Activation of Ca 2+-activated Cl - channels by store-operated Ca 2+ entry in arterial smooth muscle cells does not require reverse-mode Na +/Ca 2+ exchange

Canadian Journal of Physiology and Pharmacology

Volumn 90, Issue 7, 2012, Pages 903-921

  Angermann, Jeff E ^a   Forrest, Abigail S ^b   Greenwood, Iain A ^c   Leblanc, Normand ^b  

^a UNIVERSITY OF NEVADA   (United States)

^b UNIVERSITY OF NEVADA SCHOOL OF MEDICINE   (United States)

^c ST GEORGE'S UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Calcium activated chloride channels; Pulmonary hypertension; Sodium calcium exchange; Store operated calcium entry; Vascular smooth muscle cells

Indexed keywords

1 [2 (4 METHOXYPHENYL) 2 [3 (4 METHOXYPHENYL)PROPOXY]ETHYL] 1H IMIDAZOLE; 2 [2 [4 (4 NITROBENZYLOXY)PHENYL]ETHYL]ISOTHIOUREA METHANESULFONATE; CALCIUM CHANNEL; CALCIUM ION; CHLORIDE CHANNEL; CYCLOPIAZONIC ACID; NIFEDIPINE; NIFLUMIC ACID; SODIUM ION; STORE OPERATED CALCIUM ION CHANNEL ENTRY; UNCLASSIFIED DRUG; ANILINE DERIVATIVE; CALCIUM; CHLORIDE; FLUO 4; SODIUM CALCIUM EXCHANGE PROTEIN; XANTHENE DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG INHIBITION; ELECTROPHYSIOLOGY; HYPERPOLARIZATION; LUNG ALVEOLUS CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PATCH CLAMP; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SMOOTH MUSCLE FIBER; ANIMAL; ARTERY; KINETICS; METABOLISM; RABBIT; VASCULAR SMOOTH MUSCLE;

ANILINE COMPOUNDS; ANIMALS; ARTERIES; CALCIUM; CHLORIDE CHANNELS; CHLORIDES; KINETICS; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; RABBITS; SODIUM-CALCIUM EXCHANGER; XANTHENES;

EID: 84863665615     PISSN: 00084212     EISSN: 12057541     Source Type: Journal    
DOI: 10.1139/Y2012-081     Document Type: Article

References (91)

1. Aickin, C.C., and Brading, A.F. 1982. Measurement of intracellular chloride in guinea-pig vas deferens by ion analysis, chloride efflux and micro-electrodes. J. Physiol. 326: 139-154. PMID:7108787.
2. Albert, A.P., Saleh, S.N., Peppiatt-Wildman, C.M., and Large, W.A. 2007. Multiple activation mechanisms of store-operated TRPC channels in smooth muscle cells. J. Physiol. 583(1): 25-36. doi:10. 1113/jphysiol.2007.137802. PMID:17615095.
3. Alicia, S., Angelica, Z., Carlos, S., Alfonso, S., and Vaca, L. 2008. STIM1 converts TRPC1 from a receptor-operated to a store-operated channel: Moving TRPC1 in and out of lipid rafts. Cell Calcium, 44(5): 479-491. doi:10.1016/j.ceca.2008.03.001. PMID: 18420269.
4. - currents by phosphorylation in pulmonary arterial smooth muscle cells. J. Gen. Physiol. 128(1): 73-87. doi:10.1085/ jgp.200609507. PMID:16801382.
5. - currents in pulmonary arterial smooth muscle cells. J. Biol. Chem. 284(47): 32507-32521. doi:10.1074/jbc. M109.050401. PMID:19767392.
6. 2+ sparks in mouse airway smooth muscle. J. Gen. Physiol. 132(1): 145-160. doi:10.1085/jgp.200709933. PMID: 18591421.
7. 2+]i transients in guinea pig ventricular myocytes. Circ. Res. 61: 148-154. doi:10.1161/01.RES.61.1.148.
8. 2+ pump in proliferating human arterial myocytes. Am. J. Physiol. Cell Physiol. 297(5): C1103-C1112. doi:10.1152/ajpcell.00283.2009. PMID: 19675303.
9. Beech, D.J., Muraki, K., and Flemming, R. 2004. Non-selective cationic channels of smooth muscle and the mammalian homo-logues of Drosophila TRP. J. Physiol. 559(3): 685-706. PMID: 15272031.
10. 2+. J. Physiol. 414: 499-520. PMID:2607439.
11. 2+ entry. Nat. Cell Biol. 11(6): 669-677. doi:10.1038/ncb0609-669. PMID: 19488056.
12. Caputo, A., Caci, E., Ferrera, L., Pedemonte, N., Barsanti, C., Sondo, E., et al. 2008. TMEM16A, a membrane protein associated with calcium-dependent chloride channel activity. Science, 322(5901): 590-594. doi:10.1126/science.1163518. PMID:18772398.
13. Chipperfield, A.R., and Harper, A.A. 2000. Chloride in smooth muscle. Prog. Biophys. Mol. Biol. 74(3-5): 175-221. doi:10.1016/ S0079-6107(00)00024-9. PMID:11226512.
14. Davis, A.J., Forrest, A.S., Jepps, T.A., Valencik, M.L., Wiwchar, M., Singer, C.A., et al. 2010. Expression profile and protein translation of TMEM16A in murine smooth muscle. Am. J. Physiol. Cell Physiol. 299(5): C948-C959. doi:10.1152/ajpcell.00018.2010. PMID:20686072.
15. DeHaven, W.I., Smyth, J.T., Boyles, R.R., and Putney, J.W., Jr. 2007. Calcium inhibition and calcium potentiation of Orai1, Orai2, and Orai3 calcium release-activated calcium channels. J. Biol. Chem. 282(24): 17548-17556. doi:10.1074/jbc.M611374200. PMID: 17452328.
16. Edwards, G., and Weston, A.H. 1994. K-ATP - fact or artefact? new thoughts on the mode of action of the potassium channel openers. Cardiovasc. Res. 28(6): 735-737. doi:10.1093/cvr/28.6.735. PMID:7923272.
17. Edwards, G., Niederstehollenberg, A., Schneider, J., Noack, T., and Weston, A.H. 1994. Ion channel modulation by NS 1619, the putative BKCa channel opener, in vascular smooth muscle. Br. J. Pharmacol. 113(4): 1538-1547. PMID:7534190.
18. Forrest, A.S., Angermann, J.E., Raghunathan, R., Lachendro, C, Greenwood, I.A., and Leblanc, N. 2010. Intricate interaction between store-operated calcium entry and calcium-activated chloride channels in pulmonary artery smooth muscle cells. Adv. Exp. Med. Biol. 661: 31-55. doi:10.1007/978-1-60761-500-2_3. PMID:20204722.
19. 2+ entry in human pulmonary artery myocytes during proliferation. Am. J. Physiol. Heart Circ. Physiol. 280(2): H746-H755. PMID:11158974.
20. Greenwood, I.A., and Large, WA. 1995. Comparison of the effects of fenamates on Ca-activated chloride and potassium currents in rabbit portal vein smooth muscle cells. Br. J. Pharmacol. 116(7): 2939-2948. PMID:8680728.
21. Greenwood, I.A., and Large, WA. 1996. Analysis of the time course of calcium-activated chloride "tail" currents in rabbit portal vein smooth muscle cells. Pflugers Arch. 432(6): 970-979. doi:10. 1007/s004240050224. PMID:8781190.
22. 2+-calmodulin-dependent kinase. J. Physiol. 534(2): 395-408. doi:10.1111/j.1469-7793. 2001.00395.x. PMID:11454959.
23. Greenwood, I.A., Ledoux, J., Sanguinetti, A., Perrino, B.A., and Leblanc, N. 2004. Calcineurin Aa but not Ab augments ICl(Ca) in rabbit pulmonary artery smooth muscle cells. J. Biol. Chem. 279(37): 38830-38837. doi:10.1074/jbc.M406234200. PMID:15247251.
24. Guibert, C, Ducret, T., and Savineau, J.P. 2008. Voltage-independent calcium influx in smooth muscle. Prog. Biophys. Mol. Biol. 98(1): 10-23. doi:10.1016/j.pbiomolbio.2008.05.001. PMID:18614208.
25. 2+ entry in human platelets: evidence against the de novo conformational coupling hypothesis. Cell Calcium, 42(6): 606-617. doi:10.1016/j.ceca.2007.02.004. PMID:17383000.
26. - channels. J. Physiol. 587(10): 2127-2139. doi:10.1113/jphysiol. 2008.163709. PMID:19015192.
27. 2+ and NO. Am. J. Physiol. Heart Circ. Physiol. 277(5): H1732-H1744.
28. Hirota, S., and Janssen, L.J. 2007. Store-refilling involves both L-type calcium channels and reverse-mode sodium-calcium exchange in airway smooth muscle. Eur. Respir. J. 30(2): 269-278. doi:10. 1183/09031936.00008507. PMID:17428814.
29. 2+ mobilization. Am. J. Physiol. Lung Cell. Mol. Physiol. 292(2): L438-L447. doi:10. 1152/ajplung.00222.2006. PMID:17041014.
30. Hogg, R.C., Wang, Q., and Large, W.A. 1993. Time course of spontaneous calcium-activated chloride currents in smooth muscle cells from the rabbit portal vein. J. Physiol. 464: 15-31. PMID: 8229796.
31. Hogg, R.C., Wang, Q., and Large, W.A. 1994a. 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. 112(3): 977-984. PMID:7921628.
32. Hogg, R.C., Wang, Q., and Large, W.A. 1994b. Effects of Cl channel blockers on Ca-activated chloride and potassium currents in smooth muscle cells from rabbit portal vein. Br. J. Pharmacol. 111(4): 1333-1341. PMID:8032620.
33. Janssen, L.J., and Sims, S.M. 1994. Spontaneous transient inward currents and rhythmicity in canine and guinea-pig tracheal smooth muscle cells. Pflugers Arch. 427(5-6): 473-480. doi:10.1007/BF00374263. PMID:7526333.
34. Jardin, I., Salido, G.M., and Rosado, J.A. 2008. Role of lipid rafts in the interaction between hTRPC1, Orai1 and STIM1. Channels (Austin), 2(6): 401-403. doi:10.4161/chan.2.6.7055. PMID: 18843204.
35. Kitamura, K., and Yamazaki, J. 2001. Chloride channels and their functional roles in smooth muscle tone in the vasculature. Jpn. J. Pharmacol. 85(4): 351-357. doi:10.1254/jjp.85.351. PMID: 11388637.
36. Klöckner, U. 1993. Intracellular calcium ions activate a low-conductance chloride channel in smooth-muscle cells isolated from human mesenteric artery. Pflugers Arch. 424(3-4): 231-237. doi:10.1007/BF00384347. PMID:8414911.
37. 2+ signaling. Am. J. Physiol. Heart Circ. Physiol. 302(8): H1546-H1562. doi:10.1152/ajpheart.00944.2011. PMID: 22245772.
38. 2+ entry. Am. J. Physiol. Lung Cell. Mol. Physiol. 287(5): L962-L969. doi:10. 1152/ajplung.00452.2003. PMID:15220115.
39. Lamb, F.S., Volk, K.A., and Shibata, E.F. 1994. Calcium-activated chloride current in rabbit coronary artery myocytes. Circ. Res. 75(4): 742-750. doi:10.1161/01.RES.75.4.742. PMID:7923619.
40. - conductance in smooth muscle. Am. J. Physiol. Cell Physiol. 271(2): C435-C454.
41. 2+ exchange in rabbit portal vein smooth muscle. Am. J. Physiol. Heart Circ. Physiol. 268(5): H1906-H1917. PMID:7771540.
42. Leblanc, N., Ledoux, J., Saleh, S., Sanguinetti, A., Angermann, J., O'Driscoll, K., et al. 2005. Regulation of calcium-activated chloride channels in smooth muscle cells: a complex picture is emerging. Can. J. Physiol. Pharmacol. 83(7): 541-556. doi:10. 1139/y05-040. PMID:16091780.
43. - channels by calcineurin in rabbit coronary arterial myocytes. J. Physiol. 552(3): 701-714. doi:10.1113/jphysiol.2003.043836. PMID:12937294.
44. - channel modulation by niflumic acid in rabbit coronary arterial myocytes. Mol. Pharmacol. 67(1): 163-173. doi:10.1124/mol.104.004168. PMID:15465927.
45. 2+ channels in pulmonary arterial smooth muscle cells: a novel mechanism of hypoxic pulmonary hypertension. Circ. Res. 95(5): 496-505. doi:10.1161/ 01.RES.0000138952.16382.ad. PMID:15256480.
46. 2+ influx. Curr. Biol. 15(13): 1235-1241. doi:10.1016/j.cub.2005.05.055. PMID:16005298.
47. 2+ entry and TRPC channel expression in pulmonary arteries of monocrotaline-induced pulmonary hypertensive rats. Am. J. Physiol. Cell Physiol. 302(1): C77-C87. doi:10.1152/ajpcell.00247.2011. PMID:21940663.
48. 2+ responses to hypoxia. Am. J. Physiol. Lung Cell. Mol. Physiol. 295(1): L104-L113. doi:10.1152/ajplung. 00058.2008. PMID:18424621.
49. 2+ entry: local activation of CRAC channels by STIM1 at ER-plasma membrane junctions. J. Cell Biol. 174(6): 815-825. doi:10.1083/jcb.200604015. PMID: 16966423.
50. Luik, R.M., Wang, B., Prakriya, M., Wu, M.M., and Lewis, R.S. 2008. Oligomerization of STIM1 couples ER calcium depletion to CRAC channel activation. Nature, 454(7203): 538-542. doi:10.1038/nature07065. PMID:18596693.
51. Manoury, B., Tamuleviciute, A., and Tammaro, P. 2010. TMEM16A/ Anoctamin1 protein mediates calcium-activated chloride currents in pulmonary arterial smooth muscle cells. J. Physiol. 588(13): 2305-2314. doi:10.1113/jphysiol.2010.189506. PMID:20421283.
52. - current in retinal arteriolar smooth muscle. Invest. Ophthalmol. Vis. Sci. 50(1): 364-371. doi:10.1167/iovs.08-2524. PMID:18775864.
53. Nelson, M.T., Cheng, H., Rubart, M., Santana, L.F., Bonev, A.D., Knot, H.J., and Lederer, W.J. 1995. Relaxation of arterial smooth muscle by calcium sparks. Science, 270(5236): 633-637. doi:10. 1126/science.270.5236.633. PMID:7570021.
54. 2 + influx and contraction in rat pulmonary artery. Circ. Res. 89(10): 923-929. doi:10.1161/hh2201.100315. PMID:11701620.
55. 2+ entry in mouse pulmonary arterial smooth muscle cells. J. Physiol. 587(11): 2429-2442. doi:10.1113/ jphysiol.2009.172254. PMID:19332490.
56. Pacaud, P., Loirand, G., Lavie, J.L., Mironneau, C., and Mironneau, J. 1989. Calcium-activated chloride current in rat vascular smooth muscle cells in short-term primary culture. Pflugers Arch. 413(6): 629-636. doi:10.1007/BF00581813. PMID:2726425.
57. Pacaud, P., Loirand, G., Grégoire, G., Mironneau, C., and Mironneau, J. 1992. Calcium-dependence of the calcium-activated chloride current in smooth muscle cells of rat portal vein. Pflugers Arch. 421(2-3): 125-130. doi:10.1007/BF00374818. PMID:1382263.
58. 2+ entry (SOCE). J. Biol. Chem. 283(25): 17333-17340. doi:10.1074/jbc.M800107200. PMID:18430726.
59. Peel, S.E., Liu, B., and Hall, I.P. 2008. ORAI and store-operated calcium influx in human airway smooth muscle cells. Am. J. Respir. Cell Mol. Biol. 38(6): 744-749. doi:10.1165/rcmb.2007-0395OC. PMID:18239188.
60. 2+ entry and transient receptor potential canonical and vanilloid-related proteins in rat distal pulmonary venous smooth muscle. Am. J. Physiol. Lung Cell. Mol. Physiol. 299(5): L621-L630. doi:10.1152/ajplung. 00176.2009. PMID:20693314.
61. Penna, A., Demuro, A., Yeromin, A.V., Zhang, S.L., Safrina, O., Parker, I., and Cahalan, M.D. 2008. The CRAC channel consists of a tetramer formed by STIM-induced dimerization of Orai dimers. Nature, 456(7218): 116-120. doi:10.1038/nature07338. PMID:18820677.
62. Philipson, K.D., and Nicoll, D.A. 2000. Sodium-calcium exchange: A molecular perspective. Annu. Rev. Physiol. 62(1): 111-133. doi:10.1146/annurev.physiol.62.1.111. PMID:10845086.
63. Pifferi, S., Dibattista, M., and Menini, A. 2009. TMEM16B induces chloride currents activated by calcium in mammalian cells. Pflugers Arch. 458(6): 1023-1038. doi:10.1007/s00424-009-0684-9. PMID:19475416.
64. - channels in rabbit pulmonary artery smooth muscle cells. J. Physiol. 547(1): 181-196. doi:10.1113/ jphysiol.2002.033688. PMID:12562904.
65. - currents in rabbit pulmonary artery smooth muscle cells. J. Physiol. 539(1): 119-131. doi:10.1113/jphysiol.2001.013270. PMID:11850506.
66. 2+ entry in purinergically stimulated aorta smooth muscle cells. Circ. Res. 101(10): 1030-1038. doi:10.1161/CIRCRESAHA.107.155531. PMID:17872462.
67. Potier, M., Gonzalez, J.C., Motiani, R.K., Abdullaev, I.F., Bisaillon, J.M., Singer, H.A., and Trebak, M. 2009. Evidence for STIM1-and Orai1-dependent store-operated calcium influx through ICRAC in vascular smooth muscle cells: role in proliferation and migration. FASEB J. 23(8): 2425-2437. doi:10.1096/fj.09-131128. PMID:19364762.
68. Prakriya, M., Feske, S., Gwack, Y., Srikanth, S., Rao, A., and Hogan, P.G. 2006. Orai1 is an essential pore infunit of the CRAC channel. Nature, 443(7108): 230-233. doi:10.1038/nature05122. PMID: 16921383.
69. Remillard, C.V., and Yuan, J.X. 2006a. Transient receptor potential channels and caveolin-1: good friends in tight spaces. Mol. Pharmacol. 70(4): 1151-1154. doi:10.1124/mol.106.029280.PMID:16873578.
70. Remillard, C.V., and Yuan, J.X. 2006b. TRP channels, CCE, and the pulmonary vascular smooth muscle. Microcirculation, 13(8): 671-692. doi:10.1080/10739680600930313. PMID:17085427.
71. Schroeder, B.C., Cheng, T., Jan, Y.N., and Jan, L.Y. 2008. Expression cloning of TMEM16A as a calcium-activated chloride channel infunit. Cell, 134(6): 1019-1029. doi:10.1016/j.cell.2008.09.003. PMID:18805094.
72. 2+-ATPase of sarcoplasmic reticulum. J. Biol. Chem. 264(30): 17816-17823. PMID:2530215.
73. Shen, W.W., Frieden, M., and Demaurex, N. 2011. Remodelling of the endoplasmic reticulum during store-operated calcium entry. Biol. Cell, 103(8): 365-380. doi:10.1042/BC20100152. PMID: 21736554.
74. 2+ exchange -Molecular and pharmacological aspects. Circ. Res. 88(9): 864-876. doi:10.1161/hh0901.090298. PMID:11348995.
75. 2+]i, and ET-1-induced responses in chronically hypoxic pulmonary myocytes. Am. J. Physiol. Lung Cell. Mol. Physiol. 279(5): L884-L894. PMID:11053024.
76. Song, M.Y., Makino, A., and Yuan, J.X. 2011. STIM2 contributes to enhanced store-operated Ca entry in pulmonary artery smooth muscle cells from patients with idiopathic pulmonary arterial hypertension. Pulm. Circ. 1(1): 84-94. doi:10.4103/2045-8932.78106. PMID:21709766.
77. 2+ entry and attenuates pulmonary artery smooth muscle cell proliferation. Am. J. Physiol. Lung Cell. Mol. Physiol. 283(1): L144-L155. doi:10.1152/ajplung.00412.2001. PMID: 12060571.
78. 2+-activated Cl currents in cerebral artery smooth muscle cells. Am. J. Physiol. Heart Circ. Physiol. 301(5): H1819-H1827. doi:10.1152/ajpheart.00404.2011. PMID:21856902.
79. van Renterghem, C., and Lazdunski, M. 1993. Endothelin and vasopressin activate low conductance chloride channels in aortic smooth muscle cells. Pflugers Arch. 425(1-2): 156-163. doi:10.1007/BF00374516. PMID:8272371.
80. Vazquez, G., Wedel, B.J., Aziz, O., Trebak, M., and Putney, J.W., Jr. 2004. The mammalian TRPC cation channels. Biochim. Biophys. Acta, 1742(1-3): 21-36. doi:10.1016/j.bbamcr.2004.08.015. PMID:15590053.
81. Wang, Q., Hogg, R.C., and Large, W.A. 1992. Properties of spontaneous inward currents recorded in smooth muscle cells isolated from the rabbit portal vein. J.Physiol. 451: 525-537. PMID:1403823.
82. Wang, J., Shimoda, L.A., and Sylvester, J.T. 2004. Capacitative calcium entry and TRPC channel proteins are expressed in rat distal pulmonary arterial smooth muscle. Am. J. Physiol. Lung Cell. Mol. Physiol. 286(4): L848-L858. doi:10.1152/ajplung. 00319.2003. PMID:14672922.
83. - channels in rabbit pulmonary arterial smooth muscle cells. Br. J. Pharmacol. 158(5): 1356-1365. doi:10.1111/j.1476-5381.2009. 00405.x. PMID:19785656.
84. 2+ channels in native vascular smooth muscle cells. Circ. Res. 88(1): 84-87. doi:10.1161.01.RES.88.1.84. PMID:11139478.
85. Yamamura, A., Yamamura, H., Zeifman, A., and Yuan, J.X. 2011. Activity of Ca-activated Cl channels contributes to regulating receptor- and store-operated Ca entry in human pulmonary artery smooth muscle cells. Pulm. Circ. 1(2): 269-279. doi:10.4103/2045-8932.83447. PMID:22034612.
86. Yang, Y.D., Cho, H., Koo, J.Y., Tak, M.H., Cho, Y., Shim, W.S., et al. 2008. TMEM16A confers receptor-activated calcium-dependent chloride conductance. Nature, 455(7217): 1210-1215. doi:10.1038/nature07313. PMID:18724360.
87. Yeromin, A.V., Zhang, S.L., Jiang, W., Yu, Y., Safrina, O., and Cahalan, M.D. 2006. Molecular identification of the CRAC channel by altered ion selectivity in a mutant of Orai. Nature, 443(7108): 226-229. doi:10.1038/nature05108. PMID:16921385.
88. Yuan, X.J. 1997. Role of calcium-activated chloride current in regulating pulmonary vasomotor tone. Am. J. Physiol. 272(5): L959-L968. PMID:9176262.
89. 2+ entry. Am. J. Physiol. Lung Cell. Mol. Physiol. 292(5): L1202-L1210. doi:10.1152/ajplung.00214.2006. PMID:17189322.
90. 2+ in cultured human pulmonary artery smooth muscle cells. Am. J. Physiol. Cell Physiol. 288(2): C245-C252. doi:10.1152/ajpcell.00411.2004. PMID:15456699.
91. 2+ store to the plasma membrane. Nature, 437(7060): 902-905. doi:10.1038/nature04147. PMID:16208375.