Connexin 43 Deficiency Confers Resistance to Immunotherapy in Lung Cancer via Inhibition of the Cyclic GMP-AMP Synthase-Stimulator of Interferon Genes Pathway

J Cell Mol Med. 2024 Nov;28(22):e70211. doi: 10.1111/jcmm.70211.

Abstract

Immune checkpoint inhibitors (ICIs), especially PD-1 inhibitors, are among the first-line therapeutic drugs for the treatment of advanced non-small cell lung cancer (NSCLC). However, most patients are not sensitive to PD-1 inhibitors, and prolonged exposure can lead to acquired resistance. Thus, it is urgent to elucidate the mechanism underlying the resistance of NSCLC to ICIs. Connexin 43 (Cx43) is a gap junction (GJ) protein that is important in therapeutic efficacy to ICIs. In this study, we observed that Cx43 in murine Lewis lung carcinoma (LLC) cells mediated cyclic GMP-AMP (cGAMP) transfer to macrophages. Knockdown of Cx43 reduced T-cell activation, leading to decreased sensitivity of LLC cells to anti-PD-1 therapy. The mechanism might be that knockdown of Cx43 in LLC cells promotes macrophages differentiation into pro-tumour M2 type (TAM), thus activating the STING pathway in macrophages. These findings indicate that downregulation of Cx43 in LLC cells leads to immunotherapy resistance by negatively regulating the cGAS-STING pathway in macrophages. Therefore, Cx43/GJ-mediated signal transmission between lung cancer cells and macrophages provides new insights for increasing immunotherapy sensitivity in NSCLC.

Keywords: STING; cGAMP; connexin 43; macrophage.

MeSH terms

  • Animals
  • Carcinoma, Lewis Lung* / genetics
  • Carcinoma, Lewis Lung* / immunology
  • Carcinoma, Lewis Lung* / metabolism
  • Carcinoma, Lewis Lung* / pathology
  • Carcinoma, Non-Small-Cell Lung / genetics
  • Carcinoma, Non-Small-Cell Lung / metabolism
  • Carcinoma, Non-Small-Cell Lung / pathology
  • Cell Line, Tumor
  • Connexin 43* / genetics
  • Connexin 43* / metabolism
  • Drug Resistance, Neoplasm / genetics
  • Humans
  • Immune Checkpoint Inhibitors / pharmacology
  • Immunotherapy* / methods
  • Lung Neoplasms* / genetics
  • Lung Neoplasms* / immunology
  • Lung Neoplasms* / metabolism
  • Lung Neoplasms* / pathology
  • Macrophages* / immunology
  • Macrophages* / metabolism
  • Membrane Proteins* / genetics
  • Membrane Proteins* / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Nucleotides, Cyclic* / metabolism
  • Nucleotidyltransferases / genetics
  • Nucleotidyltransferases / metabolism
  • Signal Transduction*

Substances

  • Connexin 43
  • Membrane Proteins
  • Nucleotides, Cyclic
  • Nucleotidyltransferases
  • cyclic guanosine monophosphate-adenosine monophosphate
  • Sting1 protein, mouse
  • Immune Checkpoint Inhibitors
  • cGAS protein, mouse