Role of myocardial neuronal nitric oxide synthase-derived nitric oxide in beta-adrenergic hyporesponsiveness after myocardial infarction-induced heart failure in rat

Circulation. 2004 Oct 19;110(16):2368-75. doi: 10.1161/01.CIR.0000145160.04084.AC. Epub 2004 Oct 4.

Abstract

Background: An emerging concept is that a neuronal isoform of nitric oxide synthase (NOS1) may regulate myocardial contractility. However, a role for NOS1-derived nitric oxide (NO) in heart failure (HF) has not been defined.

Methods and results: Using a model of myocardial infarction-induced HF, we demonstrated that cardiac NOS1 expression and activity increased in HF rats (P<0.05 and P<0.001 versus shams, respectively). This was associated with translocation of NOS1 from the ryanodine receptor to the sarcolemma through interactions with caveolin-3 in HF hearts. With ex vivo and in vivo pressure-volume analysis, cardiac NOS1-derived NO was found to be negatively inotropic in shams but not HF hearts. Ventricular elastance (E(es)) was significantly reduced in HF rats (P<0.05), and tau, the time constant of left ventricular relaxation, was prolonged (both P<0.05). Acute NOS1 inhibition significantly increased E(es) by 33+/-3% and tau by 17+/-2% (P<0.05) in shams, although these effects were significantly attenuated in HF hearts. beta-Adrenergic stimulation induced a marked increase in systolic performance in sham hearts, with the responses being significantly blunted in HF hearts. E(es) increased by 163+/-42% (P<0.01) in sham hearts and 56+/-9% in HF hearts, and LV +dP/dt increased by 97+/-9% (P<0.01) in shams and 37+/-7% (P<0.05) in the HF group. Interestingly, preferential NOS1 inhibition enhanced the blunted responses of LV +dP/dt and E(es) to beta-adrenergic stimulation in HF rats but had no effect in shams.

Conclusions: These results provide the first evidence that increased NOS1-derived NO production may play a role in the autocrine regulation of myocardial contractility in HF.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adrenergic beta-Agonists / pharmacology
  • Animals
  • Autocrine Communication
  • Caveolin 3
  • Caveolins / metabolism
  • Dobutamine / pharmacology
  • Enzyme Induction
  • Heart Failure / drug therapy
  • Heart Failure / enzymology*
  • Heart Failure / etiology
  • Isoproterenol / pharmacology
  • Male
  • Myocardial Contraction / drug effects
  • Myocardial Contraction / physiology*
  • Myocardial Infarction / complications*
  • Myocardium / enzymology*
  • Nerve Tissue Proteins / physiology*
  • Nitric Oxide / physiology*
  • Nitric Oxide Synthase / physiology*
  • Nitric Oxide Synthase Type I
  • Rats
  • Rats, Wistar
  • Receptors, Adrenergic, beta / physiology*
  • Ryanodine Receptor Calcium Release Channel / metabolism
  • Sarcolemma / metabolism
  • Ventricular Dysfunction, Left / enzymology
  • Ventricular Dysfunction, Left / etiology

Substances

  • Adrenergic beta-Agonists
  • Cav3 protein, rat
  • Caveolin 3
  • Caveolins
  • Nerve Tissue Proteins
  • Receptors, Adrenergic, beta
  • Ryanodine Receptor Calcium Release Channel
  • Nitric Oxide
  • Dobutamine
  • Nitric Oxide Synthase
  • Nitric Oxide Synthase Type I
  • Nos1 protein, rat
  • Isoproterenol