Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology
Regulation of fatty acid oxidation in chicken (Gallus gallus): Interactions between genotype and diet composition
Introduction
The utilization of fatty acids as energy substrate may be of importance in tissues such as liver and oxidative or mixed type skeletal muscles, especially in case of cold exposure, fasting or exercise. In mammals, mitochondrial β-oxidation is quantitatively the main mechanism providing energy from fatty acids in cells. Long chain fatty acids are imported into the mitochondrial matrix by the carnitine–palmitoyltransferase (CPT) system (Bartlett and Eaton, 2004), where the transfer of acyl groups from coenzyme A to carnitine is controlled by the enzyme CPT1. Up to now, one liver and one muscle CPT1 isoforms have been evidenced in chicken (Skiba-Cassy et al., 2007), as is the case in humans (Britton et al., 1997). After this step, fatty acids are oxidized by the β-oxidation pathway, in which the β-hydroxyacyl CoA dehydrogenase (HAD) is considered as the rate-limiting enzyme in mammals (McGarry et al., 1989, Eaton, 2002). The provided acetyl-CoA enters the tricarboxylic acid (TCA) cycle, resulting in the reduction of co-factors. These cofactors are re-oxidized at the level of the mitochondrial respiratory chain, in which cytochrome c oxidase (COx) is the key-enzyme regulating O2 consumption. The efficiency of the resulting ATP synthesis might be modulated by a mild uncoupling. Part of this uncoupling could be controlled by uncoupling proteins UCP (i.e. avian avUCP in birds; Raimbault et al., 2001). The avUCP gene has been shown to be mainly expressed in skeletal muscles (Evock-Clover et al., 2002), and recently reported to be the avian ortholog to the mammalian UCP3 (Emre et al., 2007, Saito et al., 2008). This protein has been suggested to be involved in heat production in chicken, duckling and king penguin (Raimbault et al., 2001, Taouis et al., 2002, Toyomizu et al., 2002, Collin et al., 2003a, Collin et al., 2003c, Collin et al., 2005, Collin et al., 2007, Rey et al., 2008), in fatty acid or metabolic anion transport (Collin et al., 2003b, Mozo et al., 2005) and more recently in the limitation of reactive oxygen species (ROS) generation in avian species (Criscuolo et al., 2005), including king penguins (Talbot et al., 2003) and chickens (Abe et al., 2006, Mujahid et al., 2006).
Fast growing chickens (Gallus gallus) develop excessive adiposity besides the high muscle mass resulting from selection. Most attention has been paid to the control of lipogenesis in this species (Daval et al., 2000, Bourneuf et al., 2006). However, information is scarce about the mechanisms regulating lipolysis and energy expenditure, especially mitochondrial fatty acid utilization. In humans, a reduction in the rate of muscle lipid oxidation has been postulated to favor peripheral fat accumulation (Colberg et al., 1995, Marques-Lopes et al., 2001, Young et al., 2002), one candidate mechanism being a reduction in the activity of CPT 1 (Alam and Saggerson, 1998, Kim et al., 2000, Chan et al., 2005). In addition, rainbow trout selected for muscle high fat content presents reduced hepatic fatty acid oxidation and mitochondrial oxidative capacities in both liver and muscle when compared to their lean counterparts (Kolditz et al., 2008).
In order to better understand these mechanisms in chickens, effects of genotype and diet composition on the regulation of mitochondrial fatty acid utilization and of O2 consumption were investigated in two major tissues for fatty acid oxidation, liver and muscle. This study is the second part of an experiment (Swennen et al., 2006) substituting energy and proteins in two isoenergetic diets offered to two genetically divergent lines of broiler chickens selected on their abdominal fat content (Leclercq et al., 1980). These diets affected growth and abdominal fat content of both lines, without influencing significantly heat production or diet-induced thermogenesis (Swennen et al., 2006). In the present article, we give further insight into the control of mitochondrial fatty acid utilization, by measuring the expression or activity of several genes involved in these mechanisms in liver and skeletal muscle. In addition, we focus on the expression of the avian uncoupling protein that could play a major role in the regulation of energy metabolism (thermogenesis, prevention of oxidative stress or lipotoxicity) of avian species.
Section snippets
Experimental design
Sixty day-old male broiler chickens (Gallus gallus) of genetically fat and lean lines (INRA Nouzilly, France; Leclercq et al., 1980) were reared in the conditions described by Swennen et al. (2006).
Briefly, from 14 days of age, chickens of each line were divided into two groups, each receiving one of two isoenergetic diets (Table 1), resulting in a total of 4 groups of 15 chickens. The isoenergetic diets contained the same ingredients included in different proportions. The concentrations of
Regulation of hepatic mitochondrial metabolism
We first investigated mRNA expressions of genes involved in long-chain fatty acid transfers through the mitochondrial membrane and fatty acid utilisation in hepatic mitochondria (Fig. 1A to D).
In liver, L-CPT1 mRNA expression was 1.5 to 2-fold higher in chickens fed with the HF/LP diet compared to chickens fed with the LF/HP diet (P < 0.01; Fig. 1A). Messenger RNA expression of the muscle predominant CPT1, M-CPT1, was also regulated by the composition of the diet with a significant interaction
Experimental model
Genetically fat and lean lines of broiler chicken were developed by Leclercq et al. (1980) in order to investigate the mechanisms controlling fattening in this species. These lines differ in carcass lipid and muscle glycogen content, but exhibit similar live body weight, feed consumption and energy expenditure (Geraert et al., 1988, Sibut et al., 2008). Moreover, in the present experiment, abdominal fat content of chickens from the fat line was more affected by changes in diet composition:
Acknowledgements
The authors gratefully thank N. Millet, A. Boucard, C. Jenkins and E Godet for their technical assistance, E. Baeza, and J. Simon for helpful discussions (INRA, France), as well as G.P.J. Janssens and I. Vaesen (Belgium) for the experimental design. This work was partly supported by the Research Fund Katholieke Universiteit Leuven (OT/02/36) and INRA. R. Joubert is a PhD student supported by a grant from INRA and Région Centre, France and Quirine Swennen is supported by the Research Foundation
References (63)
- et al.
Possible role of avian uncoupling protein in down-regulating mitochondrial superoxide production in skeletal muscle of fasted chickens
FEBS Lett.
(2006) - et al.
Microarray analysis of differential gene expression in the liver of lean and fat chickens
Gene
(2006) - et al.
Fine chromosome mapping of the genes for human liver and muscle carnitine palmitoyltransferase I (CPT1A and CPT1B)
Genomics
(1997) - et al.
Reduced adiposity in bitter melon (Momordica charantia)-fed rats is associated with increased lipid oxidative enzyme activities and uncoupling protein expression
J. Nutr.
(2005) - et al.
Cold-induced enhancement of avian uncoupling protein expression, heat production and triiodothyronine concentrations in broiler chicks
Gen. Comp. Endocrinol.
(2003) - et al.
Potential involvement of mammalian and avian uncoupling proteins in the thermogenic effect of thyroid hormones
Domest. Anim. Endocrinol.
(2005) - et al.
Effects of thermal manipulation during early and late embryogenesis on thermotolerance and breast muscle characteristics in broiler chickens
Poult. Sci.
(2007) - et al.
Metabolic differences between genetically lean and fat chickens are partly attributed to alteration of insulin signaling in liver
J. Nutr.
(1999) Control of mitochondrial beta-oxidation flux
Prog. Lipid Res.
(2002)- et al.
Expression of an uncoupling protein gene homolog in chickens
Comp. Biochem. Physiol. A Mol. Integr. Physiol.
(2002)
Energy metabolism in genetically fat and lean chickens: diet- and cold-induced thermogenesis
J. Nutr.
Evidence of enhanced storage capacity in adipose tissue of genetically fat chickens
J. Nutr.
Nutritional regulation and role of peroxisome proliferator-activated receptor delta in fatty acid catabolism in skeletal muscle
Biochim. Biophys. Acta
Fatty acid regulation of hepatic gene transcription
J. Nutr.
Hepatic gene expression profiles in a long-term high-fat diet-induced obesity mouse model
Gene
De novo expression of uncoupling protein 3 is associated to enhanced mitochondrial thioesterase-1 expression and fatty acid metabolism in liver of fenofibrate-treated rats
FEBS Lett.
Kupffer cells are a dominant site of uncoupling protein 2 expression in rat liver
Biochem. Biophys. Res. Commun.
Postprandial de novo lipogenesis and metabolic changes induced by a high-carbohydrate, low-fat meal in lean and overweight men
Am. J. Clin. Nutr.
Cloning of rat uncoupling protein-3 and uncoupling protein-2 cDNAs: their gene expression in rats fed high-fat diet
FEBS Lett.
Acute heat stress stimulates mitochondrial superoxide production in broiler skeletal muscle, possibly via downregulation of uncoupling protein content
Poult. Sci.
Gene expression in breast muscle and duodenum from low and high feed efficient broilers
Poult. Sci.
Uncoupling protein 2, in vivo distribution, induction upon oxidative stress, and evidence for translational regulation
J. Biol. Chem.
Impact of dietary protein content on uncoupling protein mRNA abundance in swine
Comp. Biochem. Physiol. B Biochem. Mol. Biol.
Adaptive evolution of the uncoupling protein 1 gene contributed to the acquisition of novel nonshivering thermogenesis in ancestral eutherian mammals
Gene
Fenofibrate activates the biochemical pathways and the de novo expression of genes related to lipid handling and uncoupling protein-3 functions in liver of normal rats
Biochim. Biophys. Acta
Chicken liver and muscle carnitine palmitoyltransferase 1: nutritional regulation of messengers
Comp. Biochem. Physiol. B Biochem. Mol. Biol.
Diet-induced thermogenesis and glucose oxidation in broiler chickens: influence of genotype and diet composition
Poult. Sci.
Superoxide activates a GDP-sensitive proton conductance in skeletal muscle mitochondria from king penguin (Aptenodytes patagonicus)
Biochem. Biophys. Res. Commun.
Early-age thermal conditioning reduces uncoupling protein messenger RNA expression in pectoral muscle of broiler chicks at seven days of age
Poult. Sci.
Cold-induced mitochondrial uncoupling and expression of chicken UCP and ANT mRNA in chicken skeletal muscle
FEBS Lett.
Malonyl-CoA and the regulation of fatty acid oxidation in soleus muscle
Biochem. J.
Cited by (20)
Exposure of embryos to cyclically cold incubation temperatures durably affects energy metabolism and antioxidant pathways in broiler chickens
2014, Poultry ScienceCitation Excerpt :Surprisingly, the muscle expression of the avian UCP3, involved in the limitation of mitochondrial superoxide production in chickens (Abe et al., 2006), was reduced in the cold I group. This protein, primarily thought to be involved in thermogenesis in birds as the mammalian UCP1 (Raimbault et al., 2001;Collin et al., 2003a,b,c) or fatty acid metabolism (Collin et al., 2009), was later suspected to be part of the mitochondrial antioxidant defense (Abe et al., 2006). Perhaps this occurs by translocating lipid hydroperoxides across the mitochondrial inner membrane, as suggested for its ortholog UCP3 in mammals (Lombardi et al., 2010).
Birds and longevity: Does flight driven aerobicity provide an oxidative sink?
2012, Ageing Research ReviewsCitation Excerpt :Strenuous exercise has been shown to slow tumour growth and vascularisation (Helmrich et al., 1991; Zielinski et al., 2004), and CR stimulates glucagon secretion and lowers IGF1 with a concomitant drop in cancers (Dunn et al., 1997). CR even appears to extend the lifespan of birds (Holmes and Ottinger, 2003; Ottinger and Lavoie, 2007), as it is used to extend the lives and reproductive life span in broiler chickens (Holmes and Ottinger, 2003), and increases the expression of PGC-1α (Collin et al., 2009). Pharmacological mimics of CR are also emerging.
Creatine pyruvate enhances lipolysis and protein synthesis in broiler chicken
2011, Agricultural Sciences in China