Transcription start site scanning and the requirement for ATP during transcription initiation by RNA polymerase II

Journal of Biological Chemistry

Volumn 291, Issue 25, 2016, Pages 13040-13047

  Fishburn, James ^a   Galburt, Eric ^b   Hahn, Steven ^a  

^a Fred Hutchinson Cancer Research Center   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA SEQUENCES; NUCLEIC ACIDS; RNA; SCANNING; YEAST;

PREINITIATION COMPLEX; RNA POLYMERASE; RNA POLYMERASE II; RNA SYNTHESIS; TRANSCRIPTION INITIATION; TRANSCRIPTION START SITE; TRANSLOCASES; TSS POSITION;

TRANSCRIPTION;

ADENOSINE TRIPHOSPHATE; BINDING PROTEIN; CREATINE KINASE; DNA; GUANOSINE TRIPHOSPHATASE; GUANOSINE TRIPHOSPHATE; NUCLEOTIDE; RNA; RNA POLYMERASE; RNA POLYMERASE II; URIDINE TRIPHOSPHATE; DNA HELICASE; SACCHAROMYCES CEREVISIAE PROTEIN; SSL2 PROTEIN, S CEREVISIAE; TRANSCRIPTION FACTOR IIH;

ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; DNA STRAND; DOWNSTREAM PROCESSING; ENZYME ACTIVITY; GENE TRANSLOCATION; HYDROLYSIS; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; RNA SYNTHESIS; SACCHAROMYCES CEREVISIAE; TRANSCRIPTION INITIATION SITE; CHEMISTRY; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYSIOLOGY;

BASE SEQUENCE; DNA HELICASES; GENE EXPRESSION REGULATION, FUNGAL; MOLECULAR SEQUENCE DATA; PROMOTER REGIONS, GENETIC; RNA POLYMERASE II; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSCRIPTION FACTOR TFIIH; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION, GENETIC;

EID: 84975087436     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M116.724583     Document Type: Article

References (40)

1. Sainsbury, S., Bernecky, C., and Cramer, P. (2015) Structural basis of transcription initiation by RNA polymerase II. Nat. Rev. Mol. Cell Biol. 16, 129-143
2. Grünberg, S., and Hahn, S. (2013) Structural insights into transcription initiation by RNA polymerase II. Trends Biochem. Sci. 38, 603-611
3. Luse, D. S. (2013) Promoter clearance by RNA polymerase II. Biochim. Biophys. Acta 1829, 63- 68
4. Luse, D. S., and Jacob, G. A. (1987) Abortive initiation by RNA polymerase II in vitro at the adenovirus 2 major late promoter. J. Biol. Chem. 262, 14990-14997
5. Wang, W., Carey, M., and Gralla, J. D. (1992) Polymerase II promoter activation: closed complex formation and ATP-driven start site opening. Science 255, 450-453
6. Holstege, F. C., Fiedler, U., and Timmers, H. T. (1997) Three transitions in the RNA polymerase II transcription complex during initiation. EMBO J. 16, 7468-7480
7. Yan, M., and Gralla, J. D. (1997) Multiple ATP-dependent steps in RNA polymerase II promoter melting and initiation. EMBO J. 16, 7457-7467
8. Kugel, J. F., and Goodrich, J. A. (1998) Promoter escape limits the rate of RNA polymerase II transcription and is enhanced by TFIIE, TFIIH, and ATP on negatively supercoiled DNA. Proc. Natl. Acad. Sci. U.S.A. 95, 9232-9237
9. Pal, M., Ponticelli, A. S., and Luse, D. S. (2005) The role of the transcription bubble and TFIIB in promoter clearance by RNA polymerase II. Mol. Cell. 19, 101-110
10. Hahn, S., and Young, E. T. (2011) Transcriptional regulation in Saccharomyces cerevisiae: transcription factor regulation and function, mechanisms of initiation, and roles of activators and coactivators. Genetics 189, 705-736
11. Murakami, K., Mattei, P.-J., Davis, R. E., Jin, H., Kaplan, C. D., and Kornberg, R. D. (2015) Uncoupling promoter opening from start-site scanning. Mol. Cell 59, 133-138
12. Fishburn, J., and Hahn, S. (2012) Architecture of the yeast RNA polymerase II open complex and regulation of activity by TFIIF. Mol. Cell. Biol. 32, 12-25
13. Hahn, S., Hoar, E. T., and Guarente, L. (1985) Each of three "TATA elements" specifies a subset of the transcription initiation sites at the CYC-1 promoter of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U.S.A. 82, 8562- 8566
14. Nagawa, F., and Fink, G. R. (1985) The relationship between the "TATA" sequence and transcription initiation sites at the HIS4 gene of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U.S.A. 82, 8557- 8561
15. Chen, W., and Struhl, K. (1985) Yeast mRNA initiation sites are determined primarily by specific sequences, not by the distance from the TATA element. EMBO J. 4, 3273-3280
16. Zhang, Z., and Dietrich, F. S. (2005) Mapping of transcription start sites in Saccharomyces cerevisiae using 5′ SAGE. Nucleic Acids Res. 33, 2838-2851
17. Kuehner, J. N., and Brow, D. A. (2006) Quantitative analysis of in vivo initiator selection by yeast RNA polymerase II supports a scanning model. J. Biol. Chem. 281, 14119-14128
18. Bunick, D., Zandomeni, R., Ackerman, S., and Weinmann, R. (1982) Mechanism of RNA polymerase II-specific initiation of transcription in vitro: ATP requirement and uncapped runoff transcripts. Cell 29, 877-886
19. Sawadogo, M., and Roeder, R. G. (1984) Energy requirement for specific transcription initiation by the human RNA polymerase II system. J. Biol. Chem. 259, 5321-5326
20. Tirode, F., Busso, D., Coin, F., and Egly, J. M. (1999) Reconstitution of the transcription factor TFIIH: assignment of functions for the three enzymatic subunits, XPB, XPD, and cdk7. Mol. Cell. 3, 87-95
21. Fishburn, J., Tomko, E., Galburt, E., and Hahn, S. (2015) Double-stranded DNA translocase activity of transcription factor TFIIH and the mechanism of RNA polymerase II open complex formation. Proc. Natl. Acad. Sci. U.S.A. 112, 3961-3966
22. Grünberg, S., Warfield, L., and Hahn, S. (2012) Architecture of the RNA polymerase II preinitiation complex and mechanism of ATP-dependent promoter opening. Nat. Struct. Mol. Biol. 19, 788-796
23. Kim, T. K., Ebright, R. H., and Reinberg, D. (2000) Mechanism of ATP-dependent promoter melting by transcription factor IIH.Science288,1418-1422
24. Goel, S., Krishnamurthy, S., and Hampsey, M. (2012) Mechanism of start site selection by RNA polymerase II: interplay between TFIIB and Ssl2/ XPB helicase subunit of TFIIH. J. Biol. Chem. 287, 557-567
25. He, Y., Fang, J., Taatjes, D. J., and Nogales, E. (2013) Structural visualization of key steps in human transcription initiation. Nature 495, 481-486
26. Fazal, F. M., Meng, C. A., Murakami, K., Kornberg, R. D., and Block, S. M. (2015) Real-time observation of the initiation of RNA polymerase II transcription. Nature 525, 274-277
27. Goodrich, J. A., and Tjian, R. (1994) Transcription factors IIE and IIH and ATP hydrolysis direct promoter clearance by RNA polymerase II. Cell 77, 145-156
28. Dvir, A., Conaway, R. C., and Conaway, J. W. (1997) A role for TFIIH in controlling the activity of early RNA polymerase II elongation complexes. Proc. Natl. Acad. Sci. U.S.A. 94, 9006-9010
29. Wong, K. H., Jin, Y., and Struhl, K. (2014) TFIIH phosphorylation of the Pol II CTD stimulates mediator dissociation from the preinitiation complex and promoter escape. Mol. Cell 54, 601-612
30. Jeronimo, C., and Robert, F. (2014) Kin28 regulates the transient association of mediator with core promoters. Nat. Struct. Mol. Biol. 10.1038/nsmb.2810
31. Coin, F., and Egly, J. M. (1998) Ten years of TFIIH. Cold Spring Harb. Symp. Quant. Biol. 63, 105-110
32. Khaperskyy, D. A., Ammerman, M. L., Majovski, R. C., and Ponticelli, A. S. (2008) Functions of Saccharomyces cerevisiae TFIIF during transcription start site utilization. Mol. Cell. Biol. 28, 3757-3766
33. Hampsey, M. (1998) Molecular genetics of the RNA polymerase II general transcriptional machinery. Microbiol. Mol. Biol. Rev. 62, 465-503
34. Kaplan, C. D., Jin, H., Zhang, I. L., and Belyanin, A. (2012) Dissection of Pol II trigger loop function and Pol II activity-dependent control of start site selection in vivo. PLoS Genet. 8, e1002627
35. Zhou, X., Zolotukhin, I., Im, D. S., and Muzyczka, N. (1999) Biochemical characterization of adeno-associated virus rep68 DNA helicase and ATPase activities. J. Virol. 73, 1580-1590
36. Tuteja, N., and Tuteja, R. (2004) Prokaryotic and eukaryotic DNA helicases. FEBS J. 10.1111/j.1432-1033.2004.04093.x
37. Jiang, Y., and Gralla, J. D. (1995) Nucleotide requirements for activated RNA polymerase II open complex formation in vitro. J. Biol. Chem. 270, 1277-1281
38. Dvir, A., Garrett, K. P., Chalut, C., Egly, J. M., Conaway, J. W., and Conaway, R. C. (1996) A role for ATP and TFIIH in activation of the RNA polymerase II preinitiation complex prior to transcription initiation. J. Biol. Chem. 271, 7245-7248
39. Kostrewa, D., Zeller, M. E., Armache, K.-J., Seizl, M., Leike, K., Thomm, M., and Cramer, P. (2009) RNA polymerase II-TFIIB structure and mechanism of transcription initiation. Nature 462, 323-330
40. Jiang, Y., Yan, M., and Gralla, J. D. (1996) A three-step pathway of transcription initiation leading to promoter clearance at an activation RNA polymerase II promoter. Mol. Cell. Biol. 16, 1614-1621