Angiotensin II inhibits neuronal nitric oxide synthase activation through the ERK1/2-RSK signaling pathway to modulate central control of blood pressure

Circ Res. 2010 Mar 5;106(4):788-95. doi: 10.1161/CIRCRESAHA.109.208439. Epub 2010 Jan 7.

Abstract

Rationale: Angiotensin (Ang) II exerts diverse physiological actions in both the peripheral and central neural systems. It was reported that the activity of Ang II is higher in the nucleus tractus solitarii (NTS) of spontaneously hypertensive rats (SHRs) and that angiotensin type-1 receptors are colocalized with NAD(P)H oxidase in the neurons of the NTS, resulting in the induction of local reactive oxygen species production by Ang II. However, the signaling mechanisms of Ang II that induce hypertension remain unclear.

Objective: The aim of this study was to investigate the possible signaling pathways involved in Ang II-mediated blood pressure regulation in the NTS.

Methods and results: Male SHRs were treated with losartan or tempol for 2 weeks, after which systolic blood pressure was observed to decrease significantly. Dihydroethidium staining showed many cells with high reactive oxygen species in the NTS of SHRs. The addition of losartan or tempol decreased the numbers of reactive oxygen species-positive cells in the NTS. The systemic administration of losartan or tempol reduced the systolic blood pressure and increased NO production. Immunoblotting and immunohistochemical analysis further showed that inhibition of Ang II activity by losartan or tempol significantly increased the expression extracellular signal-regulated kinase (ERK)1/2, ribosomal protein S6 kinase (RSK), and also increased neuronal NO synthase (nNOS) phosphorylation. RSK was also found to bind directly to nNOS and induce phosphorylation at the Ser1416 position.

Conclusions: Taken together, these results suggest that the ERK1/2-RSK-nNOS signaling pathway may play a significant role in Ang II-mediated central blood pressure regulation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Angiotensin II / metabolism*
  • Angiotensin II Type 1 Receptor Blockers / pharmacology
  • Animals
  • Antihypertensive Agents / pharmacology
  • Antioxidants / pharmacology
  • Blood Pressure* / drug effects
  • Cyclic N-Oxides / pharmacology
  • Disease Models, Animal
  • Enzyme Activation
  • Flavonoids / pharmacology
  • Hypertension / drug therapy
  • Hypertension / enzymology*
  • Hypertension / physiopathology
  • Losartan / pharmacology
  • Male
  • Mitogen-Activated Protein Kinase 1 / antagonists & inhibitors
  • Mitogen-Activated Protein Kinase 1 / metabolism*
  • Mitogen-Activated Protein Kinase 3 / antagonists & inhibitors
  • Mitogen-Activated Protein Kinase 3 / metabolism*
  • Nitric Oxide / metabolism
  • Nitric Oxide Synthase / metabolism*
  • Nitric Oxide Synthase Type I
  • Oxidative Stress
  • Phosphorylation
  • Protein Kinase Inhibitors / pharmacology
  • Rats
  • Rats, Inbred SHR
  • Reactive Oxygen Species / metabolism
  • Ribosomal Protein S6 Kinases / metabolism*
  • Signal Transduction
  • Solitary Nucleus / drug effects
  • Solitary Nucleus / enzymology*
  • Spin Labels
  • Time Factors

Substances

  • Angiotensin II Type 1 Receptor Blockers
  • Antihypertensive Agents
  • Antioxidants
  • Cyclic N-Oxides
  • Flavonoids
  • Protein Kinase Inhibitors
  • Reactive Oxygen Species
  • Spin Labels
  • Angiotensin II
  • Nitric Oxide
  • Nitric Oxide Synthase
  • Nitric Oxide Synthase Type I
  • Nos1 protein, rat
  • Ribosomal Protein S6 Kinases
  • Mitogen-Activated Protein Kinase 1
  • Mitogen-Activated Protein Kinase 3
  • Losartan
  • 2-(2-amino-3-methoxyphenyl)-4H-1-benzopyran-4-one
  • tempol