Native elongating transcript sequencing reveals global anti-correlation between sense and antisense nascent transcription in fission yeast

Maxime Wery, Camille Gautier, Marc Descrimes, Mayuko Yoda, Hervé Vennin-Rendos, Valérie Migeot, Daniel Gautheret, Damien Hermand, Antonin Morillon

Résultats de recherche: Contribution à un journal/une revueArticle

Résumé

Antisense transcription can regulate sense gene expression. However, previous annotations of antisense transcription units have been based on detection of mature antisense long noncoding (aslnc)RNAs by RNA-seq and/or microarrays, only giving a partial view of the antisense transcription landscape and incomplete molecular bases for antisense-mediated regulation. Here, we used native elongating transcript sequencing to map genome-wide nascent antisense transcription in fission yeast. Strikingly, antisense transcription was detected for most protein-coding genes, correlating with low sense transcription, especially when overlapping the mRNA start site. RNA profiling revealed that the resulting aslncRNAs mainly correspond to cryptic Xrn1/Exo2-sensitive transcripts (XUTs). ChIP-seq analyses showed that antisense (as)XUT's expression is associated with specific histone modification patterns. Finally, we showed that asXUTs are controlled by the histone chaperone Spt6 and respond to meiosis induction, in both cases anti-correlating with levels of the paired-sense mRNAs, supporting physiological significance to antisense-mediated gene attenuation. Our work highlights that antisense transcription is much more extended than anticipated and might constitute an additional nonpromoter determinant of gene regulation complexity.

langue originaleAnglais
Pages (de - à)196-208
Nombre de pages13
journalRNA
Volume24
Numéro de publication2
Les DOIs
étatPublié - 1 févr. 2018

Empreinte digitale

Schizosaccharomyces
Histone Code
Histone Chaperones
Long Noncoding RNA
RNA
Messenger RNA
Meiosis
Genes
Genome
Gene Expression
Proteins

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Wery, Maxime ; Gautier, Camille ; Descrimes, Marc ; Yoda, Mayuko ; Vennin-Rendos, Hervé ; Migeot, Valérie ; Gautheret, Daniel ; Hermand, Damien ; Morillon, Antonin. / Native elongating transcript sequencing reveals global anti-correlation between sense and antisense nascent transcription in fission yeast. Dans: RNA. 2018 ; Vol 24, Numéro 2. p. 196-208.
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title = "Native elongating transcript sequencing reveals global anti-correlation between sense and antisense nascent transcription in fission yeast",
abstract = "Antisense transcription can regulate sense gene expression. However, previous annotations of antisense transcription units have been based on detection of mature antisense long noncoding (aslnc)RNAs by RNA-seq and/or microarrays, only giving a partial view of the antisense transcription landscape and incomplete molecular bases for antisense-mediated regulation. Here, we used native elongating transcript sequencing to map genome-wide nascent antisense transcription in fission yeast. Strikingly, antisense transcription was detected for most protein-coding genes, correlating with low sense transcription, especially when overlapping the mRNA start site. RNA profiling revealed that the resulting aslncRNAs mainly correspond to cryptic Xrn1/Exo2-sensitive transcripts (XUTs). ChIP-seq analyses showed that antisense (as)XUT's expression is associated with specific histone modification patterns. Finally, we showed that asXUTs are controlled by the histone chaperone Spt6 and respond to meiosis induction, in both cases anti-correlating with levels of the paired-sense mRNAs, supporting physiological significance to antisense-mediated gene attenuation. Our work highlights that antisense transcription is much more extended than anticipated and might constitute an additional nonpromoter determinant of gene regulation complexity.",
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Native elongating transcript sequencing reveals global anti-correlation between sense and antisense nascent transcription in fission yeast. / Wery, Maxime; Gautier, Camille; Descrimes, Marc; Yoda, Mayuko; Vennin-Rendos, Hervé; Migeot, Valérie; Gautheret, Daniel; Hermand, Damien; Morillon, Antonin.

Dans: RNA, Vol 24, Numéro 2, 01.02.2018, p. 196-208.

Résultats de recherche: Contribution à un journal/une revueArticle

TY - JOUR

T1 - Native elongating transcript sequencing reveals global anti-correlation between sense and antisense nascent transcription in fission yeast

AU - Wery, Maxime

AU - Gautier, Camille

AU - Descrimes, Marc

AU - Yoda, Mayuko

AU - Vennin-Rendos, Hervé

AU - Migeot, Valérie

AU - Gautheret, Daniel

AU - Hermand, Damien

AU - Morillon, Antonin

N1 - © 2018 Wery et al.; Published by Cold Spring Harbor Laboratory Press for the RNA Society.

PY - 2018/2/1

Y1 - 2018/2/1

N2 - Antisense transcription can regulate sense gene expression. However, previous annotations of antisense transcription units have been based on detection of mature antisense long noncoding (aslnc)RNAs by RNA-seq and/or microarrays, only giving a partial view of the antisense transcription landscape and incomplete molecular bases for antisense-mediated regulation. Here, we used native elongating transcript sequencing to map genome-wide nascent antisense transcription in fission yeast. Strikingly, antisense transcription was detected for most protein-coding genes, correlating with low sense transcription, especially when overlapping the mRNA start site. RNA profiling revealed that the resulting aslncRNAs mainly correspond to cryptic Xrn1/Exo2-sensitive transcripts (XUTs). ChIP-seq analyses showed that antisense (as)XUT's expression is associated with specific histone modification patterns. Finally, we showed that asXUTs are controlled by the histone chaperone Spt6 and respond to meiosis induction, in both cases anti-correlating with levels of the paired-sense mRNAs, supporting physiological significance to antisense-mediated gene attenuation. Our work highlights that antisense transcription is much more extended than anticipated and might constitute an additional nonpromoter determinant of gene regulation complexity.

AB - Antisense transcription can regulate sense gene expression. However, previous annotations of antisense transcription units have been based on detection of mature antisense long noncoding (aslnc)RNAs by RNA-seq and/or microarrays, only giving a partial view of the antisense transcription landscape and incomplete molecular bases for antisense-mediated regulation. Here, we used native elongating transcript sequencing to map genome-wide nascent antisense transcription in fission yeast. Strikingly, antisense transcription was detected for most protein-coding genes, correlating with low sense transcription, especially when overlapping the mRNA start site. RNA profiling revealed that the resulting aslncRNAs mainly correspond to cryptic Xrn1/Exo2-sensitive transcripts (XUTs). ChIP-seq analyses showed that antisense (as)XUT's expression is associated with specific histone modification patterns. Finally, we showed that asXUTs are controlled by the histone chaperone Spt6 and respond to meiosis induction, in both cases anti-correlating with levels of the paired-sense mRNAs, supporting physiological significance to antisense-mediated gene attenuation. Our work highlights that antisense transcription is much more extended than anticipated and might constitute an additional nonpromoter determinant of gene regulation complexity.

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KW - Histone Chaperones/metabolism

KW - Histone Code

KW - Meiosis/genetics

KW - Peptide Chain Elongation, Translational

KW - RNA Interference

KW - RNA Stability

KW - RNA, Antisense/biosynthesis

KW - Schizosaccharomyces pombe Proteins/metabolism

KW - Schizosaccharomyces/genetics

KW - Sequence Analysis, RNA

KW - Transcription, Genetic

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DO - 10.1261/rna.063446.117

M3 - Article

C2 - 29114019

VL - 24

SP - 196

EP - 208

JO - RNA

JF - RNA

SN - 1355-8382

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