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Calcium Signaling In Airway Smooth Muscle Cells pp 195–209Cite as

Novel Mechanisms in Ca2+ Homeostasis and Internal Store Refilling of Airway Smooth Muscle

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Abstract

Calcium is known to play a key role in excitation–contraction coupling of airway smooth muscle (ASM) and may also be important in other cellular responses, such as gene expression, migration, proliferation, and apoptosis. The sarcoplasmic reticulum acts as an agonist-releasable store of Ca2+ and as a sink to buffer changes in cytosolic [Ca2+]i. ASM also expresses, in great abundance, other Ca2+-mobilizing effectors such as voltage-dependent Ca2+ channels (Cav) and sodium/calcium exchangers (NCX) on the plasmalemma, as well as ryanodine receptors (RyRs) on the SR membrane. These three had long been held to be important in mediating electromechanical coupling (Cav), extrusion of cytosolic Ca2+ (NCX) and Ca2+-induced Ca2+ release (RyR), respectively. However, more recent data and careful consideration have challenged those associations. In this chapter, we explore the novel hypothesis that all three contribute to refilling of the SR, perhaps orchestrated or powered by electrical slow waves (which are also found in ASM of all species studied to date).

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Abbreviations

[Ca2+]i :

Cytosolic concentrations of calcium

ASM:

Airway smooth muscle

Cav :

Voltage-dependent calcium channel

CICR:

Ca2+-induced Ca2+ release

EM:

Electromechanical

MLC:

Myosin light chain

MLCK:

Myosin light chain kinase

NCX:

Na+/Ca2+ exchange

RyR:

Ryanodine receptor

SERCA:

Sarcoplasmic/endoplasmic reticulum Ca2+-ATPase

SR:

Sarcoplasmic reticulum

References

  1. Ahmed F, Foster RW, Small RC and Weston AH. Some features of the spasmogenic actions of acetylcholine and histamine in guinea-pig isolated trachealis. Br J Pharmacol 83: 227–233, 1984.

    PubMed  CAS  Google Scholar 

  2. Algara-Suarez P, Mejia-Elizondo R, Sims SM, Saavedra-Alanis VM and Espinosa-Tanguma R. The 1.3 isoform of Na+-Ca2+ exchanger expressed in guinea pig tracheal smooth muscle is less sensitive to KB-R7943. J Physiol Biochem 66: 117–125, 2010.

    PubMed  CAS  Google Scholar 

  3. Allen SL, Beech DJ, Foster RW, Morgan GP and Small RC. Electrophysiological and other aspects of the relaxant action of isoprenaline in guinea-pig isolated trachealis. Br J Pharmacol 86: 843–854, 1985.

    PubMed  CAS  Google Scholar 

  4. Allen SL, Boyle JP, Cortijo J, Foster RW, Morgan GP and Small RC. Electrical and mechanical effects of BRL34915 in guinea-pig isolated trachealis. Br J Pharmacol 89: 395–405, 1986.

    PubMed  CAS  Google Scholar 

  5. Amoako D, Qian Y, Kwan CY and Bourreau JP. Probing excitation-contraction coupling in trachealis smooth muscle with the mycotoxin cyclopiazonic acid. Clin Exp Pharmacol Physiol 23: 733–737, 1996.

    PubMed  CAS  Google Scholar 

  6. Ann TM, Harman E, Chesrown S and Hendeles L. Efficacy of calcium channel blockers as maintenance therapy for asthma. Br J Clin Pharmacol 53: 243–249, 2002.

    Google Scholar 

  7. Bai Y and Sanderson MJ. Airway smooth muscle relaxation results from a reduction in the frequency of Ca2+ oscillations induced by a cAMP-mediated inhibition of the IP3 receptor. Respir Res 7: 34, 2006.

    PubMed  Google Scholar 

  8. Beinfield WH and Seifter J. Spontaneous mechanical activities of dog trachealis muscle in vivo. J Appl Physiol 48: 320–328, 1980.

    PubMed  CAS  Google Scholar 

  9. Bergner A and Sanderson MJ. Acetylcholine-induced calcium signaling and contraction of airway smooth muscle cells in lung slices. J Gen Physiol 119: 187–198, 2002.

    PubMed  CAS  Google Scholar 

  10. Bergner A and Sanderson MJ. ATP stimulates Ca2+ oscillations and contraction in airway smooth muscle cells of mouse lung slices. Am J Physiol Lung Cell Mol Physiol 283: L1271–L1279, 2002.

    PubMed  CAS  Google Scholar 

  11. Blaustein MP and Lederer WJ. Sodium/calcium exchange: its physiological implications. Physiol Rev 79: 763–854, 1999.

    PubMed  CAS  Google Scholar 

  12. Bourreau JP, Abela AP, Kwan CY and Daniel EE. Acetylcholine Ca2+ stores refilling directly involves a dihydropyridine- sensitive channel in dog trachea. Am J Physiol 261: C497–C505, 1991.

    PubMed  CAS  Google Scholar 

  13. Bourreau JP, Kwan CY and Daniel EE. Distinct pathways to refill ACh-sensitive internal Ca2+ stores in canine airway smooth muscle. Am J Physiol 265: C28–C35, 1993.

    PubMed  CAS  Google Scholar 

  14. Boyle JP, Davies JM, Foster RW, Good DM, Kennedy I and Small RC. Spasmogen action in guinea-pig isolated trachealis: involvement of membrane K+-channels and the consequences of K+-channel blockade. Br J Pharmacol 93: 319–330, 1988.

    PubMed  CAS  Google Scholar 

  15. Burghuber OC, Kneussl M, Harmuth P, Silberbauer K, Sinzinger H and Haber P. Inhibition of acetylcholine-induced bronchoconstriction in asthmatics by nifedipine. Respiration 50: 265–272, 1986.

    PubMed  CAS  Google Scholar 

  16. Cameron AR, Johnston CF, Kirkpatrick CT and Kirkpatrick MC. The quest for the inhibitory neurotransmitter in bovine tracheal smooth muscle. Q J Exp Physiol 68: 413–426, 1983.

    PubMed  CAS  Google Scholar 

  17. Cerrina J, Denjean A, Alexandre G, Lockhart A and Duroux P. Inhibition of exercise-induced asthma by a calcium antagonist, nifedipine. Am Rev Respir Dis 123: 156–160, 1981.

    PubMed  CAS  Google Scholar 

  18. Coburn RF. Stretch-induced membrane depolarization in ferret trachealis smooth muscle cells. J Appl Physiol 62: 2320–2325, 1987.

    PubMed  CAS  Google Scholar 

  19. Corris PA, Nariman S and Gibson GJ. Nifedipine in the prevention of asthma induced by exercise and histamine. Am Rev Respir Dis 128: 991–992, 1983.

    PubMed  CAS  Google Scholar 

  20. Cox G, Miller JD, McWilliams A, Fitzgerald JM and Lam S. Bronchial thermoplasty for asthma. Am J Respir Crit Care Med 173: 965–969, 2006.

    PubMed  Google Scholar 

  21. Cox G, Thomson NC, Rubin AS, Niven RM, Corris PA, Siersted HC, Olivenstein R, Pavord ID, McCormack D, Chaudhuri R, Miller JD and Laviolette M. Asthma control during the year after bronchial thermoplasty. N Engl J Med 356: 1327–1337, 2007.

    PubMed  CAS  Google Scholar 

  22. Crimi N, Palermo F, Sorace R, Gibellino F and Mistretta A. Effect of a calcium antagonist, nifedipine, in exercise-induced asthma. Respiration 45: 262–264, 1984.

    PubMed  CAS  Google Scholar 

  23. Cuss FM and Barnes PJ. The effect of inhaled nifedipine on bronchial reactivity to histamine in man. J Allergy Clin Immunol 76: 718–723, 1985.

    PubMed  CAS  Google Scholar 

  24. Dai JM, Kuo KH, Leo JM, Pare PD, van Breemen C and Lee CH. Acetylcholine-induced asynchronous calcium waves in intact human bronchial muscle bundle. Am J Respir Cell Mol Biol 36: 600–608, 2007.

    PubMed  CAS  Google Scholar 

  25. Dai JM, Kuo KH, Leo JM, van Breemen C and Lee CH. Mechanism of ACh-induced asynchronous calcium waves and tonic contraction in porcine tracheal muscle bundle. Am J Physiol Lung Cell Mol Physiol 290: L459–L469, 2006.

    PubMed  CAS  Google Scholar 

  26. Daniel EE, Abela AP, Janssen LJ and O’Byrne PM. Effects of inflammatory mediators on canine airway neuromuscular function. Can J Physiol Pharmacol 70: 624–634, 1992.

    PubMed  CAS  Google Scholar 

  27. Daniel EE, Bourreau JP, Abela A and Jury J. The internal calcium store in airway muscle: emptying, refilling and chloride. Possible new directions for drug development. Biochem Pharmacol 43: 29–37, 1992.

    PubMed  CAS  Google Scholar 

  28. Daniel EE, Jury J, Serio R and Jager LP. Role of depolarization and calcium in contractions of canine trachealis from endogenous or exogenous acetylcholine. Can J Physiol Pharmacol 69: 518–525, 1991.

    PubMed  CAS  Google Scholar 

  29. Deshpande DA, Walseth TF, Panettieri RA and Kannan MS. CD38-cyclic ADP-ribose-mediated Ca2+ signaling contributes to airway smooth muscle hyperresponsiveness. FASEB J 2003.

    Google Scholar 

  30. Du W, McMahon TJ, Zhang ZS, Stiber JA, Meissner G and Eu JP. Excitation-contraction coupling in airway smooth muscle. J Biol Chem 281: 30143–30151, 2006.

    PubMed  CAS  Google Scholar 

  31. Du W, Stiber JA, Rosenberg PB, Meissner G and Eu JP. Ryanodine receptors in muscarinic receptor-mediated bronchoconstriction. J Biol Chem 280: 26287–26294, 2005.

    PubMed  CAS  Google Scholar 

  32. Ethier MF and Madison JM. IL-4 inhibits calcium transients in bovine trachealis cells by a ryanodine receptor-dependent mechanism. FASEB J 20: 154–156, 2006.

    PubMed  CAS  Google Scholar 

  33. Faraci FM and Heistad DD. Regulation of the cerebral circulation: role of endothelium and potassium channels. Physiological Reviews 78: 53–97, 1998.

    PubMed  CAS  Google Scholar 

  34. Farley JM and Miles PR. The sources of calcium for acetylcholine-induced contractions of dog tracheal smooth muscle. J Pharmacol Exp Ther 207: 340–346, 1978.

    PubMed  CAS  Google Scholar 

  35. Fish JE and Norman PS. Effects of the calcium channel blocker, verapamil, on asthmatic airway responses to muscarinic, histaminergic, and allergenic stimuli. Am Rev Respir Dis 133: 730–734, 1986.

    PubMed  CAS  Google Scholar 

  36. Fleckenstein A, Frey M and Fleckenstein-Grun G. Antihypertensive and arterial anticalcinotic effects of calcium antagonists. American Journal of Cardiology 57: 1D–10D, 1986.

    PubMed  CAS  Google Scholar 

  37. Fleischmann BK, Wang YX and Kotlikoff MI. Muscarinic activation and calcium permeation of nonselective cation currents in airway myocytes. Am J Physiol 272: C341–C349, 1997.

    PubMed  CAS  Google Scholar 

  38. Fleischmann BK, Wang YX, Pring M and Kotlikoff MI. Voltage-dependent calcium currents and cytosolic calcium in equine airway myocytes. J Physiol 492 ( Pt 2): 347–358, 1996.

    PubMed  Google Scholar 

  39. Foster RW, Okpalugo BI and Small RC. Antagonism of Ca2+ and other actions of verapamil in guinea-pig isolated trachealis. Br J Pharmacol 81: 499–507, 1984.

    PubMed  CAS  Google Scholar 

  40. Foster RW, Small RC and Weston AH. Evidence that the spasmogenic action of tetraethylammonium in guinea- pig trachealis is both direct and dependent on the cellular influx of calcium ion. Br J Pharmacol 79: 255–263, 1983.

    PubMed  CAS  Google Scholar 

  41. Ghayur MN, Gilani AH and Janssen LJ. Ginger attenuates acetylcholine-induced contraction and Ca2+ signalling in murine airway smooth muscle cells. Can J Physiol Pharmacol 86: 264–271, 2008.

    PubMed  CAS  Google Scholar 

  42. Ghayur MN, Gilani AH, Rasheed H, Khan A, Iqbal Z, Ismail M, Saeed SA and Janssen LJ. Cardiovascular and airway relaxant activities of peony root extract. Can J Physiol Pharmacol 86: 793–803, 2008.

    PubMed  CAS  Google Scholar 

  43. Gordon EH, Wong SC and Klaustermeyer WB. Comparison of nifedipine with a new calcium channel blocker, flordipine, in exercise-induced asthma. J Asthma 24: 261–265, 1987.

    PubMed  CAS  Google Scholar 

  44. Hartmann V and Magnussen H. Effect of diltiazem on histamine- and carbachol-induced bronchospasm in normal and asthmatic subjects. Chest 87: 174–179, 1985.

    PubMed  CAS  Google Scholar 

  45. Hay DW, Luttmann MA, Muccitelli RM and Goldie RG. Endothelin receptors and calcium translocation pathways in human airways. Naunyn Schmiedebergs Arch Pharmacol 359: 404–410, 1999.

    PubMed  CAS  Google Scholar 

  46. Hirota S, Helli P and Janssen LJ. Ionic mechanisms and Ca2+ handling in airway smooth muscle. Eur Respir J 30: 1400–1419, 2007.

    Google Scholar 

  47. Hirota S, Helli PB, Catalli A, Chew A and Janssen LJ. Airway smooth muscle excitation-contraction coupling and airway hyperresponsiveness. Can J Physiol Pharmacol 83: 725–732, 2005.

    PubMed  CAS  Google Scholar 

  48. Hirota S and Janssen LJ. Store-refilling involves both L-type calcium channels and reverse-mode sodium-calcium exchange in airway smooth muscle. Eur Respir J 30: 269–278, 2007.

    PubMed  CAS  Google Scholar 

  49. Hirota S, Pertens E and Janssen LJ. The reverse mode of the Na+/Ca2+ exchanger provides a source of Ca2+ for store refilling following agonist-induced Ca2+ mobilization. Am J Physiol Lung Cell Mol Physiol 292: L438–L447, 2007.

    PubMed  CAS  Google Scholar 

  50. Hisada T, Kurachi Y and Sugimoto T. Properties of membrane currents in isolated smooth muscle cells from guinea-pig trachea. Pflugers Arch 416: 151–161, 1990.

    PubMed  CAS  Google Scholar 

  51. Honda K, Satake T, Takagi K and Tomita T. Effects of relaxants on electrical and mechanical activities in the guinea-pig tracheal muscle. Br J Pharmacol 87: 665–671, 1986.

    PubMed  CAS  Google Scholar 

  52. Honda K and Tomita T. Electrical activity in isolated human tracheal muscle. Jpn J Physiol 37: 333–336, 1987.

    PubMed  CAS  Google Scholar 

  53. Hyvelin JM, Martin C, Roux E, Marthan R and Savineau JP. Human isolated bronchial smooth muscle contains functional ryanodine/caffeine-sensitive Ca-release channels. Am J Respir Crit Care Med 162: 687–694, 2000.

    PubMed  CAS  Google Scholar 

  54. Janssen LJ. Acetylcholine and caffeine activate Cl- and suppress K+ conductances in human bronchial smooth muscle. Am J Physiol 270: L772–L781, 1996.

    PubMed  CAS  Google Scholar 

  55. Janssen LJ. T-type and L-type Ca2+ currents in canine bronchial smooth muscle: characterization and physiological roles. Am J Physiol 272: C1757–C1765, 1997.

    PubMed  CAS  Google Scholar 

  56. Janssen LJ. Ionic mechanisms and Ca2+ regulation in airway smooth muscle contraction: do the data contradict dogma? Am J Physiol Lung Cell Mol Physiol 282: L1161–L1178, 2002.

    PubMed  CAS  Google Scholar 

  57. Janssen LJ and Daniel EE. Characterization of the prejunctional beta adrenoceptors in canine bronchial smooth muscle. J Pharmacol Exp Ther 254: 741–749, 1990.

    PubMed  CAS  Google Scholar 

  58. Janssen LJ and Daniel EE. Pre- and postjunctional muscarinic receptors in canine bronchi. Am J Physiol 259: L304–L314, 1990.

    PubMed  CAS  Google Scholar 

  59. Janssen LJ and Daniel EE. Classification of postjunctional beta adrenoceptors mediating relaxation of canine bronchi. J Pharmacol Exp Ther 256: 670–676, 1991.

    PubMed  CAS  Google Scholar 

  60. Janssen LJ and Daniel EE. Depolarizing agents induce oscillations in canine bronchial smooth muscle membrane potential: possible mechanisms. J Pharmacol Exp Ther 259: 110–117, 1991.

    PubMed  CAS  Google Scholar 

  61. Janssen LJ and Daniel EE. Pre- and postjunctional effects of a thromboxane mimetic in canine bronchi. Am J Physiol 261: L271–L276, 1991.

    PubMed  CAS  Google Scholar 

  62. Janssen LJ, Farkas L, Rahman T and Kolb MR. ATP stimulates Ca2+-waves and gene expression in cultured human pulmonary fibroblasts. Int J Biochem Cell Biol 41: 2477–2484, 2009.

    PubMed  CAS  Google Scholar 

  63. Janssen LJ, Hague C and Nana R. Ionic mechanisms underlying electrical slow waves in canine airway smooth muscle. Am J Physiol 275: L516–L523, 1998.

    PubMed  CAS  Google Scholar 

  64. Janssen LJ and Killian K. Airway smooth muscle as a target of asthma therapy: history and new directions. Respir Res 7: 123, 2006.

    PubMed  Google Scholar 

  65. Janssen LJ and Sims SM. Acetylcholine activates non-selective cation and chloride conductances in canine and guinea-pig tracheal myocytes. J Physiol 453: 197–218, 1992.

    PubMed  CAS  Google Scholar 

  66. Janssen LJ and Sims SM. Emptying and refilling of Ca2+ store in tracheal myocytes as indicated by ACh-evoked currents and contraction. Am J Physiol 265: C877–C886, 1993.

    PubMed  CAS  Google Scholar 

  67. Janssen LJ, Wattie J, Lu-Chao H and Tazzeo T. Muscarinic excitation-contraction coupling mechanisms in tracheal and bronchial smooth muscles. J Appl Physiol 91: 1142–1151, 2001.

    PubMed  CAS  Google Scholar 

  68. Kaliner MA. Evolution of asthma treatments. Ann Allergy 71: 300–305, 1993.

    PubMed  CAS  Google Scholar 

  69. Kirkpatrick CT. Excitation and contraction in bovine tracheal smooth muscle. J Physiol 244: 263–281, 1975.

    PubMed  CAS  Google Scholar 

  70. Kondo T, Tamura K, Onoe K, Takahira H, Ohta Y and Yamabayashi H. In vivo recording of electrical activity of canine tracheal smooth muscle. J Appl Physiol 72: 135–142, 1992.

    PubMed  CAS  Google Scholar 

  71. Kotlikoff MI. Calcium currents in isolated canine airway smooth muscle cells. Am J Physiol 254: C793–C801, 1988.

    PubMed  CAS  Google Scholar 

  72. Kuo KH, Dai J, Seow CY, Lee CH and van Breemen C. Relationship between asynchronous Ca2+ waves and force development in intact smooth muscle bundles of the porcine trachea. Am J Physiol Lung Cell Mol Physiol 285: L1345–L1353, 2003.

    PubMed  CAS  Google Scholar 

  73. Liu B, Peel SE, Fox J and Hall IP. Reverse mode Na+/Ca2+ exchange mediated by STIM1 contributes to Ca2+ influx in airway smooth muscle following agonist stimulation. Respir Res 11: 168, 2010.

    PubMed  CAS  Google Scholar 

  74. Liu C, Zuo J, Pertens E, Helli PB and Janssen LJ. Regulation of Rho/ROCK signaling in airway smooth muscle by membrane potential and [Ca2+]i. Am J Physiol Lung Cell Mol Physiol 289: L574–L582, 2005.

    PubMed  CAS  Google Scholar 

  75. Liu X and Farley JM. Depletion and refilling of acetylcholine- and caffeine-sensitive Ca2+ stores in tracheal myocytes. J Pharmacol Exp Ther 277: 789–795, 1996.

    PubMed  CAS  Google Scholar 

  76. Mahn K, Hirst SJ, Ying S, Holt MR, Lavender P, Ojo OO, Siew L, Simcock DE, McVicker CG, Kanabar V, Snetkov VA, O’connor BJ, Karner C, Cousins DJ, Macedo P, Chung KF, Corrigan CJ, Ward JP and Lee TH. Diminished sarco/endoplasmic reticulum Ca2+ ATPase (SERCA) expression contributes to airway remodelling in bronchial asthma. Proc Natl Acad Sci U S A 106: 10775–10780, 2009.

    PubMed  CAS  Google Scholar 

  77. Marthan R, Martin C, Amedee T and Mironneau J. Calcium channel currents in isolated smooth muscle cells from human bronchus. J Appl Physiol 66: 1706–1714, 1989.

    PubMed  CAS  Google Scholar 

  78. McCaig DJ. Electrophysiology of neuroeffector transmission in the isolated, innervated trachea of the guinea-pig. Br J Pharmacol 89: 793–801, 1986.

    PubMed  CAS  Google Scholar 

  79. Middleton E Jr. Airway smooth muscle, asthma, and calcium ions. J Allergy Clin Immunol 73: 643–650, 1984.

    PubMed  Google Scholar 

  80. Middleton E Jr. Calcium antagonists and asthma. J Allergy Clin Immunol 76: 341–346, 1985.

    PubMed  Google Scholar 

  81. Middleton E Jr. The treatment of asthma--beyond bronchodilators. N Engl Reg Allergy Proc 6: 235–237, 1985.

    PubMed  Google Scholar 

  82. Miller JD, Cox G, Vincic L, Lombard CM, Loomas BE and Danek CJ. A prospective feasibility study of bronchial thermoplasty in the human airway. Chest 127: 1999–2006, 2005.

    PubMed  Google Scholar 

  83. Mitzner W. Airway smooth muscle: the appendix of the lung. Am J Respir Crit Care Med 169: 787–790, 2004.

    PubMed  Google Scholar 

  84. Murlas CG and Doupnik CA. Electromechanical coupling of ferret airway smooth muscle in response to leukotriene C4. J Appl Physiol 66: 2533–2538, 1989.

    PubMed  CAS  Google Scholar 

  85. Nuttle LC and Farley JM. Frequency modulation of acetylcholine-induced oscillations in Ca2+ and Ca2+-activated Cl- current by cAMP in tracheal smooth muscle. J Pharmacol Exp Ther 277: 753–760, 1996.

    PubMed  CAS  Google Scholar 

  86. O’Byrne PM, Barnes PJ, Rodriguez-Roisin R, Runnerstrom E, Sandstrom T, Svensson K and Tattersfield A. Low dose inhaled budesonide and formoterol in mild persistent asthma: the OPTIMA randomized trial. Am J Respir Crit Care Med 164: 1392–1397, 2001.

    PubMed  Google Scholar 

  87. Patel KR. Calcium antagonists in exercise-induced asthma. Br Med J (Clin Res Ed) 282: 932–933, 1981.

    CAS  Google Scholar 

  88. Patel KR. The effect of calcium antagonist, nifedipine in exercise-induced asthma. Clin Allergy 11: 429–432, 1981.

    PubMed  CAS  Google Scholar 

  89. Pavord ID, Cox G, Thomson NC, Rubin AS, Corris PA, Niven RM, Chung KF and Laviolette M. Safety and efficacy of bronchial thermoplasty in symptomatic, severe asthma. Am J Respir Crit Care Med 176: 1185–1191, 2007.

    PubMed  CAS  Google Scholar 

  90. Perez JF and Sanderson MJ. The frequency of calcium oscillations induced by 5-HT, ACH, and KCl determine the contraction of smooth muscle cells of intrapulmonary bronchioles. J Gen Physiol 125: 535–553, 2005.

    PubMed  CAS  Google Scholar 

  91. Perez-Zoghbi JF and Sanderson MJ. Endothelin-induced contraction of bronchiole and pulmonary arteriole smooth muscle cells is regulated by intracellular Ca2+ oscillations and Ca2+ sensitization. Am J Physiol Lung Cell Mol Physiol 293: L1000–L1011, 2007.

    PubMed  CAS  Google Scholar 

  92. Prakash YS, Kannan MS, Walseth TF and Sieck GC. Role of cyclic ADP-ribose in the regulation of [Ca2+]i in porcine tracheal smooth muscle. Am J Physiol 274: C1653–C1660, 1998.

    PubMed  CAS  Google Scholar 

  93. Prakash YS, Pabelick CM, Kannan MS and Sieck GC. Spatial and temporal aspects of ACh-induced [Ca2+]i oscillations in porcine tracheal smooth muscle. Cell Calcium 27: 153–162, 2000.

    PubMed  CAS  Google Scholar 

  94. Qian Y and Bourreau JP. Two distinct pathways for refilling Ca2+ stores in permeabilized bovine trachealis muscle. Life Sci 64: 2049–2059, 1999.

    PubMed  CAS  Google Scholar 

  95. Quayle JM, Nelson MT and Standen NB. ATP-sensitive and inwardly rectifying potassium channels in smooth muscle. Physiol Rev 77: 1165–1232, 1997.

    PubMed  CAS  Google Scholar 

  96. Rafferty P, Varley JG, Edwards JS and Holgate ST. Inhibition of exercise-induced asthma by nifedipine: a dose–response study. Br J Clin Pharmacol 24: 479–484, 1987.

    PubMed  CAS  Google Scholar 

  97. Rahman M, Inman M, Kiss L and Janssen LJ. Reverse-mode NCX-current in mouse airway smooth muscle: Na+- and voltage-dependence, contributions to Ca2+-influx and contraction, and altered expression in a model of allergen-induced hyperresponsiveness. Acta Physiol (Oxf) 2011.

    Google Scholar 

  98. Roux E, Guibert C, Savineau JP and Marthan R. [Ca2+]i oscillations induced by muscarinic stimulation in airway smooth muscle cells: receptor subtypes and correlation with the mechanical activity. Br J Pharmacol 120: 1294–1301, 1997.

    PubMed  CAS  Google Scholar 

  99. Roux E, Noble PJ, Noble D and Marhl M. Modelling of calcium handling in airway myocytes. Prog Biophys Mol Biol 90: 64–87, 2006.

    PubMed  CAS  Google Scholar 

  100. Sears MR. The evolution of beta2-agonists. Respir Med 95 Suppl B: S2–S6, 2001

    PubMed  Google Scholar 

  101. Sears MR, Taylor DR, Print CG, Lake DC, Li QQ, Flannery EM, Yates DM, Lucas MK and Herbison GP. Regular inhaled beta-agonist treatment in bronchial asthma. Lancet 336: 1391–1396, 1990.

    PubMed  CAS  Google Scholar 

  102. SILBERT NE. Treatment of bronchial conditions with a combination of anticholinergic, adrenergic, and antihistaminic drugs; preliminary report. Ann Allergy 10: 469–472, 1952.

    PubMed  CAS  Google Scholar 

  103. Small RC. Electrical slow waves and tone of guinea-pig isolated trachealis muscle: effects of drugs and temperature changes. Br J Pharmacol 77: 45–54, 1982.

    PubMed  CAS  Google Scholar 

  104. Small RC, Berry JL, Foster RW, Blarer S and Quast U. Analysis of the relaxant action of SDZ PCO 400 in airway smooth muscle from the ox and guinea-pig. Eur J Pharmacol 219: 81–88, 1992.

    PubMed  CAS  Google Scholar 

  105. Somlyo AP and Somlyo AV. From pharmacomechanical coupling to G-proteins and myosin phosphatase. Acta Physiol Scand 164: 437–448, 1998.

    PubMed  CAS  Google Scholar 

  106. Souhrada M, Souhrada JF and Cherniack RM. Evidence for a sodium electrogenic pump in airway smooth muscle. J Appl Physiol 51: 346–352, 1981.

    PubMed  CAS  Google Scholar 

  107. Tazzeo T, Zhang Y, Keshavjee S and Janssen LJ. Ryanodine receptors decant internal Ca2+ store in human and bovine airway smooth muscle. Eur Respir J 2008.

    Google Scholar 

  108. Uyama Y, Imaizumi Y and Watanabe M. Effects of cyclopiazonic acid, a novel Ca2+-ATPase inhibitor, on contractile responses in skinned ileal smooth muscle. Br J Pharmacol 106: 208–214, 1992.

    PubMed  CAS  Google Scholar 

  109. Wade GR, Barbera J and Sims SM. Cholinergic inhibition of Ca2+ current in guinea-pig gastric and tracheal smooth muscle cells. J Physiol 491 ( Pt 2): 307–319, 1996.

    PubMed  CAS  Google Scholar 

  110. Wang Y, Deng X, Mancarella S, Hendron E, Eguchi S, Soboloff J, Tang XD and Gill DL. The calcium store sensor, STIM1, reciprocally controls Orai and CaV1.2 channels. Science 330: 105–109, 2010.

    PubMed  CAS  Google Scholar 

  111. Wang YX, Fleischmann BK and Kotlikoff MI. M2 receptor activation of nonselective cation channels in smooth muscle cells: calcium and Gi/G(o) requirements. Am J Physiol 273: C500–C508, 1997.

    PubMed  CAS  Google Scholar 

  112. Wang YX and Kotlikoff MI. Muscarinic signaling pathway for calcium release and calcium-activated chloride current in smooth muscle. Am J Physiol 273: C509–C519, 1997.

    PubMed  CAS  Google Scholar 

  113. Wang YX, Zheng YM, Mei QB, Wang QS, Collier ML, Fleischer S, Xin HB and Kotlikoff MI. FKBP12.6 and cADPR regulation of Ca2+ release in smooth muscle cells. Am J Physiol Cell Physiol 286: C538–C546, 2004.

    PubMed  CAS  Google Scholar 

  114. Welling A, Felbel J, Peper K and Hofmann F. Hormonal regulation of calcium current in freshly isolated airway smooth muscle cells. Am J Physiol 262: L351–L359, 1992.

    PubMed  CAS  Google Scholar 

  115. White TA, Johnson S, Walseth TF, Lee HC, Graeff RM, Munshi CB, Prakash YS, Sieck GC and Kannan MS. Subcellular localization of cyclic ADP-ribosyl cyclase and cyclic ADP- ribose hydrolase activities in porcine airway smooth muscle. Biochim Biophys Acta 1498: 64–71, 2000.

    PubMed  CAS  Google Scholar 

  116. Worley JF and Kotlikoff MI. Dihydropyridine-sensitive single calcium channels in airway smooth muscle cells. Am J Physiol 259: L468–L480, 1990.

    PubMed  CAS  Google Scholar 

  117. Yamaguchi H, Kajita J and Madison JM. Isoproterenol increases peripheral [Ca2+]i and decreases inner [Ca2+]i in single airway smooth muscle cells. Am J Physiol 268: C771–C779, 1995.

    PubMed  CAS  Google Scholar 

  118. Yamakage M, Hirshman CA and Croxton TL. Cholinergic regulation of voltage-dependent Ca2+ channels in porcine tracheal smooth muscle cells. Am J Physiol 269: L776–L782, 1995.

    PubMed  CAS  Google Scholar 

  119. Yang CM, Yo YL and Wang YY. Intracellular calcium in canine cultured tracheal smooth muscle cells is regulated by M3 muscarinic receptors. Br J Pharmacol 110: 983–988, 1993.

    PubMed  CAS  Google Scholar 

  120. Zheng XF, Guan YY and Kwan CY. Cyclopiazonic acid causes endothelium-dependent relaxation in rat aorta. Chung-Kuo Yao Li Hsueh Pao - Acta Pharmacologica Sinica 14: 21–26, 1993.

    CAS  Google Scholar 

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Authors and Affiliations

  1. Firestone Institute for Respiratory Health, St. Joseph’s Hospital and the Department of Medicine, McMaster University, L-314, St. Joseph’s Hospital, 50 Charlton Ave. East, Hamilton, ON, L8N 4A6, Canada

    Luke J. Janssen

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  1. Luke J. Janssen
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Correspondence to Luke J. Janssen .

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  1. Albany Medical College Center for Cardiovascular Sciences, Albany, New York, USA

    Yong-Xiao Wang

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Janssen, L.J. (2014). Novel Mechanisms in Ca2+ Homeostasis and Internal Store Refilling of Airway Smooth Muscle. In: Wang, YX. (eds) Calcium Signaling In Airway Smooth Muscle Cells. Springer, Cham. https://doi.org/10.1007/978-3-319-01312-1_10

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