In vivo live imaging of RNA polymerase II transcription factories in primary cells

Genes and Development

Volumn 27, Issue 7, 2013, Pages 767-777

  Ghamari, Alireza ^a   van de Corput, MariËtte P C ^a   Thongjuea, Supat ^b   Van Cappellen, Wiggert A ^a   Van Ijcken, Wilfred ^a   Van Haren, Jeffrey ^a   Soler, Eric ^a   Eick, Dirk ^c   Lenhard, Boris ^b   Grosveld, Frank G ^a,d,e,f  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b UNIVERSITY OF BERGEN   (Norway)

^c Munich Center for Integrated Protein Science   (Germany)

^d Centre for Biomedical Genetics   (Netherlands)

^e Center for Cancer Genomics   (Netherlands)

^f Netherlands Consortium for Systems Biology   (Netherlands)

Author keywords

Live imaging; RNA polymerase II; Transcription factory

Indexed keywords

CYCLIN DEPENDENT KINASE 7; CYCLIN DEPENDENT KINASE 9; RNA POLYMERASE II; SERINE DERIVATIVE;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL TYPE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA MODIFICATION; EMBRYO; ENZYME ACTIVITY; FLUORESCENCE; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; PRIMARY CELL CULTURE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; TRANSCRIPTION INITIATION;

ANIMALS; CELLS, CULTURED; CYCLIN-DEPENDENT KINASE 9; EMBRYONIC STEM CELLS; LUMINESCENT PROTEINS; MICE; MICROSCOPY, FLUORESCENCE; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RNA POLYMERASE II; TIME-LAPSE IMAGING; TRANSCRIPTION, GENETIC;

MUS;

EID: 84876276025     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.216200.113     Document Type: Article

References (51)

1. Bartkowiak B, Liu P, Phatnani HP, Fuda NJ, Cooper JJ, Price DH, Adelman K, Lis JT, Greenleaf AL. 2010. CDK12 is a transcription elongation-associated CTD kinase, the metazoan ortholog of yeast Ctk1. Genes Dev 24: 2303-2316.
2. Baumli S, Lolli G, Lowe ED, Troiani S, Rusconi L, Bullock AN, Debreczeni JE, Knapp S, Johnson LN. 2008. The structure of P-TEFb (CDK9/cyclin T1), its complex with flavopiridol and regulation by phosphorylation. EMBO J 27: 1907-1918.
3. Brookes E, Pombo A. 2009. Modifications of RNA polymerase II are pivotal in regulating gene expression states. EMBO Rep 10: 1213-1219.
4. Brown JM, Green J, das Neves RP, Wallace HA, Smith AJ, Hughes J, Gray N, Taylor S, Wood WG, Higgs DR, et al. 2008. Association between active genes occurs at nuclear speckles and is modulated by chromatin environment. J Cell Biol 182: 1083-1097.
5. Chandler D. 2005. Interfaces and the driving force of hydrophobic assembly. Nature 437: 640-647.
6. Chao SH, Price DH. 2001. Flavopiridol inactivates P-TEFb and blocks most RNA polymerase II transcription in vivo. J Biol Chem 276: 31793-31799.
7. Chapman RD, Heidemann M, Albert TK, Mailhammer R, Flatley A, Meisterernst M, Kremmer E, Eick D. 2007. Transcribing RNA polymerase II is phosphorylated at CTD residue serine-7. Science 318: 1780-1782.
8. de Krom M, van de Corput M, von Lindern M, Grosveld F, Strouboulis J. 2002. Stochastic patterns in globin gene expression are established prior to transcriptional activation and are clonally inherited. Mol Cell 9: 1319-1326.
9. Eskiw CH, Rapp A, Carter DR, Cook PR. 2008. RNA polymerase II activity is located on the surface of protein-rich transcription factories. J Cell Sci 121: 1999-2007.
10. Ferrai C, Xie SQ, Luraghi P, Munari D, Ramirez F, Branco MR, Pombo A, Crippa MP. 2010. Poised transcription factories prime silent uPA gene prior to activation. PLoS Biol 8: e1000270.
11. Fuda NJ, Ardehali MB, Lis JT. 2009. Defining mechanisms that regulate RNA polymerase II transcription in vivo. Nature 461: 186-192.
12. Glover-Cutter K, Larochelle S, Erickson B, Zhang C, Shokat K, Fisher RP, Bentley DL. 2009. 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 29: 5455-5464.
13. Gribnau J, de Boer E, Trimborn T, Wijgerde M, Milot E, Grosveld F, Fraser P. 1998. Chromatin interaction mechanism of transcriptional control in vivo. EMBO J 17: 6020-6027.
14. Herrmann CH, Mancini MA. 2001. The Cdk9 and cyclin T subunits of TAK/P-TEFb localize to splicing factor-rich nuclear speckle regions. J Cell Sci 114: 1491-1503.
15. Iborra FJ, Pombo A, Jackson DA, Cook PR. 1996a. Active RNA polymerases are localized within discrete transcription 'factories' in human nuclei. J Cell Sci 109: 1427-1436.
16. Iborra FJ, Pombo A, McManus J, Jackson DA, Cook PR. 1996b. The topology of transcription by immobilized polymerases. Exp Cell Res 229: 167-173.
17. Jackson DA, Cook PR. 1985. Transcription occurs at a nucleoskeleton. EMBO J 4: 919-925.
18. Jackson DA, Hassan AB, Errington RJ, Cook PR. 1993. Visualization of focal sites of transcription within human nuclei. EMBO J 12: 1059-1065.
19. Kimura H, Tao Y, Roeder RG, Cook PR. 1999. Quantitation of RNA polymerase II and its transcription factors in an HeLa cell: Little soluble holoenzyme but significant amounts of polymerases attached to the nuclear substructure. Mol Cell Biol 19: 5383-5392.
20. Kohoutek J, Blazek D. 2012. Cyclin K goes with Cdk12 and Cdk13. Cell Div 7: 12.
21. Komarnitsky P, Cho EJ, Buratowski S. 2000. Different phosphorylated forms of RNA polymerase II and associated mRNA processing factors during transcription. Genes Dev 14: 2452-2460.
22. Langmead B, Trapnell C, Pop M, Salzberg SL. 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25.
23. Larochelle S, Amat R, Glover-Cutter K, Sanso M, Zhang C, Allen JJ, Shokat KM, Bentley DL, Fisher RP. 2012. Cyclin-dependent kinase control of the initiation-to-elongation switch of RNA polymerase II. Nat Struct Mol Biol 19: 1108-1115.
24. Marenduzzo D, Finan K, Cook PR. 2006. The depletion attraction: An underappreciated force driving cellular organization. J Cell Biol 175: 681-686.
25. Marshall NF, Peng J, Xie Z, Price DH. 1996. Control of RNA polymerase II elongation potential by a novel carboxylterminal domain kinase. J Biol Chem 271: 27176-27183.
26. Michels AA, Fraldi A, Li Q, Adamson TE, Bonnet F, Nguyen VT, Sedore SC, Price JP, Price DH, Lania L, et al. 2004. Binding of the 7SK snRNA turns the HEXIM1 protein into a P-TEFb (CDK9/cyclin T) inhibitor. EMBO J 23: 2608-2619.
27. Minton AP. 2006. How can biochemical reactions within cells differ from those in test tubes? J Cell Sci 119: 2863-2869.
28. Misteli T. 2001. The concept of self-organization in cellular architecture. J Cell Biol 155: 181-185.
29. Mitchell JA, Fraser P. 2008. Transcription factories are nuclear subcompartments that remain in the absence of transcription. Genes Dev 22: 20-25.
30. Morgan M, Anders S, Lawrence M, Aboyoun P, Pages H, Gentleman R. 2009. ShortRead: A bioconductor package for input, quality assessment and exploration of high-throughput sequence data. Bioinformatics 25: 2607-2608.
31. Nechaev S, Adelman K. 2011. Pol II waiting in the starting gates: Regulating the transition from transcription initiation into productive elongation. Biochim Biophys Acta 1809: 34-45.
32. Noordermeer D, de Wit E, Klous P, van de Werken H, Simonis M, Lopez-Jones M, Eussen B, de Klein A, Singer RH, de Laat W. 2011. Variegated gene expression caused by cell-specific long-range DNA interactions. Nat Cell Biol 13: 944-951.
33. Osborne CS, Chakalova L, Brown KE, Carter D, Horton A, Debrand E, Goyenechea B, Mitchell JA, Lopes S, Reik W, et al. 2004. Active genes dynamically colocalize to shared sites of ongoing transcription. Nat Genet 36: 1065-1071.
34. Osborne CS, Chakalova L, Mitchell JA, Horton A, Wood AL, Bolland DJ, Corcoran AE, Fraser P. 2007. Myc dynamically and preferentially relocates to a transcription factory occupied by Igh. PLoS Biol 5: e192.
35. Papantonis A, Larkin JD, Wada Y, Ohta Y, Ihara S, Kodama T, Cook PR. 2010. Active RNA polymerases: Mobile or immobile molecular machines? PLoS Biol 8: e1000419.
36. Peterlin BM, Price DH. 2006. Controlling the elongation phase of transcription with P-TEFb. Mol Cell 23: 297-305.
37. Ragoczy T, Bender MA, Telling A, Byron R, Groudine M. 2006. The locus control region is required for association of the murine b-globin locus with engaged transcription factories during erythroid maturation. Genes Dev 20: 1447-1457.
38. Rahl PB, Lin CY, Seila AC, Flynn RA, McCuine S, Burge CB, Sharp PA, Young RA. 2010. c-Myc regulates transcriptional pause release. Cell 141: 432-445.
39. Rippe K. 2007. Dynamic organization of the cell nucleus. Curr Opin Genet Dev 17: 373-380.
40. Rozowsky J, Euskirchen G, Auerbach RK, Zhang ZD, Gibson T, Bjornson R, Carriero N, Snyder M, Gerstein MB. 2009. PeakSeq enables systematic scoring of ChIP-seq experiments relative to controls. Nat Biotechnol 27: 66-75.
41. Schoenfelder S, Clay I, Fraser P. 2010a. The transcriptional interactome: Gene expression in 3D. Curr Opin Genet Dev 20: 127-133.
42. Schoenfelder S, Sexton T, Chakalova L, Cope NF, Horton A, Andrews S, Kurukuti S, Mitchell JA, Umlauf D, Dimitrova DS, et al. 2010b. Preferential associations between co-regulated genes reveal a transcriptional interactome in erythroid cells. Nat Genet 42: 53-61.
43. Soler E, Andrieu-Soler C, de Boer E, Bryne JC, Thongjuea S, Stadhouders R, Palstra RJ, Stevens M, Kockx C, van Ijcken W, et al. 2010. The genome-wide dynamics of the binding of Ldb1 complexes during erythroid differentiation. Genes Dev 24: 277-289.
44. Soler E, Andrieu-Soler C, Boer E, Bryne JC, Thongjuea S, Rijkers E, Demmers J, Ijcken W, Grosveld F. 2011. A systems approach to analyze transcription factors in mammalian cells. Methods 53: 151-162.
45. Spector DL, Lamond AI. 2011. Nuclear speckles. Cold Spring Harb Perspect Biol 3: a000646.
46. Stadhouders R, Thongjuea S, Andrieu-Soler C, Palstra RJ, Bryne JC, van den Heuvel A, Stevens M, de Boer E, Kockx C, van der Sloot A, et al. 2012. Dynamic long-range chromatin interactions control Myb proto-oncogene transcription during erythroid development. EMBO J 31: 986-999.
47. Tan-Wong SM, Zaugg JB, Camblong J, Xu Z, Zhang DW, Mischo HE, Ansari AZ, Luscombe NM, Steinmetz LM, Proudfoot NJ. 2012. Gene loops enhance transcriptional directionality. Science 338: 671-675.
48. van de Corput MP, Grosveld FG. 2001. Fluorescence in situ hybridization analysis of transcript dynamics in cells. Methods 25: 111-118.
49. Wansink DG, Schul W, van der Kraan I, van Steensel B, van Driel R, de Jong L. 1993. Fluorescent labeling of nascent RNA reveals transcription by RNA polymerase II in domains scattered throughout the nucleus. J Cell Biol 122: 283-293.
50. Yamada T, Yamaguchi Y, Inukai N, Okamoto S, Mura T, Handa H. 2006. P-TEFb-mediated phosphorylation of hSpt5 C-terminal repeats is critical for processive transcription elongation. Mol Cell 21: 227-237.
51. Yik JH, Chen R, Nishimura R, Jennings JL, Link AJ, Zhou Q. 2003. Inhibition of P-TEFb (CDK9/Cyclin T) kinase and RNA polymerase II transcription by the coordinated actions of HEXIM1 and 7SK snRNA. Mol Cell 12: 971-982.