Biomarkers in marine mussels, Mytilus galloprovincialis, exposed to environmentally relevant levels of the pesticides, chlorpyrifos and penoxsulam

Aquatic Toxicology

Volumn 126, Issue , 2013, Pages 338-345

  Patetsini, E ^a   Dimitriadis, V K ^a   Kaloyianni, M ^a  

^a ARISTOTLE UNIVERSITY OF THESSALONIKI   (Greece)

Author keywords

Biomarkers; Carbonylation; DNA damage; LMS; Oxidative stress; Pollutants; ROS

Indexed keywords

BIOLOGICAL MARKER; CHLORPYRIFOS; PENOXSULAM; PESTICIDE; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

ANTIOXIDANT; BIOMARKER; CHLORPYRIFOS; CONCENTRATION (COMPOSITION); DNA; MEMBRANE; MOLLUSC; PHYSIOLOGICAL RESPONSE; POLLUTANT; PROTEIN;

ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; BLOOD CELL; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DNA DAMAGE; ENVIRONMENTAL EXPOSURE; HEMOLYMPH; LONG TERM EXPOSURE; LYSOSOME MEMBRANE; MEMBRANE STABILIZATION; MYTILUS GALLOPROVINCIALIS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN CARBONYLATION;

ANIMALS; ANTIOXIDANTS; BIOLOGICAL MARKERS; CHLORPYRIFOS; DNA DAMAGE; ENVIRONMENTAL EXPOSURE; HEMOCYTES; HEMOLYMPH; MYTILUS; PROTEIN CARBONYLATION; REACTIVE OXYGEN SPECIES; SULFONAMIDES; URIDINE; WATER POLLUTANTS, CHEMICAL;

ANIMALIA; MYTILIDAE; MYTILUS GALLOPROVINCIALIS;

EID: 84871766500     PISSN: 0166445X     EISSN: 18791514     Source Type: Journal    
DOI: 10.1016/j.aquatox.2012.09.009     Document Type: Article

References (70)

1. Alamdari H.D., Kostidou E., Paletas K., Sarigianni M., Konstas G.P.A., Karapiperidou A., Koliakos G. High sensitivity enzyme-linked immunosorbent assay (ELISA) method for measuring protein carbonyl in samples with low amounts of protein. Free Radical Biology and Medicine 2005, 39:1362-1367.
2. Alamdari H.D., Paletas K., Pegiou T., Sarigianni M., Befani C., Koliakos G. A novel assay for the evaluation of the prooxidant-antioxidant balance, before and after antioxidant vitamin administration in type II diabetes patients. Clinical Biochemistry 2007, 40:248-254.
3. Almroth C.B., Sturve J., Berglund A., Förlin L. Oxidative damage in eelpout (Zoarces viviparus), measured as protein carbonyls and TBARS, as biomarkers. Aquatic Toxicology 2005, 73:171-180.
4. Ames B.N., Shigenaga M.K., Hagen T.M. Oxidants, antioxidants, and the degenerative diseases of aging. Proceedings of the National Academy of Sciences of the United States of America 1993, 99:7915-7922.
5. Anderson D., Yu T.-W., Phillips B.J., Schmezer P. The effect of various antioxidants and other modifying agents on oxygen-radical-generated DNA damage in human lymphocytes in the Comet assay. Mutation Research 1994, 307:261-271.
6. Buss I.H., Chan T.P., Sluis K.B., Domigan N.M., Winterbourn C.C. Protein carbonyl measurement by a sensitive ELISA method. Free Radical Biology and Medicine 1997, 23:361-366.
7. Canesi L., Negri A., Barmo C., Banni M., Gallo G., et al. The Organophosphate Chlorpyrifos Interferes with the Responses to 17β-Estradiol in the digestive gland of the marine mussel Mytilus galloprovincialis. PLoS One 2011, 6(5):e19803.
8. Collin H., Meistertzheim A.L., David E., Moraga D., Boutet I. Response of the Pacific oyster Crassostrea gigas. Thunberg 1793, to pesticide exposure under experimental conditions. Journal of Experimental Biology 2010, 213:4010-4017.
9. Charizopoulos E., Papadopoulou-Mourkidou E. Occurrence of pesticides in rain of the Axios river basin, Greece. Environmental Science and Technology 1999, 33:2363-2368.
10. Clement B., Devaux A., Perrodin Y., Danjean M., Ghidini-Fatus M. Assessment of sediment ecotoxicity and genotoxicity in freshwater laboratory microcosms. Ecotoxicology 2004, 12:323-333.
11. Collen J., Pinto E., Pedersen M., Colepicolo P. Induction of oxidative stress in the red macroalga Gracilaria tenuistipitata by pollutant metals. Archives of Environment Contamination and Toxicology 2003, 45:337-342.
12. Costa V.M., Amorim M.A., Quintanilha A., Moradas-Ferreira P. Hydrogen peroxideinduced carbonylation of key metabolic enzymes in Saccharomyces cerevisiae: the involvement of the oxidative stress response regulators Yap1 and Skn7. Free Radical Biology and Medicine 2002, 33:1507-1515.
13. Dailianis S., Domouhtsidou G.P., Raftopoulou E., Kaloyianni M., Dimitriadis V.K. Evaluation of neutral red retention assay, micronucleus test, acetylocholinesterase activity and a signal transduction molecule (cAMP) in tissues of Mytilus galloprovincialis (L.) on pollution monitoring. Marine Environment Research 2003, 56:443-470.
14. + exchanger and PKC. Free Radical Research 2005, 39:1059-1070.
15. Dailianis S., Patetsini E., Kaloyianni M. The role of signalling molecules on actin glutathionylation and protein carbonylation induced by cadmium in haemocytess of mussel Mytilus galloprovincialis (Lmk). Journal of Experimental Biology 2009, 212:3612-3620.
16. Danellakis D., Ntaikou I., Kornaros M., Dailianis S. Olive oil mill wastewater toxicity in the marine environment: alterations of stress indices in tissues of mussel Mytilus galloprovincialis. Aquatic Toxicology 2011, 101:358-366.
17. Davies S.M., Poljak A., Duncan M.W., Smythe G.A., Murphy M.P. Measurements of protein carbonyls, ortho- and meta-tyrosine and oxidative phosphorylation complex activity in mitochondria from young and old rats. Free Radical Biology and Medicine 2001, 31:181-190.
18. Davies K.J.A., Delsignore M.E., Lin S.W. Protein damage by oxygen radicals. II. Modification of amino acids. Journal of Biological Chemistry 1987, 262:9902-9907.
19. Dondero F., Banni M., Negri A., Boatti L., Dagnino A., Viarengo A. Interactions of a pesticide/heavy metal mixture in marine bivalves: a transcriptomic assessment. BMC Genomics 2011, 12:195. 10.1186/1471-2164-12-195.
20. Dowling V., Pascal C., Hoarau P.C., Romeo M., O'Halloran J., van Pelt F., O'Brien N., Sheehan D. Protein carbonylation and heat shock response in Ruditapes decussatus following p,p'-dichlorodiphenyldichloroethylene (DDE) exposure: a proteomic approach reveals that DDE causes oxidative stress. Aquatic Toxicology 2006, 77:11-18.
21. Fal'f Fal'fushins'ka H.I., Hnatyshyna L.L., Stoliar O.B. Population-related peculiarities of molecular stress-responsive systems of bivalve mollusk under the effect of tetrazine pesticide. Ukrainskii Biokhimicheskii Zhurnal 2012, 84(1):90-97.
22. Franzellitti S., Capuzzo A., Viarengo A., Fabbri E. Interactive effects of nickel and chlorpyrifos on Mediterranean mussel cAMP-mediated cell signalling and MXR-related gene expressions. Comparative Biochemistry and Physiology C: Comparative Pharmacology 2011, 154:377-382.
23. Frenzilli G., Nigro M., Scarcelli V., Gorbi S., Regoli F. DNA integrity and total oxiradical scavenging capacity in the Mediterranean mussel. Mytilus galloprovinciales: a field study in a highly eutrophicated coastal lagoon. Aquatic Toxicology 2001, 53:19-32.
24. Geret F., Jouan A., Turpin V., Bebianno M.J., Cosson R.P. Influence of metal exposure on metallothionein synthesis and lipid peroxidation in two bivalves mollusks: the oyster (Crassostrea gigas) and the mussel (Mytilus edulis). Aquatic Living Resources 2002, 15:61-66.
25. Ghezzi P., Bonetto V. Redox proteomics: identification of oxidatively modified proteins. Proteomics 2003, 3:1145-1153.
26. Gómez-Mendikute A., Cajaraville M.P. Comparative effects of cadmium, copper, paraquat and benzo[a]pyrene on the actin cytoskeleton and production of reactive oxygen species (ROS) in mussel haemocytes. Toxicology In Vitro 2003, 17(5-6):539-546.
27. Grune T. Oxidative stress, aging and the proteasomal system. Biogerontology 2000, 1:31-40.
28. Gultekin F., Ozturk M., Agdogan M. The effect of organophosphate insecticide chlorpyrifos-ethyl on lipid peroxidation and antioxidant enzymes (in vitro). Molecular Toxicology 2000, 74:533-538.
29. Gupta S.C., Siddique H.R., Mathur N., Vishwakarma A.L., Mishra R.K., Saxena D.K., Chowdhuri D.K. Induction of hsp70, alterations in oxidative stress markers and apoptosis against dichlorvos exposure in transgenic Drosophila melanogaster: modulation by reactive oxygen species. Biochimica et Biophysica Acta 2007, 1770:1382-1394.
30. Irani K. Oxidant signaling in vascular cell growth, death, and survival: a review of the roles of reactive oxygen species in smooth muscle and endothelial cell mitogenic and apoptotic signalling. Circulation Research 2000, 87:179-183.
31. Ischiropoulos H., Gow A., Thom S.R., Kooy N.W., Royall J.A., Crow J.P. Detection of reactive nitrogen species using 2,7-dichlorodihydrofluorescein and dihydrorhodamine 123. Methods in Enzymology 1999, 301:367-373.
32. Itziou A., Kaloyianni M., Dimitriadis V.K. Effects of organic contaminants in reactive oxygen species, protein carbonylation and DNA damage on digestive gland and haemolymph of land snails. Chemosphere 2011, 85:1101-1107.
33. Jha A.N., Dogra Y., Turner A., Millward G.E. Impact of low doses of tritium on the marine mussel. Mytilus edulis: genotoxic effects and tissue specific bioconcentration. Mutation Research 2005, 586:47-57.
34. Kaloyianni M., Dailianis S., Chrisikopoulou E., Zannou A., Koutsogiannaki S., Alamdari D.H., Koliakos G., Dimitriadis V.K. Oxidative effects of inorganic and organic contaminants on haemolymph of mussels. Comparative Biochemistry and Physiology C: Comparative Pharmacology 2009, 149:631-639.
35. Kasprzak K.S., Diwan B.A., Rice J.M., Misra M., Eiggs C.W., Olinski R., Dizdaroglu M. Nickel(II)-mediated oxidative DNA base damage in renal cells. Chemical Research in Toxicology 1992, 5:809-815.
36. Kirchin M.A., Moore M.N., Dean R.T., Winston G.W. The role of oxyradicals in intracellular proteolysis and toxicity in mussels. Marine Environment Research 1992, 34:315-320.
37. + exchanger (NHE) activation by ROS. Aquatic Toxicology 2006, 315-324.
38. Lee M.Y., Shin H.W. Cadmium-induced changes in antioxidant enzymes from the marine alga Nannochloropsis oculata. Journal of Applied Physiology 2003, 15:13-19.
39. Lee S.E., Pâques F., Sylvan J., Haber J.E. Role of yeast SIR genes and mating type in channeling double-strand breaks to homologous and nonhomologous recombination pathways. Current Biology 1999, 9:767-770.
40. Lemus R., Abdelghani A. Chlorpyrifos: an unwelcome pesticide in our homes. Reviews on Environmental Health 2000, 15:421-433.
41. Levine R.L., Garland D., Oliver C.N., Amici A., Climent I., Lenz A. Determination of carbonyl content in oxidatively modified proteins. Methods in Enzymology 1990, 186:464-478.
42. Lowe D.M., Pipe R.K. Contaminant induced lysosomal membrane damage in marine mussel digestive cells: an in vitro study. Aquatic Toxicology 1994, 30:357-365.
43. Misra M., Olinski R., Dizdaroglu M., Kasprzak K.S. Enhancement by l-histidine of nickel(II) induced DNA protein cross-links and oxidative DNA base damage in the rat kidney. Chemical Research in Toxicology 1993, 6:33-37.
44. Moore M.N., Pipe R.K., Farrar S.V. Lysosomal and microsomal responses to environmental factors in Littorina littorea from Sullom Voe. Marine Pollutution Bulletin 1982, 13:340-345.
45. Moore M.N. Lysosomal responses to a polynuclear aromatic hydrocarbon in a marine snail: effects of exposure to phenanthrene and recovery. Marine Environment Research 1985, 17:230-233.
46. Moore M.N., Lowe D.M., Livingstone D.R., Dixon D.R. Molecular and cellular indices of pollutants effects and their use in environmental impact assessment. Water Science and Technology 1986, 18:223-232.
47. Murphy M.E., Kherer J.P. Oxidation state of tissue thiol groups and content of protein carbonyl groups in chickens with inherited muscular dystrophy. Biochemical Journal 1989, 260:359-364.
48. Myhre O., Andersen J.M., Aarnes H., Fonnum F. Evaluation of the probes 2,7-dichlorofluorescin diacetate, luminal, and lucigenin as indicators or reactive species formation. Biochemical Pharmacology 2003, 65:1575-1582.
49. Nigro M., Frenzilli G., Scarcelli V., Gorbi S., Regoli F. Induction of DNA strand breakage and apoptosis in the eel Anguilla anguilla. Marine Environment Research 2002, 54:517-520.
50. Ochi T., Takahashi K., Ohsawa M. Indirect evidence for the induction of a pro-oxidant state by cadmium chloride in cultured mammalian cells and a possible mechanism for the induction. Mutation Research 1987, 180:257-266.
51. Rahman M.F., Mahboob M., Danadevi K., Saleha B.B., Paramjit G. Assessment of genotoxic effects of chloropyriphos and acephate by the comet assay in mice leucocytes. Mutation Research 2002, 516:139-147.
52. Regoli F., Winston G.W., Gorbi S., Frenzilli G., Nigro M., Corsi I., Focardi S. Integrating enzymatic responses to organic chemical exposure with total oxyradical absorbing capacity and DNA damage in the European eel Anguilla anguilla. Environmental Toxicology and Chemistry 2003, 22:2120-2129.
53. Reinecke S.A., Reinecke A.J. The comet assay as biomarker of heavy metal genotoxicity in earthworms. Archives of Environment Contamination and Toxicology 2004, 46:208-215.
54. Ritter D., Knebel J. Genotoxicity testing in vitro-development of a higher throughput analysis method based on the comet assay. Toxicology In Vitro 2009, 23:1570-1575.
55. Rosenkranz A.R., Schmaldienst S., Stuhlmeier K.M., Chen W., Knapp W., Zlabinger G.J. A microplate assay for the detection of oxidative products using 2,7-dichlorofluorescin-diacetate. Journal of Immunological Methods 1992, 156:39-45.
56. Rota C., Chignell C.F., Mason R.P. Evidence for free radical formation during the oxidation of 2,7-dichlorofluoroscin to the fluorescent dye 20,70 dichlorofluoroscein by horseradish peroxide: possible implications for oxidative stress measurements. Free Radical Biology and Medicine 1999, 27:873-881.
57. Rota C., Fann Y.C., Mason R.P. Phenoxyl free radical formation during the oxidation of the fluorescent dye 2,7-dichlorofluoroscein by horseradish peroxide: Possible consequences for oxidative stress measurements. Journal of Biological Chemistry 1999, 274:28161-28168.
58. 2 in culrtured endothelial cells. Archives of Biochemistry and Biophysics 1993, 302:348-355.
59. Saleha B.B., Danadevi K., Rahman M.F., Ahuja Y.R., Kaiser J. Genotoxic effect of monocrotophos to sentinel species using comet assay. Food and Chemical Toxicology 2001, 39:361-366.
60. Shi H., Sui Y., Wang X., Luo Y., Ji L. Hydroxyl radical production and oxidative damage induced by cadmium and naphthalene in liver of Carassius auratus. Comparative Biochemistry and Physiology C 2005, 140:115-121.
61. Souza D.S., Ramos A.P., Nunes F.F., Moresco V., Taniguchi S., Leal D.A., Sasaki S.T., Bícego M.C., Montone R.C., Durigan M., Teixeira A.L., Pilotto M.R., Delfino N., Franco R.M., Melo C.M., Bainy A.C., Barardi C.R. Evaluation of tropical water sources and mollusks in southern Brazil using microbiological, biochemical, and chemical parameters. Ecotoxicology and Environment Safety 2012, 76:153-161.
62. Stadtman E.R., Oliver C.N. Metal-catalyzed oxidation of proteins. Journal of Biological Chemistry 1991, 266:2005-2008.
63. Tuzmen N., Candan N., Kaya E., Demiryas N. Biochemical effects of chlorpyrifos and deltamethrin on altered antioxidative defense mechanisms and lipid peroxidation in rat liver. Cell Biochemistry and Function 2008, 26:119-124.
64. Valavanidis A., Vlahogianni Th., Dassenakis M., Scoullos M. Molecular biomarkers of oxidative stress in aquatic organisms in relation to toxic environmental pollutants. Ecotoxicology and Environment Safety 2006, 64(2):178-189.
65. Vijayavel K., Gomathi D., Durgabhavani K., Balasubramanian M.P. Sublethal effect of naphthalene on lipid peroxidation and antioxidant status in the edible marine crab Scylla serrata. Marine Pollutution Bulletin 2004, 48:429-433.
66. Waisberg M., Joseph P., Hale B., Beyersmann D. Molecular and cellular mechanisms of cadmium carcinogenesis. Toxicology 2003, 192:95-117.
67. Wang Y., Fang J., Lenonard S.S., Murali Krishna Rao K. Cadmium inhibits the electron transfer chain and induces reactive oxygen species. Free Radical Biology and Medicine 2004, 36:1434-1443.
68. Winrow V.R., Winyard P.G., Morris C.J., Blake D.R. Free radicals in inflammation: second messengers and mediators of tissue destruction. British Medical Bulletin 1993, 49:506-522.
69. Yan L.J., Levine R.L., Sohal R.S. Oxidative damage during aging targets mitochondrial aconitase. Proceedings of the National Academy of Sciences of the United States of America 1997, 94:11168-11172.
70. Zhao H., Joseph J., Fales H.M., Sokolovski E.A., Levine R.L., Vasquez-Vivar J., Kalyanaraman B. Detection and characterization of the product of hydroethidine and intracellular superoxide by HPLC and limitation of fluorescence. Proceedings of the National Academy of Sciences of the United States of America 2005, 102:5727-5732. 10.1073/pnas.0501719102.