Respiratory complex I regulates dendritic cell maturation in explant model of human tumor immune microenvironment

J Immunother Cancer. 2024 Apr 11;12(4):e008053. doi: 10.1136/jitc-2023-008053.

Abstract

Background: Combining cytotoxic chemotherapy or novel anticancer drugs with T-cell modulators holds great promise in treating advanced cancers. However, the response varies depending on the tumor immune microenvironment (TIME). Therefore, there is a clear need for pharmacologically tractable models of the TIME to dissect its influence on mono- and combination treatment response at the individual level.

Methods: Here we establish a patient-derived explant culture (PDEC) model of breast cancer, which retains the immune contexture of the primary tumor, recapitulating cytokine profiles and CD8+T cell cytotoxic activity.

Results: We explored the immunomodulatory action of a synthetic lethal BCL2 inhibitor venetoclax+metformin drug combination ex vivo, discovering metformin cannot overcome the lymphocyte-depleting action of venetoclax. Instead, metformin promotes dendritic cell maturation through inhibition of mitochondrial complex I, increasing their capacity to co-stimulate CD4+T cells and thus facilitating antitumor immunity.

Conclusions: Our results establish PDECs as a feasible model to identify immunomodulatory functions of anticancer drugs in the context of patient-specific TIME.

Keywords: Breast Neoplasms; Dendritic Cells; Drug Evaluation, Preclinical; Immunity, Innate; Immunomodulation.

MeSH terms

  • Antineoplastic Agents* / pharmacology
  • Antineoplastic Agents* / therapeutic use
  • Breast Neoplasms*
  • Bridged Bicyclo Compounds, Heterocyclic*
  • Dendritic Cells
  • Electron Transport Complex I / pharmacology
  • Female
  • Humans
  • Metformin* / pharmacology
  • Metformin* / therapeutic use
  • Sulfonamides*
  • Tumor Microenvironment

Substances

  • venetoclax
  • Electron Transport Complex I
  • Antineoplastic Agents
  • Metformin
  • Sulfonamides
  • Bridged Bicyclo Compounds, Heterocyclic