Oxidative stress and heart disease: the thyroid hormone mediation

Abstract

The heart is one of the principal targets of thyroid hormones (TH) action, affecting cardiac contractility, heart rate, and diastolic function. Oxidative damage is pivotal for onset and development of cardiovascular disease (CVD) and heart failure. Specifically, free radical generation is associated to hyper-metabolic state in hyperthyroidism, whereas hypo-metabolic state induced by hypothyroidism leads to a decrease of oxidative stress. In the present review, the role of oxidative damage in CVD and failing heart-TH interplay will be considered. The main oxidative events leading to cardiac dysfunction and TH cardiac regulation at genomic and non-genomic levels will be discussed, as well as role of TH in cardioprotection and reversion of cardiac remodeling.

Keywords

Oxidative stress / heart disease / cardiac remodeling / thyroid hormones

References

[1] Tsutsui H,Matsushima S.Oxidative stress and heart failure..Am J Physiol Heart Circ Physiol2011;301:H2181-90

[2] Ho E,Liu CC,Figtree GA.Biological markers of oxidative stress: Applications to cardiovascular research and practice..Redox Biol2013;1:483-91 PMCID:PMC3830063

[3] Resch U,Tatzber F.Antioxidant status in thyroid dysfunction..Clin Chem Lab Med2002;40:1132-4

[4] Mancini A,Raimondo S.Thyroid Hormones, Oxidative Stress, and Inflammation..Mediators Inflamm2016;2016:6757154 PMCID:PMC4802023

[5] Gaggini M,Vassalle C.Iervasi G,Gerdes A.The Thyroid-Oxidative Stress Axis in Heart Failure..Thyroid and Heart.2020;ChamSpringer International Publishing171-86

[6] Mishra P.Oxidative stress and heart failure in altered thyroid States..ScientificWorldJournal2012;2012:741861 PMCID:PMC3354657

[7] Stocker R.Role of oxidative modifications in atherosclerosis..Physiol Rev2004;84:1381-478

[8] Lockwood TD.Redox control of protein degradation..Antioxid Redox Signal2000;2:851-78

[9] Thollon C,Cambarrat C,Vilaine JP.Nature of the cardiomyocyte injury induced by lipid hydroperoxides..Cardiovasc Res1995;30:648-55

[10] Schulz E,Münzel T.Mitochondrial redox signaling: Interaction of mitochondrial reactive oxygen species with other sources of oxidative stress..Antioxid Redox Signal2014;20:308-24 PMCID:PMC3887453

[11] Daiber A,Oelze M.Crosstalk of mitochondria with NADPH oxidase via reactive oxygen and nitrogen species signalling and its role for vascular function..Br J Pharmacol2017;174:1670-89 PMCID:PMC5446573

[12] Hernanz R,Salaices M.New roles for old pathways? A circuitous relationship between reactive oxygen species and cyclo-oxygenase in hypertension..Clin Sci (Lond)2014;126:111-21

[13] Dubois-Deruy E,Turkieh A.Oxidative Stress in Cardiovascular Diseases..Antioxidants (Basel)2020;9:864 PMCID:PMC7554855

[14] Wang Y,Noë A.Superoxide dismutases: Dual roles in controlling ROS damage and regulating ROS signaling..J Cell Biol2018;217:1915-28 PMCID:PMC5987716

[15] Mastorci F,Vassalle C.Cardioprotection and Thyroid Hormones in the Clinical Setting of Heart Failure..Front Endocrinol (Lausanne)2019;10:927 PMCID:PMC6997485

[16] Klein I.Thyroid hormone and the cardiovascular system..N Engl J Med2001;344:501-9

[17] Kushnir A.The ryanodine receptor in cardiac physiology and disease..Adv Pharmacol2010;59:1-30 PMCID:PMC3023997

[18] Koss KL.Phospholamban: a prominent regulator of myocardial contractility..Circ Res1996;79:1059-63

[19] Kahaly GJ.Thyroid hormone action in the heart..Endocr Rev2005;26:704-28

[20] Morkin E,Goldman S.Biochemical and physiologic effects of thyroid hormone on cardiac performance..Progress in Cardiovascular Diseases1983;25:435-64

[21] Mai W,Allioli N.Thyroid hormone receptor alpha is a molecular switch of cardiac function between fetal and postnatal life..Proc Natl Acad Sci U S A2004;101:10332-7 PMCID:PMC478572

[22] Davis PJ,Leonard JL.Nongenomic actions of thyroid hormone..Nat Rev Endocrinol2016;12:111-21

[23] Wickenden AD,Parker TG,Backx PH.Effects of development and thyroid hormone on K+ currents and K+ channel gene expression in rat ventricle..J Physiol1997;504:Pt 2271-86 PMCID:PMC1159909

[24] Cernohorský J,Pelouch V,Vetter R.Thyroid control of sarcolemmal Na+/Ca2+ exchanger and SR Ca2+-ATPase in developing rat heart..Am J Physiol1998;275:H264-73

[25] Rajagopalan S,Ramasamy S,Galis ZS.Reactive oxygen species produced by macrophage-derived foam cells regulate the activity of vascular matrix metalloproteinases in vitro. Implications for atherosclerotic plaque stability..J Clin Invest1996;98:2572-9 PMCID:PMC507715

[26] Blankenberg S,Tiret L.Adhesion molecules and atherosclerosis..Atherosclerosis2003;170:191-203

[27] Herbert J,Savi P.The mitogenic effect of H ₂ O ₂ for vascular smooth muscle cells is mediated by an increase of the affinity of basic fibroblast growth factor for its receptor..FEBS Letters1996;395:43-7

[28] Delafontaine P.Reactive oxygen species stimulate insulin-like growth factor I synthesis in vascular smooth muscle cells..Cardiovasc Res1997;33:216-22

[29] Nabel EG.A tale of coronary artery disease and myocardial infarction..N Engl J Med2012;366:54-63

[30] Frangogiannis NG.Regulation of the inflammatory response in cardiac repair..Circ Res2012;110:159-73 PMCID:PMC3690135

[31] Mukherjee SB,Sudhandiran G.Increase in cytosolic Ca2+ levels through the activation of non-selective cation channels induced by oxidative stress causes mitochondrial depolarization leading to apoptosis-like death in Leishmania donovani promastigotes..J Biol Chem2002;277:24717-27

[32] Sheeran FL.Mitochondrial Bioenergetics and Dysfunction in Failing Heart..Adv Exp Med Biol2017;982:65-80

[33] Sheeran FL.Energy deficiency in the failing heart: linking increased reactive oxygen species and disruption of oxidative phosphorylation rate..Biochim Biophys Acta2006;1757:543-52

[34] Pfeffer MA.Left ventricular remodeling after acute myocardial infarction..Annu Rev Med1995;46:455-66

[35] Cappola TP.Molecular remodeling in human heart failure..J Am Coll Cardiol2008;51:137-8

[36] Sabatino L.Iervasi G,Gerdes A.TH Treatment in Patients with Cardiac Disorders: General Aspects and Rationale..Thyroid and Heart.2020;ChamSpringer International Publishing373-80

[37] Swynghedauw B,Samuel JL,Cohen-Solal A.Molecular mechanisms in evolutionary cardiology failure..Ann N Y Acad Sci2010;1188:58-67

[38] Klein I.Thyroid hormone-targeting the heart..Endocrinology2001;142:11-2

[39] Wang B,Li L.Non-thyroidal illness syndrome in patients with cardiovascular diseases: A systematic review and meta-analysis..Int J Cardiol2017;226:1-10

[40] Pingitore A,Taddei MC,L’Abbate A.Triiodothyronine levels for risk stratification of patients with chronic heart failure..Am J Med2005;118:132-6

[41] Bianco AC,Gereben B,Larsen PR.Biochemistry, cellular and molecular biology, and physiological roles of the iodothyronine selenodeiodinases..Endocr Rev2002;23:38-89

[42] Ortiz VD,Campos C.Effects of thyroid hormones on aortic tissue after myocardial infarction in rats..Eur J Pharmacol2016;791:788-93

[43] Yao J.Decreased collagen gene expression and absence of fibrosis in thyroid hormone-induced myocardial hypertrophy. Response of cardiac fibroblasts to thyroid hormone in vitro..Circ Res1992;71:831-9

[44] Kmiec Z,Rachón D,Sworczak K.Natural killer activity and thyroid hormone levels in young and elderly persons..Gerontology2001;47:282-8

[45] Sabatino L,Kusmic C.Modification of gene expression profiling related to renin-angiotensin system in an ischemia/reperfusion rat model after T3 infusion..Mol Cell Biochem2018;449:277-83

[46] Janssen R,Kuster DW,Simonides WS.Thyroid Hormone-Regulated Cardiac microRNAs are Predicted to Suppress Pathological Hypertrophic Signaling..Front Endocrinol (Lausanne)2014;5:171 PMCID:PMC4202793

[47] Danzi S,Klein I.Triiodothyronine-mediated myosin heavy chain gene transcription in the heart..Am J Physiol Heart Circ Physiol2003;284:H2255-62

[48] Rybin V.Thyroid hormone represses protein kinase C isoform expression and activity in rat cardiac myocytes..Circ Res1996;79:388-98

[49] Ferreira JC,Mochly-Rosen D.βIIPKC and εPKC isozymes as potential pharmacological targets in cardiac hypertrophy and heart failure..J Mol Cell Cardiol2011;51:479-84 PMCID:PMC3135714