The role of triiodothyronine-induced substrate cycles in the hepatic response to overnutrition: Thyroid hormone as an antioxidant

Medical Hypotheses

Volumn 68, Issue 3, 2007, Pages 641-649

  Grant, Neville ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENINE NUCLEOTIDE TRANSLOCASE; ADENOSINE TRIPHOSPHATE; ANTIOXIDANT; BINDING PROTEIN; GLUTATHIONE; GLYCEROL 3 PHOSPHATE DEHYDROGENASE; GLYCEROPHOSPHATE; LIOTHYRONINE; PENTOSE PHOSPHATE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; THYROID HORMONE; THYROID HORMONE BINDING PROTEIN; THYROXINE; UNCLASSIFIED DRUG;

ARTICLE; BIOGENESIS; CITRIC ACID CYCLE; DEIODINATION; ELECTRON TRANSPORT; ESTERIFICATION; GENE EXPRESSION; GLYCOLYSIS; LIPOGENESIS; LIVER; LIVER CARCINOGENESIS; LIVER INJURY; MITOCHONDRIAL RESPIRATION; NONALCOHOLIC FATTY LIVER; OVERNUTRITION; OXIDATION; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; OXYGENATION; PRIORITY JOURNAL; PROTON MOTIVE FORCE;

ANTIOXIDANTS; HEPATOCYTES; HUMANS; LIVER; MODELS, BIOLOGICAL; OVERNUTRITION; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; TRIIODOTHYRONINE;

EID: 33845956672     PISSN: 03069877     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mehy.2006.07.045     Document Type: Article

References (79)

1. Burger A.G., O'Connell M., Scheidegger K., Woo R., and Danforth Jr. E. Monodeiodination of triiodothyronine and reverse triiodothyronine during low and high caloric diets. J Clin Endocrinol Metab 65 (1987) 829-835
2. Huang Q., Yeldandi A.V., Alvares K., Ide H., Reddy J.K., and Rao M.S. Localization of peroxisome proliferator-activated receptor in mouse and rat tissues and demonstration of its nuclear translocation in transfected CV-1 cells. Int J Oncology 6 (1995) 307-312
3. Loud A. Quantitative stereology of liver cells. J Cell Biol 37 (1968) 28-46
4. Guzmán M., Bijleveld C., and Geelen M.J.H. Flexibility of zonation of fatty acid oxidation in rat liver. Biochem J 311 (1995) 853-860
5. Oinonen T., and Lindros K.O. Zonation of hepatic cytochrome P-450 expression and regulation. Biochem J 329 (1998) 17-35
6. Raucy J.L., Lasker J.M., Kraner J.C., Salazar D.E., Lieber C.S., and Corcoran G.B. Induction of cytochrome P450IIE1 in the obese overfed rat. Mol Pharmacol 39 (1991) 275-280
7. Dey A., Kessova I.G., and Cederbaum A.I. Decreased protein and mRNA expression of ER stress proteins GRP78 and GRP94 in HepG2 cells over-expressing CYP2E1. Arch Biochem Biophys 447 (2006) 155-166
8. Jungermann K., and Kietzmann T. Zonation of parenchymal and nonparencymal metabolism in liver. Annu Rev Nutr 16 (1996) 179-203
9. Doublabi B.Z., Schiphorst M.P.-T., van Beeren H.C., Labruyere W.T., Lamers W.H., Fliers E., et al. TRβ1 protein is preferentially expressed in the pericentral zone of rat liver and exhibits marked diurnal variation. Endocrinology 143 (2002) 979-984
10. Harper M.-E., and Brand M. The quantitative contributions of mitochondrial proton leak and ATP turnover reactions to the changed respiration rates of hepatocytes from rats of different thyroid states. J Biol Chem 268 (1993) 14850-14860
11. Diamant S., Gorin E., and Shafrir E. Enzyme activities related to fatty-acid synthesis in liver and adipose tissue of rats treated with triiodthyronine. Eur J Biochem 26 (1972) 553-559
12. Hillgartner F.B., Salati L.M., and Goodridge A.G. Physiological and molecular mechanisms involved in nutritional regulation of fatty acid synthesis. Physiol Rev 75 (1995) 47-76
13. Yin L., Zhang Y., and Hillgartner F.B. Sterol regulatory element-binding protein-1 interacts with the nuclear thyroid receptor to enhance acetyl-CoA carboxylase-alpha transcription in hepatocytes. J Biol Chem 277 (2002) 19554-19565
14. Jackson-Hayes L., Song S., Lavrentyev E.N., et al. A thyroid response unit formed between the promoter and first intron of the carnitine palmitoyltransferase-Ia gene mediates the liver specific induction by thyroid hormone. J Biol Chem 278 (2003) 7964-7972
15. Brady P.S., Marine K.A., Brady L.J., and Ramsey R.R. Co-ordinate induction of hepatic mitochondrial and peroxisomal carnitine acyltransferase synthesis by diet and drugs. Biochem J 260 (1989) 93-100
16. Vega R.B., Huss J.M., and Kelly D.P. The coactivator PGC-1 cooperates with peroxisome proliferator-activated receptor α in transitional control of nuclear genes encoding mitochondrial fatty acid oxidation enzymes. Mol Cell Biol 20 (2000) 1868-1876
17. Weitzel J.M., Radtke C., and Seitz H.J. Two thyroid hormone-mediated gene expression patterns in vivo identified by cDNA expression arrays in rat. Nucleic Acids Res 29 (2001) 5148-5155
18. Wu Y., Delerive P., Chin W.W., and Burris T.P. Requirement of helix 1 and the AF-2 domain of the thyroid hormone receptor for coactivation b PGC-1. J Biol Chem 277 (2002) 8898-8905
19. Meirhaeghe A., Crowley V., Lenaghan C., et al. Characterization of the human, mouse, and rat PGC1β (peroxisome-proliferator-activated receptor-γ co-activator 1β) gene in vitro and in vivo. Biochem J 373 (2003) 155-165
20. Flores-Morales A., Gullberg H., Fernandez L., Ståhlberg N., Lee N.H., Vennström B., et al. Patterns of liver gene expression governed by TRβ. Mol Endocrinol 16 (2002) 1257-1268
21. Hardie D.G., and Carling D. The AMP-activated protein kinase: fuel gauge of the mammalian cell?. Eur J Biochem 246 (1997) 259-273
22. Winz R., Hess D., Aebersold R., and Brownsey R.W. Unique structural features and differential phosphorylation of the 280-kDa component (isozyme) of rat liver acetyl-CoA carboxylase. J Biol Chem 269 (1994) 14438-14445
23. Ntambi J.M., and Miyazaki M. Recent insights into stearoyl-CoA desaturase-1. Curr Opin Lipidol 14 (2003) 255-261
24. Waters K.M., and Ntambi J.M. Insulin and dietary fructose induce stearoyl-CoA desaturase 1 gene expression in the liver of diabetic mice. J Biol Chem 269 (1994) 27773-27777
25. Kansara M.S., Mehra A.K., Von Hagen J., Kabotyansky E., and Smith P.J. Physiological concentrations of insulin and T3 stimulate 3T3-L1 adipocyte acyl-CoA synthesis gene transcription. Am J Physiol 270 (1996) E873-E881
26. Waters K.M., Miller C.W., and Niambi J.M. Localization of a negative thyroid hormone-response region in hepatic stearoyl-CoA desaturase gene 1. Biochem Biophys Res Commun 233 (1997) 838-843
27. Shulman G.I., Ladenson P.W., Wolfe M.H., Ridgeway E.C., and Wolfe R.R. Substrate cycling between gluconeogenesis and glycolysis in euthyroid, hypothyroid and hyperthyroid man. J Clin Invest 76 (1985) 757-764
28. Hoppner W., and Seitz Hans J. Effect of thyroid hormones on glucokinase gene transcription in rat liver. J Biol Chem 264 (1989) 20643-20647
29. Khan A., Löw H., and Efendic S. Effect of thyroid hormones on the activity of glucose-6-phosphatase in fed and fasted rats. Horm Metabol Res 61 (1987) 613-617
30. MacDonald M.J. Feasibility of a mitochondrial pyruvate malate shuttle in pancreatic islets: further implications of cytosolic NADPH in insulin secretion. J Biol Chem 270 (1995) 20051-20063
31. Liu Y.Q., Jetton T.L., and Leahy J.L. β-Cell adaptation to insulin resistance: increased pyruvate carboxylase and malate-pyruvate shuttle activity in islets of nondiabetic Zucker fatty rats. J Biol Chem 277 (2002) 39163-39168
32. Farfari S., Schulz V., Corkey B., and Prentki M. Glucose-regulated anaplerosis and cataplerosis in pancreatic β-cells: possible implication of a pyruvate/citrate shuttle in insulin secretion. Diabetes 49 (2000) 718-726
33. Petersen K.F., Blair J.B., and Shulman G.I. Triiodothyronine treatment increases substrate cycling between pyruvate carboxylase and malic enzyme in perfused rat liver. Metabolism 44 (1995) 1380-1383
34. Weinberg M.B., and Utter M.F. Effect of thyroid hormone on the turnover of rat liver pyruvate carboxylase and pyruvate dehydrogenase. J Biol Chem 254 (1979) 9492-9499
35. Holness M.J., Bulmer K., Smith N.D., and Sugden M.C. Investigation of potential mechanisms regulating protein expression of hepatic pyruvate dehydrogenase kinase isoforms 2 and 4 by fatty acids and thyroid hormone. Biochem J 369 (2003) 687-695
36. Owen O.E., Kalhan S.C., and Hanson R.W. The key role of anaplerosis and cataplerosis for citric acid cycle function. J Biol Chem 277 (2002) 30409
37. Li R., Luciakova K., Zaid A., Betina S., Fridell E., and Nelson B.D. Thyroid hormone activates transcription from the promoter regions of some nuclear-encoded genes of the oxidative phosphorylation system. Mol Cell Endocrinol 128 (1997) 69-75
38. Sterling K., and Brenner M.A. Thyroid hormone action: effect of triiodothyronine on mitochondrial nucleotide translocase in vivo and in vitro. Metabolism 44 (1995) 193-199
39. Andersson U., Houstek J., and Cannon B. ATP synthase subunit c expression: physiological regulation of the P1 and P2 genes. Biochem J 323 (1997) 379-385
40. Muller S., and Seitz H. Cloning of a cDNA for the FAD-linked glycerol-3-phosphate dehydrogenase from the rat liver and its regulation by thyroid hormones. Proc Natl Acad Sci 91 (1994) 10581-10585
41. Werner H.V., and Berry M.N. Stimulatory effects of thyroxine administration on reducing-equivalent transfer from substrate to oxygen during hepatic metabolism of sorbitol and glycerol. Eur J Biochem 42 (1974) 315-324
42. 1 adrenoreceptor responsiveness. Am J Physiol 273 (1997) E1065-E1072
43. 2+ stimulation of rat liver mitochondrial glycerophosphate dehydrogenase. J Biol Chem 256 (1981) 12767-12771
44. Krebs H.A., and Eggleston L.V. The Regulation of the pentose phosphate cycle in the rat liver. Adv Enz Reg 12 (1974) 421-434
45. Miksicek R.J., and Towle H.C. Use of a cloned cDNA sequence to measure changes in 6-phosphogluconate dehydrogenase mRNA levels caused by thyroid hormone and dietary carbohydrate. J Biol Chem 258 (1983) 9575-9579
46. Filosa S., Fico A., Paglialunga F., Balestrieri M., Crooke A., Verde P., et al. Failure to increase glucose consumption through the pentose-phosphate pathway results in the death of glucose-6-phosphate dehydrogenase gene-depleted mouse embryonic stem cells subjected to oxidative stress. Biochem J 370 (2003) 935-943
47. Vie M.-P., Blanchet P., Samson M., Francon J., and Blondeau J.P. High affinity thyroid-binding protein in human kidney: kinetic characterization and identification by photoaffinity labeling. Endocrinology 137 (1996) 4563-4570
48. Vie M.-P., Evrard C., Osty J., Breton-Gilet A., Blaandhet P., Pomerance M., et al. Purification, molecular cloning, and functional expression of the human nicodinamide-adenine dinucleotide phosphate-regulated thyroid hormone-binding protein. Mol Endocrinol 11 (1997) 1728-1736
49. Kobayashi M., Hashizume K., Suzuki S., Ichikawa K., and Takeda T. A novel NADPH-dependent cytosolic 3,5,3′-triodo-l-thyronine binding protein (CTBP; 5.1S) in rat liver: a comparison with 4.72 NADPH-dependent CTBP. Endocrinology 129 (1991) 1701-1708
50. Weitzel J.M., Iwen K.A.H., and Seitz H.J. Regulation of mitochondrial biogenesis by thyroid hormone. Exp Physiol 88 1 (2003) 121-128
51. Uldry M., Yang W., St-Pierre J., Lin J., Seale P., and Spiegelman B.M. Complementary action of the PGC-1 coactivators in mitochondrial biogenesis and brown fat differentiation. Cell Metab 3 (2006) 333-341
52. Yang H., Magilnick N., Lee C., Kalmaz D., Ou X., Chan J., et al. Nrf1 and Nrf2 regulate glutamate-cysteine ligase catalytic subunit transcription indirectly via NF-κB and AP-1. Mol Cell Biol 25 (2005) 5933-5946
53. Myhrstad M.C., Husberg C., Murphy P., Nordstrom O., Blomhoff R., Moskaug J.O., et al. TCF11/Nrf1 overexpression increases the intracellular glutathione level and can transactivate the gamma-glutamylcysteine synthetase (GCS) heavy subunit promoter. Biochim Biophys Acta 1517 (2001) 212-219
54. Lee W.-S., Berry M.J., Hediger M.A., and Larsen P.R. The typer I iodothyronine 5′-deiodinase messenger nucleic acid is localized to the S3 segment of the rat proximal tubule. Endocrinolgy 132 (1993) 2136-2140
55. Aceves C., Escobar C., Rojas-Huidobro R., et al. Liver 5′-deiodinase activity is modified in rats under restricted feeding schedules: evidence for post-translational regulation. J Endocrinol 179 (2003) 91-96
56. Bianco A.C., Salvatore D., Gereben B., Berry M.J., and Larsen P.R. Biochemistry, cellular and molecular biology, and selenodeiodinases. Endocrine Rev 23 (2002) 38-89
57. Romert P., Ouistorff B., and Bhenke O. Histological evaluation of the zonation of colloidal gold uptake by the rat liver. Tissue Cell 25 (1993) 19-32
58. Fernandez V., Videla L.A., Tapia G., and Israel Y. Increases in tumor necrosis factor-alpha in response to thyroid hormone-induced liver oxidative stress in the rat. Free Radic Res 36 (2002) 719-725
59. Joshi V.C., and Aranda L.P. Hormonal regulation of the terminal enzyme of microsomal stearoyl coenzyme a desaturase in cultured avian liver explants: role of insulin. J Biol Chem 254 (1979) 11779-11782
60. Falvella F.S., Pascale R.M., Gariboldi M., Manenti G., De Miglio M.R., Simile M.M., et al. Stearoyl-Co desaturase 1 (Scd1) gene overexpression is associated with genetic disposition to hepatocarcinogenesis in mice and rats. Carcinogenesis 23 (2002) 1933-1936
61. Dobrzyn P., Dobrzyn A., Miyazaki M., Cohe P., Asilmaz E., Hardie D.G., et al. Stearoyl-CoA desaturase 1 deficiency increases fatty acid oxidation by activating AMP-activated protein kinase in liver. PNAS 101 (2004) 6409-6414
62. Cohen P., Miyazaki M., Socci N.D., Hagge-Greenberg A., Liedtke W., Soukas A.A., et al. Role for stearoyl-CoA desaturase-1 in leptin-mediated weight loss. Science 297 (2002) 240-243
63. Hillgartner F.B., and Romos D.R. Regulation of iodothyronine 5″-deiodination in lean and obese (ob/ob) mice. Am J Physiol 249 (1985) E209-E218
64. Biddinger S.B., Miyazaki M., Boucher J., Ntambi J.M., and Kahn C.R. Leptin suppresses stearoyl-CoA desaturase 1 by mechanisms independent of insulin and sterol regulatory element-binding protein-1c. Diabetes 55 (2006) 2032-2041
65. Lisboa P.C., Oliveira K.J., Cabanelas A., Ortiga-Carvalho T.M., and Pazos-Moura C.C. Acute cold exposure, leptin, and somatostatin analog (octreotide) modulate thyroid 5'-deiodinase activity. Am J Physiol 284 (2003) E1172-E1176
66. Cusin I., Rouru J., Visser T., Burger A.G., and Rohner-Jeanrenaud F. Involvement of thyroid hormones in the effect of intracerebroventricular leptin infusion on uncoupling protein-3 expression in rat muscle. Diabetes 49 (2000) 1101-1105
67. Caldwell S.H., Crespo D.M., Kang H.S., and Al-Osaimi A.M. Obesity and hepatocellular carcinoma. Gastroenterology 127 5 Suppl. 1 (2004) S97-S103
68. Factor V.M., Laskowska D., Jensen M.R., Woitach J.T., Popescu N.C., and Thorgeirsson S.S. Vitamin E reduces chromosomal damage and inhibits hepatic tumor formation in a transgenic mouse model. Proc Natl Acad Sci USA 97 (2000) 196-201
69. Santoni-Rugin E., Nagy P., Jensen M.R., Factor V.M., and Thorgeirsson S.S. Evolution of neoplastic development in the liver of transgenic mice co-expressing c-myc and transforming growth factor-alpha. Am J Path 149 (1996) 407-428
70. Scaglia N., and Igal R.A. Stearoyl-CoA desaturase is involved in the control of proliferation, anchorage-independent growth, and survival in human transformed cells. J Biol Chem 280 (2005) 25339-25349
71. Kim J.-w., Tchemyshyov I., Semeriza G.L., and Dang C.V. HIF-1-mediated expression of pyruvate dehydrogenase kinase: a metabolic switch required for cellular adaptation to hypoxia. Cell Metab 3 (2006) 177-185
72. Papandreaou I., Cairns R.A., Fontana L., Lim A.L., and Denko N.C. HIF-1 mediates adaptation to hypoxia by actively downregulating mitochondrial oxygen consumption. Cell Metab 3 (2006) 187-197
73. Moeller L.C., Dumitrescu A.M., and Refetoff S. Cytosolic action of thyroid hormone leads to induction of HIF-1α and glycolytic genes. Mol Endcrinol 12 (2005) 2955-2963
74. Rabelo R., Reyes C., Schifman A., and Silva J.E. Interactions among receptors, thyroid hormone response elements and ligands in the regulation of rat uncoupling protein gene expression by thyroid hormone. Endocrinology 137 (1996) 3478-3487
75. Gong D.W., He Y., Karas M., and Reitman M. Uncoupling protein-3 is a mediator of thermogenesis regulated by thyroid hormone, beta3-adrenergic agonists and leptin. J Biol Chem 272 (1997) 24129-24132
76. Lanni A., DeFelice M., Lombardi A., Moreno M., Fleury C., Ricquier D., et al. Induction of UCP2 mRNA by thyroid hormones in rat heart. FEBS Lett 418 (1997) 171-174
77. Baffy G., Zhang C.Y., Glickman J.N., and Lowell B.B. Obesity-related fatty liver is unchanged in mice deficient for mitochondrial uncoupling protein 2. Hepatology 35 (2002) 753-761
78. Chabicovsky M., Staniek K., Rossmanith W., Bursch W., Nohl H., and Schulte-Hermann R. Hepatocarcinogenesis in the context of strain differences in energy metabolism between inbred strains of mice (C57BL/6J and C3H/He). Adv Exp Med Biol 500 (2001) 607-611
79. Yang S., Zhu H., Li Y., Lin H., Gabrielson K., Trush M.A., et al. Mitochondrial adaptations to obesity-related oxidant stress. Arch Biochem Biophys 378 (2000) 259-268