Cholinergic signaling via muscarinic M1 receptor confers resistance to docetaxel in prostate cancer

Cell Rep Med. 2024 Feb 20;5(2):101388. doi: 10.1016/j.xcrm.2023.101388. Epub 2024 Jan 22.

Abstract

Docetaxel is the most commonly used chemotherapy for advanced prostate cancer (PC), including castration-resistant disease (CRPC), but the eventual development of docetaxel resistance constitutes a major clinical challenge. Here, we demonstrate activation of the cholinergic muscarinic M1 receptor (CHRM1) in CRPC cells upon acquiring resistance to docetaxel, which is manifested in tumor tissues from PC patients post- vs. pre-docetaxel. Genetic and pharmacological inactivation of CHRM1 restores the efficacy of docetaxel in resistant cells. Mechanistically, CHRM1, via its first and third extracellular loops, interacts with the SEMA domain of cMET and forms a heteroreceptor complex with cMET, stimulating a downstream mitogen-activated protein polykinase program to confer docetaxel resistance. Dicyclomine, a clinically available CHRM1-selective antagonist, reverts resistance and restricts the growth of multiple docetaxel-resistant CRPC cell lines and patient-derived xenografts. Our study reveals a CHRM1-dictated mechanism for docetaxel resistance and identifies a CHRM1-targeted combinatorial strategy for overcoming docetaxel resistance in PC.

Keywords: CHRM1; MAPK pathway; acetylcholine; cMET; dicyclomine; docetaxel resistance; muscarinic receptor; prostate cancer.

MeSH terms

  • Cell Line, Tumor
  • Cholinergic Agents / therapeutic use
  • Docetaxel / pharmacology
  • Docetaxel / therapeutic use
  • Humans
  • Male
  • Prostatic Neoplasms, Castration-Resistant* / drug therapy
  • Prostatic Neoplasms, Castration-Resistant* / genetics
  • Prostatic Neoplasms, Castration-Resistant* / metabolism
  • Receptor, Muscarinic M1* / genetics

Substances

  • Docetaxel
  • Receptor, Muscarinic M1
  • Cholinergic Agents
  • CHRM1 protein, human