RNA polymerase-induced remodelling of NusA produces a pause enhancement complex

Nucleic Acids Research

Volumn 43, Issue 5, 2015, Pages 2829-2840

  Ma, Cong ^a   Mobli, Mehdi ^b   Yang, Xiao ^a   Keller, Andrew N ^a   King, Glenn F ^b   Lewis, Peter J ^a  

^a UNIVERSITY OF NEWCASTLE   (Australia)

^b UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ELONGATION FACTOR; NUSA PROTEIN; RNA POLYMERASE; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; BACTERIAL RNA; DNA DIRECTED RNA POLYMERASE; PROTEIN BINDING; TRANSCRIPTION FACTOR;

ALLOSTERISM; ARTICLE; BACILLUS SUBTILIS; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN RNA BINDING; PROTEIN STRUCTURE; TRANSCRIPTION REGULATION; AMINO ACID SEQUENCE; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; CONFORMATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; MOLECULAR GENETICS; MUTATION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN CONFORMATION; PROTEIN TERTIARY STRUCTURE; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; BACILLUS SUBTILIS; BACTERIAL PROTEINS; BINDING SITES; DNA-DIRECTED RNA POLYMERASES; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEIC ACID CONFORMATION; PEPTIDE ELONGATION FACTORS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; RNA, BACTERIAL; SEQUENCE HOMOLOGY, AMINO ACID; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84937622542     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv108     Document Type: Article

References (49)

1. Sims, R. J. III, Belotserkovskaya, R. and Reinberg, D. (2004) Elongation by RNA polymerase II: the short and long of it. Genes Dev., 18, 2437-2468.
2. Alexander, R. D., Innocente, S. A., Barrass, J. D. and Beggs, J. D. (2010) Splicing-dependent RNA polymerase pausing in yeast. Mol. Cell, 40, 582-593.
3. Carrillo Oesterreich, F., Preibisch, S. and Neugebauer, K. M. (2010) Global analysis of nascent RNA reveals transcriptional pausing in terminal exons. Mol. Cell, 40, 571-581.
4. Saunders, A., Core, L. J., Sutcliffe, C., Lis, J. T. and Ashe, H. L. (2013) Extensive polymerase pausing during Drosophila axis patterning enables high-level and pliable transcription. Genes Dev., 27, 1146-1158.
5. Schaukowitch, K., Joo, J. Y., Liu, X., Watts, J. K., Martinez, C. and Kim, T. K. (2014) Enhancer RNA facilitates NELF release from immediate early genes. Mol. Cell, 56, 29-42.
6. Pagano, J. M., Kwak, H., Waters, C. T., Sprouse, R. O., White, B. S., Ozer, A., Szeto, K., Shalloway, D., Craighead, H. G. and Lis, J. T. (2014) Defining NELF-E RNA binding in HIV-1 and promoter-proximal pause regions. PLoS Genet., 10, e1004090.
7. Tome, J. M., Ozer, A., Pagano, J. M., Gheba, D., Schroth, G. P. and Lis, J. T. (2014) Comprehensive analysis of RNA-protein interactions by high-throughput sequencing-RNA affinity profiling. Nat. Methods, 11, 683-688.
8. Gusarov, I. and Nudler, E. (2001) Control of intrinsic transcription termination by N and NusA: the basic mechanisms. Cell, 107, 437-449.
9. Landick, R. (2006) The regulatory roles and mechanism of transcriptional pausing. Biochem. Soc. Trans., 34, 1062-1066.
10. Epshtein, V., Kamarthapu, V., McGary, K., Svetlov, V., Ueberheide, B., Proshkin, S., Mironov, A. and Nudler, E. (2014) UvrD facilitates DNA repair by pulling RNA polymerase backwards. Nature, 505, 372-377.
11. Larson, M. H., Mooney, R. A., Peters, J. M., Windgassen, T., Nayak, D., Gross, C. A., Block, S. M., Greenleaf, W. J., Landick, R. and Weissman, J. S. (2014) A pause sequence enriched at translation start sites drives transcription dynamics in vivo. Science, 344, 1042-1047.
12. Artsimovitch, I. and Landick, R. (2000) Pausing by bacterial RNA polymerase is mediated by mechanistically distinct classes of signals. Proc. Natl. Acad. Sci. U. S. A., 97, 7090-7095.
13. Farnham, P. J. and Platt, T. (1981) Rho-independent termination: dyad symmetry in DNA causes RNA polymerase to pause during transcription in vitro. Nucleic Acids Res., 9, 563-577.
14. Farnham, P. J., Greenblatt, J. and Platt, T. (1982) Effects of NusA protein on transcription termination in the tryptophan operon of Escherichia coli. Cell, 29, 945-951.
15. Lau, L. F., Roberts, J. W. and Wu, R. (1983) RNA polymerase pausing and transcript release at the lambda tR1 terminator in vitro. J. Biol. Chem., 258, 9391-9397.
16. Ha, K. S., Toulokhonov, I., Vassylyev, D. G. and Landick, R. (2010) 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., 401, 708-725.
17. Kolb, K. E., Hein, P. P. and Landick, R. (2014) Antisense oligonucleotide-stimulated transcriptional pausing reveals RNA exit channel specificity of RNA polymerase and mechanistic contributions of NusA and RfaH. J. Biol. Chem., 289, 1151-1163.
18. Yang, X., Molimau, S., Doherty, G. P., Johnston, E. B., Marles-Wright, J., Rothnagel, R., Hankamer, B., Lewis, R. J. and Lewis, P. J. (2009) The structure of bacterial RNA polymerase in complex with the essential transcription elongation factor NusA. EMBO Rep., 10, 997-1002.
19. Zheng, C. and Friedman, D. I. (1994) Reduced Rho-dependent transcription termination permits NusA-independent growth of Escherichia coli. Proc. Natl. Acad. Sci. U. S. A., 91, 7543-7547.
20. Yang, X., Ma, C. and Lewis, P. (2014) A vector system that allows simple generation of mutant Escherichia coli RNA polymerase. Plasmid, 75, 37-41.
21. Marley, J., Lu, M. and Bracken, C. (2001) A method for efficient isotopic labeling of recombinant proteins. J. Biomol. NMR, 20, 71-75.
22. Studier, F. W. (2005) Protein production by auto-induction in high density shaking cultures. Protein Expr. Purif., 41, 207-234.
23. Yang, X. and Lewis, P. J. (2008) Overproduction and purification of recombinant Bacillus subtilis RNA polymerase. Protein. Expr. Purif., 59, 86-93.
24. Ma, C., Yang, X., Kandemir, H., Mielczarek, M., Johnston, E. B., Griffith, R., Kumar, N. and Lewis, P. J. (2013) Inhibitors of bacterial transcription initiation complex formation. ACS Chem. Biol., 8, 1972-1980.
25. Mobli, M., Stern, A. S., Bermel, W., King, G. F. and Hoch, J. C. (2010) A non-uniformly sampled 4D HCC (CO) NH-TOCSY experiment processed using maximum entropy for rapid protein sidechain assignment. J. Magn. Reson., 204, 160-164.
26. Mobli, M., Maciejewski, M. W., Gryk, M. R. and Hoch, J. C. (2007) An automated tool for maximum entropy reconstruction of biomolecular NMR spectra. Nat. Methods, 4, 467-468.
27. Mobli, M., Maciejewski, M. W., Gryk, M. R. and Hoch, J. C. (2007) Automatic maximum entropy spectral reconstruction in NMR. J. Biomol. NMR., 39, 133-139.
28. Bartels, C., Xia, T. H., Billeter, M., Guntert, P. and Wuthrich, K. (1995) The program XEASY for computer-supported NMR spectral analysis of biological macromolecules. J. Biomol. NMR, 6, 1-10.
29. Vranken, W. F., Boucher, W., Stevens, T. J., Fogh, R. H., Pajon, A., Llinas, M., Ulrich, E. L., Markley, J. L., Ionides, J. and Laue, E. D. (2005) The CCPN data model for NMR spectroscopy: development of a software pipeline. Proteins, 59, 687-696.
30. Herrmann, T., Guntert, P. and Wuthrich, K. (2002) Protein NMR structure determination with automated NOE assignment using the new software CANDID and the torsion angle dynamics algorithm DYANA. J. Mol. Biol., 319, 209-227.
31. Guntert, P. (2004) Automated NMR structure calculation with CYANA. Methods Mol. Biol., 278, 353-378.
32. Cornilescu, G., Delaglio, F. and Bax, A. (1999) Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J. Biomol. NMR, 13, 289-302.
33. D'Auvergne, E. J. and Gooley, P. R. (2008) Optimisation of NMR dynamic models I. Minimisation algorithms and their performance within the model-free and Brownian rotational diffusion spaces. J. Biomol. NMR, 40, 107-119.
34. Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C. and Ferrin, T. E. (2004) UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem., 25, 1605-1612.
35. De Vries, S. J., Van Dijk, M. and Bonvin, A. M. (2010) The HADDOCK web server for data-driven biomolecular docking. Nat. Protoc., 5, 883-897.
36. Davies, K. M., Dedman, A. J., Van Horck, S. and Lewis, P. J. (2005) The NusA:RNA polymerase ratio is increased at sites of rRNA synthesis in Bacillus subtilis. Mol. Microbiol., 57, 366-379.
37. Johnston, E. B., Lewis, P. J. and Griffith, R. (2009) The interaction of Bacillus subtilis sigmaA with RNA polymerase. Protein Sci., 18, 2287-2297.
38. Artsimovitch, I., Svetlov, V., Anthony, L., Burgess, R. R. and Landick, R. (2000) RNA polymerases from Bacillus subtilis and Escherichia coli differ in recognition of regulatory signals in vitro. J. Bacteriol., 182, 6027-6035.
39. Artsimovitch, I. and Henkin, T. M. (2009) In vitro approaches to analysis of transcription termination. Methods, 47, 37-43.
40. Landick, R., Wang, D. and Chan, C. L. (1996) Quantitative analysis of transcriptional pausing by Escherichia coli RNA polymerase: his leader pause site as paradigm. Methods Enzymol., 274, 334-353.
41. Vassylyev, D. G., Sekine, S., Laptenko, O., Lee, J., Vassylyeva, M. N., Borukhov, S. and Yokoyama, S. (2002) Crystal structure of a bacterial RNA polymerase holoenzyme at 2.6 A resolution. Nature, 417, 712-719.
42. Borukhov, S., Lee, J. and Laptenko, O. (2005) Bacterial transcription elongation factors: new insights into molecular mechanism of action. Mol. Microbiol., 55, 1315-1324.
43. Shin, D. H., Nguyen, H. H., Jancarik, J., Yokota, H., Kim, R. and Kim, S. H. (2003) Crystal structure of NusA from Thermotoga maritima and functional implication of the N-terminal domain. Biochemistry, 42, 13429-13437.
44. Gill, S. C., Weitzel, S. E. and Von Hippel, P. H. (1991) Escherichia coli sigma 70 and NusA proteins. I. Binding interactions with core RNA polymerase in solution and within the transcription complex. J. Mol. Biol., 220, 307-324.
45. Worbs, M., Bourenkov, G. P., Bartunik, H. D., Huber, R. and Wahl, M. C. (2001) An extended RNA binding surface through arrayed S1 and KH domains in transcription factor NusA. Mol. Cell, 7, 1177-1189.
46. Weixlbaumer, A., Leon, K., Landick, R. and Darst, S. A. (2013) Structural basis of transcriptional pausing in bacteria. Cell, 152, 431-441.
47. Hein, P. P., Kolb, K. E., Windgassen, T., Bellecourt, M. J., Darst, S. A., Mooney, R. A. and Landick, R. (2014) RNA polymerase pausing and nascent-RNA structure formation are linked through clamp-domain movement. Nat. Struct. Mol. Biol., 21, 794-802.
48. Mooney, R. A., Davis, S. E., Peters, J. M., Rowland, J. L., Ansari, A. Z. and Landick, R. (2009) Regulator trafficking on bacterial transcription units in vivo. Mol. Cell, 33, 97-108.
49. Zhou, J., Ha, K. S., La Porta, A., Landick, R. and Block, S. M. (2011) Applied force provides insight into transcriptional pausing and its modulation by transcription factor NusA. Mol. Cell, 44, 635-646.