Defending plasma T3 is a biological priority

Clinical Endocrinology

Volumn 81, Issue 5, 2014, Pages 633-641

  Abdalla, Sherine M ^a   Bianco, Antonio C ^a  

^a RUSH UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LEVOTHYROXINE; LIOTHYRONINE; THYROTROPIN; THYROXINE; THYROXINE DEIODINASE; IODIDE PEROXIDASE;

ARTICLE; CIRCADIAN RHYTHM; DEIODINATION; GENE DISRUPTION; HOMEOSTASIS; HORMONAL REGULATION; HORMONE RELEASE; HUMAN; HYPOTHYROIDISM; LIOTHYRONINE BLOOD LEVEL; MONOTHERAPY; NEGATIVE FEEDBACK; PROTEIN EXPRESSION; THYROID GLAND; THYROTROPIN BLOOD LEVEL; BLOOD; BLOOD ANALYSIS; HYPOTHALAMUS HYPOPHYSIS SYSTEM; METABOLISM; PHYSIOLOGY; THYROID FUNCTION TEST;

BLOOD CHEMICAL ANALYSIS; HUMANS; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; HYPOTHYROIDISM; IODIDE PEROXIDASE; THYROID FUNCTION TESTS; THYROID GLAND; THYROXINE; TRIIODOTHYRONINE;

EID: 84912060980     PISSN: 03000664     EISSN: 13652265     Source Type: Journal    
DOI: 10.1111/cen.12538     Document Type: Article

References (87)

1. Brent, G.A., (2012) Mechanisms of thyroid hormone action. The Journal of Clinical Investigation, 122, 3035-3043.
2. Gereben, B., Zavacki, A.M., Ribich, S., et al,. (2008) Cellular and molecular basis of deiodinase-regulated thyroid hormone signaling. Endocrine Reviews, 29, 898-938.
3. Sagar, G.D., Gereben, B., Callebaut, I., et al,. (2007) Ubiquitination-induced conformational change within the deiodinase dimer is a switch regulating enzyme activity. Molecular and Cellular Biology, 27, 4774-4783.
4. Schussler, G.C., (2000) The thyroxine-binding proteins. Thyroid, 10, 141-149.
5. Jansen, J., Friesema, E.C., Milici, C., et al,. (2005) Thyroid hormone transporters in health and disease. Thyroid, 15, 757-768.
6. Jonklaas, J., Kahric-Janicic, N., Soldin, O.P., et al,. (2009) Correlations of free thyroid hormones measured by tandem mass spectrometry and immunoassay with thyroid-stimulating hormone across 4 patient populations. Clinical Chemistry, 55, 1380-1388.
7. Soldin, O.P., &, Soldin, S.J., (2011) Thyroid hormone testing by tandem mass spectrometry. Clinical Biochemistry, 44, 89-94.
8. Konno, N., Hagiwara, K., Taguchi, H., et al,. (1987) Measurements of serum-free thyroid hormone concentrations by ultrafiltration-a comparison with equilibrium dialysis & mathematical calculation. Annals of Nuclear Medicine, 1, 15-22.
9. Jonklaas, J., Davidson, B., Bhagat, S., et al,. (2008) Triiodothyronine levels in athyreotic individuals during levothyroxine therapy. JAMA, 299, 769-777.
10. Bianco, A.C., Salvatore, D., Gereben, B., et al,. (2002) Biochemistry, cellular and molecular biology, and physiological roles of the iodothyronine selenodeiodinases. Endocrine Reviews, 23, 38-89.
11. Laurberg, P., (1984) Mechanisms governing the relative proportions of thyroxine and 3,5,3-triiodothyronine in thyroid secretion. Metabolism, 33, 379-392.
12. Laurberg, P., (1987) Thyroxine and 3,5,3-triiodothyronine content of thyroglobulin in thyroid needle aspirates in hyperthyroidism and hypothyroidism. The Journal of Clinical Endocrinology and Metabolism, 64, 969-974.
13. Pilo, A., Iervasi, G., Vitek, F., et al,. (1990) Thyroidal and peripheral production of 3,5,3'-triiodothyronine in humans by multicompartmental analysis. The American Journal of Physiology, 258, E715-E726.
14. Callebaut, I., Curcio-Morelli, C., Mornon, J.P., et al,. (2003) The iodothyronine selenodeiodinases are thioredoxin-fold family proteins containing a glycoside hydrolase clan GH-A-like structure. The Journal of Biological Chemistry, 278, 36887-36896.
15. Curcio-Morelli, C., Gereben, B., Zavacki, A.M., et al,. (2003) In vivo dimerization of types 1, 2, and 3 iodothyronine selenodeiodinases. Endocrinology, 144, 937-946.
16. St Germain, D.L., Hernandez, A., Schneider, M.J., et al,. (2005) Insights into the role of deiodinases from studies of genetically modified animals. Thyroid, 15, 905-916.
17. Hosoi, Y., Murakami, M., Mizuma, H., et al,. (1999) Expression and regulation of type II iodothyronine deiodinase in cultured human skeletal muscle cells. The Journal of Clinical Endocrinology and Metabolism, 84, 3293-3300.
18. Mizuma, H., Murakami, M., &, Mori, M., (2001) Thyroid hormone activation in human vascular smooth muscle cells: expression of type II iodothyronine deiodinase. Circulation Research, 88, 313-318.
19. Wajner, S.M., dos Santos Wagner, M., Melo, R.C., et al,. (2007) Type 2 iodothyronine deiodinase is highly expressed in germ cells of adult rat testis. The Journal of Endocrinology, 194, 47-54.
20. Williams, A.J., Robson, H., Kester, M.H., et al,. (2008) Iodothyronine deiodinase enzyme activities in bone. Bone, 43, 126-134.
21. Gouveia, C.H., Christoffolete, M.A., Zaitune, C.R., et al,. (2005) Type 2 iodothyronine selenodeiodinase is expressed throughout the mouse skeleton and in the MC3T3-E1 mouse osteoblastic cell line during differentiation. Endocrinology, 146, 195-200.
22. Schneider, M.J., Fiering, S.N., Thai, B., et al,. (2006) Targeted disruption of the type 1 selenodeiodinase gene (dio1) results in marked changes in thyroid hormone economy in mice. Endocrinology, 147, 580-589.
23. Visser, T.J., (1994) Role of sulfation in thyroid hormone metabolism. Chemico-Biological Interactions, 92, 293-303.
24. Silva, J.E., &, Larsen, P.R., (1985) The potential of brown adipose tissue type II T4 5'-deiodinase as a local and systemic source of T3 in rats. The Journal of Clinical Investigation, 76, 2296-2305.
25. Skarulis, M.C., Celi, F.S., Mueller, E., et al,. (2010) Thyroid hormone induced brown adipose tissue and amelioration of diabetes in a patient with extreme insulin resistance. The Journal of Clinical Endocrinology and Metabolism, 95, 256-262.
26. Visser, T.J., (2007) Thyroid hormone transporters. Hormone Research, 68 (Suppl 5), 28-30.
27. Baqui, M.M., Gereben, B., Harney, J.W., et al,. (2000) Distinct subcellular localization of transiently expressed types 1 and 2 iodothyronine deiodinases as determined by immunofluorescence confocal microscopy. Endocrinology, 141, 4309-4312.
28. Silva, J.E., Dick, T.E., &, Larsen, P.R., (1978) The contribution of local tissue thyroxine monodeiodination to the nuclear 3,5,3'-triiodothyronine in pituitary, liver, and kidney of euthyroid rats. Endocrinology, 103, 1196-1207.
29. Curcio, C., Baqui, M.M., Salvatore, D., et al,. (2001) The human type 2 iodothyronine deiodinase is a selenoprotein highly expressed in a mesothelioma cell line. The Journal of Biological Chemistry, 276, 30183-30187.
30. Bianco, A.C., &, Silva, J.E., (1987) Nuclear 3,5,3'-triiiodothyronine (T3) in brown adipose tissue: receptor occupancy and sources of T3 as determined by in vivo techniques. Endocrinology, 120, 55-62.
31. Baqui, M., Botero, D., Gereben, B., et al,. (2003) Human type 3 iodothyronine selenodeiodinase is located in the plasma membrane and undergoes rapid internalization to endosomes. The Journal of Biological Chemistry, 278, 1206-1211.
32. Kallo, I., Mohacsik, P., Vida, B., et al,. (2012) A novel pathway regulates thyroid hormone availability in rat and human hypothalamic neurosecretory neurons. PLoS One, 7, e37860.
33. Jo, S., Kallo, I., Bardoczi, Z., et al,. (2012) Neuronal hypoxia induces hsp40-mediated nuclear import of type 3 deiodinase as an adaptive mechanism to reduce cellular metabolism. The Journal of Neuroscience, 32, 8491-8500.
34. Hernandez, A., (2005) Structure and function of the type 3 deiodinase gene. Thyroid, 15, 865-874.
35. Huang, S.A., (2005) Physiology and pathophysiology of type 3 deiodinase in humans. Thyroid, 15, 875-881.
36. Alexander, E.K., Marqusee, E., Lawrence, J., et al,. (2004) Timing and magnitude of increases in levothyroxine requirements during pregnancy in women with hypothyroidism. The New England Journal of Medicine, 351, 241-249.
37. Huang, S.A., Tu, H.M., Harney, J.W., et al,. (2000) Severe hypothyroidism caused by type 3 iodothyronine deiodinase in infantile hemangiomas. The New England Journal of Medicine, 343, 185-189.
38. Maynard, M.A., Marino-Enriquez, A., Fletcher, J.A., et al,. (2014) Thyroid hormone inactivation in gastrointestinal stromal tumors. The New England Journal of Medicine, 370, 1327-1334.
39. Curran, P.G., &, DeGroot, L.J., (1991) The effect of hepatic enzyme-inducing drugs on thyroid hormones and the thyroid gland. Endocrine Reviews, 12, 135-150.
40. Bianco, A.C., &, Kim, B.W., (2006) Deiodinases: implications of the local control of thyroid hormone action. The Journal of Clinical Investigation, 116, 2571-2579.
41. Andersen, S., Bruun, N.H., Pedersen, K.M., et al,. (2003) Biologic variation is important for interpretation of thyroid function tests. Thyroid, 13, 1069-1078.
42. Russell, W., Harrison, R.F., Smith, N., et al,. (2008) Free triiodothyronine has a distinct circadian rhythm that is delayed but parallels thyrotropin levels. The Journal of Clinical Endocrinology and Metabolism, 93, 2300-2306.
43. Geffner, D.L., Azukizawa, M., &, Hershman, J.M., (1975) Propylthiouracil blocks extrathyroidal conversion of thyroxine to triiodothyronine and augments thyrotropin secretion in man. The Journal of Clinical Investigation, 55, 224-229.
44. Gereben, B., &, Salvatore, D., (2005) Pretranslational regulation of type 2 deiodinase. Thyroid, 15, 855-864.
45. Inada, M., Kasagi, K., Kurata, S., et al,. (1975) Estimation of thyroxine and triiodothyronine distribution and of the conversion rate of thyroxine to triiodothyronine in man. The Journal of Clinical Investigation, 55, 1337-1348.
46. Nicoloff, J.T., Lum, S.M., Spencer, C.A., et al,. (1984) Peripheral autoregulation of thyroxine to triiodothyronine conversion in man. Hormone and Metabolic Research Supplement, 14, 74-79.
47. Lum, S.M., Nicoloff, J.T., Spencer, C.A., et al,. (1984) Peripheral tissue mechanism for maintenance of serum triiodothyronine values in a thyroxine-deficient state in man. The Journal of Clinical Investigation, 73, 570-575.
48. Gereben, B., Goncalves, C., Harney, J.W., et al,. (2000) Selective proteolysis of human type 2 deiodinase: a novel ubiquitin-proteasomal mediated mechanism for regulation of hormone activation. Molecular Endocrinology, 14, 1697-1708.
49. Arrojo e Drigo, R., &, Bianco, A.C., (2011) Type 2 deiodinase at the crossroads of thyroid hormone action. International Journal of Biochemistry & Cell Biology, 43, 1432-1441.
50. Sagar, G.D., Gereben, B., Callebaut, I., et al,. (2008) The thyroid hormone-inactivating deiodinase functions as a homodimer. Molecular Endocrinology, 22, 1382-1393.
51. Zeold, A., Pormuller, L., Dentice, M., et al,. (2006) Metabolic instability of type 2 deiodinase is transferable to stable proteins independently of subcellular localization. The Journal of Biological Chemistry, 281, 31538-31543.
52. Dentice, M., Bandyopadhyay, A., Gereben, B., et al,. (2005) The Hedgehog-inducible ubiquitin ligase subunit WSB-1 modulates thyroid hormone activation and PTHrP secretion in the developing growth plate. Nature Cell Biology, 7, 698-705.
53. Botero, D., Gereben, B., Goncalves, C., et al,. (2002) Ubc6p and ubc7p are required for normal and substrate-induced endoplasmic reticulum-associated degradation of the human selenoprotein type 2 iodothyronine monodeiodinase. Molecular Endocrinology, 16, 1999-2007.
54. Kim, B.W., Zavacki, A.M., Curcio-Morelli, C., et al,. (2003) Endoplasmic reticulum-associated degradation of the human type 2 iodothyronine deiodinase (D2) is mediated via an association between mammalian UBC7 and the carboxyl region of D2. Molecular Endocrinology, 17, 2603-2612.
55. Zavacki, A.M., Arrojo e Drigo, R., Freitas, B.C., et al,. (2009) The E3 ubiquitin ligase TEB4 mediates degradation of type 2 iodothyronine deiodinase. Molecular and Cellular Biology, 29, 5339-5347.
56. Curcio-Morelli, C., Zavacki, A.M., Christofollete, M., et al,. (2003) Deubiquitination of type 2 iodothyronine deiodinase by von Hippel-Lindau protein-interacting deubiquitinating enzymes regulates thyroid hormone activation. The Journal of Clinical Investigation, 112, 189-196.
57. Arrojo, E.D.R., Egri, P., Jo, S., et al,. (2013) The type II deiodinase is retrotranslocated to the cytoplasm and proteasomes via p97/Atx3 complex. Molecular Endocrinology, 27, 2105-2115.
58. Schneider, M.J., Fiering, S.N., Pallud, S.E., et al,. (2001) Targeted disruption of the type 2 selenodeiodinase gene (DIO2) results in a phenotype of pituitary resistance to T4. Molecular Endocrinology, 15, 2137-2148.
59. Berry, M.J., Grieco, D., Taylor, B.A., et al,. (1993) Physiological and genetic analyses of inbred mouse strains with a type I iodothyronine 5' deiodinase deficiency. The Journal of Clinical Investigation, 92, 1517-1528.
60. Christoffolete, M.A., Arrojo e Drigo, R., Gazoni, F., et al,. (2007) Mice with impaired extrathyroidal thyroxine to 3,5,3'-triiodothyronine conversion maintain normal serum 3,5,3'-triiodothyronine concentrations. Endocrinology, 148, 954-960.
61. Galton, V.A., Schneider, M., Clark, A.S., et al,. (2009) Life without T4 to T3 conversion: studies in mice devoid of the 5'-deiodinases. Endocrinology, 150, 2957-2963.
62. Fonseca, T.L., Correa-Medina, M., Campos, M.P., et al,. (2013) Coordination of hypothalamic and pituitary T3 production regulates TSH expression. The Journal of Clinical Investigation, 123, 1492-1500.
63. Riesco, G., Taurog, A., Larsen, P.R., et al,. (1977) Acute and chronic responses to iodine deficiency in rats. Endocrinology, 100, 303-313.
64. Santisteban, P., Obregon, M.J., Rodriguez-Pena, A., et al,. (1982) Are iodine-deficient rats euthyroid? Endocrinology, 110, 1780-1789.
65. Bianco, A.C., Anderson, G., Forrest, D., et al,. (2014) American thyroid association guide to investigating thyroid hormone economy and action in rodent and cell models. Thyroid, 24, 88-168.
66. Huang, S.A., &, Bianco, A.C., (2008) Reawakened interest in type III iodothyronine deiodinase in critical illness and injury. Nature Clinical Practice Endocrinology & Metabolism, 4, 148-155.
67. Escobar- Morreale, H.F., Obregon, M.J., Escobar del Rey, F., et al,. (1995) Replacement therapy for hypothyroidism with thyroxine alone does not ensure euthyroidism in all tissues, as studied in thyroidectomized rats. The Journal of Clinical Investigation, 96, 2828-2838.
68. Escobar- Morreale, H.F., Rey, F., Obregon, M.J., et al,. (1996) Only the combined treatment with thyroxine and triiodothyronine ensures euthyroidism in all tissues of the thyroidectomized rat. Endocrinology, 137, 2490-2502.
69. Stock, J.M., Surks, M.I., &, Oppenheimer, J.H., (1974) Replacement dosage of L-thyroxine in hypothyroidism. A re-evaluation. The New England Journal of Medicine, 290, 529-533.
70. Pearce, C.J., &, Himsworth, R.L., (1984) Total and free thyroid hormone concentrations in patients receiving maintenance replacement treatment with thyroxine. British Medical Journal, 288, 693-695.
71. Ito, M., Miyauchi, A., Morita, S., et al,. (2012) TSH-suppressive doses of levothyroxine are required to achieve preoperative native serum triiodothyronine levels in patients who have undergone total thyroidectomy. European Journal of Endocrinology, 167, 373-378.
72. Gullo, D., Latina, A., Frasca, F., et al,. (2011) Levothyroxine monotherapy cannot guarantee euthyroidism in all athyreotic patients. PLoS One, 6, e22552.
73. Wiersinga, W.M., Duntas, L., Fadeyev, V., et al,. (2012) 2012 ETA guidelines: the use of L-T4+ L-T3 in the treatment of hypothyroidism. European Thyroid Journal, 1, 55-71.
74. Wiersinga, W.M., (2014) Paradigm shifts in thyroid hormone replacement therapies for hypothyroidism. Nature Reviews Endocrinology, 10, 164-174.
75. Biondi, B., &, Wartofsky, L., (2012) Combination treatment with T4 and T3: toward personalized replacement therapy in hypothyroidism? The Journal of Clinical Endocrinology and Metabolism, 97, 2256-2271.
76. Appelhof, B.C., Fliers, E., Wekking, E.M., et al,. (2005) Combined therapy with levothyroxine and liothyronine in two ratios, compared with levothyroxine monotherapy in primary hypothyroidism: a double-blind, randomized, controlled clinical trial. The Journal of Clinical Endocrinology and Metabolism, 90, 2666-2674.
77. Nygaard, B., Jensen, E.W., Kvetny, J., et al,. (2009) Effect of combination therapy with thyroxine (T4) and 3,5,3'-triiodothyronine versus T4 monotherapy in patients with hypothyroidism, a double-blind, randomised cross-over study. European Journal of Endocrinology, 161, 895-902.
78. Bunevicius, R., Kazanavicius, G., Zalinkevicius, R., et al,. (1999) Effects of thyroxine as compared with thyroxine plus triiodothyronine in patients with hypothyroidism. The New England Journal of Medicine, 340, 424-429.
79. Clyde, P.W., Harari, A.E., Getka, E.J., et al,. (2003) Combined levothyroxine plus liothyronine compared with levothyroxine alone in primary hypothyroidism: a randomized controlled trial. JAMA, 290, 2952-2958.
80. Siegmund, W., Spieker, K., Weike, A.I., et al,. (2004) Replacement therapy with levothyroxine plus triiodothyronine (bioavailable molar ratio 14:1) is not superior to thyroxine alone to improve well-being and cognitive performance in hypothyroidism. Clinical Endocrinology, 60, 750-757.
81. Walsh, J.P., Shiels, L., Lim, E.M., et al,. (2003) Combined thyroxine/liothyronine treatment does not improve well-being, quality of life, or cognitive function compared to thyroxine alone: a randomized controlled trial in patients with primary hypothyroidism. The Journal of Clinical Endocrinology and Metabolism, 88, 4543-4550.
82. Grozinsky-Glasberg, S., Fraser, A., Nahshoni, E., et al,. (2006) Thyroxine-triiodothyronine combination therapy versus thyroxine monotherapy for clinical hypothyroidism: meta-analysis of randomized controlled trials. The Journal of Clinical Endocrinology and Metabolism, 91, 2592-2599.
83. Ma, C., Xie, J., Huang, X., et al,. (2009) Thyroxine alone or thyroxine plus triiodothyronine replacement therapy for hypothyroidism. Nuclear Medicine Communications, 30, 586-593.
84. Panicker, V., Saravanan, P., Vaidya, B., et al,. (2009) Common variation in the DIO2 gene predicts baseline psychological well-being and response to combination thyroxine plus triiodothyronine therapy in hypothyroid patients. The Journal of Clinical Endocrinology and Metabolism, 94, 1623-1629.
85. Saravanan, P., Siddique, H., Simmons, D.J., et al,. (2007) Twenty-four hour hormone profiles of TSH, Free T3 and free T4 in hypothyroid patients on combined T3/T4 therapy. Experimental and Clinical Endocrinology & Diabetes, 115, 261-267.
86. Celi, F.S., Zemskova, M., Linderman, J.D., et al,. (2011) Metabolic effects of liothyronine therapy in hypothyroidism: a randomized, double-blind, crossover trial of liothyronine versus levothyroxine. The Journal of Clinical Endocrinology and Metabolism, 96, 3466-3474.
87. Santini, F., Giannetti, M., Ricco, I., et al,. (2014) Steady state serum T3 concentrations for 48 hours following the oral administration of a single dose of 3,5,3'-Triiodothyronine Sulfate (T3S). Endocrine Practice, [Epub ahead of print].