RNA Polymerase II cluster dynamics predict mRNA output in living cells

eLife

Volumn 5, Issue MAY2016, 2016, Pages

  Cho, Won Ki ^a   Jayanth, Namrata ^a   English, Brian P ^b   Inoue, Takuma ^a   Andrews, J Owen ^a   Conway, William ^a   Grimm, Jonathan B ^b   Spille, Jan Hendrik ^a   Lavis, Luke D ^b   Lionnet, Timothée ^b   Cisse, Ibrahim I ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA ACTIN; MESSENGER RNA; RNA POLYMERASE II; ACTIN;

ALGORITHM; ANIMAL CELL; ARTICLE; CELL CULTURE; CELL SELECTION; CONTROLLED STUDY; CORRELATION ANALYSIS; FIBROBLAST; FLOW CYTOMETRY; FLUORESCENCE IN SITU HYBRIDIZATION; GENE EXPRESSION; GENE LOCUS; HUMAN; MESSENGER RNA SYNTHESIS; MICROSCOPY; MODEL; MOLECULAR GENETICS; MONTE CARLO METHOD; MOUSE; NONHUMAN; PROTEIN EXPRESSION; ANIMAL; BIOSYNTHESIS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY;

ACTINS; ANIMALS; CELLS, CULTURED; FIBROBLASTS; GENE EXPRESSION REGULATION; GENETIC LOCI; MICE; RNA POLYMERASE II; RNA, MESSENGER;

EID: 84979502187     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.13617     Document Type: Article

References (80)

1. Ardehali MB, Lis JT. 2009. Tracking rates of transcription and splicing in vivo. Nature Structural & Molecular Biology 16:1123-1124. doi: 10.1038/nsmb1109-1123
2. Bensaude O. 2011. Inhibiting eukaryotic transcription: Which compound to choose? How to evaluate its activity? Evidence for axonemal distortion during the flagellar b Transcription 2:103-108. doi: 10.4161/trns.2.3.16172
3. Bertrand E, Chartrand P, Schaefer M, Shenoy SM, Singer RH, Long RM. 1998. Localization of ASH1 mRNA particles in living yeast. Molecular Cell 2:437-445. doi: 10.1016/S1097-2765(00)80143-4
4. Betzig E, Patterson GH, Sougrat R, Lindwasser OW, Olenych S, Bonifacino JS, Davidson MW, Lippincott-Schwartz J, Hess HF. 2006. Imaging intracellular fluorescent proteins at nanometer resolution. Science 313:1642-1645. doi: 10.1126/science.1127344
5. Boireau S, Maiuri P, Basyuk E, de la Mata M, Knezevich A, Pradet-Balade B, Bäcker V, Kornblihtt A, Marcello A, Bertrand E. 2007. The transcriptional cycle of HIV-1 in real-time and live cells. The Journal of Cell Biology 179:291-304. doi: 10.1083/jcb.200706018
6. Brody Y, Neufeld N, Bieberstein N, Causse SZ, Böhnlein EM, Neugebauer KM, Darzacq X, Shav-Tal Y. 2011. The in vivo kinetics of RNA polymerase II elongation during co-transcriptional splicing. PLoS Biology 9:e1000573. doi: 10.1371/journal.pbio.1000573
7. Buckley MS, Lis JT. 2014. Imaging RNA Polymerase II transcription sites in living cells. Current Opinion in Genetics & Development 25:126-130. doi: 10.1016/j.gde.2014.01.002
8. Carmo-Fonseca M. 2002. The contribution of nuclear compartmentalization to gene regulation. Cell 108:513-521. doi: 10.1016/S0092-8674(02)00650-5
9. Carter DR, Eskiw C, Cook PR. 2008. Transcription factories. Biochemical Society Transactions 36:585-589. doi:10.1042/BST0360585
10. Chen B, Gilbert LA, Cimini BA, Schnitzbauer J, Zhang W, Li GW, Park J, Blackburn EH, Weissman JS, Qi LS, Huang B. 2013. Dynamic imaging of genomic loci in living human cells by an optimized Crispr/Cas system. Cell 155:1479-1491. doi: 10.1016/j.cell.2013.12.001
11. Chen J, Zhang Z, Li L, Chen BC, Revyakin A, Hajj B, Legant W, Dahan M, Lionnet T, Betzig E, Tjian R, Liu Z. 2014. Single-molecule dynamics of enhanceosome assembly in embryonic stem cells. Cell 156:1274-1285. doi: 10. 1016/j.cell.2014.01.062
12. Chong S, Chen C, Ge H, Xie XS. 2014. Mechanism of transcriptional bursting in bacteria. Cell 158:314-326. doi:10.1016/j.cell.2014.05.038
13. Chudakov DM, Lukyanov S, Lukyanov KA. 2007. Tracking intracellular protein movements using photoswitchable fluorescent proteins PS-CFP2 and Dendra2. Nature Protocols 2:2024-2032. doi: 10.1038/nprot.2007.291
14. Cisse II, Izeddin I, Causse SZ, Boudarene L, Senecal A, Muresan L, Dugast-Darzacq C, Hajj B, Dahan M, Darzacq X. 2013. Real-time dynamics of RNA polymerase II clustering in live human cells. Science 341:664-667. doi: 10. 1126/science.1239053
15. Cook PR. 2010. A model for all genomes: The role of transcription factories. Journal of Molecular Biology 395:1-10. doi: 10.1016/j.jmb.2009.10.031
16. Cremer T, Cremer M, Dietzel S, Müller S, Solovei I, Fakan S. 2006. Chromosome territories-a functional nuclear landscape. Current Opinion in Cell Biology 18:307-316. doi: 10.1016/j.ceb.2006.04.007
17. Danilition SL, Frederickson RM, Taylor CY, Miyamoto NG. 1991. Transcription factor binding and spacing constraints in the human beta-actin proximal promoter. Nucleic Acids Research 19:6913-6922. doi: 10.1093/nar/19.24.6913
18. de Wit E, de Laat W. 2012. A decade of 3C technologies: Insights into nuclear organization. Genes & Development 26:11-24. doi: 10.1101/gad.179804.111
19. DeJesus-Hernandez M, Mackenzie IR, Boeve BF, Boxer AL, Baker M, Rutherford NJ, Nicholson AM, Finch NA, Flynn H, Adamson J, Kouri N, Wojtas A, Sengdy P, Hsiung GY, Karydas A, Seeley WW, Josephs KA, Coppola G, Geschwind DH, Wszolek ZK, et al. 2011. Expanded GGGGCC hexanucleotide repeat in noncoding region of C9ORF72 causes chromosome 9p-linked FTD and ALS. Neuron 72:245-256. doi: 10.1016/j.neuron.2011.09.011
20. Dekker J, Marti-Renom MA, Mirny LA. 2013. Exploring the three-dimensional organization of genomes:Interpreting chromatin interaction data. Nature Reviews. Genetics 14:390-403. doi: 10.1038/nrg3454
21. Edelstein AD, Tsuchida MA, Amodaj N, Pinkard H, Vale RD, Stuurman N. 2014. Advanced methods of microscope control using mManager software. Journal of Biological Methods 1:e10. doi: 10.14440/jbm.2014.36
22. Fazal FM, Meng CA, Murakami K, Kornberg RD, Block SM. 2015. Real-time observation of the initiation of RNA polymerase II transcription. Nature 525:274-277. doi: 10.1038/nature14882
23. Femino AM., Fay FS., Fogarty K, Singer RH. 1998. Visualization of single RNA transcripts in situ. Science 280:585-590. doi: 10.1126/science.280.5363.585
24. Fraser P, Bickmore W. 2007. Nuclear organization of the genome and the potential for gene regulation. Nature 447:413-417. doi: 10.1038/nature05916
25. Fuchs G, Voichek Y, Benjamin S, Gilad S, Amit I, Oren M. 2014. 4sUDRB-seq: Measuring genomewide transcriptional elongation rates and initiation frequencies within cells. Genome Biology 15:R69. doi: 10.1186/gb-2014-15-5-r69
26. Ghamari A, van de Corput MP, Thongjuea S, van Cappellen WA, van Ijcken W, van Haren J, Soler E, Eick D, Lenhard B, Grosveld FG. 2013. In vivo live imaging of RNA polymerase II transcription factories in primary cells. Genes & Development 27:767-777. doi: 10.1101/gad.216200.113
27. Grimm JB, English BP, Chen J, Slaughter JP, Zhang Z, Revyakin A, Patel R, Macklin JJ, Normanno D, Singer RH, Lionnet T, Lavis LD. 2015. A general method to improve fluorophores for live-cell and single-molecule microscopy. Nature Methods 12:244-250. doi: 10.1038/nmeth.3256
28. Guo J, Price DH. 2013. RNA polymerase II transcription elongation control. Chemical Reviews 113:8583-8603. doi: 10.1021/cr400105n
29. Gurskaya NG, Verkhusha VV, Shcheglov AS, Staroverov DB, Chepurnykh TV, Fradkov AF, Lukyanov S, Lukyanov KA. 2006. Engineering of a monomeric green-to-red photoactivatable fluorescent protein induced by blue light. Nature Biotechnology 24:461-465. doi: 10.1038/nbt1191
30. Heilemann M, van de Linde S, Schüttpelz M, Kasper R, Seefeldt B, Mukherjee A, Tinnefeld P, Sauer M. 2008. Subdiffraction-resolution fluorescence imaging with conventional fluorescent probes. Angewandte Chemie 47:6172-6176. doi: 10.1002/anie.200802376
31. Hess ST, Girirajan TP, Mason MD. 2006. Ultra-high resolution imaging by fluorescence photoactivation localization microscopy. Biophysical Journal 91:4258-4272. doi: 10.1529/biophysj.106.091116
32. Iborra FJ, Pombo A, Jackson DA, Cook PR. 1996. Active RNA polymerases are localized within discrete transcription "factories’ in human nuclei. Journal of Cell Science 109:1427-1436.
33. Izeddin I, Darzacq X, Dahan M. 2013. Imaging of single molecules in live cells. Médecine/Sciences 27:547-552.
34. Izeddin I, Récamier V, Bosanac L, Cissé II, Boudarene L, Dugast-Darzacq C, Proux F, Bénichou O, Voituriez R, Bensaude O, Dahan M, Darzacq X. 2014. Single-molecule tracking in live cells reveals distinct target-search strategies of transcription factors in the nucleus. eLife 3:e02230. doi: 10.7554/eLife.02230
35. Jackson DA, Hassan AB, Errington RJ, Cook PR. 1993. Visualization of focal sites of transcription within human nuclei. The EMBO Journal 12:1059-1065.
36. Jonkers I, Kwak H, Lis JT. 2014. Genome-wide dynamics of Pol II elongation and its interplay with promoter proximal pausing, chromatin, and exons. eLife 3:e02407. doi: 10.7554/eLife.02407
37. Kalo A, Kanter I, Shraga A, Sheinberger J, Tzemach H, Kinor N, Singer RH, Lionnet T, Shav-Tal Y. 2015. Cellular levels of signaling factors are sensed by b-actin alleles to modulate transcriptional pulse intensity. Cell Reports 11:419-432. doi: 10.1016/j.celrep.2015.03.039
38. Kennedy BK, Barbie DA, Classon M, Dyson N, Harlow E. 2000. Nuclear organization of DNA replication in primary mammalian cells. Genes & Development 14:2855-2868. doi: 10.1101/gad.842600
39. Kim TH, Barrera LO, Zheng M, Qu C, Singer MA, Richmond TA, Wu Y, Green RD, Ren B. 2005. A high-resolution map of active promoters in the human genome. Nature 436:876-880. doi: 10.1038/nature03877
40. Kimura H, Sugaya K, Cook PR. 2002. The transcription cycle of RNA polymerase II in living cells. The Journal of Cell Biology 159:777-782. doi: 10.1083/jcb.200206019
41. Kumaran RI, Thakar R, Spector DL. 2008. Chromatin dynamics and gene positioning. Cell 132:929-934. doi: 10. 1016/j.cell.2008.03.004
42. Kwak H, Lis JT. 2013. Control of transcriptional elongation. Annual Review of Genetics 47:483-508. doi: 10. 1146/annurev-genet-110711-155440
43. Landgraf D, Okumus B, Chien P, Baker TA, Paulsson J. 2012. Segregation of molecules at cell division reveals native protein localization. Nature Methods 9:480-482. doi: 10.1038/nmeth.1955
44. Larson DR, Zenklusen D, Wu B, Chao JA, Singer RH. 2011. Real-time observation of transcription initiation and elongation on an endogenous yeast gene. Science 332:475-478. doi: 10.1126/science.1202142
45. Lee SH, Shin JY, Lee A, Bustamante C. 2012. Counting single photoactivatable fluorescent molecules by photoactivated localization microscopy (PALM). Proceedings of the National Academy of Sciences of the United States of America 109:17436-17441. doi: 10.1073/pnas.1215175109
46. Li G, Ruan X, Auerbach RK, Sandhu KS, Zheng M, Wang P, Poh HM, Goh Y, Lim J, Zhang J, Sim HS, Peh SQ, Mulawadi FH, Ong CT, Orlov YL, Hong S, Zhang Z, Landt S, Raha D, Euskirchen G, et al. 2012. Extensive promoter-centered chromatin interactions provide a topological basis for transcription regulation. Cell 148:84-98. doi: 10.1016/j.cell.2011.12.014
47. Lieberman-Aiden E, van Berkum NL, Williams L, Imakaev M, Ragoczy T, Telling A, Amit I, Lajoie BR, Sabo PJ, Dorschner MO, Sandstrom R, Bernstein B, Bender MA, Groudine M, Gnirke A, Stamatoyannopoulos J, Mirny LA, Lander ES, Dekker J. 2009. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326:289-293. doi: 10.1126/science.1181369
48. Lionnet T, Wu B, Grünwald D, Singer RH, Larson DR. 2011b. Nuclear Physics: Quantitative Single-Cell Approaches to Nuclear Organization and Gene Expression. Cold Spring Harbor Symposia on Quantitative Biology 75:113-126. doi: 10.1101/sqb.2010.75.057
49. Lionnet T, Czaplinski K, Darzacq X, Shav-Tal Y, Wells AL, Chao JA, Park HY, de Turris V, Lopez-Jones M, Singer RH. 2011a. A transgenic mouse for in vivo detection of endogenous labeled mRNA. Nature Methods 8:165-170. doi: 10.1038/nmeth.1551
50. Liu Z, Legant WR, Chen BC, Li L, Grimm JB, Lavis LD, Betzig E, Tjian R. 2014. 3D imaging of sox2 enhancer clusters in embryonic stem cells. eLife 3:e04236. doi: 10.7554/eLife.04236
51. Mao YS, Zhang B, Spector DL. 2011. Biogenesis and function of nuclear bodies. Trends in Genetics 27:295-306. doi: 10.1016/j.tig.2011.05.006
52. Maxwell CS, Kruesi WS, Core LJ, Kurhanewicz N, Waters CT, Lewarch CL, Antoshechkin I, Lis JT, Meyer BJ, Baugh LR. 2014. Pol II docking and pausing at growth and stress genes in C. elegans. Cell Reports 6:455-466. doi: 10.1016/j.celrep.2014.01.008
53. Misteli T, Soutoglou E. 2009. The emerging role of nuclear architecture in DNA repair and genome maintenance. Nature Reviews. Molecular Cell Biology 10:243-254. doi: 10.1038/nrm2651
54. Mitchell JA, Fraser P. 2008. Transcription factories are nuclear subcompartments that remain in the absence of transcription. Genes & Development 22:20-25. doi: 10.1101/gad.454008
55. Mostoslavsky G, Fabian AJ, Rooney S, Alt FW, Mulligan RC. 2006. Complete correction of murine artemis immunodeficiency by lentiviral vector-mediated gene transfer. Proceedings of the National Academy of Sciences of the United States of America 103:16406-16411. doi: 10.1073/pnas.0608130103
56. Muse GW, Gilchrist DA, Nechaev S, Shah R, Parker JS, Grissom SF, Zeitlinger J, Adelman K. 2007. RNA polymerase is poised for activation across the genome. Nature Genetics 39:1507-1511. doi: 10.1038/ng.2007. 21
57. Oleynikov Y, Singer RH. 2003. Real-time visualization of ZBP1 association with beta-actin mrna during transcription and localization. Current Biology 13:199-207. doi: 10.1016/S0960-9822(03)00044-7
58. Osborne CS, Chakalova L, Brown KE, Carter D, Horton A, Debrand E, Goyenechea B, Mitchell JA, Lopes S, Reik W, Fraser P. 2004. Active genes dynamically colocalize to shared sites of ongoing transcription. Nature Genetics 36:1065-1071. doi: 10.1038/ng1423
59. Papantonis A, Cook PR. 2013. Transcription factories: Genome organization and gene regulation. Chemical Reviews 113:8683-8705. doi: 10.1021/cr300513p
60. Pederson T. 2002. Dynamics and genome-centricity of interchromatin domains in the nucleus. Nature Cell Biology 4:E287-E291. doi: 10.1038/ncb1202-e287
61. Perry MW, Boettiger AN, Bothma JP, Levine M. 2010. Shadow enhancers foster robustness of drosophila gastrulation. Current Biology 20:1562-1567. doi: 10.1016/j.cub.2010.07.043
62. Piatkevich KD, English BP, Malashkevich VN, Xiao H, Almo SC, Singer RH, Verkhusha VV. 2014. Photoswitchable red fluorescent protein with a large Stokes shift. Chemistry & Biology 21:1402-1414. doi: 10.1016/j.chembiol. 2014.08.010
63. Rollins GC, Shin JY, Bustamante C, Pressé S. 2015. Stochastic approach to the molecular counting problem in superresolution microscopy. Proceedings of the National Academy of Sciences of the United States of America 112:E110-E118. doi: 10.1073/pnas.1408071112
64. Rust MJ, Bates M, Zhuang X. 2006. Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM). Nature Methods 3:793-795. doi: 10.1038/nmeth929
65. Schneider R, Grosschedl R. 2007. Dynamics and interplay of nuclear architecture, genome organization, and gene expression. Genes & Development 21:3027-3043. doi: 10.1101/gad.1604607
66. Sengupta P, Jovanovic-Talisman T, Skoko D, Renz M, Veatch SL, Lippincott-Schwartz J. 2011. Probing protein heterogeneity in the plasma membrane using PALM and pair correlation analysis. Nature Methods 8:969-975. doi: 10.1038/nmeth.1704
67. Sergé A, Bertaux N, Rigneault H, Marguet D. 2008. Dynamic multiple-target tracing to probe spatiotemporal cartography of cell membranes. Nature Methods 5:687-694. doi: 10.1038/nmeth.1233
68. Shroff H, Galbraith CG, Galbraith JA, White H, Gillette J, Olenych S, Davidson MW, Betzig E. 2007. Dual-color superresolution imaging of genetically expressed probes within individual adhesion complexes. Proceedings of the National Academy of Sciences of the United States of America 104:20308-20313. doi: 10.1073/pnas. 0710517105
69. Singh J, Padgett RA. 2009. Rates of in situ transcription and splicing in large human genes. Nature Structural & Molecular Biology 16:1128-1133. doi: 10.1038/nsmb.1666
70. Sugaya K, Vigneron M, Cook PR. 2000. Mammalian cell lines expressing functional RNA polymerase II tagged with the green fluorescent protein. Journal of Cell Science 113:2679-2683.
71. Sutherland H, Bickmore WA. 2009. Transcription factories: Gene expression in unions? Nature Reviews. Genetics 10:457-466. doi: 10.1038/nrg2592
72. Thompson RE, Larson DR, Webb WW. 2002. Precise nanometer localization analysis for individual fluorescent probes. Biophysical Journal 82:2775-2783. doi: 10.1016/S0006-3495(02)75618-X
73. Tolhuis B, Palstra RJ, Splinter E, Grosveld F, de Laat W. 2002. Looping and interaction between hypersensitive sites in the active beta-globin locus. Molecular Cell 10:1453-1465. doi: 10.1016/S1097-2765(02)00781-5
74. Veloso A, Kirkconnell KS, Magnuson B, Biewen B, Paulsen MT, Wilson TE, Ljungman M. 2014. Rate of elongation by RNA polymerase II is associated with specific gene features and epigenetic modifications. Genome Research 24:896-905. doi: 10.1101/gr.171405.113
75. Verschure PJ, van Der Kraan I, Manders EM, van Driel R. 1999. Spatial relationship between transcription sites and chromosome territories. The Journal of Cell Biology 147:13-24. doi: 10.1083/jcb.147.1.13
76. Wada Y, Ohta Y, Xu M, Tsutsumi S, Minami T, Inoue K, Komura D, Kitakami J, Oshida N, Papantonis A, Izumi A, Kobayashi M, Meguro H, Kanki Y, Mimura I, Yamamoto K, Mataki C, Hamakubo T, Shirahige K, Aburatani H, et al. 2009. A wave of nascent transcription on activated human genes. Proceedings of the National Academy of Sciences of the United States of America 106:18357-18361. doi: 10.1073/pnas.0902573106
77. Zeitlinger J, Stark A, Kellis M, Hong JW, Nechaev S, Adelman K, Levine M, Young RA. 2007. RNA polymerase stalling at developmental control genes in the Drosophila melanogaster embryo. Nature Genetics 39:1512-1516. doi: 10.1038/ng.2007.26
78. Zenklusen D, Larson DR, Singer RH. 2008. Single-RNA counting reveals alternative modes of gene expression in yeast. Nature Structural & Molecular Biology 15:1263-1271. doi: 10.1038/nsmb.1514
79. Zhang L, Gurskaya NG, Merzlyak EM, Staroverov DB, Mudrik NN, Samarkina ON, Vinokurov LM, Lukyanov S, Lukyanov KA. 2007. Method for real-time monitoring of protein degradation at the single cell level. BioTechniques 42:446-450. doi: 10.2144/000112453
80. Zhao ZW, Roy R, Gebhardt JC, Suter DM, Chapman AR, Xie XS. 2014. Spatial organization of RNA polymerase II inside a mammalian cell nucleus revealed by reflected light-sheet superresolution microscopy. Proceedings of the National Academy of Sciences of the United States of America 111:681-686. doi: 10.1073/pnas. 1318496111