The Combination of a High-fat Diet and Chronic Stress Aggravates Insulin Resistance in Wistar Male Rats

Abstract

We observed the effects of the combination of a high-fat diet and chronic stress on insulin resistance. Male Wistar rats were fed on either a control or a high-fat diet and given chronic stress with the electric foot shock or not for 10 weeks. After checking the glucose infusion rate (GIR) and the HOMA-IR index, the results showed that the three groups all revealed insulin resistance with increased free fatty acid (FFA), adrenocorticotropic hormone (ACTH) and corticosterone in the serum, in addition to increased tumour necrosis factor α (TNF-α) in the serum and adipose tissue, and decreased density of high affinity receptors (R1) and expression of peroxisome proliferator-activated receptor-α (PPARα) mRNA in the hepatocytes as compared with the control, but the highest alteration on aforementioned parameters revealed in the chronic stress fed with a high-fat diet. Significant interactions between high-fat diet and chronic stress were revealed on GIR, HOMA-IR index, FFA, ACTH, corticosterone, TNF-α (in adipose tissue) and R1. These observations strongly suggest that a combination of a high-fat diet and chronic stress can produce a synergic effect on aggravating insulin resistance associated with the abnormal hypothalamic-pituitary-adrenocortical axis, endocrine abnormality of the adipose tissue, and pathological changes of the liver.

insulin resistance - high-fat diet - chronic stress - synergistic effect

References

• 1 Abbasi F, Brown BW, Lamendola C. et al . Relationship between obesity, insulin resistance, and coronary heart disease risk.  J Am Coll Cardiol. 2002;  40 937-943
• 2 Bara Mlinar, Janja Marc. Molecular mechanisms of insulin resistance and associated diseases.  Clinica Chimica Acta. 2007;  375 20-35
• 3 Storlien LH, Pan DA, Kriketos AD. et al . High fat diet-induced insulin resistance. Lessons and implications from animal studies.  Acad. 1993;  683 82-90
• 4 Rosmond R. Role of stress in the pathogenesis of the metabolic syndrome.  Psychoneuroendocrinology. 2005;  30 1-10
• 5 Bierhaus A. Linking Stress to Inflammation.  Anesthesiology Clinics of North America. 2006;  24 325-340
• 6 Kukreja RS, Datta BN, Chakravarti RN. Catecholamine-induced aggravation of aortic and coronary atherosclerosis in monkeys.  Atherosclerosis. 1981;  40 291-298
• 7 Sood V, Chakravarti RN. Systemic stress in the production of cardiac thrombosis in hypercholesterolaemic rats.  Res Exp Med (Berl). 1976;  167 31-45
• 8 Yamaguchi K, Matsuoka A. Effects of a high fat diet and electric stress on adenylate cyclase activity and insulin release in isolated islets of Langerhans.  Nippon Naibunpi Gakkai Zasshi. 1979;  55 1482-1492
• 9 Yamaguchi K, Takashima S, Masuyama T. Effects of the electric stress on insulin secretion and glucose metabolism in rats fed with a high fat diet.  Endokrinologie. 1981;  78 253-261
• 10 Efthimia Kitrakia , George Soulisa , Kyriaki Gerozissisb . Impaired neuroendocrine response to stress following a short-term fat-enriched diet.  Neuroendocrinology. 2004;  79 338-345
• 11 Sarah E, Adam M, Jonathan K. et al . Combination of high fat diet and chronic stress retracts hippocampal dendrites.  Neuroreport. 2005;  16 39-43
• 12 Ariadne Legendre, Ruth BS. Exaggerated response to mild stress in rats fed high-fat diet.  Am J Physiol Regul Integr Comp Physiol. 2006;  291 1288-1294
• 13 Kraegen EW, Clark PW, Jenkins AB. et al . Development of muscle insulin resistance after liver insulin resistance in high-fat-fed rats.  Diabetes. 1991;  11 1397-1403
• 14 Morris F, White C, Kahn R. Molecular aspects of insulin action. In: Kahn CR, Weir GC, eds. Joslin's Diabetes Mellitus, 13th ed. Philadelphia: Lippincott Williams & Wilkins 1994
• 15 Morris F, White C, Kahn R. Molecular aspects of insulin action. In: Kahn CR, Weir GC, eds. Joslin's Diabetes Mellitus, 13th ed. Philadelphia: Lippincott Williams & Wilkins 1994
• 16 Iwashita S, Tanida M, Suzuki M. Decreased skeletal muscle insulin receptors in high-fat diet-related hypertensive rats.  Nutrition Research. 2002;  22 1049-1053
• 17 Su JL, Simmons CJ, Wisely B. Monitoring of PPAR alpha protein expression in human tissue by the use of PPAR alpha-specific MAbs.  Hybridoma. 1998;  17 47-53
• 18 Schrauwen P. High-fat diet, muscular lipotoxicity and insulin resistance.  Proc Nutr Soc. 2007;  66 33-41
• 19 Surwit RS, Schneider MS. Role of stress in the etiology and treatment of diabetes mellitus.  Psychosomatic Medicine. 1993;  55 380-393
• 20 Boden G, Chen X, Ruiz J. Mechanisms of fatty acid-induced inhibition of glucose uptake.  J Clin Invest. 1994;  93 2438-2346
• 21 Bevilacqua S, Bonadonna R, Buzzigoli G. et al . Acute elevation of free fatty acid levels leads to hepatic insulin resistance in obese subjects.  Metabolism. 1987;  36 502-506
• 22 Hotamisligil GS, Shargill NS, Spiegelman BM. Adipocyte expression of tumor necrosis factor-α: direct role in obesity-linked insulin resistance.  Science. 1993;  259 87-91
• 23 Ronit Avitsura, Annemieke Kavelaarsb, Cobi Heijnenb. et al . Social stress and the regulation of tumor necrosis factor-α secretion.  Brain, Behavior, and Immunity. 2005;  19 311-317
• 24 Iwa IH, Ohno Y, Aoki N. The Effect of Leptin, Tumor Necrosis Factor-alpha (TNF-alpha), and Nitric Oxide (NO) Production on Insulin Resistance in Otsuka Long-Evans Fatty Rats.  Endocr J. 2003;  50 673-680
• 25 Yamaguchi K, Matsuoka A. The effects of electric stress on pancreatic B cell function in rats fed a high fat diet (I). Glucose tolerance and glucose-induced insulin release from the perfused pancreas.  Metabolism. 2002;  51 708-715
• 26 Kraegen EW, James DE, Bennett SP. et al . Chishonlm, In vivo insulin sensitivity in the rat determined by euglycemic clamp.  Am J Physio. 1983;  245 1-7
• 27 Nishimura H, Kuzuya H, Okamoto M. et al . Postreceptor defect in insulin action in streptozotocin-induced diabetic rat.  A m J Physiol. 1989;  256 624-630
• 28 Rybkin I, Zhou Y, Volaufova J. et al . Effect of restraint stress on food intake and body weight is determined by time of day.  Am J Physiol. 1997;  273 1612-1622
• 29 Harris BS, Jun Zhou, Youngblood BD. et al . Effect of repeated stress on body weight and body composition of rats fed low-and high-fat diets.  Am J Physiol Regulatory Integrative Comp Physiol. 1998;  275 1928-1938
• 30 Yuka Toyoshima, Oksana Gavrilova, Shoshana Yakar. et al . A prospective analysis of the HOMA model The Mexico City Diabetes Study.  Diabetes Care. 1996;  19 1138-1141
• 31 Jellinger PS. Metabolic consequences of hyperglycemia and insulin resistance.  Clin Cornerstone. 2007;  8 30-42
• 32 Schwarz JM, Linfoot P, Dare D. et al . Hepatic de novo lipogenesis in normoinsulinemic and hyperinsulinemic subjects consuming high-fat, low-carbohydrate and low-fat, high-carbohydrate isoenergetic diets.  Am J Clin Nutr. 2003;  77 43-50
• 33 Yeaman SJ. Hormone sensitive lipase-new roles for an old enzyme.  BiochemJ. 2004;  379 1120-1121
• 34 Mead JR, Irvine SA, Ramj ID. Lipoprotein lipase: structure, function, regulation, and role in disease.  J Mol Med. 2002;  80 753-769
• 35 Mohammed taouis, Derouet M, Chevalier B. et al . Corticosterone effect on insulin receptor number and kinase activity in chicken muscle and live.  General and comparative endocrinology. 1993;  89 167-175
• 36 Stephens JM, Pekala PH. Transcriptional repression of the GLUT-4 and c/EBP genes in 3T3-L1 cells by tumor necrosis factor-alpha.  J Biol Chem. 1991;  266 21839-21845
• 37 Hotamisligil GS, Peraldi P, Budavari A. et al . IRS-1-mediated inhibition of insulin receptor tyrosine kinase activity in TNF-α and obesity induced insulin resistance.  Science. 1996;  127 665-668
• 38 Baron AD. Insulin resistance and vascular function.  J Diabetes Complications. 2002;  16 92-102
• 39 Lammert E. The vascular trigger of type II diabetes mellitus.  Exp Clin Endocrinol Diabetes. 2008;  116 S21-25
• 40 Stratmann B, Tschoepe D. Sweet heart – contributions of metabolism in the development of heart failure in diabetes mellitus.  Exp Clin Endocrinol Diabetes. 2008;  116 S40-S45

Correspondence