Differential effect of calcium-activated potassium and chloride channels on rat basilar artery vasomotion

Abstract

Spontaneous, rhythmical contractions, or vasomotion, can be recorded from cerebral vessels under both normal physiological and pathophysiological conditions. We investigated the cellular mechanisms underlying vasomotion in the cerebral basilar artery (BA) of Wistar rats. Pressure myograph video microscopy was used to study the changes in cerebral artery vessel diameter. The main results of this study were as follows: (1) The diameters of BA and middle cerebral artery (MCA) were 314.5±15.7 μm (n=15) and 233.3±10.1 μm (n=12) at 10 mmHg working pressure (P<0.05), respectively. Pressure-induced vasomotion occurred in BA (22/28, 78.6%), but not in MCA (4/31, 12.9%) from 0 to 70 mmHg working pressure. As is typical for vasomotion, the contractile phase of the response was more rapid than the relaxation phase; (2) The frequency of vasomotion response and the diameter were gradually increased in BA from 0 to 70 mmHg working pressure. The amplitude of the rhythmic contractions was relatively constant once stable conditions were achieved. The frequency of contractions was variable and the highest value was 16.7±4.7 (n=13) per 10 min at 60 mmHg working pressure; (3) The pressure-induced vasomotion of the isolated BA was attenuated by nifedipine, NFA, 18β-GA, TEA or in Ca²⁺-free medium. Nifedipine, NFA, 18β-GA or Ca²⁺-free medium not only dampened vasomotion, but also kept BA in relaxation state. In contrasts, TEA kept BA in contraction state. These results suggest that the pressure-induced vasomotion of the isolated BA results from an interaction between Ca²⁺-activated Cl⁻ channels (CaCCs) currents and K^Ca currents. We hypothesize that vasomotion of BA depends on the depolarizing of the vascular smooth muscle cells (VSMCs) to activate CaCCs. Depolarization in turn activates voltage-dependent Ca²⁺ channels, synchronizing contractions of adjacent cells through influx of extracellular calcium and the flow of calcium through gap junctions. Subsequent calcium-induced calcium release from ryanodine-sensitive stores activates K^Ca channels and hyperpolarizes VSMCs, which provides a negative feedback loop for regenerating the contractile cycle.

Keywords

pressure myograph / vasomotion / basilar artery / calcium-activated ion channels / vascular smooth muscle cell / gap junction

References

[1] SakuraiT, TeruiN. Effects of sympathetically induced vasomotion on tissue-capillary fluid exchange. Am J Physiol Heart Circ Physiol, 2006, 291(4): H1761-H1767

[2] BouskelaE, GramppW. Spontaneous vasomotion in hamster cheek pouch arterioles in varying experimental conditions. Am J Physiol, 1992, 262(2Pt2): H478-H485

[3] ColantuoniA, BertugliaS, IntagliettaM. Quantitation of rhythmic diameter changes in arterial microcirculation. Am J Physiol, 1984, 246(4Pt2): H508-H517

[4] MinamiyamaM, HanaiS. Propagation properties of vasomotion at terminal arterioles and precapillaries in the rabbit mesentery. Biorheology, 1991, 28(3–4): 275-286

[5] HundleyWG, RenaldoGJ, LevasseurJE, et al.. Vasomotion in cerebral microcirculation of awake rabbits. Am J Physiol, 1988, 254(1Pt2): H67-71

[6] FujiiK, HeistadDD, FaraciFM. Ionic mechanisms in spontaneous vasomotion of the rat basilar artery in vivo. J Physiol, 1990, 430: 389-398

[7] FujiiK, HeistadDD, FaraciFM. Vasomotion of basilar arteries in vivo. Am J Physiol, 1990, 258(6Pt2): H1829-H1834

[8] Morita-TsuzukiY, BouskelaE, HardeboJE. Vasomotion in the rat cerebral microcirculation recorded by laser-Doppler flowmetry. Acta Physiol Scand, 1992, 146(4): 431-439

[9] BertugliaS, ColantuoniA, IntagliettaM. Effects of L-NMMA and indomethacin on arteriolar vasomotion in skeletal muscle microcirculation of conscious and anesthetized hamsters. Microvasc Res, 1994, 48(1): 68-84

[10] HillCE, EadeJ, SandowSL. Mechanisms underlying spontaneous rhythmical contractions in irideal arterioles of the rat. J Physiol, 1999, 521(Pt2): 507-516

[11] PengH, MatchkovV, IvarsenA, et al.. Hypothesis for the initiation of vasomotion. Circ Res, 2001, 88(8): 810-815

[12] GustafssonH, NilssonH. Rhythmic contractions of isolated small arteries from rat: role of calcium. Acta Physiol Scand, 1993, 149(3): 283-291

[13] RuckerM, StrobelO, VollmarB, et al.. Vasomotion in critically perfused muscle protects adjacent tissues from capillary perfusion failure. Am J Physiol Heart Circ Physiol, 2000, 279(2): H550-558

[14] ShimamuraK, SekiguchiF, SunanoS. Tension oscillation in arteries and its abnormality in hypertensive animals. Clin Exp Pharmacol Physiol, 1999, 26(4): 275-284

[15] GriffithTM. Temporal chaos in the microcirculation. Cardiovasc Res, 1996, 31(3): 342-358

[16] GrattonRJ, GandleyRE, McCarthyJF, et al.. Contribution of vasomotion to vascular resistance: a comparison of arteries from virgin and pregnant rats. J Appl Physiol, 1998, 85(6): 2255-2260

[17] HudetzAG, BiswalBB, ShenH, et al.. Spontaneous fluctuations in cerebral oxygen supply. An introduction. Adv Exp Med Biol, 1998, 454: 551-559

[18] HaddockRE, HirstGD, HillCE. Voltage independence of vasomotion in isolated irideal arterioles of the rat. J Physiol, 2002, 540(Pt1): 219-229

[19] von der WeidPY, BenyJL. Simultaneous oscillations in the membrane potential of pig coronary artery endothelial and smooth muscle cells. J Physiol, 1993, 471: 13-24

[20] SegalSS, BenyJL. Intracellular recording and dye transfer in arterioles during blood flow control. Am J Physiol, 1992, 263(1Pt2): H1-7

[21] RuehlmannDO, LeeCH, PoburkoD, et al.. Asynchronous Ca(2+) waves in intact venous smooth muscle. Circ Res, 2000, 86(4): E72-79

[22] van BreemenC, ChenQ, LaherI. Superficial buffer barrier function of smooth muscle sarcoplasmic reticulum. Trends Pharmacol Sci, 1995, 16(3): 98-105

[23] BoedtkjerDM, MatchkovVV, BoedtkjerE, et al.. Vasomotion has chloride-dependency in rat mesenteric small arteries. Pflugers Arch, 2008, 457(2): 389-404

[24] LargeWA, WangQ. Characteristics and physiological role of the Ca(2+)-activated Cl- conductance in smooth muscle. Am J Physiol, 1996, 271(2Pt1): C435-454

[25] ChipperfieldAR, HarperAA. Chloride in smooth muscle. Prog Biophys Mol Biol, 2000, 74(3–5): 175-221

[26] KitamuraK, YamazakiJ. Chloride channels and their functional roles in smooth muscle tone in the vasculature. Jpn J Pharmacol, 2001, 85(4): 351-357

[27] FringsS, ReuterD, KleeneSJ. Neuronal Ca²⁺-activated Cl⁻ channels—homing in on an elusive channel species. Prog Neurobiol, 2000, 60(3): 247-289

[28] GriffithTM, EdwardsDH. Ca²⁺ sequestration as a determinant of chaos and mixed-mode dynamics in agonist-induced vasomotion. Am J Physiol, 1997, 272(4Pt2): H1696-1709

[29] EdwardsDH, GriffithTM. Entrained ion transport systems generate the membrane component of chaotic agonist-induced vasomotion. Am J Physiol, 1997, 273(2Pt2): H909-920

[30] GustafssonH, NilssonH. Rhythmic contractions in isolated small arteries of rat: role of K+ channels and the Na+,K(+)-pump. Acta Physiol Scand, 1994, 150(2): 161-170

[31] PerezGJ, BonevAD, NelsonMT. Micromolar Ca(2+) from sparks activates Ca(2+)-sensitive K(+) channels in rat cerebral artery smooth muscle. Am J Physiol Cell Physiol, 2001, 281(6): C1769-1775

[32] JaggarJH, PorterVA, LedererWJ, et al.. Calcium sparks in smooth muscle. Am J Physiol Cell Physiol, 2000, 278(2): C235-256

[33] NelsonMT, ChengH, RubartM, et al.. Relaxation of arterial smooth muscle by calcium sparks. Science, 1995, 270(5236): 633-637

[34] FaraciFM, SobeyCG. Role of potassium channels in regulation of cerebral vascular tone. J Cereb Blood Flow Metab, 1998, 18(10): 1047-1063

[35] JiangXW, SiJQ, LiL, ZhaoL, et al.. The effects of gap junction on the mesenteric artery contraction activities in normotensive rats and spontaneously hypertensive rats. Chongqing Med (Chinese), 2013, 42(12): 1365-1367

[36] AalkjaerC, BoedtkjerD, MatchkovV. Vasomotion — what is currently thought?. Acta Physiol (Oxf), 2011, 202(3): 253-269

[37] NilssonH, AalkjaerC. Vasomotion: mechanisms and physiological importance. Mol Interv, 2003, 3(2): 79-89

[38] BiegerD, FordCA, TabrizchiR. Potassium-induced intermittent vasomotion in rat isolated pulmonary artery. J Smooth Muscle Res, 2011, 47(1): 21-35

[39] MatchkovVV. Mechanisms of cellular synchronization in the vascular wall. Mechanisms of vasomotion. Dan Med Bull, 2010, 57(10): B4191

[40] ThornCE, KyteH, SlaffDW, et al.. An association between vasomotion and oxygen extraction. Am J Physiol Heart Circ Physiol, 2011, 301(1): H442-449

[41] JaggarJH, StevensonAS, NelsonMT. Voltage dependence of Ca2+ sparks in intact cerebral arteries. Am J Physiol, 1998, 274(6Pt1): C1755-1761

[42] IinoM, KasaiH, YamazawaT. Visualization of neural control of intracellular Ca2+ concentration in single vascular smooth muscle cells in situ. Embo J, 1994, 13(21): 5026-5031

[43] NeylonCB, LangRJ, FuY, et al.. Molecular cloning and characterization of the intermediate-conductance Ca(2+)-activated K(+) channel in vascular smooth muscle: relationship between K(Ca) channel diversity and smooth muscle cell function. Circ Res, 1999, 85(9): e33-43

[44] DoughtyJM, LangtonPD. Measurement of chloride flux associated with the myogenic response in rat cerebral arteries. J Physiol, 2001, 534(Pt3): 753-761

[45] LambFS, VolkKA, ShibataEF. Calcium-activated chloride current in rabbit coronary artery myocytes. Circ Res, 1994, 75(4): 742-750

[46] LambFS, BarnaTJ. Chloride ion currents contribute functionally to norepinephrine-induced vascular contraction. Am J Physiol, 1998, 275(1Pt2): H151-160

[47] MyersJH, LambFS, WebbRC. Norepinephrine-induced phasic activity in tail arteries from genetically hypertensive rats. Am J Physiol, 1985, 248(3Pt2): H419-423

[48] MatchkovVV, AalkjaerC, NilssonH. A cyclic GMP-dependent calcium-activated chloride current in smooth-muscle cells from rat mesenteric resistance arteries. J Gen Physiol, 2004, 123(2): 121-134

[49] HaddockRE, HillCE. Differential activation of ion channels by inositol 1,4,5-trisphosphate (IP3)- and ryanodine-sensitive calcium stores in rat basilar artery vasomotion. J Physiol, 2002, 545(2): 615-627

[50] WangYZ, LiuZJ, LiL, et al.. Effects of chloride channel blockers on excitatory junction potentials in smooth muscle cells of cochlear spiral modiolar artery in guinea pigs. Sheng Li Xue Bao (Chinese), 2006, 58(5): 456-462

[51] LiL, MaKT, ZhaoL, et al.. Niflumic acid hyperpolarizes the smooth muscle cells by opening BK(Ca) channels through ryanodine-sensitive Ca(2+) release in spiral modiolar artery. Sheng Li Xue Bao (Chinese), 2008, 60(6): 743-750

[52] LiL, MaKT, ZhaoL, et al.. Niflumic acid hyperpolarizes smooth muscle cells via calcium-activated potassium channel in spiral modiolar artery of guinea pigs. Acta Pharmacol Sin, 2008, 29(7): 789-799

[53] HoggRC, WangQ, LargeWA. Action of niflumic acid on evoked and spontaneous calcium-activated chloride and potassium currents in smooth muscle cells from rabbit portal vein. Br J Pharmacol, 1994, 112(3): 977-984

[54] CriddleDN, de MouraRS, GreenwoodIA, et al.. Inhibitory action of niflumic acid on noradrenaline- and 5-hydroxytryptamine-induced pressure responses in the isolated mesenteric vascular bed of the rat. Br J Pharmacol, 1997, 120(5): 813-818

[55] ChristGJ, MorenoAP, MelmanA, et al.. Gap junction-mediated intercellular diffusion of Ca2+ in cultured human corporal smooth muscle cells. Am J Physiol, 1992, 263(2Pt1): C373-383

[56] ChristGJ, MorenoAP, ParkerME, et al.. Intercellular communication through gap junctions: a potential role in pharmacomechanical coupling and syncytial tissue contraction in vascular smooth muscle isolated from the human corpus cavernosum. Life Sci, 1991, 49(24): PL195-200

[57] ChristGJ, SprayDC, el-SabbanM, et al.. Gap junctions in vascular tissues. Evaluating the role of intercellular communication in the modulation of vasomotor tone. Circ Res, 1996, 79(4): 631-646

[58] LiL, MaKT, ZhaoL, et al.. Myoendothelial coupling is unidirectional in guinea pig spiral modiolar arteries. Microvasc Res, 2012, 84(2): 211-217

[59] EarleyS, RestaTC, WalkerBR. Disruption of smooth muscle gap junctions attenuates myogenic vasoconstriction of mesenteric resistance arteries. Am J Physiol Heart Circ Physiol, 2004, 287(6): H2677-2686

[60] AndersonCM, LopezF, ZhangHY, et al.. Reduced uteroplacental perfusion alters uterine arcuate artery function in the pregnant Sprague-Dawley rat. Biol Reprod, 2005, 72(3): 762-766

[61] MaubanJR, LamontC, BalkeCW, et al.. Adrenergic stimulation of rat resistance arteries affects Ca(2+) sparks, Ca(2+) waves, and Ca(2+) oscillations. Am J Physiol Heart Circ Physiol, 2001, 280(5): H2399-2405

[62] MatchkovVV, RahmanA, PengH, et al.. Junctional and nonjunctional effects of heptanol and glycyrrhetinic acid derivates in rat mesenteric small arteries. Br J Pharmacol, 2004, 142(6): 961-972

[63] ChaytorAT, EvansWH, GriffithTM. Peptides homologous to extracellular loop motifs of connexin 43 reversibly abolish rhythmic contractile activity in rabbit arteries. J Physiol, 1997, 503(Pt1): 99-110

[64] TsaiML, WattsSW, Loch-CarusoR, et al.. The role of gap junctional communication in contractile oscillations in arteries from normotensive and hypertensive rats. J Hypertens, 1995, 13(10): 1123-1133

[65] SellM, BoldtW, MarkwardtF. Desynchronising effect of the endothelium on intracellular Ca2+ concentration dynamics in vascular smooth muscle cells of rat mesenteric arteries. Cell Calcium, 2002, 32(2): 105-120

[66] TareM, ColemanHA, ParkingtonHC. Glycyrrhetinic derivatives inhibit hyperpolarization in endothelial cells of guinea pig and rat arteries. Am J Physiol Heart Circ Physiol, 2002, 282(1): H335-341

[67] JacksonWF, MulschA, BusseR. Rhythmic smooth muscle activity in hamster aortas is mediated by continuous release of NO from the endothelium. Am J Physiol, 1991, 260(1Pt2): H248-253