Regulation of transcription elongation and termination

Biomolecules

Volumn 5, Issue 2, 2015, Pages 1063-1078

  Washburn, Robert S ^a   Gottesman, Max E ^a  

^a NewYork Presbyterian Hospital   (United States)

Author keywords

Nus factors; Transcription antitermination; Transcription elongation; Transcription pausing; Transcription termination; Transcription translation coupling

Indexed keywords

BICOZAMYCIN; DNA HELICASE; ESCHERICHIA COLI PROTEIN; TRANSCRIPTION FACTOR;

BACILLUS SUBTILIS; CARBOXY TERMINAL SEQUENCE; ESCHERICHIA COLI; GENE EXPRESSION; GENETIC ASSOCIATION; NONHUMAN; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN LOCALIZATION; REVIEW; RNA BINDING; RNA SYNTHESIS; SEQUENCE ANALYSIS; TRANSCRIPTION ELONGATION; TRANSCRIPTION REGULATION; TRANSCRIPTION TERMINATION; AMINO ACID SEQUENCE; CHEMISTRY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS;

AMINO ACID SEQUENCE; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; MOLECULAR SEQUENCE DATA; TRANSCRIPTION ELONGATION, GENETIC; TRANSCRIPTION FACTORS; TRANSCRIPTION TERMINATION, GENETIC;

EID: 85012075682     PISSN: None     EISSN: 2218273X     Source Type: Journal    
DOI: 10.3390/biom5021063     Document Type: Review

References (82)

1. Mejia, Y. X.; Nudler, E.; Bustamante, C. Trigger loop folding determines transcription rate of Escherichia coli's RNA polymerase. Proc. Natl. Acad. Sci. USA 2015, 112, 743-774.
2. Kireeva, M. L.; Kashlev, M. Mechanism of sequence-specific pausing of bacterial RNA polymerase. Proc. Natl. Acad. Sci. USA 2009, 106, 8900-8905.
3. Bochkareva, A.; Yuzenkova, Y.; Tadigotla, V. R.; Zenkin, N. Factor-independent transcription pausing caused by recognition of the RNA-DNA hybrid sequence. EMBO J. 2012, 31, 630-639.
4. Vvedenskaya, I. O.; Vahedian-Movahed, H.; Bird, J. G.; Knoblauch, J. G.; Goldman, S. R.; Zhang Y.; Ebright, R. H.; Nickels, B. E. Transcription. Interactions between RNA polymerase and the "core recognition element" counteract pausing. Science 2014, 344, 1285-1289.
5. Larson, M. H.; Mooney, R. A.; Peters, J. M.; Windgassen, T.; Nayak, D.; Gross, C. A.; Block, S. M.; Greenleaf, W. J.; Landick, R.; Weissman, J. S. A pause sequence enriched at translation start sites drives transcription dynamics in vivo. Science 2014, 344, 1042-1047.
6. Purdue, S. A.; Roberts, J. W. 70-dependent transcription pausing in Escherichia coli. J. Mol. Biol. 2011, 412, 782-792.
7. Zhilina, E.; Esyunina, D.; Brodolin, K.; Kulbachinskiy, A. Structural transitions in the transcription elongation complexes of bacterial RNA polymerase during α-dependent pausing. Nucleic Acids Res. 2012, 40, 3078-3091.
8. Wade, J. T.; Struhl, K. Association of RNA polymerase with transcribed regions in Escherichia coli. Proc. Natl. Acad. Sci. USA 2004, 101, 17777-17782.
9. Nedialkov, Y. A.; Opron, K.; Assaf, F.; Artsimovitch, I.; Kireeva, M. L.; Kashlev, M.; Cukier, R. I.; Nudler, E.; Burton, Z. F. The RNA polymerase bridge helix YFI motif in catalysis, fidelity and translocation. Biochim. Biophys. Acta 2013, 1829, 187-198.
10. Roberts, J. W. Termination factor for RNA synthesis. Nature 1969, 224, 1168-1174.
11. Peters, J. M.; Mooney, R. A.; Kuan, P. F.; Rowland, J. L.; Keles, S.; Landick, R. Rho directs widespread termination of intragenic and stable RNA transcription. Proc. Natl. Acad. Sci. USA 2009, 106, 15406-15411.
12. Opperman, T.; Richardson, J. P. Phylogenetic analysis of sequences from diverse bacteria with homology to the Escherichia coli Rho gene. J. Bacteriol. 1994, 176, 5033-5043.
13. Lowery-Goldhammer, C.; Richardson, J. P. An RNA-dependent nucleoside triphosphate phosphohydrolase (ATPase) associated with Rho termination factor. Proc. Natl. Acad. Sci. USA 1974, 71, 2003-2007.
14. Brennan, C. A.; Dombroski, A. J.; Platt, T. Transcription termination factor Rho is an RNA-DNA helicase. Cell 1987, 48, 945-952.
15. Skordalakes, E.; Berger, J. M. Structure of the Rho transcription terminator: Mechanism of mRNA recognition and helicase loading. Cell 2003, 114, 135-146.
16. Matsumoto, Y.; Shigesada, K.; Hirano, M.; Imai, M. Autogenous regulation of the gene for transcription termination factor Rho in Escherichia coli: Localization and function of its attenuators. J. Bacteriol. 1986, 166, 945-958.
17. Chen, C. Y.; Richardson, J. P. Sequence elements essential for Rho-dependent transcription termination at tR1. J. Biol. Chem. 1987, 262, 11292-11299.
18. Steinmetz, E. J.; Platt, T. Evidence supporting a tethered tracking model for helicase activity of Escherichia coli Rho factor. Proc. Natl. Acad. Sci. USA 1994, 91, 1401-1405.
19. Koslover, D. J.; Fazal, F. M.; Mooney, R. A.; Landick, R.; Block, S. M. Binding and translocation of termination factor Rho studied at the single-molecule level. J. Mol. Biol. 2012, 423, 664-676.
20. Hart, C. M.; Roberts, J. W. Rho-dependent transcription termination. Characterization of the requirement for cytidine in the nascent transcript. J. Biol. Chem. 1991, 266, 24140-24148.
21. Richardson, J. P. Activation of Rho protein ATPase requires simultaneous interaction at two kinds of nucleic acid-binding sites. J. Biol. Chem. 1982, 257, 5760-5766.
22. Skordalakes, E.; Berger, J. M. Structural insights into RNA-dependent ring closure and ATPase activation by the Rho termination factor. Cell 2006, 127, 553-564.
23. Rabhi, M.; Gocheva, V.; Jacquinot, F.; Lee, A.; Margeat, E.; Boudvillain, M. Mutagenesis-based evidence for an asymmetric configuration of the ring-shaped transcription termination factor Rho. J. Mol. Biol. 2011, 405, 497-518.
24. Epshtein, V.; Dutta, D.; Wade, J.; Nudler, E. An allosteric mechanism of Rho-dependent transcription termination. Nature 2010, 463, 245-249.
25. Park, J. S.; Roberts, J. W. Role of DNA bubble rewinding in enzymatic transcription termination. Proc. Natl. Acad. Sci. USA 2006, 103, 4870-4875.
26. Wu, S.-Y.; Platt, T. Transcriptional arrest of yeast RNA polymerase II by Escherichia coli Rho protein in vitro. Proc. Natl. Acad. Sci. USA 1993, 90, 6606-6610.
27. Alifano, P.; Rivellini, F.; Limauro, D. A consensus motif common to all Rho-dependent prokaryotic transcription terminators. Cell 1991, 64, 553-563.
28. Zalatan, F.; Platt, T. Effects of decreased cytosine content on Rho interaction with the Rho-dependent terminator trp T' in Escherichia coli. J. Biol. Chem. 1992, 267, 19082-19088.
29. Morgan, W. D.; Bear, D. G.; von Hippel, P. H. Rho-dependent termination of transcription. I. Identification and characterization of termination sites for transcription from the bacteriophage PR promoter. J. Biol. Chem. 1983, 258, 9553-9564.
30. Sullivan, S. L.; Gottesman, M. E. Requirement for E. coli NusG protein in factor-dependent transcription termination. Cell 1992, 68, 989-994.
31. Li, J.; Mason, S. W.; Greenblatt, J. Elongation factor NusG interacts with termination factor Rho to regulate termination and antitermination of transcription. Genes Dev. 1993, 7, 161-172.
32. Burns, C. M.; Richardson, L. V.; Richardson, J. P. Combinatorial effects of NusA and NusG on transcription elongation and Rho-dependent termination in Escherichia coli. J. Mol. Biol. 1998, 278, 307-316.
33. Nehrke, K. W.; Zalatan, F.; Platt, T. NusG alters Rho-dependent termination of transcription in vitro independent of kinetic coupling. Gene Expr. 1993, 3, 119-133.
34. Washburn, R. S.; Jin, D. J.; Stitt, B. L. The mechanism of early transcription termination by Rho026. J. Mol. Biol. 1996, 260, 347-358.
35. Nehrke, K. W.; Platt, T. A quaternary transcription termination complex. Reciprocal stabilization by Rho factor and NusG protein. J. Mol. Biol. 1994, 243, 830-839.
36. Mooney, R. A.; Davis, S. E.; Peters, J. M.; Rowland, J. L.; Ansari, A. Z.; Landick, R. Regulator trafficking on bacterial transcription units in vivo. Mol. Cell. 2009, 33, 97-108.
37. Kalyani, B. S.; Muteeb, G.; Qayyum, M. Z.; Sen, J. Interaction with the nascent RNA is a prerequisite for the recruitment of Rho to the transcription elongation complex in vitro. J. Mol. Biol. 2011, 413, 548-560.
38. Cardinale, C. J.; Washburn, R. S.; Tadigotla, V. R.; Brown, L. M.; Gottesman, M. E.; Nudler, E. Termination factor Rho and its cofactors NusA and NusG silence foreign DNA in E. coli. Science 2008, 320, 935-938.
39. Washburn, R. S.; Gottesman, M. E. Transcription termination maintains chromosome integrity. Proc. Natl. Acad. Sci. USA 2011, 108, 792-797.
40. Washburn, R. S.; Hashem, Y.; Sun, M.; Shen, B.; Harvey, S.; Frank, J.; Gottesman, M. E. NusG and RelA couple and tmRNA uncouples transcription with translation in E. coli. Unpublished work, 2015.
41. Harinarayanan, R.; Gowrishankar, J. Host factor titration by chromosomal R-loops as a mechanism for runaway plasmid replication in transcription termination-defective mutants of Escherichia coli. J. Mol. Biol. 2003, 332, 31-46.
42. Leela, J. K.; Syeda, A. H.; Anupama, K.; Gowrishankar, J. Rho-dependent transcription termination is essential to prevent excessive genome-wide R-loops in Escherichia coli. Proc. Natl. Acad. Sci. USA 2013, 110, 258-263.
43. Tran, L.; van Baarsel, J. A.; Washburn, R. S.; Gottesman, M. E.; Miller, J. H. Single-gene deletion mutants of Escherichia coli with altered sensitivity to bicyclomycin, an inhibitor of transcription termination factor Rho. J. Bacteriol. 2011, 193, 2229-2235.
44. Nichols, R. J.; Sen, S.; Choo, Y. J.; Beltrao, P.; Zietek, M.; Chaba, R.; Lee, S.; Kazmierczak, K. M.; Lee, K. J.; Wong, A.; et al. Phenotypic landscape of a bacterial cell. Cell 2011, 144, 143-156.
45. Dutta, D.; Shatalin, K.; Epshtein, V.; Gottesman, M. E.; Nudler, E. Linking RNA polymerase backtracking to genome instability in E. coli. Cell 2011, 146, 533-543.
46. Peters, J. M.; Mooney, R. A.; Grass, J. A.; Jessen, E. D.; Tran, F.; Landick, R. Rho and NusG suppress pervasive antisense transcription in Escherichia coli. Genes Dev. 2012, 26, 2621-2633.
47. Jin, D. J.; Burgess, R. R.; Richardson, J. P.; Gross, C. A. Termination efficiency at Rho-dependent terminators depends on kinetic coupling between RNA polymerase and Rho. Proc. Natl. Acad. Sci. USA 1992, 89, 1453-1457.
48. Navarre, W. W.; Porwollik, S.; Wang, Y.; McClelland, M.; Rosen, H.; Libby, S. J.; Fang, F. C. Selective silencing of foreign DNA with low GC content by the H-NS protein in Salmonella. Science 2006, 313, 236-238.
49. Mooney, R. A.; Schweimer, K.; Rösch, P.; Gottesman, M.; Landick, R. Two structurally independent domains of E. coli NusG create regulatory plasticity via distinct interactions with RNA polymerase and regulators. J. Mol. Biol. 2009, 391, 341-358.
50. Svetlov, V.; Nudler, E. Clamping the clamp of RNA polymerase. EMBO J. 2011, 30, 1190-1191.
51. Herbert, K. M.; Zhou, J.; Mooney, R. A.; la Porta, A.; Landick, R.; Block, S. M. E. coli NusG inhibits backtracking and accelerates pause-free transcription by promoting forward translocation of RNA polymerase. J. Mol. Biol. 2010, 399, 17-30.
52. Burmann, B. M.; Schweimer, K.; Luo, X.; Wahl, M. C.; Stitt, B. L.; Gottesman, M. E.; Rösch, P. A NusE: NusG complex links transcription and translation. Science 2010, 328, 501-504.
53. Burmann, B. M.; Knauer, S. H.; Sevostyanova, A.; Schweimer, K.; Mooney, R. A.; Landick, R.; Artsimovitch, I.; Rösch, P. An helix to barrel domain switch transforms the transcription factor RfaH into a translation factor. Cell 2012, 150, 291-303.
54. Torres, M.; Balada, J.-M.; Zellars, M.; Squires, C.; Squires, C. L. In vivo effect of NusB and NusG on rRNA transcription antitermination. J. Bacteriol. 2004, 186, 1304-1310.
55. Bakshi, S.; Siryaporn, A.; Goulian, M.; Weisshaar, J. C. Superresolution imaging of ribosomes and RNA polymerase in live Escherichia coli cells. Mol. Microbiol. 2012, 85, 21-38.
56. Yakhnin, A. V.; Babitzke, P. NusG/Spt5: Are there common functions of this ubiquitous transcription elongation factor? Curr. Opin. Microbiol. 2014, 18, 68-71.
57. Tomar, S. K.; Knauer, S. H.; Nandymazumdar, M.; Rösch, P.; Artsimovitch, I. Interdomain contacts control folding of transcription factor RfaH. Nucleic Acids Res. 2013, 41, 10077-10085.
58. Nudler, E.; Gottesman, M. E. Transcription termination and anti-termination in E. coli. Genes Cells 2002, 7, 755-768.
59. Kolb, K. E.; Hein, P. P.; Landick, R. Antisense oligonucleotide-stimulated transcriptional pausing reveals RNA exit channel specificity of RNA polymerase and mechanistic contributions of NusA and RfaH. J. Biol. Chem. 2014, 289, 1151-1163.
60. Gusarov, I.; Nudler, E. Control of intrinsic transcription termination by N and NusA: The basic mechanisms. Cell 2001, 107, 437-449.
61. Ha, K. S.; Tiulokhonev, I.; Vassylyev, D. G.; Landick, R. The NusA N-terminal domain is necessary and sufficient for enhancement of transcriptional pausing via interaction with the RNA exit channel of RNA polymerase. J. Mol. Biol. 2010, 401, 708-725.
62. Schweimer, K.; Prasch, S.; Sujatha, P. S.; Bubunenko, M.; Gottesman, M. E.; Rösch, P. NusA interaction with the subunit of E. coli RNA polymerase is via the UP element site and releases autoinhibition. Structure 2011, 19, 945-954.
63. Yang, X.; Lewis, P. J. The interaction between RNA polymerase and the elongation factor NusA. RNA Biol. 2010, 7, 272-275.
64. Washburn, R. S.; Gottesman, M. E. Columbia University Medical Center, New York, NY, USA. Unpublished work, 2015.
65. Ross, W.; Vrentas, C. E.; Sanchez-Vazquez, P.; Gaal, T.; Gourse, R. L. The magic spot: A ppGpp binding site on E. coli RNA polymerase responsible for regulation of transcription initiation. Mol. Cell 2013, 50, 420-429.
66. Lee, J. H.; Lennon, C. W.; Ross, W.; Gourse, R. L. Role of the coiled-coil tip of Escherichia coli DksA in promoter control. J. Mol. Biol. 2012, 416, 503-517.
67. Vinella, D.; Potrykus, K.; Murphy, H.; Cashel, M. Effects on growth by changes of the balance between GreA, GreB, and DksA suggest mutual competition and functional redundancy in Escherichia coli. J. Bacteriol. 2012, 194, 261-273.
68. Stepanova, E.; Lee, J.; Ozerova, M.; Semenova; E; Datsenko, K.; Wanner, B. L.; Severinov, K.; Borukhov, S. Analysis of promoter targets for Escherichia coli transcription elongation factor GreA in vivo and in vitro. J. Bacteriol. 2007, 189, 8772-8785.
69. Furman, R.; Sevostyanova, A.; Artsimovitch, I. Transcription initiation factor DksA has diverse effects on RNA chain elongation. Nucleic Acids Res. 2012, 40, 3392-3402.
70. Trautinger, B. W.; Jaktaji, R. P.; Rusakova, E.; Lloyd, R. G. RNA polymerase modulators and DNA repair activities resolve conflicts between replication and transcription. Mol. Cell 2005, 19, 247-258.
71. Tehranchi, A. K.; Blankenschien, M. D.; Zhang, Y.; Halliday, J. A.; Srivatsan, A.; Peng, J.; Herman, C.; Wang, J. D. The transcription factor DksA prevents conflicts between DNA replication and transcription machinery. Cell 2010, 141, 595-605.
72. Zhang, Y.; Mooney, R. A.; Grass, J. A.; Sivaramakrishnan, P.; Herman, C.; Landick, R.; Wang, J. D. DksA guards elongating RNA polymerase against ribosome-stalling-induced arrest. Mol. Cell 2014, 53, 766-778.
73. Satory, D.; Halliday, J. A.; Sivaramakrishnan, P.; Lua, R. C.; Herman, C. Characterization of a novel RNA polymerase mutant that alters DksA activity. J. Bacteriol. 2013, 195, 4187-4194.
74. Parks, A. R.; Court, C.; Lubkowska, L.; Jin, D. J.; Kashlev, M.; Court, D. L. Bacteriophage N protein inhibits transcription slippage by Escherichia coli RNA polymerase. Nucleic Acids Res. 2014, 42, 5823-5829.
75. Washburn, R. S.; Wang, Y.; Gottesman, M. E. Role of E. coli transcription-repair coupling factor Mfd in Nun-mediated transcription termination. J. Mol. Biol. 2003, 329, 655-662.
76. Hung; S. C.; Gottesman, M. E. Phage HK022 Nun protein arrests transcription on phage DNA in vitro and competes with the phage lambda N antitermination protein. J. Mol. Biol. 1995, 247, 428-442.
77. Uc-Mass, A.; Khodursky, A.; Brown, L.; Gottesman, M. E. Overexpression of phage HK022 Nun protein is toxic for Escherichia coli. J. Mol. Biol. 2008, 380, 812-819.
78. Chattopadhyay, S.; Hung, S. C.; Stuart, A. C.; Palmer, A. G., 3rd; Garcia-Mena, J.; Das, A.; Gottesman, M. E. Interaction between the phage HK022 Nun protein and the nut RNA of phage. Proc. Natl. Acad. Sci. USA 1995, 92, 12131-12135.
79. Vitiello, C. L.; Kireeva, M. L.; Lubkowska, L.; Kashlev, M.; Gottesman, M. Coliphage HK022 Nun protein inhibits RNA polymerase translocation. Proc. Natl. Acad. Sci. USA 2014, 111, E2368-E2375.
80. Vitiello, C. L.; Gottesman, M. E. Bacteriophage HK022 Nun protein arrests transcription by blocking lateral mobility of RNA polymerase during transcription elongation. Bacteriophage 2014, doi: 10. 4161/bact. 32187.
81. Rees, W. A.; Weitzel, S. E.; Yager, T. D.; Das, A.; von Hippel, P. H. Bacteriophage N protein alone can induce transcription antitermination in vitro. Proc. Natl. Acad. Sci. USA 1996, 93, 342-346.
82. Watnick, R. S.; Gottesman, M. E. Escherichia coli NusA is required for efficient RNA binding by phage HK022 nun protein. Proc. Natl. Acad. Sci. USA 1998, 95, 1546-1551.