Hypernegative supercoiling inhibits growth by causing RNA degradation

Journal of Bacteriology

Volumn 190, Issue 22, 2008, Pages 7346-7356

  Baaklini, Imad ^a   Usongo, Valentine ^a   Nolent, Flora ^a   Sanscartier, Patrick ^a   Hraiky, Chadi ^a   Drlica, Karl ^b   Drolet, Marc ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b PUBLIC HEALTH RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENDONUCLEASE; RIBONUCLEASE; SPECTINOMYCIN;

ARTICLE; BACTERIAL GROWTH; CONTROLLED STUDY; ESCHERICHIA COLI; GENE MUTATION; GENETIC TRANSCRIPTION; GROWTH DISORDER; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA DEGRADATION; RNA PROCESSING;

CYCLIC AMP RECEPTOR PROTEIN; DNA GYRASE; DNA TOPOISOMERASES, TYPE I, BACTERIAL; DNA, BACTERIAL; DNA, SUPERHELICAL; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; FACTOR FOR INVERSION STIMULATION PROTEIN; NUCLEIC ACID CONFORMATION; OXIDOREDUCTASES; PROTEIN BIOSYNTHESIS; RIBONUCLEASE H; RIBOSOMES; RNA STABILITY; TEMPERATURE;

ESCHERICHIA COLI;

EID: 55549147497     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00680-08     Document Type: Article

References (51)

1. Adhya, S., and M. Gottesman. 1978. Control of transcription termination. Annu. Rev. Biochem. 47:967-996.
2. Baaklini, I., C. Hraiky, F. Rallu, Y.-C. Tse-Dinh, and M. Drolet. 2004. RNase HI is required for efficient full-length RNA synthesis in the absence of topoisomerase I in Escherichia coli. Mol. Microbiol. 54:198-211.
3. Ball, C. A., R. Osuna, K. C. Ferguson, and R. C. Johnson. 1992. Dramatic changes in Fis levels upon nutrient upshift in Escherichia coli. J. Bacteriol. 174:8043-8056.
4. Broccoli, S., F. Rallu, P. Sanscartier, S. M. Cerritelli, R. J. Crouch, and M. Drolet. 2004. Effects of RNA polymerase modifications on transcription-induced supercoiling and associated R-loop formation. Mol. Microbiol. 52:1769-1779.
5. Condon, C., C. Squires, and C. L. Squires. 1995. Control of rRNA transcription in Escherichia coli. Microbiol. Rev. 59:623-645.
6. Daniels, G. A., and M. Lieber. 1995. RNA:DNA complex formation upon transcription of immunoglobulin switch regions: implications for the mechanism and regulation of class switch recombination. Nucleic Acids Res. 23:5006-5011.
7. DiNardo, S., K. A. Voelkel, R. Sternglanz, A. E. Reynolds, and A. Wright. 1982. Escherichia coli DNA topoisomerase I mutants have compensatory mutations in DNA gyrase genes. Cell 31:43-51.
8. Drlica, K., and M. Snyder. 1978. Superhelical Escherichia coli DNA: relaxation by coumermycin. J. Mol. Biol. 120:145-154.
9. Drolet, M. 2006. Growth inhibition mediated by excess negative supercoiling: the interplay between transcription elongation, R-loop formation and DNA topology. Mol. Microbiol. 59:723-730.
10. Drolet, M., X. Bi, and L. F. Liu. 1994. Hypernegative supercoiling of the DNA template during transcription elongation in vitro. J. Biol. Chem. 269:2068-2074.
11. Drolet, M., P. Phoenix, R. Menzel, E. Massé, L. F. Liu, and R. J. Crouch. 1995. Overexpression of RNase H partially complements the growth defect of an Escherichia coli delta topA mutant: R-loop formation is a major problem in the absence of DNA topoisomerase I. Proc. Natl. Acad. Sci. USA 92:3526-3530.
12. Gellert, M., K. Mizuuchi, M. H. O'Dea, and H. A. Nash. 1976. DNA gyrase: an enzyme that introduces superhelical turns into DNA. Proc. Natl. Acad. Sci. US 73:3872-3876.
13. Gellert, M., M. H. O'Dea, T. Itoh, and J. Tomizawa. 1976. Novobiocin and coumermycin inhibit DNA supercoiling catalyzed by DNA gyrase. Proc. Natl. Acad. Sci. USA 73:4474-4478.
14. Hraiky, C., M. A. Raymond, and M. Drolet. 2000. RNase H overproduction corrects a defect at the level of transcription elongation during rRNA synthesis in the absence of DNA topoisomerase I in Escherichia coli. J. Biol. Chem. 275:11257-11263.
15. Huang, F. T., K. Yu, C. L. Hsieh, and M. R. Lieber. 2006. Downstream boundary of chromosomal R-loops at murine switch regions: implications for the mechanism of class switch recombination. Proc. Natl. Acad. Sci. USA 103:5030-5035.
16. Huertas, P., and A. Aguilera. 2003. Cotranscriptionally formed DNA:RNA hybrids mediate transcription elongation impairment and transcription-associated recombination. Mol. Cell 12:711-721.
17. Iost, I., and M. Dreyfus. 1995. The stability of Escherichia coli lacZ mRNA depends upon the simultaneity of its synthesis and translation. EMBO J. 14:3252-3261.
18. Kushner, S. R. 2005. mRNA decay and processing, p. 327-345. In N. P. Higgins (ed.), The bacterial chromosome. ASM Press, Washington, DC.
19. Leroy, A., N. F. Vanzo, S. Sousa, M. Dreyfus, and A. J. Carpousis. 2002. Function in Escherichia coli of the non-catalytic part of RNase E: role in the degradation of ribosome-free mRNA. Mol. Microbiol. 45:1231-1243.
20. Lewicki, B. T., T. Margus, J. Remme, and K. H. Nierhaus. 1993. Coupling of rRNA transcription and ribosomal assembly in vivo. Formation of active ribosomal subunits in Escherichia coli requires transcription of rRNA genes by host RNA polymerase which cannot be replaced by bacteriophage T7 RNA polymerase. J. Mol. Biol. 231:581-593.
21. Li, Y., and S. Altman. 2004. Polarity effects in the lactose operon of Escherichia coli. J. Mol. Biol. 339:31-39.
22. Liu, L. F., and J. C. Wang. 1987. Supercoiling of the DNA template during transcription. Proc. Natl. Acad. Sci. USA 84:7024-7027.
23. Lodge, J. K., T. Kazic, and D. E. Berg. 1989. Formation of supercoiling domains in plasmid pBR322. J. Bacteriol. 171:2181-2187.
24. Lopez, P. J., I. Marchand, O. Yarchuk, and M. Dreyfus. 1998. Translation inhibitors stabilize Escherichia coli mRNAs independently of ribosome protection. Proc. Natl. Acad. Sci. USA 95:6067-6072.
25. Lynch, A. S., and J. C. Wang. 1993. 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. 175:1645-1655.
26. Mackie, G. A. 1998. Ribonuclease E is a 5′-end-dependent endonuclease. Nature 395:720-723.
27. Mackie, G. A., B. C. Donly, and P. C. Wong. 1990. Coupled transcription-translation of ribosomal proteins, p. 191-211. In G. Spedding (ed.), Ribosomes and protein synthesis: a practical approach. IRL Press, Oxford, United Kingdom.
28. Massé, E., and M. Drolet. 1999. Relaxation of transcription-induced negative supercoiling is an essential function of Escherichia coli DNA topoisomerase I. J. Biol. Chem. 274:16654- 16658.
29. Massé, E., and M. Drolet. 1999. Escherichia coli DNA topoisomerase I inhibits R-loop formation by relaxing transcription-induced negative supercoiling. J. Biol. Chem. 274:16659-16664.
30. Massé, E., and M. Drolet. 1999. R-loop-dependent hypernegative supercoiling in Escherichia coli topA mutants preferentially occurs at low temperatures and correlates with growth inhibition. J. Mol. Biol. 294:321-332.
31. Massé, E., P. Phoenix, and M. Drolet. 1997. DNA topoisomerases regulate R-loop formation during transcription of the rrnB operon in Escherichia coli. J. Biol. Chem. 272:12816-12823.
32. Miller, J. H. 1992. A short course in bacterial genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
33. Phoenix, P., M. A. Raymond, E. Massé, and M. Drolet. 1997. Roles of DNA topoisomerases in the regulation of R-loop formation in vitro. J. Biol. Chem. 272:1473-1479.
34. Powell, B. S., M. P. Rivas, D. L. Court, Y. Nakamura, and C. L. Turnbough, Jr. 1994. Rapid confirmation of single copy lambda prophage integration by PCR. Nucleic Acids Res. 23:1278.
35. Pruss, G. J. 1985. DNA topoisomerase I mutants. Increased heterogeneity in linking number and other replicon-dependent changes in DNA supercoiling. J. Mol. Biol. 185:51-63.
36. Pruss, G. J., and K. Drlica. 1986. Topoisomerase I mutants: the gene on pBR322 that encodes resistance to tetracycline affects plasmid DNA supercoiling. Proc. Natl. Acad. Sci. USA 83:8952-8956.
37. Pruss, G. J., S. H. Manes, and K. Drlica. 1982. Escherichia coli DNA topoisomerase I mutants: increased supercoiling is corrected by mutations near gyrase genes. Cell 31:35-42.
38. Samul, R., and F. Leng. 2007. Transcription-coupled hypernegative supercoiling of plasmid DNA by T7 RNA polymerase in Escherichia coli topoisomerase I-deficient strains. J. Mol. Biol. 374:925-935.
39. Simons, R. W., F. Houman, and N. Kleckner. 1987. Improved single and multicopy lac-based cloning vectors for protein and operon fusions. Gene 53:85-96.
40. Spirito, F., and L. Bossi. 1996. Long-distance effect of downstream transcription on activity of the supercoiling-sensitive leu-500 promoter in a topA mutant of Salmonella typhimurium. J. Bacteriol. 178:7129-7137.
41. Sternglanz, R. S. DiNardo, K. A. Voelkel, Y. Nishimura, Y. Hirota, K. Becherer, L. Zumstein, and J. C. Wang. 1981. Mutations in the gene coding for Escherichia coli DNA topoisomerase I affect transcription and transposition. Proc. Natl. Acad. Sci. USA 78:2747-2751.
42. Stupina, V. A., and J. C. Wang. 2005. Viability of Escherichia coli topA mutants lacking DNA topoisomerase I. J. Biol. Chem. 280:355-360.
43. Tous, C., and A. Aguilera. 2007. Impairment of transcription elongation by R-loops in vitro. Biochem. Biophys. Res. Commun. 360:428-432.
44. Usongo, V., F. Nolent, P. Sanscartier, C. Tanguay, S. Broccoli, I. Baaklini, K. Drlica, and M. Drolet. 2008. Depletion of RNase HI activity in Escherichia coli lacking DNA topoisomerase I leads to defects in DNA supercoiling and segregation. Mol. Microbiol. 69:968-981.
45. Wei, Y., J. M. Lee, C. Richmond, F. R. Blattner, J. A. Rafalski, and R. A. LaRossa. 2001. High-density microarray-mediated gene expression profiling of Escherichia coli. J. Bacteriol. 183:545-556.
46. Yarchuk, O., N. Jacques, J. Guillerez, and M. Dreyfus. 1992. Interdependence of translation, transcription and mRNA degradation in the lacZ gene. J. Mol. Biol. 226:581-596.
47. Yu, K., F. Chedin, C. L. Hsieh, T. E. Wilson, and M. R. Lieber. 2003. R-loops at immunoglobulin class switch regions in the chromosomes of stimulated B cells. Nat. Immunol. 4:442-451.
48. Yu, K., D. Roy, M. Bayramyan, I. S. Haworth, and M. R. Lieber. 2005. Fine-structure analysis of activation-induced deaminase accessibility to class switch region R-loops. Mol. Cell. Biol. 25:1730-1736.
49. Zechiedrich, E. L., A. B. Khodursky, S. Bachellier, R. Schneider, D. Chen, D. M. Lilley, and N. R. Cozzarelli. 2000. Roles of topoisomerases in maintaining steady-state DNA supercoiling in Escherichia coli. J. Biol. Chem. 275:8103-8113.
50. Zhang, Y., J. Zhang, K. P. Hoeflich, M. Ikura, G. Qing, and M. Inouye. 2003. MazF cleaves cellular mRNAs specifically at ACA to block protein synthesis in Escherichia coli. Mol. Cell 12:913-923.
51. Zhang, Y., L. Zhu, J. Zhang, and M. Inouye. 2005. Characterization of ChpBK, an mRNA interferase from Escherichia coli. J. Biol. Chem. 280: 26080-26088.