Longstanding Hyperthyroidism Is Associated with Normal or Enhanced Intrinsic Cardiomyocyte Function despite Decline in Global Cardiac Function

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Weltman, Nathan Y ^a   Wang, Dajun ^b   Redetzke, Rebecca A ^b   Gerdes, A Martin ^c  

^a UNIVERSITY OF SOUTH DAKOTA   (United States)

^b UNIVERSITY OF SOUTH DAKOTA   (United States)

^c NEW YORK INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

THYROID HORMONE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL FUNCTION; CELL STRUCTURE; CHRONIC HYPERTHYROIDISM; CONTROLLED STUDY; DIASTOLIC DYSFUNCTION; DISEASE DURATION; ECHOCARDIOGRAPHY; HEART DILATATION; HEART FUNCTION; HEART HEMODYNAMICS; HEART LEFT VENTRICLE FUNCTION; HEART MUSCLE CELL; HEART MUSCLE FIBROSIS; HEART VENTRICLE HYPERTROPHY; HYPERTHYROIDISM; NONHUMAN; SYSTOLIC DYSFUNCTION; WALL STRESS;

ANIMALS; CARDIOMEGALY; CELLS, CULTURED; CRICETINAE; ECHOCARDIOGRAPHY; HYPERTHYROIDISM; MYOCYTES, CARDIAC; THYROID HORMONES; VENTRICULAR REMODELING;

CRICETINAE;

EID: 84867135272     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0046655     Document Type: Article

References (71)

1. Klein I, Ojamaa K, (2001) Mechanisms of disease: Thyroid hormone and the cardiovascular system. New England Journal of Medicine 344: 501-509.
2. Gerdes AM, Iervasi G, (2010) Thyroid replacement therapy and heart failure. Circulation 122: 385-393.
3. Ojamaa K, Kenessey A, Klein I, (2000) Thyroid hormone regulation of phospholamban phosphorylation in the rat heart. Endocrinology 141: 2139-2144.
4. Shenoy R, Klein I, Ojamaa K, (2001) Differential regulation of SR calcium transporters by thyroid hormone in rat atria and ventricles. American Journal of Physiology-Heart and Circulatory Physiology 281: H1690-H1696.
5. Gomberg-Maitland M, Frishman WH, (1998) Thyroid hormone and cardiovascular disease. American Heart Journal 135: 187-196.
6. Degens H, Gilde AJ, Lindhout M, Willemsen PHM, Van der Vusse GJ, et al. (2003) Functional and metabolic adaptation of the heart to prolonged thyroid hormone treatment. American Journal of Physiology-Heart and Circulatory Physiology 284: H108-H115.
7. Gerdes AM, A MJ, P BS, (1985) Failure of propranolol to prevent chronic hyperthyroid induced cardiac hypertrophy and multifocal cellular necrosis in the rat. Canadian Journal of Cardiology 1: 340-345.
8. Petretta M, Bonaduce D, Spinelli L, Vicario MLE, Nuzzo V, et al. (2001) Cardiovascular haemodynamics and cardiac autonomic control in patients with subclinical and overt hyperthyroidism. European Journal of Endocrinology 145: 691-696.
9. Dorr M, Wolff B, Robinson DM, John U, Ludemann J, et al. (2005) The association of thyroid function with cardiac mass and left ventricular hypertrophy. Journal of Clinical Endocrinology & Metabolism 90: 673-677.
10. Biondi B, Fazio S, Cuocolo A, Sabatini D, Nicolai E, et al. (1996) Impaired cardiac reserve and exercise capacity in patients receiving long-term thyrotropin suppressive therapy with levothyroxine. Journal of Clinical Endocrinology & Metabolism 81: 4224-4228.
11. Sawin CT, Geller A, Wolf PA, Belanger AJ, Baker E, et al. (1994) Low serum thyrotropin concentrations as a risk factor for atrial fibrillation in older persons. New England Journal of Medicine 331: 1249-1252.
12. Biondi B, Fazio S, Carella C, Amato G, Cittadini A, et al. (1993) Cardiac effects of long-term thyrotropin-suppressive therapy with levothyroxine. Journal of Clinical Endocrinology & Metabolism 77: 334-338.
13. Shirani J, Barron MM, Pierrelouis MLY, Roberts WC, (1993) Congestive heart failure, dilated cardiac ventricules, and sudden death in hyperthyroidism. American Journal of Cardiology 72: 365-368.
14. Woeber KA, (1992) Current concepts- thyrotoxicosis and the heart. New England Journal of Medicine 327: 94-98.
15. Khandwala HM, (2004) A case of congestive heart failure due to reversible dilated cardiomyopdthy caused by hyperthyroidism. Southern Medical Journal 97: 1001-1003.
16. Riaz K, Forker AD, Isley WL, Hamburg MS, McCullough PA, (2003) Hyperthyroidism: a "curable" cause of congestive heart failure-three case reports and a review of the literature. Congestive heart failure (Greenwich, Conn) 9: 40-46.
17. Watanabe E, Ohsawa H, Noike H, Okamoto K, Tokuyama A, et al. (1995) Dilated cardiomyopathy associated with hyperthyroidism. Internal Medicine 34: 762-767.
18. Smit JWA, Eustatia-Rutten CFA, Corssmit EPM, Pereira AM, Frolich M, et al. (2005) Reversible diastolic dysfunction after long-term exogenous subclinical hyperthyroidism: A randomized, placebo-controlled study. Journal of Clinical Endocrinology & Metabolism 90: 6041-6047.
19. Kuzman JA, Thomas TA, Vogelsang KA, Said S, Anderson BE, et al. (2005) Effects of induced hyperthyroidism in normal and cardiomyopathic hamsters. Journal of Applied Physiology 99: 1428-1433.
20. Savinova OV, Liu YH, Aasen GA, Mao K, Weltman NY, et al. (2011) Thyroid hormone promotes remodeling of coronary resistance vessels. Plos One 6.
21. Tamura T, Said S, Harris J, Lu WY, Gerdes AM, (2000) Reverse remodeling of cardiac myocyte hypertrophy in hypertension and failure by targeting of the renin-angiotensin system. Circulation 102: 253-259.
22. Zimmer HG GA, Lortet S, Mall G, (1990) Changes in heart function and cardiac cell size in rats with chronic myocardial infarction. Journal of Molecular and Cellular Cardiology 22: 1231-1243.
23. Litwin SE, Katz SE, Weinberg EO, Lorell BH, Aurigemma GP, et al. (1995) Serial echocardiographic-Doppler assessment of left ventricular geometry and function in rats with pressure-overload hypertrophy. Chronic angiotensin-converting enzyme inhibition attenuates the transition to heart failure. Circulation 91: 2642-2654.
24. Ren J, Wold L, (2001) Measurement of cardiac mechanical function in isolated ventricular myocytes from rats and mice by computerized video-based imaging. Biological Procedures Online 3: 43-53.
25. Colligan PB, Brown-Borg HM, J D, B.H R, Ren J, (2002) Cardiac contractile function is enhanced in isolated ventricular myocytes from growth hormone transgenic mice. Journal of Endocrinology 173: 257-264.
26. Schlenker EH, Burbach JA, Singh YN, (2000) Effects of thyroxine and naloxone administration on metabolism and ventilation in hamsters. Respiration Physiology 123: 63-70.
27. Klein I, Hong C, (1986) Effects of thyroid hormone on cardiac size and myosin content of the heterotopically transplanted rat heart. Journal of Clinical Investigation 77: 1694-1698.
28. Gerdes AM, (2002) Cardiac myocyte remodeling in hypertrophy and progression to failure. Journal of Cardiac Failure 8: S264-S268.
29. Campell S, Gerdes A, (1988) Regional changes in myocyte size and number in thyroid-induced cardiac hypertrophy. Journal of Molecular and Cellular Cardiology 20: 379-387.
30. Grossman W, Jones D, McLaurin L, (1975) Wall stress and patterns of hypertrophy in the human left ventricle. Journal of Clinical Investigation 56: 56-64.
31. Brower GL, Gardner JD, Forman MF, Murray DB, Voloshenyuk T, et al. (2006) The relationship between myocardial extracellular matrix remodeling and ventricular function. European Journal of Cardio-Thoracic Surgery 30: 604-610.
32. Tamura T, Onodera T, Said S, Gerdes AM, (1998) Correlation of myocyte lengthening to chamber dilation in the spontaneously hypertensive heart failure (SHHF) rat. Journal of Molecular and Cellular Cardiology 30: 2175-2181.
33. Gerdes AM, Kellerman SE, Moore JA, Muffly KE, Clark LC, et al. (1992) Structural remodeling of cardiac myocytes in patients with ischemic cardiomyopathy. Circulation 86: 426-430.
34. Wold LE, Saari JT, Ren J, (2001) Isolated ventricular myocytes from copper-deficient rat hearts exhibit enhanced contractile function. American Journal of Physiology-Heart and Circulatory Physiology 281: H476-H481.
35. Giraud MN, Liechti EF, Tchantchaleishvili V, Siepe M, Cook S, et al. (2010) Myocardial injection of skeletal myoblasts impairs contractility of host cardiomyocytes. International Journal of Cardiology 138: 131-137.
36. Song LS, Pi Y, Kim SJ, Yatani A, Guatimosim S, et al. (2005) Paradoxical cellular Ca2+ signaling in severe but compensated canine left ventricular hypertrophy. Circulation Research 97: 457-464.
37. Anand IS, Liu DS, Chugh SS, Prahash AJC, Gupta S, et al. (1997) Isolated myocyte contractile function is normal in postinfarct remodeled rat heart with systolic dysfunction. Circulation 96: 3974-3984.
38. Chandrashekhar Y, Prahash AJ, Sen S, Gupta S, Anand IS, (1999) Cardiomyocytes from hearts with left ventricular dysfunction after ischemia-reperfusion do not manifest contractile abnormalities. Journal of the American College of Cardiology 34: 594-602.
39. Mackiewicz U, Czarnowska E, Brudek M, Pajak B, Duda M, et al. (2012) Preserved cardiomyocyte function and altered desmin pattern in transgenic mouse model of dilated cardiomyopathy. Journal of Molecular and Cellular Cardiology 52: 978-987.
40. Park M, Shen YT, Gaussin V, Heyndrickx GR, Bartunek J, et al. (2009) Apoptosis predominates in nonmyocytes in heart failure. American Journal of Physiology-Heart and Circulatory Physiology 297: H785-H791.
41. Gandhi MS, Kamalov G, Shahbaz AU, Bhattacharya SK, Ahokas RA, et al. (2011) Cellular and molecular pathways to myocardial necrosis and replacement fibrosis. Heart Failure Reviews 16: 23-34.
42. Chen Y-F, Kobayashi S, Chen J, Redetzke RA, Said S, et al. (2008) Short term triiodo-L-thyronine treatment inhibits cardiac myocyte apoptosis in border area after myocardial infarction in rats. Journal of Molecular and Cellular Cardiology 44: 180-187.
43. Rodriguez E, Weiss HR, Gonzalez M, Tse J, (1993) Effect of isoproterenol on coronary blood flow and signal transduction responses in thyroxine-treated rabbit hearts. Journal of Molecular and Cellular Cardiology 25: 939-947.
44. Tomanek RJ, Connell PM, Butters CA, Torry RJ, (1995) Compensated coronary microvascular growth in senescent rats with thyroxine-induced cardiac hypertrophy. American Journal of Physiology-Heart and Circulatory Physiology 268: H419-H425.
45. Tomanek RJ, Busch TL, (1998) Coordinated capillary and myocardial growth in response to thyroxine treatment. Anatomical Record 251: 44-49.
46. Marcus ML, Harrison DG, Chilian WM, Koyanagi S, Inou T, et al. (1987) Alterations in the coronary circulation in hypertrophied ventricles. Circulation 75(supplement 1): 1-19.
47. Swynghedauw B, (1999) Molecular mechanisms of myocardial remodeling. Physiological Reviews 79: 215-262.
48. Hein S, Arnon E, Kostin S, Schonburg M, Elsasser A, et al. (2003) Progression from compensated hypertrophy to failure in the pressure-overloaded human heart- Structural deterioration and compensatory mechanisms. Circulation 107: 984-991.
49. Heling A, Zimmermann R, Kostin S, Maeno Y, Hein S, et al. (2000) Increased expression of cytoskeletal, linkage, and extracellular proteins in failing human myocardium. Circulation Research 86: 846-853.
50. Magner JA, Clark W, Allenby P, (1988) Congestive heart failure and sudden death in a young woman with thyrotoxicosis. West J Med 149: 86-91.
51. Lewis W, (1932) The question of a specific myocardial lesion in hyperthyroidism (Basedow's disease). American Journal of Pathology 8: 255-261.
52. Schlesinger P, Benchimol AB, (1958) The Pure form of thyrotoxic heart disease. American Journal of Cardiology 2: 430-440.
53. Yao JL, Eghbali M, (1992) Decreased collagen gene expression and absence of fibrosis in thyroid hormone induced myocardial hypertrophy- response of cardiac fibroblasts to thyroid hormone in vitro. Circulation Research 71: 831-839.
54. Roy SG, Mishra S, Ghosh G, Bandyopadhyay A, (2007) Thyroid hormone induces myocardial matrix degradation by activating matrix metalloproteinase-1. Matrix Biology 26: 269-279.
55. Ziegelhoffer-Mihalovicova B, Briest W, Baba HA, Rassler B, Zimmer HG, (2003) The expression of mRNA of cytokines and of extracellular matrix proteins in triiodothyronine-treated rat hearts. Molecular and Cellular Biochemistry 247: 61-68.
56. Chen WJ, Lin KH, Lee YS, (2000) Molecular characterization of myocardial fibrosis during hypothyroidism: evidence for negative regulation of the pro-alpha 1(I) collagen gene expression by thyroid hormone receptor. Molecular and Cellular Endocrinology 162: 45-55.
57. Lee HW, Klein LE, Raser J, Eghbali-Webb M, (1998) An activator protein-1 (AP-1) response element on pro alpha(1)(I) collagen gene is necessary for thyroid hormone-induced inhibition of promoter activity in cardiac fibroblasts. Journal of Molecular and Cellular Cardiology 30: 2495-2506.
58. Fatourechi V, Edwards WD, (2000) Graves' disease and low-output cardiac dysfunction: Implications for autoimmune disease in endomyocardial biopsy tissue from eleven patients. Thyroid 10: 601-605.
59. Wang YY, Jiao B, Guo WG, Che HL, Yu ZB, (2010) Excessive thyroxine enhances susceptibility to apoptosis and decreases contractility of cardiomyocytes. Molecular and Cellular Endocrinology 320: 67-75.
60. Zierhut W, (1989) Differential effects of triiodothyronine on rat left and right ventricular function and the influence of metoprolol. Journal of Molecular and Cellular Cardiology 21: 617-624.
61. Araujo ASR, Ribeiro MFM, Enzveiler A, Schenkel P, Fernandes TRG, et al. (2006) Myocardial antioxidant enzyme activities and concentration and glutathione metabolism in experimental hyperthyroidism. Molecular and Cellular Endocrinology 249: 133-139.
62. Araujo ASR, Diniz GP, Seibel FER, Branchini G, Ribeiro MFM, et al. (2011) Reactive oxygen and nitrogen species balance in the determination of thyroid hormones-induced cardiac hypertrophy mediated by renin-angiotensin system. Molecular and Cellular Endocrinology 333: 78-84.
63. Civelek S, Seymen K, Seven A, Yigit G, Hatemi H, et al. (2001) Oxidative stress in heart tissue of hyperthyroid and iron supplemented rats. Journal of Toxicology and Environmental Health-Part A 64: 499-506.
64. Araujo ASR, Schenkel P, Enzveiler AT, Fernandes TRG, Partata WA, et al. (2008) The role of redox signaling in cardiac hypertrophy induced by experimental hyperthyroidism. Journal of Molecular Endocrinology 41: 423-430.
65. Johar S, Cave AC, Narayanapanicker A, Grieve DJ, Shah AM, (2006) Aldosterone mediates angiotensin II-induced interstitial cardiac fibrosis via a Nox2-containing NADPH oxidase. Faseb Journal 20: 1546-1548.
66. Aragno M, Mastrocola R, Alloatti G, Vercellinatto I, Bardini P, et al. (2008) Oxidative Stress Triggers Cardiac Fibrosis in the Heart of Diabetic Rats. Endocrinology 149: 380-388.
67. Maulik SK, Kumar S, (2012) Oxidative stress and cardiac hypertrophy: a review. Toxicology Mechanisms and Methods 22: 359-366.
68. Tsutsui H, Ide T, Kinugawai S, (2006) Mitochondrial oxidative stress, DNA damage, and heart failure. Antioxidants & Redox Signaling 8: 1737-1744.
69. Wheatley AM, Marcus RH, Lippe IT, Rosendorff C, (1988) Enhanced myocardial contractility but not tachycardia persists in isolated working hyperthyroid rat hearts. Basic Research in Cardiology 83: 634-646.
70. Robinson TF, Geraci MA, Sonnenblick EH, Factor SM, (1988) Coiled perimysial fibers of papillary muscle in rat heart: morphology, distribution, and changes in configuration. circulation Research 63: 577-592.
71. Brady AJ, (1991) Mechanical Properties of Isolated Cardiac Myocytes. Physiological Reviews 71: 413-428.