R-loop-dependent hypernegative supercoiling in Escherichia coli topA mutants preferentially occurs at low temperatures and correlates with growth inhibition

Journal of Molecular Biology

Volumn 294, Issue 2, 1999, Pages 321-332

  Massé, Eric ^a   Drolet, Marc ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

DNA topoisomerase I; R loop; Transcription elongation; Transcription translation coupling

Indexed keywords

BACTERIAL DNA; DNA TOPOISOMERASE; MESSENGER RNA; RIBONUCLEASE H;

ARTICLE; BACTERIAL GROWTH; BACTERIUM MUTANT; CONTROLLED STUDY; DNA SUPERCOILING; ENZYME ACTIVITY; ESCHERICHIA COLI; GROWTH INHIBITION; LOW TEMPERATURE; NONHUMAN; PRIORITY JOURNAL; RNA TRANSCRIPTION; RNA TRANSLATION;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; PROKARYOTA;

EID: 0033607485     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1999.3264     Document Type: Article

References (37)

1. Anderson P., Roth J. Spontaneous tandem genetic duplications in Salmonella typhimurium arise by unequal recombination between rRNA (rrn) cistrons. Proc. Natl Acad. Sci. USA. 78:1981;3113-3117.
2. Bourgaize D. B., Phillips T. A., VanBogelen R. A., Jones P. G., Neidhardt F. C., Fournier M. J. Loss of 4. 5S RNA induces the heat shock response and lambda prophage in Escherichia coli. J. Bacteriol. 172:1990;1151-1154.
3. Broccoli S., Phoenix P., Drolet M. Isolation of the topB gene encoding DNA topoisomerase III as a multicopy suppressor of topA null mutations in Escherichia coli. Mol. Microbiol. in the press:1999.
4. Champney W. S. Kinetics of ribosome synthesis during a nutritional shift-up in Escherichia coli K12. Mol. Gen. Genet. 152:1977;259-266.
5. Daube S. S., von Hippel P. H. RNA displacement pathways during transcription from synthetic RNA-DNA bubble duplexes. Biochemistry. 33:1994;340-347.
6. DiNardo S., Voelkel K. A., Strernglanz R., Reynolds A. E., Wright A. Escherichia coli DNA topoisomerase I mutants have compensatory mutations in DNA gyrase genes. Cell. 31:1982;43-51.
7. Drolet M., Bi X., Liu L. F. Hypernegative supercoiling of the DNA templates during transcription elongation in vitro. J. Biol. Chem. 269:1994;2068-2074.
8. Drolet M., Phoenix P., Menzel R., Massé E., Liu L. F., Crouch R. J. Overexpression of RNase H partially complements the growth defect of an Escherichia coli ΔtopA mutant: R-loop formation is a major problem in the absence of DNA topoisomerase I. Proc. Natl Acad. Sci. USA. 92:1995;3526-3530.
9. Itaya M., Crouch R. J. A combination of RNase H and recBCD or sbcB mutations in Escherichia coli adversely affects growth. Mol. Gen. Genet. 227:1991;424-432.
10. Jones P. G., Inouye M. The cold-shock response-a hot topic. Mol. Microbiol. 11:1994;811-818.
11. Jones P. G., Inouye M. RbfA, a 30S ribosomal binding factor, is a cold-shock protein whose absence triggers the cold-shock response. Mol. Microbiol. 21:1996;1207-1218.
12. Jones P. G., Cashel M., Glaser G., Neidhardt F. C. Function of a relaxed-like state following temperature downshifts in Escherichia coli. J. Bacteriol. 174:1992a;3903-3914.
13. Jones P. G., Krah R., Tafuri S. R., Wolfe A. P. DNA gyrase, CS7. 4, and the cold-shock response in Escherichia coli. J. Bacteriol. 174:1992b;5798-5802.
14. Kirkegaard K., Wang J. C. Bacterial DNA topoisomerase I can relax positively supercoiled DNA containing a single-stranded loop. J. Mol. Biol. 185:1985;625-637.
15. Lemaux P. G., Herendeen S. L., Bloch P. L., Neidhardt F. C. Transient rates of synthesis of individual polypeptides in E. coli following temperature shifts. Cell. 13:1978;427-434.
16. Lesley S. A., Jovanovich S. B., Tse-Dinh Y. C., Burgess R. R. Identification of a heat shock promoter in the topA gene of Escherichia coli. J. Bacteriol. 172:1990;6871-6874.
17. Liu L. F., Wang J. C. Supercoiling of the DNA template during transcription. Proc. Natl Acad. Sci. USA. 84:1987;7024-7027.
18. Lynch A. S., Wang J. C. Anchoring of DNA to the bacterial cytoplasmic membrane through cotranscriptional synthesis of polypeptides encoding membrane proteins or proteins for export: a mechanism of plasmid hypernegative supercoiling in mutants deficient in DNA topoisomerase I. J. Bacteriol. 175:1993;1645-1655.
19. Massé E., Drolet M. Relaxation of transcription-induced negative supercoiling is an essential function of Escherichia coli DNA topoisomerase I. J. Biol. Chem. 274:1999a;16654-16658.
20. Massé E., Drolet M. Escherichia coli DNA topoisomerase I inhibits R-loop formation by relaxing transcription-induced negative supercoiling. J. Biol. Chem. 274:1999b;16659-16664.
21. Massé E., Phoenix P., Drolet M. DNA topoisomerases regulate R-loop formation during transcription of the rrnB operon in Escherichia coli. J. Biol. Chem. 272:1997;12816-12823.
22. Miller J. H. A Short Course in Bacterial Genetics. 1992;Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
23. Ostrander E. A., Benedetti P., Wang J. C. Template supercoiling by a chimera of yeast GAL4 protein and phage T7 RNA polymerase. Science. 249:1990;1261-1265.
24. Parada C. A., Marians K. J. Transcriptional activation of pBR322 DNA can lead to duplex DNA unwinding catalyzed by the Escherichia coli preprimosome. J. Biol. Chem. 264:1989;15120-15129.
25. Phoenix P., Raymond M.-A., Massé E., Drolet M. Roles of DNA topoisomerases in the regulation of R-loop formation in vitro. J. Biol. Chem. 272:1997;1473-1479.
26. Pruss G. J., Drlica K. Topoisomerase I mutants: the gene on pBR322 that encodes resistance to tetracycline affects plasmid DNA supercoiling. Proc. Natl Acad. Sci. USA. 83:1986;8952-8956.
27. Pruss G. J., Manes S. H., Drlica K. Escherichia coli DNA topoisomerase I mutants: increased supercoiling is corrected by mutations near the gyrase genes. Cell. 31:1982;35-42.
28. 32-dependent promoter (P1) of the Escherichia coli topoisomerase I gene on thermotolerance. Mol. Microbiol. 21:1996;703-711.
29. s-dependent promoter. J. Mol. Biol. 267:1997;481-489.
30. Sambrook J., Fritsch E. F., Maniatis T. Molecular Cloning: A Laboratory Manual. 1989;Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
31. 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 alterning antibiotic resistance elements for genetic mapping of Escherichia coli. Microbiol. Rev. 53:1989;1-24.
32. Tsao Y. P., Wu H.-Y., Liu L. F. Transcription-driven supercoiling of DNA: direct biochemical evidence from in vitro studies. Cell. 56:1989;111-118.
33. VanBogelen R. A., Neidhardt F. C. Ribosomes as sensors of heat and cold shock in Escherichia coli. Proc. Natl Acad. Sci. USA. 15:1990;5589-5593.
34. VanBogelen R. A., Kelley P. M., Neidhardt F. C. Differential induction of heat shock, SOS, and oxidation stress regulons and accumulation of nucleotides in Escherichia coli. J. Bacteriol. 169:1987;26-32.
35. Wada A., Yamazaki Y., Fujita N., Ishihama A. Structure and probable genetic location of a "ribosome modulation factor" associated with 100S ribosomes in stationary-phase Escherichia coli cells. Proc. Natl Acad. Sci. USA. 87:1990;2657-2661.
36. Wang J. C. Interaction between DNA and an Escherichia coli protein omega. J. Mol. Biol. 55:1971;523-533.
37. Wu H. Y., Shyy S. H., Wang J. C., Liu L. F. Transcription generates positively and negatively supercoiled domains in the template. Cell. 53:1988;433-440.