Aluminum-Induced Oxidative Stress and Apoptosis in Liver of the Common Carp, Cyprinus carpio

  • A. C. Razo-Estrada
  • S. García-Medina
  • E. Madrigal-Bujaidar
  • L. M. Gómez-Oliván
  • M. Galar-MartínezEmail author


Although aluminum (Al) is considered innocuous to living beings, exposure to high concentrations can elicit damage. Al has been found to cause liver pathologies in various animal models. Its mechanisms of toxicity are unclear; presumably, it interacts with protein sulfhydryl groups and promotes reactive oxygen species formation causing oxidative stress. Lipid peroxidation, protein carbonyl content, and activity of superoxide dismutase, catalase, and caspase-3 were determined in liver of Cyprinus carpio exposed to 0.05, 120, and 239.42 mg Al L−1 for 12, 24, 48, 72, and 96 h. Al induced increased lipid peroxidation and protein carbonyl content as well as changes in enzymatic activity, indicating it elicits oxidative stress and apoptosis in common carp liver.


Aluminum Cyprinus carpio Liver Oxidative stress Apoptosis 



This study was made possible through support from the National Science and Technology Council (CONACyT, projects 57321 and 181541) as well as the Research and Postgraduate Division of the National Polytechnic Institute, Mexico (SIP-IPN, projects 20060186 and 200704594).


  1. Abubakar, M. G., Taylor, A., & Ferns, G. A. (2003). Aluminium administration is associated with enhanced hepatic oxidant stress that may be offset by dietary vitamin E in the rat. International Journal of Experimental Pathology, 84, 49–54.CrossRefGoogle Scholar
  2. Andrén, C. M., & Rydin, E. (2012). Toxicity of inorganic aluminium at spring snowmelt-in-stream bioassays with brown trout (Salmo trutta L.). Science of the Total Environment, 437, 422–432.CrossRefGoogle Scholar
  3. Atli, G., Alptekin, Ö., Tükel, S., & Canli, M. (2006). Response of catalase activity to Ag+, Cd2+, Cr6+, Cu2+ and Zn2+ in five tissues of freshwater fish Oreochromis niloticus. Comparative Biochemistry and Physiology, 143, 218–224.CrossRefGoogle Scholar
  4. Bagnyukova, T. V., Chahrak, O. I., & Lushchak, V. I. (2006). Coordinated response of goldfish antioxidant defenses to environmental stress. Aquatic Toxicology, 78, 325–331.CrossRefGoogle Scholar
  5. Boesterli, U. A. (2007). Mechanistic toxicology (pp. 191–198). Boca Raton: CRC Press.Google Scholar
  6. Bondy, S. C., & Cambell, A. (2001). Oxidative and inflammatory properties of aluminium: possible relevance in Alzheimer’s disease. In C. Exley (Ed.), Aluminium and Alzheimer’s disease. The science that describes the link (pp. 311–321). Amsterdam: Elsevier.CrossRefGoogle Scholar
  7. Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72, 248–254.CrossRefGoogle Scholar
  8. Buege, J. A., & Aust, S. D. (1979). Microsomal lipid peroxidation. Methods in Enzymology, 52, 302–310.CrossRefGoogle Scholar
  9. Camargo, M. M., Fernandes, M. N., & Martinez, C. B. (2009). How aluminium exposure promotes osmoregulatory disturbances in the neotropical freshwater fish Prochilus lineatus. Aquatic Toxicology, 94, 40–46.CrossRefGoogle Scholar
  10. Chunsheng, L., Ke, Y., Shi, X., Wang, J., Lam, P. K. S., Wu, R. S. S., et al. (2007). Induction of stress and apoptosis by PFOS and PFOA in primary cultured hepatocytes of freshwater tilapia (Oreochromis niloticus). Aquatic Toxicology, 82, 135–143.CrossRefGoogle Scholar
  11. Fernández-Dávila, M. L., Razo-Estrada, A. C., García-Medina, S., Gómez-Oliván, L. M., Piñón-López, M. J., Ibarra, R. G., et al. (2012). Aluminum-induced oxidative stress and neurotoxicity in grass carp (Cyprinidae-Ctenopharingodon idella). Ecotoxicology and Environmental Safety, 76, 87–92.CrossRefGoogle Scholar
  12. Flora, S. J., Mehta, A., Satsangi, K., Kannan, G. M., & Gupta, M. (2003). Aluminum-induced oxidative stress in rat brain: response to combined administration of citric acid and HEDTA. Comparative Biochemistry and Physiology-Part C, 134, 319–328.Google Scholar
  13. Galar-Martínez, M., Amaya-Chávez, A., Gómez-Oliván, L. M., Vega-López, A., Razo-Estrada, C., & García-Medina, S. (2008). Responses of three benthic organisms (Hyallela azteca, Limnodrillus hoffmeisteri and Stagnicola attenuata) to natural sediment spiked with zinc when exposed in single or multi-species test systems. Aquatic Ecosystem Health and Management, 11(4), 432–440.CrossRefGoogle Scholar
  14. Galar-Martínez, M., Gómez-Oliván, L. M., Amaya-Chávez, A., Razo-Estrada, A. C., & García-Medina, S. (2010). Oxidative stress induced on Cyprinus carpio by contaminants present in the water and sediment of Madín reservoir. Journal of Environmental Science & Health Part A, 45(2), 155–160.CrossRefGoogle Scholar
  15. García-Medina, S., Razo-Estrada, A. C., Gómez-Oliván, L. M., Amaya-Chávez, A., Madrigal-Bujaidar, E., & Galar-Martínez, M. (2010). Aluminum-induced oxidative stress in lymphocytes of common carp (Cyprinus carpio). Fish Physiology and Biochemistry, 36, 875–882.CrossRefGoogle Scholar
  16. García-Medina, S., Razo-Estrada, A. C., Galar-Martínez, M., Cortéz-Barberena, E., Gómez-Oliván, L. M., Álvarez-González, I., et al. (2011). Genotoxic and cytotoxic effects induced by aluminum in the lymphocytes of the common carp (Cyprinus carpio). Comparative Biochemistry and Physiology-Part C: Toxicology & Pharmacology, 153, 113–118.CrossRefGoogle Scholar
  17. Gupta, R. C. (2012). Aluminum. In R. C. Gupta (Ed.), Veterinary toxicology (pp. 493–498). Amsterdam: Elsevier.CrossRefGoogle Scholar
  18. Instituto Nacional de Ecología, (1989). Criterios Ecológicos de Calidad del Agua. CE-CCA-001/89. Secretaría del Medio Ambiente y Recursos Naturales, Mexico.Google Scholar
  19. Jianbing, L., Jingling, R., Jing, Z., & Sumei, L. (2008). The distribution of dissolved aluminum in the Yellow and East China seas. Journal of Ocean University of China, 7, 48–54.CrossRefGoogle Scholar
  20. Kiss, T., & Hollósi, M. (2001). The interaction of aluminium with peptides and proteins. In C. Exley (Ed.), Aluminium and Alzheimer’s disease. The science that describes the link (pp. 361–392). Amsterdam: Elsevier.CrossRefGoogle Scholar
  21. Kovačević, G., Gregorović, G., Kalafatić, M., & Jaklinović, I. (2009). The effect of aluminium on the planarian Polycelis felina (Daly). Water, Air, and Soil Pollution, 196, 333–344.CrossRefGoogle Scholar
  22. Levine, R. L., Williams, J. A., Stadtman, E. R., & Shacter, E. (1994). Carbonyl assays for determination of oxidatively modified proteins. Methods in Enzymology, 233, 346–357.CrossRefGoogle Scholar
  23. Misra, H. P., & Fidovich, I. (1972). The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. Journal of Biological Chemistry, 247(10), 3170–3175.Google Scholar
  24. Oruc, E. O., & Usta, D. (2007). Evaluation of oxidative stress responses and neurotoxicity potential of diazinon in different tissues of Cyprinus carpio. Environmental Toxicology and Pharmacology, 23, 48–55.CrossRefGoogle Scholar
  25. Park, W. H., Han, Y. H., Kim, S. H., & Kim, S. Z. (2007). Pyrogallol, ROS generation inhibits As4.1 juxtaglomerular cells via cell cycle arrest of G2 phase and apoptosis. Toxicology, 235, 130–139.CrossRefGoogle Scholar
  26. Parvez, S., & Raisuddin, S. (2005). Protein carbonyls: novel biomarkers of exposure to oxidative stress-inducing pesticides in freshwater fish Channa punctata (Bloch). Environmental Toxicology and Pharmacology, 20, 112–117.CrossRefGoogle Scholar
  27. Prasad, M. N. V. (2001). Metals in the environment (pp. 299–311). New York: Marcel Dekker.Google Scholar
  28. Radi, R., Turrens, J. F., Chand, L. Y., Bush, K. M., Carpo, J. D., & Freeman, B. A. (1991). Detection of catalase in rat heart mitochondria. Journal of Biological Chemistry, 266(32), 22028–22034.Google Scholar
  29. Semedo, M., Reis-Henriques, M. A., Rey-Salgueiro, L., Oliveira, M., Delerue-Matos, C., Morais, S., et al. (2012). Metal accumulation and oxidative stress biomarkers in octopus (Octopus vulgaris) from Northwest Atlantic. Science of the Total Environment, 433, 230–237.CrossRefGoogle Scholar
  30. Shacter, E. (2000). Quantification and significance of protein oxidation in biological samples. Drug Metabolism Reviews, 32, 307–326.CrossRefGoogle Scholar
  31. Šimonovičová, M., Tamás, L., Huttová, J., & Mistrík, I. (2004). Effect of aluminium on oxidative stress related enzymes activities in barley roots. Biologia Plantarum, 48, 261–266.CrossRefGoogle Scholar
  32. Sinha, S., Mallick, S., Misra, R. K., Singh, S., Basant, A., & Gupta, A. K. (2007). Uptake and translocation of metals in Spinacia oleracea L. grown on tannery sludge-amended and contaminated soils: effect on lipid peroxidation, morpho-anatomical changes and antioxidants. Chemosphere, 67, 176–187.CrossRefGoogle Scholar
  33. Valavanidis, A., Vlahogianni, T., Dassenakis, M., & Scoullos, M. (2006). Molecular biomarkers of oxidative stress in aquatic organisms in relation to toxic environmental pollutants. Ecotoxicology and Environmental Safety, 46, 178–189.CrossRefGoogle Scholar
  34. van der Oost, R., Beyer, J., & Vermeulen, N. P. E. (2003). Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environmental Toxicology and Pharmacology, 13, 57–149.CrossRefGoogle Scholar
  35. Vlahogianni, T., Dassenakis, M., Scoullos, M. J., & Valavanidis, A. (2007). Integrated use of biomarkers (superoxide dismutase, catalase and lipid peroxidation) in mussels Mytilus galloprovincialis for assessing heavy metals’ pollution in coastal areas from the Saronikos Gulf of Greece. Marine Pollution Bulletin, 54, 1361–1371.CrossRefGoogle Scholar
  36. Wang, D., He, Y., Liang, J., Liu, P., & Zhuang, P. (2013). Distribution and source analysis of aluminum in rivers near Xi'an City, China. Environmental Monitoring and Assessment, 185, 1041–1053. doi: 10.1007/s10661-012-2612-2.CrossRefGoogle Scholar
  37. Woodburn, K., Walton, R., MCrohan, C., & White, K. (2011). Accumulation and toxicity of aluminium-contaminated food in the freshwater crayfish, Pacifastacus leniusculus. Aquatic Toxicology, 105, 535–542.CrossRefGoogle Scholar
  38. Wu, J., Du, F., Zhang, P., Khan, I. A., Chen, J., & Liang, Y. (2005). Thermodynamics of the interaction of aluminum ions with DNA: implications for the biological function of aluminum. Journal of Inorganic Biochemistry, 99, 1145–1154.CrossRefGoogle Scholar
  39. Yousef, M. I. (2004). Aluminium-induced changes in hemato-biochemical parameters, lipid peroxidation and enzyme activities of male rabbits: protective role of ascorbic acid. Toxicology, 199, 47–57.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • A. C. Razo-Estrada
    • 1
  • S. García-Medina
    • 1
  • E. Madrigal-Bujaidar
    • 2
  • L. M. Gómez-Oliván
    • 3
  • M. Galar-Martínez
    • 1
    Email author
  1. 1.Laboratorio de Toxicología Acuática, Departamento de Farmacia, Instituto Politécnico NacionalEscuela Nacional de Ciencias BiológicasMexico CityMexico
  2. 2.Laboratorio de Genética, Departamento de Morfología, Instituto Politécnico NacionalEscuela Nacional de Ciencias BiológicasMexico CityMexico
  3. 3.Laboratorio de Toxicología Ambiental, Departamento de FarmaciaFacultad de Química, Universidad Autónoma del Estado de MéxicoTolucaMéxico

Personalised recommendations