PGC-1 alpha serine 570 phosphorylation and GCN5-mediated acetylation by angiotensin II drive catalase down-regulation and vascular hypertrophy

J Biol Chem. 2010 Jan 22;285(4):2474-87. doi: 10.1074/jbc.M109.065235. Epub 2009 Nov 23.

Abstract

Angiotensin II (Ang II) is a pleuripotential hormone that is important in the pathophysiology of multiple conditions including aging, cardiovascular and renal diseases, and insulin resistance. Reactive oxygen species (ROS) are important mediators of Ang II-induced signaling generally and have a well defined role in vascular hypertrophy, which is inhibited by overexpression of catalase, inferring a specific role of H(2)O(2). The molecular mechanisms are understood incompletely. The transcriptional coactivator peroxisome proliferator-activated receptor gamma coactivator-1 alpha (PGC-1 alpha) is a key regulator of energy metabolism and ROS-scavenging enzymes including catalase. We show that Ang II stimulates Akt-dependent PGC-1 alpha serine 570 phosphorylation, which is required for the binding of the histone acetyltransferase GCN5 (general control nonderepressible 5) to PGC-1 alpha and for its lysine acetylation. These sequential post-translational modifications suppress PGC-1 alpha activity and prevent its binding to the catalase promoter through the forkhead box O1 transcription factor, thus decreasing catalase expression. We demonstrate that overexpression of the phosphorylation-defective mutant PGC-1 alpha (S570A) prevents Ang II-induced increases in H(2)O(2) levels and hypertrophy ([(3)H]leucine incorporation). Knockdown of PGC-1 alpha by small interfering RNA promotes basal and Ang II-stimulated ROS and hypertrophy, which is reversed by polyethylene glycol-conjugated catalase. Thus, endogenous PGC-1 alpha is a negative regulator of vascular hypertrophy by up-regulating catalase expression and thus reducing ROS levels. We provide novel mechanistic insights by which Ang II may mediate its ROS-dependent pathophysiologic effects on multiple cardiometabolic diseases.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Acetylation
  • Angiotensin II / metabolism*
  • Angiotensin II / pharmacology
  • Animals
  • Aorta, Thoracic / cytology
  • Cardiovascular Diseases / metabolism*
  • Cardiovascular Diseases / pathology
  • Catalase / genetics
  • Catalase / metabolism*
  • Cells, Cultured
  • Down-Regulation / physiology
  • Forkhead Transcription Factors / metabolism
  • Hypertrophy
  • Luciferases / genetics
  • Male
  • Muscle, Smooth, Vascular / enzymology*
  • Muscle, Smooth, Vascular / pathology
  • Nerve Tissue Proteins / metabolism
  • Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha
  • Phosphorylation / drug effects
  • Phosphorylation / physiology
  • Promoter Regions, Genetic / physiology
  • Protein Processing, Post-Translational / physiology
  • Proto-Oncogene Proteins c-akt / metabolism
  • RNA-Binding Proteins / genetics
  • RNA-Binding Proteins / metabolism*
  • Rats
  • Rats, Sprague-Dawley
  • Serine / metabolism
  • Transcription Factors / genetics
  • Transcription Factors / metabolism*
  • Transcriptional Activation / drug effects
  • Transcriptional Activation / physiology
  • p300-CBP Transcription Factors / metabolism*

Substances

  • Forkhead Transcription Factors
  • Nerve Tissue Proteins
  • Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha
  • Ppargc1a protein, rat
  • RNA-Binding Proteins
  • Transcription Factors
  • Angiotensin II
  • Foxo1 protein, rat
  • Serine
  • Catalase
  • Luciferases
  • p300-CBP Transcription Factors
  • p300-CBP-associated factor
  • Proto-Oncogene Proteins c-akt