Hostname: page-component-8448b6f56d-mp689 Total loading time: 0 Render date: 2024-04-23T17:31:56.844Z Has data issue: false hasContentIssue false

Adipogenic genes expression in relation to hepatic steatosis in the liver of two duck species

Published online by Cambridge University Press:  03 May 2018

F. Hérault
Affiliation:
PEGASE, INRA, Agrocampus Ouest, Saint-Gilles, F-35590, France
C. Duby
Affiliation:
PEGASE, INRA, Agrocampus Ouest, Saint-Gilles, F-35590, France
E. Baéza
Affiliation:
URA, INRA, Nouzilly, F-37380, France
C. Diot*
Affiliation:
PEGASE, INRA, Agrocampus Ouest, Saint-Gilles, F-35590, France
Get access

Abstract

Some studies have shown that expression of peroxisome proliferator-activated receptor gamma (PPARG), a key regulator of adipogenesis, and of some adipocyte-specific genes or adipokines are expressed in hepatic steatosis, leading to the concept of ‘adipogenic hepatic steatosis’ or ‘hepatic adiposis.’ Most of these studies were conducted in genetic obese mouse models or after manipulation of gene expression. The relevance of this concept to other species and more physiological models was here addressed in ducks which are able to develop hepatic steatosis after overfeeding. The expression of PPARG and other adipocyte-specific genes was thus analyzed in the liver of ducks fed ad libitum or overfed and compared with those observed in adipose tissues. Pekin (Anas platyrhynchos) and Muscovy ducks (Cairina moschata) were analyzed, as metabolic responses to overfeeding differ according to these two species, Muscovy ducks having a greater ability to synthesize and store lipids in the liver than Pekin ducks. Our results indicate that adipocyte-specific genes are expressed in the liver of ducks, PPARG and fatty acid-binding protein 4 being upregulated and adiponectin and leptin receptor downregulated by overfeeding. However, these expression levels are much lower than those observed in adipose tissue suggesting that fatty liver cells are not transformed to adipocytes, although some hepato-specific functions are decreased in fatty liver when compared with normal liver.

Type
Research Article
Copyright
© The Animal Consortium 2018 

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.)

References

Amri, EZ, Bertrand, B, Ailhaud, G and Grimaldi, P 1991. Regulation of adipose cell differentiation. I. Fatty acids are inducers of the aP2 gene expression. Journal of Lipid Research 32, 14491456.Google Scholar
Arita, Y, Kihara, S, Ouchi, N, Takahashi, M, Maeda, K, Miyagawa, J, Hotta, K, Shimomura, I, Nakamura, T, Miyaoka, K, Kuriyama, H, Nishida, M, Yamashita, S, Okubo, K, Matsubara, K, Muraguchi, M, Ohmoto, Y, Funahashi, T and Matsuzawa, Y 1999. Paradoxical decrease of an adipose-specific protein, adiponectin, in obesity. Biochemical and Biophysical Research Communications 257, 7983.Google Scholar
Bedoucha, M, Atzpodien, E and Boelsterli, UA 2001. Diabetic KKAy mice exhibit increased hepatic PPARgamma1 gene expression and develop hepatic steatosis upon chronic treatment with antidiabetic thiazolidinediones. Journal of Hepatology 35, 1723.Google Scholar
Bourneuf, E, Hérault, F, Chicault, C, Carré, W, Assaf, S, Monnier, A, Mottier, S, Lagarrigue, S, Douaire, M, Mosser, J and Diot, C 2006. Microarray analysis of differential gene expression in the liver of lean and fat chickens. Gene 372, 162170.Google Scholar
Chartrin, P, Bernadet, MD, Guy, G, Mourot, J, Hocquette, JF, Rideau, N, Duclos, MJ and Baéza, E 2006. Does overfeeding enhance genotype effects on liver ability for lipogenesis and lipid secretion in ducks? Comparative Biochemistry and Physiology. Part A: Molecular & Integrative Physiology 145, 390396.Google Scholar
Colombo, C, Haluzik, M, Cutson, JJ, Dietz, KR, Marcus-Samuels, B, Vinson, C, Gavrilova, O and Reitman, ML 2003. Opposite effects of background genotype on muscle and liver insulin sensitivity of lipoatrophic mice. Role of triglyceride clearance. The Journal of Biological Chemistry 278, 39923999.Google Scholar
Cook, JS, Lucas, JJ, Sibley, E, Bolanowski, MA, Christy, RJ, Kelly, TJ and Lane, MD 1988. Expression of the differentiation-induced gene for fatty acid-binding protein is activated by glucocorticoid and cAMP. Proceedings of the National Academy of Sciences of the United States of America 85, 29492953.Google Scholar
Davail, S, Rideau, N, Guy, G, Andre, JM, Hermier, D and Hoo-Paris, R 2003. Hormonal and metabolic responses to overfeeding in three genotypes of ducks. Comparative Biochemistry and Physiology. Part A: Molecular & Integrative Physiology 134, 707715.Google Scholar
Distel, RJ, Robinson, GS and Spiegelman, BM 1992. Fatty acid regulation of gene expression. Transcriptional and post-transcriptional mechanisms. The Journal of Biological Chemistry 267, 59375941.Google Scholar
Fabbrini, E, Sullivan, S and Klein, S 2010. Obesity and nonalcoholic fatty liver disease: biochemical, metabolic, and clinical implications. Hepatology 51, 679689.Google Scholar
Ferré, P and Foufelle, F 2010. Hepatic steatosis: a role for de novo lipogenesis and the transcription factor SREBP-1c. Diabetes, Obesity & Metabolism 12 (suppl. 2), 8392.Google Scholar
Gavrilova, O, Haluzik, M, Matsusue, K, Cutson, JJ, Johnson, L, Dietz, KR, Nicol, CJ, Vinson, C, Gonzalez, FJ and Reitman, ML 2003. Liver peroxisome proliferator-activated receptor gamma contributes to hepatic steatosis, triglyceride clearance, and regulation of body fat mass. The Journal of Biological Chemistry 278, 3426834276.Google Scholar
Hérault, F, Saez, G, Robert, E, Al Mohammad, A, Davail, S, Chartrin, P, Baéza, E and Diot, C 2010. Liver gene expression in relation to hepatic steatosis and lipid secretion in two duck species. Animal Genetics 41, 1220.Google Scholar
Hermier, D, Guy, G, Guillaumin, S, Davail, S, André, JM and Hoo-Paris, R 2003. Differential channelling of liver lipids in relation to susceptibility to hepatic steatosis in two species of ducks. Comparative Biochemistry and Physiology. Part B: Biochemistry & Molecular Biology 135, 663675.Google Scholar
Kletzien, RF, Foellmi, LA, Harris, PK, Wyse, BM and Clarke, SD 1992. Adipocyte fatty acid-binding protein: regulation of gene expression in vivo and in vitro by an insulin-sensitizing agent. Molecular Pharmacology 42, 558562.Google Scholar
Lavoie, JM and Gauthier, MS 2006. Regulation of fat metabolism in the liver: link to non-alcoholic hepatic steatosis and impact of physical exercise. Cellular and Molecular Life Sciences 63, 13931409.Google Scholar
Lefterova, MI, Haakonsson, AK, Lazar, MA and Mandrup, S 2014. PPARgamma and the global map of adipogenesis and beyond. Trends in Endocrinology and Metabolism 25, 293302.Google Scholar
Livak, KJ and Schmittgen, TD 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods 25, 402408.Google Scholar
Matsusue, K, Haluzik, M, Lambert, G, Yim, SH, Gavrilova, O, Ward, JM, Brewer, B Jr., Reitman, ML and Gonzalez, FJ 2003. Liver-specific disruption of PPARgamma in leptin-deficient mice improves fatty liver but aggravates diabetic phenotypes. The Journal of Clinical Investigation 111, 737747.Google Scholar
Melki, SA and Abumrad, NA 1993. Expression of the adipocyte fatty acid-binding protein in streptozotocin-diabetes: effects of insulin deficiency and supplementation. Journal of Lipid Research 34, 15271534.Google Scholar
Memon, RA, Tecott, LH, Nonogaki, K, Beigneux, A, Moser, AH, Grunfeld, C and Feingold, KR 2000. Up-regulation of peroxisome proliferator-activated receptors (PPAR-alpha) and PPAR-gamma messenger ribonucleic acid expression in the liver in murine obesity: troglitazone induces expression of PPAR-gamma-responsive adipose tissue-specific genes in the liver of obese diabetic mice. Endocrinology 141, 40214031.Google Scholar
Musso, G, Gambino, R and Cassader, M 2009. Recent insights into hepatic lipid metabolism in non-alcoholic fatty liver disease (NAFLD). Progress in Lipid Research 48, 126.Google Scholar
Osman, RH, Shao, D, Liu, L, Xia, L, Sun, X, Zheng, Y, Wang, L, Zhang, R, Zhang, Y, Zhang, J, Gong, D and Geng, T 2016. Expression of mitochondria-related genes is elevated in overfeeding-induced goose fatty liver. Comparative Biochemistry and Physiology. Part B: Biochemistry & Molecular Biology 192, 3037.Google Scholar
Panera, N, Della Corte, C, Crudele, A, Stronati, L, Nobili, V and Alisi, A 2016. Recent advances in understanding the role of adipocytokines during non-alcoholic fatty liver disease pathogenesis and their link with hepatokines. Expert Review of Gastroenterology & Hepatology 10, 393403.Google Scholar
Parekh, S and Anania, FA 2007. Abnormal lipid and glucose metabolism in obesity: implications for nonalcoholic fatty liver disease. Gastroenterology 132, 21912207.Google Scholar
Polyzos, SA, Kountouras, J and Mantzoros, CS 2016. Adipokines in nonalcoholic fatty liver disease. Metabolism: Clinical and Experimental 65, 10621079.Google Scholar
Polyzos, SA, Kountouras, J, Zavos, C and Tsiaousi, E 2010. The role of adiponectin in the pathogenesis and treatment of non-alcoholic fatty liver disease. Diabetes, Obesity & Metabolism 12, 365383.Google Scholar
Rahimian, R, Masih-Khan, E, Lo, M, van Breemen, C, McManus, BM and Dube, GP 2001. Hepatic over-expression of peroxisome proliferator activated receptor gamma2 in the ob/ob mouse model of non-insulin dependent diabetes mellitus. Molecular and Cellular Biochemistry 224, 2937.Google Scholar
Ray, K 2013. NAFLD-the next global epidemic. Nature Reviews. Gastroenterology & Hepatology 10, 621.Google Scholar
Saez, G, Baéza, E, Davail, S, Durand, D, Bauchart, D and Gruffat, D 2009. Hepatic metabolism of glucose and linoleic acid varies in relation to susceptibility to fatty liver in ad libitum-fed Muscovy and Pekin ducks. The British Journal of Nutrition 101, 510517.Google Scholar
Schadinger, SE, Bucher, NL, Schreiber, BM and Farmer, SR 2005. PPARgamma 2 regulates lipogenesis and lipid accumulation in steatotic hepatocytes. American Journal of Physiology. Endocrinology and Metabolism 288, E1195E1205.Google Scholar
Scherer, PE, Williams, S, Fogliano, M, Baldini, G and Lodish, HF 1995. A novel serum protein similar to C1q, produced exclusively in adipocytes. The Journal of Biological Chemistry 270, 2674626749.Google Scholar
Schroeder, A, Mueller, O, Stocker, S, Salowsky, R, Leiber, M, Gassmann, M, Lightfoot, S, Menzel, W, Granzow, M and Ragg, T 2006. The RIN: an RNA integrity number for assigning integrity values to RNA measurements. BMC Molecular Biology 7, 3.Google Scholar
Seroussi, E, Cinnamon, Y, Yosefi, S, Genin, O, Smith, JG, Rafati, N, Bornelov, S, Andersson, L and Friedman-Einat, M 2016. Identification of the long-sought leptin in chicken and duck: Expression pattern of the highly GC-rich avian leptin fits an autocrine/paracrine rather than endocrine eunction. Endocrinology 157, 737751.Google Scholar
Stojsavljevic, S, Gomercic Palcic, M, Virovic Jukic, L, Smircic Duvnjak, L and Duvnjak, M 2014. Adipokines and proinflammatory cytokines, the key mediators in the pathogenesis of nonalcoholic fatty liver disease. World Journal of Gastroenterology 20, 1807018091.Google Scholar
Tamura, S and Shimomura, I 2005. Contribution of adipose tissue and de novo lipogenesis to nonalcoholic fatty liver disease. The Journal of Clinical Investigation 115, 11391142.Google Scholar
Tan, NS, Shaw, NS, Vinckenbosch, N, Liu, P, Yasmin, R, Desvergne, B, Wahli, W and Noy, N 2002. Selective cooperation between fatty acid binding proteins and peroxisome proliferator-activated receptors in regulating transcription. Molecular and Cellular Biology 22, 51145127.Google Scholar
Tavernier, A, Davail, S, Ricaud, K, Bernadet, MD and Gontier, K 2017. Genes involved in the establishment of hepatic steatosis in Muscovy, Pekin and mule ducks. Molecular and Cellular Biochemistry 424, 147161.Google Scholar
Tontonoz, P and Spiegelman, BM 2008. Fat and beyond: the diverse biology of PPARgamma. Annual Review of Biochemistry 77, 289312.Google Scholar
Vidal-Puig, A, Jimenez-Linan, M, Lowell, BB, Hamann, A, Hu, E, Spiegelman, B, Flier, JS and Moller, DE 1996. Regulation of PPAR gamma gene expression by nutrition and obesity in rodents. The Journal of Clinical Investigation 97, 25532561.Google Scholar
Yoda-Murakami, M, Taniguchi, M, Takahashi, K, Kawamata, S, Saito, K, Choi-Miura, NH and Tomita, M 2001. Change in expression of GBP28/adiponectin in carbon tetrachloride-administrated mouse liver. Biochemical and Biophysical Research Communications 285, 372377.Google Scholar
Yu, S, Matsusue, K, Kashireddy, P, Cao, WQ, Yeldandi, V, Yeldandi, AV, Rao, MS, Gonzalez, FJ and Reddy, JK 2003. Adipocyte-specific gene expression and adipogenic steatosis in the mouse liver due to peroxisome proliferator-activated receptor gamma1 (PPARgamma1) overexpression. The Journal of Biological Chemistry 278, 498505.Google Scholar
Zhu, LH, Meng, H, Duan, XJ, Xu, GQ, Zhang, J and Gong, DQ 2011. Gene expression profile in the liver tissue of geese after overfeeding. Poultry Science 90, 107117.Google Scholar