Deregulated Expression of Mammalian lncRNA through Loss of SPT6 Induces R-Loop Formation, Replication Stress, and Cellular Senescence

Mol Cell. 2018 Dec 20;72(6):970-984.e7. doi: 10.1016/j.molcel.2018.10.011. Epub 2018 Nov 15.

Abstract

Extensive tracts of the mammalian genome that lack protein-coding function are still transcribed into long noncoding RNA. While these lncRNAs are generally short lived, length restricted, and non-polyadenylated, how their expression is distinguished from protein-coding genes remains enigmatic. Surprisingly, depletion of the ubiquitous Pol-II-associated transcription elongation factor SPT6 promotes a redistribution of H3K36me3 histone marks from active protein coding to lncRNA genes, which correlates with increased lncRNA transcription. SPT6 knockdown also impairs the recruitment of the Integrator complex to chromatin, which results in a transcriptional termination defect for lncRNA genes. This leads to the formation of extended, polyadenylated lncRNAs that are both chromatin restricted and form increased levels of RNA:DNA hybrid (R-loops) that are associated with DNA damage. Additionally, these deregulated lncRNAs overlap with DNA replication origins leading to localized DNA replication stress and a cellular senescence phenotype. Overall, our results underline the importance of restricting lncRNA expression.

Keywords: DNA replication stress; H3K36me3; R-loop; SPT6; cellular senescence; eRNA; integrator complex; long non-coding RNA; mNET-seq; mNuc-seq.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Proliferation*
  • Cellular Senescence*
  • Chromatin Assembly and Disassembly
  • DNA Damage*
  • DNA Polymerase II / genetics
  • DNA Polymerase II / metabolism
  • DNA Replication*
  • DNA, Neoplasm / biosynthesis*
  • DNA, Neoplasm / genetics
  • Drosophila melanogaster / genetics
  • Drosophila melanogaster / metabolism
  • Female
  • Gene Expression Regulation, Neoplastic
  • HeLa Cells
  • Histones / metabolism
  • Humans
  • Methylation
  • Nucleic Acid Conformation
  • Nucleic Acid Heteroduplexes / genetics
  • Nucleic Acid Heteroduplexes / metabolism
  • RNA Stability
  • RNA, Long Noncoding / genetics
  • RNA, Long Noncoding / metabolism*
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • RNA, Neoplasm / genetics
  • RNA, Neoplasm / metabolism*
  • Transcription Factors / genetics
  • Transcription Factors / metabolism*
  • Transcription, Genetic
  • Uterine Neoplasms / genetics
  • Uterine Neoplasms / metabolism*

Substances

  • DNA, Neoplasm
  • Histones
  • Nucleic Acid Heteroduplexes
  • RNA, Long Noncoding
  • RNA, Messenger
  • RNA, Neoplasm
  • SUPT6H protein, human
  • Transcription Factors
  • DNA Polymerase II