H11 kinase/heat shock protein 22 deletion impairs both nuclear and mitochondrial functions of STAT3 and accelerates the transition into heart failure on cardiac overload

Circulation. 2011 Jul 26;124(4):406-15. doi: 10.1161/CIRCULATIONAHA.110.013847. Epub 2011 Jul 11.

Abstract

Background: Cardiac overload, a major cause of heart failure, induces the expression of the heat shock protein H11 kinase/Hsp22 (Hsp22).

Methods and results: To determine the specific function of Hsp22 in that context, a knockout mouse model of Hsp22 deletion was generated. Although comparable to wild-type mice in basal conditions, knockout mice exposed to pressure overload developed less hypertrophy and showed ventricular dilation, impaired contractile function, increased myocyte length and accumulation of interstitial collagen, faster transition into heart failure, and increased mortality. Microarrays revealed that hearts from knockout mice failed to transactivate genes regulated by the transcription factor STAT3. Accordingly, nuclear STAT3 tyrosine phosphorylation was decreased in knockout mice. Silencing and overexpression experiments in isolated neonatal rat cardiomyocytes showed that Hsp22 activates STAT3 via production of interleukin-6 by the transcription factor nuclear factor-κB. In addition to its transcriptional function, STAT3 translocates to the mitochondria where it increases oxidative phosphorylation. Both mitochondrial STAT3 translocation and respiration were also significantly decreased in knockout mice.

Conclusions: This study found that Hsp22 represents a previously undescribed activator of both nuclear and mitochondrial functions of STAT3, and its deletion in the context of pressure overload in vivo accelerates the transition into heart failure and increases mortality.

Publication types

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

MeSH terms

  • Animals
  • Cardiomegaly / enzymology
  • Cardiomegaly / genetics
  • Cell Nucleus / enzymology
  • Cell Nucleus / genetics
  • Cells, Cultured
  • Collagen / metabolism
  • Gene Deletion*
  • Gene Expression Profiling
  • HSP20 Heat-Shock Proteins / genetics*
  • Heart Failure / enzymology
  • Heart Failure / genetics*
  • Heart Failure / mortality
  • Heat-Shock Proteins
  • Interleukin-6 / biosynthesis
  • Male
  • Mice
  • Mice, Knockout
  • Mitochondria, Heart / enzymology
  • Mitochondria, Heart / genetics*
  • Molecular Chaperones
  • Muscle Proteins / genetics*
  • Myocytes, Cardiac / enzymology
  • NF-kappa B / metabolism
  • Oxidative Phosphorylation
  • Rats
  • STAT3 Transcription Factor / genetics*

Substances

  • HSP20 Heat-Shock Proteins
  • Heat-Shock Proteins
  • Hspb8 protein, mouse
  • Interleukin-6
  • Molecular Chaperones
  • Muscle Proteins
  • NF-kappa B
  • STAT3 Transcription Factor
  • Stat3 protein, mouse
  • Collagen