The interaction of the atm genotype with inflammation and oxidative stress

PLoS One. 2014 Jan 20;9(1):e85863. doi: 10.1371/journal.pone.0085863. eCollection 2014.

Abstract

In ataxia-telangiectasia (A-T) the death of neurons is associated with the loss of neuronal cell cycle control. In most Atm(-/-) mouse models, however, these cell cycle anomalies are present but the phenotype of neuronal cell loss found in humans is not. Mouse Atm(-/-) neurons re-enter a cell cycle and replicate their DNA, but they do not die--even months after initiating the cycle. In the current study, we explore whether systemic inflammation or hypoxia-induced oxidative stress can serve as second stressors that can promote cell death in ATM-deficient neurons. We find that after either immune or hypoxic challenge, the levels of cell cycle proteins--PCNA, cyclin A and cyclin B--are significantly elevated in cerebellar Purkinje cells. Both the number of cells that express cell cycle proteins as well as the intensity of the expression levels in each cell is increased in the stressed animals. The cell cycle-positive neurons also increasingly express cell death markers such as activated caspase-3, γ-H2AX and TUNEL staining. Interestingly, nuclear HDAC4 localization is also enhanced in Atm(-/-) Purkinje neurons after the immune challenge suggesting that both genetic and epigenetic changes in Atm(-/-) mice respond to environmental challenges. Our findings support the hypothesis that multiple insults are needed to drive even genetically vulnerable neurons to die a cell cycle-related cell death and point to either inflammation or oxidative stressors as potential contributors to the A-T disease process.

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
  • Caspase 3 / metabolism
  • Cyclin A / genetics
  • Cyclin A / metabolism
  • Cyclin B / genetics
  • Cyclin B / metabolism
  • Genotype*
  • Histone Deacetylases / genetics
  • Histone Deacetylases / metabolism
  • Hypoxia / genetics
  • Hypoxia / metabolism
  • Inflammation / genetics*
  • Inflammation / metabolism
  • Mice
  • Mice, Knockout
  • Neurons / metabolism*
  • Oxidative Stress / genetics*
  • Proliferating Cell Nuclear Antigen / genetics
  • Proliferating Cell Nuclear Antigen / metabolism
  • Purkinje Cells / metabolism

Substances

  • Cyclin A
  • Cyclin B
  • Proliferating Cell Nuclear Antigen
  • Ataxia Telangiectasia Mutated Proteins
  • Caspase 3
  • Hdac5 protein, mouse
  • Histone Deacetylases