Triiodothyronine potentiates vasorelaxation via pkG/VASP signaling in vascular smooth muscle cells

Cellular Physiology and Biochemistry

Volumn 41, Issue 5, 2017, Pages 1894-1904

  Samuel, Sherin ^a   Zhang, Kuo ^b   Tang, Yi Da ^b   Gerdes, A Martin ^c   Carrillo Sepulveda, Maria Alicia ^c  

^a NEW YORK INSTITUTE OF TECHNOLOGY   (United States)

^b FUWAI HOSPITAL   (China)

^c NEW YORK INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Endothelial cell; Non genomic effect; p VASP; PKG; Triiodothyronine (T3); Vascular smooth muscle cell; Vasorelaxation

Indexed keywords

ACETYLCHOLINE; CYCLIC GMP DEPENDENT PROTEIN KINASE; LIOTHYRONINE; NITRIC OXIDE; PROTEIN KINASE B; VASODILATOR STIMULATED PHOSPHOPROTEIN; ACTIN BINDING PROTEIN; CELL ADHESION MOLECULE; PHOSPHOPROTEIN; VASODILATOR-STIMULATED PHOSPHOPROTEIN;

ANIMAL CELL; AORTIC ENDOTHELIAL CELL; ARTICLE; BLOOD VESSEL REACTIVITY; CONCENTRATION RESPONSE; HUMAN; HUMAN CELL; MALE; MYOGRAPHY; NATIONAL HEALTH ORGANIZATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; THORACIC AORTA; VASCULAR SMOOTH MUSCLE CELL; VASODILATATION; WESTERN BLOTTING; ANIMAL; CELL LINE; DRUG EFFECTS; METABOLISM; SMOOTH MUSCLE CELL; SPRAGUE DAWLEY RAT; VASCULAR SMOOTH MUSCLE;

ANIMALS; CELL ADHESION MOLECULES; CELL LINE; CYCLIC GMP-DEPENDENT PROTEIN KINASES; HUMANS; MALE; MICROFILAMENT PROTEINS; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; PHOSPHOPROTEINS; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; TRIIODOTHYRONINE; VASODILATION;

EID: 85017140934     PISSN: 10158987     EISSN: 14219778     Source Type: Journal    
DOI: 10.1159/000471938     Document Type: Article

References (44)

1. Klein I, Ojamaa K: Thyroid hormone and the cardiovascular system. N Engl J Med 2001;344:501-509.
2. Klein I, Danzi S: Thyroid disease and the heart. Circulation 2007;116:1725-1735.
3. Jabbar A, Pingitore A, Pearce SH, Zaman A, Iervasi G, Razvi S: Thyroid hormones and cardiovascular disease. Nat Rev Cardiol 2017;14:39-55.
4. 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.
5. Sabatino L, Lubrano V, Balzan S, Kusmic C, Del Turco S, Iervasi G: Thyroid hormone deiodinases D1, D2, and D3 are expressed in human endothelial dermal microvascular line: Effects of thyroid hormones. Mol Cell Biochem 2015;399:87-94.
6. Pol CJ, Muller A, Zuidwijk MJ, van Deel ED, Kaptein E, Saba A, Marchini M, Zucchi R, Visser TJ, Paulus WJ, Duncker DJ, Simonides WS: Left-ventricular remodeling after myocardial infarction is associated with a cardiomyocyte-specific hypothyroid condition. Endocrinology 2011;152:669-679.
7. Weltman NY, Pol CJ, Zhang Y, Wang Y, Koder A, Raza S, Zucchi R, Saba A, Colligiani D, Gerdes AM: Long-term physiological T3 supplementation in hypertensive heart disease in rats. Am J Physiol Heart Circ Physiol 2015;309:H1059-1065.
8. Weltman NY, Ojamaa K, Schlenker EH, Chen YF, Zucchi R, Saba A, Colligiani D, Rajagopalan V, Pol CJ, Gerdes AM: Low-dose T(3) replacement restores depressed cardiac T(3) levels, preserves coronary microvasculature and attenuates cardiac dysfunction in experimental diabetes mellitus. Mol Med 2014;20:302-312.
9. Gerdes AM, Ojamaa K: Thyroid Hormone and Cardioprotection. Compr Physiol 2016;6:1199-1219.
10. Cai Y, Manio MM, Leung GP, Xu A, Tang EH, Vanhoutte PM: Thyroid hormone affects both endothelial and vascular smooth muscle cells in rat arteries. Eur J Pharmacol 2015;747:18-28.
11. Ojamaa K, Klemperer JD, Klein I: Acute effects of thyroid hormone on vascular smooth muscle. Thyroid 1996;6:505-512.
12. Yoneda K, Takasu N, Higa S, Oshiro C, Oshiro Y, Shimabukuro M, Asahi T: Direct effects of thyroid hormones on rat coronary artery: nongenomic effects of triiodothyronine and thyroxine. Thyroid 1998;8:609-613.
13. Carrillo-Sepulveda MA, Ceravolo GS, Fortes ZB, Carvalho MH, Tostes RC, Laurindo FR, Webb RC, Barreto- Chaves ML: Thyroid hormone stimulates NO production via activation of the PI3K/Akt pathway in vascular myocytes. Cardiovasc Res 2010;85:560-570.
14. van Mullem AA, van Gucht AL, Visser WE, Meima ME, Peeters RP, Visser TJ: Effects of thyroid hormone transporters MCT8 and MCT10 on nuclear activity of T3. Mol Cell Endocrinol 2016;437:252-260.
15. Cheng SY, Leonard JL, Davis PJ: Molecular aspects of thyroid hormone actions. Endocr Rev 2010;31:139-170.
16. Chettimada S, Rawat DK, Dey N, Kobelja R, Simms Z, Wolin MS, Lincoln TM, Gupte SA: Glc-6-PD and PKG contribute to hypoxia-induced decrease in smooth muscle cell contractile phenotype proteins in pulmonary artery. Am J Physiol Lung Cell Mol Physiol 2012;303:L64-74.
17. 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.
18. Neo BH, Kandhi S, Wolin MS: Roles for soluble guanylate cyclase and a thiol oxidation-elicited subunit dimerization of protein kinase G in pulmonary artery relaxation to hydrogen peroxide. Am J Physiol Heart Circ Physiol 2010;299:H1235-1241.
19. Sausbier M, Schubert R, Voigt V, Hirneiss C, Pfeifer A, Korth M, Kleppisch T, Ruth P, Hofmann F: Mechanisms of NO/cGMP-dependent vasorelaxation. Circ Res 2000;87:825-830.
20. 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.
21. Davel AP, Victorio JA, Delbin MA, Fukuda LE, Rossoni LV: Enhanced endothelium-dependent relaxation of rat pulmonary artery following beta-adrenergic overstimulation: Involvement of the NO/cGMP/VASP pathway. Life Sci 2015;125:49-56.
22. Schafer A, Burkhardt M, Vollkommer T, Bauersachs J, Munzel T, Walter U, Smolenski A: Endothelium-dependent and -independent relaxation and VASP serines 157/239 phosphorylation by cyclic nucleotide-elevating vasodilators in rat aorta. Biochem Pharmacol 2003;65:397-405.
23. Pfeifer A, Klatt P, Massberg S, Ny L, Sausbier M, Hirneiss C, Wang GX, Korth M, Aszodi A, Andersson KE, Krombach F, Mayerhofer A, Ruth P, Fassler R, Hofmann F: Defective smooth muscle regulation in cGMP kinase I-deficient mice. EMBO J 1998;17:3045-3051.
24. Zhong X, Wang Y, Wu J, Sun A, Yang F, Zheng D, Li T, Dong S, Zhao Y, Yang G, Xu C, Sun D, Lu F, Zhang W: Calcium sensing receptor regulating smooth muscle cells proliferation through initiating cystathionine-gamma-lyase/hydrogen sulfide pathway in diabetic rat. Cell Physiol Biochem 2015;35:1582-1598.
25. Huang K, Yan ZQ, Zhao D, Chen SG, Gao LZ, Zhang P, Shen BR, Han HC, Qi YX, Jiang ZL: SIRT1 and FOXO Mediate Contractile Differentiation of Vascular Smooth Muscle Cells under Cyclic Stretch. Cell Physiol Biochem 2015;37:1817-1829.
26. Ranek MJ, Terpstra EJ, Li J, Kass DA, Wang X: Protein kinase g positively regulates proteasome-mediated degradation of misfolded proteins. Circulation 2013;128:365-376.
27. Hesabi B, Danziger RS, Kotlo KU: Heterogeneous nuclear ribonucleoprotein A1 is a novel cellular target of atrial natriuretic peptide signaling in renal epithelial cells. Cell Signal 2012;24:1100-1108.
28. Zeng Y, Pan Y, Liu H, Kang K, Wu Y, Hui G, Peng W, Ramchandran R, Raj JU, Gou D: MiR-20a regulates the PRKG1 gene by targeting its coding region in pulmonary arterial smooth muscle cells. FEBS Lett 2014;588:4677-4685.
29. Fulton D, Gratton JP, McCabe TJ, Fontana J, Fujio Y, Walsh K, Franke TF, Papapetropoulos A, Sessa WC: Regulation of endothelium-derived nitric oxide production by the protein kinase Akt. Nature 1999;399:597-601.
30. Palmer RM, Ashton DS, Moncada S: Vascular endothelial cells synthesize nitric oxide from L-arginine. Nature 1988;333:664-666.
31. Ibarra-Alvarado C, Galle J, Melichar VO, Mameghani A, Schmidt HH: Phosphorylation of blood vessel vasodilator-stimulated phosphoprotein at serine 239 as a functional biochemical marker of endothelial nitric oxide/cyclic GMP signaling. Mol Pharmacol 2002;61:312-319.
32. Napoli R, Guardasole V, Angelini V, Zarra E, Terracciano D, D'Anna C, Matarazzo M, Oliviero U, Macchia V, Sacca L: Acute effects of triiodothyronine on endothelial function in human subjects. J Clin Endocrinol Metab 2007;92:250-254.
33. 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.
34. Lin CS, Liu X, Tu R, Chow S, Lue TF: Age-related decrease of protein kinase G activation in vascular smooth muscle cells. Biochem Biophys Res Commun 2001;287:244-248.
35. Li L, Hu M, Zheng L, Zhang C, Li J, Rong R, Zhu T, Jia Y: Endothelin Receptor Down-Regulation Mediated Ligand Regulation Mechanisms Protect Against Cellular Hypoxia Injury in Rat Vascular Endothelial Cells. Cell Physiol Biochem 2016;40:1443-1454.
36. Monteiro FS, Silva AC, Martins IR, Correia AC, Basilio IJ, Agra MF, Bhattacharyya J, Silva BA: Vasorelaxant action of the total alkaloid fraction obtained from Solanum paludosum Moric. (Solanaceae) involves NO/ cGMP/PKG pathway and potassium channels. J Ethnopharmacol 2012;141:895-900.
37. Yao X, Kwan HY, Chan FL, Chan NW, Huang Y: A protein kinase G-sensitive channel mediates flow-induced Ca(2+) entry into vascular endothelial cells. FASEB J 2000;14:932-938.
38. Edwards A, Cao C, Pallone TL: Cellular mechanisms underlying nitric oxide-induced vasodilation of descending vasa recta. Am J Physiol Renal Physiol 2011;300:F441-456.
39. Fellner SK, Arendshorst WJ: Complex interactions of NO/cGMP/PKG systems on Ca2+ signaling in afferent arteriolar vascular smooth muscle. Am J Physiol Heart Circ Physiol 2010;298:H144-151.
40. Moncada S, Higgs EA: The discovery of nitric oxide and its role in vascular biology. Br J Pharmacol 2006;147:S193-201.
41. Lincoln TM: Myosin phosphatase regulatory pathways: Different functions or redundant functions?. Circ Res 2007;100:10-12.
42. Holt AW, Martin DN, Shaver PR, Adderley SP, Stone JD, Joshi CN, Francisco JT, Lust RM, Weidner DA, Shewchuk BM, Tulis DA: Soluble guanylyl cyclase-activated cyclic GMP-dependent protein kinase inhibits arterial smooth muscle cell migration independent of VASP-serine 239 phosphorylation. Cell Signal 2016;28:1364-1379.
43. Murthy KS: CAMP inhibits IP(3)-dependent Ca(2+) release by preferential activation of cGMP-primed PKG. Am J Physiol Gastrointest Liver Physiol 2001;281:G1238-1245.
44. Bonifacino JS, Weissman AM: Ubiquitin and the control of protein fate in the secretory and endocytic pathways. Annu Rev Cell Dev Biol 1998;14:19-57.