Adrenergic microenvironment driven by cancer-associated Schwann cells contributes to chemoresistance in patients with lung cancer

Cancer Sci. 2024 Jul;115(7):2333-2345. doi: 10.1111/cas.16164. Epub 2024 Apr 27.

Abstract

Doublecortin (DCX)-positive neural progenitor-like cells are purported components of the cancer microenvironment. The number of DCX-positive cells in tissues reportedly correlates with cancer progression; however, little is known about the mechanism by which these cells affect cancer progression. Here we demonstrated that DCX-positive cells, which are found in all major histological subtypes of lung cancer, are cancer-associated Schwann cells (CAS) and contribute to the chemoresistance of lung cancer cells by establishing an adrenergic microenvironment. Mechanistically, the activation of the Hippo transducer YAP/TAZ was involved in the acquisition of new traits of CAS and DCX positivity. We further revealed that CAS express catecholamine-synthesizing enzymes and synthesize adrenaline, which potentiates the chemoresistance of lung cancer cells through the activation of YAP/TAZ. Our findings shed light on CAS, which drive the formation of an adrenergic microenvironment by the reciprocal regulation of YAP/TAZ in lung cancer tissues.

Keywords: YAP/TAZ; adrenaline; cancer‐associated Schwann cells; doublecortin; microenvironment.

MeSH terms

  • Adaptor Proteins, Signal Transducing / genetics
  • Adaptor Proteins, Signal Transducing / metabolism
  • Animals
  • Cell Line, Tumor
  • Doublecortin Protein
  • Drug Resistance, Neoplasm*
  • Epinephrine / metabolism
  • Epinephrine / pharmacology
  • Female
  • Humans
  • Lung Neoplasms* / drug therapy
  • Lung Neoplasms* / metabolism
  • Lung Neoplasms* / pathology
  • Male
  • Mice
  • Microtubule-Associated Proteins / metabolism
  • Neuropeptides* / metabolism
  • Schwann Cells* / metabolism
  • Schwann Cells* / pathology
  • Transcription Factors* / metabolism
  • Transcriptional Coactivator with PDZ-Binding Motif Proteins / metabolism
  • Tumor Microenvironment*
  • YAP-Signaling Proteins / genetics
  • YAP-Signaling Proteins / metabolism

Substances

  • Neuropeptides
  • Transcription Factors
  • Doublecortin Protein
  • Microtubule-Associated Proteins
  • YAP-Signaling Proteins
  • Transcriptional Coactivator with PDZ-Binding Motif Proteins
  • Epinephrine
  • YAP1 protein, human
  • WWTR1 protein, human
  • Adaptor Proteins, Signal Transducing