TGF-β receptor I inhibitor enhances response to enzalutamide in a pre-clinical model of advanced prostate cancer

Prostate. 2019 Jan;79(1):31-43. doi: 10.1002/pros.23708. Epub 2018 Aug 28.

Abstract

Background: Prostate cancer progression is navigated by the androgen receptor (AR) and transforming-growth factor-β (TGF-β) signaling. We previously demonstrated that aberrant TGF-β signaling accelerates prostate tumor progression in a transgenic mouse model of prostate cancer via effects on epithelial-mesenchymal transition (EMT), driving castration-resistant prostate cancer (CRPC).

Methods: This study examined the antitumor effect of the combination of TGF-β receptor I (TβRI) inhibitor, galunisertib, and FDA-approved antiandrogen enzalutamide, in our pre-clinical model. Age-matched genotypically characterized DNTGFβRII male mice were treated with either galunisertib and enzalutamide, in combination or as single agents in three "mini"-trials and the effects on tumor growth, phenotypic EMT, and actin cytoskeleton were evaluated.

Results: Galunisertib in combination with enzalutamide significantly suppressed prostate tumor growth, by increasing apoptosis and decreasing cell proliferation of tumor cell populations compared to the inhibitor as a monotherapy (P < 0.05). The combination treatment dramatically reduced cofilin levels, actin cytoskeleton regulator, compared to single agents. Treatment with galunisertib targeted nuclear Smad4 protein (intracellular TGF-β effector), but had no effect on nuclear AR. Consequential to TGF-β inhibition there was an EMT reversion to mesenchymal-epithelial transition (MET) and re-differentiation of prostate tumors. Elevated intratumoral TGF-β1 ligand, in response to galunisertib, was blocked by enzalutamide.

Conclusion: Our results provide novel insights into the therapeutic value of targeting TGF-β signaling to overcome resistance to enzalutamide in prostate cancer by phenotypic reprogramming of EMT towards tumor re-differentiation and cytoskeleton remodeling. This translational work is significant in sequencing TGF-β blockade and antiandrogens to optimize therapeutic response in CRPC.

Keywords: EMT; TGF-β inhibition strong; enzalutamide; therapeutic response.

Publication types

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

MeSH terms

  • Animals
  • Antineoplastic Agents / administration & dosage*
  • Benzamides
  • Drug Synergism
  • Epithelial-Mesenchymal Transition / drug effects*
  • Epithelial-Mesenchymal Transition / physiology
  • Male
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Nitriles
  • Phenylthiohydantoin / administration & dosage
  • Phenylthiohydantoin / analogs & derivatives*
  • Prostatic Neoplasms / drug therapy*
  • Prostatic Neoplasms / metabolism
  • Prostatic Neoplasms / pathology
  • Pyrazoles / administration & dosage*
  • Quinolines / administration & dosage*
  • Receptor, Transforming Growth Factor-beta Type I / antagonists & inhibitors*
  • Receptor, Transforming Growth Factor-beta Type I / metabolism

Substances

  • Antineoplastic Agents
  • Benzamides
  • Nitriles
  • Pyrazoles
  • Quinolines
  • Phenylthiohydantoin
  • LY-2157299
  • enzalutamide
  • Receptor, Transforming Growth Factor-beta Type I