FATC Domain Deletion Compromises ATM Protein Stability, Blocks Lymphocyte Development, and Promotes Lymphomagenesis

J Immunol. 2021 Mar 15;206(6):1228-1239. doi: 10.4049/jimmunol.2000967. Epub 2021 Feb 3.

Abstract

Ataxia-telangiectasia mutated (ATM) kinase is a master regulator of the DNA damage response, and loss of ATM leads to primary immunodeficiency and greatly increased risk for lymphoid malignancies. The FATC domain is conserved in phosphatidylinositol-3-kinase-related protein kinases (PIKKs). Truncation mutation in the FATC domain (R3047X) selectively compromised reactive oxygen species-induced ATM activation in cell-free assays. In this article, we show that in mouse models, knock-in ATM-R3057X mutation (AtmRX ⁠, corresponding to R3047X in human ATM) severely compromises ATM protein stability and causes T cell developmental defects, B cell Ig class-switch recombination defects, and infertility resembling ATM-null. The residual ATM-R3057X protein retains minimal yet functional measurable DNA damage-induced checkpoint activation and significantly delays lymphomagenesis in AtmRX/RX ⁠ mice compared with Atm-/- ⁠. Together, these results support a physiological role of the FATC domain in ATM protein stability and show that the presence of minimal residual ATM-R3057X protein can prevent growth retardation and delay tumorigenesis without restoring lymphocyte development and fertility.

Publication types

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

MeSH terms

  • Animals
  • Ataxia Telangiectasia Mutated Proteins / genetics
  • Ataxia Telangiectasia Mutated Proteins / metabolism
  • Carcinogenesis / genetics
  • Carcinogenesis / immunology
  • Cell Differentiation / genetics
  • Cell Differentiation / immunology
  • Codon, Nonsense
  • Disease Models, Animal
  • Gene Knock-In Techniques
  • Humans
  • Lymphocytes / immunology*
  • Lymphocytes / pathology
  • Lymphoma / genetics*
  • Lymphoma / immunology
  • Lymphoma / pathology
  • Male
  • Mice
  • Mice, Knockout
  • Protein Domains / genetics*
  • Protein Stability
  • V(D)J Recombination / genetics
  • V(D)J Recombination / immunology

Substances

  • Codon, Nonsense
  • Ataxia Telangiectasia Mutated Proteins
  • Atm protein, mouse