Iodine deficiency induces a VEGF-dependent microvascular response in salivary glands and in the stomach

Histology and Histopathology

Volumn 31, Issue 8, 2016, Pages 897-909

  Vanderstraeten, Jessica ^a   Derradji, Hanane ^b   Craps, Julie ^a   Sonveaux, Pierre ^a   Colin, Ides M ^c   Many, Marie Christine ^a   Gérard, Anne Catherine ^a,c  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^b BELGIAN NUCLEAR RESEARCH CENTRE   (Belgium)

^c Regional Hospital Center (CHR)   (Belgium)

Author keywords

Iodine deficiency; Microvasculature; Salivary glands; Stomach; VEGF

Indexed keywords

COTRANSPORTER; IODINE; SODIUM; SODIUM IODIDE SYMPORTER; VASCULAR ENDOTHELIAL GROWTH FACTOR A, MOUSE; VASCULOTROPIN A;

ANIMAL; DEFICIENCY; DISEASE MODEL; FLUORESCENT ANTIBODY TECHNIQUE; METABOLISM; MICROVASCULATURE; MOUSE; SALIVARY GLAND; STOMACH; VASCULARIZATION; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; DISEASE MODELS, ANIMAL; FLUORESCENT ANTIBODY TECHNIQUE; IODINE; MICE; MICROVESSELS; SALIVARY GLANDS; SODIUM; STOMACH; SYMPORTERS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84974846168     PISSN: 02133911     EISSN: None     Source Type: Journal    
DOI: 10.14670/HH-11-727     Document Type: Article

References (41)

1. Abnet C.C., Fan J.H., Kamangar F., Sun X.D., Taylor P.R., Ren J.S., Mark S.D., Zhao P., Fraumeni J.F. Jr, Qiao Y.L. and Dawsey S.M. (2006). Self-reported goiter is associated with a significantly increased risk of gastric noncardia adenocarcinoma in a large population-based Chinese cohort. Int. J. Cancer 119, 1508-1510.
2. Altorjay A., Dohan O., Szilagyi A., Paroder M., Wapnir I.L. and Carrasco N. (2007). Expression of the Na+/I- symporter (NIS) is markedly decreased or absent in gastric cancer and intestinal metaplastic mucosa of Barrett esophagus. BMC Cancer 7, 5.
3. Andersson M. and Zimmermann M. (2012). Global iodine nutrition: a remarkable leap forward in the past decade. IDD newsletter 40.
4. Bahar G., Feinmesser R., Shpitzer T., Popovtzer A. and Nagler R.M. (2007). Salivary analysis in oral cancer patients: DNA and protein oxidation, reactive nitrogen species, and antioxidant profile. Cancer 109, 54-59.
5. Bianco A.C., Anderson G., Forrest D., Galton V.A., Gereben B., Kim B.W., Kopp P.A., Liao X.H., Obregon M.J., Peeters R.P., Refetoff S., Sharlin D.S., Simonides W.S., Weiss R.E. and Williams G.R. (2014). American Thyroid Association Guide to investigating thyroid hormone economy and action in rodent and cell models. Thyroid 24, 88-168.
6. Bock F., Onderka J., Dietrich T., Bachmann B., Kruse F.E., Paschke M., Zahn G. and Cursiefen C. (2007). Bevacizumab as a potent inhibitor of inflammatory corneal angiogenesis and lymphangiogenesis. Invest. Ophthalmol. Vis. Sci. 48, 2545-2552.
7. Brown-Grant K. (1961). Extrathyroidal iodide concentrating mechanisms. Physiol. Rev. 41, 189-213.
8. Bruno R., Giannasio P., Ronga G., Baudin E., Travagli J.P., Russo D., Filetti S. and Schlumberger M. (2004). Sodium iodide symporter expression and radioiodine distribution in extrathyroidal tissues. J. Endocrinol. Invest. 27, 1010-1014.
9. Craps J., Wilvers C., Joris V., De Jongh B., Vanderstraeten J., Lobysheva I., Balligand J.L., Sonveaux P., Gilon P., Many M.C., Gerard A.C. and Colin I.M. (2015). Involvement of nitric oxide in iodine deficiency-induced microvascular remodeling in the thyroid gland: role of nitric oxide synthase 3 and ryanodine receptors. Endocrinology 156, 707-720.
10. Ferguson M.M. and Stephen K.W. (1972). Sex differences in the autoradiographic pattern of (125I)iodide uptake in mouse submandibular salivary gland. Arch. Oral Biol. 17, 1117-1119.
11. Geiszt M., Witta J., Baffi J., Lekstrom K. and Leto T.L. (2003). Dual oxidases represent novel hydrogen peroxide sources supporting mucosal surface host defense. FASEB J. 17, 1502-1504.
12. Gerard A.C., Humblet K., Wilvers C., Poncin S., Derradji H., de Ville de G.C., Abou-el-Ardat K., Baatout S., Sonveaux P., Denef J.F. and Colin I.M. (2012). 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 22, 699-708.
13. Gerard A.C., Poncin S., Audinot J.N., Denef J.F. and Colin I.M. (2009). Iodide deficiency-induced angiogenic stimulus in the thyroid occurs via HIF- and ROS-dependent VEGF-A secretion from thyrocytes. Am. J. Physiol. Endocrinol. Metab. 296, E1414-E1422.
14. Gerard A.C., Poncin S., Caetano B., Sonveaux P., Audinot J.N., Feron O., Colin I.M. and Soncin F. (2008). Iodine deficiency induces a thyroid stimulating hormone-independent early phase of microvascular reshaping in the thyroid. Am. J. Pathol. 172, 748-760.
15. Golkowski F., Szybinski Z., Rachtan J., Sokolowski A., Buziak-Bereza M., Trofimiuk M., Hubalewska-Dydejczyk A., Przybylik-Mazurek E. and Huszno B. (2007). Iodine prophylaxis--the protective factor against stomach cancer in iodine deficient areas. Eur. J. Nutr. 46, 251-256.
16. Gulaboglu M., Yildiz L., Celebi F., Gul M. and Peker K. (2005). Comparison of iodine contents in gastric cancer and surrounding normal tissues. Clin. Chem. Lab. Med. 43, 581-584.
17. Jhiang S.M., Cho J.Y., Ryu K.Y., De Young B.R., Smanik P.A., McGaughy V.R., Fischer A.H. and Mazzaferri E.L. (1998). An immunohistochemical study of Na+/I- symporter in human thyroid tissues and salivary gland tissues. Endocrinology 139, 4416-4419.
18. Josefsson M., Evilevitch L., Westrom B., Grunditz T. and Ekblad E. (2006). Sodium-iodide symporter mediates iodide secretion in rat gastric mucosa in vitro. Exp. Biol. Med.(Maywood.) 231, 277-281.
19. Josefsson M., Grunditz T., Ohlsson T. and Ekblad E. (2002). Sodium/iodide-symporter: distribution in different mammals and role in entero-thyroid circulation of iodide. Acta Physiol. Scand. 175, 129-137.
20. Kopp P.A. (2008). Reduce, recycle, reuse--iodotyrosine deiodinase in thyroid iodide metabolism. N. Engl. J. Med. 358, 1856-1859.
21. Kotani T., Ogata Y., Yamamoto I., Aratake Y., Kawano J.I., Suganuma T. and Ohtaki S (1998). Characterization of gastric Na+/I- symporter of the rat. Clin. Immunol. Immunopathol. 89, 271-278.
22. La Perle K.M., Kim D.C., Hall N.C., Bobbey A., Shen D.H., Nagy R.S., Wakely P.E. Jr, Lehman A., Jarjoura D. and Jhiang S.M. (2013). Modulation of sodium/iodide symporter expression in the salivary gland. Thyroid 23, 1029-1036.
23. Lazarus J.H., Harden R.M. and Robertson J.W. (1974). Quantitative studies of the inhibitory effect of perchlorate on the concentration of 36C1O minus 4 125I minus and 99mTcO minus 4 in salivary glands of male and female mice. Arch. Oral Biol. 19, 493-498.
24. Levy O., Dai G., Riedel C., Ginter C.S., Paul E.M., Lebowitz A.N. and Carrasco N. (1997). Characterization of the thyroid Na+/I- symporter with an anti-COOH terminus antibody. Proc. Natl. Acad. Sci. USA 94, 5568-5573.
25. Maier J., van S.H., van O.C., Paschke R., Weiss R.E. and Krohn K. (2007). Iodine deficiency activates antioxidant genes and causes DNA damage in the thyroid gland of rats and mice. Biochim. Biophys. Acta 1773, 990-999.
26. Miller J.K., Swanson E.W. and Spalding G.E. (1975). Iodine absorption, excretion, recycling, and tissue distribution in the dairy cow. J. Dairy Sci. 58, 1578-1593.
27. MIRD (1975). Summary of current radiation dose estimates to humans from 123I, 124I, 125I, 126I, 130I, 131I, and 132I as sodium iodide. J. Nucl. Med. 16, 857-860.
28. Nicola J.P., Basquin C., Portulano C., Reyna-Neyra A., Paroder M. and Carrasco N. (2009). The Na+/I- symporter mediates active iodide uptake in the intestine. Am. J. Physiol. Cell Physiol. 296, C654-C662.
29. Pearce E.N., Andersson M. and Zimmermann M.B. (2013). Global iodine nutrition: Where do we stand in 2013? Thyroid 23, 523-528.
30. Pedraza P.E., Obregon M.J., Escobar-Morreale H.F., del Rey F.E. and de Escobar G.M. (2006). Mechanisms of adaptation to iodine deficiency in rats: thyroid status is tissue specific. Its relevance for man. Endocrinology 147, 2098-2108.
31. Portulano C., Paroder-Belenitsky M. and Carrasco N. (2014). The Na+/Isymporter (NIS): mechanism and medical impact. Endocr. Rev. 35, 106-149.
32. Ribatti D. and Crivellato E. (2012). Mast cells, angiogenesis, and tumour growth. Biochim. Biophys. Acta (BBA). 1822, 2-8.
33. Serrano-Nascimento C., da Silva T.S., Nicola J.P., Nachbar R.T., Masini-Repiso A.M. and Nunes M.T. (2014). The acute inhibitory effect of iodide excess on sodium/iodide symporter expression and activity involves the PI3K/Akt signaling pathway. Endocrinology 155, 1145-1156.
34. Thomas E.L., Bates K.P. and Jefferson M.M. (1980). Hypothiocyanite ion: detection of the antimicrobial agent in human saliva. J. Dent. Res. 59, 1466-1472.
35. Vayre L., Sabourin J.C., Caillou B., Ducreux M., Schlumberger M. and Bidart J.M. (1999). Immunohistochemical analysis of Na+/Isymporter distribution in human extra-thyroidal tissues. Eur. J. Endocrinol. 141, 382-386.
36. Venturi S. and Venturi M. (2007). Evolution of dietary antioxidant defences. Eur. Epi-Marker 11, 1-12.
37. Venturi S. and Venturi M. (2009). Iodine in evolution of salivary glands and in oral health. Nutr. Health 20, 119-134.
38. Viglietto G., Romano A., Manzo G., Chiappetta G., Paoletti I., Califano D., Galati M.G., Mauriello V., Bruni P., Lago C.T., Fusco A. and Persico M.G. (1997). Upregulation of the angiogenic factors PlGF, VEGF and their receptors (Flt-1, Flk-1/KDR) by TSH in cultured thyrocytes and in the thyroid gland of thiouracil-fed rats suggest a TSH-dependent paracrine mechanism for goiter hypervascularization. Oncogene 15, 2687-2698.
39. WHO (2015). http://www.who.int/vmnis/database/iodine/iodine_data_status_summary/en/
40. Yeom C.J., Chung J.K., Kang J.H., Jeon Y.H., Kim K.I., Jin Y.N., Lee Y.M., Jeong J.M. and Lee D.S. (2008). Visualization of hypoxiainducible factor-1 transcriptional activation in C6 glioma using luciferase and sodium iodide symporter genes. J. Nucl. Med. 49, 1489-1497.
41. Zimmermann M.B. (2009). Iodine deficiency. Endocr. Rev. 30, 376-408.