Pigs fed saturated fat/cholesterol have a blunted hypothalamic-pituitary-adrenal function, are insulin resistant and have decreased expression of IRS-1, PGC1α and PPARα

Journal of Nutritional Biochemistry

Volumn 24, Issue 4, 2013, Pages 656-663

  Lomax, Michael A ^a   Karamanlidis, Georgios ^b   Laws, John ^c   Cremers, Stephanie G ^c   Weinberg, Peter D ^c   Clarke, Lynne ^c  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^b UNIVERSITY OF WASHINGTON   (United States)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

High saturated fatty acid cholesterol diet; Hypothalamic pituitary adrenal function; Insulin resistance; Insulin signalling; PPAR

Indexed keywords

ADIPONECTIN; ADIPONECTIN RECEPTOR 2; CORTICOTROPIN; GLUCOSE; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; HYDROCORTISONE; INSULIN; INSULIN RECEPTOR; INSULIN RECEPTOR SUBSTRATE 1; LOW DENSITY LIPOPROTEIN CHOLESTEROL; MESSENGER RNA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; SATURATED FATTY ACID;

ADIPOSE TISSUE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GLUCOSE INTOLERANCE; HYDROCORTISONE RELEASE; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; INSULIN RESISTANCE; LIPID DIET; MALE; MUSCLE; NONHUMAN; PROTEIN EXPRESSION; SWINE;

ADIPOSE TISSUE; ADRENAL GLANDS; ANIMALS; AORTA; CHOLESTEROL, DIETARY; DIETARY FATS; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; INSULIN RECEPTOR SUBSTRATE PROTEINS; INSULIN RESISTANCE; LIVER; MALE; MUSCLE, SKELETAL; PPAR ALPHA; SWINE; TRANS-ACTIVATORS;

SUIDAE;

EID: 84875072459     PISSN: 09552863     EISSN: 18734847     Source Type: Journal    
DOI: 10.1016/j.jnutbio.2012.03.013     Document Type: Article

References (67)

1. Bera T.K., Liu X.F., Yamada M., Gavrilova O., Mezey E., Tessarollo L., et al. A model for obesity and gigantism due to disruption of the Ankrd26 gene. Proc Natl Acad Sci U S A 2008, 105:270-275.
2. Gavrilova O., Geyer J., Petzinger E. In vivo relevance of Mrp2-mediated biliary excretion of the Amanita mushroom toxin demethylphalloin. Biochim Biophys Acta 2007, 1768:2070-2077.
3. Drapeau V., Therrien F., Richard D., Tremblay A. Is visceral obesity a physiological adaptation to stress?. Panminerva Med 2003, 45:189-195.
4. Nieuwenhuizen A.G., Rutters F. The hypothalamic-pituitary-adrenal-axis in the regulation of energy balance. Physiol Behav 2008, 94:169-177.
5. Reitman M.L., Mason M.M., Moitra J., Gavrilova O., Marcus-Samuels B., Eckhaus M., et al. Transgenic mice lacking white fat: models for understanding human lipoatrophic diabetes. Ann N Y Acad Sci 1999, 892:289-296.
6. Cui Y., Hosui A., Sun R., Shen K., Gavrilova O., Chen W., et al. Loss of signal transducer and activator of transcription 5 leads to hepatosteatosis and impaired liver regeneration. Hepatology 2007, 46:504-513.
7. Lee J.Y., Gavrilova O., Davani B., Na R., Robinson G.W., Hennighausen L. The transcription factors Stat5a/b are not required for islet development but modulate pancreatic beta-cell physiology upon aging. Biochim Biophys Acta 2007, 1773:1455-1461.
8. Cheung K.J., Tzameli I., Pissios P., Rovira I., Gavrilova O., Ohtsubo T., et al. Xanthine oxidoreductase is a regulator of adipogenesis and PPARgamma activity. Cell Metab 2007, 5:115-128.
9. Garcia-Prieto M.D., Tebar F.J., Nicolas F., Larque E., Zamora S., Garaulet M. Cortisol secretary pattern and glucocorticoid feedback sensitivity in women from a Mediterranean area: relationship with anthropometric characteristics, dietary intake and plasma fatty acid profile. Clin Endocrinol (Oxf) 2007, 66:185-191.
10. Jankord R., Ganjam V.K., Turk J.R., Hamilton M.T., Laughlin M.H. Exercise training alters effect of high-fat feeding on the ACTH stress response in pigs. Appl Physiol Nutr Metab 2008, 33:461-469.
11. Duong M., Cohen J.I., Convit A. High cortisol levels are associated with low quality food choice in type 2 diabetes. Endocrine 2011.
12. Postic C., Girard J. Contribution of de novo fatty acid synthesis to hepatic steatosis and insulin resistance: lessons from genetically engineered mice. J Clin Invest 2008, 118:829-838.
13. Tremblay F., Brule S. Hee Um S, Li Y, Masuda K, Roden M, Sun XJ, Krebs M, Polakiewicz RD, Thomas G, Marette A: Identification of IRS-1 Ser-1101 as a target of S6K1 in nutrient- and obesity-induced insulin resistance. Proc Natl Acad Sci U S A 2007, 104:14056-14061.
14. Anderwald C., Roden M. Adipotoxicity and the insulin resistance syndrome. Pediatr Endocrinol Rev 2004, 1:310-319.
15. Kelley D.E., Goodpaster B., Wing R.R., Simoneau J.A. Skeletal muscle fatty acid metabolism in association with insulin resistance, obesity, and weight loss. Am J Physiol 1999, 277:E1130-E1141.
16. Koves T.R., Ussher J.R., Noland R.C., Slentz D., Mosedale M., Ilkayeva O., et al. Mitochondrial overload and incomplete fatty acid oxidation contribute to skeletal muscle insulin resistance. Cell Metab 2008, 7:45-56.
17. Muoio D.M., Koves T.R. Skeletal muscle adaptation to fatty acid depends on coordinated actions of the PPARs and PGC1 alpha: implications for metabolic disease. Appl Physiol Nutr Metab 2007, 32:874-883.
18. Hu E., Liang P., Spiegelman B.M. AdipoQ is a novel adipose-specific gene dysregulated in obesity. J Biol Chem 1996, 271:10697-10703.
19. Hu X., She M., Hou H., Li Q., Shen Q., Luo Y., et al. Adiponectin decreases plasma glucose and improves insulin sensitivity in diabetic swine. Acta Biochim Biophys Sin (Shanghai) 2007, 39:131-136.
20. Kadowaki T., Yamauchi T. Adiponectin and adiponectin receptors. Endocr Rev 2005, 26:439-451.
21. Liu B.H., Wang P.H., Wang Y.C., Cheng W.M., Mersmann H.J., Ding S.T. Fasting regulates the expression of adiponectin receptors in young growing pigs. J Anim Sci 2008, 86:3377-3384.
22. Barnea M., Shamay A., Stark A.H., Madar Z. A high-fat diet has a tissue-specific effect on adiponectin and related enzyme expression. Obesity (Silver Spring) 2006, 14:2145-2153.
23. Sacks F.M., Katan M. Randomized clinical trials on the effects of dietary fat and carbohydrate on plasma lipoproteins and cardiovascular disease. Am J Med 2002, 113(Suppl. 9B):13S-24S.
24. Corson A.M., Laws J., Litten J.C., Dodds P.F., Lean I.J., Clarke L. Effect of dietary supplementation of different oils during the first or second half of pregnancy on the glucose tolerance of the sow. Animal 2008, 2:1045-1054.
25. Kimberly M.M., Leary E.T., Cole T.G., Waymack P.P. Selection, validation, standardization, and performance of a designated comparison method for HDL-cholesterol for use in the cholesterol reference method laboratory network. Clin Chem 1999, 45:1803-1812.
26. Schermer S.J., Bird J.A., Lomax M.A., Shepherd D.A.L., Symonds M.E. Effect of fetal thyroidectomy on brown adipose tissue and thermoregulation in newborn lambs. Reprod Fertil Dev 1996, 8:995-1002.
27. Mostyn A., Litten J.C., Perkins K.S., Euden P.J., Corson A.M., Symonds M.E., et al. Influence of size at birth on the endocrine profiles and expression of uncoupling proteins in subcutaneous adipose tissue, lung, and muscle of neonatal pigs. Am J Physiol Regul Integr Comp Physiol 2005, 288:R1536-R1542.
28. Cremers S.G., Weinberg P.D. Use of a desktop scanner and spreadsheet software for mapping arterial disease. Scanning 2005, 27:126-131.
29. Lomax M.A., Sadiq F., Karamanlidis G., Karamitri A., Trayhurn P., Hazlerigg D.G. Ontogenic loss of brown adipose tissue sensitivity to beta-adrenergic stimulation in the ovine. Endocrinology 2007, 148:461-468.
30. Shore A., Karamitri A., Kemp P., Speakman J.R., Lomax M.A. Role of Ucp1 enhancer methylation and chromatin remodelling in the control of Ucp1 expression in murine adipose tissue. Diabetologia 2010, 53:1164-1173.
31. Dyson M.C., Alloosh M., Vuchetich J.P., Mokelke E.A., Sturek M. Components of metabolic syndrome and coronary artery disease in female Ossabaw swine fed excess atherogenic diet. Comp Med 2006, 56:35-45.
32. 2O labeling of the deoxyribose moiety of DNA. Proc Natl Acad Sci U S A 2002, 99:15345-15350.
33. Rudanova E.E., Gavrilova O.V., Voloshko L.N. Response of siphoneal alga (Vaucheria sessilis) to the gravity factor. Aviakosm Ekolog Med 2000, 34:44-47.
34. Larsen M.O., Rolin B., Wilken M., Carr R.D., Svendsen O. High-fat high-energy feeding impairs fasting glucose and increases fasting insulin levels in the Gottingen minipig: results from a pilot study. Ann N Y Acad Sci 2002, 967:414-423.
35. Johansen T., Hansen H.S., Richelsen B., Malmlof R. The obese Gottingen minipig as a model of the metabolic syndrome: dietary effects on obesity, insulin sensitivity, and growth hormone profile. Comp Med 2001, 51:150-155.
36. Puigserver P., Spiegelman B.M. Peroxisome proliferator-activated receptor-gamma coactivator 1 alpha (PGC-1 alpha): transcriptional coactivator and metabolic regulator. Endocr Rev 2003, 24:78-90.
37. Yim S.H., Shah Y., Tomita S., Morris H.D., Gavrilova O., Lambert G., et al. Disruption of the Arnt gene in endothelial cells causes hepatic vascular defects and partial embryonic lethality in mice. Hepatology 2006, 44:550-560.
38. Matoba S., Kang J.G., Patino W.D., Wragg A., Boehm M., Gavrilova O., et al. p53 regulates mitochondrial respiration. Science 2006, 312:1650-1653.
39. Anagnostis P., Athyros V.G., Tziomalos K., Karagiannis A., Mikhailidis D.P. Clinical review: the pathogenetic role of cortisol in the metabolic syndrome: a hypothesis. J Clin Endocrinol Metab 2009, 94:2692-2701.
40. Kyrou I., Tsigos C. Stress hormones: physiological stress and regulation of metabolism. Curr Opin Pharmacol 2009, 9:787-793.
41. Rosmond R. Stress induced disturbances of the HPA axis: a pathway to Type 2 diabetes?. Med Sci Monit 2003, 9:RA35-RA39.
42. Dallman M.F. Stress update adaptation of the hypothalamic-pituitary-adrenal axis to chronic stress. Trends Endocrinol Metab 1993, 4:62-69.
43. Kumari M., Shipley M., Stafford M., Kivimaki M. Association of diurnal patterns in salivary cortisol with all-cause and cardiovascular mortality: findings from the Whitehall II study. J Clin Endocrinol Metab 2011, 96:1478-1485.
44. Rosmond R., Dallman M.F., Bjorntorp P. Stress-related cortisol secretion in men: relationships with abdominal obesity and endocrine, metabolic and hemodynamic abnormalities. J Clin Endocrinol Metab 1998, 83:1853-1859.
45. Gautam D., Gavrilova O., Jeon J., Pack S., Jou W., Cui Y., et al. Beneficial metabolic effects of M3 muscarinic acetylcholine receptor deficiency. Cell Metab 2006, 4:363-375.
46. Szendroedi J., Roden M. Mitochondrial fitness and insulin sensitivity in humans. Diabetologia 2008, 51:2155-2167.
47. Xi S., Yin W., Wang Z., Kusunoki M., Lian X., Koike T., et al. A minipig model of high-fat/high-sucrose diet-induced diabetes and atherosclerosis. Int J Exp Pathol 2004, 85:223-231.
48. Gerrity R.G., Natarajan R., Nadler J.L., Kimsey T. Diabetes-induced accelerated atherosclerosis in swine. Diabetes 2001, 50:1654-1665.
49. Spurlock M.E., Gabler N.K. The development of porcine models of obesity and the metabolic syndrome. J Nutr 2008, 138:397-402.
50. Tovar A.R., Torres N. The role of dietary protein on lipotoxicity. Biochim Biophys Acta 2010, 1801:367-371.
51. Honors M.A., Hargrave S.L., Kinzig K.P. Glucose tolerance in response to a high-fat diet is improved by a high-protein diet. Obesity (Silver Spring) 2011.
52. Delarue J., Magnan C. Free fatty acids and insulin resistance. Curr Opin Clin Nutr Metab Care 2007, 10:142-148.
53. Basciano H., Miller A.E., Naples M., Baker C., Kohen R., Xu E., et al. Metabolic effects of dietary cholesterol in an animal model of insulin resistance and hepatic steatosis. Am J Physiol Endocrinol Metab 2009, 297:E462-E473.
54. Abe H., Yamada N., Kamata K., Kuwaki T., Shimada M., Osuga J., et al. Hypertension, hypertriglyceridemia, and impaired endothelium-dependent vascular relaxation in mice lacking insulin receptor substrate-1. J Clin Invest 1998, 101:1784-1788.
55. Karamitri A., Shore A.M., Docherty K., Speakman J.R., Lomax M.A. Combinatorial transcription factor regulation of the cyclic AMP-response element on the Pgc-1alpha promoter in white 3T3-L1 and brown HIB-1B preadipocytes. J Biol Chem 2009, 284:20738-20752.
56. Karamanlidis G., Karamitri A., Docherty K., Hazlerigg D.G., Lomax M.A. C/EBPbeta reprograms white 3T3-L1 preadipocytes to a Brown adipocyte pattern of gene expression. J Biol Chem 2007, 282:24660-24669.
57. Kallwitz E.R., McLachlan A., Cotler S.J. Role of peroxisome proliferators-activated receptors in the pathogenesis and treatment of nonalcoholic fatty liver disease. World J Gastroenterol 2008, 14:22-28.
58. Holden P.R., Tugwood J.D. Peroxisome proliferator-activated receptor alpha: role in rodent liver cancer and species differences. J Mol Endocrinol 1999, 22:1-8.
59. Cheon Y., Nara T.Y., Band M.R., Beever J.E., Wallig M.A., Nakamura M.T. Induction of overlapping genes by fasting and a peroxisome proliferator in pigs: evidence of functional PPARalpha in nonproliferating species. Am J Physiol Regul Integr Comp Physiol 2005, 288:R1525-R1535.
60. Luci S., Konig B., Giemsa B., Huber S., Hause G., Kluge H., et al. Feeding of a deep-fried fat causes PPARalpha activation in the liver of pigs as a non-proliferating species. Br J Nutr 2007, 97:872-882.
61. Dai M.H., Xia T., Zhang G.D., Chen X.D., Gan L., Feng S.Q., et al. Cloning, expression and chromosome localization of porcine adiponectin and adiponectin receptors genes. Domest Anim Endocrinol 2006, 30:117-125.
62. Sabio G., Das M., Mora A., Zhang Z., Jun J.Y., Ko H.J., et al. A stress signaling pathway in adipose tissue regulates hepatic insulin resistance. Science 2008, 322:1539-1543.
63. Lord E., Ledoux S., Murphy B.D., Beaudry D., Palin M.F. Expression of adiponectin and its receptors in swine. J Anim Sci 2005, 83:565-578.
64. Liu B.H., Wang Y.C., Wu S.C., Mersmann H.J., Cheng W.T., Ding S.T. Insulin regulates the expression of adiponectin and adiponectin receptors in porcine adipocytes. Domest Anim Endocrinol 2008, 34:352-359.
65. Norman J.F., LeVeen R.F. Maternal atherogenic diet in swine is protective against early atherosclerosis development in offspring consuming an atherogenic diet post-natally. Atherosclerosis 2001, 157:41-47.
66. Hill B.J., Price E.M., Dixon J.L., Sturek M. Increased calcium buffering in coronary smooth muscle cells from diabetic dyslipidemic pigs. Atherosclerosis 2003, 167:15-23.
67. Subramanian S., Han C.Y., Chiba T., McMillen T.S., Wang S.A., Haw A., et al. Dietary cholesterol worsens adipose tissue macrophage accumulation and atherosclerosis in obese LDL receptor-deficient mice. Arterioscler Thromb Vasc Biol 2008, 28:685-691.