Breast Tumor Kinase (Brk/PTK6) Is Induced by HIF, Glucocorticoid Receptor, and PELP1-Mediated Stress Signaling in Triple-Negative Breast Cancer

Cancer Res. 2016 Mar 15;76(6):1653-63. doi: 10.1158/0008-5472.CAN-15-2510. Epub 2016 Jan 29.

Abstract

Cancer cells use stress response pathways to sustain their pathogenic behavior. In breast cancer, stress response-associated phenotypes are mediated by the breast tumor kinase, Brk (PTK6), via the hypoxia-inducible factors HIF-1α and HIF-2α. Given that glucocorticoid receptor (GR) is highly expressed in triple-negative breast cancer (TNBC), we investigated cross-talk between stress hormone-driven GR signaling and HIF-regulated physiologic stress. Primary TNBC tumor explants or cell lines treated with the GR ligand dexamethasone exhibited robust induction of Brk mRNA and protein that was HIF1/2-dependent. HIF and GR coassembled on the BRK promoter in response to either hypoxia or dexamethasone, indicating that Brk is a direct GR/HIF target. Notably, HIF-2α, not HIF-1α, expression was induced by GR signaling, and the important steroid receptor coactivator PELP1 was also found to be induced in a HIF-dependent manner. Mechanistic investigations showed how PELP1 interacted with GR to activate Brk expression and demonstrated that physiologic cell stress, including hypoxia, promoted phosphorylation of GR serine 134, initiating a feed-forward signaling loop that contributed significantly to Brk upregulation. Collectively, our findings linked cellular stress (HIF) and stress hormone (cortisol) signaling in TNBC, identifying the phospho-GR/HIF/PELP1 complex as a potential therapeutic target to limit Brk-driven progression and metastasis in TNBC patients.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Basic Helix-Loop-Helix Transcription Factors / genetics*
  • Cell Line, Tumor
  • Co-Repressor Proteins / genetics*
  • Dexamethasone / pharmacology
  • Female
  • HeLa Cells
  • Humans
  • Hypoxia / genetics
  • Hypoxia-Inducible Factor 1, alpha Subunit / genetics*
  • Neoplasm Proteins / genetics*
  • Phosphorylation / drug effects
  • Phosphorylation / genetics
  • Promoter Regions, Genetic / drug effects
  • Promoter Regions, Genetic / genetics
  • Protein-Tyrosine Kinases / genetics*
  • RNA, Messenger / genetics
  • Receptors, Glucocorticoid / genetics*
  • Signal Transduction / drug effects
  • Signal Transduction / genetics
  • Stress, Physiological / drug effects
  • Stress, Physiological / genetics*
  • Transcription Factors / genetics*
  • Triple Negative Breast Neoplasms / drug therapy
  • Triple Negative Breast Neoplasms / genetics*
  • Up-Regulation / drug effects
  • Up-Regulation / genetics

Substances

  • Basic Helix-Loop-Helix Transcription Factors
  • Co-Repressor Proteins
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • Neoplasm Proteins
  • PELP1 protein, human
  • RNA, Messenger
  • Receptors, Glucocorticoid
  • Transcription Factors
  • endothelial PAS domain-containing protein 1
  • Dexamethasone
  • Protein-Tyrosine Kinases
  • PTK6 protein, human