Changes in the Daphnia magna midgut upon ingestion of copper oxide nanoparticles: A transmission electron microscopy study

Water Research

Volumn 45, Issue 1, 2011, Pages 179-190

  Heinlaan, Margit ^a,c   Kahru, Anne ^a   Kasemets, Kaja ^a   Arbeille, Brigitte ^b   Prensier, Gérard ^b   Dubourguier, Henri Charles ^a,c  

^a NATIONAL INSTITUTE OF CHEMICAL PHYSICS AND BIOPHYSICS   (Estonia)

^b UNIVERSITÉ DE TOURS   (France)

^c ESTONIAN UNIVERSITY OF LIFE SCIENCES   (Estonia)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; CYTOLOGY; HIGH RESOLUTION TRANSMISSION ELECTRON MICROSCOPY; METAL IONS; NANOPARTICLES; TOXICITY;

ACUTE TOXICITY; COPPER OXIDE NANOPARTICLES; CU IONS; CUO NANOPARTICLES; DAPHNIA MAGNA; DAPHNIDS; EPITHELIAL CELLS; FOLLOW UP; ULTRASTRUCTURAL CHANGES; WATER FLEA;

COPPER OXIDES;

COPPER ION; COPPER OXIDE; COPPER OXIDE NANOPARTICLE; METAL NANOPARTICLE; UNCLASSIFIED DRUG;

BACTERIUM; CATION; COPPER COMPOUND; CRUSTACEAN; DOSE-RESPONSE RELATIONSHIP; ECOTOXICOLOGY; INGESTION RATE; NANOTECHNOLOGY; OXIDE; POLLUTION EXPOSURE; RECOMBINATION; SECRETION; TOXICITY TEST; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE;

ARTICLE; BACTERIAL COLONIZATION; CELL MEMBRANE; CELL ULTRASTRUCTURE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DAPHNIA; ENVIRONMENTAL EXPOSURE; EPITHELIUM CELL; INGESTION; MEMBRANE VESICLE; MICROVILLUS; MIDGUT; NANOSENSOR; NANOTOXICOLOGY; NONHUMAN; PARTICLE SIZE; PRIORITY JOURNAL; STOMACH SECRETION; TOXICITY; TRANSMISSION ELECTRON MICROSCOPY;

BACTERIA (MICROORGANISMS); CLADOCERA; DAPHNIA MAGNA; DAPHNIIDAE;

EID: 78649649690     PISSN: 00431354     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.watres.2010.08.026     Document Type: Article

References (45)

1. Alves D.M.A., Diniz, M.S., Mendonça, E., Peres, I., Silva, L., Brito Correia, J., Picado, A., 2009. Histopathological and ultrastructural observations of Daphnia magna exposed to diamond nanoparticles. In: Abstract of the Joint Congress of the Spanish and Portuguese Microscopy Societies, Segovia, Spain, June 16-19, 2009.
2. Arnold W.R., Santore R.C., Cotsifas J.S. Predicting copper toxicity in estuarine and marine waters using the biotic ligand model. Marine Pollution Bulletin 2005, 50:1634-1640.
3. 2 to microalgae Pseudokirchneriella subcapitata. Science of the Total Environment 2009, 407:1461-1468.
4. Avtsyn A.P., Petrova T.P. Resistance of the alimentary canal of Daphnia magna Straus to enteropathogenic Nag vibrios. Bulletin of Experimental Biology and Medicine 1986, 102(3):1269-1272.
5. Bambang Y., Thuet P., Charmantier-Daures M., Trilles J.P., Charmantier G. Effect of copper on survival and osmoregulation of various developmental stages of the shrimp Penaeus japonicus bate (crustacea, decapoda). Aquatic Toxicology 1995, 33:125-139.
6. Baun A., Hartmann N.B., Grieger K. Ecotoxicity of engineered nanoparticles to aquatic invertebrates: a brief review and recommendations for future toxicity testing. Ecotoxicology 2008, 17:387-395.
7. Bianchini A., Martins S.E.G., Barcarolli I.F. Mechanism of acute copper toxicity in euryhaline crustaceans: implications for the Biotic Ligand Model. International Congress Series 2004, 1275:189-194.
8. Blinova I., Ivask A., Heinlaan M., Mortimer M., Kahru A. Ecotoxicity of nanoparticles of CuO and ZnO in natural water. Environmental Pollution 2010, 158(1):41-47.
9. Bodar C.W.M., van Donselaar E.G., Herwing H.J. Cytopathological investigations of digestive tract and storage cells in Daphnia magna exposed to cadmium and tributyltin. Aquatic Toxicology 1990, 17:325-338.
10. Brooks S.J., Mills C.L. The effect of copper on osmoregulation in the freshwater amphipod Gammarus pulex. Comparative Biochemistry and Physiology, Part A 2003, 135:527-537.
11. Chatton E. Les membranes péritrophiques des Drosophiles (Diptères) et des Daphnies (Cladocères); leur genèse et leur role a'légard des parasites intestinaux. Bulletin de la Société Zoologique de France 1920, 45:265-280.
12. Daphtoxkit F™magna Crustacean Toxicity Screening Test for Freshwater 1996, Standard Operational Procedure, Creasel, Deinze, Belgium, p. 16.
13. Gaino E., Rebora M., Taddei A.R., Mazzini M. Ultrastructural aspects of the alimentary canal in some mayflies. Ephemeroptera & Plecoptera 1997, 332-337. Biology-Ecology-Systematics, Mauron + Tinguely & Lachat, SA, Fribourg. P. Landolt, M. Sartori (Eds.).
14. Griffiths P.R.E. Morphological and ultrastructural effects of sublethal cadmium poisoning on Daphnia. Environmental Research 1980, 22:277-284.
15. Griffitt R.J., Luo J., Gao J., Bonzongo J.-C., Barber D.S. Effects of particle composition and species on toxicity of metallic nanomaterials in aquatic organisms. Environmental Toxicology and Chemistry 2008, 27(8):1972-1978.
16. Hansen U., Peters W. Structure and permeability of the peritrophic membranes of some small crustaceans. Zoologischer Anzeiger -A Journal of Comparative Zoology 1997/1998, 236:103-108.
17. 2 to bacteria Vibrio fischeri and crustaceans Daphnia magna and Thamnocephalus platyurus. Chemosphere 2008, 71(7):1308-1316.
18. Ivask, A., Bondareno, O., Jepihhina, N., Kahru, A. Profiling of the reactive oxygen species related ecotoxicity of CuO, ZnO, TiO2, silver and fullerene nanoparticles using a set of recombinant luminescent Escherichia coli strains: differentiating the impact of particles and solubilised metals. Analytical and Bioanalytical Chemistry, in press, doi:10.1007/s00216-010-3962-7.
19. Ivask A., Rõlova T., Kahru A. A suite of recombinant luminescent bacterial strains for the quantification of bioavailable heavy metals and toxicity testing. BMC Biotechnology 2009, 9:41. 10.1186/1472-6750-9-41.
20. Kahru A., Dubourguier H.-C. From ecotoxicology to nanoecotoxicology. Toxicology 2010, 269(2-3):105-119.
21. Kahru A., Dubourguier H.-C., Blinova I., Ivask A., Kasemets K. Biotests and biosensors for ecotoxicology of metal oxide nanoparticles: a minireview. Sensors 2008, 8:5156-5170.
22. Kahru A., Savolainen K. Potential hazard of nanoparticles: from properties to biological and environmental effects. Toxicology 2010, 269(2-3):89-91.
23. Karlsson H.K., Cronholm P., Gustafsson J., Möller L. Copper oxide nanoparticles are highly toxic: a comparison between metal oxide nanoparticles and carbon nanotubes. Chemical Research in Toxicology 2008, 21(9):1726-1732.
24. 2 to yeast Saccharomyces cerevisiae. Toxicology In Vitro 2009, 23(6):1116-1122.
25. Kühnel D., Busch W., Meißner T., Springer A., Potthoff A., Richter V., Gelinsky M., Scholz S., Schirmer K. Agglomeration of tungsten carbide nanoparticles in exposure medium does not prevent uptake and toxicity toward a rainbow trout gill cell line. Aquatic Toxicology 2009, 93:91-99.
26. Leedjärv A., Ivask A., Virta M., Kahru A. Analysis of bioavailable phenols from natural samples by recombinant luminescent bacterial sensors. Chemosphere 2006, 64:1910-1919.
27. Limbach L.K., Wick P., Manser P., Grass R.N., Bruinink A., Stark W.J. Exposure of engineered nanoparticles to human lung epithelial cells: influence of chemical composition and catalytic activity on oxidative stress. Environmental Science and Technology 2007, 41:4158-4163.
28. Lovern S.B., Owen H.A., Klaper R. Electron microscopy of gold nanoparticle intake in the gut of Daphnia magna. Nanotoxicology 2008, 2(1):43-48.
29. Material Safety Data Sheet: Cupric Oxide 2008, (CAS No.: 1317-38-0). Available at, (Last accessed 29.06.10). http://www.jtbaker.com/msds/englishhtml/C5885.htm.
30. McDowell E.M., Trump B.J. Histological fixatives suitable for diagnostic light and electron microscopy. Archives of Pathology and Laboratory Medicine 1976, 100:405-414.
31. Mortimer M., Kasemets K., Kahru A. Toxicity of ZnO and CuO nanoparticles to ciliated protozoa Tetrahymena thermophila. Toxicology 2010, 269(2-3):182-189.
32. Mühlfeld C., Rothen-Rutishauser B., Vanhecke D., Blank F., Gehr P., Ochs M. Visualization and quantitative analysis of nanoparticles in the respiratory tract by transmission electron microscopy. Particle and Fibre Toxicology 2007, 4:11. 10.1186/1743-8977-4-11.
33. Nogueira I.C.G., Lobo-da-Cunha A., Vasconcelos V.M. Effects of Cylindrospermopsis raciborskii and Aphanizomenon ovalisporum (cyanobacteria) ingestion on Daphnia magna midgut and associated diverticula epithelium. Aquatic Toxicology 2006, 80(2):194-203.
34. OECD OECD Guidelines for the Testing of Chemicals/Section 2: Effects on Biotic Systems, Test No. 202: Daphnia sp. Acute Immobilisation Test 2004, OECD Publishing.
35. Peter H., Sommaruga R. An evaluation of methods to study the gut bacterial community composition of freshwater zooplankton. Journal of Plankton Research 2008, 30(9):997-1006.
36. Petersen E.J., Akkanen J., Kukkonen J.V.K., Weber W.J. Biological uptake and depuration of carbon nanotubes by Daphnia magna. Environmental Science and Technology 2009, 43(8):2969-2975.
37. Poynton H.C., Varshavsky J.R., Chang B., Cavigiolio G., Chan S., Holman P.S., Loguinov A.V., Bauer D.J., Komachi K., Theil E.C., Perkins E.J., Hughes O., Vulpe C.D. Daphnia magna ecotoxicogenomics provides mechanistic insights into metal toxicity. Environmental Science and Technology 2007, 41:1044-1050.
38. Quaglia A., Sabelli B., Villiani L. Studies on the intestine of Daphnidae (Crustacea, Cladocera). Ultrastructure of the midgut of Daphnia magna and Daphnia obtusa. Journal of Morphology 1976, 150:711-726.
39. Rosenkranz P., Chaudhry Q., Stone V., Fernandes T.F. A comparison of nanoparticle and fine particle uptake by Daphnia magna. Environmental Toxicology and Chemistry 2009, 28(10):2142-2149.
40. Schoenberg S.A., Maccubbin A.E., Hodson R.E. Cellulose digestion by freshwater microrustacea. Limnology and Oceanography 1984, 29(5):1132-1136.
41. Schultz T.W., Kennedy J.R. The fine structure of the digestive system of Daphnia pulex (crustacea: Cladocera). Tissue and Cell 1976, 3:479-490.
42. Sutcliffe D.W. Quantitative aspects of oxygen uptake by Gammarus (Crustacea, Amphipoda): a critical review. Freshwater Biology 1984, 14(5):443-489.
43. Tervonen K., Waissi G., Petersen E.J., Akkanen J., Kukkonen J.V.K. Analysis of fullerene-C60 and kinetic measurements for its accumulation and depuration in Daphnia magna. Environmental Toxicology and Chemistry 2009, 29(5):1072-1078.
44. Thomas K.V., Brooks S. The environmental fate and effects of antifouling paint biocides. Biofouling 2010, 26(1):73-88.
45. 60 nanoparticles protect against short-term UV and fluoranthene photo-induced toxicity, but cause long term cellular damage in Daphnia magna. Aquatic Toxicology 2009, 10.1016/j.aquatox.2009.08.011.