Early long-term L-T3 replacement rescues mitochondria and prevents ischemic cardiac remodelling in rats

Journal of Cellular and Molecular Medicine

Volumn 15, Issue 3, 2011, Pages 514-524

  Forini, Francesca ^a   Lionetti, Vincenzo ^a,b   Ardehali, Hossein ^c   Pucci, Angela ^d   Cecchetti, Federica ^e   Ghanefar, Mohsen ^c   Nicolini, Giuseppina ^a   Ichikawa, Yoshihiko ^c   Nannipieri, Monica ^e   Recchia, Fabio A ^b,f   Iervasi, Giorgio ^a  

^a INSTITUTE OF CLINICAL PHYSIOLOGY   (Italy)

^b SCUOLA SUPERIORE SANT ANNA   (Italy)

^c NORTHWESTERN UNIVERSITY   (United States)

^d UNIVERSITY HOSPITAL OF PISA   (Italy)

^e UNIVERSITY OF PISA   (Italy)

^f NEW YORK MEDICAL COLLEGE   (United States)

Author keywords

Angiogenesis; L triiodothyronine; MitoKATP; Myocardial infarction; Remodelling

Indexed keywords

HIF1A PROTEIN, RAT; HYDROGEN PEROXIDE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; LIOTHYRONINE; OXIDIZING AGENT; THYROXINE;

ANIMAL; APOPTOSIS; ARTICLE; BLOOD; CAPILLARY; CELL CULTURE; CYTOLOGY; DRUG EFFECT; GENETICS; HEART INFARCTION; HEART MUSCLE CELL; HEART VENTRICLE REMODELING; HEMODYNAMICS; HORMONE SUBSTITUTION; MALE; METABOLISM; MITOCHONDRION; PATHOPHYSIOLOGY; RANDOMIZATION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SUBCUTANEOUS DRUG ADMINISTRATION; TIME; WESTERN BLOTTING; WISTAR RAT;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CAPILLARIES; CELLS, CULTURED; HEMODYNAMICS; HORMONE REPLACEMENT THERAPY; HYDROGEN PEROXIDE; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; INFUSIONS, SUBCUTANEOUS; MALE; MITOCHONDRIA; MYOCARDIAL INFARCTION; MYOCYTES, CARDIAC; OXIDANTS; RANDOM ALLOCATION; RATS; RATS, WISTAR; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; THYROXINE; TIME FACTORS; TRIIODOTHYRONINE; VENTRICULAR REMODELING;

RATTUS;

EID: 79953293966     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1582-4934.2010.01014.x     Document Type: Article

References (54)

1. Iervasi G, Pingitore A, Landi P, et al Low-T3 syndrome: a strong prognostic predictor of death in patients with heart disease. Circulation. 2003; 107: 708-13.
2. Pingitore A, Galli E, Barison A, et al Acute effects of triiodothyronine (T3) replacement therapy in patients with chronic heart failure and low-T3 syndrome: a randomized, placebo-controlled study. J Clin Endocrinol Metab. 2008; 93: 1351-8.
3. Hamilton MA, Stevenson LW, Luu M, et al Altered thyroid hormone metabolism in advanced heart failure. J Am Coll Cardiol. 1990; 16: 91-5.
4. Wiersinga WM, Lie KI, Touber JL. Thyroid hormones in acute myocardial infarction. Clin Endocrinol. 1981; 14: 367-74.
5. Friberg L, Drvota V, Bjelak AH, et al Association between increased levels of reverse triiodothyronine and mortality after acute myocardial infarction. Am J Med. 2001; 111: 699-703.
6. Wrutniak-Cabello C, Casas F, Cabello G. Thyroid hormone action in mitochondria. J Mol Endocrinol. 2001; 26: 67-77.
7. Goldenthal MJ, Ananthakrishnan R, Marín-García J. Nuclear-mitochondrial cross-talk in cardiomyocyte T3 signaling: a time-course analysis. J Mol Cell Cardiol. 2005; 39: 319-26.
8. Goldenthal MJ, Weiss HR, Marín-García J. Bioenergetic remodeling of heart mitochondria by thyroid hormone. Mol Cell Biochem. 2004; 265: 97-106.
9. Marín-García J, Goldenthal MJ. Mitochondrial centrality in heart failure. Heart Fail Rev. 2008; 13: 137-50.
10. Zhu L, Yu Y, Chua BH, et al Regulation of sodium-calcium exchange and mitochondrial energetics by Bcl-2 in the heart of transgenic mice. J Mol Cell Cardiol. 2001; 33: 2135-44.
11. Huss JM, Kelly DP. Mitochondrial energy metabolism in heart failure: a question of balance. J Clin Invest. 2005; 115: 547-55.
12. Cannino G, Di Liegro CM, Rinaldi AM. Nuclear-mitochondrial interaction. Mitochondrion. 2007; 7: 359-66.
13. Chavez A, Miranda LF, Pichiule P, et al Mitochondria and hypoxia-induced gene expression mediated by hypoxia-inducible factors. Ann NY Acad Sci. 2008; 1147: 312-20.
14. Sun Y. Myocardial repair/remodelling following infarction: roles of local factors. Cardiovasc Res. 2009; 81: 482-90.
15. Ikeuchi M, Matsusaka H, Kang D, et al Overexpression of mitochondrial transcription factor A ameliorates mitochondrial deficiencies and cardiac failure after myocardial infarction. Circulation. 2005; 112: 683-90.
16. Kang D, Kim SH, Hamasaki N. Mitochondrial transcription factor A (TFAM): roles in maintenance of mtDNA and cellular functions. Mitochondrion. 2007; 7: 39-44.
17. Ventura-Clapier R, Garnier A, Veksler V. Transcriptional control of mitochondrial biogenesis: the central role of PGC-1alpha. Cardiovasc Res. 2008; 79: 208-17.
18. Russell LK, Mansfield CM, Lehman JJ, et al Cardiacspecific 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: 525-33.
19. Garnier A, Fortin D, Deloménie C, et al Depressed mitochondrial transcription factors and oxidative capacity in ratfailing cardiac and skeletal muscles. J Physiol. 2003; 551: 491-501.
20. Ardehali H, O'Rourke B, Marbán E. Cardioprotective role of the mitochondrial ATPbinding cassette protein 1. Circ Res. 2005; 97: 740-2.
21. Ventura C, Cantoni S, Bianchi F, et al Hyaluronan mixed esters of butyric and retinoic Acid drive cardiac and endothelial fate in term placenta human mesenchymal stem cells and enhance cardiac repair in infarcted rat hearts. J Biol Chem. 2007; 282: 14243-52.
22. Henderson KK, Danzi S, Paul JT, et al Physiological replacement of T3 improves left ventricular function in an animal model of myocardial infarction-induced congestive heart failure. Circ Heart Fail. 2009; 2: 243-52.
23. Ojamaa K, Kenessey A, Shenoy R, et al Thyroid hormone metabolism and cardiac gene expression after acute myocardial infarction in the rat. Am J Physiol Endocrinol Metab. 2000; 279: E1319-24.
24. Shiomi T, Tsutsui H, Hayashidani S, et al Pioglitazone, a peroxisome proliferator-activated receptor-gamma agonist, attenuates lef ventricular remodeling and failure after experimental myocardial infarction. Circulation. 2002; 106: 3126-32.
25. Kasdallah AG, Mornagui B, Gharbi N, et al Metabolic and endocrine effects of water and/or food deprivation in rats. C R Biol. 2005; 328: 463-70.
26. Olivetti G, Ricci R, Beghi C, et al Response of the border zone to myocardial infarction in rats. Am J Pathol. 1986; 125: 476-83.
27. Davani S, Marandin A, Mersin N, et al Mesenchymal progenitor cells differentiate into an endothelial phenotype, enhance vascular density, and improve heart function in a rat cellular cardiomyoplasty model. Circulation. 2003; 108: 253-8.
28. Pucci A, Zanini C, Granata R, et al Myocardial insulinlike growth factor-1 and insulin-like growth factor binding protein-3 gene expression in failing hearts harvested from patients undergoing cardiac transplantation. J Heart Lung Transplant. 2009; 28: 402-5.
29. Morrish F, Buroker NE, Ge M, et al Thyroid hormone receptor isoforms localize to cardiac mitochondrial matrix with potential for binding to receptor elements on mtDNA. Mitochondrion. 2006; 6: 143-8.
30. Guo D, Nguyen T, Ogbi M, et al Protein kinase C-epsilon coimmunoprecipitates with cytochrome oxidase subunit IV and is associated with improved cytochrome-c oxidase activity and cardioprotection. Am J Physiol Heart Circ Physiol. 2007; 293: H2219-30.
31. Hassouna A, Loubani M, Matata BM, et al Mitochondrial dysfunction as the cause of the failure to precondition the diabetic human myocardium. Cardiovasc Res. 2006; 69: 450-8.
32. Morgunov I, Srere PA. Interaction between citrate synthase and malate dehydrogenase. Substrate channeling of oxaloacetate. J Biol Chem. 1998; 273: 29540-4.
33. 2 in cardiac myocytes. J Biol Chem. 2003; 278: 25542-7.
34. Korge P, Honda HM, Weiss JN. Protection of cardiac mitochondria by diazoxide and protein kinase C:implications for ischemic preconditioning. Proc Natl Acad Sci USA. 2002; 99: 3312-7.
35. Park JY, Wang P, Matsumoto T, et al p53 Improves aerobic exercise capacity and augments skeletal muscle mitochondrial DNA content. Circ Res. 2009; 105: 705-12.
36. Fukui S, Kitagawa-Sakakida S, Kawamata S, et al Therapeutic effect of midkine on cardiac remodeling in infarcted rat hearts. Ann Thorac Surg. 2008; 85: 562-70.
37. Makino A, Suarez J, Wang H, et al Thyroid hormone receptor-beta is associated with coronary angiogenesis during pathological cardiac hypertrophy. Endocrinology. 2009; 150: 2008-15.
38. Eckle T, Köhler D, Lehmann R, et al Hypoxia-inducible factor-1 is central to cardioprotection: a new paradigm for ischemic preconditioning. Circulation. 2008; 118: 166-75.
39. Lee SH, Wolf PL, Escudero R, et al Early expression of angiogenesis factors in acute myocardial ischemia and infarction. N Engl J Med. 2000; 342: 626-33.
40. Pingitore A, Landi P, Taddei MC, et al Triiodothyronine levels for risk stratification of patients with chronic heart failure. Am J Med. 2005; 118: 132-6.
41. Chen YF, Kobayashi S, Chen J, et al Short term triiodo-Lthyronine treatment inhibits cardiac myocyte apoptosis in border area after myocardial infarction in rats. J Mol Cell Cardiol. 2008; 44: 180-7.
42. Kahaly GJ, Dillmann WH. Thyroid hormone action in the heart. Endocr Rev. 2005; 26: 704-28.
43. Pfeffer MA, Braunwald E. Ventricular remodeling after myocardial infarction. Experimental observations and clinical implications. Circulation. 1990; 81: 1161-72.
44. Sigurdsson A, Eriksson SV, Hall C, et al Early neurohormonal effects of trandolapril in patients with left ventricular dysfunction and a recent acute myocardial infarction: a double-blind, randomized, placebo-controlled multicentre study. Eur J Heart Fail. 2001; 3: 69-78.
45. Pantos C, Mourouzis I, Markakis K, et al Longterm thyroid hormone administration reshapes left ventricular chamber and improves cardiac function after myocardial infarction in rats. Basic Res Cardiol. 2008; 103: 308-18.
46. Karch R, Neumann F, Ullrich R, et al The spatial pattern of coronary capillaries in patients with dilated, ischemic, or inflammatory cardiomyopathy. Cardiovasc Pathol. 2005; 14: 135-44.
47. Dorn GW 2nd. Apoptotic and non-apoptotic programmed cardiomyocyte death in ventricular remodelling. Cardiovasc Res. 2009; 81: 465-73.
48. Goto K, Takemura G, Maruyama R, et al Unique mode of cell death in freshly isolated adult rat ventricular cardiomyocytes exposed to hydrogen peroxide. Med Mol Morphol. 2009; 42: 92-101.
49. Kido M, Du L, Sullivan CC, et al Hypoxia-inducible factor 1-alpha reduces infarction and attenuates progression of cardiac dysfunction after myocardial infarction in the mouse. J Am Coll Cardiol. 2005; 46: 2116-24.
50. Marín-Garcia J. Thyroid hormone and myocardial mitochondrial biogenesis. Vascul Pharmacol. 2009 [Epub ahead of print]. Doi:
51. Ide T, Tsutsui H, Hayashidani S, et al Mitochondrial DNA damage and dysfunction associated with oxidative stress in failing hearts after myocardial infarction. Circ Res. 2001; 88: 529-35.
52. Yamaguchi O, Higuchi Y, Hirotani S, et al Targeted deletion of apoptosis signalregulating kinase 1 attenuates left ventricular remodeling. Proc Natl Acad Sci USA. 2003; 100: 15883-8.
53. Akao M, Ohler A, O'Rourke B, et al Mitochondrial ATP-sensitive potassium channels inhibit apoptosis induced by oxidative stress in cardiac cells. Circ Res. 2001; 88: 1267-75.
54. Pitts KR, Toombs CF. Studying ischemia and reperfusion in isolated neonatal rat ventricular myocytes using coverslip hypoxia. Methods Mol Med. 2007; 139: 271-81.