The transcription cycle in eukaryotes: From productive initiation to RNA polymerase II recycling

Biochimica et Biophysica Acta - Gene Regulatory Mechanisms

Volumn 1819, Issue 5, 2012, Pages 391-400

  Shandilya, Jayasha ^a   Roberts, Stefan G E ^a  

^a UNIVERSITY AT BUFFALO   (United States)

Author keywords

Gene looping; Promoter; RNA polymerase II; Transcription initiation; Transcription termination; Transcriptional pausing

Indexed keywords

CLEAVAGE AND POLYADENYLATION SPECIFICITY FACTOR; CYCLIN DEPENDENT KINASE 7; CYCLIN DEPENDENT KINASE 9; HISTONE; MESSENGER RNA; POLYNUCLEOTIDE ADENYLYLTRANSFERASE; RNA; RNA POLYMERASE II;

ACETYLATION; CHROMATIN; EUKARYOTE; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENE FUNCTION; GENETIC ANALYSIS; GENETIC TRANSCRIPTION; HUMAN; METHYLATION; NONHUMAN; NUCLEOSOME; PRIORITY JOURNAL; PROTEIN PROCESSING; PROTEIN STRUCTURE; REVIEW;

EUKARYOTA; EUKARYOTIC CELLS; GENE EXPRESSION REGULATION; HUMANS; PROMOTER REGIONS, GENETIC; RNA POLYMERASE II; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EUKARYOTA;

EID: 84859060758     PISSN: 18749399     EISSN: 18764320     Source Type: Journal    
DOI: 10.1016/j.bbagrm.2012.01.010     Document Type: Review

References (88)

1. Thomas M.C., Chiang C.M. The general transcription machinery and general cofactors. Crit. Rev. Biochem. Mol. Biol. 2006, 41:105-178.
2. Juven-Gershon T., Hsu J.Y., Theisen J.W., Kadonaga J.T. The RNA polymerase II core promoter - the gateway to transcription. Curr. Opin. Cell Biol. 2008, 20:253-259.
3. Mathis D.J., Chambon P. The SV40 early region TATA box is required for accurate in vitro initiation of transcription. Nature 1981, 290:310-315.
4. Baumann M., Pontiller J., Ernst W. Structure and basal transcription complex of RNA polymerase II core promoters in the mammalian genome: an overview. Mol. Biotechnol. 2010, 45:241-247.
5. Kuras L., Struhl K. Binding of TBP to promoters in vivo is stimulated by activators and requires Pol II holoenzyme. Nature 1999, 399:609-613.
6. Cang Y., Auble D.T., Prelich G. A new regulatory domain on the TATA-binding protein. EMBO J. 1999, 18:6662-6671.
7. Kraemer S.M., Ranallo R.T., Ogg R.C., Stargell L.A. TFIIA interacts with TFIID via association with TATA-binding protein and TAF40. Mol. Cell. Biol. 2001, 21:1737-1746.
8. Deng W., Malecova B., Oelgeschlager T., Roberts S.G. TFIIB recognition elements control the TFIIA-NC2 axis in transcriptional regulation. Mol. Cell. Biol. 2009, 29:1389-1400.
9. Deng W., Roberts S.G. TFIIB and the regulation of transcription by RNA polymerase II. Chromosoma 2007, 116:417-429.
10. Bushnell D.A., Westover K.D., Davis R.E., Kornberg R.D. Structural basis of transcription: an RNA polymerase II-TFIIB cocrystal at 4.5Angstroms. Science 2004, 303:983-988.
11. Liu X., Bushnell D.A., Wang D., Calero G., Kornberg R.D. Structure of an RNA polymerase II-TFIIB complex and the transcription initiation mechanism. Science 2010, 327:206-209.
12. Kostrewa D., Zeller M.E., Armache K.J., Seizl M., Leike K., Thomm M., Cramer P. RNA polymerase II-TFIIB structure and mechanism of transcription initiation. Nature 2009, 462:323-330.
13. Laine J.P., Egly J.M. When transcription and repair meet: a complex system. Trends Genet. 2006, 22:430-436.
14. Basehoar A.D., Zanton S.J., Pugh B.F. Identification and distinct regulation of yeast TATA box-containing genes. Cell 2004, 116:699-709.
15. Zanton S.J., Pugh B.F. Changes in genomewide occupancy of core transcriptional regulators during heat stress. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:16843-16848.
16. Venters B.J., Wachi S., Mavrich T.N., Andersen B.E., Jena P., Sinnamon A.J., Jain P., Rolleri N.S., Jiang C., Hemeryck-Walsh C., Pugh B.F. A comprehensive genomic binding map of gene and chromatin regulatory proteins in Saccharomyces. Mol Cell 2011, 41:480-492.
17. Venters B.J., Pugh B.F. A canonical promoter organization of the transcription machinery and its regulators in the Saccharomyces genome. Genome Res. 2009, 19:360-371.
18. Zeitlinger J., Stark A., Kellis M., Hong J.W., Nechaev S., Adelman K., Levine M., Young R.A. RNA polymerase stalling at developmental control genes in the Drosophila melanogaster embryo. Nat. Genet. 2007, 39:1512-1516.
19. Core L.J., Waterfall J.J., Lis J.T. Nascent RNA sequencing reveals widespread pausing and divergent initiation at human promoters. Science 2008, 322:1845-1848.
20. Muse G.W., Gilchrist D.A., Nechaev S., Shah R., Parker J.S., Grissom S.F., Zeitlinger J., Adelman K. RNA polymerase is poised for activation across the genome. Nat. Genet. 2007, 39:1507-1511.
21. Glover-Cutter K., Larochelle S., Erickson B., Zhang C., Shokat K., Fisher R.P., Bentley D.L. TFIIH-associated Cdk7 kinase functions in phosphorylation of C-terminal domain Ser7 residues, promoter-proximal pausing, and termination by RNA polymerase II. Mol. Cell. Biol. 2009, 29:5455-5464.
22. Mason P.B., Struhl K. Distinction and relationship between elongation rate and processivity of RNA polymerase II in vivo. Mol. Cell 2005, 17:831-840.
23. Saunders A., Core L.J., Lis J.T. Breaking barriers to transcription elongation. Nat. Rev. Mol. Cell Biol. 2006, 7:557-567.
24. Liu X., Bushnell D.A., Silva D.A., Huang X., Kornberg R.D. Initiation complex structure and promoter proofreading. Science 2011, 333:633-637.
25. Li B., Carey M., Workman J.L. The role of chromatin during transcription. Cell 2007, 128:707-719.
26. Ansari K.I., Mishra B.P., Mandal S.S. MLL histone methylases in gene expression, hormone signaling and cell cycle. Front. Biosci. 2009, 14:3483-3495.
27. Hager G.L., McNally J.G., Misteli T. Transcription dynamics. Mol. Cell 2009, 35:741-753.
28. Clapier C.R., Cairns B.R. The biology of chromatin remodeling complexes. Annu. Rev. Biochem. 2009, 78:273-304.
29. Adkins M.W., Tyler J.K. The histone chaperone Asf1p mediates global chromatin disassembly in vivo. J. Biol. Chem. 2004, 279:52069-52074.
30. Angelov D., Bondarenko V.A., Almagro S., Menoni H., Mongelard F., Hans F., Mietton F., Studitsky V.M., Hamiche A., Dimitrov S., Bouvet P. Nucleolin is a histone chaperone with FACT-like activity and assists remodeling of nucleosomes. EMBO J. 2006, 25:1669-1679.
31. Shandilya J., Gadad S., Swaminathan V., Kundu T.K. Histone chaperones in chromatin dynamics: implications in disease manifestation. Subcell. Biochem. 2007, 41:111-124.
32. McCracken S., Fong N., Yankulov K., Ballantyne S., Pan G., Greenblatt J., Patterson S.D., Wickens M., Bentley D.L. The C-terminal domain of RNA polymerase II couples mRNA processing to transcription. Nature 1997, 385:357-361.
33. Egloff S., Murphy S. Cracking the RNA polymerase II CTD code. Trends Genet. 2008, 24:280-288.
34. Xu Y.X., Manley J.L. Pin1 modulates RNA polymerase II activity during the transcription cycle. Genes Dev. 2007, 21:2950-2962.
35. Gomes N.P., Bjerke G., Llorente B., Szostek S.A., Emerson B.M., Espinosa J.M. Gene-specific requirement for P-TEFb activity and RNA polymerase II phosphorylation within the p53 transcriptional program. Genes Dev. 2006, 20:601-612.
36. Chapman R.D., Heidemann M., Albert T.K., Mailhammer R., Flatley A., Meisterernst M., Kremmer E., Eick D. Transcribing RNA polymerase II is phosphorylated at CTD residue serine-7. Science 2007, 318:1780-1782.
37. Buratowski S. The CTD code. Nat. Struct. Biol. 2003, 10:679-680.
38. Margeat E., Kapanidis A.N., Tinnefeld P., Wang Y., Mukhopadhyay J., Ebright R.H., Weiss S. Direct observation of abortive initiation and promoter escape within single immobilized transcription complexes. Biophys. J. 2006, 90:1419-1431.
39. Ohkuma Y., Roeder R.G. Regulation of TFIIH ATPase and kinase activities by TFIIE during active initiation complex formation. Nature 1994, 368:160-163.
40. Komarnitsky P., Cho E.J., Buratowski S. Different phosphorylated forms of RNA polymerase II and associated mRNA processing factors during transcription. Genes Dev. 2000, 14:2452-2460.
41. Wang Y., Fairley J.A., Roberts S.G. Phosphorylation of TFIIB links transcription initiation and termination. Curr. Biol. 2010, 20:548-553.
42. Lis J.T., Mason P., Peng J., Price D.H., Werner J. P-TEFb kinase recruitment and function at heat shock loci. Genes Dev. 2000, 14:792-803.
43. Yamada T., Yamaguchi Y., Inukai N., Okamoto S., Mura T., Handa H. P-TEFb-mediated phosphorylation of hSpt5 C-terminal repeats is critical for processive transcription elongation. Mol. Cell 2006, 21:227-237.
44. Wen Y., Shatkin A.J. Transcription elongation factor hSPT5 stimulates mRNA capping. Genes Dev. 1999, 13:1774-1779.
45. Chiba K., Yamamoto J., Yamaguchi Y., Handa H. Promoter-proximal pausing and its release: molecular mechanisms and physiological functions. Exp. Cell Res. 2010, 316:2723-2730.
46. Cheng B., Price D.H. Properties of RNA polymerase II elongation complexes before and after the P-TEFb-mediated transition into productive elongation. J. Biol. Chem. 2007, 282:21901-21912.
47. Peterlin B.M., Price D.H. Controlling the elongation phase of transcription with P-TEFb. Mol. Cell 2006, 23:297-305.
48. Reyes-Reyes M., Hampsey M. Role for the Ssu72 C-terminal domain phosphatase in RNA polymerase II transcription elongation. Mol. Cell. Biol. 2007, 27:926-936.
49. Mosley A.L., Pattenden S.G., Carey M., Venkatesh S., Gilmore J.M., Florens L., Workman J.L., Washburn M.P. Rtr1 is a CTD phosphatase that regulates RNA polymerase II during the transition from serine 5 to serine 2 phosphorylation. Mol. Cell 2009, 34:168-178.
50. Jeronimo C., Forget D., Bouchard A., Li Q., Chua G., Poitras C., Therien C., Bergeron D., Bourassa S., Greenblatt J., Chabot B., Poirier G.G., Hughes T.R., Blanchette M., Price D.H., Coulombe B. Systematic analysis of the protein interaction network for the human transcription machinery reveals the identity of the 7SK capping enzyme. Mol. Cell 2007, 27:262-274.
51. Fuda N.J., Ardehali M.B., Lis J.T. Defining mechanisms that regulate RNA polymerase II transcription in vivo. Nature 2009, 461:186-192.
52. Kaplan C.D., Laprade L., Winston F. Transcription elongation factors repress transcription initiation from cryptic sites. Science 2003, 301:1096-1099.
53. Schwabish M.A., Struhl K. Evidence for eviction and rapid deposition of histones upon transcriptional elongation by RNA polymerase II. Mol. Cell. Biol. 2004, 24:10111-10117.
54. Carrozza M.J., Li B., Florens L., Suganuma T., Swanson S.K., Lee K.K., Shia W.J., Anderson S., Yates J., Washburn M.P., Workman J.L. Histone H3 methylation by Set2 directs deacetylation of coding regions by Rpd3S to suppress spurious intragenic transcription. Cell 2005, 123:581-592.
55. Ardehali M.B., Lis J.T. Tracking rates of transcription and splicing in vivo. Nat. Struct. Mol. Biol. 2009, 16:1123-1124.
56. Kuehner J.N., Pearson E.L., Moore C. Unravelling the means to an end: RNA polymerase II transcription termination. Nat. Rev. Mol. Cell Biol. 2011, 12:283-294.
57. Ahn S.H., Kim M., Buratowski S. Phosphorylation of serine 2 within the RNA polymerase II C-terminal domain couples transcription and 3' end processing. Mol. Cell 2004, 13:67-76.
58. Nag A., Narsinh K., Martinson H.G. The poly(A)-dependent transcriptional pause is mediated by CPSF acting on the body of the polymerase. Nat. Struct. Mol. Biol. 2007, 14:662-669.
59. Vasiljeva L., Buratowski S. Nrd1 interacts with the nuclear exosome for 3' processing of RNA polymerase II transcripts. Mol. Cell 2006, 21:239-248.
60. Marquardt S., Hazelbaker D.Z., Buratowski S. Distinct RNA degradation pathways and 3' extensions of yeast non-coding RNA species. Transcription 2011, 2:145-154.
61. Egloff S., O'Reilly D., Chapman R.D., Taylor A., Tanzhaus K., Pitts L., Eick D., Murphy S. Serine-7 of the RNA polymerase II CTD is specifically required for snRNA gene expression. Science 2007, 318:1777-1779.
62. Hsin J.P., Sheth A., Manley J.L. RNAP II CTD phosphorylated on threonine-4 is required for histone mRNA 3' end processing. Science 2011, 334:683-686.
63. Archambault J., Pan G., Dahmus G.K., Cartier M., Marshall N., Zhang S., Dahmus M.E., Greenblatt J. FCP1, the RAP74-interacting subunit of a human protein phosphatase that dephosphorylates the carboxyl-terminal domain of RNA polymerase IIO. J. Biol. Chem. 1998, 273:27593-27601.
64. Meinhart A., Kamenski T., Hoeppner S., Baumli S., Cramer P. A structural perspective of CTD function. Genes Dev. 2005, 19:1401-1415.
65. Sarge K.D., Park-Sarge O.K. Gene bookmarking: keeping the pages open. Trends Biochem. Sci. 2005, 30:605-610.
66. Hahn S. Structure and mechanism of the RNA polymerase II transcription machinery. Nat. Struct. Mol. Biol. 2004, 11:394-403.
67. Yudkovsky N., Ranish J.A., Hahn S. A transcription reinitiation intermediate that is stabilized by activator. Nature 2000, 408:225-229.
68. El Kaderi B., Medler S., Raghunayakula S., Ansari A. Gene looping is conferred by activator-dependent interaction of transcription initiation and termination machineries. J. Biol. Chem. 2009, 284:25015-25025.
69. Calvo O., Manley J.L. Strange bedfellows: polyadenylation factors at the promoter. Genes Dev. 2003, 17:1321-1327.
70. Singh B.N., Hampsey M. A transcription-independent role for TFIIB in gene looping. Mol. Cell 2007, 27:806-816.
71. Malik S., Guermah M., Roeder R.G. A dynamic model for PC4 coactivator function in RNA polymerase II transcription. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:2192-2197.
72. Banerjee S., Kumar B.R., Kundu T.K. General transcriptional coactivator PC4 activates p53 function. Mol. Cell. Biol. 2004, 24:2052-2062.
73. Wang Z., Roeder R.G. DNA topoisomerase I and PC4 can interact with human TFIIIC to promote both accurate termination and transcription reinitiation by RNA polymerase III. Mol. Cell 1998, 1:749-757.
74. He X., Khan A.U., Cheng H., Pappas D.L., Hampsey M., Moore C.L. Functional interactions between the transcription and mRNA 3' end processing machineries mediated by Ssu72 and Sub1. Genes Dev. 2003, 17:1030-1042.
75. Knaus R., Pollock R., Guarente L. Yeast SUB1 is a suppressor of TFIIB mutations and has homology to the human co-activator PC4. EMBO J. 1996, 15:1933-1940.
76. Calvo O., Manley J.L. The transcriptional coactivator PC4/Sub1 has multiple functions in RNA polymerase II transcription. EMBO J. 2005, 24:1009-1020.
77. Osborne C.S., Chakalova L., Brown K.E., Carter D., Horton A., Debrand E., Goyenechea B., Mitchell J.A., Lopes S., Reik W., Fraser P. Active genes dynamically colocalize to shared sites of ongoing transcription. Nat. Genet. 2004, 36:1065-1071.
78. Xu M., Cook P.R. Similar active genes cluster in specialized transcription factories. J. Cell Biol. 2008, 181:615-623.
79. Odawara J., Harada A., Yoshimi T., Maehara K., Tachibana T., Okada S., Akashi K., Ohkawa Y. The classification of mRNA expression levels by the phosphorylation state of RNAPII CTD based on a combined genome-wide approach. BMC Genomics 2011, 12:516.
80. Min I.M., Waterfall J.J., Core L.J., Munroe R.J., Schimenti J., Lis J.T. Regulating RNA polymerase pausing and transcription elongation in embryonic stem cells. Genes Dev. 2011, 25:742-754.
81. Galburt E.A., Grill S.W., Wiedmann A., Lubkowska L., Choy J., Nogales E., Kashlev M., Bustamante C. Backtracking determines the force sensitivity of RNAP II in a factor-dependent manner. Nature 2007, 446:820-823.
82. Hodges C., Bintu L., Lubkowska L., Kashlev M., Bustamante C. Nucleosomal fluctuations govern the transcription dynamics of RNA polymerase II. Science 2009, 325:626-628.
83. Andrecka J., Treutlein B., Arcusa M.A., Muschielok A., Lewis R., Cheung A.C., Cramer P., Michaelis J. Nano positioning system reveals the course of upstream and nontemplate DNA within the RNA polymerase II elongation complex. Nucleic Acids Res. 2009, 37:5803-5809.
84. Wada T., Takagi T., Yamaguchi Y., Ferdous A., Imai T., Hirose S., Sugimoto S., Yano K., Hartzog G.A., Winston F., Buratowski S., Handa H. DSIF, a novel transcription elongation factor that regulates RNA polymerase II processivity, is composed of human Spt4 and Spt5 homologs. Genes Dev. 1998, 12:343-356.
85. Yamaguchi Y., Takagi T., Wada T., Yano K., Furuya A., Sugimoto S., Hasegawa J., Handa H. NELF, a multisubunit complex containing RD, cooperates with DSIF to repress RNA polymerase II elongation. Cell 1999, 97:41-51.
86. Swaminathan V., Reddy B.A., Ruthrotha Selvi B., Sukanya M.S., Kundu T.K. Small molecule modulators in epigenetics: implications in gene expression and therapeutics. Subcell. Biochem. 2007, 41:397-428.
87. Selvi B.R., Mohankrishna D.V., Ostwal Y.B., Kundu T.K. Small molecule modulators of histone acetylation and methylation: a disease perspective. Biochim. Biophys. Acta 2010, 1799:810-828.
88. Rodriguez-Martinez J.A., Peterson-Kaufman K.J., Ansari A.Z. Small-molecule regulators that mimic transcription factors. Biochim. Biophys. Acta 2010, 1799:768-774.