Best Practice & Research Clinical Endocrinology & Metabolism
Volume 21, Issue 2 , Pages 237-251 , June 2007

Tissue uptake of thyroid hormone by amino acid transporters

  • Peter M. Taylor (Principal Investigator)

      Affiliations

    • Corresponding Author InformationCorresponding author. Tel.: +44 (0) 1382 384961; Fax: +44 (0) 1382 385507.

References 

  1. Werner A, Ingbar SH. In:  Braverman LE,  Utiger RD editor. The Thyroid - A Fundamental Clinical Text. Philadelphia: Lippinncott Williams & Wilkins; 2000;
  2. Larsen PR, Silva JE, Kaplan MM. Relationships between circulating and intracellular thyroid hormones: physiological and clinical implications. Endocrine Reviews. 1981;2:87–102
  3. Hennemann G, Docter R, Friesema EC, et al. Plasma membrane transport of thyroid hormones and its role in thyroid hormone metabolism and bioavailability. Endocrine Reviews. 2001;22:451–476
  4. Yen PM. Physiological and molecular basis of thyroid hormone action. Physiological Reviews. 2001;81:1097–1142
  5. Lai CS, Korytowski W, Niu CH, et al. Transverse motion of spin-labeled 3,3′,5-triiodo-l-thyronine in phospholipid bilayers. Biochemical and Biophysical Research Communications. 1985;131:408–412
  6. Abe T, Suzuki T, Unno M, et al. Thyroid hormone transporters: recent advances. Trends in Endocrinology and Metabolism. 2002;13:215–220
  7. Friesema EC, Jansen J, Milici C, et al. Thyroid hormone transporters. Vitamins and Hormones. 2005;70:137–167
  8. Shi YB, Ritchie JW, Taylor PM. Complex regulation of thyroid hormone action: multiple opportunities for pharmacological intervention. Pharmacology & Therapeutics. 2002;94:235–251
  9. Ritchie JW, Peter GJ, Shi YB, et al. Thyroid hormone transport by 4F2hc-IU12 heterodimers expressed in Xenopus oocytes. The Journal of Endocrinology. 1999;163:R5–R9
  10. Zhou Y, Samson M, Francon J, et al. Thyroid hormone concentrative uptake in rat erythrocytes. Involvement of the tryptophan transport system T in countertransport of tri-iodothyronine and aromatic amino acids. The Biochemical Journal. 1992;281:81–86
  11. Friesema EC, Docter R, Moerings EP, et al. Thyroid hormone transport by the heterodimeric human system L amino acid transporter. Endocrinology. 2001;142:4339–4348
  12. Friesema EC, Ganguly S, Abdalla A, et al. Identification of monocarboxylate transporter 8 as a specific thyroid hormone transporter. The Journal of Biological Chemistry. 2003;278:40128–40135
  13. Abe T, Kakyo M, Sakagami H, et al. Molecular characterization and tissue distribution of a new organic anion transporter subtype (oatp3) that transports thyroid hormones and taurocholate and comparison with oatp2. The Journal of Biological Chemistry. 1998;273:22395–22401
  14. Friesema EC, Docter R, Moerings EP, et al. Identification of thyroid hormone transporters. Biochemical and Biophysical Research Communications. 1999;254:497–501
  15. Ribeiro RCJ, Cavalieri RR, Lomri N, et al. Thyroid hormone export regulates cellular hormone content and response. The Journal of Biological Chemistry. 1996;271:17147–17151
  16. Mitchell AM, Tom M, Mortimer RH. Thyroid hormone export from cells: contribution of P-glycoprotein. The Journal of Endocrinology. 2005;185:93–98
  17. van der Putten HH, Friesema EC, Abumrad NA, et al. Thyroid hormone transport by the rat fatty acid translocase. Endocrinology. 2003;144:1315–1323
  18. Ritchie JW, Shi YB, Hayashi Y, et al. A role for thyroid hormone transporters in transcriptional regulation by thyroid hormone receptors. Molecular Endocrinology (Baltimore, Md.). 2003;17:653–661
  19. Friesema EC, Kuiper GG, Jansen J, et al. Thyroid hormone transport by the human monocarboxylate transporter 8 and its rate-limiting role in intracellular metabolism. Molecular Endocrinology (Baltimore, Md.). 2006;20:2761–2772
  20. Mackenzie B, Erickson JD. Sodium-coupled neutral amino acid (System N/A) transporters of the SLC38 gene family. Pflügers Archiv. 2004;447:784–795
  21. Chen NH, Reith ME, Quick MW. Synaptic uptake and beyond: the sodium- and chloride-dependent neurotransmitter transporter family SLC6. Pflügers Archiv. 2004;447:519–531
  22. Verrey F, Closs EI, Wagner CA, et al. CATs and HATs: the SLC7 family of amino acid transporters. Pflügers Archiv. 2004;447:532–542
  23. Kanai Y, Hediger MA. The glutamate and neutral amino acid transporter family: physiological and pharmacological implications. European Journal of Pharmacology. 2003;479:237–247
  24. Broer S. The SLC6 orphans are forming a family of amino acid transporters. Neurochemistry International. 2006;48:559–567
  25. Palacin M, Estevez R, Bertran J, et al. Molecular biology of mammalian plasma membrane amino acid transporters. Physiological Reviews. 1998;78:969–1054
  26. Christensen HN, Albritton LM, Kakuda DK, et al. Gene-product designations for amino acid transporters. The Journal of Experimental Biology. 1994;196:51–57
  27. Fleck C, Schwertfeger M, Taylor PM. Regulation of renal amino acid (AA) transport by hormones, drugs and xenobiotics - a review. Amino Acids. 2003;24:347–374
  28. Verrey F, Meier C, Rossier G, et al. Glycoprotein-associated amino acid exchangers: broadening the range of transport specificity. Pflügers Archiv. 2000;440:503–512
  29. Milot C, Prahlad KV, Hampel AE. Effect of triiodo-l-thyronine on amino acid transport by Xenopus laevis embryos. Developmental Biology. 1980;80:483–488
  30. Robison D, Prahlad KV, Hampel AE. Amino acid uptake by Xenopus laevis embryos: effect of triiodo-l-thyronine. Comparative Biochemistry and Physiology. B. 1972;43:749–754
  31. Blondeau JP, Beslin A, Chantoux F, et al. Triiodothyronine is a high-affinity inhibitor of amino acid transport system L1 in cultured astrocytes. Journal of Neurochemistry. 1993;60:1407–1413
  32. Prasad PD, Leibach FH, Mahesh VB, et al. Relationship between thyroid hormone transport and neutral amino acid transport in JAR human choriocarcinoma cells. Endocrinology. 1994;134:574–581
  33. Mitchell AM, Rowan KA, Manley SW, et al. Comparison of mechanisms mediating uptake and efflux of thyroid hormones in the human choriocarcinoma cell line, JAR. The Journal of Endocrinology. 1999;161:107–113
  34. Powell KA, Mitchell AM, Manley SW, et al. Different transporters for tri-iodothyronine (T(3)) and thyroxine (T(4)) in the human choriocarcinoma cell line, JAR. The Journal of Endocrinology. 2000;167:487–492
  35. Mitchell AM, Manley SW, Mortimer RH. Interactions between transport of triiodothyronine and tryptophan in JAR cells. Molecular and Cellular Endocrinology. 1994;101:203–210
  36. Mastroberardino L, Spindler B, Pfeiffer R, et al. Amino-acid transport by heterodimers of 4F2hc/CD98 and members of a permease family. Nature. 1998;395:288–291
  37. Feral CC, Nishiya N, Fenczik CA, et al. CD98hc (SLC3A2) mediates integrin signaling. Proceedings of the National Academy of Sciences of the United States of America. 2005;102:355–360
  38. Nakamura E, Sato M, Yang H, et al. 4F2 (CD98) heavy chain is associated covalently with an amino acid transporter and controls intracellular trafficking and membrane topology of 4F2 heterodimer. The Journal of Biological Chemistry. 1999;274:3009–3016
  39. Ritchie JW, Collingwood CJ, Taylor PM. Effect of hypothyroidism on pathways for iodothyronine and tryptophan uptake into rat adipocytes. American Journal of Physiology. Endocrinology and Metabolism. 2001;280:E254–E259
  40. Ritchie JW, Taylor PM. Role of the System L permease LAT1 in amino acid and iodothyronine transport in placenta. The Biochemical Journal. 2001;356:719–725
  41. Babu E, Kanai Y, Chairoungdua A, et al. Identification of a novel system L amino acid transporter structurally distinct from heterodimeric amino acid transporters. The Journal of Biological Chemistry. 2003;278:43838–43845
  42. Bodoy S, Martin L, Zorzano A, et al. Identification of LAT4, a novel amino acid transporter with system L activity. The Journal of Biological Chemistry. 2005;280:12002–12011
  43. Zhou Y, Samson M, Osty J, et al. Evidence for a close link between the thyroid hormone transport system and the aromatic amino acid transport system T in erythrocytes. The Journal of Biological Chemistry. 1990;265:17000–17004
  44. McLeese JM, Eales JG. Characteristics of the uptake of 3,5,3′-triiodo-l-thyronine and l-thyroxine into red blood cells of rainbow trout (Oncorhynchus mykiss). General and Comparative Endocrinology. 1996;103:200–208
  45. Shimada N, Yamauchi K. Characteristics of 3,5,3′-triiodothyronine (T3)-uptake system of tadpole red blood cells: effect of endocrine-disrupting chemicals on cellular T3 response. The Journal of Endocrinology. 2004;183:627–637
  46. Yamauchi K, Eguchi R, Shimada N, et al. The effects of endocrine-disrupting chemicals on thyroid hormone binding to Xenopus laevis transthyretin and thyroid hormone receptor. Clinical Chemistry and Laboratory Medicine. 2002;40:1250–1256
  47. van der Putten HH, Joosten BJ, Klaren PH, et al. Uptake of tri-iodothyronine and thyroxine in myoblasts and myotubes of the embryonic heart cell line H9c2(2-1). The Journal of Endocrinology. 2002;175:587–596
  48. Kemp HF, Taylor PM. Interactions between thyroid hormone and tryptophan transport in rat liver are modulated by thyroid status. The American Journal of Physiology. 1997;272:E809–E816
  49. Kim DK, Kanai Y, Chairoungdua A, et al. Expression cloning of a Na+-independent aromatic amino acid transporter with structural similarity to H+/monocarboxylate transporters. The Journal of Biological Chemistry. 2001;276:17221–17228
  50. Kim DK, Kanai Y, Matsuo H, et al. The human T-type amino acid transporter-1: characterization, gene organization, and chromosomal location. Genomics. 2002;79:95–103
  51. Koepsell H. Organic cation transporters in intestine, kidney, liver, and brain. Annual Review of Physiology. 1998;60:243–266
  52. Croop JM, Tiller GE, Fletcher JA, et al. Isolation and characterization of a mammalian homolog of the Drosophila white gene. Gene. 1997;185:77–85
  53. Alderson R, Pastan I, Cheng S. Characterization of the 3,3′,5-triiodo-l-thyronine-binding site on plasma membranes from human placenta. Endocrinology. 1985;116:2621–2630
  54. Pliam NB, Goldfine ID. High affinity thyroid hormone binding sites on purified rat liver plasma membranes. Biochemical and Biophysical Research Communications. 1977;79:166–172
  55. Gordon A, Spira O. Triiodothyronine binding in rat anterior pituitary, posterior pituitary, median eminence and brain. Endocrinology. 1975;96:1357–1365
  56. Prasad PD, Mahesh VB, Leibach FH, et al. Functional coupling between a bafilomycin A1-sensitive proton pump and a probenecid-sensitive folate transporter in human placental choriocarcinoma cells. Biochimica et Biophysica Acta. 1994;1222:309–314
  57. Liang VC, Sedgwick T, Shi YB. Characterization of the Xenopus homolog of an immediate early gene associated with cell activation: sequence analysis and regulation of its expression by thyroid hormone during amphibian metamorphosis. Cell Research. 1997;7:179–193
  58. Benvenga S, Robbins J. Thyroid hormone efflux from monolayer cultures of human fibroblasts and hepatocytes. Effect of lipoproteins and other thyroxine transport proteins. Endocrinology. 1998;139:4311–4318
  59. Bobek S, Sechman A, Wieczorek E, et al. Reverse 3,3′,5′-triiodothyronine (rT3) enhances hyperglycemic and lipemic effects of heat-stress in chickens. Hormone and Metabolic Research. 1997;29:252–254
  60. Dutkowsky JP, Smith RA, Calandruccio RA, et al. Effect of fetal thyroid hormone (RT3) on sarcoma cells in culture. Journal of Orthopaedic Research. 1993;11:379–385
  61. du Pont JS. Is reverse triiodothyronine a physiological nonactive competitor for the action of triiodothyronine upon the electrical properties of GH3 cells?. Neuroendocrinology. 1991;54:146–150
  62. Blondeau JP. Saturable binding of thyroid hormone to isolated rat hepatocytes. FEBS Letters. 1986;204:41–46
  63. Gharbi-Chihi J, Torresani J. Thyroid hormone binding to plasma membrane preparations: studies in different thyroid states and tissues. Journal of Endocrinological Investigation. 1981;4:177–183
  64. Samson M, Osty J, Blondeau JP. Identification by photoaffinity labeling of a membrane thyroid hormone- binding protein associated with the triiodothyronine transport system in rat erythrocytes. Endocrinology. 1993;132:2470–2476
  65. Obata T, Kitagawa S, Gong QH, et al. Thyroid hormone down-regulates p55, a thyroid hormone-binding protein that is homologous to protein disulfide isomerase and the beta-subunit of prolyl-4-hydroxylase. The Journal of Biological Chemistry. 1988;263:782–785
  66. Couet J, de Bernard S, Loosfelt H, et al. Cell surface protein disulfide-isomerase is involved in the shedding of human thyrotropin receptor ectodomain. Biochemistry. 1996;35:14800–14805
  67. Pardridge WM. Carrier-mediated transport of thyroid hormones through the rat blood- brain barrier: primary role of albumin-bound hormone. Endocrinology. 1979;105:605–612
  68. Pardridge WM. Plasma protein-mediated transport of steroid and thyroid hormones. The American Journal of Physiology. 1987;252:E157–E164
  69. Freake HC, Moon YK. Hormonal and nutritional regulation of lipogenic enzyme mRNA levels in rat primary white and brown adipocytes. Journal of Nutritional Science and Vitaminology. 2003;49:40–46
  70. Silva JE. Thyroid hormone and the energetic cost of keeping body temperature. Bioscience Reports. 2005;25:129–148
  71. Klaus S, Casteilla L, Hentz E, et al. The mRNA of protein disulfide isomerase and its homologue the thyroid hormone binding protein is strongly expressed in adipose tissue. Molecular and Cellular Endocrinology. 1990;73:105–110
  72. Darras VM, Hume R, Visser TJ. Regulation of thyroid hormone metabolism during fetal development. Molecular and Cellular Endocrinology. 1999;151:37–47
  73. Kohrle J. Transfer and metabolism of thyroid gland hormones in the placenta. Acta Medica Austriaca. 1997;24:138–143
  74. Ekins RP, Sinha AK, Pickard MR, et al. Transport of thyroid hormones to target tissues. Acta Medica Austriaca. 1994;21:26–34
  75. Okamoto Y, Sakata M, Ogura K, et al. Expression and regulation of 4F2hc and hLAT1 in human trophoblasts. American Journal of Physiology. Cell Physiology. 2002;282:C196–C204
  76. Chernow B, Burman KD, Johnson DL, et al. T3 may be a better agent than T4 in the critically ill hypothyroid patient: evaluation of transport across the blood-brain barrier in a primate model. Critical Care Medicine. 1983;11:99–104
  77. Boado RJ, Li JY, Nagaya M, et al. Selective expression of the large neutral amino acid transporter at the blood-brain barrier. Proceedings of the National Academy of Sciences of the United States of America. 1999;96:12079–12084
  78. Pardridge WM. The role of blood-brain barrier transport of tryptophan and other neutral amino acids in the regulation of substrate-limited pathways of brain amino acid metabolism. Journal of Neural Transmission. Supplementum. 1979;43–54
  79. Herrero E, Aragon MC, Diez-Guerra J, et al. Ontogenetic studies on tryptophan transport into plasma membrane vesicles derived from rat brain synaptosomes: effect of thyroid hormones. Neurochemical Research. 1985;10:579–589
  80. Herrero E, Diez-Guerra J, Aragon MC, et al. Developmental studies on the uptake of tyrosine by synaptosomes and plasma membrane vesicles derived from rat brain. Effect of thyroid hormones. International Journal of Developmental Neuroscience. 1986;4:13–20
  81. Usui T, Nagumo Y, Watanabe A, et al. Brasilicardin a, a natural immunosuppressant, targets amino Acid transport system L. Chemistry & Biology. 2006;13:1153–1160
  82. Kudo Y, Boyd CA. Placental tyrosine transport and maternal phenylketonuria. Acta Paediatrica. 1996;85:109–110
  83. Thompson G, Francis D, Kirby D, et al. Pregnancy in phenylketonuria: dietary treatment aimed at normalizing maternal plasma phenylalanine concentration. Archives of Disease in Childhood. 1991;66:1346–1349
  84. Koch R, Hanley W, Levy H, et al. The Maternal Phenylketonuria International Study: 1984–2002. Pediatrics. 2003;112:1523–1529
  85. Calomme M, Vanderpas J, Francois B, et al. Effects of selenium supplementation on thyroid hormone metabolism in phenylketonuria subjects on a phenylalanine restricted diet. Biological Trace Element Research. 1995;47:349–353
  86. Jochum F, Terwolbeck K, Meinhold H, et al. Effects of a low selenium state in patients with phenylketonuria. Acta Paediatrica. 1997;86:775–777
  87. Bell C, Abrams J, Nutt D. Tryptophan depletion and its implications for psychiatry. The British Journal of Psychiatry. 2001;178:399–405
  88. Cowen PJ, Smith KA. Serotonin, dieting, and bulimia nervosa. Advances in Experimental Medicine and Biology. 1999;467:101–104
  89. Williams WA, Shoaf SE, Hommer D, et al. Effects of acute tryptophan depletion on plasma and cerebrospinal fluid tryptophan and 5-hydroxyindoleacetic acid in normal volunteers. Journal of Neurochemistry. 1999;72:1641–1647
  90. Carew LB, Alster FA, Foss DC, et al. Effect of a tryptophan deficiency on thyroid gland, growth hormone and testicular functions in chickens. The Journal of Nutrition. 1983;113:1756–1765
  91. Kulikov A, Moreau X, Jeanningros R. Effects of experimental hypothyroidism on 5-HT1A, 5-HT2A receptors, 5- HT uptake sites and tryptophan hydroxylase activity in mature rat brain1. Neuroendocrinology. 1999;69:453–459
  92. Smith KA, Fairburn CG, Cowen PJ. Symptomatic relapse in bulimia nervosa following acute tryptophan depletion. Archives of General Psychiatry. 1999;56:171–176
  93. Ooka H, Segall PE, Timiras PS. Neural and endocrine development after chronic tryptophan deficiency in rats: II. Pituitary-thyroid axis. Mechanisms of Ageing and Development. 1978;7:19–24

PII: S1521-690X(07)00023-1

doi: 10.1016/j.beem.2007.03.002

Best Practice & Research Clinical Endocrinology & Metabolism
Volume 21, Issue 2 , Pages 237-251 , June 2007