ATM deficiency promotes development of murine B-cell lymphomas that resemble diffuse large B-cell lymphoma in humans

Blood. 2015 Nov 12;126(20):2291-301. doi: 10.1182/blood-2015-06-654749. Epub 2015 Sep 23.

Abstract

The serine-threonine kinase ataxia-telangiectasia mutated (ATM) plays a central role in maintaining genomic integrity. In mice, ATM deficiency is exclusively associated with T-cell lymphoma development, whereas B-cell tumors predominate in human ataxia-telangiectasia patients. We demonstrate in this study that when T cells are removed as targets for lymphomagenesis and as mediators of immune surveillance, ATM-deficient mice exclusively develop early-onset immunoglobulin M(+) B-cell lymphomas that do not transplant to immunocompetent mice and that histologically and genetically resemble the activated B cell-like (ABC) subset of human diffuse large B-cell lymphoma (DLBCL). These B-cell lymphomas show considerable chromosomal instability and a recurrent genomic amplification of a 4.48-Mb region on chromosome 18 that contains Malt1 and is orthologous to a region similarly amplified in human ABC DLBCL. Of importance, amplification of Malt1 in these lymphomas correlates with their dependence on nuclear factor (NF)-κB, MALT1, and B-cell receptor (BCR) signaling for survival, paralleling human ABC DLBCL. Further, like some human ABC DLBCLs, these mouse B-cell lymphomas also exhibit constitutive BCR-dependent NF-κB activation. This study reveals that ATM protects against development of B-cell lymphomas that model human ABC DLBCL and identifies a potential role for T cells in preventing the emergence of these tumors.

Publication types

  • Research Support, N.I.H., Intramural

MeSH terms

  • Animals
  • Ataxia Telangiectasia Mutated Proteins / deficiency*
  • Ataxia Telangiectasia Mutated Proteins / immunology
  • Caspases / genetics
  • Caspases / immunology
  • Cell Line, Tumor
  • Chromosomal Instability / immunology
  • Genetic Loci / immunology
  • Humans
  • Immunologic Surveillance*
  • Lymphoma, Large B-Cell, Diffuse / genetics
  • Lymphoma, Large B-Cell, Diffuse / immunology*
  • Lymphoma, Large B-Cell, Diffuse / pathology
  • Mice
  • Mice, Knockout
  • Mucosa-Associated Lymphoid Tissue Lymphoma Translocation 1 Protein
  • NF-kappa B / genetics
  • NF-kappa B / immunology
  • Neoplasm Proteins / genetics
  • Neoplasm Proteins / immunology
  • Receptors, Antigen, B-Cell / genetics
  • Receptors, Antigen, B-Cell / immunology
  • T-Lymphocytes / immunology
  • T-Lymphocytes / pathology
  • Tumor Suppressor Proteins / deficiency*
  • Tumor Suppressor Proteins / immunology

Substances

  • NF-kappa B
  • Neoplasm Proteins
  • Receptors, Antigen, B-Cell
  • Tumor Suppressor Proteins
  • ATM protein, human
  • Ataxia Telangiectasia Mutated Proteins
  • Atm protein, mouse
  • Caspases
  • MALT1 protein, human
  • Malt1 protein, mouse
  • Mucosa-Associated Lymphoid Tissue Lymphoma Translocation 1 Protein

Associated data

  • GEO/GSE59578
  • GEO/GSE68505