Skip to main content
SpringerLink
Log in

Effects of heavy metals on transcription and enzyme activity of Na+/K+-ATPase in the monogonont rotifer, Brachionus koreanus

  • Research Article
  • Published:
Toxicology and Environmental Health Sciences Aims and scope Submit manuscript

Abstract

Heavy metals can lead to osmotic stress by disrupting the regulation of sodium ion in aquatic organisms. In this study, gene expression patterns and enzymatic activities of Na+/K+-ATPase in the monogonont rotifer, Brachionus koreanus were measured after exposure to different Cd (7.5, 15, and 30 mg/L), and Pb (0.1, 0.5, and 1.0 mg/L), respectively. As results, a significant increase in Bk Na+/K+-ATPase activity was observed after exposure to Cd and Pb in a concentration-dependent manner. Bk Na +/K +-ATPase mRNA level was significantly upregulated in the Cd-exposed group, whereas its level was reduced in the Pb-exposed group. These findings indicate that heavy metals could induce osmotic stress in B. koreanus, and Na+/K+-ATPase may be involved in cellular ho-meostasis in response to heavy metal exposure. This study is helpful for the understanding of the molecular mode of action of B. koreanus in response to heavy metals.

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

Similar content being viewed by others

References

  1. Palmgren, M. G. & Axelsen, K. B. Evolution of P-type ATPases. Biochim. Biophys. Acta. 1365, 37–45 (1998).

    Article  CAS  PubMed  Google Scholar 

  2. Saez, A. G., Lozano, E. & Zaldivar-Riveron, A. Evolutionary history of Na,K-ATPases and their osmoregulatory role. Genetica 136, 479–490 (2009).

    Article  CAS  PubMed  Google Scholar 

  3. 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).

    Article  CAS  PubMed  Google Scholar 

  4. Fairbrother, A., Wenstel, R., Sappington, K. & Wood, W. Framework for Metals Risk Assessment. Ecotoxicol. Environ. Saf. 68, 145–227 (2007).

    Article  CAS  PubMed  Google Scholar 

  5. Mosleh, Y. Y., Paris-Palacios, S. & Biagianti-Risbourg, S. Metallothioneins induction and antioxidative response in aquatic worms Tubifex tubifex (Oligochaeta. Tubificidae) exposed to copper. Chemosphere 64, 121–128 (2006).

    Article  CAS  PubMed  Google Scholar 

  6. Gallego, A., Martin-Gonzales, A., Ortega, R. & Gutierrez, J. C. Flow cytometry assessment of cytotoxicity and reactive oxygen species generation by single and binary mixtures of cadmium. zinc and copper on populations of the ciliated protozoan Tetrahymena thermophile. Chemosphere 68, 647–661 (2007).

    Article  CAS  PubMed  Google Scholar 

  7. Jozefczak, M., Remans, T., Vangronsveld, J. & Cuypers, A. Glutathione is a key player in metal-induced oxidative stress defenses. Int. J. Mol. Sci. 13, 3145–3175 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Rico, D., Martin-Gonzalez, A., Diaz, S., de Lucas, P. & Gutierrez, J. C. Heavy metals generate reactive oxygen species in terrestrial and aquatic ciliated protozoa. Comp. Biochem. Physiol. Par. C 149, 90–96 (2009).

    Google Scholar 

  9. Poopal, R. K., Ramesh, M. & Dinesh, B. Short-term mercury exposure on Na+/K+-ATPase activity and ionoregulation in gill and brain of an Indian major carp. Cirrhinus mrigala. J. Trace. Elem. Med. Biol. 27, 70–75 (2013).

    Article  CAS  PubMed  Google Scholar 

  10. Rogers, J. T., Patel, M., Gilmour, K. M. & Wood, C. M. Mechanisms behind Pb-induced disruption of Na+ and Cl-balance in rainbow trout (Oncorhynchus mykiss). Am. J. Physiol. Regul. Integr. Comp. Physiol. 289, 463–472 (2005).

    Article  Google Scholar 

  11. Martins, C. M., Almeida, D. V., Marins, L. F. & Bianchini, A. mRNA expression and activity of ion-transporting proteins in gills of the blue crab Callinectes sapidus: effects of waterborne copper. Environ. Toxicol. Chem. 30, 206–211 (2011).

    Article  CAS  PubMed  Google Scholar 

  12. Mosher, S., Cope, W. G., Weber, F. X., Shea, D. & Kwak, T. J. Effects of lead on Na+,K+-ATPase and hemolymph ion concentrations in the freshwater mussel Elliptio complanata. Environ. Toxicol. 27, 268–276 (2010).

    Article  PubMed  Google Scholar 

  13. Brooks, S. J. & Mills, C. L. “The Effect of Copper on Osmoregulation in the Freshwater Amphipod Gammarus Pulex”. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 135, 527–537 (2003).

    Article  PubMed  Google Scholar 

  14. Hagiwara, A., Kotani, T., Snell, T. W., Assava-Aree, M. & Hirayama, K. Morphology, reproduction, genetics, and mating behavior of small, tropical marine Brachionus strains (Rotifera). J. Exp. Mar. Biol. Ecol. 194, 25–37 (1995).

    Article  Google Scholar 

  15. Gómez, A. & Snell, T. W. Sibling Species and Cryptic Speciation in the Brachionus Plicatilis Species Complex (Rotifera). J. Phylogenetics. Evol. Biol. 9, 953–964 (1996).

    Article  Google Scholar 

  16. Dahms, H. U., Hagiwara, A. & Lee, J.-S. Ecotoxicology, ecophysiology, and mechanistic studies with rotifers. Aquat. Toxicol. 101, 1–12 (2011).

    Article  CAS  PubMed  Google Scholar 

  17. Janssen, C. R., Ferrando, M. D. & Persoone, G. Ecotoxicological Studies with the Freshwater Rotifer Brachionus calyciflorus: IV. Rotifer Behavior as a Sensitive and Rapid Sublethal Test Criterion. Ecotoxicol. Environ. Saf. 28, 244–255 (1994).

    Article  CAS  PubMed  Google Scholar 

  18. Juarez-Franco, M. F., Sarma, S. S. S. & Nandini, S. Effect of cadmium and zinc on the population growth of Brachionus havanaensis (Rotifera: Brachionidae). J. Environ. Sci. Health A Tox. Hazard Subst. Environ. Eng. 42, 1489–1493 (2007).

    Article  CAS  PubMed  Google Scholar 

  19. Arnold, W. R., Diamond, R. L. & Smith, D. S. Acute and chronic toxicity of copper to the euryhaline rotifer. Brachionus plicatilis (“L” strain). Arch. Environ. Contam. Toxicol. 60, 250–260 (2011).

    Article  CAS  PubMed  Google Scholar 

  20. Grosell, M., Gerdes, R. M. & Brix, K. Chronic toxicity of lead to three freshwater invertebrates Brachionus calyciflorus, Chironomus tentans, and Lymnaea stagnalis. Environ. Toxicol. Chem. 25, 97–104 (2006).

    Article  CAS  PubMed  Google Scholar 

  21. 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. Healt. Sci. 4, 235–242 (2012).

    Article  Google Scholar 

  22. Yim, B., Kim, H, Jung M. Y., Lee, Y. M. Cadmium modulates the mRNA expression and activity of glutathione S-transferase in the monogonont rotifer Brachionus koreanus. Toxicol. Environ. Health. Sci. 7, 217–223 (2015).

    Article  Google Scholar 

  23. Lionetto, M. O., Giordano, M. E., Vilella, S. & Schettino, T. Inhibition of eel enzymatic activities by cadmium. Aquat. Toxicol. 48, 561–571 (2000).

    Article  CAS  PubMed  Google Scholar 

  24. Postel, U. et al. Inhibition of Na+/K+-ATPase and of active ion-transport functions in the gills of the shore crab Carcinus maenas induced by cadmium. Mar. Biol. 130, 407–416 (1998).

    Article  CAS  Google Scholar 

  25. Lowe, C. D., Kemp, S. J., Bates, A. D. & Montagnes, D. J. S. Evidence that the rofiter Brachionus plicatilis is not an osmoconformer. Mar. Biol. 146, 923–929 (2005).

    Article  Google Scholar 

  26. Felten, V. et al. Physiological and Behavioural Responses of Gammarus Pulex (Crustacea: Amphipoda) Exposed to Cadmium. Aquat. Toxicol. 86, 413–425 (2008).

    Article  CAS  PubMed  Google Scholar 

  27. Rodriguez Moreno, P. A., Schwarzbaum, P. J. & Rodriguez, E. M. Effects of cadmium on gill Na,K-ATPase of the estuarine crab Chasmagnathus granulata (Decapoda, Grapsidae) during postmolt: in vivo and in vitro studies. Bull. Environ. Contam. Toxicol. 61, 629–636 (1998).

    Article  CAS  PubMed  Google Scholar 

  28. MacDonald, A., Silk, L., Schwartz, M. & Playle, R. C. A lead-gill binding model to predict acute lead toxicity to rainbow trout (Oncorhynchus mykiss). Comp. Biochem. Physiol. C 133, 227–242 (2002).

    Article  Google Scholar 

  29. Rainbow, P. S. Ecophysiology of trace metal uptake in crustaceans. Estuar. Coast. Shel. Sci. 44, 169–176 (1997).

    Article  CAS  Google Scholar 

  30. Rogers, J. T., Richards, J. G. & Wood, C. M. Ionoregulatory disruption as the acute toxic mechanism for lead in the rainbow trout (Oncorhynchus mykiss). Aquat. Toxicol. 64, 215–234 (2003).

    Article  CAS  PubMed  Google Scholar 

  31. McGeer, J. C., Szebedinszky, C., McDonald, D. G. & Wood, C. M. Effects of chronic sublethal exposure to waterborne Cu. Cd or Zn in rainbow trout. 2. Tissue specific metal accumulation. Aquat. Toxicol. 50, 245–256 (2000).

    Article  CAS  PubMed  Google Scholar 

  32. Birceanu, O. et al. Modes of metal toxicity and impaired branchial ionoregulation in rainbow trout exposed to mixtures of Pb and Cd in soft water. Aquat. Toxicol. 89, 222–239 (2008).

    Article  CAS  PubMed  Google Scholar 

  33. Chetty, C. S., Cooper, A., McNeil, C. & Rajanna, B. The effects of cadmium in vitro on adenosine triphosphatase system and protection by thiol reagents in rat brain microsomes. Arch Environ. Contam. Toxicol. 22, 456–458 (1992).

    Article  CAS  PubMed  Google Scholar 

  34. Silvestre, F., Trausch, G. & Devos, P. Hyper-osmoregulation capacity of the Chinese mitten crab (Eriocheir sinensis) exposed to cadmium; acclimation during chronic exposure. Comp. Biochem. Physiol. 140C, 29–37 (2005).

    CAS  Google Scholar 

  35. Zhou, Q., Zhang, J., Fu, J., Shi, J. & Jiang, G. Biomonitoring: an appealing tool for assessment of metal pollution in the aquatic ecosystem. Anal. Chim. Acta 606, 135–150 (2008).

    Article  CAS  PubMed  Google Scholar 

  36. Alvarado-Flores, J. et al. Bioconcentration and localization of lead in the freshwater rotifer Brachionus calyciflorus Pallas 1677 (Rotifera: Monogononta). Aquat. Toxicol. 109, 127–132 (2012).

    Article  CAS  PubMed  Google Scholar 

  37. Rainbow, P. S. The significance of trace metal concentrations in decapods. Symp. Soc. Lond. 59, 291–313 (1988).

    Google Scholar 

  38. Sparla, A. M. & Overnell, J. The binding of cadmium to crab cadmium metallothionein. A polarographic investigation. Biochem. J. 267, 539–540 (1990).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Viarengo, A. & Nott, J. A. Mechanisms of heavy metal cation homeostasis in marine invertebrates. Comp. Biochem. Physiol. 104C, 355–372 (1993).

    CAS  Google Scholar 

  40. Williams, K. A., Green, W. J. & Pascoe, D. Studies on the acute toxicity of pollutants to freshwater macroinvertebrates. 1. Cadmium. Arch. Hydrobiol. 102, 461–471 (1985).

    CAS  Google Scholar 

  41. Rhee, J. S. et al. Genomic organization of selected genes in the small monogonont rotifer. Brachionus koreanus. Gene 505, 108–113 (2012).

    Article  CAS  PubMed  Google Scholar 

  42. Giuliani, M. E., Benedetti, M., Arukwe, A. & Regoli, F. Transcriptional and catalytic responses of antioxidant and biotransformation pathways inmussels, Mytilus galloprovincialis, exposed to chemical mixtures. Aquat. Toxicol. 134-135, 120–127 (2013).

    Article  CAS  PubMed  Google Scholar 

  43. Kanerva, M., Vehmas, A., Nikinmaa, M. & Vuori, K. A. Spatial variation in transcript and protein abundance of Atlantic salmon during feeding migration in the Baltic Sea. Environ. Sci. Technol. 48, 13969–13977 (2014).

    Article  CAS  PubMed  Google Scholar 

  44. Regoli, F., Giuliani, M. E., Benedetti, M. & Arukwe, A. Molecular and biochemical biomarkers in environmental monitoring: a comparison of biotransformation and antioxidant defense systems inmultiple tissues. Aquat. Toxicol. 105, 56–66 (2011).

    Article  CAS  PubMed  Google Scholar 

  45. Thevenod, F. Cadmium (CD)-mediated oxidative stress in proximal tubule (PT) cells induces degradation of Na+/K+-ATPase through proteasomal and endo-/lysosomal proteolytic pathways. FASE. J 13, A64 (1999).

    Google Scholar 

  46. 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).

    Article  PubMed  Google Scholar 

  47. Livak, K. J. & Schmittgen, T. D. Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2-CT Method. Methods 25, 402–408 (2001).

    Article  CAS  PubMed  Google Scholar 

  48. Jorge, M. B. et al. Mortality. Bioaccumulation and Physiological Responses in Juvenile Freshwater Mussels (Lampsilis Siliquoidea) Chronically Exposed to Copper. Aquat. Toxicol. 126, 137–147 (2013).

    Article  CAS  PubMed  Google Scholar 

  49. 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).

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Life Science, College of Natural Sciences, Sangmyung University, Seoul, 03016, Korea

    Hokyun Kim, Bora Lim, Byung-Do Kim & Young-Mi Lee

Authors
  1. Hokyun Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bora Lim
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Byung-Do Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Young-Mi Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Young-Mi Lee.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kim, H., Lim, B., Kim, BD. et al. Effects of heavy metals on transcription and enzyme activity of Na+/K+-ATPase in the monogonont rotifer, Brachionus koreanus . Toxicol. Environ. Health Sci. 8, 128–134 (2016). https://doi.org/10.1007/s13530-016-0270-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13530-016-0270-4

Keywords

Search

Navigation