Advertisement

Molecular and Cellular Biochemistry

, Volume 424, Issue 1–2, pp 147–161 | Cite as

Genes involved in the establishment of hepatic steatosis in Muscovy, Pekin and mule ducks

  • Annabelle Tavernier
  • Stéphane Davail
  • Karine Ricaud
  • Marie-Dominique Bernadet
  • Karine Gontier
Article

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.

Keywords

Hepatic steatosis Lipids Gene expression Ducks NAFLD 

Notes

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].

Supplementary material

11010_2016_2850_MOESM1_ESM.docx (20 kb)
Supplementary material 1 (DOCX 19 kb)

References

  1. 1.
    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 CrossRefPubMedGoogle Scholar
  2. 2.
    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 26:331–339CrossRefPubMedGoogle Scholar
  3. 3.
    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):428–435Google Scholar
  4. 4.
    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 CrossRefGoogle Scholar
  5. 5.
    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 CrossRefGoogle Scholar
  6. 6.
    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 CrossRefPubMedGoogle Scholar
  7. 7.
    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 CrossRefGoogle Scholar
  8. 8.
    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 CrossRefGoogle Scholar
  9. 9.
    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 CrossRefPubMedGoogle Scholar
  10. 10.
    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 CrossRefPubMedGoogle Scholar
  11. 11.
    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 CrossRefPubMedGoogle Scholar
  12. 12.
    FOLCH (1959) A rapid method of total lipid extraction. Can J Biochem Physiol 37:911–917CrossRefGoogle Scholar
  13. 13.
    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 CrossRefPubMedGoogle Scholar
  14. 14.
    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 CrossRefGoogle Scholar
  15. 15.
    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 CrossRefGoogle Scholar
  16. 16.
    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):131–141Google Scholar
  17. 17.
    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 CrossRefPubMedGoogle Scholar
  18. 18.
    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 CrossRefPubMedGoogle Scholar
  19. 19.
    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 CrossRefPubMedGoogle Scholar
  20. 20.
    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 CrossRefGoogle Scholar
  21. 21.
    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 PubMedGoogle Scholar
  22. 22.
    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 CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    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 Google Scholar
  24. 24.
    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 CrossRefPubMedGoogle Scholar
  25. 25.
    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 CrossRefPubMedGoogle Scholar
  26. 26.
    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 CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    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 PubMedGoogle Scholar
  28. 28.
    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 CrossRefPubMedGoogle Scholar
  29. 29.
    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 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Annabelle Tavernier
    • 1
    • 2
  • Stéphane Davail
    • 1
    • 2
  • Karine Ricaud
    • 1
    • 2
  • Marie-Dominique Bernadet
    • 3
  • Karine Gontier
    • 1
    • 2
  1. 1.UMR 1419 INRA UPPA NuMéAMont De MarsanFrance
  2. 2.UMR 1419 INRA UPPA NuMéASaint Pée Sur NivelleFrance
  3. 3.INRA UEPFGBenquetFrance

Personalised recommendations