Rapid dynamics of general transcription factor TFIIB binding during preinitiation complex assembly revealed by single-molecule analysis

Genes and Development

Volumn 30, Issue 18, 2016, Pages 2106-2118

  Zhang, Zhengjian ^a   English, Brian P ^a   Grimm, Jonathan B ^a   Kazane, Stephanie A ^b   Hu, Wenxin ^a   Tsai, Albert ^a   Inouye, Carla ^c   You, Changjiang ^d   Piehler, Jacob ^d   Schultz, Peter G ^b   Lavis, Luke D ^a   Revyakin, Andrey ^e   Tjian, Robert ^a,c  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF OSNABRÜCK   (Germany)

^e UNIVERSITY OF LEICESTER   (United Kingdom)

Author keywords

Dynamic analysis; Fluorescence imaging; In vitro reconstitution; Preinitiation complex; Single molecule; Transcription

Indexed keywords

DNA; RNA POLYMERASE II; TATA BINDING PROTEIN; TRANSCRIPTION FACTOR IIA; TRANSCRIPTION FACTOR IIB; TRANSCRIPTION FACTOR IID; PROTEIN BINDING; TRANSCRIPTION FACTOR II;

ARTICLE; CONTROLLED STUDY; DNA BINDING; IN VITRO STUDY; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN DNA INTERACTION; TRANSCRIPTION INITIATION; GENE DELETION; HUMAN; INTERFERENCE MICROSCOPY; METABOLISM; PHYSIOLOGY; PROTEIN MULTIMERIZATION; TIME FACTOR; TUMOR CELL LINE;

CELL LINE, TUMOR; HUMANS; MICROSCOPY, INTERFERENCE; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTEIN MULTIMERIZATION; RNA POLYMERASE II; SEQUENCE DELETION; TIME FACTORS; TRANSCRIPTION FACTORS, TFII; TRANSCRIPTIONAL ACTIVATION;

EID: 84990987757     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.285395.116     Document Type: Article

References (57)

1. Albright SR, Tjian R. 2000. TAFs revisited: more data reveal new twists and confirm old ideas. Gene 242: 1-13.
2. Bagby S, Mal TK, Liu D, Raddatz E, Nakatani Y, Ikura M. 2000. TFIIA-TAF regulatory interplay: NMR evidence for overlapping binding sites on TBP. FEBS Lett 468: 149-154.
3. Blair RH, Goodrich JA, Kugel JF. 2012. Single-molecule fluorescence resonance energy transfer shows uniformity in TATA binding protein-induced DNA bending and heterogeneity in bending kinetics. Biochemistry 51: 7444-7455.
4. Buratowski S, Hahn S, Guarente L, Sharp PA. 1989. Five intermediate complexes in transcription initiation by RNA polymerase II. Cell 56: 549-561.
5. Cabart P, Ujvari A, Pal M, Luse DS. 2011. Transcription factor TFIIF is not required for initiation by RNA polymerase II, but it is essential to stabilize transcription factor TFIIB in early elongation complexes. Proc Natl Acad Sci 108: 15786-15791.
6. Chen HT, Hahn S. 2003. Binding of TFIIB to RNA polymerase II: mapping the binding site for the TFIIB zinc ribbon domain within the preinitiation complex. Mol Cell 12: 437-447.
7. Chen D, Hinkley CS, HenryRW, Huang S. 2002. TBP dynamics in living human cells: constitutive association of TBP with mitotic chromosomes. Mol Biol Cell 13: 276-284.
8. Chen J, Zhang Z, Li L, Chen BC, Revyakin A, Hajj B, Legant W, Dahan M, Lionnet T, Betzig E, et al. 2014. Single-molecule dynamics of enhanceosome assembly in embryonic stem cells. Cell 156: 1274-1285.
9. Cianfrocco MA, Kassavetis GA, Grob P, Fang J, Juven-Gershon T, Kadonaga JT, Nogales E. 2013. Human TFIID binds to core promoter DNA in a reorganized structural state. Cell 152: 120-131.
10. Coleman RA, Pugh BF. 1995. Evidence for functional binding and stable sliding of the TATA binding protein on nonspecific DNA. J Biol Chem 270: 13850-13859.
11. Coleman RA, Pugh BF. 1997. Slow dimer dissociation of the TATA binding protein dictates the kinetics of DNA binding. Proc Natl Acad Sci 94: 7221-7226.
12. Coleman RA, Taggart AK, Burma S, Chicca JJ II, Pugh BF. 1999. TFIIA regulates TBP and TFIID dimers. Mol Cell 4: 451-457.
13. Dedecker P, Duwe S, Neely RK, Zhang J. 2012. Localizer: fast, accurate, open-source, and modular software package for superresolution microscopy. J Biomed Opt 17: 126008.
14. Deng W, Roberts SG. 2006. Core promoter elements recognized by transcription factor IIB. Biochem Soc Trans 34: 1051-1053.
15. El Beheiry M, Dahan M. 2013. ViSP: representing single-particle localizations in three dimensions. Nat Methods 10: 689-690.
16. Elf J, Li GW, Xie XS. 2007. Probing transcription factor dynamics at the single-molecule level in a living cell. Science 316: 1191-1194.
17. Elsby LM, O’Donnell AJ, Green LM, Sharrocks AD, Roberts SG. 2006. Assembly of transcription factor IIB at a promoter in vivo requires contact with RNA polymerase II. EMBO Rep 7: 898-903.
18. English BP, Singer RH. 2015. A three-camera imaging microscope for high-speed single-molecule tracking and super-resolution imaging in living cells. Proc SPIE Int Soc Opt Eng 9550: 955008.
19. Friedman LJ, Gelles J. 2015. Multi-wavelength single-molecule fluorescence analysis of transcription mechanisms. Methods 86: 27-36.
20. Geiger JH, Hahn S, Lee S, Sigler PB. 1996. Crystal structure of the yeast TFIIA/TBP/DNA complex. Science 272: 830-836.
21. GrimmJB, English BP, Chen J, Slaughter JP, Zhang Z, Revyakin A, Patel R, Macklin JJ, Normanno D, Singer RH, et al. 2015. A general method to improve fluorophores for live-cell and singlemolecule microscopy. Nat Methods 12: 244-250.
22. Guglielmi B, La Rochelle N, Tjian R. 2013. Gene-specific transcriptional mechanisms at the histone gene cluster revealed by single-cell imaging. Mol Cell 51: 480-492.
23. Hawley DK, Roeder RG. 1987. Functional steps in transcription initiation and reinitiation from the major late promoter in a HeLa nuclear extract. J Biol Chem 262: 3452-3461.
24. Hayashi-Takanaka Y, Yamagata K, Wakayama T, Stasevich TJ, Kainuma T, Tsurimoto T, Tachibana M, Shinkai Y, Kurumizaka H, Nozaki N, et al. 2011. Tracking epigenetic histone modifications in single cells using Fab-based live endogenous modification labeling. Nucleic Acids Res 39: 6475-6488.
25. He Y, Yan C, Fang J, Inouye C, Tjian R, Ivanov I, Nogales E. 2016. Near-atomic resolution visualization of human transcription promoter opening. Nature 533: 359-365.
26. Horn AE, Kugel JF, Goodrich JA. 2016. Single molecule microscopy reveals mechanistic insight into RNA polymerase II preinitiation complex assembly and transcriptional activity. Nucleic Acids Res 44: 7132-7143.
27. Jacobson RH, Ladurner AG, King DS, Tjian R. 2000. Structure and function of a human TAFII250 double bromodomain module. Science 288: 1422-1425.
28. Juven-Gershon T, Kadonaga JT. 2010. Regulation of gene expression via the core promoter and the basal transcriptional machinery. Dev Biol 339: 225-229.
29. Juven-Gershon T, Cheng S, Kadonaga JT. 2006. Rational design of a super core promoter that enhances gene expression. Nat Methods 3: 917-922.
30. Kim TK, Ebright RH, Reinberg D. 2000. Mechanism of ATP-dependent promoter melting by transcription factor IIH. Science 288: 1418-1422.
31. Kosa PF, Ghosh G, Dedecker BS, Sigler PB. 1997. The 2.1-Å crystal structure of an archaeal preinitiation complex: TATA-boxbinding protein/transcription factor (II)B core/TATA-box. Proc Natl Acad Sci 94: 6042-6047.
32. Lagrange T, Kapanidis AN, Tang H, Reinberg D, Ebright RH. 1998. New core promoter element in RNA polymerase II-dependent transcription: sequence-specific DNA binding by transcription factor IIB. Genes Dev 12: 34-44.
33. Larson DR, Fritzsch C, Sun L, Meng X, Lawrence DS, Singer RH. 2013. Direct observation of frequency modulated transcription in single cells using light activation. Elife 2: e00750.
34. Lauberth SM, Nakayama T,Wu X, Ferris AL, Tang Z, Hughes SH, Roeder RG. 2013. H3K4me3 interactions with TAF3 regulate preinitiation complex assembly and selective gene activation. Cell 152: 1021-1036.
35. Lin YS, Ha I, Maldonado E, Reinberg D, Green MR. 1991. Binding of general transcription factor TFIIB to an acidic activating region. Nature 353: 569-571.
36. Liu D, Ishima R, Tong KI, Bagby S, Kokubo T, Muhandiram DR, Kay LE, Nakatani Y, Ikura M. 1998. Solution structure of a TBP-TAF(II)230 complex: protein mimicry of the minor groove surface of the TATA box unwound by TBP. Cell 94: 573-583.
37. Louder RK, He Y, Lopez-Blanco JR, Fang J, Chacon P, Nogales E. 2016. Structure of promoter-bound TFIID and model of human pre-initiation complex assembly. Nature 531: 604-609.
38. Matangkasombut O, Auty R, Buratowski S. 2004. Structure and function of the TFIID complex. Adv Protein Chem 67: 67-92.
39. Mortensen KI, Churchman LS, Spudich JA, Flyvbjerg H. 2010. Optimized localization analysis for single-molecule tracking and super-resolution microscopy. Nat Methods 7: 377-381.
40. Nakajima N, Horikoshi M, Roeder RG. 1988. Factors involved in specific transcription by mammalian RNA polymerase II: purification, genetic specificity, and TATA box-promoter interactions of TFIID. Mol Cell Biol 8: 4028-4040.
41. Parvin JD, Sharp PA. 1993. DNA topology and a minimal set of basal factors for transcription by RNA polymerase II. Cell 73: 533-540.
42. Presolski SI, Hong VP, Finn MG. 2011. Copper-catalyzed azide-alkyne click chemistry for bioconjugation. Curr Protoc Chem Biol 3: 153-162.
43. Purnell BA, Emanuel PA, Gilmour DS. 1994. TFIID sequence recognition of the initiator and sequences farther downstream in Drosophila class II genes. Genes Dev 8: 830-842.
44. Revyakin A, Zhang Z, Coleman RA, Li Y, Inouye C, Lucas JK, Park SR, Chu S, Tjian R. 2012. Transcription initiation by human RNA polymerase II visualized at single-molecule resolution. Genes Dev 26: 1691-1702.
45. Robert F, Douziech M, Forget D, Egly JM, Greenblatt J, Burton ZF, Coulombe B. 1998. Wrapping of promoter DNA around the RNA polymerase II initiation complex induced by TFIIF. Mol Cell 2: 341-351.
46. Sainsbury S, Niesser J, Cramer P. 2013. Structure and function of the initially transcribing RNA polymerase II-TFIIB complex. Nature 493: 437-440.
47. Tan S, HunzikerY, Sargent DF, Richmond TJ. 1996. Crystal structureofayeastTFIIA/TBP/DNAcomplex. Nature381:127-151.
48. Thomas MC, Chiang CM. 2006. The general transcription machinery and general cofactors. Crit Rev Biochem Mol Biol 41: 105-178.
49. Tsai FT, Sigler PB. 2000. Structural basis of preinitiation complex assembly on human pol II promoters. EMBO J 19: 25-36.
50. Tsai A, Petrov A, Marshall RA, Korlach J, Uemura S, Puglisi JD. 2012. Heterogeneous pathways and timing of factor departure during translation initiation. Nature 487: 390-393.
51. Werner F, Grohmann D. 2011. Evolution of multisubunit RNA polymerases in the three domains of life. Nat Rev Microbiol 9: 85-98.
52. Wilson CJ, Chao DM, Imbalzano AN, Schnitzler GR, Kingston RE, Young RA. 1996. RNA polymerase II holoenzyme contains SWI/SNF regulators involved in chromatin remodeling. Cell 84: 235-244.
53. WuSY, Kershnar E, Chiang CM. 1998. TAFII-independent activation mediated by human TBP in the presence of the positive cofactor PC4. EMBO J 17: 4478-4490.
54. Xie XS, Choi PJ, LiGW, Lee NK, Lia G. 2008. Single-molecule approach to molecular biology in living bacterial cells. AnnuRev Biophys 37: 417-444.
55. Zhang Z, Revyakin A, Grimm JB, Lavis LD, Tjian R. 2014. Singlemolecule tracking of the transcription cycle by sub-second RNA detection. Elife 3: e01775.
56. Zhang Z, Boskovic Z, Hussain MM, Hu W, Inouye C, Kim HJ, Abole AK, Doud MK, Lewis TA, Koehler AN, et al. 2015. Chemical perturbation of an intrinsically disordered region of TFIID distinguishes two modes of transcription initiation. Elife 4: e07777.
57. Zhao X, Herr W. 2002. A regulated two-step mechanism of TBP binding to DNA: a solvent-exposed surface of TBP inhibits TATA box recognition. Cell 108: 615-627.