Involvement of nitric oxide in iodine deficiency-induced microvascular remodeling in the thyroid gland: Role of nitric oxide synthase 3 and ryanodine receptors

Endocrinology (United States)

Volumn 156, Issue 2, 2015, Pages 707-720

  Craps, J ^a   Wilvers, C ^a   Joris, V ^a   De Jongh, B ^a   Vanderstraeten, J ^a   Lobysheva, I ^a   Balligand, J L ^a   Sonveaux, P ^a   Gilon, P ^a   Many, M C ^a   Gerard A C ^b   Colin, I M ^a,b  

^a U d'Endocrinologie et Metabolisme   (Belgium)

^b Centre Hospitalier Régional   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

BEVACIZUMAB; CALCIUM; ENDOTHELIAL NITRIC OXIDE SYNTHASE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MESSENGER RNA; N ACETYL S NITROSOPENICILLAMINE; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; RYANODINE; RYANODINE RECEPTOR; RYANODINE RECEPTOR 1; RYANODINE RECEPTOR 2; THAPSIGARGIN; VASCULOTROPIN A; IODINE; REACTIVE OXYGEN METABOLITE;

ANIMAL CELL; ARTICLE; CALCIUM TRANSPORT; CONTROLLED STUDY; ENZYME ACTIVATION; FEMALE; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IN VITRO STUDY; IN VIVO STUDY; IODINE DEFICIENCY; MALE; MICROVASCULARIZATION; NONHUMAN; ORGAN BLOOD FLOW; PRIMARY CULTURE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; THYROID BLOOD FLOW; THYROID CELL; ANIMAL; CELL LINE; DEFICIENCY; METABOLISM; MOUSE; THYROID GLAND; VASCULARIZATION;

ANIMALS; CALCIUM; CELL LINE; FEMALE; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; IODINE; MALE; MICE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; RATS; REACTIVE OXYGEN SPECIES; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL; THYROID GLAND; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84921635388     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2014-1729     Document Type: Article

References (62)

1. Kopp PA. Reduce, recycle, reuse-iodotyrosine deiodinase in thyroid iodide metabolism. N Engl J Med. 2008;358:1856-1859.
2. Gnidehou S, Caillou B, Talbot M, et al. Iodotyrosine dehalogenase 1 (DEHAL1) is a transmembrane protein involved in the recycling of iodide close to the thyroglobulin iodination site. FASEB J. 2004; 18:1574-1576.
3. Pedraza PE, Obregon MJ, Escobar-Morreale HF, del Rey FE, de Escobar GM. Mechanisms of adaptation to iodine deficiency in rats: thyroid status is tissue specific. Its relevance for man. Endocrinology. 2006;147:2098-2108.
4. Wollman SH, Herveg JP, Zeligs JD, Ericson LE. Blood capillary enlargement during the development of thyroid hyperplasia in the rat. Endocrinology. 1978;103:2306-2314.
5. Gérard AC, Denef JF, Many MC, et al. Relationships between cell division, expression of growth factors and microcirculation in the thyroids of Tg-A2aR transgenic mice and patients with Graves disease. J Endocrinol. 2003;177:269-277.
6. Gérard AC, Xhenseval V, Colin IM, Many MC, Denef JF. Evidence for co-ordinated changes between vascular endothelial growth factor and nitric oxide synthase III immunoreactivity, the functional status of the thyroid follicles, and the microvascular bed during chronic stimulation by low iodine and propylthiouracyl in old mice. Eur J Endocrinol. 2000;142:651-660.
7. Gérard AC, Many MC, Daumerie C, et al. Structural changes in the angiofollicular units between active and hypofunctioning follicles align with differences in the epithelial expression of newly discovered proteins involved in iodine transport and organification. J Clin Endocrinol Metab. 2002;87:1291-1299.
8. Colin I, Gérard AC. The thyroid angiofollicular units, a biological model of functional and morphological integration. Bull Mem Acad R Med Belg. 2010;165:218-228; discussion 228-230.
9. Colin IM, Denef JF, Lengelé B, Many MC, Gérard AC. Recent insights into the cell biology of thyroid angiofollicular units. Endocr Rev. 2013;34:209-238.
10. Many MC, Denef JF, Gathy P, Haumont S. Morphological and functional changes during thyroid hyperplasia and involution in C3H Mice: evidence for folliculoneogenesis during involution. Endocrinology. 1983;112:1292-1302.
11. Denef JF, Ovaert C, Many MC. [Experimental goitrogenesis]. Ann Endocrinol (Paris). 1989;50:1-15.
12. Ramsden JD, Buchanan MA, Egginton S, Watkinson JC, Mautner V, Eggo MC. Complete inhibition of goiter in mice requires combined gene therapy modification of angiopoietin, vascular endothelial growth factor, and fibroblast growth factor signaling. Endocrinology. 2005;146:2895-2902.
13. Gérard AC, Poncin S, Caetano B, et al. Iodine deficiency induces a thyroid stimulating hormone-independent early phase of microvascular reshaping in the thyroid. Am J Pathol. 2008;172:748-760.
14. Gérard AC, Poncin S, Audinot JN, Denef JF, Colin IM. Iodide deficiency- induced angiogenic stimulus in the thyroid occurs via HIFand ROS-dependent VEGF-A secretion from thyrocytes. Am J Physiol Endocrinol Metab. 2009;296:E1414-E1422.
15. Colin IM, Nava E, Toussaint D, et al. Expression of nitric oxide synthase isoforms in the thyroid gland: evidence for a role of nitric oxide in vascular control during goiter formation. Endocrinology. 1995;136:5283-5290.
16. Colin IM, Kopp P, Zbären J, Häberli A, Grizzle WE, Jameson JL. Expression of nitric oxide synthase III in human thyroid follicular cells: evidence for increased expression in hyperthyroidism. Eur J Endocrinol. 1997;136:649-655.
17. Fusco A, BerlingieriMT,Di Fiore PP, Portella G, Grieco M, Vecchio G. One- and two-step transformations of rat thyroid epithelial cells by retroviral oncogenes. Mol Cell Biol. 1987;7:3365-3370.
18. Zucchi R, Ronca-Testoni S. The sarcoplasmic reticulum Ca2+ channel/ryanodine receptor: modulation by endogenous effectors, drugs and disease states. Pharmacol Rev. 1997;49:1-51.
19. Nilsson M, Husmark J, Nilsson B, Tisell LE, Ericson LE. Primary culture of human thyrocytes in Transwell bicameral chamber: thyrotropin promotes polarization and epithelial barrier function. Eur J Endocrinol. 1996;135:469-480.
20. Bianco AC, Anderson G, Forrest D, et al. American thyroid association guide to investigating thyroid hormone economy and action in rodent and cell models. Thyroid. 2014;24:88-168.
21. Gérard AC, Humblet K, Wilvers C, et al. Iodine-deficiency-induced long lasting angiogenic reaction in thyroid cancers occurs via a vascular endothelial growth factor-hypoxia inducible factor-1-dependent, but not a reactive oxygen species-dependent, pathway. Thyroid. 2012;22:699-708.
22. Frérart F, Lobysheva I, Gallez B, Dessy C, Feron O. Vascular caveolin deficiency supports the angiogenic effects of nitrite, a major end product of nitric oxide metabolism in tumors. Mol Cancer Res. 2009;7:1056-1063.
23. Lobysheva I, Rath G, Sekkali B, et al. Moderate caveolin-1 downregulation prevents NADPH oxidase-dependent endothelial nitric oxide synthase uncoupling by angiotensin II in endothelial cells. Arterioscler Thromb Vasc Biol. 2011;31:2098-2105.
24. Hood JD, Meininger CJ, Ziche M, Granger HJ. VEGF upregulates ecNOS message, protein, andNOproduction in human endothelial cells. Am J Physiol. 1998;274:H1054-H1058.
25. Kimura H, Esumi H. Reciprocal regulation between nitric oxide and vascular endothelial growth factor in angiogenesis. Acta Biochim Pol. 2003;50:49-59.
26. Gentile C, Muise-Helmericks RC, Drake CJ. VEGF-mediated phosphorylation of eNOS regulates angioblast and embryonic endothelial cell proliferation. Dev Biol. 2013;373:163-175.
27. Gélinas DS, Bernatchez PN, Rollin S, Bazan NG, Sirois MG. Immediate and delayed VEGF-mediated NO synthesis in endothelial cells: role of PI3K, PKC and PLC pathways. Br J Pharmacol. 2002; 137:1021-1030.
28. Papapetropoulos A, Garca-Cardeña G, Madri JA, Sessa WC. Nitric oxide production contributes to the angiogenic properties of vascular endothelial growth factor in human endothelial cells. J Clin Invest. 1997;100:3131-3139.
29. Fleming I, Fisslthaler B, Dimmeler S, Kemp BE, Busse R. Phosphorylation of Thr(495) regulates Ca(2-)/calmodulin-dependent endothelial nitric oxide synthase activity. Circ Res. 2001;88:E68-E75.
30. Fisslthaler B, Dimmeler S, Hermann C, Busse R, Fleming I. Phosphorylation and activation of the endothelial nitric oxide synthase by fluid shear stress. Acta Physiol Scand. 2000;168:81-88.
31. Lytton J, Westlin M, Hanley MR. Thapsigargin inhibits the sarcoplasmic or endoplasmic reticulum Ca-ATPase family of calcium pumps. J Biol Chem. 1991;266:17067-17071.
32. AnderssonM,Karumbunathan V, ZimmermannMB.Global iodine status in 2011 and trends over the past decade. J Nutr. 2012;142: 744-750.
33. Venturi S, Donati FM, Venturi A, Venturi M, Grossi L, Guidi A. Role of iodine in evolution and carcinogenesis of thyroid, breast and stomach. Adv Clin Path. 2000;4:11-17.
34. Shakhtarin VV, Tsyb AF, Stepanenko VF, Orlov MY, Kopecky KJ, Davis S. Iodine deficiency, radiation dose, and the risk of thyroid cancer among children and adolescents in the Bryansk region of Russia following the Chernobyl power station accident. Int J Epidemiol. 2003;32:584-591.
35. Poncin S, Colin IM, Gérard AC. Minimal oxidative load: a prerequisite for thyroid cell function. J Endocrinol. 2009;201:161-167.
36. Motohashi S, Kasai K, Banba N, Hattori Y, Shimoda S. Nitric oxide inhibits cell growth in cultured human thyrocytes. Life Sci. 1996; 59:L227-L234.
37. Balligand JL, Feron O, Dessy C. eNOS activation by physical forces: from short-term regulation of contraction to chronic remodeling of cardiovascular tissues. Physiol Rev. 2009;89:481-534.
38. van der Zee R, Murohara T, Luo Z, et al. Vascular endothelial growth factor/vascular permeability factor augments nitric oxide release from quiescent rabbit and human vascular endothelium. Circulation. 1997;95:1030-1037.
39. Ziche M, Morbidelli L. Nitric oxide and angiogenesis. J Neurooncol. 2000;50:139-148.
40. Schleicher M, Yu J, Murata T, et al. The Akt1-eNOS axis illustrates the specificity of kinase-substrate relationships in vivo. Sci Signal. 2009;2:ra41.
41. Sessa WC. eNOS at a glance. J Cell Sci. 2004;117:2427-2429.
42. Gielis JF, Lin JY, Wingler K, Van Schil PE, Schmidt HH, Moens AL. Pathogenetic role of eNOS uncoupling in cardiopulmonary disorders. Free Radic Biol Med. 2011;50:765-776.
43. Dimmeler S, Fleming I, Fisslthaler B, Hermann C, Busse R, Zeiher AM. Activation of nitric oxide synthase in endothelial cells by Aktdependent phosphorylation. Nature. 1999;399:601-605.
44. Chin K, Kurashima Y, Ogura T, Tajiri H, Yoshida S, Esumi H. Induction of vascular endothelial growth factor by nitric oxide in human glioblastoma and hepatocellular carcinoma cells. Oncogene. 1997;15:437-442.
45. Simo F, Pagnussat AS, Seo JH, et al. Pro-angiogenic effects of resveratrol in brain endothelial cells: nitric oxide-mediated regulation of vascular endothelial growth factor and metalloproteinases. J Cereb Blood Flow Metab. 2012;32:884-895.
46. Jozkowicz A, Cooke JP, Guevara I, et al. Genetic augmentation of nitric oxide synthase increases the vascular generation of VEGF. Cardiovasc Res. 2001;51:773-783.
47. Ronco MT, Francés D, de Luján Alvarez M, et al. Vascular endothelial growth factor and nitric oxide in rat liver regeneration. Life Sci. 2007;81:750-755.
48. Schneider JC, El Kebir D, Chéreau C, et al. Involvement of Ca2+/ calmodulin-dependent protein kinase II in endothelial NO production and endothelium-dependent relaxation. Am J Physiol Heart Circ Physiol. 2003;284:H2311-H2319.
49. Venema RC, Sayegh HS, Kent JD, Harrison DG. Identification, characterization, and comparison of the calmodulin-binding domains of the endothelial and inducible nitric oxide synthases. J Biol Chem. 1996;271:6435-6440.
50. Sun QA, Hess DT, Nogueira L, et al. Oxygen-coupled redox regulation of the skeletal muscle ryanodine receptor-Ca2+release channel by NADPH oxidase 4. Proc Natl Acad Sci USA. 2011;108: 16098-16103.
51. Kemmerling U, Muñoz P, Mller M, et al. Calcium release by ryanodine receptors mediates hydrogen peroxide-induced activation of ERK and CREB phosphorylation in N2a cells and hippocampal neurons. Cell Calcium. 2007;41:491-502.
52. Sun J, Yamaguchi N, Xu L, Eu JP, Stamler JS, Meissner G. Regulation of the cardiac muscle ryanodine receptor by O(2) tension and S-nitrosoglutathione. Biochemistry. 2008;47:13985-13990.
53. Xu L, Eu JP, Meissner G, Stamler JS. Activation of the cardiac calcium release channel (ryanodine receptor) by poly-S-nitrosylation. Science. 1998;279:234-237.
54. De Deken X, Wang D, Dumont JE, Miot F. Characterization of ThOX proteins as components of the thyroid H(2)O(2)-generating system. Exp Cell Res. 2002;273:187-196.
55. Song Y, Ruf J, Lothaire P, Dequanter D, et al. Association of duoxes with thyroid peroxidase and its regulation in thyrocytes. J Clin Endocrinol Metab 2010;95:375-382.
56. Weyemi U, Caillou B, Talbot M, et al. Intracellular expression of reactive oxygen species-generating NADPH oxidase NOX4 in normal and cancer thyroid tissues. Endocr Relat Cancer. 2010; 17:27-37.
57. Collins Y, Chouchani ET, James AM, Menger KE, Cochemé HM, Murphy MP. Mitochondrial redox signalling at a glance. J Cell Sci. 2012;125:801-806.
58. Kakkar P, Singh BK. Mitochondria: a hub of redox activities and cellular distress control. Mol Cell Biochem. 2007;305:235-253.
59. Franceschi S. Iodine intake and thyroid carcinoma-a potential risk factor. Exp Clin Endocrinol Diabetes. 1998;106(suppl 3):S38-S44.
60. Andersson M, de Benoist B, Rogers L. Epidemiology of iodine deficiency: salt iodisation and iodine status. Best Pract Res Clin Endocrinol Metab. 2010;24:1-11.
61. Zimmermann MB, Andersson M. Update on iodine status worldwide. Curr Opin Endocrinol Diabetes Obes. 2012;19:382-387.
62. Grodski S, Delbridge L. An update on papillary microcarcinoma. Curr Opin Oncol. 2009;21:1-4.