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Effect of high-fat feeding on metabolic efficiency and mitochondrial oxidative capacity in adult rats

Published online by Cambridge University Press:  09 March 2007

Susanna Iossa ,
Lillà Lionetti ,
Maria P. Mollica ,
Raffaella Crescenzo ,
Monica Botta ,
Antonio Barletta  and
Giovanna Liverini
Susanna Iossa
Affiliation:
Department of General and Environmental Physiology, University of Naples ‘FEDERICO II’, Via Mezzocannone 8, I-80134 Napoli, Italy
Lillà Lionetti
Affiliation:
Department of General and Environmental Physiology, University of Naples ‘FEDERICO II’, Via Mezzocannone 8, I-80134 Napoli, Italy
Maria P. Mollica
Affiliation:
Department of General and Environmental Physiology, University of Naples ‘FEDERICO II’, Via Mezzocannone 8, I-80134 Napoli, Italy
Raffaella Crescenzo
Affiliation:
Department of General and Environmental Physiology, University of Naples ‘FEDERICO II’, Via Mezzocannone 8, I-80134 Napoli, Italy
Monica Botta
Affiliation:
Department of General and Environmental Physiology, University of Naples ‘FEDERICO II’, Via Mezzocannone 8, I-80134 Napoli, Italy
Antonio Barletta
Affiliation:
Department of General and Environmental Physiology, University of Naples ‘FEDERICO II’, Via Mezzocannone 8, I-80134 Napoli, Italy
Giovanna Liverini*
Affiliation:
Department of General and Environmental Physiology, University of Naples ‘FEDERICO II’, Via Mezzocannone 8, I-80134 Napoli, Italy
*
*Corresponding author: Professor Giovanna Liverini, fax +39 081 2535090, email liverini@unina.it
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Abstract

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The changes in metabolic efficiency, body composition, and nutrient partitioning induced by high-fat feeding were evaluated in adult rats (90d of age). The alterations in serum free triiodothyronine, insulin, and leptin levels, as well as in hepatic and skeletal muscle metabolism, were also assessed. Rats were fed either a low- or a high-fat diet for 2 weeks. Relative to the low-fat feeding, energy intake and expenditure, as well as body-energy gain, lipid gain, and energetic efficiency, were increased by the high-fat feeding. Increased serum leptin levels accompanied these variations. A positive correlation between serum leptin levels and percentage of body fat was found in the rats fed the low- or high-fat diet, with a significant divergence between the slope of the regression lines. Furthermore, a negative correlation between serum leptin level and energy intake was found in the rats fed the low-fat diet, while a positive correlation was found in the rats fed the high-fat diet. Finally, the high-fat feeding decreased the hepatic and skeletal muscle mitochondrial oxidative capacity. It is concluded that, in adult rats, a nutritional factor such as a high level of fat in the diet induces obesity, leptin resistance, and impairment of mitochondrial capacity, all phenomena typical of unrestrained aged rats.

Keywords

Energy balanceMitochondrial capacityTriiodothyronineLeptin
Type
Research Article
Information
British Journal of Nutrition , Volume 90 , Issue 5 , November 2003 , pp. 953 - 960
Copyright
Copyright © The Nutrition Society 2003

References

Ames, BN, Shigenaga, MK & Hagen, TN (1995) Mitochondrial decay in aging. Biochim Biophys Acta 1271, 165–170.CrossRefGoogle ScholarPubMed
Barzilai, N & Rossetti, L (1995) Relationship between changes in body composition and insulin responsiveness in models of the aging rat. Am J Physiol 269, E591–E597.Google ScholarPubMed
Bobyleva, V, Pazienza, L, Muscatello, U, Kneer, N & Lardy, H (2000) Short-term hypothermia activates hepatic mitochondria sn-glycerol 3-phosphate dehydrogenase and thermogenic systems. Arch Biochem Biophys 380, 367–372.CrossRefGoogle Scholar
Brooks, SPJ, Lampi, BJ, Sarwar, G & Botting, HG (1995) A comparison of methods for determining total body protein. Anal Biochem 226, 26–30.CrossRefGoogle ScholarPubMed
Collins, S, Daniel, KW, Petro, AN & Surwit, RS (1997) Strain-specific response to β3-adrenergic receptor agonist treatment of diet-induced obesity in mice. Endocrinology 138, 405–413.CrossRefGoogle Scholar
Danforth, E & Burger, AG (1989) The impact on nutrition on thyroid hormone physiology and action. Annu Rev Nutr 9, 201–227.CrossRefGoogle ScholarPubMed
El-Haschimi, K, Pierroz, DD, Hileman, SM, Bjorbaek, C & Flier, JS (2000) Two defects contribute to hypothalamic leptin resistance in mice with diet-induced obesity. J Clin Invest 105, 1827–1832.CrossRefGoogle ScholarPubMed
Estabrook, RW (1967) Mitochondrial respiratory control and the polarographic measurement of ADP:O ratios. Methods Enzymol 10, 41–47.CrossRefGoogle Scholar
Evans, BA, Agar, L & Summers, RJ (1999) The role of the sympathetic nervous system in the regulation of leptin synthesis in C57BL/6 mice. FEBS Lett 444, 149–154.CrossRefGoogle ScholarPubMed
Folch, J, Lees, M & Sloane-Stanley, GH (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226, 497–510.CrossRefGoogle ScholarPubMed
Freake, HG & Oppenheimer, JH (1995) Thermogenesis and thyroid function. Annu Rev Nutr 15, 263–291.CrossRefGoogle ScholarPubMed
Friedman, JM (2002) The function of leptin in nutrition, weight, and physiology. Nutr Rev 60, S1–S14.CrossRefGoogle ScholarPubMed
Hartree, EF (1972) Determination of protein: a modification of the Lowry method that gives a linear photometric response. Anal Biochem 48, 422–427.CrossRefGoogle ScholarPubMed
Hill, JO, Melanson, EL & Wyatt, HT (2000) Dietary fat intake and regulation of energy balance: implication for obesity. J Nutr 130, 284S–288S.CrossRefGoogle ScholarPubMed
Iossa, S, Lionetti, L, Mollica, MP, Barletta, A & Liverini, G (1999a) Fat balance and hepatic mitochondrial function in response to fat feeding in mature rats. Int J Obes Relat Metab Disord 23, 1122–1128.CrossRefGoogle ScholarPubMed
Iossa, S, Lionetti, L, Mollica, MP, Barletta, A & Liverini, G (1999b) Energy intake and utilization vary during development in rats. J Nutr 129, 1593–1596.CrossRefGoogle ScholarPubMed
Iossa, S, Lionetti, L, Mollica, MP, Crescenzo, R, Botta, M & Liverini, G (2001) Mitochondrial respiration and triiodothyronine concentration in liver from postpubertal and adult rats. Horm Metab Res 33, 1–5.CrossRefGoogle Scholar
Iossa, S, Mollica, MP, Lionetti, L, Barletta, A & Liverini, G (1995) Hepatic mitochondrial respiration and transport of reducing equivalents in rats fed an energy dense diet. Int J Obes Relat Metab Disord 19, 539–543.Google ScholarPubMed
Iossa, S, Mollica, MP, Lionetti, L, Barletta, A & Liverini, G (1997) Energy balance and liver respiratory activity in rats fed on an energy-dense diet. Br J Nutr 77, 99–105.CrossRefGoogle Scholar
Iossa, S, Mollica, MP, Lionetti, L, Crescenzo, R, Botta, M & Liverini, G (2002) Skeletal muscle oxidative capacity in rats fed high-fat diet. Int J Obes Relat Metab Disord 26, 65–72.CrossRefGoogle ScholarPubMed
Jéquier, E (2002) Pathways to obesity. Int J Obes Relat Metab Disord 26, S12–S17.CrossRefGoogle ScholarPubMed
Kumar, MV, Moore, RL & Scarpace, PJ (1999) β 3 -Adrenergic regulation of leptin, food intake, and adiposity is impaired with age. Pflügers Arch 438, 681–688.Google ScholarPubMed
Lardy, H, Kneer, N, Bellei, M & Bobyleva, V (1995) Induction of thermogenic enzymes by DHEA and its metabolites. Ann N Y Acad Sci 29, 171–179.CrossRefGoogle Scholar
Lee, YP & Lardy, HA (1965) Influences of thyroid hormones on L-α-glycerophosphate and other dehydrogenases in various organs of the rat. J Biol Chem 240, 1427–1436.CrossRefGoogle ScholarPubMed
Leibel, RL (2002) The role of leptin in the control of body weight. Nutr Rev 60, S15–S19.CrossRefGoogle ScholarPubMed
Li, H, Matheny, M & Scarpace, PJ (1997) β 3 -Adrenergic-mediated suppression of leptin gene expression in rats. Am J Physiol 272, E1031–E1036.Google ScholarPubMed
Liverini, G, Iossa, S, Mollica, MP, Lionetti, L & Barletta, A (1996) Hepatic fatty acid supported respiration in rats fed an energy dense diet. Cell Biochem Funct 14, 283–289.CrossRefGoogle ScholarPubMed
McCrory, MA, Fuss, PJ, Saltzman, E & Roberts, SB (2000) Dietary determinants of energy intake and weight regulation in healthy adults. J Nutr 130, 276S–279S.CrossRefGoogle ScholarPubMed
Mollica, MP, Iossa, S, Liverini, G & Soboll, S (1999) Stimulation of oxygen consumption following addition of lipid substrates in liver and skeletal muscle from rats fed high fat diet. Metabolism 48, 1230–1235.CrossRefGoogle Scholar
Muller, MJ & Seitz, HJ (1984) Thyroid hormone action on intermediary metabolism. I Respiration, thermogenesis and carbohydrate metabolism. Klin Wochenschr 62, 11–18.CrossRefGoogle ScholarPubMed
Nemeth, PM, Rosser, BWC, Choksi, RM, Norris, BJ & Baker, KM (1992) Metabolic response to a high-fat diet in neonatal and adult rat muscle. Am J Physiol 262, C282–C286.CrossRefGoogle ScholarPubMed
Porte, D Jr, Baskin, DG & Schwartz, MW (2002) Leptin and insulin action in the central nervous system. Nutr Rev 60, S20–S29.CrossRefGoogle ScholarPubMed
Pullar, JD & Webster, AJF (1977) The energy cost of fat and protein deposition in the rat. Br J Nutr 37, 355–363.CrossRefGoogle ScholarPubMed
Rolfe, DFS & Brown, GC (1997) Cellular energy utilization and molecular origin of standard metabolic rate in mammals. Physiol Rev 77, 731–758.CrossRefGoogle ScholarPubMed
Rothwell, NJ & Stock, MJ (1982) Energy expenditure of ‘cafeteria-fed’ rats determined from measurements of energy balance and indirect calorimetry. J Physiol 382, 371–377.CrossRefGoogle Scholar
Rothwell, NJ, Stock, MJ & Warwick, BP (1985) Energy balance and brown fat activity in rats fed cafeteria diets or high-fat, semisynthetic diets at several levels of intake. Metabolism 34, 474–480.CrossRefGoogle ScholarPubMed
Scarpace, PJ, Matheny, M, Moore, RL & Tumer, N (2000) Impaired leptin responsiveness in aged rats. Diabetes 49, 432–435.CrossRefGoogle ScholarPubMed
Schwartz, MW, Seeley, RJ, Campfield, LA, Burn, P & Baskin, DG (1996) Identification of targets of leptin action in rat hypothalamus. J Clin Invest 98, 1101–1106.CrossRefGoogle ScholarPubMed
Smith, BK, Kelly, LA, Pina, R, York, DA & Bray, GA (1998) Preferential fat intake increases adiposity but not body weight in Sprague-Dawley rats. Appetite 31, 127–139.CrossRefGoogle Scholar
Spicer, (2002) Effect of high-fat diet on body composition and hormone responses to glucose tolerance tests. Endocrine 19, 327–332.Google Scholar
Tyzbir, RS, Kunin, AS, Sims, NM & Danforth, E (1981) Influence of diet composition on serum triiodothyronine (T3) concentration, hepatic mitochondrial metabolism and shuttle system activity in rats. J Nutr 111, 252–259.CrossRefGoogle ScholarPubMed
Woods, SC, Seeley, RJ, Rushing, PA, D'Alessio, D & Tso, P (2003) A controlled high-fat diet induces an obese syndrome in rats. J Nutr 133, 1081–1087.CrossRefGoogle ScholarPubMed
World Health Organization (1998) Obesity: Preventing and Managing the Global Epidemic Geneva, Switzerland: World Health Organization.Google Scholar