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The Use of EPR Spectroscopy for the Identification of the Nature of Endothelium-Derived Relaxing Factor

  • Yann A. Henry

Abstract

The discovery by Furchgott and Zawadzki in 19801 of an obligatory entity derived from endothelial cells necessary for the relaxation of underlying arterial smooth muscle by acetylcholine was followed by the hypothesis made simultaneously by Furchgott and by Ignarro in 1986 that the endothelium-derived relaxing factor (EDRF) was in fact NO.2–5 This was immediately confirmed by Ignarro and Moncada’s groups,6–9 explaining the prime functional importance of the stimulation of guanylate cyclase by NO, earlier discovered by Murad et al and Ignarro et al.10–12 Vanhoutte questioned whether it was the end of the quest for EDRF.13 Read this thrilling part of scientific history recently related by Furchgott!14

Keywords

Nitric Oxide Nitric Oxide Guanylate Cyclase Dinitrosyl Iron Dinitrosyl Iron Complex 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. 1.
    Furchgott RF, Zawadzki JV. The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature 1980; 288:373–376.PubMedCrossRefGoogle Scholar
  2. 2.
    Furchgott RF. Studies on relaxation of rabbit aorta by sodium nitrite: the basis for the proposal that the acid-activatable inhibitory factor from bovine retractor penis is inorganic nitrite and the endothelial-derived relaxing factor is nitric oxide. In: Vanhoutte PM, ed. Vasodilatation: Vascular Smooth Muscle, Peptides, Autonomic Nerves, and Endothelium. New York, Raven Press, 1988:401–414.Google Scholar
  3. 3.
    Khan MT, Furchgott RF. Additional evidence that endothelium-derived relaxing factor is nitric oxide. In: Rand MJ, Raper C, eds. Pharmacology. Amsterdam, Elsevier, 1987:341–344.Google Scholar
  4. 4.
    Ignarro LJ, Wood KS, Byrns RE. Pharmacological and biochemical properties of endothelium-derived relaxing factor (EDRF): evidence that EDRF is closely related to nitric oxide (NO) radical. Circulation 1986; 74:II–287 (Abstr).Google Scholar
  5. 5.
    Ignarro LJ, Byrns RE, Wood KS. Biochemical and pharmacological properties of endothelium-derived relaxing factor and its similarity to nitric oxide radical. In: Vanhoutte PM, ed. Vasodilatation: Vascular Smooth Muscle, Peptides, Autonomic Nerves, and Endothelium. New York, Raven Press, 1988:427–435.Google Scholar
  6. 6.
    Ignarro LJ, Buga GM, Wood KS et al. Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide. Proc Natl Acad Sci USA 1987; 84:9265–9269.PubMedCrossRefGoogle Scholar
  7. 7.
    Palmer RMJ, Ferrige AG, Moncada S. Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature 1987; 327:524–526.PubMedCrossRefGoogle Scholar
  8. 8.
    Radomski MW, Palmer RMJ, Moncada S. The role of nitric oxide and cGMP in platelets adhesion to vascular endothelium. Biochem Biophys Res Commun 1987; 148:1482–1489.PubMedCrossRefGoogle Scholar
  9. 9.
    Moncada S, Radomski MW, Palmer RMJ. Endothelium-derived relaxing factor. Identification as nitric oxide and role in the control of vascular tone and platelet function. Biochem Pharmacol 1988; 37:2495–2501.PubMedCrossRefGoogle Scholar
  10. 10.
    Arnold WP, Mittal CK, Katsuki S et al. Nitric oxide activates guanylate cyclase and increases guanosine3′:5′-cyclic monophosphate levels in various tissue preparations. Proc Natl Acad Sci USA 1977; 74:3203–3207.PubMedCrossRefGoogle Scholar
  11. 11.
    Murad F, Mittal CK, Arnold WP et al. Guanylate cyclase: activation by azide, nitro compounds, nitric oxide, and hydroxyl radical and inhibition by hemoglobin and myoglobin. Adv Cyclic Nucleotide Res 1978; 9:145–158.PubMedGoogle Scholar
  12. 12.
    Gruetter CA, Barry BK, McNamara DB et al. Relaxation of bovine coronary artery and activation of coronary arterial guanylate cyclase by nitric oxide, nitroprusside and a carcinogenic nitrosoamine. J Cyclic Nucleotide Res 1979; 5:211–224.PubMedGoogle Scholar
  13. 13.
    Vanhoutte PM. The end of the quest? Nature 1987; 327:459–460.PubMedCrossRefGoogle Scholar
  14. 14.
    Furchgott RF. A research trail over half a century. Annu Rev Pharmacol Toxicol 1995; 35:1–27.PubMedCrossRefGoogle Scholar
  15. 15.
    Palmer RMJ, Rees DD, Ashton DS et al. L-arginine is the physiological precursor for the formation of nitric oxide in endothelium dependent relaxation. Biochem Biophys Res Commun 1988; 153:1251–1256.PubMedCrossRefGoogle Scholar
  16. 16.
    Schmidt HHHW, Nau H, Wittfoht W et al. Arginine is a physiological precursor of endothelium-derived nitric oxide. Eur J Pharmacol 1988; 154:213–216.PubMedCrossRefGoogle Scholar
  17. 17.
    Hibbs JB, Taintor RR, Vavrin Z. Macrophage cytotoxicity: role for L-arginine deiminase and imino nitrogen oxidation to nitrite. Science 1987; 235:473–476.PubMedCrossRefGoogle Scholar
  18. 18.
    Hibbs JB, Vavrin Z, Taintor RR. L-arginine is required for expression of the activated macrophage effector mechanism causing selective metabolic inhibition in target cells. J Immunol 1987; 138:550–565.PubMedGoogle Scholar
  19. 19.
    Stuehr DJ, Marietta MA. Mammalian nitrate biosynthesis: mouse macrophages produce nitrite and nitrate in response to Escherichia coli lipopolysaccharide. Proc Natl Acad Sci USA 1985; 82:7738–7742.CrossRefGoogle Scholar
  20. 20.
    Stuehr DJ, Marietta MA. Induction of nitrite/nitrate synthesis in murine macrophages by BCG infection, lymphokines, or interferon-γ. J Immunol 1987; 139:518–525.PubMedGoogle Scholar
  21. 21.
    Iyengar R, Stuehr DJ, Marietta MA. Macrophage synthesis of nitrite, nitrate, and N-nitrosamines: precursors and role of the respiratoty burst. Proc Natl Acad Sci USA 1987; 84:6369–6373.PubMedCrossRefGoogle Scholar
  22. 22.
    Marietta MA. Mammalian synthesis of nitrite, nitrate, nitric oxide, and N-nitrosating agents. Chem Res Toxicol 1988; 1:249–257.CrossRefGoogle Scholar
  23. 23.
    Marietta MA, Yoon PS, Iyengar R et al. Macrophage oxidation of L-arginine to nitrite and nitrate: nitric oxide is an intermediate. Biochemistry 1988; 27:8706–8711.CrossRefGoogle Scholar
  24. 24.
    Stuehr DJ, Nathan CF. Nitric oxide. A macrophage product responsible for cytos-tasis and respiratory inhibition in tumor target cells. J Exp Med 1989; 169:1543–1555.PubMedCrossRefGoogle Scholar
  25. 25.
    Stuehr DJ, Gross SS, Sakuma I et al. Activated murine macrophages secrete a metabolite of arginine with the bioactivity of endothelium-derived relaxing factor and the chemical reactivity of nitric oxide. J Exp Med 1989; 169:1011–1020.PubMedCrossRefGoogle Scholar
  26. 26.
    Garthwaite J, Charles SL, Chess-Williams R. Endothelium-derived relaxing factor release on activation of NMDA receptors suggests role as intercellular messenger in the brain. Nature 1988; 336:385–388.PubMedCrossRefGoogle Scholar
  27. 27.
    Furchgott RF, Vanhoutte PM. Endothelium-derived relaxing and contracting factors. FASEB J 1989; 3:2007–2018.PubMedGoogle Scholar
  28. 28.
    Keim M, Feelisch M, Spahr R et al. Quantitative and kinetic characterisation of nitric oxide and EDRF released from cultured endothelial cells. Biochem Biophys Res Commun 1988; 154:236–244.CrossRefGoogle Scholar
  29. 29.
    Keim M, Schräder J. Control of coronary vascular tone by nitric oxide. Circ Res 1990; 66:1561–1575.Google Scholar
  30. 30.
    Feelisch M, te Poel M, Zamora R et al. Understanding the controversy over the identity of EDRF. Nature 1994; 368:62–65.PubMedCrossRefGoogle Scholar
  31. 31.
    Vanin AF. Endothelium-derived relaxing factor is a nitrosyl iron complex with thiol ligands. FEBS Lett 1991; 289:1–3.PubMedCrossRefGoogle Scholar
  32. 32.
    Mülsch A, Mordvintcev P, Vanin AF et al. The potent vasodilating and guanylyl cyclase activating dinitrosyl-iron(II) complex is stored in a protein-bound form in vascular tissue and is released by thiols. FEBS Lett 1991; 294:252–256.PubMedCrossRefGoogle Scholar
  33. 33.
    Vedernikov YP, Mordvintcev PI, Malenkova IV et al. Similarity between the vasorelaxing activity of dinitrosyl iron cysteine complexes and endothelium-derived relaxing factor. Eur J Pharmacol 1992; 211:313–317.PubMedCrossRefGoogle Scholar
  34. 34.
    Rubanyi GM, Johns A, Harrison D et al. Evidence that endothelium-derived relaxing factor may be identical with an S-nitro-sothiol and not with free nitric oxide. Circulation 1988; 80 (Suppl II):Abstr II–281.Google Scholar
  35. 35.
    Myers PR, Minor RL, Guerra R et al. Vasorelaxant properties of the endothelium-derived relaxing factor more closely resemble S-nitrosocysteine than nitric oxide. Nature 1990; 345:161–163.PubMedCrossRefGoogle Scholar
  36. 36.
    Kowaluk E, Fung H-L. Spontaneous liberation of nitric oxide cannot account for in vitro vascular relaxation by S-nitrosothiols. J Pharmacol Exp Ther 1990; 255:1256–1264.PubMedGoogle Scholar
  37. 37.
    Hogg N, Singh RJ, Kalyanaraman B. The role of glutathione in the transport and catabolism of nitric oxide. FEBS Lett 1996; 382:223–228.PubMedCrossRefGoogle Scholar
  38. 38.
    Jia L, Bonaventura C, Bonaventura J et al. S-nitrosohaemoglobin: a dynamic activity of blood involved in vascular control. Nature 1996; 380:221–226.PubMedCrossRefGoogle Scholar
  39. 39.
    Fukuto JM, Chiang K, Hszieh R et al. The pharmacological activity of nitroxyl: a potent vasodilator with activity similar to nitric oxide and/or endothelium-derived relaxing factor. J Pharmacol Exp Ther 1992; 263:546–551.PubMedGoogle Scholar
  40. 40.
    DeMaster EG, Raij L, Archer SL et al. Hydroxylamine is a vasorelaxant and a possible intermediate in the oxidative conversion of L-arginine to nitric oxide. Biochem Biophys Res Commun 1989; 163:527–533.PubMedCrossRefGoogle Scholar
  41. 41.
    Thomas G, Ram well PW. Vascular relaxation mediated by hydroxylamines and oximes: their conversion to nitrites and mechanism of endothelium dependent vascular relaxation. Biochem Biophys Res Commun 1989; 164:889–893.PubMedCrossRefGoogle Scholar
  42. 42.
    Stuehr DJ, Kwon NS, Nathan CF et al. Nω-hydroxy-L-arginine is an intermediate in the biosynthesis of nitric oxide from L-argin-ine. J Biol Chem 1991; 266:6259–6263.PubMedGoogle Scholar
  43. 43.
    Chenais B, Yapo A, Lepoivre M et al. Highperformance liquid chromatographic analysis of the unusual pathway of oxidation of L-arginine to citrulline and nitric oxide in mammalian cells. J Chromatogr 1991; 539:433–441.PubMedCrossRefGoogle Scholar
  44. 44.
    Boucher J-L, Genet A, Vadon S et al. Cytochrome P450 catalyzes the oxidation of Nω-hydroxy-L-arginine by NADPH and O2 to nitric oxide and citrulline. Biochem Biophys Res Commun 1992; 187:880–886.PubMedCrossRefGoogle Scholar
  45. 45.
    Boucher J-L, Chopard C, Vadon S et al. Nitric oxide formation by oxidation of Nω-hydroxy-L-arginine by linoleic acid hydroperoxide catalyzed by soybean lipoxygenase L1. Endothelium 1993; 1:S17.Google Scholar
  46. 46.
    Renaud J-P, Boucher J-L, Vadon S et al. Particular hability of liver P450s3A to catalyze the oxidation of Nω-hydroxy-L-argin-ine to citrulline and nitrogen oxides and occurence in NO synthases of a sequence very similar to the heme-binding sequence in P450s. Biochem Biophys Res Commun 1993; 192:53–60.PubMedCrossRefGoogle Scholar
  47. 47.
    Zembowicz A, Hecker M, Macarthur H et al. Nitric oxide and another potent vasodilator are formed from NG-hydroxy-L-arginine by cultured endothelial cells. Proc Natl Acad Sci USA 1991; 88:11172–11176.PubMedCrossRefGoogle Scholar
  48. 48.
    Zembowicz A, Swierkosz TA, Southan GJ et al. Mechanisms of the endothelium-de-pendent relaxation induced by NG-hydroxy-L-arginine. Cardiovasc Pharmacol 1992; 20:S57–S59.Google Scholar
  49. 49.
    Zembowicz A, Swierkosz TA, Southan GJ et al. Potentiation of the vasorelaxant activity of nitric oxide by hydroxyguanidine: implications for the nature of endothelium-derived relaxing factor. Br J Pharmacol 1992; 107:1001–1007.PubMedGoogle Scholar
  50. 50.
    Zembowicz A, Chlopicki S, Radziszewski W et al. NG-hydroxy-L-arginine and hydroxyguanidine potentiate the biological activity of endothelium-derived relaxing factor released from the rabbit aorta. Biochem Biophys Res Commun 1992; 189:711–716.PubMedCrossRefGoogle Scholar
  51. 51.
    Schott CA, Bogen CM, Vetrovsky P et al. Exogenous NG-hydroxy-L-arginine causes nitrite production in vascular smooth muscle cells in the absence of nitric oxide synthase activity. FEBS Lett 1994; 341:203–207.PubMedCrossRefGoogle Scholar
  52. 52.
    Chenais B, Yapo A, Lepoivre M et al. Nω-hydroxy-L-arginine, a reactional intermediate in nitric oxide biosynthesis, induces cytostasis in human and murine tumor cells. Biochem Biophys Res Commun 1993; 196:1558–1565.PubMedCrossRefGoogle Scholar
  53. 53.
    Schaffner A, Blau N, Schneemann M et al. Tetrahydrobiopterin as another EDRF in man. Biochem Biophys Res Commun 1994; 205:516–523.PubMedCrossRefGoogle Scholar
  54. 54.
    Hecker M, Boese M, Schini-Kerth VB et al. Characterization of the stable L-arginine-derived relaxing factor released from cytok-ine-stimulated vascular smooth muscle cells as an NG-hydroxy-L-arginine-nitric oxide adduct. Proc Natl Acad Sci USA 1995; 92:4671–4675.PubMedCrossRefGoogle Scholar
  55. 55.
    Greenberg SS, Wilcox DE, Rubanyi GM. Endothelium-derived relaxing factor released from canine femoral artery by acethycholine cannot be identified as free nitric oxide by electron paramagnetic resonance spectroscopy. Circ Res 1990; 67:1446–1452.PubMedGoogle Scholar
  56. 56.
    Wennmalm Å, Lanne B, Petersson A-S. Detection of endothelium-derived factor in human plasma in the basal state and following ischemia using electron paramagnetic resonance spectrometry. Anal Biochem 1990; 187:359–363.PubMedCrossRefGoogle Scholar
  57. 57.
    Ignarro LJ. Biosynthesis and metabolism of endothelium-derived nitric oxide. Annu Rev Pharmacol Toxicol 1990; 30:535–560.PubMedCrossRefGoogle Scholar
  58. 58.
    Rosenblum W. Endothelium-derived relaxing factor in brain blood vessels is not nitric oxide. Stroke 1992; 23:1527–1532.PubMedCrossRefGoogle Scholar
  59. 59.
    Busse R, Miilsch A, Fleming I et al. Mechanisms of nitric oxide release from the vascular endothelium. Circulation 1993; 87[suppl V]:V-18-V-25.Google Scholar
  60. 60.
    Zamora Pino R, Feelisch M. Bioassay discrimination between nitric oxide (NO) and nitroxyl (NO) using L-cysteine. Biochem Biophys Res Commun 1994; 201:54–62.CrossRefGoogle Scholar
  61. 61.
    Vanin AF. On the stability of the dinitrosyl-iron-cysteine complex, a candidate for the endothelium-derived relaxation factor. Biochemistry (Moscow) 1995; 60:225–230.Google Scholar
  62. 62.
    Saran M, Michel C, Bors W. Reaction of NO with O2 -. Implications for the action of endothelium-derived relaxing factor (EDRF). Free Rad Res Comms 1990; 10:221–226.CrossRefGoogle Scholar
  63. 63.
    Lancaster JR. Simulation of the diffusion and reaction of endogenously produced nitric oxide. Proc Natl Acad Sci USA 1994; 91:8137–8141.PubMedCrossRefGoogle Scholar
  64. 64.
    Saran M, Bors W. Signalling by O2 -• and NO: how far can either radical, or any specific reaction product, transmit a message under in vivo conditions? Chem-Biol Interact 1994; 90:35–45.PubMedCrossRefGoogle Scholar
  65. 65.
    Wood J, Garthwaite J. Models of the diffu-sional spread of nitric oxide: implications for neural nitric oxide signalling and its pharmacological properties. Neuropharmacol 1994; 33:1235–1244.CrossRefGoogle Scholar
  66. 66.
    Vanderkooi JM, Wright WW, Erecinska M. Nitric oxide diffusion coefficients in solutions, proteins and membranes determined by phosphorescence. Biochim Biophys Acta 1994; 1207:249–254.PubMedCrossRefGoogle Scholar
  67. 67.
    Garthwaite J, Boulton CL. Nitric oxide signaling in the central nervous system. Annu Rev Physiol 1995; 57:683–706.PubMedCrossRefGoogle Scholar
  68. 68.
    Squadrito GL, Pryor WA. The formation of peroxynitrite in vivo from nitric oxide and superoxide. Chem-Biol Interact 1995; 96:203–206.PubMedCrossRefGoogle Scholar
  69. 69.
    Malinski T, Taha Z, Grunfeld S et al. Diffusion of nitric oxide in the aorta wall monitored in situ by porphyrinic microsensors. Biochem Biophys Res Commun 1993; 193:1076–1082.PubMedCrossRefGoogle Scholar
  70. 70.
    Malinski T, Kapturczak M, Dayharsh et al. Nitric oxide synthase activity in genetic hypertension. Biochem Biophys Res Commun 1993; 194:654–658.PubMedCrossRefGoogle Scholar
  71. 71.
    Laurent M, Lepoivre M, Tenu J-P. Kinetic modelling of the nitric oxide gradient generated in vitro by adherent cells expressing inducible nitric oxide synthase. Biochem J 1996; 314:109–113.PubMedGoogle Scholar
  72. 72.
    Vanin AF. Identification of divalent iron complexes with cysteine in biological systems by the EPR method. Biokhimiya 1967; 32:277–282 (English translation 228–232).Google Scholar
  73. 73.
    Vanin AF, Vakhnina LV, Chetverikov AG. Nature of the EPR signals of a new type found in cancer tissues. Biofizika 1970; 15:1044–1051 (English translation 1082–1089).Google Scholar
  74. 74.
    Vithayathil AJ, Ternberg JL, Commoner B. Changes in electron spin resonance signals of rat liver during chemical carcinogenesis. Nature 1965; 207:1246–1249.PubMedCrossRefGoogle Scholar
  75. 75.
    Woolum JC, Tiezzi E, Commoner B. Electron spin resonance of iron-nitric oxide complexes with amino acids, peptides and proteins. Biochim Biophys Acta 1968; 160:311–320.PubMedGoogle Scholar
  76. 76.
    Woolum JC, Commoner B. Isolation and identification of a paramagnetic complex from the livers of carcinogen-treated rats. Biochim Biophys Acta 1970; 201:131–140.PubMedGoogle Scholar
  77. 77.
    Mülsch A, Mordvintcev P, Vanin AF et al. Formation and release of dinitrosyl iron complexes by endothelial cells. Biochem Biophys Res Commun 1993; 196:1303–1308.PubMedCrossRefGoogle Scholar
  78. 78.
    Vanin AF, Mordvintcev PI, Hauschildt S et al. The relationship between L-arginine-dependent nitric oxide synthesis, nitrite release and dinitrosyl-iron complex formation by activated macrophages. Biochim Biophys Acta 1993; 1177:37–42.PubMedCrossRefGoogle Scholar
  79. 79.
    Vanin AF, Malenkova IV, Mordvintcev PI et al. Dinitrosyl iron complexes with thiol-containing ligands and their reversible conversion intro nitrosothiols. Biokhimya 1993; 58:1094–1103 (English Translation 773–779).Google Scholar
  80. 80.
    Drapier J-C, Pellat C, Henry Y. Generation of EPR-detectable nitrosyl-iron complexes in tumor target cells cocultured with activated macrophages. J Biol Chem 1991; 266:10162–10167.PubMedGoogle Scholar
  81. 81.
    Vanin AF, Men’shikov GB, Moroz IA et al. The source of non-heme iron that binds nitric oxide in cultivated macrophages. Biochim Biophys Acta 1992; 1135:275–279.PubMedCrossRefGoogle Scholar
  82. 82.
    Pellat C, Henry Y, Drapier J-C. Detection of nitrosyl-iron complexes in tumor target cells after coculture with activated macrophages. In: Melzer MS, Mantovani A, eds. Cellular and Cytokine Networks in Tissue Immunity. Wiley-Liss, 1991: 229–234.Google Scholar
  83. 83.
    Drapier J-C, Pellat C, Henry Y. Characterization of the nitrosyl-iron complexes generated in tumour cells after co-culture with activated macrophages. In: Moncada S, Marietta MA, Hibbs JB et al, eds. The Biology of Nitric Oxide. London, UK: Portland Press, 1992: 72–76.Google Scholar
  84. 84.
    McAninly J, Williams DLH, Askew SC et al. Metal ion catalysis in nitrosothiols (RSNO) decomposition. J Chem Soc Chem Commun 1993:1758–1759.Google Scholar
  85. 85.
    Askew SC, Barnett DJ, McAninly J et al. Catalysis by Cu2+ of nitric oxide release from S-nitrosothiols (RSNO). J Chem Soc Perkin Trans 2 1995:741–745.Google Scholar
  86. 86.
    Misra HP, Sata T, Kubota E et al. ESR spectroscopic studies of endothelial-depen-dent relaxation factor in guinea pig pulmonary artery. J Vascul Med Biol 1989; 1:189 (Abstr).Google Scholar
  87. 87.
    Forray C, Arroyo CM, El-Fakahany E et al. L-arginine related spin adducts generated during muscarinic receptor-mediated activation of guanylate cyclase. Arch Int Pharm Ther 1990; 305:Abs 42, 245.Google Scholar
  88. 88.
    Arroyo CM, Forray C, El-Fakahany E et al. Receptor-mediated generation of an EDRF-like intermediate in a neuronal cell line detected by spin trapping techniques. Biochem Biophys Res Commun 1990; 170:1177–1183.PubMedCrossRefGoogle Scholar
  89. 89.
    Kanai AJ, Strauss HC, Truskey GA et al. Shear stress induces ATP-dependent transient nitric oxide release from vascular endothelial cells, measured directly with a porphyrinic microsensor. Circ Res 1995; 77:284–293.PubMedGoogle Scholar
  90. 90.
    Malinski T, Tana Z. Nitric oxide release from a single cell measured in situ by a porphyrinic-based microsensor. Nature 1992; 358:676–678.PubMedCrossRefGoogle Scholar
  91. 91.
    Bedioui F, Trévin S, Devynck J. The use of gold electrodes in the electrochemical detection of nitric oxide in aqueous solution. J Electroanal Chem 1994; 377:295–298.CrossRefGoogle Scholar
  92. 92.
    Lantoine F, Trévin S, Bedioui F et al. Selective and sensitive electrochemical measurement of nitric oxide in aqueous solution: discussion and new results. J Electroanal Chem 1995; 392:85–89.CrossRefGoogle Scholar
  93. 93.
    Lantoine F, Brunet A, Bedioui F et al. Direct measurement of nitric oxide production in platelets: relationship with cytosolic Ca2+concentration. Biochem Biophys Res Commun 1995; 215:842–848.PubMedCrossRefGoogle Scholar
  94. 94.
    Cespuglio R, Burlet S, Marinesco S et al. NO voltammetric detection in the rat brain. Variations of the signal throughout the sleep-waking cycle. C R Acad Sci Paris 1996; 319:191–200.PubMedGoogle Scholar
  95. 95.
    Buguet A, Burlet S, Auzelle F et al. Dual intervention of NO in experimental African trypanosomiasis. C R Acad Sci Paris 1996; 319:201–207.PubMedGoogle Scholar
  96. 96.
    Vallance P, Patton S, Bhagat K et al. Direct measurement of nitric oxide in human beings. Lancet 1995; 346:153–154.PubMedCrossRefGoogle Scholar

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  • Yann A. Henry

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