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Neurological Research
A Journal of Progress in Neurosurgery, Neurology and Neurosciences
Volume 28, 2006 - Issue 7
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Articles

Ion channels and calcium signaling in cerebral arteries following subarachnoid hemorrhage

Pages 690-702 | Published online: 19 Jul 2013

REFERENCES

  • Dietrich HH, Dacey RG, Jr. Molecular keys to the problems of cerebral vasospasm. Neurosurgery 2000; 46: 517–530
  • Kassell NF, Sasaki T, Colohan AR, et al. Cerebral vasospasm following aneurysmal subarachnoid hemorrhage. Stroke 1985; 16: 562–572
  • Macdonald RL, Weir BK. A review of hemoglobin and the pathogenesis of cerebral vasospasm. Stroke 1991; 22: 971–982
  • Treggiari-Venzi MM, Suter PM, Romand JA. Review of medical prevention of vasospasm after aneurysmal subarachnoid hemor-rhage: A problem of neurointensive care. Neurosurgery 2001; 48: 249–261
  • Jakobsen M, Overgaard J, Marcussen E, et al. Relation between angiographic cerebral vasospasm and regional CBE in patients with SAH. Acta Neurol Scand 1990; 82: 109–115
  • Ohkuma H, Manabe H, Tanaka M, et al. Impact of cerebral microcirculatory changes on cerebral blood flow during cerebral vasospasm after aneurysmal subarachnoid hemorrhage. Stroke 2000; 31: 1621–1627
  • Shimoda M, Takeuchi M, Tominaga J, et al. Asymptomatic versus symptomatic infarcts from vasospasm in patients with subarach-noid hemorrhage: Serial magnetic resonance imaging. Neurosurgery 2001; 49: 1341–1348
  • Ishiguro M, Puryear CB, Bisson E, et al. Enhanced myogenic tone in cerebral arteries from a rabbit model of subarachnoid hemorrhage. Am J Physiol Heart Circ Physiol 2002; 283: H2217—H2225
  • Ishiguro M, Wellman TL, Honda A, et al. Emergence of a R-type Ca2+ channel (Cav 2.3) contributes to cerebral artery constriction after subarachnoid hemorrhage. Circ Res 2005; 96: 419–426
  • Bayliss WM. On the local reactions of the arterial wall to changes of internal pressure. J Physiol (Lond) 1902; 28: 220–231
  • Johnson PC. The myogenic response. In: Bohr DF, Somlyo AP, Sparks HV, Jr, eds. Handbook of Physiology. The Cardiovascular System. Vol. II. Vascular Smooth Muscle, Bethesda, MD: American Physiological Society, 1980: pp. 409–442
  • Lee KR, Hoff JT. Intracranial pressure. In: Youmans JR, ed. Neurological Surgery, Philadelphia, PA: WB Saunders Co., 1996: pp. 491–518
  • Takeuchi H, Handa Y, Kobayashi H, et al. Impairment of cerebral autoregulation during the development of chronic cerebral vasospasm after subarachnoid hemorrhage in primates. Neurosurgery 1991; 28: 41–48
  • Knuckey NW, Fox RA, Surveyor I, et al. Early cerebral blood flow and computerized tomography in predicting ischemia after cerebral aneurysm rupture. J Neurosurg 1985; 62: 850–855
  • Hai CM, Murphy RA. Ca2+, crossbridge phosphorylation, and contraction. Annu Rev Physiol 1989; 51: 285–298
  • Knot HJ, Nelson MT. Regulation of arterial diameter and wall [Ca2+1 in cerebral arteries of rat by membrane potential and intravascular pressure. J Physiol (Lond) 1998; 508: 199–209
  • Nelson MT, Patlak JB, Worley JF, et al. Calcium channels, potassium channels, and voltage dependence of arterial smooth muscle tone. Am] Physiol 1990; 259: C3—C18
  • Wellman GC, Nelson MT. Ion Channels in Cerebral Arteries. In: Krause DN, Edvinsson L, eds. Cerebral Blood Flow and Metabolism, Baltimore, MD: Lippincott Williams & Wilkins, 2002: pp. 71–87
  • Laher I, Zhang JH. Protein kinase C and cerebral vasospasm. J Cereb Blood Flow Metab 2001; 21: 887–906
  • Nishizawa S, Laher I. Signaling mechanisms in cerebral vasospasm. Trends Cardiovasc Med 2005; 15: 24–34
  • Zhang JH. Role of MAPK in cerebral vasospasm. Drug News Perspect 2001; 14: 261–267
  • Bootman MD, Lipp P, Berridge MJ. The organisation and functions of local Ca2+ signals. J Cell Sci 2001; 114: 2213–2222
  • Clapham DE. Calcium signaling. Cell 1995; 80: 259–268
  • Bito H, Deisseroth K, Tsien RW. CREB phosphorylation and dephosphorylation: A Ca2+- and stimulus duration-dependent switch for hippocampal gene expression. Cell 1996; 87: 1203–1214
  • Cartin L, Lounsbury KM, Nelson MT. Coupling of Ca2+ to CREB activation and gene expression in intact cerebral arteries from mouse: Roles of ryanodine receptors and voltage-dependent Ca2+ channels. Circ Res 2000; 86: 760–767
  • Wellman GC, Cartin L, Eckman DM, et al. Membrane depolar-ization, elevated Ca2± entry, and gene expression in cerebral arteries of hypertensive rats. Am J Physiol Heart Circ Physiol 2001; 281: H2559—H2567
  • Amberg GC, Rossow CF, Navedo MF, et al. NFATc3 regulates Kv2.1 expression in arterial smooth muscle. J Biol Chem 2004; 279: 47326–47334
  • Gomez MF, Stevenson AS, Bonev AD, et al. Opposing Actions of inositol 1,4,5-trisphosphate and ryanodine receptors on nuclear factor of activated t-cells regulation in smooth muscle. J Biol Chem 2002; 277: 37756–37764
  • Graef IA, Chen F, Chen L, et al. Signals transduced by Ca2+/ calcineurin and NFATc3/c4 pattern the developing vasculature. Cell 2001; 105: 863–875
  • Hill-Eubanks DC, Gomez MF, Stevenson AS, et al. NFAT regulation in smooth muscle. Trends Cardiovasc Med 2003; 13: 56–62
  • Shaw JP, Utz PJ, Durand DB, et al. Identification of a putative regulator of early T cell activation genes. Science 1988; 241: 202–205
  • Stevenson AS, Gomez MF, Hill-Eubanks DC, et al. NFAT4 movement in native smooth muscle. A role for differential Ca2+ signal ing. J Biol Chem 2001; 276: 15018-15024
  • Wellman GC, Nelson MT. Signaling between SR and plasma-lemma in smooth muscle: Sparks and the activation of Ca2+senstive ion channels. Cell Calcium 2003; 34: 211–229
  • Jaggar JH, Porter VA, Lederer WJ, et al. Calcium sparks in smooth muscle. Am] Physiol Cell Physiol 2000; 278: C235—C256
  • Nelson MT, Cheng H, Rubart M, et al. Relaxation of arterial smooth muscle by calcium sparks. Science 1995; 270: 633–637
  • Sakaki S, Ohue S, Kohno K, et al. Impairment of vascular reactivity and changes in intracellular calcium and calmodulin levels of smooth muscle cells in canine basilar arteries after subarachnoid hemorrhage. Neurosurgery 1989; 25: 753–761
  • Tani E, Matsumoto T. Continuous elevation of intracellular Ca2+ is essential for the development of cerebral vasospasm. Curr Vasc Pharmacol 2004; 2:13–21
  • Harder DR, Dernbach P, Waters A. Possible cellular mechanism for cerebral vasospasm after experimental subarachnoid hemor-rhage in the dog. J Clin Invest 1987; 80: 875–880
  • Jahromi BS, Aihara Y, Yassari R, et al. Potassium channels in experimental cerebral vasospasm. In: Macdonald RL, ed. Cerebral Vasospasm. Advances in Research and Treatment, New York: Thieme, 2005, pp. 20–24
  • Sobey CG, Faraci FM. Subarachnoid haemorrhage: What happens to the cerebral arteries? Clin Exp Pharmacol Physiol 1998; 25: 867–876
  • Waters A, Harder DR. Altered membrane properties of cerebral vascular smooth muscle following subarachnoid hemorrhage: An electrophysiological study. I. Changes in resting membrane potential (Em) and effect on the electrogenic pump potential contribution to Em. Stroke 1985; 16: 990–997
  • Zuccarello M, Bonasso CL, Lewis Al, et al. Relaxation of subarachnoid hemorrhage-induced spasm of rabbit basilar artery by the K+ channel activator cromakalim. Stroke 1996; 27: 311–316
  • Bulter WE, Peterson JW, Zervas NT, et al. Intracellular calcium, myosin light chain phosphorylation, and contractile force in experimental cerebral vasospasm. Neurosurgery 1996; 38: 781–787
  • Kim P, Yoshimoto Y, lino M, et al. Impaired calcium regulation of smooth muscle during chronic vasospasm following sub-arachnoid hemorrhage. J Cereb Blood Flow Metab 1996; 16: 334–341
  • Sahlin C, Owman C, Chang JY, et al. Changes in contractile response and effect of a calcium antagonist, nimodi-pine, in isolated intracranial arteries of baboon following experimental subarachnoid hemorrhage. Brain Res Bull 1990; 24: 355–361
  • lwabuchi S, Marton LS, Zhang JH. Role of protein tyrosine phosphorylation in erythrocyte lysate-induced intracellular free calcium concentration elevation in cerebral smooth-muscle cells. J Neurosurg 1999; 90: 743–751
  • Zhang H, Weir B, Marton LS, et al. Mechanisms of hemolysate-induced [Ca2+]; elevation in cerebral smooth muscle cells. Am] Physiol 1995; 269: H1874—H1890
  • Arikkath J, Campbell KP. Auxiliary subunits: Essential compo-nents of the voltage-gated calcium channel complex. Curr Opin Neurobiol 2003; 13: 298–307
  • Catterall WA. Structure and regulation of voltage-gated Ca2+ channels. Annu Rev Cell Dev Biol 2000; 16: 521–555
  • Catteral I WA, Striessnig J, Snutch TP, et al. International Union of Pharmacology. XL. Compendium of voltage-gated ion channels: Calcium channels. Pharmacol Rev 2003; 55: 579–581
  • Ertel EA, Campbell KP, Harpold MM, et al. Nomenclature of voltage-gated calcium channels. Neuron 2000; 25: 533–535
  • Moreno DH. Molecular and functional diversity of voltage-gated calcium channels. Ann NY Acad Sci 1999; 868: 102–117
  • Perez-Reyes E, Cribbs LL, Daud A, et al. Molecular characteriza-tion of a neuronal low-voltage-activated T-type calcium channel. Nature 1998; 391: 896–900
  • Randall AD, Tsien RW. Contrasting biophysical and pharmaco-logical properties of T-type and R-type calcium channels. Neuropharmacology 1997; 36: 879–893
  • McDonough SI, Bean BP. Mibefradil inhibition of T-type calcium channels in cerebellar purkinje neurons. Mol Pharmacol 1998; 54: 1080–1087
  • Misra HP, Fridovich I. The generation of superoxide radical during the autoxidation of hemoglobin. J Biol Chem 1972; 247: 6960–6962
  • Bezprozvanny I, Tsien RW. Voltage-dependent blockade of diverse types of voltage-gated Ca' channels expressed in Xenopus oocytes by the Ca2+ channel antagonist mibefradil (Ro 40-5967). Mol Pharmacol 1995; 48: 540–549
  • Jimenez C, Bourinet E, Leuranguer V, et al. Determinants of voltage-dependent inactivation affect Mibefradil block of calcium channels. Neuropharmacology 2000; 39: 1–10
  • Chuang RS, Jaffe H, Cribbs L, et al. Inhibition of T-type voltage-gated calcium channels by a new scorpion toxin. Nat Neurosci 1998; 1: 668–674
  • Sidach SS, Mintz IM. Kurtoxin, a gating modifier of neuronal high- and low-threshold ca channels. J Neurosci 2002; 22: 2023–2034
  • McCleskey EW, Fox AP, Feldman DH, et al. Omega-conotoxin: Direct and persistent blockade of specific types of calcium channels in neurons but not muscle. Proc Natl Acad Sci USA 1987; 84: 4327–4331
  • Mintz IM, Venema N/J, Swiderek KM, et al. P-type calcium channels blocked by the spider toxin omega-Aga-IVA. Nature 1992; 355: 827–829
  • Mintz IM, Bean BP. Block of calcium channels in rat neurons by synthetic omega-Aga-IVA. Neuropharmacology 1993; 32: 1161–1169
  • Randall A, Tsien RW. Pharmacological dissection of multiple types of Ca2+ channel currents in rat cerebellar granule neurons. J Neurosci 1995; 15: 2995–3012
  • Newcomb R, Szoke B, Palma A, et al. Selective peptide antagonist of the class E calcium channel from the venom of the tarantula Hysterocrates gigas. Biochemistry 1998; 37: 15353–15362
  • Hille B. Ionic Channels of Excitable Membranes, Sunderland, MA: Sinauer Associates, Inc., 1992
  • Randall AD. The molecular basis of voltage-gated Ca2+ channel diversity: Is it time for T? J Membr Biol 1998; 161: 207–213
  • Nelson MT, Worley JF. Dihydropyridine inhibition of single calcium channels and contraction in rabbit mesenteric artery depends on voltage. J Physiol 1989; 412: 65–91
  • Striessnig J, Grabner M, Mitterdorfer J, et al. Structural basis of drug binding to L Ca2+ channels. Trends Pharmacol Sci 1998; 19: 108–115
  • de Weille JR, Schweitz H, Maes P, et al. Calciseptine, a peptide isolated from black mamba venom, is a specific blocker of the [-type calcium channel. Proc Natl Acad Sci USA 1991; 88: 2437–2440
  • Gokina NI, Knot Hi, Nelson MT, et al. Increased Ca2+ sensitivity as a key mechanism of PKC-induced constriction in pressurized cerebral arteries. Am] Physiol 1999; 277: H1178—H1188
  • Hill MA, Zou H, Potocnik SJ, et al. Invited review: Arteriolar smooth muscle mechanotransduction: Ca2+ signaling pathways underlying myogenic reactivity. J Appl Physiol 2001; 91: 973–983
  • Wesselman JP, VanBavel E, Pfaffendorf M, et al. Voltage-operated calcium channels are essential for the myogenic responsiveness of cannulated rat mesenteric small arteries. J Vasc Res 1996; 33: 32–41
  • Petruk KC, West M, Mohr G, et al. Nimodipine treatment in poor-grade aneurysm patients. Results of a multicenter double-blind placebo-controlled trial. J Neurosurg 1988; 68: 505–517
  • Chen CC, Lamping KG, Nuno DW, et al. Abnormal coronary function in mice deficient in alpha1H T-type Ca2+ channels. Science 2003; 302: 1416–1418
  • Hansen PB, Jensen BL, Andreasen D, et al. Differential expression of T- and [-type voltage-dependent calcium channels in renal resistance vessels. Circ Res 2001; 89: 630–638
  • Hansen PB, Jensen BL, Andreasen D, et al. Vascular smooth muscle cells express the alpha(1A) subunit of a P-/Q-type voltage-dependent Ca(2+) Channel, and it is functionally important in renal afferent arterioles. Circ Res 2000; 87: 896–902
  • Itonaga Y, Nakajima T, Morita H, et al. Contribution of nifedipine-insensitive voltage-dependent Ca2+ channel to dia-meter regulation in rabbit mesenteric artery. Life Sci 2002; 72: 487–500
  • Morita H, Cousins H, Onoue H, et al. Predominant distribution of nifedipine-insensitive, high voltage-activated Ca2+ channels in the terminal mesenteric artery of guinea pig. Circ Res 1999; 85: 596–605
  • Blood AB, Zhao Y, Long W, et al. [-type Ca2+ channels in fet al and adult ovine cerebral arteries. Am] Physiol Regul Integr Comp Physiol 2002; 282: R131—R138
  • Pesic A, Madden JA, Pesic M, et al. High blood pressure upregulates arterial [-type Ca2+ channels: Is membrane depolar-ization the signal? Circ Res 2004; 94: e97—e104
  • Pratt PF, Bonnet S, Ludwig LM, et al. Upregulation of [-type Ca2+ channels in mesenteric and skelet al arteries of SHR. Hypertension 2002; 40: 214–219
  • Aihara Y, Jahromi BS, Yassari R, et al. Molecular profile of vascular ion channels after experimental subarachnoid hemor-rhage. J Cereb Blood Flow Metab 2004; 24: 75–83
  • Cook DA, Vollrath B. Free radicals and intracellular events associated with cerebrovascular spasm. Cardiovasc Res 1995; 30: 493–500
  • Zimmermann M, Seifert V. Endothel in and subarachnoid hemorrhage: An overview. Neurosurgery 1998; 43: 863–875
  • Takeuchi K, Miyata N, Renic M, et al. Hemoglobin, NO and 20-HETE interactions in mediating cerebral vasoconstriction following SAH. Am] Physiol Regul Integr Comp Physiol 2005; 290: R84–R89
  • Gebremedhin D, Lange AR, Narayanan J, et al. Cat cerebral arterial smooth muscle cells express cytochrome P4504A2 enzyme and produce the vasoconstrictor 20-HETE which enhances [-type Ca2 + current. Physiol 1998; 507: 771–781
  • Nelson MT, Standen NB, Brayden JE, et al. Noradrenaline contracts arteries by activating voltage-dependent calcium channels. Nature 1988; 336: 382–385
  • Worley JF, Quayle JM, Standen NB, et al. Regulation of single calcium channels in cerebral arteries by voltage, serotonin, and dihydropyridines. Am] Physiol 1991; 261: H1951—H1960
  • Kim CJ, Weir B, Macdonald RL, et al. Hemolysate inhibits [-type Ca2+ channels in rat basilar smooth muscle cells. J Vasc Res 1996; 33: 258–264
  • Jewell RP, Saundry CM, Bonev AD, et al. Inhibition of Ca++ sparks by oxyhemoglobin in rabbit cerebral arteries. J Neurosurg 2004; 100: 295–302
  • Nishizawa S, Nezu N, Uemura K. Direct evidence for a key role of protein kinase C in the development of vasospasm after subarachnoid hemorrhage. J Neurosurg 1992; 76: 635–639
  • Miyagi Y, Carpenter RC, Meguro T, et al. Upregulation of rho A and rho kinase messenger RNAs in the basilar artery of a rat model of subarachnoid hemorrhage. J Neurosurg 2000; 93: 471–476
  • Sato M, Tani E, Fujikawa H, et al. Involvement of Rho-kinase-mediated phosphorylation of myosin light chain in enhancement of cerebral vasospasm. Circ Res 2000; 87: 195–200
  • Watanabe Y, Faraci FM, Heistad DD. Activation of Rho-associated kinase during augmented contraction of the basilar artery to serotonin after subarachnoid hemorrhage. Am Physiol Heart Circ Physiol 2005; 288: H2653—H2658
  • Sasaki T, Kasuya H, Onda H, et al. Role of p38 mitogen-activated protein kinase on cerebral vasospasm after subarachnoid hemorrhage. Stroke 2004; 35: 1466–1470
  • Tibbs R, Zubkov A, Aoki K, et al. Effects of mitogen-activated protein kinase inhibitors on cerebral vasospasm in a double-hemorrhage model in dogs. J Neurosurg 2000; 93: 1041–1047
  • Fujikawa H, Tani E, Yamaura I, et al. Activation of protein kinases in canine basilar artery in vasospasm. J Cereb Blood Flow Metab 1999; 19: 44–52
  • Kusaka G, Kimura H, Kusaka I, et al. Contribution of Src tyrosine kinase to cerebral vasospasm after subarachnoid hemorrhage. J Neurosurg 2003; 99: 383–390
  • Obara K, Nishizawa S, Koide M, et al. Interactive role of protein kinase C-delta with rho-kinase in the development of cerebral vasospasm in a canine two-hemorrhage model. J Vasc Res 2005; 42: 67–76
  • Surks HK, Richards CT, Mendelsohn ME. Myosin phosphatase-Rho interacting protein. A new member of the myosin phosphatase complex that directly binds RhoA. J Biol Chem 2003; 278: 51484–51493
  • Callaghan B, Koh SD, Keef KD. Muscarinic M2 receptor stimulation of Cav1.2b requires phosphatidylinositol 3-kinase, protein kinase C, and c-Src. Circ Res 2004; 94: 626–633
  • Wijetunge S, Hughes AD. pp60c-src increases voltage-operated calcium channel currents in vascular smooth muscle cells. Biochem Biophys Res Commun 1995; 217: 1039–1044
  • Keef KD, Hume JR, Zhong J. Regulation of cardiac and smooth muscle Ca” channels (CaV1.2a,b) by protein kinases. Am J Physiol Cell Physiol 2001; 281: C1743—C1756
  • Schuhmann K, Groschner K. Protein kinase-C mediates dual modulation of [-type Ca” channels in human vascular smooth muscle. FEBS Lett 1994; 341: 208–212
  • Faraci FM, Heistad DD. Regulation of the cerebral circulation: Role of endothelium and potassium channels. Physiol Rev 1998; 78: 53–97
  • Jackson WE. Potassium channels in the peripheral microcircula-tion. Microcirculation 2005; 12: 113–127
  • Nelson MT, Quayle JM. Physiological roles and properties of potassium channels in arterial smooth muscle. Am J Physiol 1995; 268: C799—C822
  • Coetzee WA, Amarillo Y, Chiu J, et al. Molecular diversity of K+ channels. Ann NY Acad Sci 1999; 868: 233–285
  • Cole WC, Clement-Chomienne 0, Aiello EA. Regulation of 4-aminopyridine-sensitive, delayed rectifier K+ channels in vas-cular smooth muscle by phosphorylation. Biochem Cell Biol 1996; 74: 439–447
  • Knot HJ, Nelson MT. Regulation of membrane potential and diameter by voltage-dependent K+ channels in rabbit myogenic cerebral arteries. Am] Physiol 1995; 269: H348—H355
  • Quan L, Sobey CG. Selective effects of subarachnoid hemorrhage on cerebral vascular responses to 4-aminopyridine in rats. Stroke 2000; 31: 2460–2465
  • Robertson BE, Nelson MT. Aminopyridine inhibition and voltage dependence of K+ currents in smooth muscle cells from cerebral arteries. Am] Physiol 1994; 267: C1589—C1597
  • Gutman GA, Chandy KG, Adelman JP, et al. International Union of Pharmacology. XLI. Compendium of voltage-gated ion channels: potassium channels. Pharmacol Rev 2003; 55: 583–586
  • Jan LY, Jan YN. Voltage-gated and inwardly rectifying potassium channels. J Physiol 1997; 505: 267–282
  • Albarwani S, Nemetz LT, Madden JA, et al. Voltage-gated K+ channels in rat small cerebral arteries: Molecular identity of the functional channels. J Physiol 2003; 551: 751–763
  • Kerr PM, Clement-Chomienne 0, Thorneloe KS, et al. Heteromultimeric Kv1.2-Kv1.5 channels underlie 4-aminopyridine-sensitive delayed rectifier K+ current of rabbit vascular myocytes. Circ Res 2001; 89: 1038–1044
  • Plane F, Johnson R, Kerr P, et al. Heteromultimeric Kv1 channels contribute to myogenic control of arterial diameter. Circ Res 2005; 96: 216–224
  • Thorneloe KS, Chen TT, Kerr PM, et al. Molecular composition of 4-aminopyridine-sensitive voltage-gated K+ channels of vascular smooth muscle. Circ Res 2001; 89: 1030–1037
  • Aiello EA, Clement-Chomienne 0, Sontag DP, et al. Protein kinase C inhibits delayed rectifier K+ current in rabbit vascular smooth muscle cells. Am Physiol 1996; 271: H109—H119
  • Holmes TC, Fadool DA, Levitan IB. Tyrosine phosphorylation of the Kv1.3 potassium channel. J Neurosci 1996; 16: 1581–1590
  • Huang XY, Morielli AD, Peralta EG. Tyrosine kinase-dependent suppression of a potassium channel by the G protein-coupled ml muscarinic acetylcholine receptor. Cell 1993; 75: 1145–1156
  • Meera P, Wallner M, Song M, et al. Large conductance voltage-and calcium-dependent K+ channel, a distinct member of voltage-dependent ion channels with seven N-terminal trans-membrane segments (S0-S6), an extracellular N terminus, and an intracellular (S9-S10) C terminus. Proc Natl Acad Sci USA 1997; 94: 14066–14071
  • Magleby KL. Gating mechanism of BK (Slo1) channels: So near, yet so far. J Gen Physiol 2003; 121: 81–96
  • Brenner R, Perez GJ, Bonev AD, et al. Vasoregulation by the beta1 subunit of the calcium-activated potassium channel. Nature 2000; 407: 870–876
  • Tanaka Y, Meera P, Song M, et al. Molecular constituents of maxi Kca channels in human coronary smooth muscle: Predominant alpha + beta subunit complexes. J Physiol 1997; 502: 545–557
  • Brayden JE, Nelson MT. Regulation of arterial tone by activation of calcium-dependent potassium channels. Science 1992; 256: 532–535
  • Gebremedhin D, Ma YH, Falck JR, et al. Mechanism of action of cerebral epoxyeicosatrienoic acids on cerebral arterial smooth muscle. Am] Physiol 1992; 263: H519—H525
  • Wellman GC, Bonev AD, Nelson MT, et al. Gender differences in coronary artery diameter involve estrogen, nitric oxide, and Ca2+-dependent K+ channels. Circ Res 1996; 79: 1024–1030
  • Perez GJ, Bonev AD, Patlak JB, et al. Functional coupling of ryanodine receptors to Kca channels in smooth muscle cells from rat cerebral arteries. J Gen Physiol 1999; 113: 229–238
  • Wellman GC, Nathan DJ, Saundry CM, et al. Ca2+ sparks and their function in human cerebral arteries. Stroke 2002; 33: 802–808
  • Jaggar JH, Wellman GC, Heppner TJ, et al. Ca2+ channels, ryanodine receptors and Ca2+-activated K+ channels: A func-tional unit for regulating arterial tone. Acta Physiol Scand 1998; 164: 577–587
  • Porter VA, Bonev AD, Knot HJ, et al. Frequency modulation of Ca2+ sparks is involved in regulation of arterial diameter by cyclic nucleotides. Am Physiol 1998; 274: C1346—C1355
  • Wellman GC, Santana LF, Bonev AD, et al. Role of phospho-lamban in the modulation of arterial Ca2+ sparks and Ca2+ activated K+ channels by cAMP. Am] Physiol Cell Physiol 2001; 281: C1029—C1037
  • Collier ML, Ji G, Wang Y, et al. Calcium-induced calcium release in smooth muscle: Loose coupling between the action potential and calcium release. J Gen Physiol 2000; 115: 653–662
  • ZhuGe R, Tuft RA, Fogarty KE, et al. The influence of sarcoplasmic reticulum Ca2+ concentration on Ca2+ sparks and spontaneous transient outward currents in single smooth muscle cells. J Gen Physiol 1999; 113: 215–228
  • Bonev AD, Jaggar JH, Rubart M, et al. Activators of protein kinase C decrease Ca' spark frequency in smooth muscle cells from cerebral arteries. Am Physiol 1997; 273: C2090—C2095
  • Alioua A, Mahajan A, Nishimaru K, et al. Coupling of c-Src to large conductance voltage- and Ca2+-activated K± channels as a new mechanism of agonist-induced vasoconstriction. Proc Natl Acad Sci USA 2002; 99: 14560–14565
  • Kehl F, Cambj-Sapunar L, Maier KG, et al. 20-HETE contributes to the acute fall in cerebral blood flow after subarachnoid hemorrhage in the rat. Am] Physiol Heart Circ Physiol 2002; 282: H1556—H1565
  • Harder DR, Gebremedhin D, Narayanan J, et al. Formation and action of a P-4504A metabolite of arachidonic acid in cat cerebral microvessels. Am Physiol 1994; 266: H2098—H2107
  • Zou AP, Fleming JT, Falck JR, et al. 20-HETE is an endogenous inhibitor of the large-conductance Ca2+-activated K+ channel in renal arterioles. Am Physiol 1996; 270: R228—R237
  • Wickman G, Lan C, Vollrath B. Functional roles of the rho/rho kinase pathway and protein kinase C in the regulation of cerebrovascular constriction mediated by hemoglobin: Relevance to subarachnoid hemorrhage and vasospasm. Circ Res 2003; 92: 809–816
  • Arai T, Takeyama N, Tanaka T. Glutathione monoethyl ester and inhibition of the oxyhemoglobin-induced increase in cytosolic calcium in cultured smooth-muscle cells. J Neurosurg 1999; 90: 527–532
  • Kawakami M, Okabe E. Superoxide anion radical-triggered Ca2+ release from cardiac sarcoplasmic reticulum through ryanodine receptor Ca2+ channel. Mol Pharmacol 1998; 53: 497–503
  • Okabe E, Odajima C, Taga R, et al. The effect of oxygen free radicals on calcium permeability and calcium loading at steady state in cardiac sarcoplasmic reticulum. Mol Pharmacol 1988; 34: 388–394
  • Pluta RM. Delayed cerebral vasospasm and nitric oxide: Review, new hypothesis, and proposed treatment. Pharmacol Ther 2005; 105: 23–56
  • Quayle JM, Nelson MT, Standen NB. ATP-sensitive and inwardly rectifying potassium channels in smooth muscle. Physiol Rev 1997; 77: 1165–1232
  • Nichols CG, Lopatin AN. Inward rectifier potassium channels. Annu Rev Physiol 1997; 59: 171–191
  • Knot HJ, Zimmermann PA, Nelson MT. Extracellular K+-induced hyperpolarizations and dilatations of rat coronary and cerebral arteries involve inward rectifier K+ channels. J Physiol (Lond) 1996; 492: 419–430
  • Quayle JM, McCarron JG, Brayden JE, et al. Inward rectifier K+ currents in smooth muscle cells from rat resistance-sized cerebral arteries. Am] Physiol 1993; 265: C1363—C1370
  • Hirst GD, Edwards FR. Sympathetic neuroeffector transmission in arteries and arterioles. Physiol Rev 1989; 69: 546–604
  • Paulson OB, Newman EA. Does the release of potassium from astrocyte endfeet regulate cerebral blood flow? Science 1987; 237: 896–898
  • Zaritsky JJ, Eckman DM, Wellman GC, et al. Targeted disruption of Kir2.1 and Kir2.2 genes reveals the essential role of the inwardly rectifying K+ current in K+-mediated vasodilation. Circ Res 2000; 87: 160–166
  • Weyer GW, Jahromi BS, Aihara Y, et al. Expression and function of inwardly rectifying potassium channels after experimental subarachnoid hemorrhage. J Cereb Blood Flow Metab 2006; 26: 382–391
  • Clement JP, Kunjilwar K, Gonzalez G, et al. Association and stoichiometry of K(ATP) channel subunits. Neuron 1997; 18: 827–838
  • Yamada M, Isomoto S, Matsumoto S, et al. Sulphonylurea receptor 2B and Kir6.1 form a sulphonylurea-sensitive but ATP-insensitive K+ channel. J Physiol 1997; 499: 715–720
  • Standen NB, Quayle JM, Davies NW, et al. Hyperpolarizing vasodilators activate ATP-sensitive K+ channels in arterial smooth muscle. Science 1989; 245: 177–180
  • Kovalev H, Quayle JM, Kamishima T, et al. Molecular analysis of the subtype-selective inhibition of cloned KATP channels by PNU-37883A. Br] Pharmacol 2004; 141: 867–873
  • Wellman GC, Barrett-Jolley R, Koppel H, et al. Inhibition of vascular KA-rp channels by U-37883A: A comparison with cardiac and skelet al muscle. Br] Pharmacol 1999; 128: 909–916
  • Quayle JM, Bonev AD, Brayden JE, et al. Calcitonin gene-related peptide activated ATP-sensitive K+ currents in rabbit arterial smooth muscle via protein kinasePhysiol 1994; 475:9–13
  • Wellman GC, Quayle JM, Standen NB. ATP-sensitive K+ channel activation by calcitonin gene-related peptide and protein kinase A in pig coronary arterial smooth muscle. J Physiol 1998; 507: 117–129
  • Edvinsson L, Delgado-Zygmunt T, Ekman R, et al. Involvement of perivascular sensory fibers in the pathophysiology of cerebral vasospasm following subarachnoid hemorrhage. J Cereb Blood Flow Metab 1990; 10: 602–607
  • Edvinsson L, Juul R, Jansen I. Perivascular neuropeptides (NPY, VIP, CGRP and SP) in human brain vessels after subarachnoid haemorrhage. Acta Neurol Scand 1994; 90: 324–330
  • Sobey CG, Heistad DD, Faraci FM. Effect of subarachnoid hemorrhage on dilatation of rat basilar artery in vivo. Am J Physiol 1996; 271: H126—H132
  • Sugai K, Yaganisawa T, Motohashi 0, et al. Levcromakalim decreases cytoplasmic Ca2+ and vascular tone in basilar artery of SAH model dogs. J Cardiovasc Pharmacol 1999; 33: 868–875
  • Ahmad I, Imaizumi S, Shimizu H, et al. Development of calcitonin gene-related peptide slow-release tablet implanted in CSF space for prevention of cerebral vasospasm after experi-mental subarachnoid haemorrhage. Acta Neurochir (Wien) 1996; 138: 1230-1240
  • Inoue T, Shimizu H, Kaminuma T, et al. Prevention of cerebral vasospasm by calcitonin gene-related peptide slow-release tablet after subarachnoid hemorrhage in monkeys. Neurosurgery 1996; 39: 984–990
  • Effect of calcitonin-gene-related peptide in patients with delayedpostoperativecerebralischaemiaafteraneurysmal subarachnoid haemorrhage. European CGRP in Subarachnoid Haemorrhage Study Group. Lancet 1992; 339: 831–834
  • Bell BA. The neuroprotective effect of calcitonin gene-related peptide following subarachnoid hemorrhage. European CGRP in Subarachnoid Haemorrhage Study Group. Ann NY Acad Sci 1995; 765: 299–300
  • Toyoda K, Faraci FM, Russo AF, et al. Gene transfer of calcitonin gene-related peptide to cerebral arteries. Am] Physiol Heart Circ Physiol 2000; 278: H586—H594
  • Satoh M, Perkins E, Kimura H, et al. Posttreatment with adenovirus-mediated gene transfer of calcitonin gene-related peptide to reverse cerebral vasospasm in dogs. J Neurosurg 2002; 97: 136–142
  • Toyoda K, Faraci FM, Watanabe Y, et al. Gene transfer of calcitonin gene-related peptide prevents vasoconstriction after subarachnoid hemorrhage. Circ Res 2000; 87: 818–824

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