DUSP6 inhibition overcomes neuregulin/HER3-driven therapy tolerance in HER2+ breast cancer

EMBO Mol Med. 2024 Jul;16(7):1603-1629. doi: 10.1038/s44321-024-00088-0. Epub 2024 Jun 17.

Abstract

Despite clinical benefits of tyrosine kinase inhibitors (TKIs) in cancer, most tumors can reactivate proliferation under TKI therapy. Here we present transcriptional profiling of HER2+ breast cancer cells transitioning from dormant drug tolerant cells to re-proliferating cells under continuous HER2 inhibitor (HER2i) therapy. Focusing on phosphatases, expression of dual-specificity phosphatase DUSP6 was found inhibited in dormant cells, but strongly induced upon regrowth. DUSP6 expression also selectively associated with poor patient survival in HER2+ breast cancers. DUSP6 overexpression conferred apoptosis resistance, whereas its pharmacological blockade prevented therapy tolerance development under HER2i therapy. DUSP6 targeting also synergized with clinically used HER2i combination therapies. Mechanistically DUSP6 is a positive regulator of HER3 expression, and its impact on HER2i tolerance was mediated by neuregulin-HER3 axis. In vivo, genetic targeting of DUSP6 reduced tumor growth in brain metastasis model, whereas its pharmacological targeting induced synthetic lethal therapeutic effect in combination with HER2i. Collectively this work demonstrates that DUSP6 drives escape from HER2i-induced dormancy, and that DUSP6 is a druggable target to overcome HER3-driven TKI resistance.

Keywords: BCI; FOXM1; Lapatinib; Neratinib; Non-genetic Drug Tolerance.

MeSH terms

  • Animals
  • Antineoplastic Agents / pharmacology
  • Antineoplastic Agents / therapeutic use
  • Breast Neoplasms* / drug therapy
  • Breast Neoplasms* / genetics
  • Breast Neoplasms* / metabolism
  • Breast Neoplasms* / pathology
  • Cell Line, Tumor
  • Drug Resistance, Neoplasm / drug effects
  • Dual Specificity Phosphatase 6* / genetics
  • Dual Specificity Phosphatase 6* / metabolism
  • Female
  • Humans
  • Mice
  • Protein Kinase Inhibitors / pharmacology
  • Receptor, ErbB-2* / metabolism
  • Receptor, ErbB-3* / antagonists & inhibitors
  • Receptor, ErbB-3* / genetics
  • Receptor, ErbB-3* / metabolism

Substances

  • Dual Specificity Phosphatase 6
  • DUSP6 protein, human
  • Receptor, ErbB-2
  • Receptor, ErbB-3
  • ERBB2 protein, human
  • ERBB3 protein, human
  • Antineoplastic Agents
  • Protein Kinase Inhibitors