Hostname: page-component-8448b6f56d-t5pn6 Total loading time: 0 Render date: 2024-04-18T01:37:13.569Z Has data issue: false hasContentIssue false

Thyroid hormone in the frontier of cell protection, survival and functional recovery

Published online by Cambridge University Press:  25 May 2015

Luis A. Videla*
Affiliation:
Molecular and Clinical Pharmacology Program, Institute of Biomedical Sciences, Faculty of Medicine, University of Chile, Santiago, Chile
Virginia Fernández
Affiliation:
Molecular and Clinical Pharmacology Program, Institute of Biomedical Sciences, Faculty of Medicine, University of Chile, Santiago, Chile
Pamela Cornejo
Affiliation:
School of Medical Technology, Faculty of Health and Odontology, Diego Portales University, Santiago, Chile
Romina Vargas
Affiliation:
Molecular and Clinical Pharmacology Program, Institute of Biomedical Sciences, Faculty of Medicine, University of Chile, Santiago, Chile
Iván Castillo
Affiliation:
School of Medicine, Faculty of Medicine, Catholic University of Maule, Talca, Chile
*
*Corresponding author: Luis A. Videla, Molecular and Clinical Pharmacology Program, Institute of Biomedical Sciences, Faculty of Medicine, University of Chile, Santiago, Chile. E-mail: lvidela@med.uchile.cl

Abstract

Thyroid hormone (TH) exerts important actions on cellular energy metabolism, accelerating O2 consumption with consequent reactive oxygen species (ROS) generation and redox signalling affording cell protection, a response that is contributed by redox-independent mechanisms. These processes underlie genomic and non-genomic pathways, which are integrated and exhibit hierarchical organisation. ROS production led to the activation of the redox-sensitive transcription factors nuclear factor-κB, signal transducer and activator of transcription 3, activating protein 1 and nuclear factor erythroid 2-related factor 2, promoting cell protection and survival by TH. These features involve enhancement in the homeostatic potential including antioxidant, antiapoptotic, antiinflammatory and cell proliferation responses, besides higher detoxification capabilities and energy supply through AMP-activated protein kinase upregulation. The above aspects constitute the molecular basis for TH-induced preconditioning of the liver that exerts protection against ischemia-reperfusion injury, a strategy also observed in extrahepatic organs of experimental animals and with other types of injury, which awaits application in the clinical setting. Noteworthy, re-adjusting TH to normal levels results in several beneficial effects; for example, it lengthens the cold storage time of organs for transplantation from brain-dead donors; allows a superior neurological outcome in infants of <28 weeks of gestation; reduces the cognitive side-effects of lithium and improves electroconvulsive therapy in patients with bipolar disorders.

Type
Review Article
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1. Oetting, A. and Yen, P.M. (2007) New insights into thyroid hormone action. Best Practice Research Clinical Endocrinology and Metabolism 21, 193-208 CrossRefGoogle ScholarPubMed
2. Mullur, R., Liu, Y.-Y. and Brent, G.A. (2014) Thyroid hormone regulation of metabolism. Physiological Reviews 94, 355-382 CrossRefGoogle ScholarPubMed
3. Calabrese, E.J. (2008) Converging concepts: adaptive response, preconditioning, and the Yerkes-Dodson law manifestations of hormesis. Ageing Research Reviews 7, 8-20 CrossRefGoogle ScholarPubMed
4. Videla, L.A. (2010) Hormetic responses of thyroid hormone calorigenesis in the liver: association with oxidative stress. IUBMB Life 62, 460-466 CrossRefGoogle ScholarPubMed
5. Bernardes, S.S. et al. (2014) Reactive oxygen species play a role in muscle wasting during thyrotoxicosis. Cell and Tissue Research 357, 803-814 CrossRefGoogle ScholarPubMed
6. Mourouzis, I., Politi, E. and Pantos, C. (2013) Thyroid hormone and tissue repair: new tricks for an old hormone? Journal of Thyroid Research Article ID 312104, 1-5 doi:10.1155/2013/312104 CrossRefGoogle ScholarPubMed
7. Fernández, V. et al. (2007) Thyroid hormone preconditioning: protection against ischemia-reperfusion liver injury in the rat. Hepatology 45, 170-177 CrossRefGoogle ScholarPubMed
8. Selzner, N., Boehnert, M. and Selzner, M. (2012) Preconditioning, postconditioning, and remote conditioning in solid organ transplantation: basic mechanisms and translational applications. Transplantation Reviews 26, 115-124 CrossRefGoogle ScholarPubMed
9. D'Espessailles, A. et al. (2013) Hormonal pretreatment preserves liver regenerative capacity and minimizes inflammation after partial hepatectomy. Annals of Hepatology 12, 881-891 CrossRefGoogle ScholarPubMed
10. van Wassenaer, A.G. and Kok, J.H. (2008) Trials with thyroid hormone in preterm infants: clinical and neurodevelopmental effects. Seminars in Perinatology 32, 423-430 CrossRefGoogle ScholarPubMed
11. Tremont, G., Stern, R.A. (2000) Minimizing the cognitive effects of lithium and electroconvulsive therapy using thyroid hormone. International Journal of Neuropsychopharmacology 3, 175-186 CrossRefGoogle ScholarPubMed
12. Cooper, D.C.K. et al. (2009) A review of studies relating thyroid hormone therapy in brain-dead organ donors. Frontiers in Bioscience 14, 3750-3770 CrossRefGoogle ScholarPubMed
13. Dikdan, G.S., Mora-Esteves, C. and Koneru, B. (2012) Review of randomized clinical trials of donor management and organ preservation in deceased donors: opportunities and issues. Transplantation 94, 425-441 CrossRefGoogle ScholarPubMed
14. Mi, Z. et al. (2015) The optimal hormonal replacement modality selection for multiple organ procurement from brain-dead organ donors. Clinical Epidemiology 7, 17-27 Google ScholarPubMed
15. Oppenheimer, J.H., Schwartz, H.L. and Surks, M.I. (1974) Tissue differences in the concentration of triiodothyronine nuclear binding sites in the rat: liver, kidney, pituitary, heart, brain, spleen, and testis. Endocrinology 95, 897-903 CrossRefGoogle ScholarPubMed
16. Lanni, A. et al. (2003) Thyroid hormone and uncoupling proteins. FEBS Letters 543, 5-10 CrossRefGoogle ScholarPubMed
17. Fernández, V. and Videla, L.A. (1993) Influence of hyperthyroidism on superoxide radical and hydrogen peroxide production by rat liver submitochondrial particles. Free Radical Research Communications 18, 329-335 CrossRefGoogle ScholarPubMed
18. Venditti, P., De Rosa, R. and Di Meo, S. (2003) Effect of thyroid state on H2O2 production by rat liver mitochondria. Molecular and Cellular Endocrinology 205, 185-192 CrossRefGoogle ScholarPubMed
19. Davis, P.J., Leonard, J.L. and Davis, F.B. (2008) Mechanisms of nongenomic actions of thyroid hormone. Frontiers in Neuroendocrinology 29, 211-218 CrossRefGoogle ScholarPubMed
20. Arnold, S., Goglia, F. and Kadenbach, B. (1998) 3,4-Diiodothyronine binds to subunit Va of cytochrome-c oxidase and abolishes the allosteric inhibition of respiration by ATP. European Journal of Biochemistry 252, 325-330 CrossRefGoogle ScholarPubMed
21. Fernández, V. et al. (2003) Effects of γ-hexachlorocyclohexane and L-3,3,5-triiodothyronine on rat liver cytochrome P4502E1-dependent activity and content in relation to microsomal superoxide radical generation. Biological Research 36, 359-365 CrossRefGoogle Scholar
22. Ram, P.A. and Waxman, D.J. (1992) Thyroid hormone stimulation of NADPH P450 reductase expression in liver and extrahepatic tissues. Journal of Biological Chemistry 267, 3294-3301 CrossRefGoogle ScholarPubMed
23. Fernández, V. et al. (1985) Superoxide radical generation, NADPH oxidase activity, and cytochrome P450 content in an experimental hyperthyroid state: relation to lipid peroxidation. Endocrinology 117, 496-501 CrossRefGoogle Scholar
24. Simon-Giavarotti, K.A. et al. (1998) Liver microsomal parameters related to oxidative stress and antioxidant systems in hyperthyroid rats subjected to acute lindane treatment. Free Radical Research 29, 35-42 CrossRefGoogle ScholarPubMed
25. Huh, K. et al. (1998) Role of the hepatic xanthine oxidase in thyroid dysfunction: effect of thyroid hormones in oxidative stress in rat liver. Archives of Pharmaceutical Research 21, 236-240 CrossRefGoogle ScholarPubMed
26. Just, W.W. and Hartl, F.U. (1983) Rat liver peroxisomes. II. Stimulation of peroxisomal fatty-acid beta-oxidation by thyroid hormones. Hoppe-Seyler's Zeitschrift fur Physiologische Chemie 364, 1541-1547 CrossRefGoogle ScholarPubMed
27. Tapia, G. et al. (1997) Kupffer cell function in thyroid hormone-induced liver oxidative stress in the rat. Free Radical Research 26, 267-279 Google ScholarPubMed
28. Forman, H.J., Maiorino, M. and Ursini, F. (2010) Signaling functions of reactive oxygen species. Biochemistry 49, 835-842 CrossRefGoogle ScholarPubMed
29. Videla, L.A. (2009) Oxidative stress signaling underlying liver disease and hepatoprotective mechanisms. World Journal of Hepatology 1, 73-79 CrossRefGoogle ScholarPubMed
30. Bilzer, M., Roggel, F. and Gerbes, A.L. (2006) Role of Kupffer cells in host defense and liver disease. Liver International 26, 1175-1186 CrossRefGoogle ScholarPubMed
31. Gomes, L.F. et al. (2004) Triiodothyronine differentially induces Kupffer cell ERD1/ED2 subpopulations. Molecular Aspects of Medicine 25, 183-190 CrossRefGoogle Scholar
32. Sellitti, D.F., Oliver, C. and Latham, K.R. (1985) Antibodies to nuclear thyroid hormone-binding proteins. Antibody characterization and immunofluorescent localization. Experimental Cell Research 158, 223-236 CrossRefGoogle ScholarPubMed
33. Tapia, G. et al. (2003) Thyroid hormone-induced oxidative stress triggers nuclear factor-κB activation and cytokine gene expression in rat liver. Free Radical Biology and Medicine 35, 257-265 CrossRefGoogle ScholarPubMed
34. Tapia, G. et al. (2006) The acute-phase response of the liver in relation to thyroid hormone-induced redox signaling. Free Radical Biology and Medicine 40, 1628-1635 CrossRefGoogle ScholarPubMed
35. Fernández, V. et al. (2007) Involvement of Kupffer cell-dependent signaling in T3-induced hepatocyte proliferation in vivo . Biological Chemistry 388, 831-837 CrossRefGoogle ScholarPubMed
36. Troncoso, P., Smok, G. and Videla, L.A. (1997) Potentiation of ischemia-reperfusion liver injury by hyperthyroidism in the rat. Free Radical Biology and Medicine 23, 19-25 CrossRefGoogle ScholarPubMed
37. Videla, L.A. et al. (1995) Influence of hyperthyroidism on lindane-induced hepatotoxicity in the rat. Biochemical Pharmacology 50, 1557-1565 CrossRefGoogle ScholarPubMed
38. Venditti, P. and Di Meo, S. (2006) Thyroid hormone-induced oxidative stress. Cellular and Molecular Life Sciences 63, 414-434 CrossRefGoogle ScholarPubMed
39. Tran-Thi, T.A., Decker, K. and Baeuerle, P.A. (1995) Differential activation of transcription factors NF-κB an AP-1 in rat liver macrophages. Hepatology 22, 613-619 CrossRefGoogle ScholarPubMed
40. Vrba, J. and Modriansky, M. (2002) Oxidative burst of Kupffer cells: target for liver injury treatment. Biomedical Papers 146, 15-20 CrossRefGoogle ScholarPubMed
41. Tsukamoto, H. (2002) Redox regulation of cytokine expression in Kupffer cells. Antioxidants and Redox Signaling 4, 741-748 CrossRefGoogle ScholarPubMed
42. Hayden, M.S. and Ghosh, S. (2004) Signaling to NF-κB. Genes and Development 18, 2195-2224 CrossRefGoogle ScholarPubMed
43. Fernández, V. et al. (2005) Redox regulation of thyroid hormone-induced Kupffer cell-dependent IκB-α phosphorylation in relation to inducible nitric oxide synthase expression. Free Radical Research 39, 411-418 CrossRefGoogle ScholarPubMed
44. Fernández, V. et al. (2005) Redox up-regulated expression of rat liver manganese superoxide dismutase and Bcl2 by thyroid hormone is associated with inhibitor of κB-α phosphorylation and nuclear factor-κB activation. Journal of Endocrinology 186, 539-547 CrossRefGoogle ScholarPubMed
45. Nandakumar, D.N. et al. (2008) Activation of NF-κB in lymphocytes and increase in serum immunoglobulin in hyperthyroidism: possible role of oxidative stress. Immunobiology 213, 409-415 CrossRefGoogle ScholarPubMed
46. Samols, D., Agrawal, A. and Krushner, I. (2003) Acute phase proteins. In Cytokine Reference On-Line (Oppenheim, J.J. and Feldman, M., eds), pp. 1-16, Academic Press, London Google Scholar
47. Gruys, E. et al. (2005) Acute phase reaction and acute phase proteins. Journal of Zhejiant University Science 6B, 1045-1056 CrossRefGoogle Scholar
48. Erns, M. and Jenkins, B.J. (2004) Acquiring signaling specificity from the cytokine receptor gp130. Trends in Genetics 20, 23-32 CrossRefGoogle Scholar
49. Griffin, E.E. and Miller, L.L. (1973) Effects of hypothyroidism, hyperthyroidism, and thyroxine on net synthesis of plasma proteins by the isolated perfused rat liver. Journal of Biological Chemistry 248, 4716-4723 CrossRefGoogle ScholarPubMed
50. Fitch, C.A., Song, Y. and Leversom, C.W. (1999) Developmental regulation of hepatic ceruloplasmin mRNA and serum activity by exogenous thyroxine and dexamethasone. Proceedings of the Society for Experimental Biology and Medicine 221, 27-31 CrossRefGoogle ScholarPubMed
51. Lin, K.H. et al. (2003) Plasma protein regulation of thyroid hormone. Journal of Endocrinology 179, 367-377 CrossRefGoogle ScholarPubMed
52. Leedman, P.J. et al. (1996) Thyroid hormone modulates the interaction between iron regulatory proteins and the ferritin mRNA iron-responsive element. Journal of Biological Chemistry 271, 12017-12023 CrossRefGoogle ScholarPubMed
53. Francavilla, A. et al. (1994) Hepatocyte proliferation and gene expression induced by triiodothyronine in vivo and in vitro. Hepatology 20, 13237-13241 Google ScholarPubMed
54. Bungay, A. et al. (2008) Microarray analysis of mitogenic effects of T3 on the rat liver. Journal of Gastroenterology and Hepatology 23, 1926-1933 CrossRefGoogle ScholarPubMed
55. Fausto, N., Campbell, J.S. and Riehle, K.J. (2006) Liver regeneration. Hepatology 43, S45-S53 CrossRefGoogle ScholarPubMed
56. Pibiri, M. et al. (2001) Cyclin D1 is an early target in hepatocyte proliferation induced by thyroid hormone (T3). FASEB Journal 15, 1006-1013 CrossRefGoogle ScholarPubMed
57. Fanti, M. et al. (2014) Tri-iodothyronine induces hepatocyte proliferation by protein kinase A-dependent β-catenin activation in rodents. Hepatology 59, 2309-2320 CrossRefGoogle ScholarPubMed
58. Oren, R. et al. (1999) Role of thyroid hormone in stimulating liver repopulation in the rat by transplanted hepatocytes. Hepatology 30, 903-913 CrossRefGoogle ScholarPubMed
59. Ledda-Columbano, G.M. et al. (2000) Cell proliferation induced by triiodothyronine in rat liver is associated with nodule regression and reduction of hepatocellular carcinomas. Cancer Research 60, 603-609 Google ScholarPubMed
60. Taki-Eldin, A. et al. (2012) Triiodothyronine attenuates hepatic ischemia/reperfusion injury in a partial hepatectomy model through inhibition of proinflammatory cytokines, transcription factors, and adhesion molecules. Journal of Surgical Research 178, 646-656 CrossRefGoogle Scholar
61. Gloire, G., Legrand-Poels, S. and Piette, J. (2006) NF-κB activation by reactive oxygen species: fifteen years later. Biochemical Pharmacology 72, 1493-1505 CrossRefGoogle ScholarPubMed
62. Zhang, D.D. (2006) Mechanistic studies of the Nrf2-Keap1 signaling pathway. Drug Metabolism Reviews 38, 769-789 CrossRefGoogle ScholarPubMed
63. Romanque, P. et al. (2011) Thyroid hormone administration induces rat liver Nrf2 activation: suppression by N-acetylcysteine pretreatment. Thyroid 21, 655-662 CrossRefGoogle ScholarPubMed
64. Videla, L.A. et al. (2012) Thyroid hormone-induced cytosol-to-nuclear translocation of rat liver Nrf2 is dependent on Kupffer cell functioning. Scientific World Journal 2012, 1-10, Article ID 301494, doi:10.1100/2012/301494 Google ScholarPubMed
65. Videla, L.A. et al. (2012) Thyroid hormone-induced regulatory interrelations in rat liver Nrf2-Keap1 signaling related to antioxidant enzyme expression. In Advances in Medicine and Biology, vol. 55 (Berhardt, L.V., ed.), pp. 179-191, Nova Science Publishers Inc., New York Google Scholar
66. Cornejo, P., Vargas, R. and Videla, L.A. (2013) Nrf2-regulated phase-II detoxification enzymes and phase-III transporters are induced by thyroid hormone in rat liver. BioFactors 39, 514-521 CrossRefGoogle ScholarPubMed
67. Kurose, K. et al. (2008) Thyroid hormone receptor mediates human MDR1 gene expression. Identification of the response region essential for gene expression. Archives of Biochemistry and Biophysics 474, 82-90 CrossRefGoogle ScholarPubMed
68. Fernández, V. and Videla, L.A. (1989) Thyroid hormone, active oxygen, and lipid peroxidation. In Handbook of Free Radicals and Antioxidants in Biomedicine (Miquel, J., Quintanilha, A.T., and Weber, H., eds), pp. 105-115, CRC Press, Boca Raton Google Scholar
69. O'Connor, P. and Feely, J. (1987) Clinical pharmacokinetics and endocrine disorders. Therapeutic implications. Clinical Pharmacokinetics 13, 345-364 CrossRefGoogle ScholarPubMed
70. Scott, A.K. et al. (1984) Oxazepan pharmacokinetics in thyroid disease. British Journal of Clinical Pharmacology 17, 49-53 CrossRefGoogle Scholar
71. Chopra, J.J. et al. (1992) A radioimmunoassay for measurement of 3,5,3,-triiodothyronine sulfate: studies in thyroidal and non-thyroidal diseases, pregnancy, and neonatal life. Journal of Clinical Endocrinology and Metabolism 75, 189-194 Google Scholar
72. Nishio, N. et al. (2005) Modulation of P-glycoprotein expression in hyperthyroid rat tissues. Drug Metabolism and Disposition 33, 1584-1587 CrossRefGoogle ScholarPubMed
73. Jin, M. et al. (2005) Long-term levothyroxine treatment decreases the oral bioavailability of ciclosporin A by inducing P-glycoprotein in small intestine. Drug Metabolism and Pharmacokinetics 20, 324-330 CrossRefGoogle ScholarPubMed
74. Vessel, E.S. et al. (1975) Altered plasma half-lives of antipyrine, propylthiouracil, and methimazole in thyroid dysfunction. Clinical Pharmacology and Therapeutics 17, 48-56 CrossRefGoogle Scholar
75. Videla, L.A. and Fernández, V. (2009) Redox signaling in thyroid hormone action: a novel strategy for liver preconditioning. In Thyroid Hormones: Functions, Related Diseases, and Uses (Kuehn, F.S., Lozada, M.P., eds), pp. 49-74, Nova Science Publishers Inc., New York Google Scholar
76. Videla, L.A. et al. (2012) Metabolic basis for thyroid hormone preconditioning: upregulation of AMP-regulated protein kinase signaling. Scientific World Journal 2012, 1-10, Article ID 475675, doi:10.1100/2012/475675 Google Scholar
77. Viollet, B. et al. (2009) AMP-activated protein kinase in the regulation of hepatic energy metabolism: from physiology to therapeutic perspectives. Acta Physiologica 196, 81-98 CrossRefGoogle ScholarPubMed
78. Vargas, R. et al. (2013) Thyroid hormone activates rat liver adenosine 5,-monphosphate-activated protein kinase: relation to CaMKKβ, TAK1, and LKB1 expression and energy status. Journal of Biological Regulators and Homeostatic Agents 27, 989-999 Google ScholarPubMed
79. Wallach, S. et al. (1972) Thyroxine-induced stimulation of hepatic cell transport of calcium and magnesium. Journal of Clinical Investigation 51, 1572-1577 CrossRefGoogle ScholarPubMed
80. Hummerich, K. and Sobol, S. (1989) Rapid stimulation of calcium uptake into rat liver by L-triiodothyronine. Biochemical Journal 258, 363-367 CrossRefGoogle Scholar
81. Yehuda-Shniadman, E. et al. (2010) Gating of the mitochondrial permeability transition pore by thyroid hormone. FASEB Journal 24, 93-104 CrossRefGoogle Scholar
82. Videla, L.A. et al. (2014) T3-induced liver AMPK signaling: redox dependency and upregulation of downstream targets. World Journal of Gastroenterology 20, 17416-17425 CrossRefGoogle ScholarPubMed
83. Ismail-Beigi, F. et al. (1973) Effects of thyroid hormone on adenine nucleotide content of rat liver. Proceedings of the Society for Experimental Biology and Medicine 144, 471-474 CrossRefGoogle ScholarPubMed
84. Sinha, R.A. et al. (2012) Thyroid hormone stimulates hepatic lipid catabolism via activation of autophagy. Journal of Clinical Investigation 122, 2428-2438 CrossRefGoogle ScholarPubMed
85. Handa, N. et al. (2011) Structural basis for compound C inhibition of the human AMP-activated protein kinase α2 subunit kinase domain. Acta Crystallographica D67, 480-487 Google Scholar
86. De Lange, P. et al. (2008) Rapid activation by 3,5,3,-L-triiodothyronine of adenosine 5,-monophosphate-activated protein kinase/acetyl-coenzyme A carboxylase and Akt/protein kinase B signaling pathways: relation to changes in fuel metabolism and myosin heavy-chain protein content in rat gastrocnemius muscle in vivo . Endocrinology 149, 6462-6470 CrossRefGoogle Scholar
87. Fernández, V. et al. (2008) Causal role of oxidative stress in liver preconditioning by thyroid hormone in rats. Free Radical Biology and Medicine 44, 1724-1731 CrossRefGoogle ScholarPubMed
88. Tapia, G. et al. (2010) Kupffer-cell activity is essential for thyroid hormone rat liver preconditioning. Molecular and Cellular Endocrinology 323, 292-297 CrossRefGoogle ScholarPubMed
89. Pantos, C.I. et al. (2002) Long-term thyroxine administration protects the heart in a pattern similar to ischemic preconditioning. Thyroid 12, 325-329 CrossRefGoogle Scholar
90. Kumar, A., Taliyan, R. and Sharma, P.L. (2012) Evaluation of thyroid hormone induced pharmacological preconditioning on cardiomyocyte protection against ischemic-reperfusion injury. Indian Journal of Pharmacology 44, 68-72 Google ScholarPubMed
91. de Castro, A.L. et al. (2014) Cardioprotective effects of thyroid hormones in a rat model of myocardial infarction are associated with oxidative stress reduction. Molecular and Cellular Endocrinology 391, 22-29 CrossRefGoogle Scholar
92. Redout, E.M. et al. (2010) Antioxidant treatment attenuates pulmonary arterial hypertension-induced heart failure. American Journal of Physiology - Heart and Circulatory Physiology 298, H1038-H1047 CrossRefGoogle ScholarPubMed
93. Pantos, C. et al. (2006) Hyperthyroid hearts display a phenotype of cardioprotection against ischemic stress: a possible involvement of heat shock protein 70. Hormone and Metabolic Research 38, 308-313 CrossRefGoogle Scholar
94. Mourouzis, I. et al. (2013) Thyroid hormone improves the mechanical performance of the post-infarcted diabetic myocardium: a response associated with up-regulation of Akt/mTOR and AMPK activation. Metabolism 62, 1387-1393 CrossRefGoogle ScholarPubMed
95. Nicolini, G. et al. (2013) New insights into mechanisms of cardioprotection mediated by thyroid hormones. Journal of Thyroid Research 2013, 1-9, Article ID 264387, doi: 10.1155/2013/264387 CrossRefGoogle ScholarPubMed
96. Hajje, G. et al. (2014) Hypothyroidism and its rapid correction alter cardiac remodeling. PLoS ONE 9, e109753 CrossRefGoogle ScholarPubMed
97. Talukder, M.A.H. et al. (2011) Detrimental effects of thyroid hormone analog DITPA in the mouse heart: increased mortality with in vivo acut myocardial ischemia-reperfusion. American Journal of Physiology – Heart and Circulatory Physiology 300, H702-H711 CrossRefGoogle Scholar
98. Li, F. et al. (2011) Heme-oxygenase-1 is induced by thyroid hormone and involved in thyroid hormone preconditioning-induced protection against renal warm ischemia in rat. Molecular and Cellular Endocrinology 339, 54-62 CrossRefGoogle ScholarPubMed
99. Ferreyra, C. et al. (2009) Effect of preconditioning with triiodothyronine on renal ischemia/reperfusión injury and poly(ADP-ribose) polymerase expression in rats. Transplantation Proceedings 41, 2073-2075 CrossRefGoogle ScholarPubMed
100. Kim, S.M. et al. (2014) Preconditioning with thyroid hormone (3,5,3-triiodothyronine) prevents renal ischemia-reperfusion injury in mice. Surgery 155, 554-561 CrossRefGoogle ScholarPubMed
101. Sutter, P.M. et al. (1988) Beneficial effect of thyroxin in the treatment of ischemic acute renal failure. Pediatric Nephrology 2, 1-7 CrossRefGoogle ScholarPubMed
102. Wang, P.-L. et al. (2012) Thyroid hormone preconditioning alleviates reperfusion-induced renal inflammation in mice. Academic Journal of Second Military Medical University 34, 364-367 Google Scholar
103. Genovese, T. et al. (2013) Post-ischemic thyroid hormone treatment in a rat model of acute stroke. Brain Research 1513, 92-102 CrossRefGoogle Scholar
104. Losi, G., Garzon, G. and Puia, G. (2008) Nongenomic regulation of glutamatergic neurotransmission in hippocampus by thyroid hormones. Neuroscience 151, 155-163 CrossRefGoogle ScholarPubMed
105. Mendes-de-Aguiar, C.B. et al. (2008) Thyroid hormone increases astrocyte glutamate uptake and protects astrocytes and neurons against glutamate toxicity. Journal of Neuroscience Research 86, 3117-3125 CrossRefGoogle ScholarPubMed
106. Lin, H.-Y. et al. (2011) Molecular basis for certain neuroprotective effects of thyroid hormone. Frontiers in Molecular Neuroscience 4, Article 29, 1-6 CrossRefGoogle ScholarPubMed
107. Park, S.H. et al. (2002) Effects of thyroid state on AMP-activated protein kinase and acetyl-CoA carboxylase expression in muscle. Journal of Applied Physiolology 93, 2081-2088 CrossRefGoogle ScholarPubMed
108. Irrcher, I. et al. (2008) Thyroid hormone (T3) rapidly activates p38 and AMPK in skeletal muscle in vivo . Journal of Applied Physiology 104, 178-185 CrossRefGoogle ScholarPubMed
109. Yamauchi, M. et al. (2008) Thyroid hormone activates adenosine 5,-monphosphate-activated protein kinase via intracellular calcium mobilization and activation of calcium/calmodulin-dependent kinase kinase-β. Molecular Endocrinology 22, 893-903 CrossRefGoogle Scholar
110. Heather, L.C. et al. (2010) Adenosine monophosphate-activated protein kinase activation, substrate transporter translocation, and metabolism in the contracting hyperthyroid heart. Endocrinology 151, 422-431 CrossRefGoogle Scholar
111. Fukuyama, K. et al. (2006) Thyroid hormone inhibits vascular remodeling through suppression of cAMP response element binding protein activity. Arteriosclerosis Thrombosis and Vascular Biology 26, 2049-2055 CrossRefGoogle ScholarPubMed
112. Shulga, A. et al. (2009) Thyroxin regulates BDNF expression to promote survival of injured neurons. Molecular and Cellular Neuroscience 42, 408-418 CrossRefGoogle ScholarPubMed
113. Panaite, P.A. and Barakat-Walter, I. (2010) Thyroid hormone enhances transected axonal regeneration and muscle reinervation following rat sciatic nerve injury. Journal of Neuroscience Research 88, 1751-1763 CrossRefGoogle Scholar
114. Bhargava, M. et al. (2008) Triiodo-L-thyronine rapidly stimulates alveolar fluid clearance in normal and hyperoxia-injured lungs. American Journal of Respiratory and Critical Care Medicine 178, 506-521 CrossRefGoogle ScholarPubMed
115. Safer, J.D., Crawford, T.M. and Holick, M.F. (2004) A role for thyroid hormone in wound healing through keratin gene expression. Endocrinology 145, 2357-2361 CrossRefGoogle ScholarPubMed
116. Kassem, R. et al. (2012) Harnessing the skin-thyroid connection for wound healing: a prospective controlled trial in guinea pigs. Journal of Clinical and Experimental Dermatology 37, 850-856 CrossRefGoogle ScholarPubMed
117. Verga Falzacappa, C. et al. (2012) T3 preserves ovarian granulosa cells from chemotherapy induced apoptosis. Journal of Endocrinology 215, 281-289 CrossRefGoogle ScholarPubMed
118. Kuzman, J.A. et al. (2005) Thyroid hormone activates Akt and prevents serum starvation-induced cell death in neonatal rat cardiomyocytes. Journal of Molecular and Cellular Cardiology 39, 841-844 CrossRefGoogle ScholarPubMed
119. Videla, L.A. et al. (2007) Thyroid hormone calorigenesis and mitochondrial redox signaling: upregulation of gene expression. Frontiers in Bioscience 12, 1220-1228 CrossRefGoogle ScholarPubMed
120. Goglia, F. and Skulachev, V.P. (2003) A function for novel uncoupling proteins: antioxidant defense of mitochondrial matrix by translocating fatty acid peroxides from inner to outer membrane leaflet. FASEB Journal 17, 1585-1591 CrossRefGoogle ScholarPubMed
121. Aldrighetti, L. et al. (2006) Impact of preoperative steroids administration on ischemia-reperfusion injury and systemic responses in liver surgery: a prospective randomized study. Liver Transplantation 12, 941-949 CrossRefGoogle ScholarPubMed
122. Bahde, R. and Spiegel, H.-U. (2010) Hepatic ischemia-reperfusion injury from bench to bedside. British Journal of Surgery 97, 1461-1475 CrossRefGoogle ScholarPubMed
123. Duntas, L.H. and Biondi, B. (2013) The interactions between obesity, thyroid function, and autoimmunity: the multifold role of leptin. Thyroid 23, 646-653 CrossRefGoogle Scholar
124. Santini, F. et al. (2014) The crosstalk between thyroid gland and adipose tissue: signal integration in health and disease. European Journal of Endocrinology 171, R137-R152 CrossRefGoogle ScholarPubMed
125. Coppola, M. et al. (2014) Thyroid hormone analogues and derivatives: actions in fatty liver. World Journal of Hepatology 6, 114-129 CrossRefGoogle ScholarPubMed
126. Antonelli, A. et al. (2011) 3,5-Diiodo-L-thyronine increases resting metabolic rate and reduces body weight without undesirable side effects. Journal of Biological Regulators and Homeostatic Agents 25, 655-660 Google ScholarPubMed