Toxicity of copper oxide nanoparticles in the blue mussel, Mytilus edulis: A redox proteomic investigation

Chemosphere

Volumn 108, Issue , 2014, Pages 289-299

  Hu, Wentao ^a   Culloty, Sarah ^a   Darmody, Grainne ^a   Lynch, Sharon ^a   Davenport, John ^a   Ramirez Garcia, Sonia ^b   Dawson, Kenneth A ^b   Lynch, Iseult ^b   Blasco, Julian ^c   Sheehan, David ^a  

^a UNIVERSITY COLLEGE CORK   (Ireland)

^b UNIVERSITY COLLEGE DUBLIN   (Ireland)

^c INSTITUTO DE CIENCIAS MARINAS DE ANDALUCÍA   (Spain)

Author keywords

Copper; Nanoparticles; Oxidative stress; Protein carbonyl; Protein thiols

Indexed keywords

BINARY ALLOYS; CARBONYLATION; COLLAGEN; COPPER; ELECTROPHORESIS; ENZYMES; GOLD COMPOUNDS; LIGHT SCATTERING; METAL NANOPARTICLES; METALS; MOLLUSCS; MUSCULOSKELETAL SYSTEM; NANOPARTICLES; OXIDATIVE STRESS; SUSPENSIONS (FLUIDS); TISSUE; TITANIUM OXIDES; TOXICITY; ZINC ALLOYS; ZINC COMPOUNDS;

COPPER OXIDE NANOPARTICLES; METAL OXIDE NANOPARTICLES; NANOPARTICLE TRACKING ANALYSIS; PEPTIDE MASS FINGERPRINTING; PROTEIN CARBONYLS; PROTEIN THIOLS; TRIOSEPHOSPHATE ISOMERASE; TWO-DIMENSIONAL GEL ELECTROPHORESIS;

COPPER OXIDES;

ACTIN; ALPHA TUBULIN; BETA TUBULIN; CARBONYL DERIVATIVE; CHROMIUM; COBALT; COPPER OXIDE; COPPER ZINC SUPEROXIDE DISMUTASE; METAL OXIDE; NANOMATERIAL; NANOPARTICLE; THIOL; TRIOSEPHOSPHATE ISOMERASE; TROPOMYOSIN;

BIOACCUMULATION; COPPER COMPOUND; HISTOLOGY; INGESTION RATE; MUSSEL CULTURE; PEPTIDE; PROTEIN; REDOX CONDITIONS; TOXICITY TEST;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATOMIC EMISSION SPECTROMETRY; CONNECTIVE TISSUE; CONTROLLED STUDY; DIGESTIVE SYSTEM; GILL; HISTOLOGY; LIGHT SCATTERING; MUSSEL; MYTILUS EDULIS; NANOTECHNOLOGY; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PROTEIN ANALYSIS; PROTEOMICS; SKELETAL MUSCLE; TISSUE DISTRIBUTION; TRANSMISSION ELECTRON MICROSCOPY; TWO DIMENSIONAL GEL ELECTROPHORESIS;

MYTILUS EDULIS;

COPPER; NANOPARTICLES; OXIDATIVE STRESS; PROTEIN CARBONYL; PROTEIN THIOLS;

ANIMALS; COPPER; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; GILLS; METAL NANOPARTICLES; MYTILUS EDULIS; OXIDATION-REDUCTION; PROTEIN CARBONYLATION; PROTEINS; PROTEOMICS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; SULFHYDRYL COMPOUNDS; WATER POLLUTANTS, CHEMICAL;

EID: 84901608505     PISSN: 00456535     EISSN: 18791298     Source Type: Journal    
DOI: 10.1016/j.chemosphere.2014.01.054     Document Type: Article

References (73)

1. Ahn B., Rhee S.G., Stadtman E.R. Use of fluorescein hydrazide and fluorescein thiosemicarbazide reagents for the fluorometric determination of protein carbonyl groups and for the detection of oxidized protein on polyacrylamide gels. Anal. Biochem. 1987, 1987(161):245-257.
2. Amiard J.C., Pineau A., Boiteau H.L., Metayer C., Amiard-Triquet C. Application of atomic-absorption spectrophotometry using Zeeman effect to the determination of 8 trace-elements (Ag, Cd, Cr, Cu, Mn, Ni, Pb and Se) in biological-materials. Water Res. 1987, 21:693-697.
3. Barrena R., Casals E., Colon J., Font X., Sanchez A., Puntes V. Evaluation of the ecotoxicity of model nanoparticles. Chemosphere 2009, 75:850-857.
4. Baty J.W., Hampton M.B., Winterbourn C.C. Proteomic detection of hydrogen peroxide-sensitive thiol proteins in Jurkat cells. Biochem. J. 2005, 389:785-795.
5. Bayne B.L. Responses to environmental stress: tolerance, resistance and adaptation. Marine Biology of Polar Regions and Effects of Stress on Marine Organisms 1985, 331-349. Wiley, London. B.L. Bayne (Ed.).
6. Bexiga E., Varela J.A., Wang F., Fenaroli F., Salvati A., Lynch I., Simpson J.C., Dawson K.A. Cationic nanoparticles induce caspase 3-, 7- and 9-mediated cytotoxicity in a human astrocytoma cell line. Nanotoxicology 2011, 5:557-567.
7. Bonneris E., Perceval O., Masson S., Hare L., Campbell P.G.C. Sub-cellular partitioning of Cd, Cu and Zn in tissues of indigenous unionid bivalves living along a metal exposure gradient and links to metal-induced effects. Environ. Pollut. 2005, 135:195-208.
8. Bradford M.M. A rapid and sensitive assay for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254.
9. Canesi L., Ciacci C., Betti M., Fabbri R., Canonico B., Fantinati A., Marcornini A., Pojano G. Immunotoxicity of carbon black nanoparticles to blue mussel hemocytes. Environ. Int. 2008, 34:1114-1119.
10. 2) on Mytilus hemocytes. Aquat. Toxicol. 2010, 96:151-158.
11. Canesi L., Ciacci C., Fabbri R., Marcornini A., Pojano G., Gallo G. Bivalve molluscs as a unique target group for nanoparticle toxicity. Mar. Environ. Res. 2012, 76:16-21.
12. Cannito S., Novo E., di Bonzo L.V., Busletta C., Colombatto S., Parola M. Epithelial-mesenchymal transition: from molecular mechanisms, redox regulation to implications in human health and disease. Antiox. Redox Signal. 2010, 12:1383-1430.
13. Cajaraville M.P., Abascal I., Etxeberria M., Marigomez I. Lysosomes as cellular markers of environmental pollution: time and dose-dependent responses of the digestive lysosomal system of mussels after petroleum hydrocarbon exposure. Environ. Toxicol. Water Qual. 1995, 10:1-8.
14. Cedervall T., Lynch I., Lindman S., Berggard T., Thulin E., Nilsson H., Dawson K.A., Linse S. Understanding the nanoparticle-protein corona using methods to quantify exchange rates and affinities of proteins for nanoparticles. Proc. Natl. Acad. Sci. USA 2007, 104:2050-2055.
15. Cho W.-S., Duffin R., Thielbeer F., Bradley M., Megson I.L., MacNee W., Poland C.A., Tran C.L., Donaldson K. Zeta potential and solubility to toxic ions as mechanisms of lung inflammation caused by metal/metal oxide nanoparticles. Toxicol. Sci. 2012, 126:469-477.
16. Davda J., Labhasetwar V. Characterization of nanoparticle uptake by endothelialcells. Int. J. Pharmaceut. 2002, 232:51-59.
17. Davies M.J. The oxidative environment and protein damage. Biochim. Biophys. Acta - Prot. Proteom. 2005, 1703:93-109.
18. Defossez J.M., Hawkins A.J.S. Selective feeding in shellfish: Size-dependent rejection of large particles within pseudofaeces from Mytilus edulis, Ruditapes philippinarum and Tapes decussatus. Mar. Biol. 1997, 129:139-147.
19. Dickson D., Liu G., Li C., Tachiev G., Cai Y. Dispersion and stability of bare hematite nanoparticles: Effects of dispersion tools, nanoparticle concentration, humic acid and ionic strength. Sci. Total Environ. 2012, 419:170-177.
20. Domouhtsidou G.P., Dailianis S., Kaloyianni M., Dimitriadis V.K. Lysosomal membrane stability and metallothionein content in Mytilus galloprovincialis (L.), as biomarkers combination with trace concentrations. Mar. Poll. Bull. 2004, 48:572-586.
21. Domouhtsidou G.P., Dimitriadis V.K. Lysosomal and lipid alterations in the digestive gland of mussels, Mytilus galloprovincialis (L.) as biomarkers of environmental stress. Environ. Poll. 2001, 155:123-137.
22. Domouhtsidou G.P., Dimitriadis V.K. Ultrastructural localization of heavy metals (Hg, Ag, Pb, and Cu) in gills and digestive gland of mussels, Mytilus galloprovincialis (L.). Arch. Environ. Contam. Toxicol. 2000, 38:472-478.
23. Dyballa N., Metzger S. Fast and sensitive colloidal coomassie G-250 staining for protein in polyacrylamide gels. JoVE 2009, 30.
24. Elsaesser A., Howard C.V. Toxicology of nanoparticles. Adv. Drug Deliv. Rev. 2012, 64:129-137.
25. Finkel T., Holbrook N.J. Oxidants, oxidative stress and the nature of ageing. Nature 2000, 408:239-247.
26. Gomes T., Pinheiro J.P., Cancio I., Pereira C.G., Cardosos C., Bebianno M.J. Effects of copper nanoparticles exposure in the mussel Mytilus galloprovincialis. Exp. Sci. Technol. 2011, 45:9356-9362.
27. Holman M.W., Lackner D.I. The Nanotech Report 2006, Lux Research, New York, pp. 1-25. fourth ed.
28. Gunawant C., Teoh W.Y., Marquis C.P., Amal R. Cytotoxic origin of copper (II) Oxide nanoparticles: Comparative studies with micron-sized particles, leachate, and metal salts. ACS Nano 2011, 5:7214-7225.
29. Hsin Y.-H., Chena C.F., Huang S., Shih T.-S., Lai P.-S., Chueh P.J. The apoptotic effect of nanosilver is mediated by a ROS and JNK-dependent mechanism involving the mitochondrial pathway in NIH3T3 cells. Toxicol. Lett. 2008, 179:130-139.
30. Kahru A., Ivask A. Mapping the dawn of nanoecotoxicological research. Acc. Chem. Res. 2013, 46:823-833.
31. Klaine S.J., Alvarez P.J.J., Batley G.E., Fernandes T.F., Handy R.D., Lyon D.Y., Mahendra S., McLaughlin M.J., Lead J.R. Nanomaterials in the environment: behavior, fate, bioavailability and effects. Environ. Toxicol. Chem. 2008, 27:1825-1851.
32. Koehler A., Marx U., Broeg K., Bahns S., Bressling J. Effects of nanoparticles in Mytilus edulis gill and hepatopancreas - a new threat to marine life. Mar. Environ. Res. 2008, 66:12-14.
33. Lin T., Xing J., Sheng X., Tang X., Zhan W. Development of a monoclonal antibody specific to granulocytes in scallop Chlamys farreri after acute viral necrobiotic virus (AVNV) infection. Fish Shellfish Immunol. 2011, 30:1348-1353.
34. Lowe D.M., Clarke K.R. Contaminant-induced changes in the structure of the digestive epithelium of Mytilus edulis. Aquat. Toxicol. 1989, 15:345-358.
35. Lowe D.M., Fossato V.U., Depledge M.H. Contaminant-induced lysosomal membrane damage in blood cells of mussels Mytilus galloprovincialis from the Venice Lagoon: an in vitro study. Mar. Ecol. - Prog. Ser. 1995, 129:189-196.
36. Lynch I., Cedervall T., Lundquist M., Cabaleiro-Lago C., Linse S., Dawson K.A. The nanoparticle-protein complex as a biological entity: a complex fluids and surface science challenge for the 21st century. Adv. Colloid Interface Sci. 2007, 134:167-174.
37. Lyons C., Dowling V., Tedengren M., Hartl M.G.J., O'Brien N.M., van Pelt F.N.A.M., O'Halloran J., Sheehan D. Immunoblotting determination of levels of heat shock protein and glutathione S-transferase in blue mussel, Mytilus edulis, sampled from Cork Harbour, Ireland, the North and Baltic Seas. Mar. Environ. Res. 2003, 56:585-597.
38. Martin C.R. Nanomaterials - a membrane-based synthetic approach. Science 1994, 266:1961-1966.
39. McDonagh B., Tyther R., Sheehan D. Carbonylation and glutathionylation of proteins in the blue mussel Mytilus edulis detected by proteomic analysis and western blotting: actin as a target for oxidative stress. Aquat. Toxicol. 2005, 73:315-326.
40. Moore M.N. Cellular responses to pollutants. Mar. Poll. Bull. 1985, 16:134-139.
41. Moore M.N. Lysosomal cytochemistry in marine environmental monitoring. J. Histochem. 1990, 22:187-191.
42. Moore M.N. Do nanoparticles present ecotoxicological risks for the health of the aquatic environment?. Environ. Int. 2006, 32:967-976.
43. Moore M.N. Lysosomal cytotoxicity of carbon nanoparticles in cells of the molluscan immune system: an in vivo study. Nanotoxicology 2009, 3:40-45.
44. Nel A.E., Madler L., Velegol D., Xia T., Hoek E.M.V., Somosundaran P., Klaessig F., Castranova V., Thomson M. Understanding biophysicochemical interactions at the nano-bio interface. Nat. Mater. 2009, 8:543-557.
45. Oberdörster G., Oberdörster E., Oberdörster J. Nanotoxicology: an emerging discipline evolving from studies of ultrafine particles. Environ. Health Perspect. 2005, 113:823-839.
46. Oberdörster G., Stone V., Donaldson K. Toxicology of nanoparticles: a historical perspective. Nanotoxicology 2007, 1:2-25.
47. Poland C.A., Duffin R., Kinloch I., Maynard A., Wallace W.A.H., Seaton A., Stone V., Brown S., MacNee W., Donaldson K. Carbon nanotubes introduced into the abdominal cavity of mice show asbestos-like pathogenicity in a pilot study. Nat. Nanotechnol. 2008, 3:423-428.
48. Pipe R.K., Coles J.A., Carissan F.M.M., Ramanathan K. Copper induced immunomodulation in the marine mussel, Mytilus edulis. Aquat. Toxicol. 1999, 46:43-54.
49. Regoli F. Lysosomal responses as a sensitive stress index in biomonitoring heavy-metal pollution. Mar. Ecol.-Prog. Ser. 1992, 84:63-69.
50. Rickwood C.J., Galloway T.S. Acetylcholinesterase inhibition as a biomarker of adverse effect a study of Mytilus edulis exposed to the priority pollutant chlorfenvinphos. Aquat. Toxicol. 2004, 67:45-56.
51. Shahul H.M.S., Sharma S.P. The structure of the thioredoxin-triosephosphate isomerase complex provides insights into the reversible glutathione-mediated regulation of triosephosphate isomerase. Biochemistry 2012, 51:533-544.
52. Sharifi S., Behzadi S., Laurent S., Forrest M.L., Stroeve P., Mahmoudi M. Toxicity of nanomaterials. Chem. Soc. Rev. 2012, 41:2323-2343.
53. Shevchenko A., Wilm M., Vorm O., Mann M. Mass spectrometric sequencing of proteins from silver-stained polyacrylamide gels. Anal. Chem. 1996, 68:850-858.
54. Smith A.M., Duan H.W., Moh A.M., Nie S.M. Bioconjugated quantum dots for in vivo molecular and cellular imaging. Adv. Drug Deliv. Rev. 2008, 60:1226-1240.
55. Stoeger T., Reinhard C., Takenaka S., Schroeppel A., Karg E., Ritter B., Heyder J., Schulz H. Instillation of six different ultrafine carbon particles indicates a surface area threshold dose for acute lung inflammation in mice. Environ. Health Perspect. 2006, 114:328-333.
56. Sund J., Alenius H., Vippola M., Savolainen K., Puustinen S. Proteomic characterization of engineered nanomaterial-protein interactions in relation to surface reactivity. ACS Nano 2011, 5:4300-4309.
57. Taurozzi, J.S., Hackley, V.A., Weisner, M.R., 2012 Protocol for preparation of nanoparticle dispersions from powdered material using ultrasonic dispersion. doi: http://www.ceint.duke.edu/protocol/preparation-nanoparticle-dispersions-powdered-material-using-ultrasonic-disruption (accessed 30.10.13).
58. Tedesco S., Doyle H., Redmond G., Sheehan D. Gold nanoparticles and oxidative stress in Mytilus edulis. Mar. Environ. Res. 2008, 66:131-133.
59. Tedesco S., Sheehan D. Nanomaterials as emerging environmental threats. Curr. Chem. Biol. 2010, 4:151-160.
60. Tedesco S., Doyle H., Blasco J., Redmond G., Sheehan D. Oxidative stress and toxicity of gold nanoparticles in Mytilus edulis. Aquat. Toxicol. 2010, 100:178-196.
61. Tedesco S., Doyle H., Blasco J., Redmond G., Sheehan D. Exposure of the blue mussel, Mytilus edulis, to gold nanoparticles and the pro-oxidant menadione. Comp. Biochem. Physiol. Part C 2010, 151:167-174.
62. Thomas C.R., George S., Horst A.M., Ji Z.X., Miller R.J., Peralta-Videa J.R., Xia T.A., Pokhrel S., Madler L., Gardea-Torresday J.L., Holden P.A., Keller A.A., Lenihan H.S., Nel A.E., Zink J.L. Nanomaterials in the environment: from materials to high-throughput screening to organisms. ACS Nano 2011, 5:13-20.
63. Tiede K., Hasselly M., Breitbarth E., Chaudhry Q., Boxall A.B.A. Considerations for environmental fate and ecotoxicity testing to support environmental risk assessments for engineered nanoparticles. J. Chromatogr. Part A 2009, 1216:503-509.
64. Unfried K., Albrecht C., Klotz L.O., Von Mikecz A., Grether-Beck S., Schins R.P.F. Cellular responses to nanoparticles: target structures and mechanisms. Nanotoxicology 2007, 1:52-71.
65. Viarengo A., Moore M.N., Mancinelli G., Mazzucotelli A., Pipe R.K., Farrar S.V. Metallothioneins and lysosomes in metal toxicity and accumulation in marine mussels: the effect of cadmium in the presence and absence of phenanthrene. Mar. Biol. 1987, 94:251-257.
66. Ward J.E., Kach D.J. Marine aggregates facilitate ingestion of nanoparticles by suspension-feeding bivalves. Mar. Environ. Res. 2009, 68:137-142.
67. Warheit D.B. Debunking some misconceptions about nanotoxicology. Nano Lett. 2010, 10:4777-4782.
68. Widdows J., Donkin P. Mussels and environmental contaminants: bioaccumulation and physiological aspects. The Mussel Mytilus: Ecology, Physiology, Genetics and Culture 1992, 383-424. Elsevier, Amsterdam. E. Gosling (Ed.).
69. Winston G.W., Moore M.N., Kirchin M.A., Soverchia C. Production of reactive oxygen species by Hemocytes from the marine mussel, Mytilus edulis: Lysosomal localization and effect of xenobiotics. Comp. Biochem. Physiol. Part C 1996, 133:221-229.
70. Winterbourn C. Reconciling the chemistry and biology of reactive oxygen species. Nat. Chem. Biol. 2008, 4:278-286.
71. Wishkovsky A. Chemiluminescence: an advanced tool for measuring phagocytosis. In disease processes in marine bivalve molluscs. Am. Fish. Soc. 1988, 18:292-298.
72. Xia T., Kovochich M., Brant J., Hotze M., Sempf J., Oberley T., Sioutas C., Yeh J.I., Wiesner M.R., Nel A.E. Comparison of the abilities of ambient and engineered nanoparticles to induce cellular toxicity according to an oxidative stress paradigm. Nano Lett. 2006, 6:1794-1807.
73. 2 nanoparticle aggregates in Daphnia magna. Chemosphere 2010, 78:209-215.