Looping back to leap forward: Transcription enters a new era

Cell

Volumn 157, Issue 1, 2014, Pages 13-25

  Levine, Michael ^a   Cattoglio, Claudia ^a   Tjian, Robert ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; DNA BINDING PROTEIN; MESSENGER RNA; RNA POLYMERASE; RNA POLYMERASE II; TRANSCRIPTION FACTOR;

CELL NUCLEUS; DNA REPAIR; DNA REPLICATION; ENHANCER REGION; GENE; GENE CONTROL; GENE NUMBER; GENETIC ANALYSIS; GENETIC TRANSCRIPTION; HUMAN; HUMAN GENOME; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; REGULATORY DNA SEQUENCE; REGULATORY MECHANISM; REVIEW; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; GENETIC ASSOCIATION; GENETIC IDENTIFICATION; MOLECULAR DYNAMICS;

ANIMALS; CELL DIFFERENTIATION; DNA-DIRECTED RNA POLYMERASES; ENHANCER ELEMENTS, GENETIC; GENE EXPRESSION REGULATION; HUMANS; PROMOTER REGIONS, GENETIC; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84897138228     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2014.02.009     Document Type: Review

References (137)

1. S. Abrahamsson, J. Chen, B. Hajj, S. Stallinga, A.Y. Katsov, J. Wisniewski, G. Mizuguchi, P. Soule, F. Mueller, and C. Dugast Darzacq et al. Fast multicolor 3D imaging using aberration-corrected multifocus microscopy Nat. Methods 10 2013 60 63
2. K. Adelman, and J.T. Lis Promoter-proximal pausing of RNA polymerase II: emerging roles in metazoans Nat. Rev. Genet. 13 2012 720 731
3. T. Amano, T. Sagai, H. Tanabe, Y. Mizushina, H. Nakazawa, and T. Shiroishi Chromosomal dynamics at the Shh locus: limb bud-specific differential regulation of competence and active transcription Dev. Cell 16 2009 47 57
4. G. Andrey, T. Montavon, B. Mascrez, F. Gonzalez, D. Noordermeer, M. Leleu, D. Trono, F. Spitz, and D. Duboule A switch between topological domains underlies HoxD genes collinearity in mouse limbs Science 340 2013 1234167
5. S.L. Ang, A. Wierda, D. Wong, K.A. Stevens, S. Cascio, J. Rossant, and K.S. Zaret The formation and maintenance of the definitive endoderm lineage in the mouse: involvement of HNF3/forkhead proteins Development 119 1993 1301 1315
6. C.D. Arnold, D. Gerlach, C. Stelzer, Ł.M. Boryń, M. Rath, and A. Stark Genome-wide quantitative enhancer activity maps identified by STARR-seq Science 339 2013 1074 1077
7. C. Attanasio, A.S. Nord, Y. Zhu, M.J. Blow, Z. Li, D.K. Liberton, H. Morrison, I. Plajzer-Frick, A. Holt, and R. Hosseini et al. Fine tuning of craniofacial morphology by distant-acting enhancers Science 342 2013 1241006
8. J. Banerji, S. Rusconi, and W. Schaffner Expression of a beta-globin gene is enhanced by remote SV40 DNA sequences Cell 27 1981 299 308
9. F.A. Bava, C. Eliscovich, P.G. Ferreira, B. Miñana, C. Ben-Dov, R. Guigó, J. Valcárcel, and R. Méndez CPEB1 coordinates alternative 3′-UTR formation with translational regulation Nature 495 2013 121 125
10. B.E. Bernstein, E. Birney, I. Dunham, E.D. Green, C. Gunter, M. Snyder ENCODE Project Consortium An integrated encyclopedia of DNA elements in the human genome Nature 489 2012 57 74
11. E. Betzig, G.H. Patterson, R. Sougrat, O.W. Lindwasser, S. Olenych, J.S. Bonifacino, M.W. Davidson, J. Lippincott-Schwartz, and H.F. Hess Imaging intracellular fluorescent proteins at nanometer resolution Science 313 2006 1642 1645
12. M. Bulger, and M. Groudine Functional and mechanistic diversity of distal transcription enhancers Cell 144 2011 327 339
13. D.A. Bushnell, K.D. Westover, R.E. Davis, and R.D. Kornberg Structural basis of transcription: an RNA polymerase II-TFIIB cocrystal at 4.5 Angstroms Science 303 2004 983 988
14. C. Bustamante, W. Cheng, and Y.X. Mejia Revisiting the central dogma one molecule at a time Cell 144 2011 480 497
15. V.C. Calhoun, and M. Levine Long-range enhancer-promoter interactions in the Scr-Antp interval of the Drosophila Antennapedia complex Proc. Natl. Acad. Sci. USA 100 2003 9878 9883
16. E. Calo, and J. Wysocka Modification of enhancer chromatin: what, how, and why? Mol. Cell 49 2013 825 837
17. J.M. Caravaca, G. Donahue, J.S. Becker, X. He, C. Vinson, and K.S. Zaret Bookmarking by specific and nonspecific binding of FOXA1 pioneer factor to mitotic chromosomes Genes Dev. 27 2013 251 260
18. Y.F. Chan, M.E. Marks, F.C. Jones, G. Villarreal Jr., M.D. Shapiro, S.D. Brady, A.M. Southwick, D.M. Absher, J. Grimwood, and J. Schmutz et al. Adaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx1 enhancer Science 327 2010 302 305
19. K. Chen, J. Johnston, W. Shao, S. Meier, C. Staber, and J. Zeitlinger A global change in RNA polymerase II pausing during the Drosophila midblastula transition Elife 2 2013 e00861
20. J. Chen, Z. Zhang, L. Li, B. Chen, A. Revyakin, B. Hajj, W. Legant, M. Dahan, T. Lionnet, and E. Betzig et al. Single-molecule dynamics of enhanceosome assembly in embryonic stem cells Cell 2014 10.1016/j.cell.2014.01.062 Published online March 13, 2014
21. A.C. Cheung, S. Sainsbury, and P. Cramer Structural basis of initial RNA polymerase II transcription EMBO J. 30 2011 4755 4763
22. M.A. Cianfrocco, G.A. Kassavetis, P. Grob, J. Fang, T. Juven-Gershon, J.T. Kadonaga, and E. Nogales Human TFIID binds to core promoter DNA in a reorganized structural state Cell 152 2013 120 131
23. L.A. Cirillo, F.R. Lin, I. Cuesta, D. Friedman, M. Jarnik, and K.S. Zaret Opening of compacted chromatin by early developmental transcription factors HNF3 (FOXA) and GATA-4 Mol. Cell 9 2002 279 289
24. I.I. Cisse, I. Izeddin, S.Z. Causse, L. Boudarene, A. Senecal, L. Muresan, C. Dugast-Darzacq, B. Hajj, M. Dahan, and X. Darzacq Real-time dynamics of RNA polymerase II clustering in live human cells Science 341 2013 664 667
25. P. Cramer Multisubunit RNA polymerases Curr. Opin. Struct. Biol. 12 2002 89 97
26. P. Cramer, D.A. Bushnell, J. Fu, A.L. Gnatt, B. Maier-Davis, N.E. Thompson, R.R. Burgess, A.M. Edwards, P.R. David, and R.D. Kornberg Architecture of RNA polymerase II and implications for the transcription mechanism Science 288 2000 640 649
27. J.A. D'Alessio, K.J. Wright, and R. Tjian Shifting players and paradigms in cell-specific transcription Mol. Cell 36 2009 924 931
28. N. Dahan, and M. Choder The eukaryotic transcriptional machinery regulates mRNA translation and decay in the cytoplasm Biochim. Biophys. Acta 1829 2013 169 173
29. X. Darzacq, J. Yao, D.R. Larson, S.Z. Causse, L. Bosanac, V. de Turris, V.M. Ruda, T. Lionnet, D. Zenklusen, and B. Guglielmi et al. Imaging transcription in living cells Annu. Rev. Biophys. 38 2009 173 196
30. W. de Laat, and D. Duboule Topology of mammalian developmental enhancers and their regulatory landscapes Nature 502 2013 499 506
31. E. de Wit, and W. de Laat A decade of 3C technologies: insights into nuclear organization Genes Dev. 26 2012 11 24
32. M.D. Deato, and R. Tjian Switching of the core transcription machinery during myogenesis Genes Dev. 21 2007 2137 2149
33. G.I. Dellino, D. Cittaro, R. Piccioni, L. Luzi, S. Banfi, S. Segalla, M. Cesaroni, R. Mendoza-Maldonado, M. Giacca, and P.G. Pelicci Genome-wide mapping of human DNA-replication origins: levels of transcription at ORC1 sites regulate origin selection and replication timing Genome Res. 23 2013 1 11
34. W. Deng, J. Lee, H. Wang, J. Miller, A. Reik, P.D. Gregory, A. Dean, and G.A. Blobel Controlling long-range genomic interactions at a native locus by targeted tethering of a looping factor Cell 149 2012 1233 1244
35. A.A. Deniz, S. Mukhopadhyay, and E.A. Lemke Single-molecule biophysics: at the interface of biology, physics and chemistry J. R. Soc. Interface 5 2008 15 45
36. R. Dikstein, S. Zhou, and R. Tjian Human TAFII 105 is a cell type-specific TFIID subunit related to hTAFII130 Cell 87 1996 137 146
37. E.C. Dykhuizen, D.C. Hargreaves, E.L. Miller, K. Cui, A. Korshunov, M. Kool, S. Pfister, Y.J. Cho, K. Zhao, and G.R. Crabtree BAF complexes facilitate decatenation of DNA by topoisomerase IIα Nature 497 2013 624 627
38. W.S. Dynan, and R. Tjian The promoter-specific transcription factor Sp1 binds to upstream sequences in the SV40 early promoter Cell 35 1983 79 87
39. Y.W. Fong, C. Inouye, T. Yamaguchi, C. Cattoglio, I. Grubisic, and R. Tjian A DNA repair complex functions as an Oct4/Sox2 coactivator in embryonic stem cells Cell 147 2011 120 131
40. S.L. Forsburg Eukaryotic MCM proteins: beyond replication initiation Microbiol. Mol. Biol. Rev. 68 2004 109 131
41. L.J. Friedman, and J. Gelles Mechanism of transcription initiation at an activator-dependent promoter defined by single-molecule observation Cell 148 2012 679 689
42. L. Gao, L. Shao, C.D. Higgins, J.S. Poulton, M. Peifer, M.W. Davidson, X. Wu, B. Goldstein, and E. Betzig Noninvasive imaging beyond the diffraction limit of 3D dynamics in thickly fluorescent specimens Cell 151 2012 1370 1385
43. H.G. Garcia, M. Tikhonov, A. Lin, and T. Gregor Quantitative imaging of transcription in living Drosophila embryos links polymerase activity to patterning Curr. Biol. 23 2013 2140 2145
44. J.H. Gibcus, and J. Dekker The hierarchy of the 3D genome Mol. Cell 49 2013 773 782
45. D.M. Gilbert, S.I. Takebayashi, T. Ryba, J. Lu, B.D. Pope, K.A. Wilson, and I. Hiratani Space and time in the nucleus: developmental control of replication timing and chromosome architecture Cold Spring Harb. Symp. Quant. Biol. 75 2010 143 153
46. D.A. Gilchrist, G. Dos Santos, D.C. Fargo, B. Xie, Y. Gao, L. Li, and K. Adelman Pausing of RNA polymerase II disrupts DNA-specified nucleosome organization to enable precise gene regulation Cell 143 2010 540 551
47. A.L. Gnatt, P. Cramer, J. Fu, D.A. Bushnell, and R.D. Kornberg Structural basis of transcription: an RNA polymerase II elongation complex at 3.3 A resolution Science 292 2001 1876 1882
48. J.A. Goodrich, and R. Tjian Unexpected roles for core promoter recognition factors in cell-type-specific transcription and gene regulation Nat. Rev. Genet. 11 2010 549 558
49. M. Groudine, R. Eisenman, R. Gelinas, and H. Weintraub Developmental aspects of chromatin structure and gene expression Prog. Clin. Biol. Res. 134 1983 159 182
50. S. Grünberg, and S. Hahn Structural insights into transcription initiation by RNA polymerase II Trends Biochem. Sci. 38 2013 603 611
51. R. Gualdi, P. Bossard, M. Zheng, Y. Hamada, J.R. Coleman, and K.S. Zaret Hepatic specification of the gut endoderm in vitro: cell signaling and transcriptional control Genes Dev. 10 1996 1670 1682
52. B. Guglielmi, N. La Rochelle, and R. Tjian Gene-specific transcriptional mechanisms at the histone gene cluster revealed by single-cell imaging Mol. Cell 51 2013 480 492
53. Y. Guo, K. Monahan, H. Wu, J. Gertz, K.E. Varley, W. Li, R.M. Myers, T. Maniatis, and Q. Wu CTCF/cohesin-mediated DNA looping is required for protocadherin α promoter choice Proc. Natl. Acad. Sci. USA 109 2012 21081 21086
54. G. Haimovich, M. Choder, R.H. Singer, and T. Trcek The fate of the messenger is pre-determined: a new model for regulation of gene expression Biochim. Biophys. Acta 1829 2013 643 653
55. G. Haimovich, D.A. Medina, S.Z. Causse, M. Garber, G. Millán-Zambrano, O. Barkai, S. Chávez, J.E. Pérez- Ortín, X. Darzacq, and M. Choder Gene expression is circular: factors for mRNA degradation also foster mRNA synthesis Cell 153 2013 1000 1011
56. M.M. Harrison, X.Y. Li, T. Kaplan, M.R. Botchan, and M.B. Eisen Zelda binding in the early Drosophila melanogaster embryo marks regions subsequently activated at the maternal-to-zygotic transition PLoS Genet. 7 2011 e1002266
57. Y. He, J. Fang, D.J. Taatjes, and E. Nogales Structural visualization of key steps in human transcription initiation Nature 495 2013 481 486
58. N.D. Heintzman, G.C. Hon, R.D. Hawkins, P. Kheradpour, A. Stark, L.F. Harp, Z. Ye, L.K. Lee, R.K. Stuart, and C.W. Ching et al. Histone modifications at human enhancers reflect global cell-type-specific gene expression Nature 459 2009 108 112
59. K.M. Herbert, W.J. Greenleaf, and S.M. Block Single-molecule studies of RNA polymerase: motoring along Annu. Rev. Biochem. 77 2008 149 176
60. D. Hnisz, B.J. Abraham, T.I. Lee, A. Lau, V. Saint-André, A.A. Sigova, H.A. Hoke, and R.A. Young Super-enhancers in the control of cell identity and disease Cell 155 2013 934 947
61. D. Hu, X. Gao, M.A. Morgan, H.M. Herz, E.R. Smith, and A. Shilatifard The MLL3/MLL4 branches of the COMPASS family function as major histone H3K4 monomethylases at enhancers Mol. Cell. Biol. 33 2013 4745 4754
62. B. Huang, M. Bates, and X. Zhuang Super-resolution fluorescence microscopy Annu. Rev. Biochem. 78 2009 993 1016
63. Y. Huang, W. Li, X. Yao, Q.J. Lin, J.W. Yin, Y. Liang, M. Heiner, B. Tian, J. Hui, and G. Wang Mediator complex regulates alternative mRNA processing via the MED23 subunit Mol. Cell 45 2012 459 469
64. J. Huisken, J. Swoger, F. Del Bene, J. Wittbrodt, and E.H. Stelzer Optical sectioning deep inside live embryos by selective plane illumination microscopy Science 305 2004 1007 1009
65. F. Jin, Y. Li, J.R. Dixon, S. Selvaraj, Z. Ye, A.Y. Lee, C.A. Yen, A.D. Schmitt, C.A. Espinoza, and B. Ren A high-resolution map of the three-dimensional chromatin interactome in human cells Nature 503 2013 290 294
66. T. Juven-Gershon, and J.T. Kadonaga Regulation of gene expression via the core promoter and the basal transcriptional machinery Dev. Biol. 339 2010 225 229
67. S. Karmakar, M.C. Mahajan, V. Schulz, G. Boyapaty, and S.M. Weissman A multiprotein complex necessary for both transcription and DNA replication at the β-globin locus EMBO J. 29 2010 3260 3271
68. P.J. Keller, A.D. Schmidt, J. Wittbrodt, and E.H. Stelzer Reconstruction of zebrafish early embryonic development by scanned light sheet microscopy Science 322 2008 1065 1069
69. H. Kettenberger, K.J. Armache, and P. Cramer Complete RNA polymerase II elongation complex structure and its interactions with NTP and TFIIS Mol. Cell 16 2004 955 965
70. R.D. Kornberg, and Y. Lorch Twenty-five years of the nucleosome, fundamental particle of the eukaryote chromosome Cell 98 1999 285 294
71. I. Kwon, M. Kato, S. Xiang, L. Wu, P. Theodoropoulos, H. Mirzaei, T. Han, S. Xie, J.L. Corden, and S.L. McKnight Phosphorylation-regulated binding of RNA polymerase II to fibrous polymers of low-complexity domains Cell 155 2013 1049 1060
72. M. Lagha, J.P. Bothma, and M. Levine Mechanisms of transcriptional precision in animal development Trends Genet. 28 2012 409 416
73. M. Lagha, J.P. Bothma, E. Esposito, S. Ng, L. Stefanik, C. Tsui, J. Johnston, K. Chen, D.S. Gilmour, J. Zeitlinger, and M.S. Levine Paused Pol II coordinates tissue morphogenesis in the Drosophila embryo Cell 153 2013 976 987
74. N. Le May, D. Fradin, I. Iltis, P. Bougnères, and J.M. Egly XPG and XPF endonucleases trigger chromatin looping and DNA demethylation for accurate expression of activated genes Mol. Cell 47 2012 622 632
75. M. Levine Transcriptional enhancers in animal development and evolution Curr. Biol. 20 2010 R754 R763
76. M. Levine Paused RNA polymerase II as a developmental checkpoint Cell 145 2011 502 511
77. M. Levine, and R. Tjian Transcription regulation and animal diversity Nature 424 2003 147 151
78. M. Lewis Allostery and the lac Operon J. Mol. Biol. 425 2013 2309 2316
79. H.L. Liang, C.Y. Nien, H.Y. Liu, M.M. Metzstein, N. Kirov, and C. Rushlow The zinc-finger protein Zelda is a key activator of the early zygotic genome in Drosophila Nature 456 2008 400 403
80. C. Lin, A.S. Garruss, Z. Luo, F. Guo, and A. Shilatifard The RNA Pol II elongation factor Ell3 marks enhancers in ES cells and primes future gene activation Cell 152 2013 144 156
81. W.L. Liu, R.A. Coleman, E. Ma, P. Grob, J.L. Yang, Y. Zhang, G. Dailey, E. Nogales, and R. Tjian Structures of three distinct activator-TFIID complexes Genes Dev. 23 2009 1510 1521
82. Z. Liu, D.R. Scannell, M.B. Eisen, and R. Tjian Control of embryonic stem cell lineage commitment by core promoter factor, TAF3 Cell 146 2011 720 731
83. X. Liu, D.A. Bushnell, and R.D. Kornberg RNA polymerase II transcription: structure and mechanism Biochim. Biophys. Acta 1829 2013 2 8
84. R. Losick Summary: three decades after sigma Cold Spring Harb. Symp. Quant. Biol. 63 1998 653 666
85. T. Lucas, T. Ferraro, B. Roelens, J. De Las Heras Chanes, A.M. Walczak, M. Coppey, and N. Dostatni Live imaging of bicoid-dependent transcription in Drosophila embryos Curr. Biol. 23 2013 2135 2139
86. D.I. Martin, S. Fiering, and M. Groudine Regulation of beta-globin gene expression: straightening out the locus Curr. Opin. Genet. Dev. 6 1996 488 495
87. D. May, M.J. Blow, T. Kaplan, D.J. McCulley, B.C. Jensen, J.A. Akiyama, A. Holt, I. Plajzer-Frick, M. Shoukry, and C. Wright et al. Large-scale discovery of enhancers from human heart tissue Nat. Genet. 44 2012 89 93
88. D.B. McKay, and T.A. Steitz Structure of catabolite gene activator protein at 2.9 A resolution suggests binding to left-handed B-DNA Nature 290 1981 744 749
89. J.E. Miller, and J.C. Reese Ccr4-Not complex: the control freak of eukaryotic cells Crit. Rev. Biochem. Mol. Biol. 47 2012 315 333
90. A.P. Monaghan, K.H. Kaestner, E. Grau, and G. Schütz Postimplantation expression patterns indicate a role for the mouse forkhead/HNF-3 alpha, beta and gamma genes in determination of the definitive endoderm, chordamesoderm and neuroectoderm Development 119 1993 567 578
91. F. Mueller, T.J. Stasevich, D. Mazza, and J.G. McNally Quantifying transcription factor kinetics: at work or at play? Crit. Rev. Biochem. Mol. Biol. 48 2013 492 514
92. K.S. Murakami, S. Masuda, E.A. Campbell, O. Muzzin, and S.A. Darst Structural basis of transcription initiation: an RNA polymerase holoenzyme-DNA complex Science 296 2002 1285 1290
93. K. Murakami, H. Elmlund, N. Kalisman, D.A. Bushnell, C.M. Adams, M. Azubel, D. Elmlund, Y. Levi-Kalisman, X. Liu, and M. Levitt et al. Architecture of an RNA polymerase II transcription pre-initiation complex Science 342 2013 1238724
94. C.Y. Nien, H.L. Liang, S. Butcher, Y. Sun, S. Fu, T. Gocha, N. Kirov, J.R. Manak, and C. Rushlow Temporal coordination of gene networks by Zelda in the early Drosophila embryo PLoS Genet. 7 2011 e1002339
95. T.J. Parry, J.W. Theisen, J.Y. Hsu, Y.L. Wang, D.L. Corcoran, M. Eustice, U. Ohler, and J.T. Kadonaga The TCT motif, a key component of an RNA polymerase II transcription system for the translational machinery Genes Dev. 24 2010 2013 2018
96. N.P. Pavletich, and C.O. Pabo Zinc finger-DNA recognition: crystal structure of a Zif268-DNA complex at 2.1 A Science 252 1991 809 817
97. A. Pavlopoulou, and I. Michalopoulos State-of-the-art bioinformatics protein structure prediction tools (Review) Int. J. Mol. Med. 28 2011 295 310
98. A.A. Philippakis, B.W. Busser, S.S. Gisselbrecht, F.S. He, B. Estrada, A.M. Michelson, and M.L. Bulyk Expression-guided in silico evaluation of candidate cis regulatory codes for Drosophila muscle founder cells PLoS Comput. Biol. 2 2006 e53
99. M. Ptashne Regulation of transcription: from lambda to eukaryotes Trends Biochem. Sci. 30 2005 275 279
100. B.F. Pugh, and R. Tjian Mechanism of transcriptional activation by Sp1: evidence for coactivators Cell 61 1990 1187 1197
101. N.H. Putnam, T. Butts, D.E. Ferrier, R.F. Furlong, U. Hellsten, T. Kawashima, M. Robinson-Rechavi, E. Shoguchi, A. Terry, and J.K. Yu et al. The amphioxus genome and the evolution of the chordate karyotype Nature 453 2008 1064 1071
102. A. Rada-Iglesias, R. Bajpai, S. Prescott, S.A. Brugmann, T. Swigut, and J. Wysocka Epigenomic annotation of enhancers predicts transcriptional regulators of human neural crest Cell Stem Cell 11 2012 633 648
103. A. Revyakin, Z. Zhang, R.A. Coleman, Y. Li, C. Inouye, J.K. Lucas, S.R. Park, S. Chu, and R. Tjian Transcription initiation by human RNA polymerase II visualized at single-molecule resolution Genes Dev. 26 2012 1691 1702
104. R.G. Roeder Nuclear RNA polymerases: role of general initiation factors and cofactors in eukaryotic transcription Methods Enzymol. 273 1996 165 171
105. J.L. Ronan, W. Wu, and G.R. Crabtree From neural development to cognition: unexpected roles for chromatin Nat. Rev. Genet. 14 2013 347 359
106. A.J. Ruthenburg, H. Li, D.J. Patel, and C.D. Allis Multivalent engagement of chromatin modifications by linked binding modules Nat. Rev. Mol. Cell Biol. 8 2007 983 994
107. A. Saunders, L.J. Core, C. Sutcliffe, J.T. Lis, and H.L. Ashe Extensive polymerase pausing during Drosophila axis patterning enables high-level and pliable transcription Genes Dev. 27 2013 1146 1158
108. L. Shao, P. Kner, E.H. Rego, and M.G. Gustafsson Super-resolution 3D microscopy of live whole cells using structured illumination Nat. Methods 8 2011 1044 1046
109. M.D. Shapiro, M.E. Marks, C.L. Peichel, B.K. Blackman, K.S. Nereng, B. Jónsson, D. Schluter, and D.M. Kingsley Genetic and developmental basis of evolutionary pelvic reduction in threespine sticklebacks Nature 428 2004 717 723
110. P.A. Sharp Split genes and RNA splicing Cell 77 1994 805 815
111. J. Shi, W.A. Whyte, C.J. Zepeda-Mendoza, J.P. Milazzo, C. Shen, J.S. Roe, J.L. Minder, F. Mercan, E. Wang, and M.A. Eckersley-Maslin et al. Role of SWI/SNF in acute leukemia maintenance and enhancer-mediated Myc regulation Genes Dev. 27 2013 2648 2662
112. O. Simakov, F. Marletaz, S.J. Cho, E. Edsinger-Gonzales, P. Havlak, U. Hellsten, D.H. Kuo, T. Larsson, J. Lv, and D. Arendt et al. Insights into bilaterian evolution from three spiralian genomes Nature 493 2013 526 531
113. L.E. Simone, and J.D. Keene Mechanisms coordinating ELAV/Hu mRNA regulons Curr. Opin. Genet. Dev. 23 2013 35 43
114. E. Smith, and A. Shilatifard Transcriptional elongation checkpoint control in development and disease Genes Dev. 27 2013 1079 1088
115. A. Soufi, G. Donahue, and K.S. Zaret Facilitators and impediments of the pluripotency reprogramming factors' initial engagement with the genome Cell 151 2012 994 1004
116. K. Struhl, D. Kadosh, M. Keaveney, L. Kuras, and Z. Moqtaderi Activation and repression mechanisms in yeast Cold Spring Harb. Symp. Quant. Biol. 63 1998 413 421
117. W. Su, S. Jackson, R. Tjian, and H. Echols DNA looping between sites for transcriptional activation: self-association of DNA-bound Sp1 Genes Dev. 5 1991 820 826
118. M. Sun, B. Schwalb, N. Pirkl, K.C. Maier, A. Schenk, H. Failmezger, A. Tresch, and P. Cramer Global analysis of eukaryotic mRNA degradation reveals Xrn1-dependent buffering of transcript levels Mol. Cell 52 2013 52 62
119. D.J. Taatjes, A.M. Näär, F. Andel III, E. Nogales, and R. Tjian Structure, function, and activator-induced conformations of the CRSP coactivator Science 295 2002 1058 1062
120. W. Tadros, J.T. Westwood, and H.D. Lipshitz The mother-to-child transition Dev. Cell 12 2007 847 849
121. R. Tjian, and T. Maniatis Transcriptional activation: a complex puzzle with few easy pieces Cell 77 1994 5 8
122. B. Treutlein, A. Muschielok, J. Andrecka, A. Jawhari, C. Buchen, D. Kostrewa, F. Hög, P. Cramer, and J. Michaelis Dynamic architecture of a minimal RNA polymerase II open promoter complex Mol. Cell 46 2012 136 146
123. B. van Steensel, and J. Dekker Genomics tools for unraveling chromosome architecture Nat. Biotechnol. 28 2010 1089 1095
124. A. Visel, M.J. Blow, Z. Li, T. Zhang, J.A. Akiyama, A. Holt, I. Plajzer-Frick, M. Shoukry, C. Wright, and F. Chen et al. ChIP-seq accurately predicts tissue-specific activity of enhancers Nature 457 2009 854 858
125. P. Voigt, W.W. Tee, and D. Reinberg A double take on bivalent promoters Genes Dev. 27 2013 1318 1338
126. D. Wang, D.A. Bushnell, K.D. Westover, C.D. Kaplan, and R.D. Kornberg Structural basis of transcription: role of the trigger loop in substrate specificity and catalysis Cell 127 2006 941 954
127. O.L. Wapinski, T. Vierbuchen, K. Qu, Q.Y. Lee, S. Chanda, D.R. Fuentes, P.G. Giresi, Y.H. Ng, S. Marro, and N.F. Neff et al. Hierarchical mechanisms for direct reprogramming of fibroblasts to neurons Cell 155 2013 621 635
128. M.T. Weirauch, and T.R. Hughes A catalogue of eukaryotic transcription factor types, their evolutionary origin, and species distribution Subcell. Biochem. 52 2011 25 73
129. K.D. Westover, D.A. Bushnell, and R.D. Kornberg Structural basis of transcription: nucleotide selection by rotation in the RNA polymerase II active center Cell 119 2004 481 489
130. W.A. Whyte, D.A. Orlando, D. Hnisz, B.J. Abraham, C.Y. Lin, M.H. Kagey, P.B. Rahl, T.I. Lee, and R.A. Young Master transcription factors and mediator establish super-enhancers at key cell identity genes Cell 153 2013 307 319
131. Y. Wu, R. Christensen, D. Colón-Ramos, and H. Shroff Advanced optical imaging techniques for neurodevelopment Curr. Opin. Neurobiol. 23 2013 1090 1097
132. M.D. Wyatt Advances in understanding the coupling of DNA base modifying enzymes to processes involving base excision repair Adv. Cancer Res. 119 2013 63 106
133. T. Xia, N. Li, and X. Fang Single-molecule fluorescence imaging in living cells Annu. Rev. Phys. Chem. 64 2013 459 480
134. K.S. Zaret, and J.S. Carroll Pioneer transcription factors: establishing competence for gene expression Genes Dev. 25 2011 2227 2241
135. Y. Zhang, X.O. Zhang, T. Chen, J.F. Xiang, Q.F. Yin, Y.H. Xing, S. Zhu, L. Yang, and L.L. Chen Circular intronic long noncoding RNAs Mol. Cell 51 2013 792 806
136. Q. Zhou, T. Li, and D.H. Price RNA polymerase II elongation control Annu. Rev. Biochem. 81 2012 119 143
137. H. Zhou, T. Kaplan, Y. Li, I. Grubisic, Z. Zhang, P.J. Wang, M.B. Eisen, and R. Tjian Dual functions of TAF7L in adipocyte differentiation Elife 2 2013 e00170