Malignant A-to-I RNA editing by ADAR1 drives T cell acute lymphoblastic leukemia relapse via attenuating dsRNA sensing

Cell Rep. 2024 Feb 27;43(2):113704. doi: 10.1016/j.celrep.2024.113704. Epub 2024 Jan 23.

Abstract

Leukemia-initiating cells (LICs) are regarded as the origin of leukemia relapse and therapeutic resistance. Identifying direct stemness determinants that fuel LIC self-renewal is critical for developing targeted approaches. Here, we show that the RNA-editing enzyme ADAR1 is a crucial stemness factor that promotes LIC self-renewal by attenuating aberrant double-stranded RNA (dsRNA) sensing. Elevated adenosine-to-inosine editing is a common attribute of relapsed T cell acute lymphoblastic leukemia (T-ALL) regardless of molecular subtype. Consequently, knockdown of ADAR1 severely inhibits LIC self-renewal capacity and prolongs survival in T-ALL patient-derived xenograft models. Mechanistically, ADAR1 directs hyper-editing of immunogenic dsRNA to avoid detection by the innate immune sensor melanoma differentiation-associated protein 5 (MDA5). Moreover, we uncover that the cell-intrinsic level of MDA5 dictates the dependency on the ADAR1-MDA5 axis in T-ALL. Collectively, our results show that ADAR1 functions as a self-renewal factor that limits the sensing of endogenous dsRNA. Thus, targeting ADAR1 presents an effective therapeutic strategy for eliminating T-ALL LICs.

Keywords: CP: Cancer; CP: Immunology; RNA editing; epitranscriptome; leukemia-initiating cells; pediatric leukemia.

MeSH terms

  • Chronic Disease
  • Humans
  • Precursor T-Cell Lymphoblastic Leukemia-Lymphoma*
  • RNA Editing
  • RNA, Double-Stranded*
  • T-Lymphocytes

Substances

  • RNA, Double-Stranded
  • ADAR protein, human