Mechanism of subclinical hypothyroidism accelerating endothelial dysfunction (Review)
- Authors:
- Ming Lu
- Chong‑Bo Yang
- Ling Gao
- Jia‑Jun Zhao
-
Affiliations: Department of Endocrinology and Metabolism, Shandong Provincial Hospital Affiliated to Shandong University, Jinan, Shandong, P.R. China, Institute of Endocrinology and Metabolic Diseases, Shandong Academy of Clinical Medicine, Jinan, Shandong, P.R. China - Published online on: October 27, 2014 https://doi.org/10.3892/etm.2014.2037
- Pages: 3-10
This article is mentioned in:
Abstract
Surks MI, Ortiz E, Daniels GH, et al: Subclinical thyroid disease: scientific review and guidelines for diagnosis and management. JAMA. 291:228–238. 2004. View Article : Google Scholar : PubMed/NCBI | |
Cooper DS and Biondi B: Subclinical thyroid disease. Lancet. 379:1142–1154. 2012. View Article : Google Scholar : PubMed/NCBI | |
Boelaert K: Thyroid dysfunction in the elderly. Nat Rev Endocrinol. 9:194–204. 2013. View Article : Google Scholar : PubMed/NCBI | |
Hak AE, Pols HA, Visser TJ, Drexhage HA, Hofman A and Witteman JC: Subclinical hypothyroidism is an independent risk factor for atherosclerosis and myocardial infarction in elderly women: the Rotterdam study. Ann Intern Med. 132:270–278. 2000. View Article : Google Scholar : PubMed/NCBI | |
Rodondi N, Newman AB, Vittinghoff E, et al: Subclinical hypothyroidism and the risk of heart failure, other cardiovascular events, and death. Arch Intern Med. 165:2460–2466. 2005. View Article : Google Scholar : PubMed/NCBI | |
Walsh JP, Bremner AP, Bulsara MK, et al: Subclinical thyroid dysfunction as a risk factor for cardiovascular disease. Arch Intern Med. 165:2467–2472. 2005. View Article : Google Scholar : PubMed/NCBI | |
Razvi S, Weaver JU, Vanderpump MP and Pearce SH: The incidence of ischemic heart disease and mortality in people with subclinical hypothyroidism: reanalysis of the Whickham Survey cohort. J Clin Endocrinol Metab. 95:1734–1740. 2010. View Article : Google Scholar : PubMed/NCBI | |
Rodondi N, den Elzen WP, Bauer DC, et al: Subclinical hypothyroidism and the risk of coronary heart disease and mortality. JAMA. 304:1365–1374. 2010. View Article : Google Scholar : PubMed/NCBI | |
Tseng FY, Lin WY, Lin CC, et al: Subclinical hypothyroidism is associated with increased risk for all-cause and cardiovascular mortality in adults. J Am Coll Cardiol. 60:730–737. 2012. View Article : Google Scholar : PubMed/NCBI | |
Gencer B, Collet TH, Virgini V, Auer R and Rodondi N: Subclinical thyroid dysfunction and cardiovascular outcomes among prospective cohort studies. Endocr Metab Immune Disord Drug Targets. 13:4–12. 2013. View Article : Google Scholar : PubMed/NCBI | |
Lusis AJ: Atherosclerosis. Nature. 407:233–241. 2000. View Article : Google Scholar : PubMed/NCBI | |
Galkina E and Ley K: Immune and inflammatory mechanisms of atherosclerosis. Ann Rev Immunol. 27:1652009. View Article : Google Scholar | |
Libby P, Ridker PM and Hansson GK: Progress and challenges in translating the biology of atherosclerosis. Nature. 473:317–325. 2011. View Article : Google Scholar : PubMed/NCBI | |
Bonetti PO, Lerman LO and Lerman A: Endothelial dysfunction: a marker of atherosclerotic risk. Arterioscler Thromb Vasc Biol. 23:168–175. 2003. View Article : Google Scholar : PubMed/NCBI | |
Makino A and Kamata K: Possible modulation by endothelin-1, nitric oxide, prostaglandin I2 and thromboxane A2 of vasoconstriction induced by an α-agonist in mesenteric arterial bed from diabetic rats. Diabetologia. 41:1410–1418. 1998. View Article : Google Scholar : PubMed/NCBI | |
Beckman JS and Koppenol WH: Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and the ugly. Am J Physiol. 40:C14241996. | |
Alderton WK, Cooper CE and Knowles RG: Nitric oxide synthases: structure, function and inhibition. Biochem J. 357:593–615. 2001. View Article : Google Scholar : PubMed/NCBI | |
Hollenberg SM and Cinel I: Bench-to-bedside review: nitric oxide in critical illness-update 2008. Crit Care. 13:2182009. View Article : Google Scholar | |
Esper RJ, Nordaby RA, Vilariño JO, Paragano A, Cacharrón JL and Machado RA: Endothelial dysfunction: a comprehensive appraisal. Cardiovasc Diabetol. 5:4–22. 2006. View Article : Google Scholar : PubMed/NCBI | |
Mudau M, Genis A, Lochner A and Strijdom H: Endothelial dysfunction: the early predictor of atherosclerosis. Cardiovasc J Afr. 23:222–231. 2012. View Article : Google Scholar : PubMed/NCBI | |
Frank PG, Pavlides S and Lisanti MP: Caveolae and transcytosis in endothelial cells: role in atherosclerosis. Cell Tissue Res. 335:41–47. 2009. View Article : Google Scholar | |
Sowa G: Caveolae, caveolins, cavins, and endothelial cell function: new insights. Front Physiol. 2:1202012. View Article : Google Scholar : PubMed/NCBI | |
Widlansky ME, Gokce N, Keaney JF Jr and Vita JA: The clinical implications of endothelial dysfunction. J Am Coll Cardiol. 42:1149–1160. 2003. View Article : Google Scholar : PubMed/NCBI | |
Kim VN: MicroRNA biogenesis: coordinated cropping and dicing. Nat Rev Mol Cell Biol. 6:376–385. 2005. View Article : Google Scholar : PubMed/NCBI | |
Sun X, Belkin N and Feinberg MW: Endothelial microRNAs and atherosclerosis. Curr Atheroscler Rep. 15:1–13. 2013. View Article : Google Scholar | |
Loyer X, Potteaux S, Vion AC, et al: Inhibition of MicroRNA-92a Prevents Endothelial Dysfunction and Atherosclerosis in Mice. Circ Res. 114:434–443. 2014. View Article : Google Scholar | |
Menghini R, Casagrande V and Federici M: MicroRNAs in endothelial senescence and atherosclerosis. J Cardiovasc Transl Res. 6:924–930. 2013. View Article : Google Scholar : PubMed/NCBI | |
Zhang X, Shao S, Geng H, et al: Expression profiles of six circulating microRNAs critical to atherosclerosis in patients with subclinical hypothyroidism: a clinical study. J Clin Endocrinol Metab. 99:E766–774. 2014. View Article : Google Scholar : PubMed/NCBI | |
Turemen EE, Cetinarslan B, Sahin T, Canturk Z and Tarkun I: Endothelial dysfunction and low grade chronic inflammation in subclinical hypothyroidism due to autoimmune thyroiditis. Endocr J. 58:349–354. 2011. View Article : Google Scholar : PubMed/NCBI | |
Dardano A, Ghiadoni L, Plantinga Y, et al: Recombinant human thyrotropin reduces endothelium-dependent vasodilation in patients monitored for differentiated thyroid carcinoma. J Clin Endocrinol Metab. 91:4175–4178. 2006. View Article : Google Scholar : PubMed/NCBI | |
Gao N, Zhang W, Zhang YZ, Yang Q and Chen SH: Carotid intima-media thickness in patients with subclinical hypothyroidism: a meta-analysis. Atherosclerosis. 227:18–25. 2013. View Article : Google Scholar | |
Balzan S, Del Carratore R, Nicolini G, et al: Proangiogenic effect of TSH in human microvascular endothelial cells through its membrane receptor. J Clin Endocrinol Metab. 97:1763–1770. 2012. View Article : Google Scholar : PubMed/NCBI | |
Tian L, Zhang L, Liu J, Guo T, Gao C and Ni J: Effects of TSH on the function of human umbilical vein endothelial cells. J Mol Endocrinol. 52:215–222. 2014. View Article : Google Scholar : PubMed/NCBI | |
Wang Y, Zhong J, Wei W, et al: Developmental iodine deficiency and hypothyroidism impair neural development, upregulate caveolin-1, and downregulate synaptotagmin-1 in the rat cerebellum. Biol Trace Elem Res. 144:1039–1049. 2011. View Article : Google Scholar : PubMed/NCBI | |
Gong J, Dong J, Wang Y, et al: Developmental iodine deficiency and hypothyroidism impair neural development, up-regulate caveolin-1 and down-regulate synaptophysin in rat hippocampus. J Neuroendocrinology. 22:129–139. 2010. View Article : Google Scholar | |
Sarati LI, Martinez CR, Artés N, et al: Hypothyroidism: age-related influence on cardiovascular nitric oxide system in rats. Metabolism. 61:1301–1311. 2012. View Article : Google Scholar : PubMed/NCBI | |
Latif R, Ando T and Davies TF: Lipid rafts are triage centers for multimeric and monomeric thyrotropin receptor regulation. Endocrinology. 148:3164–3175. 2007. View Article : Google Scholar : PubMed/NCBI | |
Ito A, Tsao PS, Adimoolam S, Kimoto M, Ogawa T and Cooke JP: Novel mechanism for endothelial dysfunction: dysregulation of dimethylarginine dimethylaminohydrolase. Circulation. 99:3092–3095. 1999. View Article : Google Scholar : PubMed/NCBI | |
Nofer J-R, van der Giet M, Tölle M, et al: HDL induces NO-dependent vasorelaxation via the lysophospholipid receptor S1P3. J Clin Invest. 113:569–581. 2004. View Article : Google Scholar : PubMed/NCBI | |
Lai Y, Wang J, Jiang F, et al: The relationship between serum thyrotropin and components of metabolic syndrome. Endocr J. 58:23–30. 2011. View Article : Google Scholar | |
Åsvold BO, Vatten LJ, Nilsen TI and Bjøro T: The association between TSH within the reference range and serum lipid concentrations in a population-based study. The HUNT Study. Eur J Endocrinol. 156:181–186. 2007. View Article : Google Scholar : PubMed/NCBI | |
Geng H, Zhang X, Wang C, et al: Even mildly elevated TSH is associated with an atherogenic lipid profile in postmenopausal women with subclinical hypothyroidism. Endocr Res. Mar 28–2014.(Epub ahead of print). View Article : Google Scholar : PubMed/NCBI | |
Xiang GD, Xiang LW, He HL and Zhao LS: Postprandial lipaemia suppresses endothelium-dependent arterial dilation in patients with hypothyroidism. Endocrine. 42:391–398. 2012. View Article : Google Scholar : PubMed/NCBI | |
Tian L, Song Y, Xing M, et al: A novel role for thyroid-stimulating hormone: Up-regulation of hepatic 3-hydroxy-3-methyl-glutaryl-coenzyme a reductase expression through the cyclic adenosine monophosphate/protein kinase A/cyclic adenosine monophosphate-responsive element binding protein pathway. Hepatology. 52:1401–1409. 2010. View Article : Google Scholar : PubMed/NCBI | |
Taddei S, Caraccio N, Virdis A, et al: Low-grade systemic inflammation causes endothelial dysfunction in patients with Hashimoto’s thyroiditis. J Clin Endocrinol Metab. 91:5076–5082. 2006. View Article : Google Scholar : PubMed/NCBI | |
Ridker PM, Rifai N, Stampfer MJ and Hennekens CH: Plasma concentration of interleukin-6 and the risk of future myocardial infarction among apparently healthy men. Circulation. 101:1767–1772. 2000. View Article : Google Scholar : PubMed/NCBI | |
Antunes TT, Gagnon A, Bell A and Sorisky A: Thyroid-stimulating hormone stimulates interleukin-6 release from 3T3-L1 adipocytes through a cAMP-protein kinase A pathway. Obes Res. 13:2066–2071. 2005. View Article : Google Scholar | |
Zhang C, Xu X, Potter BJ, et al: TNF-alpha contributes to endothelial dysfunction in ischemia/reperfusion injury. Arterioscler Thromb Vasc Biol. 26:475–480. 2006. View Article : Google Scholar | |
Whetsell M, Bagriacik EU, Seetharamaiah GS, Prabhakar BS and Klein JR: Neuroendocrine-induced synthesis of bone marrow-derived cytokines with inflammatory immunomodulating properties. Cell Immunol. 192:159–166. 1999. View Article : Google Scholar : PubMed/NCBI | |
Christ-Crain M, Meier C, Guglielmetti M, et al: Elevated C-reactive protein and homocysteine values: cardiovascular risk factors in hypothyroidism? A cross-sectional and a double-blind, placebo-controlled trial. Atherosclerosis. 166:379–386. 2003. View Article : Google Scholar : PubMed/NCBI | |
Kvetny J, Heldgaard PE, Bladbjerg EM and Gram J: Subclinical hypothyroidism is associated with a low-grade inflammation, increased triglyceride levels and predicts cardiovascular disease in males below 50 years. Clin Endocrinol (Oxf). 61:232–238. 2004. View Article : Google Scholar | |
Tuzcu A, Bahceci M, Gokalp D, Tuzun Y and Gunes K: Subclinical hypothyroidism may be associated with elevated high-sensitive c-reactive protein (low grade inflammation) and fasting hyperinsulinemia. Endocr J. 52:89–94. 2005. View Article : Google Scholar : PubMed/NCBI | |
Verma S, Li S-H, Badiwala MV, et al: Endothelin antagonism and interleukin-6 inhibition attenuate the proatherogenic effects of C-reactive protein. Circulation. 105:1890–1896. 2002. View Article : Google Scholar : PubMed/NCBI | |
Cai H and Harrison DG: Endothelial dysfunction in cardiovascular diseases: the role of oxidant stress. Circ Res. 87:840–844. 2000. View Article : Google Scholar : PubMed/NCBI | |
Lubos E, Handy DE and Loscalzo J: Role of oxidative stress and nitric oxide in atherothrombosis. Front Biosci. 13:5323–5344. 2008. View Article : Google Scholar : PubMed/NCBI | |
Higashi Y, Noma K, Yoshizumi M and Kihara Y: Endothelial function and oxidative stress in cardiovascular diseases. Circ J. 73:411–418. 2009. View Article : Google Scholar : PubMed/NCBI | |
Coria MJ, Pastran AI and Gimenez MS: Serum oxidative stress parameters of women with hypothyroidism. Acta Biomed. 80:135–139. 2009.PubMed/NCBI | |
Torun AN, Kulaksizoglu S, Kulaksizoglu M, Pamuk BO, Isbilen E and Tutuncu NB: Serum total antioxidant status and lipid peroxidation marker malondialdehyde levels in overt and subclinical hypothyroidism. Clin Endocrinol (Oxf). 70:469–474. 2009. View Article : Google Scholar | |
Cebeci E, Alibaz-Oner F, Usta M, Yurdakul S and Erguney M: Evaluation of oxidative stress, the activities of paraoxonase and arylesterase in patients with subclinical hypothyroidism. J Investig Med. 60:23–28. 2012. | |
Ozturk U, Vural P, Ozderya A, Karadag B, Dogru-Abbasoglu S and Uysal M: Oxidative stress parameters in serum and low density lipoproteins of Hashimoto’s thyroiditis patients with subclinical and overt hypothyroidism. Int Immunopharmacol. 14:349–352. 2012. View Article : Google Scholar | |
GDX, JHP, HLS and LSZ: Alpha-lipoic acid improves endothelial dysfunction in patients with subclinical hypothyroidism. Exp Clin Endocrinol Diabetes. 118:625–629. 2010. View Article : Google Scholar | |
Fujii N, Tsuchihashi K, Sasao H, et al: Insulin resistance functionally limits endothelium-dependent coronary vasodilation in nondiabetic patients. Heart Vessels. 23:9–15. 2008. View Article : Google Scholar : PubMed/NCBI | |
Kim J-a, Montagnani M, Koh KK and Quon MJ: Reciprocal relationships between insulin resistance and endothelial dysfunction molecular and pathophysiological mechanisms. Circulation. 113:1888–1904. 2006. View Article : Google Scholar : PubMed/NCBI | |
Gen R, Akbay E and Sezer K: Insulin resistance and cardiovascular risk factors in patients with mild and severe subclinical hypothyroidism. The Endocrinologist. 20:128–130. 2010. View Article : Google Scholar | |
Maratou E, Hadjidakis DJ, Kollias A, et al: Studies of insulin resistance in patients with clinical and subclinical hypothyroidism. Eur J Endocrinol. 160:785–790. 2009. View Article : Google Scholar : PubMed/NCBI | |
Al Sayed A, Al Ali N and Alfadhli E: Subclinical hypothyroidism is associated with early insulin resistance in Kuwaiti women. Endocr J. 53:653–657. 2006. View Article : Google Scholar : PubMed/NCBI | |
Peeters RP, Van Der Deure WM, Van Den Beld AW, et al: The Asp727Glu polymorphism in the TSH receptor is associated with insulin resistance in healthy elderly men. Clin Endocrinol (Oxf). 66:808–815. 2007. View Article : Google Scholar | |
Taddei S, Caraccio N, Virdis A, et al: Impaired endothelium-dependent vasodilatation in subclinical hypothyroidism: beneficial effect of levothyroxine therapy. J Clin Endocrinol Metab. 88:3731–3737. 2003. View Article : Google Scholar : PubMed/NCBI | |
Monzani F, Caraccio N, Kozakowa M, et al: Effect of levothyroxine replacement on lipid profile and intima-media thickness in subclinical hypothyroidism: a double-blind, placebo-controlled study. J Clin Endocrinol Metab. 89:2099–2106. 2004. View Article : Google Scholar : PubMed/NCBI | |
Oner FA, Yurdakul S, Oner E, Uzum AK and Erguney M: Evaluation of the effect of L-thyroxin therapy on endothelial functions in patients with subclinical hypothyroidism. Endocrine. 40:280–284. 2011. View Article : Google Scholar : PubMed/NCBI | |
Razvi S, Ingoe L, Keeka G, Oates C, McMillan C and Weaver JU: The beneficial effect of L-thyroxine on cardiovascular risk factors, endothelial function, and quality of life in subclinical hypothyroidism: randomized, crossover trial. J Clin Endocrinol Metab. 92:1715–1723. 2007. View Article : Google Scholar : PubMed/NCBI | |
Adrees M, Gibney J, El-Saeity N and Boran G: Effects of 18 months of l-T4 replacement in women with subclinical hypothyroidism. Clin Endocrinol (Oxf). 71:298–303. 2009. View Article : Google Scholar | |
Cabral MD, Teixeira P, Soares D, Leite S, Salles E and Waisman M: Effects of thyroxine replacement on endothelial function and carotid artery intima-media thickness in female patients with mild subclinical hypothyroidism. Clinics (Sao Paulo). 66:1321–1328. 2011. | |
Pasqualetti G, Tognini S, Polini A, Caraccio N and Monzani F: Is subclinical hypothyroidism a cardiovascular risk factor in the elderly? J Clin Endocrinol Metab. 98:2256–2266. 2013. View Article : Google Scholar : PubMed/NCBI | |
Razvi S, Weaver JU, Butler TJ and Pearce SH: Levothyroxine treatment of subclinical hypothyroidism, fatal and nonfatal cardiovascular events, and mortality. Arch Intern Med. 178:811–817. 2012. | |
Cooper DS: Clinical practice. Subclinical hypothyroidism. N Engl J Med. 345:260–265. 2001. View Article : Google Scholar : PubMed/NCBI |