Expression and function of thyroid hormone transporters in the microvillous plasma membrane of human term placental syncytiotrophoblast

Endocrinology

Volumn 153, Issue 12, 2012, Pages 6126-6135

  Loubiere L S ^a   Vasilopoulou, E ^a   Glazier, J D ^c   Taylor, P M ^d   Franklyn, J A ^a   Kilby, M D ^a,b   Chan, Shiao Y ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b BIRMINGHAM CHILDREN S HOSPITAL NHS FOUNDATION TRUST   (United Kingdom)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

^d UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CD98 ANTIGEN; L TYPE AMINO ACID TRANSPORTER 1; LIOTHYRONINE; MONOCARBOXYLATE TRANSPORTER 10; MONOCARBOXYLATE TRANSPORTER 8; ORGANIC TRANSPORTING POLYPEPTIDE 1A2; ORGANIC TRANSPORTING POLYPEPTIDE 4A1; SODIUM; THYROID HORMONE; THYROID HORMONE TRANSPORTER; THYROXINE; UNCLASSIFIED DRUG;

ARTICLE; HUMAN; HUMAN TISSUE; MICROVILLUS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; SYNCYTIOTROPHOBLAST; WESTERN BLOTTING;

ANIONS; BIOLOGICAL TRANSPORT; CELL MEMBRANE; FEMALE; GENE EXPRESSION REGULATION; HUMANS; IODIDE PEROXIDASE; KINETICS; MATERNAL-FETAL EXCHANGE; MICROVILLI; PEPTIDES; PLACENTA; PREGNANCY; THYROXINE; TRIIODOTHYRONINE; TROPHOBLASTS;

EID: 84870160180     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2012-1753     Document Type: Article

References (48)

1. Haddow JE, Palomaki GE, Allan WC, Williams JR, Knight GJ, Gagnon J, O'Heir CE, Mitchell ML, Hermos RJ, Waisbren SE, Faix JD, Klein RZ 1999 Maternal thyroid deficiency during pregnancy and subsequent neuropsychological development of the child. N Engl J Med 341:549-555
2. Pop VJ, Brouwers EP, Vader HL, Vulsma T, van Baar AL, de Vijlder JJ 2003 Maternal hypothyroxinaemia during early pregnancy and subsequent child development: a 3-year follow-up study. Clin Endocrinol 59:282-288
3. Li Y, Shan Z, Teng W, Yu X, Li Y, Fan C, Teng X, Guo R, Wang H, Li J, Chen Y, Wang W, Chawinga M, Zhang L, Yang L, Zhao Y, Hua T 2010 Abnormalities of maternal thyroid function during pregnancy affect neuropsychological development of their children at 25-30 months. Clin Endocrinol 72:825-829
4. de Escobar GM, Obregón MJ, del Rey FE 2004 Maternal thyroid hormones early in pregnancy and fetal brain development. Best Pract Res Clin Endocrinol Metab 18:225-248
5. Patel J, Landers K, Li H, Mortimer RH, Richard K 2011 Delivery of maternal thyroid hormones to the fetus. Trends Endocrinol Metab 22:164-170
6. Calvo RM, Jauniaux E, Gulbis B, Asunción M, Gervy C, ContempréB, Morreale de Escobar G 2002 Fetal tissues are exposed to biologically relevant free thyroxine concentrations during early phases of development. J Clin Endocrinol Metab 87:1768-1777
7. Costa A, Arisio R, Benedetto C, Bertino E, Fabris C, Giraudi G, Marozio L, Maulà V, Pagliano M, Testori O 1991 Thyroid hormones in tissues from human embryos and fetuses. J Endocrinol Invest 14:559-568
8. Chan S, Kachilele S, McCabe CJ, Tannahill LA, Boelaert K, Gittoes NJ, Visser TJ, Franklyn JA, Kilby MD 2002 Early expression of thyroid hormone deiodinases and receptors in human fetal cerebral cortex. Brain Res Dev Brain Res 138:109-116
9. Chan SY, Martín-Santos A, Loubière LS, González AM, Stieger B, Logan A, McCabe CJ, Franklyn JA, Kilby MD 2011 The expression of thyroid hormone transporters in the human fetal cerebral cortex during early development and in N-Tera-2 neurodifferentiation. J Physiol 589:2827-2845
10. Vulsma T, Gons MH, de Vijlder JJ 1989 Maternal-fetal transfer of thyroxine in congenital hypothyroidism due to a total organification defect or thyroid agenesis. N Engl J Med 321:13-16
11. van Wassenaer AG, Kok JH, Dekker FW, de Vijlder JJ 1997 Thyroid function in very preterm infants: influences of gestational age and disease. Pediatr Res 42:604-609
12. Barber KJ, Franklyn JA, McCabe CJ, Khanim FL, Bulmer JN, Whitley GS, Kilby MD 2005 The in vitro effects of triiodothyronine on epidermal growth factor-induced trophoblast function. J Clin Endocrinol Metab 90:1655-1661
13. Oki N, Matsuo H, Nakago S, Murakoshi H, Laoag-Fernandez JB, Maruo T 2004 Effects of 3,5,3′-triiodothyronine on the invasive potential and the expression of integrins and matrix metalloproteinases in cultured early placental extravillous trophoblasts. J Clin Endocrinol Metab 89:5213-5221
14. Kilby MD, Barber K, Hobbs E, Franklyn JA 2005 Thyroid hormone action in the placenta. Placenta 26:105-113
15. Sibley CP, Birdsey TJ, Brownbill P, Clarson LH, Doughty I, Glazier JD, Greenwood SL, Hughes J, Jansson T, Mylona P, Nelson DM, Powell T 1998 Mechanisms of maternofetal exchange across the human placenta. Biochem Soc Trans 26:86-91
16. Chan SY, Vasilopoulou E, Kilby MD 2009 The role of the placenta in thyroid hormone delivery to the fetus. Nat Clin Pract Endocrinol Metab 5:45-54
17. Chan S, Kachilele S, Hobbs E, Bulmer JN, Boelaert K, McCabe CJ, Driver PM, Bradwell AR, Kester M, Visser TJ, Franklyn JA, Kilby MD2003 Placental iodothyronine deiodinase expression in normal and growth-restricted human pregnancies. J Clin Endocrinol Metab 88:4488-4495
18. Mortimer RH, Galligan JP, Cannell GR, Addison RS, Roberts MS 1996 Maternal to fetal thyroxine transmission in the human term placenta is limited by inner ring deiodination. J Clin Endocrinol Metab 81:2247-2249
19. Loubière LS, Vasilopoulou E, Bulmer JN, Taylor PM, Stieger B, Verrey F, McCabe CJ, Franklyn JA, Kilby MD, Chan SY 2010 Expression of thyroid hormone transporters in the human placenta and changes associated with intrauterine growth restriction. Placenta 31:295-304
20. Chan SY, Franklyn JA, Pemberton HN, Bulmer JN, Visser TJ, McCabe CJ, Kilby MD 2006 Monocarboxylate transporter 8 expression in the human placenta: the effects of severe intrauterine growth restriction. J Endocrinol 189:465-471
21. Glazier JD, Jones CJ, Sibley CP 1988 Purification and Na+ uptake by human placental microvillus membrane vesicles prepared by three different methods. Biochim Biophys Acta 945:127-134
22. Glazier JD, Sibley CP 2006 In vitro methods for studying human placental amino acid transport: placental plasma membrane vesicles. Methods Mol Med 122:241-252
23. Jones CJ, Fox H 1976 An ultrahistochemical study of the distribution of acid and alkaline phosphatases in placentae from normal and complicated pregnancies. J Pathol 118:143-151
24. Vasilopoulou E, Loubière LS, Martín-Santos A, McCabe CJ, Franklyn JA, Kilby MD, Chan SY 2010 Differential triiodothyronine responsiveness and transport by human cytotrophoblasts from normal and growth-restricted pregnancies. J Clin Endocrinol Metab 95:4762-4770
25. Huber RD, Gao B, Sidler Pfändler MA, Zhang-Fu W, Leuthold S, Hagenbuch B, Folkers G, Meier PJ, Stieger B 2007 Characterization of two splice variants of human organic anion transporting polypeptide 3A1 isolated from human brain. Am J Physiol Cell Physiol 292:C795-C806
26. Ritchie JW, Taylor PM 2001 Role of the System L permease LAT1 in amino acid and iodothyronine transport in placenta. Biochem J 356:719-725
27. Friesema EC, Docter R, Moerings EP, Verrey F, Krenning EP, Hennemann G, Visser TJ 2001 Thyroid hormone transport by the heterodimeric human system L amino acid transporter. Endocrinology 142:4339-4348
28. Friesema EC, Ganguly S, Abdalla A, Manning Fox JE, Halestrap AP, Visser TJ 2003 Identification of monocarboxylate transporter 8 as a specific thyroid hormone transporter. J Biol Chem 278:40128-40135
29. Friesema EC, Jansen J, Jachtenberg JW, Visser WE, Kester MH, Visser TJ 2008 Effective cellular uptake and efflux of thyroid hormone by human monocarboxylate transporter 10. Mol Endocrinol 22:1357-1369
30. Kemp HF, Taylor PM 1997 Interactions between thyroid hormone and tryptophan transport in rat liver are modulated by thyroid status. Am J Physiol 272:E809-E816
31. Mitchell AM, Rowan KA, Manley SW, Mortimer RH 1999 Comparison of mechanisms mediating uptake and efflux of thyroid hormones in the human choriocarcinoma cell line, JAR. J Endocrinol 161:107-113
32. Ritchie JW, Taylor PM 2010 Tryptophan and iodothyronine transport interactions in HepG2 human hepatoma cells. Amino Acids 38:1361-1367
33. Roth S, Kinne A, Schweizer U 2010 The tricyclic antidepressant desipramine inhibits T3 import into primary neurons. Neurosci Lett 478:5-8
34. Wirth EK, Roth S, Blechschmidt C, Hölter SM, Becker L, Racz I, Zimmer A, Klopstock T, Gailus-Durner V, Fuchs H, Wurst W, Naumann T, Bräuer A, de Angelis MH, Köhrle J, Grüters A, Schweizer U 2009 Neuronal 3′,3,5-triiodothyronine (T3) uptake and behavioral phenotype of mice deficient in Mct8, the neuronal T3 transporter mutated in Allan-Herndon-Dudley syndrome. J Neurosci 29:9439-9449
35. Sato K, Sugawara J, Sato T, Mizutamari H, Suzuki T, Ito A, Mikkaichi T, Onogawa T, Tanemoto M, Unno M, Abe T, Okamura K 2003 Expression of organic anion transporting polypeptide E (OATP-E) in human placenta. Placenta 24:144-148
36. Okamoto Y, Sakata M, Ogura K, Yamamoto T, Yamaguchi M, Tasaka K, Kurachi H, Tsurudome M, Murata Y 2002 Expression and regulation of 4F2hc and hLAT1 in human trophoblasts. Am J Physiol Cell Physiol 282:C196-C204
37. Jansson T, Scholtbach V, Powell TL 1998 Placental transport of leucine and lysine is reduced in intrauterine growth restriction. Pediatr Res 44:532-537
38. Lewis RM, Glazier J, Greenwood SL, Bennett EJ, Godfrey KM, Jackson AA, Sibley CP, Cameron IT, Hanson MA 2007 L-serine uptake by human placental microvillous membrane vesicles. Placenta 28:445-452
39. Gao B, Hagenbuch B, Kullak-Ublick GA, Benke D, Aguzzi A, Meier PJ 2000 Organic anion-transporting polypeptides mediate transport of opioid peptides across blood-brain barrier. J Pharmacol Exp Ther 294:73-79
40. Kullak-Ublick GA, Ismair MG, Stieger B, Landmann L, Huber R, Pizzagalli F, Fattinger K, Meier PJ, Hagenbuch B 2001 Organic anion-transporting polypeptide B (OATP-B) and its functional comparison with three other OATPs of human liver. Gastroenterology 120:525-533
41. Cleal JK, Glazier JD, Ntani G, Crozier SR, Day PE, Harvey NC, Robinson SM, Cooper C, Godfrey KM, Hanson MA, Lewis RM 2011 Facilitated transporters mediate net efflux of amino acids to the fetus across the basal membrane of the placental syncytiotrophoblast. J Physiol 589:987-997
42. Jansson T, Ekstrand Y, Wennergren M, Powell TL 2001 Placental glucose transport in gestational diabetes mellitus. Am J Obstet Gynecol 184:111-116
43. Patel P, Weerasekera N, Hitchins M, Boyd CA, Johnston DG, Williamson C 2003 Semi quantitative expression analysis of MDR3, FIC1, BSEP, OATP-A, OATP-C, OATP-D, OATP-E and NTCP gene transcripts in 1st and 3rd trimester human placenta. Placenta 24:39-44
44. Taylor PM, Ritchie JW 2007 Tissue uptake of thyroid hormone by amino acid transporters. Best Pract Res Clin Endocrinol Metab 21:237-251
45. Hennemann G, Docter R, Friesema EC, de Jong M, Krenning EP, Visser TJ 2001 Plasma membrane transport of thyroid hormones and its role in thyroid hormone metabolism and bioavailability. Endocr Rev 22:451-476
46. McKinnon B, Li H, Richard K, Mortimer R 2005 Synthesis of thyroid hormone binding proteins transthyretin and albumin by human trophoblast. J Clin Endocrinol Metab 90:6714-6720
47. Landers KA, McKinnon BD, Li H, Subramaniam VN, Mortimer RH, Richard K 2009 Carrier-mediated thyroid hormone transport into placenta by placental transthyretin. J Clin Endocrinol Metab 94:2610-2616
48. Abe T, Kakyo M, Tokui T, Nakagomi R, Nishio T, Nakai D, Nomura H, Unno M, Suzuki M, Naitoh T, Matsuno S, Yawo H 1999 Identification of a novel gene family encoding human liver-specific organic anion transporter LST-1. J Biol Chem 274:17159-17163