PLK2-mediated phosphorylation of SQSTM1 S349 promotes aggregation of polyubiquitinated proteins upon proteasomal dysfunction

Autophagy. 2024 Oct;20(10):2221-2237. doi: 10.1080/15548627.2024.2361574. Epub 2024 Jun 19.

Abstract

Dysregulation in protein homeostasis results in accumulation of protein aggregates, which are sequestered into dedicated insoluble compartments so-called inclusion bodies or aggresomes, where they are scavenged through different mechanisms to reduce proteotoxicity. The protein aggregates can be selectively scavenged by macroautophagy/autophagy called aggrephagy, which is mediated by the autophagic receptor SQSTM1. In this study, we have identified PLK2 as an important regulator of SQSTM1-mediated aggregation of polyubiquitinated proteins. PLK2 is upregulated following proteasome inhibition, and then associates with and phosphorylates SQSTM1 at S349. The phosphorylation of SQSTM1 S349 strengthens its binding to KEAP1, which is required for formation of large SQSTM1 aggregates/bodies upon proteasome inhibition. Our findings suggest that PLK2-mediated phosphorylation of SQSTM1 S349 represents a critical regulatory mechanism in SQSTM1-mediated aggregation of polyubiquitinated proteins.

Keywords: PLK2; Phosphorylation; SQSTM1/p62; polyubiquitination; proteasome; protein aggregation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Autophagy / physiology
  • HEK293 Cells
  • Humans
  • Kelch-Like ECH-Associated Protein 1 / metabolism
  • Phosphorylation
  • Proteasome Endopeptidase Complex* / metabolism
  • Protein Aggregates*
  • Protein Binding
  • Protein Serine-Threonine Kinases* / metabolism
  • Sequestosome-1 Protein* / metabolism
  • Ubiquitinated Proteins / metabolism
  • Ubiquitination

Substances

  • Sequestosome-1 Protein
  • Proteasome Endopeptidase Complex
  • SQSTM1 protein, human
  • Protein Serine-Threonine Kinases
  • Protein Aggregates
  • Ubiquitinated Proteins
  • Kelch-Like ECH-Associated Protein 1
  • KEAP1 protein, human

Grants and funding

This work was supported by the National Natural Science Foundation of China (32188101 and 32070775), the CAMS Innovation Fund for Medical Sciences (2019-I2M-5-071), the Major Scientific and Technological Project of Hubei Province (2022ACA005), and the Fundamental Research Funds for the Central Universities (2042022dx0003).