中文

Chinese Journal of Nature >

2023 , Vol. 45 >Issue 2: 79 - 88

DOI: https://doi.org/10.3969/j.issn.0253-9608.2023.02.001

Invited Special Paper

Assembly and promoter recognition mechanisms of pretranscriptional initiation complexes

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  • Fudan University Shanghai Cancer Center/Institutes of Biomedical Sciences, Shanghai Medical College of Fudan University, Shanghai 200032, China

Received date: 2022-12-19

  Online published: 2023-03-29

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Abstract

As the key step of the genetic central dogma, transcription generates RNA using DNA as template to control differential gene expression. The transcription initiation occurs in highly diverse promoter regions of tens of thousands of different genes. The preinitiation complex (PIC) assembly on core promoter is a key step of eukaryotic transcription initiation and requires precise regulation. Previous structural studies focused on PIC assembled on TATA box promoters with TFIID replaced by its subunit, TATA box-binding protein (TBP). However, the TFIID complex is essential for PIC assembly for almost all Pol II-mediated transcription, especially on the TATA-less promoters, which account for more than 85% of core promoters of human coding genes. The functions of TFIID could not be replaced by TBP. The recent breakthrough in structure determination of TFIID-based PIC complexes in different assembly stages and in complex of the +1 nucleosome revealed mechanistic insights into PIC assembly on core promotes and in the context of chromatin, providing a framework for further investigation of transcription initiation.

Cite this article

CHEN Xizi, XU Yanhui . Assembly and promoter recognition mechanisms of pretranscriptional initiation complexes[J]. Chinese Journal of Nature, 2023 , 45(2) : 79 -88 . DOI: 10.3969/j.issn.0253-9608.2023.02.001

References

[1] ROEDER R G, RUTTER W J. Multiple forms of DNA-dependent RNA polymerase in eukaryotic organisms [J]. Nature, 1969,
224(5216): 234-237.
[2] ROEDER R G, RUTTER W J. Specific nucleolar and nucleoplasmic RNA polymerases [J]. Proc Natl Acad Sci USA, 1970, 65(3): 675-682.
[3] ZYLBER E A, PENMAN S. Products of RNA polymerases in HeLa cell nuclei [J]. Proc Natl Acad Sci USA, 1971, 68(11): 2861-2865.

[4] WEIL P A, BLATTI S P. HeLa cell deoxyribonucleic acid dependent RNA polymerases: function and properties of the class III enzymes [J]. Biochemistry, 1976, 15(7): 1500-1509.
[5] JUVEN-GERSHON T, KADONAGA J T. Regulation of gene expression via the core promoter and the basal transcriptional
machinery [J]. Dev Biol, 2010, 339(2): 225-229.
[6] VO NGOC L, WANG Y L, KASSAVETIS G A, et al. The punctilious RNA polymerase II core promoter [J]. Genes Dev, 2017,
31(13): 1289-1301.
[7] SANDELIN A, CARNINCI P, LENHARD B, et al. Mammalian RNA polymerase II core promoters: insights from genome-wide
studies [J]. Nat Rev Genet, 2007, 8(6): 424-436.
[8] VO NGOC L, HUANG C Y, CASSIDY C J, et al. Identification of the human DPR core promoter element using machine learning [J]. Nature, 2020, 585(7825): 459-463.
[9] THOMAS M C, CHIANG C M. The general transcription machinery and general cofactors [J]. Crit Rev Biochem Mol Biol,
2006, 41(3): 105-178.
[10] BURATOWSKI S, HAHN S, GUARENTE L, et al. Five intermediate complexes in transcription initiation by RNA polymerase II [J]. Cell, 1989, 56(4): 549-561.
[11] VAN DYKE M W, ROEDER R G, SAWADOGO M. Physical analysis of transcription preinitiation complex assembly on a class II
gene promoter [J]. Science, 1988, 241(4871): 1335-1338.
[12] ZAWEL L, REINBERG D. Initiation of transcription by RNA polymerase II: a multi-step process [J]. Prog Nucleic Acid Res Mol
Biol, 1993, 44: 67-108.
[13] CHEN X, QI Y, WU Z, et al. Structural insights into preinitiation complex assembly on core promoters [J]. Science, 2021, 372(6541): eaba8490.
[14] BAEK I, FRIEDMAN L J, GELLES J, et al. Single-molecule studies reveal branched pathways for activator-dependent assembly
of RNA polymerase II pre-initiation complexes [J]. Mol Cell, 2021, 81(17): 3576-3588.e6.
[15] NGUYEN V Q, RANJAN A, LIU S, et al. Spatiotemporal coordination of transcription preinitiation complex assembly in live
cells [J]. Mol Cell, 2021, 81(17): 3560-3575.e6.
[16] ZHANG Z, ENGLISH B P, GRIMM J B, et al. Rapid dynamics of general transcription factor TFIIB binding during preinitiation
complex assembly revealed by single-molecule analysis [J]. Genes Dev, 2016, 30(18): 2106-2118.
[17] SVEJSTRUP J Q, WANG Z, FEAVE W J, et al. Different forms of TFIIH for transcription and DNA repair: holo-TFIIH and a
nucleotide excision repairosome [J]. Cell, 1995, 80(1): 21-28.
[18] SOUTOURINA J. Transcription regulation by the Mediator complex [J]. Nat Rev Mol Cell Biol, 2018, 19(4): 262-274.
[19] PETERSON M G, TANESE N, PUGH B F, et al. Functional domains and upstream activation properties of cloned human TATA
binding protein [J]. Science, 1990, 248(4963): 1625-1630.
[20] VERRIJZER C P, CHEN J-L, YOKOMORI K, et al. Binding of TAFs to core elements directs promoter selectivity by RNA polymerase II [J]. Cell, 1995, 81(7): 1115-1125.
[21] NOGALES E, LOUDER R K, HE Y. Structural insights into the eukaryotic transcription initiation machinery [J]. Annu Rev Biophys, 2017, 46: 59-83.
[22] DONCZEW R, HAHN S. Mechanistic differences in transcription initiation at TATA-less and TATA-containing promoters [J]. Mol
Cell Biol, 2018, 38(1): e00448-17.
[23] DONCZEW R, WARFIELD L, PACHECO D, et al. Two roles for the yeast transcription coactivator SAGA and a set of genes redundantly regulated by TFIID and SAGA [J]. eLife, 2020, 9: e50109.
[24] TAATJES D J. The continuing SAGA of TFIID and RNA polymerase II transcription [J]. Mol Cell, 2017, 68(1): 1-2.
[25] NIKOLOV D B, CHEN H, HALAY E D, et al. Crystal structure of a TFIIB-TBP-TATA-element ternary complex [J]. Nature, 1995,
377(6545): 119-128.
[26] ZHAO X, HERR W. A regulated two-step mechanism of TBP binding to DNA: a solvent-exposed surface of TBP inhibits TATA
box recognition [J]. Cell, 2002, 108(5): 615-627.
[27] PATEL A B, LOUDER R K, GREBER B J, et al. Structure of human TFIID and mechanism of TBP loading onto promoter DNA [J].
Science, 2018, 362(6421): aau8872.
[28] LOUDER R K, HE Y, LÓPEZ-BLANCO J R, et al. Structure of promoter-bound TFIID and model of human pre-initiation complex
assembly [J]. Nature, 2016, 531(7596): 604-609.
[29] CIANFROCCO M A, KASSAVETIS G A, GROB P, et al. Human TFIID binds to core promoter DNA in a reorganized structural state [J]. Cell, 2013, 152(1/2): 120-131.
[30] KOLESNIKOVA O, BEN-SHEM A, LUO J, et al. Molecular structure of promoter-bound yeast TFIID [J]. Nat Commun, 2018,
9(1): 4666.
[31] JUVEN-GERSHON T, CHENG S, KADONAGA J T. Rational design of a super core promoter that enhances gene expression [J].
Nat Methods, 2006, 3(11): 917-922.
[32] LIU X, BUSHNELL D A, WANG D, et al. Structure of an RNA polymerase II-TFIIB complex and the transcription initiation
mechanism [J]. Science, 2010, 327(5962): 206-209.
[33] KOSTREWA D, ZELLER M E, ARMACHE K-J, et al. RNA polymerase II-TFIIB structure and mechanism of transcription initiation [J]. Nature, 2009, 462(7271): 323-330.
[34] ROBINSON P J, TRNKA M J, BUSHNELL D A, et al. Structure of a complete Mediator-RNA polymerase II pre-initiation complex [J]. Cell, 2016, 166(6): 1411-1422. e16.
[35] PLASCHKA C, HANTSCHE M, DIENEMANN C, et al. Transcription initiation complex structures elucidate DNA opening [J]. Nature, 2016, 533(7603): 353-358.
[36] HE Y, YAN C, FANG J, et al. Near-atomic resolution visualization of human transcription promoter opening [J]. Nature, 2016,
533(7603): 359-365.
[37] PLASCHKA C, LARIVIÈRE L, WENZECK L, et al. Architecture of the RNA polymerase II-Mediator core initiation complex [J].
Nature, 2015, 518(7539): 376-380.
[38] MURAKAMI K, TSAI K-L, KALISMAN N, et al. Structure of an RNA polymerase II preinitiation complex [J]. Proc Natl Acad Sci
USA, 2015, 112(44): 13543-13548.
[39] MURAKAMI K, ELMLUND H, KALISMAN N, et al. Architecture of an RNA polymerase II transcription pre-initiation complex [J].
Science, 2013, 342(6159): 1238724.
[40] HE Y, FANG J, TAATJES D J, et al. Structural visualization of key steps in human transcription initiation [J]. Nature, 2013, 495(7442): 481-486.
[41] SCHILBACH S, AIBARA S, DIENEMANN C, et al. Structure of RNA polymerase II pre-initiation complex at 2.9 Å defines initial
DNA opening [J]. Cell, 2021, 184(15): 4064-4072. e28.
[42] AIBARA S, SCHILBACH S, CRAMER P. Structures of mammalian RNA polymerase II pre-initiation complexes [J]. Nature, 2021,
594(7861): 124-128.
[43] YANG C, FUJIWARA R, KIM H J, et al. Structural visualization of de novo transcription initiation by Saccharomyces cerevisiae RNA polymerase II [J]. Mol Cell, 2022, 82: 660-676. e9.
[44] RENGACHARI S, SCHILBACH S, AIBARA S, et al. Structure of the human Mediator-RNA polymerase II pre-initiation complex [J]. Nature, 2021, 594(7861): 129-133.
[45] ABDELLA R, TALYZINA A, CHEN S, et al. Structure of the human Mediator-bound transcription preinitiation complex [J].
Science, 2021, 372(6537): 52-56.
[46] SCHILBACH S, HANTSCHE M, TEGUNOV D, et al. Structures of transcription pre-initiation complex with TFIIH and Mediator [J]. Nature, 2017, 551(7679): 204-209.
[47] GRUNBERG S, WARFIELD L, HAHN S. Architecture of the RNA polymerase II preinitiation complex and mechanism of ATPdependent promoter opening [J]. Nat Struct Mol Biol, 2012, 19(8): 788-796.
[48] CHEN X, QI Y, WU Z, et al. Structural insights into preinitiation complex assembly on core promoters [J]. Science, 2021, 372(6541): eaba8490.
[49] CHEN X, YIN X, LI J, et al. Structures of the human Mediator and Mediator-bound preinitiation complex [J]. Science, 2021,
372(6546): eabg0635.
[50] HABERLE V, STARK A. Eukaryotic core promoters and the functional basis of transcription initiation [J]. Nat Rev Mol Cell
Biol, 2018, 19(10): 621-637.
[51] WEBER C M, RAMACHANDRAN S, HENIKOFF S. Nucleosomes are context-specific, H2A.Z-modulated barriers to RNA polymerase [J]. Mol Cell, 2014, 53(5): 819-830.
[52] TEVES S S, WEBER C M, HENIKOFF S. Transcribing through the nucleosome [J]. Trends Biochem Sci, 2014, 39(12): 577-586.
[53] LAI W K M, PUGH B F. Understanding nucleosome dynamics and their links to gene expression and DNA replication [J]. Nat Rev Mol Cell Biol, 2017, 18(9): 548-562.
[54] JIANG C, PUGH B F. Nucleosome positioning and gene regulation: advances through genomics [J]. Nat Rev Genet, 2009, 10(3): 161-172.
[55] KORNBERG R D, LORCH Y. Primary role of the nucleosome [J]. Mol Cell, 2020, 79(3): 371-375.
[56] STRUHL K, SEGAL E. Determinants of nucleosome positioning [J]. Nat Struct Mol Biol, 2013, 20(3): 267-273.
[57] JIN C, ZANG C, WEI G, et al. H3.3/H2A.Z double variantcontaining nucleosomes mark ‘nucleosome-free regions’ of active
promoters and other regulatory regions [J]. Nat Genet, 2009, 41(8): 941-945.
[58] RHEE H S, BATAILLE A R, ZHANG L, et al. Subnucleosomal structures and nucleosome asymmetry across a genome [J]. Cell,
2014, 159(6): 1377-1388.
[59] SCHONES D E, CUI K, CUDDAPAH S, et al. Dynamic regulation of nucleosome positioning in the human genome [J]. Cell, 2008, 132(5): 887-898.
[60] MAVRICH T N, JIANG C, IOSHIKHES I P, et al. Nucleosome organization in the Drosophila genome [J]. Nature, 2008, 453(7193): 358-362.
[61] TRAMANTANO M, SUN L, AU C, et al. Constitutive turnover of histone H2A.Z at yeast promoters requires the preinitiation complex [J]. eLife, 2016, 5: e14243.

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