Expressions of Heat Shock and Metallothionein Genes in the Heart of Common Carp (Cyprinus Carpio): Effects of Temperature Shock and Heavy Metal Exposure


Heat shock proteins (HSPs) and metallothioneins (MTs) play important roles in protection against environmental stressors. The present study analyzes and compares the regulation of heat shock (hsp70, hsc70-1 and hsp90α) and metallothionein (MT-1 and MT-2) genes in the heart of common carp, in response to elevated temperature, cold shock and exposure to several heavy metal ions (As3+, Cd2+ and Cu2+), in whole-animal experiments. Among these metals, arsenate proved to be the most potent inducer of the examined stress genes; the hsp90α and MT-1 mRNA levels were elevated 11- and 10-fold, respectively, after a 24-h exposure. In contrast, Cd2+ at 10 mg/L had no impact on the expression of hsp90α, and the MT genes also proved to be rather insensitive to Cd2+ treatment in the heart: only a 2-2.5-fold induction was observed in response to 10 mg/L Cd2+. Heat shock resulted in a transient induction of hsp70 (19-fold) and hsp90α (15-fold), while elevated temperature had no effect on the expression of the MTs. Direct cold shock induced hsp70 expression (14-fold), while the hsp90α (26-fold) and MT-2 (2-fold) expressions peaked after the recovery period following a direct cold shock. The five stress genes examined in this study exhibited a unique, tissue-specific basal expression pattern and a characteristic sensitivity to metal treatments and temperature shocks.


  1. 1.

    Ali, K. S., Dorgai, L., Abraham, M., Hermesz, E. (2003) Tissue- and stressor-specific differential expression of two hsc70 genes in carp. Biochem. Biophys. Research Com. 307, 503–509.

    CAS  Article  Google Scholar 

  2. 2.

    Cho, Y. S., Le, S. Y., Kim, K. Y., Bang, I. C., Kim, D. S., Nam, Y. K. (2008) Gene structure and expression of metallothionein during metal exposures in Hemibarbus mylodon. Ecotoxicol. Environ. 71, 125–137.

    CAS  Article  Google Scholar 

  3. 3.

    Cullen, K. E., Sarge, K. D. (1997) Characterization of hypothermia induced cellular stress response in mouse tissues. J. Biol. Chem. 272, 1742–1746.

    CAS  Article  Google Scholar 

  4. 4.

    Csermely, P., Schnaider, T., Sőti, C., Prohászka, Z., Nardai, G. (1998) The 90-kDa molecular chaperone family: structure, function, and clinical applications. A comprehensive review. Pharmacol. Ther 79, 129–168.

    CAS  Article  Google Scholar 

  5. 5.

    De Boeck, G., Ngo, T. T., Van Campenhout, K., Blust, R. (2003) Differential metallothionein induction patterns in three freshwater fish during sublethal copper exposure. Aquat. Toxicol. 65, 413–424.

    Article  Google Scholar 

  6. 6.

    Delogu, G., Signore, M., Mechelli, A., Famularo, G. (2002) Heat shock proteins and their role in heart injury. Curr Opin. Crit. Care 8, 411–416.

    Article  Google Scholar 

  7. 7.

    Eller-Jessen, K., Crivello, J. F. (1998) Subcutaneous NaAs3+ exposure increases metallothionein mRNA and protein expression in juvenile winter flounder. Aquat. Toxicol. 42, 301–320.

    CAS  Article  Google Scholar 

  8. 8.

    Feng, W., Benz, F. W., Cai, J., Pierce, W. M., Kang, Y. J. (2006) Metallothionein disulfides are present in metallothionein-overexpressing transgenic mouse heart and increase under conditions of oxidative stress. J. Biol. Chem. 281, 681–687.

    CAS  Article  Google Scholar 

  9. 9.

    Fujikake, N., Nagai, Y., Popiel, H. A., Kano, H., Yamaguchi, M., Toda, T. (2005) Alternative splicing regulates the transcriptional activity of Drosophila heat shock transcription factor in response to heat/cold stress. FEBS Lett. 579, 3842–3848.

    CAS  Article  Google Scholar 

  10. 10.

    Gao, D., Wang, G. T., Chen, X. T., Nie, P. (2009) Metallothionein-2 gene from the mandarin fish Siniperca chuatsi: cDNA cloning, tissue expression, and immunohistochemical localization. Comp. Biochem. Phys. C. 149, 18–25.

    Google Scholar 

  11. 11.

    Hartl, F. U. (1996) Molecular chaperones in cellular protein folding. Nature 381, 571–579.

    CAS  Article  Google Scholar 

  12. 12.

    Hermesz, E., Ábrahám, M., Nemcsók, J. (2001) Tissue-specific expression of two metallothionein genes in common carp during cadmium exposure and temperature shock. Comp. Biochem. Physiol. C. 128, 457–456.

    CAS  Google Scholar 

  13. 13.

    Hermesz, E., Ábrahám, M., Nemcsók, J. (2001) Identification of two hsp90 genes in carp. Comp. Biochem. Physiol. Part C 129, 397–407.

    CAS  Google Scholar 

  14. 14.

    Hermesz, E., Gazdag, A. P., Ali, K. S., Nemcsók, J., Ábrahám, M. (2002) Differential regulation of the two metallothionein genes in common carp. Acta Biol. Hung. 53, 343–350.

    CAS  Article  Google Scholar 

  15. 15.

    Kagi, J. H. R. (1993) Evolution, structure and chemical activity of class I metallothioneins: In: Suzuki, K. T., Imura, N., Kimura, M. (eds), Metallothionein III. Basel, Birkhäuser-Verlag, pp. 29–55.

    Google Scholar 

  16. 16.

    Kang, Y. J., Chen, Y., Yu, A., Voss-McCowan, M., Epstein, P. N. (1997) Overexpression of metallothionein in the heart of transgenic mice suppresses doxorubicin cardiotoxicity. J. Clin. Investig. 100, 1501–1506.

    CAS  Article  Google Scholar 

  17. 17.

    Kang, Y. J., Li, Y., Sun, X., Sun, X. (2003) Antiapoptotic effect and inhibition of ischemia/reperfusion-induced myocardial injury in metallothionein-overexpressing transgenic mice. Am. J. Pathol. 163, 1579–1586.

    CAS  Article  Google Scholar 

  18. 18.

    Kim, J. H., Wang, S. Y., Kim, I. C., Ki, J. S., Raisuddin, S., Lee, J. S., Han, K. N. (2008) Cloning of a river pufferfish (Takifugu obscurus) metallothionein cDNA and study of its induction profile in cadmium-exposed fish. Chemosphere 71, 1251–1259.

    CAS  Article  Google Scholar 

  19. 19.

    Kregel, K. C. J. (2002) Heat shock proteins: modifying factors in physiological stress responses and acquired thermotolerance. Appl. Physiol. 92, 2177–2186.

    CAS  Article  Google Scholar 

  20. 20.

    Latchman, D. S. (2001) Heat shock proteins and cardiac protection. Cardiovasc. Res. 51, 637–646.

    CAS  Article  Google Scholar 

  21. 21.

    Margoshes, M., Vallee, B. L. (1957) A cadmium protein from equine kidney cortex. J. Am. Chem. Soc. 79, 4813–4814.

    CAS  Article  Google Scholar 

  22. 22.

    Misra, S., Zafarullah, M., Price-Haugghey, J., Gedamu, L. (1989) Analysis of stress-induced gene expression in fish cell lines exposed to heavy metals and heat shock. Biochem. Biophys. Acta 1007, 325–333.

    CAS  Google Scholar 

  23. 23.

    Sass, J. B., Krone, P. H. (1997) Hsp90a gene expression may be a conserved feature of vertebrate somitogenesis. Exp. Cell Res. 233, 391–394.

    CAS  Article  Google Scholar 

  24. 24.

    Valko, M., Morris, H., Cronin, M. T. (2005) Metals, toxicity and oxidative stress. Curr. Med. Chem. 12, 1161–1208.

    CAS  Article  Google Scholar 

  25. 25.

    Van Campenhout, K., Infante, H. G., Adams, F., Blust, R. (2004) Induction and binding of Cd, Cu, and Zn to metallothionein in carp (Cyprinus carpio) using HPLC-ICP-TOFMS. Toxicol. Sci. 80, 276–287.

    Article  Google Scholar 

  26. 26.

    Weber, T. E., Bosworth, B. G. (2005) Effects of 28 day exposure to cold temperature or feed restriction on growth, body composition, and expression of genes related to muscle growth and metabolism in channel catfish. Aquaculture 246, 483–492.

    CAS  Article  Google Scholar 

  27. 27.

    Yellon, D. M., Latchman, D. S. (1992) Stress proteins and myocardial protection. J. Mol. Cell. Cardiol. 24, 113–124.

    CAS  Article  Google Scholar 

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Correspondence to Edit Hermesz.

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Said Ali, K., Ferencz, Á., Nemcsók, J. et al. Expressions of Heat Shock and Metallothionein Genes in the Heart of Common Carp (Cyprinus Carpio): Effects of Temperature Shock and Heavy Metal Exposure. BIOLOGIA FUTURA 61, 10–23 (2010).

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  • Carp
  • heart
  • heat shock
  • heavy metal
  • metallothionein