Multi-biomarker responses in the freshwater mussel Dreissena polymorpha exposed to polychlorobiphenyls and metals

Comparative Biochemistry and Physiology - C Toxicology and Pharmacology

Volumn 149, Issue 3, 2009, Pages 281-288

  Faria, Melissa ^a   Carrasco, Luis ^b   Diez, Sergi ^b,c   Riva, Maria Carmen ^a   Bayona, Josep Maria ^b   Barata, Carlos ^b  

^a UNIVERSITAT POLITÈCNICA DE CATALUNYA   (Spain)

^b INSTITUTE OF ENVIRONMENTAL ASSESSMENT AND WATER RESEARCH   (Spain)

^c INSTITUTE OF EARTH SCIENCES JAUME ALMERA   (Spain)

Author keywords

Cadmium; Dreissena polymorpha; EROD; Mercury; Methyl mercury; Oxidative stress; PCB

Indexed keywords

AROCLOR 1260; BIOLOGICAL MARKER; CADMIUM; CYTOCHROME P450 1A; ETHOXYRESORUFIN DEETHYLASE; GLUTATHIONE; MERCURY CHLORIDE; METALLOTHIONEIN; METHYLMERCURY; POLYCHLORINATED BIPHENYL DERIVATIVE;

ANIMAL EXPERIMENT; ARTICLE; BEHAVIOR CHANGE; CHEMICAL ANALYSIS; CONTROLLED STUDY; DNA STRAND BREAKAGE; DREISSENA; DREISSENA POLYMORPHA; ENVIRONMENTAL EXPOSURE; ENZYME ACTIVITY; EXOCRINE GLAND; LIPID PEROXIDATION; NONHUMAN; PRIORITY JOURNAL;

DREISSENA POLYMORPHA;

EID: 60949106024     PISSN: 15320456     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cbpc.2008.07.012     Document Type: Article

References (83)

1. Akcha F., Tanguy A., Leday G., Pelluhet L., Budzinski H., and Chiffoleau J.F. Measurement of DNA single-strand breaks in gill and hemolymph cells of mussels, Mytilus sp., collected on the French Atlantic Coast. Mar. Environ. Res. 2-5 (2004) 753-756
2. Aebi H. Catalase. In: Bergmeyer H.U. (Ed). Methods of Enzymatic Analysis (1974), Academic Press, London 671-684
3. Amiard J.C., Amiard-Triquet C., Barka S., Pellerin J., and Rainbow P.S. Metallothioneins in aquatic invertebrates: their role in metal detoxification and their use as biomarkers. Aquat. Toxicol. 76 (2006) 160-202
4. Anguiano G., Llera-Herrera R., Rojas E., and Vazquez-Boucard C. Subchronic organismal toxicity, cytotoxicity, genotoxicity, and feeding response of Pacific oyster (Crassostrea gigas) to lindane (gamma-HCH) exposure under experimental conditions. Environ. Toxicol. Chem 26 (2007) 2192-2197
5. Barata C., and Baird D.J. Determining the ecotoxicological mode of action of chemicals from measurements made on individuals: results from short-duration chronic tests with Daphnia magna Straus. Aquat. Toxicol. 48 (2000) 195-209
6. Barata C., Lekumberri I., Vila-Escale M., Prat N., and Porte C. Trace metal concentration, antioxidant enzyme activities and susceptibility to oxidative stress in the tricoptera larvae Hydropsyche exocellata from the Llobregat river basin (NE Spain). Aquat. Toxicol 74 (2005) 3-19
7. Bebianno M.J., Lopes B., Guerra L., Hoarau P., and Ferreira A.M. Glutathione S-transferases and cytochrome P450 activities in Mytilus galloprovincialis from the South coast of Portugal: effect of abiotic factors. Environ. Int. 33 (2007) 550-558
8. Berny P., Lachaux O., Buronfosse T., Mazallon M., and Gillet C. Zebra mussels (Dreissena polymorpha) as indicators of freshwater contamination with lindane. Environ. Res 90 (2002) 142-151
9. Binelli A., Galassi S., and Provini A. Factors affecting the use of Dreissena polymorpha as a bioindicator: the PCB pollution in Lake Como (N. Italy). Water Air Soil Pollut. 1-4 (2001) 19-32
10. Binelli A., Ricciardi F., Riva C., and Provini A. Screening of POP pollution by AChE and EROD activities in Zebra mussels from the Italian Great Lakes. Chemosphere 61 (2005) 1074-1082
11. Binelli A., Ricciardi F., Riva C., and Provini A. New evidences for old biomarkers: effects of several xenobiotics on EROD and AChE activities in zebra mussel (Dreissena polymorpha). Chemosphere 4 (2006) 510-519
12. Binelli A., Ricciardi F., Riva C., and Provini A. Integrated use of biomarkers and bioaccumulation data in Zebra mussel (Dreissena polymorpha) for site-specific quality assessment. Biomarkers 11 (2006) 428-448
13. Binelli A., Riva C., and Provini A. Biomarkers in Zebra mussel for monitoring and quality assessment of Lake Maggiore (Italy). Biomarkers 12 (2007) 349-386
14. Binelli A., Riva C., Cogni G., and Provini A. Genotox effects of p,p¢-DDT (1,1,1-Trichloro-2,2-Bis-(Chlorophenyl) ethane) and its metabolites in Zebra mussel (Dreissena polymorpha) by SCGE assay and micronucleous. Environ. Mol. Mutagen. 49 (2008) 406-415
15. Bradford M.M. Rapid and sensitive method for quantification of microgram quantities of protein utilizing principle of protein-dye binding. Anal. Biochem 1-2 (1976) 248-254
16. Burke M.D., and Mayer R.T. Ethoxyresorufin-direct fluorimetric assay of a microsomal O-dealkylation which is preferentially inducible by 3-methlycholanthrene. Drug Metab. Dispos. 2 (1974) 583-588
17. Camusso M., Balestrini R., and Binelli A. Use of zebra mussel (Dreissena polymorpha) to assess trace metal contamination in the largest Italian subalpine lakes. Chemosphere 44 (2001) 263-270
18. Canesi L., Viarengo A., Leonzio C., Filippelli M., and Gallo G. Heavy metals and glutathione metabolism in mussel tissues. Aquat. Toxicol 46 (1999) 67-76
19. Carlberg I., and Mannervik B. Glutathione reductase. Methods Enzymol. 113 (1985) 484-490
20. Cheung C.C.C., Zheng G.J., Lam P.K.S., and Richardson B.J. Relationships between tissue concentrations of chlorinated hydrocarbons (polychlorinated biphenyls and chlorinated pesticides) and antioxidant responses of marine mussels, Perna viridis. Mar. Pollut. Bull. 45 (2002) 181-191
21. Cheung C.C.C., Siu W.H.L., Richardson B., De Luca-Abbott S.B., and Lam P.K.S. Antioxidant responses to benzo[a]pyrene and Aroclor 1254 exposure in the green-lipped mussel, Perna viridis. Environ. Pollut. 128 (2004) 393-403
22. Clements W.H. Integrating effects of contaminants across levels of biological organization: an overview. J. Aquat. Ecosyst. Stress Recovery 7 (2000) 113-116
23. Cooper N.L., and Bidwell J.R. Cholinesterase inhibition and impacts on behavior of the Asian clam, Corbicula fluminea, after exposure to an organophosphate insecticide. Aquat. Toxicol. 3-4 (2006) 258-267
24. Coughlan J. Estimation of filtering rate from clearance of suspensions. Mar. Biol. 2 (1969) 356-358
25. Damiens G., Gnassia-Barelli M., Loques F., Romeo M., and Salbert V. Integrated biomarker response index as a useful tool for environmental assessment evaluated using transplanted mussels. Chemosphere 66 (2007) 574-583
26. De Lafontaine Y., Gagne F., Blaise C., Costan G., Gagnon P., and Chan H.M. Biomarkers in zebra mussels (Dreissena polymorpha) for the assessment and monitoring of water quality of the St Lawrence River (Canada). Aquat. Toxicol. 50 (2000) 51-71
27. De Luca-Abbott S.B., Richardson B.J., Mcclellan K.E., Zheng G.J., Martin M., and Lam P.K.S. Field validation of antioxidant enzyme biomarkers in mussels (Perna viridis) and clams (Ruditapes philippinarum) transplanted in Hong Kong coastal waters. Mar. Pollut. Bull. 51 (2005) 694-707
28. den Besten P.J. Concepts for the implementation of biomarkers in environmental monitoring. Mar. Environ. Res. 46 (1998) 1-5
29. Diez S., Montuori P., Querol X., and Bayona J.M. Total mercury in the hair of children by combustion atomic absorption spectrometry (Comb-AAS). J. Anal. Toxicol. 3 (2007) 144-149
30. Diez S., B., C., and Raldua D. Exposure to mercury: a critical assessment of adverse ecological and human health effects. In: Prasad M.N.V. (Ed). Trace Elements as Contaminants and Nutrients: Consequences in Ecosystems and Human Health (2008), Clapter 15, John Wiley & Sons, Inc., New Cork 345-373
31. Di Giulio R.T., Benson W.H., Sanders B.M.E., and Van Veld P.A. Biochemical mechanisms: metabolism, adaptation and toxicity. Fundamentals of Aquatic Toxicology. Effects, Environmental Fate and Risk Assessment (1995), E. G. R. T. A. Francis, London
32. Duquesne S., Liess M., and Bird D.J. Sub-lethal effects of metal exposure: physiological and behavioural responses of the estuarine bivalve Macoma balthica. Mar. Environ. Res. 2-5 (2004) 245-250
33. Engelken J., and Hildebrandt A. cDNA cloning and cadmium-induced expression of metallothionein mRNA in the zebra mussel Dreissena polymorpha. Biochem. Cell Biol. 77 (1999) 237-241
34. Esterbauer H., Schaur R.J., and Zollner H. Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radic. Biol. Med. 11 (1991) 81-128
35. Giambérini L., and Cajaraville M.P. Lysosomal responses in the digestive gland of the freshwater mussel, Dreissena polymorpha, experimentally exposed to cadmium. Environ. Res. 98 (2005) 210-214
36. Giguère A., Couillard Y., Campbell P.G.C., Perceval O., Hare L., Pinel-Alloul B., and Pellerin J. Steady-state distribution of metals among metallothionein and other cytosolic ligands and links to cytotoxicity in bivalves living along a polymetallic gradient. Aquat. Toxicol. 64 (2003) 185-200
37. Guerlet E., Ledy K., Meyer A., and Giambérini L. Towards a validation of a cellular biomarker suite in native and transplanted zebra mussels: a 2 year integrative field study of seasonal and polluted-induced variations. Aquat. Toxicol. 81 (2007) 377-388
38. Habig W.H., Pabst M.J., and Jakoby W.B. Glutathione S-transferase-first enzymatic step in mercapturic acid formation. J. Biol. Chem. 249 (1974) 7130-7139
39. Hanari N., Kannan K., Horii Y., Taniyasu S., Yamashita N., Jude D.J., and Berg M.B. Polychlorinated naphthalenes and polychlorinated biphenyls in benthic organisms of a Great Lakes food chain. Arch. Environ. Contam. Toxicol. 47 (2004) 84-93
40. Halliwell B., and Gutteridge J.M.C. Free radicals in biology and medicine (1999), Oxford University Press, London
41. Jewell C.S.E., and Winston G.W. Characterization of the microsomal mixed-function oxygenase system if the hepatopancreas and green gland of the red swamp crayfish, Procambarus clarkii. Comp. Biochem. Physiol. B 92 (1989) 329-339
42. Jorgensen C.B. Bivalve filter feeding revisited. Mar. Ecol.,Prog. Ser. 142 (1996) 287-302
43. Kamencic H., Lyon A., Paterson P.G., and Juurlink B.H.J. Monochlorobimane fluorometric method to measure tissue glutathione. Anal. Biochem. 286 (2000) 35-37
44. Kono Y., and Fridovich I. Speroxide radical inhibits catalase. J. Biol. Chem. 257 (1982) 5751-5754
45. Kraak M.H.S., Scholten M.C.T., Peeters W.H.M., and Dekock W.C. Biomonitoring of heavy-metals in the Western-European rivers Rhine and Meuse using the fresh-water mussel Dreissena polymorpha. Environ. Pollut. 74 (1991) 101-114
46. Kraak M.H.S., Kuipers F., Schoon H., Degroot C.J., and Admiraal W. The filtration-rate of the zebra mussel Dreissena polymorpha used for water-quality assessment in Dutch rivers. Hydrobiologia 294 (1994) 13-16
47. Kraak M.H.S., Wijnands P., Govers H.A.J., Admiraal W., and Devoogt P. Structural-based differences in ecotoxicity of benzoquinoline isomers to the zebra mussel (Dreissena polymorpha). Environ. Toxicol. Chem. 10 (1997) 2158-2163
48. Lawrence R.A., and Burk R.F. Glutathione peroxidase activity in selenium deficient rat liver. Biochem. Biophys. Res. Commun. 71 (1976) 952-958
49. Lecoeur S., Videmann B., and Berny P. Evaluation of metallothionein as a biomarker of single and combined Cd/Cu exposure in Dreissena polymorpha. Environ. Res. 94 (2004) 184-191
50. Lehmann D.W., Levine J.F., and Law J.M. Polychlorinated biphenyl exposure causes gonadal atrophy and oxidative stress in Corbicula fluminea clams. Toxicol. Pathol. 35 (2007) 356-365
51. Livingstone D.R. Contaminant-stimulated reactive oxygen species production and oxidative damage in aquatic organisms. Mar. Pollut. Bull. 42 (2001) 656-666
52. Livingstone D.R., and Stegeman J.J. Cytochrome P450 forms and functions in animals. Xenobiotica 19 (1989) 1037-1039
53. Livingstone D.R., Arnold R., Chipman K., Kirchin M.A., and Marsh J. The mixed-function oxygenase systems in mollusks-metabolism, responses to xenobiotics and toxicity. Biochem Mar Org 16 (1990) 331-347
54. Livingstone D.R., Martinez P.G., Michel X., Narbonne J.F., Ohara S., Ribera D., and Winston G.W. Oxyradical production as a pollution mediated mechanism of toxicity in the common mussel, Mytilus edulis and other molluscs. Funct. Ecol. 4 (1990) 415-424
55. Livingstone D.R., Lips F., Martinez P.G., and Pipe R.K. Antioxidant enzymes in the digestive gland of the common mussel Mytilus edulis. Mar. Biol. 112 (1992) 265-276
56. Livingstone D.R. Oxidative stress in aquatic organisms in relation to pollution and aquaculture. Rev. Med. Vet - Toulouse 154 (2003) 427-430
57. Marie V., Gonzalez P., Baudrimont M., Bourdineaud J.P., and Boudou A. Metallothionein response to cadmium and zinc exposures compared in two freshwater bivalves, Dreissena polymorpha and Corbicula fluminea. BioMetals 19 (2006) 300-407
58. Mc Cord J.M., and Fridovic I. Superoxide dismutase an enzymatic function for erythrocuprein (hemocuprein). J. Biol. Chem. 244 (1969) 6049
59. Minier C., Abarnou A., Jaouen-Madoulet A., and Le Guellec A.M. A pollution-monitoring pilot study involving contaminant and biomarker measurements in the Seine Estuary, France, using zebra mussels (Dreissena polymorpha). Environ. Toxicol. Chem. 25 (2006) 112-119
60. Mikac N., Picer M., Stegnar P., and Tusek-Znidaric M. Mercury distribution in a polluted marine area-ratio of total mercury, methyl mercury and selenium in sediments, mussels and fish. Water Res. 19 (1985) 1387-1392
61. Narbonne J.F., Mora P., Michel X., Budzinski H., Garrigues P., Lafaurie M., Salaun J.P., Berge J.B., Den Besten P., Pagano G., Porte C., Livingstone D., Hansen P.D., and Herbert A. Biological markers of environmental contamination in marine ecosystems: BIOMAR project. J. Toxicol., -Toxin Rev. 18 (1999) 205-220
62. Ni W., Trelease R.N., and Eising R. Two temporally synthesized charge subunits interact to form the five isoforms of cottonseed (Gossypium hirsutum) catalase. Biochemistry 269 (1990) 233-238
63. Olive P.L. DNA precipitation assay-a rapid and simple method for detecting DNA damage in mammalian cells. Environ. Mol. Mutagen. 11 (1988) 487-495
64. Osman A.M., van den Heuvel H., and van Noort P.C.M. Differential responses of biomarkers in tissues of a freshwater mussel, Dreissena polymorpha, to the exposure of sediment extracts with different levels of contamination. J. Appl. Toxicol. 27 (2007) 51-59
65. Paglia D.E., and Valentin W. Studies on quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J. Lab. Clin. Med. 70 (1967) 158-162
66. Pampanin D.M., Andersen O.K., Viarengo A., and Garrigues P. Background for the BEEP Stavanger workshops: biological effects on marine organisms in two common, large, C laboratory experiments and in a field study-comparison of the value (sensitivity, specificity, etc.) of core and new biomarkers. Aquat. Toxicol. 78 (2006) S1-S4
67. Porte C., Lemaire P., Peters L.D., and Livingstone D.R. Partial-purification and properties of cytochrome-P450 from digestive gland microsomes of the common mussel, Mytilus edulis L. Mar. Environ. Res. 39 (1995) 27-31
68. Porte C., Biosca X., Sole M., and Albaiges J. The integrated use of chemical analysis, cytochrome P450 and stress proteins in mussels to assess pollution along the Galician coast (NW Spain). Environ. Pollut 112 (2001) 261-268
69. Pruski A.M., and Dixon D.R. Effects of cadmium on nuclear integrity and DNA repair efficiency in the gill cells of Mytilus edulis L. Aquat. Toxicol. 57 (2002) 127-137
70. Ricciardi F., Binelli A., and Provini A. Use of two biomarkers (CYP450) in zebra mussel for the biomonitoring of Lake Maggiore (northern Italy). Ecotoxicol. Environ. Saf. 63 (2006) 406-412
71. Rocher B., Le Goff J., Peluhet L., Briand M., Manduzio H., Gallois J., Devier M.H., Geffard O., Gricourt L., Augagneur S., Budzinski H., Pottier D., Andre V., Lebailly P., and Cachot J. Genotoxicant accumulation and cellular defence activation in bivalves chronically exposed to waterborne contaminants from the Seine River. Aquat. Toxicol. 79 (2006) 65-77
72. Regoli F., Winston G.W., Mastrangelo V., Principato G., and Bompadre S. Total oxyradical scavenging capacity in mussel Mytilus sp. as a new index of biological resistance to oxidative stress. Chemosphere 37 (1998) 2773-2783
73. Rutzke M.A., Gutenmann W.H., Lisk D.J., and Mills E.L. Toxic and nutrient element concentrations in soft tissues of zebra and quagga mussels from Lakes Erie and Ontario. Chemosphere 40 (2000) 1353-1356
74. Schlenk D., Wolford L., Chelius M., Steevens J., and Chan K.M. Effect of arsenite, arsenate, and the herbicide monosodium methyl arsenate (MSMA) on hepatic metallothionein expression and lipid peroxidation in channel catfish. Comp. Biochem. Physiol. C. 118 (1997) 177-183
75. Sjoblom A., Meili M., and Sundbom M. The influence of humic substances on the speciation and bioavailability of dissolved mercury and methyl mercury, measured as uptake by Chaoborus larvae and loss by volatilization. Sci. Total Environ. 1-3 (2000) 115-124
76. Sole M., and Livingstone D.R. Components of the cytochrome P450-dependent monooxygenase system and NADPH-independent benzo[a]pyrene hydroxylase activity in a wide range of marine invertebrate species. Comp. Biochem. Physiol. C 1 (2005) 20-31
77. Stohs S.J., and Bagchi D. Oxidative mechanisms in the toxicity of metal-ions. Free Radic. Biol. Med. 18 (1995) 321-336
78. Van Der Oost R., Beyer J., and Vermeulen N.P.E. Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ. Toxicol. Pharmacol. 13 (2003) 57-149
79. Viarengo A., Burlando B., Cavaletto M., Marchi B., Ponzano E., and Blasco J. Role of metallothionein against oxidative stress in the mussel Mytilus galloprovincialis. Am. J. Physiol 277 (1999) R1612-R1619
80. Viarengo A., Burlando B., Ceratto N., and Panfoli I. Antioxidant role of metallothioneins: a comparative overview. Cell. Mol. Biol 46 (2000) 407-417
81. Voets J., Talloen W., de Tender T., van Dongen S., Covaci A., Blust R., and Bervoets L. Microcontaminant accumulation, physiological condition and bilateral asymmetry in zebra mussels (Dreissena polymorpha) from clean and contaminated surface waters. Aquat Toxicol. 79 (2006) 213-225
82. Whyte J.J., Jung R.E., Schmitt C.J., and Tillitt D.E. Ethoxyresorufin-O-deethylase (EROD) activity in fish as a biomarker of chemical exposure. Crit. Rev. Toxicol. 30 (2000) 347-570
83. Zar J.H. Biostatistical Analysis (1996), Prentice-Hall International, Inc., New Jersey