Type 2 iodothyronine deiodinase activity is required for rapid stimulation of PI3K by thyroxine in human umbilical vein endothelial cells

Endocrinology

Volumn 156, Issue 11, 2015, Pages 4312-4324

  Aoki, Tomoyuki ^a   Tsunekawa, Katsuhiko ^a   Araki, Osamu ^a   Ogiwara, Takayuki ^a   Nara, Makoto ^a   Sumino, Hiroyuki ^a   Kimura, Takao ^a   Murakami, Masami ^a  

^a GUNMA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP; IOPANOIC ACID; LIOTHYRONINE; OXIDOREDUCTASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; RAC1 PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SMALL INTERFERING RNA; THYROXINE; TYPE 2 IODOTHYRONINE DEIODINASE; UNCLASSIFIED DRUG; IODIDE PEROXIDASE; IODOTHYRONINE DEIODINASE TYPE II; THYROID HORMONE RECEPTOR ALPHA;

ARTICLE; CELL MIGRATION; CONTROLLED STUDY; DEIODINATION; ENZYME ACTIVITY; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; STIMULATION; UMBILICAL VEIN ENDOTHELIAL CELL; CELL CULTURE; CELL MOTION; DRUG EFFECTS; GENETICS; METABOLISM; PHOSPHORYLATION; SIGNAL TRANSDUCTION;

CELL MOVEMENT; CELLS, CULTURED; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; IODIDE PEROXIDASE; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; RAC1 GTP-BINDING PROTEIN; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; THYROID HORMONE RECEPTORS ALPHA; THYROXINE; TRIIODOTHYRONINE;

EID: 84946075053     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2014-1988     Document Type: Article

References (45)

1. Klein I, Ojamaa K. Thyroid hormone and the cardiovascular system. N Engl J Med. 2001;344:501-509.
2. Ojamaa K, Klemperer JD, Klein I. Acute effects of thyroid hormone on vascular smooth muscle. Thyroid. 1996;6:505-512.
3. Carrillo-Sepúlveda MA, Ceravolo GS, Fortes ZB, et al. Thyroid hormone stimulates NO production via activation of the PI3K/Akt pathway in vascular myocytes. Cardiovasc Res. 2010;85:560-570.
4. Cheng SY, Leonard JL, Davis PJ. Molecular aspects of thyroid hormone actions. Endocr Rev. 2010;31:139-170.
5. Botta JA, de Mendoza D, Morero RD, Farías RN. High affinity L-triiodothyronine binding sites on washed rat erythrocyte membranes. J Biol Chem. 1983;258:6690-6692.
6. Bergh JJ, Lin HY, Lansing L, et al. Integrin alphaVbeta3 contains a cell surface receptor site for thyroid hormone that is linked to activation of mitogen-Activated protein kinase and induction of angio-genesis. Endocrinology. 2005;146:2864-2871.
7. Davis PJ, Davis FB, Mousa SA, Luidens MK, Lin HY. Membrane receptor for thyroid hormone: physiologic and pharmacologic implications. Annu Rev Pharmacol Toxicol. 2011;51:99-115.
8. Storey NM, O'Bryan JP, Armstrong DL. Rac and Rho mediate opposing hormonal regulation of the ether-A-go-go-related potassium channel. Curr Biol. 2002;12:27-33.
9. Vicinanza R, Coppotelli G, Malacrino C, Nardo T, Buchetti B, Lenti L, Celi FS, Scarpa S. Oxidized low-density lipoproteins impair endothelial function by inhibiting non-genomic action of thyroid hormone-mediated nitric oxide production in human endothelial cells. Thyroid. 2013;23:231-238.
10. Hiroi Y, Kim HH, Ying H, Furuya F, Huang Z, Simoncini T, Noma K, Ueki K, Nguyen NH, Scanlan TS, Moskowitz MA, Cheng SY, Liao JK. Rapid nongenomic actions of thyroid hormone. Proc Natl Acad Sci USA. 2006;103:14104-14109.
11. Cao X, Kambe F, Moeller LC, Refetoff S, Seo H. Thyroid hormone induces rapid activation of Akt/protein kinase B-mammalian target of rapamycin-p70S6K cascade through phosphatidylinositol 3-ki-nase in human fibroblasts. Mol Endocrinol. 2005;19:102-112.
12. Gauthier KF. Nongenomic, TR/3-dependent, thyroid hormone response gets genetic support. Endocrinology. 2014;155:3206-3209.
13. Martin NP, Marron Fernandez de Velasco E, Mizuno F, et al. A rapid cytoplasmic mechanism for PI3 kinase regulation by the nuclear thyroid hormone receptor, TR/3, and genetic evidence for its role in the maturation of mouse hippocampal synapses in vivo. Endocrinology. 2014;155:3713-3724.
14. Kalyanaraman H, Schwappacher R, Joshua J, et al. Nongenomic thyroid hormone signaling occurs through a plasma membrane-localized receptor. Sci Signal. 2014;7:ra48.
15. Nagata D, Mogi M, Walsh K. AMP-Activated protein kinase (AMPK) signaling in endothelial cells is essential for angiogenesis in response to hypoxic stress. J Biol Chem. 2003;278:31000-31006.
16. Dormond O, Foletti A, Paroz C, Rüegg C. NSAIDs inhibit alpha V beta 3 integrin-mediated and Cdc42/Rac-dependent endothelial-cell spreading, migration and angiogenesis. Nat Med. 2001;7:1041-1047.
17. Takashima S, Sugimoto N, Takuwa N, et al. G12/13 and Gq mediate S1P2-induced inhibition of Rac and migration in vascular smooth muscle in a manner dependent on Rho but not Rho kinase. Cardiovasc Res. 2008;79:689-697.
18. Okamoto H, Takuwa N, Yokomizo T, et al. Inhibitory regulation of Rac activation, membrane ruffling, and cell migration by the G protein-coupled sphingosine-1-phosphate receptor EDG5 but not EDG1 or EDG3. Mol Cell Biol. 2000;20:9247-9261.
19. Zvibel I, Atias D, Phillips A, Halpern Z, Oren R. Thyroid hormones induce activation of rat hepatic stellate cells through increased expression of p75 neurotrophin receptor and direct activation of Rho. Lab Invest. 2010;90:674-684.
20. Bianco AC, Salvatore D, Gereben B, Berry MJ, Larsen PR. Biochemistry, cellular and molecular biology, and physiological roles of the iodothyronine selenodeiodinases. Endocr Rev. 2002;23:38-89.
21. Davey JC, Becker KB, Schneider MJ, St Germain DL, Galton VA. Cloning of a cDNA for the type II iodothyronine deiodinase. J Biol Chem. 1995;270:26786-26789.
22. Croteau W, Davey JC, Galton VA, St Germain DL. Cloning of the mammalian type II iodothyronine deiodinase. A selenoprotein differentially expressed and regulated in human and rat brain and other tissues. J Clin Invest. 1996;98:405-417.
23. Salvatore D, Bartha T, Harney JW, Larsen PR. Molecular biological and biochemical characterization of the human type 2 selenodeio-dinase. Endocrinology. 1996;137:3308-3315.
24. Salvatore D, Tu H, Harney JW, Larsen PR. Type 2 iodothyronine deiodinase is highly expressed in human thyroid. J Clin Invest. 1996; 98:962-968.
25. Mizuma H, Murakami M, Mori M. Thyroid hormone activation in human vascular smooth muscle cells: Expression of type II iodothyronine deiodinase. Circ Res. 2001;88:313-318.
26. Ishikawa T, Chijiwa T, Hagiwara M, Mamiya S, Hidaka H. Thyroid hormones directly interact with vascular smooth muscle strips. Mol Pharmacol. 1989;35:760-765.
27. Zwaveling J, Pfaffendorf M, van Zwieten PA. The direct effects of thyroid hormones on rat mesenteric resistance arteries. Fundam Clin Pharmacol. 1997;11:41-46.
28. Park KW, Dai HB, Ojamaa K, Lowenstein E, Klein I, Sellke FW. The direct vasomotor effect of thyroid hormones on rat skeletal muscle resistance arteries. Anesth Analg. 1997;85:734-738.
29. Leonard JL, Rosenberg IN. Iodothyronine 5'-deiodinase from rat kidney: Substrate specificity and the 5'-deiodination of reverse triiodothyronine. Endocrinology. 1980;107:1376-1383.
30. Murakami M, Tanaka K, Greer MA, Mori M. Anterior pituitary type II thyroxine 5'-deiodinase activity is not affected by lesions of the hypothalamic paraventricular nucleus which profoundly depress pituitary thyrotropin secretion. Endocrinology. 1988;123: 1676-1681.
31. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976;72:248-254.
32. Richard K, Hume R, Kaptein E, et al. Ontogeny of iodothyronine deiodinases in human liver. J Clin Endocrinol Metab. 1998;83: 2868-2874.
33. Morimura T, Tsunekawa K, Kasahara T, et al. Expression of type 2 iodothyronine deiodinase in human osteoblast is stimulated by thyrotropin. Endocrinology. 2005;146:2077-2084.
34. Bornfeldt KE, Graves LM, Raines EW, et al. Sphingosine-1-phosphate inhibits PDGF-induced chemotaxis of human arterial smooth muscle cells: Spatial and temporal modulation of PDGF chemotactic signal transduction. J Cell Biol. 1995;130:193-206.
35. Cao X, Kambe F, Yamauchi M, Seo H. Thyroid-hormone-dependent activation of the phosphoinositide 3-kinase/Akt cascade requires Src and enhances neuronal survival. Biochem J. 2009;424: 201-209.
36. Lin HY, Sun M, Tang HY, et al. L-Thyroxine vs. 3, 5, 3'-triiodo-L-thyronine and cell proliferation: Activation of mitogen-Activated protein kinase and phosphatidylinositol 3-kinase. Am J Physiol Cell Physiol. 2009;296:C980-C991.
37. Ojamaa K. Signaling mechanisms in thyroid hormone-induced cardiac hypertrophy. Vascul Pharmacol. 2010;52:113-119.
38. Zamoner A, Funchal C, Jacques-Silva MC, Gottfried C, Barreto Silva FR, Pessoa-Pureur R. Thyroid hormones reorganize the cyto-skeleton of glial cells through Gfap phosphorylation and Rhoa-de-pendent mechanisms. Cell Mol Neurobiol. 2007;27:845-865.
39. Kasahara T, Tsunekawa K, Seki K, Mori M, Murakami M. Regulation of iodothyronine deiodinase and roles of thyroid hormones in human coronary artery smooth muscle cells. Atherosclerosis. 2006; 186:207-214.
40. Ohba K, Yoshioka T, Muraki T. Identificationof two novel splicing variants of human type II iodothyronine deiodinase mRNA. Mol Cell Endocrinol. 2001;172:169-175.
41. Dirks WG, Drexler HG, MacLeod RA. ECV304 (endothelial) is really T24 (bladder carcinoma): Cell line cross-contamination at source. In Vitro Cell Dev Biol. 1999;35:558-559.
42. Huang SA, Dorfman DM, Genest DR, Salvatore D, Larsen PR. Type 3 iodothyronine deiodinase is highly expressed in the human uteroplacental unit and in fetal epithelium. J Clin Endocrinol Metab. 2003;88:1384-1388.
43. Koenig RJ. Regulation of thyroxine 5'-deiodinase by thyroid hormones and activators of protein kinase C in GH4C1 cells. Endocrinology. 1986;118:1491-1497.
44. Dumitrescu AM, Liao XH, Abdullah MS, et al. Mutations in SE-CISBP2 result in abnormal thyroid hormone metabolism. Nat Genet. 2005;37:1247-1252.
45. Billon C, Canaple L, Fleury S, et al. TRa protects against atherosclerosis in male mice: Identification of a novel anti-inflammatory property for TRa in mice. Endocrinology. 2014;155:2735-2745.