Skip to main content

Advertisement

Springer Nature Link
Log in

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

  • Published:
Water, Air, & Soil Pollution Aims and scope Submit manuscript

Abstract

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.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Similar content being viewed by others

References

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Bagnyukova, T. V., Chahrak, O. I., & Lushchak, V. I. (2006). Coordinated response of goldfish antioxidant defenses to environmental stress. Aquatic Toxicology, 78, 325–331.

    Article  CAS  Google Scholar 

  • Boesterli, U. A. (2007). Mechanistic toxicology (pp. 191–198). Boca Raton: CRC Press.

    Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Buege, J. A., & Aust, S. D. (1979). Microsomal lipid peroxidation. Methods in Enzymology, 52, 302–310.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Gupta, R. C. (2012). Aluminum. In R. C. Gupta (Ed.), Veterinary toxicology (pp. 493–498). Amsterdam: Elsevier.

    Chapter  Google Scholar 

  • Instituto Nacional de Ecología, (1989). Criterios Ecológicos de Calidad del Agua. CE-CCA-001/89. Secretaría del Medio Ambiente y Recursos Naturales, Mexico.

  • 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.

    Article  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Prasad, M. N. V. (2001). Metals in the environment (pp. 299–311). New York: Marcel Dekker.

    Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Shacter, E. (2000). Quantification and significance of protein oxidation in biological samples. Drug Metabolism Reviews, 32, 307–326.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

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).

Author information

Authors and Affiliations

  1. Laboratorio de Toxicología Acuática, Departamento de Farmacia, Instituto Politécnico Nacional, Escuela Nacional de Ciencias Biológicas, Av. Wilfrido Massieu s/n, Col. Industrial Vallejo, Mexico City, Mexico

    A. C. Razo-Estrada, S. García-Medina & M. Galar-Martínez

  2. Laboratorio de Genética, Departamento de Morfología, Instituto Politécnico Nacional, Escuela Nacional de Ciencias Biológicas, Mexico City, Mexico

    E. Madrigal-Bujaidar

  3. Laboratorio de Toxicología Ambiental, Departamento de Farmacia, Facultad de Química, Universidad Autónoma del Estado de México, Toluca, México

    L. M. Gómez-Oliván

Authors
  1. A. C. Razo-Estrada
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. García-Medina
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. E. Madrigal-Bujaidar
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. L. M. Gómez-Oliván
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. M. Galar-Martínez
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M. Galar-Martínez.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Razo-Estrada, A.C., García-Medina, S., Madrigal-Bujaidar, E. et al. Aluminum-Induced Oxidative Stress and Apoptosis in Liver of the Common Carp, Cyprinus carpio . Water Air Soil Pollut 224, 1510 (2013). https://doi.org/10.1007/s11270-013-1510-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11270-013-1510-8

Keywords

Search

Navigation