Pathological neoangiogenesis depends on oxidative stress regulation by ATM

Nat Med. 2012 Aug;18(8):1208-16. doi: 10.1038/nm.2846. Epub 2012 Jul 15.

Abstract

The ataxia telangiectasia mutated (ATM) kinase, a master regulator of the DNA damage response (DDR), acts as a barrier to cellular senescence and tumorigenesis. Aside from DDR signaling, ATM also functions in oxidative defense. Here we show that Atm in mice is activated specifically in immature vessels in response to the accumulation of reactive oxygen species (ROS). Global or endothelial-specific Atm deficiency in mice blocked pathological neoangiogenesis in the retina. This block resulted from increased amounts of ROS and excessive activation of the mitogen activated kinase p38α rather than from defects in the canonical DDR pathway. Atm deficiency also lowered tumor angiogenesis and enhanced the antiangiogenic action of vascular endothelial growth factor (Vegf) blockade. These data suggest that pathological neoangiogenesis requires ATM-mediated oxidative defense and that agents that promote excessive ROS generation may have beneficial effects in the treatment of neovascular disease.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acetylcysteine / pharmacology
  • Acetylcysteine / therapeutic use
  • Animals
  • Antioxidants / pharmacology
  • Antioxidants / therapeutic use
  • Apoptosis
  • Ataxia Telangiectasia Mutated Proteins
  • Cell Cycle Proteins / deficiency
  • Cell Cycle Proteins / genetics
  • Cell Cycle Proteins / physiology*
  • Cells, Cultured / drug effects
  • Cells, Cultured / metabolism
  • DNA Repair
  • DNA-Binding Proteins / deficiency
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / physiology*
  • Endothelium, Vascular / physiopathology
  • Enzyme Activation
  • Eye Proteins / physiology
  • Female
  • Humans
  • Hydrogen Peroxide / antagonists & inhibitors
  • Hydrogen Peroxide / toxicity
  • Ischemia / drug therapy
  • Ischemia / pathology
  • Ischemia / physiopathology
  • Lipid Peroxidation / drug effects
  • Male
  • Melanoma, Experimental / blood supply
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Morpholines / pharmacology
  • Neovascularization, Pathologic / physiopathology*
  • Neovascularization, Pathologic / prevention & control
  • Oxidative Stress* / physiology
  • Protein Serine-Threonine Kinases / deficiency
  • Protein Serine-Threonine Kinases / genetics
  • Protein Serine-Threonine Kinases / physiology*
  • Pyrones / pharmacology
  • Reactive Oxygen Species / metabolism
  • Retinal Neovascularization / pathology
  • Retinal Neovascularization / physiopathology*
  • Retinal Neovascularization / prevention & control
  • Retinal Vessels / drug effects
  • Retinal Vessels / pathology
  • Signal Transduction / drug effects
  • Tumor Suppressor Proteins / deficiency
  • Tumor Suppressor Proteins / genetics
  • Tumor Suppressor Proteins / physiology*
  • Vascular Endothelial Growth Factor A / antagonists & inhibitors
  • Vascular Endothelial Growth Factor A / physiology
  • p38 Mitogen-Activated Protein Kinases / physiology

Substances

  • 2-morpholin-4-yl-6-thianthren-1-yl-pyran-4-one
  • Antioxidants
  • Cell Cycle Proteins
  • DNA-Binding Proteins
  • Eye Proteins
  • Morpholines
  • Pyrones
  • Reactive Oxygen Species
  • Tumor Suppressor Proteins
  • Vascular Endothelial Growth Factor A
  • vascular endothelial growth factor A, mouse
  • Hydrogen Peroxide
  • ATM protein, human
  • Ataxia Telangiectasia Mutated Proteins
  • Atm protein, mouse
  • Protein Serine-Threonine Kinases
  • p38 Mitogen-Activated Protein Kinases
  • Acetylcysteine