CoChat
Sign Up
Cited by 115Genomics and Chromatin DynamicsNuclear Structure and FunctionChromatin Remodeling and Cancer

Spatiotemporal coordination of transcription preinitiation complex assembly in live cells

Open access
Nguyen, Vu Q., Ranjan, Anand, Liu, Sheng, Tang, Xiaona, Ling, Yick Hin, Wisniewski, Jan, Mizuguchi, Gaku, Li, Kai Yu +5 more·2021·Molecular Cell
DOI 10.1016/j.molcel.2021.07.022PMC PMC8420877

Published version of a preprint

Open this paper in CoChat — free account

Abstract

Transcription initiation by RNA polymerase II (RNA Pol II) requires preinitiation complex (PIC) assembly at gene promoters. In the dynamic nucleus, where thousands of promoters are broadly distributed in chromatin, it is unclear how multiple individual components converge on any target to establish the PIC. Here we use live-cell, single-molecule tracking in S. cerevisiae to visualize constrained exploration of the nucleoplasm by PIC components and Mediator's key role in guiding this process. On chromatin, TFIID/TATA-binding protein (TBP), Mediator, and RNA Pol II instruct assembly of a short-lived PIC, which occurs infrequently but efficiently within a few seconds on average. Moreover, PIC exclusion by nucleosome encroachment underscores regulated promoter accessibility by chromatin remodeling. Thus, coordinated nuclear exploration and recruitment to accessible targets underlies dynamic PIC establishment in yeast. Our study provides a global spatiotemporal model for transcription initiation in live cells.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1016/j.molcel.2021.07.022

Cites

6 of 6 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Molecular processes that transmit regulatory information from enhancers to promoters, and those associated with promoter operation itself, are stochastic and dynamic.

    “Molecular processes that are thought to transmit regulatory information from enhancers to promoters (such as recruitment of transcription factors and coactivators, assembly of the Mediator complex40), as well as those that are associated with promoter operation itself (such as pre-initiation complex assembly, RNA polymerase II pausing and release41,42) are also stochastic and dynamic43.”

    From Nonlinear control of transcription through enhancer–promoter interactions (2022) · cites this paper as [41]

    The Results section, “Highly dynamic target search and low promoter occupancy by PIC components” (page unavailable), reports dynamic target search and infrequent PIC formation at yeast promoters. This supports the claim about dynamic promoter-associated PIC assembly, but the cited passages do not establish that enhancer-to-promoter signaling or RNA polymerase II pausing and release are stochastic and dynamic. (LLM, conf=0.84)

    Experimental — accuracy not yet measured

  • Regulatory processes at the interface between enhancers and promoters have been estimated to occur in the order of tens of seconds.

    “Regulatory processes at the interface between enhancers and promoters have been estimated to occur in the order of tens of seconds41,43,46, consistent with the condition that intermediate regulatory steps should be faster than bursting kinetics (Fig. 3f).”

    From Nonlinear control of transcription through enhancer–promoter interactions (2022) · cites this paper as [41]

    The Results section, “Highly dynamic target search and low promoter occupancy by PIC components” (page not provided), estimates 8–48 seconds for Mediator and general transcription factors to search for targets in yeast. That supports the timescale, but the measured process is target search, not specifically a regulatory step at the enhancer–promoter interface. (LLM, conf=0.84)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 99

  1. Ansari SA, He Q, and Morse RH (2009). Mediator complex association with constitutively transcribed genes in yeast. Proc National Acad Sci 106, 16734– 16739. PMC2757859 19805365
  2. Baek HJ, Malik S, Qin J, and Roeder RG (2002). Requirement of TRAP/Mediator for Both Activator-Independent and Activator-Dependent Transcription in Conjunction with TFIID-Associated TAFIIs. Mol Cell Biol 22, 2842– 2852. 11909976 PMC133729
  3. Baek HJ, Kang YK, and Roeder RG (2006). Human Mediator Enhances Basal Transcription by Facilitating Recruitment of Transcription Factor IIB during Preinitiation Complex Assembly. Journal of Biological Chemistry 281, 15172– 15181. 16595664
  4. Ball DA, Mehta GD, Salomon-Kent R, Mazza D, Morisaki T, Mueller F, McNally JG, and Karpova TS (2016). Single molecule tracking of Ace1p in Saccharomyces cerevisiae defines a characteristic residence time for non-specific interactions of transcription factors with chromatin. Nucleic Acids Research 44, gkw744. PMC5137432 27566148
  5. Baptista T, Grünberg S, Minoungou N, Koster MJE, Timmers HTM, Hahn S, Devys D, and Tora L (2017). SAGA Is a General Cofactor for RNA Polymerase II Transcription. Molecular Cell 68, 130– 143.e5. 28918903 PMC5632562
  6. Boija A, Klein IA, Sabari BR, Dall’Agnese A, Coffey EL, Zamudio AV, Li CH, Shrinivas K, Manteiga JC, Hannett NM, (2018). Transcription Factors Activate Genes through the Phase-Separation Capacity of Their Activation Domains. Cell 175, 1842– 1855.e16. 30449618 PMC6295254
  7. Booher KR, and Kaiser P (2008). A PCR-based strategy to generate yeast strains expressing endogenous levels of amino-terminal epitope-tagged proteins. 18320568
  8. Borggrefe T, Davis R, Bareket-Samish A, and Kornberg RD (2001). Quantitation of the RNA polymerase II transcription machinery in yeast. The Journal of Biological Chemistry 276, 47150– 47153. 11591727
  9. Brahma S, and Henikoff S (2018). RSC-Associated Subnucleosomes Define MNase-Sensitive Promoters in Yeast. Molecular Cell 73, 238– 249.e3. 30554944 PMC6475595
  10. Cherry JM, Adler C, Ball C, Chervitz SA, Dwight SS, Hester ET, Jia Y, Juvik G, Roe T, Schroeder M, (1998). SGD: Saccharomyces Genome Database. Nucleic Acids Res 26, 73– 79. 9399804 PMC147204
  11. Cho W-K, Jayanth N, English BP, Inoue T, Andrews JO, Conway W, Grimm JB, Spille J-H, Lavis LD, Lionnet T, (2016). RNA Polymerase II cluster dynamics predict mRNA output in living cells. ELife 5, 1123. PMC4929003 27138339
  12. Cho W-K, Spille J-H, Hecht M, Lee C, Li C, Grube V, and Cisse II (2018). Mediator and RNA polymerase II clusters associate in transcription-dependent condensates. Science 361, 412– 415. 29930094 PMC6543815
  13. Cisse II, Izeddin I, Causse SZ, Boudarene L, Senecal A, Muresan L, Dugast-Darzacq C, Hajj B, Dahan M, and Darzacq X (2013). Real-Time Dynamics of RNA Polymerase II Clustering in Live Human Cells. Science 341, 664– 667. 23828889
  14. Compe E, Genes CM, Braun C, Coin F, and Egly J-M (2019). TFIIE orchestrates the recruitment of the TFIIH kinase module at promoter before release during transcription. Nature Communications 10, 2084. PMC6504876 31064989
  15. Cramer P (2019). Organization and regulation of gene transcription. Nature 573, 45– 54. 31462772
  16. Dion V, and Gasser SM (2013). Chromatin movement in the maintenance of genome stability. Cell 152, 1355– 1364. 23498942
  17. Donczew R, Warfield L, Pacheco D, Erijman A, and Hahn S (2020). Two roles for the yeast transcription coactivator SAGA and a set of genes redundantly regulated by TFIID and SAGA. Elife 9, e50109. 31913117 PMC6977968
  18. Donovan BT, Huynh A, Ball DA, Patel HP, Poirier MG, Larson DR, Ferguson ML, and Lenstra TL (2019). Live- cell imaging reveals the interplay between transcription factors, nucleosomes, and bursting. The EMBO Journal 38, e51794. PMC6576174 31101674
  19. Fujiwara R, Damodaren N, Wilusz JE, and Murakami K (2019). The capping enzyme facilitates promoter escape and assembly of a follow-on preinitiation complex for reinitiation. Proceedings of the National Academy of Sciences 116, 22573– 22582. PMC6842614 31591205
  20. Ganguli D, Chereji RV, Iben JR, Cole HA, and Clark DJ (2014). RSC-dependent constructive and destructive interference between opposing arrays of phased nucleosomes in yeast. Genome Research 24, 1637– 1649. 25015381 PMC4199373
  21. Gebhardt JCM, Suter DM, Roy R, Zhao ZW, Chapman AR, Basu S, Maniatis T, and Xie XS (2013). Single-molecule imaging of transcription factor binding to DNA in live mammalian cells. Nature Methods 10, 421– 426. 23524394 PMC3664538
  22. Gietz RD, and Schiestl RH (2007). High-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method. Nature Protocols 2, 31– 34. 17401334
  23. Grimaldi Y, Ferrari P, and Strubin M (2014). Independent RNA polymerase II preinitiation complex dynamics and nucleosome turnover at promoter sites in vivo. Genome Research 24, 117– 124. 24298073 PMC3875852
  24. Grimm JB, English BP, Chen J, Slaughter JP, Zhang Z, Revyakin A, Patel R, Macklin JJ, Normanno D, Singer RH, (2015). A general method to improve fluorophores for live-cell and single-molecule microscopy. Nature Methods 12, 244– 50-3 p following 250. 25599551 PMC4344395
  25. Grünberg S, Henikoff S, Hahn S, and Zentner GE (2016). Mediator binding to UASs is broadly uncoupled from transcription and cooperative with TFIID recruitment to promoters. The EMBO Journal 35, 2435– 2446. 27797823 PMC5109241
  26. Guidi BW, Bjornsdottir G, Hopkins DC, Lacomis L, Erdjument-Bromage H, Tempst P, and Myers LC (2004). Mutual Targeting of Mediator and the TFIIH Kinase Kin28*. J Biol Chem 279, 29114– 29120. 15126497
  27. Haberle V, and Stark A (2018). Eukaryotic core promoters and the functional basis of transcription initiation. Nat Rev Mol Cell Bio 19, 621– 637. 29946135 PMC6205604
  28. Hammond CM, Strømme CB, Huang H, Patel DJ, and Groth A (2017). Histone chaperone networks shaping chromatin function. Nature Reviews Molecular Cell Biology 18, 141– 158. 28053344 PMC5319910
  29. Hansen AS, Pustova I, Cattoglio C, Tjian R, and Darzacq X (2017). CTCF and cohesin regulate chromatin loop stability with distinct dynamics. ELife 6, 2848. PMC5446243 28467304
  30. Hansen AS, Woringer M, Grimm JB, Lavis LD, Tjian R, and Darzacq X (2018). Robust model-based analysis of single-particle tracking experiments with Spot-On. ELife 7. PMC5809147 29300163
  31. Hansen AS, Amitai A, Cattoglio C, Tjian R, and Darzacq X (2020). Guided nuclear exploration increases CTCF target search efficiency. Nat Chem Biol 16, 257– 266. 31792445 PMC7036004
  32. Hartley PD, and Madhani HD (2009). Mechanisms that Specify Promoter Nucleosome Location and Identity. Cell 137, 445– 458. 19410542 PMC2677553
  33. Haruki H, Nishikawa J, and Laemmli UK (2008). The anchor-away technique: rapid, conditional establishment of yeast mutant phenotypes. Molecular Cell 31, 925– 932. 18922474
  34. Ho B, Baryshnikova A, and Brown GW (2018). Unification of Protein Abundance Datasets Yields a Quantitative Saccharomyces cerevisiae Proteome. Cell Systems 6, 192– 205.e3. 29361465
  35. Iben S, Tschochner H, Bier M, Hoogstraten D, Hozák P, Egly J-M, and Grummt I (2002). TFIIH Plays an Essential Role in RNA Polymerase I Transcription. Cell 109, 297– 306. 12015980
  36. Izeddin I, Récamier V, Bosanac L, Cissé II, Boudarene L, Dugast-Darzacq C, Proux F, Bénichou O, Voituriez R, Bensaude O, (2014). Single-molecule tracking in live cells reveals distinct target-search strategies of transcription factors in the nucleus. ELife 3. PMC4095940 24925319
  37. Jeronimo C, and Robert F (2014). Kin28 regulates the transient association of Mediator with core promoters. Nature Structural & Molecular Biology 21, 449– 455. PMC3997488 24704787
  38. Jeronimo C, Langelier M-F, Bataille AR, Pascal JM, Pugh BF, and Robert F(2016). Tail and Kinase Modules Differently Regulate Core Mediator Recruitment and Function In Vivo. Molecular Cell 64, 455– 466. 27773677 PMC5824718
  39. Johnson KM, and Carey M (2003). Assembly of a Mediator/TFIID/TFIIA Complex Bypasses the Need for an Activator. Curr Biol 13, 772– 777. 12725737
  40. Johnson KM, Wang J, Smallwood A, Arayata C, and Carey M (2002). TFIID and human mediator coactivator complexes assemble cooperatively on promoter DNA. Genes & Development 16, 1852– 1863. 12130544 PMC186393
  41. Joo YJ, Ficarro SB, Soares LM, Chun Y, Marto JA, and Buratowski S (2017). Downstream promoter interactions of TFIID TAFs facilitate transcription reinitiation. Genes & Development 31, 2162– 2174. 29203645 PMC5749164
  42. Kent S, Brown K, Yang C, Alsaihati N, Tian C, Wang H, and Ren X (2020). Phase-Separated Transcriptional Condensates Accelerate Target-Search Process Revealed by Live-Cell Single-Molecule Imaging. Cell Reports 33, 108248. 33053359 PMC7593837
  43. Keogh M-C, Cho E-J, Podolny V, and Buratowski S (2002). Kin28 Is Found within TFIIH and a Kin28-Ccl1-Tfb3 Trimer Complex with Differential Sensitivities to T-Loop Phosphorylation. Mol Cell Biol 22, 1288– 1297. 11839796 PMC134711
  44. Klein-Brill A, Joseph-Strauss D, Appleboim A, and Friedman N (2019). Dynamics of Chromatin and Transcription during Transient Depletion of the RSC Chromatin Remodeling Complex. Cell Reports 26, 279– 292.e5. 30605682 PMC6315372
  45. Knoll ER, Zhu ZI, Sarkar D, Landsman D, and Morse RH (2018). Role of the pre-initiation complex in Mediator recruitment and dynamics. ELife 7. PMC6322861 30540252
  46. Knoll ER, Zhu ZI, Sarkar D, Landsman D, and Morse RH (2020). Kin28 depletionincreases association of TFIID subunits Taf1 and Taf4 with promoters in Saccharomyces cerevisiae. Nucleic Acids Res 48, 4244– 4255. 32182349 PMC7192586
  47. Kraemer SM, Ranallo RT, Ogg RC, and Stargell LA (2001). TFIIA Interacts with TFIID via Association with TATA-Binding Protein and TAF40. Mol Cell Biol 21, 1737– 1746. 11238911 PMC86722
  48. Kubik S, Bruzzone MJ, Jacquet P, Falcone J-L, Rougemont J, and Shore D (2015). Nucleosome Stability Distinguishes Two Different Promoter Types at All Protein-Coding Genes in Yeast. Molecular Cell 60, 422– 434. 26545077
  49. Lauberth SM, Nakayama T, Wu X, Ferris AL, Tang Z, Hughes SH, and Roeder RG (2013). H3K4me3 Interactions with TAF3 Regulate Preinitiation Complex Assembly and Selective Gene Activation. Cell 152, 1021– 1036. 23452851 PMC3588593
  50. Layer JH, and Weil PA (2013). Direct TFIIA-TFIID protein contacts drive budding yeast ribosomal protein gene transcription. The Journal of Biological Chemistry 288, 23273– 23294. 23814059 PMC3743499
  51. Le SN, Brown CR, Harvey S, Boeger H, Elmlund H, and Elmlund D (2019). The TAFs of TFIID Bind and Rearrange the Topology of the TATA-Less RPS5 Promoter. International Journal of Molecular Sciences 20, 3290. PMC6650902 31277458
  52. Lee S, and Hahn S (1995). Model for binding of transcription factor TFIIB to the TBP-DNA complex. Nature 376, 609– 612. 7637813
  53. Lerner J, Gomez-Garcia PA, McCarthy RL, Liu Z, Lakadamyali M, and Zaret KS (2020). Two-Parameter Mobility Assessments Discriminate Diverse Regulatory Factor Behaviors in Chromatin. Mol Cell. PMC7483934 32574554
  54. Li J, Dong A, Saydaminova K, Chang H, Wang G, Ochiai H, Yamamoto T, and Pertsinidis A (2019). Single-Molecule Nanoscopy Elucidates RNA Polymerase II Transcription at Single Genes in Live Cells. Cell 178, 491– 506.e28. 31155237 PMC6675578
  55. Lim MK, Tang V, Saux AL, Schüller J, Bongards C, and Lehming N (2007). Gal11p Dosage-compensates Transcriptional Activator Deletions via Taf14p. J Mol Biol 374, 9– 23. 17919657
  56. Lionnet T, and Wu C (2021). Single-molecule tracking of transcription protein dynamics in living cells: seeing is believing, but what are we seeing? Curr Opin Genet Dev 67, 94– 102. 33422933 PMC9150788
  57. Loffreda A, Jacchetti E, Antunes S, Rainone P, Daniele T, Morisaki T, Bianchi ME, Tacchetti C, and Mazza D (2017). Live-cell p53 single-molecule binding is modulated by C-terminal acetylation and correlates with transcriptional activity. Nature Communications 8, 313. PMC5567047 28827596
  58. Los GV, Encell LP, McDougall MG, Hartzell DD, Karassina N, Zimprich C, Wood MG, Learish R, Ohana RF, Urh M, (2008). HaloTag: a novel protein labeling technology for cell imaging and protein analysis. ACS Chemical Biology 3, 373– 382. 18533659
  59. Maxon ME, Goodrich JA, and Tjian R (1994). Transcription factor IIE binds preferentially to RNA polymerase IIa and recruits TFIIH: a model for promoter clearance. Gene Dev 8, 515– 524. 7926747
  60. Mazza D, Abernathy A, Golob N, Morisaki T, and McNally JG (2012). A benchmark for chromatin binding measurements in live cells. Nucleic Acids Research 40, e119. 22844090 PMC3424588
  61. McSwiggen DT, Hansen AS, Teves SS, Marie-Nelly H, Hao Y, Heckert AB, Umemoto KK, Dugast-Darzacq C, Tjian R, and Darzacq X (2019). Evidence for DNA-mediated nuclear compartmentalization distinct from phase separation. Elife 8, e47098. 31038454 PMC6522219
  62. Medler S, and Ansari A (2015). Gene looping facilitates TFIIH kinase-mediated termination of transcription. Sci Rep-Uk 5, 12586. PMC4541409 26286112
  63. Mehta GD, Ball DA, Eriksson PR, Chereji RV, Clark DJ, McNally JG, and Karpova TS (2018). Single-Molecule Analysis Reveals Linked Cycles of RSC Chromatin Remodeling and Ace1p Transcription Factor Binding in Yeast. Molecular Cell 72, 875– 887.e9. 30318444 PMC6289719
  64. Miné-Hattab J, Recamier V, Izeddin I, Rothstein R, and Darzacq X (2017). Multi-scale tracking reveals scale-dependent chromatin dynamics after DNA damage. Mol Biol Cell 28, 3323– 3332. PMC5687033 28794266
  65. Murakami K, Mattei P-J, Davis RE, Jin H, Kaplan CD, and Kornberg RD (2015). Uncoupling Promoter Opening from Start-Site Scanning. Molecular Cell 59, 133– 138. 26073544 PMC4490988
  66. Neil H, Malabat C, d’Aubenton-Carafa Y, Xu Z, Steinmetz LM, and Jacquier A (2009). Widespread bidirectional promoters are the major source of cryptic transcripts in yeast. Nature 457, 1038– 1042. 19169244
  67. Normanno D, Dahan M, and Darzacq X (2012). Intra-nuclear mobility and target search mechanisms of transcription factors: A single-molecule perspective on gene expression. Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms 1819, 482– 493. 22342464
  68. Papai G, Tripathi MK, Ruhlmann C, Layer JH, Weil PA, and Schultz P (2010). TFIIA and the transactivator Rap1 cooperate to commit TFIID for transcription initiation. Nature 465, 956– 960. 20559389 PMC2900199
  69. Patel AB, Louder RK, Greber BJ, Grünberg S, Luo J, Fang J, Liu Y, Ranish J, Hahn S, and Nogales E (2018). Structure of human TFIID and mechanism of TBP loading onto promoter DNA. Science 362, eaau8872. 30442764 PMC6446905
  70. Pelechano V, Chávez S, and Pérez-Ortín JE (2010). A Complete Set of Nascent Transcription Rates for Yeast Genes. PLoS ONE 5, e15442. 21103382 PMC2982843
  71. Petrenko N, Jin Y, Wong KH, and Struhl K (2016). Mediator Undergoes a Compositional Change during Transcriptional Activation. Molecular Cell 64, 443– 454. 27773675 PMC5096951
  72. Petrenko N, Jin Y, Wong KH, and Struhl K (2017). Evidence that Mediator is essential for Pol II transcription, but is not a required component of the preinitiation complex in vivo. ELife 6. PMC5529107 28699889
  73. Qiu C, Jin H, Vvedenskaya I, Llenas JA, Zhao T, Malik I, Schwartz SL, Cui P, Čabart P, Han KH, (2019). Promoter scanning during transcription initiation in Saccharomyces cerevisiae: Pol II in the “shooting gallery.” Biorxiv 810127. PMC7265651 32487207
  74. Ramachandran S, Zentner GE, and Henikoff S (2015). Asymmetric nucleosomes flank promoters in the budding yeast genome. Genome Research 25, 381– 390. 25491770 PMC4352886
  75. Rani PG, Ranish JA, and Hahn S (2004). RNA Polymerase II (Pol II)-TFIIF and Pol II-Mediator Complexes: the Major Stable Pol II Complexes and Their Activity in Transcription Initiation and Reinitiation. Mol Cell Biol 24, 1709– 1720. 14749386 PMC344180
  76. Ranjan A, Nguyen VQ, Liu S, Wisniewski J, Kim JM, Tang X, Mizuguchi G, Elalaoui E, Nickels TJ, Jou V, (2020). Live-cell single particle imaging reveals the role of RNA polymerase II in histone H2A.Z eviction. Elife 9, e55667. 32338606 PMC7259955
  77. Rhee HS, and Pugh BF (2012). Genome-wide structure and organization of eukaryotic pre-initiation complexes. Nature 483, 295– 301. 22258509 PMC3306527
  78. Rimel JK, and Taatjes DJ (2018). The essential and multifunctional TFIIH complex. Protein Science 27, 1018– 1037. 29664212 PMC5980561
  79. Robinson PJ, Trnka MJ, Bushnell DA, Davis RE, Mattei P-J, Burlingame AL, and Kornberg RD (2016). Structure of a Complete Mediator-RNA Polymerase II Pre-Initiation Complex. Cell 166, 1411– 1422.e16. 27610567 PMC5589196
  80. Rodríguez-Molina JB, Tseng SC, Simonett SP, Taunton J, and Ansari AZ (2016). Engineered Covalent Inactivation of TFIIH-Kinase Reveals an Elongation Checkpoint and Results in Widespread mRNA Stabilization. Molecular Cell 63, 433– 444. 27477907 PMC5122673
  81. Schilbach S, Hantsche M, Tegunov D, Dienemann C, Wigge C, Urlaub H, and Cramer P (2017). Structures of transcription pre-initiation complex with TFIIH and Mediator. Nature 551, 204– 209. 29088706 PMC6078178
  82. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B, (2012). Fiji: an open-source platform for biological-image analysis. Nat Methods 9, 676– 682. 22743772 PMC3855844
  83. Shrinivas K, Sabari BR, Coffey EL, Klein IA, Boija A, Zamudio AV, Schuijers J, Hannett NM, Sharp PA, Young RA, (2019). Enhancer Features that Drive Formation of Transcriptional Condensates. Molecular Cell 75, 549– 561.e7. 31398323 PMC6690378
  84. Tatavosian R, Duc HN, Huynh TN, Fang D, Schmitt B, Shi X, Deng Y, Phiel C, Yao T, Zhang Z, (2018). Live-cell single-molecule dynamics of PcG proteins imposed by the DIPG H3.3K27M mutation. Nature Communications 9, 2080. PMC5970213 29802243
  85. Thevenaz P, Ruttimann UE, and Unser M (1998). A pyramid approach to subpixel registration based on intensity. Ieee T Image Process 7, 27– 41. 18267377
  86. Tuttle LM, Pacheco D, Warfield L, Luo J, Ranish J, Hahn S, and Klevit RE (2018). Gcn4-Mediator Specificity Is Mediated by a Large and Dynamic Fuzzy Protein-Protein Complex. Cell Reports 22, 3251– 3264. 29562181 PMC5908246
  87. Vallotton P, and Olivier S (2013). Tri-track: Free Software for Large-Scale Particle Tracking. Microscopy and Microanalysis 19, 451– 460. 23448973
  88. Vermeulen M, Mulder KW, Denissov S, Pijnappel WWMP, van Schaik FMA, Varier RA, Baltissen MPA, Stunnenberg HG, Mann M, and Timmers H.Th.M. (2007). Selective Anchoring of TFIID to Nucleosomes by Trimethylation of Histone H3 Lysine 4. Cell 131, 58– 69. 17884155
  89. Warfield L, Ramachandran S, Baptista T, Devys D, Tora L, and Hahn S (2017). Transcription of Nearly All Yeast RNA Polymerase II-Transcribed Genes Is Dependent on Transcription Factor TFIID. Molecular Cell 68. PMC5679267 28918900
  90. van Werven FJ, van Teeffelen HAAM, Holstege FCP, and Timmers HTM (2009). Distinct promoter dynamics of the basal transcription factor TBP across the yeast genome. Nature Structural & Molecular Biology 16, 1043– 1048. 19767748
  91. Wieser S, and Schütz GJ (2008). Tracking single molecules in the live cell plasma membrane—Do’s and Don’t’s. Methods 46, 131– 140. 18634880
  92. Wong KH, Jin Y, and Struhl K (2014). TFIIH phosphorylation of the Pol II CTD stimulates mediator dissociation from the preinitiation complex and promoter escape. Molecular Cell 54, 601– 612. 24746699 PMC4035452
  93. Woringer M, and Darzacq X (2018). Protein motion in the nucleus: from anomalous diffusion to weak interactions. Biochem Soc T 46, BST20170310. PMC6103463 30065106
  94. Woringer M, Darzacq X, and Izeddin I (2014). Geometry of the nucleus: a perspective on gene expression regulation. Current Opinion in Chemical Biology 20, 112– 119. 24981829
  95. Xu Z, Wei W, Gagneur J, Perocchi F, Clauder-Münster S, Camblong J, Guffanti E, Stutz F, Huber W, and Steinmetz LM (2009). Bidirectional promoters generate pervasive transcription in yeast. Nature 457, 1033– 1037. 19169243 PMC2766638
  96. Xue Y, Pradhan SK, Sun F, Chronis C, Tran N, Su T, Van C, Vashisht A, Wohlschlegel J, Peterson CL, (2017). Mot1, Ino80C, and NC2 Function Coordinately to Regulate Pervasive Transcription in Yeast and Mammals. Molecular Cell 67, 594– 607.e4. 28735899 PMC5573681
  97. Zawel L, Kumar KP, and Reinberg D (1995). Recycling of the general transcription factors during RNA polymerase II transcription. Gene Dev 9, 1479– 1490. 7601352
  98. Zhang Z, English BP, Grimm JB, Kazane SA, Hu W, Tsai A, Inouye C, You C, Piehler J, Schultz PG, (2016). Rapid dynamics of general transcription factor TFIIB binding during preinitiation complex assembly revealed by single-molecule analysis. Genes & Development 30, 2106– 2118. 27798851 PMC5066616
  99. Zheng Q, Ayala AX, Chung I, Weigel AV, Ranjan A, Falco N, Grimm JB, Tkachuk AN, Wu C, Lippincott-Schwartz J, (2019). Rational Design of Fluorogenic and Spontaneously Blinking Labels for Super-Resolution Imaging. Acs Central Sci 5, 1602– 1613. PMC6764213 31572787

Cited by

Sorted by citations

Authors
Nguyen, V. Q., Ranjan, A., Liu, S., Tang, X., Ling, Y. H., Wisniewski, J., Mizuguchi, G., Li, K. Y., Jou, V., Zheng, Q., Lavis, L. D., Lionnet, T., & Wu, C.
Affiliations
  • Johns Hopkins University (US)
  • Howard Hughes Medical Institute (US)
  • NYU Langone Health (US)
Corresponding author
Wu, Carl
ORCID
Venue
Molecular Cell
Publisher
Elsevier BV
Published
2021-09
Volume
81
Issue
17
Pages
3560-3575.e6
ISSN
1097-2765 (ISSN-L)
DOI
10.1016/j.molcel.2021.07.022
PMC
PMC8420877
OpenAlex
W3189598002
Cited by
115
References
6
Citations by year
2026: 10 · 2025: 26 · 2024: 32 · 2023: 15 · 2022: 19 · 2021: 13
FWCI
6.20
Type
journal article
Language
en
Open access
Licence
Locations
  • Molecular Cell (publishedVersion)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • Howard Hughes Medical Institute
  • National Institutes of Health (GM132290-01, JF552/646)
  • Damon Runyon Cancer Research Foundation
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nuclear Structure and Function
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Chromatin Remodeling and Cancer
Keywords
RNA polymerase II, Mediator complex, TFIID, TATA-binding protein, promoter accessibility, chromatin remodeling, spatiotemporal coordination, single-molecule tracking, live-cell imaging, Saccharomyces cerevisiae
MeSH terms
Chromatin, Nucleosomes, Promoter Regions, Genetic, Protein Binding, RNA Polymerase II, Saccharomyces cerevisiae, Transcription, Genetic, Saccharomyces cerevisiae Proteins, TATA-Box Binding Protein, Transcription Factor TFIID, Chromatin Assembly and Disassembly, Mediator Complex, Transcription Initiation, Genetic, Spatio-Temporal Analysis

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review