MYC Inhibition Potentiates CD8+ T Cells Against Multiple Myeloma and Overcomes Immunomodulatory Drug Resistance

Clin Cancer Res. 2024 Jul 15;30(14):3023-3035. doi: 10.1158/1078-0432.CCR-24-0256.

Abstract

Purpose: Immunomodulatory drugs (IMiDs), such as lenalidomide and pomalidomide, are a cornerstone of multiple myeloma (MM) therapies, yet the disease inevitably becomes refractory. IMiDs exert cytotoxicity by inducing cereblon-dependent proteasomal degradation of IKZF1 and IKZF3, resulting in downregulation of the oncogenic transcription factors IRF4 and MYC. To date, clinical IMiD resistance independent of cereblon or IKZF1/3 has not been well explored. Here, we investigated the roles of IRF4 and MYC in this context.

Experimental design: Using bone marrow aspirates from patients with IMiD-naïve or refractory MM, we examined IKZF1/3 protein levels and IRF4/MYC gene expression following ex vivo pomalidomide treatment via flow cytometry and qPCR. We also assessed exvivo sensitivity to the MYC inhibitor MYCi975 using flow cytometry.

Results: We discovered that although pomalidomide frequently led to IKZF1/3 degradation in MM cells, it did not affect MYC gene expression in most IMiD-refractory samples. We subsequently demonstrated that MYCi975 exerted strong anti-MM effects in both IMiD-naïve and -refractory samples. Unexpectedly, we identified a cluster of differentiation 8+ (CD8+ T) cells from patients with MM as crucial effectors of MYCi975-induced cytotoxicity in primary MM samples, and we discovered that MYCi975 enhanced the cytotoxic functions of memory CD8+ T cells. We lastly observed synergy between MYCi975 and pomalidomide in IMiD-refractory samples, suggesting that restoring MYC downregulation can re-sensitize refractory MM to IMiDs.

Conclusions: Our study supports the concept that MYC represents an Achilles' heel in MM across disease states and that MYCi975 may be a promising therapeutic for patients with MM, particularly in combination with IMiDs.

MeSH terms

  • CD8-Positive T-Lymphocytes* / drug effects
  • CD8-Positive T-Lymphocytes* / immunology
  • CD8-Positive T-Lymphocytes* / metabolism
  • Cell Line, Tumor
  • Drug Resistance, Neoplasm*
  • Female
  • Gene Expression Regulation, Neoplastic / drug effects
  • Humans
  • Ikaros Transcription Factor* / genetics
  • Ikaros Transcription Factor* / metabolism
  • Immunomodulating Agents* / pharmacology
  • Interferon Regulatory Factors* / genetics
  • Interferon Regulatory Factors* / metabolism
  • Lenalidomide / pharmacology
  • Lenalidomide / therapeutic use
  • Male
  • Multiple Myeloma* / drug therapy
  • Multiple Myeloma* / immunology
  • Multiple Myeloma* / pathology
  • Proto-Oncogene Proteins c-myc* / genetics
  • Proto-Oncogene Proteins c-myc* / metabolism
  • Thalidomide* / analogs & derivatives
  • Thalidomide* / pharmacology

Substances

  • Proto-Oncogene Proteins c-myc
  • pomalidomide
  • Ikaros Transcription Factor
  • Thalidomide
  • interferon regulatory factor-4
  • Immunomodulating Agents
  • Interferon Regulatory Factors
  • IKZF1 protein, human
  • IKZF3 protein, human
  • MYC protein, human
  • Lenalidomide