In Vitro Analysis of Early Genotoxic and Cytotoxic Effects of Okadaic Acid in Different Cell Types of the Mussel Mytilus galloprovincialis

REFERENCES

• Akcha, F., Tanguy, A., Leday, G., Pelluhet, L., Budzinski, H., and Chiffoleau, J. F. 2004. Measurement of DNA single-strand breaks in gill and hemolymph cells of mussels, Mytilus sp., collected on the French Atlantic Coast. Mar. Environ. Res. 58: 753–756.
   PubMed Web of Science ®Google Scholar
• Anderson, D. M. 2005. The ecology and oceanography or harmful algal blooms: Multidisciplinary approaches to research and management. Intergovernmental Oceanographic Commission, UNESCO.
   Google Scholar
• Bialojan, C., and Takai, A. 1988. Inhibitory effect of a marine-sponge toxin, okadaic acid, on protein phosphatases. Specificity and kinetics. Biochem. J. 256: 283–290.
   PubMed Web of Science ®Google Scholar
• Carvalho Pinto-Silva, C. R., Ferreira, J. F., Costa, R. H. R., Belli Filho, P., Creppy, E. E., and Matias, W. G. 2003. Micronucleus induction in mussels exposed to okadaic acid. Toxicon 41: 93–97.
   PubMed Web of Science ®Google Scholar
• Coughlan, B. M., Hartl, M. G. J., O’Reilly, S. J., Sheehan, D., Morthersill, C., van Pelt, F. F. N. A. M., O’Halloran, J., and O’Brien, N. M. 2002. Detecting genotoxicity using the Comet assay following chronic exposure of Manila clam Tapes semidecussatus to polluted estuarine sediments. Mar. Pollut. Bull. 44: 1359–1365.
   PubMed Web of Science ®Google Scholar
• da Silva, C., Oba, E. T., Ramsdorf, W. A., Magalhaes, V. F., Cestari, M. M., Magalhães, V., Oliveira Ribeiro, C. A., and Cestari, M. M. 2011. First report about saxitoxins in freshwater fish Hoplias malabaricus through trophic exposure. Toxicon 57: 141–147.
   Google Scholar
• Díaz, P. A., Reguera, B., Ruiz-Villarreal, M., Pazos, Y., Velo-Suárez, L., Berger, H., and Sourisseau, M. 2013. Climate variability and oceanographic settings associated with interannual variability in the initiation of Dinophysis acuminata blooms. Mar. Drugs 11: 2964–2981.
   PubMed Web of Science ®Google Scholar
• Dominguez, H., Paz, B., Daranas, A., Norte, M., Franco, J., and Fernández, J. 2010. Dinoflagellate polyether within the yessotoxin, pectenotoxin and okadaic acid toxin groups: Characterization, analysis and human health implications. Toxicon 56: 191–217.
   PubMed Web of Science ®Google Scholar
• Eriksson, B. K. 2011. Does overfishing promote algal blooms? Directorate-General for Internal Policies, European Parliament.
   Google Scholar
• Ferraz-Mello, D., Proença, L. A. d. O., and Barracco, M. A. 2010. Comparative study of various immune parameters in three bivalve species during a natural bloom of Dinophysis acuminata in Santa Catarina Island, Brazil. Toxins 2: 1166–1178.
   PubMedGoogle Scholar
• Flórez-Barrós, F., Prado-Alvarez, M., Méndez, J., and Fernández-Tajes, J. 2011. Evaluation of genotoxicity in gills and hemolymph of clam Ruditapes decussatus fed with the toxic dinoflagellate Prorocentrum lima. J. Toxicol. Environ. Health A 74: 971–979.
   PubMed Web of Science ®Google Scholar
• Goldberg, E. D. 1986. The mussel watch concept. Environ. Monit. Assess. 7: 91–103.
   PubMed Web of Science ®Google Scholar
• Haberkorn, H., Lambert, C., Le Goïc, N., Moal, J., Suquet, M., Guéguen, M., Sunila, I., and Soudant, P. 2010. Effects of Alexandrium minutum exposure on nutrition-related processes and reproductive output in oysters Crassostrea gigas. Harmful Algae 9: 427–439.
   Web of Science ®Google Scholar
• Hanana, H., Talarmin, H., Pennec, J.-P., Droguet, M., Morel, J., and Dorange, G. 2012. Effect of okadaic acid on cultured clam heart cells: Involvement of MAPkinase pathways. Open Biol. 1: 1192–1199.
   Google Scholar
• Hégaret, H., da Silva, P. M., Wikfors, G. H., Haberkorn, H., Shumway, S. E., and Soudant, P. 2011.In vitro interactions between several species of harmful algae and haemocytes of bivalve molluscs. Cell Biol. Toxicol. 27: 249–266.
   PubMed Web of Science ®Google Scholar
• Hégaret, H., da Silva, P. M., Wikfors, G. H., Lambert, C., De Bettignies, T., Shumway, S. E., and Soudant, P. 2007. Hemocyte responses of Manila clams, Ruditapes philippinarum, with varying parasite, Perkinsus olseni, severity to toxic-algal exposures. Aquat. Toxicol. 84: 469–479.
   PubMed Web of Science ®Google Scholar
• Juhel, G., O’Halloran, J., Culloty, S. C., O’Riordan, R., Davenport, J., O’Brien, N. M., James, K. F., Furey, A., and Allis, O. 2007. In vivo exposure to microcystins induces DNA damage in the haemocytes of the zebra mussel, Dreissena polymorpha, as measured with the comet assay. Environ. Mol. Mutagen. 48: 22–29.
   PubMed Web of Science ®Google Scholar
• Lee, R. F., and Steinert, S. 2003. Use of the single cell gel electrophoresis/comet assay for detecting DNA damage in aquatic (marine and freshwater) animals. Mutat. Res. Rev. Mutat. 544: 43–64.
   PubMed Web of Science ®Google Scholar
• Malagoli, D., Casarini, L., and Ottaviani, E. 2008. Effects of the marine toxins okadaic acid and palytoxin on mussel phagocytosis. Fish Shellfish Immun. 24: 180–186.
   PubMed Web of Science ®Google Scholar
• McCarthy, M., O’Halloran, J., O’Brien, N. M., and van Pelt, F. F. N. A. M. 2014. Does the marine biotoxin okadaic acid cause DNA fragmentation in the blue mussel and the pacific oyster? Mar. Environ. Res. 101: 153–160.
   PubMed Web of Science ®Google Scholar
• Mitchelmore, C. L., and Chipman, J. K. 1998. DNA strand breakage in aquatic organisms and the potential value of the comet assay in environmental monitoring. Mutat. Res. 399: 135–147.
   PubMed Web of Science ®Google Scholar
• Pérez-Cadahía, B., Laffon, B., Pásaro, E., and Méndez, J. 2004. Evaluation of PAH bioaccumulation and DNA damage in mussels (Mytilus galloprovincialis) exposed to spilled Prestige crude oil. Comp. Biochem. Phys. C 138: 453–460.
   PubMed Web of Science ®Google Scholar
• Prado-Alvarez, M., Flórez-Barrós, F., Méndez, J., and Fernandez-Tajes, J. 2013. Effect of okadaic acid on carpet shell clam (Ruditapes decussatus) haemocytes by in vitro exposure and harmful algal bloom simulation assays. Cell Biol. Toxicol. 29: 189–197.
   PubMed Web of Science ®Google Scholar
• Prado-Alvarez, M., Flórez-Barrós, F., Sexto-Iglesias, A., Méndez, J., and Fernandez-Tajes, J. 2012. Effects of okadaic acid on haemocytes from Mytilus galloprovincialis: A comparison between field and laboratory studies. Mar. Environ. Res. 81: 90–93.
   PubMed Web of Science ®Google Scholar
• Prego-Faraldo, M. V., Valdiglesias, V., Méndez, J., and Eirín-López, J. M. 2013. Okadaic acid meet and greet: An insight into detection methods, response strategies and genotoxic effects in marine invertebrates. Mar. Drugs 11: 2829–2845.
   PubMed Web of Science ®Google Scholar
• Rank, J., and Jensen, K. 2003. Comet assay on gill cells and hemocytes from the blue mussel Mytilus edulis. Ecotoxicol. Environ. Safety 54: 323–329.
   PubMed Web of Science ®Google Scholar
• Rodríguez-Rodríguez, G., Villasante, S., and García-Negro, M. d. C. 2011. Are red tides affecting economically the commercialization of the Galician (NW Spain) mussel farming? Mar. Policy 35: 252–257.
   Web of Science ®Google Scholar
• Rossignoli, A. E., Fernández, D., Regueiro, J., Mariño, C., and Blanco, J. 2011. Esterification of okadaic acid in the mussel Mytilus galloprovincialis. Toxicon 57: 712–720.
   PubMed Web of Science ®Google Scholar
• Rossini, G. P., Sgarbi, N., and Malaguti, C. 2001. The toxic responses induced by okadaic acid involve processing of multiple caspase isoforms. Toxicon 39: 763–770.
   PubMed Web of Science ®Google Scholar
• Souid-Mensi, G., Moukha, S., Mobio, T. A., Maaroufi, K., and Creppy, E. E. 2008. The cytotoxicity and genotoxicity of okadaic acid are cell-line dependent. Toxicon 51: 1338–1344.
   PubMed Web of Science ®Google Scholar
• Svensson, S., and Förlin, L. 1998. Intracellular effects of okadaic acid in the blue mussel Mytilus edulis, and rainbow trout Oncorhynchus mykiss. Mar. Environ. Res. 46: 449–452.
   Web of Science ®Google Scholar
• Svensson, S., Särngren, A., and Förlin, L. 2003. Mussel blood cells, resistant to the cytotoxic effects of okadaic acid, do not express cell membrane p-glycoprotein activity (multixenobiotic resistance). Aquat. Toxicol. 65: 27–37.
   PubMed Web of Science ®Google Scholar
• Talarmin, H., Droguet, M., Pennec, J. P., Schröder, H. C., Muller, W. E. G., Gioux, M., and Dorange, G. 2008. Effects of a phycotoxin, okadaic acid, on oyster heart cell survival. Toxicol. Environ. Chem. 90: 153–168.
   Google Scholar
• Valdiglesias, V., Fernández-Tajes, J., Costa, C., Méndez, J., Pásaro, E., and Laffon, B. 2012a. Alterations in metabolism-related genes induced in SHSY5Y cells by okadaic acid exposure. J. Toxicol. Environ. Health A 75: 844–856.
   PubMed Web of Science ®Google Scholar
• Valdiglesias, V., Fernández-Tajes, J., Pásaro, E., Méndez, J., and Laffon, B. 2012b. Identification of differentially expressed genes in SHSY5Y cells exposed to okadaic acid by suppression subtractive hybridization. BMC Genomics 13: 46.
   PubMed Web of Science ®Google Scholar
• Valdiglesias, V., Méndez, J., Pásaro, E., Cemeli, E., Anderson, D., and Laffon, B. 2010. Assessment of okadaic acid effects on cytotoxicity, DNA damage and DNA repair in human cells. Mutat. Res. 689: 74–79.
   PubMed Web of Science ®Google Scholar
• Valdiglesias, V., Prego-Faraldo, M. V., Pasaro, E., Mendez, J., and Laffon, B. 2013. Okadaic acid: More than a diarrheic toxin. Mar. Drugs 11: 4328–4349.
   PubMed Web of Science ®Google Scholar
• Van Dolah, F. M. 2000. Marine algal toxins: Origins, health effects, and their increased occurrence. Environ. Health Perspect. 108: 133–141.
   PubMed Web of Science ®Google Scholar
• Venier, P., Maron, S., and Canova, S. 1997. Detection of micronuclei in gill cells and haemocytes of mussels exposed to benzo[a]pyrene. Mutat. Res. Gen. Toxicol. Eng. 390: 33–44.
   PubMed Web of Science ®Google Scholar
• Viarengo, A., and Canesi, L. 1991. Mussels as biological indicators of pollution. Aquaculture 94: 225–243.
   Web of Science ®Google Scholar
• Wilson, J. T., Pascoe, P. L., Parry, J. M., and Dixon, D. R. 1998. Evaluation of the comet assay as a method for the detection of DNA damage in the cells of a marine invertebrate, Mytilus edulis L. (Mollusca: Pelecypoda). Mutat. Res. 399: 87–95.
   PubMed Web of Science ®Google Scholar
• Yasumoto, T., Murata, M., Oshima, Y., Sano, M., Matsumoto, G. K., and Clardy, J. 1985. Diarrhetic shellfish toxins. Tetrahedron 41: 1019–1025.
   Web of Science ®Google Scholar