Water, Air, & Soil Pollution

, 226:2215 | Cite as

Interaction of Carbon Nanomaterial Fullerene (C60) and Microcystin-LR in Gills of Fish Cyprinus carpio (Teleostei: Cyprinidae) Under the Incidence of Ultraviolet Radiation

  • Roberta Socoowski Britto
  • Juliana Artigas Flores
  • Daniel de Lima Mello
  • Camilla da Costa Porto
  • José María Monserrat


One of the most widely used carbon nanomaterials is fullerene (C60), a lipophilic organic compound that potentially can behave as a carrier of toxic molecules, enhancing the entry of environmental contaminants in specific organs. Microcystins (MC) are cyanotoxins very toxic for human and environmental health. Several studies showed that exposure to MC or C60 generates reactive oxygen species (ROS) and changes in antioxidant levels. Also, another factor that can come to enhance the toxic potential of both MC and C60 is UVA radiation. Therefore, it was evaluated the effects on oxidative stress parameters of ex vivo co-exposure of MC and C60 (5 mg/l) in gills of the fish Cyprinus carpio under UVA radiation incidence. The results showed that (a) there was a loss of antioxidant capacity after low MC concentration (L, 50 μg/l) + C60 co-exposure under UVA, (b) C60 under UVA decreased glutathione-S-transferase (GST) activity, (c) high MC concentration (H, 200 μg/l) + C60 co-exposure decreased the concentrations of glutathione (GSH) under UVA or in the dark, (d) L under UVA increased lipid peroxidation, and (e) C60 did not cause a higher bioaccumulation of MC in gills. The lowering of GSH in H + C60 co-exposure should compromise MC detoxification mediated by GST, although toxin accumulation is not influenced by C60.


Oxidative stress Nanotoxicology Aquatic environment Ultraviolet radiation Cyanotoxin 



J.M. Monserrat receives a productivity research fellowship from the Brazilian agency CNPq (process number PQ 307880/2013-3). The logistic and material support from the Instituto Nacional de Ciência e Tecnologia de Nanomateriais de Carbono (CNPq) was essential for the execution of the present study. The support of DECIT/SCTIE-MS through Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and Fundação de Amparo à Pesquisa do Estado do Rio Grande do Sul (FAPERGS, Proc. 10/0036-5–PRONEX/Conv. 700545/2008) is also acknowledged. J.M. Monserrat acknowledges the support of Nanotoxicology Network (MCTI/CNPq process number 552131/2011-3).


  1. Aitken, R. J., Chaudhry, M. Q., Boxall, A. B. A., & Hull, M. (2006). Manufacture and use of nanomaterials: current status in the UK and global trends. Occupational Medicine-Oxford, 56, 300–306.Google Scholar
  2. Amado, L. L., & Monserrat, J. M. (2010). Oxidative stress generation by microcystins in aquatic animals: why and how. Environment International, 36, 226–235.CrossRefGoogle Scholar
  3. Amado, L. L., Garcia, M. L., Ramos, P. B., Freitas, R. F., Zafalon, B., Ferreira, J. L. R., Yunes, J. S., & Monserrat, J. M. (2009). A method to measure total antioxidant capacity against peroxyl radicals in aquatic organisms: application to evaluate microcystins toxicity. Science of the Total Environment, 407, 2115–2123.Google Scholar
  4. Andrievsky, G., Klochkov, V., & Derevyanchenko, L. (2005). Is the C60 fullerene molecule toxic?! Fullerenes, Nanotubes, and Carbon Nanostructures, 13, 363–376.CrossRefGoogle Scholar
  5. Baun, A., Sorensen, S. N., Rasmussen, R. F., Hartmann, N. B., & Koch, C. B. (2008). Toxicity and bioaccumulation of xenobiotic organic compounds in the presence of aqueous suspensions of aggregates of nano-C60. Aquatic Toxicology, 86, 379–387.CrossRefGoogle Scholar
  6. Britto, R. S., Garcia, M. L., da Rocha, A. M., Flores, J. A., Pinheiro, M. V. B., Monserrat, J. M., & Ferreira, J. L. R. (2012). Effects of carbon nanomaterials fullerene C60 and fullerol C60 (OH)18–22 on gills of fish Cyprinus carpio (Cyprinidae) exposed to ultraviolet radiation. Aquatic Toxicology, 114–115, 80–87.CrossRefGoogle Scholar
  7. Buratti, F. M., Scardala, S., Funari, E., & Testai, E. (2011). Human glutathione transferases catalyzing the conjugation of the hepatotoxin microcystin-LR. Chemical Research in Toxicology, 20, 926–933.CrossRefGoogle Scholar
  8. Canesi, L., Fabbri, R., Gallo, G., Vallotto, D., Marcomini, A., & Pojana, G. (2010). Biomarkers in Mytilus galloprovincialis exposed to suspensions of selected nanoparticles (nano carbon black, C60 fullerene, nano-TiO2, nano-SiO2). Aquatic Toxicology, 15, 168–177.CrossRefGoogle Scholar
  9. Cazenave, J., Nores, M. L., Miceli, M., Díaz, M. P., Wunderlin, D. A., & Bistoni, M. A. (2008). Changes in the swimming activity and the glutathione S-transferase activity of Jenynsia multidentata fed with microcystin-RR. Water Research, 42, 1299–1307.CrossRefGoogle Scholar
  10. Costa, C. L. A., Chaves, I. S., Ventura-Lima, J., Ferreira, J. R., Ferraz, L., Carvalho, L. M., & Monserrat, J. M. (2012). In vitro evaluation of co-exposure of arsenium and an organic nanomaterial (fullerene, C60) in zebrafish hepatocytes. Comparative Biochemistry and Physiology. C, 155, 206–212.Google Scholar
  11. da Rocha, A. M., De Freitas, D. P. S., Burns, M., Vieira, J. P., De la Torre, F. R., & Monserrat, J. M. (2009). Seasonal and organ variations in antioxidant capacity, detoxifying competence and oxidative damage in freshwater and estuarine fishes from southern Brazil. Comparative Biochemistry and Physiology. C, 150, 512–520.Google Scholar
  12. Ferreira, J. R. F., Barros, D. M., Geracitano, L. A., Fillmann, G., Fossa, C. E., De Almeida, E. A., Prado, M. C., Neves, B. R. A., Pinheiro, M. V. B., & Monserrat, J. M. (2012). Influence of in vitro exposure to fullerene C60 in redox state and lipid peroxidation of brain and gills of carp Cyprinus carpio (Cyprinidae). Environmental Toxicology and Chemistry, 31, 961–967.CrossRefGoogle Scholar
  13. Ferreira, J. L. R., Lonné, M. N., França, T. A., Maximilla, N. R., Lugokenski, T. H., Costa, P. G., Fillmann, G., Antunes Soares, F. A., de la Torre, F. R., & Monserrat, J. M. (2014). Co-exposure of the organic nanomaterial fullerene C60 with benzo[a]pyrene in Danio rerio (zebrafish) hepatocytes: evidence of toxicological interactions. Aquatic Toxicology, 147, 76–83.CrossRefGoogle Scholar
  14. Fujitani, Y., Kobayashi, T., Arashidani, K., Kunugita, N., & Suemura, K. (2008). Measurement of the physical properties of aerosols in a fullerene factory for inhalation exposure assessment. Journal of Occupational and Environmental Hygiene, 5, 380–389.CrossRefGoogle Scholar
  15. Gallego-Urrea, J. A., Tuoriniemi, J., & Hassellöv, M. (2011). Applications of particle-tracking analysis to the determination of size distributions and concentrations of nanoparticles in environmental, biological and food samples. Trends in Analytical Chemistry, 30, 473–483.Google Scholar
  16. Gehringer, M. M., Shephard, E. G., Downing, T. G., Wiegand, C., & Neilan, B. A. (2004). An investigation into the detoxification of microcystin-LR by the glutathione pathway in Balb/c mice. The International Journal of Biochemistry & Cell Biology, 36, 931–941.CrossRefGoogle Scholar
  17. Guldi, D. M., & Prato, M. (2000). Excited-state properties of C(60) fullerene derivatives. Accounts of Chemical Research, 33, 695–703.CrossRefGoogle Scholar
  18. Halliwell, B., & Gutteridge, J. C. M. (2007). Free radicals in biology and medicine. Oxford: Oxford University Press.Google Scholar
  19. Henry, T. B., Petersen, E. J., & Compton, R. N. (2011). Aqueous fullerene aggregates (nC60) generate minimal reactive oxygen species and are of low toxicity in fish: a revision of previous reports. Current Opinion in Biotechnology, 22, 533–537.CrossRefGoogle Scholar
  20. Howard, A. G. (2010). On the challenge of quantifying man-made nanoparticles in the aquatic environment. Journal of Environmental Monitoring, 12, 135–142.CrossRefGoogle Scholar
  21. Johnston, H. J., Hutchison, G. R., Christensen, F. M., Aschberger, K., & Stone, V. (2010). The biological mechanisms and physico-chemical characteristics responsible for driving fullerene toxicity. Toxicological Sciences, 114, 162–182.CrossRefGoogle Scholar
  22. Kahru, A., & Dubourguier, H. C. (2010). From ecotoxicology to nanoecotoxicology. Toxicology, 269, 105–119.CrossRefGoogle Scholar
  23. Kamat, J. P., Devasagayam, T. P. A., Priyadarsini, K. I., & Mohan, H. (2000). Reactive oxygen species mediated membrane damage induced by fullerene derivatives and its possible biological implications. Toxicology, 155, 55–61.CrossRefGoogle Scholar
  24. Limbach, L. K., Peter, W., Pius, M., Grass, R. N., Bruinink, A., & Stark, W. J. (2007). Exposure of engineered nanoparticles to human lung epithelial cells: influence of chemical composition and catalytic activity on oxidative stress. Environmental Science & Technology, 41, 4158–4163.CrossRefGoogle Scholar
  25. Limbach, L. K., Gras, R. N., & Stark, W. J. (2009). Physico-chemical differences between particle- and molecule-derived toxicity: can we make inherently safe nanoparticles? Chimia, 63, 38–43.Google Scholar
  26. Pinho, G. L. L., Rosa, C. M., Maciel, F. E., Bianchini, A., Yunes, J. S., Proença, L. A. O., & Monserrat, J. M. (2005). Antioxidant responses and oxidative stress after microcystin exposure in the hepatopancreas of estuarine crab species. Ecotoxicology and Environmental Safety, 61, 353–360.CrossRefGoogle Scholar
  27. Roberts, J. E., Wielgus, A. R., Boyes, W. J., Andley, U., & Chignell, C. F. (2008). Phototoxicity and cytotoxicity of fullerol in human lens epithelial cells. Toxicology and Applied Pharmacology, 228, 49–58.CrossRefGoogle Scholar
  28. Sakurai, H., Yasui, H., Yamada, T., Nishimura, H., & Shigemoto, M. (2005). Detection of reactive oxygen species in the skin of live mice and rats exposed to UVA light: a research review on chemiluminescence and trials for UVA protection. Photochemical & Photobiological Sciences, 4, 715–720.CrossRefGoogle Scholar
  29. Shinohara, N., Matsumoto, T., Gamo, M., Miyauchi, A., Endo, S., Yonezawa, Y., & Nakanishi, J. (2009). Is lipid peroxidation induced by the aqueous suspension of fullerene C60 nanoparticles in the brains of Cyprinus carpio? Environmental Science & Technology, 43, 948–953.CrossRefGoogle Scholar
  30. Spohn, P., Hirsch, C., Hasler, F., Bruinink, A., Krug, H. F., & Wick, P. (2009). C60 fullerene: a powerful antioxidant or a damaging agent? The importance of an in-depth material characterization prior to toxicity assays. Environmental Pollution, 157, 1134–1139.CrossRefGoogle Scholar
  31. Sun, H., Lü, K., Minter, E. J., Chen, Y., Yang, Z., & Montagnes, D. J. (2012). Combined effects of ammonia and microcystin on survival, growth, antioxidant responses, and lipid peroxidation of bighead carp Hypophthalmythys nobilis larvae. Journal of Hazardous Materials, 221, 213–219.CrossRefGoogle Scholar
  32. Wang, Z., Xiao, B., Song, L., Wang, C., & Zhang, J. (2012). Responses and toxin bioaccumulation in duckweed (Lemna minor) under microcystin-LR, linear alkylbenzene sulfonate and their joint stress. Journal of Hazardous Materials, 229, 137–144.CrossRefGoogle Scholar
  33. Wiegand, C., & Pflugmacher, S. (2005). Ecotoxicological effects of selected cyanobacterial secondary metabolites a short review. Toxicology and Applied Pharmacology, 203, 201–218.CrossRefGoogle Scholar
  34. Xia, X. R., Monteiro-Riviere, N. A., & Riviere, J. E. (2010). Skin penetration and kinetics of pristine fullerenes (C60) topically exposed in industrial organic solvents. Toxicology and Applied Pharmacology, 242, 29–37.CrossRefGoogle Scholar
  35. Xie, L., Yokoyama, A., Nakamura, K., & Park, H. (2007). Accumulation of microcystins in various organs of the freshwater snail Sinotaia histrica and three fishes in a temperate lake, the eutrophic Lake Suwa, Japan. Toxicon, 49, 646–652.CrossRefGoogle Scholar
  36. Zar, J. H. (2010). Biostatistical analysis. New Jersey: Prentice Hall.Google Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  • Roberta Socoowski Britto
    • 1
    • 2
  • Juliana Artigas Flores
    • 1
  • Daniel de Lima Mello
    • 1
  • Camilla da Costa Porto
    • 1
  • José María Monserrat
    • 1
    • 2
    • 3
    • 4
  1. 1.Instituto de Ciências Biológicas (ICB)Universidade Federal do Rio Grande–FURGRio GrandeBrazil
  2. 2.Programa de Pós Graduação em Fisiologia Animal Comparada–Fisiologia Animal ComparadaFURGRio GrandeBrazil
  3. 3.Instituto Nacional de Ciência e Tecnologia de Nanomateriais de Carbono (CNPq)Rio GrandeBrazil
  4. 4.Rede de Nanotoxicologia (MCTI/CNPq), Nanotoxicologia Ocupacional e Ambiental: Subsídios Científicos para estabelecer marcos regulatórios e avaliação de riscosRio GrandeBrazil

Personalised recommendations