Journal of Molecular and Cellular Cardiology
Volume 46, Issue 3 , Pages 420-430 , March 2009

Increased expression and intramitochondrial translocation of cyclophilin-D associates with increased vulnerability of the permeability transition pore to stress-induced opening during compensated ventricular hypertrophy

  • Jimmy Matas

      Affiliations

    • Département de kinésiologie, Université de Montréal, C.P. 6128, Succursale Centre-Ville, Montréal, Québec, Canada H3C 3J7
  • ,
  • Nicholas Tien Sing Young

      Affiliations

    • Experimental Cardiovascular Biology Research Unit, Institut de recherches cliniques de Montréal, Montreal, Quebec, Canada H2W 1R7
  • ,
  • Céline Bourcier-Lucas

      Affiliations

    • Département de kinésiologie, Université de Montréal, C.P. 6128, Succursale Centre-Ville, Montréal, Québec, Canada H3C 3J7
  • ,
  • Alexis Ascah

      Affiliations

    • Département de kinésiologie, Université de Montréal, C.P. 6128, Succursale Centre-Ville, Montréal, Québec, Canada H3C 3J7
  • ,
  • Mariannick Marcil

      Affiliations

    • Département de kinésiologie, Université de Montréal, C.P. 6128, Succursale Centre-Ville, Montréal, Québec, Canada H3C 3J7
  • ,
  • Christian F. Deschepper

      Affiliations

    • Experimental Cardiovascular Biology Research Unit, Institut de recherches cliniques de Montréal, Montreal, Quebec, Canada H2W 1R7
  • ,
  • Yan Burelle

      Affiliations

    • Département de kinésiologie, Université de Montréal, C.P. 6128, Succursale Centre-Ville, Montréal, Québec, Canada H3C 3J7
    • Corresponding Author InformationCorresponding author. Tel.: +1 514 343 6083; fax: +1 514 343 2181.

Received 9 July 2008 ,Revised 9 October 2008 ,Accepted 15 October 2008.

References 

  1. Ide T, Tsutsui H, Hayashidani S, Kang D, Suematsu N, Nakamura K, et al. Mitochondrial DNA damage and dysfunction associated with oxidative stress in failing hearts after myocardial infarction. Circ Res. 2001 Mar 16;88(5):529–535
  2. Jarreta D, Orus J, Barrientos A, Miro O, Roig E, Heras M, et al. Mitochondrial function in heart muscle from patients with idiopathic dilated cardiomyopathy. Cardiovasc Res. 2000 Mar;45(4):860–865
  3. Ozcan C, Bienengraeber M, Hodgson DM, Mann DL, Terzic A. Mitochondrial tolerance to stress impaired in failing heart. J. Mol. Cell. Cardiol. 2003 Sep;35(9):1161–1166
  4. Sharov VG, Todor AV, Silverman N, Goldstein S, Sabbah HN. Abnormal mitochondrial respiration in failed human myocardium. J. Mol. Cell. Cardiol. 2000;32(12):2361
  5. Javadov S, Huang C, Kirshenbaum L, Karmazyn M. NHE-1 inhibition improves impaired mitochondrial permeability transition and respiratory function during postinfarction remodelling in the rat. J. Mol. Cell. Cardiol. 2005 Jan;38(1):135–143
  6. Sharov VG, Todor A, Khanal S, Imai M, Sabbah HN. Cyclosporine A attenuates mitochondrial permeability transition and improves mitochondrial respiratory function in cardiomyocytes isolated from dogs with heart failure. J. Mol. Cell. Cardiol. 2007 Jan;42(1):150–158
  7. Moe GW, Naik G, Konig A, Lu X, Feng Q. Early and persistent activation of myocardial apoptosis, bax and caspases: insights into mechanisms of progression of heart failure. Pathophysiology. 2002 Jun;8(3):183–192
  8. Narula J, Pandey P, Arbustini E, Haider N, Narula N, Kolodgie FD, et al. Apoptosis in heart failure: release of cytochrome c from mitochondria and activation of caspase-3 in human cardiomyopathy. Proc. Natl. Acad. Sci. U. S. A. 1999 Jul 6;96(14):8144–8149
  9. Olivetti G, Abbi R, Quaini F, Kajstura J, Cheng W, Nitahara JA, et al. Apoptosis in the failing human heart. N. Engl. J. Med. 1997 Apr 17;336(16):1131–1141
  10. 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 Feb 6;39(3):481–488
  11. Scheubel RJ, Tostlebe M, Simm A, Rohrbach S, Prondzinsky R, Gellerich FN, et al. Dysfunction of mitochondrial respiratory chain complex I in human failing myocardium is not due to disturbed mitochondrial gene expression. J. Am. Coll. Cardiol. 2002 Dec 18;40(12):2174–2181
  12. Regula KM, Kirshenbaum LA. Apoptosis of ventricular myocytes: a means to an end. J. Mol. Cell Cardiol. 2005 Jan;38(1):3–13
  13. van Empel VP, Bertrand AT, Hofstra L, Crijns HJ, Doevendans PA, De Windt LJ. Myocyte apoptosis in heart failure. Cardiovasc Res. 2005 Jul 1;67(1):21–29
  14. Marcil M, Ascah A, Matas J, Bélanger S, Deschepper CF, Burelle Y. Compensated volume overload increases the vulnerability of heart mitochondria without affecting their functions in absence of stress. J. Mol. Cell. Cardiol. 2006;41(6):998–1009
  15. Bernardi P, Scorrano L, Colonna R, Petronilli V, Di Lisa F. Mitochondria and cell death. Mechanistic aspects and methodological issues. Eur. J. Biochem. 1999;264(3):687–701
  16. Zoratti M, Szabo I. The mitochondrial permeability transition. Biochim. Biophys. Acta. 1995 Jul 17;1241(2):139–176
  17. Connern CP, Halestrap AP. Recruitment of mitochondrial cyclophilin to the mitochondrial inner membrane under conditions of oxidative stress that enhance the opening of a calcium-sensitive non-specific channel. Biochem. J. 1994 Sep 1;302(Pt 2):321–324
  18. Connern CP, Halestrap AP. Chaotropic agents and increased matrix volume enhance binding of mitochondrial cyclophilin to the inner mitochondrial membrane and sensitize the mitochondrial permeability transition to [Ca2+]. Biochemistry. 1996 Jun 25;35(25):8172–8180
  19. Crompton M. The mitochondrial permeability transition pore and its role in cell death. Biochem. J. 1999 Jul 15;341(Pt 2):233–249
  20. Nakayama H, Chen X, Baines CP, Klevitsky R, Zhang X, Zhang H, et al. Ca2+-and mitochondrial-dependent cardiomyocyte necrosis as a primary mediator of heart failure. J. Clin. Invest. 2007 Sep;117(9):2431–2444
  21. 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(7033):658
  22. Garcia R, Diebold S. Simple, rapid, and effective method of producing aortocaval shunts in the rat. Cardiovasc. Res. 1990 May;24(5):430–432
  23. Souzeau E, Llamas B, Belanger S, Picard S, Deschepper CF. A genetic locus accentuates the effect of volume overload on adverse left ventricular remodeling in male and female rats. Hypertension. 2006 January 1, 2006;47(1):128–133
  24. Emaus RK, Grunwald R, Lemasters JJ. Rhodamine 123 as a probe of transmembrane potential in isolated rat-liver mitochondria: spectral and metabolic properties. Biochim. Biophys. Acta. 1986 Jul 23;850(3):436–448
  25. Csukly K, Ascah A, Matas J, Gardiner PF, Fontaine E, Burelle Y. Muscle denervation promotes opening of the permeability transition pore and increases the expression of cyclophilin D. J. Physiol. 2006 Jul 1;574(Pt 1):319–327
  26. Bernardi P. Modulation of the mitochondrial cyclosporin A-sensitive permeability transition pore by the proton electrochemical gradient. Evidence that the pore can be opened by membrane depolarization. J. Biol. Chem. 1992 May 5;267(13):8834–8839
  27. Turrens JF. Superoxide production by the mitochondrial respiratory chain. Biosci. Rep. 1997 Feb;17(1):3–8
  28. Chien KR. Stress pathways and heart failure. Cell. 1999 Sep 3;98(5):555–558
  29. Giordano FJ. Oxygen, oxidative stress, hypoxia, and heart failure. J. Clin. Invest. 2005 Mar;115(3):500–508
  30. Balke CW, Shorofsky SR. Alterations in calcium handling in cardiac hypertrophy and heart failure. Cardiovasc Res. 1998 Feb;37(2):290–299
  31. Yano M, Ikeda Y, Matsuzaki M. Altered intracellular Ca2+ handling in heart failure. J. Clin. Invest. 2005 Mar;115(3):556–564
  32. Nakagawa T, Shimizu S, Watanabe T, Yamaguchi O, Otsu K, Yamagata H, et al. Cyclophilin D-dependent mitochondrial permeability transition regulates some necrotic but not apoptotic cell death. Nature. 2005 Mar 31;434(7033):652–658
  33. Andreeva L, Heads R, Green CJ. Cyclophilins and their possible role in the stress response. Int. J. Exp. Pathol. 1999 Dec;80(6):305–315
  34. Bose S, Weikl T, Bugl H, Buchner J. Chaperone function of Hsp90-associated proteins. Science (New York, NY. 1996 Dec 6;274(5293):1715–1717
  35. Freeman BC, Toft DO, Morimoto RI. Molecular chaperone machines: chaperone activities of the cyclophilin Cyp-40 and the steroid aporeceptor-associated protein p23. Science (New York, NY. 1996 Dec 6;274(5293):1718–1720
  36. Johnson JL. Toft DO, A novel chaperone complex for steroid receptors involving heat shock proteins, immunophilins, and p23. J. Biol. Chem. 1994 Oct 7;269(40):24989–24993
  37. Tanonaka K, Toga W, Takahashi M, Yoshida H, Oikawa R, Takeo S. Induction of heat shock protein 72 in the failing heart is attenuated after an exposure to heat shock. Mol. Cell. Biochem. 2004 Apr;259(1–2):211–215
  38. Tanonaka K, Yoshida H, Toga W, Furuhama K, Takeo S. Myocardial heat shock proteins during the development of heart failure. Biochem. Biophys. Res. Commun. 2001 May 4;283(2):520–525
  39. Toga W, Tanonaka K, Takeo S. Changes in Hsp60 level of the failing heart following acute myocardial infarction and the effect of long-term treatment with trandolapril. Biol. Pharm. Bull. 2007 Jan;30(1):105–110
  40. Brustovetsky N, Brustovetsky T, Purl KJ, Capano M, Crompton M, Dubinsky JM. Increased susceptibility of striatal mitochondria to calcium-induced permeability transition. J. Neurosci. 2003 Jun 15;23(12):4858–4867
  41. Eliseev RA, Filippov G, Velos J, VanWinkle B, Goldman A, Rosier RN, et al. Role of cyclophilin D in the resistance of brain mitochondria to the permeability transition. Neurobiol. Aging. 2007 Oct;28(10):1532–1542
  42. Connern CP, Halestrap AP. Purification and N-terminal sequencing of peptidyl-prolyl cis-trans-isomerase from rat liver mitochondrial matrix reveals the existence of a distinct mitochondrial cyclophilin. Biochem. J. 1992 Jun 1;284(Pt 2):381–385
  43. Tanveer A, Virji S, Andreeva L, Totty NF, Hsuan JJ, Ward JM, et al. Involvement of cyclophilin D in the activation of a mitochondrial pore by Ca2+ and oxidant stress. Eur. J. Biochem. 1996 May 15;238(1):166–172
  44. Andreeva L, Tanveer A, Crompton M. Evidence for the involvement of a membrane-associated cyclosporin-A-binding protein in the Ca(2+)-activated inner membrane pore of heart mitochondria. Eur. J. Biochem. 1995 Jun 15;230(3):1125–1132
  45. Benderdour M, Charron G, Comte B, Ayoub R, Beaudry D, Foisy S, et al. Decreased cardiac mitochondrial NADP+-isocitrate dehydrogenase activity and expression: a marker of oxidative stress in hypertrophy development. Am. J. Physiol. Heart Circ. Physiol. 2004 Nov;287(5):H2122–2131
  46. Benderdour M, Charron G, DeBlois D, Comte B, Des Rosiers C. Cardiac mitochondrial NADP+-isocitrate dehydrogenase is inactivated through 4-hydroxynonenal adduct formation: an event that precedes hypertrophy development. J. Biol. Chem. 2003 Nov 14;278(46):45154–45159
  47. Berenji K, Drazner MH, Rothermel BA, Hill JA. Does load-induced ventricular hypertrophy progress to systolic heart failure?. Am. J. Physiol. Heart Circ. Physiol. 2005 July 1, 2005;289(1):H8–16
  48. Frey N, Olson EN. Cardiac hypertrophy: the good, the bad, and the ugly. Annu. Rev. Physiol. 2003;65:45–79
  49. Crompton M, Virji S, Ward JM. Cyclophilin-D binds strongly to complexes of the voltage-dependent anion channel and the adenine nucleotide translocase to form the permeability transition pore. Eur. J. Biochem. 1998 Dec 1;258(2):729–735

PII: S0022-2828(08)01364-3

doi: 10.1016/j.yjmcc.2008.10.020

Journal of Molecular and Cellular Cardiology
Volume 46, Issue 3 , Pages 420-430 , March 2009