Thyroid hormone stimulates NO production via activation of the PI3K/Akt pathway in vascular myocytes

Cardiovascular Research

Volumn 85, Issue 3, 2010, Pages 560-570

  Carrillo Sepúlveda, Maria Alícia ^a,b   Ceravolo, Graziela S ^a   Fortes, Zuleica Bruno ^a   Carvalho, Maria Helena ^a   Tostes, Rita C ^a,b   Laurindo, Francisco R ^a   Webb, R Clinton ^b   Barreto Chaves, Maria Luiza M ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

Nitric oxide; Non genomic actions; PI3K Akt pathway; Relaxation; Thyroid hormone; Vascular smooth muscle cell

Indexed keywords

LIOTHYRONINE; MYOSIN LIGHT CHAIN; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; PHENYLEPHRINE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; ENZYME PHOSPHORYLATION; IMMUNOCYTOCHEMISTRY; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; SMOOTH MUSCLE FIBER; VASCULAR RING; VASCULAR SMOOTH MUSCLE; WESTERN BLOTTING;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; CELLS, CULTURED; ENDOTHELIUM, VASCULAR; MALE; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; MYOSIN LIGHT CHAINS; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; PHENYLEPHRINE; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, WISTAR; SIGNAL TRANSDUCTION; THYROID HORMONES; VASOCONSTRICTION;

EID: 74249095308     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvp304     Document Type: Article

References (47)

1. Kahaly GJ, Dillmann WH. Thyroid hormone action in the heart. Endocr Rev 2005; 26:704-728.
2. Celsing F, Blomstrand E, Melichna J, Terrados N, Clausen N, Lins PE et al. Effect of hyperthyroidism on fibre-type composition, fibre area, glycogen content and enzyme activity in human skeletal muscle. Clin Physiol 1986;6:171-181.
3. Capo LA, Sillau AH. The effect of hyperthyroidism on capillarity and oxidative capacity in rat soleus and gastrocnemius muscles. J Physiol 1983;342:1-14.
4. Anjos-Ramos L, Carneiro-Ramos MS, Diniz GP, Martins-Silva J, Barreto-Chaves ML. Early cardiac hypertrophy induced by thyroxine is accompanied by an increase in VEGF-A expression but not by an increase in capillary density. Virchows Archiv 2006;448:472-479.
5. Park KW, Dai HB, Ojamaa K, Lowenstein E, Klein I, Sellke FW. The direct vaso-motor effect of thyroid hormones on rat skeletal muscle resistance arteries. Anesth Analg 1997;85:734-738.
6. Napoli R, Biondi B, Guardasole V, Matarazzo M, Pardo F, Angelini V et al. Impact of hyperthyroidism and its correction on vascular reactivity in humans. Circulation 2001;104:3076-3080.
7. McAllister RM, Grossenburg VD, Delp MD, Laughlin MH. Effects of hyperthyroid-ism on vascular contractile and relaxation responses. Am J Physiol 1998;274: E946-E953.
8. McAllister RM, Luther KL, Pfeifer PC. Thyroid status and response to endothelin-1 in rat arterial vessels. Am J Physiol 2000;279:E252-E258.
9. Ojamaa K, Klemperer JD, Klein I. Acute effects of thyroid hormone on vascular smooth muscle. Thyroid 1996;6:505-512.
10. Hashimoto T, Kihara M, Ishida J, Imai N, Yoshida S, Toya Y et al. Apelin stimulates myosin light chain phosphorylation in vascular smooth muscle cells. Arterioscler Thromb Vasc Biol 2006;26:1267-1272.
11. Hathaway DR, March KL, Lash JA, Adam LP, Wilensky RL. Vascular smooth muscle. A review of the molecular basis of contractility. Circulation 1991;83: 382-390.
12. Lee JH, Xia S, Ragolia L. Upregulation of AT2 receptor and iNOS impairs angio-tensin II-induced contraction without endothelium influence in young normoten-sive diabetic rats. Am J Physiol 2008;295:R144-R154.
13. McAllister RM, Albarracin I, Price EM, Smith TK, Turk JR, Wyatt KD. Thyroid status and nitric oxide in rat arterial vessels. J Endocrinol 2005;185:111-119.
14. Ojamaa K, Kenessey A, Klein I. Thyroid hormone regulation of phospholamban phosphorylation in the rat heart. Endocrinology 2000;141:2139-2144.
15. Yen PM. Physiological and molecular basis of thyroid hormone action. Physiol Rev 2001;81:1097-1142.
16. Nadaud S, Philippe M, Arnal JF, Michel JB, Soubrier F. Sustained increase in aortic endothelial nitric oxide synthase expression in vivo in a model of chronic high blood flow. Circ Res 1996;79:857-863.
17. Davis PJ, Leonard JL, Davis FB. Mechanisms of nongenomic actions of thyroid hormone. Front Neuroendocrinol 2008;29:211-218.
18. Klemperer JD, Klein I, Gomez M, Helm RE, Ojamaa K, Thomas SJ et al. Thyroid hormone treatment after coronary-artery bypass surgery. N Engl J Med 1995; 333:1522-1527.
19. Kapitola J, Vilimovska D. Inhibition of the early circulatory effects of triiodothyr-onine in rats by propranolol. Physiologia Bohemoslovaca 1981;30:347-351.
20. Klemperer JD, Zelano J, Helm RE, Berman K, Ojamaa K, Klein I et al. Triiodothyr-onine improves left ventricular function without oxygen wasting effects after global hypothermic ischemia. J Thorac Cardiovasc Surg 1995;109:457-465.
21. Han G, Ma H, Chintala R, Miyake K, Fulton DJ, Barman SA et al. Nongenomic, endothelium-independent effects of estrogen on human coronary smooth muscle are mediated by type I (neuronal) NOS and PI3-kinase-Akt signaling. Am J Physiol 2007;293:H314-H321.
22. Ross R. The smooth muscle cell. II. Growth of smooth muscle in culture and formation of elastic fibers. J Cell Biol 1971;50:172-186.
23. Foster FM, Traer CJ, Abraham SM, Fry MJ. The phosphoinositide (PI) 3-kinase family. J Cell Sci 2003;116:3037-3040.
24. Lee JH, Ragolia L. AKT phosphorylation is essential for insulin-induced relaxation of rat vascular smooth muscle cells. Am J Physiol 2006;291:C1355-C1365.
25. Alves GM, Barao MA, Odo LN, Nascimento Gomes G, Franco M C, Nigro D et al. L-Arginine effects on blood pressure and renal function of intrauterine restricted rats. Pediatr Nephrol 2002;17:856-862.
26. Formoso G, Chen H, Kim JA, Montagnani M, Consoli A, Quon MJ. Dehydroepian-drosterone mimics acute actions of insulin to stimulate production of both nitric oxide and endothelin 1 via distinct phosphatidylinositol 3-kinase-and mitogen-activated protein kinase-dependent pathways in vascular endothelium. Mol Endo-crinol 2006;20:1153-1163.
27. Nakatsubo N, Kojima H, Kikuchi K, Nagoshi H, Hirata Y, Maeda D et al. Direct evidence of nitric oxide production from bovine aortic endothelial cells using new fluorescence indicators: diaminofluoresceins. FEBS Lett 1998;427:263-266.
28. Montagnani M, Chen H, Barr VA, Quon MJ. Insulin-stimulated activation of eNOS is independent of Ca2+ but requires phosphorylation by Akt at Ser(1179). J Biol Chem 2001;276:30392-30398.
29. Worth NF, Rolfe BE, Song J, Campbell GR. Vascular smooth muscle cell pheno-typic modulation in culture is associated with reorganization of contractile and cytoskeletal proteins. Cell Motil Cytoskeleton 2001;49:130-145.
30. Diniz GP, Carneiro-Ramos MS, Barreto-Chaves ML. Angiotensin type 1 (AT1) and type 2 (AT2) receptors mediate the increase in TGF-beta1 in thyroid hormone-induced cardiac hypertrophy. Pflugers Arch 2007;454:75-81.
31. Skalli O, Bloom WS, Ropraz P, Azzarone B, Gabbiani G. Cytoskeletal remodeling of rat aortic smooth muscle cells in vitro: relationships to culture conditions and analogies to in vivo situations. J Submicrosc Cytol 1986;18:481-493.
32. Owens GK, Loeb A, Gordon D, Thompson MM. Expression of smooth muscle-specific alpha-isoactin in cultured vascular smooth muscle cells: relationship between growth and cytodifferentiation. J Cell Biol 1986;102:343-352.
33. Caruso-Neves C, Kwon SH, Guggino WB. Albumin endocytosis in proximal tubule cells is modulated by angiotensin II through an AT2 receptor-mediated protein kinase B activation. Proc Natl Acad Sci USA 2005;102:17513-17518.
34. Klein I, Ojamaa K. Thyroid hormone and the cardiovascular system. N Engl J Med 2001;344:501-509.
35. Hiroi Y, Kim HH, Ying H, Furuya F, Huang Z, Simoncini T et al. Rapid nongenomic actions of thyroid hormone. Proc Natl Acad Sci USA 2006;103:14104-14109.
36. Tamajusuku AS, Carrillo-Sepulveda MA, Braganhol E, Wink MR, Sarkis JJ, Barreto-Chaves ML et al. Activity and expression of ecto-5'-nucleotidase/CD73 are increased by thyroid hormones in vascular smooth muscle cells. Mol Cell Biochem 2006;289:65-72.
37. Zhu Z, Arendshorst WJ. Angiotensin II-receptor stimulation of cytosolic calcium concentration in cultured renal resistance arterioles. Am J Physiol 1996;271: F1239-F1247.
38. Yan C, Kim D, Aizawa T, Berk BC. Functional interplay between angiotensin II and nitric oxide: cyclic GMP as a key mediator. Arterioscler Thromb Vasc Biol 2003;23: 26-36.
39. Schini-Kerth VB, Vanhoutte PM. Nitric oxide synthases in vascular cells. Exp Physiol 1995;80:885-905.
40. Kleinert H, Pautz A, Linker K, Schwarz PM. Regulation of the expression of indu-cible nitric oxide synthase. Eur J Pharmacol 2004;500:255-266.
41. Kuo PC, Schroeder RA. The emerging multifaceted roles of nitric oxide. Ann Surg 1995;221:220-235.
42. Hattori Y, Hattori S, Kasai K. Lipopolysaccharide activates Akt in vascular smooth muscle cells resulting in induction of inducible nitric oxide synthase through nuclear factor-kappa B activation. Eur J Pharmacol 2003;481:153-158.
43. Mizuma H, Murakami M, Mori M. Thyroid hormone activation in human vascular smooth muscle cells. Circ Res 2001;88:313-318.
44. Davis PJ, Leonard JL, Davis FB. Mechanims of nongenomic actions of thyroid hormone. Front Neuroendocrinol 2008;29:211-218.
45. Kuzman JA, Vogelsang KA, Thomas TA, Gerdes AM. L-thyroxine activates Akt signaling in the heart. J Mol Cell Cardiol 2005;39:251-258.
46. Diniz GP, Carneiro-Ramos MS, Barreto-Chaves ML. Angiotensin Type 1 receptor mediates thyroid hormone-induced cardiomyocytes hypertrophy through the Akt/GSK-3beta/mTOR signaling pathway. Basic Res Cardiol 2009; epub ahead of print July 2009, doi: 10.1007/s00395-009-0043-1.
47. Scivoletto R, Fortes ZB, Garcia-Leme J. Thyroid hormones and vascular reactivity: role of endothelial cell. Eur J Pharmacol 1986;129:271-278.