The Placenta as a Compensatory Iodine Storage Organ
Abstract
Background: The production of iodine-containing thyroid hormones necessary for brain development in the fetus depends not only on maternal dietary intake but also on placental iodine transport. The optimum level of iodine nutrition during pregnancy and the proportion of the pregnant population reaching this level have previously been evaluated. Little information exists on the ability of the placenta to either accumulate or store iodine. This study aims to investigate iodine uptake and tissue iodine content within placental tissue obtained from women delivering at term.
Methods: Samples (∼1 cm3) obtained from placental cotyledons (n = 19), thyroid (n = 4), and uterine myometrial (n = 4) tissue were incubated for 6 hours with 125I in the presence and absence of potassium perchlorate. To account for variation in tissue composition, results were expressed in cpm 125I/μg DNA.
Results: Placental uptake of 125I (375 cpm/μg DNA) was significantly higher than that of control myometrial tissue (226 cpm/μg DNA) (p < 0.05) and was ∼25% that of thyroid tissue (1702 cpm/μg DNA). Uptake of 125I could be partially blocked in the thyroid and placenta, respectively, by potassium perchlorate (100 μM), which had no effect on uptake by myometrial tissue. Iodine content of tissue samples measured using an alkaline ashing technique with Sandell-Kolthoff colorimetry gave a mean value for total iodine of 30.4 ng/g placental tissue (range 21–50 ng/g), 1.74 ng/g myometrial tissue, and 1037 ng/g thyroid tissue.
Conclusions: Placental iodine content was only ∼3% that of the thyroid, but on the basis that neonatal iodine stores are very low and highly sensitive to fluctuations in maternal iodine supply, we postulate that placental iodine bioavailability makes a significant contribution to protection against neonatal hypothyroidism. These findings suggest that the placenta has a role not only in uptake but also in storing iodine as a possible means of protecting the fetus from inadequacies in maternal dietary iodine intake.
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References
1.
Brown-Grant K1961. Extrathyroidal iodide concentrating mechanismsPhysiol Rev41189-213. 1. Brown-Grant K 1961 Extrathyroidal iodide concentrating mechanisms. Physiol Rev 41:189–213.
2.
Gulaboglu MBorekci BHalici Z2007. Placental tissue iodine level and blood magnesium concentration in pre-eclamptic and normal pregnancyInt J Gynaecol Obstet98100-104. 2. Gulaboglu M, Borekci B, Halici Z 2007 Placental tissue iodine level and blood magnesium concentration in pre-eclamptic and normal pregnancy. Int J Gynaecol Obstet 98:100–104.
3.
Delange F2001. Iodine deficiency as a cause of brain damagePostgrad Med J77217-220. 3. Delange F 2001 Iodine deficiency as a cause of brain damage. Postgrad Med J 77:217–220.
4.
Glinoer D1997. The regulation of thyroid function in pregnancy: pathways of endocrine adaptation from physiology to pathologyEndocr Rev18404-433. 4. Glinoer D 1997 The regulation of thyroid function in pregnancy: pathways of endocrine adaptation from physiology to pathology. Endocr Rev 18:404–433.
5.
Delange F1998. Screening for congenital hypothyroidism used as an indicator of the degree of iodine deficiency and of its controlThyroid81185-1192. 5. Delange F 1998 Screening for congenital hypothyroidism used as an indicator of the degree of iodine deficiency and of its control. Thyroid 8:1185–1192.
6.
Delange F1994. The disorders induced by iodine deficiencyThyroid4107-128. 6. Delange F 1994 The disorders induced by iodine deficiency. Thyroid 4:107–128.
7.
Delange FLaurence MPeneva LWalfish PWillgerodt H1993. Neonatal Thyroid Function in Iodine Deficiency., Iodine Deficiency in Europe241NATO ASI Series199-207. 7. Delange F, Laurence M, Peneva L, Walfish P, Willgerodt H 1993 Neonatal Thyroid Function in Iodine Deficiency. Iodine Deficiency in Europe, vol. 241. NATO ASI Series, pp 199–207.
8.
Bidart JMLacroix LEvain-Brion DCaillou BLazar VFrydman RBellet DFiletti SSchlumberger M2000. Expression of Na+/I− symporter and Pendred syndrome genes in trophoblast cellsJ Clin Endocrinol Metab854367-4372. 8. Bidart JM, Lacroix L, Evain-Brion D, Caillou B, Lazar V, Frydman R, Bellet D, Filetti S, Schlumberger M 2000 Expression of Na+/I− symporter and Pendred syndrome genes in trophoblast cells. J Clin Endocrinol Metab 85:4367–4372.
9.
Mitchell AMManley SWMorris JCPowell KABergert ERMortimer RH2001. Sodium iodide symporter (NIS) gene expression in human placentaPlacenta22256-258. 9. Mitchell AM, Manley SW, Morris JC, Powell KA, Bergert ER, Mortimer RH 2001 Sodium iodide symporter (NIS) gene expression in human placenta. Placenta 22:256–258.
10.
Di Cosmo CFanelli GTonacchera MFerrarini EDimida AAgretti PDe Marco GVitti PPinchera ABevilacqua GNaccarato AGViacava P2006. The sodium-iodide symporter expression in placental tissue at different gestational age: an immunohistochemical studyClin Endocrinol (Oxf)65544-548. 10. Di Cosmo C, Fanelli G, Tonacchera M, Ferrarini E, Dimida A, Agretti P, De Marco G, Vitti P, Pinchera A, Bevilacqua G, Naccarato AG, Viacava P 2006 The sodium-iodide symporter expression in placental tissue at different gestational age: an immunohistochemical study. Clin Endocrinol (Oxf) 65:544–548.
11.
Arturi FLacroix LPresta IScarpelli DCaillou BSchlumberger MRusso DBidart JMFiletti S2002. Regulation by human chorionic gonadotropin of sodium/iodide symporter gene expression in the JAr human choriocarcinoma cell lineEndocrinology1432216-2220. 11. Arturi F, Lacroix L, Presta I, Scarpelli D, Caillou B, Schlumberger M, Russo D, Bidart JM, Filetti S 2002 Regulation by human chorionic gonadotropin of sodium/iodide symporter gene expression in the JAr human choriocarcinoma cell line. Endocrinology 143:2216–2220.
12.
Li HRichard KMcKinnon BMortimer RH2007. Effect of iodide on hCG, sodium-iodide symporter expression and iodide uptake in BeWo choriocarcinoma cellsJ Clin Endocrinol Metab924046-4051. 12. Li H, Richard K, McKinnon B, Mortimer RH 2007 Effect of iodide on hCG, sodium-iodide symporter expression and iodide uptake in BeWo choriocarcinoma cells. J Clin Endocrinol Metab 92:4046–4051.
13.
Manley SWLi HMortimer RH2005. The BeWo choriocarcinoma cell line as a model of iodide transport by placentaPlacenta26380-386. 13. Manley SW, Li H, Mortimer RH 2005 The BeWo choriocarcinoma cell line as a model of iodide transport by placenta. Placenta 26:380–386.
14.
Eskandari SLoo DDDai GLevy OWright EMCarrasco N1997. Thyroid Na+/I− symporter. Mechanism, stoichiometry, and specificityJ Biol Chem27227230-27238. 14. Eskandari S, Loo DD, Dai G, Levy O, Wright EM, Carrasco N 1997 Thyroid Na+/I− symporter. Mechanism, stoichiometry, and specificity. J Biol Chem 272:27230–27238.
15.
Spitzweg CJoba WMorris JCHeufelder AE1999. Regulation of sodium iodide symporter gene expression in FRTL-5 rat thyroid cellsThyroid9821-830. 15. Spitzweg C, Joba W, Morris JC, Heufelder AE 1999 Regulation of sodium iodide symporter gene expression in FRTL-5 rat thyroid cells. Thyroid 9:821–830.
16.
Yoshida ASasaki NMori ATaniguchi SMitani YUeta YHattori KSato RHisatome IMori TShigemasa CKosugi S1997. Different electrophysiological character of I−, ClO4−, and SCN− in the transport by Na+/I− symporterBiochem Biophys Res Commun231731-734. 16. Yoshida A, Sasaki N, Mori A, Taniguchi S, Mitani Y, Ueta Y, Hattori K, Sato R, Hisatome I, Mori T, Shigemasa C, Kosugi S 1997 Different electrophysiological character of I−, ClO4−, and SCN− in the transport by Na+/I− symporter. Biochem Biophys Res Commun 231:731–734.
17.
Chan SKachilele SHobbs EBulmer JNBoelaert KMcCabe CJDriver PMBradwell ARKester MVisser TJFranklyn JAKilby MD2003. Placental iodothyronine deiodinase expression in normal and growth-restricted human pregnanciesJ Clin Endocrinol Metab884488-4495. 17. Chan S, Kachilele S, Hobbs E, Bulmer JN, Boelaert K, McCabe CJ, Driver PM, Bradwell AR, Kester M, Visser TJ, Franklyn JA, Kilby MD 2003 Placental iodothyronine deiodinase expression in normal and growth-restricted human pregnancies. J Clin Endocrinol Metab 88:4488–4495.
18.
Schroder-van der Elst JPvan der Heide DKastelijn JRousset BObregón MJ2001. The expression of the sodium/iodide symporter is up-regulated in the thyroid of fetuses of iodine-deficient ratsEndocrinology1423736-3741. 18. Schroder-van der Elst JP, van der Heide D, Kastelijn J, Rousset B, Obregón MJ 2001 The expression of the sodium/iodide symporter is up-regulated in the thyroid of fetuses of iodine-deficient rats. Endocrinology 142:3736–3741.
19.
Glinoer D1997. The regulation of thyroid function in pregnancy: pathways of endocrine adaptation from physiology to pathologyEndocr Rev18404-433. 19. Glinoer D 1997 The regulation of thyroid function in pregnancy: pathways of endocrine adaptation from physiology to pathology. Endocr Rev 18:404–433.
20.
Nawoor ZBurns RSmith DFSheehan SO'Herlihy CSmyth PP2006. Iodine intake in pregnancy in Ireland—a cause for concern?Ir J Med Sci17521-24. 20. Nawoor Z, Burns R, Smith DF, Sheehan S, O'Herlihy C, Smyth PP 2006 Iodine intake in pregnancy in Ireland—a cause for concern? Ir J Med Sci 175:21–24.
21.
Carrasco N1993. Iodide transport in the thyroid glandBiochim Biophys Acta115465-82. 21. Carrasco N 1993 Iodide transport in the thyroid gland. Biochim Biophys Acta 1154:65–82.
22.
Delange F2004. Optimal iodine nutrition during pregnancy, lactation and the neonatal periodInt J Endocrinol Metab20041-12. 22. Delange F 2004 Optimal iodine nutrition during pregnancy, lactation and the neonatal period. Int J Endocrinol Metab 2004:1–12.
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Copyright 2011, Mary Ann Liebert, Inc.
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Published online: 19 May 2011
Published in print: May 2011
Published ahead of print: 21 March 2011
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