Thyroid hormone contributes to the hypolipidemic effect of polyunsaturated fatty acids from fish oil: In vivo evidence for cross talking mechanisms

Journal of Endocrinology

Volumn 211, Issue 1, 2011, Pages 65-72

  Souza, Luana Lopes ^b   Cordeiro, Aline ^b   Oliveira, Lorraine Soares ^b   De Paula, Gabriela Silva Monteiro ^b   Faustino, Larissa Costa ^b   Maria, Tania Ortiga Carvalho ^b   Oliveira, Karen Jesus ^a   Cabanelas, Carmen Pazos Moura ^b  

^a FLUMINENSE FEDERAL UNIVERSITY   (Brazil)

^b FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLESTEROL; FISH OIL; GLYCEROL 3 PHOSPHATE DEHYDROGENASE; LIOTRIX; MESSENGER RNA; OMEGA 3 FATTY ACID; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; THIAMAZOLE; THYROID HORMONE; TRIACYLGLYCEROL; ALPHA-GLYCEROPHOSPHORIC ACID; ANTILIPEMIC AGENT; GLYCEROPHOSPHATE; THYROID HORMONE RECEPTOR BETA; UNSATURATED FATTY ACID;

ANIMAL EXPERIMENT; ARTICLE; BODY FAT; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; HYPOLIPEMIA; HYPOTHYROIDISM; IN VIVO STUDY; LIPID METABOLISM; LIVER METABOLISM; MALE; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN EXPRESSION; RAT; RECEPTOR UPREGULATION; TRIACYLGLYCEROL BLOOD LEVEL; ANIMAL; ANIMAL MODEL; BLOOD; DRUG EFFECT; LIVER; METABOLISM; ORAL DRUG ADMINISTRATION; PHYSIOLOGY; SIGNAL TRANSDUCTION; WISTAR RAT;

ADMINISTRATION, ORAL; ANIMALS; CHOLESTEROL; FATTY ACIDS, UNSATURATED; FISH OILS; GLYCEROPHOSPHATES; HYPOLIPIDEMIC AGENTS; LIVER; MALE; MODELS, ANIMAL; PPAR ALPHA; RATS; RATS, WISTAR; RECEPTOR CROSS-TALK; SIGNAL TRANSDUCTION; THYROID HORMONE RECEPTORS BETA; THYROID HORMONES; TRIGLYCERIDES;

EID: 80555125121     PISSN: 00220795     EISSN: 14796805     Source Type: Journal    
DOI: 10.1530/JOE-11-0142     Document Type: Article

References (59)

1. Abrams JJ, Grundy SM & Ginsberg H 1981 Metabolism of plasma triglycerides in hypothyroidism and hyperthyroidism in man. Journal of Lipid Research 22 307-322.
2. Adams AC, Astapova I, Fisher FM, Badman MK, Kurgansky KE, Flier JS, Hollenberg AN & Maratos-Flier E 2010 Thyroid hormone regulates hepatic expression of fibroblast growth factor 21 in a PPARalphadependent manner. Journal of Biological Chemistry 285 14078-14082. (doi:10.1074/jbc.C110.107375)
3. Agren JJ, Hänninen O, Julkunen A, Fogelholm L, Vidgren H, Schwab U, Pynnönen O & Uusitupa M 1996 Fish diet, fish oil and docosahexaenoic acid rich oil lower fasting and postprandial plasma lipid levels. European Journal of Clinical Nutrition 50 765-771.
4. Akamine R, Yamamoto T, Watanabe M, Yamazaki N, Kataoka M, Ishikawa M, Ooie T, Baba Y & Shinohara Y 2007 Usefulness of the 5' region of the cDNA encoding acidic ribosomal phosphoprotein P0 conserved among rats, mice, and humans as a standard probe for gene expression analysis in different tissues and animal species. Journal of Biochemical and Biophysical Methods 70 481-486. (doi:10.1016/j.jbbm.2006.11.008)
5. Araki O, Ying H, Zhu XG, Willingham MC & Cheng SY 2009 Distinct dysregulation of lipid metabolism by unliganded thyroid hormone receptor isoforms. Molecular Endocrinology 23 308-315. (doi:10.1210/me.2008-0311)
6. Awad AB, Bernardis LL & Fink CS 1990 Failure to demonstrate an effect of dietary fatty acid composition on body weight, body composition and parameters of lipid metabolism in mature rats. Journal of Nutrition 120 1277-1282.
7. Bonilla S, Redonnet A, Noël-Suberville C, Groubet R, Pallet V & Higueret P 2001 Effect of a pharmacological activation of PPAR on the expression of RAR and TR in rat liver. Journal of Physiology and Biochemistry 57 1-8. (doi:10.1007/BF03179807)
8. Bordoni A, Di Nunzio M, Danesi F & Biagi PL 2006 Polyunsaturated fatty acids: from diet to binding to PPARs and other nuclear receptors. Genes and Nutrition 1 95-106. (doi:10.1007/BF02829951)
9. Bradford MM 1976 A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72 248-254. (doi:10.1016/0003-2697 (76)90527-3)
10. Buroker NE, Young ME, Wei C, Serikawa K, Ge M, Ning XH & Portman MA 2007 The dominant negative thyroid hormone receptor beta-mutant {Delta}337T alters PPAR{alpha} signaling in heart. American Journal of Physiology. Endocrinology and Metabolism 292 E453-E460. (doi:10.1152/ajpendo.00267.2006)
11. Couture P & Hulbert AJ 1995 Relationship between body mass, tissue metabolic rate, and sodium pump activity in mammalian liver and kidney. American Journal of Physiology 268 641-650.
12. Dallongeville J, Baugé E, Tailleux A, Peters JM, Gonzalez FJ, Fruchart JC & Staels B 2001 Peroxisome proliferator-activated receptor alpha is not ratelimiting for the lipoprotein-lowering action of fish oil. Journal of Biological Chemistry 276 4634-4639. (doi:10.1074/jbc.M008809200)
13. Duplus E & Forest C 2002 Is there a single mechanism for fatty acid regulation of gene transcription? Biochemical Pharmacology 64 893-901. (doi:10.1016/S0006-2952(02)01157-7)
14. Erem C, Deĝer O, Bostan M, Orem A, Sönmez M, Ulusoy S & Telatar M 1999 Plasma lipoprotein (a) concentrations in hypothyroid, euthyroid and hyperthyroid subjects. Acta Cardiologica 54 77-81.
15. 3 in hypothyroidism but not in euthyroidism in mice. Experimental Physiology 96 790-800. (doi:10.1113/expphysiol.2011.058172)
16. Flores-Morales A, Gullberg H, Fernandez L, Sta°hlberg N, Lee NH, Vennström B & Norstedt G 2002 Patterns of liver gene expression governed by TRbeta. Molecular Endocrinology 16 1257-1268. (doi:10.1210/me.16.6. 1257)
17. Gaíva MH, Couto RC, Oyama LM, Couto GE, Silveira VL, Riberio EB & Nascimento CM 2001 Polyunsaturated fatty acid-rich diets: effect on adipose tissue metabolism in rats. British Journal of Nutrition 86 371-377. (doi:10.1079/BJN2001392)
18. Gani AO & Sylte I 2008 Molecular recognition of docosahexaenoic acid by peroxisome proliferator-activated receptors and retinoid-X receptor a. Journal of Molecular Graphics & Modelling 27 217-224. (doi:10.1016/j.jmgm. 2008.04.008)
19. Gullberg H, Rudling M, Forrest D, Angelin B & Vennström B 2000 Thyroid hormone receptor beta-deficient mice show complete loss of the normal cholesterol 7alpha-hydroxylase (CYP7A) response to thyroid hormone but display enhanced resistance to dietary cholesterol. Molecular Endocrinology 14 1739-1749. (doi:10.1210/me.14.11.1739)
20. 3 regulation of cholesterol metabolism in mice. Molecular Endocrinology 16 1767-1777. (doi:10.1210/me.2002-0009)
21. Hashimoto K, Cohen RN, Yamada M, Markan KR, Monden T, Satoh T, Mori M & Wondisford FE 2006 Cross-talk between thyroid hormone receptor and liver X receptor regulatory pathways is revealed in a thyroid hormone resistance mouse model. Journal of Biological Chemistry 281 295-302. (doi:10.1074/jbc.M507877200)
22. Hodin RA, Lazar MA & Chin WW 1990 Differential and tissue-specific regulation of the multiple rat c-erbA messenger RNA species by thyroid hormone. Journal of Clinical Investigation 85 101-105. (doi:10.1172/JCI114398)
23. Howell G III, Deng X, Yellaturu C, Park EA, Wilcox HG, Raghow R & Elam MB 2009 N-3 polyunsaturated fatty acids suppress insulin-induced SREBP-1c transcription via reduced trans-activating capacity of LXRalpha. Biochimica et Biophysica Acta 1791 1190-1196. (doi:10.1016/j.bbalip. 2009.08.008)
24. Hulbert AJ, Faulks SC & Buffenstein R 2006 Oxidation-resistant membrane phospholipids can explain longevity differences among the longest-living rodents and similarly-sized mice. Journals of Gerontology. Series A, Biological Sciences and Medical Sciences 61 1009-1018.
25. Johansson L, Rudling M, Scanlan TS, Lunda°sen T, Webb P, Baxter J, Angelin B & Parini P 2005 Selective thyroid receptor modulation by GC-1 reduces serum lipids and stimulates steps of reverse cholesterol transport in euthyroid mice. PNAS 102 10297-10302. (doi:10.1073/pnas. 0504379102)
26. Jump DB 2008 N-3 polyunsaturated fatty acid regulation of hepatic gene transcription. Current Opinion in Lipidology 19 242-247. (doi:10.1097/MOL.0b013e3282ffaf6a)
27. Jump DB, Botolin D, Wang Y, Xu J, Demeure O & Christian B 2008 Docosahexaenoic acid (DHA) and hepatic gene transcription. Chemistry and Physics of Lipids 153 3-13. (doi:10.1016/j.chemphyslip.2008.02.007)
28. de Lange P, Feola A, Ragni M, Senese R, Moreno M, Lombardi A, Silvestri E, Amat R, Villarroya F, Goglia F et al. 2007 Differential 3,5,3'-triiodothyronine- mediated regulation of uncoupling protein 3 transcription: role of fatty acids. Endocrinology 148 4064-4072. (doi:10.1210/en.2007-0206)
29. Lee YP & Lardy HA 1965 Influence of thyroid hormones on l-alphaglycerophosphate dehydrogenases and other dehydrogenases in various organs of the rat. Journal of Biological Chemistry 240 1427-1436.
30. Liu YY & Brent GA 2010 Thyroid hormone crosstalk with nuclear receptor signaling in metabolic regulation. Trends in Endocrinology and Metabolism 21 166-173. (doi:10.1016/j.tem.2009.11.004)
31. Liu YY, Heymann RS, Moatamed F, Schultz JJ, Sobel D & Brent GA 2007 A mutant thyroid hormone receptor alpha antagonizes peroxisome proliferator-activated receptor alpha signaling in vivo and impairs fatty acid oxidation. Endocrinology 148 1206-1217. (doi:10.1210/en.2006-0836)
32. Lu C & Cheng SY 2010 Thyroid hormone receptors regulate adipogenesis and carcinogenesis via crosstalk signaling with peroxisome proliferatoractivated receptors. Journal of Molecular Endocrinology 44 143-154. (doi:10. 1677/JME-09-0107)
33. Machado DS, Sabet A, Santiago LA, Sidhaye AR, Chiamolera MI, Ortiga-Carvalho TM & Wondisford FE 2009 A thyroid hormone receptor mutation that dissociates thyroid hormone regulation of gene expression in vivo. PNAS 106 9441-9446. (doi:10.1073/pnas.0903227106)
34. Manna S, Janarthan M, Ghosh B, Rana B, Rana A & Chatterjee M 2010 Fish oil regulates cell proliferation, protect DNA damages and decrease HER-2/neu and c-Myc protein expression in rat mammary carcinogenesis. Clinical Nutrition 29 531-537. (doi:10.1016/j.clnu.2009.12.012)
35. Menahan LA & Sobocinski KA 1983 Comparison of carbohydrate and lipid metabolism in mice and rats during fasting. Comparative Biochemistry and Physiology, Part B 74 859-864. (doi:10.1016/0305-0491(83)90157-8)
36. Ortiga-Carvalho TM, Curty FH, Nascimento-Saba CC, Moura EG, Polak J & Pazos-Moura CC 1997 Pituitary neuromedin B content in experimental fasting and diabetes mellitus and correlation with thyrotropin secretion. Metabolism 46 149-153. (doi:10.1016/S0026-0495(97)90293-6)
37. Pacot C, Charmoillaux M, Goudonnet H, Truchot RC & Latruffe N 1993 Role of thyroid state on induction by ciprofibrate of laurate hydroxylase and peroxisomal enzymes in rat liver microsomes. Biochemical Pharmacology 45 1437-1446. (doi:10.1016/0006-2952(93)90043-V)
38. Patsouris D, Mandard S, Voshol PJ, Escher P, Tan NS, Havekes LM, KoenigW, MärzW, Tafuri S, WahliWet al. 2004 PPARalpha governs glycerol metabolism. Journal of Clinical Investigation 114 94-103. (doi:10.1172/JCI20468)
39. Redonnet A, Groubet R, Noël-Suberville C, Bonilla S, Martinez A & Higueret P 2001 Exposure to an obesity-inducing diet early affects the pattern of expression of peroxisome proliferator, retinoic acid, and triiodothyronine nuclear receptors in the rat. Metabolism 50 1161-1167. (doi:10.1053/meta.2001.26759)
40. Reeves PG, Nielsen FH & Fahey GC Jr 1997 AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. Journal of Nutrition 123 1939-1951.
41. Sadow PM, Chassande O, Gauthier K, Samarut J, Xu J, O'Malley BW & Weiss RE 2003 Specificity of thyroid hormone receptor subtype and steroid receptor coactivator-1 on thyroid hormone action. American Journal of Physiology. Endocrinology and Metabolism 284 E36-E46. (doi:10.1152/ajpendo.00226.2002)
42. Shoemaker RL & Yamazaki RK 1991 Thyroid hormone-independent regulation of mitochondrial glycerol-3-phosphate dehydrogenase by the peroxisome proliferator clofibric acid. Biochemical Pharmacology 41 652-655. (doi:10.1016/0006-2952(91)90644-K)
43. Souza LL, Nunes MO, Paula GS, Cordeiro A, Penha-Pinto V, Neto JF, Oliveira KJ, do Carmo MG & Pazos-Moura CC 2010 Effects of dietary fish oil on thyroid hormone signaling in the liver. Journal of Nutritional Biochemistry 21 935-940. (doi:10.1016/j.jnutbio.2009.07.008)
44. Spector AA 1999 Essentiality of fatty acids. Lipids 34 S1-S3. (doi:10.1007/BF02562220)
45. Stansbie D, Brownsey RW, Crettaz M & Denton RM 1976 Acute effects in vivo of anti-insulin serum on rates of fatty acid synthesis and activities of acetyl-coenzyme A carboxylase and pyruvate dehydrogenase in liver and epididymal adipose tissue of fed rats. Biochemical Journal 160 413-416.
46. Strait KA, Schwartz HL, Perez-Castillo A & Oppenheimer JH 1990 Relationship of c-erbA mRNA content to tissue triiodothyronine nuclear binding capacity and function in developing and adult rats. Journal of Biological Chemistry 265 10514-10521.
47. Su W & Jones PJ 1993 Dietary fatty acid composition influences energy accretion in rats. Journal of Nutrition 123 2109-2114.
48. Sugiyama E, Ishikawa Y, Li Y, Kagai T, Nobayashi M, Tanaka N, Kamijo Y, Yokoyama S, Hara A & Aoyama T 2008 Eicosapentaenoic acid lowers plasma and liver cholesterol levels in the presence of peroxisome proliferators-activated receptor alpha. Life Sciences 83 19-28. (doi:10.1016/j.lfs.2008.04.011)
49. Suzuki K, Takahashi K, Nishimaki-Mogami T, Kagechika H, Yamamoto M & Itabe H 2009 Docosahexaenoic acid induces adipose differentiation-related protein through activation of retinoid X receptor in human choriocarcinoma BeWo cells. Biological & Pharmaceutical Bulletin 32 1177-1182. (doi:10.1248/bpb.32.1177)
50. Villicev CM, Freitas FR, Aoki MS, Taffarel C, Scanlan TS, Moriscot AS, Ribeiro MO, Bianco AC & Gouveia CH 2007 Thyroid hormone receptor beta-specific agonist GC-1 increases energy expenditure and prevents fatmass accumulation in rats. Journal of Endocrinology 193 21-29. (doi:10.1677/joe.1.07066)
51. Wakutsu M, Tsunoda N, Shiba S, Muraki E & Kasono K 2010 Peroxisome proliferator-activated receptors (PPARs)-independent functions of fish oil on glucose and lipid metabolism in diet-induced obese mice. Lipids in Health and Disease 9 101. (doi:10.1186/1476-511X-9-101)
52. Weitzel JM, Hamann S, Jauk M, Lacey M, Filbry A, Radtke C, Iwen KA, Kutz S, Harneit A, Lizardi PM et al. 2003 Hepatic gene expression patterns in thyroid hormone-treated hypothyroid rats. Journal of Molecular Endocrinology 31 291-303. (doi:10.1677/jme.0.0310291)
53. Yahagi N, Shimano H, Hasty AH, Amemiya-Kudo M, Okazaki H, Tamura Y, Iizuka Y, Shionoiri F, Ohashi K, Osuga J et al. 1999 A crucial role of sterol regulatory element-binding protein-1 in the regulation of lipogenic gene expression by polyunsaturated fatty acids. Journal of Biological Chemistry 274 35840-35844. (doi:10.1074/jbc.274.50.35840)
54. Yen PM 2001 Physiological and molecular basis of thyroid hormone action. Physiological Reviews 81 1097-1142.
55. Ying H, Araki O, Furuya F, Kato Y & Cheng SY 2007 Impaired adipogenesis caused by a mutated thyroid hormone alpha1 receptor. Molecular and Cellular Biology 27 2359-2371. (doi:10.1128/MCB.02189-06)
56. Yoshikawa T, Shimano H, Yahagi N, Ide T, Amemiya-Kudo M, Matsuzaka T, Nakakuki M, Tomita S, Okazaki H, Tamura Y et al. 2002 Polyunsaturated fatty acids suppress sterol regulatory element-binding protein 1c promoter activity by inhibition of liver X receptor (LXR) binding to LXR response elements. Journal of Biological Chemistry 277 1705-1711. (doi:10.1074/jbc. M105711200)
57. Yu YH, Wang PH, Cheng WT, Mersmann HJ, Wu SC & Ding ST 2010 Porcine peroxisome proliferator-activated receptor delta mediates the lipolytic effects of dietary fish oil to reduce body fat deposition. Journal of Animal Science 88 2009-2018. (doi:10.2527/jas.2009-2597)
58. Zandieh-Doulabi B, Platvoetter Schiphorst M, Kalsbeek A, Wiersinga WM & Bakker O 2004 Hyper and hypothyroidism change the expression and diurnal variation of thyroid hormone receptor isoforms in rat liver without major changes in their zonal distribution. Molecular and Cellular Endocrinology 219 69-75. (doi:10.1016/j.mce.2004.01.008)
59. Zavacki AM, Ying H, Christoffolete MA, Aerts G, So E, Harney JW, Cheng SY, Larsen PR & Bianco AC 2005 Type 1 iodothyronine deiodinase is a sensitive marker of peripheral thyroid status in the mouse. Endocrinology 146 1568-1575. (doi:10.1210/en.2004-1392)