HMGB1 represses the anti-cancer activity of sunitinib by governing TP53 autophagic degradation via its nucleus-to-cytoplasm transport

Autophagy. 2018;14(12):2155-2170. doi: 10.1080/15548627.2018.1501134. Epub 2018 Sep 11.

Abstract

Sunitinib, a multikinase inhibitor approved for a number of cancer indications has a low response rate. Identifying mechanisms of resistance could lead to rational combination regimens that could improve clinical outcomes. Here we report that resistance to sunitinib therapy was driven by autophagic degradation of TP53/p53. Deletion of ATG7 or ATG5 suppressed TP53 degradation, as did knockdown of SQSTM1/p62. Mechanistically, the transport of TP53 from the nucleus to the cytoplasm was essential for the sunitinib-induced autophagic degradation of TP53 and did not require TP53 nuclear export signals (NESs). Moreover, TP53 degradation was achieved by the transport of its nuclear binding target, HMGB1, which shifted TP53 from the nucleus to the cytoplasm. The inhibition of HMGB1 sensitized cancer cells to sunitinib. Importantly, sunitinib induced the degradation of all TP53 proteins, except for TP53 proteins with mutations in the interaction domain of TP53 with HMGB1 (amino acids 313 to 352). In conclusion, our data identify an alternative HMGB1-mediated TP53 protein turnover mechanism that participates in the resistance of sunitinib and suggest HMGB1 as a potential therapeutic target for improving clinical outcomes of sunitinib.

Keywords: Autophagy-lysosomal degradation; HMGB1; TP53; nuclear export; sunitinib.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Active Transport, Cell Nucleus / drug effects
  • Active Transport, Cell Nucleus / genetics
  • Adult
  • Aged
  • Aged, 80 and over
  • Animals
  • Autophagy / physiology
  • Cell Nucleus / drug effects
  • Cell Nucleus / metabolism*
  • Cells, Cultured
  • Cytoplasm / drug effects
  • Cytoplasm / metabolism*
  • Drug Resistance, Neoplasm / drug effects
  • Drug Resistance, Neoplasm / genetics*
  • HCT116 Cells
  • HEK293 Cells
  • HMGB1 Protein / antagonists & inhibitors
  • HMGB1 Protein / physiology*
  • HT29 Cells
  • Hep G2 Cells
  • Humans
  • K562 Cells
  • Male
  • Mice
  • Middle Aged
  • Protein Transport / drug effects
  • Protein Transport / genetics
  • Proteolysis* / drug effects
  • RNA, Small Interfering / pharmacology
  • Sunitinib / pharmacology
  • Sunitinib / therapeutic use*
  • Tumor Suppressor Protein p53 / metabolism*
  • Xenograft Model Antitumor Assays

Substances

  • HMGB1 Protein
  • HMGB1 protein, human
  • RNA, Small Interfering
  • TP53 protein, human
  • Tumor Suppressor Protein p53
  • Sunitinib

Grants and funding

This work was supported by National Natural Science Foundation for Distinguished Young Scholar of China (No.81625024), National Natural Science Foundation of China (Nos. 81673457 and 81473288) and Public Projects of Zhejiang Province (No.2016C31005).