Antisense transcription-dependent chromatin signature modulates sense transcript dynamics

Thomas Brown, Françoise S. Howe, Struan C. Murray, Meredith Wouters, Philipp Lorenz, Emily Seward, Scott Rata, Andrew Angel* (Corresponding Author), Jane Mellor* (Corresponding Author)

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

35 Citations (Scopus)

Abstract

Antisense transcription is widespread in genomes. Despite large differences in gene size and architecture, we find that yeast and human genes share a unique, antisense transcription-associated chromatin signature. We asked whether this signature is related to a biological function for antisense transcription. Using quantitative RNA-FISH, we observed changes in sense transcript distributions in nuclei and cytoplasm as antisense transcript levels were altered. To determine the mechanistic differences underlying these distributions, we developed a mathematical framework describing transcription from initiation to transcript degradation. At GAL1, high levels of antisense transcription alter sense transcription dynamics, reducing rates of transcript production and processing, while increasing transcript stability. This relationship with transcript stability is also observed as a genome-wide association. Establishing the antisense transcription-associated chromatin signature through disruption of the Set3C histone deacetylase activity is sufficient to similarly change these rates even in the absence of antisense transcription. Thus, antisense transcription alters sense transcription dynamics in a chromatin-dependent manner.

Original languageEnglish
Article numbere8007
Number of pages21
JournalMolecular Systems Biology
Volume14
Issue number2
Early online date12 Feb 2018
DOIs
Publication statusPublished - Feb 2018
Externally publishedYes

Data Availability Statement

Images for RNA‐FISH experiments, computer codes and all source data are available from Mendeley https://doi.org/10.17632/dhnvj4xs5d.1. Computer code is provided as Computer Code EV1.

Funding

We thank the J.M. and A.A. laboratories for critical discussions, Anitha Nair for excellent technical support, Simon Haenni for 5′ and 3′ RACE mapping of the transcripts, and Ilan Davis and Micron Oxford for microscopy support. This work was supported by: The Wellcome Trust (WT089156MA to J.M.); the BBSRC (BB/P00296X/1 to J.M.); the Leverhulme Trust (RPG-2016-405 to J.M.); a Wellcome Trust Strategic Award (091911) supporting advanced microscopy at Micron Oxford (http://micronoxford.com); EPSRC and BBSRC studentships (EP/F500394/1 to T.B.; EP/G03706X/1 to S.R.; BB/J014427/1 to E.S.; BB/ M011224/1 to P.L.) and a Royal Society University Research Fellowship (UF120327 to A.A.).

FundersFunder number
Wellcome TrustWT089156MA
Engineering and Physical Sciences Research CouncilEP/F500394/1, EP/G03706X/1
BBSRCBB/J014427/1, BB/M011224/1, BB/P00296X/1
The Leverhulme Trust091911, RPG-2016-405
Royal Historical SocietyUF120327

    Keywords

    • antisense transcription
    • chromatin
    • sense transcript dynamics
    • Set3C lysine deacetylase
    • stochastic model

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