Ubiquitin-specific peptidase 7 (USP7)-mediated deubiquitination of the histone deacetylase SIRT7 regulates gluconeogenesis

J Biol Chem. 2017 Aug 11;292(32):13296-13311. doi: 10.1074/jbc.M117.780130. Epub 2017 Jun 27.

Abstract

Sirtuin 7 (SIRT7), a member of the NAD+-dependent class III histone deacetylases, is involved in the regulation of various cellular processes and in resisting various stresses, such as hypoxia, low glucose levels, and DNA damage. Interestingly, SIRT7 is linked to the control of glycolysis, suggesting a role in glucose metabolism. Given the important roles of SIRT7, it is critical to clarify how SIRT7 activity is potentially regulated. It has been reported that some transcriptional and post-transcriptional regulatory mechanisms are involved. However, little is known how SIRT7 is regulated by the post-translational modifications. Here, we identified ubiquitin-specific peptidase 7 (USP7), a deubiquitinase, as a negative regulator of SIRT7. We showed that USP7 interacts with SIRT7 both in vitro and in vivo, and we further demonstrated that SIRT7 undergoes endogenous Lys-63-linked polyubiquitination, which is removed by USP7. Although the USP7-mediated deubiquitination of SIRT7 had no effect on its stability, the deubiquitination repressed its enzymatic activity. We also showed that USP7 coordinates with SIRT7 to regulate the expression of glucose-6-phosphatase catalytic subunit (G6PC), a gluconeogenic gene. USP7 depletion by RNA interference increased both G6PC expression and SIRT7 enzymatic activity. Moreover, SIRT7 targeted the G6PC promoter through the transcription factor ELK4 but not through forkhead box O1 (FoxO1). In summary, SIRT7 is a USP7 substrate and has a novel role as a regulator of gluconeogenesis. Our study may provide the basis for new clinical approaches to treat metabolic disorders related to glucose metabolism.

Keywords: deubiquitylation (deubiquitination); gene expression; gluconeogenesis; post-translational modification; sirtuin.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Substitution
  • Cell Line, Tumor
  • Gene Deletion
  • Gene Expression Regulation, Enzymologic*
  • Gluconeogenesis
  • Glucose-6-Phosphatase / antagonists & inhibitors
  • Glucose-6-Phosphatase / genetics
  • Glucose-6-Phosphatase / metabolism*
  • HEK293 Cells
  • Humans
  • Hydrolysis
  • Lysine / metabolism
  • Mutation
  • Peptide Fragments / antagonists & inhibitors
  • Peptide Fragments / genetics
  • Peptide Fragments / metabolism
  • Promoter Regions, Genetic*
  • Protein Interaction Domains and Motifs
  • Protein Processing, Post-Translational*
  • Protein Subunits / genetics
  • Protein Subunits / metabolism
  • RNA Interference
  • Recombinant Fusion Proteins / chemistry
  • Recombinant Fusion Proteins / metabolism
  • Sirtuins / antagonists & inhibitors
  • Sirtuins / genetics
  • Sirtuins / metabolism*
  • Substrate Specificity
  • Ubiquitin Thiolesterase / antagonists & inhibitors
  • Ubiquitin Thiolesterase / genetics
  • Ubiquitin Thiolesterase / metabolism*
  • Ubiquitin-Specific Peptidase 7
  • Ubiquitination
  • ets-Domain Protein Elk-4 / genetics
  • ets-Domain Protein Elk-4 / metabolism*

Substances

  • ELK4 protein, human
  • Peptide Fragments
  • Protein Subunits
  • Recombinant Fusion Proteins
  • SIRT7 protein, human
  • ets-Domain Protein Elk-4
  • G6PC1 protein, human
  • Glucose-6-Phosphatase
  • USP7 protein, human
  • Ubiquitin Thiolesterase
  • Ubiquitin-Specific Peptidase 7
  • Sirtuins
  • Lysine