Angiotensin II Induces Skeletal Muscle Atrophy by Activating TFEB-Mediated MuRF1 Expression

Circ Res. 2015 Aug 14;117(5):424-36. doi: 10.1161/CIRCRESAHA.114.305393. Epub 2015 Jul 2.

Abstract

Rationale: Skeletal muscle wasting with accompanying cachexia is a life threatening complication in congestive heart failure. The molecular mechanisms are imperfectly understood, although an activated renin-angiotensin aldosterone system has been implicated. Angiotensin (Ang) II induces skeletal muscle atrophy in part by increased muscle-enriched E3 ubiquitin ligase muscle RING-finger-1 (MuRF1) expression, which may involve protein kinase D1 (PKD1).

Objective: To elucidate the molecular mechanism of Ang II-induced skeletal muscle wasting.

Methods and results: A cDNA expression screen identified the lysosomal hydrolase-coordinating transcription factor EB (TFEB) as novel regulator of the human MuRF1 promoter. TFEB played a key role in regulating Ang II-induced skeletal muscle atrophy by transcriptional control of MuRF1 via conserved E-box elements. Inhibiting TFEB with small interfering RNA prevented Ang II-induced MuRF1 expression and atrophy. The histone deacetylase-5 (HDAC5), which was directly bound to and colocalized with TFEB, inhibited TFEB-induced MuRF1 expression. The inhibition of TFEB by HDAC5 was reversed by PKD1, which was associated with HDAC5 and mediated its nuclear export. Mice lacking PKD1 in skeletal myocytes were resistant to Ang II-induced muscle wasting.

Conclusion: We propose that elevated Ang II serum concentrations, as occur in patients with congestive heart failure, could activate the PKD1/HDAC5/TFEB/MuRF1 pathway to induce skeletal muscle wasting.

Keywords: angiotensin II; gene expression regulation; heart failure; histone deacetylase 5; muscle RING-finger-1; protein kinase D; transcription factor EB.

Publication types

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

MeSH terms

  • Angiotensin II / toxicity*
  • Animals
  • Basic Helix-Loop-Helix Leucine Zipper Transcription Factors / physiology*
  • Gene Expression Regulation
  • Humans
  • Mice
  • Mice, Knockout
  • Muscle Proteins / biosynthesis*
  • Muscular Atrophy / chemically induced*
  • Muscular Atrophy / metabolism*
  • Tripartite Motif Proteins
  • Ubiquitin-Protein Ligases / biosynthesis*

Substances

  • Basic Helix-Loop-Helix Leucine Zipper Transcription Factors
  • Muscle Proteins
  • TFEB protein, human
  • Tripartite Motif Proteins
  • Angiotensin II
  • TRIM63 protein, human
  • Ubiquitin-Protein Ligases