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.