American Journal of Cardiology
Volume 103, Issue 9 , Pages 1261-1268 , 1 May 2009

Effects of Left Ventricular Volume Overload on Mitochondrial and Death-Receptor–Mediated Apoptotic Pathways in the Transition to Heart Failure

  • Narain Moorjani, MD, FRCS (C-Th)

      Affiliations

    • Department of Cardiothoracic Surgery, Oxford Heart Centre, John Radcliffe Hospital, Oxford, United Kingdom
    • National Heart and Lung Institute Division, Faculty of Medicine, Imperial College, London, United Kingdom
    • Corresponding Author InformationCorresponding author: Tel: 44-0-1865-220269; fax: 44-0-1865-220268
    • ,
  • Stephen Westaby, PhD, FRCS

      Affiliations

    • Department of Cardiothoracic Surgery, Oxford Heart Centre, John Radcliffe Hospital, Oxford, United Kingdom
    • ,
  • Jagat Narula, MD, PhD

      Affiliations

    • School of Medicine, University of California, Irvine, California
    • ,
  • Pedro A. Catarino, FRCS

      Affiliations

    • Department of Cardiothoracic Surgery, Oxford Heart Centre, John Radcliffe Hospital, Oxford, United Kingdom
    • ,
  • Robin Brittin, MSc

      Affiliations

    • Department of Pathology and Laboratory Medicine, Hospital of the University of Pennsylvania, Philadelphia, Pennsylvania
    • ,
  • Tim J. Kemp, PhD

      Affiliations

    • National Heart and Lung Institute Division, Faculty of Medicine, Imperial College, London, United Kingdom
    • ,
  • Navneet Narula, MD

      Affiliations

    • Department of Pathology and Laboratory Medicine, Hospital of the University of Pennsylvania, Philadelphia, Pennsylvania
    • ,
  • Peter H. Sugden, PhD

      Affiliations

    • National Heart and Lung Institute Division, Faculty of Medicine, Imperial College, London, United Kingdom

Received 5 November 2008 ,Revised 13 January 2009 ,Accepted 13 January 2009.

References 

  1. Narula J, Haider N, Virmani R, DiSalvo T, Kolodgie FD, Hajjar RJ, et al. Apoptosis in cardiomyocytes in end-stage heart failure. N Engl J Med. 1996;335:1182–1189
  2. Kemp TJ, Sadusky TJ, Saltisi F, Carey N, Moss J, Yang SY, et al. Identification of Ankrd2, a novel skeletal muscle gene coding for a stretch-responsive ankyrin-repeat protein. Genomics. 2000;66:229–241
  3. Clerk A, Kemp TJ, Harrison JG, Mullen AJ, Barton PJ, Sugden PH. Up-regulation of c-jun mRNA in cardiac myocytes requires the extracellular signal-regulated kinase cascade, but c-Jun N-terminal kinases are required for efficient up-regulation of c-Jun protein. Biochem J. 2002;368:101–110
  4. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976;72:248–254
  5. Dimmeler S, Haendeler J, Nehls M, Zeiher AM. Suppression of apoptosis by nitric oxide via inhibition of interleukin-1beta–converting enzyme (ICE)-like and cysteine protease protein (CPP)-32–like proteases. J Exp Med. 1997;185:601–607
  6. Ohno M, Takemura G, Ohno A, Misao J, Hayakawa Y, Minatoguchi S, et al. “Apoptotic” myocytes in infarct area in rabbit hearts may be oncotic myocytes with DNA fragmentation: analysis by immunogold electron microscopy combined with in situ nick end-labeling. Circulation. 1998;98:1422–1430
  7. Kockx MM, Muhring J, Knaapen MW, de Meyer GR. RNA synthesis and splicing interferes with DNA in situ end labeling techniques used to detect apoptosis. Am J Pathol. 1998;152:885–888
  8. Kanoh M, Takemura G, Misao J, Hayakawa Y, Aoyama T, Nishigaki K, et al. Significance of myocytes with positive DNA in situ nick end-labelling (TUNEL) in hearts with dilated cardiomyopathy: not apoptosis but DNA repair. Circulation. 1999;99:2757–2764
  9. Narula J, Haider N, Arbustini E, Chandrashekhar Y. Mechanisms of disease: apoptosis in heart failure—seeing hope in death. Nat Cardiovasc Med Clin Pract. 2006;3:681–688
  10. Chipuk JE, Kuwana T, Bouchier-Hayes L, Droin NM, Newmeyer DD, Schuler M, et al. Direct activation of Bax by p53 mediates mitochondrial membrane permeabilization and apoptosis. Science. 2004;303:1010–1014
  11. Di Napoli P, Taccardi AA, Grilli A, Felaco M, Balbone A, Angelucci D, et al. Left ventricular wall stress as a direct correlate of cardiomyocyte apoptosis in patients with severe dilated cardiomyopathy. Am Heart J. 2003;146:1105–1111
  12. Latif N, Khan MA, Birks E, O'Farrell A, Westbrook J, Dunn MJ, et al. Upregulation of the Bcl-2 family of proteins in end stage heart failure. J Am Coll Cardiol. 2000;35:1769–1777
  13. Akyürek O, Akyürek N, Sayin T, Dincer I, Berkalp B, Akyol G, et al. Association between the severity of heart failure and the susceptibility of myocytes to apoptosis in patients with idiopathic dilated cardiomyopathy. Int J Cardiol. 2001;80:29–36
  14. Narula N, Narula J, Zhang PJ, Haider N, Raghunath PN, Brittin R, et al. Is the myofibrillarlytic myocyte a forme fruste apoptotic myocyte?. Ann Thorac Surg. 2005;79:1333–1337
  15. Mihara M, Erster S, Zaika A, Petrenko O, Chittenden T, Pancoska P, et al. P53 has a direct apoptogenic role at the mitochondria. Mol Cell. 2003;11:577–590
  16. McCarthy N, Mercer J, Bennett M. Apoptotic proteins (P53 and c-myc related pathways). Cardiol Clin. 2001;19:75–89
  17. Birks EJ, Latif N, Enesa K, Folkvang T, Luong LA, Sarathchandra P, et al. Elevated p53 expression is associated with dysregulation of the ubiquitin-proteasome system in dilated cardiomyopathy. Cardiovasc Res. 2008;79:472–480
  18. Leri A, Claudio PP, Li Q, Wang X, Reiss K, Wang S, et al. Stretch-mediated release of angiotensin II induces myocyte apoptosis by activating p53 that enhances the local renin-angiotensin system and decreases the Bcl-2-to-Bax protein ratio in the cell. J Clin Invest. 1998;101:1326–1342
  19. Kim R. Unknotting the roles of Bcl-2 and Bcl-xL in cell death. Biochem Biophys Res Commun. 2005;333:336–343
  20. Baines CP, Kaiser RA, Purcell NH, Blair NS, Osinska H, Hambleton MA, et al. Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature. 2005;434:658–662
  21. Thorburn A. Death receptor-induced cell killing. Cell Signal. 2004;16:139–144
  22. Philipp S, Pagel I, Höhnel K, Lutz J, Buttgereit J, Langenickel T, et al. Regulation of caspase 3 and Fas in pressure overload-induced left ventricular dysfunction. Eur J Heart Fail. 2004;6:845–851
  23. Cheng W, Li B, Kajstura J, Li P, Wolin MS, Sonnenblick EH, et al. Stretch-induced programmed myocyte cell death. J Clin Invest. 1995;96:2247–2259
  24. Wollert KC, Heineke J, Westermann J, Lüdde M, Fiedler B, Zierhut W, et al. The cardiac Fas (APO-1/CD95) Receptor/Fas ligand system: relation to diastolic wall stress in volume-overload hypertrophy in vivo and activation of the transcription factor AP-1 in cardiac myocytes. Circulation. 2000;101:1172–1178
  25. Scheubel RJ, Bartling B, Simm A, Silber RE, Drogaris K, Darmer D, et al. Apoptotic pathway activation from mitochondria and death receptors without caspase-3 cleavage in failing human myocardium: fragile balance of myocyte survival?. J Am Coll Cardiol. 2002;39:481–488
  26. Narula J, Arbustini E, Chandrashekhar Y, Schwaiger M. Apoptosis and the systolic dysfunction in congestive heart failure (Story of apoptosis interruptus and zombie myocytes). Cardiol Clin. 2001;19:113–126
  27. Haider N, Narula N, Narula J. Apoptosis in heart failure represents programmed cell survival, not death, of cardiomyocytes and likelihood of reverse remodeling. J Card Fail. 2002;8(suppl):S512–S517
  28. Communal C, Sumandea M, de Tombe P, Narula J, Solaro RJ, Hajjar RJ. Functional consequences of caspase activation in cardiac myocytes. Proc Natl Acad Sci U S A. 2002;99:6252–6256
  29. Moretti A, Weig HJ, Ott T, Seyfarth M, Holthoff HP, Grewe D, et al. Essential myosin light chain as a target for caspase-3 in failing myocardium. Proc Natl Acad Sci USA. 2002;99:11860–11865

 Dr. Moorjani was supported by a Junior Research Fellowship from the British Heart Foundation.

PII: S0002-9149(09)00105-2

doi: 10.1016/j.amjcard.2009.01.013

American Journal of Cardiology
Volume 103, Issue 9 , Pages 1261-1268 , 1 May 2009

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