Targeting ATM ameliorates mutant Huntingtin toxicity in cell and animal models of Huntington's disease

Sci Transl Med. 2014 Dec 24;6(268):268ra178. doi: 10.1126/scitranslmed.3010523.

Abstract

Age-related neurodegenerative disorders including Alzheimer's disease and Huntington's disease (HD) consistently show elevated DNA damage, but the relevant molecular pathways in disease pathogenesis remain unclear. One attractive gene is that encoding the ataxia-telangiectasia mutated (ATM) protein, a kinase involved in the DNA damage response, apoptosis, and cellular homeostasis. Loss-of-function mutations in both alleles of ATM cause ataxia-telangiectasia in children, but heterozygous mutation carriers are disease-free. Persistently elevated ATM signaling has been demonstrated in Alzheimer's disease and in mouse models of other neurodegenerative diseases. We show that ATM signaling was consistently elevated in cells derived from HD mice and in brain tissue from HD mice and patients. ATM knockdown protected from toxicities induced by mutant Huntingtin (mHTT) fragments in mammalian cells and in transgenic Drosophila models. By crossing the murine Atm heterozygous null allele onto BACHD mice expressing full-length human mHTT, we show that genetic reduction of Atm gene dosage by one copy ameliorated multiple behavioral deficits and partially improved neuropathology. Small-molecule ATM inhibitors reduced mHTT-induced death of rat striatal neurons and induced pluripotent stem cells derived from HD patients. Our study provides converging genetic and pharmacological evidence that reduction of ATM signaling could ameliorate mHTT toxicity in cellular and animal models of HD, suggesting that ATM may be a useful therapeutic target for HD.

Publication types

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

MeSH terms

  • Adult
  • Aged
  • Animals
  • Ataxia Telangiectasia Mutated Proteins / metabolism*
  • Behavior, Animal / drug effects
  • Brain / drug effects
  • Brain / metabolism
  • Brain / pathology
  • Cell Line
  • Cytoprotection / drug effects
  • Disease Models, Animal
  • Drosophila melanogaster / metabolism
  • Gene Dosage
  • Gene Knockdown Techniques
  • Histones / metabolism
  • Humans
  • Huntingtin Protein
  • Huntington Disease / metabolism
  • Huntington Disease / pathology*
  • Induced Pluripotent Stem Cells / cytology
  • Induced Pluripotent Stem Cells / drug effects
  • Induced Pluripotent Stem Cells / metabolism
  • Mice, Neurologic Mutants
  • Middle Aged
  • Morpholines / pharmacology
  • Mutant Proteins / toxicity*
  • Nerve Tissue Proteins / toxicity*
  • Neurons / drug effects
  • Neurons / metabolism
  • Neurons / pathology
  • Oxidative Stress / drug effects
  • Postmortem Changes
  • Serotonin Plasma Membrane Transport Proteins / toxicity*
  • Signal Transduction / drug effects
  • Thioxanthenes / pharmacology

Substances

  • 2-(2,6-dimethylmorpholin-4-yl)-N-(5-(6-morpholin-4-yl-4-oxo-4H-pyran-2-yl)-9H-thioxanthen-2-yl)acetamide
  • HTT protein, human
  • Histones
  • Huntingtin Protein
  • Morpholines
  • Mutant Proteins
  • Nerve Tissue Proteins
  • Serotonin Plasma Membrane Transport Proteins
  • Slc6a4 protein, mouse
  • Thioxanthenes
  • Ataxia Telangiectasia Mutated Proteins