IL-10R inhibition reprograms tumor-associated macrophages and reverses drug resistance in multiple myeloma

Leukemia. 2024 Nov;38(11):2355-2365. doi: 10.1038/s41375-024-02391-8. Epub 2024 Aug 30.

Abstract

Multiple myeloma (MM) is the cancer of plasma cells within the bone marrow and remains incurable. Tumor-associated macrophages (TAMs) within the tumor microenvironment often display a pro-tumor phenotype and correlate with tumor proliferation, survival, and therapy resistance. IL-10 is a key immunosuppressive cytokine that leads to recruitment and development of TAMs. In this study, we investigated the role of IL-10 in MM TAM development as well as the therapeutic application of IL-10/IL-10R/STAT3 signaling inhibition. We demonstrated that IL-10 is overexpressed in MM BM and mediates M2-like polarization of TAMs in patient BM, 3D co-cultures in vitro, and mouse models. In turn, TAMs promote MM proliferation and drug resistance, both in vitro and in vivo. Moreover, inhibition of IL-10/IL-10R/STAT3 axis using a blocking IL-10R monoclonal antibody and STAT3 protein degrader/PROTAC prevented M2 polarization of TAMs and the consequent TAM-induced proliferation of MM, and re-sensitized MM to therapy, in vitro and in vivo. Therefore, our findings suggest that inhibition of IL-10/IL-10R/STAT3 axis is a novel therapeutic strategy with monotherapy efficacy and can be further combined with current anti-MM therapy, such as immunomodulatory drugs, to overcome drug resistance. Future investigation is warranted to evaluate the potential of such therapy in MM patients.

MeSH terms

  • Animals
  • Cell Line, Tumor
  • Cell Proliferation / drug effects
  • Drug Resistance, Neoplasm*
  • Humans
  • Interleukin-10*
  • Mice
  • Multiple Myeloma* / drug therapy
  • Multiple Myeloma* / pathology
  • Receptors, Interleukin-10* / antagonists & inhibitors
  • Receptors, Interleukin-10* / metabolism
  • STAT3 Transcription Factor* / antagonists & inhibitors
  • STAT3 Transcription Factor* / metabolism
  • Signal Transduction / drug effects
  • Tumor Microenvironment* / drug effects
  • Tumor-Associated Macrophages* / drug effects
  • Tumor-Associated Macrophages* / immunology
  • Tumor-Associated Macrophages* / metabolism

Substances

  • Receptors, Interleukin-10
  • STAT3 Transcription Factor
  • Interleukin-10
  • STAT3 protein, human
  • IL10 protein, human