Skip to main content
SpringerLink
Log in

Effects of Copper and Cadmium on Lipogenic Metabolism and Metal Element Composition in the Javelin Goby (Synechogobius hasta) After Single and Combined Exposure

  • Published:
Archives of Environmental Contamination and Toxicology Aims and scope Submit manuscript

Abstract

The present study was performed to determine the effects of single and combined exposure of copper (Cu) and cadmium (Cd) on lipogenic metabolism and metal element composition of javelin goby Synechogobius hasta. Two hundred and forty uniform-sized S. hasta (initial mean weight 20.3 ± 0.3 g [mean ± SEM throughout]; initial body length 15.2 ± 0.2 cm) were randomly assigned to 12 fiberglass tanks (water volume 300 l) with 20 fish/tank. The fish were exposed to four treatments with different Cu and Cd concentration for 30 days, respectively: (1) control (without extra Cu and Cd addition), (2) Cu (nominal concentrations of 77 μg/l), (3) Cd (79 μg/l), and (4) Cu + Cd (Cu/Cd coexposure). Growth decreased, but hepatosomatic index, viscerosomatic index, and lipid content increased after metal exposure. Staining with Oil Red O and haematoxylin and eosin showed extensive alterations in liver of metals-exposed fish. Metal exposure influenced the accumulation of metal elements (Cu, Cd, iron, zinc, and manganese) in several tissues (muscle, gill, intestine, liver, and spleen) and increased hepatic 6-phosphogluconate dehydrogenase, glucose-6-phosphate dehydrogenase, malic enzyme, isocitrate dehydrogenase, and fatty acid synthase activities. The results of the present study indicated that the changes in lipogenic metabolism and metal element compositions of fish under Cu and Cd coexposure could not be explained by synergism of the addition of the effects observed in singly Cu- or Cd-exposed fish. To our knowledge the present study, for the first time, investigated the effects of Cu and Cd coexposure on hepatic lipogenic metabolism and metal element compositions in a wide range of tissues and organs in fish, which provided new evidence for Cu and Cd interactions in fish.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Abdel-Tawwab M, Mousa MAA, Ahmad MH, Sakr SFM (2007) The use of calcium pre-exposure as a protective agent against environmental copper toxicity for juvenile Nile tilapia, Oreochromis niloticus (L.). Aquaculture 264:236–246

    Article  CAS  Google Scholar 

  • Arredondo M, Muñoz P, Mura CV, Núñez MT (2003) DMT1, a physiologically relevant apical Cu1+ transporter of intestinal cells. Am J Physiol Cell Physiol 84:C1525–C1530

    Article  Google Scholar 

  • Association of Official Analytical Chemists (1995) Official methods of analysts, 16th edn. AOAC, Arlington

    Google Scholar 

  • Barroso JB, Peragón J, García-Salguero L, de la Higuera M, Lupiáñez JA (1999) Variations in the kinetic behaviour of the NADPH-production systems in different tissues of the trout when fed on an amino-acid-based diet at different frequencies. Int J Biochem Cell Biol 31:277–290

    Article  CAS  Google Scholar 

  • Berglund M, Akesson A, Nermell B, Vahter M (1994) Intestinal absorption of dietary cadmium in women depends on body iron stores and fiber intake. Environ Health Perspect 102:1058–1066

    Article  CAS  Google Scholar 

  • Bernt E, Bergmeyer HU (1974) Isocitrate dehydrogenase. In: Bergmeyer HU (ed) Methods of enzymatic analysis, vol 2. Academic Press, New York, pp 624–627

    Chapter  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  Google Scholar 

  • Brungs A, Leonard EN, McKim JM (1973) Acute and long-term accumulation of copper by the brown bullhead Ictalurus nebulosus. J Fish Res Bd Can 30:583–586

    Article  CAS  Google Scholar 

  • Buckley JT, Roch M, McCarter JA, Rendell CA, Matheson AT (1982) Chronic exposure of Coho salmon to sublethal concentrations of copper–1. Effect on growth, on accumulation and distribution of copper, and on copper tolerance. Comp Biochem Physiol C 72:15–19

    Article  CAS  Google Scholar 

  • Campbell H, Handy R, Sims D (2002) Increased metabolic cost of swimming and consequent alterations to circadian activity in rainbow trout (Oncorhynchus mykiss) exposed to dietary copper. Can J Fish Aquat Sci 59:768–777

    Article  CAS  Google Scholar 

  • Chakrabarty K, Leveille GA (1969) Acetyl CoA carboxylase and fatty acid synthetase activities in liver and adipose tissue of meal-fed rats. Exp Biol Med 131:1051–1054

    Article  CAS  Google Scholar 

  • Chang HC, Seidman I, Teebor G, Lane MD (1967) Liver acetyl CoA carboxylase and fatty acid synthetase: relative activities in the normal state and in hereditary obesity. Biochem Biophys Res Commun 28:682–686

    Article  CAS  Google Scholar 

  • Chen QL, Luo Z, Zheng JL, Li XD, Liu CX, Zhao YH et al (2012) Protective effects of calcium on copper toxicity in Pelteobagrus fulvidraco: copper accumulation, enzymatic activities, histology. Ecotoxicol Environ Saf 76:126–134

    Article  CAS  Google Scholar 

  • Chen QL, Luo Z, Liu X, Song YF, Liu CX, Zheng JL et al (2013) Effects of waterborne chronic copper exposure on hepatic lipid metabolism and metal-element composition in Synechogobius hasta. Arch Environ Contam Toxicol 64:301–315

    Article  CAS  Google Scholar 

  • Chmielnicka J, Cherian MG (1986) Environmental exposure to cadmium and factors affecting trace-element metabolism and metal toxicity. Biol Trace Element Res 10:243–262

    Article  CAS  Google Scholar 

  • Cowey CB, Walton MJ (1989) Intermediary metabolism. In: Halver JE (ed) Fish nutrition, 1st edn. Academic Press, New York, pp 259–329

    Google Scholar 

  • Dallinger R, Egg M, Köck G, Hofer R (1997) The role of metallothionein in cadmium accumulation of Arctic char (Salvelinus alpinus) from high alpine lakes. Aquat Toxicol 38:47–66

    Article  CAS  Google Scholar 

  • Dang F, Wang WX (2009) Assessment of tissue-specific accumulation and effects of cadmium in a marine fish fed contaminated commercially produced diet. Aquat Toxicol 95:248–255

    Article  CAS  Google Scholar 

  • Dang F, Zhong H, Wang WX (2009) Copper uptake kinetics and regulation in a marine fish after waterborne copper acclimation. Aquat Toxicol 94:238–244

    Article  CAS  Google Scholar 

  • Dautremepuits C, Paris-Palaciosa S, Betoullea S, Vernet G (2004) Modulation in hepatic and head kidney parameters of carp (Cyprinus carpio L.) induced by copper and chitosan. Comp Biochem Physiol C 137:325–333

    Google Scholar 

  • De Boeck G, Vlaeminck A, Blust R (1997) Effects of sublethal copper exposure on copper accumulation, food consumption, growth, energy stores, and nucleic acid content in common carp. Arch Environ Contam Toxicol 33:415–422

    Article  Google Scholar 

  • Eisler R, Gardner GR (1979) Acute toxicology to an estuarine teleost of mixtures of cadmium, copper and zinc salts. J Fish Biol 5:131–142

    Article  Google Scholar 

  • Figueiredo-Fernandes A, Ferreira-Cardoso JV, Garcia-Santos S, Monteiro SM, Carrola J, Matos P (2007) Histopathological changes in liver and gill epithelium of Niletilapia, Oreochromis niloticus, exposed to waterborne copper. Pesqui Vet Bras 27:103–109

    Article  Google Scholar 

  • Gambling L, Danzeisen R, Fosset C, Andersen HS, Dunford S, Srai SKS et al (2003) Iron and copper interactions in development and the effect on pregnancy outcome. J Nutr 133:1554S–1556S

    CAS  Google Scholar 

  • Gill TS, Bianchi CP, Epple A (1992) Trace metal (Cu and Zn) adaptation of organ systems of the American eel, Anguilla rostrata, to external concentrations of cadmium. Comp Biochem Physiol C 102:361–371

    Article  CAS  Google Scholar 

  • Gunshin H, Mackenzie B, Berger UV, Gunshin Y, Romero MF, Boron WF et al (1997) Cloning and characterization of a mammalian proton-coupled metal-ion transporter. Nature 388:482–488

    Article  CAS  Google Scholar 

  • Hollis L, Hogstrand C, Wood C (2001) Tissue-specific cadmium accumulation, metallothionein induction, and tissue zinc and copper levels during chronic sublethal cadmium exposure in juvenile rainbow trout. Arch Environ Contam Toxicol 41:468–474

    Article  CAS  Google Scholar 

  • Kraemer LD, Campbell PGC, Hare L (2005) Dynamics of Cd, Cu and Zn accumulation in organs and sub-cellular fractions in field transplanted juvenile yellow perch (Perca flavescens). Environ Pollut 138:324–337

    Article  CAS  Google Scholar 

  • Lanno RP, Slinger SJ, Hilton JW (1985) Maximum tolerable and toxicity levels of dietary copper in rainbow trout (Salmo gairdneri Richardson). Aquaculture 49:257–268

    Article  CAS  Google Scholar 

  • Liu XJ, Luo Z, Xiong B, Liu X, Zhao Y, Hu G et al (2010) Effect of waterborne copper exposure on growth, hepatic enzymatic activities and histology in Synechogobius hasta. Ecotoxicol Environ Saf 73:1286–1291

    Article  CAS  Google Scholar 

  • Liu XJ, Luo Z, Li CH, Xiong BX, Zhao YH, Li XD (2011) Antioxidant responses, hepatic intermediary metabolism, histology and ultrastructure in Synechogobius hasta exposed to waterborne cadmium. Ecotoxicol Environ Saf 74:1156–1163

    Article  CAS  Google Scholar 

  • Long A, Wang WX (2005) Metallothionein induction and bioaccumulation kinetics of Cd and Ag in the marine fish Terapon jarbua challenged with dietary or waterborne Ag and Cu. Mar Ecol Prog Ser 291:215–226

    Article  CAS  Google Scholar 

  • Lundebye AK, Berntssen M, Bonga S, Maage A (1999) Biochemical and physiological responses in Atlantic salmon (Salmo salar) following dietary exposure to copper and cadmium. Mar Pollut Bull 39:137–144

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Marr J, Lipton J, Cacela D, Hansen J, Bergman H, Meyer J, Hogstrand C (1996) Relationship between copper exposure duration, tissue copper concentration, and rainbow trout growth. Aquat Toxicol 36:17–30

    Article  CAS  Google Scholar 

  • Martinez-Finley EJ, Chakraborty S, Fretham SJB, Aschner M (2012) Cellular transport and homeostasis of essential and nonessential metals. Metallomics 4:593–605

    Article  CAS  Google Scholar 

  • McGeer JC, Szebedinszky C, McDonald DG, Wood CM (2000) Effects of chronic sublethal exposure to waterborne Cu, Cd or Zn in rainbow trout. 1: iono-regulatory disturbance and metabolic costs. Aquat Toxicol 50:231–243

    Article  CAS  Google Scholar 

  • Meshitsuka S, Nose T, Ishizawa M (1983) Specific effects of copper ions on the uptake and release of cadmium by KB cells. Yonago Acta Medica 26:87–98

    CAS  Google Scholar 

  • Meshitsuka S, Ishizawa M, Nose T (1987) Uptake and toxic effects of heavy metal ions: interactions among cadmium, copper and zinc in cultured cells. Experientia 43:151–156

    Article  CAS  Google Scholar 

  • Pelgrom S, Lamers L, Lock R, Balm P, Bonga S (1995) Interactions between copper and cadmium modify metal organ distribution in mature tilapia, (Oreochromis mossambicus). Environ Pollut 90:415–423

    Article  CAS  Google Scholar 

  • Reid S, McDonald D (1988) Effects of cadmium, copper, and low pH on ion fluxes in the rainbow trout, Salmo gairdneri. Can J Fish Aquat Sci 45:244–253

    Article  CAS  Google Scholar 

  • Schümann K, Friebel P, Schmolke G, Elsenhans B (1996) State of iron repletion and cadmium tissue accumulation as a function of growth in young rats after oral cadmium exposure. Arch Environ Contam Toxicol 31:483–487

    Article  Google Scholar 

  • Song YF, Luo Z, Chen QL, Liu X, Liu CX, Zheng JL (2013) Protective effects of calcium pre-exposure against waterborne cadmium toxicity in Synechogobius hasta. Arch Environ Contam Toxicol 65:105–121

    Article  CAS  Google Scholar 

  • Spisni E, Tugnoli M, Ponticelli A, Mordenti T, Tomasi V (1998) Hepatic steatosis in artificially fed marine teleosts. J Fish Dis 21:177–184

    Article  CAS  Google Scholar 

  • Taylor LN, McGeer JC, Wood CM, McDonald DG (2000) Physiological effects of chronic copper exposure to rainbow trout (Oncorhynchus mykiss) in hard and soft water: evaluation of chronic indicators. Environ Toxicol Chem 19:2298–2308

    Article  CAS  Google Scholar 

  • Van Dyk JC, Pieterse GM, van Vuren JHJ (2008) Histological changes in the liver of Oreochromis mossambicus (Cichlidae) after exposure to cadmium and zinc. Ecotoxicol Environ Saf 66:432–440

    Google Scholar 

  • Velmurugan B, Selvanayagam M, Cengiz EI, Unlu E (2007) Histopathology of lambda-cyhalothrin on tissues (gill, kidney, liver and intestine) of Cirrhinus mrigala. Environ Toxicol Pharmacol 24:286–291

    Article  CAS  Google Scholar 

  • Wang JT, Liu YJ, Tian LX, Mai KS, Du ZY, Wang Y et al (2005) Effect of dietary lipid level on growth performance, lipid deposition, hepatic lipogenesis in juvenile cobia (Rachycentron canadum). Aquaculture 249:439–447

    Article  CAS  Google Scholar 

  • Watanabe T, Kiron V, Satoh S (1997) Trace minerals in fish nutrition. Aquaculture 151:185–207

    Article  CAS  Google Scholar 

  • Westernhagen HV, Dethlefsen V, Rosenthal H (1979) Combined effects of cadmium, copper and lead on developing herring eggs and larvae. Helgolander Wiss Meeresunters 32:257–278

    Article  Google Scholar 

  • Wise EM, Ball EG (1964) Malic enzyme and lipogenesis. Proc Natl Acad Sci USA 52:1255–1263

    Article  CAS  Google Scholar 

  • Woods AE, Ellis RC (1994) Laboratory histopathology: a complete reference. Churchill Livingstone, Churchill

    Google Scholar 

  • Zhan YJ (2005) The status quo of heavy metal pollution in Bohai sea and the abecedarian estimate of the effect of heavy metals on the growth of typical phytoplankton [in Chinese with English abstract]. Doctoral dissertation. Ocean University of China, Qingdao

  • Zhou H, Cadigan KM, Thiele DJ (2003) A copper regulated transporter required for copper acquisition, pigmentation, and specific stages of development in Drosophila melanogaster. J Biol Chem 278:48210–48218

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We are grateful to the staff of Panjin Guanghe Fishery Co. Ltd for providing the experimental base and for logistic support during the study. This work was supported by National Natural Science Fund of China (Grants Nos. 30800850, 31072226, and 31372547) and by the Fundamental Research Funds for the Central Universities (Grants Nos. 2011PY115 and 2013PY073).

Author information

Authors and Affiliations

  1. Key Laboratory of Freshwater Animal Breeding, Ministry of Agriculture, Fishery College, Huazhong Agricultural University, Wuhan, 430070, China

    Yu-Feng Song, Zhi Luo, Ya-Xiong Pan, Chao Huang & Qi-Liang Chen

  2. Freshwater Aquaculture Collaborative Innovative Center of Hubei Province, Wuhan, 430070, China

    Yu-Feng Song, Zhi Luo, Ya-Xiong Pan, Chao Huang & Qi-Liang Chen

  3. Postgraduate Research Base, Panjin Guanghe Fishery Co. Ltd, Panjin, 124200, China

    Xu Liu

Authors
  1. Yu-Feng Song
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zhi Luo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ya-Xiong Pan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xu Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Chao Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Qi-Liang Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zhi Luo.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Song, YF., Luo, Z., Pan, YX. et al. Effects of Copper and Cadmium on Lipogenic Metabolism and Metal Element Composition in the Javelin Goby (Synechogobius hasta) After Single and Combined Exposure. Arch Environ Contam Toxicol 67, 167–180 (2014). https://doi.org/10.1007/s00244-014-0011-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00244-014-0011-0

Keywords

Search

Navigation