Unusually long-lived pause required for regulation of a Rho-dependent transcription terminator

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 19, 2014, Pages

  Hollands, Kerry ^a,b,c,d   Sevostiyanova, Anastasia ^a   Groisman, Eduardo A ^a,b,c  

^a Department of Microbial Pathogenesis ^*  (United States)

^b YALE UNIVERSITY   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^d DUPONT COMPANY   (United States)

Author keywords

Magnesium; RNA polymerase

Indexed keywords

TRANSCRIPTION TERMINATION FACTOR RHO;

5' UNTRANSLATED REGION; ARTICLE; BACTERIAL GENE; GENE CONTROL; IN VITRO STUDY; LONGEVITY; MGTA GENE; NONHUMAN; PRIORITY JOURNAL; RIBOSWITCH; RNA SEQUENCE; SALMONELLA ENTERICA; TRANSCRIPTION ELONGATION; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION TERMINATION;

MAGNESIUM; RNA POLYMERASE;

ADENOSINE TRIPHOSPHATASES; BACTERIAL PROTEINS; BASE SEQUENCE; DNA-DIRECTED RNA POLYMERASES; GENE EXPRESSION REGULATION, BACTERIAL; MAGNESIUM; MEMBRANE TRANSPORT PROTEINS; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; RHO FACTOR; RIBOSWITCH; RNA, BACTERIAL; RNA, MESSENGER; SALMONELLA ENTERICA; TERMINATOR REGIONS, GENETIC;

EID: 84900483146     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1319193111     Document Type: Article

References (62)

1. Peters JM, Vangeloff AD, Landick R (2011) Bacterial transcription terminators: The RNA 3′-end chronicles. J Mol Biol 412(5):793-813.
2. Peters JM, et al. (2009) Rho directs widespread termination of intragenic and stable RNA transcription. Proc Natl Acad Sci USA 106(36):15406-15411.
3. Cardinale CJ, et al. (2008) Termination factor Rho and its cofactors NusA and NusG silence foreign DNA in E. coli. Science 320(5878):935-938.
4. Roberts JW (1969) Termination factor for RNA synthesis. Nature 224(5225):1168-1174.
5. Richardson JP, Grimley C, Lowery C (1975) Transcription termination factor rho activity is altered in Escherichia coli with suA gene mutations. Proc Natl Acad Sci USA 72(5):1725-1728.
6. Menouni R, Champ S, Espinosa L, Boudvillain M, Ansaldi M (2013) Transcription termination controls prophage maintenance in Escherichia coli genomes. Proc Natl Acad Sci USA 110(35):14414-14419.
7. Dutta D, Shatalin K, Epshtein V, Gottesman ME, Nudler E (2011) Linking RNA poly-merase backtracking to genome instability in E. coli. Cell 146(4):533-543.
8. Leela JK, Syeda AH, Anupama K, Gowrishankar J (2013) Rho-dependent transcription termination is essential to prevent excessive genome-wide R-loops in Escherichia coli. Proc Natl Acad Sci USA 110(1):258-263.
9. Washburn RS, Gottesman ME (2011) Transcription termination maintains chromosome integrity. Proc Natl Acad Sci USA 108(2):792-797.
10. Peters JM, et al. (2012) Rho and NusG suppress pervasive antisense transcription in Escherichia coli. Genes Dev 26(23):2621-2633.
11. Boudvillain M, Figueroa-Bossi N, Bossi L (2013) Terminator still moving forward: Expanding roles for Rho factor. Curr Opin Microbiol 16(2):118-124.
12. Konan KV, Yanofsky C (2000) Rho-dependent transcription termination in the tna operon of Escherichia coli: Roles of the boxA sequence and the rut site. J Bacteriol 182(14):3981-3988.
13. Stewart V, Landick R, Yanofsky C (1986) Rho-dependent transcription termination in the tryptophanase operon leader region of Escherichia coli K-12. J Bacteriol 166(1): 217-223.
14. Yanofsky C, Konan KV, Sarsero JP (1996) Some novel transcription attenuation mechanisms used by bacteria. Biochimie 78(11-12):1017-1024.
15. Matsumoto Y, Shigesada K, Hirano M, Imai M (1986) Autogenous regulation of the gene for transcription termination factor rho in Escherichia coli: Localization and function of its attenuators. J Bacteriol 166(3):945-958.
16. Bossi L, Schwartz A, Guillemardet B, Boudvillain M, Figueroa-Bossi N (2012) A role for Rho-dependent polarity in gene regulation by a noncoding small RNA. Genes Dev 26(16):1864-1873.
17. Hollands K, et al. (2012) Riboswitch control of Rho-dependent transcription termination. Proc Natl Acad Sci USA 109(14):5376-5381.
18. Rabhi M, Rahmouni AR, Boudvillain M (2010) Transcription termination factor Rho: A ring-shaped RNA helicase from bacteria. RNA Helicases, ed Jankowsky E (Royal Society of Chemistry, Cambridge, UK), pp 243-271.
19. Chen CY, Richardson JP (1987) Sequence elements essential for rho-dependent transcription termination at lambda tR1. J Biol Chem 262(23):11292-11299.
20. Ciampi MS (2006) Rho-dependent terminators and transcription termination. Microbiology 152(Pt 9):2515-2528.
21. Graham JE, Richardson JP (1998) rut Sites in the nascent transcript mediate Rho-dependent transcription termination in vivo. J Biol Chem 273(33):20764-20769.
22. Lau LF, Roberts JW, Wu R (1983) RNA polymerase pausing and transcript release at the lambda tR1 terminator in vitro. J Biol Chem 258(15):9391-9397.
23. Zalatan F, Galloway-Salvo J, Platt T (1993) Deletion analysis of the Escherichia coli rho-dependent transcription terminator trp t′. J Biol Chem 268(23):17051-17056.
24. Zhu AQ, von Hippel PH (1998) Rho-dependent termination within the trp t′ terminator. I. Effects of rho loading and template sequence. Biochemistry 37(32):11202-11214.
25. Cromie MJ, Shi Y, Latifi T, Groisman EA (2006) An RNA sensor for intracellular Mg(2+). Cell 125(1):71-84.
26. Henkin TM (2008) Riboswitch RNAs: Using RNA to sense cellular metabolism. Genes Dev 22(24):3383-3390.
27. Liu M, Tolstorukov M, Zhurkin V, Garges S, Adhya S (2004) A mutant spacer sequence between-35 and-10 elements makes the Plac promoter hyperactive and cAMP receptor protein-independent. Proc Natl Acad Sci USA 101(18):6911-6916.
28. Sasse-Dwight S, Gralla JD (1991) Footprinting protein-DNA complexes in vivo. Methods Enzymol 208:146-168.
29. Landick R, Wang D, Chan CL (1996) Quantitative analysis of transcriptional pausing by Escherichia coli RNA polymerase: his leader pause site as paradigm. Methods Enzymol 274:334-353.
30. Hatoum A, Roberts J (2008) Prevalence of RNA polymerase stalling at Escherichia coli promoters after open complex formation. Mol Microbiol 68(1):17-28.
31. Yakhnin AV, Yakhnin H, Babitzke P (2006) RNA polymerase pausing regulates translation initiation by providing additional time for TRAP-RNA interaction. Mol Cell 24(4):547-557.
32. Yakhnin AV, Yakhnin H, Babitzke P (2008) Function of the Bacillus subtilis transcription elongation factor NusG in hairpin-dependent RNA polymerase pausing in the trp leader. Proc Natl Acad Sci USA 105(42):16131-16136.
33. Kainz M, Roberts JW (1995) Kinetics of RNA polymerase initiation and pausing at the lambda late gene promoter in vivo. J Mol Biol 254(5):808-814.
34. Lau LF, Roberts JW, Wu R (1982) Transcription terminates at lambda tR1 in three clusters. Proc Natl Acad Sci USA 79(20):6171-6175.
35. Wu AM, Christie GE, Platt T (1981) Tandem termination sites in the tryptophan op-eron of Escherichia coli. Proc Natl Acad Sci USA 78(5):2913-2917.
36. Landick R (2006) The regulatory roles and mechanism of transcriptional pausing. Biochem Soc Trans 34(Pt 6):1062-1066.
37. King RA, Banik-Maiti S, Jin DJ, Weisberg RA (1996) Transcripts that increase the processivity and elongation rate of RNA polymerase. Cell 87(5):893-903.
38. Komissarova N, et al. (2008) Inhibition of a transcriptional pause by RNA anchoring to RNA polymerase. Mol Cell 31(5):683-694.
39. Herbert KM, et al. (2006) Sequence-resolved detection of pausing by single RNA polymerase molecules. Cell 125(6):1083-1094.
40. Kireeva ML, Kashlev M (2009) Mechanism of sequence-specific pausing of bacterial RNA polymerase. Proc Natl Acad Sci USA 106(22):8900-8905.
41. Weixlbaumer A, Leon K, Landick R, Darst SA (2013) Structural basis of transcriptional pausing in bacteria. Cell 152(3):431-441.
42. Chan CL, Landick R (1989) The Salmonella typhimurium his operon leader region contains an RNA hairpin-dependent transcription pause site. Mechanistic implications of the effect on pausing of altered RNA hairpins. J Biol Chem 264(34):20796-20804.
43. Lee DN, Phung L, Stewart J, Landick R (1990) Transcription pausing by Escherichia coli RNA polymerase is modulated by downstream DNA sequences. J Biol Chem 265(25): 15145-15153.
44. Levin JR, Chamberlin MJ (1987) Mapping and characterization of transcriptional pause sites in the early genetic region of bacteriophage T7. J Mol Biol 196(1):61-84.
45. Yakhnin AV, Babitzke P (2010) Mechanism of NusG-stimulated pausing, hairpin-dependent pause site selection and intrinsic termination at overlapping pause and termination sites in the Bacillus subtilis trp leader. Mol Microbiol 76(3):690-705.
46. Artsimovitch I, Landick R (1998) Interaction of a nascent RNA structure with RNA polymerase is required for hairpin-dependent transcriptional pausing but not for transcript release. Genes Dev 12(19):3110-3122.
47. Artsimovitch I, Landick R (2000) Pausing by bacterial RNA polymerase is mediated by mechanistically distinct classes of signals. Proc Natl Acad Sci USA 97(13):7090-7095.
48. Chan CL, Landick R (1993) Dissection of the his leader pause site by base substitution reveals a multipartite signal that includes a pause RNA hairpin. J Mol Biol 233(1): 25-42.
49. Landick R, Yanofsky C (1984) Stability of an RNA secondary structure affects in vitro transcription pausing in the trp operon leader region. J Biol Chem 259(18):11550-11555.
50. Kohn H, Widger W (2005) The molecular basis for the mode of action of bicyclomycin. Curr Drug Targets Infect Disord 5(3):273-295.
51. Zwiefka A, Kohn H, Widger WR (1993) Transcription termination factor rho: The site of bicyclomycin inhibition in Escherichia coli. Biochemistry 32(14):3564-3570.
52. Coppins RL, Hall KB, Groisman EA (2007) The intricate world of riboswitches. Curr Opin Microbiol 10(2):176-181.
53. Wickiser JK, Winkler WC, Breaker RR, Crothers DM (2005) The speed of RNA transcription and metabolite binding kinetics operate an FMN riboswitch. Mol Cell 18(1): 49-60.
54. Park SY, Cromie MJ, Lee EJ, Groisman EA (2010) A bacterial mRNA leader that employs different mechanisms to sense disparate intracellular signals. Cell 142(5): 737-748.
55. Zhao G, Kong W, Weatherspoon-Griffin N, Clark-Curtiss J, Shi Y (2011) Mg2+ facilitates leader peptide translation to induce riboswitch-mediated transcription termination. EMBO J 30(8):1485-1496.
56. Loh E, et al. (2009) A trans-acting riboswitch controls expression of the virulence regulator PrfA in Listeria monocytogenes. Cell 139(4):770-779.
57. Snavely MD, Miller CG, Maguire ME (1991) The mgtB Mg2+ transport locus of Salmonella typhimurium encodes a P-type ATPase. J Biol Chem 266(2):815-823.
58. Elbing K, Brent R (2002) Media preparation and bacteriological tools. Curr Protoc Mol Biol, Chapter 1:Unit 1.1.
59. Holmes DS, Quigley M (1981) A rapid boiling method for the preparation of bacterial plasmids. Anal Biochem 114(1):193-197.
60. Belogurov GA, et al. (2007) Structural basis for converting a general transcription factor into an operon-specific virulence regulator. Mol Cell 26(1):117-129.
61. Grainger DC, Goldberg MD, Lee DJ, Busby SJ (2008) Selective repression by Fis and H-NS at the Escherichia coli dps promoter. Mol Microbiol 68(6):1366-1377.
62. Artsimovitch I, Henkin TM (2009) In vitro approaches to analysis of transcription termination. Methods 47(1):37-43.