Evaluation of cytotoxicity, morphological alterations and oxidative stress in Chinook salmon cells exposed to copper oxide nanoparticles

Protoplasma

Volumn 253, Issue 3, 2016, Pages 873-884

  Srikanth, Koigoora ^a,b   Pereira, Eduarda ^a   Duarte, Armando C ^a   Rao, Janapala Venkateswara ^b  

^a UNIVERSITY OF AVEIRO   (Portugal)

^b INDIAN INSTITUTE OF CHEMICAL TECHNOLOGY   (India)

Author keywords

Chinook salmon; Copper oxide nanoparticles; Cytotoxicity; Lipid peroxidation; Morphology; Oxidative stress

Indexed keywords

8-OXO-7-HYDRODEOXYGUANOSINE; CATALASE; COPPER; CUPROUS OXIDE; DEOXYGUANOSINE; GLUTATHIONE; GLUTATHIONE TRANSFERASE; NANOPARTICLE; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE;

ANALOGS AND DERIVATIVES; ANIMAL; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; EMBRYOLOGY; LIPID PEROXIDATION; METABOLISM; NONMAMMALIAN EMBRYO; OXIDATIVE STRESS; PROCEDURES; PROTEIN CARBONYLATION; SALMONINE; TOXICITY TESTING;

ANIMALS; CATALASE; CELLS, CULTURED; COPPER; DEOXYGUANOSINE; EMBRYO, NONMAMMALIAN; GLUTATHIONE; GLUTATHIONE TRANSFERASE; LIPID PEROXIDATION; NANOPARTICLES; OXIDATIVE STRESS; PROTEIN CARBONYLATION; REACTIVE OXYGEN SPECIES; SALMON; SUPEROXIDE DISMUTASE; TOXICITY TESTS;

EID: 84933544063     PISSN: 0033183X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00709-015-0849-7     Document Type: Article

References (56)

1. Aebi H (1984) Catalase. Methods Enzymol 2:673–684
2. Ahamed M, Siddiqui MA, Akhtar MJ, Ahmad I, Pant AB, Alhadlaq HA (2010) Genotoxic potential of copper oxide nanoparticles in human lung epithelial cells. Biochem Biophy Res Comm 396:578–583
3. Ahamed M, Akhtar MJ, Siddiqui MA, Ahmad J, Musarrat J, Al-Khedhairy AA, AlSalhi MS, Alrokayan SA (2011) Oxidative stress mediated apoptosis induced by nickel ferrite nanoparticles in cultured A549 cells. Toxicology 283:101–108
4. Alarifi S, Ali D, Verma A, Alakhtani S, Ali BA (2013) Cytotoxicity and genotoxicity of copper oxide nanoparticles in human skin keratinocytes cells. Int J Toxicol 32(4):296–307
5. Al-Bairuty GA, Shaw BJ, Handy RD, Henry TB (2013) Histopathological effects of waterborne copper nanoparticles and copper sulphate on the organs of rainbow trout Oncorhynchus mykiss. Aquat Toxicol 126:104–115
6. Anjum NA, Srikanth K, Mohmood I, Sayeed I, Trindade T, Duarte AC, Pereira E, Ahmad I (2014) Brain glutathione redox system significance for the control of silica-coated magnetite nanoparticles with or without mercury co-exposures mediated oxidative stress in European eel (Anguilla anguilla L.). Environ Sci Pollut Res 12:7746–7756
7. Aruoma OI, Halliwell B, Gajewski E, Dizdaroglu M (1991) Copper-iondependent damage to the bases in DNA in the presence of hydrogen peroxide. Biochem J 273:601–604
8. Berntsen P, Park CY, Rothen-Rutishauser B, Tsuda A, Sager TM, Molina RM, Donaghey TC, Alencar AM, Kasahara DI, Ericsson T, Millet EJ, Swenson J, Tschumperlin DJ, Butler JP, Brain JD, Fredberg JJ, Gehr P, Zhou EH (2010) Biomechanical effects of environmental and engineered particles on human airway smooth muscle cells. J R Soc Interface 7:S331–S340
9. Beutler E (1984) A manual of biochemical methods. Grune and Stratlon, Orlando, pp 74–76
10. Borenfreund E, Puerner JA (1985) A simple quantitative procedure using monolayer cultures for cytotoxicity assays (HTD/NR-90). J Tissue Cult Methods 9:7–9
11. Castano A, Vega M, Tarazona J (1995) Acute toxicity of selected metals and phenols on RTG-2 and CHSE-214 fish cell lines. Bull Environ Contam Toxicol 55:222–229
12. Chang H, Jwo CS, Lo CH, Tsung TT, Kao MJ, Lin HM (2005) Rheology of CuO nanoparticle suspension prepared by ASNSS. Rev Adv Mater Sci 10:128–132
13. Chen Z, Meng H, Yuan H, Xing G, Chen C, Zhao F, Wang Y, Zhang C, Zhao Y (2007) Identification of target organs of copper nanoparticles with ICPMS technique. J Radioanal Nucl Chem 272:599–603
14. Chio CP, Chen WY, Chou WC, Hsieh NH, Ling MP, Liao CM (2012) Assessing the potential risks to zebrafish posed by environmentally relevant copper and silver nanoparticles. Sci Total Environ 420:111–118
15. Davoren M, Fogarty AM (2006) In vitro cytotoxicity assessment of the biocidal agents sodium phenylphenol, sodiumbenzyl-chlorophenol, and sodium-tertiary amylphenol using established fish cell lines. Toxicol in Vitro 20:1190–1201
16. DeWitte-Orr S, Bols N (2005) Gliotoxin-induced cytotoxicity in three salmonid cell lines: Cell death by apoptosis and necrosis. Comp Biochem Physiol Part C: Toxicol Pharmacol 141:157–167
17. Fahmy B, Cormier SA (2009) Copper oxide nanoparticles induce oxidative stress and cytotoxicity in airway epithelial cells. Toxicol In Vitro 23:1365–1371
18. Fairey ER, Edmunds J, Deamer-Melia NJ, Glasgow H Jr, Johnson FM, Moeller PR, Burkholder J, Ramsdell JS (1999) Reporter gene assay for fish-killing activity produced by Pfiesteria piscicida. Environ Health Perspect 107:711
19. Farkas J, Christian P, Gallego-Urrea JA, Roos N, Hassellöv M, Tollefsen KE, Thomas KV (2011) Uptake and effects of manufactured silver nanoparticles in rainbow trout (Oncorhynchus mykiss) gill cells. Aquat Toxicol 101:117–125
20. Farkas J, Christian P, Urrea JA, Roos N, Hassellöv M, Tollefsen KE, Thomas KV (2010) Effects of silver and gold nanoparticles on rainbow trout (Oncorhynchus mykiss) hepatocytes. Aquat Toxicol 96:44–52
21. Farré M, Gajda-Schrantz K, Kantiani L, Barceló D (2009) Ecotoxicity and analysis of nanomaterials in the aquatic environment. Anal Bioanal Chem 393(1):81–95
22. Gomes T, Pereira CG, Cardoso C, Pinheiro JP, Cancio I, Bebianno MJ (2012) Accumulation and toxicity of copper oxide nanoparticles in the digestive gland of Mytilus galloprovincialis. Aquat Toxicol 118–119:72–79
23. Gomes T, Pinheiro JP, Cancio I, Pereira CG, Cardoso C, Bebianno MJ (2011) Effects of copper nanoparticles exposure in the mussel Mytilus galloprovincialis. Environ Sci Technol 21:9356–9362
24. Griffitt RJ, Weil R, Hyndman KA, Denslow ND, Powers K, Taylor D, Barber DS (2007) Exposure to copper nanoparticles causes gill injury and acute lethality in zebrafish (Danio rerio). Environ Sci Technol 41:8178–8186
25. Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione-S-transferase. The first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139
26. Hu W, Culloty S, Darmody G, Lynch S, Davenport J, Ramirez-Garcia S, Dawson KA, Lynch I, Blasco J, Sheehan D (2014) Toxicity of copper oxide nanoparticles in the blue mussel, Mytilus edulis: a redox proteomic investigation. Chemosphere 108:288–299
27. Kamei Y, Aoki M (2007) A chlorophyll c2 analogue from the marine brown alga Eisenia bicyclis inactivates the infectious hematopoietic necrosis virus, a fish rhabdovirus. Arch Virol 152:861–869
28. Karlsson HL, Cronholm P, Gustafsson J, Möller L (2008) Copper oxide nanoparticles are highly toxic: a comparison between metal oxide nanoparticles and carbon nanotubes. Chem Res Toxicol 21:1726–1732
29. Karlsson HL, Cronholm P, Hedberg Y, Tornberg M, De Battice L, Svedhem S, Wallinder IO (2013) Cell membrane damage and protein interaction induced by copper containing nanoparticles--importance of the metal release process. Toxicology 313:59–69
30. Kono Y (1978) Generation of superoxide radical during auto-oxidation of hydroxylamine and an assay for superoxide dismutase. Arch Biochem Biophys 186:189–195
31. Levine RL (1994) Carbonyl assays for determination of oxidatively modified proteins. Methods Enzymol 233:346–357
32. Linder MC (2001) Copper and genomic stability in mammals. Mutat Res Fundam Mol Mech Mutagen 475:141–152
33. Marroquí L, Estepa A, Perez L (2008) Inhibitory effect of mycophenolic acid on the replication of infectious pancreatic necrosis virus and viral hemorrhagic septicemia virus. Antivir Res 80:332–338
34. Midander K, Cronholm P, Karlsson HL, Elihn K, Möller L, Leygraf C, Wallinder IO (2009) Surface characteristics, copper release, and toxicity of nano- and micrometer-sized copper and copper (II) oxide particles: a cross disciplinary study. Small 5:389–399
35. Mori M, Wakabayashi M (2000) Cytotoxicity evaluation of chemicals using cultured fish cells. Water Sci Technol 42:277–282
36. Mossman T (1983) Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytotoxicity assays. J Immunol Methods 65:55–63
37. Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95:351–358
38. Ooi EL, Verjan N, Hirono I, Nochi T, Kondo H, Aoki T, Kiyono H, Yuki Y (2008) Biological characterisation of a recombinant Atlantic salmon type I interferon synthesized in Escherichia coli. Fish Shellfish Immunol 24:506–513
39. Radu M, Munteanu MC, Petrache S, Serban AI, Dinu D, Hermenean A, Sima C, Dinischiotu A (2010) Depletion of intracellular glutathione and increased lipid peroxidation mediate cytotoxicity of hematite nanoparticles in MRC-5 cells. Acta Biochim Pol 57:355–360
40. Rosenkranz P, Fernández-Cruz ML, Conde E, Ramírez-Fernández MB, Flores JC, Fernández M, Navas JM (2012) Effects of cerium oxide nanoparticles to fish and mammalian cell lines: an assessment of cytotoxicity and methodology. Toxicol In Vitro 26:888–896
41. Sayes CM, Reed KL, Warheit DB (2007) Assessing toxicity of fine and nanoparticles: comparing in vitro measurements to in vivo pulmonary toxicity profiles. Toxicol Sci 97:163–180
42. Semisch A, Ohle J, Witt B, Hartwig A (2014) Cytotoxicity and genotoxicity of nano – and microparticulate copper oxide: role of solubility and intracellular bioavailability. Part Fibre Toxicol 11:10
43. Shaw BJ, Al-Bairuty G, Handy RD (2012) Effects of waterborne copper nanoparticles and copper sulphate on rainbow trout,(Oncorhynchus mykiss): physiology and accumulation. Aquat Toxicol 116:90–101
44. Siddiqui MA, Alhadlaq HA, Ahmad J, Al-Khedhairy AA, Musarrat J, Ahamed M (2013) Copper oxide nanoparticles induced mitochondria mediated apoptosis in human hepatocarcinoma cells. PLoS ONE 8:e69534
45. Skjelbred B, Horsberg TE, Tollefsen KE, Andersen T, Edvardsen B (2011) Toxicity of the ichthyotoxic marine flagellate Pseudochattonella (Dictyochophyceae, Heterokonta) assessed by six bioassays. Harmful Algae 10:144–154
46. Skocaj M, Filipic M, Petkovic J, Novak S (2011) Titanium dioxide in our everyday life; is it safe? Radiol Oncol 45:227–247
47. Srikanth K, Ahmad I, Rao JV, Trindade T, Duarte AC, Pereira E (2014) Modulation of glutathione and its dependent enzymes in gill cells of Anguilla anguilla exposed to silica coated iron oxide nanoparticles with or without mercury co-exposure under in vitro condition. Comp Biochem Physiol C Toxicol Pharmacol 162:7–14
48. Tedesco S, Doyle H, Blasco J, Redmond G, Sheehan D (2010) Oxidative stress and toxicity of gold nanoparticles in Mytilus edulis. Aquat Toxicol 100:178–196
49. Tietze F (1969) Enzymic method for quantitative determination of nanogram amounts of total and oxidized glutathione: Applications to mammalian blood and other tissues. Anal Biochem 27:502–522
50. Wang Z, Li N, Zhao J, White JC, Qu P, Xing B (2012) CuO nanoparticle interaction with human epithelial cells: Cellular uptake, location, export, and genotoxicity. Chem Res Toxicol 25:1512–1521
51. Wang H, Joseph JA (1999) Quantifying cellular oxidative stress by dichlorofluorescin assay using microplate reader. Free Radic Biol Med 27:612–616
52. 4 magnetic nanoparticles on A549 Cells. Int J Mol Sci 14:15546–15560
53. Winterbourn C (2008) Reconciling the chemistry and biology of reactive oxygen species. Nat Chem Biol 4:278–286
54. 2, ZnO and their bulk counterparts on zebrafish: Acute toxicity, oxidative stress and oxidative damage. Sci Total Environ 409:1444–1452
55. Yang H, Liu C, Yang D, Zhang H, Xi Z (2009) Comparative study of cytotoxicity, oxidative stress and genotoxicity induced by four typical nanomaterials: the role of particle size, shape and composition. J Appl Toxicol 29:69–78
56. Zhou K, Wang R, Xu B, Li Y (2006) Synthesis, characterization and catalytic properties of CuO nanocrystals with various shapes. Nanotechnology 17:3939–3943