Advertisement

Involvement of Na+/Ca2+ Exchange in Normal Cardiac Excitation-Contraction Coupling and in Ca2+ Overload during Ischemia and Reperfusion

  • Hiroshi Satoh
  • Hideki Katoh
  • Hajime Terada
  • Hideharu Hayashi
Part of the Progress in Experimental Cardiology book series (PREC, volume 6)

Summary

The Ca2+ overload is known to play a major role in cellular dysfunction and death in ischemic and reperfused myocardium. The sarcolemmal Na+/Ca2+ exchange (NCX) is one of the essential regulators of Ca2+ homeostasis in normal excitation-contraction (E-C) coupling and can be a possible route for Ca2+ overload during ischemia and reperfusion. NCX is a bidirectional transport process, capable of moving Ca2+ in either direction across the sarcolemma, depending on the membrane potential and the transmembrane gradients of Na+ and Ca2+. In normal E-C coupling, NCX mainly operates to extrude Ca2+ from cytoplasm and the role of Ca2+ entering via NCX seems to be rather small, although there may be species difference. During ischemia, the decrease in Ca2+ efflux via the forward mode of NCX by high [Na+]i,membrane depolarization, low pHi, and low ATP would delay the Ca2+ transient decay and would increase diastolic [Ca2+]i. After reperfusion, the recovery of NCX activity, with sustained cellular Na+ loading, can induce Ca2+ influx via the reverse mode of NCX, causing spontaneous Ca2+ release from the sarcoplasmic reticulum and triggered arrhythmias. While there are some possible therapeutic agents which may reduce ischemia/reperfusion injury, a relatively specific blocker of the reverse mode of NCX has been shown to protect myocardium from Ca2+ overload. These findings indicate the importance of NCX for normal E-C coupling and Ca2+ overload in ischemia/reperfusion injury, and the possibility of specific and clinically useful drugs targeting NCX.

Keywords

Na+/Ca2+ exchange excitation-contraction coupling ischemia and reperfusion Ca2+ overload 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Bers DM. 2001. Excitation-contraction coupling and cardiac contractile force. Second edition. Dordrecht, Netherlands; Kluwer Academic Press.CrossRefGoogle Scholar
  2. 2.
    Fabiato A. 1985. Time and calcium dependence of activation and inactivation of calcium induced release of calcium from the sarcoplasmic reticulum of a skinned canine cardiac Purkinje fiber. J Gen Physiol 85:247–289.PubMedCrossRefGoogle Scholar
  3. 3.
    Hilgemann DW, Collins A, Matsuoka S. 1992. Steady-state and dynamic properties of cardiac sodium-calcium exchange: secondary modulation by cytoplasmic calcium and ATP. J Gen Physiol 100:933–961.PubMedCrossRefGoogle Scholar
  4. 4.
    Shigekawa M, Iwamoto T. 2001. Cardiac Na+-Ca2+ exchange. Molecular and pharmacological aspects. Circ Res 88:864–876.PubMedCrossRefGoogle Scholar
  5. 5.
    Leblanc N, Hume JR. 1990. Sodium current-induced release of calcium from cardiac sarcoplasmic reticulum. Science 248:372–376.PubMedCrossRefGoogle Scholar
  6. 6.
    Lipp P, Niggli E. 1994. Sodium current induced calcium signals in isolated guinea-pig ventricular myocyte. J Physiol 474:439–446.PubMedGoogle Scholar
  7. 7.
    Wasserstrom JA, Vites AM. 1996. The role of Na+-Ca2+ exchange in activation of excitation-contraction coupling in rat ventricular myocytes. J Physiol 493:529–554.PubMedGoogle Scholar
  8. 8.
    Litwin SE, Li J, Bridge JH. 1998. Na-Ca exchange and the trigger for sarcoplasmic reticulum Ca release: studies in adult rabbit ventricular myocytes. Biophys J 75:359–371.PubMedCrossRefGoogle Scholar
  9. 9.
    Tani M, Neely JR. 1989. Role of intracellular Na in Ca overload and depressed recovery of ventricular function of reperfused ischemic rat heart. Circ Res 65:1045–1056.PubMedCrossRefGoogle Scholar
  10. 10.
    Nishida M, Borzak S, Kraemer B, Navas JP, Kelly RA, Smith TW, Marsh JD. 1993. Role of cation gradients in hypercontracture of myocytes during simulated ischemia and reperfusion. Am J Physiol 264:H1896–H1906.PubMedGoogle Scholar
  11. 11.
    Noble D, LeGuennec JY, Winslow R. 1996. Functional roles of sodium-calcium exchange in normal and abnormal cardiac rhythm. Ann NY Acad Sci 15:779:480–489.CrossRefGoogle Scholar
  12. 12.
    Schlotthauer K, Bers DM. 2000. Sarcoplasmic reticulum Ca2+ release causes myocyte depolarization. Underlying mechanism and threshold for triggered action potentials. Circ Res 87:774–780.PubMedCrossRefGoogle Scholar
  13. 13.
    Tani M, Neely JR. 1990. Na+ accumulation increases Ca2+ overload and impairs function in anoxic rat heart. J Mol Cell Cardiol 22:57–72.PubMedCrossRefGoogle Scholar
  14. 14.
    Poole-Wilson PA, Harding DP, Bourdillon PDV, Tones MA. 1984. Calcium out of control. J Mol Cell Cardiol 16:175–187.PubMedCrossRefGoogle Scholar
  15. 15.
    Murphy JG, Smith TW, Marsh JD. 1988. Mechanisms of reoxygenation-induced calcium overload in cultured chick embryo heart cells. Am J Physiol 254:H1133–H1141.PubMedGoogle Scholar
  16. 16.
    Hano O, Silverman HS, Blank PS, Mellits ED, Baumgardner R, Lakatta EG, Stern MD. 1991. Nicardipine prevents calcium loading and “oxygen paradox” in anoxic single rat myocytes by a mechanism independent of calcium channel blockade. Circ Res 69:1500–1505.PubMedCrossRefGoogle Scholar
  17. 17.
    Carafoli E. 1985. The homeostasis of calcium in heart cells. J Mol Cell Cardiol 17:203–212.PubMedCrossRefGoogle Scholar
  18. 18.
    Lazdunski M, Frelin C, Vigue P 1985. The sodium/hydrogen exchange system in cardiac cells: its biochemical and pharmacological properties and its role in regulating internal concentrations of sodium and internal pH. J Mol Cell Cardiol 17:1029–1042.PubMedCrossRefGoogle Scholar
  19. 19.
    Piwnica-Worms D, Jacob R, Shigeto N, Horres CR, Lieberman M. 1986. Na/H exchange in cultured chick heart cells: secondary stimulation of electrogenic transport during recovery from intracellular acidosis. J Mol Cell Cardiol 18:1109–1116.PubMedCrossRefGoogle Scholar
  20. 20.
    Satoh H, Hayashi H, Noda N, Terada H, Kobayashi A, Hirano M, Yamashita Y, Yamazaki N. 1994. Regulation of [Na+]i, and [Ca2+]i in guinea pig myocytes: dual loading of fluorescent indicators SBFI and fluo 3. Am J Physiol 266:H568–H576.PubMedGoogle Scholar
  21. 21.
    Miura Y, Kimura J. 1989. Sodium-calcium exchange current: dependence on internal Ca and Na and competitive binding of external Na and Ca. J Gen Physiol 93:1129–1145.PubMedCrossRefGoogle Scholar
  22. 22.
    Bassani JWM, Bassani RA, Bers DM. 1994. Relaxation in rabbit and rat cardiac cells: species-dependent differences in cellular mechanisms. J Physiol 476.2:279–293.Google Scholar
  23. 23.
    Callewaert G. 1992. Excitation-contraction coupling in mammalian cardiac cells. Cardiovasc Res 26:923–932.PubMedCrossRefGoogle Scholar
  24. 24.
    Levesque PC, Leblanc N, Hume JR. 1994. Release of calcium from guinea pig cardiac sarcoplasmic reticulum induced by sodium-calcium exchange. Cardiovasc Res 28:370–378.PubMedCrossRefGoogle Scholar
  25. 25.
    Sipido KR, Maes MM, Van de Werf. 1997. Low efficiency of Ca2+ entry through the Na/Ca exchanger as trigger for Ca2+ release from the sarcoplasmic reticulum. Circ Res 81:1034–1044.PubMedCrossRefGoogle Scholar
  26. 26.
    Yao A, Nonaka A, Zubair I, Lu L, Philipson KD, Bridge JHB, Barry H. 1998. Effects of overexpression of the Na+-Ca2+ exchanger on [Ca2+]i transients in murine ventricular myocytes. Circ Res 82:657–665.PubMedCrossRefGoogle Scholar
  27. 27.
    Iwamoto T, Watano T, Shigekawa M. 1996. A novel isothiourea derivative selectively inhibits the reverse mode of Na+/Ca2+ exchange in cells expressing NCX1. J Biol Chem 271:22391–22397.PubMedCrossRefGoogle Scholar
  28. 28.
    Watano T, Kimura J, Morita T, Nakanishi H. 1996. A novel antagonist, No.7943 of the Na+/Ca2+ exchange current in guinea-pig cardiac ventricular cells. Br J Pharmacol 119:555–563.PubMedCrossRefGoogle Scholar
  29. 29.
    Lee CO, Dagostino M. 1982. Effect of strophanthidin on intracellular Na ion activity and twitch tension of constantly driven canine cardiac Purkinje fibers. Biophys J 40:185–198.PubMedCrossRefGoogle Scholar
  30. 30.
    Terada H, Hayashi H, Satoh H, Katoh H, Yamazaki N. 1994. Simultaneous measurement of [Na+]i and Ca2+ transients in an isolated myocyte: effects of strophanthidin. Biochem Biophys Res Commun 203.2:1050–1056.CrossRefGoogle Scholar
  31. 31.
    Diaz ME, Trafford AW, O’Neill SC, Eisner DA. 1997. Measurement of sarcoplasmic reticulum Ca2+ content and sarcolemmal Ca2+ fluxes in isolated rat ventricular myocytes during spontaneous Ca2+ release. J Physiol 501:3–16.PubMedCrossRefGoogle Scholar
  32. 32.
    Satoh H, Ginsburg KS, Qing K, Terada H, Hayashi H, Bers DM. 2000. KB-R7943 block of Ca2+ influx via Na+/Ca2+ exchange does not alter twitches or glycoside inotropy, but prevents Ca2+ overload in rat ventricular myocytes. Circulation 101:1441–1446.PubMedCrossRefGoogle Scholar
  33. 33.
    Watano T, Harada Y, Harada K, Nishimura N. 1999. Effect of Na+/Ca2+ exchange inhibitor, KBR7943, on ouabain-induced arrhythmias in guinea-pigs. Br J Pharmacol 127:1846–1850.PubMedCrossRefGoogle Scholar
  34. 34.
    Hayashi H, Satoh H, Noda N, Terada H, Kobayashi A, Hirano M, Yamashita Y, Yamazaki N. 1994. Simultaneous measurement of intracellular Na+ and Ca2+ during K+-free perfusion in isolated myocytes. Am J Physiol 266:C416–C422.PubMedGoogle Scholar
  35. 35.
    Frelin C, Vigue P, Lazdunski M. 1984. The role of the Na+/H+ exchange system in cardiac cells in relation to the control of the internal Na+ concentration. A molecular basis for the antagonistic effect of ouabain and amiloride on the heart. J Biol Chem 259:8880–8885.PubMedGoogle Scholar
  36. 36.
    Pike MM, Luo CS, Clark MD, Kirk K, Kitakaze M, Madden MC, Cragoe EJ, Pohost GM. 1993. NMR measurments of Na+ and cellular energy in ischemic rat heart: role of Na+-H+ exchange. Am J Physiol 265:H2017–H2026.PubMedGoogle Scholar
  37. 37.
    Karmazyn M, Gan XT, Humphreys RA, Yoshida H, Kusumoto K. 1999. The myocardial Na+-H+ exchange: structure, regulation, and its role in heart disease. Circ Res 85:777–786.PubMedCrossRefGoogle Scholar
  38. 38.
    Bountra C, Powell T, Vaughan-Jones RD. 1990. Comparison of intracellular pH transients in single ventricular myocytes and isolated ventricular muscle of guinea-pig. J Physiol 424:343–365.PubMedGoogle Scholar
  39. 39.
    Bertrand B, Wakabayashi S, Ikeda T, Pouysségur J, Shigekawa M. 1994. The Na+/H+ exchanger isoform 1 (NHE-1) is a novel member of the calmodulin-binding proteins. J Biol Chem 269:13703–13709.PubMedGoogle Scholar
  40. 40.
    Wu M-L, Vaughan-Jones RD. 1997. Interaction between Na+ and H+ ions on Na-H exchange in sheep cardiac Purkinje fibers. J Mol Cell Cardiol 29:1131–1140.PubMedCrossRefGoogle Scholar
  41. 41.
    Sabri A, Byron KL, Samarel AM, Bell J, Lucchesi PA. 1998. Hydrogen peroxide activates mitogen-activated protein kinases and Na+-H+ exchange in neonatal rat cardiac myocytes. Circ Res 82:1053–1062.PubMedCrossRefGoogle Scholar
  42. 42.
    Katoh H, Terada H, Iimuro M, Sugiyama S, Qing K, Satoh H, Hayashi H. 1998. Heterogeneity and underlying mechanism for inotropic action of endothelin-1 in rat ventricular myocytes. Br J Pharmacol 123:1343–1350.PubMedCrossRefGoogle Scholar
  43. 43.
    Khandoudi N, Ho J, Karmazyn M. 1994. Role of Na+-H+ exchange in mediating effects of endothelin-1 on normal and ischemic/reperfused hearts. Circ Res 75:369–378.PubMedCrossRefGoogle Scholar
  44. 44.
    Dizon J, Burkhoff D, Tauskela J, Whang J, Cannon P, Katz J. 1998. Metabolic inhibition in the perfused rat heart: evidence for glycolytic requirement for normal sodium homeostasis. Am J Physiol 274:H1082–H1089.PubMedGoogle Scholar
  45. 45.
    Glitisch HG, Tappe A. 1993. The Na+/K+ pump of cardiac Purkinje cells is preferentially fueled by glycolytic ATP production. Pflügers Arch 422:380–385.CrossRefGoogle Scholar
  46. 46.
    Hilgemann DW 1997. Cytoplasmic ATP-dependent regulation of ion transporters and channels: Mechanisms and messengers. Annu Rev Physiol 59:193–220.PubMedCrossRefGoogle Scholar
  47. 47.
    Wu M-L, Vaughan-Jones RD. 1994. Effect of metabolic inhibitors and second messengers upon Na+-H+ exchange in the sheep cardiac Purkinje fibre. J Physiol 471:583–597.Google Scholar
  48. 48.
    Sugiyama S, Satoh H, Nomura N, Terada H, Watanabe H, Hayashi H. 2001. The importance of glycolytic ally-derived ATP for the Na+/H+ exchange activity in guinea pig ventricular myocytes. Mol Cell Biochem 217:153–161.PubMedCrossRefGoogle Scholar
  49. 49.
    Satoh H, Sugiyama S, Nomura N, Terada H, Hayashi H. 2001. Importance of glycolytically-derived ATP for Na+ loading via Na+/H+ exchange during metabolic inhibition in guinea pig ventricular myocytes. Clin Sci 101:243–251.PubMedCrossRefGoogle Scholar
  50. 50.
    Berger DS, Fellner SK, Robinson KA, Vlasica K, Godoy IE, Shroff SG. 1999. Disparate effects of three types of extracellular acidosis on left ventricular function. Am J Physiol 276:H582–H594.PubMedGoogle Scholar
  51. 51.
    Shimada Y, Hearse DJ, Avkiran M. 1996. Impact of extracellular buffer composition on cardioprotective efficacy of Na+/H+ exchange inhibitors. Am J Physiol 270:H692–H700.PubMedGoogle Scholar
  52. 52.
    MacLeod KT. 1989. Effects of hypoxia and metabolic inhibition on the intracellular sodium activity of mammalian ventricular muscle. J Physiol 416:455–468.PubMedGoogle Scholar
  53. 53.
    Grinwald PM, Brosnahan C. 1987. Sodium imbalance as a cause of calcium overload in posthypoxic reoxygenation injury. J Mol Cell Cardiol 19:487–495.PubMedCrossRefGoogle Scholar
  54. 54.
    Katoh H, Satoh H, Nakamura T, Terada H, Hayashi H. 1994. The role of Na+/H+ exchange and the Na+/K+ pump in the regulation of [Na+]i during metabolic inhibition in guinea pig myocytes. Biochem Biophys Res Commun 203:93–98.PubMedCrossRefGoogle Scholar
  55. 55.
    Garner JA, Hearse DJ, Bernier M. 1990. R56865, a potent new antiarrhythmic agent, effective during ischemia and reperfusion in the rat heart. J Cardiovasc Pharmacol 16:468–479.PubMedCrossRefGoogle Scholar
  56. 56.
    Lu HR, Yang P, Remeysen P, Saels A, Dai DZ, De Clerck F. 1999. Ischemia/reperfusion-induced arrhythmias in anaesthetized rats: a role of Na+ and Ca2+ influx. Eur J Pharmacol 365:233–239.PubMedCrossRefGoogle Scholar
  57. 57.
    Haigney MCP, Miyata H, Lakatta EG, Stern MD, Silvermann HS. 1992. Dependence of hypoxic cellular calcium loading on Na+-Ca2+ exchange. Circ Res 71:547–557.PubMedCrossRefGoogle Scholar
  58. 58.
    Cross HR, Lu L, Steenbergen C, Philipson KD, Murphy E. 1998. Overexpression of the cardiac Na+/Ca2+ exchanger increases susceptibility to ischemia/reperfusion injury in male, but not female, transgenic mice. Circ Res 83:1215–1223.PubMedCrossRefGoogle Scholar
  59. 59.
    Crake T, Poole-Wilson PA. 1990. Calcium exchange in rabbit myocardium during and after hypoxia: role of sodium-calcium exchange. J Mol Cell Cardiol 122:1051–1064.CrossRefGoogle Scholar
  60. 60.
    Haworth RA, Gokner AB. 1992. ATP dependence of calcium uptake by the Na-Ca exchanger of adult heart cells. Circ Res 71:210–217.PubMedCrossRefGoogle Scholar
  61. 61.
    Hilgemann DW 1990. Regulation and deregulation of cardiac Na+-Ca2+ exchange in giant excised sarcolemmal membrane patches. Nature 344:242–245.PubMedCrossRefGoogle Scholar
  62. 62.
    Guarnieri T. 1987. Intracellular sodium-calcium dissociation in early contractile failure in hypoxic ferret papillary muscle. J Physiol 388:449–465.PubMedGoogle Scholar
  63. 63.
    Satoh H, Hayashi H, Katoh H, Terada H, Kobayashi A. 1995. Na+/H+ and Na+/Ca2+ exchange in regulation of [Na+]i and [Ca2+]i during metabolic inhibition. Am J Physiol 268:H1239–H1248.PubMedGoogle Scholar
  64. 64.
    DiPolo R, Beauge L. 1987. Characterization of the reverse Na/Ca exchange in squid axons and its modulation by Cai, and ATP. Cai-dependent Nai/Cao, and Nai/Nao exchange modes. J Gen Physiol 90:505–525.PubMedCrossRefGoogle Scholar
  65. 65.
    He Z, Feng S, Tong Q, Hilgemann DW, Philipson KD. 2000. Interaction of PIP2 with the XIP region of the cardiac Na/Ca exchanger. Am J Physiol 278:C661–C666.Google Scholar
  66. 66.
    Haworth RA, Biggs AV. 1997. Effect of ATP depletion on kinetics of Na/Ca exchange-mediated Ca influx in Na-loaded heart cells. J Mol Cell Cardiol 29:503–514.PubMedCrossRefGoogle Scholar
  67. 67.
    Doering AE, Lederer WJ. 1993. The mechanism by which cytoplasmic protons inhibit the sodium-calcium exchanger in guinea-pig heart cells. J Physiol 466:481–499.PubMedGoogle Scholar
  68. 68.
    Philipson KD, Bersohn MM, Nishimoto AY. 1982. Effects of pH on Na+-Ca2+ exchange in canine cardiac sarcolemmal vesicles. Circ Res 50:287–293.PubMedCrossRefGoogle Scholar
  69. 69.
    Fedida D, Noble D, Rankin AC, Spindler AJ. 1987. The arrhythmogenic transient inward current Iti and related contraction in isolated guinea pig ventricular myocytes. J Physiol 392:523–542.PubMedGoogle Scholar
  70. 70.
    Philipson KD, Ward R. 1985. Effects of fatty acids on Na+-Ca2+ exchange and Ca2+ permeability of cardiac sarcolemmal vesicles. J Biol Chem 260:9666–9671.PubMedGoogle Scholar
  71. 71.
    Goldhaber JI. 1996. Free radicals enhance Na+/Ca2+ exchange in ventricular myocytes. Am J Physiol 271:H823–H833.PubMedGoogle Scholar
  72. 72.
    Dennis SC, Coetzee WA, Cragoe Jr EJ, Opie LH. 1990. Effects of proton buffering and of amiloride derivatives on reperfusion arrhythmias in isolated rat hearts. Circ Res 66:1156–1159.PubMedCrossRefGoogle Scholar
  73. 73.
    Panagiotopoulos S, Daly MJ, Nayler WG. 1990. Effect of acidosis and alkalosis on postischemic Ca gain in isolated rat heart. Am J Physiol 258:H821–H828.PubMedGoogle Scholar
  74. 74.
    Ladilov YV, Siegmund B, Piper HM. 1995. Protection of reoxygenated cardiomyocytes against hypercontracture by inhibition of Na+/H+ exchange. Am J Physiol 268:H1531–H1539.PubMedGoogle Scholar
  75. 75.
    Nakamura T, Hayashi H, Satoh H, Katoh H, Kaneko M, Terada H. 1999. A single cell model of myocardial reperfusion injury: changes in intracellular Na+ and Ca2+ concentrations in guinea pig ventricular myocytes. Mol Cell Biochem 194:147–157.PubMedCrossRefGoogle Scholar
  76. 76.
    Imahashi K, Kusuoka H, Hashimoto K, Yoshioka J, Yamaguchi H, Nishimura T. 1999. Intracellular sodium accumulation during ischemia as the substrate for reperfusion injury. Circ Res 84:1401–1406.PubMedCrossRefGoogle Scholar
  77. 77.
    Ladilov YS, Haffner S, Balser-Schafer C, Maxeiner H, Piper HM. 1999. Cardioprotective effects of KB-R7943: a novel inhibitor of the reverse mode of Na+/Ca2+ exchange. Am J Physiol 276:H1868–H1876.PubMedGoogle Scholar
  78. 78.
    Mukai M, Terada H, Sugiyama S, Satoh H, Hayashi H, Ohno R. 2000. Effects of a selective inhibitor of Na+/Ca2+ exchange, KB-R7943, on reoxygenation-induced injuries in guinea pig papillary muscles. J Cardiovasc Pharmacol 35:121–128.PubMedCrossRefGoogle Scholar
  79. 79.
    Elias CL, Lukas A, Shurraw S, Scott J, Omelchenko A, Gross GJ, Hnatowich M, Harding DP, Hryshko LV. 2001. Inhibition of Na+/Ca2+ exchange by KB-R7943: transport mode selectivity and antiarrhythmic consequences. Am J Physiol 281:H1334–H1345.Google Scholar
  80. 80.
    Bond JM, Chacon E, Herman B, Lemasters J. 1993. Intracellular pH and Ca2+ homeostasis in the pH paradox of reperfusion injury to neonatal rat cardiac myocytes. Am J Physiol 265:C129–C137.PubMedGoogle Scholar
  81. 81.
    Nomura N, Satoh H, Terada H, Matsunaga M, Watanabe H, Hayashi H. 2002. CaMKII-dependent reactivation of SR Ca2+ uptake and contractile recovery during intracellular acidosis. Am J Physiol Heart Circ Physiol 283: H193–H293.PubMedGoogle Scholar
  82. 82.
    Barrington PL, Meier CF Jr, Weglicki WB. 1988. Abnormal electrical activity induced by free radical generating systems in isolated cardiocytes. J Mol Cell Cardiol 20:1163–1178.PubMedCrossRefGoogle Scholar
  83. 83.
    Hayashi H, Miyata H, Watanabe H, Kobayashi A, Yamazaki N. 1989. Effects of hydrogen peroxide on action potentials and intracellular Ca2+ concentration of guinea pig heart. Cardiovasc Res 23:767–773.PubMedCrossRefGoogle Scholar
  84. 84.
    Matsuura H, Shattock MJ. 1991. Effects of oxidant stress on steady-state background currents in isolated ventricular myocytes. Am J Physiol 261:H1358–H1365.PubMedGoogle Scholar
  85. 85.
    Goldhaber JI, Liu E. 1994. Excitation-contraction coupling in single guinea-pig ventricular myocytes exposed to hydrogen peroxide. J Physiol 477.1: 135–147.Google Scholar
  86. 86.
    Boraso A, Williams AJ. 1994. Modification of the gating of the cardiac sarcoplasmic reticulum Ca2+­release channel by H2O2 and dithiothreitol. Am J Physiol 267:H1010–1016.PubMedGoogle Scholar
  87. 87.
    Shattock MJ, Matsuura H. 1993. Measurement of Na+-K+ pump current in isolated rabbit ventricular myocytes using the whole-cell voltage-clamp technique. Inhibition of the pump by oxidant stress. Circ Res 72:91–101.PubMedCrossRefGoogle Scholar
  88. 88.
    Harris EJ, Booth R, Cooper MB. 1982. The effect of superoxide generation on the ability of mitochondria to take up and retain Ca2+. FEBS Lett 146:267–272.PubMedCrossRefGoogle Scholar
  89. 89.
    Langer GA, Frank JS, Philipson KD. 1981. Correlation of alterations in cation exchange and sarcolemmal ultrastructure produced by neuraminidase and phospholipases in cardiac cell tissue culture. Circ Res 49:1289–1299.PubMedCrossRefGoogle Scholar
  90. 90.
    Kusuoka H, Marban E. 1992. Cellular mechanisms of myocardial stunning. Annu Rev Physiol 54:243–256.PubMedCrossRefGoogle Scholar
  91. 91.
    Miller WP, McDonald KS, Moss RL. 1996. Onset of reduced Ca2+ sensitivity of tension during stunning in porcine myocardium. J Mol Cell Cardiol 28:689–697.PubMedCrossRefGoogle Scholar
  92. 92.
    Lemaster JJ. 1999. The mitochondrial permeability transition and the calcium, oxygen and pH paradox: one paradox after another. Cardiovasc Res 44:470–473.CrossRefGoogle Scholar
  93. 93.
    Ruiz-Meana M, Garcia-Dorado D, Hofstaetter B, Piper HM, Soler-Soler J. 1999. Propagation of cardiomyocyte hypercontracture by passage of Na+ through gap junctions. Circ Res 85:280–287.PubMedCrossRefGoogle Scholar
  94. 94.
    Li F, Sugishita K, Su Z, Ueda I, Warry WH. 2001. Activation of connexin-43 hemichannels can elevate [Ca2+]i and [Na+]i in rabbit ventricular myocytes during metabolic inhibition. J Mol Cell Cardiol 33:2145–2155.PubMedCrossRefGoogle Scholar
  95. 95.
    Rupprecht HJ, vom Dahl J, Terres W, Seyfarth KM, Richardt G, Schultheibeta HP, Buerke M, Sheehan FH, Drexler H. 2000. Cardioprotective effects of the Na+/H+ exchange inhibitor cariporide in patients with acute anterior myocardial infarction undergoing direct PTCA. Circulation 101:2902–2908.PubMedCrossRefGoogle Scholar
  96. 96.
    Theroux P, Chaitman BR, Danchin N, Erhardt L, Meinertz T, Schroeder JS, Tognoni G, White HD, Willerson JT, Jessel A. 2000. Inhibition of the sodium-hydrogen exchanger with cariporide to prevent myocardial infarction in high-risk ischemic situations. Main results of the GUARDIAN trial. Guard during ischemia against necrosis (GUARDIAN) investigators. Circulation 102:3032–3038.PubMedCrossRefGoogle Scholar
  97. 97.
    Karmazyn M. 1988. Amiloride enhances postischemic ventricular recovery: possible role of Na+­H+ exchange. Am J Physiol 255:H608–H615.PubMedGoogle Scholar
  98. 98.
    Hendrikx M, Mubagwa K, Verdonck F, Overloop K, Van Hecke P, Vanstapel F, Van Lommel A, Verbeken E, Lauweryns J, Flameng W. 1994. New Na+-H+ exchange inhibitor HOE694 improves postischemic function and high-energy phosphate resynthesis and reduces Ca2+ overload in isolated perfused rabbit heart. Circulation 89:2787–2798.PubMedCrossRefGoogle Scholar
  99. 99.
    Klein HH, Pich S, Bohle RM, Wollenweber J, Nebendahl K. 1995. Myocardial protection by Na+­H+ exchange inhibition in ischemic, reperfused porcine hearts. Circulation 92:912–917.PubMedCrossRefGoogle Scholar
  100. 100.
    Moffat MP, Karmazyn M. 1993. Protective effects of the potent Na/H exchange inhibitor methylisobutyl amiloride against post-ischemic contractile dysfunction in rat and guinea-pig hearts. J Mol Cell Cardiol 25:959–971.PubMedCrossRefGoogle Scholar
  101. 101.
    Maddaford TG, Pierce GN. 1997. Myocardial dysfunction is associated with activation of Na+/H+ exchange immediately during reperfusion. Am J Physiol 273:H2232–H2239.PubMedGoogle Scholar
  102. 102.
    Sweatt JD, Connolly TM, Cragoe EJ, Limbird LE. 1986. Evidence that Na+/H+ exchange regulates receptor-mediated phospholipase A2 activation in human platelets. J Biol Chem 261:8667–8673.PubMedGoogle Scholar
  103. 103.
    Simchovitz L, Cragoe EJ. 1986. Regulation of human neutrophil chemotaxis by intracellular pH. J BioI Chem 261:6492–6500.Google Scholar
  104. 104.
    Watano T, Kimura J. 1998. Calcium-dependent inhibition of the soium-calcium exchange current by KB-R7943. Can J Cardiol 14:259–262.PubMedGoogle Scholar
  105. 105.
    Matsuda T, Arakawa N, Takuma K, Kishida Y, Kawasaki Y, Sakaue M, Takahashi K, Takahashi T, Suzuki T, Ota T, Hamano-Takahashi A, Onishi M, Tanaka Y, Kameo K, Baba A. 2001. SEA0400, a novel and selective inhibitor of the Na+-Ca2+ exchanger, attenuates reperfusion injury in the in vitro and in vivo cerebral ischemic models. J Pharmacol Exp Therap 298:249–256.Google Scholar
  106. 106.
    Echt DS, Liebson PR, Mitchell LB, Peters RW, Obias-Manno D, Barker AH, Arensberg D, Baker A, Friedman L, Greene HL, et al. 1991. Mortality and morbidity in patients receiving encainide, flecainide, or placebo. The Cardiac Arrhythmia Suppression Trial. N Engl J Med 324:781–788.PubMedCrossRefGoogle Scholar
  107. 107.
    Van Emous JG, Nederhoff MG, Ruigrok TJ, van Echteld CJ. 1997. The role of the Na+ channel in the accumulation of intracellular Na+ during myocardial ischemia: consequences for post-ischemic recovery. J Mol Cell Cardiol 29:85–96.PubMedCrossRefGoogle Scholar
  108. 108.
    Hayashi H, Terada H, Katoh H, McDonald TF. 1996. Prevention of reoxygenation-induced arrhythmias in guinea pig papillary muscles. J Cardiovasc Pharmacol 27:816–824.PubMedCrossRefGoogle Scholar
  109. 109.
    Ver Donck L, Borgers M, Verdonck F. 1993. Inhibition of sodium and calcium overload pathology in the myocardium: a new cytoprotective principle. Cardiovasc Res 27:349–357.CrossRefGoogle Scholar
  110. 110.
    Swies J, Omogbai EK, Smith GM. 1990. Occlusion and reperfusion-induced arrhythmias in rats: involvement of platelets and effects of calcium antagonists. J Cardiovasc Pharmacol 15(5):816–825.PubMedCrossRefGoogle Scholar
  111. 111.
    Baxter GF, Yellon DM. 1993. Attenuation of reperfusion-induced ventricular fibrillation in the rat isolated hypertrophied heart by preischemic diltiazem treatment. Cardiovasc Drugs Ther 7:225–231.PubMedCrossRefGoogle Scholar
  112. 112.
    O’Rourke B. 2000. Myocardial KATP channels in preconditioning. Circ Res 87:845–855.PubMedCrossRefGoogle Scholar
  113. 113.
    Holmuhamedov EL, Wang L, Terzic A. 1999. ATP-sensitive K+ channel openers prevent Ca2+ overload in rat cardiac mitochondria. J Physiol 519.2:347–360.PubMedCrossRefGoogle Scholar
  114. 114.
    Grover GJ, Garlid KD. 2000. ATP-sensitive potassium channels: a review of their cardioprotective pharmacology. J Mol Cell Cardiol 32:677–695.PubMedCrossRefGoogle Scholar
  115. 115.
    Sato T, Sasaki N, Seharaseyon J, O’Rourke B, Marban E. 2000. Selective pharmacological agents implicate mitochondrial but not sarcolemmal KATP channels in ischemic cardioprotection. Circulation 101:2418–2423.PubMedCrossRefGoogle Scholar
  116. 116.
    Matsuda N, Kuroda H, Mori T. 1991. Beneficial actions of acidic initial reperfusate in stunned myocardium of rat hearts. Basic Res Cardiol 86:317–326.PubMedCrossRefGoogle Scholar
  117. 117.
    Sugishita K, Su Z, Li F, Philipson KD, Barry WH. 2001. Gender influences [Ca2+]i during metabolic inhibition in myocytes overexpressing the Na+-Ca2+ exchanger. Circulation 104:2101–2106.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2003

Authors and Affiliations

  • Hiroshi Satoh
    • 1
  • Hideki Katoh
    • 1
  • Hajime Terada
    • 1
  • Hideharu Hayashi
    • 1
  1. 1.Division of Cardiology, Internal Medicine IIIHamamatsu University School of MedicineHamamatsuJapan

Personalised recommendations