Aberrant activation of adenine nucleotide translocase 3 promotes progression and chemoresistance in multiple myeloma dependent on PINK1 transport

Int J Biol Sci. 2025 Jan 1;21(1):233-250. doi: 10.7150/ijbs.101850. eCollection 2025.

Abstract

Chemoresistance is an important factor in multiple myeloma (MM) relapse and overall survival. However, the mechanism underlying resistance remains unclear. In this study, we identified adenine nucleotide translocase 3 (ANT3) as a novel biomarker and therapeutic target for MM progression and resistance to the proteasome inhibitor bortezomib (BTZ). The oncogenic functions of ANT3 in MM were verified using MM sensitive/drug-resistant cells, bone marrow tissues from patients with MM, orthotopic MM model, and subcutaneous tumor model. ANT3 knockdown impaired MM cell proliferation owing to a lack of cellular ATP levels, causing cell cycle arrest in the G0/G1 phase. Moreover, our study showed that ANT3 leads to BTZ resistance by promoting mitophagy. Notably, ANT3-mediated mitophagy is independent of its biological function as an ADP/ATP translocase. Mechanistically, ANT3 interacts with mitochondrial inner and outer membrane transporters, including Timm22 and Tomm20, thus restricting PINK1 import to the inner membrane of mitochondria. In this case, PINK1 is stabilized in the outer membrane of the mitochondria and recruits Parkin, resulting in mitophagy. Furthermore, targeted intervention with ANT3 combined with BTZ limited the growth of BTZ-resistant myeloma in vivo. This study identified ANT3 as a novel biomarker and therapeutic target for MM.

Keywords: Adenine nucleotide translocase 3; Bortezomib resistance; Mitophagy; Multiple myeloma.

MeSH terms

  • Adenine Nucleotide Translocator 3 / metabolism
  • Animals
  • Bortezomib* / pharmacology
  • Bortezomib* / therapeutic use
  • Cell Line, Tumor
  • Cell Proliferation / drug effects
  • Disease Progression
  • Drug Resistance, Neoplasm*
  • Female
  • Humans
  • Male
  • Mice
  • Mitochondrial Precursor Protein Import Complex Proteins
  • Mitophagy* / drug effects
  • Multiple Myeloma* / drug therapy
  • Multiple Myeloma* / metabolism
  • Multiple Myeloma* / pathology
  • Protein Kinases* / metabolism
  • Ubiquitin-Protein Ligases

Substances

  • Protein Kinases
  • Bortezomib
  • PTEN-induced putative kinase
  • Adenine Nucleotide Translocator 3
  • parkin protein
  • TOMM20 protein, human
  • Mitochondrial Precursor Protein Import Complex Proteins
  • Ubiquitin-Protein Ligases