Global SUMOylation on active chromatin is an acute heat stress response restricting transcription

Einari A Niskanen, Marjo Malinen, Päivi Sutinen, Sari Toropainen, Ville Paakinaho, Anniina Vihervaara, Jenny Joutsen, Minna U Kaikkonen, Lea Sistonen, Jorma J Palvimo

Research output: Contribution to journalArticleScientificpeer-review


BACKGROUND: Cells have developed many ways to cope with external stress. One distinctive feature in acute proteotoxic stresses, such as heat shock (HS), is rapid post-translational modification of proteins by SUMOs (small ubiquitin-like modifier proteins; SUMOylation). While many of the SUMO targets are chromatin proteins, there is scarce information on chromatin binding of SUMOylated proteins in HS and the role of chromatin SUMOylation in the regulation of transcription.

RESULTS: We mapped HS-induced genome-wide changes in chromatin occupancy of SUMO-2/3-modified proteins in K562 and VCaP cells using ChIP-seq. Chromatin SUMOylation was further correlated with HS-induced global changes in transcription using GRO-seq and RNA polymerase II (Pol2) ChIP-seq along with ENCODE data for K562 cells. HS induced a rapid and massive rearrangement of chromatin SUMOylation pattern: SUMOylation was gained at active promoters and enhancers associated with multiple transcription factors, including heat shock factor 1. Concomitant loss of SUMOylation occurred at inactive intergenic chromatin regions that were associated with CTCF-cohesin complex and SETDB1 methyltransferase complex. In addition, HS triggered a dynamic chromatin binding of SUMO ligase PIAS1, especially onto promoters. The HS-induced SUMOylation on chromatin was most notable at promoters of transcribed genes where it positively correlated with active transcription and Pol2 promoter-proximal pausing. Furthermore, silencing of SUMOylation machinery either by depletion of UBC9 or PIAS1 enhanced expression of HS-induced genes.

CONCLUSIONS: HS-triggered SUMOylation targets promoters and enhancers of actively transcribed genes where it restricts the transcriptional activity of the HS-induced genes. PIAS1-mediated promoter SUMOylation is likely to regulate Pol2-associated factors in HS.

Original languageEnglish
Pages (from-to)153
Issue number1
Publication statusPublished - 28 Jul 2015
MoE publication typeA1 Journal article-refereed


  • Chromatin/metabolism
  • DNA-Binding Proteins/physiology
  • Gene Expression Regulation
  • Heat Shock Transcription Factors
  • Heat-Shock Response/genetics
  • Humans
  • K562 Cells
  • Promoter Regions, Genetic
  • Protein Inhibitors of Activated STAT/metabolism
  • RNA Polymerase II/metabolism
  • Small Ubiquitin-Related Modifier Proteins/metabolism
  • Sumoylation
  • Transcription Factors/physiology
  • Transcription, Genetic


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