Abstract
The aim of this study was to determine the potential mechanisms of exposure to waterborne zinc (Zn) on lipid metabolism in three extrahepatic tissues (ovary, muscle and mesenteric adipose tissue) of female yellow catfish Pelteobagrus fulvidraco. Female yellow catfish were chronically exposed to Zn (0.05, 0.35 or 0.86 mg Zn/l; duration of treatment 8 weeks) or acutely exposed to a high level of Zn (4.71 mg Zn/l for 96 h). Following the respective treatment, lipid deposition and mRNA levels of 11 genes (CPT IA, CPT IB, PPARα, PPARγ, SREBP-1, G6PD, 6PGD, FAS, ACCa, ACCb and LPL) involved in lipid metabolism were determined. Waterborne Zn exposure significantly reduced growth performance and lipid content in muscle but had no significant effect on lipid content in ovary and mesenteric adipose tissue. The change in the levels of the mRNA genes under study was Zn concentration-dependent and tissue-dependent. Pearson correlations between the mRNA levels of three transcriptional factors and enzymes in these tissues revealed that variations in gene expression as a result of the different Zn treatments underlay the patterns of lipid metabolism, which in turn affected fat storage and mobilization. To our knowledge, this is the first study to demonstrate the effect of waterborne Zn exposure on lipid metabolism in extrahepatic tissues at the molecular level. These results therefore contribute to our understanding of Zn-induced toxicity in fish.
Similar content being viewed by others
References
Abu-Elheiga L, Almarza-Ortega DB, Baldini A, Wakil SJ (1997) Human acetyl-CoA carboxylase 2 molecular cloning, characterization, chromosomal mapping, and evidence for two isoforms. J Biol Chem 272:10669–10677
Aksnes A, Gjerde B, Roald SO (1986) Biological, chemical and organoleptic changes during maturation of farmed Atlantic salmon, Salmo salar. Aquaculture 53:7–20
Albalat A, Saera-Vila A, Capilla E, Gutierrez J, Perez-Sanchez J, Navarro I (2007) Insulin regulation of lipoprotein lipase (LPL) activity and expression in gilthead sea bream (Sparus aurata). Comp Biochem Physiol 148B:151–159
Amemiya-Kudo M, Shimano H, Hasty AH, Yahagi N, Yoshikawa T, Matsuzaka T, Okazaki H, Tamura Y, Iizuka Y, Ohashi K (2002) Transcriptional activities of nuclear SREBP-1a,-1c, and-2 to different target promoters of lipogenic and cholesterogenic genes. J Lipid Res 43:1220–1235
Bonnefont JP, Demaugre F, Prip-Buus C, Saudubray JM, Brivet M, Abadi N, Thuillier L (1999) Carnitine palmitoyltransferase deficiencies. Mol Genet Metab 68:424–440
Brandt JM, Djouadi F, Kelly DP (1998) Fatty acids activate transcription of the muscle carnitine palmitoyltransferase I gene in cardiac myocytes via the peroxisome proliferator-activated receptor α. J Biol Chem 273:23786–23792
Brungs WA (1969) Chronic toxicity of zinc to the fathead minnow, Pimephales promelas Rafinesque. Trans Am Fish Soc 98:272–279
Cui Y, Miyoshi K, Claudio E, Siebenlist UK, Gonzalez FJ, Flaws J, Wagner K-U, Hennighausen L (2002) Loss of the peroxisome proliferation-activated receptor gamma (PPARγ) does not affect mammary development and propensity for tumor formation but leads to reduced fertility. J Biol Chem 277:17830–17835
Desvergne B, Wahli W (1999) Peroxisome proliferator-activated receptors: nuclear control of metabolism. Endocr Rev 20:649–688
Giardina A, Larson SF, Wisner B, Wheeler J, Chao M (2009) Long-term and acute effects of zinc contamination of a stream on fish mortality and physiology. Environ Toxicol Chem 28:287–295
Goldberg IJ (1996) Lipoprotein lipase and lipolysis: central roles in lipoprotein metabolism and atherogenesis. J Lipid Res 37:693–707
Heath AG (1987) Water pollution and fish physiology. CRC Press, Baton Rouge
Hoar W (1988) The physiology of smolting salmonids. Fish Physiol 11:275–323
Horton JD, Shimomura I, Ikemoto S, Bashmakov Y, Hammer RE (2003) Overexpression of sterol regulatory element-binding protein-1a in mouse adipose tissue produces adipocyte hypertrophy, increased fatty acid secretion, and fatty liver. J Biol Chem 278:36652–36660
Ibanez AJ, Peinado-Onsurbe J, Sanchez E, Cerda-Reverter JM, Prat F (2008) Lipoprotein lipase (LPL) is highly expressed and active in the ovary of European sea bass (Dicentrarchus labrax L.), during gonadal development. Comp Biochem Physiol 150A:347–354
Kerner J, Hoppel C (2000) Fatty acid import into mitochondria. Biochim Biophys Acta 1486:1–17
Levesque H, Moon T, Campbell P, Hontela A (2002) Seasonal variation in carbohydrate and lipid metabolism of yellow perch (Perca flavescens) chronically exposed to metals in the field. Aquat Toxicol 60:257–267
Luo Z, Li X, Bai H, Gong S (2008) Effects of dietary fatty acid composition on muscle composition and hepatic fatty acid profile in juvenile Synechogobius hasta. J Appl Ichthyol 24:116–119
Luo Z, Tan X-Y, Zheng J-L, Chen Q-L, Liu C-X (2011) Quantitative dietary zinc requirement of juvenile yellow catfish Pelteobagrus fulvidraco, and effects on hepatic intermediary metabolism and antioxidant responses. Aquaculture 319:150–155
Ma J, Zhang T, Zhuang P, Yan S, Zhang L, Tian M, Gao L (2011) The role of lipase in blood lipoprotein metabolism and accumulation of lipids in oocytes of the Siberian sturgeon Acipenser baerii during maturation. J Appl Ichthyol 27:246–250
Mandrup S, Lane MD (1997) Regulating adipogenesis. J Biol Chem 272:5367–5370
McGarry JD, Leatherman GF, Foster DW (1978) Carnitine palmitoyltransferase I. The site of inhibition of hepatic fatty acid oxidation by malonyl-CoA. J Biol Chem 253:4128–4136
Munkittrick K, Dixon D (1988) Growth, fecundity, and energy stores of white sucker (Catostomus commersoni) from lakes containing elevated levels of copper and zinc. Can J Fish Aquat Sci 45:1355–1365
Napal L, Marrero PF, Haro D (2005) An intronic peroxisome proliferator-activated receptor-binding sequence mediates fatty acid induction of the human carnitine palmitoyltransferase 1A. J Mol Biol 354:751–759
Nilsson-Ehle P, Garfinkel AS, Schotz MC (1980) Lipolytic enzymes and plasma lipoprotein metabolism. Annu Rev Biochem 49:667–693
Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45
Reddy JK, Hashimoto T (2001) Peroxisomal β-oxidation and peroxisome proliferator-activated receptor α: an adaptive metabolic system. Annu Rev Nutr 21:193–230
Regost C, Arzel J, Cardinal M, Robin J, Laroche M, Kaushik S (2001) Dietary lipid level, hepatic lipogenesis and flesh quality in turbot (Psetta maxima). Aquaculture 193:291–309
Rho HK, Park J, Suh JH, Kim JB (2005) Transcriptional regulation of mouse 6-phosphogluconate dehydrogenase by ADD1/SREBP1c. Biochem Biophys Res Commun 332:288–296
Rosen ED, Spiegelman BM (2006) Adipocytes as regulators of energy balance and glucose homeostasis. Nature 444:847–853
Sambasiva Rao M, Reddy JK (2004) PPARα in the pathogenesis of fatty liver disease. Hepatology 40:783–786
Sheridan MA, Kao YH (1998) Regulation of metamorphosis-associated changes in the lipid metabolism of selected vertebrates. Am Zool 38:350–368
Song S, Attia RR, Connaughton S, Niesen MI, Ness GC, Elam MB, Hori RT, Cook GA, Park EA (2010) Peroxisome proliferator activated receptorα (PPARα) and PPAR gamma coactivator (PGC-1α) induce carnitine palmitoyltransferase IA (CPT-1A) via independent gene elements. Mol Cell Endocrinol 325:54–63
Spiegelman B, Hu E, Kim J, Brun R (1997) PPARγ and the control of adipogenesis. Biochimie 79:111–112
Tan XY, Luo Z, Liu X, Xie CX (2011) Dietary copper requirement of juvenile yellow catfish Pelteobagrus fulvidraco. Aquacult Nutr 17:170–176
Tyler C, Lubberink K (1996) Identification of four ovarian receptor proteins that bind vitellogenin but not other homologous plasma lipoproteins in the rainbow trout, Oncorhynchus mykiss. J Comp Physiol 166B:11–20
Uviovo E, Beatty D (1979) Effects of chronic exposure to zinc on reproduction in the guppy (Poecilia reticulata). Bull Environ Contam Toxicol 23:650–657
van Dyk JC, Pieterse GM, van Vuren JH (2007) Histological changes in the liver of Oreochromis mossambicus (Cichlidae) after exposure to cadmium and zinc. Ecotoxicol Environ Saf 66:432–440
Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3(7)RESEARCH0034
Watanabe T, Kiron V (1994) Prospects in larval fish dietetics. Aquaculture 124:223–251
Wiegand MD (1996) Composition, accumulation and utilization of yolk lipids in teleost fish. Rev Fish Biol Fish 6:259–286
Yamasaki M, Ikeda A, Oji M, Tanaka Y, Hirao A, Kasai M, Iwata T, Tachibana H, Yamada K (2003) Modulation of body fat and serum leptin levels by dietary conjugated linoleic acid in Sprague–Dawley rats fed various fat-level diets. Nutrition 19:30–35
Zhang H, Yang Z, Shen Y, Tong L (2003) Crystal structure of the carboxyltransferase domain of acetyl-coenzyme A carboxylase. Science 299:2064–2067
Zhao Y, Gul Y, Li S, Wang W (2011) Cloning, identification and accurate normalization expression analysis of PPARα gene by GeNorm in Megalobrama amblycephala. Fish Shellfish Immunol 31:462–468
Zheng JL, Luo Z, Chen QL, Liu CX, Zhao YH, Gong Y (2011) Effect of waterborne zinc exposure on metal accumulation, enzymatic activities and histology of Synechogobius hasta. Ecotoxicol Environ Saf 74:1864–1873
Zheng JL, Luo Z, Liu CX, Chen QL, Tan XY, Zhu QL, Gong Y (2013a) Differential effects of acute and chronic zinc (Zn) exposure on hepatic lipid deposition and metabolism in yellow catfish Pelteobagrus fulvidraco. Aquat Toxicol 2013(132):173–181
Zheng JL, Luo Z, Zhu QL, Chen QL, Gong Y (2013b) Molecular characterization, tissue distribution and kinetic analysis of carnitine palmitoyltransferase I in juvenile yellow catfish Pelteobagrus fulvidraco. Genomics 101:195–203
Zheng JL, Luo Z, Liu CX, Chen QL, Zhu QL, Hu W, Gong Y (2013c) Differential effects of the chronic and acute zinc exposure on carnitine composition, kinetics of carnitine palmitoyltransferases I (CPT I) and mRNA levels of CPT I isoforms in yellow catfish Pelteobagrus fulvidraco. Chemosphere 92:616–625
Acknowledgments
This work was supported by the Fundamental Research Funds for the Central Universities (Grant Nos. 2009PY007, 2011PY115, 2013PY073), by the Postgraduates Innovation Research Project of Huazhong Agricultural University (Grant No. 2009sc018) and partly by the National Natural Science Foundation of China (Grant No. 31372547).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Zheng, JL., Luo, Z., Zhu, QL. et al. Differential effects of acute and chronic zinc exposure on lipid metabolism in three extrahepatic tissues of juvenile yellow catfish Pelteobagrus fulvidraco . Fish Physiol Biochem 40, 1349–1359 (2014). https://doi.org/10.1007/s10695-014-9929-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10695-014-9929-4