Modulation of stretch-induced myocyte remodeling and gene expression by nitric oxide: a novel role for lipoma preferred partner in myofibrillogenesis

Am J Physiol Heart Circ Physiol. 2013 May 15;304(10):H1302-13. doi: 10.1152/ajpheart.00004.2013. Epub 2013 Mar 15.

Abstract

Prolonged hemodynamic load as a result of hypertension eventually leads to maladaptive cardiac adaptation and heart failure. The signaling pathways that underlie these changes are still poorly understood. The adaptive response to mechanical load is mediated by mechanosensors that convert the mechanical stimuli into a biological response. We examined the effect of cyclic mechanical stretch on myocyte adaptation using neonatal rat ventricular myocytes with 10% (adaptive) or 20% (maladaptive) maximum strain at 1 Hz for 48 h to mimic in vivo mechanical stress. Cells were also treated with and without nitro-L-arginine methyl ester (L-NAME), a general nitric oxide synthase (NOS) inhibitor to suppress NO production. Maladaptive 20% mechanical stretch led to a significant loss of intact sarcomeres that were rescued by L-NAME (P < 0.05; n ≥ 5 cultures). We hypothesized that the mechanism was through NO-induced alteration of myocyte gene expression. L-NAME upregulated the mechanosensing proteins muscle LIM protein (MLP; by 100%; P < 0.05; n = 5 cultures) and lipoma preferred partner (LPP), a novel cardiac protein (by 80%; P < 0.05; n = 4 cultures). L-NAME also significantly altered the subcellular localization of LPP and MLP in a manner that favored growth and adaptation. These findings suggest that NO participates in stretch-mediated adaptation. The use of isoform selective NOS inhibitors indicated a complex interaction between inducible NOS and neuronal NOS isoforms regulate gene expression. LPP knockdown by small intefering RNA led to formation of α-actinin aggregates and Z bodies showing that myofibrillogenesis was impaired. There was an upregulation of E3 ubiquitin ligase (MUL1) by 75% (P < 0.05; n = 5 cultures). This indicates that NO contributes to stretch-mediated adaptation via the upregulation of proteins associated with mechansensing and myofibrillogenesis, thereby presenting potential therapeutic targets during the progression of heart failure.

Keywords: heart; heart failure; hypertrophy; mechanotransduction; stretch.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actinin / metabolism
  • Actinin / physiology
  • Animals
  • Blotting, Western
  • Cells, Cultured
  • Enzyme Inhibitors / pharmacology
  • Gene Expression / drug effects
  • Gene Expression / genetics
  • Gene Expression / physiology*
  • Image Processing, Computer-Assisted
  • Immunohistochemistry
  • LIM Domain Proteins / physiology*
  • Microfilament Proteins / genetics
  • Microfilament Proteins / physiology*
  • Muscle Development / drug effects
  • Muscle Development / genetics
  • Muscle Development / physiology*
  • Myocytes, Cardiac / physiology*
  • NG-Nitroarginine Methyl Ester / pharmacology
  • Nitric Oxide / physiology*
  • Nitric Oxide Synthase / antagonists & inhibitors
  • Nitric Oxide Synthase / metabolism
  • Oncogene Proteins / genetics
  • Oncogene Proteins / physiology*
  • RNA, Small Interfering / genetics
  • Rats
  • Rats, Sprague-Dawley
  • Sarcomeres / physiology
  • Subcellular Fractions / metabolism
  • Ubiquitin-Protein Ligases / metabolism
  • Ubiquitin-Protein Ligases / physiology

Substances

  • Enzyme Inhibitors
  • LIM Domain Proteins
  • Lpp protein, rat
  • Microfilament Proteins
  • Oncogene Proteins
  • RNA, Small Interfering
  • Actinin
  • Nitric Oxide
  • Nitric Oxide Synthase
  • Ubiquitin-Protein Ligases
  • NG-Nitroarginine Methyl Ester