoded replication elements. Proc Natl Acad Sci U S A. 1991 Jan 15;88(2):405–409. doi: 10.1073/pnas.88.2.405. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Brenner M., Tomizawa J. Rom transcript of plasmid ColE1. Nucleic Acids Res. 1989 Jun 12;17(11):4309–4326. doi: 10.1093/nar/17.11.4309. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cesareni G., Muesing M. A., Polisky B. Control of ColE1 DNA replication: the rop gene product negatively affects transcription from the replication primer promoter. Proc Natl Acad Sci U S A. 1982 Oct;79(20):6313–6317. doi: 10.1073/pnas.79.20.6313. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cooper S., Helmstetter C. E. Chromosome replication and the division cycle of Escherichia coli B/r. J Mol Biol. 1968 Feb 14;31(3):519–540. doi: 10.1016/0022-2836(68)90425-7. [DOI] [PubMed] [Google Scholar]
  9. Ehrenberg M., Blomberg C. Thermodynamic constraints on kinetic proofreading in biosynthetic pathways. Biophys J. 1980 Sep;31(3):333–358. doi: 10.1016/S0006-3495(80)85063-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Ehrenberg M., Kurland C. G. Costs of accuracy determined by a maximal growth rate constraint. Q Rev Biophys. 1984 Feb;17(1):45–82. doi: 10.1017/s0033583500005254. [DOI] [PubMed] [Google Scholar]
  11. Ehrenberg M., Sverredal A. A model for copy number control of the plasmid R1. J Mol Biol. 1995 Mar 3;246(4):472–485. doi: 10.1006/jmbi.1994.0099. [DOI] [PubMed] [Google Scholar]
  12. Freter R. R., Savageau M. A. Proofreading systems of multiple stages for improved accuracy of biological discrimination. J Theor Biol. 1980 Jul 7;85(1):99–123. doi: 10.1016/0022-5193(80)90284-2. [DOI] [PubMed] [Google Scholar]
  13. Gerdes K., Larsen J. E., Molin S. Stable inheritance of plasmid R1 requires two different loci. J Bacteriol. 1985 Jan;161(1):292–298. doi: 10.1128/jb.161.1.292-298.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Itoh T., Tomizawa J. Formation of an RNA primer for initiation of replication of ColE1 DNA by ribonuclease H. Proc Natl Acad Sci U S A. 1980 May;77(5):2450–2454. doi: 10.1073/pnas.77.5.2450. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Keasling J. D., Palsson B. O. ColE1 plasmid replication: a simple kinetic description from a structured model. J Theor Biol. 1989 Dec 19;141(4):447–461. doi: 10.1016/s0022-5193(89)80230-9. [DOI] [PubMed] [Google Scholar]
  16. Keasling J. D., Palsson B. O. On the kinetics of plasmid replication. J Theor Biol. 1989 Feb 22;136(4):487–492. doi: 10.1016/s0022-5193(89)80161-4. [DOI] [PubMed] [Google Scholar]
  17. Lacatena R. M., Banner D. W., Castagnoli L., Cesareni G. Control of initiation of pMB1 replication: purified Rop protein and RNA I affect primer formation in vitro. Cell. 1984 Jul;37(3):1009–1014. doi: 10.1016/0092-8674(84)90435-5. [DOI] [PubMed] [Google Scholar]
  18. Leonard A. C., Helmstetter C. E. Replication patterns of multiple plasmids coexisting in Escherichia coli. J Bacteriol. 1988 Mar;170(3):1380–1383. doi: 10.1128/jb.170.3.1380-1383.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Masukata H., Tomizawa J. Control of primer formation for ColE1 plasmid replication: conformational change of the primer transcript. Cell. 1986 Jan 17;44(1):125–136. doi: 10.1016/0092-8674(86)90491-5. [DOI] [PubMed] [Google Scholar]
  20. Merlin S., Polisky B. Assessment of quantitative models for plasmid ColE1 copy number control. J Mol Biol. 1995 Apr 28;248(2):211–219. doi: 10.1016/s0022-2836(95)80043-3. [DOI] [PubMed] [Google Scholar]
  21. Morita M., Oka A. The structure of a transcriptional unit on colicin E1 plasmid. Eur J Biochem. 1979 Jul;97(2):435–443. doi: 10.1111/j.1432-1033.1979.tb13131.x. [DOI] [PubMed] [Google Scholar]
  22. Ninio J. Kinetic amplification of enzyme discrimination. Biochimie. 1975;57(5):587–595. doi: 10.1016/s0300-9084(75)80139-8. [DOI] [PubMed] [Google Scholar]
  23. Nordström K., Wagner E. G. Kinetic aspects of control of plasmid replication by antisense RNA. Trends Biochem Sci. 1994 Jul;19(7):294–300. doi: 10.1016/0968-0004(94)90008-6. [DOI] [PubMed] [Google Scholar]
  24. Skarstad K., Boye E., Steen H. B. Timing of initiation of chromosome replication in individual Escherichia coli cells. EMBO J. 1986 Jul;5(7):1711–1717. doi: 10.1002/j.1460-2075.1986.tb04415.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Tomizawa J. Control of ColE1 plasmid replication: binding of RNA I to RNA II and inhibition of primer formation. Cell. 1986 Oct 10;47(1):89–97. doi: 10.1016/0092-8674(86)90369-7. [DOI] [PubMed] [Google Scholar]
  26. Tomizawa J. Control of ColE1 plasmid replication: the process of binding of RNA I to the primer transcript. Cell. 1984 Oct;38(3):861–870. doi: 10.1016/0092-8674(84)90281-2. [DOI] [PubMed] [Google Scholar]
  27. Tomizawa J., Itoh T. Plasmid ColE1 incompatibility determined by interaction of RNA I with primer transcript. Proc Natl Acad Sci U S A. 1981 Oct;78(10):6096–6100. doi: 10.1073/pnas.78.10.6096. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Tomizawa J., Som T. Control of ColE1 plasmid replication: enhancement of binding of RNA I to the primer transcript by the Rom protein. Cell. 1984 Oct;38(3):871–878. doi: 10.1016/0092-8674(84)90282-4. [DOI] [PubMed] [Google Scholar]

Articles from Biophysical Journal are provided here courtesy of The Biophysical Society

RESOURCES