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Molecular Pharmacology

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Research ArticleArticle

Role of S-Nitrosation of Cysteine Residues in Long-Lasting Inhibitory Effect of Nitric Oxide on Arterial Tone

Jacicarlos L. Alencar, Irina Lobysheva, Michel Geffard, Mamadou Sarr, Christa Schott, Valérie B. Schini-Kerth, Françoise Nepveu, Jean-Claude Stoclet and Bernard Muller
Molecular Pharmacology May 2003, 63 (5) 1148-1158; DOI: https://doi.org/10.1124/mol.63.5.1148
Jacicarlos L. Alencar
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Irina Lobysheva
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Michel Geffard
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Mamadou Sarr
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Christa Schott
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Valérie B. Schini-Kerth
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Françoise Nepveu
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Jean-Claude Stoclet
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Bernard Muller
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Abstract

S-Nitrosation of cysteine residues plays an important role in nitric oxide (NO) signaling and transport. The aim of the present study was to investigate the role ofS-nitrosothiols as a storage form of NO, which may account for the long-lasting effects in the vasculature. Rat aorta exposed to S-nitrosoglutathione (GSNO) displayed, even after washout of the drug, a persistent increase in cysteine-NO residues (detected by immunostaining using an antiserum that selectively recognized S-nitrosoproteins) and in NO content (detected by NO spin-trapping), a persistent attenuation of the effect of vasoconstrictors, and a relaxant response upon addition of low molecular weight (LMW) thiols. Rat mesenteric and porcine coronary artery exposed in vitro to GSNO, as well as aorta and mesenteric arteries removed from rats treated in vivo with GSNO, displayed similar modifications of contraction. In isolated aorta exposed to GSNO, the decrease of the contractile response and the relaxant effect of LMW thiols were both blunted by NO scavengers (oxyhemoglobin or 2-(4-carboxyphenyl)-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide) or by a cyclic GMP-dependent protein kinase inhibitor (Rp-8-bromoguanosine-3′,5′-cyclic monophosphorothioate). In these arteries, mercuric chloride (which cleaves the cysteine-NO bond) exerted a transient relaxation, completely abolished the one of LMW thiols, and blunted the increase in cysteine-NO residues and NO content. Together, these data support the idea thatS-nitrosation of cysteine residues is involved in long-lasting effects of NO on arterial tone. They suggest thatS-nitrosation of tissue thiols is a mechanism of formation of local NO stores from which biologically active NO can subsequently be released.

Footnotes

  • This work was partially supported by a grant from Fondation de France. J.L.A. is the recipient of a fellowship from CAPES-Brazil and IL (visitor scientist from Institute of Chemical Physics, Russian Academy of Science, Moscow) from ARC.

  • Abbreviations:
    NO
    nitric oxide
    NOS
    nitric-oxide synthase
    LMW
    low molecular weight
    GSNO
    S-nitrosoglutathione
    NAC
    N-acetylcysteine
    DETC
    diethyldithiocarbamate
    PBS
    phosphate-buffered saline
    EPR
    electron paramagnetic resonance
    NE
    norepinephrine
    PHE
    phenylephrine
    p-HMBA
    para-hydroxymercuribenzoic acid
    p-CMPS
    para-chloromercuriphenylsulfonic acid
    ELISA
    enzyme-linked immunosorbent assay
    BSA
    bovine serum albumin
    g-BSA
    glutaraldehyde-conjugated bovine serum albumin
    U46619
    U46619, 9,11-dideoxy-11α,9α-epoxymethanoprostaglandin
    oxyHb
    oxyhemoglobin
    carboxy-PTIO
    2-(4-carboxyphenyl)-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide
    MANOVA
    multivariate analysis of variance
    ANOVA
    analysis of variance
    Rp-8-Br-cGMPS
    Rp-8-bromoguanosine 3′,5′-cyclic monophosphorothioate
    SOD
    superoxide dismutase
    • Received November 4, 2002.
    • Accepted February 7, 2002.
  • The American Society for Pharmacology and Experimental Therapeutics
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Molecular Pharmacology: 63 (5)
Molecular Pharmacology
Vol. 63, Issue 5
1 May 2003
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Research ArticleArticle

Role of S-Nitrosation of Cysteine Residues in Long-Lasting Inhibitory Effect of Nitric Oxide on Arterial Tone

Jacicarlos L. Alencar, Irina Lobysheva, Michel Geffard, Mamadou Sarr, Christa Schott, Valérie B. Schini-Kerth, Françoise Nepveu, Jean-Claude Stoclet and Bernard Muller
Molecular Pharmacology May 1, 2003, 63 (5) 1148-1158; DOI: https://doi.org/10.1124/mol.63.5.1148

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Research ArticleArticle

Role of S-Nitrosation of Cysteine Residues in Long-Lasting Inhibitory Effect of Nitric Oxide on Arterial Tone

Jacicarlos L. Alencar, Irina Lobysheva, Michel Geffard, Mamadou Sarr, Christa Schott, Valérie B. Schini-Kerth, Françoise Nepveu, Jean-Claude Stoclet and Bernard Muller
Molecular Pharmacology May 1, 2003, 63 (5) 1148-1158; DOI: https://doi.org/10.1124/mol.63.5.1148
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