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Nitric Oxide Derived from Perivascular Nerves and Endothelium

  • Tomio Okamura
  • Noboru Toda
Part of the Nitric Oxide in Biology and Medicine book series (NOBM, volume 1)

Abstract

Endothelium-derived relaxing factor (EDRF) was discovered by Furchgott and Zawadzki (1980), who observed that acetylcholine-induced relaxation of the isolated rabbit aorta was endothelium-dependent and that vascular smooth muscle directly responded to acetylcholine with slight contraction. The discovery brought us the marvelous idea that vascular endothelium influences not only the blood stream but also the smooth muscle cells, thus participating in the regulation of platelet aggregation and adhesion and of vascular tone. In 1988 EDRF was identified as nitric oxide (NO), a highly diffusible and short-lived free radical, synthesized by NO synthase from L-arginine (Palmer et al. 1988a). Specific inhibitors of NO synthase (NOS), introduced by Palmer et al. (1988b), enabled us to clarify the physiological roles of endogenous NO. This lipophilic gas molecule is now recognized to be a new intercellular messenger not only in the circulatory system but also in the central nervous and immune systems.

Keywords

Nitric Oxide Nitric Oxide Cerebral Artery Temporal Artery Cereb Blood Flow 
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. Aisaka K, Gross SS, Griffith OW, & Levi R. 1989. N G-Methylarginine, an inhibitor of endothelium-derived nitric oxide synthesis, is a potent pressor agent in the guinea pig: does nitric oxide regulate blood pressure in vivo? Biochem Biophys Res Commun 160:881–886.PubMedCrossRefGoogle Scholar
  2. Angus JA, & Cocks TM. 1989. Endothelium-derived relaxing factor. Pharmacol Ther 41:303–351.PubMedCrossRefGoogle Scholar
  3. Ayata C, Ma J, Meng W, Huang P, & Moskowitz MA. 1996. L-NA-sensitive rCBF augmentation during vibrissal stimulation in type III nitric oxide synthase mutant mice. J Cereb Blood Flow Metab 16:539–541.PubMedCrossRefGoogle Scholar
  4. Baggia S, Perkins K, & Greenberg B. 1997. Endothelium-dependent relaxation is not unformly impaired in chronic heart failure. J Cardiovasc Pharmacol 29:389–396.PubMedCrossRefGoogle Scholar
  5. Bredt DS, Hwang PM, & Snyder SH. 1990. Localization of nitric oxide synthase indicating a neural role for nitric oxide. Nature 347:768–770.PubMedCrossRefGoogle Scholar
  6. Cases A, Stulak JM, Katusic Z, Villa E, & Romero JC. 1997. Hemodynamic and renal effects of cross-linked hemoglobin infusion. Am J Physiol 272.R793–R799.PubMedGoogle Scholar
  7. Chauhan A, More RS, Mullins PA, Taylor G, Petch C, & Schofield PM. 1996. Aging associated endothelial dysfunction in humans is reversed by L-arginine. J Am Coll Car-diol 28:1796–1804.CrossRefGoogle Scholar
  8. Chu A, Lin CC, Chambers DE, Kuehl WD, Palmer RMJ, Moncada S, & Cobb FR. 1991. Effects of inhibition of nitric oxide formation on basal tone and endothelium-dependent responses of the coronary arteries in awake dogs. J Clin Invest 87:1964–1968.PubMedCrossRefGoogle Scholar
  9. Dijkhorst O, Rabelink TJ, Boer P, & Koomans HA. 1997. Nifedipine attenuates systemic and renal vasoconstriction during nitric oxide inhibition in humans. Hypertension 29:1192–1198.CrossRefGoogle Scholar
  10. Edvinsson L, Muculloch J, & Uddman R. 1981. Immunohistochemical localization and effect upon cat pial arteries in vivo and in situ. J Physiol 318:251–258.PubMedGoogle Scholar
  11. Feletou M, & Vanhoutte PM. 1996. Endothelium-derived hyperpolarizing factor. Clin Exp Pharmacol Physiol 23:1082–1090.PubMedCrossRefGoogle Scholar
  12. Furchgott RF. 1983. Role of endothelium in responses of vascular smooth muscle. Circ Res 53:557–513.PubMedCrossRefGoogle Scholar
  13. Furchgott RF. 1984. The role of endothelium in the responses of vascular smooth muscle to drugs. Annu Rev Pharmacol Toxicol 24:175–197.PubMedCrossRefGoogle Scholar
  14. Furchgott RF, & Zawadzki JV. 1980. The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature 288:373–316.PubMedCrossRefGoogle Scholar
  15. Gardiner SM, Compton AM, Bennett T, Palmer RMJ, & Moncada S. 1990. Control of regional blood flow by endothelium-derived nitric oxide. Hypertension 15:486–492.PubMedCrossRefGoogle Scholar
  16. Gaw AJ, Wadsworth RM, & Humphrey PPA. 1990. Neurotransmission in the sheep middle cerebral artery: modulation of responses by 5-HT and haemolysate. J Cereb Blood Flow Metab 10:409–416.PubMedCrossRefGoogle Scholar
  17. Griffith TM, Edwards DH, Lewis MJ, Newby AC, & Henderson AH. 1984. The nature of endothelium-derived vascular relaxing factor. Nature 329:442–445.CrossRefGoogle Scholar
  18. Haynes WG, Noon JP, Walker BR, & Webb DJ. 1993. Inhibition of nitric oxide synthesis increases blood pressure in healthy humans. J Hypertens 11:1375–1380.PubMedCrossRefGoogle Scholar
  19. Hibbs JB Jr, Taintor RR, & Vavrin Z. 1987. Macrophage cytotoxicity: role for L-arginine deiminase activity and imino nitrogen oxidation to nitrite. Science 235:473–416.PubMedCrossRefGoogle Scholar
  20. Hill C, Lateef AM, Engels K, Samsell L, & Baylis C. 1997. Basal and stimulated nitric oxide in control of kidney function in the aging rat. Am J Physiol, 272:R1747–R1753.PubMedGoogle Scholar
  21. Huang PL, Huang Z, Mashimo H, Bloch KD, Moskowitz MA, Bevan JA, & Fishman MC. 1995. Hypertension in mice lacking the gene for endothelial nitric oxide synthase. Nature 377:239–242.PubMedCrossRefGoogle Scholar
  22. Kawasaki H, Takasaki T, Saito A, & Goto K. 1988. Calcitonin gene-related peptide acts as a novel vasodilator neurotransmitter in mesenteric resistance vessels of the rat. Nature 335:164–167.PubMedCrossRefGoogle Scholar
  23. Klabunde RE, Ritger RC, & Helgren MC. 1991. Cardiovascular actions of inhibitors of endothelium-derived relaxing factor (nitric oxide) formation/release in anesthetized dogs. Eur J Pharmacol 199:51–59.PubMedCrossRefGoogle Scholar
  24. Larsson LI, Edvinsson L, Fahrenkrug J, Hakanson R., Owman C, Schaffalitzky-deMuckadell O, & Sundler F. 1976. Immunohistochemical localization of a vasodilatory polypeptide (VIP) in cerebrovascular nerves. Brain Res 113:400–404.PubMedCrossRefGoogle Scholar
  25. Leckstrom A, Ahlner J, Grundstrom N, & Axelsson KL. 1993. Involvement of nitric oxide and peptides in the inhibitory non-adrenergic, non-cholinergic (NANC) response in bovine mesenteric artery. Pharmacol Toxicol 72:194–198.PubMedCrossRefGoogle Scholar
  26. Lee JJ, Oimos L, & Vanhoutte PM. 1996. Recovery of endothelium-dependent relaxations four weeks after ischemia and progressive reperfusion in canine coronary arteries. Proc AssocAm Physician 108:362–367.Google Scholar
  27. Lee TJ-F, Sarwinski SJ. 1991. Nitric oxidergic vasodilation in the porcine basilar artery. Blood Vessels 28:407–412.PubMedGoogle Scholar
  28. Liu SF, Crawley DE, Rohde JAL, Evans TW, & Barnes PJ. 1992. Role of nitric oxide and guanosine 3’, 5’-cyclic monophosphate in mediating nonadrenergic, noncholinergic relaxation in guinea-pig pulmonary arteries. Br J Pharmacol 107:861–866.PubMedCrossRefGoogle Scholar
  29. Lockette W, Otsuka Y, & Carretero O. 1986. The loss of endothelium-dependent vascular relaxation in hypertension. Hypertension 8(Suppl):II6Ū66.Google Scholar
  30. Moncada S, Palmer RMJ, & Higgs EA. 1991. Nitric oxide: physiology, pathophysiology and pharmacology. Pharmacol Rev 43:109–142.PubMedGoogle Scholar
  31. Montecot C, Borredon J, Seylaz J, & Pinard E. 1997. Nitric oxide of neuronal origin is involved in cerebral blood flow increase during seizures induced by kainate. J Cereb Blood Flow Metab 17:94–99.PubMedCrossRefGoogle Scholar
  32. Okamura T, & Toda N. 1994a. Nitric oxide (NO)-mediated, vasodilator nerve function and its susceptibility to calcium antagonists. J Auton Nerv Sys 49:S55–S58.CrossRefGoogle Scholar
  33. Okamura T, & Toda N. 1994b. Inhibition by calmodulin antagonists of the neurogenic relaxation in cerebral arteries. Eur J Pharmacol 256:79–83.PubMedCrossRefGoogle Scholar
  34. Okamura T, & Toda N. 1994c. Mechanism underlying nicotine-induced relaxation in dog saphenous arteries. Eur J Pharmacol 263:85–91.PubMedCrossRefGoogle Scholar
  35. Okamura T, Inoue S, & Toda N. 1989a. Action of atrial natriuretic peptide (ANP) on dog cerebral arteries: evidence that neurogenic relaxation is not mediated by release of ANP. Br J Pharmacol 97:1258–1264.PubMedCrossRefGoogle Scholar
  36. Okamura T, Minami Y, Toda N. 1989b. Endothelium-dependent and independent mechnisms of action of acetylcholine in monkey and dog isolated arteries. Pharmacology 35:279–288.CrossRefGoogle Scholar
  37. Okamura T, Ayajiki K, & Toda N. 1995. Basilar arterial constriction caused by intracisternal N G-nitro-L-arginine in anesthetized monkeys. Cardiovasc Res 30:663–667.PubMedGoogle Scholar
  38. Okamura T, Ayajiki K, & Toda N. 1996. Neural mechanism of pressor action of nitric oxide synthase inhibition in anesthetized monkeys. Hypertension 28:341–346.PubMedCrossRefGoogle Scholar
  39. Palmer RMJ, Ashton DS, & Moncada S. 1988a. Vascular endothelial cells synthesize nitric oxide from L-arginine. Nature 333:664–666.PubMedCrossRefGoogle Scholar
  40. Palmer RMJ, Rees DD, Ashton DS, & Moncada S. 1988b. L-Arginine is the physiological precursor for the formation of nitric oxide in the endothelium-dependent relaxation. Biochem Biophys Res Commun 153:1251–1256.PubMedCrossRefGoogle Scholar
  41. Possas OS, & Lewis SJ. 1997. NO-containing factors mediate hindlimb vasodilation produced by superior laryngeal nerve stimulation. Am J Physiol 273:H234–H243.PubMedGoogle Scholar
  42. Rees DD, Palmer RMJ, Hodson HF, & Moncada S. 1989a. A specific inhibitor of nitric oxide formation from L-arginine attenuates endothelium-dependent relaxation. Br J Pharmacol 96:418–424.PubMedCrossRefGoogle Scholar
  43. Rees DD, Palmer RMJ, & Moncada S. 1989b. Role of endothelium-derived nitric oxide in the regulation of blood pressure. Proc Natl Acad Sci USA 86:3375–3378.PubMedCrossRefGoogle Scholar
  44. Rees DD, Schulz R, Hodson HF, Palmer RMJ, & Moncada S. 1990. Characterization of three inhibitors of endothelial nitric oxide synthase in vitro and in vivo. Br J Pharmacol 101:746–752.PubMedCrossRefGoogle Scholar
  45. Rubanyi GM, Romero JC, & Vanhoutte PM. 1992. Flow-induced release of endotheliumderived relaxing factor. Am J Physiol 250:H1145–H1149.Google Scholar
  46. Sessa WC, Barber CM, & Lynch KR. 1993. Mutation of N-myristoylation site converts endothelial nitric oxide synthase from a membrane to a cytosolic protein. Circ Res 72i921–924.Google Scholar
  47. Shimokawa H, Yasutake H, Fujii K, Owada MK, Nakaike R, Fukumoto Y, Takayanagi T, Nagao T, Egashira K, Fujishima M, & Takeshita A. 1996. The importance of the hyper-polarizing mechanism increases as the vessel size decreases in endothelium-dependent relaxations in rat mesenteric circulation. J Cardiovasc Pharmacol 28:703–711.PubMedCrossRefGoogle Scholar
  48. Toda N. 1975. Nicotine-induced relaxation in isolated canine cerebral arteries. J Pharmacol ExpTher 193:376–384.Google Scholar
  49. Toda N. 1978. Heterogeneity in the relaxation of vascular smooth muscle. In: Vanhoutte PM, ed. Vasodilatation. Basel: Karger, pp 129–136.Google Scholar
  50. Toda N. 1982. Relaxant responses to transmural stimulation and nicotine of dog and monkey cerebral arteries. Am J Physiol 243:H145–H153.PubMedGoogle Scholar
  51. Toda N. 1988. Hemolysate inhibits cerebral artery relaxation. J Cereb Blood Flow Metab 8:46–53.PubMedCrossRefGoogle Scholar
  52. Toda N. 1993. Mediation by nitric oxide of neurally-induced human cerebral artery relaxation. Experientia 49:51–53.PubMedCrossRefGoogle Scholar
  53. Toda N. 1994. Nitroxidergic innervation in smooth muscle. In: Matsuo Y, Kasuya Y, Tuchiya M, & Nagao F, eds. Gastrointestinal Function; Regulation and Disturbances, Vol 12. Tokyo: Excerpta Medica, pp3–7.Google Scholar
  54. Toda N. 1995. Nitric oxide and regulation of cerebral arterial tone. In: Vincent R, ed. Nitric Oxide in the Nervous System. New York: Academic Press, pp 207–225.CrossRefGoogle Scholar
  55. Toda N, & Okamura T. 1990a. Possible role of nitric oxide in transmitting information from vasodilator nerve to cerebroarterial muscle. Biochem Biophys Res Commun 170:308–313.PubMedCrossRefGoogle Scholar
  56. Toda N, & Okamura T. 1990b. Mechanism underlying the response to vasodilator nerve stimulation in isolated dog and monkey cerebral arteries. Am J Physiol 259: H1511–H1517.PubMedGoogle Scholar
  57. Toda N, & Okamura T. 1991. Suppression by N G-monomethyl-L-arginine of cerebroarteial responses to nonadrenergic, noncholinergic vasodilator nerve stimulation. J Cardiovasc Pharmacol 17 (Suppl 3:S234–S237.CrossRefGoogle Scholar
  58. Toda N, & Okamura T. 1992a. Regulation by nitroxidergic nerve of arterial tone. News Physiol Sci 7:148–152.Google Scholar
  59. Toda N, & Okamura T. 1992b. Different susceptibility of vasodilator nerve, endothelium and smooth muscle functions to Ca++ antagonists in cerebral arteries. J Pharmacol Exp Ther 261:234–239.PubMedGoogle Scholar
  60. Toda N, & Okamura T. 1992c. Mechanism of neurally induced monkey mesenteric artery relaxation and contraction. Hypertension 19:161–166.PubMedCrossRefGoogle Scholar
  61. Toda N, Minami Y, & Okamura T. 1990. Inhibitory effects of L-N G-nitro-arginine on the synthesis of EDRF and the cerebroarterial response to vasodilator nerve stimulation. Life Sci 47:345–351.PubMedCrossRefGoogle Scholar
  62. Toda N, Kawakami M, Yamazaki M, & Okamura T. 1991a. Comparison of endothelium-dependent responses of monkey cerebral and temporal arteries. Br J Pharmacol 102:805–810.PubMedCrossRefGoogle Scholar
  63. Toda N, Kitamura Y, & Okamura T. 1991b. New idea on the mechanism of hypertension: suppression of nitroxidergic vasodilator nerve function. J Vasc Med Biol 3:235–241.Google Scholar
  64. Toda N, Yoshida K, & Okamura T. 1991c. Analysis of the potentiating action of N G-nitro L-arginine on the contraction of the dog temporal artery elicited by transmural stimulation of noradrenergic nerves. Naunyn Schmiedeberg’s Arch Pharmacol 343:221–224.CrossRefGoogle Scholar
  65. Toda N, Ayajiki K, & Okamura T. 1993a. Endothelial modulation of contractions caused by oxyhemoglobin and N G-nitro-L-arginine in isolated dog and monkey cerebral arteries. Stroke 24: 584–1588.CrossRefGoogle Scholar
  66. Toda N, Ayajiki K, & Okamura T. 1993b. Neural mechanism underlying basilar arterial constriction by intracisternal L-NNA in anesthetized dogs. Am J Physiol 265:H103–H107.PubMedGoogle Scholar
  67. Toda N, Kitamura Y, & Okamura T. 1993c. Neural mechanism of hypertension by nitric oxide synthase inhibitor in dogs. Hypertension 21:3–8.PubMedCrossRefGoogle Scholar
  68. Toda N, Kimura T, Yoshida K, Bredt DS, Snyder SH, Yoshida Y, & Okamura T. 1994. Human uterine arterial relaxation induced by nitroxidergic nerve stimulation. Am J Physiol 266:H1446–H1450.PubMedGoogle Scholar
  69. Toda N, Uchiyama M, & Okamura T. 1995. Prejunctional modulation of nitroxidergic nerve function in canine cerebral arteries. Brain Res 700:213–218.PubMedCrossRefGoogle Scholar
  70. Toda N, Ayajiki K, & Okamura T. 1998. Effect of Ca2+/calmodulin-dependent protein ki-nase II inhibitors on the neurogenic cerebroarterial relaxation. Eur J Pharmacol 340:59–65.CrossRefGoogle Scholar
  71. Togashi H, Sakuma I, Yoshioka M, Kobayashi T, Yasuda H, Kitabatake A, Saito H, Gross SS, & Levi R. 1992. A central nervous system action of nitric oxide in blood pressure regulation. J Pharmacol Exp Ther 262:343–347.PubMedGoogle Scholar
  72. Wanaka K, Matsuyama T, Yoneda S, Kimura K, Kamada T, Girgis S, Macintyre I, Emson P, & Tohyama M. 1986. Origins and distribution of calcitonin gene-related peptide-containing nerves in the wall of the cerebral arteries of the guinea pig with special reference to the coexistence with substance P. Brain Res 369:185–192.PubMedCrossRefGoogle Scholar
  73. Wang Y, Okamura T, & Toda N. 1993. Mechanisms of acetylcholine-induced relaxation in dog external and internal ophthalmic arteries. Exp Eye Res 57:275–281.PubMedCrossRefGoogle Scholar
  74. Weiner CP, Lizasoain I, Baylis SA, Knowles RG, Charles IG, & Moncada S. 1994. Induction of calcium-dependent nitric oxide synthases by sex hormones. Proc Natl Acad Sci USA 91:5212–5216.PubMedCrossRefGoogle Scholar
  75. Yoshida K, Okamura T, Kimura H, Bredt DS, Snyder SH, & Toda N. 1993. Nitric oxide synthase-immunoreactive nerve fibers in dog cerebral and peripheral arteries. Brain Res 629:67–72.PubMedCrossRefGoogle Scholar
  76. Yoshida K, Okamura T, & Toda N. 1994. Histological and functional studies on the nitroxidergic nerve innervating monkey cerebral, mesenteric and temporal arteries. Jpn J Pharmacol 65:351–359.PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media New York 2000

Authors and Affiliations

  • Tomio Okamura
  • Noboru Toda

There are no affiliations available

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