Abstract
Our main objectives were to determine the genes involved in the establishment of hepatic steatosis in three genotypes of palmipeds. To respond to this question, we have compared Muscovy ducks, Pekin ducks and their crossbreed the mule duck fed ad libitum or overfed. We have shown a hepatic overexpression of fatty acid synthase (FAS) and di-acyl glycerol acyl transferase 2 (DGAT2) in overfed individuals, where DGAT2 seemed to be more regulated. This increase in lipogenesis genes is associated with a decrease of lipoprotein formation in Muscovy and mule ducks, especially apolipoprotein B (ApoB) and Microsomal Triglyceride Transfer Protein (MTTP), leading to lipid accumulation in liver. In Pekin ducks, MTTP expression is upregulated suggesting a better hepatic lipids exportation. Regarding lipids re-uptake, fatty acid-binding protein 4 and very-low-density-lipoprotein receptor are overexpressed in liver of mule ducks at the end of the overfeeding period. This phenomenon puts light on a mechanism unknown until today. In fact, mule can incorporate more lipids in liver than the two other genotypes leading to an intensified hepatic steatosis. To conclude, our results confirmed the genotype variability to overfeeding. Furthermore, similar observations are already described in non-alcoholic fatty liver disease in human, and ask if ducks could be an animal model to study hepatic triglyceride accumulation.
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References
Fernandez X, Bouillier-Oudot M, Molette C et al (2011) Duration of transport and holding in lairage at constant postprandial delay to slaughter—effects on fatty liver and breast muscle quality in mule ducks. Poult Sci 90:2360–2369. doi:10.3382/ps.2011-01483
Hermier D, Saadoun A, Salichonb M et al (1991) Plasma lipoproteins and liver lipids in two breeds of geese with different susceptibility to hepatic steatosis : changes induced by development and force-feeding. Lipids 26:331–339
Saadoun A, Leclercq B (1986) In vivo lipogenesis of genetically lean and fat chickens : effects of nutritional state and dietary fat. J Nutr 117(3):428–435
Chartrin P, Bernadet M-D, Guy G et al (2006) Does overfeeding enhance genotype effects on liver ability for lipogenesis and lipid secretion in ducks? Comp Biochem Physiol A 145:390–396. doi:10.1016/j.cbpa.2006.07.014
Davail S, Rideau N, Guy G et al (2003) Hormonal and metabolic responses to overfeeding in three genotypes of ducks. Comp Biochem Physiol Part A Mol Integr Physiol 134:707–715. doi:10.1016/S1095-6433(02)00365-3
Saez G, Davail S, Gentès G et al (2009) Gene expression and protein content in relation to intramuscular fat content in Muscovy and Pekin ducks. Poult Sci 88:2382–2391. doi:10.3382/ps.2009-00208
André JM, Guy G, Gontier-Latonnelle K et al (2007) Influence of lipoprotein-lipase activity on plasma triacylglycerol concentration and lipid storage in three genotypes of ducks. Comp Biochem Physiol A 148:899–902. doi:10.1016/j.cbpa.2007.09.006
Hermier D, Guy G, Guillaumin S et al (2003) Differential channelling of liver lipids in relation to susceptibility to hepatic steatosis in two species of ducks. Comp Biochem Physiol Part B Biochem Mol Biol 135:663–675. doi:10.1016/S1096-4959(03)00146-5
Hérault F, Saez G, Robert E et al (2010) Liver gene expression in relation to hepatic steatosis and lipid secretion in two duck species. Anim Genet 41:12–20. doi:10.1111/j.1365-2052.2009.01959.x
McFarlan JT, Bonen A, Guglielmo CG (2009) Seasonal upregulation of fatty acid transporters in flight muscles of migratory white-throated sparrows (Zonotrichia albicollis). J Exp Biol 212:2934–2940. doi:10.1242/jeb.031682
Weber J-M (2009) The physiology of long-distance migration: extending the limits of endurance metabolism. J Exp Biol 212:593–597. doi:10.1242/jeb.015024
FOLCH (1959) A rapid method of total lipid extraction. Can J Biochem Physiol 37:911–917
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the \(2^{{ - \Delta \Delta C_{\text{t}} }}\) method. Methods 25:402–408. doi:10.1006/meth.2001.1262
Guy G, Rousselot-Pailley D, Gourichon D (1995) Comparaison des performances de l’oie, du canard mulard et du canard de Barbarie soumis au gavage. Ann Zootech 44:297–305. doi:10.1016/0003-424X(96)89755-2
Chartrin P, Bernadet M-D, Guy G et al (2006) Does overfeeding enhance genotype effects on energy metabolism and lipid deposition in breast muscle of ducks? Comp Biochem Physiol A 145:413–418. doi:10.1016/j.cbpa.2006.07.024
Baeza E, Rideau N, Chartrin P et al (2005) Canards de Barbarie, Pékin et leurs hybrides : aptitude à l’engraissement. INRA Prod Anim 18(2):131–141
Parkes HA, Preston E, Wilks D et al (2006) Overexpression of acyl-CoA synthetase-1 increases lipid deposition in hepatic (HepG2) cells and rodent liver in vivo. Am J Physiol Endocrinol Metab 291:E737–E744. doi:10.1152/ajpendo.00112.2006
Zhu LH, Meng H, Duan XJ et al (2011) Gene expression profile in the liver tissue of geese after overfeeding. Poult Sci 90:107–117. doi:10.3382/ps.2009-00616
Monetti M, Levin MC, Watt MJ et al (2007) Dissociation of hepatic steatosis and insulin resistance in mice overexpressing DGAT in the liver. Cell Metab 6:69–78. doi:10.1016/j.cmet.2007.05.005
Cheol SC, Savage DB, Kulkarni A et al (2007) Suppression of diacylglycerol acyltransferase-2 (DGAT2), but not DGAT1, with antisense oligonucleotides reverses diet-induced hepatic steatosis and insulin resistance. J Biol Chem 282:22678–22688. doi:10.1074/jbc.M704213200
Furuhashi M, Saitoh S, Shimamoto K, Miura T (2014) Fatty acid-binding protein 4 (FABP4): pathophysiological insights and potent clinical biomarker of metabolic and cardiovascular diseases. Clin Med Insights Cardiol 8:23–33. doi:10.4137/CMC.S17067
Auguet T, Berlanga A, Guiu-Jurado E et al (2014) Altered fatty acid metabolism-related gene expression in liver from morbidly obese women with non-alcoholic fatty liver disease. Int J Mol Sci 15:22173–22187. doi:10.3390/ijms151222173
Nakamuta M, Fujino T, Yada R et al (2010) Impact of cholesterol metabolism and the LXR-SREBP-1c pathway on nonalcoholic fatty liver disease. Int J Mol Med 26:837–843. doi:10.3892/ijmm
Ahmadian M, Suh JM, Hah N et al (2013) PPARgamma signaling and metabolism: the good, the bad and the future. Nat Med 19:557–566. doi:10.1038/nm.3159
Wang Y, Mu Y, Li H et al (2008) Peroxisome proliferator-activated receptor-γ gene: a key regulator of adipocyte differentiation in chickens. Poult Sci 87:226–232. doi:10.3382/ps.2007-00329
Rogue A, Spire C, Brun M et al (2010) Gene expression changes induced by PPAR gamma agonists in animal and human liver. PPAR Res 2010:325183. doi:10.1155/2010/325183
Memon RA, Tecott LH, Nonogaki K et al (2000) Up-regulation of peroxisome proliferator-activated acid expression in the liver in murine obesity : troglitazone induces expression of PPAR-γ responsive adipose tissue-specific genes in the liver of obese diabetic mice. Endocrinology 141:4021–4031. doi:10.1210/en.141.11.4021
Bax ML, Chambon C, Marty-Gasset N et al (2012) Proteomic profile evolution during steatosis development in ducks. Poult Sci 91:112–120. doi:10.3382/ps.2011-01663
Theron L, Fernandez X, Marty-Gasset N et al (2011) Identification by proteomic analysis of early post-mortem markers involved in the variability in fat loss during cooking of mule duck “foie Gras”. J Agric Food Chem 59:12617–12628. doi:10.1021/jf203058x
Acknowledgments
We thank the “Conseil Général des Landes” and the “Comité Interprofessionnel des Palmipèdes à Foie Gras” (CIFOG) for financing this work. We also thank the technical staff of INRA Artiguères for rearing ducks (Certificate of Authorization to Experiment on Living animals, No. B40-037-1, Ministry of Agriculture and Fish Products, ethic committee Aquitaine birds and fish no.C2EA-73). We are grateful to Hélène Manse and team of GenPhySE for their excellent technical assistance in Folch analysis (INRA UMR 1388 Génétique, Physiologie et Systèmes d’Elevage (GenPhySE), F-31326 Castanet-Tolosan, France). We would also like to thank Frédéric Martins and Jean-José Maoret for performing Fluidigm analysis [Génopole Toulouse/Midi-pyrénées, Plateau Transcriptomique Quantitative (TQ), Toulouse, France].
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Tavernier, A., Davail, S., Ricaud, K. et al. Genes involved in the establishment of hepatic steatosis in Muscovy, Pekin and mule ducks. Mol Cell Biochem 424, 147–161 (2017). https://doi.org/10.1007/s11010-016-2850-7
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DOI: https://doi.org/10.1007/s11010-016-2850-7