A preclinical model of peripheral T-cell lymphoma GATA3 reveals DNA damage response pathway vulnerability

EMBO Mol Med. 2022 Jun 8;14(6):e15816. doi: 10.15252/emmm.202215816. Epub 2022 May 5.

Abstract

Peripheral T-cell lymphoma (PTCL) represents a rare group of heterogeneous diseases in urgent need of effective treatments. A scarcity of disease-relevant preclinical models hinders research advances. Here, we isolated a novel mouse (m)PTCL by serially transplanting a lymphoma from a germinal center B-cell hyperplasia model (Cγ1-Cre Blimp1fl/fl ) through immune-competent mice. Lymphoma cells were identified as clonal TCRβ+ T-helper cells expressing T-follicular helper markers. We also observed coincident B-cell activation and development of a de novo B-cell lymphoma in the model, reminiscent of B-cell activation/lymphomagenesis found in human PTCL. Molecular profiling linked the mPTCL to the high-risk "GATA3" subtype of PTCL, showing GATA3 and Th2 gene expression, PI3K/mTOR pathway enrichment, hyperactivated MYC, and genome instability. Exome sequencing identified a human-relevant oncogenic β-catenin mutation possibly involved in T-cell lymphomagenesis. Prolonged treatment responses were achieved in vivo by targeting ATR in the DNA damage response (DDR), a result corroborated in PTCL cell lines. This work provides mechanistic insight into the molecular and immunological drivers of T-cell lymphomagenesis and proposes DDR inhibition as an effective and readily translatable therapy in PTCL.

Keywords: DNA damage response; GATA3; T-follicular helper cell; peripheral T-cell lymphoma; syngeneic mouse model.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • B-Lymphocytes / immunology
  • B-Lymphocytes / metabolism
  • DNA Damage*
  • GATA3 Transcription Factor* / genetics
  • Lymphoma, T-Cell, Peripheral* / genetics
  • Lymphoma, T-Cell, Peripheral* / immunology
  • Lymphoma, T-Cell, Peripheral* / metabolism
  • Lymphoma, T-Cell, Peripheral* / pathology
  • Mice
  • T-Lymphocytes / immunology
  • T-Lymphocytes / metabolism

Substances

  • GATA3 Transcription Factor
  • Gata3 protein, mouse