Genotoxicity assessment and detoxification induction in Dreissena polymorpha exposed to benzo[a]pyrene

Mutagenesis

Volumn 27, Issue 6, 2012, Pages 703-711

  Châtel, Amélie ^a,b,d   Faucet Marquis, Virginie ^c   Perret, Marine ^a   Gourlay Francé, Catherine ^a   Uher, Emmanuelle ^a   Pfohl Leszkowicz, Annie ^c   Vincent Hubert, Françoise ^a  

^a CEMAGREF   (France)

^b UNIVERSITÉ DE NANTES   (France)

^c UNIVERSITÉ DE TOULOUSE   (France)

^d UNIVERSITÉ CATHOLIQUE DE L'OUEST   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATIC HYDROCARBON; AROMATIC HYDROCARBON RECEPTOR; BENZO[A]PYRENE; CATALASE; GLUTATHIONE TRANSFERASE; HEAT SHOCK PROTEIN 70; HYDROCARBON; MULTIDRUG RESISTANCE PROTEIN; PHOSPHORUS 32; RIBOSOME PROTEIN; SUPEROXIDE DISMUTASE;

ARTICLE; BIOACCUMULATION; BIOLOGICAL MONITORING; CONTROLLED STUDY; DETOXIFICATION; DNA ADDUCT; DNA STRAND BREAKAGE; DREISSENA; DREISSENA POLYMORPHA; EXCISION REPAIR; EXOCRINE GLAND; FRESHWATER ENVIRONMENT; GENE EXPRESSION; GENOTOXICITY; GILL; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA EXTRACTION;

ANIMALS; BENZO(A)PYRENE; CATALASE; DNA DAMAGE; DREISSENA; ENVIRONMENTAL MONITORING; FRESH WATER; GENE EXPRESSION REGULATION; GILLS; GLUTATHIONE TRANSFERASE; HSP70 HEAT-SHOCK PROTEINS; METABOLIC DETOXICATION, DRUG; P-GLYCOPROTEIN; RECEPTORS, ARYL HYDROCARBON; RNA, MESSENGER; SUPEROXIDE DISMUTASE; WATER POLLUTANTS, CHEMICAL;

DREISSENA POLYMORPHA;

EID: 84868566831     PISSN: 02678357     EISSN: 14643804     Source Type: Journal    
DOI: 10.1093/mutage/ges036     Document Type: Article

References (74)

1. Bodin, N., Burgeot, T., Stanisière, J. Y., et al. (2004) Seasonal variations of a battery of biomarkers and physiological indices for the mussel Mytilus galloprovincialis transplanted into the northwest Mediterranean Sea. Comp. Biochem. Physiol. C. Toxicol. Pharmacol. 138, 411-427.
2. Le Goff, J., Gallois, J., Pelhuet, L., Devier, M. H., Budzinski, H., Pottier, D., André, V. and Cachot, J. (2006) DNA adduct measurements in zebra mussels, Dreissena polymorpha, Pallas: potential use for genotoxicant biomonitoring of fresh water ecosystems. Aquat. Toxicol., 79, 55-64.
3. Rocher, B., Le Goff, J., Peluhet, L., et al. (2006) Genotoxicant accumulation and cellular defence activation in bivalves chronically exposed to waterborne contaminants from the Seine River. Aquat. Toxicol., 79, 65-77.
4. Al-Subiai, S. N., Arlt, V. M., Frickers, P. E., Readman, J. W., Stolpe, B., Lead, J. R., Moody, A. J. and Jha, A. N. (2012) Merging nano-genotox-icology with eco-genotoxicology: an integrated approach to determine interactive genotoxic and sub-lethal toxic effects of C(60) fullerenes and fluoranthene in marine mussels, Mytilus sp. Mutat. Res. doi 10.1016.
5. Binelli, A., Riva, C. and Provini, A. (2007) Biomarkers in zebra mussel for monitoring and quality assessment of Lake Maggiore (Italy). Biomarkers, 12, 349-368.
6. Jha, A. N. (2008) Ecotoxicological applications and significance of the comet assay. Mutagenesis, 23, 207-221.
7. Bourgeault, A., Gourlay-France, C., Vincent-Hubert, F., Palais, F., Geffard, A., Biagianti-Risbourg, S., Pain-Devin, S. and Tusseau-Vuillemin, M. H. (2010) Lessons from a transplantation of zebra mussels into a small urban river: an integrated ecotoxicological assessment. Environ. Toxicol., 25, 468-478.
8. Michel, C. and Vincent-Hubert, F. (2012) Detection of 8-oxodG in Dreissena polymorpha gill cells exposed to model contaminants. Mutat. Res., 741, 1-6.
9. Kraak, M. H., Scholten, M. C., Peeters, W. H. and de Kock, W. C. (1991) Biomonitoring of heavy metals in the western European rivers Rhine and Meuse using the freshwater mussel Dreissena polymorpha. Environ. Pollut., 74, 101-114.
10. Secor, C. L., Mills, E. L., Harshberger, J., Kuntz, H. T., Gutenmann, W. H. and Lisk, D. J. (1993) Bioaccumulation of toxicants, element and nutrient composition, and soft tissue histology of zebra mussels (Dreissena poly-morpha) from New York state waters. Chemosphere, 26, 1559-1575.
11. de Lafontaine, Y., Gagne, F., Blaise, C., Costan, G., Gagnon, P. and Chan, H. M. (2000) Biomarkers in zebra mussels (Dreissena polymorpha) for the assessment and monitoring of water quality of the St Lawrence River (Canada). Aquat. Toxicol., 50, 51-71.
12. Fisher, S. W., Gossiaux, D. C., Bruner, K. A. and Landrum P. F. (1993) Investigations of the toxicokinetics of hydrophobic contaminants Cd in the zebra mussel (Dreissena polymorpha). In Nalepa, T. F. and Schloesser, D. W. (eds.), Zebra Mussels: Biology, Impacts, and Control. Lewis Publishers, Boca Raton, FL, USA, pp. 465-490.
13. Morton, B. (1997). The aquatic nuisance species problem: a global perspective and review. In D'Itri, F. M. (ed.), Zebra Mussels and Aquatic Nuisance Species. Ann Arbor Press, Inc, Chelsea, MI, USA, pp. 1-54.
14. Akopian, M., Garnier, J., Testard, P. and Ficht, A. (2001). Estimating the benthic population of Dreissena polymorpha and its impact in the lower Seine River, France. Estuaries, 24, 1003-1014.
15. Shaw, G. R. and Connell, D. W. (1994) Prediction and monitoring of the carcinogenicity of polycyclic aromatic compounds (PACs). Rev. Environ. Contam. Toxicol., 135, 1-62.
16. Kurelec, B., Chacko, M. and Gupta, R. C. (1988) Postlabeling analysis of carcinogen-DNA adducts in mussel, Mytilus galloprovincialis. Mar. Environ. Res. 24, 317-320.
17. Skarphéinsdóttir, H., Ericson, G., Dalla Zuanna, L. and Gilek, M. (2003) Tissue differences, dose-response relationship and persistence of DNA adducts in blue mussels (Mytilus edulis L.) exposed to benzo[a]pyrene. Aquat. Toxicol., 62, 165-177.
18. Pisoni, M., Cogotzi, L., Frigeri, A., et al. (2004) DNA adducts, benzo(a) pyrene monooxygenase activity, and lysosomal membrane stability in Mytilus galloprovincialis from different areas in Taranto coastal waters (Italy). Environ. Res., 96, 163-175.
19. Canova, S., Degan, P., Peters, L. D., Livingstone, D. R., Voltan, R. and Venier, P. (1998) Tissue dose, DNA adducts, oxidative DNA damage and CYP1A-immunopositive proteins in mussels exposed to waterborne benzo[a]pyrene. Mutat. Res., 399, 17-30.
20. Akcha, F., Izuel, C., Venier, P., Budzinski, H., Burgeot, T. and Narbonne, J. F. (2000) Enzymatic biomarker measurement and study of DNA adduct formation in benzo[a]pyrene contaminated mussels, Mytilus galloprovin-cialis. Aquat. Toxicol., 49, 269-287.
21. Randerath, K., Reddy, M. V. and Gupta, R. C. (1981) 32P-labeling test for DNA damage. Proc. Natl Acad. Sci. U.S.A., 78, 6126-6129.
22. Harvey, J. S. and Parry, J. M. (1997) The detection of genotoxin-induced DNA adducts in the common mussel Mytilus edulis. Mutagenesis, 12, 153-158.
23. Ericson, G., Skarphedinsdottir, H., Zuanna, L. D. and Svavarsson, J. (2002) DNA adducts as indicators of genotoxic exposure in indigenous and transplanted mussels, Mytilus edulis L. from Icelandic coastal sites. Mutat. Res., 516, 91-99.
24. Akcha, F., Vincent Hubert, F. and Pfhol-Leszkowicz, A. (2003) Potential value of the comet assay and DNA adduct measurement in dab (Limanda limanda) for assessment of in situ exposure to genotoxic compounds. Mutat. Res., 534, 21-32.
25. 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.
26. Fitzpatrick, P. J., O'Halloran, J., Sheehan, D. and Walsh, A. R. (1997) Assessment of glutathione-S-transferase and related proteins in the gill and digestive gland of Mytilus edulis as a potential organic pollution biomark-ers. Biomarkers, 2, 51-56.
27. Navarro, A., Faria, M., Barata, C. and Pina, B. (2011) Transcriptional response of stress genes to metal exposure in zebra mussel larvae and adults. Environ. Pollut., 159, 100-107.
28. Ketterer, B., Coles, B. and Meyer, D. J. (1983) The role of glutathione in detoxication. Environ. Health Perspect., 49, 59-69.
29. Pain, S. and Parant, M. (2003) Multixenobiotic defense mechanism (MDMX) in bivalves. C. R. Biol., 326, 659-672.
30. Minier, C., Abarnou, A., Jaouen-Madoulet, A., Le Guellec, A. M., Tutundjian, R., Bocquené, G. and Leboulenger, F. (2006) A pollution-monitoring pilot study involving contaminant and biomarker measurements in the Seine Estuary, France, using zebra mussels (Dreissena polymorpha). Environ. Toxicol. Chem., 25, 112-119.
31. Jha, A. N. (2004) Genotoxicological studies in aquatic organisms: an overview. Mutat. Res., 552, 1-17.
32. Faucet, V., Pfohl-Leszkowicz, A., Dai, J., Castegnaro, M. and Manderville, R. A. (2004) Evidence for covalent DNA adduction by ochratoxin A following chronic exposure to rat and subacute exposure to pig. Chem. Res. Toxicol., 17, 1289-1296.
33. Amat-Bronnert, A., Castegnaro, M. and Pfohl-Leszkowicz, A. (2006) Genotoxic activity and induction of biotransformation enzymes in two human cell lines after treatment by Erika fuel extract. Environ. Toxicol. Pharmacol., 23, 89-95.
34. Grebenjuk, V. A., Kuusksalu, A., Kelve, M., Schutze, J., Schroder, H. C. and Muller, W. E. (2002) Induction of (2'-5')oligoadenylate synthetase in the marine sponges Suberites domuncula and Geodia cydonium by the bacterial endotoxin lipopolysaccharide. Eur. J. Biochem., 269, 1382-1392.
35. Contardo-Jara, V., Pflugmacher, S., Nutzmann, G., Kloas, W. and Wiegand, C. (2010) The beta receptor blocker metoprolol alters detoxification processes in the non-target organism Dreissena polymorpha. Environ. Pollut., 158, 2059-2066.
36. Phillips, D. H. and Castegnaro, M. (1999) Standardization and validation of DNA adduct postlabelling methods: report of interlaboratory trials and production of recommended protocols. Mutagenesis, 14, 301-315.
37. Faucet-Marquis, V. (2005) Identification des métabolites de l'ochratoxine A responsable des effets cancérogènes et des adduits à l'ADN. Thèse. INP Toulouse.
38. Amat, A., Castegnaro, M. and Pfohl-Leszkowicz, A. (2004) Genotoxic activity of thiophenes on human cell line (HEPG2). Polycycl. Aromat. Hydrocarbon, 24, 733-742.
39. Newbold, R. F and Brookes, P. (1976) Exceptional mutagenicity of a benzo(a)pyrene diol epoxide in cultured mammalian cells. Nature, 261, 52-54.
40. Osborne, M. R., Jacobs, S., Harvey, R. G. and Brookes, P. (1981) Minor products from the reaction of (+) and (-) benzo[a]pyreneanti-diol epoxide with DNA. Carcinogenesis, 2 553-558.
41. 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. (Fundam. Mol. Mech. Mutat.), 399, 87-95.
42. Mitchelmore, C. L., Birmelin, C., Livingstone, D. R. and Chipman, J. K. (1998) Detection of DNA strand breaks in isolated mussel (Mytilus edu-lis L.) digestive gland cells using the "Comet" assay. Ecotoxicol. Environ. Saf., 41, 51-58.
43. Akcha, F., Burgeot, T., Venier, P. and Narbonne, J. F. (1999) Relationship between kinetics of benzo[a]pyrene bioaccumulation and DNA binding in the mussel Mytilus galloprovincialis. Bull. Environ. Contam. Toxicol., 62, 455-462.
44. Skarphéinsdóttir, H., Ericson, G. Halldórsson, H. P. and Svavarsson, J. (2005). Seasonal and intertidal impact on DNA adduct levels in gills of blue mussels (Mytilus edulis L.). Environ. Pollut., 136, 1-9.
45. Seo, Y. R. and Jung, H. J. (2004) The potential roles of p53 tumor suppressor in nucleotide excision repair (NER) and base excision repair (BER). Exp. Mol. Med., 36, 505-509.
46. Smith, M. L., Ford, J. M., Hollander, M. C., Bortnick, R. A., Amundson, S. A., Seo, Y. R., Deng, C. X., Hanawalt, P. C. and Fornace, A. J., Jr. (2000) p53-Mediated DNA repair responses to UV radiation: studies of mouse cells lacking p53, p21, and/or gadd45 genes. Mol. Cell Biol., 20, 3705-3714.
47. Prevodnik, A., Lilja, K. and Bollner, T. (2007) Benzo[a]pyrene up-regu-lates the expression of the proliferating cell nuclear antigen (PCNA) and multixenobiotic resistance polyglycoprotein (P-gp) in Baltic Sea blue mussels (Mytilus edulis L.). Comp. Biochem. Physiol. C. Toxicol. Pharmacol., 145, 265-274.
48. Whitlock, J. P., Jr. (1999) Induction of cytochrome P4501A1. Annu. Rev. Pharmacol. Toxicol., 39, 103-125.
49. Hankinson, O. (1993) Research on the aryl hydrocarbon (dioxin) receptor is primed to take off. Arch. Biochem. Biophys., 300, 1-5.
50. Hahn, M. E., Allan, L. L. and Sherr, D. H. (2009) Regulation of constitutive and inducible AHR signaling: complex interactions involving the AHR repressor. Biochem. Pharmacol., 77, 485-497.
51. Contardo-Jara, V., Lorenz, C., Pflugmacher, S., Nutzmann, G., Kloas, W. and Wiegand, C. (2011) Molecular effects and bioaccumulation of lev-onorgestrel in the non-target organism Dreissena polymorpha. Environ. Pollut., 159, 38-44.
52. Pelkonen, O. and Nebert, D. W. (1982). Metabolism of polycyclic aromatic hydrocarbons: etiologic role in carcinogenesis. Pharmacol. Rev., 34, 189.
53. Porte, C., Sole, M., Albaiges, J. and Livingstone, D. R. (1991) Responses of mixed-function oxygenase and antioxidase enzyme system of Mytilus sp. to organic pollution. Comp. Biochem. Physiol. C., 100, 183-186.
54. Sole, M., Porte, C. and Albaiges, J. (1995) The use of biomarkers for assessing the effects of organic pollution in mussels. Sci. Total Environ., 159, 147-153.
55. Regoli, F., Winston, G. W., Gorbi, S., Frenzilli, G., Nigro, M., Corsi, I. and Focardi, S. (2003) Integrating enzymatic responses to organic chemical exposure with total oxyradical absorbing capacity and DNA damage in the European eel Anguilla anguilla. Environ. Toxicol. Chem., 22, 2120-219.
56. Osman, A. M., van den Heuvel, H., van Noort, P. C. (2007) Differential responses of biomarkers in tissues of a freshwater mussel, Dreissena poly-morpha, to the exposure of sediment extracts with different levels of contamination. J. Appl. Toxicol., 27, 51-59.
57. Fitzpatrick, P. J. and Sheehan, D. (1993) Separation of multiple forms of glutathione S-transferase from the blue mussel, Mytilus edulis. Xenobiotica, 23, 851-861.
58. Fitzpatrick, P. J., Krag, T. O., Højrup, P. and Sheehan, D. (1995) Characterization of a glutathione S-transferase and a related glutathione-binding protein from gill of the blue mussel, Mytilus edulis. Biochem. J., 305, 145-150.
59. Santovito, G., Piccinni, E., Cassini, A., Irato, P. and Albergoni, V. (2005) Antioxidant responses of the Mediterranean mussel, Mytilus galloprovin-cialis, to environmental variability of dissolved oxygen. Comp. Biochem. Physiol. C. Toxicol. Pharmacol., 140, 321-329.
60. Hoarau, P., Garello, G., Gnassia-Barelli, M., Romeo, M. and Girard, J. P. (2002) Purification and partial characterization of seven glutathione S-transferase isoforms from the clam Ruditapes decussatus. Eur. J. Biochem., 269, 4359-4366.
61. Board, P. G., Baker, R. T., Chelvanayagam, G. and Jermiin, L. S. (1997) Zeta, a novel class of glutathione transferases in a range of species from plants to humans. Biochem. J., 328, 929-935.
62. Edwards, R., Dixon, D. P. and Walbot, V. (2000) Plant glutathione S-transferases: enzymes with multiple functions in sickness and in health. Trends Plant Sci., 5, 193-198.
63. Sheehan, D., Meade, G., Foley, V. M. and Dowd, C. A. (2001) Structure, function and evolution of glutathione transferases: implications for classification of non-mammalian members of an ancient enzyme superfamily. Biochem. J., 360, 1-16.
64. Hoarau, P., Garello, G., Gnassia-Barelli, M., Romeo, M. and Girard, J. P. (2004) Effect of three xenobiotic compounds on glutathione S-transferase in the clam Ruditapes decussatus. Aquat. Toxicol., 68, 87-94.
65. Hoarau, P., Damiens, G., Roméo, M., Gnassia-Barelli, M. and Bebianno, M. J. (2006) Cloning and expression of a GST-pi gene in Mytilus gallopro-vincialis. Attempt to use the GST-pi transcript as a biomarker of pollution. Comp. Biochem. Physiol. C. Toxicol. Pharmacol., 143, 196-203.
66. Bard, S. M. (2000) Multixenobiotic resistance as a cellular defense mechanism in aquatic organisms. Aquat. Toxicol., 1, 357-389.
67. Smital, T., Sauerborn, R. and Hackenberger, B. K. (2003) Inducibility of the P-glycoprotein transport activity in the marine mussel Mytilus gal-loprovincialis and the freshwater mussel Dreissena polymorpha. Aquat. Toxicol., 65, 443-465.
68. Franzellitti, S., Buratti, S., Valbonesi, P., Capuzzo, A. and Fabbri, E. (2011) The β-blocker propranolol affects cAMP-dependent signaling and induces the stress response in Mediterranean mussels, Mytilus galloprovincialis. Aquat. Toxicol., 101, 299-308.
69. Kurelec, B. (1995) Reversion of the multixenobiotic resistance mechanism in gills of marine mussel Mytilus galloprovincialis by a model inhibitor and environmental modulators of P170-glycoprotien. Aquat. Toxicol., 33, 93-103.
70. Zheng, S. L., Sun, T. H., Xiao, H., Qiu, X. Y. and Song, Y. F. (2008) Low dose benzo(a)pyrene up-regulated the transcription of HSP70 and HSP90 in Eisenia fetida. Ying Yong Sheng Tai Xue Bao, 19, 401-406.
71. Werner, E. E. (1998) Ecological experiments and a research program in community ecology. In Resetarits, W. J. J. and Bernardo, J. (eds.), Experimental Ecology: Issues and Perspectives. Oxford University Press, Oxford, UK, pp. 3-26.
72. Sole, M., Porte, C., Biosca, X., Mitchelmore, C. L., Chipman, J. K. and Livingstone, D. R. (1996) Effects of the 'Aegean Sea' oil spill on biotransformation enzymes, oxidative stress and DNA-adducts in digestive gland of the mussel (Mytilus edulis L.). Comp. Biochem. Physiol., 113, 257-265.
73. Contardo-Jara V. and Wiegand C. (2008) Molecular biomarkers of Dreissena polymorpha for evaluation of renaturation success of a formerly sewage polluted stream. Environ. Pollut., 155, 182-189.
74. Vincent-Hubert, F., Arini, A. and Gourlay-Francé, C. (2011) Early geno-toxic effects in gill cells and haemocytes of Dreissena polymorpha exposed to cadmium, B[a]P and a combination of B[a]P and Cd. Mutat. Res., 723, 26-35.