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Review Article

Collaborators or competitors: the communication between RNA polymerase II and the nucleosome during eukaryotic transcription

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Received 26 Nov 2023, Accepted 12 Jan 2024, Published online: 30 Jan 2024

References

  • Abril-Garrido J, Dienemann C, Grabbe F, Velychko T, Lidschreiber M, Wang H, Cramer P. 2023. Structural basis of transcription reduction by a promoter-proximal +1 nucleosome. Mol Cell. 83(11):1798–1809 e1797. doi: 10.1016/j.molcel.2023.04.011.
  • Akhtar MS, Heidemann M, Tietjen JR, Zhang DW, Chapman RD, Eick D, Ansari AZ. 2009. TFIIH kinase places bivalent marks on the carboxy-terminal domain of RNA polymerase II. Mol Cell. 34(3):387–393. doi: 10.1016/j.molcel.2009.04.016.
  • Allfrey VG, Faulkner R, Mirsky AE. 1964. Acetylation and methylation of histones and their possible role in the regulation of RNA synthesis. Proc Natl Acad Sci USA. 51(5):786–794. doi: 10.1073/pnas.51.5.786.
  • Allison LA, Moyle M, Shales M, Ingles CJ. 1985. Extensive homology among the largest subunits of eukaryotic and prokaryotic RNA polymerases. Cell. 42(2):599–610. doi: 10.1016/0092-8674(85)90117-5.
  • Bae HJ, Dubarry M, Jeon J, Soares LM, Dargemont C, Kim J, Geli V, Buratowski S. 2020. The Set1 N-terminal domain and Swd2 interact with RNA polymerase II CTD to recruit COMPASS. Nat Commun. 11(1):2181. doi: 10.1038/s41467-020-16082-2.
  • Barillà D, Lee BA, Proudfoot NJ. 2001. Cleavage/polyadenylation factor IA associates with the carboxyl-terminal domain of RNA polymerase II in Saccharomyces cerevisiae. Proc Natl Acad Sci USA. 98(2):445–450. doi: 10.1073/pnas.98.2.445.
  • Belotserkovskaya R, Oh S, Bondarenko VA, Orphanides G, Studitsky VM, Reinberg D. 2003. FACT facilitates transcription-dependent nucleosome alteration. Science. 301(5636):1090–1093. doi: 10.1126/science.1085703.
  • Bhattacharya S, Levy MJ, Zhang N, Li H, Florens L, Washburn MP, Workman JL. 2021. The methyltransferase SETD2 couples transcription and splicing by engaging mRNA processing factors through its SHI domain. Nat Commun. 12(1):1443. doi: 10.1038/s41467-021-21663-w.
  • Bondarenko VA, Steele LM, Ujvári A, Gaykalova DA, Kulaeva OI, Polikanov YS, Luse DS, Studitsky VM. 2006. Nucleosomes can form a polar barrier to transcript elongation by RNA polymerase II. Mol Cell. 24(3):469–479. doi: 10.1016/j.molcel.2006.09.009.
  • Buratowski S. 2003. The CTD code. Nat Struct Biol. 10(9):679–680. doi: 10.1038/nsb0903-679.
  • Bushnell DA, Kornberg RD. 2003. Complete, 12-subunit RNA polymerase II at 4.1-Å resolution: implications for the initiation of transcription. Proc Natl Acad Sci USA. 100(12):6969–6973. doi: 10.1073/pnas.1130601100.
  • Chen S, Li J, Wang DL, Sun FL. 2012. Histone H2B lysine 120 monoubiquitination is required for embryonic stem cell differentiation. Cell Res. 22(9):1402–1405. doi: 10.1038/cr.2012.114.
  • Chen X, Wang X, Liu W, Ren Y, Qu X, Li J, Yin X, Xu Y. 2022. Structures of +1 nucleosome-bound PIC-Mediator complex. Science. 378(6615):62–68. doi: 10.1126/science.abn8131.
  • Chen X, Liu W, Wang Q, Wang X, Ren Y, Qu X, Li W, Xu Y. 2023. Structrual visualization of transcription initiation in action. Science. 382(6677):eadi5120. doi: 10.1126/science.adi5120.
  • Chen ZJ, Gabizon R, Brown AI, Lee A, Song AX, Díaz-Celis C, Kaplan CD, Koslover EF, Yao TT, Bustamante C. 2019. High-resolution and high-accuracy topographic and transcriptional maps of the nucleosome barrier. Elife. 8:e48281. doi: 10.7554/eLife.48281.
  • Cho EJ, Takagi T, Moore CR, Buratowski S. 1997. mRNA capping enzyme is recruited to the transcription complex by phosphorylation of the RNA polymerase II carboxy-terminal domain. Genes Dev. 11(24):3319–3326. doi: 10.1101/gad.11.24.3319.
  • Chow CM, Georgiou A, Szutorisz H, Maia e Silva A, Pombo A, Barahona I, Dargelos E, Canzonetta C, Dillon N. 2005. Variant histone H3.3 marks promoters of transcriptionally active genes during mammalian cell division. EMBO Rep. 6(4):354–360. doi: 10.1038/sj.embor.7400366.
  • Clements A, Poux AN, Lo WS, Pillus L, Berger SL, Marmorstein R. 2003. Structural basis for histone and phosphohistone binding by the GCN5 histone acetyltransferase. Mol Cell. 12(2):461–473. doi: 10.1016/s1097-2765(03)00288-0.
  • Cobos SN, Bennett SA, Torrente MP. 2019. The impact of histone post-translational modifications in neurodegenerative diseases. Biochim Biophys Acta Mol Basis Dis. 1865(8):1982–1991. doi: 10.1016/j.bbadis.2018.10.019.
  • Cole HA, Ocampo J, Iben JR, Chereji RV, Clark DJ. 2014. Heavy transcription of yeast genes correlates with differential loss of histone H2B relative to H4 and queued RNA polymerases. Nucleic Acids Res. 42(20):12512–12522. doi: 10.1093/nar/gku1013.
  • Corden JL, Cadena DL, Ahearn JM, Jr., Dahmus ME. 1985. A unique structure at the carboxyl terminus of the largest subunit of eukaryotic RNA polymerase II. Proc Natl Acad Sci USA. 82(23):7934–7938. doi: 10.1073/pnas.82.23.7934.
  • Cosgrove MS, Boeke JD, Wolberger C. 2004. Regulated nucleosome mobility and the histone code. Nat Struct Mol Biol. 11(11):1037–1043. doi: 10.1038/nsmb851.
  • Cramer P, Bushnell DA, Fu J, Gnatt AL, Maier-Davis B, Thompson NE, Burgess RR, Edwards AM, David PR, Kornberg RD. 2000. Architecture of RNA polymerase II and implications for the transcription mechanism. Science. 288(5466):640–649. doi: 10.1126/science.288.5466.640.
  • Cramer P, Bushnell DA, Kornberg RD. 2001. Structural basis of transcription: RNA polymerase II at 2.8 Ångstrom resolution. Science. 292(5523):1863–1876. doi: 10.1126/science.1059493.
  • Czudnochowski N, Bösken CA, Geyer M. 2012. Serine-7 but not serine-5 phosphorylation primes RNA polymerase II CTD for P-TEFb recognition. Nat Commun. 3(1):842. doi: 10.1038/ncomms1846.
  • Dey A, Chitsaz F, Abbasi A, Misteli T, Ozato K. 2003. The double bromodomain protein Brd4 binds to acetylated chromatin during interphase and mitosis. Proc Natl Acad Sci USA. 100(15):8758–8763. doi: 10.1073/pnas.1433065100.
  • Dion MF, Kaplan T, Kim M, Buratowski S, Friedman N, Rando OJ. 2007. Dynamics of replication-independent histone turnover in budding yeast. Science. 315(5817):1405–1408. doi: 10.1126/science.1134053.
  • Escobar EE, Ramani MKV, Zhang Y, Brodbelt JS. 2021. Evaluating spatiotemporal dynamics of phosphorylation of RNA polymerase II carboxy-terminal domain by ultraviolet photodissociation mass spectrometry. J Am Chem Soc. 143(22):8488–8498. doi: 10.1021/jacs.1c03321.
  • Edwards AM, Kane CM, Young RA, Kornberg RD. 1991. Two dissociable subunits of yeast RNA polymerase II stimulate the initiation of transcription at a promoter in vitro. J Biol Chem. 266(1):71–75. doi: 10.1016/S0021-9258(18)52403-0.
  • Ehara H, Yokoyama T, Shigematsu H, Yokoyama S, Shirouzu M, Sekine SI. 2017. Structure of the complete elongation complex of RNA polymerase II with basal factors. Science. 357(6354):921–924. doi: 10.1126/science.aan8552.
  • Ehara H, Kujirai T, Fujino Y, Shirouzu M, Kurumizaka H, Sekine SI. 2019. Structural insight into nucleosome transcription by RNA polymerase II with elongation factors. Science. 363(6428):744–747. doi: 10.1126/science.aav8912.
  • Ehara H, Kujirai T, Shirouzu M, Kurumizaka H, Sekine SI. 2022. Structural basis of nucleosome disassembly and reassembly by RNAPII elongation complex with FACT. Science. 377(6611):eabp9466. doi: 10.1126/science.abp9466.
  • Eick D, Geyer M. 2013. The RNA polymerase II carboxy-terminal domain (CTD) code. Chem Rev. 113(11):8456–8490. doi: 10.1021/cr400071f.
  • Farnung L, Ochmann M, Engeholm M, Cramer P. 2021. Structural basis of nucleosome transcription mediated by Chd1 and FACT. Nat Struct Mol Biol. 28(4):382–387. doi: 10.1038/s41594-021-00578-6.
  • Farnung L, Ochmann M, Garg G, Vos SM, Cramer P. 2022. Structure of a backtracked hexasomal intermediate of nucleosome transcription. Mol Cell. 82(17):3126–3134 e3127. doi: 10.1016/j.molcel.2022.06.027.
  • Farnung L, Vos SM, Cramer P. 2018. Structure of transcribing RNA polymerase II-nucleosome complex. Nat Commun. 9(1):5432. doi: 10.1038/s41467-018-07870-y.
  • Fetian T, McShane BM, Horan NL, Shodja DN, True JD, Mosley AL, Arndt KM. 2023. Paf1 complex subunit Rtf1 stimulates H2B ubiquitylation by interacting with the highly conserved N-terminal helix of Rad6. Proc Natl Acad Sci USA. 120(22):e2220041120. doi: 10.1073/pnas.2220041120.
  • Fianu I, Chen Y, Dienemann C, Dybkov O, Linden A, Urlaub H, Cramer P. 2021. Structural basis of Integrator-mediated transcription regulation. Science. 374(6569):883–887. doi: 10.1126/science.abk0154.
  • Filipovski M, Soffers JHM, Vos SM, Farnung L. 2022. Structural basis of nucleosome retention during transcription elongation. Science. 376(6599):1313–1316. doi: 10.1126/science.abo3851.
  • Filippakopoulos P, Qi J, Picaud S, Shen Y, Smith WB, Fedorov O, Morse EM, Keates T, Hickman TT, Felletar I, et al. 2010. Selective inhibition of BET bromodomains. Nature. 468(7327):1067–1073. doi: 10.1038/nature09504.
  • Glover-Cutter K, Larochelle S, Erickson B, Zhang C, Shokat K, Fisher RP, Bentley DL. 2009. TFIIH-associated Cdk7 kinase functions in phosphorylation of C-terminal domain Ser7 residues, promoter-proximal pausing, and termination by RNA polymerase II. Mol Cell Biol. 29(20):5455–5464. doi: 10.1128/MCB.00637-09.
  • Gnatt AL, Cramer P, Fu J, Bushnell DA, Kornberg RD. 2001. Structural basis of transcription: an RNA polymerase II elongation complex at 3.3 A resolution. Science. 292(5523):1876–1882. doi: 10.1126/science.1059495.
  • Hintermair C, Heidemann M, Koch F, Descostes N, Gut M, Gut I, Fenouil R, Ferrier P, Flatley A, Kremmer E, et al. 2012. Threonine-4 of mammalian RNA polymerase II CTD is targeted by Polo-like kinase 3 and required for transcriptional elongation. EMBO J. 31(12):2784–2797. doi: 10.1038/emboj.2012.123.
  • Hirano R, Ehara H, Kujirai T, Uejima T, Takizawa Y, Sekine SI, Kurumizaka H. 2022. Structural basis of RNA polymerase II transcription on the chromatosome containing linker histone H1. Nat Commun. 13(1):7287. doi: 10.1038/s41467-022-35003-z.
  • Hsin JP, Sheth A, Manley JL. 2011. RNAP II CTD phosphorylated on threonine-4 is required for histone mRNA 3′ end processing. Science. 334(6056):683–686. doi: 10.1126/science.1206034.
  • Hyun K, Jeon J, Park K, Kim J. 2017. Writing, erasing and reading histone lysine methylations. Exp Mol Med. 49(4):e324–e324. doi: 10.1038/emm.2017.11.
  • Irani S, Sipe SN, Yang WJ, Burkholder NT, Lin B, Sim K, Matthews WL, Brodbelt JS, Zhang Y. 2019. Structural determinants for accurate dephosphorylation of RNA polymerase II by its cognate C-terminal domain (CTD) phosphatase during eukaryotic transcription. J Biol Chem. 294(21):8592–8605. doi: 10.1074/jbc.RA119.007697.
  • Itzen F, Greifenberg AK, Bösken CA, Geyer M. 2014. Brd4 activates P-TEFb for RNA polymerase II CTD phosphorylation. Nucleic Acids Res. 42(12):7577–7590. doi: 10.1093/nar/gku449.
  • Jacobson RH, Ladurner AG, King DS, Tjian R. 2000. Structure and function of a human TAFII250 double bromodomain module. Science. 288(5470):1422–1425. doi: 10.1126/science.288.5470.1422.
  • Jamai A, Imoberdorf RM, Strubin M. 2007. Continuous histone H2B and transcription-dependent histone H3 exchange in yeast cells outside of replication. Mol Cell. 25(3):345–355. doi: 10.1016/j.molcel.2007.01.019.
  • Kettenberger H, Armache KJ, Cramer P. 2003. Architecture of the RNA polymerase II-TFIIS complex and implications for mRNA cleavage. Cell. 114(3):347–357. doi: 10.1016/S0092-8674(03)00598-1.
  • Kim M, Krogan NJ, Vasiljeva L, Rando OJ, Nedea E, Greenblatt JF, Buratowski S. 2004. The yeast Rat1 exonuclease promotes transcription termination by RNA polymerase II. Nature. 432(7016):517–522. doi: 10.1038/nature03041.
  • Kimura H, Cook PR. 2001. Kinetics of core histones in living human cells: little exchange of H3 and H4 and some rapid exchange of H2B. J Cell Biol. 153(7):1341–1353. doi: 10.1083/jcb.153.7.1341.
  • Kireeva ML, Walter W, Tchernajenko V, Bondarenko V, Kashlev M, Studitsky VM. 2002. Nucleosome remodeling induced by RNA polymerase II: loss of the H2A/H2B dimer during transcription. Mol Cell. 9(3):541–552. doi: 10.1016/s1097-2765(02)00472-0.
  • Knezetic JA, Luse DS. 1986. The presence of nucleosomes on a DNA template prevents initiation by RNA polymerase II in vitro. Cell. 45(1):95–104. doi: 10.1016/0092-8674(86)90541-6.
  • Komar D, Juszczynski P. 2020. Rebelled epigenome: histone H3S10 phosphorylation and H3S10 kinases in cancer biology and therapy. Clin Epigenetics. 12(1):147. doi: 10.1186/s13148-020-00941-2.
  • Krogan NJ, Dover J, Wood A, Schneider J, Heidt J, Boateng MA, Dean K, Ryan OW, Golshani A, Johnston M, et al. 2003. The Paf1 complex is required for histone H3 methylation by COMPASS and Dot1p: linking transcriptional elongation to histone methylation. Mol Cell. 11(3):721–729. doi: 10.1016/s1097-2765(03)00091-1.
  • Krogan NJ, Kim M, Tong A, Golshani A, Cagney G, Canadien V, Richards DP, Beattie BK, Emili A, Boone C, et al. 2003. Methylation of histone H3 by Set2 in Saccharomyces cerevisiae is linked to transcriptional elongation by RNA polymerase II. Mol Cell Biol. 23(12):4207–4218. doi: 10.1128/MCB.23.12.4207-4218.2003.
  • Kujirai T, Ehara H, Fujino Y, Shirouzu M, Sekine SI, Kurumizaka H. 2018. Structural basis of the nucleosome transition during RNA polymerase II passage. Science. 362(6414):595–598. doi: 10.1126/science.aau9904.
  • Kulaeva OI, Gaykalova DA, Pestov NA, Golovastov VV, Vassylyev DG, Artsimovitch I, Studitsky VM. 2009. Mechanism of chromatin remodeling and recovery during passage of RNA polymerase II. Nat Struct Mol Biol. 16(12):1272–1278. doi: 10.1038/nsmb.1689.
  • Lauberth SM, Nakayama T, Wu X, Ferris AL, Tang Z, Hughes SH, Roeder RG. 2013. H3K4me3 interactions with TAF3 regulate preinitiation complex assembly and selective gene activation. Cell. 152(5):1021–1036. doi: 10.1016/j.cell.2013.01.052.
  • Lee JE, Park YK, Park S, Jang Y, Waring N, Dey A, Ozato K, Lai B, Peng W, Ge K. 2017. Brd4 binds to active enhancers to control cell identity gene induction in adipogenesis and myogenesis. Nat Commun. 8(1):2217. doi: 10.1038/s41467-017-02403-5.
  • Lee JS, Shukla A, Schneider J, Swanson SK, Washburn MP, Florens L, Bhaumik SR, Shilatifard A. 2007. Histone crosstalk between H2B monoubiquitination and H3 methylation mediated by COMPASS. Cell. 131(6):1084–1096. doi: 10.1016/j.cell.2007.09.046.
  • Lin Y, Qiu T, Wei G, Que Y, Wang W, Kong Y, Xie T, Chen X. 2022. Role of histone post-translational modifications in inflammatory diseases. Front Immunol. 13:852272. doi: 10.3389/fimmu.2022.852272.
  • Lo WS, Duggan L, Emre NCT, Belotserkovskya R, Lane WS, Shiekhattar R, Berger SL. 2001. Snf1 - a histone kinase that works in concert with the histone acetyltransferase Gcn5 to regulate transcription. Science. 293(5532):1142–1146. doi: 10.1126/science.1062322.
  • Lo WS, Trievel RC, Rojas JR, Duggan L, Hsu JY, Allis CD, Marmorstein R, Berger SL. 2000. Phosphorylation of serine 10 in histone H3 is functionally linked in vitro and in vivo to Gcn5-mediated acetylation at lysine 14. Mol Cell. 5(6):917–926. doi: 10.1016/s1097-2765(00)80257-9.
  • Lu H, Flores O, Weinmann R, Reinberg D. 1991. The nonphosphorylated form of RNA polymerase II preferentially associates with the preinitiation complex. Proc Natl Acad Sci USA. 88(22):10004–10008. doi: 10.1073/pnas.88.22.10004.
  • Lu H, Zawel L, Fisher L, Egly JM, Reinberg D. 1992. Human general transcription factor IIH phosphorylates the C-terminal domain of RNA polymerase II. Nature. 358(6388):641–645. doi: 10.1038/358641a0.
  • Luger K, Mäder AW, Richmond RK, Sargent DF, Richmond TJ. 1997. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature. 389(6648):251–260. doi: 10.1038/38444.
  • Marshall NF, Peng J, Xie Z, Price DH. 1996. Control of RNA polymerase II elongation potential by a novel carboxyl-terminal domain kinase. J Biol Chem. 271(43):27176–27183. doi: 10.1074/jbc.271.43.27176.
  • Martin BJE, Brind’Amour J, Kuzmin A, Jensen KN, Liu ZC, Lorincz M, Howe LJ. 2021. Transcription shapes genome-wide histone acetylation patterns. Nat Commun. 12(1):210. doi: 10.1038/s41467-020-20543-z.
  • Mayer A, Lidschreiber M, Siebert M, Leike K, Söding J, Cramer P. 2010. Uniform transitions of the general RNA polymerase II transcription complex. Nat Struct Mol Biol. 17(10):1272–1278. doi: 10.1038/nsmb.1903.
  • Mayfield JE, Irani S, Escobar EE, Zhang Z, Burkholder NT, Robinson MR, Mehaffey MR, Sipe SN, Yang W, Prescott NA, et al. 2019. Tyr1 phosphorylation promotes phosphorylation of Ser2 on the C-terminal domain of eukaryotic RNA polymerase II by P-TEFb. Elife. 8:e48725. doi: 10.7554/eLife.48725.
  • McCracken S, Fong N, Yankulov K, Ballantyne S, Pan G, Greenblatt J, Patterson SD, Wickens M, Bentley DL. 1997. The C-terminal domain of RNA polymerase II couples mRNA processing to transcription. Nature. 385(6614):357–361. doi: 10.1038/385357a0.
  • Meinhart A, Cramer P. 2004. Recognition of RNA polymerase II carboxy-terminal domain by 3’-RNA-processing factors. Nature. 430(6996):223–226. doi: 10.1038/nature02679.
  • Michels AA, Fraldi A, Li Q, Adamson TE, Bonnet F, Nguyen VT, Sedore SC, Price JP, Price DH, Lania L, et al. 2004. Binding of the 7SK snRNA turns the HEXIM1 protein into a P-TEFb (CDK9/cyclin T) inhibitor. Embo J. 23(13):2608–2619. doi: 10.1038/sj.emboj.7600275.
  • Miller T, Krogan NJ, Dover J, Erdjument-Bromage H, Tempst P, Johnston M, Greenblatt JF, Shilatifard A. 2001. COMPASS: a complex of proteins associated with a trithorax-related SET domain protein. Proc Natl Acad Sci USA. 98(23):12902–12907. doi: 10.1073/pnas.231473398.
  • Moreno RY, Juetten KJ, Panina SB, Butalewicz JP, Floyd BM, Ramani MKV, Marcotte EM, Brodbelt JS, Zhang YJ. 2023. Distinctive interactomes of RNA polymerase II phosphorylation during different stages of transcription. Iscience. 26(9):107581. doi: 10.1016/j.isci.2023.107581.
  • Mylonas C, Lee C, Auld AL, Cisse II, Boyer LA. 2021. A dual role for H2A.Z.1 in modulating the dynamics of RNA polymerase II initiation and elongation. Nat Struct Mol Biol. 28(5):435–442. doi: 10.1038/s41594-021-00589-3.
  • Ng HH, Robert F, Young RA, Struhl K. 2003. Targeted recruitment of Set1 histone methylase by elongating Pol II provides a localized mark and memory of recent transcriptional activity. Mol Cell. 11(3):709–719. doi: 10.1016/s1097-2765(03)00092-3.
  • Nguyen VT, Kiss T, Michels AA, Bensaude O. 2001. 7SK small nuclear RNA binds to and inhibits the activity of CDK9/cyclin T complexes. Nature. 414(6861):322–325. doi: 10.1038/35104581.
  • Orlicky SM, Tran PT, Sayre MH, Edwards AM. 2001. Dissociable Rpb4-Rpb7 subassembly of RNA polymerase II binds to single-strand nucleic acid and mediates a post-recruitment step in transcription initiation. J Biol Chem. 276(13):10097–10102. doi: 10.1074/jbc.M003165200.
  • Osumi K, Kujirai T, Ehara H, Ogasawara M, Kinoshita C, Saotome M, Kagawa W, Sekine SI, Takizawa Y, Kurumizaka H. 2023. Structural basis of damaged nucleotide recognition by transcribing RNA polymerase II in the nucleosome. J Mol Biol. 435(13):168130. doi: 10.1016/j.jmb.2023.168130.
  • Peplow M. 2020. Cryo-electron microscopy reaches resolution milestone. ACS Cent Sci. 6(8):1274–1277. doi: 10.1021/acscentsci.0c01048.
  • Piro AS, Mayekar MK, Warner MH, Davis CP, Arndt KM. 2012. Small region of Rtf1 protein can substitute for complete Paf1 complex in facilitating global histone H2B ubiquitylation in yeast. Proc Natl Acad Sci USA. 109(27):10837–10842. doi: 10.1073/pnas.1116994109.
  • Ramachandran S, Ahmad K, Henikoff S. 2017. Transcription and remodeling produce asymmetrically unwrapped nucleosomal intermediates. Mol Cell. 68(6):1038–1053.e1034. doi: 10.1016/j.molcel.2017.11.015.
  • Ramani MKV, Escobar EE, Irani S, Mayfield JE, Moreno RY, Butalewicz JP, Cotham VC, Wu HY, Tadros M, Brodbelt JS, et al. 2020. Structural motifs for CTD kinase specificity on RNA polymerase II during eukaryotic transcription. ACS Chem Biol. 15(8):2259–2272. doi: 10.1021/acschembio.0c00474.
  • Ramazi S, Allahverdi A, Zahiri J. 2020. Evaluation of post-translational modifications in histone proteins: a review on histone modification defects in developmental and neurological disorders. J Biosci. 45:135. doi: 10.1007/s12038-020-00099-2
  • Roeder RG, Rutter WJ. 1969. Multiple forms of DNA-dependent RNA polymerase in eukaryotic organisms. Nature. 224(5216):234–237. doi: 10.1038/224234a0.
  • Rossetto D, Avvakumov N, Côté J. 2012. Histone phosphorylation: a chromatin modification involved in diverse nuclear events. Epigenetics. 7(10):1098–1108. doi: 10.4161/epi.21975.
  • Schilbach S, Wang HB, Dienemann C, Cramer P. 2023. Yeast PIC- mediator structure with RNA polymerase II C-terminal domain. Proc Natl Acad Sci USA. 120(15):e2220542120. doi: 10.1073/pnas.2220542120.
  • Schneider J, Wood A, Lee JS, Schuster R, Dueker J, Maguire C, Swanson SK, Florens L, Washburn MP, Shilatifard A. 2005. Molecular regulation of histone H3 trimethylation by COMPASS and the regulation of gene expression. Mol Cell. 19(6):849–856. doi: 10.1016/j.molcel.2005.07.024.
  • Simboeck E, Sawicka A, Zupkovitz G, Senese S, Winter S, Dequiedt F, Ogris E, Di Croce L, Chiocca S, Seiser C. 2010. A phosphorylation switch regulates the transcriptional activation of cell cycle regulator p21 by histone deacetylase inhibitors. J Biol Chem. 285(52):41062–41073. doi: 10.1074/jbc.M110.184481.
  • Simpson RT. 1978. Structure of the chromatosome, a chromatin particle containing 160 base pairs of DNA and all the histones. Biochemistry. 17(25):5524–5531. doi: 10.1021/bi00618a030.
  • Skaar JR, Ferris AL, Wu X, Saraf A, Khanna KK, Florens L, Washburn MP, Hughes SH, Pagano M. 2015. The integrator complex controls the termination of transcription at diverse classes of gene targets. Cell Res. 25(3):288–305. doi: 10.1038/cr.2015.19.
  • Sklar VE, Schwartz LB, Roeder RG. 1975. Distinct molecular structures of nuclear class I, II, and III DNA-dependent RNA polymerases. Proc Natl Acad Sci USA. 72(1):348–352. doi: 10.1073/pnas.72.1.348.
  • Tahirov TH, Babayeva ND, Varzavand K, Cooper JJ, Sedore SC, Price DH. 2010. Crystal structure of HIV-1 Tat complexed with human P-TEFb. Nature. 465(7299):747–751. doi: 10.1038/nature09131.
  • Tamburri S, Lavarone E, Fernández-Pérez D, Conway E, Zanotti M, Manganaro D, Pasini D. 2020. Histone H2AK119 mono-ubiquitination is essential for polycomb-mediated transcriptional repression. Mol Cell. 77(4):840–856 e845. doi: 10.1016/j.molcel.2019.11.021.
  • Tomkuvienė M, Meier M, Ikasalaitė D, Wildenauer J, Kairys V, Klimašauskas S, Manelytė L. 2022. Enhanced nucleosome assembly at CpG sites containing an extended 5-methylcytosine analogue. Nucleic Acids Res. 50(11):6549–6561. doi: 10.1093/nar/gkac444.
  • Tramantano M, Sun L, Au C, Labuz D, Liu Z, Chou M, Shen C, Luk E. 2016. Constitutive turnover of histone H2A.Z at yeast promoters requires the preinitiation complex. Elife. 5:e14243. doi: 10.7554/eLife.14243.
  • Urbanek A, Popovic M, Elena-Real CA, Morató A, Estaña A, Fournet A, Allemand F, Gil AM, Cativiela C, Cortés J, et al. 2020. Evidence of the reduced abundance of proline cis conformation in protein poly proline tracts. J Am Chem Soc. 142(17):7976–7986. doi: 10.1021/jacs.0c02263.
  • Venkatesh S, Workman JL. 2015. Histone exchange, chromatin structure and the regulation of transcription. Nat Rev Mol Cell Biol. 16(3):178–189. doi: 10.1038/nrm3941.
  • Vermeulen M, Mulder KW, Denissov S, Pijnappel WW, van Schaik FM, Varier RA, Baltissen MP, Stunnenberg HG, Mann M, Timmers HT. 2007. Selective anchoring of TFIID to nucleosomes by trimethylation of histone H3 lysine 4. Cell. 131(1):58–69. doi: 10.1016/j.cell.2007.08.016.
  • Vojnic E, Simon B, Strahl BD, Sattler M, Cramer P. 2006. Structure and carboxyl-terminal domain (CTD) binding of the Set2 SRI domain that couples histone H3 Lys36 methylation to transcription. J Biol Chem. 281(1):13–15. doi: 10.1074/jbc.C500423200.
  • Wada T, Takagi T, Yamaguchi Y, Ferdous A, Imai T, Hirose S, Sugimoto S, Yano K, Hartzog GA, Winston F, et al. 1998. DSIF, a novel transcription elongation factor that regulates RNA polymerase II processivity, is composed of human Spt4 and Spt5 homologs. Genes Dev. 12(3):343–356. doi: 10.1101/gad.12.3.343.
  • Wang H, Fan Z, Shliaha PV, Miele M, Hendrickson RC, Jiang X, Helin K. 2023. H3K4me3 regulates RNA polymerase II promoter-proximal pause-release. Nature. 615(7951):339–348. doi: 10.1038/s41586-023-05780-8.
  • Wang H, Schilbach S, Ninov M, Urlaub H, Cramer P. 2023. Structures of transcription preinitiation complex engaged with the +1 nucleosome. Nat Struct Mol Biol. 30(2):226–232. doi: 10.1038/s41594-022-00865-w.
  • Weber CM, Henikoff S. 2014. Histone variants: dynamic punctuation in transcription. Genes Dev. 28(7):672–682. doi: 10.1101/gad.238873.114.
  • West MH, Bonner WM. 1980. Histone 2B can be modified by the attachment of ubiquitin. Nucleic Acids Res. 8(20):4671–4680. doi: 10.1093/nar/8.20.4671.
  • Weiss MS, Jabs A, Hilgenfeld R. 1998. Peptide bonds revisited. Nat Struct Biol. 5(8):676. doi: 10.1038/1368.
  • Wood A, Schneider J, Dover J, Johnston M, Shilatifard A. 2003. The Paf1 complex is essential for histone monoubiquitination by the Rad6-Bre1 complex, which signals for histone methylation by COMPASS and Dot1p. J Biol Chem. 278(37):34739–34742. doi: 10.1074/jbc.C300269200.
  • Yamada T, Yamaguchi Y, Inukai N, Okamoto S, Mura T, Handa H. 2006. P-TEFb-mediated phosphorylation of hSpt5 C-terminal repeats is critical for processive transcription elongation. Mol Cell. 21(2):227–237. doi: 10.1016/j.molcel.2005.11.024.
  • Yamaguchi Y, Takagi T, Wada T, Yano K, Furuya A, Sugimoto S, Hasegawa J, Handa H. 1999. NELF, a multisubunit complex containing RD, cooperates with DSIF to repress RNA polymerase II elongation. Cell. 97(1):41–51. doi: 10.1016/s0092-8674(00)80713-8.
  • Yang Z, Yik JH, Chen R, He N, Jang MK, Ozato K, Zhou Q. 2005. Recruitment of P-TEFb for stimulation of transcriptional elongation by the bromodomain protein Brd4. Mol Cell. 19(4):535–545. doi: 10.1016/j.molcel.2005.06.029.
  • Yang Z, Zhu Q, Luo K, Zhou Q. 2001. The 7SK small nuclear RNA inhibits the CDK9/cyclin T1 kinase to control transcription. Nature. 414(6861):317–322. doi: 10.1038/35104575.
  • Yik JH, Chen R, Nishimura R, Jennings JL, Link AJ, Zhou Q. 2003. Inhibition of P-TEFb (CDK9/Cyclin T) kinase and RNA polymerase II transcription by the coordinated actions of HEXIM1 and 7SK snRNA. Mol Cell. 12(4):971–982. doi: 10.1016/s1097-2765(03)00388-5.
  • Yuan W, Xu M, Huang C, Liu N, Chen S, Zhu B. 2011. H3K36 methylation antagonizes PRC2-mediated H3K27 methylation. J Biol Chem. 286(10):7983–7989. doi: 10.1074/jbc.M110.194027.
  • Zhang G, Campbell EA, Minakhin L, Richter C, Severinov K, Darst SA. 1999. Crystal structure of Thermus aquaticus core RNA polymerase at 3.3 A resolution. Cell. 98(6):811–824. doi: 10.1016/s0092-8674(00)81515-9.
  • Zhang M, Wang XJ, Chen X, Bowman ME, Luo Y, Noel JP, Ellington AD, Etzkorn FA, Zhang Y. 2012. Structural and kinetic analysis of prolyl-isomerization/phosphorylation cross-talk in the CTD code. ACS Chem Biol. 7(8):1462–1470. doi: 10.1021/cb3000887.
  • Zhang W, Prakash C, Sum C, Gong Y, Li Y, Kwok JJT, Thiessen N, Pettersson S, Jones SJM, Knapp S, et al. 2012. Bromodomain-containing protein 4 (BRD4) regulates RNA polymerase II serine 2 phosphorylation in human CD4+ T cells. J Biol Chem. 287(51):43137–43155. doi: 10.1074/jbc.M112.413047.
  • Zheng B, Gold S, Iwanaszko M, Howard BC, Wang L, Shilatifard A. 2023. Distinct layers of BRD4-PTEFb reveal bromodomain-independent function in transcriptional regulation. Mol Cell. 83(16):2896–2910 e2894. doi: 10.1016/j.molcel.2023.06.032.

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