Complex regulation of orphan nuclear receptor Nur77 (Nr4a1) transcriptional activity by SUMO2 and PIASγ

Biochim Biophys Acta Mol Cell Res. 2021 Feb;1868(2):118908. doi: 10.1016/j.bbamcr.2020.118908. Epub 2020 Nov 13.

Abstract

Nur77 (NGFI-B) is a nuclear receptor that belongs to the Nr4a family of orphan nuclear receptors (Nr4a1). This transcription factor has been implicated in the regulation of multiple functions, such as cell cycle regulation, apoptosis, inflammation, glucose and lipid metabolism, and brain function. However, the mechanisms involved in its different regulatory properties remain unclear. In search for regulatory mechanisms of Nur77 function, we identified that Protein Inhibitor of Activated STAT gamma (PIASγ), an E3 SUMO-protein ligase, potently repressed Nur77 transcriptional activity in HEK-293T cells. This PIASγ activity was sensitive to Sentrin SUMO-specific protease 1 (SENP1). Substitution of two putative phylogenetically well-conserved small ubiquitin-like modifier (SUMO) acceptor sites, lysine 102 (K102) and 577 (K577) by arginine residues (R) modulated Nur77 transcriptional activity. In particular, Nur77-K102R and Nur77-K102R/K577R mutants strongly decreased the transcriptional activity of Nur77, whereas single K577R substitution increased transcriptional activity of Nur77. Repression of Nur77 transcriptional activity by SUMO2 and PIASγ was reduced by the K577R mutation, whereas the K102R mutant remained insensitive to SUMO2. Interestingly, the roles of these SUMO acceptor sites in Nur77 are distinct from previously observed activities on its close homolog Nurr1. Thus, the present study identified SUMO2 and PIASγ as important transcriptional co-regulators of Nur77.

Keywords: Amino acid residue specific mutation; Gene reporter assays; NGFI-B; Nurr1; Phylogenetic analysis; Protein inhibitor of activated STAT; SENP1; Small ubiquitin-like modifier protein.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cysteine Endopeptidases / genetics
  • Cysteine Endopeptidases / metabolism
  • Gene Expression Regulation
  • HEK293 Cells
  • Humans
  • Nuclear Receptor Subfamily 4, Group A, Member 1 / genetics
  • Nuclear Receptor Subfamily 4, Group A, Member 1 / metabolism*
  • Plasmids / genetics
  • Poly-ADP-Ribose Binding Proteins / genetics
  • Poly-ADP-Ribose Binding Proteins / metabolism*
  • Protein Inhibitors of Activated STAT / genetics
  • Protein Inhibitors of Activated STAT / metabolism*
  • Signal Transduction / genetics
  • Small Ubiquitin-Related Modifier Proteins / genetics
  • Small Ubiquitin-Related Modifier Proteins / metabolism*
  • Transcription, Genetic / genetics*
  • Transcriptional Activation*
  • Transfection

Substances

  • NR4A1 protein, human
  • Nuclear Receptor Subfamily 4, Group A, Member 1
  • PIAS4 protein, human
  • Poly-ADP-Ribose Binding Proteins
  • Protein Inhibitors of Activated STAT
  • SUMO2 protein, human
  • Small Ubiquitin-Related Modifier Proteins
  • SENP1 protein, human
  • Cysteine Endopeptidases