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Effect of cold exposure on energy balance and liver respiratory capacity in post-weaning rats fed a high-fat diet

Published online by Cambridge University Press:  09 March 2007

Susanna Iossa
Affiliation:
Department of General and Environmental Physiology, University of Naples‘FEDERICO II’, Italy
Lillà Lionetti
Affiliation:
Department of General and Environmental Physiology, University of Naples‘FEDERICO II’, Italy
Maria P. Mollica
Affiliation:
Department of General and Environmental Physiology, University of Naples‘FEDERICO II’, Italy
Raffaella Crescenzo
Affiliation:
Department of General and Environmental Physiology, University of Naples‘FEDERICO II’, Italy
Antonio Barletta
Affiliation:
Department of General and Environmental Physiology, University of Naples‘FEDERICO II’, Italy
Giovanna Liverini*
Affiliation:
Department of General and Environmental Physiology, University of Naples‘FEDERICO II’, Italy
*
Corresponding author: Professor Giovanna Liverini, fax +39 081 5424 848 email: [email protected]
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Abstract

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Variations in energy balance, body composition, and nutrient partitioning induced by high-fat feeding, cold exposure or by concomitant high-fat feeding and cold exposure were studied in young Wistar rats. Changes in hepatic metabolism as well as in serum free triiodothyronine and leptin levels were also evaluated. Rats were exposed to either 24 or 4°C and fed either a low- or high-fat diet (10 % or 50 % energy respectively) for 2 weeks. Relative to low-fat feeding at 24°C, both energy intake and expenditure were increased by high-fat feeding or by cold exposure, and these changes were accompanied by increased serum triiodothyronine levels. In response to concomitant high-fat feeding and cold exposure, serum triiodothyronine tended to be further elevated, but no further increases in energy intake or energy expenditure were observed. Independently of diet, the increased energy expenditure in cold-exposed rats was not completely balanced by adaptive hyperphagia, with consequential reductions in protein and fat gain, accompanied by marked decreases in serum leptin. Furthermore, unlike high-fat feeding at 24°C, cold exposure enhanced hepatic mitochondrial oxidative capacity both in the low-fat- and high-fat-fed groups. It is concluded that in this strain of young Wistar rats, despite similarly marked stimulation of energy expenditure by high-fat feeding at 24°C, by cold exposure and by concomitant high-fat feeding and cold exposure, an increased hepatic oxidative capacity occurred only in the presence of the cold stimulus.

Type
Research Article
Copyright
Copyright © The Nutrition Society 2001

References

Abelenda, M & Puerta, ML (1991) Relationship among food intake, thyroid state, and chronic cold-exposure in the rat. Hormone and Metabolic Research 23, 9091.CrossRefGoogle Scholar
Allard, M, & Le Blanc, J (1988) Effect of cold acclimation, cold exposure, and palatability on postprandial thermogenesis in rats. International Journal of Obesity 12, 169178.Google ScholarPubMed
Barney, CC, Katovich, MJ, Fregly, MJ & Tyler, PE (1980) Changes in β-adrenergic responsiveness of rats during chronic cold exposure. Journal of Applied Physiology 49, 923929.CrossRefGoogle ScholarPubMed
Bing, C, Frankish, HM, Pickavance, L, Wang, Q, Hopkins, DFC, Stock, MJ & Williams, G (1998) Hyperphagia in cold-exposed rats is accompanied by decreased plasma leptin but unchanged hypothalamic NPY. American Journal of Physiology 274, R62R68.Google ScholarPubMed
Brooks, SPJ, Lampi, BJ, Sarwar, G & Botting, HG (1995) A comparison of methods for determining total body protein. Analytical Biochemistry 226, 2630.CrossRefGoogle ScholarPubMed
Chance, B & Williams, GR (1956) The respiratory chain and oxidative phosphorylation. Advances in Enzymology 17, 65134.Google ScholarPubMed
Danforth, E & Burger, AG (1989) The impact of nutrition on thyroid hormone physiology and action. Annual Review of Nutrition 9, 201227.CrossRefGoogle ScholarPubMed
De Matteis, R, Dashtipour, K, Ognibene, A & Cinti, S (1998) Localisation of leptin slice variants in mouse peripheral tissues by immunohistochemistry. Proceedings of Nutrition Society 57, 441448.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 Letters 444, 149154.CrossRefGoogle ScholarPubMed
Folch, J, Lees, M & Stanley, GHS (1957) A simple method for the isolation and purification of total lipides from animal tissues. Journal of Biological Chemistry 226, 497510.CrossRefGoogle ScholarPubMed
Foster, DO & Frydman, ML (1979) Tissue distribution of cold induced thermogenesis in conscious warm- or cold-acclimated rats re-evaluated from changes in tissue blood flow: the dominant role of brown adipose tissue in the replacement of shivering by nonshivering thermogenesis. Canadian Journal of Physiology and Pharmacology 57, 257270.CrossRefGoogle ScholarPubMed
Freake, HC & Oppenheimer, JH (1995) Thermogenesis and thyroid function. Annual Review of Nutrition 15, 263291.CrossRefGoogle ScholarPubMed
Friedman, JM (1998) Leptin, leptin receptors, and the control of body weight. Nutrition Reviews 2, S38S46.Google Scholar
Friedman, JM & Halaas, JL (1998) Leptin and the regulation of body weight in mammals. Nature 395, 763770.CrossRefGoogle ScholarPubMed
Goglia, F, Liverini, G, De Leo, T & Barletta, A (1983) Thyroid state and mitochondrial population during cold exposure. Pflügers Archive-European Journal of Physiology 396, 4953.CrossRefGoogle ScholarPubMed
Goubern, M, Laury, MC, Razanoelina, M & Portet, R (1988) Effect of environmental temperature on dietary obesity in Osborne-Mendel rats. Annals of Nutrition and Metabolism 32, 340346.CrossRefGoogle ScholarPubMed
Hansen, PA, Han, DH, Nolte, LA, Chen, M & Holloszy, JO (1997) DHEA protects against visceral obesity and muscle insulin resistance in rats fed a high-fat diet. American Journal of Physiology 273, R1704R1708.Google ScholarPubMed
Inestrosa, NC, Bronfman, M & Leighton, F (1979) Detection of peroxisomal fatty acyl-Coenzyme A oxidase activity.. Biochemical Journal 182, 779788.CrossRefGoogle ScholarPubMed
Iossa, S, Lionetti, L, Mollica, MP, Barletta, A & Liverini, G (1999) Fat balance and hepatic mitochondrial function in response to fat feeding in mature rats. International Journal of Obesity 23, 11221128.CrossRefGoogle ScholarPubMed
Iossa, S, Lionetti, L, Mollica, MP, Crescenzo, R, Barletta, A & Liverini, G (2000) Effect of long-term high-fat feeding on energy balance and liver oxidative activity in rats. British Journal of Nutrition (In the Press).CrossRefGoogle ScholarPubMed
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. International Journal of Obesity 19, 539543.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. British Journal of Nutrition 77, 99105.CrossRefGoogle Scholar
Iossa, S, Liverini, G & Barletta, A (1991) Physiological changes due to cold adaptation in rat liver. Cellular Physiology and Biochemistry 1, 226239.CrossRefGoogle Scholar
Iossa, S, Liverini, G & Barletta, A (1992) Relationship between the resting metabolic rate and hepatic metabolism in rats: effect of hyperthyroidism and fasting for 24 hours. Journal of Endocrinology 135, 4551.CrossRefGoogle ScholarPubMed
Li, H, Matheny, M & Scarpace, PJ (1997) β3-Adrenergic-mediated suppression of leptin gene expression in rats. American Journal of Physiology 272, E1031E10x36.Google Scholar
Lionetti, L, Iossa, S, Brand, MD & Liverini, G (1996) Relationship between membrane potential and respiration rate in isolated liver mitochondria from rats fed an energy dense diet. Molecular and Cellular Biochemistry 158, 133138.Google ScholarPubMed
Lionetti, L, Iossa, S, Brand, MD & Liverini, G (1996) The mechanism of stimulation of respiration in isolated hepatocytes from rats fed an energy-dense diet. Nutritional Biochemistry 7, 571576.CrossRefGoogle Scholar
Luz, J & Griggio, MA (1987) Effect of food intake on oxygen consumption in cold-acclimated rats. Brazilian Journal of Medical and Biological Research 20, 619622.Google ScholarPubMed
Matsuda, J, Hosoda, K, Itoh, H, Son, C, Doi, K, Tanaka, T, Fukunaga, Y, Inoue, G, Nishimura, H, Yoshimasa, Y, Yamori, Y & Nakao, K (1997) Cloning of rat uncoupling protein-3 and uncoupling protein-2 cDNAs: their gene expression in rats fed high-fat diet. FEBS Letters 418, 200204.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 a high-fat diet. Metabolism 48, 12301235.CrossRefGoogle ScholarPubMed
Naim, M, Brand, JG, Kare, MR & Carpenter, RG (1985) Energy intake, weight gain, and fat deposition in rats fed nutritionally controlled diet in a multichoice (‘cafeteria’) design. Journal of Nutrition 115, 14471458.CrossRefGoogle Scholar
Nemecz, M, Preininger, K, English, R, Fürnsinn, C, Schneider, B, Waldhäusl, W & Roden, M (1999) Acute effect of leptin on hepatic glycogenolysis and gluconeogenesis in perfused rat liver. Hepatology 29, 166172.CrossRefGoogle ScholarPubMed
Oppenheimer, JH, Schwartz, HL, Lane, JT & Thompson, MP (1991) Functional relationship of thyroid hormone-induced lipogenesis, lipolysis, and thermogenesis in the rat. Journal of Clinical Investigation 87, 125132.CrossRefGoogle ScholarPubMed
Papamandjaris, AA3MacDougall, DE & Jones, PJH (1998) Medium chain fatty acid metabolism and energy expenditure: obesity treatment implications. Life Sciences 62, 12031215.CrossRefGoogle ScholarPubMed
Pullar, JD & Webster, AJF (1977) The energy cost of fat and protein deposition in the rat. British Journal of Nutrition 37, 355363.CrossRefGoogle ScholarPubMed
Rothwell, NJ & Stock, MJ (1979) A role for brown adipose tissue in diet-induced thermogenesis. Nature 281, 3135.CrossRefGoogle ScholarPubMed
Rothwell, NJ & Stock, MJ (1980) Similarities between cold- and diet-induced thermogenesis in the rat. Canadian Journal of Physiology and Pharmacology 58, 842848.CrossRefGoogle Scholar
Rothwell, NJ & Stock, MJ (1982) Energy expenditure of ‘cafeteria-fed’ rats determined from measurements of energy balance and indirect calorimetry. Journal of Physiology 382, 371377.CrossRefGoogle Scholar
Rothwell, NJ, Stock, MJ (1986) Brown adipose tissue in diet-induced thermogenesis. In Brown Adipose Tissue, pp.269286, [P, Trayhurn & DG, Nicholls, editors]. London: Edward Arnold.Google 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, 474480.CrossRefGoogle ScholarPubMed
Shiota, M, Tanaka, T & Sugano, T (1985) Effect of norepinephrine on gluconeogenesis in perfused livers of cold-exposed rats. American Journal of Physiology 249, E281E489.Google ScholarPubMed
Stanley, BG & Leibowitz, SF (1984) Neuropeptide Y injected into hypothalamus: a powerful neurochemical inducer of hyperphagia and obesity. Proceedings of the National Academy of Science, USA 82, 39403943.CrossRefGoogle Scholar
Vallerand, AL, Lupien, J & Bukowiecki, LJ (1986) Cold exposure reverses the diabetogenic effects of high-fat feeding. Diabetes 35, 329334.CrossRefGoogle ScholarPubMed
Vallerand, AL, Perusse, F & Bukowiecki, LJ (1990) Stimulatory effects of cold exposure and cold acclimation on glucose uptake in rat peripheral tissues. American Journal of Physiology 259, R1043R1049.Google ScholarPubMed
Widdowson, PS, Upton, R, Buckingham, R, Arch, J & Williams, G (1997) Inhibition of food response to intracerebroventricular injection of leptin is attenuated in rats with diet-induced obesity. Diabetes 46, 17821785.CrossRefGoogle ScholarPubMed
Young, JB & Landsberg, L (1979) Effect of diet and cold exposure on norepinephrine turnover in pancreas and liver. American Journal of Physiology 236, E524E533.Google Scholar