Nitric oxide suppresses cerebral vasomotion by sgc-independent effects on ryanodine receptors and voltage-gated calcium channels

Journal of Vascular Research

Volumn 47, Issue 2, 2010, Pages 93-107

  Yuill, Kathryn H ^a   McNeish, Alister J ^a   Kansui, Yasuo ^a   Garland, Christopher J ^b   Dora, Kim A ^b  

^a University of Bath   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Calcium signalling; Cerebral arteries; Membrane potential; Nitric oxide; Vascular smooth muscle; Vasomotion

Indexed keywords

1H 1,2,4 OXADIAZOLO[4,3 A]QUINOXALIN 1 ONE; 3,3 BIS(2 AMINOETHYL) 1 HYDROXY 2 OXOTRIAZENE; CALCIUM; CALCIUM CHANNEL L TYPE; GUANYLATE CYCLASE; IBERIOTOXIN; N(G) NITROARGININE METHYL ESTER; NIFEDIPINE; NITRIC OXIDE; RYANODINE; RYANODINE RECEPTOR; VOLTAGE GATED CALCIUM CHANNEL;

ANIMAL CELL; ARTERY TONE; ARTICLE; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CONTROLLED STUDY; HYPERPOLARIZATION; MALE; MIDDLE CEREBRAL ARTERY; NONHUMAN; PRIORITY JOURNAL; RAT; RECEPTOR UPREGULATION; SMOOTH MUSCLE FIBER MEMBRANE POTENTIAL;

ANIMALS; CALCIUM; CALCIUM CHANNEL BLOCKERS; CALCIUM CHANNELS, L-TYPE; CALCIUM SIGNALING; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOTHELIUM, VASCULAR; ENZYME INHIBITORS; GUANYLATE CYCLASE; LARGE-CONDUCTANCE CALCIUM-ACTIVATED POTASSIUM CHANNELS; MALE; MEMBRANE POTENTIALS; MIDDLE CEREBRAL ARTERY; MUSCLE, SMOOTH, VASCULAR; NITRIC OXIDE; NITRIC OXIDE DONORS; NITRIC OXIDE SYNTHASE; POTASSIUM CHANNEL BLOCKERS; RATS; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL; TIME FACTORS; VASOCONSTRICTION; VASODILATION;

EID: 69549125975     PISSN: 10181172     EISSN: None     Source Type: Journal    
DOI: 10.1159/000235964     Document Type: Article

References (44)

1. Davis MJ, Hill MA: Signaling mechanisms underlying the vascular myogenic response. Physiol Rev 1999; 79:387-423.
2. Fujii K, Heistad DD, Faraci FM: Ionic mechanisms in spontaneous vasomotion of the rat basilar artery in vivo. J Physiol 1990; 430: 389-398.
3. 2+ signaling pathways underlying myogenic reactivi-t y. J Appl Physiol 2001; 91: 973-983.
4. Diehl RR, Diehl B, Sitzer M, Hennerici M: Spontaneous oscillations in cerebral blood flow velocity in normal humans and in patients with carotid artery disease. Neurosci Lett 1991; 127: 5-8.
5. Dirnagl U, Lindauer U, Villringer A: Nitric oxide synthase blockade enhances vasomo-tion in the cerebral microcirculation of anesthetized rats. Microvasc Res 1993; 45:318-323.
6. Peng H, Matchkov V, Ivarsen A, Aalkjaer C, Nilsson H: Hypothesis for the initiation of vasomotion. Circ Res 2001; 88: 8 1 0-8 1 5.
7. 3)-and ryanodine-sensitive calcium stores in rat basilar artery vasomotion. J Physiol 2002; 545: 615-627.
8. Biswal BB, Hudetz AG: Synchronous oscillations in cerebrocortical capillary red blood cell velocity after nitric oxide synthase inhibition. Microvasc Res 1996; 52:1-12.
9. Jung CS, Oldfield EH, Harvey-White J, Es-pey MG, Zimmermann M, Seifert V, Pluta RM: Association of an endogenous inhibitor of nitric oxide synthase with cerebral vaso-spasm in patients with aneurysmal sub-arachnoid hemorrhage. J Neurosurg 2007; 10 7: 945-950.
10. Pluta RM: Delayed cerebral vasospasm and nitric oxide: review, new hypothesis, and proposed treatment. Pharmacol Ther 2005; 105:23-56.
11. Garcia SR, Bund SJ: Nitric oxide modulation of coronary artery myogenic tone in spontaneously hypertensive and Wistar-Kyoto rats. Clin Sci (Lond) 1998; 94:225-229.
12. Graves JE, Greenwood IA, Large WA: Tonic regulation of vascular tone by nitric oxide and chloride ions in rat isolated small coronary arteries. Am J Physiol Heart Circ Physi-ol 2000; 279:H2604-H2611.
13. Ca channels in cerebral EDHF-mediated dilations. Am J Physiol Heart Circ Physiol 2003; 285:H1590-H1599.
14. Golding EM, Steenberg ML, Johnson TD, Bryan RM: Nitric oxide in the potassium-induced response of the rat middle cerebral artery: a possible permissive role. Brain Res 2001; 889: 98-104.
15. i in rat cerebral arteries: is there a role for membrane potential? Am J Physiol Heart Circ Physiol 1998; 274:H655-H662.
16. + channel openers in cerebral arteries from diabetic rats. Circ Res 1997; 81:996-1004.
17. + channels. J Physiol 1996; 492:419-430.
18. + in endothelium-derived hyperpo-larizing factor-linked dilatation in rat mid-d le cerebral ar ter y. Stroke 2005; 36: 1526-1532.
19. Geary GG, Krause DN, Duckles SP: Estrogen reduces myogenic tone through a nitric oxide-dependent mechanism in rat cerebral arteries. Am J Physiol Heart Circ Physiol 1998; 275:H292-H300.
20. Sakagami K, Kawamura H, Wu DM, Puro DG: Nitric oxide/cGMP-induced inhibition of calcium and chloride currents in retinal pericytes. Microvasc Res 2001; 62:196-203.
21. Bolotina VM, Najibi S, Palacino JJ, Pagano PJ, Cohen RA: Nitric oxide directly activates calcium-dependent potassium channels in vascu lar smooth muscle. Nature 1994; 368: 850-853.
22. Ca) in smooth muscle cells isolated from the rat mesenteric artery. Br J Pharmacol 1998; 124: 1131-114 0.
23. Homer KL, Wanstall JC: Cyclic GMP-inde-pendent relaxation of rat pulmonary artery by spermine NONOate, a diazeniumdiolate nitric oxide donor. Br J Pharmacol 2000; 131: 673-682.
24. Robertson BE, Schubert R, Hescheler J, Nelson MT: cGMP-dependent protein kinase activates Ca-activated K channels in cerebral artery smooth muscle cells. Am J Physiol Cell Physiol 1993; 265:C299-C303.
25. Archer SL, Huang JMC, Hampl V, Nelson DP, Shultz PJ, Weir EK: Nitric oxide and cGMP cause vasorelaxation by activation of a charybdotoxin-sensitive K channel by cGMP-dependent protein kinase. Proc Natl Acad Sci USA 1994; 91: 7583-7587.
26. Mandala M, Heppner TJ, Bonev AD, Nelson MT: Effect of endogenous and exogenous nitric oxide on calcium sparks as targets for va-sodilation in rat cerebral artery. Nitric Oxide 2007; 16:104-109.
27. Eu JP, Xu L, Stamler JS, Meissner G: Regulation of ryanodine receptors by reactive nitrogen species. Biochem Pharmacol 1999; 57: 1079-1084.
28. Suko J, Maurer-Fogy I, Plank B, Bertel O, Wyskovsky W, Hohenegger M, Hellmann G: Phosphorylation of serine 2843 in ryanodine receptor-calcium release channel of skeletal muscle by cAMP-, cGMP-and CaM-dependent protein kinase. Biochim Biophys Acta 1993; 1175:193-206.
29. 2+ channels in cerebral arterioles. Circ Res 2001; 88: 359-365.
30. Quignard JF, Frapier JM, Harricane MC, Al-bat B, Nargeot J, Richard S: Voltage-gated calcium channel currents in human coronary myocytes. Regulation by cyclic GMP and nitric oxide. J Clin Invest 1997; 99:185-193.
31. 2+ channel availability in basilar artery smooth muscle cells. Pflugers Arch 1997; 433:304-311.
32. 2+ current in vestibular hair cells by nitric oxide. J Neuro-physiol 2007; 97:1188-1195.
33. 2+ current in glomus cells of the rabbit carotid body via a cGMP-independent mechanism. Journal of neurophysiolog y 1999; 81: 1449-1457.
34. Jian K, Chen M, Cao X, Zhu XH, Fung ML, Gao TM: Nitric oxide modulation of voltage-gated calcium current by S-nitrosylation and cGMP pathway in cultured rat hippocampal neurons. Biochem Biophys Res Commun 2007; 359: 481-485.
35. Garland CJ, McPherson GA: Evidence that nitric oxide does not mediate the hyperpo-larization and relaxation to acetylcholine in the rat small mesenteric artery. Br J Pharmacol 1992; 10 5: 429-435.
36. Haddock RE, Hill CE: Rhythmicity in arterial smooth muscle. J Physiol 2005; 566:645-656.
37. Ca channels in hyperpolarizing responses of the rat middle cerebral artery. Stroke 2006; 37:1277-1282.
38. Ahern GP, Klyachko VA, Jackson MB: cGMP and S-nitrosylation: two routes for modulation of neuronal excitability by NO. Trends Neurosci 2002; 25:510-517.
39. Klyachko VA, Ahern GP, Jackson MB: cGMP-mediated facilitation in nerve terminals by enhancement of the spike afterhyper-polarization. Neuron 2001; 31: 1015-1025.
40. Alborch E, Salom JB, Torregrosa G: Calcium channels in cerebral arteries. Pharmacol Ther 1995; 68:1-34.
41. 2+ channels. Trends Pharmacol Sci 1998; 19: 108-115. (Pubitemid 28197812)
42. V 1.2b with Src kinase protein binding domains: effect of nitrotyro-sylation. Am J Physiol Cel l Physiol 2007; 293: C1983-C1990.
43. Sanders KM: Invited review: mechanisms of calcium handling in smooth muscles. J Appl Physiol 20 01; 91: 14 3 8-14 4 9.
44. 2+ oscillations, gradients, and homeostasis in vascular smooth muscle. Am J Physiol Heart Circ Physiol 2002; 282: H1571-H1583.