Differential effects of SUMO1 and SUMO2 on circadian protein PER2 stability and function

Sci Rep. 2021 Jul 13;11(1):14431. doi: 10.1038/s41598-021-93933-y.

Abstract

Posttranslational modification (PTM) of core circadian clock proteins, including Period2 (PER2), is required for proper circadian regulation. PER2 function is regulated by casein kinase 1 (CK1)-mediated phosphorylation and ubiquitination but little is known about other PER2 PTMs or their interaction with PER2 phosphorylation. We found that PER2 can be SUMOylated by both SUMO1 and SUMO2; however, SUMO1 versus SUMO2 conjugation had different effects on PER2 turnover and transcriptional suppressor function. SUMO2 conjugation facilitated PER2 interaction with β-TrCP leading to PER2 proteasomal degradation. In contrast, SUMO1 conjugation, mediated by E3 SUMO-protein ligase RanBP2, enhanced CK1-mediated PER2S662 phosphorylation, inhibited PER2 degradation and increased PER2 transcriptional suppressor function. PER2 K736 was critical for both SUMO1- and SUMO2-conjugation. A PER2K736R mutation was sufficient to alter PER2 protein oscillation and reduce PER2-mediated transcriptional suppression. Together, our data revealed that SUMO1 versus SUMO2 conjugation acts as a determinant of PER2 stability and function and thereby affects the circadian regulatory system and the expression of clock-controlled genes.

MeSH terms

  • Animals
  • Circadian Rhythm / genetics
  • HEK293 Cells
  • Humans
  • Molecular Chaperones
  • Nuclear Pore Complex Proteins
  • Period Circadian Proteins* / genetics
  • Period Circadian Proteins* / metabolism
  • Phosphorylation
  • Protein Processing, Post-Translational
  • Protein Stability*
  • SUMO-1 Protein* / genetics
  • SUMO-1 Protein* / metabolism
  • Small Ubiquitin-Related Modifier Proteins / genetics
  • Small Ubiquitin-Related Modifier Proteins / metabolism
  • Sumoylation

Substances

  • Period Circadian Proteins
  • SUMO-1 Protein
  • PER2 protein, human
  • Small Ubiquitin-Related Modifier Proteins
  • SUMO2 protein, human
  • ran-binding protein 2
  • SUMO1 protein, human
  • Molecular Chaperones
  • Nuclear Pore Complex Proteins