Regulation of rRNA transcription is remarkably robust: FIS compensates for altered nucleoside triphosphate sensing by mutant RNA polymerases at Escherichia coli rrn P1 promoters

Journal of Bacteriology

Volumn 182, Issue 7, 2000, Pages 1969-1977

  Bartlett, Michael S ^a,b   Gaal, Tamas ^a   Ross, Wilma ^a   Gourse, Richard L ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MUTANT PROTEIN; NUCLEOSIDE TRIPHOSPHATE; RIBOSOME RNA; RNA POLYMERASE; TRANSCRIPTION FACTOR;

ARTICLE; CONTROLLED STUDY; DNA SEQUENCE; ESCHERICHIA COLI; GROWTH RATE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; RNA SYNTHESIS; RNA TRANSCRIPTION; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; WESTERN BLOTTING;

CARRIER PROTEINS; CELL DIVISION; DNA-DIRECTED RNA POLYMERASES; ENZYME ACTIVATION; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; FACTOR FOR INVERSION STIMULATION PROTEIN; GENE EXPRESSION REGULATION, BACTERIAL; GENES, RRNA; INTEGRATION HOST FACTORS; KINETICS; LAC OPERON; MUTATION; PROMOTER REGIONS (GENETICS); PROTEIN BINDING; RNA, BACTERIAL; RNA-BINDING PROTEINS; RRNA OPERON; THERMODYNAMICS; TRANSCRIPTION, GENETIC;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; NEGIBACTERIA; PROKARYOTA;

EID: 0034118883     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.182.7.1969-1977.2000     Document Type: Article

References (45)

1. Afflerbach, H., O. Schroder, and R. Wagner. 1998. Effects of the Escherichia coli DNA-binding protein H-NS on rRNA synthesis in vivo. Mol. Microbiol. 28:541-653.
2. Afflerbach, H., O. Schröder, and R. Wagner. 1999 Conformational changes of the upstream DNA mediated by H-NS and FIS regulate E. coli rrnB P1 promoter activity. J. Mol. Biol. 286:339-353.
3. Appleman, J. A., W. Ross, J. Salomon, and R. L. Gourse. 1998. Activation of Escherichia coli rRNA transcription by FIS during a growth cycle. J. Bacteriol. 180:1525-1532.
4. Bachmann, B. J. 1987. Derivatives and genotypes of some mutant derivatives of Escherichia coli K-12, p. 1190-1219. In F. C. Neidhardt et al. (ed)., Escherichia coli and Salmonella typhimurium: cellular and molecular biology, vol. 2. American Society for Microbiology, Washington, D.C.
5. Bali, 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.
6. Bartlett, M. S., and R. L. Gourse. 1994. Growth rate-dependent control of the rrnB P1 core promoter in Escherichia coli. J. Bacteriol. 176:5560-5564.
7. Bartlett, M. S., T. Gaal, W. Ross, and R. L. Gourse. 1998. RNA polymerase mutants that destabilize RNA polymerase-promoter complexes alter NTP-sensing by rrn P1 promoters. J. Mol. Biol. 279:331-345.
8. Bokal, A. J., W. Ross, and R. L. Gourse. 1995. The transcriptional activator protein FIS: DNA interactions and cooperative interactions with RNA polymerase at the Escherichia coli rrnB P1 promoter. J. Mol. Biol. 245:197-207.
9. Bokal, A. J., W. Ross, T. Gaal, R. C. Johnson, and R. L. Gourse. 1997. Molecular anatomy of a transcription activation patch: FIS-RNA polymerase interactions at the Escherichia coli rrnB P1 promoter. EMBO J. 16:154-162.
10. Cashel, M., D. R. Gentry, V. J. Hernandez, and D. Vinella. 1996. The stringent response, p. 1458-1496. In F. C. Neidhardt et al. (ed.), Escherichia coli and Salmonella typhimurium: cellular and molecular biology, vol. 1. American Society for Microbiology, Washington, D.C.
11. Condon, C., C. Squires, and C. L. Squires. 1995. Control of rRNA transcription in Escherichia coli. Microbiol. Rev. 59:623-645.
12. Dong, H., L. A. Kirsebom, and L. Nilsson. 1996. Growth rate regulation of 4.5 S RNA and M1 RNA, the catalytic subunit of Escherichia coli RNase P. J. Mol. Biol. 261:303-308.
13. Emilsson. V., and L. Nilsson. 1995. Factor for inversion stimulation-dependent growth rate regulation of serine and threonine tRNA species. J. Biol. Chem. 270:16610-16614.
14. Estrem, S. T., W. Ross, T. Gaal, Z. W. S. Chen, W. Niu, R. H. Ebright, and R. L. Gourse. 1999. Bacterial promoter architecture: subsite structure of UP elements and interactions with the C-terminal domain of the RNA polymerase alpha subunit. Genes Dev. 13:2134-2147.
15. Gaal, T., M. S. Bartlett, W. Ross, C. L. Turnbough, Jr., and R. L. Gourse. 1997. Transcription regulation by initiating NTP concentration: rRNA synthesis in bacteria. Science 278:2092-2097.
16. Gosink, K. K., T. Gaal, A. J. Bokal IV, and R. L. Gourse. 1996. A positive control mutant of the transcription activator protein FIS. J. Bacteriol. 178: 5182-5187.
17. Gourse, R. L., H. A. de Boer, and M. Nomura. 1986. DNA determinants of rRNA synthesis in E. coli: growth rate dependent regulation, feedback inhibition, upstream activation, antitermination. Cell 44:197-205.
18. Gourse, R. L., T. Gaal, S. E. Aiyar, M. M. Barker, S. T. Estrem, C. A. Hirvonen, and W. Ross. 1998. Strength and regulation without transcription factors: lessons from bacterial rRNA promoters. Cold Spring Harbor Symp. Quant. Biol. 63:131-139.
19. Gourse, R. L., T. Gaal, M. S. Bartlett, J. A. Appleman, and W. Ross. 1996. rRNA transcription and growth rate-dependent regulation of ribosome synthesis in Escherichia coli. Annu. Rev. Microbiol. 50:645-677.
20. Jinks-Robertson, S., and M. Nomura. 1987. Ribosomes and tRNA, p. 1358-1385. In F. C. Neidhardt et al. (ed.), Escherichia coli and Salmonella typhimurium: cellular and molecular biology, vol. 2. American Society for Microbiology, Washington, D.C.
21. Jinks-Robertson, S., R. L. Gourse, and M. Nomura. 1983. Expression of rRNA and tRNA genes in Escherichia coli: evidence for feedback regulation by products of rRNA operons. Cell 33:865-876.
22. Johnson, R. C., C. A. Ball, D. Pfeffer, and M. L. Simon. 1988. Isolation of the jene encoding the Hin recombinational enhancer binding protein. Proc. Natl. Acad. Sci. USA 85:3484-3488.
23. Keener, J., and M. Nomura. 1996. Regulation of ribosome synthesis, p. 1417-1431. In F. C. Neidhardt et al. (ed.), Escherichia coli and Salmonella typhimurium: cellular and molecular biology, vol. 1. American Society for Microbiology, Washington, D.C.
24. Little, J. W., D. P. Shepley, and D. W. West. 1999. Robustness of a gene regulatory circuit. EMBO J. 18:4299-4307.
25. Miller, J. H. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N. Y.
26. Muskhelishvili, G., M. Buckle, H. Heumann, R. Kahmann, and A. A. Travers. 1997. FIS activates sequential steps during transcription initiation at a stable RNA promoter. EMBO J. 16:3655-3665.
27. Nilsson, L., and V. Emilsson. 1994. Factor for inversion stimulation-dependent growth rate regulation of individual tRNA species in Escherichia coli. J. Biol. Chem. 269:9460-9465.
28. Nilsson, L., A. Vanet, E. Vijgenboom, and L. Bosch. 1990. The role of FIS in trans activation of stable RNA operons of E. coli. EMBO J. 9:727-734.
29. Nilsson, L., H. Verbeek, E. Vijgenboom, C. van Drunen, A. Vanet, and L. Bosch. 1992. FIS-dependent trans activation of stable RNA operons of Escherichia coli under various growth conditions. J. Bacteriol. 174:921-929.
30. Ninnemann, O., C. Koch, and R. Kahmann. 1992. The E. coli Fis promoter is subject to stringent control and autoregulation. EMBO J. 11:1075-1083.
31. Osuna, R., D. Lienau, K. T. Hughes, and R. C. Johnson. 1995. Sequence, regulation, and functions of fis in Salmonella typhimurium. J. Bacteriol. 177:2021-2032.
32. Pokholok, D. K., M. Redlak, C. L. Turnbough, Jr., S. Dylla, and W. M. Holmes. 1999. Multiple mechanisms are used for growth rate and stringent control of leuV transcriptional initiation in Escherichia coli. J. Bacteriol. 181:5771-5782.
33. Pratt, T. S., T. Steiner, L. S. Feldman, K. A. Walker, and R. Osuna. 1997. Deletion analysis of the fis promoter region in Escherichia coli: antagonistic effects of integration host factor and Fis. J. Bacteriol. 179:6367-6377.
34. Rao, L., W. Ross, J. A. Appleman, T. Gaal, S. Leirmo, P. J. Schlax, M. T. Record, Jr., and R. L. Gourse. 1994. Factor independent activation of rrnB P1. An "extended" promoter with an upstream element that dramatically increases promoter strength. J. Mol. Biol. 235:1421-1435.
35. Ross, W., K. K. Gosink, J. Salomon, K. Igarashi, C. Zou, A. Ishihama, K. Severinov, and R. L. Gourse. 1993. A third recognition element in bacterial promoters: DNA binding by the alpha subunit of RNA polymerase. Science 262:1407-1413.
36. Ross, W., J. Salomon, W. M. Holmes, and R. L. Gourse. 1999. Activation of Escherichia coli leuV transcription by FIS. J. Bacteriol. 181:3864-3868.
37. Ross, W., J. F. Thompson, J. T. Newlands, and R. L. Gourse. 1990. E. coli Fis protein activates ribosomal RNA transcription in vitro and in vivo. EMBO J. 9:3733-3742.
38. Rowley, K. B., R. M. Elford, I. Roberts, and W. M. Holmes. 1993. In vivo regulatory responses of four Escherichia coli operons which encode leucyl-tRNAs. J. Bacteriol. 175:1309-1315.
39. Sander, P., W. Langert, and K. Mueller. 1993. Mechanisms of upstream activation of the rrnD promoter P1 of Escherichia coli. J. Biol. Chem. 268: 16907-16916.
40. Sarmientos, P., and M. Cashel. 1983. Carbon starvation and growth rate-dependent regulation of the Escherichia coli ribosomal RNA promoters: differential control of dual promoters. Proc. Natl. Acad. Sci. USA 80:7010-7013.
41. Schneider, R., A. Travers, and G. Muskhelishvili. 1997. FIS modulates growth phase-dependent topological transitions of DNA in Escherichia coli. Mol. Microbiol. 26:519-530.
42. Singer, M., T. A. Baker, C. Schnitzler, S. M. Deischel, M. Goel, W. Dove, K. J. Jaacks, A. D. Grossman, J. W. Erickson, and C. A. Gross. 1989. A collection of strains containing genetically linked alternating antibiotic resistance elements for genetic mapping of Escherichia coli. Microbiol. Rev. 53:1-24.
43. Wackwitz, B., J. Bongaerts, S. D. Goodman, and G. Unden. 1999. Growth phase-dependent regulation of nuoA-N expression in Escherichia coli K-12 by the Fis protein: upstream binding sites and bioenergetic significance. Mol. Gen. Genet. 262:876-883.
44. Walker, K. A., C. L. Atkins, and R. Osuna. 1999. Functional determinants of the Escherichia coli fis promoter: roles of -35, -10, and transcription initiation regions in the response to stringent control and growth phase-dependent regulation. J. Bacteriol. 181:1269-1280.
45. Zacharias, M., H. U. Goringer, and R. Wagner. 1992. Analysis of the Fis-dependent and Fis-independent transcription activation mechanisms of the Escherichia coli ribosomal RNA P1 promoter. Biochemistry 31:2621-2628.