Regulation of reactive oxygen species by Atm is essential for proper response to DNA double-strand breaks in lymphocytes

J Immunol. 2007 Jan 1;178(1):103-10. doi: 10.4049/jimmunol.178.1.103.

Abstract

The ataxia telangiectasia-mutated (ATM) gene plays a pivotal role in the maintenance of genomic stability. Although it has been recently shown that antioxidative agents inhibited lymphomagenesis in Atm(-/-) mice, the mechanisms remain unclear. In this study, we intensively investigated the roles of reactive oxygen species (ROS) in phenotypes of Atm(-/-) mice. Reduction of ROS by the antioxidant N-acetyl-l-cysteine (NAC) prevented the emergence of senescent phenotypes in Atm(-/-) mouse embryonic fibroblasts, hypersensitivity to total body irradiation, and thymic lymphomagenesis in Atm(-/-) mice. To understand the mechanisms for prevention of lymphomagenesis, we analyzed development of pretumor lymphocytes in Atm(-/-) mice. Impairment of Ig class switch recombination seen in Atm(-/-) mice was mitigated by NAC, indicating that ROS elevation leads to abnormal response to programmed double-strand breaks in vivo. Significantly, in vivo administration of NAC to Atm(-/-) mice restored normal T cell development and inhibited aberrant V(D)J recombination. We conclude that Atm-mediated ROS regulation is essential for proper DNA recombination, preventing immunodeficiency, and lymphomagenesis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acetylcysteine / pharmacology
  • Animals
  • Antioxidants / pharmacology
  • Ataxia Telangiectasia Mutated Proteins
  • B-Lymphocytes / drug effects
  • B-Lymphocytes / metabolism
  • Cell Cycle Proteins / genetics
  • Cell Cycle Proteins / physiology*
  • Cellular Senescence / drug effects
  • Cellular Senescence / genetics
  • Cellular Senescence / immunology
  • DNA Breaks, Double-Stranded*
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / physiology*
  • Gene Rearrangement, beta-Chain T-Cell Antigen Receptor* / drug effects
  • Gene Rearrangement, gamma-Chain T-Cell Antigen Receptor* / drug effects
  • Immunoglobulin Class Switching / drug effects
  • Immunoglobulin Class Switching / genetics
  • Lymphoma / genetics*
  • Lymphoma / immunology
  • Lymphoma / prevention & control
  • Mice
  • Mice, Mutant Strains
  • Protein Serine-Threonine Kinases / genetics
  • Protein Serine-Threonine Kinases / physiology*
  • Radiation Tolerance / drug effects
  • Reactive Oxygen Species / antagonists & inhibitors
  • Reactive Oxygen Species / metabolism*
  • T-Lymphocytes / drug effects
  • T-Lymphocytes / immunology
  • Tumor Suppressor Proteins / genetics
  • Tumor Suppressor Proteins / physiology*

Substances

  • Antioxidants
  • Cell Cycle Proteins
  • DNA-Binding Proteins
  • Reactive Oxygen Species
  • Tumor Suppressor Proteins
  • Ataxia Telangiectasia Mutated Proteins
  • Atm protein, mouse
  • Protein Serine-Threonine Kinases
  • Acetylcysteine