Structural coupling between RNA polymerase composition and DNA supercoiling in coordinating transcription: A global role for the omega subunit?

mBio

Volumn 2, Issue 4, 2011, Pages

  Geertz, Marcel ^a,e   Travers, Andrew ^b,c   Mehandziska, Sanja ^a   Sobetzko, Patrick ^a   Janga, Sarath Chandra ^b,f   Shimamoto, Nobuo ^d   Muskhelishvilia, Georgi ^a  

^a JACOBS UNIVERSITY BREMEN   (Germany)

^b MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^c Ecole Normale Superieure de Cachan   (France)

^d NATIONAL INSTITUTE OF GENETICS   (Japan)

^e UNIVERSITY OF GENEVA   (Switzerland)

^f UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HOLOENZYME; PLASMID DNA; RNA POLYMERASE;

ARTICLE; BACTERIAL GROWTH; BACTERIUM MUTANT; CONTROLLED STUDY; DNA SUPERCOILING; ENZYME STRUCTURE; ENZYME SUBUNIT; ESCHERICHIA COLI; GENE IDENTIFICATION; GENETIC TRANSCRIPTION; IN VIVO STUDY; NONHUMAN; OMEGA CHAIN; PRIORITY JOURNAL; PROMOTER REGION;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 80052607370     PISSN: None     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00034-11     Document Type: Article

References (88)

1. Jeong KS, Ahn J, Khodursky AB. 2004. Spatial patterns of transcriptional activity in the chromosome of Escherichia coli. Genome Biol. 5:R86.
2. Peter BJ, et al. 2004. Genomic transcriptional response to loss of chromosomal supercoiling in Escherichia coli. Genome Biol. 5:R87.
3. Blot N, Mavathur R, Geertz M, Travers A, Muskhelishvili G. 2006. Homeostatic regulation of supercoiling sensitivity coordinates transcription of the bacterial genome. EMBO Rep. 7:710-715.
4. Balke VL, Gralla JD. 1987. Changes in the linking number of supercoiled DNA accompany growth transitions in Escherichia coli. J. Bacteriol. 169: 4499-4506.
5. Travers A, Muskhelishvili G. 2005. Bacterial chromatin. Curr. Opin. Genet. Dev. 15:507-514.
6. Browning DF, Grainger DC, Busby SJW. 2010. Effects of nucleoidassociated proteins on bacterial chromosome structure and gene expression. Curr. Opin. Microbiol. 13:773-780.
7. Dillon SC, Dorman CJ. 2010. Bacterial nucleoid-associated proteins, nucleoid structure and gene expression. Nat. Rev. Microbiol. 8:185-195.
8. Rimsky S, Travers A. 2011. Pervasive regulation of nucleoid structure and function by nucleoid-associated proteins. Curr. Opin. Microbiol. 14: 136-141.
9. Malik M, Bensaid A, Rouviere-Yaniv J, Drlica K. 1996. Histone-like proteinHUand bacterialDNAtopology: suppression of anHUdeficiency by gyrase mutations. J. Mol. Biol. 256:66-76.
10. Schneider R, Travers A, Kutateladze T, Muskhelishvili G. 1999. A DNA architectural protein couples cellular physiology and DNA topology in Escherichia coli. Mol. Microbiol. 34:953-964.
11. Travers A, Schneider R, Muskhelishvili G. 2001. DNA supercoiling and transcription in Escherichia coli-the FIS connection. Biochimie 83: 213-217.
12. Hatfield GW, Benham CJ. 2002. DNA topology-mediated control of global gene expression in Escherichia coli. Annu. Rev. Genet. 36:175-203.
13. Keane OM, Dorman C. 2003. The gyr genes of Salmonella enterica serovar Typhimurium are repressed by the factor for inversion stimulation, Fis. Mol. Gen. Genet. 270:56-65.
14. Travers A, Muskhelishvili G. 2005. DNA supercoiling-a global transcriptional regulator for enterobacterial growth? Nat. Rev. Microbiol. 3:157-169.
15. Cróinín TO, Dorman CJ. 2007. Expression of the Fis protein is sustained in late-exponential- and stationary-phase cultures of Salmonella enterica serovar Typhimurium grown in the absence of aeration. Mol. Microbiol. 66:237-251.
16. Weinstein-Fischer D, Altuvia S. 2007. Differential regulation of Escherichia coli topoisomerase I by Fis. Mol. Microbiol. 63:1131-1144.
17. Muskhelishvili G, Travers A. 2009. Intrinsic in vivo modulators: negative supercoiling and the constituents of the bacterial nucleoid, p 69-95. In Buc H, Strick T (ed), RNA polymerases as molecular motors. RSC Publishing, Cambridge, United Kingdom.
18. Berger M, et al. 2010. Coordination of genomic structure and transcription by the main bacterial nucleoid-associated protein HU. EMBO Rep. 11:59-64.
19. Menzel R, Gellert M. 1983. Regulation of the genes for E. coli DNA gyrase: homeostatic control of DNA supercoiling. Cell 34:105-113.
20. González-Gil G, Kahmann R, Muskhelishvili G. 1998. Regulation of crp transcription by oscillation between distinct nucleoprotein complexes. EMBO J. 17:2877-2885.
21. Schneider R, Travers A, Muskhelishvili G. 2000. The expression of the Escherichia coli fis gene is strongly dependent on the superhelical density of DNA. Mol. Microbiol. 38:167-175.
22. Hulton CS, et al. 1990. Histone-like protein H1 (H-NS), DNA supercoiling, and gene expression in bacteria. Cell 63:631-642.
23. Drlica K. 1992. Control of bacterial DNA supercoiling. Mol. Microbiol. 6:425-433.
24. Dorman CJ, Deighan P. 2003. Regulation of gene expression by histonelike proteins in bacteria. Curr. Opin. Genet. Dev. 13:179-184.
25. Dame RT. 2005. The role of nucleoid-associated proteins in the organization and compaction of bacterial chromatin. Mol. Microbiol. 56: 858-870.
26. Deng S, Stein RA, Higgins NP. 2005. Organization of supercoil domains and their reorganization by transcription. Mol. Microbiol. 57:1511-1521.
27. Hardy CD, Cozzarelli NR. 2005. A genetic selection for supercoiling mutants of Escherichia coli reveals proteins implicated in chromosome structure. Mol. Microbiol. 57:1636-1652.
28. Kar S, et al. 2006. Right-handed DNA supercoiling by an octameric form of histone-like protein HU: modulation of cellular transcription. J. Biol. Chem. 281:40144-40153.
29. Ogata Y, et al. 1997. Heat shock-induced excessive relaxation of DNA in Escherichia coli mutants lacking the histone-like protein HU. Biochim. Biophys. Acta 1353:298-306.
30. Weinstein-Fischer D, Elgrably-Weiss M, Altuvia S. 2000. Escherichia coli response to hydrogen peroxide: a role for DNA supercoiling, topoisomerase I and Fis. Mol. Microbiol. 35:1413-1420.
31. Kar S, Edgar R, Adhya S. 2005. Nucleoid remodeling by an altered HU protein: reorganization of the transcription program. Proc. Natl. Acad. Sci. U. S. A. 102:16397-16402.
32. Marr C, Geertz M, Hütt MT, Muskhelishvili G. 2008. Dissecting the logical types of network control in gene expression profiles. BMC Syst. Biol. 2:18.
33. Dorman CJ. 1996. Flexible response: DNA supercoiling, transcription and bacterial adaptation to environmental stress. Trends Microbiol. 4:214-216.
34. Tse-Dinh YC, Qi H, Menzel R. 1997. DNA supercoiling and bacterial adaptation: thermotolerance and thermoresistance. Trends Microbiol. 5:323-326.
35. Cheung KJ, Badarinarayana V, Selinger DW, Janse D, Church GM. 2003. A microarray-based antibiotic screen identifies a regulatory role for supercoiling in the osmotic stress response of Escherichia coli. Genome Res. 13:206-215.
36. Sonnenschein N, Geertz M, Muskhelishvili G, Hütt M-T. 2011. Analog regulation of metabolic demand. BMC Syst. Biol. 5:40.
37. Hsieh LS, Rouviere-Yaniv J, Drlica K. 1991. Bacterial DNA supercoiling and ATP/ADP ratio: changes associated with salt shock. J. Bacteriol. 173: 3914-3917.
38. van Workum M, et al. 1996. DNA supercoiling depends on the phosphorylation potential in Escherichia coli. Mol. Microbiol. 20:351-360.
39. Snoep JL, van der Weijden CC, Andersen HW, Westerhoff HV, Jensen PR. 2002. DNA supercoiling in Escherichia coli is under tight and subtle homeostatic control, involving gene-expression and metabolic regulation of both topoisomerase I and DNA gyrase. Eur. J. Biochem. 269: 1662-1669.
40. Muskhelishvili G, Sobetzko P, Geertz M, Berger M. 2010. General organisational principles of the transcriptional regulation system: a tree or a circle? Mol. Biosyst. 6:662- 676.
41. Ishihama A. 2000. Functional modulation of Escherichia coli RNA polymerase. Annu. Rev. Microbiol. 54:499-518.
42. Weber H, Polen T, Heuveling J, Wendisch VF, Hengge R. 2005. Genome-wide analysis of the general stress response network in Escherichia coli: sigmaS-dependent genes, promoters, and sigma factor selectivity. J. Bacteriol. 187:1591-1603.
43. S (RpoS) and the general stress response in Escherichia coli. Res. Microbiol. 160:667- 676.
44. Kusano S, Ding Q, Fujita N, Ishihama A. 1996. Promoter selectivity of Escherichia coli RNA polymerase Eσ70 and Eσ38 holoenzymes. Effect of DNA supercoiling. J. Biol. Chem. 271:1998-2004.
45. S-dependent transcription in Escherichia coli. Mol. Microbiol. 48:561-571.
46. Mukherjee K, Nagai H, Shimamoto N, Chatterji D. 1999. GroEL is involved in activation of Escherichia coli RNA polymerase devoid of the ω subunit in vivo. Eur. J. Biochem. 266:228-235.
47. Minakhin L, et al. 2001. Bacterial RNA polymerase subunit omega and eukaryotic RNA polymerase subunit RPB6 are sequence, structural, and functional homologs and promote RNA polymerase assembly. Proc. Natl. Acad. Sci. U. S. A. 98:892-897.
48. S and σ70 of Escherichia coli to utilize promoters containing half or full UP-element sites. Mol. Microbiol. 55:250-260.
49. Salgado H, et al. 2006. Regulon DB (version 5.0): Escherichia coli K-12 transcriptional regulatory network, operon organization, and growth conditions. Nucleic Acids Res. 34 (database issue):D394-D397.
50. Liu LF, Wang JC. 1987. Supercoiling of the DNA template during transcription. Proc. Natl. Acad. Sci. U. S. A. 84:7024-7027.
51. Cabrera JE, Cagliero C, Quan S, Squires CL, Jin DJ. 2009. Active transcription of rRNA operons condenses the nucleoid in Escherichia coli: examining the effect of transcription on nucleoid structure in the absence of transertion. J. Bacteriol. 191:4180-4185.
52. Arnold GF, Tessman I. 1988. Regulation of DNA superhelicity by rpoB mutations that suppress defective Rho-mediated transcription termination in Escherichia coli. J. Bacteriol. 170:4266-4271.
53. Drlica K, Franco RJ, Steck TR. 1988. Rifampin and rpoB mutations can alter DNA supercoiling in Escherichia coli. J. Bacteriol. 170:4983-4985.
54. S subunit of RNA polymerase. Mol. Microbiol. 63:1296-1306.
55. Shin M, et al. 2005. DNA looping-mediated repression by histone-like protein H-NS: specific requirement of E σ70 as a cofactor for looping. Genes Dev 19:2388-2398.
56. Cheng B, Zhu C-X, Ji C, Ahumada A, Tse-Dinh Y-C. 2003. Direct interaction between Escherichia coli RNA polymerase and the zinc ribbon domains of DNA topoisomerase. I. J. Biol. Chem. 278:30705-30710.
57. Gupta R, China A, Manjunatha UH, Ponnanna NM, Nagaraja V. 2006. A complex of DNA gyrase and RNA polymerase fosters transcription in Mycobacterium smegmatis. Biochem. Biophys. Res. Commun. 4:1141-1145.
58. Hu P, et al. 2009. Global functional atlas of Escherichia coli encompassing previously uncharacterized proteins. PLoS Biol. 7:e96.
59. 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.
60. Jin DJ, Cabrera JE. 2006. Coupling the distribution of RNA polymerase to global gene regulation and the dynamic structure of the bacterial nucleoid in Escherichia coli. J. Struct. Biol. 156:284-291.
61. Mathew R, Chatterji D. 2006. The evolving story of the omega subunit of bacterial RNA polymerase. Trends Microbiol. 14:450-455.
62. Jishage M, Kvint K, Shingler V, Nyström T. 2002. Regulation of sigma factor competition by the alarmone ppGpp. Genes Dev. 16:1260-1270.
63. Magnusson LU, Farewell A, Nyström T. 2005. pp Gpp: a global regulator in Escherichia coli. Trends Microbiol. 13:236-242.
64. Gentry DR, Xiao H, Burgess R, Cashel M. 1991. The omega subunit of Escherichia coli K-12 RNA polymerase is not required for stringent RNA control in vivo. J. Bacteriol. 12:3901-3903.
65. Chatterji D, Ogawa Y, Shimada T, Ishihama A. 2007. The role of RNA polymerase omega subunit in expression of the relA gene in Escherichia coli. FEMS Microbiol. Lett. 267:51-55.
66. Vrentas CE, Gaal T, Ross W, Ebright RH, Gourse RL. 2005. Response of RNA polymerase to ppGpp: requirement for the omega subunit and relief of this requirement by DksA. Genes Dev. 19:2378-2387.
67. Potrykus K, et al. 2006. Antagonistic regulation of Escherichia coli ribosomal RNA rrnB P1 promoter activity by GreA and DksA. J. Biol. Chem. 22:15238-15248.
68. Magnusson LU, Gummesson B, Joksimovi P, Farewell A, Nyström T. 2007. Identical, independent and opposing roles of pp Gpp and DksA in Escherichia coli. J. Bacteriol. 189:5193-5202.
69. Gaal T, Mandel MJ, Silhavy TJ, Gourse RL. 2006. Crl facilitates RNA polymerase holoenzyme formation. J. Bacteriol. 188:7966-7970.
70. S activity and levels. EMBO J. 26:1569-1578.
71. Flores N, et al. 2008. New insights into the role of sigma factor RpoS revealed in Escherichia coli strains lacking the phosphoenolpyruvate: carbohydrate phosphotransferase system. J. Mol. Microbiol. Biotechnol. 14:176-192.
72. Colland F, Barth M, Hengge-Aronis R, Kolb A. 2000. Sigma factor selectivity of Escherichia coli RNA polymerase: role for CRP, IHF and lrp transcription factors. EMBO J. 19:3028-3037.
73. Rochman M, Aviv M, Glaser G, Muskhelishvili G. 2002. Promoter protection by a transcription factor acting as a local topological homeostat. EMBO Rep. 3:355-360.
74. Xu J, Johnson RC. 1995. Identification of genes negatively regulated by Fis: Fis and RpoS comodulate growth-phase-dependent gene expression in Escherichia coli. J. Bacteriol. 177:938-947.
75. Gummesson B, et al. 2009. Increased RNA polymerase availability directs resources towards growth at the expense of maintenance. EMBO J. 28: 2209-2219.
76. Zhou YN, Jin DJ. 1998. The rpoB mutants destabilizing initiation complexes at stringently controlled promoters behave like stringent RNA polymerases in Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 95: 2908-2913.
77. Crozat E, Philippe N, Lenski RE, Geiselmann J, Schneider D. 2005. Long-term experimental evolution in Escherichia coli. XII. DNA topology as a key target of selection. Genetics 169:523-532.
78. Magnusson LU, Nystrom T, Farewell A. 2003. Underproduction of σ70 mimics a stringent response. A proteome approach. J. Biol. Chem. 278: 968-973.
79. S promoter selectivity in Escherichia coli. Mol. Microbiol. 59: 1037-1051.
80. Cairns BR. 2009. The logic of chromatin architecture and remodeling at promoters. Nature 461:193-198.
81. Amann E, Brosius J. 1985. ATG vectors for regulated high-level expression of cloned genes in Escherichia coli. Gene 40:183-190.
82. Schneider R, Travers A, Muskhelishvili G. 1997. Fis modulates growth phase-dependent topological transitions of DNA in Escherichia coli. Mol. Microbiol. 26:519-530.
83. Sternbach H, Engelhardt R, Lezius AG. 1975. Rapid isolation of highly active RNA polymerase from Escherichia coli and its subunits by matrixbound heparin. Eur. J. Biochem. 60:51-55.
84. Hager DA, Jin DJ, Burgess RR. 1990. Use of Mono Q high-resolution ion-exchange chromatography to obtain highly pure and active Escherichia coli RNA polymerase. Biochemistry 29:7890-7894.
85. Keller W. 1975. Determination of the number of superhelical turns in simian virus 40 DNA by gel electrophoresis. Proc. Natl. Acad. Sci. U. S. A. 72:4876-4880.
86. Saeed AI, et al. 2003. TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34:374-378.
87. Cleveland W, Devlin S. 1988. Locally weighted linear regression: an approach to regression analysis by local fitting. J. Am. Stat. Assoc. 83: 596-609.
88. Pan W. 2002. A comparative review of statistical methods for discovering differentially expressed genes in replicated microarray experiments. Bioinformatics 18:546-554.