Temporal Aspects of Ca2+ Signaling in Airway Myocytes

  • Etienne RouxEmail author


This chapter discusses how variation in intracytoplasmic Ca2+ concentration ([Ca2+]i) over time can be considered as a signal for the contractile machinery. It presents an overview of the literature that describes the Ca2+ response pattern to different contractile or relaxant agonists in several types of airway smooth muscle cells (ASMCs) depending on the species and location in the airway tree and recording methods, insisting on the temporal aspects of this response. Since the dynamics of the Ca2+ signal depends on the dynamics of the mechanisms responsible for this signal, the chapter presents an overview of the main mechanisms responsible for Ca2+ homeodynamics in ASMCs. By analyzing some examples, it shows how the kinetics of these mechanisms determine the pattern of the Ca2+ signal. The consequence of cell-to-cell variations in the Ca2+ signal is also discussed, with special attention to oscillatory versus nonoscillatory responses. The last part of the chapter presents the relationship between the parameter of the Ca2+ signal and the pattern of the contractile response. The mechanisms of the contractile apparatus itself will not be detailed, this question being beyond the scope of the chapter, but the temporal relationship between the Ca2+ signal and the subsequent contraction is analyzed.


Calcium dynamics Oscillations Kinetics Model Contraction 


  1. 1.
    Ikeda, M., K. Kurokawa, and Y. Maruyama, Cyclic nucleotide-dependent regulation of agonist-induced calcium increases in mouse megakaryocytes. J Physiol, 1992. 447: p. 711–28.PubMedGoogle Scholar
  2. 2.
    Roux, E. and M. Marhl, Role of sarcoplasmic reticulum and mitochondria in ca(2+) removal in airway myocytes. Biophys J, 2004. 86(4): p. 2583–95.PubMedCrossRefGoogle Scholar
  3. 3.
    Csete, M. and J. Doyle, Bow ties, metabolism and disease. Trends in Biotechnology, 2004. 22(9): p. 446–450.PubMedCrossRefGoogle Scholar
  4. 4.
    Ma, H.W. and A.P. Zeng, The connectivity structure, giant strong component and centrality of metabolic networks. Bioinformatics, 2003. 19(11): p. 1423–1430.PubMedCrossRefGoogle Scholar
  5. 5.
    Marhl, M., M. Perc, and S. Schuster, Selective regulation of cellular processes via protein cascades acting as band-pass filters for time-limited oscillations. FEBS Lett., 2005. 579(25): p. 5461–5465.PubMedCrossRefGoogle Scholar
  6. 6.
    Schuster, S., B. Knoke, and M. Marhl, Differential regulation of proteins by bursting calcium oscillations - a theoretical study. Biosystems, 2005. 81(1): p. 49–63.PubMedCrossRefGoogle Scholar
  7. 7.
    Bai, Y., M. Edelmann, and M.J. Sanderson, The contribution of inositol 1,4,5-trisphosphate and ryanodine receptors to agonist-induced Ca(2+) signaling of airway smooth muscle cells. Am J Physiol Lung Cell Mol Physiol, 2009. 297(2): p. L347–61.PubMedCrossRefGoogle Scholar
  8. 8.
    Hyvelin, J.M., et al., Cellular mechanisms of acrolein-induced alteration in calcium signaling in airway smooth muscle. Toxicol Appl Pharmacol, 2000. 164(2): p. 176–83.PubMedCrossRefGoogle Scholar
  9. 9.
    Roux, E., et al., [Ca 2+ ] i oscillations induced by muscarinic stimulation in airway smooth muscle cells: receptor subtypes and correlation with the mechanical activity. Br J Pharmacol, 1997. 120: p. 1294–1301.PubMedCrossRefGoogle Scholar
  10. 10.
    Roux, E., et al., Muscarinic stimulation of airway smooth muscle cells. Gen Pharmacol, 1998. 31(3): p. 349–56.PubMedCrossRefGoogle Scholar
  11. 11.
    Liu, X. and J.M. Farley, Frequency modulation of acetylcholine-induced Ca(++)-dependent Cl- current oscillations are mediated by 1, 4, 5-trisphosphate in tracheal myocytes. J Pharmacol Exp Ther, 1996. 277: p. 796–804.PubMedGoogle Scholar
  12. 12.
    Kannan, M.S., et al., Role of ryanodine receptor channels in Ca2+ oscillations of porcine tracheal smooth muscle. Am J Physiol, 1997. 272(4 Pt 1): p. L659–64.PubMedGoogle Scholar
  13. 13.
    Prakash, Y.S., M.S. Kannan, and G.C. Sieck, Regulation of intracellular calcium oscillations in porcine tracheal smooth muscle cells. Am J Physiol, 1997. 272(3 Pt 1): p. C966–75.PubMedGoogle Scholar
  14. 14.
    Prakash, Y.S., et al., Role of cyclic ADP-ribose in the regulation of [Ca2+]i in porcine tracheal smooth muscle. Am J Physiol, 1998. 274(6 Pt 1): p. C1653–60.PubMedGoogle Scholar
  15. 15.
    Marthan, R., et al., Calcium channel currents in isolated smooth muscle cells from human bronchus. J Appl Physiol, 1989. 66: p. 1706–1714.PubMedGoogle Scholar
  16. 16.
    Kotlikoff, L., Calcium currents in isolated canine airway smooth muscle cells. Am J Physiol, 1988. 254: p. C793–C801.PubMedGoogle Scholar
  17. 17.
    Rodger, I.W., Voltage-dependent and receptor-operated calcium channels, in Airways smooth muscle: biochemical control of contraction and relaxation, D. Raeburn and M.A. Giembycz, Editors. 1994, Birkhäuser Verlag: Basel. p. 155–168.Google Scholar
  18. 18.
    McFadzean, I. and A. Gibson, The developing relationship between receptor-operated and store-operated calcium channels in smooth muscle. Br J Pharmacol, 2002. 135(1): p. 1–13.PubMedCrossRefGoogle Scholar
  19. 19.
    Mounkaila, B., R. Marthan, and E. Roux, Biphasic effect of extracellular ATP on human and rat airways is due to multiple P2 purinoceptor activation. Respir Res, 2005. 6(1): p. 143.PubMedCrossRefGoogle Scholar
  20. 20.
    Sanders, K.M., Invited review: mechanisms of calcium handling in smooth muscles. J Appl Physiol, 2001. 91(3): p. 1438–49.PubMedGoogle Scholar
  21. 21.
    Helli, P.B., E. Pertens, and L.J. Janssen, Cyclopiazonic acid activates a Ca2+−permeable, nonselective cation conductance in porcine and bovine tracheal smooth muscle. J Appl Physiol, 2005. 99(5): p. 1759–68.PubMedCrossRefGoogle Scholar
  22. 22.
    Ay, B., et al., Store-operated Ca2+ entry in porcine airway smooth muscle. Am J Physiol Lung Cell Mol Physiol, 2004. 286(5): p. L909–17.PubMedCrossRefGoogle Scholar
  23. 23.
    Marthan, R., Store-operated calcium entry and intracellular calcium release channels in airway smooth muscle. Am J Physiol Lung Cell Mol Physiol, 2004. 286(5): p. L907–8.PubMedCrossRefGoogle Scholar
  24. 24.
    Janssen, L.J., D.K. Walters, and J. Wattie, Regulation of [Ca2+]i in canine airway smooth muscle by Ca(2+)-ATPase and Na+/Ca2+ exchange mechanisms. Am J Physiol, 1997. 273(2 Pt 1): p. L322–30.PubMedGoogle Scholar
  25. 25.
    Flores-Soto, E., et al., In airways ATP refills sarcoplasmic reticulum via P2X smooth muscle receptors and induces contraction through P2Y epithelial receptors. Pflugers Arch, 2011. 461(2): p. 261–75.PubMedCrossRefGoogle Scholar
  26. 26.
    Liu, B., et al., Reverse mode Na+/Ca2+ exchange mediated by STIM1 contributes to Ca2+ influx in airway smooth muscle following agonist stimulation. Respir Res, 2010. 11: p. 168.PubMedCrossRefGoogle Scholar
  27. 27.
    Iwamoto, T. and M. Shigekawa, Differential inhibition of Na+/Ca2+ exchanger isoforms by divalent cations and isothiourea derivative. Am J Physiol, 1998. 275(2 Pt 1): p. C423–30.PubMedGoogle Scholar
  28. 28.
    Pitt, A. and A.J. Knox, Molecular characterization of the human airway smooth muscle Na+/Ca2+ exchanger. Am J Respir Cell Mol Biol, 1996. 15(6): p. 726–30.PubMedCrossRefGoogle Scholar
  29. 29.
    Sims, S.M., Y. Jiao, and Z.G. Zheng, Intracellular calcium stores in isolated tracheal smooth muscle cells. Am J Physiol, 1996. 271(2 Pt 1): p. L300–9.PubMedGoogle Scholar
  30. 30.
    Roux, E., J.-P. Mazat, and M. Marhl, Role of mitochondria in calcium homeostasis and contraction of smooth muscle cells, in Mitochondria: Structure, Functions and Dysfunctions, O.L. Svensson, Editor. 2009, Nova Publisher: Hauppauge NY.Google Scholar
  31. 31.
    Roux, E., et al., Modelling of calcium handling in airway myocytes. Prog Biophys Mol Biol, 2006. 90(1–3): p. 64–87.PubMedCrossRefGoogle Scholar
  32. 32.
    Marhl, M., et al., Modelling oscillations of calcium and endoplasmic reticulum transmembrane potential; role of the signalling and buffering proteins and of the size of the Ca2+ sequestering ER subcompartments. Bioelectrochem Bioenerg, 1998. 46: p. 79–90.CrossRefGoogle Scholar
  33. 33.
    Bai, Y. and M.J. Sanderson, The contribution of Ca2+ signaling and Ca2+ sensitivity to the regulation of airway smooth muscle contraction is different in rats and mice. Am J Physiol Lung Cell Mol Physiol, 2009. 296(6): p. L947–58.PubMedCrossRefGoogle Scholar
  34. 34.
    Mbikou, P., et al., Theoretical and experimental investigation of calcium-contraction coupling in airway smooth muscle. Cell Biochem Biophys, 2006. 46(3): p. 233–52.PubMedCrossRefGoogle Scholar
  35. 35.
    Roux, E., M. Duvert, and R. Marthan, Combined effect of chronic hypoxia and in vitro exposure to gas pollutants on airway reactivity. Am J Physiol Lung Cell Mol Physiol, 2002. 283(3): p. L628–35.PubMedGoogle Scholar
  36. 36.
    Roux, E., et al., Calcium signaling in airway smooth muscle cells is altered by in vitro exposure to the aldehyde acrolein. Am J Respir Cell Mol Biol, 1998. 19(3): p. 437–44.PubMedCrossRefGoogle Scholar
  37. 37.
    Perez-Zoghbi, J.F., Y. Bai, and M.J. Sanderson, Nitric oxide induces airway smooth muscle cell relaxation by decreasing the frequency of agonist-induced Ca2+ oscillations. J Gen Physiol, 2010. 135(3): p. 247–59.PubMedCrossRefGoogle Scholar
  38. 38.
    Jiang, H., et al., Phosphoinositide 3-kinase gamma regulates airway smooth muscle contraction by modulating calcium oscillations. J Pharmacol Exp Ther, 2010. 334(3): p. 703–9.PubMedCrossRefGoogle Scholar
  39. 39.
    Delmotte, P. and M.J. Sanderson, Effects of formoterol on contraction and Ca2+ signaling of mouse airway smooth muscle cells. Am J Respir Cell Mol Biol, 2010. 42(3): p. 373–81.PubMedCrossRefGoogle Scholar
  40. 40.
    Bai, Y., M. Zhang, and M.J. Sanderson, Contractility and Ca2+ signaling of smooth muscle cells in different generations of mouse airways. Am J Respir Cell Mol Biol, 2007. 36(1): p. 122–30.PubMedCrossRefGoogle Scholar
  41. 41.
    Bergner, A., et al., Ca2+−signaling in airway smooth muscle cells is altered in T-bet knock-out mice. Respir Res, 2006. 7: p. 33.PubMedCrossRefGoogle Scholar
  42. 42.
    Perez, J.F. and M.J. Sanderson, 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, 2005. 125(6): p. 535–53.PubMedCrossRefGoogle Scholar
  43. 43.
    Bergner, A. and M.J. Sanderson, Acetylcholine-induced calcium signaling and contraction of airway smooth muscle cells in lung slices. J Gen Physiol, 2002. 119(2): p. 187–98.PubMedCrossRefGoogle Scholar
  44. 44.
    Campos-Bedolla, P., et al., Airway smooth muscle relaxation induced by 5-HT(2A) receptors: role of Na(+)/K(+)-ATPase pump and Ca(2+)-activated K(+) channels. Life Sci, 2008. 83(11–12): p. 438–46.PubMedCrossRefGoogle Scholar
  45. 45.
    Oguma, T., et al., Roles of P2X receptors and Ca2+ sensitization in extracellular adenosine triphosphate-induced hyperresponsiveness in airway smooth muscle. Clin Exp Allergy, 2007. 37(6): p. 893–900.PubMedCrossRefGoogle Scholar
  46. 46.
    Janssen, L.J., T. Tazzeo, and J. Zuo, Enhanced myosin phosphatase and Ca(2+)-uptake mediate adrenergic relaxation of airway smooth muscle. Am J Respir Cell Mol Biol, 2004. 30(4): p. 548–54.PubMedCrossRefGoogle Scholar
  47. 47.
    Prakash, Y.S., et al., Spatial and temporal aspects of ACh-induced [Ca2+]i oscillations in porcine tracheal smooth muscle. Cell Calcium, 2000. 27(3): p. 153–62.PubMedCrossRefGoogle Scholar
  48. 48.
    Fleischmann, B.K., Y.X. Wang, and M.I. Kotlikoff, Muscarinic activation and calcium permeation of nonselective cation currents in airway myocytes. Am J Physiol, 1997. 272(1 Pt 1): p. C341-9.PubMedGoogle Scholar
  49. 49.
    Wang, Y.X., B.K. Fleischmann, and M.I. Kotlikoff, M2 receptor activation of nonselective cation channels in smooth muscle cells: calcium and Gi/G(o) requirements. Am J Physiol, 1997. 273(2 Pt 1): p. C500–8.PubMedGoogle Scholar
  50. 50.
    Kajita, J. and H. Yamaguchi, Calcium mobilization by muscarinic cholinergic stimulation in bovine single airway smooth muscle. Am J Physiol, 1993. 264: p. L496–L503.PubMedGoogle Scholar
  51. 51.
    Schaafsma, D., et al., Differential Rho-kinase dependency of full and partial muscarinic receptor agonists in airway smooth muscle contraction. Br J Pharmacol, 2006. 147(7): p. 737–43.PubMedCrossRefGoogle Scholar
  52. 52.
    Janssen, L.J. and S.M. Sims, Ca(2+)-dependent Cl- current in canine tracheal smooth muscle cells. Am J Physiol, 1995. 269(1 Pt 1): p. C163–9.PubMedGoogle Scholar
  53. 53.
    McCann, J.D. and M.J. Welsh, Calcium-activated potassium channels in canine airway smooth muscle. J Physiol, 1986. 372: p. 113–27.PubMedGoogle Scholar
  54. 54.
    Wade, G.R. and S.M. Sims, Muscarinic stimulation of tracheal smooth muscle cells activates large-conductance Ca(2+)-dependent K+ channel. Am J Physiol, 1993. 265(3 Pt 1): p. C658–65.PubMedGoogle Scholar
  55. 55.
    Amrani, Y., et al., Ca2+ increase and Ca(2+)-influx in human tracheal smooth muscle cells: role of Ca2+ pools controlled by sarco-endoplasmic reticulum Ca(2+)-ATPase 2 isoform. Br J Pharmacol, 1995. 115(7): p. 1204–10.PubMedCrossRefGoogle Scholar
  56. 56.
    Govindaraju, V., et al., The effects of extracellular purines and pyrimidines on human airway smooth muscle cells. J Pharmacol Exp Ther, 2005. 315(2): p. 941–8.PubMedCrossRefGoogle Scholar
  57. 57.
    Hyvelin, J.M., et al., Human isolated bronchial smooth muscle contains functional ryanodine/caffeine-sensitive Ca-release channels. Am J Respir Crit Care Med, 2000. 162(2 Pt 1): p. 687–94.PubMedCrossRefGoogle Scholar
  58. 58.
    Ressmeyer, A.R., et al., Human airway contraction and formoterol-induced relaxation is determined by Ca2+ oscillations and Ca2+ sensitivity. Am J Respir Cell Mol Biol, 2010. 43(2): p. 179–91.PubMedCrossRefGoogle Scholar
  59. 59.
    Liu, X. and J.M. Farley, Acetylcholine-induced Ca++−dependent chloride current oscillations are mediated by inositol 1,4,5-trisphosphate in tracheal myocytes. J Pharmacol Exp Ther, 1996. 277(2): p. 796–804.PubMedGoogle Scholar
  60. 60.
    Roux, E., et al., Modelling of Ca2+−activated chloride current in tracheal smooth muscle cells. Acta Biotheoretica, 2001. 49(4): p. 291–300.PubMedCrossRefGoogle Scholar
  61. 61.
    Marhl, M., et al., Complex calcium oscillations and the role of mitochondria and cytosolic proteins. Biosystems, 2000. 57(2): p. 75–86.PubMedCrossRefGoogle Scholar
  62. 62.
    Liu, X. and J.M. Farley, Acetylcholine-induced chloride current oscillations in swine tracheal smooth muscle cells. J Pharmacol Exp Ther, 1996. 276(1): p. 178–86.PubMedGoogle Scholar
  63. 63.
    Bai, Y. and M.J. Sanderson, 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, 2006. 7: p. 34.PubMedCrossRefGoogle Scholar
  64. 64.
    Ouedraogo, N., et al., Effects of intravenous anesthetics on normal and passively sensitized human isolated airway smooth muscle. Anesthesiology, 1998. 88(2): p. 317–26.PubMedCrossRefGoogle Scholar
  65. 65.
    Haberichter, T., et al., The influence of different InsP(3) receptor isoforms on Ca(2+) signaling in tracheal smooth muscle cells. Bioelectrochemistry, 2002. 57(2): p. 129.PubMedCrossRefGoogle Scholar
  66. 66.
    Marhl, M., D. Noble, and E. Roux, Modeling of molecular and cellular mechanisms involved in Ca2+ signal encoding in airway myocytes. Cell Biochem Biophys, 2006. 46(3): p. 285–302.PubMedCrossRefGoogle Scholar
  67. 67.
    Berridge, M.J., P. Lipp, and M.D. Bootman, The versatility and universality of calcium signalling. Nat Rev Mol Cell Biol, 2000. 1(1): p. 11–21.PubMedCrossRefGoogle Scholar
  68. 68.
    Babcock, D.F., et al., Mitochondrial participation in the intracellular Ca2+ network. J Cell Biol, 1997. 136(4): p. 833–44.PubMedCrossRefGoogle Scholar
  69. 69.
    Drummond, R.M. and F.S. Fay, Mitochondria contribute to Ca2+ removal in smooth muscle cells. Pflugers Arch, 1996. 431(4): p. 473–82.PubMedCrossRefGoogle Scholar
  70. 70.
    Fall, C.P. and J.E. Keizer, Mitochondrial modulation of intracellular Ca(2+) signaling. J Theor Biol, 2001. 210(2): p. 151–65.PubMedCrossRefGoogle Scholar
  71. 71.
    Wylam, M.E., A. Xue, and G.C. Sieck, Mechanisms of intrinsic force in small human airways. Respir Physiol Neurobiol, 2012. 181(1): p. 99–108.PubMedCrossRefGoogle Scholar
  72. 72.
    Wang, I.Y., et al., A mathematical analysis of agonist- and KCl-induced Ca(2+) oscillations in mouse airway smooth muscle cells. Biophys J, 2010. 98(7): p. 1170–81.PubMedCrossRefGoogle Scholar
  73. 73.
    Bergner, A. and M.J. Sanderson, ATP stimulates Ca2+ oscillations and contraction in airway smooth muscle cells of mouse lung slices. Am J Physiol Lung Cell Mol Physiol, 2002. 283(6): p. L1271–9.PubMedGoogle Scholar
  74. 74.
    Hagar, R.E. and B.E. Ehrlich, Regulation of the type III InsP(3) receptor by InsP(3) and ATP. Biophysical Journal, 2000. 79(1): p. 271–278.PubMedCrossRefGoogle Scholar
  75. 75.
    Moraru, II, et al., Regulation of type 1 inositol 1,4,5-trisphosphate-gated calcium channels by InsP3 and calcium: Simulation of single channel kinetics based on ligand binding and electrophysiological analysis. J Gen Physiol, 1999. 113(6): p. 837–49.PubMedCrossRefGoogle Scholar
  76. 76.
    Ramos-Franco, J., et al., Single channel function of recombinant type-1 inositol 1,4,5-trisphosphate receptor ligand binding domain splice variants. Biophys J, 1998. 75(6): p. 2783–93.PubMedCrossRefGoogle Scholar
  77. 77.
    Ramos-Franco, J., M. Fill, and G.A. Mignery, Isoform-specific function of single inositol 1,4,5-trisphosphate receptor channels. Biophys J, 1998. 75(2): p. 834–9.PubMedCrossRefGoogle Scholar
  78. 78.
    Dupont, G. and A. Goldbeter, One-pool model for Ca2+ oscillations involving Ca2+ and inositol 1,4,5-trisphosphate as co-agonists for Ca2+ release. Cell Calcium, 1993. 14(4): p. 311–22.PubMedCrossRefGoogle Scholar
  79. 79.
    Morel, J.L., et al., Crucial role of type 2 inositol 1,4,5-trisphosphate receptors for acetylcholine-induced Ca2+ oscillations in vascular myocytes. Arterioscler Thromb Vasc Biol, 2003. 23(9): p. 1567–75.PubMedCrossRefGoogle Scholar
  80. 80.
    Parthimos, D., D.H. Edwards, and T.M. Griffith, Minimal model of arterial chaos generated by coupled intracellular and membrane Ca2+ oscillators. Am J Physiol, 1999. 277(3 Pt 2): p. H1119–44.PubMedGoogle Scholar
  81. 81.
    Roux, E., P. Mbikou, and A. Fajmut, Role of Protein Kinase Network in Excitation-Contraction Coupling in Smooth Muscle Cell, in Protein Kinases, G. Da Silva Xavier, Editor. 2012, InTech: Rijeka. p. 287–320.Google Scholar
  82. 82.
    Mbikou, P., E. Roux, and A. Fajmut, Couplage excitation-contraction du muscle lisse des voies aeriennes. 2010, Sarrebruck: Éditions universitaires européennes. 144.Google Scholar
  83. 83.
    Mbikou, P., et al., Contribution of Rho kinase to the early phase of the calcium-contraction coupling in airway smooth muscle. Exp Physiol, 2011. 96(2): p. 240–58.PubMedCrossRefGoogle Scholar
  84. 84.
    Hai, C.M. and B. Szeto, Agonist-induced myosin phosphorylation during isometric contraction and unloaded shortening in airway smooth muscle. Am J Physiol, 1992. 262(1 Pt 1): p. L53–62.PubMedGoogle Scholar
  85. 85.
    Ouedraogo, N., R. Marthan, and E. Roux, The effects of propofol and etomidate on airway contractility in chronically hypoxic rats. Anesth Analg, 2003. 96(4): p. 1035–41.PubMedCrossRefGoogle Scholar
  86. 86.
    Hai, C.M. and R.A. Murphy, Regulation of shortening velocity by cross-bridge phosphorylation in smooth muscle. Am J Physiol Cell Physiol, 1988. 255(1): p. C86–94.Google Scholar
  87. 87.
    Hai, C.-M. and H.R. Kim, An expanded latch-bridge model of protein kinase C-mediated smooth muscle contraction. J Appl Physiol, 2005. 98(4): p. 1356–1365.PubMedCrossRefGoogle Scholar
  88. 88.
    Hai, C.M. and R.A. Murphy, Cross-bridge phosphorylation and regulation of latch state in smooth muscle. Am. J. Physiol. Cell Physiol., 1988. 254(1): p. C99–106.Google Scholar
  89. 89.
    Lauzon, A.M., et al., A multi-scale approach to airway hyperresponsiveness: from molecule to organ. Front Physiol, 2012. 3: p. 191.PubMedCrossRefGoogle Scholar
  90. 90.
    Berridge, M.J., P.H. Cobbold, and K.S. Cuthbertson, Spatial and temporal aspects of cell signalling. Philos Trans R Soc Lond B Biol Sci, 1988. 320(1199): p. 325–43.PubMedCrossRefGoogle Scholar
  91. 91.
    Marhl, M., et al., Importance of cell variability for calcium signaling in rat airway myocytes. Biophys Chem, 2010. 148: p. 42–50.PubMedCrossRefGoogle Scholar
  92. 92.
    Burdakov, D. and A. Verkhratsky, Biophysical re-equilibration of Ca2+ fluxes as a simple biologically plausible explanation for complex intracellular Ca2+ release patterns. FEBS Lett, 2006. 580(2): p. 463–8.PubMedCrossRefGoogle Scholar

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© Springer International Publishing Switzerland 2014

Authors and Affiliations

  1. 1.Adaptation cardiovasculaire à l’ischémie INSERM U 1034University of BordeauxPessacFrance

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