Ryanodine Receptors, Calcium Signaling, and Regulation of Vascular tone in the cerebral parenchymal microcirculation

Microcirculation

Volumn 20, Issue 4, 2013, Pages 307-316

  Dabertrand, Fabrice ^a   Nelson, Mark T ^a,b   Brayden, Joseph E ^a  

^a UNIVERSITY OF VERMONT   (United States)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Acidosis; Brain parenchymal arteriole; Cerebral blood flow; Potassium channel; Ryanodine receptor

Indexed keywords

INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR; RYANODINE RECEPTOR;

ACIDOSIS; AUTOREGULATION; BLOOD VESSEL TONE; BRAIN BLOOD FLOW; BRAIN CIRCULATION; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; HUMAN; MICROCIRCULATION; MUSCLE CELL; PHYSIOLOGY; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; SARCOPLASMIC RETICULUM; VASCULARIZATION; VASOCONSTRICTION;

ANIMALS; CALCIUM SIGNALING; CEREBRAL CORTEX; CEREBROVASCULAR CIRCULATION; HUMANS; MICROCIRCULATION; MUSCLE TONUS; MUSCLE, SMOOTH, VASCULAR; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL;

EID: 84877664270     PISSN: 10739688     EISSN: 15498719     Source Type: Journal    
DOI: 10.1111/micc.12027     Document Type: Review

References (134)

1. Amos BJ, Mathie A, Richards CD. Activation of group I metabotropic glutamate receptors elicits pH changes in cultured rat cortical glia and neurons. Neuroscience 86: 1109-1120, 1998.
2. Andresen JJ, Shafi NI, Durante W, Bryan RM Jr. Effects of carbon monoxide and heme oxygenase inhibitors in cerebral vessels of rats and mice. Am J Physiol Heart Circ Physiol 291: H223-H230, 2006.
3. Apkon M, Boron WF. Extracellular and intracellular alkalinization and the constriction of rat cerebral arterioles. J Physiol 484(Pt III): 743-753, 1995.
4. 2+ signalling in rat portal vein myocytes. Cell Calcium 22: 399-411, 1997.
5. Attwell D, Buchan AM, Charpak S, Lauritzen M, Macvicar BA, Newman EA. Glial and neuronal control of brain blood flow. Nature 468: 232-243, 2010.
6. Austin C, Dilly K, Eisner D, Wray S. Simultaneous measurement of intracellular pH, calcium, and tension in rat mesenteric vessels: effects of extracellular pH. Biochem Biophys Res Commun 222: 537-540, 1996.
7. + depolarization. J Physiol 469: 1-10, 1993.
8. Austin C, Wray S. Interactions between Ca(2+) and H(+) and functional consequences in vascular smooth muscle. Circ Res 86: 355-363, 2000.
9. Bayliss WM. On the local reactions of the arterial wall to changes of internal pressure. J Physiol 28: 220-231, 1902.
10. Berridge MJ. Elementary and global aspects of calcium signalling. J Physiol 499(Pt II): 291-306, 1997.
11. Berridge MJ. Smooth muscle cell calcium activation mechanisms. J Physiol 586: 5047-5061, 2008.
12. Berridge MJ. Inositol trisphosphate and calcium signalling mechanisms. Biochim Biophys Acta 1793: 933-940, 2009.
13. Berridge MJ, Lipp P, Bootman MD. The versatility and universality of calcium signalling. Nat Rev Mol Cell Biol 1: 11-21, 2000.
14. Bezprozvanny I, Ehrlich BE. Inositol (1, 4, 5)-trisphosphate (InsP3)-gated Ca channels from cerebellum: conduction properties for divalent cations and regulation by intraluminal calcium. J Gen Physiol 104: 821-856, 1994.
15. Bezprozvanny I, Watras J, Ehrlich BE. Bell-shaped calcium-response curves of Ins(1, 4, 5)P3- and calcium-gated channels from endoplasmic reticulum of cerebellum. Nature 351: 751-754, 1991.
16. Bootman MD, Berridge MJ. The elemental principles of calcium signaling. Cell 83: 675-678, 1995.
17. 2+. Biochem J 306(Pt II): 445-451, 1995.
18. Bovo E, Mazurek SR, Blatter LA, Zima AV. Regulation of sarcoplasmic reticulum Ca(2)(+) leak by cytosolic Ca(2)(+) in rabbit ventricular myocytes. J Physiol 589: 6039-6050, 2011.
19. Brandt NR, Caswell AH, Brandt T, Brew K, Mellgren RL. Mapping of the calpain proteolysis products of the junctional foot protein of the skeletal muscle triad junction. J Membr Biol 127: 35-47, 1992.
20. Cheng H, Lederer WJ, Cannell MB. Calcium sparks: elementary events underlying excitation-contraction coupling in heart muscle. Science 262: 740-744, 1993.
21. Cheng H, Lederer MR, Lederer WJ, Cannell MB. Calcium sparks and [Ca2+]i waves in cardiac myocytes. Am J Physiol 270: C148-C159, 1996.
22. Chesler M, Kraig RP. Intracellular pH of astrocytes increases rapidly with cortical stimulation. Am J Physiol 253: R666-R670, 1987.
23. Cipolla MJ, Li R, Vitullo L. Perivascular innervation of penetrating brain parenchymal arterioles. J Cardiovasc Pharmacol 44: 1-8, 2004.
24. Cipolla MJ, Smith J, Kohlmeyer MM, Godfrey JA. SKCa and IKCa channels, myogenic tone, and vasodilator responses in middle cerebral arteries and parenchymal arterioles: effect of ischemia and reperfusion. Stroke 40: 1451-1457, 2009.
25. Dabertrand F, Fritz N, Mironneau J, Macrez N, Morel JL. Role of RYR3 splice variants in calcium signaling in mouse nonpregnant and pregnant myometrium. Am J Physiol Cell Physiol 293: C848-C854, 2007.
26. Dabertrand F, Mironneau J, Henaff M, Macrez N, Morel JL. Comparison between gentamycin and exon skipping treatments to restore ryanodine receptor subtype 2 functions in mdx mouse duodenum myocytes. Eur J Pharmacol 628: 36-41, 2010.
27. Dabertrand F, Mironneau J, Macrez N, Morel JL. Full length ryanodine receptor subtype 3 encodes spontaneous calcium oscillations in native duodenal smooth muscle cells. Cell Calcium 44: 180-189, 2008.
28. Dabertrand F, Morel JL, Sorrentino V, Mironneau J, Mironneau C, Macrez N. Modulation of calcium signalling by dominant negative splice variant of ryanodine receptor subtype 3 in native smooth muscle cells. Cell Calcium 40: 11-21, 2006.
29. Dabertrand F, Nelson MT, Brayden JE. Acidosis dilates brain parenchymal arterioles by conversion of calcium waves to sparks to activate BK channels. Circ Res 110: 285-294, 2012.
30. Dabertrand F, Porte Y, Macrez N, Morel JL. Spaceflight regulates ryanodine receptor subtype 1 in portal vein myocytes in the opposite way of hypertension. J Appl Physiol 112: 471-480, 2012.
31. 2+ signaling complex with ryanodine receptors and BKCa channels. Circ Res 97: 1270-1279, 2005.
32. Edwards RM, Stack EJ, Trizna W. Calcitonin gene-related peptide stimulates adenylate cyclase and relaxes intracerebral arterioles. J Pharmacol Exp Ther 257: 1020-1024, 1991.
33. Faraci FM, Heistad DD. Regulation of large cerebral arteries and cerebral microvascular pressure. Circ Res 66: 8-17, 1990.
34. Fernandez-Klett F, Offenhauser N, Dirnagl U, Priller J, Lindauer U. Pericytes in capillaries are contractile in vivo, but arterioles mediate functional hyperemia in the mouse brain. Proc Natl Acad Sci U S A 107: 22290-22295, 2010.
35. Fill M, Copello JA. Ryanodine receptor calcium release channels. Physiol Rev 82: 893-922, 2002.
36. Filosa JA, Bonev AD, Nelson MT. Calcium dynamics in cortical astrocytes and arterioles during neurovascular coupling. Circ Res 95: e73-e81, 2004.
37. Filosa JA, Bonev AD, Straub SV, Meredith AL, Wilkerson MK, Aldrich RW, Nelson MT. Local potassium signaling couples neuronal activity to vasodilation in the brain. Nat Neurosci 9: 1397-1403, 2006.
38. Finch EA, Turner TJ, Goldin SM. Calcium as a coagonist of inositol 1, 4, 5-trisphosphate-induced calcium release. Science 252: 443-446, 1991.
39. Fleming BP, Barron KW, Howes TW, Smith JK. Response of the microcirculation in rat cremaster muscle to peripheral and central sympathetic stimulation. Circ Res 61: II26-II31, 1987.
40. 2+ release channels. Physiol Rev 87: 593-658, 2007.
41. Franzini-Armstrong C. STUDIES OF THE TRIAD: I. Structure of the junction in frog twitch fibers. J Cell Biol 47: 488-499, 1970.
42. Gebremedhin D, Ma YH, Falck JR, Roman RJ, VanRollins M, Harder DR. Mechanism of action of cerebral epoxyeicosatrienoic acids on cerebral arterial smooth muscle. Am J Physiol 263: H519-H525, 1992.
43. Giannini G, Sorrentino V. Molecular structure and tissue distribution of ryanodine receptors calcium channels. Med Res Rev 15: 313-323, 1995.
44. 2+ and BK channels determine both arteriolar dilation and constriction. Proc Natl Acad Sci U S A 107: 3811-3816, 2010.
45. Gomez MF, Stevenson AS, Bonev AD, Hill-Eubanks DC, Nelson MT. 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 277: 37756-37764, 2002.
46. 2+ release from the sarcoplasmic reticulum is required for sustained TRPM4 activity in cerebral artery smooth muscle cells. Am J Physiol Cell Physiol 299: C279-C288, 2010.
47. Gordienko DV, Bolton TB. Crosstalk between ryanodine receptors and IP(3) receptors as a factor shaping spontaneous Ca(2+)-release events in rabbit portal vein myocytes. J Physiol 542: 743-762, 2002.
48. Gordienko DV, Greenwood IA, Bolton TB. Direct visualization of sarcoplasmic reticulum regions discharging Ca(2+)sparks in vascular myocytes. Cell Calcium 29: 13-28, 2001.
49. Hamel E. Perivascular nerves and the regulation of cerebrovascular tone. J Appl Physiol 100: 1059-1064, 2006.
50. Hamilton SL. Ryanodine receptors. Cell Calcium 38: 253-260, 2005.
51. Hannah RM, Dunn KM, Bonev AD, Nelson MT. Endothelial SK(Ca) and IK(Ca) channels regulate brain parenchymal arteriolar diameter and cortical cerebral blood flow. J Cereb Blood Flow Metab 31: 1175-1186, 2011.
52. Harder DR. A cellular mechanism for myogenic regulation of cat cerebral arteries. Ann Biomed Eng 13: 335-339, 1985.
53. 2+ waves in smooth muscle cells of pressurized cerebral arteries. Am J Physiol Heart Circ Physiol 283: H2169-H2176, 2002.
54. Hill-Eubanks DC, Werner ME, Heppner TJ, Nelson MT. Calcium signaling in smooth muscle. Cold Spring Harb Perspect Biol 3: a004549, 2011.
55. Hirsch S, Reichold J, Schneider M, Szekely G, Weber B. Topology and hemodynamics of the cortical cerebrovascular system. J Cereb Blood Flow Metab 32: 952-967, 2012.
56. +-induced local and conducted responses in cerebral penetrating arterioles. Stroke 33: 2692-2699, 2002.
57. Iadecola C. Neurovascular regulation in the normal brain and in Alzheimer's disease. Nat Rev Neurosci 5: 347-360, 2004.
58. Iadecola C, Nedergaard M. Glial regulation of the cerebral microvasculature. Nat Neurosci 10: 1369-1376, 2007.
59. Itoh Y, Suzuki N. Control of brain capillary blood flow. J Cereb Blood Flow Metab 32: 1167-1176, 2012.
60. Jaggar JH, Porter VA, Lederer WJ, Nelson MT. Calcium sparks in smooth muscle. Am J Physiol Cell Physiol 278: C235-C256, 2000.
61. 2+ stores in single smooth muscle cells from rat cerebral arteries. J Physiol 501(Pt III): 497-508, 1997.
62. 2+] in cerebral arteries of rat by membrane potential and intravascular pressure. J Physiol 508(Pt I): 199-209, 1998.
63. + channels. J Physiol 508(Pt I): 211-221, 1998.
64. + (BK) channels. Proc Natl Acad Sci U S A 109: E1387-E1395, 2012.
65. 2+ spark activity after subarachnoid hemorrhage disables BK channel control of cerebral artery tone. J Cereb Blood Flow Metab 31: 3-16, 2011.
66. Lanner JT, Georgiou DK, Joshi AD, Hamilton SL. Ryanodine receptors: structure, expression, molecular details, and function in calcium release. Cold Spring Harb Perspect Biol 2: a003996, 2010.
67. Lecrux C, Hamel E. The neurovascular unit in brain function and disease. Acta Physiol (Oxf) 203: 47-59, 2011.
68. Ledbetter MW, Preiner JK, Louis CF, Mickelson JR. Tissue distribution of ryanodine receptor isoforms and alleles determined by reverse transcription polymerase chain reaction. J Biol Chem 269: 31544-31551, 1994.
69. Ledoux J, Taylor MS, Bonev AD, Hannah RM, Solodushko V, Shui B, Tallini Y, Kotlikoff MI, Nelson MT. Functional architecture of inositol 1, 4, 5-trisphosphate signaling in restricted spaces of myoendothelial projections. Proc Natl Acad Sci U S A 105: 9627-9632, 2008.
70. Leffler CW, Parfenova H, Jaggar JH. Carbon monoxide as an endogenous vascular modulator. Am J Physiol Heart Circ Physiol 301: H1-H11, 2011.
71. Lipton P. Ischemic cell death in brain neurons. Physiol Rev 79: 1431-1568, 1999.
72. Liu X, Li C, Falck JR, Roman RJ, Harder DR, Koehler RC. Interaction of nitric oxide, 20-HETE, and EETs during functional hyperemia in whisker barrel cortex. Am J Physiol Heart Circ Physiol 295: H619-H631, 2008.
73. Lohn M, Jessner W, Furstenau M, Wellner M, Sorrentino V, Haller H, Luft FC, Gollasch M. Regulation of calcium sparks and spontaneous transient outward currents by RyR3 in arterial vascular smooth muscle cells. Circ Res 89: 1051-1057, 2001.
74. Magnotta VA, Heo HY, Dlouhy BJ, Dahdaleh NS, Follmer RL, Thedens DR, Welsh MJ, Wemmie JA. Detecting activity-evoked pH changes in human brain. Proc Natl Acad Sci U S A 109: 8270-8273, 2012.
75. Meininger GA, Davis MJ. Cellular mechanisms involved in the vascular myogenic response. Am J Physiol 263: H647-H659, 1992.
76. Metea MR, Newman EA. Glial cells dilate and constrict blood vessels: a mechanism of neurovascular coupling. J Neurosci 26: 2862-2870, 2006.
77. Monkawa T, Miyawaki A, Sugiyama T, Yoneshima H, Yamamoto-Hino M, Furuichi T, Saruta T, Hasegawa M, Mikoshiba K. Heterotetrameric complex formation of inositol 1, 4, 5-trisphosphate receptor subunits. J Biol Chem 270: 14700-14704, 1995.
78. Morel JL, Dabertrand F, Fritz N, Henaff M, Mironneau J, Macrez N. The decrease of expression of ryanodine receptor sub-type 2 is reversed by gentamycin sulphate in vascular myocytes from mdx mice. J Cell Mol Med 13: 3122-3130, 2009.
79. 2+ oscillations in vascular myocytes. Arterioscler Thromb Vasc Biol 23: 1567-1575, 2003.
80. Morikawa T, Kajimura M, Nakamura T, Hishiki T, Nakanishi T, Yukutake Y, Nagahata Y, Ishikawa M, Hattori K, Takenouchi T, Takahashi T, Ishii I, Matsubara K, Kabe Y, Uchiyama S, Nagata E, Gadalla MM, Snyder SH, Suematsu M. Hypoxic regulation of the cerebral microcirculation is mediated by a carbon monoxide-sensitive hydrogen sulfide pathway. Proc Natl Acad Sci U S A 109: 1293-1298, 2012.
81. Moskowitz MA, Lo EH, Iadecola C. The science of stroke: mechanisms in search of treatments. Neuron 67: 181-198, 2010.
82. 2+ waves. J Physiol 588: 3983-4005, 2010.
83. Narayanan D, Adebiyi A, Jaggar JH. Inositol trisphosphate receptors in smooth muscle cells. Am J Physiol Heart Circ Physiol 302: H2190-H2210, 2012.
84. Nedergaard M, Kraig RP, Tanabe J, Pulsinelli WA. Dynamics of interstitial and intracellular pH in evolving brain infarct. Am J Physiol 260: R581-R588, 1991.
85. Nelson MT, Cheng H, Rubart M, Santana LF, Bonev AD, Knot HJ, Lederer WJ. Relaxation of arterial smooth muscle by calcium sparks. Science 270: 633-637, 1995.
86. Ngai AC, Coyne EF, Meno JR, West GA, Winn HR. Receptor subtypes mediating adenosine-induced dilation of cerebral arterioles. Am J Physiol Heart Circ Physiol 280: H2329-H2335, 2001.
87. Nishimura N, Schaffer CB, Friedman B, Lyden PD, Kleinfeld D. Penetrating arterioles are a bottleneck in the perfusion of neocortex. Proc Natl Acad Sci U S A 104: 365-370, 2007.
88. Nystoriak MA, O'Connor KP, Sonkusare SK, Brayden JE, Nelson MT, Wellman GC. Fundamental increase in pressure-dependent constriction of brain parenchymal arterioles from subarachnoid hemorrhage model rats due to membrane depolarization. Am J Physiol Heart Circ Physiol 300: H803-812, 2010.
89. Ogawa Y, Kurebayashi N, Murayama T. Putative roles of type 3 ryanodine receptor isoforms (RyR3). Trends Cardiovasc Med 10: 65-70, 2000.
90. Osol G, Halpern W. Myogenic properties of cerebral blood vessels from normotensive and hypertensive rats. Am J Physiol 249: H914-H921, 1985.
91. + channels in cerebral vasodilatation induced by increases in cyclic GMP and cyclic AMP in the rat. Stroke 27: 1603-1607, 1996; discussion 1607-1608.
92. Peng X, Carhuapoma JR, Bhardwaj A, Alkayed NJ, Falck JR, Harder DR, Traystman RJ, Koehler RC. Suppression of cortical functional hyperemia to vibrissal stimulation in the rat by epoxygenase inhibitors. Am J Physiol Heart Circ Physiol 283: H2029-H2037, 2002.
93. 2+]i in rat cerebral arteries: is there a role for membrane potential?. Am J Physiol 274: H655-H662, 1998.
94. Peppiatt CM, Howarth C, Mobbs P, Attwell D. Bidirectional control of CNS capillary diameter by pericytes. Nature 443: 700-704, 2006.
95. Perez GJ, Bonev AD, Nelson MT. Micromolar Ca(2+) from sparks activates Ca(2+)-sensitive K(+) channels in rat cerebral artery smooth muscle. Am J Physiol Cell Physiol 281: C1769-C1775, 2001.
96. Petzold GC, Murthy VN. Role of astrocytes in neurovascular coupling. Neuron 71: 782-797, 2011.
97. Pozzan T, Rizzuto R, Volpe P, Meldolesi J. Molecular and cellular physiology of intracellular calcium stores. Physiol Rev 74: 595-636, 1994.
98. 2+ release channels. J Clin Invest 115: 2033-2038, 2005.
99. 2+ in myocytes from guinea-pig small mesenteric arteries. J Physiol 539: 25-39, 2002.
100. Raichle ME, Plum F. Hyperventilation and cerebral blood flow. Stroke 3: 566-575, 1972.
101. Rossi DJ, Brady JD, Mohr C. Astrocyte metabolism and signaling during brain ischemia. Nat Neurosci 10: 1377-1386, 2007.
102. Roy CS, Sherrington CS. On the regulation of the blood-supply of the brain. J Physiol 11: 85-158, 1890. 117.
103. Shi Y, Liu X, Gebremedhin D, Falck JR, Harder DR, Koehler RC. Interaction of mechanisms involving epoxyeicosatrienoic acids, adenosine receptors, and metabotropic glutamate receptors in neurovascular coupling in rat whisker barrel cortex. J Cereb Blood Flow Metab 28: 111-125, 2008.
104. 2+ binding site in the type I inositol 1, 4, 5-trisphosphate receptor. J Biol Chem 271: 27005-27012, 1996.
105. Siesjo BK. Pathophysiology and treatment of focal cerebral ischemia. Part I: Pathophysiology. J Neurosurg 77: 169-184, 1992.
106. Simard M, Arcuino G, Takano T, Liu QS, Nedergaard M. Signaling at the gliovascular interface. J Neurosci 23: 9254-9262, 2003.
107. Simon RP. Acidotoxicity trumps excitotoxicity in ischemic brain. Arch Neurol 63: 1368-1371, 2006.
108. Straub SV, Bonev AD, Wilkerson MK, Nelson MT. Dynamic inositol trisphosphate-mediated calcium signals within astrocytic endfeet underlie vasodilation of cerebral arterioles. J Gen Physiol 128: 659-669, 2006.
109. + channels. Circ Res 76: 1057-1062, 1995.
110. Takano T, Tian GF, Peng W, Lou N, Libionka W, Han X, Nedergaard M. Astrocyte-mediated control of cerebral blood flow. Nat Neurosci 9: 260-267, 2006.
111. Takeshima H, Nishimura S, Matsumoto T, Ishida H, Kangawa K, Minamino N, Matsuo H, Ueda M, Hanaoka M, Hirose T, Numa S. Primary structure and expression from complementary DNA of skeletal muscle ryanodine receptor. Nature 339: 439-445, 1989.
112. Tasker PN, Taylor CW, Nixon GF. Expression and distribution of InsP(3) receptor subtypes in proliferating vascular smooth muscle cells. Biochem Biophys Res Commun 273: 907-912, 2000.
113. Tian R, Vogel P, Lassen NA, Mulvany MJ, Andreasen F, Aalkjaer C. Role of extracellular and intracellular acidosis for hypercapnia-induced inhibition of tension of isolated rat cerebral arteries. Circ Res 76: 269-275, 1995.
114. Toda N, Hatano Y, Mori K. Mechanisms underlying response to hypercapnia and bicarbonate of isolated dog cerebral arteries. Am J Physiol 257: H141-H146, 1989.
115. Tu H, Wang Z, Bezprozvanny I. Modulation of mammalian inositol 1, 4, 5-trisphosphate receptor isoforms by calcium: a role of calcium sensor region. Biophys J 88: 1056-1069, 2005.
116. 2+-signals in myocytes of retinal arterioles. Cell Calcium 41: 451-466, 2007.
117. Tunwell RE, Wickenden C, Bertrand BM, Shevchenko VI, Walsh MB, Allen PD, Lai FA. The human cardiac muscle ryanodine receptor-calcium release channel: identification, primary structure and topological analysis. Biochem J 318(Pt II): 477-487, 1996.
118. Vaithianathan T, Narayanan D, Asuncion-Chin MT, Jeyakumar LH, Liu J, Fleischer S, Jaggar JH, Dopico AM. Subtype identification and functional characterization of ryanodine receptors in rat cerebral artery myocytes. Am J Physiol Cell Physiol 299: C264-C278, 2010.
119. Vinall PE, Simeone FA. Cerebral autoregulation: an in vitro study. Stroke 12: 640-642, 1981.
120. 2+-sensitive ion channels. Cell Calcium 34: 211-229, 2003.
121. Westcott EB, Goodwin EL, Segal SS, Jackson WF. Function and expression of ryanodine receptors and inositol 1, 4, 5-trisphosphate receptors in smooth muscle cells of murine feed arteries and arterioles. J Physiol 590: 1849-1869, 2012.
122. Westcott EB, Jackson WF. Heterogeneous function of ryanodine receptors, but not IP3 receptors, in hamster cremaster muscle feed arteries and arterioles. Am J Physiol Heart Circ Physiol 300: H1616-H1630, 2011.
123. Wray S, Burdyga T. Sarcoplasmic reticulum function in smooth muscle. Physiol Rev 90: 113-178, 2010.
124. 2+ release. Circ Res 102: 1118-1126, 2008.
125. Xi Q, Tcheranova D, Basuroy S, Parfenova H, Jaggar JH, Leffler CW. Glutamate-induced calcium signals stimulate CO production in piglet astrocytes. Am J Physiol Heart Circ Physiol 301: H428-H433, 2011.
126. 2+ signals in smooth muscle cells of newborn piglet brain slice arterioles through astrocyte- and heme oxygenase-dependent mechanisms. Am J Physiol Heart Circ Physiol 298: H562-H569, 2010.
127. 2+ release channels (ryanodine receptors). J Biol Chem 277: 41778-41785, 2002.
128. Xiong ZG, Zhu XM, Chu XP, Minami M, Hey J, Wei WL, MacDonald JF, Wemmie JA, Price MP, Welsh MJ, Simon RP. Neuroprotection in ischemia: blocking calcium-permeable acid-sensing ion channels. Cell 118: 687-698, 2004.
129. 2+ signals, and vasoconstriction in cerebral arteries. Am J Physiol Cell Physiol 295: C1376-C1384, 2008.
130. Zhao G, Neeb ZP, Leo MD, Pachuau J, Adebiyi A, Ouyang K, Chen J, Jaggar JH. Type 1 IP3 receptors activate BKCa channels via local molecular coupling in arterial smooth muscle cells. J Gen Physiol 136: 283-291, 2010.
131. 2+ sparks and spontaneous transient outward currents in single smooth muscle cells. J Gen Physiol 113: 215-228, 1999.
132. Ziemann AE, Allen JE, Dahdaleh NS, Drebot II, Coryell MW, Wunsch AM, Lynch CM, Faraci FM, Howard MA 3rd, Welsh MJ, Wemmie JA. The amygdala is a chemosensor that detects carbon dioxide and acidosis to elicit fear behavior. Cell 139: 1012-1021, 2009.
133. Zonta M, Angulo MC, Gobbo S, Rosengarten B, Hossmann KA, Pozzan T, Carmignoto G. Neuron-to-astrocyte signaling is central to the dynamic control of brain microcirculation. Nat Neurosci 6: 43-50, 2003.
134. 2+ release channel (ryanodine receptor) of skeletal muscle sarcoplasmic reticulum. J Biol Chem 265: 2244-2256, 1990.