NEK2 induces autophagy-mediated bortezomib resistance by stabilizing Beclin-1 in multiple myeloma

Mol Oncol. 2020 Apr;14(4):763-778. doi: 10.1002/1878-0261.12641. Epub 2020 Jan 29.

Abstract

NEK2 is associated with drug resistance in multiple cancers. Our previous studies indicated that high NEK2 confers inferior survival in multiple myeloma (MM); thus, a better understanding of the mechanisms by which NEK2 induces drug resistance in MM is required. In this study, we discovered that NEK2 enhances MM cell autophagy, and a combination of autophagy inhibitor chloroquine (CQ) and chemotherapeutic bortezomib (BTZ) significantly prevents NEK2-induced drug resistance in MM cells. Interestingly, NEK2 was found to bind and stabilize Beclin-1 protein but did not affect its mRNA expression and phosphorylation. Moreover, autophagy enhanced by NEK2 was significantly prevented by knockdown of Beclin-1 in MM cells, suggesting that Beclin-1 mediates NEK2-induced autophagy. Further studies demonstrated that Beclin-1 ubiquitination is decreased through NEK2 interaction with USP7. Importantly, knockdown of Beclin-1 sensitized NEK2-overexpressing MM cells to BTZ in vitro and in vivo. In conclusion, we identify a novel mechanism whereby autophagy is activated by the complex of NEK2/USP7/Beclin-1 in MM cells. Targeting the autophagy signaling pathway may provide a promising therapeutic strategy to overcome NEK2-induced drug resistance in MM.

Keywords: Beclin-1; NEK2; autophagy; multiple myeloma; ubiquitination.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antineoplastic Agents / pharmacology*
  • Antineoplastic Agents / therapeutic use
  • Autophagy / drug effects
  • Beclin-1 / metabolism*
  • Bortezomib / pharmacology*
  • Bortezomib / therapeutic use
  • Cell Line, Tumor
  • Drug Resistance, Neoplasm*
  • Humans
  • Mice
  • Multiple Myeloma / drug therapy*
  • Multiple Myeloma / metabolism
  • NIMA-Related Kinases / metabolism*
  • Protein Stability / drug effects

Substances

  • Antineoplastic Agents
  • Beclin-1
  • Bortezomib
  • NEK2 protein, human
  • NIMA-Related Kinases