Muscarinic receptors promote castration-resistant growth of prostate cancer through a FAK-YAP signaling axis

Oncogene. 2020 May;39(20):4014-4027. doi: 10.1038/s41388-020-1272-x. Epub 2020 Mar 23.

Abstract

Prostate cancer (PCa) innervation contributes to the progression of PCa. However, the precise impact of innervation on PCa cells is still poorly understood. By focusing on muscarinic receptors, which are activated by the nerve-derived neurotransmitter acetylcholine, we show that muscarinic receptors 1 and 3 (m1 and m3) are highly expressed in PCa clinical specimens compared with all other cancer types, and that amplification or gain of their corresponding encoding genes (CHRM1 and CHRM3, respectively) represent a worse prognostic factor for PCa progression free survival. Moreover, m1 and m3 gene gain or amplification is frequent in castration-resistant PCa (CRPC) compared with hormone-sensitive PCa (HSPC) specimens. This was reflected in HSPC-derived cells, which show aberrantly high expression of m1 and m3 under androgen deprivation mimicking castration and androgen receptor inhibition. We also show that pharmacological activation of m1 and m3 signaling is sufficient to induce the castration-resistant growth of PCa cells. Mechanistically, we found that m1 and m3 stimulation induces YAP activation through FAK, whose encoding gene, PTK2 is frequently amplified in CRPC cases. Pharmacological inhibition of FAK and knockdown of YAP abolished m1 and m3-induced castration-resistant growth of PCa cells. Our findings provide novel therapeutic opportunities for muscarinic-signal-driven CRPC progression by targeting the FAK-YAP signaling axis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing / genetics
  • Adaptor Proteins, Signal Transducing / metabolism*
  • Focal Adhesion Kinase 1 / genetics
  • Focal Adhesion Kinase 1 / metabolism*
  • Humans
  • Male
  • Neoplasm Proteins / genetics
  • Neoplasm Proteins / metabolism*
  • PC-3 Cells
  • Prostatic Neoplasms, Castration-Resistant / genetics
  • Prostatic Neoplasms, Castration-Resistant / metabolism*
  • Prostatic Neoplasms, Castration-Resistant / pathology
  • Receptor, Muscarinic M1 / biosynthesis*
  • Receptor, Muscarinic M1 / genetics
  • Receptor, Muscarinic M3 / biosynthesis*
  • Receptor, Muscarinic M3 / genetics
  • Signal Transduction*
  • Transcription Factors / genetics
  • Transcription Factors / metabolism*
  • YAP-Signaling Proteins

Substances

  • Adaptor Proteins, Signal Transducing
  • CHRM1 protein, human
  • CHRM3 protein, human
  • Neoplasm Proteins
  • Receptor, Muscarinic M1
  • Receptor, Muscarinic M3
  • Transcription Factors
  • YAP-Signaling Proteins
  • YAP1 protein, human
  • Focal Adhesion Kinase 1
  • PTK2 protein, human