IRF4 requires ARID1A to establish plasma cell identity in multiple myeloma

Cancer Cell. 2024 Jul 8;42(7):1185-1201.e14. doi: 10.1016/j.ccell.2024.05.026. Epub 2024 Jun 20.

Abstract

Multiple myeloma (MM) is an incurable plasma cell malignancy that exploits transcriptional networks driven by IRF4. We employ a multi-omics approach to discover IRF4 vulnerabilities, integrating functional genomics screening, spatial proteomics, and global chromatin mapping. ARID1A, a member of the SWI/SNF chromatin remodeling complex, is required for IRF4 expression and functionally associates with IRF4 protein on chromatin. Deleting Arid1a in activated murine B cells disrupts IRF4-dependent transcriptional networks and blocks plasma cell differentiation. Targeting SWI/SNF activity leads to rapid loss of IRF4-target gene expression and quenches global amplification of oncogenic gene expression by MYC, resulting in profound toxicity to MM cells. Notably, MM patients with aggressive disease bear the signature of SWI/SNF activity, and SMARCA2/4 inhibitors remain effective in immunomodulatory drug (IMiD)-resistant MM cells. Moreover, combinations of SWI/SNF and MEK inhibitors demonstrate synergistic toxicity to MM cells, providing a promising strategy for relapsed/refractory disease.

Keywords: ARID1A; CRISPR; IRF4; MYC; SWI/SNF; multiple myeloma; plasma cell; proteogenomics; proteomics; transcription.

MeSH terms

  • Animals
  • Cell Differentiation / drug effects
  • Cell Line, Tumor
  • DNA-Binding Proteins* / genetics
  • DNA-Binding Proteins* / metabolism
  • Gene Expression Regulation, Neoplastic / drug effects
  • Humans
  • Interferon Regulatory Factors* / genetics
  • Interferon Regulatory Factors* / metabolism
  • Mice
  • Multiple Myeloma* / drug therapy
  • Multiple Myeloma* / genetics
  • Multiple Myeloma* / metabolism
  • Multiple Myeloma* / pathology
  • Plasma Cells* / drug effects
  • Plasma Cells* / metabolism
  • Plasma Cells* / pathology
  • Transcription Factors* / genetics
  • Transcription Factors* / metabolism

Substances

  • Interferon Regulatory Factors
  • interferon regulatory factor-4
  • Transcription Factors
  • DNA-Binding Proteins
  • ARID1A protein, human
  • Arid1a protein, mouse