Targets for TNFα-induced lipolysis in gilthead sea bream(Sparus aurata L.) adipocytes isolated from lean and fat juvenile fish

Journal of Experimental Biology - Tập 212 Số 14 - Trang 2254-2260 - 2009

Lourdes Cruz-Garcia¹, Alfonso Saera-Vila², Isabel Navarro¹, Josep À. Calduch-Giner², Jaume Pérez‐Sánchez²

¹Departament de Fisiología, Facultat de Biología, Universitat de Barcelona, 08028 Barcelona, Spain

²Instituto de Acuicultura de Torre de la Sal (CSIC), Departamento de Biología, Cultivo y Patología de Especies Marinas, 12595 Ribera de Cabanes, Castellón, Spain

Tóm tắt

SUMMARY The present study aimed to analyze adiposity heterogeneity and the role of liver X receptor (LXRα) and peroxisome proliferator-activated receptors(PPARs) as targets of tumour necrosis factor-α (TNFα) in gilthead sea bream (Sparus aurata L.). The screening of 20 fish at the beginning of the warm season identified two major groups with fat and lean phenotypes. Fat fish showed increased liver and mesenteric fat depots. This increased adiposity was concurrent in the adipose tissue to enhanced expression of lipoprotein lipase (LPL) whereas mRNA levels of the hormone-sensitive lipase (HSL) remained almost unchanged. The resulting LPL/HSL ratio was thereby highest in fat fish, which suggests that this group of fish has not reached its peak fat storage capacity. This is not surprising given the increased expression of PPARγ in the absence of a counter-regulatory raise of TNFα. However, this lipolytic cytokine exerted dual effects in primary adipocyte cultures that differ within and between lean and fat fish. One set of fat fish did not respond to TNFαtreatment whereas a second set exhibited a lipolytic response (increased glycerol release) that was apparently mediated by the downregulated expression of PPARβ. In lean fish, TNFα exerted a strong and non-transcriptionally mediated lipolytic action. Alternatively, TNFαwould inhibit lipid deposition via the downregulated expression of adipogenic nuclear factors (PPARγ and LXRα). TNFα targets are therefore different in fish with lean and fat phenotypes, which is indicative of the complex network involved in the regulation of fish lipid metabolism.

Từ khóa

Tài liệu tham khảo

Al-Hasani, H. and Joost, H. G. (2005). Nutrition-/diet-induced changes in gene expression in white adipose tissue. Best Pract. Res. Clin. Endocrinol. Metab.19,589-603.

Albalat, A., Gómez-Requeni, P., Rojas, P., Médale,F., Kaushik, S., Vianen, G. J., Van den Thillart, G., Gutiérrez, J.,Pérez-Sánchez, J. and Navarro, I. (2005a). Nutritional and hormonal control of lipolysis in isolated gilthead seabream(Sparus aurata) adipocytes. Am. J. Physiol. Regul. Integr. Comp. Physiol.289,R259-R265.

Albalat, A., Liarte, C., MacKenzie, S., Tort, L., Planas, J. V. and Navarro, I. (2005b). Control of adipose tissue lipid metabolism by tumor necrosis factor-α in rainbow trout (Oncorhynchus mykiss). J. Endocrinol.184,527-534.

Albalat, A., Saera-Vila, A., Capilla, E., Gutiérrez, J.,Pérez-Sánchez, J. and Navarro, I. (2007). Insulin regulation of lipoprotein lipase (LPL) activity and expression in gilthead sea bream (Sparus aurata). Comp. Biochem. Physiol.148B,151-159.

Archer, A., Lauter, G., Hauptmann, G., Mode, A. and Gustafsson,J. A. (2008). Transcriptional activity and developmental expression of liver X receptor (lxr) in zebrafish. Dev. Dyn.237,1090-1098.

Barak, Y., Liao, D., He, W., Ong, E. S., Nelson, M. C., Olefsky,J. M., Boland, R. and Evans, R. M. (2002). Effects of peroxisome proliferator-activated receptor δ on placentation, adiposity,and colorectal cancer. Proc. Natl. Acad. Sci. USA99,303-308.

Benedito-Palos, L., Saera-Vila, A., Calduch-Giner, J. A.,Kaushik, S. and Pérez-Sánchez, J. (2007). Combined replacement of fish meal and oil in practical diets for fast growing juveniles of gilthead sea bream (Sparus aurata L.): networking of systemic and local components of GH/IGF axis. Aquaculture267,199-212.

Benedito-Palos, L., Navarro, J. C., Sitjà-Bobadilla, A.,Gordon Bell, J., Kaushik, S. and Pérez-Sánchez, J.(2008). High levels of vegetable oils in plant protein-rich diets fed to gilthead sea bream (Sparus aurata L.): growth performance,muscle fatty acid profiles and histological alterations of target tissues. Br. J. Nutr.100,992-1003.

Boukouvala, E., Antonopoulou, E., Favre-Krey, L., Diez, A.,Bautista, J. M., Leaver, M. J., Tocher, D. R. and Krey, G.(2004). Molecular characterization of three peroxisome proliferator-activated receptors from the sea bass (Dicentrarchus labrax). Lipids39,1085-1092.

Bouraoui, L., Gutierrez, J. and Navarro, I.(2008). Regulation of proliferation and differentiation of adipocyte precursor cells in rainbow trout (Oncorhynchus mykiss). J. Endocrinol.198,459-469.

Caballero, M. J., Izquierdo, M. S., Kjorsvik, E., Fernandez, A. J. and Rosenlund, G. (2004). Histological alterations in the liver of sea bream, Sparus aurata L., caused by short- or long-term feeding with vegetable oils: recovery of normal morphology after feeding fish oil as the sole lipid source. J. Fish Dis.27,531-541.

Calduch-Giner, J. A., Mingarro, M., Vega-Rubín de Celis,S., Boujard, D. and Pérez-Sánchez, J. (2003). Molecular cloning and characterization of gilthead sea bream (Sparus aurata) growth hormone receptor (GHR): assessment of alternative splicing. Comp. Biochem. Physiol.136B, 1-13.

Chawla, A., Repa, J. J., Evans, R. M. and Mangelsdorf, D. J.(2001). Nuclear receptors and lipid physiology: opening the X-Files. Science294,1866-1870.

Chinetti, G., Lestavel, S., Bocher, V., Remaley, A. T., Neve,B., Torra, I. P., Teissier, E., Minnich, A., Jaye, M., Duverger, N. et al.(2001). PPAR-alpha and PPAR-gamma activators induce cholesterol removal from human macrophage foam cells through stimulation of the ABCA1 pathway. Nat. Med.7,53-58.

Cruz-Garcia, L., Minghetti, M., Navarro, I. and Tocher, D. R. (2009). Molecular cloning, tissue expression and regulation of liver X Receptor (LXR) transcripotion factors of Atlantic salmon(Salmo salar) and rainbow trout (Oncorhynchus mykiss). Comp. Biochem. Physiol. B153B,81-88.

Desvergne, B., Michalik, L. and Wahli, W.(2006). Transcriptional regulation of metabolism. Physiol. Rev.86,465-514.

Diez, A., Menoyo, D., Perez-Benavente, S., Calduch-Giner, J. A.,Vega-Rubin de Celis, S., Obach, A., Favre-Krey, L., Boukouvala, E., Leaver, M. J., Tocher, D. R. et al. (2007). Conjugated linoleic acid affects lipid composition, metabolism, and gene expression in gilthead sea bream (Sparus aurata L). J. Nutr.137,1363-1369.

Farrell, A. P. (2002). Coronary arteriosclerosis in salmon: growing old or growing fase? Comp. Biochem. Physiol.132A,723-735.

Fonseca-Alaniz, M. H., Takada, J., onso-Vale, M. I. and Lima, F. B. (2007). Adipose tissue as an endocrine organ: from theory to practice. J. Pediatr.83,S192-S203.

González-Yanes, C. and Sánchez-Margalet, V.(2006). Signalling mechanisms regulating lipolysis. Cell. Signal.18,401-408.

Guilherme, A., Virbasius, J. V., Puri, V. and Czech, M. P.(2008). Adipocyte dysfunctions linking obesity to insulin resistance and type 2 diabetes. Nat. Rev. Mol. Cell. Biol.9,367-377.

Harmon, J. S., Rieniets, L. M. and Sheridan, M. A.(1993). Glucagon and insulin regulate lipolysis in trout liver by altering phosphorylation of triacylglycerol lipase. Am. J. Physiol. Regul. Integr. Comp. Physiol.265,R255-R260.

Hazel, J. R. and Sidell, B. D. (2004). The substrate specificity of hormone-sensitive lipase from adipose tissue of the Antarctic fish Trematomus newnesi.J. Exp. Biol.207,897-903.

Holm, C., Osterlund, T., Laurell, H. and Contreras, J. A.(2000). Molecular mechanisms regulating hormone-sensitive lipase and lipolysis. Annu. Rev. Nutr.20,365-393.

Kern, P. A., Ranganathan, S., Li, C., Wood, L. and Ranganathan,G. (2001). Adipose tissue tumor necrosis factor and interleukin-6 expression in human obesity and insulin resistance. Am. J. Physiol. Endocrinol. Metab.280,E745-E751.

Kim, M. S., Sweeney, T. R., Shigenaga, J. K., Chui, L. G.,Moser, A., Grunfeld, C. and Feingold, K. R. (2007). Tumor necrosis factor and interleukin 1 decrease RXRα, PPARα,PPARγ, LXRα, and the coactivators SRC-1, PGC-1α, and PGC-1β in liver cells. Metabolism56,267-279.

Kliewer, S. A., Forman, B. M., Blumberg, B., Ong, E. S.,Borgmeyer, U., Mangelsdorf, D. J., Umesono, K. and Evans, R. M.(1994). Differential expression and activation of a family of murine peroxisome proliferator-activated receptors. Proc. Natl. Acad. Sci. USA91,7355-7359.

Leaver, M. J., Boukouvala, E., Antonopoulou, E., Diez, A.,Favre-Krey, L., Ezaz, M. T., Bautista, J. M., Tocher, D. R. and Krey, G.(2005). Three peroxisome proliferator-activated receptor isotypes from each of two species of marine fish. Endocrinology146,3150-3162.

Leaver, M. J., Bautista, J. M., Björnsson, B. T.,Jönsson, E., Krey, G., Tocher, D. R. and Torstensen, B. E.(2008). Towards fish lipid nutrigenomics: current state and prospects for fin-fish aquaculture. Rev. Fish. Sci.16, 73-94.

Lee, C. H., Olson, P., Hevener, A., Mehl, I., Chong, L. W.,Olefsky, J. M., Gonzalez, F. J., Ham, J., Kang, H., Peters, J. M. et al.(2006). PPARδ regulates glucose metabolism and insulin sensitivity. Proc. Natl. Acad. Sci. USA103,3444-3449.

Livak, K. J. and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT method. Methods25,402-408.

Michelsen, K. G., Harmon, J. S. and Sheridan, M. A.(1994). Adipose tissue lipolysis in rainbow trout, Oncorhynchus mykiss, is modulated by phosphorylation of triacylglycerol lipase. Comp. Biochem. Physiol.107B,509-513.

Ou, J., Tu, H., Shan, B., Luk, A., Bose-Boyd, R. A., Bashmakov,Y., Goldstein, J. L. and Brown, M. S. (2001). Unsaturated fatty acids inhibit transcription of the sterol regulatory element-binding protein-1c (SREBP-1c) gene by antagonizing ligand-dependent activation of the LXR. Proc. Natl. Acad. Sci. USA98,6027-6032.

Peet, D. J., Turley, S. D., Ma, W., Janowski, B. A., Lobaccaro,J. M., Hammer, R. E. and Mangelsdorf, D. J. (1998). Cholesterol and bile acid metabolism are impaired in mice lacking the nuclear oxysterol receptor LXR α. Cell93,693-704.

Peters, J. M., Lee, S. S. T., Li, W., Ward, J. M., Gavrilova,O., Everett, C., Reitman, M. L., Hudson, L. D. and Gonzalez, F. J.(2000). Growth, adipose, brain, and skin alterations resulting from targeted disruption of the mouse peroxisome proliferator-activated receptor β(δ). Mol. Cell. Biol.20,5119-5128.

Repa, J. J., Turley, S. D., Lobaccaro, J. M. A., Medina, J., Li,L., Lustig, K., Shan, B., Heyman, R. A., Dietschy, J. M. and Mangelsdorf, D. J. (2000). Regulation of absorption and ABC1-mediated efflux of cholesterol by RXR heterodimers. Science289,1524-1529.

Rosen, E. D., Sarraf, P., Troy, A. E., Bradwin, G., Moore, K.,Milstone, D. S., Spiegelman, B. M. and Mortensen, R. M.(1999). PPARγ is required for the differentiation of adipose tissue in vivo and in vitro.Mol. Cell4,611-617.

Ruyter, B., Andersen, Ø., Dehli, A., Östlund Farrants, A. K., Gjøen, T. and Thomassen, M. S.(1997). Peroxisome proliferator activated receptors in Atlantic salmon (Salmo salar): effects on PPAR transcription and acyl-CoA oxidase activity in hepatocytes by peroxisome proliferators and fatty acids. Biochim. Biophys. Acta1348,331-338.

Saera-Vila, A., Calduch-Giner, J. A., Gómez-Requeni, P.,Médale, F., Kaushik, S. and Pérez-Sánchez, J.(2005). Molecular characterization of gilthead sea bream(Sparus aurata) lipoprotein lipase. Transcriptional regulation by season and nutritional condition in skeletal muscle and fat storage tissues. Comp. Biochem. Physiol.142B,224-232.

Saera-Vila, A., Calduch-Giner, J. A., Navarro, I. and Pérez-Sánchez, J. (2007). Tumour necrosis factor (TNF)α as a regulator of fat tissue mass in the Mediterranean gilthead sea bream (Sparus aurata L.). Comp. Biochem. Physiol. B Biochem. Mol. Biol.146,338-345.

Schmidt, A., Endo, N., Rutledge, S. J., Vogel, R., Shinar, D. and Rodan, G. A. (1992). Identification of a new member of the steroid hormone receptor superfamily that is activated by a peroxisome proliferator and fatty acids. Mol. Endocrinol.6,1634-1641.

Seedorf, U. and Aberle, J. (2007). Emerging roles of PPARδ in metabolism. Biochim. Biophys. Acta1771,1125-1131.

Shearer, K. D. and Swanson, P. (2000). The effect of whole body lipid on early sexual maturation of 1+ age male chinook salmon (Oncorhynchus tshawytscha). Aquaculture190,343-367.

Silverstein, J. T., Shimma, H. and Ogata, H.(1997). Early maturity in amago salmon (Oncorhynchus masu ishikawai): an association with energy storage. Can. J. Fish. Aquat. Sci.54,444-451.

Silverstein, J. T., Shearer, K. D., Dickhoff, W. W. and Plisetskaya, E. M. (1998). Effects of growth and fatness on sexual development of chinook salmon (Oncorhynchus tshawytscha) parr. Can. J. Fish. Aquat. Sci.55,2376-2382.

Sitjà-Bobadilla, A., Mingarro, M., Pujalte, M. J., Garay,E., Alvarez-Pellitero, P. and Pérez-Sánchez, J.(2003). Immunological and pathological status of gilthead sea bream (Sparus aurata L.) under different long-term feeding regimes. Aquaculture220,707-724.

Sitjà-Bobadilla, A., Peña-Llopis, S.,Gómez-Requeni, P., Médale, F., Kaushik, S. and Pérez-Sánchez, J. (2005). Effect of fish meal replacement by plant protein sources on non-specific defence mechanisms and oxidative stress in gilthead sea bream (Sparus aurata). Aquaculture249,387-400.

Skurk, T., berti-Huber, C., Herder, C. and Hauner, H.(2007). Relationship between adipocyte size and adipokine expression and secretion. J. Clin. Endocrinol. Metab.92,1023-1033.

Tebar, F., Soley, M. and Ramírez, I.(1996). The antilipolytic effects of insulin and epidermal growth factor in rat adipocytes are mediated by different mechanisms. Endocrinology137,4181-4188.

Tontonoz, P. and Spiegelman, B. M. (2008). Fat and beyond: the diverse biology of PPARγ. Annu. Rev. Biochem.77,289.

Warne, J. P. (2003). Tumor necrosis factorα: a key regulator of adipose tissue mass. J. Endocrinol.177,351-355.

Wójcicka, G., Jamroz-Wisniewska, A., Horoszewicz, K. and Beltowski, J. (2007). Liver X receptors (LXRs). Part I:structure, function, regulation of activity, and role in lipid metabolism. Postepy Hig. Med. Dosw.61,736-759.

Ye, J. (2008). Regulation of PPARγfunction by TNF-α. Biochem. Biophys. Res. Commun.374,405-408.

Zhang, Y. and Mangelsdorf, D. J. (2002). LuXuRies of lipid homeostasis: the unity of nuclear hormone receptors,transcription regulation, and cholesterol sensing. Mol. Interv.2,78-87.

Zhang, Y., Repa, J. J., Gauthier, K. and Mangelsdorf, D. J.(2001). Regulation of lipoprotein lipase by the oxysterol receptors, LXRα and LXRβ. J. Biol. Chem.276,43018-43024.

Zhao, S. P. and Dong, S. Z. (2008). Effect of tumor necrosis factor α on cholesterol efflux in adipocytes. Clin. Chim. Acta389,67-71.

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