RNA transcript 3-2-proximal sequence affects translocation bias of RNA polymerase

Biochemistry

Volumn 50, Issue 32, 2011, Pages 7002-7014

  Hein, Pyae P ^a   Palangat, Murali ^a   Landick, Robert ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE; E. COLI; ELONGATION COMPLEX; EXONUCLEASE; FOOTPRINTING; MULTISUBUNIT; RNA POLYMERASE; THERMOPHILUS;

ELONGATION; ESCHERICHIA COLI; NUCLEOTIDES; POLYMERS;

RNA;

EXONUCLEASE; PYROPHOSPHATE; RNA POLYMERASE;

ARTICLE; BASE PAIRING; DNA SEQUENCE; ESCHERICHIA COLI; NONHUMAN; PHOSPHORYLATION; PRIORITY JOURNAL; RNA SEQUENCE; RNA TRANSCRIPTION; RNA TRANSPORT; THERMUS THERMOPHILUS;

DNA-DIRECTED RNA POLYMERASES; ESCHERICHIA COLI; HYDROLYSIS; PROTEIN TRANSPORT; RNA, MESSENGER; THERMUS THERMOPHILUS;

BACTERIA (MICROORGANISMS); EUKARYOTA;

EID: 80051538984     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi200437q     Document Type: Article

References (52)

1. Zhang, J. a. L. R. (2009) Substrate loading, nucleotide addition, and translocation by RNA Polymerase, in RNA Polymerase as Molecular Motors (Buc, H. a. S. T., Ed.) 1 st ed., pp 206-235, Royal Society of Chemistry, Cambridge, UK.
2. Kireeva, M., Kashlev, M., and Burton, Z. F. Translocation by multi-subunit RNA polymerases. Biochim. Biophys. Acta 2010, not supplied.
3. Sosunov, V., Sosunova, E., Mustaev, A., Bass, I., Nikiforov, V., and Goldfarb, A. (2003) Unified two-metal mechanism of RNA synthesis and degradation by RNA polymerase EMBO J. 22, 2234-2244 (Pubitemid 36565546)
4. Guajardo, R. and Sousa, R. (1997) A model for the mechanism of polymerase translocation J. Mol. Biol. 265, 8-19 (Pubitemid 27110561)
5. Abbondanzieri, E. A., Greenleaf, W. J., Shaevitz, J. W., Landick, R., and Block, S. M. (2005) Direct observation of base-pair stepping by RNA polymerase Nature 438, 460-465 (Pubitemid 41742012)
6. Bai, L., Fulbright, R. M., and Wang, M. D. (2007) Mechanochemical kinetics of transcription elongation Phys. Rev. Lett. 98, 068103
7. Landick, R. (2006) The regulatory roles and mechanism of transcriptional pausing Biochem. Soc. Trans. 34, 1062-1066 (Pubitemid 46768989)
8. Landick, R. (2009) Transcriptional pausing without backtracking Proc. Natl. Acad. Sci. U. S. A. 106, 8797-8798
9. Galburt, E. A., Grill, S. W., Wiedmann, A., Lubkowska, L., Choy, J., Nogales, E., Kashlev, M., and Bustamante, C. (2007) Backtracking determines the force sensitivity of RNAP II in a factor-dependent manner Nature 446, 820-823 (Pubitemid 46582033)
10. Mejia, Y. X., Mao, H., Forde, N. R., and Bustamante, C. (2008) Thermal probing of E. coli RNA polymerase off-pathway mechanisms J. Mol. Biol. 382, 628-637
11. Depken, M., Galburt, E. A., and Grill, S. W. (2009) The origin of short transcriptional pauses Biophys. J. 96, 2189-2193
12. Bai, L., Shundrovsky, A., and Wang, M. D. (2004) Sequence-dependent kinetic model for transcription elongation by RNA polymerase J. Mol. Biol. 344, 335-349 (Pubitemid 39441208)
13. Komissarova, N. and Kashlev, M. (1997) Transcriptional arrest: Escherichia coli RNA polymerase translocates backward, leaving the 3-2 end of the RNA intact and extruded Proc. Natl. Acad. Sci. U. S. A. 94, 1755-1760
14. Nudler, E., Mustaev, A., Lukhtanov, E., and Goldfarb, A. (1997) The RNA:DNA hybrid maintains the register of transcription by preventing backtracking of RNA polymerase Cell 89, 33-41
15. Larson, M. H., Greenleaf, W. J., Landick, R., and Block, S. M. (2008) Applied force reveals mechanistic and energetic details of transcription termination Cell 132, 971-982 (Pubitemid 351381740)
16. Santangelo, T. J. and Roberts, J. W. (2004) Forward translocation is the natural pathway of RNA release at an intrinsic terminator Mol. Cell 14, 117-126 (Pubitemid 38469914)
17. Epshtein, V., Cardinale, C. J., Ruckenstein, A. E., Borukhov, S., and Nudler, E. (2007) An allosteric path to transcription termination Mol. Cell 28, 991-1001 (Pubitemid 350297020)
18. Epshtein, V., Dutta, D., Wade, J., and Nudler, E. (2010) An allosteric mechanism of Rho-dependent transcription termination Nature 463, 245-249
19. Bar-Nahum, G., Epshtein, V., Ruckenstein, A., Rafikov, R., Mustaev, A., and Nudler, E. (2005) A ratchet mechanism of transcription elongation and its control Cell 120, 183-193 (Pubitemid 40174762)
20. Pasman, Z. and von Hippel, P. H. (2000) Regulation of rho-dependent transcription termination by NusG is specific to the Escherichia coli elongation complex Biochemistry 39, 5573-5585 (Pubitemid 30257100)
21. Rozovskaya, T. A., Chenchik, A. A., and Beabealashvilli, R. (1982) Processive pyrophosphorolysis of RNA by Escherichia coli RNA polymerase FEBS Lett. 137, 100-104 (Pubitemid 12102610)
22. Toulokhonov, I., Zhang, J., Palangat, M., and Landick, R. (2007) A central role of the RNA polymerase trigger loop in active-site rearrangement during transcriptional pausing Mol. Cell 27, 406-419 (Pubitemid 47126936)
23. Vassylyeva, M. N., Lee, J., Sekine, S. I., Laptenko, O., Kuramitsu, S., Shibata, T., Inoue, Y., Borukhov, S., Vassylyev, D. G., and Yokoyama, S. (2002) Purification, crystallization and initial crystallographic analysis of RNA polymerase holoenzyme from Thermus thermophilus Acta Crystallogr., Sect. D: Biol. Crystallogr. 58, 1497-1500 (Pubitemid 35028853)
24. Hu, X., Malik, S., Negroiu, C. C., Hubbard, K., Velalar, C. N., Hampton, B., Grosu, D., Catalano, J., Roeder, R. G., and Gnatt, A. (2006) A Mediator-responsive form of metazoan RNA polymerase II Proc. Natl. Acad. Sci. U. S. A. 103, 9506-9511 (Pubitemid 43955855)
25. Kyzer, S., Ha, K. S., Landick, R., and Palangat, M. (2007) Direct versus limited-step reconstitution reveals key features of an RNA hairpin-stabilized paused transcription complex J. Biol. Chem. 282, 19020-19028 (Pubitemid 47100138)
26. Maxam, A. M. and Gilbert, W. (1980) Sequencing end-labeled DNA with base-specific chemical cleavages Methods Enzymol. 65, 499-560
27. Johnson, K. A., Simpson, Z. B., and Blom, T. (2009) Global kinetic explorer: a new computer program for dynamic simulation and fitting of kinetic data Anal. Biochem. 387, 20-29
28. Johnson, K. A., Simpson, Z. B., and Blom, T. (2009) FitSpace explorer: an algorithm to evaluate multidimensional parameter space in fitting kinetic data Anal. Biochem. 387, 30-41
29. Foster, J. E., Holmes, S. F., and Erie, D. A. (2001) Allosteric binding of nucleoside triphosphates to RNA polymerase regulates transcription elongation Cell 106, 243-252 (Pubitemid 32772634)
30. Molnar, J. and Lorand, L. (1961) Studies on apyrases Arch. Biochem. Biophys. 93, 353-363
31. Kashkina, E., Anikin, M., Tahirov, T. H., Kochetkov, S. N., Vassylyev, D. G., and Temiakov, D. (2006) Elongation complexes of Thermus thermophilus RNA polymerase that possess distinct translocation conformations Nucleic Acids Res. 34, 4036-4045 (Pubitemid 44391017)
32. Vassylyev, D., Vassylyeva, M., Zhang, J., Palangat, M., Artsimovitch, I., and Landick, R. (2007) Structural basis for substrate loading in bacterial RNA polymerase Nature 448, 163-168 (Pubitemid 47067369)
33. Landick, R. and Yanofsky, C. (1987) Isolation and structural analysis of the Escherichia coli trp leader paused transcription complex J. Mol. Biol. 196, 363-377
34. Kireeva, M. L., Nedialkov, Y. A., Cremona, G. H., Purtov, Y. A., Lubkowska, L., Malagon, F., Burton, Z. F., Strathern, J. N., and Kashlev, M. (2008) Transient reversal of RNA polymerase II active site closing controls fidelity of transcription elongation Mol. Cell 30, 557-566 (Pubitemid 351755063)
35. Zhang, J., Palangat, M., and Landick, R. (2010) Role of the RNA polymerase trigger loop in catalysis and pausing Nat. Struct. Mol. Biol. 17, 99-104
36. Orlova, M., Newlands, J., Das, A., Goldfarb, A., and Borukhov, S. (1995) Intrinsic transcript cleavage activity of RNA polymerase Proc. Natl. Acad. Sci. U. S. A. 92, 4596-4600
37. Surratt, C. K., Milan, S. C., and Chamberlin, M. J. (1991) Spontaneous cleavage of RNA in ternary complexes of Escherichia coli RNA polymerase and its significance for the mechanism of transcription Proc. Natl. Acad. Sci. U. S. A. 88, 7983-7987 (Pubitemid 21915279)
38. Guo, Q. and Sousa, R. (2006) Translocation by T7 RNA polymerase: a sensitively poised Brownian ratchet J. Mol. Biol. 358, 241-254
39. Marchand, B., Tchesnokov, E. P., and Gotte, M. (2007) The pyrophosphate analogue foscarnet traps the pre-translocational state of HIV-1 reverse transcriptase in a Brownian ratchet model of polymerase translocation J. Biol. Chem. 282, 3337-3346 (Pubitemid 47084323)
40. Yin, Y. W. and Steitz, T. A. (2004) The structural mechanism of translocation and helicase activity in T7 RNA polymerase Cell 116, 393-404 (Pubitemid 38366316)
41. Vassylyev, D., Vassylyeva, M., Perederina, A., Tahirov, T., and Artsimovitch, I. (2007) Structural basis for transcription elongation by bacterial RNA polymerase Nature 448, 157-162 (Pubitemid 47067370)
42. Westover, K. D., Bushnell, D. A., and Kornberg, R. D. (2004) Structural basis of transcription: separation of RNA from DNA by RNA polymerase II Science 303, 1014-1016 (Pubitemid 38209705)
43. Kettenberger, H., Armache, K. J., and Cramer, P. (2004) Complete RNA polymerase II elongation complex structure and its interactions with NTP and TFIIS Mol. Cell 16, 955-965 (Pubitemid 40018405)
44. Gnatt, A. (2002) Elongation by RNA polymerase II: structure-function relationship Biochim. Biophys. Acta 1577, 175-190 (Pubitemid 35223212)
45. Marchand, B. and Gotte, M. (2003) Site-specific footprinting reveals differences in the translocation status of HIV-1 reverse transcriptase. Implications for polymerase translocation and drug resistance J. Biol. Chem. 278, 35362-35372 (Pubitemid 37102305)
46. Liu, C. and Martin, C. T. (2001) Fluorescence characterization of the transcription bubble in elongation complexes of T7 RNA polymerase J. Mol. Biol. 308, 465-475 (Pubitemid 33027613)
47. Kashkina, E., Anikin, M., Brueckner, F., Lehmann, E., Kochetkov, S. N., McAllister, W. T., Cramer, P., and Temiakov, D. (2007) Multisubunit RNA polymerases melt only a single DNA base pair downstream of the active site J. Biol. Chem. 282, 21578-21582 (Pubitemid 47195724)
48. Chan, C. L. and 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, 25-42 (Pubitemid 23288909)
49. Chan, C., Wang, D., and Landick, R. (1997) Spacing from the transcript 3-2 end determines whether a nascent RNA hairpin interacts with RNA polymerase to prolong pausing or triggers termination J. Mol. Biol. 268, 54-68
50. Kireeva, M. L. and Kashlev, M. (2009) Mechanism of sequence-specific pausing of bacterial RNA polymerase Proc. Natl. Acad. Sci. U. S. A. 106, 8900-8905
51. Aivazashvili, V. A., Bibilashvili, R., Vartikian, R. M., and Kutateladze, T. A. (1981) [Effect of the primary structure of RNA on the pulse character of RNA elongation in vitro by Escherichia coli RNA polymerase: a model] Mol. Biol. (Moscow) 15, 915-929
52. Herbert, K. M., Greenleaf, W. J., and Block, S. M. (2008) Single-molecule studies of RNA polymerase: motoring along Annu. Rev. Biochem. 77, 149-176