Skip to main content

Role of apoptosis in myocardial hibernation and myocardial stunning

  • Chapter
Myocardial Viability

Part of the book series: Developments in Cardiovascular Medicine ((DICM,volume 226))

Abstract

Clinicians have long recognized that left ventricular dysfunction in patients with coronary disease is a reversible condition [1,2]. In 1975 Vatner and associates first described post-ischemic myocardial dysfunction in conscious dogs produced by brief coronary occlusions followed by reperfusion [3]. In 1982, Braunwald and Kloner [4] coined the term ‘myocardial stunning’ to describe prolonged but reversible myocardial dysfunction following restoration of myocardial blood flow. In 1985, Rahimtoola observed progressive recovery of chronic left ventricular dysfunction following coronary artery bypass grafting in the absence of transmural necrosis [5]. He described these findings as ‘hibernating myocardium’ reflecting a state of persistently impaired myocardial function at rest due to reduced coronary blood flow that can be partially or completely restored to normal if the net balance between myocardial oxygen supply and demand is favorably altered [6]. The major difference between stunned and hibernating myocardium is the level of myocardial perfusion which is chronically reduced in hibernating myocardium but normal in stunned myocardium. Until recently, the observation of functional recovery was thought to imply that the structural morphology of stunned and hibernating myocardium must be essentially normal. However, increasing evidence from analysis of myocardial biopsy specimens obtained during coronary artery bypass surgery have revealed that stunned and hibernating myocardium are accompanied by several structural changes including apoptotic cell death.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 199.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Rees G, Bristow JD, Kremkau EL et al. Influence of aortocoronary bypass on left ventricular performance. N Engl J Med 1971;284:1116–1120.

    Article  PubMed  CAS  Google Scholar 

  2. Chatterjee K, Swan HJC, Parmley WW, Sustaita H, Marcus HS, Matloff J. Influence of direct direct myocardial revascularization on left ventricular asynergy and function in patients with coronary artery disease: with and without previous myocardial infarction. Circulation 1973;47:276–286.

    Article  PubMed  CAS  Google Scholar 

  3. Heyndrickx GR, Millard RW, McRitchie RJ et al. Regional myocardial function and electrophysiological alterations after brief coronary artery occlusion in conscious dogs. J Clin Invest 1975;56:978–985.

    Article  PubMed  CAS  Google Scholar 

  4. Braunwald E, Kloner RA. The stunned myocardium: prolonged, postischemic ventricular dysfunction. Circulation 1982;66:1146–1149.

    Article  PubMed  CAS  Google Scholar 

  5. Rahimtoola SH. A perspective on the three large multicenter randomized clinical trials of coronary bypass surgery for chronic stable angina. Circulation 1985;72:123–135.

    Article  Google Scholar 

  6. Rahimtoola SH. The hibernating myocardium. Am Heart J 1989;117:211–221.

    Article  PubMed  CAS  Google Scholar 

  7. Wackers FJ, Vogt-Hoerner G. Presence of focal bionecrosis in the epithelium of the acini in the human mammary gland. Ann Anat Pathol 1967;12:21–34.

    CAS  Google Scholar 

  8. Maulik N, Kagan VE, Tyurin VA, Das DK. Redistribution of phosphatidylethanolamine and phosphatidylserine precedes reperfusion-induced apoptosis. Am J Physiol 1998;274:H242–248.

    PubMed  CAS  Google Scholar 

  9. Blankenberg FG, Katsikis PD, Tait JF et al. In vivo detection and imaging of phosphatidylserine expression during programmed cell death. Proc Natl Acad Sci USA 1998;95:6349–6354.

    Article  PubMed  CAS  Google Scholar 

  10. Nagata S. Apoptosis by death factor. Cell 1997;88:355–365.

    Article  PubMed  CAS  Google Scholar 

  11. Liu X, Kim CN, Yang J, Jemmerson R, Wang X. Induction of apoptotic program in cell-free extracts requirements for dATP and Cytochrom C. Cell 1996;86:147–157.

    Article  PubMed  CAS  Google Scholar 

  12. Li P, Nijhawan D, Budihardjo I et al. Cytochrome C and dATP dependent formation of Apaf-1/Caspase 9 complex initiates an apoptotic protease cascade. Cell 1997;91:479–489.

    Article  PubMed  CAS  Google Scholar 

  13. Luo X, Budihardjol I, Zon H, Slaughter C, Wang X. Bid, a Bcl-2 interacting protein, mediates Cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell 1998;94:481–490.

    Article  PubMed  CAS  Google Scholar 

  14. Narula J, Haider N, Virmani et al. Apoptosis in myocytes in end-stage heart failure. N Engl J Med 1996;335:1182–1189.

    Article  PubMed  CAS  Google Scholar 

  15. Olivetti G, Abbi R, Quaini F et al. Apoptosis in the failing human heart. N Engl J Med 1997;336:1131–1141.

    Article  PubMed  CAS  Google Scholar 

  16. Gottlieb RA, Buresldon KO, Kloner RA, Babior BM, Engler RL. Reperfusion injury induces apoptosis in rabbit cardiac myocytes. J Clin Invest 1994;74:86–107.

    Google Scholar 

  17. Kajustura J, Cigola E, Malhotra A et al. Angiotensin II induces apoptosis of adult ventricular myocytes in vitro. J Mol Cell Cardiol 1997;29:859–870.

    Article  Google Scholar 

  18. Liu Y, Cigola E, Cheng W et al. Myocyte nuclear mitotic division and programmed myocyte cell death characterize the cardiac myopathy induced rapid ventricular pacing in dogs. Lab Invest 1995;73:771–787.

    PubMed  CAS  Google Scholar 

  19. Cheng W, Li B, Kajstura J et al. Stretch-induced programmed myocyte cell death. J Clin Invest 1995;96:2247–2259.

    Article  PubMed  CAS  Google Scholar 

  20. Teiger E, Than VD, Richard L, et al. Apoptosis in pressure overload induced heart hypertrophy in the rat. J Clin Invest 1996;97:2891–2897.

    Article  PubMed  CAS  Google Scholar 

  21. Hamet R, Richard L, Dam TV et al. Apoptosis in target organs of hypertension. Hypertension 1995;26:642–648.

    Article  PubMed  CAS  Google Scholar 

  22. Kajustura J, Cheng W, Reiss K et al. Apoptotic and necrotic myocyte cell deaths are independent contributing variables of infarct size in rats. Lab Invest 1996;74:86–107.

    Google Scholar 

  23. Fliss H, Gattinger D. Apoptosis in ischemic and reperfused rat myocardium. Circ Res 1996;79:949–956.

    Article  PubMed  CAS  Google Scholar 

  24. Bialik S, Geenen DL, Sasson IE et al. Myocardial apoptosis during acute myocardial infarction in the mouse localizes to hypoxic regions but occurs independently of p53. J Clin Invest 1997;100:1363–1372.

    Article  PubMed  CAS  Google Scholar 

  25. Yaoita H, Ogawa K, Maehara K, Maruyama Y. Attenuation of ischemia/perfusion injury in rats by a caspase inhibitor. Circulation 1998;97:276–281.

    Article  PubMed  CAS  Google Scholar 

  26. Saraste A, Pulkki K, Kallajoki M, Henriksen K, Parvinen M, Voipio-Pukki LM. Apoptosis in human myocardial infarction. Circulation 1997;95:320–323.

    Article  PubMed  CAS  Google Scholar 

  27. Kharbanda S, Arbustini E, Kolodgie FD et al. Release of cytochrome c from mitochondria, activation of caspases and apoptosis in explanted cardiomyopathic hearts from cardiac allograft recipients [abstract]. Circulation 1997;96(8 Suppl):I-l 15–16.

    Google Scholar 

  28. Kloner RA, Pryzklenk K, Whittacker P. Deleterious effects of oxygen radicals in oxygen/reperfusion: resolved and unresolved issues. Circulation 1989;80:1115–1127.

    Article  PubMed  CAS  Google Scholar 

  29. Entman ML, Smith CW. Post-reperfusion inflammation: a model for reaction to injury in cardiovascular disease. Cardiovasc Res 1994;28:1301–1311.

    Article  PubMed  CAS  Google Scholar 

  30. Jeroudi MO, Hartely CJ, Bolli R. Myocardial perfusion injury: role of oxygen radicals and potential therapy with antioxidants. Am J Cardiol 1994;73:2B–7B.

    Article  PubMed  CAS  Google Scholar 

  31. Urabe K, Miura TM, Iwamoto TI et al. Pre-conditioning enhances myocardial resistance to post-ischemic myocardial stunning via adenosine receptor activation. Cardiovasc Res 1993;27:657–662.

    Article  PubMed  CAS  Google Scholar 

  32. Cohen MV, Liu GS, Downey JM. Preconditioning causes improved wall motion as well as smaller infarcts after transient coronary occlusion in rabbits. Circulation 1991;84:341–349.

    Article  PubMed  CAS  Google Scholar 

  33. Piot CA, Padmanabhan D, Ursell PC, Sievers RE, Wolfe CL. Ischemic preconditioning decreases apotosis in rat hearts in vivo. Circulation 1997;96:1598–1604.

    Article  PubMed  CAS  Google Scholar 

  34. Mizukami Y, Yoshioka K, Morimoto S, Yoshida K. A novel mechanism of JNK activation: nuclear translocation and activation of JNK1 during ischemia and reperfusion. J Biol Chem 1997;272:16657–16662.

    Article  PubMed  CAS  Google Scholar 

  35. Nayler WG. Calcium, calcium antagonists, stunning and hibernation: on overview. In: Opie LH, editor. Stunning, hibernation and calcium in myocardial ischemia and reperfusion. Boston: Springer Science+Business Media Dordrecht, 1992. p. 226–234.

    Chapter  Google Scholar 

  36. Ausma J, Cleutjens J, Thone F, Falmeng W, Raemaekers W, Borgers M. Chronic hibernating myocardium: interstitial changes. Mol Cell Biochem 1995;147:35–42.

    Article  PubMed  CAS  Google Scholar 

  37. Vanoverschelde JL, Depre C, Wijns M, Bol A, Dion R, Gerber B, Borgers M, Melin J. Physiopathologie de l’hibernation chronique: apports de la tomographic par emissions positrons. Med Sci 1995;11:1315–1322.

    Google Scholar 

  38. Borgers M, Thone F, Wouters L, Ausma J, Shivalkar B, Flameng W. Structural correlates of regional myocardial dysfunction in patients with critical coronary artery stenosis: chronic hibernation? Cardiovasc Pathol 1993;2:237–245.

    Article  Google Scholar 

  39. Schwarz ER, Schaper J, vom Dahl J, et al. Myocyte degeneration and cell death in hibernating human myocardium. J Am Coll Cardiol 1996;26:1577–1585.

    Article  Google Scholar 

  40. Shivalkar B, Maes A, Borgers M et al. Only hibernating myocardium invariably shows early recovery after coronary revascularization. Circulation 1996;94:308–315.

    Article  PubMed  CAS  Google Scholar 

  41. Vanoverscheide JL, Wijns W, Depre C et al. Mechanism of chronic regional postischemic dysfunction in humans: new insights from the study of noninfarcted collateral-depednent myocardium. Circulation 1993;87:1513–1523.

    Article  Google Scholar 

  42. Ausma J, Schaart G, Thone F et al. Chronic ischemic viable myocardium in man: aspects of dedifferentiation. Cardiovasc Pathol 1995;4:29–37.

    Article  Google Scholar 

  43. Elässer A, Schlepper M, Klovekorn WP et al. C, Munkel B, Schaper W, Schaper J. Hibernating myocardium: an incomplete adaptation to ischemia. Circulation 1997;96:1931–2920.

    Google Scholar 

  44. Schwarz ER, Schoendube FA, Kostin S, et al. Prolonged myocardial hibernation exacerbates cardiomyocyte degeneration and impairs recovery of function after revascularization. J Am Coll Cardiol 1998;31:1018–1026.

    Article  PubMed  CAS  Google Scholar 

  45. Chen C, Lijie MA, Linfert DR et al. Myocardial cell death and apoptosis in hibernating myocardium. J Am Coll Cardiol 1997;30:1407–1412.

    Article  PubMed  CAS  Google Scholar 

  46. Jennings RB, Somers HM, Herson PB, Kaltenbach JP. Ischemic injury of myocardium. Ann NY Acad Sci 1969;156:61–78.

    Article  PubMed  CAS  Google Scholar 

  47. Schaper J, Mulch J, Winkler B, Schaper W. Ultrastructural, functional, and biochemical criteria for estimation of reversiblity of ischemic injury: a study on the effects of global ischemia on the isolated dog heart. J Mol Cell Cardiol 1979;11:521–541.

    Article  PubMed  CAS  Google Scholar 

  48. Webster KA, Discher DJ, Bishoporic NH. Regulation of fos and jun immediate-early genes by redox or metabolic stress in cardiac myocytes. Circ Res 1994;74:679–686.

    Article  PubMed  CAS  Google Scholar 

  49. Pierzchalski P, Reiss K, Cheng W et al. p53 induces myocyte apoptosis via the activation of the renin-angiotensin system. Exp Cell Res 1997;234:57–65.

    Article  PubMed  CAS  Google Scholar 

  50. Kajustura J, Liu Y, Baldini A et al. Coronary artery constriction in rats: necrotic and apoptotic myocyte death. Am J Cardiol 1998;82:30K–41K.

    Article  Google Scholar 

  51. Yamada T, Horiuchi M, Dzau VJ. Angiotension II type 2 receptor mediates programmed cell death. Proc Natl Acad Sci USA 1996;93:156–160.

    Article  PubMed  CAS  Google Scholar 

  52. Horiuchi M, Yamada T, Hayashida W, Dzau VJ. Interferon regulatory factor-1 up-regulates angiotensin II type 2 receptor and induces apoptosis. J Biol Chem 1997;272:11952–11958.

    Article  PubMed  CAS  Google Scholar 

  53. Li Z, Bing OH, Long X, Robinson KG, Lakatta EG. Increased cardiomyocyte apoptosis during transition to heart failure in the spontaneously hypertensive rat. Am J Physiol 1997;272:H2313–2319.

    PubMed  CAS  Google Scholar 

  54. Goussev A, Sharov VG, Shimoyama H et al. Effects of ACE inhibition on cardiomyocyte apoptosis in dogs with heart failure. Am J Physiol 1998;275:H626–631.

    PubMed  CAS  Google Scholar 

  55. Sheng Z, Knowlton K, Chen J, Hoshijima M, Brown JH, Chien KR. Cardiotrophin 1 (CT-1) inhibition of cardiac myocyte apoptosis via a mitogen-activated protein kinase-dependent pathway. Divergence from downstream CT-1 signals for myocardial cell hypertrophy. J Biol Chem 1997;272:5783–5791.

    Article  PubMed  CAS  Google Scholar 

  56. Stephenou A, Brar B, Heads R et al. Cardiotrophin-1 induces heat shock protein accumulation in cultured cardiac cells and protects from stressful stimuli. J Mol Cell Cardiol 1998;30:849–855.

    Article  Google Scholar 

  57. Sawyer DB, Baliga RR, Schneider J, Marchionni, MA, Kelly RA, Smith TW. Neuregulin stimulates ErB4 receptor phosphorylation in neonatal rat ventricular myocytes [abstract]. Circulation 1996;94(8 Suppl):I-644.

    Google Scholar 

  58. Zhao YY, Sawyer DR, Baliga RR et al. Neuregulins promote survival and growth of cardiac myocytes: persistence of ErbB2/ErbB4 expression in neonatal and adult ventricular myocytes. J Biol Chem 1998;273:10261–10269.

    Article  PubMed  CAS  Google Scholar 

  59. Baliga RR, Simmons WW, Sawyer DB et al. The Role of MEK-MAPK-RSK pathway, PI3 kinase pathway, and p70S6K in neuregulin induced growth of cardiac myocytes [abstract]. Circulation 1997;96(8 Suppl):I-362.

    Google Scholar 

  60. Sadoshima J, Qiu Z, Morgan JP, Izumo S. Angiotensin II and other hypertrophic stimuli mediated by G protein-coupled receptors activate tyrosine kinase, mitogen-activated protein kinase, and 90-kD S6 kinase in cyardiac myocyte. The critical role of CA(2+)-dependent signaling. Circ Res 1995;76:1–5.

    Article  PubMed  CAS  Google Scholar 

  61. Krown KA, Page MT, Nguyen C et al. Tumour necrosis factor α-induced apoptosis in cardiac myocytes. Involvement of the sphingolipid signaling cascade in cardiac cell death. J Clin Invest 1996;98:2854–2865.

    Article  PubMed  CAS  Google Scholar 

  62. Yue TL, Ma XL, Wang X et al. Possible involvement of stress activated protein kinase signaling patwhay and Fas receptor expression in prevention of ischemia/reperfusion induced cardiomyocyte apoptosis by Carvedilol. Circ Res 1998;82:166–174.

    Article  PubMed  CAS  Google Scholar 

  63. Radford NB, Fina M, Benjamin IJ et al. Cardioprotective effects of 70-kDa heat shock protein in transgenic mice. Proc Natl Acad Sci USA 1996;93:2339–2342.

    Article  PubMed  CAS  Google Scholar 

  64. Hutter JJ, Mestril R, Tarn EK, Sievers RE, Dillmann WH, Wolfe CL. Overexpression of heat shock protein 72 in transgenic mice decreases infarct size in vivo. Circulation 1996;94:1408–1411.

    Article  PubMed  CAS  Google Scholar 

  65. Williams RS. Heat shock proteins and ischemic injury to the myocardium. Circulation 1997;96:4138–4140.

    Article  PubMed  CAS  Google Scholar 

  66. Benjamin IJ, McMillan DR. Stress (heat shock) proteins: molecular chaperones in cardiovascular biology and disease. Circ Res 1998;83:117–132.

    Article  PubMed  CAS  Google Scholar 

  67. Plumier JC, Rossie BM, Currie TW, Angelidis CE, Kazlaris H, Kollias G, Pagoulatos GN. Transgenic mice expressing the human heat shock protein 70 have improved post-ischemic myocardial recovery. J Clin Invest 1995;95:1854–1860.

    Article  PubMed  CAS  Google Scholar 

  68. Marber MS, Mestril R, Chi SH, Sayen MR, Yellon DM, Dillmann WH. Overexpression of the rat inducible 70-kD heat stress protein in a transgenic mouse increases the resistance of the heart to ischemic injury. J Clin Invest 1995;95:1446–1456.

    Article  PubMed  CAS  Google Scholar 

  69. Ferrari R, Bongrazio M, Cargnoni A et al. Heat shock protein changes in hibernation: a similarity with heart failure. J Mol Cell Cardiol 1996;28:2383–2395.

    Article  PubMed  CAS  Google Scholar 

  70. Demeester S, Buchman T, Qiu Y et al. Heat shock induces Iκß and prevents stress-induced endothelial cell apoptosis. Arch Surg 1997;132:1283–1287.

    Article  PubMed  CAS  Google Scholar 

  71. Garcia-Bermejo L. Vilaboa N, Perez C, Galan A, De Blas E, Aller P. Modulation of heat-shock protein 70 (HSP 70) gene expression by sodium butyrate in U-937 promonocytic cells: relationships with differentiation and apoptosis. Exp Cell Res 1997;236:268–274.

    Article  PubMed  CAS  Google Scholar 

  72. Mosser D, Caron A, Bourget L, Denis-Larose C, Massie B. Role of the human heat shock protein hsp70 in protection against stress-induced apoptosis. Mol Cell Biol 1997;17:5317–5327.

    PubMed  CAS  Google Scholar 

  73. Dix DJ, Allen JW, Collins BW et al. Targeted gene disruption of Hsp70-2 results in failied meiosis, germ cell apoptosis and male fertility. Proc Natl Acad Sci USA 1996;93:3264–3268.

    Article  PubMed  CAS  Google Scholar 

  74. Gabai V, Merin A, Mosser D et al. Hsp 70 prevents activation of stress kinases. J Biol Chem 1997;272:18033–18037.

    Article  PubMed  CAS  Google Scholar 

  75. Mehlen P, Schulze-Osthoff K, Arrigo AP. Small stress proteins as novel regulators of apoptosis: heat shock protein 27 blocks Fas/APO-1 and staurosporine-induced cell death. J Biol Chem 1996;271:16510–16514.

    Article  PubMed  CAS  Google Scholar 

  76. Mehlen P, Mehlen A, Godet J, Arrigo AP. Hsp27 as a switch between differentiation and apoptosis in murine embryonic cells. J Biol Chem 1997;272:31657–31665.

    Article  PubMed  CAS  Google Scholar 

  77. Radi R, Beckman JS, Bush KM, Freeman BA. Peroxynitrate oxidation of sulfhydryls. The cytotoxic potential of superoxide and nitrixc oxide. J Biol Chem 1991;266:4244–4250.

    PubMed  CAS  Google Scholar 

  78. Ischiropoulos H, Zhu L, Chen J et al. Peroxynitrate-mediated tyrosine nitration catalyzed by superoxide dismutase. Arch Biochem Biophys 1992;298:431–437.

    Article  PubMed  CAS  Google Scholar 

  79. Mannick JB, Miao XQ, Stamler JS. Nitric oxide inhibits Fas-induced apoptosis. J Biol Chem 1997;272:24125–24128.

    Article  PubMed  CAS  Google Scholar 

  80. Dennis SC, Gevers W, Opie LH. Protons in ischemia: where do they come from; where do they go? J Mol Cell Cardiol 1991;23:1077–1086.

    Article  PubMed  CAS  Google Scholar 

  81. Gottlieb RA, Giesing HA, Zhu JY, Engler RL, Babior BM. Cell acidification in apoptosis: granulocyte colony-stimulating factor delays programmed cell death in neutrophils by up-regulating the vaculor hydrogen-ATPase. Proc Natl Acad Sci USA 1995;92:5965–5968.

    Article  PubMed  CAS  Google Scholar 

  82. Lagadic-Gossmann D, Buckler KJ, Vaughan-Jones RD. Role of bicarbonate in pH recovery from intracellular acidosis in guinea-pig ventricular myocyte. J Physiol (Lond) 1992;458:361–384.

    CAS  Google Scholar 

  83. Vaughan-Jones RD. An investigation of chloride-bicarbonate exchanger in the sheep cardiac Purkinje fibres. J Physiol (Lond) 1986;379:377.

    CAS  Google Scholar 

  84. Gottlieb RA, Gruol DL, Zhu JY, Engler RL. Preconditioning in rabbit cardiomyocytes: role of pH, vacuolar proton ATPase and apoptosis. J Clin Invest 1996;97:2391–2398.

    Article  PubMed  CAS  Google Scholar 

  85. Karwatowksa-Prokopczuk E, Nordberg JA, Li H-L, Engler RL, Gottlieb RA. Effect of vaculolar proton ATPase on pHi, calcium and apotosis in neonatal cardiomyocytes during metabolic inhibition/recovery. Circ Res 1998;82:1139–1144.

    Article  Google Scholar 

  86. Gerber B, Melin JA, Bol A, Vanoverschelde JL. Attenuated response of myocardial glucose utilization to insulin stimulation in hibernating myocardium [abstract]. Circulation 1995;92(8 suppl):I-313.

    Google Scholar 

  87. Maki M, Luotoolahti M, Nuutila P et al. Glucose uptake in the chronically dysfunctional but viable myocardium. Circulation 1996;93:1658–1666.

    Article  PubMed  CAS  Google Scholar 

  88. Marinho NVS, Keogh BE, Costa DC et al. Pathophysiology of chronic left ventricular dysfunction: new insights from the measurement of absolute myocardial blood flow and glucose utilization. Circulation 1996;93:737–744.

    Article  PubMed  CAS  Google Scholar 

  89. Maddaford TG, Russell JC, Pierce GN. Postischemic cardiac performance in the insulin resistant JCRLLA-cp rat. Am J Physiol 1997;273:H1187–1192.

    PubMed  CAS  Google Scholar 

  90. Schultz R, Rose J, Martin C Brodde OE, Heusch G. Development of short-term myocardial hibernation: its limitation by the severity of ischemia and inotropic stimulation. Circulation 1993;88:684–695.

    Article  Google Scholar 

  91. Baliga R, Lammertsma A, Rhodes CJ, Aitman TJ, Scott J, Kooner JS. Positron emission tomography localises insulin resistance to skel et al muscle in premature coronary heart disease [abstract]. Circulation 1995;92(8 Suppl);I16–17.

    Google Scholar 

  92. Paternostoro G, Camici PG, Lammertsmaa A et al. Cardiac and skel et al muscle insulin resistance in patients with coronary artery disease. A study with positron emission tomography. J Clin Invest 1996;98:2094–2099.

    Article  Google Scholar 

  93. Gao WD, Atar D, Liu Y, Perez NG, Murphy AM, Marban E. Role of troponin I in the pathogenesis of stunned myocardium. Circ Res 1997;80:393–399.

    PubMed  CAS  Google Scholar 

  94. Zhao M, Zhang H, Robinson TF, Factor SM, Sonnenblick EH, Eng C. Profound structural alterations of the extracellular collagen matrix in postischemic dysfunctional (’stunned’) but viable myocardium. J Am Coll Cardiol 1987;10:1322–1334.

    Article  PubMed  CAS  Google Scholar 

  95. Charney RH, Takahashi S, Zhao M, Sonnenblick EH, Eng C. Collagen loss in the stunned myocardium. Circulation 1992;85:1483–1490.

    Article  PubMed  CAS  Google Scholar 

  96. Borg T, Johnson LD, Lill PH. Specific attachment of collagen to cardiac myocytes: in-vivo and in-vitro. Dev Biol 1983;97:417–423.

    Article  PubMed  CAS  Google Scholar 

  97. Hynes RO. Integrins: a family of cell surface receptors. Cell 1987;48:549–554.

    Article  PubMed  CAS  Google Scholar 

  98. Terrado L, Rubin K, Gullberg D et al. Expression of collagen binding integrins during cardiac development and hypertrophy. Circ Res 1991;68:734–744.

    Article  Google Scholar 

  99. Ross RS, Pham C, Shai S-Y et al. ßl integrins participate in the hypertrophic response of rat ventricular myocytes. Circ Res 1998;82:1160–1172.

    Article  PubMed  CAS  Google Scholar 

  100. Baliga RR, Brooks WW, Bing OH, Singh K, Colucci WS. Beta-1 integrins in cardiac hypertrophy and failure. Accepted for the 72nd annual scientific sessions of the American Heart Association, Dallas, Nov, 1999. Circulation. In press 1999.

    Google Scholar 

  101. Zhao M, Sonneblick EH, Zhang H, Eng C. Increase in myofilament separation in the’ stunned’ myocardium. J Mol Cell Cardiol 1992;24:269–276.

    Article  PubMed  CAS  Google Scholar 

  102. Robinson BL, Morito T, Toft DO, Morris JJ. Accelerated recovery of postischemic stunned myocardium after induced expression of myocardial heat-shock protein (Hsp 70). J Thorac Cardiovasc Surg 1995;109:753–764.

    Article  PubMed  CAS  Google Scholar 

  103. Zhao M, Forman R, Sonnenblick EH et al. Sarcomere mis-registration in the stunned myocardium: evidence for intracellular slippage [abstract]. Circulation 1989;80(4 Suppl):II513.

    Google Scholar 

  104. Zhao M, Sonnenblick EH, Zhang H, Factor SM, Eng C. Cytoskel et al alterations in the stunned myocardium [abstract]. FASEB J 1992;6:A1245.

    Google Scholar 

  105. Caceres-Cortes J, Rajotte D, Dumouchel J, Haddad P, Hoang T. Product of the Steel locus suppresses apotosis in hemopoietic cells: comparison with pathways activated by granulocyte macrophage colony-stimulating factor. J Biol Chem 1994;269:12084–12091.

    PubMed  CAS  Google Scholar 

  106. Kida M, Fujiwara H, Ishida M et al. Ischemic preconditioning preserves creatine phosphate and intracellular pH. Circulation 1991;84:2495–2503.

    Article  PubMed  CAS  Google Scholar 

  107. Wolfe CL, Sievers RE, Visseren FL, Donnelly TJ. Loss of myocardial protection after preconditioning correlates with the time course of glycogen recovery within the preconditioned segment. Circulation 1993;87:881–892.

    Article  PubMed  CAS  Google Scholar 

  108. de Albuquerque CP, Gerstenblith G, Weiss RG. Importance of metabolic inhibition and cellular pH in mediating preconditioning contractile and metabolic effects in rat hearts. Circ Res 1994;74:139–150.

    Article  PubMed  Google Scholar 

  109. Schaefer S, Carr LJ, Prussel E, Ramasamy R. Effects of glycogen depletion on ischemic injury in isolated rat hearts: insights into preconditioning. Am J Physiol 1995;268:H935–944.

    PubMed  CAS  Google Scholar 

  110. Yamanaka O, Yasumasa F, Nakamura T et al. Myocardial stunning like phenomenon during a crisis of phechromocytoma. Jpn Circ J 1994;58:737–742.

    Article  PubMed  CAS  Google Scholar 

  111. Quigg RJ, Om A. Reversal of severe cardiac systolic dyfunction caused by pheochromocytoma in a heart transplant candidate. J Heart Lung Transplant 1994;13:525–532.

    PubMed  CAS  Google Scholar 

  112. Communal C, Singh K, Pimentel DR, Colucci WS. Norepinephrine stimulates apoptosis in adult rat ventriclar myocytes by activation of the ß-adrenergic pathway. Circulation 1998;98:1329–1334.

    Article  PubMed  CAS  Google Scholar 

  113. Lagadic-Gossmann D, Le Prigent K, Feuvray D. Effects of trimetazidine on intracellular pH regulation in the rat isolated ventricular myocyte. Br J Pharmacol 1996;117:831–838.

    Article  PubMed  CAS  Google Scholar 

  114. Thornberry NA. Caspases: Key mediators of apoptosis. Chem Biol 1998;5:R97–103.

    Article  PubMed  CAS  Google Scholar 

  115. Bolli R. Mechanism of myocardial stunning. Circulation 1990;82:723–738.

    Article  PubMed  CAS  Google Scholar 

  116. Olivetti G, Quaini F, Sala R et al. Acute myocardial infarction in humans is associated with activation of programmed myocyte cell death in the surviving portion of the heart. J Mol Cell Cardiol 1996;28:2005–2016.

    Article  PubMed  CAS  Google Scholar 

  117. Kerr JFR, Wyllie AH, Currie AR. Apoptosis: a basic biologic phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 1972;26:239–257.

    Article  PubMed  CAS  Google Scholar 

Download references

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2000 Springer Science+Business Media Dordrecht

About this chapter

Cite this chapter

Baliga, R.R., Schaper, J., Narula, J. (2000). Role of apoptosis in myocardial hibernation and myocardial stunning. In: Iskandrian, A.E., Van Der Wall, E.E. (eds) Myocardial Viability. Developments in Cardiovascular Medicine, vol 226. Springer, Dordrecht. https://doi.org/10.1007/978-94-011-4080-5_2

Download citation

  • DOI: https://doi.org/10.1007/978-94-011-4080-5_2

  • Publisher Name: Springer, Dordrecht

  • Print ISBN: 978-94-010-5793-6

  • Online ISBN: 978-94-011-4080-5

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics