Transcription in Living Cells: Molecular Mechanisms of Bursting

Literature Cited

1. 1. 

   Miller OL, Beatty BR. 1969. Visualization of nucleolar genes. Science 164:955–57
   [Google Scholar]
2. 2. 

   McKnight SL, Miller OL Jr 1979. Post-replicative nonribosomal transcription units in D. melanogaster embryos. Cell 17:551–63
   [Google Scholar]
3. 3. 

   Dar RD, Razooky BS, Singh A, Trimeloni TV, McCollum JM et al. 2012. Transcriptional burst frequency and burst size are equally modulated across the human genome. PNAS 109:17454–59
   [Google Scholar]
4. 4. 

   Ko MS. 1991. A stochastic model for gene induction. J. Theor. Biol. 153:181–94
   [Google Scholar]
5. 5. 

   Ko MS, Nakauchi H, Takahashi N 1990. The dose dependence of glucocorticoid-inducible gene expression results from changes in the number of transcriptionally active templates. EMBO J 9:2835–42
   [Google Scholar]
6. 6. 

   Tokunaga M, Imamoto N, Sakata-Sogawa K 2008. Highly inclined thin illumination enables clear single-molecule imaging in cells. Nat. Methods 5:159–61
   [Google Scholar]
7. 7. 

   Chen B-C, Legant WR, Wang K, Shao L, Milkie DE et al. 2014. Lattice light-sheet microscopy: imaging molecules to embryos at high spatiotemporal resolution. Science 346:1257998
   [Google Scholar]
8. 8. 

   Chen J, Zhang Z, Li L, Chen BC, Revyakin A et al. 2014. Single-molecule dynamics of enhanceosome assembly in embryonic stem cells. Cell 156:1274–85
   [Google Scholar]
9. 9. 

   Paakinaho V, Presman DM, Ball DA, Johnson TA, Schiltz RL et al. 2017. Single-molecule analysis of steroid receptor and cofactor action in living cells. Nat. Commun. 8:15896
   [Google Scholar]
10. 10. 

    Grimm JB, English BP, Chen J, Slaughter JP, Zhang Z et al. 2015. A general method to improve fluorophores for live-cell and single-molecule microscopy. Nat. Meth 12:244–50
    [Google Scholar]
11. 11. 

    Swinstead EE, Miranda TB, Paakinaho V, Baek S, Goldstein I et al. 2016. Steroid receptors reprogram FoxA1 occupancy through dynamic chromatin transitions. Cell 165:593–605
    [Google Scholar]
12. 12. 

    Hansen AS, Pustova I, Cattoglio C, Tjian R, Darzacq X 2017. CTCF and cohesin regulate chromatin loop stability with distinct dynamics. eLife 6:e25776
    [Google Scholar]
13. 13. 

    Liu Z, Legant WR, Chen B-C, Li L, Grimm JB et al. 2014. 3D imaging of Sox2 enhancer clusters in embryonic stem cells. eLife 3:e04236
    [Google Scholar]
14. 14. 

    Bertrand E, Chartrand P, Schaefer M, Shenoy SM, Singer RH, Long RM 1998. Localization of ASH1 mRNA particles in living yeast. Mol. Cell 2:437–45
    [Google Scholar]
15. 15. 

    Janicki SM, Tsukamoto T, Salghetti SE, Tansey WP, Sachidanandam R et al. 2004. From silencing to gene expression: real-time analysis in single cells. Cell 116:683–98
    [Google Scholar]
16. 16. 

    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 332:475–78
    [Google Scholar]
17. 17. 

    Dolgosheina EV, Jeng SCY, Panchapakesan SS, Cojocaru R, Chen PSK et al. 2014. RNA Mango aptamer-fluorophore: a bright, high-affinity complex for RNA labeling and tracking. ACS Chem. Biol. 9:2412–20
    [Google Scholar]
18. 18. 

    Trachman RJ III, Autour A, Jeng SCY, Abdolahzadeh A, Andreoni A et al. 2019. Structure and functional reselection of the Mango-III fluorogenic RNA aptamer. Nat. Chem. Biol. 15:472–79
    [Google Scholar]
19. 19. 

    Braselmann E, Wierzba AJ, Polaski JT, Chrominski M, Holmes ZE et al. 2018. A multicolor riboswitch-based platform for imaging of RNA in live mammalian cells. Nat. Chem. Biol. 14:964–71
    [Google Scholar]
20. 20. 

    Nelles DA, Fang MY, O'Connell MR, Xu JL, Markmiller SJ et al. 2016. Programmable RNA tracking in live cells with CRISPR/Cas9. Cell 165:488–96
    [Google Scholar]
21. 21. 

    Yang LZ, Wang Y, Li SQ, Yao RW, Luan PF et al. 2019. Dynamic imaging of RNA in living cells by CRISPR-Cas13 systems. Mol. Cell 76:981–97.e7
    [Google Scholar]
22. 22. 

    Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E 2012. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337:816–21
    [Google Scholar]
23. 23. 

    Gall JG, Pardue ML. 1969. Formation and detection of RNA-DNA hybrid molecules in cytological preparations. PNAS 63:378–83
    [Google Scholar]
24. 24. 

    Hornung G, Bar-Ziv R, Rosin D, Tokuriki N, Tawfik DS et al. 2012. Noise-mean relationship in mutated promoters. Genome Res 22:2409–17
    [Google Scholar]
25. 25. 

    Dadiani M, van Dijk D, Segal B, Field Y, Ben-Artzi G et al. 2013. Two DNA-encoded strategies for increasing expression with opposing effects on promoter dynamics and transcriptional noise. Genome Res 23:966–76
    [Google Scholar]
26. 26. 

    Raveh-Sadka T, Levo M, Shabi U, Shany B, Keren L et al. 2012. Manipulating nucleosome disfavoring sequences allows fine-tune regulation of gene expression in yeast. Nat. Genet. 44:743–50
    [Google Scholar]
27. 27. 

    van Dijk D, Sharon E, Lotan-Pompan M, Weinberger A, Segal E, Carey LB 2017. Large-scale mapping of gene regulatory logic reveals context-dependent repression by transcriptional activators. Genome Res 27:87–94
    [Google Scholar]
28. 28. 

    Donovan BT, Huynh A, Ball DA, Patel HP, Poirier MG et al. 2019. Live-cell imaging reveals the interplay between transcription factors, nucleosomes, and bursting. EMBO J 38:e100809
    [Google Scholar]
29. 29. 

    Radman-Livaja M, Rando OJ. 2010. Nucleosome positioning: How is it established, and why does it matter?. Dev. Biol. 339:258–66
    [Google Scholar]
30. 30. 

    Condamin S, Bénichou O, Tejedor V, Voituriez R, Klafter J 2007. First-passage times in complex scale-invariant media. Nature 450:77–80
    [Google Scholar]
31. 31. 

    Senecal A, Munsky B, Proux F, Ly N, Braye FE et al. 2014. Transcription factors modulate c-Fos transcriptional bursts. Cell Rep 8:75–83
    [Google Scholar]
32. 32. 

    Stavreva DA, Garcia DA, Fettweis G, Gudla PR, Zaki GF et al. 2019. Transcriptional bursting and co-bursting regulation by steroid hormone release pattern and transcription factor mobility. Mol. Cell 75:1161–77.e11
    [Google Scholar]
33. 33. 

    Nelson DE, Ihekwaba AE, Elliott M, Johnson JR, Gibney CA et al. 2004. Oscillations in NF-κB signaling control the dynamics of gene expression. Science 306:704–8
    [Google Scholar]
34. 34. 

    Lahav G, Rosenfeld N, Sigal A, Geva-Zatorsky N, Levine AJ et al. 2004. Dynamics of the p53-Mdm2 feedback loop in individual cells. Nat. Genet. 36:147–50
    [Google Scholar]
35. 35. 

    Suter DM, Molina N, Gatfield D, Schneider K, Schibler U, Naef F 2011. Mammalian genes are transcribed with widely different bursting kinetics. Science 332:472–74
    [Google Scholar]
36. 36. 

    Hendy O, Campbell J, Weissman JD, Larson DR, Singer DS 2017. Differential context-specific impact of individual core promoter elements on transcriptional dynamics. Mol. Biol. Cell 28:3360–70
    [Google Scholar]
37. 37. 

    Tunnacliffe E, Corrigan AM, Chubb JR 2018. Promoter-mediated diversification of transcriptional bursting dynamics following gene duplication. PNAS 115:8364–69
    [Google Scholar]
38. 38. 

    Banerji J, Rusconi S, Schaffner W 1981. Expression of a β-globin gene is enhanced by remote SV40 DNA sequences. Cell 27:299–308
    [Google Scholar]
39. 39. 

    Catarino RR, Stark A. 2018. Assessing sufficiency and necessity of enhancer activities for gene expression and the mechanisms of transcription activation. Genes Dev 32:202–23
    [Google Scholar]
40. 40. 

    Fang B, Everett LJ, Jager J, Briggs E, Armour SM et al. 2014. Circadian enhancers coordinate multiple phases of rhythmic gene transcription in vivo. Cell 159:1140–52
    [Google Scholar]
41. 41. 

    Hah N, Danko CG, Core L, Waterfall JJ, Siepel A et al. 2011. A rapid, extensive, and transient transcriptional response to estrogen signaling in breast cancer cells. Cell 145:622–34
    [Google Scholar]
42. 42. 

    Lettice LA, Heaney SJ, Purdie LA, Li L, de Beer P et al. 2003. A long-range Shh enhancer regulates expression in the developing limb and fin and is associated with preaxial polydactyly. Hum. Mol. Genet. 12:1725–35
    [Google Scholar]
43. 43. 

    Cinghu S, Yang P, Kosak JP, Conway AE, Kumar D et al. 2017. Intragenic enhancers attenuate host gene expression. Mol. Cell 68:104–17.e6
    [Google Scholar]
44. 44. 

    Dufourt J, Trullo A, Hunter J, Fernandez C, Lazaro J et al. 2018. Temporal control of gene expression by the pioneer factor Zelda through transient interactions in hubs. Nat. Commun. 9:5194
    [Google Scholar]
45. 45. 

    Pennacchio LA, Bickmore W, Dean A, Nobrega MA, Bejerano G 2013. Enhancers: five essential questions. Nat. Rev. Genet. 14:288–95
    [Google Scholar]
46. 46. 

    Thanos D, Maniatis T. 1995. Virus induction of human IFNβ gene expression requires the assembly of an enhanceosome. Cell 83:1091–100
    [Google Scholar]
47. 47. 

    Fukaya T, Lim B, Levine M 2016. Enhancer control of transcriptional bursting. Cell 166:358–68
    [Google Scholar]
48. 48. 

    Walters MC, Fiering S, Eidemiller J, Magis W, Groudine M, Martin DI 1995. Enhancers increase the probability but not the level of gene expression. PNAS 92:7125–29
    [Google Scholar]
49. 49. 

    Bartman CR, Hsu SC, Hsiung CC, Raj A, Blobel GA 2016. Enhancer regulation of transcriptional bursting parameters revealed by forced chromatin looping. Mol. Cell 62:237–47
    [Google Scholar]
50. 50. 

    Chen H, Levo M, Barinov L, Fujioka M, Jaynes JB, Gregor T 2018. Dynamic interplay between enhancer-promoter topology and gene activity. Nat. Genet. 50:1296–303
    [Google Scholar]
51. 51. 

    Rodriguez J, Ren G, Day CR, Zhao K, Chow CC, Larson DR 2019. Intrinsic dynamics of a human gene reveal the basis of expression heterogeneity. Cell 176:213–26.e18
    [Google Scholar]
52. 52. 

    Fishilevich S, Nudel R, Rappaport N, Hadar R, Plaschkes I et al. 2017. GeneHancer: genome-wide integration of enhancers and target genes in GeneCards. Database 2017.bax028
    [Google Scholar]
53. 53. 

    Carroll JS, Meyer CA, Song J, Li W, Geistlinger TR et al. 2006. Genome-wide analysis of estrogen receptor binding sites. Nat. Genet. 38:1289–97
    [Google Scholar]
54. 54. 

    Fullwood MJ, Liu MH, Pan YF, Liu J, Xu H et al. 2009. An oestrogen-receptor-α-bound human chromatin interactome. Nature 462:58–64
    [Google Scholar]
55. 55. 

    Alexander JM, Guan J, Li B, Maliskova L, Song M et al. 2019. Live-cell imaging reveals enhancer-dependent Sox2 transcription in the absence of enhancer proximity. eLife 8:e41769
    [Google Scholar]
56. 56. 

    Mikhaylichenko O, Bondarenko V, Harnett D, Schor IE, Males M et al. 2018. The degree of enhancer or promoter activity is reflected by the levels and directionality of eRNA transcription. Genes Dev 32:42–57
    [Google Scholar]
57. 57. 

    Hah N, Murakami S, Nagari A, Danko CG, Kraus WL 2013. Enhancer transcripts mark active estrogen receptor binding sites. Genome Res 23:1210–23
    [Google Scholar]
58. 58. 

    Rahman S, Zorca CE, Traboulsi T, Noutahi E, Krause MR et al. 2017. Single-cell profiling reveals that eRNA accumulation at enhancer-promoter loops is not required to sustain transcription. Nucleic Acids Res 45:3017–30
    [Google Scholar]
59. 59. 

    Li W, Notani D, Ma Q, Tanasa B, Nunez E et al. 2013. Functional roles of enhancer RNAs for oestrogen-dependent transcriptional activation. Nature 498:516–20
    [Google Scholar]
60. 60. 

    Mousavi K, Zare H, Dell'Orso S, Grontved L, Gutierrez-Cruz G et al. 2013. eRNAs promote transcription by establishing chromatin accessibility at defined genomic loci. Mol. Cell 51:606–17
    [Google Scholar]
61. 61. 

    Hsieh CL, Fei T, Chen Y, Li T, Gao Y et al. 2014. Enhancer RNAs participate in androgen receptor-driven looping that selectively enhances gene activation. PNAS 111:7319–24
    [Google Scholar]
62. 62. 

    Lam MTY, Cho H, Lesch HP, Gosselin D, Heinz S et al. 2013. Rev-Erbs repress macrophage gene expression by inhibiting enhancer-directed transcription. Nature 498:511–15
    [Google Scholar]
63. 63. 

    Orom UA, Derrien T, Beringer M, Gumireddy K, Gardini A et al. 2010. Long noncoding RNAs with enhancer-like function in human cells. Cell 143:46–58
    [Google Scholar]
64. 64. 

    Paralkar VR, Taborda CC, Huang P, Yao Y, Kossenkov AV et al. 2016. Unlinking an lncRNA from its associated cis element. Mol. Cell 62:104–10
    [Google Scholar]
65. 65. 

    Schaukowitch K, Joo JY, Liu X, Watts JK, Martinez C, Kim TK 2014. Enhancer RNA facilitates NELF release from immediate early genes. Mol. Cell 56:29–42
    [Google Scholar]
66. 66. 

    Feng J, Bi C, Clark BS, Mady R, Shah P, Kohtz JD 2006. The Evf-2 noncoding RNA is transcribed from the Dlx-5/6 ultraconserved region and functions as a Dlx-2 transcriptional coactivator. Genes Dev 20:1470–84
    [Google Scholar]
67. 67. 

    Melo CA, Drost J, Wijchers PJ, van de Werken H, de Wit E et al. 2013. eRNAs are required for p53-dependent enhancer activity and gene transcription. Mol. Cell 49:524–35
    [Google Scholar]
68. 68. 

    Tsai PF, Dell'Orso S, Rodriguez J, Vivanco KO, Ko KD et al. 2018. A muscle-specific enhancer RNA mediates cohesin recruitment and regulates transcription in trans. Mol. Cell 71:129–41.e8
    [Google Scholar]
69. 69. 

    De Santa F, Barozzi I, Mietton F, Ghisletti S, Polletti S et al. 2010. A large fraction of extragenic RNA pol II transcription sites overlap enhancers. PLOS Biol 8:e1000384
    [Google Scholar]
70. 70. 

    Core L, Adelman K. 2019. Promoter-proximal pausing of RNA polymerase II: a nexus of gene regulation. Genes Dev 33:960–82
    [Google Scholar]
71. 71. 

    Gilmour DS, Lis JT. 1986. RNA polymerase II interacts with the promoter region of the noninduced hsp70 gene in Drosophila melanogaster cells. Mol. Cell. Biol. 6:3984–89
    [Google Scholar]
72. 72. 

    Bentley DL. 2014. Coupling mRNA processing with transcription in time and space. Nat. Rev. Genet. 15:163–75
    [Google Scholar]
73. 73. 

    O'Brien T, Lis JT. 1991. RNA polymerase II pauses at the 5′ end of the transcriptionally induced Drosophila hsp70 gene. Mol. Cell. Biol. 11:5285–90
    [Google Scholar]
74. 74. 

    Steurer B, Janssens RC, Geverts B, Geijer ME, Wienholz F et al. 2018. Live-cell analysis of endogenous GFP-RPB1 uncovers rapid turnover of initiating and promoter-paused RNA Polymerase II. PNAS 115:E4368–76
    [Google Scholar]
75. 75. 

    Darzacq X, Shav-Tal Y, de Turris V, Brody Y, Shenoy SM et al. 2007. In vivo dynamics of RNA polymerase II transcription. Nat. Struct. Mol. Biol. 14:796–806
    [Google Scholar]
76. 76. 

    Henriques T, Scruggs BS, Inouye MO, Muse GW, Williams LH et al. 2018. Widespread transcriptional pausing and elongation control at enhancers. Genes Dev 32:26–41
    [Google Scholar]
77. 77. 

    Krebs AR, Imanci D, Hoerner L, Gaidatzis D, Burger L, Schubeler D 2017. Genome-wide single-molecule footprinting reveals high RNA polymerase II turnover at paused promoters. Mol. Cell 67:411–22.e4
    [Google Scholar]
78. 78. 

    Bartman CR, Hamagami N, Keller CA, Giardine B, Hardison RC et al. 2019. Transcriptional burst initiation and polymerase pause release are key control points of transcriptional regulation. Mol. Cell 73:519–32.e4
    [Google Scholar]
79. 79. 

    Levens D, Baranello L, Kouzine F 2016. Controlling gene expression by DNA mechanics: emerging insights and challenges. Biophys. Rev. 8:259–68
    [Google Scholar]
80. 80. 

    Liu LF, Wang JC. 1987. Supercoiling of the DNA template during transcription. PNAS 84:7024–27
    [Google Scholar]
81. 81. 

    Brill SJ, DiNardo S, Voelkel-Meiman K, Sternglanz R 1987. Need for DNA topoisomerase activity as a swivel for DNA replication for transcription of ribosomal RNA. Nature 326:414–16
    [Google Scholar]
82. 82. 

    Yamagishi M, Nomura M. 1988. Deficiency in both type I and type II DNA topoisomerase activities differentially affect rRNA and ribosomal protein synthesis in Schizosaccharomyces pombe. Curr. Genet 13:305–14
    [Google Scholar]
83. 83. 

    Joshi RS, Pina B, Roca J 2010. Positional dependence of transcriptional inhibition by DNA torsional stress in yeast chromosomes. EMBO J 29:740–48
    [Google Scholar]
84. 84. 

    Chong S, Chen C, Ge H, Xie XS 2014. Mechanism of transcriptional bursting in bacteria. Cell 158:314–26
    [Google Scholar]
85. 85. 

    Ju BG, Lunyak VV, Perissi V, Garcia-Bassets I, Rose DW et al. 2006. A topoisomerase IIβ-mediated dsDNA break required for regulated transcription. Science 312:1798–802
    [Google Scholar]
86. 86. 

    Trotter KW, King HA, Archer TK 2015. Glucocorticoid receptor transcriptional activation via the BRG1-dependent recruitment of TOP2β and Ku70/86. Mol. Cell. Biol. 35:2799–817
    [Google Scholar]
87. 87. 

    Tantale K, Mueller F, Kozulic-Pirher A, Lesne A, Victor J-M et al. 2016. A single-molecule view of transcription reveals convoys of RNA polymerases and multi-scale bursting. Nat. Commun. 7:12248
    [Google Scholar]
88. 88. 

    Zenklusen D, Larson DR, Singer RH 2008. Single-RNA counting reveals alternative modes of gene expression in yeast. Nat. Struct. Mol. Biol. 15:1263–71
    [Google Scholar]
89. 89. 

    Fritzsch C, Baumgartner S, Kuban M, Steinshorn D, Reid G, Legewie S 2018. Estrogen-dependent control and cell-to-cell variability of transcriptional bursting. Mol. Syst. Biol. 14:e7678
    [Google Scholar]
90. 90. 

    Harper CV, Finkenstädt B, Woodcock DJ, Friedrichsen S, Semprini S et al. 2011. Dynamic analysis of stochastic transcription cycles. PLOS Biol 9:e1000607
    [Google Scholar]
91. 91. 

    Pedraza JM, Paulsson J. 2008. Effects of molecular memory and bursting on fluctuations in gene expression. Science 319:339–43
    [Google Scholar]
92. 92. 

    Lenstra TL, Coulon A, Chow CC, Larson DR 2015. Single-molecule imaging reveals a switch between spurious and functional ncRNA transcription. Mol. Cell 60:597–610
    [Google Scholar]
93. 93. 

    Cho W-K, Jayanth N, English BP, Inoue T, Andrews JO et al. 2016. RNA Polymerase II cluster dynamics predict mRNA output in living cells. eLife 5:e13617
    [Google Scholar]
94. 94. 

    Larsson AJM, Johnsson P, Hagemann-Jensen M, Hartmanis L, Faridani OR et al. 2019. Genomic encoding of transcriptional burst kinetics. Nature 565:251–54
    [Google Scholar]
95. 95. 

    Zhang Z, English BP, Grimm JB, Kazane SA, Hu W et al. 2016. Rapid dynamics of general transcription factor TFIIB binding during preinitiation complex assembly revealed by single-molecule analysis. Genes Dev 30:2106–18
    [Google Scholar]
96. 96. 

    Zhang Z, Revyakin A, Grimm JB, Lavis LD, Tjian R 2014. Single-molecule tracking of the transcription cycle by sub-second RNA detection. eLife 3:e01775
    [Google Scholar]
97. 97. 

    Revyakin A, Zhang Z, Coleman RA, Li Y, Inouye C et al. 2012. Transcription initiation by human RNA polymerase II visualized at single-molecule resolution. Genes Dev 26:1691–702
    [Google Scholar]
98. 98. 

    Levi V, Ruan Q, Plutz M, Belmont AS, Gratton E 2005. Chromatin dynamics in interphase cells revealed by tracking in a two-photon excitation microscope. Biophys. J. 89:4275–85
    [Google Scholar]
99. 99. 

    Larson DR, Fritzsch C, Sun L, Meng X, Lawrence DS, Singer RH 2013. Direct observation of frequency modulated transcription in single cells using light activation. eLife 2:e00750
    [Google Scholar]
100. 100. 

     Hahn S. 1998. Activation and the role of reinitiation in the control of transcription by RNA polymerase II. Cold Spring Harb. Symp. Quant. Biol. 63:181–88
     [Google Scholar]
101. 101. 

     Jiang Y, Gralla JD. 1993. Uncoupling of initiation and reinitiation rates during HeLa RNA polymerase II transcription in vitro. Mol. Cell. Biol. 13:4572–77
     [Google Scholar]
102. 102. 

     Szentirmay MN, Sawadogo M. 1991. Transcription factor requirement for multiple rounds of initiation by human RNA polymerase II. PNAS 88:10691–95
     [Google Scholar]
103. 103. 

     Zawel L, Kumar KP, Reinberg D 1995. Recycling of the general transcription factors during RNA polymerase II transcription. Genes Dev 9:1479–90
     [Google Scholar]
104. 104. 

     Kraus WL, Kadonaga JT. 1998. p300 and estrogen receptor cooperatively activate transcription via differential enhancement of initiation and reinitiation. Genes Dev 12:331–42
     [Google Scholar]
105. 105. 

     Sheridan PL, Mayall TP, Verdin E, Jones KA 1997. Histone acetyltransferases regulate HIV-1 enhancer activity invitro. Genes Dev 11:3327–40
     [Google Scholar]
106. 106. 

     Yudkovsky N, Ranish JA, Hahn S 2000. A transcription reinitiation intermediate that is stabilized by activator. Nature 408:225–29
     [Google Scholar]
107. 107. 

     Bintu B, Mateo LJ, Su JH, Sinnott-Armstrong NA, Parker M et al. 2018. Super-resolution chromatin tracing reveals domains and cooperative interactions in single cells. Science 362:eaau1783
     [Google Scholar]
108. 108. 

     Li J, Dong A, Saydaminova K, Chang H, Wang G et al. 2019. Single-molecule nanoscopy elucidates RNA polymerase II transcription at single genes in live cells. Cell 178:491–506.e28
     [Google Scholar]
109. 109. 

     Kimura H, Cook PR. 2001. Kinetics of core histones in living human cells. J. Cell Biol. 153:1341–54
     [Google Scholar]
110. 110. 

     Misteli T, Gunjan A, Hock R, Bustin M, Brown DT 2000. Dynamic binding of histone H1 to chromatin in living cells. Nature 408:877–81
     [Google Scholar]
111. 111. 

     Deal RB, Henikoff JG, Henikoff S 2010. Genome-wide kinetics of nucleosome turnover determined by metabolic labeling of histones. Science 328:1161–64
     [Google Scholar]
112. 112. 

     Dion MF, Kaplan T, Kim M, Buratowski S, Friedman N, Rando OJ 2007. Dynamics of replication-independent histone turnover in budding yeast. Science 315:1405–8
     [Google Scholar]
113. 113. 

     Kraushaar DC, Jin W, Maunakea A, Abraham B, Ha M, Zhao K 2013. Genome-wide incorporation dynamics reveal distinct categories of turnover for the histone variant H3.3. Genome Biol 14:R121
     [Google Scholar]
114. 114. 

     Deaton AM, Gómez-Rodríguez M, Mieczkowski J, Tolstorukov MY, Kundu S et al. 2016. Enhancer regions show high histone H3.3 turnover that changes during differentiation. eLife 5:e15316
     [Google Scholar]
115. 115. 

     Mito Y, Henikoff JG, Henikoff S 2005. Genome-scale profiling of histone H3.3 replacement patterns. Nat. Genet. 37:1090–97
     [Google Scholar]
116. 116. 

     Henikoff S, Shilatifard A. 2011. Histone modification: cause or cog. Trends Genet 27:389–96
     [Google Scholar]
117. 117. 

     Bowman GD, Poirier MG. 2015. Post-translational modifications of histones that influence nucleosome dynamics. Chem. Rev. 115:2274–95
     [Google Scholar]
118. 118. 

     Nicolas D, Zoller B, Suter DM, Naef F 2018. Modulation of transcriptional burst frequency by histone acetylation. PNAS 115:7153–58
     [Google Scholar]
119. 119. 

     Chen LF, Lin YT, Gallegos DA, Hazlett MF, Gomez-Schiavon M et al. 2019. Enhancer histone acetylation modulates transcriptional bursting dynamics of neuronal activity-inducible genes. Cell Rep 26:1174–88.e5
     [Google Scholar]
120. 120. 

     Allis CD, Berger SL, Cote J, Dent S, Jenuwien T et al. 2007. New nomenclature for chromatin-modifying enzymes. Cell 131:633–36
     [Google Scholar]
121. 121. 

     Downey M, Baetz K. 2016. Building a KATalogue of acetyllysine targeting and function. Brief. Funct. Genom. 15:109–18
     [Google Scholar]
122. 122. 

     Waterborg JH. 1993. Histone synthesis and turnover in alfalfa: fast loss of highly acetylated replacement histone variant H3.2. J. Biol. Chem. 268:4912–17
     [Google Scholar]
123. 123. 

     Bintu L, Yong J, Antebi YE, McCue K, Kazuki Y et al. 2016. Dynamics of epigenetic regulation at the single-cell level. Science 351:720–24
     [Google Scholar]
124. 124. 

     Muramoto T, Müller I, Thomas G, Melvin A, Chubb JR 2010. Methylation of H3K4 is required for inheritance of active transcriptional states. Curr. Biol. 20:397–406
     [Google Scholar]
125. 125. 

     Ng KKH, Yui MA, Mehta A, Siu S, Irwin B et al. 2018. A stochastic epigenetic switch controls the dynamics of T-cell lineage commitment. eLife 7:e37851
     [Google Scholar]
126. 126. 

     Dey SS, Foley JE, Limsirichai P, Schaffer DV, Arkin AP 2015. Orthogonal control of expression mean and variance by epigenetic features at different genomic loci. Mol. Syst. Biol. 11:806
     [Google Scholar]
127. 127. 

     Luo Y, North JA, Rose SD, Poirier MG 2014. Nucleosomes accelerate transcription factor dissociation. Nucleic Acids Res 42:3017–27
     [Google Scholar]
128. 128. 

     Parmar JJ, Das D, Padinhateeri R 2015. Theoretical estimates of exposure timescales of protein binding sites on DNA regulated by nucleosome kinetics. Nucleic Acids Res 44:1630–41
     [Google Scholar]
129. 129. 

     Brown CR, Mao C, Falkovskaia E, Jurica MS, Boeger H 2013. Linking stochastic fluctuations in chromatin structure and gene expression. PLOS Biol 11:e1001621
     [Google Scholar]
130. 130. 

     Dixon JR, Selvaraj S, Yue F, Kim A, Li Y et al. 2012. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 485:376–80
     [Google Scholar]
131. 131. 

     Nora EP, Lajoie BR, Schulz EG, Giorgetti L, Okamoto I et al. 2012. Spatial partitioning of the regulatory landscape of the X-inactivation centre. Nature 485:381–85
     [Google Scholar]
132. 132. 

     Mirny LA, Imakaev M, Abdennur N 2019. Two major mechanisms of chromosome organization. Curr. Opin. Cell Biol. 58:142–52
     [Google Scholar]
133. 133. 

     Falk M, Feodorova Y, Naumova N, Imakaev M, Lajoie BR et al. 2019. Heterochromatin drives compartmentalization of inverted and conventional nuclei. Nature 570:395–99
     [Google Scholar]
134. 134. 

     Sanborn AL, Rao SSP, Huang S-C, Durand NC, Huntley MH et al. 2015. Chromatin extrusion explains key features of loop and domain formation in wild-type and engineered genomes. PNAS 112:E6456–65
     [Google Scholar]
135. 135. 

     Symmons O, Uslu VV, Tsujimura T, Ruf S, Nassari S et al. 2014. Functional and topological characteristics of mammalian regulatory domains. Genome Res 24:390–400
     [Google Scholar]
136. 136. 

     Hughes JR, Roberts N, McGowan S, Hay D, Giannoulatou E et al. 2014. Analysis of hundreds of cis-regulatory landscapes at high resolution in a single, high-throughput experiment. Nat. Genet. 46:205–12
     [Google Scholar]
137. 137. 

     Mifsud B, Tavares-Cadete F, Young AN, Sugar R, Schoenfelder S et al. 2015. Mapping long-range promoter contacts in human cells with high-resolution capture Hi-C. Nat. Genet. 47:598–606
     [Google Scholar]
138. 138. 

     Schoenfelder S, Furlan-Magaril M, Mifsud B, Tavares-Cadete F, Sugar R et al. 2015. The pluripotent regulatory circuitry connecting promoters to their long-range interacting elements. Genome Res 25:582–97
     [Google Scholar]
139. 139. 

     Tang Z, Luo OJ, Li X, Zheng M, Zhu JJ et al. 2015. CTCF-mediated human 3D genome architecture reveals chromatin topology for transcription. Cell 163:1611–27
     [Google Scholar]
140. 140. 

     Finn EH, Pegoraro G, Brandao HB, Valton AL, Oomen ME et al. 2019. Extensive heterogeneity and intrinsic variation in spatial genome organization. Cell 176:1502–15.e10
     [Google Scholar]
141. 141. 

     Rao SSP, Huang S-C St, Hilaire BG, Engreitz JM, Perez EM et al. 2017. Cohesin loss eliminates all loop domains. Cell 171:305–20.e24
     [Google Scholar]
142. 142. 

     Boettiger AN, Bintu B, Moffitt JR, Wang S, Beliveau BJ et al. 2016. Super-resolution imaging reveals distinct chromatin folding for different epigenetic states. Nature 529:418–22
     [Google Scholar]
143. 143. 

     Mateo LJ, Murphy SE, Hafner A, Cinquini IS, Walker CA, Boettiger AN 2019. Visualizing DNA folding and RNA in embryos at single-cell resolution. Nature 568:49–54
     [Google Scholar]
144. 144. 

     Cardozo Gizzi AM, Cattoni DI, Fiche J-B, Espinola SM, Gurgo J et al. 2019. Microscopy-based chromosome conformation capture enables simultaneous visualization of genome organization and transcription in intact organisms. Mol. Cell 74:212–22.e5
     [Google Scholar]
145. 145. 

     Flavahan WA, Drier Y, Liau BB, Gillespie SM, Venteicher AS et al. 2016. Insulator dysfunction and oncogene activation in IDH mutant gliomas. Nature 529:110–14
     [Google Scholar]
146. 146. 

     Lupianez DG, Kraft K, Heinrich V, Krawitz P, Brancati F et al. 2015. Disruptions of topological chromatin domains cause pathogenic rewiring of gene-enhancer interactions. Cell 161:1012–25
     [Google Scholar]
147. 147. 

     Ren G, Jin W, Cui K, Rodrigez J, Hu G et al. 2017. CTCF-mediated enhancer-promoter interaction is a critical regulator of cell-to-cell variation of gene expression. Mol. Cell 67:1049–58.e6
     [Google Scholar]
148. 148. 

     Jackson DA, Hassan AB, Errington RJ, Cook PR 1993. Visualization of focal sites of transcription within human nuclei. EMBO J 12:1059–65
     [Google Scholar]
149. 149. 

     Schoenfelder S, Sexton T, Chakalova L, Cope NF, Horton A et al. 2010. Preferential associations between co-regulated genes reveal a transcriptional interactome in erythroid cells. Nat. Genet. 42:53–61
     [Google Scholar]
150. 150. 

     Fanucchi S, Shibayama Y, Burd S, Weinberg MS, Mhlanga MM 2013. Chromosomal contact permits transcription between coregulated genes. Cell 155:606–20
     [Google Scholar]
151. 151. 

     Cisse II, Izeddin I, Causse SZ, Boudarene L, Senecal A et al. 2013. Real-time dynamics of RNA polymerase II clustering in live human cells. Science 341:664–67
     [Google Scholar]
152. 152. 

     Papantonis A, Larkin JD, Wada Y, Ohta Y, Ihara S et al. 2010. Active RNA polymerases: mobile or immobile molecular machines?. PLOS Biol 8:e1000419
     [Google Scholar]
153. 153. 

     Spudich JL, Koshland DE Jr 1976. Non-genetic individuality: chance in the single cell. Nature 262:467–71
     [Google Scholar]
154. 154. 

     Peccoud J, Ycart B. 1995. Markovian modeling of gene-product synthesis. Theor. Popul. Biol. 48:222–34
     [Google Scholar]
155. 155. 

     Chubb JR, Trcek T, Shenoy SM, Singer RH 2006. Transcriptional pulsing of a developmental gene. Curr. Biol. 16:1018–25
     [Google Scholar]
156. 156. 

     Golding I, Paulsson J, Zawilski SM, Cox EC 2005. Real-time kinetics of gene activity in individual bacteria. Cell 123:1025–36
     [Google Scholar]
157. 157. 

     Kim JK, Marioni JC. 2013. Inferring the kinetics of stochastic gene expression from single-cell RNA-sequencing data. Genome Biol 14:R7
     [Google Scholar]
158. 158. 

     Palangat M, Larson DR. 2012. Complexity of RNA polymerase II elongation dynamics. Biochim. Biophys. Acta 1819:667–72
     [Google Scholar]
159. 159. 

     Anders S, Huber W. 2010. Differential expression analysis for sequence count data. Genome Biol 11:R106
     [Google Scholar]
160. 160. 

     Love MI, Huber W, Anders S 2014. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15:550
     [Google Scholar]
161. 161. 

     Robinson MD, Smyth GK. 2007. Moderated statistical tests for assessing differences in tag abundance. Bioinformatics 23:2881–87
     [Google Scholar]
162. 162. 

     Raj A, Peskin CS, Tranchina D, Vargas DY, Tyagi S 2006. Stochastic mRNA synthesis in mammalian cells. PLOS Biol 4:e309
     [Google Scholar]
163. 163. 

     Corrigan AM, Tunnacliffe E, Cannon D, Chubb JR 2016. A continuum model of transcriptional bursting. eLife 5:e13051
     [Google Scholar]