CD19-CAR T cells undergo exhaustion DNA methylation programming in patients with acute lymphoblastic leukemia

Cell Rep. 2021 Nov 30;37(9):110079. doi: 10.1016/j.celrep.2021.110079.

Abstract

CD19-CAR T cell therapy has evolved into the standard of care for relapsed/refractory B cell acute lymphoblastic leukemia (ALL); however, limited persistence of the CAR T cells enables tumor relapse for many patients. To gain a deeper understanding of the molecular characteristics associated with CAR T cell differentiation, we performed longitudinal genome-wide DNA methylation profiling of CD8+ CD19-CAR T cells post-infusion in ALL patients. We report that CAR T cells undergo a rapid and broad erasure of repressive DNA methylation reprograms at effector-associated genes. The CAR T cell post-infusion changes are further characterized by repression of genes (e.g., TCF7 and LEF1) associated with memory potential and a DNA methylation signature (e.g., demethylation at CX3CR1, BATF, and TOX) demarcating a transition toward exhaustion-progenitor T cells. Thus, CD19-CAR T cells undergo exhaustion-associated DNA methylation programming, indicating that efforts to prevent this process may be an attractive approach to improve CAR T cell efficacy.

Keywords: CAR T cells; DNA methylation; differentiation; effector; exhaustion; leukemia; memory.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adolescent
  • Adult
  • Antigens, CD19 / immunology*
  • CD8-Positive T-Lymphocytes / immunology*
  • Child
  • Child, Preschool
  • DNA Methylation*
  • Female
  • Gene Expression Regulation, Neoplastic*
  • Humans
  • Immunotherapy, Adoptive / methods*
  • Infant
  • Male
  • Precursor Cell Lymphoblastic Leukemia-Lymphoma / genetics
  • Precursor Cell Lymphoblastic Leukemia-Lymphoma / immunology
  • Precursor Cell Lymphoblastic Leukemia-Lymphoma / pathology
  • Precursor Cell Lymphoblastic Leukemia-Lymphoma / therapy*
  • Receptors, Antigen, T-Cell / immunology*
  • Young Adult

Substances

  • Antigens, CD19
  • Receptors, Antigen, T-Cell