Abstract
The physiological mechanisms of thermogenesis, energy balance and energy expenditure are poorly understood in poultry. The aim of this study was designed to investigate the physiological roles of avian uncoupling protein (avUCP) regulating in energy balance and thermogenesis by using three chicken breeds of existence striking genetic difference and feeding with different dietary protein levels. Three chicken breeds including broilers, hybrid chickens, and non-selection Wuding chickens were used in this study. Total 150 chicks of 1 day of age, with 50 from each breed were reared under standard conditions on starter diets to 30 days. At 30 days of age, forty chicks from each breed chicks were divided into two groups. One group was fed low protein diet (LP, 17.0 %), and the other group was fed high protein diet (HP, 19.5 %) for 60 days. Wuding chickens showed the lowest feed conversion efficiency (FCE) and the highest expressions of avUCP mRNA association with high plasma T3 and insulin concentrations. Hybrid chickens showed the lowest expressions of avUCP mRNA association with high FCE and energy efficiency. Expressions of avUCP mRNA association with diet-induced thermogenesis (DIT) were only observed in broiler and hybrid chickens. The expressions of avUCP mRNA were positive association with plasma insulin, T3 and NEFA concentrations. Age influence on the expression of avUCP mRNA were observed only for hybrid and broiler chickens. It seems that both roles of avUCP regulation thermogenesis and lipid utilisation as fuel were observed in the present study response to variation in dietary protein and breeds.
Similar content being viewed by others
References
Palmieri F (1994) Mitochondrial carrier proteins. FEBS Lett 346:48–56
Fleury C, Neverova M, Collins S, Raimbault S, Champigny O, Levi-Meyrueis C, Bouillaud F, Seldin MF, Surwit RS, Ricquier D, Warden CH (1997) Uncoupling protein-2: a novel gene linked to obesity and hyperinsulinemia. Nat Genet 15:269–272
Boss O, Samec S, Paoloni-Giocobino A, Rossier C, Dulloo A, Seydoux J, Muzzin P, Giacobino JP (1997) Uncoupling protein-3, a new member of the mitochondrial carrier family with tissue-specific expression. FEBS Lett 408:39–42
Sanchis D, Fleury C, Chomiki N, Goubern M, Huang Q, Neverova M, Gregoire F, Easlick J, Raimbault S, Levi-Meyrueis C, Miroux B, Collins S, Seldin M, Richard D, Warden C, Bouillaud F, Ricquier D (1998) BMCP1, a novel mitochondrial carrier with high expression in the central nervous system of humans and rodents, and respiration uncoupling activity in recombinant yeast. J Biol Chem 273:34611–34615
Mao W, Yua XX, Zhong A, Li WL, Brush J, Sherwood SW, Adams SH, Pan GH (1999) UCP4, a novel brain-specific mitochondrial protein that reduces membrane potential in mammalian cells. FEBS Lett 443:326–330
Adams SA (2000) Uncoupling protein homologs: emerging views of physiological function. J Nutr 130:711–714
Boss O, Hagen T, Lowell BB (2000) Uncoupling proteins 2 and 3, potential regulators of mitochondrial energy metabolism. Diabetes 49:143–156
Dulloo AG, Samec S (2001) Uncoupling proteins, their roles in adaptive thermogenesis and substrate metabolism reconsidered. Br J Nutr 86:123–139
Raimbault S, Dridi S, Denjean F (2001) An uncoupling protein homologue putatively involved in facultative thermogenesis in birds. Biochem J 353:441–444
Gabarrou JF, Geraert PA, Picard M, Bordas A (1997) Diet-induced thermogenesis in cockerels is modulated by genetic selection for high or low residual feed intake. J Nutr 127:2371–2376
Collin A, Buyse J, Van AP, Darras VM, Malheiros RD, Moraes VMB, Reyns GE, Taouis M, Decuypere E (2003) Cold-induced enhancement of avian uncoupling protein expression, heat production, and triiodothyronine concentrations in broiler chicks. Gen Comp Endocrinol 130:70–77
Collin A, Taouis M, Buyse J, Ifuta NB, Darras VM, Van AP, Malheiros RD, Moraes VM, Decuypere E (2003) Thyroid status, but not insulin status, affects expression of avian uncoupling protein mRNA in chicken. Am J Physiol Endocrinol Metab 284:771–777
Swennen Q, Delezie E, Collin A, Decuypere E, Buyse J (2007) Further investigations on the role of diet-induced thermogenesis in the regulation of feed intake in chickens: comparison of age-matched broiler versus layer cockerels. Poult Sci 86:895–903
National Research Council (1994) Nutrient requirements of poultry, 9th edn. National Academy Press, Washington, DC
Chinese chicken Feeding Standard (2004) Feeding standard of chicken, First edn. National Agricultural Ministry Press, Beijing
Cunniff P (ed) (1997) Official methods of analysis of AOAC International, 16th edn. AOAC International, Gaithersberg, MD
Van Milgen J, Noblet J (1999) Energy partitioning in growing pigs: the use of a multivariate model as an alternative for the factorial analysis. J Anim Sci 77:2154–2162
Gurr ML, Mawson R, Rothwell NJ, Stock MJ (1980) Effect of manipulating dietary protein and energy on energy balance and thermogenesis in the pig. J Nutr 110:532–542
Rothwell N, Stock MJ (1987) Effect of environmental temperature on energy balance and thermogenesis in rats fed normal or low protein diets. J Nutr 117:833–837
Li LP, Li JZ (1985) Clinical biochemistry. Shanghai Science and Technology Publication Press, Shanghai
Petzke KJ, Riese C, Klaus S (2007) Short-term, increasing dietary protein and fat moderately affect energy expenditure, substrate oxidation and uncoupling protein gene expression in rats. J Nutr Biochem 18:400–407
Adeola O, Young LG (1989) Dietary protein-induced changes in porcine muscle respiration, protein synthesis and adipose tissue metabolism. J Anim Sci 67:664–673
Ramsay TG, Mitchell AD, Richards MP (2008) Uncoupling protein expression in skeletal muscle and adipose tissue in response to in vivo porcine somatotropin treatment. Domest Anim Endocrinol 35:130–141
Wang HFL, Dai YL, Chen KW, Li BL, Wang ZY, Zhang J (2010) Effect of dietary crude protein and energy on Gaoyou Duckling Growth performance and carcass trait. J Anim Vet Adv 9:826–830
MacLeod MG (1990) Energy and nitrogen intake, expenditure and retention at 20° in growing fowl given diets with a wide range of energy and protein contents. Br J Nutr 64:625–637
Buyse J, Decuypere E, Berghman L, Kühn ER, Vandesande F (1992) The effect of dietary protein content on episodic growth hormone secretion and on heat production of male broilers. Br Poult Sci 33:1101–1109
Nieto R, Aguilera JF, Fernandez-Figares I, Prieto C (1997) Effect of a low protein diet on the energy metabolism of growing chickens. Arch Tierernahr 50:105–109
Collin A, Malheiros RD, Moraes VMB, Van As P, Darras VM, Taouis M, Decuypere E, Buyse J (2003) Effects of dietary macronutrient content on energy metabolism and uncoupling protein mRNA expression in broiler chickens. Br J Nutr 90:261–269
Dairo FAS, Adesehinwa AOK, Oluwasola TA, Oluyemi JA (2010) High and low dietary energy and protein levels for broiler chickens. J Agric Res 5:2030–2038
Kita K, Muramatsu T, Okumura J (1993) Effect of dietary protein and energy intakes on whole-body protein turnover and its contribution to heat production in chicks. Br J Nutr 69:681–688
Yu HX (2008) Effect of dietary levels on the growth performance and feed conversion efficiency in Chinese Native chicken breeds. Yunnan Agricultural University, Dissertation
Musharafa NA, Latshawa JD (1999) Heat increment as affected by protein and amino acid nutrition. World Poul Sci J 55:233–240
Gousa RM, Morrisa TR (2005) Nutritional interventions in alleviating the effects of high temperatures in broiler production. World Poul Sci J 61:463–475
Rahimi G, Hassanzadeh M (2007) Effects of different protein and energy contents of the diet on growth performance and hormonal parameters in two commercial broiler strains. Int J Poult Sci 6:195–200
Rosebrough RW, Mitchell AD, McMurtry JP (1996) Dietary crude protein changes rapidly alter metabolism and plasma insulin-like growth factor-I concentrations in broiler chickens. J Nutr 126:2888–2898
Rosebrough RW, McMurtry JP, Vasilatos-Younken R (1999) Dietary fat and protein interactions in broilers. Poult Sci 78:992–998
Jia J, Jois M, McDowell GH (2005) Increased tissue expression of uncoupling proteins in piglets fed a low protein diet: a role for UCP2 and UCP3 in diet induced thermogenesis. Anim Sci 81:283–293
Swennen Q, Janssens GPJ, Decuypere E, Buyse J (2004) Effects of substitution between fat and protein on feed intake and its regulatory mechanisms in broiler chickens: energy and protein metabolism and diet-induced thermogenesis. Poult Sci 83:1997–2004
Swennen Q, Janssens GPJ, Collin A, Le Bihan-Duval E, Verbeke K, Decuypere E, Buyse J (2006) Diet-induced thermogenesis and glucose oxidation in broiler chickens: influence of genotype and diet composition. Poult Sci 85:731–742
Stock MJ (1999) Gluttony and thermogenesis revisited. Int J Obes 23:1105–1117
Thurlby P, Trayhurm P (1979) Thermoregulatory thermogenesis in the development of obesity in genetically obese (ob/ob) mice pair fed with lean siblings. Br J Nutr 42:377–385
El-Kazzi M, Bordas A, Gandemer G, Minvielle F (1995) Divergent selection for residual feed intake in Rhode island Red egg-laying lines: gross carcase composition, carcase adiposity and lipid contents of tissues. Br Poult Sci 36:719–728
Tixier M, Bordas A, Mérat P (1988) Divergent selection for residual feed intake in laying hens: effects on growth and fatness. In: Leclercq B, Whitehead C (eds) Leannes in domestic birds. Butterworths, London, pp 129–132
Zein-el-Dein A, Bordas A, Mérat P (1985) Sélection diver-gente pour la composante’résiduelle’ de la consommation alimentaire des poules pondeuses: Effets sur la composition corporelle. Arch Geflügelk 49:158–160
Géraert PA, Guillaumin S, Bordas A, Mérat P (1991) Evidence of a genetic control of diet-induced thermogenesis in poultry. Proceedings of 12th symposium of energy metabolism of farm animals. Eur Assoc Anim Prod 58:380–383
Luiting P (1990) Genetic variation of energy partitioning in laying hens: causes of variation in residual feed consumption. World Poult Sci 74:1259–1268
Jéquier E (1985) Nutrient-induced thermogenesis in man: its role in body weight regulation. J Physiol 80:129–140
Elsaesser F, Faffl MWP, Meyer HHD, Serpek B, Sauerwein H (2002) Differences in the somatotropic axis, in blood cortisol, insulin and thyroid hormone concentrations between two pig genotypes with markedly divergent growth rates and the effects of growth hormone treatment. Anim Sci 74:423–430
Ricquier D, Bouillaud F (2000) The uncoupling protein homologues: UCP1, UCP2, UCP3, StUCP and AtUCP. Biochem J 345:161–179
Zhao G, Li H, Wang YX, Meng H (2005) The expression characterization of chicken uncoupling protein gene. Asian-Aust J Anim Sci 11:1552–1556
Christina M, Evock C, Poch SM, Richards PM, Ashewll CM, John PM (2002) Expression of an uncoupling protein gene homolog in chickens. Comp Biochem Physiol A Physiol 133:345–358
Musharaf NA, Latshaw JD (1999) Heat increment as affected by protein and amino acid nutrition. World Poul Sci J 55:233–240
Gous RM, Morris TR (2005) Nutritional interventions in alleviating the effects of high temperatures in broiler production. World Poul Sci J 61:463–475
Masanés RM, Yubero P, Rafecas I, Remesar X (2002) Changes in UCP expression in tissues of Zucker rats fed diets with different protein content. J Physiol Biochem 58:135–141
Ochoa MC, Santos JL, Azcona C, Maria J, Aliaga M, Martínez-González MA, Martínez A, Marti A, Members G (2007) Association between obesity and insulin resistance with UCP2–UCP3 gene variants in Spanish children and adolescents. Mol Genet Metab 92:351–358
Jia JJ, Zhang X, Ge CR, Jois M (2009) The polymorphisms of UCP2 and UCP3 genes associated with fat metabolism, obesity and diabetes. Obes Rev 10:519–526
Chen HH, Lee W, Wang W, Huang MT, Lee YC, Pan WH (2007) Ala55Val polymorphism on UCP2 gene predicts greater weight loss in morbidly obese patients undergoing gastric banding. Obes Surg 17:926–933
Lee YH, Kim W, Yu BC, Lae PBL, Kim LH, Shin HD (2008) Association of the Ins/Del polymorphisms of uncoupling protein 2 (UCP2) with BMI in a Korean population. Biochem Biophys Res Commun 371:767–771
Bao S, Kennedy A, Wojciechowski B, Wallace P, Ganaway E, Garvey WT (1998) Expression of mRNAs encoding uncoupling proteins in human skeletal muscle. Diabetes 47:1935–1940
Medina-Gomez G, Virtue S, Lelliott C, Boiani R, Campbell M et al (2005) The link between nutritional status and insulin sensitivity is dependent on the adipocyte-specific peroxisome proliferator-activated receptor-gamma2 isoform. Diabetes 54:1706–1716
Medina-Gomez G, Hernandez A, Calvo RM, Martin E, Obregon MJ (2003) Potent thermogenic action of triiodothyroacrtic acid in brown adipocytes. Cell Mol Life Sci 60:1957–1967
Evock-Clover CM, Poch SM, Richards MP, Ashwell CM, McMurtry JP (2002) Expression of an uncoupling protein gene homolog in chickens. Comp Biochem Physiol A 133:345–358
Chan C, MacDonald PE, Saleh MC, Johns DC, Marban E, Wheeler MB (1999) Over-expression of uncoupling protein 2 inhibits glucose-stimulated insulin secretion from rat islets. Diabetes 48:1482–1486
Brand MD, Esteves TC (2005) Physiological functions of the mitochondrial uncoupling proteins UCP2 and UCP3. Cell Metab 2:85–93
Zhang CY, Baffy G, Perret P, Krauss S, Peroni O, Grujic D et al (2001) Uncoupling protein-2 negatively regulates insulin secretion and is a major link between obesity, beta cell dysfunction, and type 2 diabetes. Cell 105:745–755
Langin D (2003) The role of uncoupling protein 2 in the development of type 2 diabetes. Drugs Today (Barc) 39:287–295
Jin JH, Zhang TM, Zhang EY, Li Y (2000) Regulatory effects of fasting and insulin on expression of uncoupling protein-1, 2, 3 genes. China J Biochem Mol Biol 16:394–399
Brun S, Carmona MC, Mampel T, Viñas O, Giralt M, Iglesias R, Villarroya F (1999) Activators of peroxisome proliferator-activated receptor-a induce the expression of the uncoupling protein-3 gene in skeletal muscle. A potential mechanism for the lipid intake-dependent activation of uncoupling protein-3 gene expression at birth. Diabetes 48:1217–1222
Acknowledgments
This work was funded by National 863 Proposal of P. R. China (Wuding Chicken Molecular Breeding, 2100AA100305); National and Yunnan Provincial Natural Science foundation Research Projects (31260532;2009CD060; 2011FA015); Found for Talented Man Training in Yunnan Province of the P. R. China (2008PY043), The Research Found from Scholarship Council of Education Ministry of P. R. China.
Author information
Authors and Affiliations
Corresponding authors
Additional information
Qihua Li and Zhiqiang Xu contributed equally to this work.
Rights and permissions
About this article
Cite this article
Li, Q., Xu, Z., Liu, L. et al. Effects of breeds and dietary protein levels on the growth performance, energy expenditure and expression of avUCP mRNA in chickens. Mol Biol Rep 40, 2769–2779 (2013). https://doi.org/10.1007/s11033-012-2030-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11033-012-2030-0