Trends in Cardiovascular Medicine
Volume 15, Issue 3 , Pages 118-123 , April 2005

The Mitochondrial Biogenesis Regulatory Program in Cardiac Adaptation to Ischemia—A Putative Target for Therapeutic Intervention

  • Christopher J. McLeod
    • ,
  • Ines Pagel
    • ,
  • Michael N. Sack

      Affiliations

    • Corresponding Author InformationAddress correspondence to: Michael N. Sack, MD, PhD, NHLBI/NIH, Building 10-CRC, Room 5-3150, 10 Center Drive, Bethesda, MD 20892-1454, USA. Tel.: (+1) 301-402-9259; fax: (+1) 301-402-0888.

References 

  1. Baker JE, Holman P, Kalyanaraman B, et al. Adaptation to chronic hypoxia confers tolerance to subsequent myocardial ischemia by increased nitric oxide production. Ann NY Acad Sci. 1999;874:236–253
  2. Barth E, Stammler G, Speiser B, Schaper J. Ultrastructural quantification of mitochondria and myofilaments in cardiac muscle from 10 different animal species including man. J Mol Cell Cardiol. 1992;24:669–681
  3. Bienengraeber M, Ozcan C, Terzic A. Stable transfection of UCP1 confers resistance to hypoxia/reoxygenation in a heart-derived cell line. J Mol Cell Cardiol. 2003;35:861–865
  4. Bolli R. The late phase of preconditioning. Circ Res. 2000;87:972–983
  5. Chen Z, Siu B, Ho YS, et al. Overexpression of MnSOD protects against myocardial ischemia/reperfusion injury in transgenic mice. J Mol Cell Cardiol. 1998;30:2281–2289
  6. Dhanasekaran A, Kotamraju S, Kalivendi SV, et al. Supplementation of endothelial cells with mitochondria-targeted antioxidants inhibit peroxide-induced mitochondrial iron uptake, oxidative damage, and apoptosis. J Biol Chem. 2004;279:37575–37587
  7. Eells JT, Henry MM, Gross GJ, Baker JE. Increased mitochondrial K(ATP) channel activity during chronic myocardial hypoxia: is cardioprotection mediated by improved bioenergetics?. Circ Res. 2000;87:915–921
  8. Eliseev RA, Vanwinkle B, Rosier RN, Gunter TE. Diazoxide-mediated preconditioning against apoptosis involves activation of cAMP-response element-binding protein (CREB) and NFkappaB. J Biol Chem. 2004;279:46748–46754
  9. Finck BN, Bernal-Mitrachi C, Han DH, et al. A potential link between muscle peroxisome proliferator-activated receptor-alpha signaling and obesity-related diabetes. Cell Metab. 2005;1:133–144
  10. Herzig RP, Scacco S, Scarpulla RC. Sequential serum-dependent activation of CREB and NRF-1 leads to enhanced mitochondrial respiration through the induction of cytochrome c. J Biol Chem. 2000;275:13134–13141
  11. Hoerter J, Gonzalez-Barroso MD, Couplan E, et al. Mitochondrial uncoupling protein 1 expressed in the heart of transgenic mice protects against ischemic-reperfusion damage. Circulation. 2004;110:528–533
  12. Huss JM, Kelly DP. Nuclear receptor signaling and cardiac energetics. Circ Res. 2004;95:568–578
  13. Huss JM, Torra IP, Staels B, et al. Estrogen-related receptor {alpha} directs peroxisome proliferator-activated receptor a signaling in the transcriptional control of energy metabolism in cardiac and skeletal muscle. Mol Cell Biol. 2004;24:9079–9091
  14. Kelly DP, Scarpulla RC. Transcriptional regulatory circuits controlling mitochondrial biogenesis and function. Genes Dev. 2004;18:357–368
  15. Knaapen MW, Vrolijk BC, Wenink AC. Ultrastructural changes in the myocardium in the embryonic rat heart. Anat Rec. 1997;248:233–241
  16. Lee HC, Yin PH, Lu CY, et al. Increase of mitochondria and mitochondrial DNA in response to oxidative stress in human cells. Biochem J. 2000;348(Pt 2):425–432
  17. Lehman JJ, Barger PM, Kovacs A, et al. Peroxisome proliferator-activated receptor gamma coactivator-1 promotes cardiac mitochondrial biogenesis. J Clin Invest. 2000;106:847–856
  18. Li B, Holloszy JO, Semenkovich CF. Respiratory uncoupling induces delta-aminolevulinate synthase expression through a nuclear respiratory factor-1-dependent mechanism in HeLa cells. J Biol Chem. 1999;274:17534–17540
  19. Liu HR, Tao L, Gao E, et al. Anti-apoptotic effects of rosiglitazone in hypercholesterolemic rabbits subjected to myocardial ischemia and reperfusion. Cardiovasc Res. 2004;62:135–144
  20. Lygate CA, Hulbert K, Monfared M, et al. The PPARgamma-activator rosiglitazone does not alter remodeling but increases mortality in rats post-myocardial infarction. Cardiovasc Res. 2003;58:632–637
  21. Marin-Garcia J, Ananthakrishnan R, Agrawal N, Goldenthal MJ. Mitochondrial gene expression during bovine cardiac growth and development. J Mol Cell Cardiol. 1994;26:1029–1036
  22. McCarthy J, McLeod CJ, Minners J, et al. PKC epsilon activation augments cardiac mitochondrial post-anoxic reserve: a putative mechanism in PKC epsilon cardioprotection. J Mol Cell Cardiol. 2005;38:697–700
  23. McLeod CJ, Jeyabalan AP, Minners JO, et al. Delayed ischemic preconditioning activates nuclear-encoded electron-transfer-chain gene expression in parallel with enhanced postanoxic mitochondrial respiratory recovery. Circulation. 2004;110:534–539
  24. Meerson FZ, Gomzakov OA, Shimkovich MV. Adaptation to high altitude hypoxia as a factor preventing development of myocardial ischemic necrosis. Am J Cardiol. 1973;31:30–34
  25. Minners J, McLeod CJ, Sack MN. Mitochondrial plasticity in classical ischemic preconditioning: Moving beyond the mitochondrial KATP channel. Cardiovasc Res. 2003;59:1–6
  26. Nisoli E, Clementi E, Paolucci C, et al. Mitochondrial biogenesis in mammals: the role of endogenous nitric oxide. Science. 2003;299:896–899
  27. Nisoli E, Clementi E, Moncada S, Carruba MO. Mitochondrial biogenesis as a cellular signaling framework. Biochem Pharmacol. 2004;67:1–15
  28. Nisoli E, Falcone S, Tonello C, et al. Mitochondrial biogenesis by NO yields functionally active mitochondria in mammals. Proc Natl Acad Sci USA. 2004;101:16507–16512
  29. Opie LH, Sack MN. Metabolic plasticity and the promotion of cardiac protection in ischemia and ischemic preconditioning. J Mol Cell Cardiol. 2002;34:1077–1089
  30. Ou LC, Tenney SM. Properties of mitochondria from hearts of cattle acclimatized to high altitude. Respir Physiol. 1970;8:151–159
  31. Rabinowitz M, Zak R. Mitochondria and cardiac hypertrophy. Circ Res. 1975;36:367–376
  32. Russell LK, Finck BN, Kelly DP. Mouse models of mitochondrial dysfunction and heart failure. J Mol Cell Cardiol. 2005;38:81–91
  33. Russell LK, Mansfield CM, Lehman JJ, et al. Cardiac-specific induction of the transcriptional coactivator peroxisome proliferator-activated receptor gamma coactivator-1alpha promotes mitochondrial biogenesis and reversible cardiomyopathy in a developmental stage-dependent manner. Circ Res. 2004;94:525–533
  34. Scarpulla RC. Transcriptional activators and coactivators in the nuclear control of mitochondrial function in mammalian cells. Gene. 2002;286:81–89
  35. Shiomi T, Tsutsui H, Hayashidani S, et al. Pioglitazone, a peroxisome proliferator-activated receptor-gamma agonist, attenuates left ventricular remodeling and failure after experimental myocardial infarction. Circulation. 2002;106:3126–3132
  36. St-Pierre J, Lin J, Krauss S, et al. Bioenergetic analysis of peroxisome proliferator-activated receptor gamma coactivators 1alpha and 1beta (PGC-1α and PGC-1β) in muscle cells. J Biol Chem. 2003;278:26597–26603
  37. Szweda LI, Lucas DT, Humphries KM, Szweda PA. Cardiac reperfusion injury: aging, lipid peroxidation, and mitochondrial function. In:  Lemasters JJ,  Nieminen A editor. Mitochondria in pathogenesis. New York: Kluwer Academic; 2001;p. 95–111
  38. Teshima Y, Akao M, Jones SP, Marban E. Uncoupling protein-2 overexpression inhibits mitochondrial death pathway in cardiomyocytes. Circ Res. 2003;93:192–200
  39. Vanden Hoek T, Becker LB, Shao ZH, et al. Preconditioning in cardiomyocytes protects by attenuating oxidant stress at reperfusion. Circ Res. 2000;86:541–548
  40. Weitzel JM, Iwen KA, Seitz HJ. Regulation of mitochondrial biogenesis by thyroid hormone. Exp Physiol. 2003;88:121–128
  41. Wilson-Fritch L, Burkart A, Bell G, et al. Mitochondrial biogenesis and remodeling during adipogenesis and in response to the insulin sensitizer rosiglitazone. Mol Cell Biol. 2003;23:1085–1094
  42. Wilson-Fritch L, Nicoloro S, Chouinard M, et al. Mitochondrial remodeling in adipose tissue associated with obesity and treatment with rosiglitazone. J Clin Invest. 2004;114:1281–1289
  43. Wu Z, Puigserver P, Andersson U, et al. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell. 1999;98:115–124
  44. Xia Y, Buja LM, Scarpulla RC, McMillin JB. Electrical stimulation of neonatal cardiomyocytes results in the sequential activation of nuclear genes governing mitochondrial proliferation and differentiation. Proc Natl Acad Sci USA. 1997;94:11399–11404
  45. Xu Y, Gen M, Lu L, Fox J. PPAR-gamma activation fails to provide myocardial protection in ischemia and reperfusion in pigs. Am J Physiol Heart Circ Physiol. 2005;288:H1314–H1323
  46. Yamashita N, Hoshida S, Taniguchi N, et al. A “second window of protection” occurs 24 h after ischemic preconditioning in the rat heart. J Mol Cell Cardiol. 1998;30:1181–1189
  47. Yellon DM, Downey JM. Preconditioning the myocardium: from cellular physiology to clinical cardiology. Physiol Rev. 2003;83:1113–1151
  48. Yue TL, Bao W, Gu JL, et al. Rosiglitazone treatment in Zucker diabetic fatty rats is associated with ameliorated cardiac insulin resistance and protection from ischemia/reperfusion-induced myocardial injury. Diabetes. 2005;54:554–562
  49. Zong H, Ren JM, Young LH, et al. AMP kinase is required for mitochondrial biogenesis in skeletal muscle in response to chronic energy deprivation. Proc Natl Acad Sci USA. 2002;99:15983–15987
  50. Zweier JL. Measurement of superoxide-derived free radicals in the reperfused heart. Evidence for a free radical mechanism of reperfusion injury. J Biol Chem. 1988;263:1353–1357

PII: S1050-1738(05)00055-1

doi: 10.1016/j.tcm.2005.05.001

Trends in Cardiovascular Medicine
Volume 15, Issue 3 , Pages 118-123 , April 2005

Article Tools

* Image Usage & Resolution