Transcription elongation rate affects nascent histone pre-mRNA folding and 3' end processing

Genes & Development
Tassa SaldiDavid L Bentley

Abstract

Transcription elongation rate influences cotranscriptional pre-mRNA maturation, but how such kinetic coupling works is poorly understood. The formation of nonadenylated histone mRNA 3' ends requires recognition of an RNA structure by stem-loop-binding protein (SLBP). We report that slow transcription by mutant RNA polymerase II (Pol II) caused accumulation of polyadenylated histone mRNAs that extend past the stem-loop processing site. UV irradiation, which decelerates Pol II elongation, also induced long poly(A)+ histone transcripts. Inhibition of 3' processing by slow Pol II correlates with failure to recruit SLBP to histone genes. Chemical probing of nascent RNA structure showed that the stem-loop fails to fold in transcripts made by slow Pol II, thereby explaining the absence of SLBP and failure to process 3' ends. These results show that regulation of transcription speed can modulate pre-mRNA processing by changing nascent RNA structure and suggest a mechanism by which alternative processing could be controlled.

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Citations

Jul 29, 2018·Nature Reviews. Genetics·Eric J StrobelJulius B Lucks
Oct 12, 2018·FASEB Journal : Official Publication of the Federation of American Societies for Experimental Biology·Incheol RyuYoon Ki Kim
Apr 17, 2019·The EMBO Journal·Magdalena M MaslonJavier F Cáceres
Dec 11, 2019·Nucleic Acids Research·Katarzyna BucholcZbigniew Dominski
May 7, 2020·Nucleic Acids Research·Nicolás Nieto MorenoAlberto R Kornblihtt
Jul 14, 2020·Wiley Interdisciplinary Reviews. RNA·Rebekah Eleazer, Yvonne N Fondufe-Mittendorf
Jun 5, 2020·Cold Spring Harbor Symposia on Quantitative Biology·Tucker J Carrocci, Karla M Neugebauer
Aug 3, 2019·Cold Spring Harbor Perspectives in Biology·Karla M Neugebauer
Sep 28, 2018·The Journal of Cell Biology·Shweta MendirattaGenevieve Almouzni
May 6, 2020·Nature Structural & Molecular Biology·Pavla GajduškováDalibor Blazek
Sep 10, 2020·International Journal of Molecular Sciences·Jung-Im WonDong-Hoon Jeong
Apr 3, 2019·Nature Structural & Molecular Biology·Angela M Yu, Julius B Lucks
Oct 22, 2020·Current Protocols in Molecular Biology·Kirsten A Reimer, Karla M Neugebauer
Jun 26, 2020·Molecular Cell·Tomasz W TurowskiDavid Tollervey
Nov 26, 2019·Cell·Margaret L Rodgers, Sarah A Woodson
Mar 4, 2021·Trends in Biochemical Sciences·Martin DutertreStéphan Vagner
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Jul 25, 2021·DNA Repair·Daisy Castillo-Guzman, Frédéric Chédin
Aug 21, 2021·Seminars in Cancer Biology·Beatrix R Bradford, Chunyuan Jin

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