Beyond low plasma T 3: Local thyroid hormone metabolism during inflammation and infection

Endocrine Reviews

Volumn 32, Issue 5, 2011, Pages 670-693

  Boelen, Anita ^a   Kwakkel, Joan ^a   Fliers, Eric ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

DEIODINASE 1; DEIODINASE 2; DEIODINASE 3; IODIDE PEROXIDASE; LIOTHYRONINE; PRALMORELIN; PROTIRELIN; THYROTROPIN; UNCLASSIFIED DRUG; THYROID HORMONE; THYROID HORMONE RECEPTOR;

ACUTE DISEASE; ADIPOSE TISSUE; BACTERIAL INFECTION; GENE ACTIVATION; GENE ACTIVITY; GENETIC TRANSCRIPTION; HORMONE ACTION; HORMONE TRANSPORT; HUMAN; IMMUNE RESPONSE; INFLAMMATION; LIOTHYRONINE BLOOD LEVEL; LIPID METABOLISM; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; RNA TRANSLATION; SKELETAL MUSCLE; THYROID HORMONE METABOLISM; BLOOD; CHRONIC DISEASE; ENZYMOLOGY; EUTHYROID SICK SYNDROME; GENE EXPRESSION; GENETICS; GRANULOCYTE; HYPOPHYSIS; HYPOTHALAMUS; INFECTION; LIVER; METABOLISM; MUSCLE; PATHOPHYSIOLOGY; PHYSIOLOGY; THYROID GLAND;

ACUTE DISEASE; ADIPOSE TISSUE; BACTERIAL INFECTIONS; CHRONIC DISEASE; EUTHYROID SICK SYNDROMES; GENE EXPRESSION; GRANULOCYTES; HUMANS; HYPOTHALAMUS; INFECTION; INFLAMMATION; IODIDE PEROXIDASE; LIVER; MUSCLES; PITUITARY GLAND; RECEPTORS, THYROID HORMONE; THYROID GLAND; THYROID HORMONES; TRIIODOTHYRONINE;

EID: 83355164457     PISSN: 0163769X     EISSN: None     Source Type: Journal    
DOI: 10.1210/er.2011-0007     Document Type: Review

References (183)

1. Docter R, Krenning EP, de Jong M, Hennemann G 1993 The sick euthyroid syndrome: changes in thyroid hormone serum parameters and hormone metabolism. Clin Endocrinol (Oxf) 39:499-518
2. Kaptein EM, MacIntyre SS, Weiner JM, Spencer CA, Nicoloff JT 1981 Free thyroxine estimates in nonthyroidal illness: comparison of eight methods. J Clin Endocrinol Metab 52:1073-1077
3. Bello G, Pennisi MA, Montini L, Silva S, Maviglia R, Cavallaro F, Bianchi A, De Marinis L, Antonelli M 2009 Nonthyroidal illness syndrome and prolonged mechanical ventilation in patients admitted to the ICU. Chest 135:1448-1454
4. Gangemi EN, Garino F, Berchialla P, Martinese M, Arecco F, Orlandi F, Stella M 2008 Low triiodothyronine serum levels as a predictor of poor prognosis in burn patients. Burns 34:817-824
5. Boelen A, Wiersinga WM, Kohrle J 2006 Contributions of cytokines to nonthyroidal illness. Curr Opin Endocrinol Diabetes 13:444-450
6. Sato K, Satoh T, Shizume K, Ozawa M, Han DC, Imamura H, Tsushima T, Demura H, Kanaji Y, Ito Y 1990 Inhibition of 125I organification and thyroid hormone release by interleukin-1, tumor necrosis factor-α, and interferon-γ in human thyrocytes in suspension culture. J Clin Endocrinol Metab 70:1735-1743
7. Tominaga T, Yamashita S, Nagayama Y, Morita S, Yokoyama N, Izumi M, Nagataki S 1991 Interleukin 6 inhibits human thyroid peroxidase gene expression. Acta Endocrinol (Copenh) 124:290-294
8. Tang KT, Braverman LE, DeVito WJ 1995 Tumor necrosis factor-α and interferon-γ modulate gene expression of type I 5′-deiodinase, thyroid peroxidase, and thyroglobulin in FRTL-5 rat thyroid cells. Endocrinology 136:881-888
9. van der Poll T, Romijn JA, Wiersinga WM, Sauerwein HP 1990 Tumor necrosis factor: a putative mediator of the sick euthyroid syndrome in man. J Clin Endocrinol Metab 71:1567-1572
10. Stouthard JM, van der Poll T, Endert E, Bakker PJ, Veenhof CH, Sauerwein HP, Romijn JA 1994 Effects of acute and chronic interleukin-6 administration on thyroid hormone metabolism in humans. J Clin Endocrinol Metab 79:1342-1346
11. Boelen A, Platvoet-ter Schiphorst MC, Bakker O, Wiersinga WM 1995 The role of cytokines in the lipopolysaccharide- induced sick euthyroid syndrome in mice. J Endocrinol 146:475-483
12. Hermus RM, Sweep CG, van derMeer MJ, Ross HA, Smals AG, Benraad TJ, Kloppenborg PW 1992 Continuous infusion of interleukin-1β induces a nonthyroidal illness syndrome in the rat. Endocrinology 131:2139-2146
13. Wiersinga WM 2005 Nonthyroidal illness. In: Braverman LE, Utiger RD, eds. The thyroid. 8th ed. Philadelphia: Lippincott; 246-263
14. Fliers E, Guldenaar SE, Wiersinga WM, Swaab DF 1997 Decreased hypothalamic thyrotropin-releasing hormone gene expression in patients with nonthyroidal illness. J Clin Endocrinol Metab 82:4032-4036
15. Vanden Berghe G, Wouters P, Weekers F, Mohan S, Baxter RC, Veldhuis JD, Bowers CY, Bouillon R 1999 Reactivation of pituitary hormone release and metabolic improvement by infusion of growth hormone-releasing peptide and thyrotropin-releasing hormone in patients with protracted critical illness. J Clin Endocrinol Metab 84:1311-1323
16. Boelen A, Kwakkel J, Thijssen-Timmer DC, Alkemade A, Fliers E, Wiersinga WM 2004 Simultaneous changes in central and peripheral components of the hypothalamuspituitary- thyroid axis in lipopolysaccharide-induced acute illness in mice. J Endocrinol 182:315-323
17. Sugiyama D, Kusuhara H, Taniguchi H, Ishikawa S, Nozaki Y, Aburatani H, Sugiyama Y 2003 Functional characterization of rat brain-specific organic anion transporter (Oatp14) at the blood-brain barrier: high affinity transporter for thyroxine. J Biol Chem 278:43489-43495
18. Heuer H, Maier MK, Iden S, Mittag J, Friesema EC, Visser TJ, Bauer K 2005 The monocarboxylate transporter 8 linked to human psychomotor retardation is highly expressed in thyroid hormone-sensitive neuron populations. Endocrinology 146:1701-1706
19. Alkemade A, Friesema EC, Unmehopa UA, Fabriek BO, Kuiper GG, Leonard JL, Wiersinga WM, Swaab DF, Visser TJ, Fliers E 2005 Neuroanatomical pathways for thyroid hormone feedback in the human hypothalamus. J Clin Endocrinol Metab 90:4322-4334
20. Visser WE, Friesema EC, Visser TJ 2011 Minireview: thyroid hormone transporters: the knowns and the unknowns. Mol Endocrinol 25:1-14
21. Braun D, Kinne A, Bräuer AU, Sapin R, Klein MO, Köhrle J, Wirth EK, Schweizer U 2011 Developmental and cell type-specific expression of thyroid hormone transporters in the mouse brain and in primary brain cells. Glia 59:463-471
22. Alkemade A, Friesema EC, Kalsbeek A, Swaab DF, Visser TJ, Fliers E 2011 Expression of thyroid hormone transporters in the human hypothalamus. J Clin Endocrinol Metab 96:E967-E971
23. Mebis L, Debaveye Y, Ellger B, Derde S, Ververs EJ, Langouche L, Darras VM, Fliers E, Visser TJ, Van den Berghe G 2009 Changes in the central component of the hypothalamus-pituitary-thyroid axis in a rabbit model of prolonged critical illness. Crit Care 13:R147
24. Köhrle J 2000 The selenoenzyme family of deiodinase isozymes controls local thyroid hormone availability. Rev Endocr Metab Disord 1:49-58
25. Jakobs TC, Schmutzler C, Meissner J, Köhrle J 1997 The promoter of the human type I 5′-deiodinase gene-mapping of the transcription start site and identification of a DR4 thyroid-hormone-responsive element. Eur J Biochem 247:288-297
26. Toyoda N, Zavacki AM, Maia AL, Harney JW, Larsen PR 1995 Anovel retinoid Xreceptor-independent thyroid hormone response element is present in the human type 1 deiodinase gene. Mol Cell Biol 15:5100-5112
27. Burmeister LA, Pachucki J, St Germain DL 1997 Thyroid hormones inhibit type 2 iodothyronine deiodinase in the rat cerebral cortex by both pre- and posttranslational mechanisms. Endocrinology 138:5231-5237
28. Sagar GD, Gereben B, Callebaut I, Mornon JP, Zeöld A, da Silva WS, Luongo C, Dentice M, Tente SM, Freitas BC, Harney JW, Zavacki AM, Bianco AC 2007 Ubiquitination- induced conformational change within the deiodinase dimer is a switch regulating enzyme activity. Mol Cell Biol 27:4774-4783
29. Gereben B, Zeöld A, Dentice M, Salvatore D, Bianco AC 2008 Activation and inactivation of thyroid hormone by deiodinases: local action with general consequences. Cell Mol Life Sci 65:570-590
30. Coppola A, Liu ZW, Andrews ZB, Paradis E, Roy MC, Friedman JM, Ricquier D, Richard D, Horvath TL, Gao XB, Diano S 2007 A central thermogenic-like mechanism in feeding regulation: an interplay between arcuate nucleus T3 and UCP2. Cell Metab 5:21-33
31. Fekete C, Gereben B, Doleschall M, Harney JW, Dora JM, Bianco AC, Sarkar S, Liposits Z, Rand W, Emerson C, Kacskovics I, Larsen PR, Lechan RM 2004 Lipopolysaccharide induces type 2 iodothyronine deiodinase in the mediobasal hypothalamus: implications for the nonthyroidal illness syndrome. Endocrinology 145:1649-1655
32. Boelen A, Kwakkel J, Wiersinga WM, Fliers E 2006 Chronic local inflammation in mice results in decreased TRH and type 3 deiodinase mRNA expression in the hypothalamic paraventricular nucleus independently of diminished food intake. J Endocrinol 191:707-714
33. Boelen A, Kwakkel J, Wieland CW, St Germain DL, Fliers E, Hernandez A 2009 Impaired bacterial clearance in type 3 deiodinase-deficient mice infected with Streptococcus pneumoniae. Endocrinology 150:1984-1990
34. Coppola A, Meli R, Diano S 2005 Inverse shift in circulating corticosterone and leptin levels elevates hypothalamic deiodinase type 2 in fasted rats. Endocrinology 146:2827-2833
35. Fekete C, Sarkar S, Christoffolete MA, Emerson CH, Bianco AC, Lechan RM 2005 Bacterial lipopolysaccharide (LPS)-induced type 2 iodothyronine deiodinase (D2) activation in the mediobasal hypothalamus (MBH) is independent of the LPS-induced fall in serum thyroid hormone levels. Brain Res 1056:97-99
36. Sánchez E, Singru PS, Fekete C, Lechan RM 2008 Induction of type 2 iodothyronine deiodinase in the mediobasal hypothalamus by bacterial lipopolysaccharide: role of corticosterone. Endocrinology 149:2484-2493
37. Zeöld A, Doleschall M, Haffner MC, Capelo LP, Menyhért J, Liposits Z, da Silva WS, Bianco AC, Kacskovics I, Fekete C, Gereben B 2006 Characterization of the nuclear factor-κB responsiveness of the human dio2 gene. Endocrinology 147:4419-4429
38. Sánchez E, Singru PS, Wittmann G, Nouriel SS, Barrett P, Fekete C, Lechan RM 2010 Contribution of TNF-α and nuclear factor-κB signaling to type 2 iodothyronine deiodinase activation in the mediobasal hypothalamus after lipopolysaccharide administration. Endocrinology 151:3827-3835
39. Boelen A, Kwakkel J, Chassande O, Fliers E 2009 Thyroid hormone receptor β mediates acute illness-induced alterations in central thyroid hormone metabolism. J Neuroendocrinol 21:465-472
40. Bassett JH, Harvey CB, Williams GR 2003 Mechanisms of thyroid hormone receptor-specific nuclear and extranuclear actions. Mol Cell Endocrinol 213:1-11
41. Liu RT, Suzuki S, Miyamoto T, Takeda T, Ozata M, De-Groot LJ 1995 The dominant negative effect of thyroid hormone receptor splicing variant α 2 does not require binding to a thyroid response element. Mol Endocrinol 9:86-95
42. Chassande O, Fraichard A, Gauthier K, Flamant F, Legrand C, Savatier P, Laudet V, Samarut J 1997 Identification of transcripts initiated from an internal promoter in the c-erbA α locus that encode inhibitors of retinoic acid receptor-α and triiodothyronine receptor activities. Mol Endocrinol 11:1278-1290
43. Yen PM 2001 Physiological and molecular basis of thyroid hormone action. Physiol Rev 81:1097-1142
44. Wood WM, Dowding JM, Haugen BR, Bright TM, Gordon DF, Ridgway EC 1994 Structural and functional characterization of the genomic locus encoding the murine β 2 thyroid hormone receptor. Mol Endocrinol 8:1605-1617
45. Wallis K, Dudazy S, van Hogerlinden M, Nordström K, Mittag J, Vennström B 2010 The thyroid hormone receptor α1 protein is expressed in embryonic postmitotic neurons and persists in most adult neurons. Mol Endocrinol 24:1904-1916
46. Fliers E, Alkemade A, Wiersinga WM, Swaab DF 2006 Hypothalamic thyroid hormone feedback in health and disease. Prog Brain Res 153:189-207
47. Abel ED, Ahima RS, Boers ME, Elmquist JK, Wondisford FE 2001 Critical role for thyroid hormone receptor β2 in the regulation of paraventricular thyrotropin-releasing hormone neurons. J Clin Invest 107:1017-1023
48. Boelen A, Kwakkel GJ, Chassande O, Fliers E 2009 A possible role for the thyroid hormone receptor α in inflammation- induced changes in pituitary thyroid hormone metabolism. Thyroid 19(s1):s68 (abstract ATA)
49. Lechan RM, Fekete C 2004 Feedback regulation of thyrotropin- releasing hormone (TRH): mechanisms for the nonthyroidal illness syndrome. J Endocrinol Invest 27:105-119
50. Freitas BC, Gereben B, Castillo M, Kalló I, Zeöld A, Egri P, Liposits Z, Zavacki AM, Maciel RM, Jo S, Singru P, Sanchez E, Lechan RM, Bianco AC 2010 Paracrine signaling by glial cell-derived triiodothyronine activates neuronal gene expression in the rodent brain and human cells. J Clin Invest 120:2206-2217
51. Arem R, Wiener GJ, Kaplan SG, Kim HS, Reichlin S, Kaplan MM 1993 Reduced tissue thyroid hormone levels in fatal illness. Metabolism 42:1102-1108
52. Sagar SM, Price KJ, Kasting NW, Sharp FR 1995 Anatomic patterns of Fos immunostaining in rat brain following systemic endotoxin administration. Brain Res Bull 36:381-392
53. Marvel FA, Chen CC, Badr N, Gaykema RP, Goehler LE 2004 Reversible inactivation of the dorsal vagal complex blocks lipopolysaccharide-induced social withdrawal and c-Fos expression in central autonomic nuclei. Brain Behav Immun 18:123-134
54. Fekete C, Singru PS, Sarkar S, Rand WM, Lechan RM 2005 Ascending brainstem pathways are not involved in lipopolysaccharide- induced suppression of thyrotropin-releasing hormone gene expression in the hypothalamic paraventricular nucleus. Endocrinology 146:1357-1363
55. Alkemade A, Friesema EC, Kuiper GG, Wiersinga WM, Swaab DF, Visser TJ, Fliers E 2006 Novel neuroanatomical pathways for thyroid hormone action in the human anterior pituitary. Eur J Endocrinol 154:491-500
56. Trajkovic M, Visser TJ, Mittag J, Horn S, Lukas J, Darras VM, Raivich G, Bauer K, Heuer H 2007 Abnormal thyroid hormone metabolism in mice lacking the monocarboxylate transporter 8. J Clin Invest 117:627-635
57. Schneider MJ, Fiering SN, Pallud SE, Parlow AF, St Germain DL, Galton VA 2001 Targeted disruption of the type 2 selenodeiodinase gene (DIO2) results in a phenotype of pituitary resistance to T4. Mol Endocrinol 15:2137-2148
58. Baur A, Bauer K, Jarry H, Köhrle J 2000 Effects of proinflammatory cytokines on anterior pituitary 5′-deiodinase type I and type II. J Endocrinol 167:505-515
59. Boelen A, Kwakkel J, Platvoet-ter Schiphorst M, Baur A, Köhrle J, Wiersinga WM 2004 Contribution of interleukin- 12 to the pathogenesis of non-thyroidal illness. Horm Metab Res 36:101-106
60. Boelen A, Kwakkel J, Platvoet-ter Schiphorst M, Mentrup B, Baur A, Koehrle J, Wiersinga WM 2004 Interleukin-18, a proinflammatory cytokine, contributes to the pathogenesis of non-thyroidal illness mainly via the central part of the hypothalamus-pituitary-thyroid axis. Eur J Endocrinol 151:497-502
61. Li M, Boyages SC 1997 Expression ofβ2-thyroid hormone receptor in euthyroid and hypothyroid rat pituitary gland: an in situ hybridization and immunocytochemical study. Brain Res 773:125-131
62. Wood WM, Ocran KW, Gordon DF, Ridgway EC 1991 Isolation and characterization of mouse complementary DNAsencodingα andβ thyroid hormone receptors from thyrotrope cells: the mouse pituitary-specific β2 isoform differs at the amino terminus from the corresponding species from rat pituitary tumor cells. Mol Endocrinol 5:1049-1061
63. Forrest D, Reh TA, Rüsch A 2002 Neurodevelopmental control by thyroid hormone receptors. Curr Opin Neurobiol 12:49-56
64. Fekete C, Lechan RM 2007 Negative feedback regulation of hypophysiotropic thyrotropin-releasing hormone (TRH) synthesizing neurons: role of neuronal afferents and type 2 deiodinase. Front Neuroendocrinol 28:97-114
65. Rocchi R, Kimura H, Tzou SC, Suzuki K, Rose NR, Pinchera A, Ladenson PW, Caturegli P 2007 Toll-like receptor- MyD88and Fc receptor pathways of mast cells mediate the thyroid dysfunctions observed during nonthyroidal illness. Proc Natl Acad Sci USA 104:6019-6024
66. Nakabayashi K, Matsumi H, Bhalla A, Bae J, Mosselman S, Hsu SY, Hsueh AJ 2002 Thyrostimulin, a heterodimer of two new human glycoprotein hormone subunits, activates the thyroid-stimulating hormone receptor. J Clin Invest 109:1445-1452
67. Okada SL, Ellsworth JL, Durnam DM, Haugen HS, Holloway JL, Kelley ML, Lewis KE, Ren H, Sheppard PO, Storey HM, Waggie KS, Wolf AC, Yao LY, Webster PJ 2006 A glycoprotein hormone expressed in corticotrophs exhibits unique binding properties on thyroid-stimulating hormone receptor. Mol Endocrinol 20:414-425
68. Prummel MF, Brokken LJ, Meduri G, Misrahi M, Bakker O, Wiersinga WM 2000 Expression of the thyroid-stimulating hormone receptor in the folliculo-stellate cells of the human anterior pituitary. J Clin Endocrinol Metab 85:4347-4353
69. Sudo S, Kuwabara Y, Park JI, Hsu SY, Hsueh AJ 2005 Heterodimeric fly glycoprotein hormone-α2 (GPA2) and glycoprotein hormone-β5 (GPB5) activate fly leucine-rich repeat-containing G protein-coupled receptor-1 (DLGR1) and stimulation of human thyrotropin receptors by chimeric fly GPA2 and human GPB5. Endocrinology 146:3596-3604
70. Okajima Y, Nagasaki H, Suzuki C, Suga H, Ozaki N, Arima H, Hamada Y, Civelli O, Oiso Y 2008 Biochemical roles of the oligosaccharide chains in thyrostimulin, a heterodimeric hormone of glycoprotein hormone subunits α2 (GPA2) and β5 (GPB5). Regul Pept 148:62-67
71. Dos Santos S, Bardet C, Bertrand S, Escriva H, Habert D, Querat B 2009 Distinct expression patterns of glycoprotein hormone-α2 and -β5 in a basal chordate suggest independent developmental functions. Endocrinology 150:3815-3822
72. Suzuki C, Nagasaki H, Okajima Y, Suga H, Ozaki N, Arima H, Iwasaki Y, Oiso Y 2009 Inflammatory cytokines regulate glycoprotein subunit β5 of thyrostimulin through nuclear factor-κB. Endocrinology 150:2237-2243
73. van Zeijl CJ, Surovtseva OV, Wiersinga WM, Fliers E, Boelen A 2011 Acute inflammation increases pituitary and hypothalamic glycoprotein hormone subunit B5 (GPB5) mRNA expression in association with decreased TSH receptor mRNA expression in mice. J Neuroendocrinol 23:310-319
74. Boelen A, Platvoet-Ter Schiphorst MC, Wiersinga WM 1993 Association between serum interleukin-6 and serum 3,5,3′- triiodothyronine in nonthyroidal illness. J Clin Endocrinol Metab 77:1695-1699
75. Hashimoto H, Igarashi N, Yachie A, Miyawaki T, Sato T 1994 The relationship between serum levels of interleukin- 6 and thyroid hormone in children with acute respiratory infection. J Clin Endocrinol Metab 78:288-291
76. Raja SG, Berg GA 2007 Outcomes of off-pump coronary artery bypass surgery: current best available evidence. Indian Heart J 59:15-27
77. Sabatino L, Cerillo AG, Ripoli A, Pilo A, Glauber M, Iervasi G 2002 Is the low tri-iodothyronine state a crucial factor in determining the outcome of coronary artery bypass patients? Evidence from a clinical pilot study. J Endocrinol 175:577-586
78. Pålsson-McDermott EM, O'Neill LA 2004 Signal transduction by the lipopolysaccharide receptor, Toll-like receptor- 4. Immunology 113:153-162
79. Amma LL, Campos-Barros A, Wang Z, Vennström B, Forrest D 2001 Distinct tissue-specific roles for thyroid hormone receptorsβ and α1 in regulation of type 1 deiodinase expression. Mol Endocrinol 15:467-475
80. Macchia PE, Takeuchi Y, Kawai T, Cua K, Gauthier K, Chassande O, Seo H, Hayashi Y, Samarut J, Murata Y, Weiss RE, Refetoff S 2001 Increased sensitivity to thyroid hormone in mice with complete deficiency of thyroid hormone receptor α. Proc Natl Acad Sci USA 98:349-354
81. Wolf M, Hansen N, Greten H 1994 Interleukin 1β, tumor necrosis factor-α and interleukin 6 decrease nuclear thyroid hormone receptor capacity in a liver cell line. Eur J Endocrinol 131:307-312
82. Kwakkel J, Wiersinga WM, Boelen A 2006 Differential involvement of nuclear factor-κB and activator protein-1 pathways in the interleukin-1β-mediated decrease of deiodinase type 1 and thyroid hormone receptor β1 mRNA. J Endocrinol 189:37-44
83. Kwakkel J, Wiersinga WM, Boelen A 2007 Interleukin-1β modulates endogenous thyroid hormone receptor α gene transcription in liver cells. J Endocrinol 194:257-265
84. Schug J, Overton GC 1998 TESS: Transcription element search software on the WWW. Technical Report CBILTR- 1997-1001-v0.0. 8th ed. Philadelphia: Computational Biology and Informatics Laboratory, School of Medicine University of Pennsylvania; 1-10
85. Beigneux AP, Moser AH, Shigenaga JK, Grunfeld C, Feingold KR 2003 Sick euthyroid syndrome is associated with decreased TR expression and DNA binding in mouse liver. Am J Physiol Endocrinol Metab 284:E228-E236
86. Beigneux AP, Moser AH, Shigenaga JK, Grunfeld C, Feingold KR 2000 The acute phase response is associated with retinoid X receptor repression in rodent liver. J Biol Chem 275:16390-16399
87. Kwakkel J, Chassande O, van Beeren HC, Wiersinga WM, Boelen A 2008 Lacking thyroid hormone receptor β gene does not influence alterations in peripheral thyroid hormone metabolism during acute illness. J Endocrinol 197:151-158
88. Kwakkel J, Chassande O, van Beeren HC, Fliers E, Wiersinga WM, Boelen A 2010 Thyroid hormone receptor α modulates lipopolysaccharide-induced changes in peripheral thyroid hormone metabolism. Endocrinology 151:1959-1969
89. Jakobs TC, Mentrup B, Schmutzler C, Dreher I, Köhrle J 2002 Proinflammatory cytokines inhibit the expression and function of human type I 5′-deiodinase in HepG2 hepatocarcinoma cells. Eur J Endocrinol 146:559-566
90. Nagaya T, Fujieda M, Otsuka G, Yang JP, Okamoto T, Seo H 2000 A potential role of activated NF-κB in the pathogenesis of euthyroid sick syndrome. J Clin Invest 106:393-402
91. Yu J, Koenig RJ 2000 Regulation of hepatocyte thyroxine 5′-deiodinase by T3 and nuclear receptor coactivators as a model of the sick euthyroid syndrome. J Biol Chem 275:38296-38301
92. Yu J, Koenig RJ 2006 Induction of type 1 iodothyronine deiodinase to prevent the nonthyroidal illness syndrome in mice. Endocrinology 147:3580-3585
93. Wajner SM, Goemann IM, Bueno AL, Larsen PR, Maia AL 2011 IL-6 promotes nonthyroidal illness syndrome by blocking thyroxine activation while promoting thyroid hormone inactivation in human cells. J Clin Invest 121:1834-1845
94. Boelen A, Kwakkel J, Alkemade A, Renckens R, Kaptein E, Kuiper G, Wiersinga WM, Visser TJ 2005 Induction of type 3 deiodinase activity in inflammatory cells of mice with chronic local inflammation. Endocrinology 146:5128-5134
95. Huang SA, Mulcahey MA, Crescenzi A, Chung M, Kim BW, Barnes C, Kuijt W, Turano H, Harney J, Larsen PR 2005 Transforming growth factor-β promotes inactivation of extracellular thyroid hormones via transcriptional stimulation of type 3 iodothyronine deiodinase. Mol Endocrinol 19:3126-3136
96. Mebis L, Paletta D, Debaveye Y, Ellger B, Langouche L, D'Hoore A, Darras VM, Visser TJ, Van den Berghe G 2009 Expression of thyroid hormone transporters during critical illness. Eur J Endocrinol 161:243-250
97. Dozin B, Magnuson MA, Nikodem VM 1986 Thyroid hormone regulation of malic enzyme synthesis. Dual tissue- specific control. J Biol Chem 261:10290-10292
98. Jump DB, Narayan P, Towle H, Oppenheimer JH 1984 Rapid effects of triiodothyronine on hepatic gene expression. Hybridization analysis of tissue-specific triiodothyronine regulation of mRNAS14. J Biol Chem 259:2789-2797
99. Gullberg H, Rudling M, Forrest D, Angelin B, Vennström B 2000 Thyroid hormone receptor β-deficient mice show complete loss of the normal cholesterol 7α-hydroxylase (CYP7A) response to thyroid hormone but display enhanced resistance to dietary cholesterol. Mol Endocrinol 14:1739-1749
100. Feingold KR, Spady DK, Pollock AS, Moser AH, Grunfeld C 1996 Endotoxin, TNF, and IL-1 decrease cholesterol 7 α-hydroxylase mRNA levels and activity. J Lipid Res 37:223-228
101. Simonides WS, van Hardeveld C 2008 Thyroid hormone as a determinant of metabolic and contractile phenotype of skeletal muscle. Thyroid 18:205-216
102. Yu F, Göthe S, Wikström L, Forrest D, Vennström B, Larsson L 2000 Effects of thyroid hormone receptor gene disruption on myosin isoform expression in mouse skeletal muscles. Am J Physiol Regul Integr Comp Physiol 278: R 1545-R1554
103. Rodriguez-Perez A, Palos-Paz F, Kaptein E, Visser TJ, Dominguez-Gerpe L, Alvarez-Escudero J, Lado-Abeal J 2008 Identification of molecular mechanisms related to nonthyroidal illness syndrome in skeletal muscle and adipose tissue from patients with septic shock. Clin Endocrinol (Oxf) 68:821-827
104. Maia AL, Kim BW, Huang SA, Harney JW, Larsen PR 2005 Type 2 iodothyronine deiodinase is the major source of plasma T3 in euthyroid humans. J Clin Invest 115:2524-2533
105. Larsen PR 2009 Type 2 iodothyronine deiodinase in hu- manskeletal muscle:newinsights into its physiological role and regulation. J Clin Endocrinol Metab 94:1893-1895
106. Heemstra KA, Soeters MR, Fliers E, Serlie MJ, Burggraaf J, van Doorn MB, van der Klaauw AA, Romijn JA, Smit JW, Corssmit EP, Visser TJ 2009 Type 2 iodothyronine deiodinase in skeletal muscle: effects of hypothyroidism and fasting. J Clin Endocrinol Metab 94:2144-2150
107. Feingold KR, Moser A, Patzek SM, Shigenaga JK, Grunfeld C 2009 Infection decreases fatty acid oxidation and nuclear hormone receptors in the diaphragm. J Lipid Res 50:2055-2063
108. Mebis L, Langouche L, Visser TJ, Van den Berghe G 2007 The type II iodothyronine deiodinase is up-regulated in skeletal muscle during prolonged critical illness. J Clin Endocrinol Metab 92:3330-3333
109. Sun X, Wray C, Tian X, Hasselgren PO, Lu J 2003 Expression of uncoupling protein 3 is upregulated in skeletal muscle during sepsis. Am J Physiol Endocrinol Metab 285: E512-E520
110. Yu XX, Barger JL, Boyer BB, Brand MD, Pan G, Adams SH 2000 Impact of endotoxin on UCP homolog mRNA abundance, thermoregulation, and mitochondrial proton leak kinetics. Am J Physiol Endocrinol Metab 279:E433- E446
111. Lado-Abeal J, Romero A, Castro-Piedras I, Rodriguez- Perez A, Alvarez-Escudero J 2010 Thyroid hormone receptors are down-regulated in skeletal muscle of patients with non-thyroidal illness syndrome secondary to non-septic shock. Eur J Endocrinol 163:765-773
112. Cheng SY, Leonard JL, Davis PJ 2010 Molecular aspects of thyroid hormone actions. Endocr Rev 31:139-170
113. Mentuccia D, Proietti-Pannunzi L, Tanner K, Bacci V, Pollin TI, Poehlman ET, Shuldiner AR, Celi FS 2002 Association between a novel variant of the human type 2 deiodinase gene Thr92Ala and insulin resistance: evidence of interaction with the Trp64Arg variant of the β-3-adrenergic receptor. Diabetes 51:880-883
114. Canani LH, Capp C, Dora JM, Meyer EL, Wagner MS, Harney JW, Larsen PR, Gross JL, Bianco AC, Maia AL 2005 The type 2 deiodinase A/G (Thr92Ala) polymorphism is associated with decreased enzyme velocity and increased insulin resistance in patients with type 2 diabetes mellitus. J Clin Endocrinol Metab 90:3472-3478
115. Dora JM, Machado WE, Rheinheimer J, Crispim D, Maia AL 2010 Association of the type 2 deiodinase Thr92Ala polymorphism with type 2 diabetes: case-control study and meta-analysis. Eur J Endocrinol 163:427-434
116. Cornell RP 1989 Hyperinsulinemia elicited by interleukin- 1 and nonlethal endotoxemia in rats. Circ Shock 28:121-130
117. Frisard MI, McMillan RP, Marchand J, Wahlberg KA, Wu Y, Voelker KA, Heilbronn L, Haynie K, Muoio B, Li L, Hulver MW 2010 Toll-like receptor 4 modulates skeletal muscle substrate metabolism. Am J Physiol Endocrinol Metab 298:E988-E998
118. Harper ME, Seifert EL 2008 Thyroid hormone effects on mitochondrial energetics. Thyroid 18:145-156
119. Moreno M, de Lange P, Lombardi A, Silvestri E, Lanni A, Goglia F 2008 Metabolic effects of thyroid hormone derivatives. Thyroid 18:239-253
120. Wrutniak-Cabello C, Casas F, Cabello G 2001 Thyroid hormone action in mitochondria. J Mol Endocrinol 26:67-77
121. Lu B, Moser AH, Shigenaga JK, Feingold KR, Grunfeld C 2006 Type II nuclear hormone receptors, coactivator, and target gene repression in adipose tissue in the acute-phase response. J Lipid Res 47:2179-2190
122. Klieverik LP, Coomans CP, Endert E, Sauerwein HP, Havekes LM, Voshol PJ, Rensen PC, Romijn JA, Kalsbeek A, Fliers E 2009 Thyroid hormone effects on whole-body energy homeostasis and tissue-specific fatty acid uptake in vivo. Endocrinology 150:5639-5648
123. Khovidhunkit W, Kim MS, Memon RA, Shigenaga JK, Moser AH, Feingold KR, Grunfeld C 2004 Effects of infection and inflammation on lipid and lipoprotein metabolism: mechanisms and consequences to the host. J Lipid Res 45:1169-1196
124. O'Mara BA, Dittrich W, Lauterio TJ, St Germain DL 1993 Pretranslational regulation of type I 5′-deiodinase by thyroid hormones and in fasted and diabetic rats. Endocrinology 133:1715-1723
125. Wartofsky L, Latham KR, Djuh YY, Burman KD 1981 Alterations in T3 and T4 receptor binding in fasting and diabetes mellitus. Life Sci 28:1683-1691
126. Chopra IJ, Huang TS, Boado R, Solomon DH, Chua Teco GN 1987 Evidence against benefit from replacement doses of thyroid hormones in nonthyroidal illness (NTI): studies using turpentine oil-injected rat. J Endocrinol Invest 10:559-564
127. Van der Geyten S, Buys N, Sanders JP, Decuypere E, Visser TJ, Kühn ER, Darras VM 1999 Acute pretranslational regulation of type III iodothyronine deiodinase by growth hormone and dexamethasone in chicken embryos. Mol Cell Endocrinol 147:49-56
128. Turnbull AV, Smith GW, Lee S, Vale WW, Lee KF, Rivier C 1999 CRF type I receptor-deficient mice exhibit a pronounced pituitary-adrenal response to local inflammation. Endocrinology 140:1013-1017
129. Gyorffy A, Sayed-Ahmed A, Zsarnovszky A, Frenyó VL, Decuypere E, Bartha T 2009 Effects of energy restriction on thyroid hormone metabolism in chickens. Acta Vet Hung 57:319-330
130. Malik IA, Baumgartner BG, Naz N, Sheikh N, Moriconi F, Ramadori G 2010 Changes in gene expression of DORand other thyroid hormone receptors in rat liver during acutephase response. Cell Tissue Res 342:261-272
131. Chamba A, Neuberger J, Strain A, Hopkins J, Sheppard MC, Franklyn JA 1996 Expression and function of thyroid hormone receptor variants in normal and chronically diseased human liver. J Clin Endocrinol Metab 81:360-367
132. Kwakkel J, van Beeren HC, Ackermans MT, Platvoet-Ter Schiphorst MC, Fliers E, Wiersinga WM, Boelen A 2009 Skeletal muscle deiodinase type 2 regulation during illness in mice. J Endocrinol 203:263-270
133. Silva JE, Larsen PR 1983 Adrenergic activation of triiodothyronine production in brown adipose tissue. Nature 305:712-713
134. Dentice M, Marsili A, Ambrosio R, Guardiola O, Sibilio A, Paik JH, Minchiotti G, DePinho RA, Fenzi G, Larsen PR, Salvatore D 2010 The FoxO3/type 2 deiodinase pathway is required for normal mouse myogenesis and muscle regeneration. J Clin Invest 120:4021-4030
135. Watanabe M, Houten SM, Mataki C, Christoffolete MA, Kim BW, Sato H, Messaddeq N, Harney JW, Ezaki O, Kodama T, Schoonjans K, Bianco AC, Auwerx J 2006 Bile acids induce energy expenditure by promoting intracellular thyroid hormone activation. Nature 439:484-489
136. Grozovsky R, Ribich S, Rosene ML, Mulcahey MA, Huang SA, Patti ME, Bianco AC, Kim BW 2009 Type 2 deiodinase expression is induced by peroxisomal proliferator- activated receptor-γ agonists in skeletal myocytes. Endocrinology 150:1976-1983
137. Köhrle J 1999 Local activation and inactivation of thyroid hormones: the deiodinase family. Mol Cell Endocrinol 151:103-119
138. Vary TC, O'Neill P, Cooney RN, Maish 3rd G, Shumate M 1999 Chronic infusion of interleukin 1 induces hyperlactatemia and altered regulation of lactate metabolism in skeletal muscle. JPEN J Parenter Enteral Nutr 23:213-217
139. Goglia F, Lanni A, Barth J, Kadenbach B 1994 Interaction of diiodothyronines with isolated cytochrome c oxidase. FEBS Lett 346:295-298
140. Dellinger RP, Levy MM, Carlet JM, Bion J, Parker MM, Jaeschke R, Reinhart K, Angus DC, Brun-Buisson C, Beale R, Calandra T, Dhainaut JF, Gerlach H, Harvey M, Marini JJ, Marshall J, Ranieri M, Ramsay G, Sevransky J, Thompson BT, Townsend S, Vender JS, Zimmerman JL, Vincent JL 2008 Surviving sepsis campaign: international guidelines for management of severe sepsis and septic shock: 2008. Crit Care Med 36:296-327
141. Bernard GR, Vincent JL, Laterre PF, La Rosa SP, Dhainaut JF, Lopez-Rodriguez A, Steingrub JS, Garber GE, Helterbrand JD, Ely EW, Fisher Jr JC 2001 Efficacy and safety of recombinant human activated protein C for severe sepsis. N Engl J Med 344:699-709
142. McClean KL, Sheehan GJ, Harding GK 1994 Intraabdominal infection: a review. Clin Infect Dis 19:100-116
143. Richmand DA, Molitch ME, O'Donnell TF 1980 Altered thyroid hormone levels in bacterial sepsis: the role of nutritional adequacy. Metabolism 29:936-942
144. Woeber KA 1971 Alterations in thyroid hormone economy during acute infection with Diplococcus pneumoniae in the rhesus monkey. J Clin Invest 50:378-387
145. Burgi U, Feller C, Gerber AU 1986 Effects of an acute bacterial infection on serum thyroid hormones and nuclear triiodothyronine receptors in mice. Endocrinology 119:515-521
146. Pinsky MR 2004 Dysregulation of the immune response in severe sepsis. Am J Med Sci 328:220-229
147. den Brinker M, Dumas B, Visser TJ, Hop WC, Hazelzet JA, Festen DA, Hokken-Koelega AC, Joosten KF 2005 Thyroid function and outcome in children who survived meningococcal septic shock. Intensive Care Med31:970-976
148. Bernstein JM 1999 Treatment of community-acquired pneumonia-IDSA guidelines. Infectious Diseases Society of America. Chest 115:9S-13S
149. Knapp S, Hareng L, Rijneveld AW, Bresser P, van der Zee JS, Florquin S, Hartung T, van der Poll T 2004 Activation of neutrophils and inhibition of the proinflammatory cytokine response by endogenous granulocyte colony-stimulating factor in murine pneumococcal pneumonia. J Infect Dis 189:1506-1515
150. Renckens R, Roelofs JJ, Florquin S, de Vos AF, Lijnen HR, van't Veer C, van der Poll T 2006 Matrix metalloproteinase- 9 deficiency impairs host defense against abdominal sepsis. J Immunol 176:3735-3741
151. Boelen A, Boorsma J, Kwakkel J, Wieland CW, Renckens R, Visser TJ, Fliers E, Wiersinga WM 2008 Type 3 deiodinase is highly expressed in infiltrating neutrophilic granulocytes in response to acute bacterial infection. Thyroid 18:1095-1103
152. Angstwurm MW, Schopohl J, Gaertner R 2004 Selenium substitution has no direct effect on thyroid hormone metabolism in critically ill patients. Eur J Endocrinol 151:47-54
153. Fredriksson K, Hammarqvist F, Strigård K, Hultenby K, Ljungqvist O, Wernerman J, Rooyackers O 2006 Derangements in mitochondrial metabolism in intercostal and leg muscle of critically ill patients with sepsis-induced multiple organ failure. Am J Physiol Endocrinol Metab 291:E1044-E1050
154. Zang Q, Maass DL, Tsai SJ, Horton JW 2007 Cardiac mitochondrial damage and inflammation responses in sepsis. Surg Infect (Larchmt) 8:41-54
155. Levy RJ, Deutschman CS 2007 Cytochrome c oxidase dysfunction in sepsis. Crit Care Med 35:S468-S475
156. Stevens RD, Dowdy DW, Michaels RK, Mendez-Tellez PA, Pronovost PJ, Needham DM 2007 Neuromuscular dysfunction acquired in critical illness: a systematic review. Intensive Care Med 33:1876-1891
157. Klebanoff SJ 2005 Myeloperoxidase: friend and foe. J Leukoc Biol 77:598-625
158. Klebanoff SJ 1967 Iodination of bacteria: a bactericidal mechanism. J Exp Med 126:1063-1078
159. Siegel E, Sachs BA 1964 In vitro leukocyte uptake of 131-I labeled iodide, thyroxine and triiodothyronine, and its relation to thyroid function. J Clin Endocrinol Metab 24:313-318
160. Woeber KA, Ingbar SH 1973 Metabolism of L-thyroxine by phagocytosing human leukocytes. J Clin Invest 52:1796-1803
161. Adelberg HM, Siemsen JK, Jung RC, Nicoloff JT 1971 Scintigraphic detection of pulmonary bacterial infections with labeled thyroid hormones and pertechnetate. Radiology 99:141-146
162. Gregerman RI, Solomon N 1967 Acceleration of thyroxine and triiodothyronine turnover during bacterial pulmonary infections and fever: implications for the functional state of the thyroid during stress and in senescence. J Clin Endocrinol Metab 27:93-105
163. Kaptein EM, Robinson WJ, Grieb DA, Nicoloff JT 1982 Peripheral serum thyroxine, triiodothyronine and reverse triiodothyronine kinetics in the low thyroxine state of acute nonthyroidal illnesses. A noncompartmental analysis. J Clin Invest 69:526-535
164. Boelen A, Mikita J, Boiziau C, Chassande O, Fliers E, Petry KG 2009 Type 3 deiodinase expression in inflammatory spinal cord lesions in rat experimental autoimmune encephalomyelitis. Thyroid 19:1401-1406
165. Van den Berghe G 2001 The neuroendocrine response to stress is a dynamic process. Best Pract Res Clin Endocrinol Metab 15:405-419
166. Weekers F, Van Herck E, Coopmans W, Michalaki M, Bowers CY, Veldhuis JD, Van den Berghe G 2002 A novel in vivo rabbit model of hypercatabolic critical illness reveals a biphasic neuroendocrine stress response. Endocrinology 143:764-774
167. Peeters RP, Wouters PJ, Kaptein E, van Toor H, Visser TJ, Van den Berghe G 2003 Reduced activation and increased inactivation of thyroid hormone in tissues of critically ill patients. J Clin Endocrinol Metab 88:3202-3211
168. Peeters RP, Kester MH, Wouters PJ, Kaptein E, van Toor H, Visser TJ, Van den Berghe G 2005 Increased thyroxine sulfate levels in critically ill patients as a result of a decreased hepatic type I deiodinase activity. J Clin Endocrinol Metab 90:6460-6465
169. Peeters RP, Wouters PJ, van Toor H, Kaptein E, Visser TJ, Van den Berghe G 2005 Serum 3,3′,5′-triiodothyronine (rT3) and 3,5,3′-triiodothyronine/rT3 are prognostic markers in critically ill patients and are associated with postmortem tissue deiodinase activities. J Clin Endocrinol Metab 90:4559-4565
170. Williams GR, Franklyn JA, Neuberger JM, Sheppard MC 1989 Thyroid hormone receptor expression in the "sick euthyroid" syndrome. Lancet 2:1477-1481
171. Thijssen-Timmer DC, Peeters RP, Wouters P, Weekers F, Visser TJ, Fliers E, Wiersinga WM, Bakker O, Van Den Berghe G 2007 Thyroid hormone receptor isoform expression in livers of critically ill patients. Thyroid 17:105-112
172. Weekers F, Giulietti AP, Michalaki M, Coopmans W, Van Herck E, Mathieu C, Van den Berghe G 2003 Metabolic, endocrine, and immune effects of stress hyperglycemia in a rabbit model of prolonged critical illness. Endocrinology 144:5329-5338
173. Weekers F, Michalaki M, Coopmans W, Van Herck E, Veldhuis JD, Darras VM, Van den Berghe G 2004 Endocrine and metabolic effects of growth hormone (GH) compared with GH-releasing peptide, thyrotropin-releasing hormone, and insulin infusion in a rabbit model of prolonged critical illness. Endocrinology 145:205-213
174. Debaveye Y, Ellger B, Mebis L, Van Herck E, Coopmans W, Darras V, Van den Berghe G 2005 Tissue deiodinase activity during prolonged critical illness: effects of exogenous thyrotropin-releasing hormone and its combination with growth hormone-releasing peptide-2. Endocrinology 146:5604-5611
175. Simonides WS, Mulcahey MA, Redout EM, Muller A, Zuidwijk MJ, Visser TJ, Wassen FW, Crescenzi A, da-Silva WS, Harney J, Engel FB, Obregon MJ, Larsen PR, Bianco AC, Huang SA 2008 Hypoxia-inducible factor induces local thyroid hormone inactivation during hypoxic-ischemic disease in rats. J Clin Invest 118:975-983
176. Debaveye Y, Ellger B, Mebis L, Visser TJ, Darras VM, Van den Berghe G 2008 Effects of substitution and high-dose thyroid hormone therapy on deiodination, sulfoconjugation, and tissue thyroid hormone levels in prolonged critically ill rabbits. Endocrinology 149:4218-4228
177. Vanhorebeek I, De Vos R, Mesotten D, Wouters PJ, De Wolf-Peeters C, Van den Berghe G 2005 Protection of hepatocyte mitochondrial ultrastructure and function by strict blood glucose control with insulin in critically ill patients. Lancet 365:53-59
178. Kaptein EM, Beale E, Chan LS 2009 Thyroid hormone therapy for obesity and nonthyroidal illnesses: a systematic review. J Clin Endocrinol Metab 94:3663-3675
179. Van den Berghe G, de Zegher F, Bouillon R 1998 Clinical review 95: acute and prolonged critical illness as different neuroendocrine paradigms. J Clin Endocrinol Metab 83:1827-1834
180. Pingitore A, Galli E, Barison A, Iervasi A, Scarlattini M, Nucci D, L'abbate A, Mariotti R, Iervasi G 2008 Acute effects of triiodothyronine (T3) replacement therapy in patients with chronic heart failure and low-T3 syndrome: a randomized, placebo-controlled study. J Clin Endocrinol Metab 93:1351-1358
181. Kaptein EM, Sanchez A, Beale E, Chan LS 2010 Clinical review: thyroid hormone therapy for postoperative nonthyroidal illnesses: a systematic review and synthesis. J Clin Endocrinol Metab 95:4526-4534
182. Debaveye Y, Ellger B, Mebis L, Darras VM, Van den Berghe G 2008 Regulation of tissue iodothyronine deiodinase activity in a model of prolonged critical illness. Thyroid 18:551-560
183. Weekers F, Van den Berghe G 2004 Endocrine modifications and interventions during critical illness. Proc Nutr Soc 63:443-450