Horm Metab Res 2012; 44(06): 458-464
DOI: 10.1055/s-0032-1306300
Animals
© Georg Thieme Verlag KG Stuttgart · New York

Early Exposure to a High-Fat Diet has more Drastic Consequences on Metabolism Compared with Exposure During Adulthood in Rats

L. F. Barella
1   Department of Cell Biology and Genetics, Laboratory of Secretion Cell Biology, State University of Maringá, Maringá, Paraná, Brazil
,
J. C. de Oliveira
1   Department of Cell Biology and Genetics, Laboratory of Secretion Cell Biology, State University of Maringá, Maringá, Paraná, Brazil
,
R.C. S. Branco
1   Department of Cell Biology and Genetics, Laboratory of Secretion Cell Biology, State University of Maringá, Maringá, Paraná, Brazil
,
R. L. Camargo
1   Department of Cell Biology and Genetics, Laboratory of Secretion Cell Biology, State University of Maringá, Maringá, Paraná, Brazil
,
R. M. Gomes
1   Department of Cell Biology and Genetics, Laboratory of Secretion Cell Biology, State University of Maringá, Maringá, Paraná, Brazil
,
F.C. V. Mendes
1   Department of Cell Biology and Genetics, Laboratory of Secretion Cell Biology, State University of Maringá, Maringá, Paraná, Brazil
,
R. A. Miranda
1   Department of Cell Biology and Genetics, Laboratory of Secretion Cell Biology, State University of Maringá, Maringá, Paraná, Brazil
,
C. Gravena
1   Department of Cell Biology and Genetics, Laboratory of Secretion Cell Biology, State University of Maringá, Maringá, Paraná, Brazil
,
R. Torrezan
1   Department of Cell Biology and Genetics, Laboratory of Secretion Cell Biology, State University of Maringá, Maringá, Paraná, Brazil
,
S. Grassiolli
1   Department of Cell Biology and Genetics, Laboratory of Secretion Cell Biology, State University of Maringá, Maringá, Paraná, Brazil
,
P. C. de Freitas Mathias
1   Department of Cell Biology and Genetics, Laboratory of Secretion Cell Biology, State University of Maringá, Maringá, Paraná, Brazil
› Author Affiliations
Further Information

Publication History

received 11 August 2011

accepted after second revision 09 February 2012

Publication Date:
21 March 2012 (online)

Abstract

The aim of this study was determine whether the introduction of a high-fat diet during the peripubertal phase induces significant changes in body weight control, glucose homeostasis and the parasympathetic tonus compared with the administration of this diet to adult rats. High-fat diet was offered to male Wistar rats at weaning or during adulthood. A group of rats received high-fat diet for 60 days, from weaning to 81-day-old (HF81) or from 60 to 120-day-old (HF120), whereas 2 other groups received a normal-fat diet (i. e., NF81 and NF120). We analyzed adiposity, glucose homeostasis, insulin sensitivity, and vagal nerve activity. High-fat diet increased the accumulation of adipose tissue in all of the rats, but the difference was greater in the rats that were fed the high-fat diet since weaning (p<0.001). The HF rats showed glucose intolerance with high levels of insulin secretion during the glucose tolerance test (p<0.01). Rats that were fed the high-fat diet presented severe insulin resistance, indicated by a low K itt (p<0.01). Interestingly, the HF81 rats exhibited greater insulin resistance compared with the HF120 rats (p<0.05). The recordings of vagus nerve activity showed that the HF rats had higher parasympathetic activity than the NF rats irrespective of age (p<0.01). Our results show that a high-fat diet offered to rats just after weaning or in adulthood both cause impairment of glycemic homeostasis and imbalance in parasympathetic activity. Importantly, the consumption of high-fat diet immediately after weaning has more drastic consequences compared with the consumption of the same diet during adulthood.

 
  • References

  • 1 Bell RR, Spencer MJ, Sherriff JL. Voluntary exercise and monounsaturated canola oil reduce fat gain in mice fed diets high in fat. J Nutr 1997; 127: 2006-2010
  • 2 Martinez JA. Body-weight regulation: causes of obesity. Proc Nutr Soc 2000; 59: 337-345
  • 3 Haslam DW, James WP. Obesity. Lancet 2005; 366 (9492) 1197-1209
  • 4 Badman MK, Flier JS. The adipocyte as an active participant in energy balance and metabolism. Gastroenterology 2007; 132: 2103-2115
  • 5 Gerozissis K. Brain insulin, energy and glucose homeostasis; genes, environment and metabolic pathologies. Eur J Pharmacol 2008; 585: 38-49
  • 6 Fehm HL, Kern W, Peters A. The selfish brain: competition for energy resources. Prog Brain Res 2006; 153: 129-140
  • 7 Ahren B. Autonomic regulation of islet hormone secretion – implications for health and disease. Diabetologia 2000; 43: 393-410
  • 8 Lenz A, Diamond Jr FB. Obesity: the hormonal milieu. Curr Opin Endocrinol Diabetes Obes 2008; 15: 9-20
  • 9 Teff KL. Visceral nerves: vagal and sympathetic innervation. JPEN J Parenter Enteral Nutr 2008; 32: 569-571
  • 10 Balbo SL, Grassiolli S, Ribeiro RA, Bonfleur ML, Gravena C, Brito Mdo N, Andreazzi AE, Mathias PC, Torrezan R. Fat storage is partially dependent on vagal activity and insulin secretion of hypothalamic obese rat. Endocrine 2007; 31: 142-148
  • 11 Bray GA, York DA. Hypothalamic and genetic obesity in experimental animals: an autonomic and endocrine hypothesis. Physiol Rev 1979; 59: 719-809
  • 12 Bray GA, York DA. The MONA LISA hypothesis in the time of leptin. Recent Prog Horm Res 1998; 53: 95-117; discussion 117–118
  • 13 Balbo SL, Mathias PC, Bonfleur ML, Alves HF, Siroti FJ, Monteiro OG, Ribeiro FB, Souza AC. Vagotomy reduces obesity in MSG-treated rats. Res Commun Mol Pathol Pharmacol 2000; 108: 291-296
  • 14 Balbo SL, Bonfleur ML, Carneiro EM, Amaral ME, Filiputti E, Mathias PC. Parasympathetic activity changes insulin response to glucose and neurotransmitters. Diabetes Metab 2002; (6 Pt 2) 3S13-3S17; discussion 13S108–13S112
  • 15 Prada PO, Pauli JR, Ropelle ER, Zecchin HG, Carvalheira JB, Velloso LA, Saad MJ. Selective modulation of the CAP/Cbl pathway in the adipose tissue of high fat diet treated rats. FEBS Lett 2006; 580: 4889-4894
  • 16 De Souza CT, Araujo EP, Bordin S, Ashimine R, Zollner RL, Boschero AC, Saad MJ, Velloso LA. Consumption of a fat-rich diet activates a proinflammatory response and induces insulin resistance in the hypothalamus. Endocrinology 2005; 146: 4192-4199
  • 17 McCormick CM, Mathews IZ. HPA function in adolescence: role of sex hormones in its regulation and the enduring consequences of exposure to stressors. Pharmacol Biochem Behav 2007; 86: 220-233
  • 18 Livingstone C, Collison M.. Sex steroids and insulin resistance. Clin Sci (Lond) 2002; 102: 151-166
  • 19 Sisk CL, Zehr JL. Pubertal hormones organize the adolescent brain and behavior. Front Neuroendocrinol 2005; 26: 163-174
  • 20 Michel C, Dunn-Meynell A, Levin BE. Reduced brain CRH and GR mRNA expression precedes obesity in juvenile rats bred for diet-induced obesity. Behav Brain Res 2004; 154: 511-517
  • 21 Boukouvalas G, Antoniou K, Papalexi E, Kitraki E. Post weaning high fat feeding affects rats’ behavior and hypothalamic pituitary adrenal axis at the onset of puberty in a sexually dimorphic manner. Neuroscience 2008; 153: 373-382
  • 22 Ropelle ER, Pauli JR, Prada PO, de Souza CT, Picardi PK, Faria MC, Cintra DE, Fernandes MF, Flores MB, Velloso LA, Saad MJ, Carvalheira JB. Reversal of diet-induced insulin resistance with a single bout of exercise in the rat: the role of PTP1B and IRS-1 serine phosphorylation. J Physiol 2006; 577 (Pt 3) 997-1007
  • 23 Vicente LL, de Moura EG, Lisboa PC, Monte Alto Costa A, Amadeu T, Mandarim-de-Lacerda CA, Passos MC. Malnutrition during lactation in rats is associated with higher expression of leptin receptor in the pituitary of adult offspring. Nutrition 2004; 20: 924-928
  • 24 Bernardis LL, Patterson BD. Correlation between “Lee Index” and carcass fat content in weanling and adults female rats with hypothalamic lesions. J Endocrinol 1968; 40: 527-528
  • 25 Rogers P, Webb GP. Estimation of body fat in normal and obese mice. Br J Nutr 1980; 43: 83-86
  • 26 Bergmeyer HU, Gawehn K. Methods of enzymatic analysis. 2nd English ed. Weinheim: Verlag Chemie; New York, London: Academic Press; 1974
  • 27 Scott AM, Atwater I, Rojas E. A method for the simultaneous measurement of insulin release and B cell membrane potential in single mouse islets of Langerhans. Diabetologia 1981; 21: 470-475
  • 28 Lundbaek K. Intravenous glucose tolerance as a tool in definition and diagnosis of diabetes mellitus. Br Med J 1962; 1 (5291) 1507-1513
  • 29 Scomparin DX, Gomes RM, Grassiolli S, Rinaldi W, Martins AG, de Oliveira JC, Gravena C, de Freitas Mathias PC. Autonomic activity and glycemic homeostasis are maintained by precocious and low intensity training exercises in MSG-programmed obese mice. Endocrine 2009; 36: 510-517
  • 30 Erdei N, Toth A, Pasztor ET, Papp Z, Edes I, Koller A, Bagi Z. High-fat diet-induced reduction in nitric oxide-dependent arteriolar dilation in rats: role of xanthine oxidase-derived superoxide anion. Am J Physiol Heart Circ Physiol 2006; 291: H2107-H2115
  • 31 Woods SC, D’Alessio DA, Tso P, Rushing PA, Clegg DJ, Benoit SC, Gotoh K, Liu M, Seeley RJ. Consumption of a high-fat diet alters the homeostatic regulation of energy balance. Physiol Behav 2004; 83: 573-578
  • 32 Estadella D, Oyama LM, Damaso AR, Ribeiro EB, Oller Do Nascimento CM. Effect of palatable hyperlipidic diet on lipid metabolism of sedentary and exercised rats. Nutrition 2004; 20: 218-224
  • 33 Mohamed-Ali V, Pinkney JH, Coppack SW. Adipose tissue as an endocrine and paracrine organ. Int J Obes Relat Metab Disord 1998; 22: 1145-1158
  • 34 Wajchenberg BL, Nery M, Cunha MR, Silva ME. Adipose tissue at the crossroads in the development of the metabolic syndrome, inflammation and atherosclerosis. Arq Bras Endocrinol Metabol 2009; 53: 145-150
  • 35 Raz I, Eldor R, Cernea S, Shafrir E. Diabetes: insulin resistance and derangements in lipid metabolism. Cure through intervention in fat transport and storage. Diabetes Metab Res Rev 2005; 21: 3-14
  • 36 Savastano DM, Covasa M. Adaptation to a high-fat diet leads to hyperphagia and diminished sensitivity to cholecystokinin in rats. J Nutr 2005; 135: 1953-1959
  • 37 Leibowitz SF, Dourmashkin JT, Chang GQ, Hill JO, Gayles EC, Fried SK, Wang J. Acute high-fat diet paradigms link galanin to triglycerides and their transport and metabolism in muscle. Brain Res 2004; 1008: 168-178
  • 38 Warwick ZS. Probing the causes of high-fat diet hyperphagia: a mechanistic and behavioral dissection. Neurosci Biobehav Rev 1996; 20: 155-161
  • 39 Borst SE, Conover CF. High-fat diet induces increased tissue expression of TNF-alpha. Life Sci 2005; 77: 2156-2165
  • 40 Posey KA, Clegg DJ, Printz RL, Byun J, Morton GJ, Vivekanandan-Giri A, Pennathur S, Baskin DG, Heinecke JW, Woods SC, Schwartz MW, Niswender KD. Hypothalamic proinflammatory lipid accumulation, inflammation, and insulin resistance in rats fed a high-fat diet. Am J Physiol Endocrinol Metab 2009; 296: E1003-E1012
  • 41 Sclafani A. Psychobiology of food preferences. Int J Obes Relat Metab Disord 2001; 25 (Suppl. 05) S13-S16
  • 42 Flatt JP. Use and storage of carbohydrate and fat. Am J Clin Nutr 1995; 61 (4 Suppl) 952S-959S
  • 43 Schutz Y, Flatt JP, Jequier E. Failure of dietary fat intake to promote fat oxidation: a factor favoring the development of obesity. Am J Clin Nutr 1989; 50: 307-314
  • 44 Flatt JP. Dietary fat, carbohydrate balance, and weight maintenance: effects of exercise. Am J Clin Nutr 1987; 45 (1 Suppl) 296-306
  • 45 Lalli CA, Pauli JR, Prada PO, Cintra DE, Ropelle ER, Velloso LA, Saad MJ. Statin modulates insulin signaling and insulin resistance in liver and muscle of rats fed a high-fat diet. Metabolism 2008; 57: 57-65
  • 46 Moore MC, Connolly CC, Cherrington AD. Autoregulation of hepatic glucose production. Eur J Endocrinol 1998; 138: 240-248
  • 47 Fujimoto S, Mochizuki K, Shimada M, Murayama Y, Goda T. Variation in gene expression of inflammatory cytokines in leukocyte-derived cells of high-fat-diet-induced insulin-resistant rats. Biosci Biotechnol Biochem 2008; 72: 2572-2579
  • 48 Gupte AA, Bomhoff GL, Swerdlow RH, Geiger PC. Heat treatment improves glucose tolerance and prevents skeletal muscle insulin resistance in rats fed a high-fat diet. Diabetes 2009; 58: 567-578
  • 49 MacLean PS, Higgins JA, Jackman MR, Johnson GC, Fleming-Elder BK, Wyatt HR, Melanson EL, Hill JO. Peripheral metabolic responses to prolonged weight reduction that promote rapid, efficient regain in obesity-prone rats. Am J Physiol Regul Integr Comp Physiol 2006; 290: R1577-R1588
  • 50 Figlewicz DP. Adiposity signals and food reward: expanding the CNS roles of insulin and leptin. Am J Physiol Regul Integr Comp Physiol 2003; 284: R882-R892
  • 51 Figlewicz DP, MacDonald Naleid A, Sipols AJ. Modulation of food reward by adiposity signals. Physiol Behav 2007; 91: 473-478
  • 52 Cerf ME, Louw J. High fat programming induces glucose intolerance in weanling Wistar rats. Horm Metab Res 2010; 42: 307-310
  • 53 Fagundes AT, Moura EG, Passos MC, Santos-Silva AP, de Oliveira E, Trevenzoli IH, Casimiro-Lopes G, Nogueira-Neto JF, Lisboa PC. Temporal evaluation of body composition, glucose homeostasis and lipid profile of male rats programmed by maternal protein restriction during lactation. Horm Metab Res 2009; 41: 866-873