Bases of antisense lncRNA-associated regulation of gene expression in fission yeast

Maxime Wery, Camille Gautier, Marc Descrimes, Mayuko Yoda, Valérie Migeot, Damien Hermand, Antonin Morillon

Research output: Contribution to journalArticle

Abstract

Antisense (as)lncRNAs can regulate gene expression but the underlying mechanisms and the different cofactors involved remain unclear. Using Native Elongating Transcript sequencing, here we show that stabilization of antisense Exo2-sensitivite lncRNAs (XUTs) results in the attenuation, at the nascent transcription level, of a subset of highly expressed genes displaying prominent promoter-proximal nucleosome depletion and histone acetylation. Mechanistic investigations on the catalase gene ctt1 revealed that its induction following oxidative stress is impaired in Exo2-deficient cells, correlating with the accumulation of an asXUT. Interestingly, expression of this asXUT was also activated in wild-type cells upon oxidative stress, concomitant to ctt1 induction, indicating a potential attenuation feedback. This attenuation correlates with asXUT abundance, it is transcriptional, characterized by low RNAPII-ser5 phosphorylation, and it requires an histone deacetylase activity and the conserved Set2 histone methyltransferase. Finally, we identified Dicer as another RNA processing factor acting on ctt1 induction, but independently of Exo2. We propose that asXUTs could modulate the expression of their paired-sense genes when it exceeds a critical threshold, using a conserved mechanism independent of RNAi.

Original languageEnglish
Pages (from-to)e1007465
JournalPLoS Genetics
Volume14
Issue number7
DOIs
Publication statusPublished - Jul 2018
Externally publishedYes

Fingerprint

Long Noncoding RNA
Schizosaccharomyces
Schizosaccharomyces pombe
gene expression regulation
Gene Expression Regulation
gene expression
yeast
histones
gene
Oxidative Stress
oxidative stress
Genes
antisense RNA
Antisense RNA
histone deacetylase
nucleosomes
Histone Deacetylases
genes
Nucleosomes
methyltransferases

Keywords

  • Acetylation
  • Catalase/genetics
  • Endoribonucleases/metabolism
  • Exodeoxyribonucleases/genetics
  • Gene Expression Regulation, Fungal
  • Histone-Lysine N-Methyltransferase/genetics
  • Oxidative Stress/genetics
  • Promoter Regions, Genetic
  • RNA Interference
  • RNA, Antisense/metabolism
  • RNA, Fungal/metabolism
  • RNA, Long Noncoding/metabolism
  • Schizosaccharomyces/genetics
  • Schizosaccharomyces pombe Proteins/genetics
  • Transcription, Genetic/genetics

Cite this

Wery, Maxime ; Gautier, Camille ; Descrimes, Marc ; Yoda, Mayuko ; Migeot, Valérie ; Hermand, Damien ; Morillon, Antonin. / Bases of antisense lncRNA-associated regulation of gene expression in fission yeast. In: PLoS Genetics. 2018 ; Vol. 14, No. 7. pp. e1007465.
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Bases of antisense lncRNA-associated regulation of gene expression in fission yeast. / Wery, Maxime; Gautier, Camille; Descrimes, Marc; Yoda, Mayuko; Migeot, Valérie; Hermand, Damien; Morillon, Antonin.

In: PLoS Genetics, Vol. 14, No. 7, 07.2018, p. e1007465.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Bases of antisense lncRNA-associated regulation of gene expression in fission yeast

AU - Wery, Maxime

AU - Gautier, Camille

AU - Descrimes, Marc

AU - Yoda, Mayuko

AU - Migeot, Valérie

AU - Hermand, Damien

AU - Morillon, Antonin

PY - 2018/7

Y1 - 2018/7

N2 - Antisense (as)lncRNAs can regulate gene expression but the underlying mechanisms and the different cofactors involved remain unclear. Using Native Elongating Transcript sequencing, here we show that stabilization of antisense Exo2-sensitivite lncRNAs (XUTs) results in the attenuation, at the nascent transcription level, of a subset of highly expressed genes displaying prominent promoter-proximal nucleosome depletion and histone acetylation. Mechanistic investigations on the catalase gene ctt1 revealed that its induction following oxidative stress is impaired in Exo2-deficient cells, correlating with the accumulation of an asXUT. Interestingly, expression of this asXUT was also activated in wild-type cells upon oxidative stress, concomitant to ctt1 induction, indicating a potential attenuation feedback. This attenuation correlates with asXUT abundance, it is transcriptional, characterized by low RNAPII-ser5 phosphorylation, and it requires an histone deacetylase activity and the conserved Set2 histone methyltransferase. Finally, we identified Dicer as another RNA processing factor acting on ctt1 induction, but independently of Exo2. We propose that asXUTs could modulate the expression of their paired-sense genes when it exceeds a critical threshold, using a conserved mechanism independent of RNAi.

AB - Antisense (as)lncRNAs can regulate gene expression but the underlying mechanisms and the different cofactors involved remain unclear. Using Native Elongating Transcript sequencing, here we show that stabilization of antisense Exo2-sensitivite lncRNAs (XUTs) results in the attenuation, at the nascent transcription level, of a subset of highly expressed genes displaying prominent promoter-proximal nucleosome depletion and histone acetylation. Mechanistic investigations on the catalase gene ctt1 revealed that its induction following oxidative stress is impaired in Exo2-deficient cells, correlating with the accumulation of an asXUT. Interestingly, expression of this asXUT was also activated in wild-type cells upon oxidative stress, concomitant to ctt1 induction, indicating a potential attenuation feedback. This attenuation correlates with asXUT abundance, it is transcriptional, characterized by low RNAPII-ser5 phosphorylation, and it requires an histone deacetylase activity and the conserved Set2 histone methyltransferase. Finally, we identified Dicer as another RNA processing factor acting on ctt1 induction, but independently of Exo2. We propose that asXUTs could modulate the expression of their paired-sense genes when it exceeds a critical threshold, using a conserved mechanism independent of RNAi.

KW - Acetylation

KW - Catalase/genetics

KW - Endoribonucleases/metabolism

KW - Exodeoxyribonucleases/genetics

KW - Gene Expression Regulation, Fungal

KW - Histone-Lysine N-Methyltransferase/genetics

KW - Oxidative Stress/genetics

KW - Promoter Regions, Genetic

KW - RNA Interference

KW - RNA, Antisense/metabolism

KW - RNA, Fungal/metabolism

KW - RNA, Long Noncoding/metabolism

KW - Schizosaccharomyces/genetics

KW - Schizosaccharomyces pombe Proteins/genetics

KW - Transcription, Genetic/genetics

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DO - 10.1371/journal.pgen.1007465

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VL - 14

SP - e1007465

JO - PLoS Genetics

JF - PLoS Genetics

SN - 1553-7390

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ER -