Space exploration by the promoter of a long human gene during one transcription cycle

Nucleic Acids Research

Volumn 41, Issue 4, 2013, Pages 2216-2227

  Larkin, Joshua D ^a   Papantonis, Argyris ^a,b   Cook, Peter R ^a   Marenduzzo, Davide ^c  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF COLOGNE   (Germany)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

RNA; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; DNA CONFORMATION; DNA SEQUENCE; ENZYME IMMOBILIZATION; GENE; GENE FUNCTION; GENE LOCATION; GENE SWITCHING; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IMAGE ANALYSIS; MOLECULAR MECHANICS; MONTE CARLO METHOD; PRIORITY JOURNAL; PROMOTER REGION; SAMD4A GENE; TRANSCRIPTION INITIATION;

CELLS, CULTURED; DNA-DIRECTED RNA POLYMERASES; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; IN SITU HYBRIDIZATION, FLUORESCENCE; MODELS, GENETIC; MONTE CARLO METHOD; PROMOTER REGIONS, GENETIC; REPRESSOR PROTEINS; RNA; TEMPLATES, GENETIC; TRANSCRIPTION, GENETIC;

EID: 84876402853     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gks1441     Document Type: Article

References (51)

1. Alberts, B., Johnson, A., Lewis, J., Raff, M., Roberts, K. and Walter, P. (2002) Molecular Biology of the Cell. Garland Science, New York.
2. Jackson, D.A., Hassan, A.B., Errington, R.J. and Cook, P.R. (1993) Visualization of focal sites of transcription within human nuclei. EMBO J., 12, 1059-1065.
3. Chakalova, L. and Fraser, P. (2010) Organization of transcription. Cold Spring Harb. Perspect. Biol., 2, a000729.
4. Cook, P.R. (2010) A model for all genomes: the role of transcription factories. J. Mol. Biol., 395, 1-10.
5. Eskiw, C.H., Rapp, A., Carter, D.R. and Cook, P.R. (2008) RNA polymerase II activity is located on the surface of protein-rich transcription factories. J. Cell Sci., 121, 1999-2007.
6. Eskiw, C.H. and Fraser, P. (2011) Ultrastructural study of transcription factories in mouse erythroblasts. J. Cell Sci., 124, 3676-3683.
7. Dekker, J., Rippe, K., Dekker, M. and Kleckner, N. (2002) Capturing chromosome conformation. Science, 295, 1306-1311.
8. Brown, J.M., Leach, J., Reittie, J.E., Atzberger, A., Lee-Prudhoe, J., Wood, W.G., Higgs, D.R., Iborra, F.J. and Buckle, V.J. (2006) Coregulated human globin genes are frequently in spatial proximity when active. J. Cell Biol., 172, 177-187.
9. Simonis, M., Klous, P., Splinter, E., Moshkin, Y., Willemsen, R., de Wit, E., van Steensel, B. and de Laat, W. (2006) Nuclear organization of active and inactive chromatin domains uncovered by chromosome conformation capture-on-chip (4C). Nat. Genet., 38, 1348-1354.
10. Schoenfelder, S., Sexton, T., Chakalova, L., Cope, N.F., Horton, A., Andrews, S., Kurukuti, S., Mitchell, J.A., Umlauf, D., Dimitrova, D.S. et al. (2010) Preferential associations between co-regulated genes reveal a transcriptional interactome in erythroid cells. Nat. Genet., 42, 53-61.
11. Li, G., Ruan, X., Auerbach, R.K., Sandhu, K.S., Zheng, M., Wang, P., Poh, H.-M., Goh, Y., Lim, J., Zhang, J. et al. (2012) Extensive promoter-centered chromatin interactions provide a topological basis for transcription regulation. Cell, 148, 84-98.
12. Melnik, S., Deng, B., Papantonis, A., Baboo, S., Carr, I.M. and Cook, P.R. (2011) The proteomes of transcription factories containing RNA polymerases I, II, or III. Nat. Methods, 8, 962-968.
13. Papantonis, A., Larkin, J.D., Wada, Y., Ohta, Y., Ihara, S., Kodama, T. and Cook, P.R. (2010) Active RNA polymerases: mobile or immobile molecular machines? PLoS Biol., 8, e1000419.
14. Smale, S.T. (2010) Selective transcription in response to an inflammatory stimulus. Cell, 140, 833-844.
15. Wada, Y., Ohta, Y., Xu, M., Tsutsumi, S., Minami, T., Inoue, K., Komura, D., Kitakami, J., Oshida, N., Papantonis, A. et al. (2009) A wave of nascent transcription on activated human genes. Proc. Natl Acad. Sci. USA, 106, 18357-18361.
16. Larkin, J.D., Cook, P.R. and Papantonis, A. (2012) Dynamic reconfiguration of long human genes during one transcription cycle. Mol. Cell. Biol., 32, 2738-2747.
17. Thompson, R.E., Larson, D.R. and Webb, W.W. (2002) Precise nanometer localization analysis for individual fluorescent probes. Biophys. J., 82, 2775-2783.
18. Yildiz, A., Forkey, J.N., McKinney, S.A., Ha, T., Goldman, Y.E. and Selvin, P.R. (2003) Myosin V walks hand-over-hand: single fluorophore imaging with 1.5-nm localization. Science, 300, 2061-2065.
19. Larkin, J.D. and Cook, P.R. (2012) Maximum precision closed-form solution for localizing diffraction-limited spots in noisy images. Opt. Express, 20, 18478-18493.
20. Hagége, H., Klous, P., Braem, C., Splinter, E., Dekker, J., Cathala, G., de Laat, W. and Forné, T. (2007) Quantitative analysis of chromosome conformation capture assays (3C-qPCR). Nat. Protoc., 2, 1722-1733.
21. Chubb, J.R., Trcek, T., Shenoy, S.M. and Singer, R.H. (2006) Transcriptional pulsing of a developmental gene. Curr. Biol., 16, 1018-1025.
22. Raj, A., Peskin, C.S., Tranchina, D., Vargas, D.Y. and Tyagi, S. (2006) Stochastic mRNA synthesis in mammalian cells. PLoS Biol., 4, e309.
23. Zenklusen, D., Larson, D.R. and Singer, R.H. (2008) Single-RNA counting reveals alternative modes of gene expression in yeast. Nat. Struct. Mol. Biol., 15, 1263-1271.
24. Femino, A.M., Fay, F.S., Fogarty, K. and Singer, R.H. (1998) Visualization of single RNA transcripts in situ. Science, 280, 585-590.
25. Rosa, A. and Everaers, R. (2008) Structure and dynamics of interphase chromosomes. PLoS Comput. Biol., 4, e1000153.
26. Bystricky, K., Heun, P., Gehlen, L., Langowski, J. and Gasser, S.M. (2004) Long-range compaction and flexibility of interphase chromatin in budding yeast analyzed by high-resolution imaging techniques. Proc. Natl Acad. Sci. USA, 101, 16495-16500.
27. Cook, P.R. and Marenduzzo, D. (2009) Entropic organization of interphase chromosomes. J. Cell Biol., 186, 825-834.
28. Weidemann, T., Wachsmuth, M., Knoch, T.A., Müller, G., Waldeck, W. and Langowski, J. (2003) Counting nucleosomes in living cells with a combination of fluorescence correlation spectroscopy and confocal imaging. J. Mol. Biol., 334, 229-240.
29. Landau, D.P. and Binder, K. (2000) A Guide to Monte Carlo Simulations in Statistical Physics. Cambridge University Press, New York.
30. Kratky, O. and Porod, G. (1949) Diffuse small-angle scattering of X-rays in colloid systems. J. Colloid Sci., 4, 35-70.
31. Langowski, J. (2006) Polymer chain models of DNA and chromatin. Eur. Phys. J. E Soft Matter, 19, 241-249.
32. Bohn, M. and Heermann, D.W. (2010) Diffusion-driven looping provides a consistent framework for chromatin organization. PLoS One, 5, e12218.
33. Cui, Y. and Bustamante, C. (2000) Pulling a single chromatin fiber reveals the forces that maintain its higher-order structure. Proc. Natl Acad. Sci. USA, 97, 127-132.
34. Doi, M. and Edwards, S.F. (1986) The Theory of Polymer Dynamics. Oxford Science Publications, Cambridge.
35. Mateos-Langerak, J., Manfred Bohn, M., de Leeuw, W., Giromus, O., Manders, E.M.M., Verschure, P.J., Indemans, M.H.G., Gierman, H.J., Heermann, D.W., van Driel, R. et al. (2009) Spatially confined folding of chromatin in the interphase nucleus. Proc. Natl Acad. Sci. USA, 106, 3812-3817.
36. Lieberman-Aiden, E., van Berkum, N.L., Williams, L., Imakaev, M., Ragoczy, T., Telling, A., Amit, I., Lajoie, B.R., Sabo, P.J., Dorschner, M.O. et al. (2009) Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science, 326, 289-293.
37. Göndör, A., Rougier, C. and Ohlsson, R. (2008) High-resolution circular chromosome conformation capture assay. Nat. Protoc., 3, 303-313.
38. Levi, V., Ruan, Q., Plutz, M., Belmont, A.S. and Gratton, E. (2005) Chromatin dynamics in interphase cells revealed by tracking in a two-photon excitation microscope. Biophys. J., 89, 4275-4285.
39. Wachsmuth, M., Caudron-Herger, M. and Rippe, K. (2008) Genome organization: balancing stability and plasticity. Biochim. Biophys. Acta., 1783, 2061-2079.
40. Faro-Trindade, I. and Cook, P.R. (2006) A conserved organization of transcription during embryonic stem cell differentiation and in cells with high C value. Mol. Biol. Cell, 17, 2910-2920.
41. Bon, M., Marenduzzo, D. and Cook, P.R. (2006) Modeling a self-avoiding chromatin loop: relation to the packing problem, action-at-a-distance, and nuclear context. Structure, 14, 197-204.
42. Papantonis, A., Kohro, T., Baboo, S., Larkin, J.D., Deng, B., Short, P., Tsutsumi, S., Taylor, S., Kanki, Y., Kobayashi, M. et al. (2012) TNFa signals through specialized factories where responsive coding and miRNA genes are transcribed. EMBO J., 31, 4404-4414.
43. Raney, B.J., Cline, M.S., Rosenbloom, K.R., Dreszer, T.R., Learned, K., Barber, G.P., Meyer, L.R., Sloan, C.A., Malladi, V.S., Roskin, K.M. et al. (2011) ENCODE whole-genome data in the UCSC genome browser (2011 update). Nucleic Acids Res., 39, D871-D875.
44. Zentner, G.E., Tesar, P.J. and Scacheri, P.C. (2011) Epigenetic signatures distinguish multiple classes of enhancers with distinct cellular functions. Genome Res., 21, 1273-1283.
45. Kim, T.K., Hemberg, M., Gray, J.M., Costa, A.M., Bear, D.M., Wu, J., Harmin, D.A., Laptewicz, M., Barbara-Haley, K. et al. (2010) Widespread transcription at neuronal activity-regulated enhancers. Nature, 465, 182-187.
46. Wang, D., Garcia-Bassets, I., Benner, C., Li, W., Su, X., Zhou, Y., Qiu, J., Liu, W., Kaikkonen, M.U., Ohgi, K.A. et al. (2011) Reprogramming transcription by distinct classes of enhancers functionally defined by eRNA. Nature, 474, 390-394.
47. Ørom, U.A., Derrien, T., Beringer, M., Gumireddy, K., Gardini, A., Bussotti, G., Lai, F., Zytnicki, M., Notredame, C., Huang, Q. et al. (2010) Long noncoding RNAs with enhancer-like function in human cells. Cell, 143, 46-58.
48. Kolovos, P., Knoch, T.A., Grosveld, F.G., Cook, P.R. and Papantonis, A. (2012) Enhancers and silencers: an integrated and simple model for their function. Epigenetics Chromatin, 5, 1.
49. Raj, A. and van Oudenaarden, A. (2008) Stochastic gene expression and its consequences. Cell, 135, 216-226.
50. Finan, K. and Cook, P.R. (2012) In: Rippe, K. (ed.), Transcriptional initiation: frequency, bursting, and transcription factories. Genome Organization and Function in the Cell Nucleus. Wiley-VCH Verlag GmbH & Co, KGaA, Weinheim, Germany, pp. 235-254.
51. Lionnet, T. and Singer, R.H. (2012) Transcription goes digital. EMBO Rep., 13, 313-321.