Cardiac-specific inhibition of kinase activity in calcium/calmodulin-dependent protein kinase kinase-β leads to accelerated left ventricular remodeling and heart failure after transverse aortic constriction in mice

PLoS One. 2014 Sep 25;9(9):e108201. doi: 10.1371/journal.pone.0108201. eCollection 2014.

Abstract

Background: The mechanism of cardiac energy production against sustained pressure overload remains to be elucidated.

Methods and results: We generated cardiac-specific kinase-dead (kd) calcium/calmodulin-dependent protein kinase kinase-β (CaMKKβ) transgenic (α-MHC CaMKKβkd TG) mice using α-myosin heavy chain (α-MHC) promoter. Although CaMKKβ activity was significantly reduced, these mice had normal cardiac function and morphology at baseline. Here, we show that transverse aortic binding (TAC) in α-MHC CaMKKβkd TG mice led to accelerated death and left ventricular (LV) dilatation and dysfunction, which was accompanied by significant clinical signs of heart failure. CaMKKβ downstream signaling molecules, including adenosine monophosphate-activated protein kinase (AMPK), were also suppressed in α-MHC CaMKKβkd TG mice compared with wild-type (WT) mice. The expression levels of peroxisome proliferator-activated receptor-γ coactivator (PGC)-1α, which is a downstream target of both of CaMKKβ and calcium/calmodulin kinases, were also significantly reduced in α-MHC CaMKKβkd TG mice compared with WT mice after TAC. In accordance with these findings, mitochondrial morphogenesis was damaged and creatine phosphate/β-ATP ratios assessed by magnetic resonance spectroscopy were suppressed in α-MHC CaMKKβkd TG mice compared with WT mice after TAC.

Conclusions: These data indicate that CaMKKβ exerts protective effects on cardiac adaptive energy pooling against pressure-overload possibly through phosphorylation of AMPK and by upregulation of PGC-1α. Thus, CaMKKβ may be a therapeutic target for the treatment of heart failure.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Triphosphate
  • Animals
  • Calcium-Calmodulin-Dependent Protein Kinase Kinase / genetics*
  • Calcium-Calmodulin-Dependent Protein Kinase Kinase / metabolism
  • Disease Models, Animal
  • Gene Expression Regulation
  • Heart Failure / etiology*
  • Heart Failure / metabolism
  • Heart Failure / mortality
  • Heart Failure / physiopathology
  • Heart Ventricles / metabolism
  • Heart Ventricles / pathology
  • Magnetic Resonance Spectroscopy
  • Male
  • Mice
  • Mice, Transgenic
  • Mitochondria, Heart / genetics
  • Mitochondria, Heart / metabolism
  • Myosin Heavy Chains / genetics
  • Phosphorylation
  • Promoter Regions, Genetic
  • Signal Transduction
  • Up-Regulation
  • Ventricular Dysfunction, Left / genetics
  • Ventricular Dysfunction, Left / physiopathology
  • Ventricular Remodeling / genetics*

Substances

  • Myh6 protein, mouse
  • Adenosine Triphosphate
  • Calcium-Calmodulin-Dependent Protein Kinase Kinase
  • Myosin Heavy Chains

Grants and funding

This work was supported in part by the Global COE program “Center for Frontier Medicine” and by a Grant-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology (MEXT) of Japan to K. Ono, K. Hasegawa, T. Kita, and T. Kimura, and in part by the Innovative Techno-Hub for Integrated Medical Bio-imaging of the Project for Developing Innovation Systems, from the Ministry of Education, Culture, Sports, Science and Technology (MEXT) of Japan to M. Narazaki and T. Matsuda. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.