Mitochondrial Excitation-Energy Coupling in Airway Smooth Muscle

  • Niccole Schaible
  • Philippe Delmotte
  • Gary C. SieckEmail author
Part of the Respiratory Medicine book series (RM, volume 15)


Force generation and contraction of human airway smooth muscle (ASM) involves both an increase in intracellular Ca2 + and an increase in the demand for energy in the form of ATP. Excitation-contraction coupling (ECC) represents a cascade of events that connects the initiating signal, an elevation of cytosolic Ca2 +([Ca2 +]cyt), with the ensuing ATP-consuming mechanical work. Mitochondria play a vital role in this overall process by producing ATP. Moreover, mitochondria also possess the ability to sense [Ca2 +]cyt through a coupled increase in mitochondrial Ca2 +([Ca2 +]mito). In fact, an increase in [Ca2 +]mito leads to an increase in ATP production. Thus, the linkage between [Ca2 +]cyt and [Ca2 +]mito may reflect an “excitation-energy coupling” in ASM that mirrors the energy demand that results from excitation-contraction coupling. The result, in ASM, is the maintenance of an energy supply despite transient and/or sustained energetic demands – an energy homeostasis.


Excitation-contraction coupling Metabolism Ca2+ signaling Homeostasis Energetics 


  1. 1.
    Ali F, Chin L, Pare PD, Seow CY. Mechanism of partial adaptation in airway smooth muscle after a step change in length. J Appl Physiol. 2007;103:569–77.PubMedGoogle Scholar
  2. 2.
    Anesti V, Scorrano L. The relationship between mitochondrial shape and function and the cytoskeleton. Biochim Biophys Acta. 2006;1757:692–9.PubMedGoogle Scholar
  3. 3.
    Balaban NQ, Schwarz US, Riveline D, Goichberg P, Tzur G, Sabanay I, Mahalu D, Safran S, Bershadsky A, Addadi L, Geiger B. Force and focal adhesion assembly: a close relationship studied using elastic micropatterned substrates. Nat Cell Biol. 2001;3:466–72.PubMedGoogle Scholar
  4. 4.
    Benard G, Bellance N, James D, Parrone P, Fernandez H, Letellier T, Rossignol R. Mitochondrial bioenergetics and structural network organization. J Cell Sci. 2007;120: 838–48.PubMedGoogle Scholar
  5. 5.
    Bereiter-Hahn J, Voth M. Dynamics of mitochondria in living cells: shape changes, dislocations, fusion, and fission of mitochondria. Microsc Res Tech. 1994;27:198–219.PubMedGoogle Scholar
  6. 6.
    Boldogh IR, Pon LA. Mitochondria on the move. Trends Cell Biol. 2007;17:502–10.PubMedGoogle Scholar
  7. 7.
    Bose S, French S, Evans FJ, Joubert F, Balaban RS. Metabolic network control of oxidative phosphorylation: multiple roles of inorganic phosphate. J Biol Chem. 2003;278:39155–65.PubMedGoogle Scholar
  8. 8.
    Brenner B. The cross-bridge cycle in muscle. Mechanical, biochemical, and structural studies on single skinned rabbit psoas fibers to characterize cross-bridge kinetics in muscle for correlation with the actomyosin-ATPase in solution. Basic Res Cardiol. 1986;81 Suppl 1:1–15.PubMedGoogle Scholar
  9. 9.
    Brenner B, Eisenberg E. Rate of force generation in muscle: correlation with actomyosin ATPase activity in solution. Proc Natl Acad Sci U S A. 1986;83:3542–6.PubMedCentralPubMedGoogle Scholar
  10. 10.
    Brough D, Schell MJ, Irvine RF. Agonist-induced regulation of mitochondrial and endoplasmic reticulum motility. Biochem J. 2005;392:291–7.PubMedCentralPubMedGoogle Scholar
  11. 11.
    Brown GC. Control of respiration and ATP synthesis in mammalian mitochondria and cells. Biochem J. 1992;284(Pt 1):1–13.PubMedCentralPubMedGoogle Scholar
  12. 12.
    Campello S, Scorrano L. Mitochondrial shape changes: orchestrating cell pathophysiology. EMBO Rep. 2010;11:678–84.PubMedCentralPubMedGoogle Scholar
  13. 13.
    Chada SR, Hollenbeck PJ. Nerve growth factor signaling regulates motility and docking of axonal mitochondria. Curr Biol. 2004;14:1272–6.PubMedGoogle Scholar
  14. 14.
    Chalmers S, Olson ML, MacMillan D, Rainbow RD, McCarron JG. Ion channels in smooth muscle: regulation by the sarcoplasmic reticulum and mitochondria. Cell Calcium. 2007;42: 447–66.PubMedGoogle Scholar
  15. 15.
    Chan DC. Mitochondrial fusion and fission in mammals. Annu Rev Cell Dev Biol. 2006;22:79–99.PubMedGoogle Scholar
  16. 16.
    Chance B, Williams GR. Respiratory enzymes in oxidative phosphorylation I. Kinetics of oxygen utilization. J Biol Chem. 1955;217:383–93.PubMedGoogle Scholar
  17. 17.
    Chance B, Williams GR. The respiratory chain and oxidative phosphorylation. Adv Enzymol Relat Subj Biochem. 1956;17:65–134.PubMedGoogle Scholar
  18. 18.
    Chen T, Zhu L, Wang T, Ye H, Huang K, Hu Q. Mitochondria depletion abolishes agonist-induced Ca2+ plateau in airway smooth muscle cells: potential role of H2O2. Am J Physiol Lung Cell Mol Physiol. 2010;298:L178–88.PubMedGoogle Scholar
  19. 19.
    Dai J, Kuo KH, Leo JM, van Breemen C, Lee CH. Rearrangement of the close contact between the mitochondria and the sarcoplasmic reticulum in airway smooth muscle. Cell Calcium. 2005;37:333–40.PubMedGoogle Scholar
  20. 20.
    Davidson SM, Duchen MR. Calcium microdomains and oxidative stress. Cell Calcium. 2006;40:561–74.PubMedGoogle Scholar
  21. 21.
    de Brito OM, Scorrano L. Mitofusin 2 tethers endoplasmic reticulum to mitochondria. Nature. 2008;456:605–10.PubMedGoogle Scholar
  22. 22.
    De Vos KJ, Allan VJ, Grierson AJ, Sheetz MP. Mitochondrial function and actin regulate dynamin-related protein 1-dependent mitochondrial fission. Curr Biol. 2005;15:678–83.PubMedGoogle Scholar
  23. 23.
    Delmotte P, Ressmeyer AR, Bai Y, Sanderson MJ. Mechanisms of airway smooth muscle relaxation induced by beta2-adrenergic agonists. Front Biosci. 2010;15:750–64.Google Scholar
  24. 24.
    Delmotte PF, Yang B, Thompson MA, Pabelick CM, Prakash YS, Sieck GC. Inflammation alters regional mitochondrial calcium in human airway smooth muscle cells. Am J Physiol Cell Physiol. 2012;303:C244–56.PubMedCentralPubMedGoogle Scholar
  25. 25.
    Denton RM. Regulation of mitochondrial dehydrogenases by calcium ions. Biochim Biophys Acta. 2009;1787:1309–16.PubMedGoogle Scholar
  26. 26.
    Denton RM, McCormack JG. Ca2+ as a second messenger within mitochondria of the heart and other tissues. Annu Rev Physiol. 1990;52:451–66.PubMedGoogle Scholar
  27. 27.
    Drummond RM, Tuft RA. Release of Ca2+ from the sarcoplasmic reticulum increases mitochondrial [Ca2+] in rat pulmonary artery smooth muscle cells. J Physiol. 1999;516(Pt 1): 139–47.PubMedCentralPubMedGoogle Scholar
  28. 28.
    Duchen MR. Mitochondria in health and disease: perspectives on a new mitochondrial biology. Mol Aspects Med. 2004;25:365–451.PubMedGoogle Scholar
  29. 29.
    Fenn WO. A quantitative comparison between the energy liberated and the work performed by the isolated sartorius muscle of the frog. J Physiol. 1923;58:175–203.PubMedCentralPubMedGoogle Scholar
  30. 30.
    Filippin L, Magalhaes PJ, Di Benedetto G, Colella M, Pozzan T. Stable interactions between mitochondria and endoplasmic reticulum allow rapid accumulation of calcium in a subpopulation of mitochondria. J Biol Chem. 2003;278:39224–34.PubMedGoogle Scholar
  31. 31.
    Foskett JK, White C, Cheung KH, Mak DO. Inositol trisphosphate receptor Ca2+ release channels. Physiol Rev. 2007;87:593–658.PubMedCentralPubMedGoogle Scholar
  32. 32.
    Galbraith CG, Yamada KM, Sheetz MP. The relationship between force and focal complex development. J Cell Biol. 2002;159:695–705.PubMedCentralPubMedGoogle Scholar
  33. 33.
    Galloway CA, Yoon Y. Perspectives on: SGP symposium on mitochondrial physiology and medicine: what comes first, misshape or dysfunction? The view from metabolic excess. J Gen Physiol. 2012;139:455–63.PubMedCentralPubMedGoogle Scholar
  34. 34.
    Garcia-Perez C, Schneider TG, Hajnoczky G, Csordas G. Alignment of sarcoplasmic reticulum-mitochondrial junctions with mitochondrial contact points. Am J Physiol Heart Circ Physiol. 2011;301:H1907–15.PubMedCentralPubMedGoogle Scholar
  35. 35.
    GINA report. Global Initiative for Asthma. 2012. Accessed 20 Sep 2012
  36. 36.
    Glancy B, Balaban RS. Role of mitochondrial Ca2+ in the regulation of cellular energetics. Biochemistry. 2012;51:2959–73.PubMedCentralPubMedGoogle Scholar
  37. 37.
    Griffiths EJ, Rutter GA. Mitochondrial calcium as a key regulator of mitochondrial ATP production in mammalian cells. Biochim Biophys Acta. 2009;1787:1324–33.PubMedGoogle Scholar
  38. 38.
    Groen AK, Wanders RJ, Westerhoff HV, van der Meer R, Tager JM. Quantification of the contribution of various steps to the control of mitochondrial respiration. J Biol Chem. 1982;257:2754–7.PubMedGoogle Scholar
  39. 39.
    Gunst SJ, Tang DD. The contractile apparatus and mechanical properties of airway smooth muscle. Eur Respir J. 2000;15:600–16.PubMedGoogle Scholar
  40. 40.
    Gunst SJ, Tang DD, Opazo Saez A. Cytoskeletal remodeling of the airway smooth muscle cell: a mechanism for adaptation to mechanical forces in the lung. Respir Physiol Neurobiol. 2003;137:151–68.PubMedGoogle Scholar
  41. 41.
    Gunst SJ, Zhang W. Actin cytoskeletal dynamics in smooth muscle: a new paradigm for the regulation of smooth muscle contraction. Am J Physiol Cell Physiol. 2008;295:C576–87.PubMedCentralPubMedGoogle Scholar
  42. 42.
    Gunter TE, Buntinas L, Sparagna G, Eliseev R, Gunter K. Mitochondrial calcium transport: mechanisms and functions. Cell Calcium. 2000;28:285–96.PubMedGoogle Scholar
  43. 43.
    Gunter TE, Sheu SS. Characteristics and possible functions of mitochondrial Ca(2+) transport mechanisms. Biochim Biophys Acta. 2009;1787:1291–308.PubMedCentralPubMedGoogle Scholar
  44. 44.
    Hai CM, Murphy RA. Cross-bridge phosphorylation and regulation of latch state in smooth muscle. Am J Physiol. 1988;254:C99–106.PubMedGoogle Scholar
  45. 45.
    Hajnoczky G, Hager R, Thomas AP. Mitochondria suppress local feedback activation of inositol 1,4, 5-trisphosphate receptors by Ca2+. J Biol Chem. 1999;274:14157–62.PubMedGoogle Scholar
  46. 46.
    Hajnoczky G, Robb-Gaspers LD, Seitz MB, Thomas AP. Decoding of cytosolic calcium oscillations in the mitochondria. Cell. 1995;82:415–24.PubMedGoogle Scholar
  47. 47.
    Halestrap AP. The regulation of the matrix volume of mammalian mitochondria in vivo and in vitro and its role in the control of mitochondrial metabolism. Biochim Biophys Acta. 1989;973:355–82.PubMedGoogle Scholar
  48. 48.
    Halestrap AP, Quinlan PT, Whipps DE, Armston AE. Regulation of the mitochondrial matrix volume in vivo and in vitro. The role of calcium. Biochem J. 1986;236:779–87.PubMedCentralPubMedGoogle Scholar
  49. 49.
    Herrera AM, Martinez EC, Seow CY. Electron microscopic study of actin polymerization in airway smooth muscle. Am J Physiol Lung Cell Mol Physiol. 2004;286:L1161–8.PubMedGoogle Scholar
  50. 50.
    Hodgkinson JL, Newman TM, Marston SB, Severs NJ. The structure of the contractile apparatus in ultrarapidly frozen smooth muscle: freeze-fracture, deep-etch, and freeze-substitution studies. J Struct Biol. 1995;114:93–104.PubMedGoogle Scholar
  51. 51.
    Hollenbeck PJ. The pattern and mechanism of mitochondrial transport in axons. Front Biosci. 1996;1:d91–102.PubMedGoogle Scholar
  52. 52.
    Hoppe UC. Mitochondrial calcium channels. FEBS Lett. 2010;584:1975–81.PubMedGoogle Scholar
  53. 53.
    Huxley H, Hanson J. Changes in the cross-striations of muscle during contraction and stretch and their structural interpretation. Nature. 1954;173:973–6.PubMedGoogle Scholar
  54. 54.
    Huxley AF, Niedergerke R. Structural changes in muscle during contraction; interference microscopy of living muscle fibres. Nature. 1954;173:971–3.PubMedGoogle Scholar
  55. 55.
    Ijpma G, Al-Jumaily AM, Cairns SP, Sieck GC. Myosin filament polymerization and depolymerization in a model of partial length adaptation in airway smooth muscle. J Appl Physiol. 2011;111:735–42.PubMedCentralPubMedGoogle Scholar
  56. 56.
    Ishida Y, Riesinger I, Wallimann T, Paul RJ. Compartmentation of ATP synthesis and utilization in smooth muscle: roles of aerobic glycolysis and creatine kinase. Mol Cell Biochem. 1994;133–134:39–50.PubMedGoogle Scholar
  57. 57.
    Jones KA, Lorenz RR, Prakash YS, Sieck GC, Warner DO. ATP hydrolysis during contraction of permeabilized airway smooth muscle. Am J Physiol. 1999;277:L334–42.PubMedGoogle Scholar
  58. 58.
    Jones KA, Perkins WJ, Lorenz RR, Prakash YS, Sieck GC, Warner DO. F-actin stabilization increases tension cost during contraction of permeabilized airway smooth muscle in dogs. J Physiol. 1999;519(Pt 2):527–38.PubMedCentralPubMedGoogle Scholar
  59. 59.
    Jouaville LS, Pinton P, Bastianutto C, Rutter GA, Rizzuto R. Regulation of mitochondrial ATP synthesis by calcium: evidence for a long-term metabolic priming. Proc Natl Acad Sci U S A. 1999;96:13807–12.PubMedCentralPubMedGoogle Scholar
  60. 60.
    Kannan MS, Fenton AM, Prakash YS, Sieck GC. Cyclic ADP-ribose stimulates sarcoplasmic reticulum calcium release in porcine coronary artery smooth muscle. Am J Physiol. 1996;270:H801–6.PubMedGoogle Scholar
  61. 61.
    Kannan MS, Prakash YS, Brenner T, Mickelson JR, Sieck GC. Role of ryanodine receptor channels in Ca2+ oscillations of porcine tracheal smooth muscle. Am J Physiol. 1997;272:L659–64.PubMedGoogle Scholar
  62. 62.
    Krisanda JM, Paul RJ. Phosphagen and metabolite content during contraction in porcine carotid artery. Am J Physiol. 1983;244:C385–90.PubMedGoogle Scholar
  63. 63.
    Kuo KH, Herrera AM, Seow CY. Ultrastructure of airway smooth muscle. Respir Physiol Neurobiol. 2003;137:197–208.PubMedGoogle Scholar
  64. 64.
    Kuo KH, Herrera AM, Wang L, Pare PD, Ford LE, Stephens NL, Seow CY. Structure-function correlation in airway smooth muscle adapted to different lengths. Am J Physiol Cell Physiol. 2003;285:C384–90.PubMedGoogle Scholar
  65. 65.
    Kuo KH, Wang L, Pare PD, Ford LE, Seow CY. Myosin thick filament lability induced by mechanical strain in airway smooth muscle. J Appl Physiol. 2001;90:1811–6.PubMedGoogle Scholar
  66. 66.
    Landolfi B, Curci S, Debellis L, Pozzan T, Hofer AM. Ca2+ homeostasis in the agonist-sensitive internal store: functional interactions between mitochondria and the ER measured In situ in intact cells. J Cell Biol. 1998;142:1235–43.PubMedCentralPubMedGoogle Scholar
  67. 67.
    McCarron JG, Chalmers S, Bradley KN, MacMillan D, Muir TC. Ca2+ microdomains in smooth muscle. Cell Calcium. 2006;40:461–93.PubMedGoogle Scholar
  68. 68.
    Mehta D, Gunst SJ. Actin polymerization stimulated by contractile activation regulates force development in canine tracheal smooth muscle. J Physiol. 1999;519(Pt 3):829–40.PubMedCentralPubMedGoogle Scholar
  69. 69.
    Murphy RA, Rembold CM. The latch-bridge hypothesis of smooth muscle contraction. Can J Physiol Pharmacol. 2005;83:857–64.PubMedCentralPubMedGoogle Scholar
  70. 70.
    Nassar A, Simpson AW. Elevation of mitochondrial calcium by ryanodine-sensitive calcium-induced calcium release. J Biol Chem. 2000;275:23661–5.PubMedGoogle Scholar
  71. 71.
    Nicholls DG. Mitochondria and calcium signaling. Cell Calcium. 2005;38:311–7.PubMedGoogle Scholar
  72. 72.
    Pabelick CM, Prakash YS, Kannan MS, Sieck GC. Spatial and temporal aspects of calcium sparks in porcine tracheal smooth muscle cells. Am J Physiol. 1999;277:L1018–25.PubMedGoogle Scholar
  73. 73.
    Pabelick CM, Sieck GC, Prakash YS. Invited review: significance of spatial and temporal heterogeneity of calcium transients in smooth muscle. J Appl Physiol. 2001;91:488–96.PubMedGoogle Scholar
  74. 74.
    Pacher P, Csordas P, Schneider T, Hajnoczky G. Quantification of calcium signal transmission from sarco-endoplasmic reticulum to the mitochondria. J Physiol. 2000;529(Pt 3):553–64.PubMedCentralPubMedGoogle Scholar
  75. 75.
    Palmieri L, Pardo B, Lasorsa FM, del Arco A, Kobayashi K, Iijima M, Runswick MJ, Walker JE, Saheki T, Satrustegui J, Palmieri F. Citrin and aralar1 are Ca2+-stimulated aspartate/glutamate transporters in mitochondria. EMBO J. 2001;20:5060–9.PubMedCentralPubMedGoogle Scholar
  76. 76.
    Park MK, Ashby MC, Erdemli G, Petersen OH, Tepikin AV. Perinuclear, perigranular and sub-plasmalemmal mitochondria have distinct functions in the regulation of cellular calcium transport. EMBO J. 2001;20:1863–74.PubMedCentralPubMedGoogle Scholar
  77. 77.
    Paul RJ. Smooth muscle energetics. Annu Rev Physiol. 1989;51:331–49.PubMedGoogle Scholar
  78. 78.
    Pizzo P, Drago I, Filadi R, Pozzan T. Mitochondrial Ca2+ homeostasis: mechanism, role, and tissue specificities. Pflugers Arch. 2012;464:3–17.PubMedGoogle Scholar
  79. 79.
    Prakash YS, Kannan MS, Sieck GC. Regulation of intracellular calcium oscillations in porcine tracheal smooth muscle cells. Am J Physiol. 1997;272:C966–75.PubMedGoogle Scholar
  80. 80.
    Prakash YS, Kannan MS, Walseth TF, Sieck GC. Role of cyclic ADP-ribose in the regulation of [Ca2+]i in porcine tracheal smooth muscle. Am J Physiol. 1998;274:C1653–60.PubMedGoogle Scholar
  81. 81.
    Prakash YS, Pabelick CM, Kannan MS, Sieck GC. Spatial and temporal aspects of ACh-induced [Ca2+]i oscillations in porcine tracheal smooth muscle. Cell Calcium. 2000;27:153–62.PubMedGoogle Scholar
  82. 82.
    Rapizzi E, Pinton P, Szabadkai G, Wieckowski MR, Vandecasteele G, Baird G, Tuft RA, Fogarty KE, Rizzuto R. Recombinant expression of the voltage-dependent anion channel enhances the transfer of Ca2+ microdomains to mitochondria. J Cell Biol. 2002;159:613–24.PubMedCentralPubMedGoogle Scholar
  83. 83.
    Rizzuto R, Bastianutto C, Brini M, Murgia M, Pozzan T. Mitochondrial Ca2+ homeostasis in intact cells. J Cell Biol. 1994;126:1183–94.PubMedGoogle Scholar
  84. 84.
    Rizzuto R, Brini M, Murgia M, Pozzan T. Microdomains with high Ca2+ close to IP3-sensitive channels that are sensed by neighboring mitochondria. Science. 1993;262:744–7.PubMedGoogle Scholar
  85. 85.
    Rizzuto R, Duchen MR, Pozzan T. Flirting in little space: the ER/mitochondria Ca2+ liaison. Sci STKE. 2004;2004:re1.PubMedGoogle Scholar
  86. 86.
    Rizzuto R, Pinton P, Carrington W, Fay FS, Fogarty KE, Lifshitz LM, Tuft RA, Pozzan T. Close contacts with the endoplasmic reticulum as determinants of mitochondrial Ca2+ responses. Science. 1998;280:1763–6.PubMedGoogle Scholar
  87. 87.
    Rizzuto R, Pozzan T. Microdomains of intracellular Ca2+: molecular determinants and functional consequences. Physiol Rev. 2006;86:369–408.PubMedGoogle Scholar
  88. 88.
    Rudolf R, Mongillo M, Magalhaes PJ, Pozzan T. In vivo monitoring of Ca2+ uptake into mitochondria of mouse skeletal muscle during contraction. J Cell Biol. 2004;166:527–36.PubMedCentralPubMedGoogle Scholar
  89. 89.
    Sanderson MJ, Delmotte P, Bai Y, Perez-Zogbhi JF. Regulation of airway smooth muscle cell contractility by Ca2+ signaling and sensitivity. Proc Am Thorac Soc. 2008;5:23–31.PubMedGoogle Scholar
  90. 90.
    Scholz TD, Laughlin MR, Balaban RS, Kupriyanov VV, Heineman FW. Effect of substrate on mitochondrial NADH, cytosolic redox state, and phosphorylated compounds in isolated hearts. Am J Physiol. 1995;268:H82–91.PubMedGoogle Scholar
  91. 91.
    Seow CY. Myosin filament assembly in an ever-changing myofilament lattice of smooth muscle. Am J Physiol Cell Physiol. 2005;289:C1363–8.PubMedGoogle Scholar
  92. 92.
    Sharma VK, Ramesh V, Franzini-Armstrong C, Sheu SS. Transport of Ca2+ from sarcoplasmic reticulum to mitochondria in rat ventricular myocytes. J Bioenerg Biomembr. 2000;32:97–104.PubMedGoogle Scholar
  93. 93.
    Sieck GC, Gransee HM. Respiratory muscles structure, function and regulation. In: Colloquium series on integrated systems physiology, from molecule to function to disease, vol. 34. San Rafael:Morgan & Claypool Life Sciences; 2012. p. 1. Online resource (viii, 87 p).Google Scholar
  94. 94.
    Sieck GC, Han YS, Pabelick CM, Prakash YS. Temporal aspects of excitation-contraction coupling in airway smooth muscle. J Appl Physiol. 2001;91:2266–74.PubMedGoogle Scholar
  95. 95.
    Sieck GC, Han YS, Prakash YS, Jones KA. Cross-bridge cycling kinetics, actomyosin ATPase activity and myosin heavy chain isoforms in skeletal and smooth respiratory muscles. Comp Biochem Physiol B Biochem Mol Biol. 1998;119:435–50.PubMedGoogle Scholar
  96. 96.
    Sieck GC, Kannan MS, Prakash YS. Heterogeneity in dynamic regulation of intracellular calcium in airway smooth muscle cells. Can J Physiol Pharmacol. 1997;75:878–88.PubMedGoogle Scholar
  97. 97.
    Sieck GC, Prakash YS. Cross-bridge kinetics in respiratory muscles. Eur Respir J. 1997;10: 2147–58.PubMedGoogle Scholar
  98. 98.
    Somlyo AP, Somlyo AV. Signal transduction by G-proteins, rho-kinase and protein phosphatase to smooth muscle and non-muscle myosin II. J Physiol. 2000;522(Pt 2):177–85.PubMedCentralPubMedGoogle Scholar
  99. 99.
    Sparagna GC, Gunter KK, Sheu SS, Gunter TE. Mitochondrial calcium uptake from physiological-type pulses of calcium. A description of the rapid uptake mode. J Biol Chem. 1995;270:27510–5.PubMedGoogle Scholar
  100. 100.
    Spurway NC, Wray S. A phosphorus nuclear magnetic resonance study of metabolites and intracellular pH in rabbit vascular smooth muscle. J Physiol. 1987;393:57–71.PubMedCentralPubMedGoogle Scholar
  101. 101.
    Szabadkai G, Simoni AM, Chami M, Wieckowski MR, Youle RJ, Rizzuto R. Drp-1-dependent division of the mitochondrial network blocks intraorganellar Ca2+ waves and protects against Ca2+-mediated apoptosis. Mol Cell. 2004;16:59–68.PubMedGoogle Scholar
  102. 102.
    Szado T, Kuo KH, Bernard-Helary K, Poburko D, Lee CH, Seow C, Ruegg UT, van Breemen C. Agonist-induced mitochondrial Ca2+ transients in smooth muscle. FASEB J. 2003;17: 28–37.PubMedGoogle Scholar
  103. 103.
    Szalai G, Csordas G, Hantash BM, Thomas AP, Hajnoczky G. Calcium signal transmission between ryanodine receptors and mitochondria. J Biol Chem. 2000;275:15305–13.PubMedGoogle Scholar
  104. 104.
    Tarasov AI, Griffiths EJ, Rutter GA. Regulation of ATP production by mitochondrial Ca2+. Cell Calcium. 2012;52:28–35.PubMedCentralPubMedGoogle Scholar
  105. 105.
    Territo PR, French SA, Dunleavy MC, Evans FJ, Balaban RS. Calcium activation of heart mitochondrial oxidative phosphorylation: rapid kinetics of mVO2, NADH, and light scattering. J Biol Chem. 2001;276:2586–99.PubMedGoogle Scholar
  106. 106.
    Trian T, Benard G, Begueret H, Rossignol R, Girodet PO, Ghosh D, Ousova O, Vernejoux JM, Marthan R, Tunon-de-Lara JM, Berger P. Bronchial smooth muscle remodeling involves calcium-dependent enhanced mitochondrial biogenesis in asthma. J Exp Med. 2007;204:3173–81.PubMedCentralPubMedGoogle Scholar
  107. 107.
    Varadi A, Johnson-Cadwell LI, Cirulli V, Yoon Y, Allan VJ, Rutter GA. Cytoplasmic dynein regulates the subcellular distribution of mitochondria by controlling the recruitment of the fission factor dynamin-related protein-1. J Cell Sci. 2004;117:4389–400.PubMedGoogle Scholar
  108. 108.
    White TA, Kannan MS, Walseth TF. Intracellular calcium signaling through the cADPR pathway is agonist specific in porcine airway smooth muscle. FASEB J. 2003;17:482–4.PubMedGoogle Scholar
  109. 109.
    Wylam ME, Xue A, Sieck GC. Mechanisms of intrinsic force in small human airways. Respir Physiol Neurobiol. 2012;181:99–108.PubMedCentralPubMedGoogle Scholar
  110. 110.
    Xu JQ, Harder BA, Uman P, Craig R. Myosin filament structure in vertebrate smooth muscle. J Cell Biol. 1996;134:53–66.PubMedGoogle Scholar
  111. 111.
    Yi M, Weaver D, Hajnoczky G. Control of mitochondrial motility and distribution by the calcium signal: a homeostatic circuit. J Cell Biol. 2004;167:661–72.PubMedCentralPubMedGoogle Scholar
  112. 112.
    Zalk R, Lehnart SE, Marks AR. Modulation of the ryanodine receptor and intracellular calcium. Annu Rev Biochem. 2007;76:367–85.PubMedGoogle Scholar
  113. 113.
    Zhang W, Gunst SJ. Interactions of airway smooth muscle cells with their tissue matrix: implications for contraction. Proc Am Thorac Soc. 2008;5:32–9.PubMedCentralPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Niccole Schaible
    • 1
  • Philippe Delmotte
    • 1
  • Gary C. Sieck
    • 1
    Email author
  1. 1.Department of Physiology and Biomedical EngineeringMayo Clinic College of MedicineRochesterUSA

Personalised recommendations