Deficiency of neuronal nitric oxide synthase increases mortality and cardiac remodeling after myocardial infarction: role of nitroso-redox equilibrium

Circulation. 2005 Nov 29;112(22):3415-22. doi: 10.1161/CIRCULATIONAHA.105.557892. Epub 2005 Nov 21.

Abstract

Background: Neuronal nitric oxide synthase (NOS1) plays key cardiac physiological roles, regulating excitation-contraction coupling and exerting an antioxidant effect that maintains tissue NO-redox equilibrium. After myocardial infarction (MI), NOS1 translocates from the sarcoplasmic reticulum to the cell membrane, where it inhibits beta-adrenergic contractility, an effect previously predicted to have adverse consequences. Counter to this idea, we tested the hypothesis that NOS1 has a protective effect after MI.

Methods and results: We studied mortality, cardiac remodeling, and upregulation of oxidative stress pathways after MI in NOS1-deficient (NOS1(-/-)) and wild-type C57BL6 (WT) mice. Compared with WT, NOS1(-/-) mice had greater mortality (hazard ratio, 2.06; P=0.036), worse left ventricular (LV) fractional shortening (19.7+/-1.5% versus 27.2+/-1.5%, P<0.05), higher LV diastolic diameter (5.5+/-0.2 versus 4.9+/-0.1 mm, P<0.05), greater residual cellular width (14.9+/-0.5 versus 12.8+/-0.5 microm, P<0.01), and equivalent beta-adrenergic hyporesponsiveness despite similar MI size. Superoxide production increased after MI in both NOS1(-/-) and WT animals, although NO increased only in WT. NADPH oxidase (P<0.05) activity increased transiently in both groups after MI, but NOS1(-/-) mice had persistent basal and post-MI elevations in xanthine oxidoreductase activity.

Conclusions: Together these findings support a protective role for intact NOS1 activity in the heart after MI, despite a potential contribution to LV dysfunction through beta-adrenergic hyporesponsiveness. NOS1 deficiency contributes to an imbalance between oxidative stress and tissue NO signaling, providing a plausible mechanism for adverse consequences of NOS1 deficiency in states of myocardial injury.

Publication types

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

MeSH terms

  • Animals
  • Cardiomegaly / enzymology*
  • Cardiomegaly / etiology
  • Cardiomegaly / mortality
  • Homeostasis
  • Mice
  • Mice, Knockout
  • Mortality
  • Myocardial Infarction / complications*
  • Myocardial Infarction / mortality*
  • NADPH Oxidases / metabolism
  • Nitric Oxide / metabolism
  • Nitric Oxide Synthase Type I / deficiency*
  • Nitric Oxide Synthase Type I / physiology
  • Oxidation-Reduction
  • Oxidative Stress
  • Superoxides / metabolism
  • Ventricular Dysfunction, Left / etiology

Substances

  • Superoxides
  • Nitric Oxide
  • Nitric Oxide Synthase Type I
  • NADPH Oxidases