Proteomic discovery of biomarkers of metal contamination in Sydney Rock oysters (Saccostrea glomerata)

Aquatic Toxicology

Volumn 109, Issue , 2012, Pages 202-212

  Thompson, Emma L ^a,b   Taylor, Daisy A ^a,b   Nair, Sham V ^a   Birch, Gavin ^c   Haynes, Paul A ^a   Raftos, David A ^a,b  

^a MACQUARIE UNIVERSITY   (Australia)

^b SYDNEY INSTITUTE OF MARINE SCIENCE   (Australia)

^c UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Metal contamination; Molecular biomarkers; Proteomics; Saccostrea glomerata; Sydney Rock oysters; Two dimensional electrophoresis

Indexed keywords

BIOLOGICAL MARKER; CADMIUM; COPPER; LEAD; ZINC;

BIOMARKER; BIOMONITORING; CONCENTRATION (COMPOSITION); ELECTROKINESIS; ENVIRONMENTAL MONITORING; MASS SPECTROMETRY; MOLLUSC; PROTEOMICS;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BIOACCUMULATION; BIOLOGICAL MONITORING; CELL ACTIVITY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYTOSKELETON; ENVIRONMENTAL MONITORING; HEMOLYMPH; LIQUID CHROMATOGRAPHY; NONHUMAN; OYSTER; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS; PROTEOMICS; SACCOSTREA GLOMERATA; TANDEM MASS SPECTROMETRY; TWO DIMENSIONAL ELECTROPHORESIS; WATER ANALYSIS; WATER QUALITY;

ANIMALS; BIOLOGICAL MARKERS; ENVIRONMENTAL MONITORING; GENE EXPRESSION REGULATION; METALS, HEAVY; OSTREIDAE; PROTEOMICS; WATER POLLUTANTS, CHEMICAL;

OSTREIDAE; SACCOSTREA GLOMERATA;

EID: 84856618679     PISSN: 0166445X     EISSN: 18791514     Source Type: Journal    
DOI: 10.1016/j.aquatox.2011.09.018     Document Type: Article

References (67)

1. Andon N.L., Eckert D., Yates J.R., Haynes P.A. High-throughput functional affinity purification of mannose binding proteins from Oryza sativa. Proteomics 2003, 3:1270-1278.
2. Andrew M.N., Dunstan R.H., O'Connor W.A., Van Zwieten L., Nixon B., MacFarlane G.R. Effects of 4-nonylphenol and 17[alpha]-ethynylestradiol exposure in the Sydney rock oyster, Saccostrea glomerata: Vitellogenin induction and gonadal development. Aquatic Toxicology 2008, 88(1):39-47.
3. Apraiz I., Mi J., Cristobal S. Identification of proteomic signatures of exposure to marine pollutants in mussels (Mytilus edulis). Molecular and Cellular Proteomics 2006, 5(7):1274-1285.
4. Bailey K. Invertebrate tropomyosin. Biochimica et Biophysica Acta 1957, 24:612-619.
5. Birch G., Taylor S. Source of heavy metals in sediments of the Port Jackson estuary, Australia. The Science of the Total Environment 1999, 227(2-3):123-138.
6. Birch G.F. Marine pollution in Australia, with special emphasis on central New South Wales estuaries and adjacent continental margin. International Journal of Environment and Pollution 2000, 13:1-6.
7. Boutet I., Tanguy A., Moraga D. Response of the Pacific oyster Crassostrea gigas to hydrocarbon contamination under experimental conditions. Gene 2004, 329:147-157.
8. Bradley B.P., Shrader E.A., Kimmel D.G., Meiller J.C. Protein expression signatures: an application of proteomics. Marine Environmental Research 2002, 54(3-5):373-377.
9. Brown K.R., McPherson R.G. Concentrations of copper, zinc and lead in the Sydney rock oyster, Saccostrea commercialis (Iredale and Roughley) from the Georges River, New South Wales. The Science of The Total Environment 1992, 126(1-2):27-33.
10. Butler R.A., Roesijadi G. Metallothionein (MT) gene expression and cadmium-induced immunotoxicity in hemocytes of the eastern oyster Crassostrea virginica. Marine Environment Research 2000, 50(1-5):470.
11. Chase M.E., Jones S.H., Hennigar P., Sowles J., Harding G.C.H., Freeman K., Wells P.G., Krahforst C., Coombs K., Crawford R., Pederson J., Taylor D. Gulfwatch: Monitoring Spatial and Temporal Patterns of Trace Metal and Organic Contaminants in the Gulf of Maine (1991-1997) with the Blue Mussel, Mytilus edulis L. Marine Pollution Bulletin 2001, 42(6):490-504.
12. Choi Y.K., Jo P.G., Choi C.Y. Cadmium affects the expression of heat shock protein 90 and metallothionein mRNA in the Pacific oyster, Crassostrea gigas. Comparative Biochemistry and Physiology. Part C: Toxicology and Pharmacology 2008, 147(3):286-292.
13. Craig R., Beavis R.C. A method for reducing the time required to match protein sequences with tandem mass spectra. Rapid Communications in Mass Spectrometry 2003, 17(20):2310-2316.
14. Craig R., Beavis R.C. TANDEM: matching proteins with tandem mass spectra. Bioinformatics 2004, 20(9):1466-1467.
15. Cruz-Rodríguez L.A., Chu F.-L.E. Heat-shock protein (HSP70) response in the eastern oyster, Crassostrea virginica, exposed to PAHs sorbed to suspended artificial clay particles and to suspended field contaminated sediments. Aquatic Toxicology 2002, 60(3-4):157-168.
16. Dahlhoff E., Stillman P., Menge H.B.A. Physiological community ecology: variation in metabolic activity of ecologically important rocky intertidal invertebrates along environmental gradients. Integrative and Comparative Biology 2002, 862-871.
17. Duarte C.A., Giarratano E., Amin O.A., Comoglio L.I. Heavy metal concentrations and biomarkers of oxidative stress in native mussels (Mytilus edulis chilensis) from Beagle Channel coast (Tierra del Fuego, Argentina). Marine Pollution Bulletin 2011, 62(8):1895-1904.
18. Fagotti A., Di Rosa I., Simoncelli F., Pipe R.K., Panara F., Pascolini R. The effects of copper on actin and fibronectin Organization in Mytilus galloprovincialls haemocytes. Developmental & Comparative Immunology 1996, 20(6):383-391.
19. Faria M., Carrasco L., Diez S., Riva M.C., Bayona J.M., Barata C. Multi-biomarker responses in the freshwater mussel Dreissena polymorpha exposed to polychlorobiphenyls and metals. Comparative Biochemistry and Physiology. Part C: Toxicology and Pharmacology 2009, 149(3):281-288.
20. Gagnaire B., Gagné F., André C., Blaise C., Abbaci K., Budzinski H., Dévier M.-H., Garric J. Development of biomarkers of stress related to endocrine disruption in gastropods: Alkali-labile phosphates, protein-bound lipids and vitellogenin-like proteins. Aquatic Toxicology 2009, 92(3):155-167.
21. Gagné F., Blaise C., Salazar M., Salazar S., Hansen P.D. Evaluation of estrogenic effects of municipal effluents to the freshwater mussel Elliptio complanata. Comparative Biochemistry and Physiology. Part C: Toxicology and Pharmacology 2001, 128(2):213-225.
22. Giguère A., Couillard Y., Campbell P.G.C., Perceval O., Hare L., Pinel-Alloul B., Pellerin J. Steady-state distribution of metals among metallothionein and other cytosolic ligands and links to cytotoxicity in bivalves living along a polymetallic gradient. Aquatic Toxicology 2003, 64(2):185-200.
23. Gillikin D.P., Dehairs F., Baeyens W., Navez J., Lorrain A., Andre L. Inter- and intra-annual variations of Pb/Ca ratios in clam shells (Mercenaria mercenaria): A record of anthropogenic lead pollution?. Marine Pollution Bulletin 2005, 50(12):1530-1540.
24. 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.
25. Gomiero A., Pampanin D.M., Bjornstad A., Larsen B.K., Provan F., Lyng E., Andersen O.K. An ecotoxicoproteomic approach (SELDI-TOF mass spectrometry) to biomarker discovery in crab exposed to pollutants under laboratory conditions. Aquatic Toxicology 2006, 78(Supplement 1):S34-S41.
26. Gray J.S. Biological and ecological effects of marine pollutants and their detection. Marine Pollution Bulletin 1992, 25:48-50.
27. Greenway S.C., Storey K.B. The effect of prolonged anoxia on enzyme activities in oysters (Crassostrea virginica) at different seasons. Journal of Experimental Marine Biology and Ecology 1999, 242(2):259-272.
28. Hardiman S., Pearson B. Heavy metals, TBT and DDT in the Sydney rock oyster (Saccostrea commercialis) sampled from the Hawkesbury River estuary, NSW, Australia. Marine Pollution Bulletin 1995, 30(8):563-567.
29. Jamieson D.D., de Rome P. Energy metabolism of the heart of the mollusc Tapes watlingi. Comparative Biochemistry and Physiology Part B: Comparative Biochemistry 1979, 63(3):399-405.
30. Jonsson H., Schiedek D., Grosvik B.E., Goksoyr A. Protein responses in blue mussels (Mytilus edulis) exposed to organic pollutants: A combined CYP-antibody/proteomic approach. Aquatic Toxicology 2006, 78(Supplement 1):S49-S56.
31. Lannig G., Flores J.F., Sokolova I.M. Temperature-dependent stress response in oysters, Crassostrea virginica: pollution reduces temperature tolerance in oysters. Aquatic Toxicology 2006, 79(3):278-287.
32. Li X., Wai O.W.H., Li Y.S., Coles B.J., Ramsey M.H., Thornton I. Heavy metal distribution in sediment profiles of the Pearl River estuary, South China. Applied Geochemistry 2000, 15(5):567-581.
33. Mount A.S., Wheeler A.P., Paradkar R.P., Snider D. Hemocyte-mediated shell mineralization in the eastern oyster. Science 2004, 304(5668):297-300.
34. Nesatyy V.J., Suter M.J.F. Proteomics for the analysis of environmental stress responses in organisms. Environmental Science and Technology 2007, 41(20):6891-6900.
35. Newton T.J., Bartsch M.R. Lethal and sublethal effects of ammonia to juvenile Lampsilis mussels (Unionidae) in sediment and water-only exposures. Environmental Toxicology and Chemistry 2007, 26(10):2057.
36. Nicholson S., Lam P.K.S. Pollution monitoring in Southeast Asia using biomarkers in the mytilid mussel Perna viridis (Mytilidae: Bivalvia). Environment International 2005, 31(1):121-132.
37. Pedersen S.N., Lundebye A.-K. Metallothionein and stress protein levels in shore crabs (Carcinus maenas) along a trace metal gradient in the Fal estuary (UK). Marine Environment Research 1996, 42(1-4):241-246.
38. Piatigorsky J., Kozmik Z., Horwitz J., Ding L., Carosa E., Robison W.G., Steinbach P.J., Tamm E.R. Ω-Crystallin of the scallop lens. Journal of Biological Chemistry 2000, 275(52):41064-41073.
39. Riffeser M., Hock B. Vitellogenin levels in mussel hemolymph--a suitable biomarker for the exposure to estrogens?. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology 2002, 132(1):75-84.
40. Rodríguez-Ariza A., Rodríguez-Ortega M.J., Marenco J.L., Amezcua O., Alhama J., López-Barea J. Uptake and clearance of PCB congeners in Chamaelea gallina: response of oxidative stress biomarkers. Comparative Biochemistry and Physiology. Part C: Toxicology and Pharmacology 2003, 134(1):57-67.
41. Rodríguez-Ortega M.J., Grøsvik B.E., Rodríguez-Ariza A., Goksøyr A., López-Barea J. Changes in protein expression profiles in bivalve molluscs (Chamaelea gallina) exposed to four model environmental pollutants. Proteomics 2003, 3(8):1535-1543.
42. Roman Y.E., De Schamphelaere K.A.C., Nguyen L.T.H., Janssen C.R. Chronic toxicity of copper to five benthic invertebrates in laboratory-formulated sediment: Sensitivity comparison and preliminary risk assessment. Science of The Total Environment 2007, 387(1-3):128-140.
43. Rothman J.E. Polypeptide chain binding proteins: catalysts of protein folding and related processes in cells. Cell 1989, 59:591-601.
44. Sanders B.M., Martin L.S., Nelson W.G., Phelps D.K., Welch W. Relationships between accumulation of a 60kDa stress protein and scope-for-growth in Mytilus edulis exposed to a range of copper concentrations. Marine Environment Research 1991, 31(2):81-97.
45. Sanders M.J., Du Preez H.H., Van Vuren J.H.J. The freshwater river crab, Potamonautes warreni, as a bioaccumulative indicator of iron and manganese pollution in two aquatic systems. Ecotoxicology and Environmental Safety 1998, 41(2):203-214.
46. Scanes P.R. Uptake and depuration of organochlorine compounds in Sydney rock oysters (Saccosstrea commercialis). Marine and Freshwater Research 1997, 48:1-6.
47. Scanes P.R, Roach A.C. Determining natural 'background' concentrations of trace metals in oysters from New South Wales, Australia. Environmental Pollution 1999, 105(3):437-446.
48. Schiedek D., Broeg K., Barsiene J., Lehtonen K.K., Gercken J., Pfeifer S., Vuontisjärvi H., Vuorinen P.J., Dedonyte V., Koehler A., Balk L., Schneider R. Biomarker responses as indication of contaminant effects in blue mussel (Mytilus edulis) and female eelpout (Zoarces viviparus) from the southwestern Baltic Sea. Marine Pollution Bulletin 2006, 53(8-9):387-405.
49. Seals J.D., Grossman S.H. Purification and characterization of arginine kinase from the sea cucumber Caudina arenicola. Comparative Biochemistry and Physiology Part B: Comparative Biochemistry 1988, 89(4):701-707.
50. Sellers J.R. Myosins: a diverse superfamily. Biochimica et Biophysica Acta (BBA) - Molecular Cell Research 2000, 1496(1):3-22.
51. Snowdon R., Birch G.F. The nature and distribution of copper, lead and zinc in soils of highly urbanised sub-catchment (iron cove) of Port Jackson, Sydney. Australian Journal of Soil Research 2004, 42:329-338.
52. Soetaert A., Vandenbrouck T., van der Ven K., Maras M., van Remortel P., Blust R., De Coen W.M. Molecular responses during cadmium-induced stress in Daphnia magna: integration of differential gene expression with higher-level effects. Aquatic Toxicology 2007, 83(3):212-222.
53. Stark J.S. Effects of copper on macrobenthic assemblages in soft sediments: a laboratory experimental study. Ecotoxicology 1998, 7:161-173.
54. Steinert S.A., Pickwell G.V. Induction of HSP70 proteins in mussels by ingestion of tributyltin. Marine Environment Research 1993, 35(1-2):89-93.
55. Suzuki M., Nagasawa H. The structure-function relationship analysis of Prismalin-14 from the prismatic layer of the Japanese pearl oyster, (Pinctada fucata). FEBS Journal 2007, 274(19):5158-5166.
56. Tanabe S., Prudente M.S., Kan-atireklap S., Subramanian A. Mussel watch: marine pollution monitoring of butyltins and organochlorines in coastal waters of Thailand, Philippines and India. Ocean & Coastal Management 2000, 43(8-9):819-839.
57. Thompson E.L., Taylor D.A., Nair S.V., Birch G., Haynes P.A., Raftos D.A. A proteomic analysis of the effects of metal contamination on Sydney Rock Oyster (Saccostrea glomerata) haemolymph. Aquatic Toxicology 2011, 103(3-4):241-249.
58. Ulrich P.N., Marsh A.G. Interindividual variation of malate dehydrogenase activity in the oyster Crassostrea virginica. Marine and Freshwater Behaviour and Physiology 2006, 39:293-306.
59. Valavanidis A., Vlahogianni T., Dassenakis M., Scoullos M. Molecular biomarkers of oxidative stress in aquatic organisms in relation to toxic environmental pollutants. Ecotoxicology and Environmental Safety 2006, 64(2):178-189.
60. van der Oost R., Goksøyr A., Celander M., Heida H., Vermeulen N.P.E. Biomonitoring of aquatic pollution with feral eel (Anguilla anguilla). II. Biomarkers: pollution-induced biochemical responses. Aquatic Toxicology 1996, 36(3-4):189-222.
61. Venier P., De Pittà C., Pallavicini A., Marsano F., Varotto L., Romualdi C., Dondero F., Viarengo A., Lanfranchi G. Development of mussel mRNA profiling: can gene expression trends reveal coastal water pollution?. Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis 2006, 602(1-2):121-134.
62. Viant M.R., Pincetich C.A., Walton J.H., Tjeerdema R.S., Hinton D.E. Utilizing in vivo nuclear magnetic resonance spectroscopy to study sublethal stress in aquatic organisms. Marine Environmental Research 2002, 54(3-5):553-557.
63. Wang Z., Wu Z., Jian J., Lu Y. Cloning and expression of an actin gene in the haemocytes of pearl oyster (Pinctada fucata, Gould 1850). Marine Genomics 2008, 1(2):63-67.
64. Wu R.S.S., Siu W.H.L., Shin P.K.S. Induction, adaptation and recovery of biological responses: implications for environmental monitoring. Marine Pollution Bulletin 2005, 51(8-12):623-634.
65. Zann L.P. The State of the Marine Environment Report for Australia (SOMER): process, findings and perspectives. Ocean and Coastal Management 1996, 33(1-3):63-86.
66. Zubkoff P.L., Ho M.-S. Krebs cycle intermediates of the oyster, Crassostrea virginica and the mussel, Geukensia demissa. Comparative Biochemistry and Physiology Part B: Comparative Biochemistry 1982, 72(4):577-580.
67. Zwann A., Holwerda De., Veenhof D.A.P.R. Anaerobic malate metabolism in mitochondria of the sea mussel Mytilus edulis. Marine Biology Letters 1981, 2:131-140.