Cisplatin-mediated activation of glucocorticoid receptor induces platinum resistance via MAST1

Nat Commun. 2021 Aug 16;12(1):4960. doi: 10.1038/s41467-021-24845-8.

Abstract

Agonists of glucocorticoid receptor (GR) are frequently given to cancer patients with platinum-containing chemotherapy to reduce inflammation, but how GR influences tumor growth in response to platinum-based chemotherapy such as cisplatin through inflammation-independent signaling remains largely unclear. Combined genomics and transcription factor profiling reveal that MAST1, a critical platinum resistance factor that reprograms the MAPK pathway, is upregulated upon cisplatin exposure through activated transcription factor GR. Mechanistically, cisplatin binds to C622 in GR and recruits GR to the nucleus for its activation, which induces MAST1 expression and consequently reactivates MEK signaling. GR nuclear translocation and MAST1 upregulation coordinately occur in patient tumors collected after platinum treatment, and align with patient treatment resistance. Co-treatment with dexamethasone and cisplatin restores cisplatin-resistant tumor growth, whereas addition of the MAST1 inhibitor lestaurtinib abrogates tumor growth while preserving the inhibitory effect of dexamethasone on inflammation in vivo. These findings not only provide insights into the underlying mechanism of GR in cisplatin resistance but also offer an effective alternative therapeutic strategy to improve the clinical outcome of patients receiving platinum-based chemotherapy with GR agonists.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apoptosis / drug effects
  • Cell Line, Tumor
  • Cell Nucleus
  • Cell Survival
  • Cisplatin / pharmacology*
  • Cytokines
  • Drug Resistance, Neoplasm / drug effects
  • Drug Resistance, Neoplasm / genetics
  • Female
  • Gene Expression / drug effects
  • Humans
  • Mice
  • Mice, Inbred C57BL
  • Microtubule-Associated Proteins / genetics
  • Microtubule-Associated Proteins / metabolism*
  • Platinum / pharmacology*
  • Protein Serine-Threonine Kinases / metabolism*
  • Receptors, Glucocorticoid / drug effects*
  • Receptors, Glucocorticoid / genetics
  • Receptors, Glucocorticoid / metabolism*
  • Signal Transduction / drug effects
  • Transcription Factors
  • Up-Regulation / drug effects
  • Xenograft Model Antitumor Assays

Substances

  • Cytokines
  • Microtubule-Associated Proteins
  • Receptors, Glucocorticoid
  • Transcription Factors
  • Platinum
  • MAST1 protein, human
  • Protein Serine-Threonine Kinases
  • Cisplatin