Hostname: page-component-76fb5796d-25wd4 Total loading time: 0 Render date: 2024-04-26T14:59:30.163Z Has data issue: false hasContentIssue false
  • English
  • Français

Tissue expression of uncoupling proteins in piglets given a low protein diet: a rôle for UCP2 and UCP3 in diet-induced thermogenesis

Published online by Cambridge University Press:  09 March 2007

J. Jia ,
M. Jois  and
G. H. McDowell
J. Jia
Affiliation:
Department of Agricultural Sciences, La Trobe University, Victoria 3086, Australia
M. Jois*
Affiliation:
Department of Agricultural Sciences, La Trobe University, Victoria 3086, Australia
G. H. McDowell
Affiliation:
La Trobe University, Victoria 3086, Australia
*
‡ E-mail: M.Jois@latrobe.edu.au
Get access

Abstract

The purpose of the study was to investigate the rôle of novel mitochondrial uncoupling proteins UCP2 and UCP3 in the poor efficiency of energy utilization observed in piglets offered a low protein diet. Eight male piglets (Landrace × Large White) from different litters were allocated randomly to one of two groups; a high protein group (HP) was given restricted amounts of a diet containing 270 g/kg of crude protein whereas the low protein group (LP) was offered ad libitum a diet containing 27 g/kg of crude protein. The experimental period extended over 4 weeks, including an initial period of 1 week for adaptation. Live weights were recorded weekly and food residues were weighed daily. During the 2nd and 3rd weeks, faeces were collected for measurement of digestible energy intake. Over the last 2 weeks whole body oxygen consumption was measured by indirect calorimetry before, 1·5 h after and 3·5 h after the start of feeding. The piglets were killed at the end of week 4 and tissue expressions of UCP2 and UCP3 were measured by Northern blot analyses using a partial length pig UCP2 probe that had high homology to both UCP2 and UCP3. The HP group maintained their live weight during the experimental period whereas the live weight of the LP group increased significantly (P < 0·01) but only slightly despite a digestible energy intake that was more than twice that of the HP group (P < 0·01). Whole body oxygen consumption of the LP piglets was about three times that of the HP piglets (P < 0·05), with similar increases 1·5 h after feeding (P < 0·05) in both groups indicating increased thermogenesis. A marked increase in the expression of UCP2 and UCP3 was observed in the skeletal muscle, adipose tissue and spleen of the LP piglets. The results are consistent with a rôle for UCP2 and UCP3 in diet-induced thermogenesis in piglets and specifically in the regulation of efficiency of energy utilization in pigs.

Keywords

dietary proteingene expressionheat productionpigsuncoupling proteins
Type
Research Article
Information
Animal Science , Volume 81 , Issue 2 , October 2005 , pp. 283 - 287
Copyright
Copyright © British Society of Animal Science 2005

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

†Faculty of Animal Science, Yunnan Agricultural University, Kunming, 650201, People's Republic of China.

References

Association of Official Analytical Chemists. 1995. Official methods of analysis, 16th edition. AOAC, Arlington, VA.Google Scholar
Astrup, A., Toubro, S., Dalgaard, L. T., Urhammer, S. A., Sorensen, T. I. A. and Pedersen, O. 1999. Impact of the v/v 55 polymorphism of the uncoupling protein 2 gene on 24-h energy expenditure and substrate oxidation. International Journal of Obesity 23: 1030–1034.CrossRefGoogle Scholar
Blaxter, K. 1989. Energy metabolism in animals and man. Cambridge University Press.Google Scholar
Boss, O., Samec, S. and Giacobino, J.P. 1997. Uncoupling protein-3: a new member of the mitochondrial carrier family with tissue-specific expression. FEBS Letters 408: 39–42.CrossRefGoogle ScholarPubMed
Cannon, B. and Nedergaard, J. 2004. Brown adipose tissue: function and physiological significance. Physiological Reviews 84: 277–359.CrossRefGoogle ScholarPubMed
Chomczynski, P. and Sacchi, N. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Analytical Biochemistry 162: 156–159.CrossRefGoogle ScholarPubMed
Clapham, J. C., Arch, J.R.S., Chapman, H., Haynes, A., Lister, G., Moore, G.B.T., Piercy, V., Carter, S.A., Lehner, I., Smith, S.A., Beeley, L.J., Godden, R.J., Herrity, N., Skehel, M., Changanl, K., Hockings, P.D., Reid, D.G., Squires, S.M., Hatcher, J., Trall, B., Lathcham, J., Rastan, S., Harper, A.J., Cadenas, S., Buckingham, J.A., Brand, M.D. and Abuin, A. 2000. Mice over expressing human uncoupling-3 in skeletal muscle are hyperphagic and lean. Nature 406: 415–418.CrossRefGoogle Scholar
Damon, M., Vincent, A., Herpin, P. and Lombardi, A. 2000. First evidence of uncoupling protein-2 (UCP-2) and -3 (UCP-3) gene expression in piglet skeletal muscle and adipose tissue. Gene 246: 133–141.CrossRefGoogle ScholarPubMed
Dulloo, A.G., Seydoux, J. and Jacquet, J. 2004. Adaptive thermogenesis and uncoupling proteins: a reappraisal of their roles in fat metabolism and energy balance. Physiology and Behavior 83: 587–602.CrossRefGoogle ScholarPubMed
Fleury, C., Neverova, M., Collins, S., Raimbaul, S., Champigny, O., Levi-Meyrueis, C., Bouillaud, F., Seldin, M.F., Surwit, R.S., Ricquier, D. and Warden, C.H. 1997. Uncoupling protein-2: a novel gene linked to obesity and hyerinsulinemia. Nature Genetics 15: 269–272.CrossRefGoogle Scholar
Gurr, M.L., Mawson, R., Rothwell, N.J. and Stock, M.J. 1980. Effect of manipulating dietary protein and energy on energy balance and thermogenesis in the pig. Journal of Nutrition 110: 532–542.CrossRefGoogle ScholarPubMed
Herpin, P., Vincent, A. and Damon, M. 2004. Effect of breed and body weight on thermoregulatory abilities of European (Pietrain × (Landrace × Large White)) and Chinese (Meishan) piglets at birth. Livestock Production Science 88: 17–26.CrossRefGoogle Scholar
Jucker, B.M., Ren, J., Dufour, S., Ren, J., Cao, X., Previs, S.F., Cadman, K.S. and Shulman, G.I. 2000. 13C/31P NMR assessment of mitochondrial energy coupling in skeletal muscle of awake fed and fasted rats: relationship with uncoupling protein 3 expression. Journal of Biological Chemistry 275: 39279–39286.CrossRefGoogle ScholarPubMed
Lebon, V., Dufour, S., Petersen, K.F., Ren, J., Jucker, B.M., Slezak, L.A., Cline, G.W., Rothman, D.L. and Shulman, G.I. 2001. Effect of triiodothyronine on mitochondrial energy coupling in human skeletal muscle. Journal of Clinical Investigation 108: 733–737.CrossRefGoogle ScholarPubMed
Le Dividich, J., Mormede, P., Catheline, M. and Caritez, J.-C. 1991. Body composition and cold resistance of the neonatal pig from European ( Large White) and Chinese (Meishan) breeds. Biology of the Neonate 59: 268–274.CrossRefGoogle ScholarPubMed
Lowell, B.B. and Spiegelman, B.M. 2000. Toward a molecularunderstanding of adaptive thermogenesis. Nature 404: 625–660.CrossRefGoogle Scholar
Miller, D.S. and Mumford, P. 1967. Gluttony. 1. An experimental study of overeating on high protein diets. American Journal of Clinical Nutrition 20: 1212–1222.CrossRefGoogle ScholarPubMed
Miller, D.S., Mumford, P. and Stock, M.J. 1967. Gluttony. 2. Thermogenesis in overeating man. American Journal of Clinical Nutrition 20: 1223–1229.CrossRefGoogle ScholarPubMed
Miller, D.S. and Payne, P.R. 1962. Weight maintenance and food intake. Journal of Nutrition 78: 255–262.CrossRefGoogle Scholar
Ricquier, D. and Bouillaud, F. 2000 The uncoupling protein homologues: UCP1, UCP2, UCP3, StUCP and AtUCP. Biochemical Journal 345: 161–179.CrossRefGoogle ScholarPubMed
Rothwell, N. and Stock, M.J. 1983. Diet-induced thermogenesis. In Mammalian thermogenesis (ed. Girardier, L. and Stock, M. J.), pp. 208–233. Chapman and Hall, London.CrossRefGoogle Scholar
Rothwell, N. and Stock, M.J. 1987. Influence of carbohydrate and fat intake on diet-induced thermogenesis and brown fat activity in rats fed low protein diets. Journal of Nutrition 117: 1721–1726.CrossRefGoogle Scholar
Schrauwen, P., Walder, K. and Ravussin, E. 1999. Human uncoupling proteins and obesity. Obesity Research 7: 97–105.CrossRefGoogle ScholarPubMed
Solanes, G., Vidalpuig, A., Grujic, D., Flier, J.S. and Lowell, B.B. 1997. The human uncoupling protien-3 gene. Genomic structure, chromosomal localisation, and genetic basis for short and long transcripts. Journal of Biolological Chemistry 272: 25433–25436.CrossRefGoogle Scholar
Stirling, J. and Stock, M. J. 1968. Metabolic origins of thermogenesis induced by diet. Nature 220: 801–802.CrossRefGoogle ScholarPubMed
Stock, M.J. 1999. Gluttony and thermogenesis revisited. International Journal of Obesity 23: 1105–1117.CrossRefGoogle ScholarPubMed
Trayhurn, P., Temple, N.J. and Van Aerde, J. 1989. Evidence from immunoblotting studies on uncoupling protein that brown adipose tissue is not present in the domestic pig. Canadian Journal of Physiology and Pharmacology 67: 1480–1485.CrossRefGoogle Scholar
Walder, K., Norman, R.A. and Hanson, R.L. 1998. Association between uncoupling protein polymorphism (UCP2-UCP3) and energy metabolism/ obesity in Pima Indians. Human Molecular Genetics 7: 1431–1435.CrossRefGoogle ScholarPubMed