Thyroid hormone as a therapeutic option for treating ischaemic heart disease: From early reperfusion to late remodelling

Vascular Pharmacology

Volumn 52, Issue 3-4, 2010, Pages 157-165

  Pantos, Constantinos ^a   Mourouzis, Iordanis ^a   Cokkinos, Dennis V ^b,c  

^a UNIVERSITY OF ATHENS MEDICAL SCHOOL   (Greece)

^b ONASSIS CARDIAC SURGERY CENTER   (Greece)

^c BIOMEDICAL RESEARCH FOUNDATION   (Greece)

Author keywords

Myocardial ischaemia; Postischaemic cardiac remodelling; Thyroid hormone

Indexed keywords

ADRENERGIC RECEPTOR STIMULATING AGENT; HEAT SHOCK PROTEIN; HORMONE ANALOG; JANUS KINASE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; PHOSPHATIDYLINOSITOL 3 KINASE; THYROID HORMONE;

CELL SHAPE; CLINICAL PRACTICE; CYTOSKELETON; DRUG EFFICACY; DRUG MECHANISM; GEOMETRY; HEART DEVELOPMENT; HEART DISEASE; HEART FUNCTION; HEART MUSCLE ISCHEMIA; HEART PROTECTION; HEMODYNAMICS; HUMAN; NONHUMAN; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REPERFUSION INJURY; REVIEW;

ANIMALS; HEMODYNAMICS; HUMANS; MYOCARDIAL CONTRACTION; MYOCARDIAL ISCHEMIA; SIGNAL TRANSDUCTION; THYROID HORMONES; VENTRICULAR REMODELING;

EID: 76849112311     PISSN: 15371891     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.vph.2009.11.006     Document Type: Review

References (64)

1. Belke D.D., Gloss B., Hollander J.M., Swanson E.A., Duplain H., and Dillmann W.H. In vivo gene delivery of HSP70i by adenovirus and adeno-associated virus preserves contractile function in mouse heart following ischemia-reperfusion. Am. J. Physiol. Heart Circ. Physiol. 291 6 (2006) H2905-H2910
2. Bhargava M., Runyon M.R., Smirnov D., Lei J., Groppoli T.J., Mariash C.N., Wangensteen O.D., and Ingbar D.H. Triiodo-l-thyronine rapidly stimulates alveolar fluid clearance in normal and hyperoxia-injured lungs. Am. J. Respir. Crit. Care Med. 178 5 (2008) 506-512
3. Bogoyevitch M.A., Gillespie-Brown J., Ketterman A.J., Fuller S.J., Ben-Levy R., Ashworth A., Marshall C.J., and Sugden P.H. Stimulation of the stress-activated mitogen-activated protein kinase subfamilies in perfused heart. p38/RK mitogen-activated protein kinases and c-Jun N-terminal kinases are activated by ischemia/reperfusion. Circ. Res. 79 2 (1996) 162-173
4. Buser P.T., Wikman-Coffelt J., Wu S.T., Derugin N., Parmley W.W., and Higgins C.B. Postischemic recovery of mechanical performance and energy metabolism in the presence of left ventricular hypertrophy. A 31P-MRS study. Circ. Res. 66 3 (1990) 735-746
5. Chen H., Wu X.J., Lu X.Y., Zhu L., Wang L.P., Yang H.T., Chen H.Z., and Yuan W.J. Phosphorylated heat shock protein 27 is involved in enhanced heart tolerance to ischemia in short-term type 1 diabetic rats. Acta Pharmacol. Sin. 26 7 (2005) 806-812
6. Choi Y.S., Kwak Y.L., Kim J.C., Chun D.H., Hong S.W., and Shim J.K. Peri-operative oral triiodothyronine replacement therapy to prevent postoperative low triiodothyronine state following valvular heart surgery. Anaesthesia 64 8 (2009) 871-877
7. Cooper, D. K., Novitzky, D., Wicomb, W. N., Basker, M., Rosendale, J. D., and Myron Kauffman, H. 2009. A review of studies relating to thyroid hormone therapy in brain-dead organ donors. Front. Biosci. 143750-143770.
8. Dyke C.M., Ding M., Abd-Elfattah A.S., Loesser K., Dignan R.J., Wechsler A.S., and Salter D.R. Effects of triiodothyronine supplementation after myocardial ischemia. Ann. Thorac. Surg. 56 2 (1993) 215-222
9. Dyke C.M., Yeh Jr. T., Lehman J.D., Abd-Elfattah A., Ding M., Wechsler A.S., and Salter D.R. Triiodothyronine-enhanced left ventricular function after ischemic injury. Ann. Thorac. Surg. 52 1 (1991) 14-19
10. Eaton P., Fuller W., Bell J.R., and Shattock M.J. AlphaB crystallin translocation and phosphorylation: signal transduction pathways and preconditioning in the isolated rat heart. J. Mol. Cell. Cardiol. 33 9 (2001) 1659-1671
11. Fernandez V., Castillo I., Tapia G., Romanque P., Uribe-Echevarria S., Uribe M., Cartier-Ugarte D., Santander G., Vial M.T., and Videla L.A. Thyroid hormone preconditioning: protection against ischemia-reperfusion liver injury in the rat. Hepatology 45 1 (2007) 170-177
12. Goldman S., McCarren M., Morkin E., Ladenson P.W., Edson R., Warren S., Ohm J., Thai H., Churby L., Barnhill J., O'Brien T., Anand I., Warner A., Hattler B., Dunlap M., Erikson J., Shih M.C., and Lavori P. DITPA (3, 5-Diiodothyropropionic Acid), a thyroid hormone analog to treat heart failure: phase II trial veterans affairs cooperative study. Circulation 119 24 (2009) 3093-3100
13. Hambleton M., Hahn H., Pleger S.T., Kuhn M.C., Klevitsky R., Carr A.N., Kimball T.F., Hewett T.E., Dorn II G.W., Koch W.J., and Molkentin J.D. Pharmacological- and gene therapy-based inhibition of protein kinase Calpha/beta enhances cardiac contractility and attenuates heart failure. Circulation 114 6 (2006) 574-582
14. Holland II F.W., Brown Jr. P.S., and Clark R.E. Acute severe postischemic myocardial depression reversed by triiodothyronine. Ann. Thorac. Surg. 54 2 (1992) 301-305
15. Kadletz M., Mullen P.G., Ding M., Wolfe L.G., and Wechsler A.S. Effect of triiodothyronine on postischemic myocardial function in the isolated heart. Ann. Thorac. Surg. 57 3 (1994) 657-662
16. Kenessey A., Sullivan E.A., and Ojamaa K. Nuclear localization of protein kinase C-alpha induces thyroid hormone receptor-alpha1 expression in the cardiomyocyte. Am. J. Physiol. Heart Circ. Physiol. 290 1 (2006) H381-H389
17. Khoynezhad A., Jalali Z., and Tortolani A.J. Apoptosis: pathophysiology and therapeutic implications for the cardiac surgeon. Ann. Thorac. Surg. 78 3 (2004) 1109-1118
18. Kim Y.K., Suarez J., Hu Y., McDonough P.M., Boer C., Dix D.J., and Dillmann W.H. Deletion of the inducible 70-kDa heat shock protein genes in mice impairs cardiac contractile function and calcium handling associated with hypertrophy. Circulation 113 22 (2006) 2589-2597
19. Kinugawa K., Jeong M.Y., Bristow M.R., and Long C.S. Thyroid hormone induces cardiac myocyte hypertrophy in a thyroid hormone receptor alpha1-specific manner that requires TAK1 and p38 mitogen-activated protein kinase. Mol. Endocrinol. 19 6 (2005) 1618-1628
20. Klein I. Thyroid hormone and cardiac contractility. Am. J. Cardiol. 91 11 (2003) 1331-1332
21. Klein I., and Ojamaa K. Thyroid hormone-targeting the heart. Endocrinology 142 1 (2001) 11-12
22. Klemperer J.D., Zelano J., Helm R.E., Berman K., Ojamaa K., Klein I., Isom O.W., and Krieger K. Triiodothyronine improves left ventricular function without oxygen wasting effects after global hypothermic ischemia. J. Thorac. Cardiovasc. Surg. 109 3 (1995) 457-465
23. Kuzman J.A., Gerdes A.M., Kobayashi S., and Liang Q. Thyroid hormone activates Akt and prevents serum starvation-induced cell death in neonatal rat cardiomyocytes. J. Mol. Cell. Cardiol. 39 5 (2005) 841-844
24. Li G., Ali I.S., and Currie R.W. Insulin-induced myocardial protection in isolated ischemic rat hearts requires p38 MAPK phosphorylation of Hsp27. Am. J. Physiol. Heart Circ. Physiol. 294 1 (2008) H74-H87
25. Litwin S.E., Zhang D., Roberge P., and Pennock G.D. DITPA prevents the blunted contraction-frequency relationship in myocytes from infarcted hearts. Am. J. Physiol. Heart Circ. Physiol. 278 3 (2000) H862-H870
26. Liu Q., Clanachan A.S., and Lopaschuk G.D. Acute effects of triiodothyronine on glucose and fatty acid metabolism during reperfusion of ischemic rat hearts. Am. J. Physiol. 275 3 Pt 1 (1998) E392-E399
27. Mahaffey K.W., Raya T.E., Pennock G.D., Morkin E., and Goldman S. Left ventricular performance and remodeling in rabbits after myocardial infarction. Effects of a thyroid hormone analogue. Circulation 91 3 (1995) 794-801
28. Moruzzi P., Doria E., and Agostoni P.G. Medium-term effectiveness of l-thyroxine treatment in idiopathic dilated cardiomyopathy. Am. J. Med. 101 5 (1996) 461-467
29. Mourouzis I., Saranteas T., Perimenis P., Tesseromatis C., Kostopanagiotou G., Pantos C., and Cokkinos D.V. Morphine administration at reperfusion fails to improve postischaemic cardiac function but limits myocardial injury probably via heat-shock protein 27 phosphorylation. Eur. J. Anaesthesiol. 26 7 (2009) 572-581
30. Naito H., Melnychenko I., Didie M., Schneiderbanger K., Schubert P., Rosenkranz S., Eschenhagen T., and Zimmermann W.H. Optimizing engineered heart tissue for therapeutic applications as surrogate heart muscle. Circulation 114 1 Suppl (2006) I72-I178
31. Novitzky D., Cooper D.K., and Swanepoel A. Inotropic effect of triiodothyronine (T3) in low cardiac output following cardioplegic arrest and cardiopulmonary bypass: an initial experience in patients undergoing open heart surgery. Eur. J. Cardiothorac. Surg. 3 2 (1989) 140-145
32. Novitzky, D., Matthews, N., Shawley, D., Cooper, D. K., and Zuhdi, N. 1991. Triiodothyronine in the recovery of stunned myocardium in dogs. Ann Thorac Surg 51(1), 10-6; discussion 16-7.
33. Ojamaa K., Kenessey A., Shenoy R., and Klein I. Thyroid hormone metabolism and cardiac gene expression after acute myocardial infarction in the rat. Am. J. Physiol. Endocrinol. Metab. 279 6 (2000) E1319-E1324
34. Pantos C., Dritsas A., Mourouzis I., Dimopoulos A., Karatasakis G., Athanassopoulos G., Mavrogeni S., Manginas A., and Cokkinos D.V. Thyroid hormone is a critical determinant of myocardial performance in patients with heart failure: potential therapeutic implications. Eur. J. Endocrinol. 157 4 (2007) 515-520
35. Pantos C., Malliopoulou V., Mourouzis I., Karamanoli E., Moraitis P., Tzeis S., Paizis I., Cokkinos A.D., Carageorgiou H., Varonos D.D., and Cokkinos D.V. Thyroxine pretreatment increases basal myocardial heat-shock protein 27 expression and accelerates translocation and phosphorylation of this protein upon ischaemia. Eur. J. Pharmacol. 478 1 (2003) 53-60
36. Pantos C., Malliopoulou V., Mourouzis I., Thempeyioti A., Paizis I., Dimopoulos A., Saranteas T., Xinaris C., and Cokkinos D.V. Hyperthyroid hearts display a phenotype of cardioprotection against ischemic stress: a possible involvement of heat shock protein 70. Horm. Metab. Res. 38 5 (2006) 308-313
37. Pantos C., Malliopoulou V., Paizis I., Moraitis P., Mourouzis I., Tzeis S., Karamanoli E., Cokkinos D.D., Carageorgiou H., Varonos D., and Cokkinos D.V. Thyroid hormone and cardioprotection: study of p38 MAPK and JNKs during ischaemia and at reperfusion in isolated rat heart. Mol. Cell. Biochem. 242 1-2 (2003) 173-180
38. Pantos C., Mourouzis I., and Cokkinos D.V. Myocardial ischemia: basic concepts. In: Cokkinos D.V., Pantos C., Heusch G., and Taegtmeyer H. (Eds). Myocardial Ischemia: From Mechanisms to Theurapeutic Potentials (2006), New York, Springer 11-77
39. Pantos C., Mourouzis I., Dimopoulos A., Markakis K., Panagiotou M., Xinaris C., Tzeis S., Kokkinos A.D., and Cokkinos D.V. Enhanced tolerance of the rat myocardium to ischemia and reperfusion injury early after acute myocardial infarction. Basic Res. Cardiol. 102 4 (2007) 327-333
40. Pantos C., Mourouzis I., Markakis K., Dimopoulos A., Xinaris C., Kokkinos A.D., Panagiotou M., and Cokkinos D.V. Thyroid hormone attenuates cardiac remodeling and improves hemodynamics early after acute myocardial infarction in rats. Eur. J. Cardiothorac. Surg. 32 2 (2007) 333-339
41. Pantos C., Mourouzis I., Markakis K., Tsagoulis N., Panagiotou M., and Cokkinos D.V. Long-term thyroid hormone administration re-shapes left ventricular chamber and improves cardiac function after myocardial infarction in rats. Basic Res. Cardiol. 103 4 (2008) 308-318
42. Pantos C., Mourouzis I., Saranteas T., Clave G., Ligeret H., Noack-Fraissignes P., Renard P.Y., Massonneau M., Perimenis P., Spanou D., Kostopanagiotou G., and Cokkinos D.V. Thyroid hormone improves postischaemic recovery of function while limiting apoptosis: a new therapeutic approach to support hemodynamics in the setting of ischaemia-reperfusion?. Basic Res. Cardiol. 104 1 (2009) 69-77
43. Pantos C., Mourouzis I., Tsagoulis N., Markakis K., Galanopoulos G., Roukounakis N., Perimenis P., Liappas A., and Cokkinos D.V. Thyroid hormone at supra-physiological dose optimizes cardiac geometry and improves cardiac function in rats with old myocardial infarction. J. Physiol. Pharmacol. 60 3 (2009) 49-56
44. Pantos C., Mourouzis I., Tzeis S., Moraitis P., Malliopoulou V., Cokkinos D.D., Carageorgiou H., Varonos D., and Cokkinos D. Dobutamine administration exacerbates postischaemic myocardial dysfunction in isolated rat hearts: an effect reversed by thyroxine pretreatment. Eur. J. Pharmacol. 460 2-3 (2003) 155-161
45. Pantos C., Xinaris C., Mourouzis I., Malliopoulou V., Kardami E., and Cokkinos D.V. Thyroid hormone changes cardiomyocyte shape and geometry via ERK signaling pathway: potential therapeutic implications in reversing cardiac remodeling?. Mol. Cell. Biochem. 297 1-2 (2007) 65-72
46. Pantos C., Xinaris C., Mourouzis I., Perimenis P., Politi E., Spanou D., and Cokkinos D.V. Thyroid hormone receptor alpha 1: a switch to cardiac cell "metamorphosis"?. J. Physiol. Pharmacol. 59 2 (2008) 253-269
47. Pantos C.I., Malliopoulou V.A., Mourouzis I.S., Karamanoli E.P., Paizis I.A., Steimberg N., Varonos D.D., and Cokkinos D.V. Long-term thyroxine administration protects the heart in a pattern similar to ischemic preconditioning. Thyroid 12 4 (2002) 325-329
48. Pantos C.I., Malliopoulou V.A., Mourouzis I.S., Karamanoli E.P., Tzeis S.M., Carageorgiou H.C., Varonos D.D., and Cokkinos D.V. Long-term thyroxine administration increases heat stress protein-70 mRNA expression and attenuates p38 MAP kinase activity in response to ischaemia. J. Endocrinol. 170 1 (2001) 207-215
49. Pennock G.D., Spooner P.H., Summers C.E., and Litwin S.E. Prevention of abnormal sarcoplasmic reticulum calcium transport and protein expression in post-infarction heart failure using 3,5-diiodothyropropionic acid (DITPA). J. Mol. Cell. Cardiol. 32 11 (2000) 1939-1953
50. Pingitore A., Galli E., Barison A., Iervasi A., Scarlattini M., Nucci D., L'Abbate A., Mariotti R., and Iervasi G. 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. 93 4 (2008) 1351-1358
51. Pingitore A., Iervasi G., Barison A., Prontera C., Pratali L., Emdin M., Giannessi D., and Neglia D. Early activation of an altered thyroid hormone profile in asymptomatic or mildly symptomatic idiopathic left ventricular dysfunction. J. Card. Fail. 12 7 (2006) 520-526
52. Pingitore A., Landi P., Taddei M.C., Ripoli A., L'Abbate A., and Iervasi G. Triiodothyronine levels for risk stratification of patients with chronic heart failure. Am. J. Med. 118 2 (2005) 132-136
53. Ranasinghe A.M., Quinn D.W., Pagano D., Edwards N., Faroqui M., Graham T.R., Keogh B.E., Mascaro J., Riddington D.W., Rooney S.J., Townend J.N., Wilson I.C., and Bonser R.S. Glucose-insulin-potassium and tri-iodothyronine individually improve hemodynamic performance and are associated with reduced troponin I release after on-pump coronary artery bypass grafting. Circulation 114 1 Suppl (2006) I245-I250
54. Sakamoto K., Urushidani T., and Nagao T. Translocation of HSP27 to sarcomere induced by ischemic preconditioning in isolated rat hearts. Biochem. Biophys. Res. Commun. 269 1 (2000) 137-142
55. Scruggs S.B., Walker L.A., Lyu T., Geenen D.L., Solaro R.J., Buttrick P.M., and Goldspink P.H. Partial replacement of cardiac troponin I with a non-phosphorylatable mutant at serines 43/45 attenuates the contractile dysfunction associated with PKCepsilon phosphorylation. J. Mol. Cell. Cardiol. 40 4 (2006) 465-473
56. Spinale F.G. Cellular and molecular therapeutic targets for treatment of contractile dysfunction after cardioplegic arrest. Ann. Thorac. Surg. 68 5 (1999) 1934-1941
57. Tomanek R.J., Doty M.K., and Sandra A. Early coronary angiogenesis in response to thyroxine: growth characteristics and upregulation of basic fibroblast growth factor. Circ. Res. 82 5 (1998) 587-593
58. Walker J.D., Crawford Jr. F.A., and Spinale F.G. 3,5,3′ Triiodo-l-thyronine pretreatment with cardioplegic arrest and chronic left ventricular dysfunction. Ann. Thorac. Surg. 60 2 (1995) 292-299
59. Wong K., Boheler K.R., Petrou M., and Yacoub M.H. Pharmacological modulation of pressure-overload cardiac hypertrophy: changes in ventricular function, extracellular matrix, and gene expression. Circulation 96 7 (1997) 2239-2246
60. Xinaris, C., Mourouzis, I., Carageorgiou, H., Pantos, C., and Cokkinos, D. V. 2006a. Differential activation of stress kinase signaling by phenylephrine and thyroid hormone in neonatal cardiomyocytes. J. Mol. Cell. Cardiol. 40999.
61. Xinaris, C., Mourouzis, I., Pantos, C., and Cokkinos, D. V. 2006b. Thyroid hormone promotes cardiac myocyte plasticity via activation of stress kinase signalling. J. Mol. Cell. Cardiol. 40(6), 218 (Abstract).
62. Yao J., and Eghbali M. Decreased collagen gene expression and absence of fibrosis in thyroid hormone-induced myocardial hypertrophy. Response of cardiac fibroblasts to thyroid hormone in vitro. Circ. Res. 71 4 (1992) 831-839
63. Ziegelhoffer-Mihalovicova B., Briest W., Baba H.A., Rassler B., and Zimmer H.G. The expression of mRNA of cytokines and of extracellular matrix proteins in triiodothyronine-treated rat hearts. Mol. Cell. Biochem. 247 1-2 (2003) 61-68
64. Zinman T., Shneyvays V., Tribulova N., Manoach M., and Shainberg A. Acute, nongenomic effect of thyroid hormones in preventing calcium overload in newborn rat cardiocytes. J. Cell. Physiol. 207 1 (2006) 220-231