Transcription Factor IID Parks and Drives Preinitiation Complexes at Sharp or Broad Promoters

Overview

Journal Trends Biochem Sci

Specialty Biochemistry

Date 2023 Aug 13

PMID 37574371

Authors

Andrea Bernardini

Camille Hollinger

Damaris Willgenss

Ferenc Muller

Didier Devys

Laszlo Tora

Affiliations

Soon will be listed here.

Abstract

Core promoters are sites where transcriptional regulatory inputs of a gene are integrated to direct the assembly of the preinitiation complex (PIC) and RNA polymerase II (Pol II) transcription output. Until now, core promoter functions have been investigated by distinct methods, including Pol II transcription initiation site mappings and structural characterization of PICs on distinct promoters. Here, we bring together these previously unconnected observations and hypothesize how, on metazoan TATA promoters, the precisely structured building up of transcription factor (TF) IID-based PICs results in sharp transcription start site (TSS) selection; or, in contrast, how the less strictly controlled positioning of the TATA-less promoter DNA relative to TFIID-core PIC components results in alternative broad TSS selections by Pol II.

Citing Articles

Full-length mRNA sequencing resolves novel variation in 5' UTR length for genes expressed during human CD4 T-cell activation.

Woolley C, Chariker J, Rouchka E, Ford E, Hudson E, Rasche K Immunogenetics. 2025; 77(1):14.

PMID: 39904916 PMC: 11794378. DOI: 10.1007/s00251-025-01371-1.

RNA polymerase II transcription initiation in holo-TFIID-depleted mouse embryonic stem cells.

Hisler V, Bardot P, Detilleux D, Bernardini A, Stierle M, Sanchez E Cell Rep. 2024; 43(10):114791.

PMID: 39352809 PMC: 11551524. DOI: 10.1016/j.celrep.2024.114791.

Rice Promoter Editing: An Efficient Genetic Improvement Strategy.

Wu B, Luo H, Chen Z, Amin B, Yang M, Li Z Rice (N Y). 2024; 17(1):55.

PMID: 39212859 PMC: 11364747. DOI: 10.1186/s12284-024-00735-7.

Tata-box-binding protein-associated factor 15 as a new potential marker in gastrointestinal tumors.

Elpek G World J Gastroenterol. 2024; 30(28):3367-3372.

PMID: 39091718 PMC: 11290397. DOI: 10.3748/wjg.v30.i28.3367.

Mechanisms and Functions of the RNA Polymerase II General Transcription Machinery during the Transcription Cycle.

Archuleta S, Goodrich J, Kugel J Biomolecules. 2024; 14(2).

PMID: 38397413 PMC: 10886972. DOI: 10.3390/biom14020176.

References

Chen X, Xu Y . Structural insights into assembly of transcription preinitiation complex. Curr Opin Struct Biol. 2022; 75:102404. DOI: 10.1016/j.sbi.2022.102404. View

Luse D, Parida M, Spector B, Nilson K, Price D . A unified view of the sequence and functional organization of the human RNA polymerase II promoter. Nucleic Acids Res. 2020; 48(14):7767-7785. PMC: 7641323. DOI: 10.1093/nar/gkaa531. View

Lenhard B, Sandelin A, Carninci P . Metazoan promoters: emerging characteristics and insights into transcriptional regulation. Nat Rev Genet. 2012; 13(4):233-45. DOI: 10.1038/nrg3163. View

Patel A, Greber B, Nogales E . Recent insights into the structure of TFIID, its assembly, and its binding to core promoter. Curr Opin Struct Biol. 2019; 61:17-24. PMC: 7156316. DOI: 10.1016/j.sbi.2019.10.001. View

Chou S, Alexander A, Rice E, Choate L, Danko C . Genetic dissection of the RNA polymerase II transcription cycle. Elife. 2022; 11. PMC: 9286732. DOI: 10.7554/eLife.78458. View

Brand M, Leurent C, Mallouh V, Tora L, Schultz P . Three-dimensional structures of the TAFII-containing complexes TFIID and TFTC. Science. 1999; 286(5447):2151-3. DOI: 10.1126/science.286.5447.2151. View

FitzGerald P, Shlyakhtenko A, Mir A, Vinson C . Clustering of DNA sequences in human promoters. Genome Res. 2004; 14(8):1562-74. PMC: 509265. DOI: 10.1101/gr.1953904. View

Cianfrocco M, Kassavetis G, Grob P, Fang J, Juven-Gershon T, Kadonaga J . Human TFIID binds to core promoter DNA in a reorganized structural state. Cell. 2013; 152(1-2):120-31. PMC: 3552382. DOI: 10.1016/j.cell.2012.12.005. View

Schug J, Schuller W, Kappen C, Salbaum J, Bucan M, Stoeckert Jr C . Promoter features related to tissue specificity as measured by Shannon entropy. Genome Biol. 2005; 6(4):R33. PMC: 1088961. DOI: 10.1186/gb-2005-6-4-r33. View

10.

Abril-Garrido J, Dienemann C, Grabbe F, Velychko T, Lidschreiber M, Wang H . Structural basis of transcription reduction by a promoter-proximal +1 nucleosome. Mol Cell. 2023; 83(11):1798-1809.e7. PMC: 10237034. DOI: 10.1016/j.molcel.2023.04.011. View

11.

Weil P, Luse D, Segall J, Roeder R . Selective and accurate initiation of transcription at the Ad2 major late promotor in a soluble system dependent on purified RNA polymerase II and DNA. Cell. 1979; 18(2):469-84. DOI: 10.1016/0092-8674(79)90065-5. View

12.

Haberle V, Stark A . Eukaryotic core promoters and the functional basis of transcription initiation. Nat Rev Mol Cell Biol. 2018; 19(10):621-637. PMC: 6205604. DOI: 10.1038/s41580-018-0028-8. View

13.

Muller F, Demeny M, Tora L . New problems in RNA polymerase II transcription initiation: matching the diversity of core promoters with a variety of promoter recognition factors. J Biol Chem. 2007; 282(20):14685-9. DOI: 10.1074/jbc.R700012200. View

14.

Aibara S, Schilbach S, Cramer P . Structures of mammalian RNA polymerase II pre-initiation complexes. Nature. 2021; 594(7861):124-128. DOI: 10.1038/s41586-021-03554-8. View

15.

Vo Ngoc L, Huang C, Cassidy C, Medrano C, Kadonaga J . Identification of the human DPR core promoter element using machine learning. Nature. 2020; 585(7825):459-463. PMC: 7501168. DOI: 10.1038/s41586-020-2689-7. View

16.

Louder R, He Y, Lopez-Blanco J, Fang J, Chacon P, Nogales E . Structure of promoter-bound TFIID and model of human pre-initiation complex assembly. Nature. 2016; 531(7596):604-9. PMC: 4856295. DOI: 10.1038/nature17394. View

17.

Warfield L, Ramachandran S, Baptista T, Devys D, Tora L, Hahn S . Transcription of Nearly All Yeast RNA Polymerase II-Transcribed Genes Is Dependent on Transcription Factor TFIID. Mol Cell. 2017; 68(1):118-129.e5. PMC: 5679267. DOI: 10.1016/j.molcel.2017.08.014. View

18.

Bhuiyan T, Timmers H . Promoter Recognition: Putting TFIID on the Spot. Trends Cell Biol. 2019; 29(9):752-763. DOI: 10.1016/j.tcb.2019.06.004. View

19.

Chen X, Yin X, Li J, Wu Z, Qi Y, Wang X . Structures of the human Mediator and Mediator-bound preinitiation complex. Science. 2021; 372(6546). DOI: 10.1126/science.abg0635. View

20.

Chen X, Qi Y, Wu Z, Wang X, Li J, Zhao D . Structural insights into preinitiation complex assembly on core promoters. Science. 2021; 372(6541). DOI: 10.1126/science.aba8490. View