O-GlcNAcylation of MITF regulates its activity and CDK4/6 inhibitor resistance in breast cancer

Nat Commun. 2024 Jul 3;15(1):5597. doi: 10.1038/s41467-024-49875-w.

Abstract

Cyclin-dependent kinases 4 and 6 (CDK4/6) play a pivotal role in cell cycle and cancer development. Targeting CDK4/6 has demonstrated promising effects against breast cancer. However, resistance to CDK4/6 inhibitors (CDK4/6i), such as palbociclib, remains a substantial challenge in clinical settings. Using high-throughput combinatorial drug screening and genomic sequencing, we find that the microphthalmia-associated transcription factor (MITF) is activated via O-GlcNAcylation by O-GlcNAc transferase (OGT) in palbociclib-resistant breast cancer cells and tumors. Mechanistically, O-GlcNAcylation of MITF at Serine 49 enhances its interaction with importin α/β, thus promoting its translocation to nuclei, where it suppresses palbociclib-induced senescence. Inhibition of MITF or its O-GlcNAcylation re-sensitizes resistant cells to palbociclib. Moreover, clinical studies confirm the activation of MITF in tumors from patients who are palbociclib-resistant or undergoing palbociclib treatment. Collectively, our studies shed light on the mechanism regulating palbociclib resistance and present clinical evidence for developing therapeutic approaches to treat CDK4/6i-resistant breast cancer patients.

MeSH terms

  • Animals
  • Breast Neoplasms* / drug therapy
  • Breast Neoplasms* / genetics
  • Breast Neoplasms* / metabolism
  • Breast Neoplasms* / pathology
  • Cell Line, Tumor
  • Cyclin-Dependent Kinase 4* / antagonists & inhibitors
  • Cyclin-Dependent Kinase 4* / metabolism
  • Cyclin-Dependent Kinase 6* / antagonists & inhibitors
  • Cyclin-Dependent Kinase 6* / metabolism
  • Drug Resistance, Neoplasm* / drug effects
  • Female
  • Humans
  • Mice
  • Microphthalmia-Associated Transcription Factor* / genetics
  • Microphthalmia-Associated Transcription Factor* / metabolism
  • N-Acetylglucosaminyltransferases* / antagonists & inhibitors
  • N-Acetylglucosaminyltransferases* / genetics
  • N-Acetylglucosaminyltransferases* / metabolism
  • Piperazines* / pharmacology
  • Protein Kinase Inhibitors / pharmacology
  • Pyridines* / pharmacology
  • Xenograft Model Antitumor Assays

Substances

  • Cyclin-Dependent Kinase 4
  • Cyclin-Dependent Kinase 6
  • Microphthalmia-Associated Transcription Factor
  • palbociclib
  • Piperazines
  • Pyridines
  • CDK4 protein, human
  • N-Acetylglucosaminyltransferases
  • CDK6 protein, human
  • MITF protein, human
  • Protein Kinase Inhibitors
  • O-GlcNAc transferase