Crosstalk between AMPK activation and angiotensin II-induced hypertrophy in cardiomyocytes: the role of mitochondria

J Cell Mol Med. 2014 Apr;18(4):709-20. doi: 10.1111/jcmm.12220. Epub 2014 Jan 20.

Abstract

AMP-kinase (AMPK) activation reduces cardiac hypertrophy, although underlying molecular mechanisms remain unclear. In this study, we elucidated the anti-hypertrophic action of metformin, specifically, the role of the AMPK/eNOS/p53 pathway. H9c2 rat cardiomyocytes were treated with angiotensin II (AngII) for 24 hrs in the presence or absence of metformin (AMPK agonist), losartan [AngII type 1 receptor (AT1R) blocker], Nω-nitro-L-arginine methyl ester (L-NAME, pan-NOS inhibitor), splitomicin (SIRT1 inhibitor) or pifithrin-α (p53 inhibitor). Results showed that treatment with metformin significantly attenuated AngII-induced cell hypertrophy and death. Metformin attenuated AngII-induced activation (cleavage) of caspase 3, Bcl-2 down-regulation and p53 up-regulation. It also reduced AngII-induced AT1R up-regulation by 30% (P < 0.05) and enhanced AMPK phosphorylation by 99% (P < 0.01) and P-eNOS levels by 3.3-fold (P < 0.01). Likewise, losartan reduced AT1R up-regulation and enhanced AMPK phosphorylation by 54% (P < 0.05). The AMPK inhibitor, compound C, prevented AT1R down-regulation, indicating that metformin mediated its effects via AMPK activation. Beneficial effects of metformin and losartan converged on mitochondria that demonstrated high membrane potential (Δψm ) and low permeability transition pore opening. Thus, this study demonstrates that the anti-hypertrophic effects of metformin are associated with AMPK-induced AT1R down-regulation and prevention of mitochondrial dysfunction through the SIRT1/eNOS/p53 pathway.

Keywords: AMP kinase; angiotensin II receptors; hypertrophy; metformin; mitochondria.

Publication types

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

MeSH terms

  • AMP-Activated Protein Kinases / biosynthesis
  • AMP-Activated Protein Kinases / metabolism*
  • Angiotensin II / administration & dosage*
  • Angiotensin II Type 1 Receptor Blockers / administration & dosage
  • Animals
  • Cardiomegaly / drug therapy
  • Cardiomegaly / metabolism*
  • Cardiomegaly / pathology
  • Gene Expression Regulation / drug effects
  • Losartan / administration & dosage
  • Metformin / administration & dosage
  • Mitochondria / drug effects
  • Mitochondria / metabolism*
  • Mitochondria / pathology
  • Myocytes, Cardiac / drug effects
  • Myocytes, Cardiac / metabolism*
  • Myocytes, Cardiac / pathology
  • Nitric Oxide Synthase Type III / metabolism
  • Rats
  • Receptor, Angiotensin, Type 1 / biosynthesis
  • Signal Transduction
  • Sirtuin 1 / metabolism
  • Tumor Suppressor Protein p53 / metabolism

Substances

  • Angiotensin II Type 1 Receptor Blockers
  • Receptor, Angiotensin, Type 1
  • Tumor Suppressor Protein p53
  • Angiotensin II
  • Metformin
  • Nitric Oxide Synthase Type III
  • Nos3 protein, rat
  • AMP-Activated Protein Kinases
  • Sirt1 protein, rat
  • Sirtuin 1
  • Losartan