Advertisement

Toxicology and Environmental Health Sciences

, Volume 7, Issue 3, pp 217–223 | Cite as

Cadmium modulates the mRNA expression and activity of glutathione S-transferase in the monogonont Rotifer Brachionus koreanus

  • Bora Yim
  • Hokyun Kim
  • Mi-Young Jung
  • Young-Mi LeeEmail author
Research article

Abstract

Cadmium has adverse effects on aquatic organisms. Here, we measured the ROS level, total GSH contents and total GST activity after exposure to Cd. In addition, the mRNA expression of four GST isoforms was investigated in response to Cd using real-time RT-PCR in the monogonant rotifer, Brachionus koreanus. As results, intracellular ROS level was elevated, total GSH content was declined, and GST activity was significantly elevated in Cd-exposed group, indicating that Cd can induce oxidative stress by producing ROS, and GSH and GST may be involved in cellular protection against Cd-induced toxicity. After exposure to Cd, mRNA expression of Bk-GST isoforms was differently modulated. In particular, Bk-GST-omega mRNA level was highly sensitive to Cd exposure, indicating that this isoform play a key role in protective responses to Cd in this species and would be useful as a molecular biomarker for monitoring of heavy metal toxicity in aquatic environment.

Keywords

Brachionus koreanus Cadmium Glutathione S-transferase Quantitative real-time RT-PCR Rotifer 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Sabolic, I., Herak-Kramberger, C. M. & Brown, D. Subchronic cadmium treatment affects the abundance and arrangement of cytoskeletal proteins in rat renal proximal tubule cells. Toxicology 165, 205–216 (2001).CrossRefPubMedGoogle Scholar
  2. 2.
    Sharma, S. S. & Dietz, K. J. The relationship between metal toxicity and cellular redox imbalance. Trends Plant Sci. 14, 43–50 (2009).CrossRefPubMedGoogle Scholar
  3. 3.
    Sheehan, D., Meade, G., Foley, V. M. & Dowd, C. A. Structure, function and evolution of glutathione transferases: implications for classification of non-mammalian members of an ancient enzyme superfamily. Biochem. J. 360, 1–16 (2001).PubMedCentralCrossRefPubMedGoogle Scholar
  4. 4.
    Valavanidis, A., Vlahogianni, T., Dassenakis, M. & Scoullos, M. Molecular biomarkers of oxidative stress in aquatic organisms in relation to toxic environmental pollutants. Ecotoxicol. Environ. Saf. 64, 178–189 (2006).CrossRefPubMedGoogle Scholar
  5. 5.
    Rhee, J.-S. et al. Molecular cloning and characterization of omega class glutathione S-transferase (GST-O) from the polychaete Neanthes succinea: Biochemical comparison with theta class glutathione S-transferase (GST-T). Comp. Biochem. Physiol. C 146, 471–477 (2007a).Google Scholar
  6. 6.
    Rhee, J.-S. et al. Molecular cloning, expression, biochemical characteristics, and biomarker potential of theta class glutathione S-transferase (GST-T) from the polychaete Neanthes succinea. Aquat. Toxicol. 83, 104–115 (2007b).CrossRefPubMedGoogle Scholar
  7. 7.
    Lee, K. W. et al. Expression of glutathione S-transferase (GST) genes in the marine copepod Tigriopus japonicus exposed to trace metals. Aquat. Toxicol. 89, 158–166 (2008).CrossRefPubMedGoogle Scholar
  8. 8.
    Won, E.-J. et al. Response of glutathione S-tranferase (GST) genes to cadmium exposure in the marine pollution indicator worm, Perinereis nuntia. Comp. Biochem. Physiol. C 154, 82–92 (2011).Google Scholar
  9. 9.
    Dahms, H.-U., Hagiwara, A. & Lee, J.-S. Ecotoxicology, ecophysiology, and mechanistic studies with rotifers. Aquat. Toxicol. 101, 1–12 (2011).CrossRefPubMedGoogle Scholar
  10. 10.
    Han, J. et al. Effect of copper exposure on GST activity and on the expression of four GSTs under oxidative stress condition in the monogonont rotifer Brachionus koreanus. Comp. Biochem. Physiol. Part C 158, 90–100 (2013).Google Scholar
  11. 11.
    Chelomin, V. P., Zakhartsev, M. V., Kurilenko, A. V. & Belcheva, N. N. An in vitro study of the effect of reactive oxygen species on subcellular distribution of deposited cadmium in digestive gland of mussel Crenomytilus grayanus. Aquat. Toxicol. 73, 181–189 (2005).CrossRefPubMedGoogle Scholar
  12. 12.
    Bocchetti, R., Fattorini, D., Gambi, M. C. & Regoli, F. Trace metal concentrations and susceptibility to oxidative stress in the Polychaete Sabella spallanzanii (Gmelin) (Sabellidae): potential role of antioxidants in revealing stressful environmental conditions in the mediterranean. Arch. Environ. Contam. Toxicol. 46, 353–361 (2004).CrossRefPubMedGoogle Scholar
  13. 13.
    Rico, D. et al. Heavy metals generate reactive oxygen species in terrestrial and aquatic ciliated protozoa. Comp. Biochem. Physiol. C 149, 90–96 (2009).Google Scholar
  14. 14.
    Kim, S. H., Kim, S. J., Lee, J. S. & Lee, Y. M. Acute effects of heavy metals on the expression of glutathione-related antioxidant genes in the marine ciliate Euplotes crassus. Mar. Pollut. Bull. 85, 455–462 (2014).CrossRefPubMedGoogle Scholar
  15. 15.
    Hassoun, E. A. & Stohs, S. J. Cadmium-induced production of superoxide anion and nitric oxide, DNA single strand breaks and lactate dehydrogenase leakage in J774A1 cell cultures. Toxicology 112, 219–226 (1996).CrossRefPubMedGoogle Scholar
  16. 16.
    Pulido, M. D. & Parrish, A. R. Metal-induced apoptosis: mechanisms. Mut. Res. 533, 227–241 (2003).CrossRefGoogle Scholar
  17. 17.
    Hultberg, B., Andersson, A. & Isaksson, A. Interaction of metals and thiols in cell damage and lutathione distribution: potentiation of mercury toxicity by dithiothreitol. Toxicology 156, 93–100 (2001).CrossRefPubMedGoogle Scholar
  18. 18.
    Flora, S. J., Mittal, M. & Mehta, A. Heavy metal induced oxidative stress & its possible reversal by chelation therapy. Indian J. Med. Res. 128, 501–523 (2008).PubMedGoogle Scholar
  19. 19.
    Shakoori, F. R. et al. Response of glutathione level in a protozoan ciliate, Stylonychia mytilus, to increasing uptake of and tolerance to nickel and zinc in the medium, Pakistan. J. Zool. 43, 569–574 (2011).Google Scholar
  20. 20.
    Firat, O., Cogun, H. Y., Aslanyavrusu, S. & Kargin, F. Antioxidant responses and metal accumulation in tissues of Nile tilapia Oreochromis niloticus under Zn, Cd and Zn+Cd exposures. J. Appl. Toxicol. 29, 295–301 (2009).CrossRefPubMedGoogle Scholar
  21. 21.
    Souid, G., Souayed, N., Yaktiti, F. & Maaroufi, K. Effect of acute cadmium exposure on metal accumulation and oxidative stress biomarkers of Sparus aurata. Ecotoxicol. Environ. Saf. 89, 1–7 (2013).CrossRefPubMedGoogle Scholar
  22. 22.
    Ivania, A. V., Cherkasov, A. S. & Sokolova, I. M. Effects of cadmium on cellular protein and glutathione synthesis and expression of stress proteins in eastern oysters, Crassostrea virginica Gmelin. J. Exp. Biol. 211, 577–586 (2008).CrossRefGoogle Scholar
  23. 23.
    Wang, L. et al. Effects of cadmium on glutathione synthesis in hepatopancreas of freshwater crab, Sinopotamon yangtsekiense. Chemosphere 74, 51–56 (2008).CrossRefPubMedGoogle Scholar
  24. 24.
    Zirong, X. & Shijun, B. Effect of waterborne Cd exposure on glutathione metabolism in Nile tilapia (Oreochromis niloticus) liver. Ecotoxicol. Environ. Saf. 67, 89–94 (2007).CrossRefPubMedGoogle Scholar
  25. 25.
    Saint-Denis, M., Narbonne, J. F., Arnaud, C. & Ribera, D. Biochemical responses of the earthworm Eisenia fetida Andrei exposed to contaminated artificial soil: effects of lead acetate. Soil Biol. Biochem. 33, 395–404 (2001).CrossRefGoogle Scholar
  26. 26.
    Cao, L. et al. Tissue-specific accumulation of cadmium and its effects on antioxidative responses in Japanese flounder juveniles. Environ. Toxicol. Pharmacol. 33, 16–25 (2012).CrossRefPubMedGoogle Scholar
  27. 27.
    Lee, J. S. & Raisuddin, S. in Interdisciplinary Studies on Environmental Chemistry: Biological Responses to Chemical Pollutants (eds., Murakami, Y. et al.) 95–105 (TERRAPUB, Tokyo, 2008).Google Scholar
  28. 28.
    Won, E.-J. et al. Susceptibility to oxidative stress and modulated expression of antioxidant genes in the copper-exposed polychaete Perinereis nuntia. Comp. Biochem. Physiol. C 155, 344–351 (2012).Google Scholar
  29. 29.
    Board, P. G. et al. Identification, characterization, and crystal structure of the omega class glutathione transferases. J. Biol. Chem. 275, 24798 (2000).CrossRefPubMedGoogle Scholar
  30. 30.
    Jung, M. Y. & Lee, Y. M. Expression profiles of heat shock protein gene families in the Monogonont Rotifer Brachionus koreanus-exposed to copper and cadmium. Toxicol. Environ. Health. Sci. 4, 235–242 (2012).CrossRefGoogle Scholar
  31. 31.
    Small, B. C. et al. Stability of reference genes for realtime PCR analyses in channel catfish (Ictalurus punctatus) tissues under varying physiological conditions. Comp. Biochem. Physiol. B 151, 296–304 (2008).CrossRefPubMedGoogle Scholar
  32. 32.
    Livak, K. J. & Schmittgen, T. D. Analysis of relative gene expression data using real time quantitative PCR and the 2-ΔΔCt method. Methods 25, 402–408 (2001).CrossRefPubMedGoogle Scholar
  33. 33.
    Bradford, M. M. A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein-dye-binding. Anal. Biochem. 7, 248–254 (1976).CrossRefGoogle Scholar

Copyright information

© Korean Society of Environmental Risk Assessment and Health Science and Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • Bora Yim
    • 1
  • Hokyun Kim
    • 1
  • Mi-Young Jung
    • 1
  • Young-Mi Lee
    • 1
    Email author
  1. 1.Department of Life Science, College of Natural SciencesSangmyung UniversitySeoulKorea

Personalised recommendations