Earthworms and humans in vitro: Characterizing evolutionarily conserved stress and immune responses to silver nanoparticles

Environmental Science and Technology

Volumn 46, Issue 7, 2012, Pages 4166-4173

  Hayashi, Yuya ^a   Engelmann, Péter ^b   Foldbjerg, Rasmus ^a   Szabó, Mariann ^b   Somogyi, Ildikó ^b   Pollák, Edit ^b   Molnár, László ^b   Autrup, Herman ^a   Sutherland, Duncan S ^a   Scott Fordsmand, Janeck ^a   Heckmann, Lars Henrik ^a  

^a AARHUS UNIVERSITY   (Denmark)

^b UNIVERSITY OF PÉCS   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL KINGDOM; BIOLOGICAL PROCESS; CELLULAR TOXICITIES; COELOMOCYTES; EARTHWORM EISENIA FETIDA; ECOSYSTEM HEALTH; HUMAN CELLS; IMMUNE RESPONSE; IN-VITRO; IN-VITRO ANALYSIS; INNATE IMMUNITY; INTRACELLULAR ACCUMULATION; MOLECULAR SIGNATURES; PERIPHERAL BLOOD MONONUCLEAR CELLS; POTENTIAL THREATS; PRIMARY CELLS; SIGNALING PROCESS; SILVER NANOPARTICLES; SILVER SALTS; SOIL INVERTEBRATES; TIME-RESOLVED;

CELL CULTURE; CELLS; GENES; IMMUNOLOGY; NANOPARTICLES; TOXICITY; TRANSMISSION ELECTRON MICROSCOPY;

SILVER;

CATALASE; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 70 KDA PROTEIN 8; METALLOTHIONEIN II; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE 1; MYELOID DIFFERENTIATION FACTOR 88; PROTEIN KINASE C; PROTEIN KINASE C1; REACTIVE OXYGEN METABOLITE; SILVER NANOPARTICLE; UNCLASSIFIED DRUG;

EARTHWORM; ECOSYSTEM HEALTH; ECOTOXICOLOGY; GENE EXPRESSION; HOMINID; IMMUNE RESPONSE; IMMUNITY; MOLECULAR ANALYSIS; NANOTECHNOLOGY; SILVER; SOIL FAUNA; TOXICITY TEST;

ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; CELL DIFFERENTIATION; CELL STRAIN THP 1; CELL TYPE; CELL VIABILITY; CELLULAR IMMUNITY; CELOMOCYTE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOTOXICITY; EISENIA FETIDA; FEMALE; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IMMUNOMODULATION; IN VITRO STUDY; INNATE IMMUNITY; INTRACELLULAR TRANSPORT; LEUKEMIA CELL; LEUKEMIA CELL LINE; MALE; NONHUMAN; OXIDATIVE STRESS; PERIPHERAL BLOOD MONONUCLEAR CELL; PHAGOCYTOSIS; TRANSMISSION ELECTRON MICROSCOPY;

ANIMALS; BIOLOGICAL EVOLUTION; CELL DEATH; CELL LINE; FEMALE; GENE EXPRESSION REGULATION; HUMANS; IMMUNITY; LEUKOCYTES, MONONUCLEAR; MALE; METAL NANOPARTICLES; OLIGOCHAETA; REACTIVE OXYGEN SPECIES; SILVER; STRESS, PHYSIOLOGICAL; TIME FACTORS;

ANIMALIA; EISENIA FETIDA; INVERTEBRATA;

EID: 84859366514     PISSN: 0013936X     EISSN: 15205851     Source Type: Journal    
DOI: 10.1021/es3000905     Document Type: Article

References (40)

1. Benn, T. M.; Westerhoff, P. Nanoparticle silver released into water from commercially available sock fabrics Environ. Sci. Technol. 2008, 42 (11) 4133-4139
2. Kim, B.; Park, C.-S.; Murayama, M.; Hochella, M. F. Discovery and characterization of silver sulfide nanoparticles in final sewage sludge products Environ. Sci. Technol. 2010, 44 (19) 7509-7514
3. Liu, J.; Pennell, K. G.; Hurt, R. H. Kinetics and mechanisms of nanosilver oxysulfidation Environ. Sci. Technol. 2011, 45 (17) 7345-7353
4. Coutris, C.; Hertel-Aas, T.; Lapied, E.; Joner, E. J.; Oughton, D. H. Bioavailability of cobalt and silver nanoparticles to the earthworm Eisenia fetida Nanotoxicology 2012, 6 (2) 186-195
5. Heckmann, L.-H.; Hovgaard, M.; Sutherland, D.; Autrup, H.; Besenbacher, F.; Scott-Fordsmand, J. Limit-test toxicity screening of selected inorganic nanoparticles to the earthworm Eisenia fetida Ecotoxicology 2011, 20 (1) 226-233
6. Shoults-Wilson, W. A.; Reinsch, B. C.; Tsyusko, O. V.; Bertsch, P. M.; Lowry, G. V.; Unrine, J. M. Effect of silver nanoparticle surface coating on bioaccumulation and reproductive toxicity in earthworms (Eisenia fetida) Nanotoxicology 2011, 5 (3) 432-444
7. Lapied, E.; Moudilou, E.; Exbrayat, J.-M.; Oughton, D. H.; Joner, E. J. Silver nanoparticle exposure causes apoptotic response in the earthworm Lumbricus terrestris (Oligochaeta) Nanomedicine 2010, 5 (6) 975-984
8. Shoults-Wilson, W.; Zhurbich, O.; McNear, D.; Tsyusko, O.; Bertsch, P.; Unrine, J. Evidence for avoidance of Ag nanoparticles by earthworms (Eisenia fetida) Ecotoxicology 2011, 20 (2) 385-396
9. Hartenstein, V. Blood cells and blood cell development in the animal kingdom Annu. Rev. Cell Dev. Biol. 2006, 22 (1) 677-712
10. Cooper, E. L.; Roch, P. Earthworm immunity: A model of immune competence Pedobiologia 2004, 47, 676-688
11. Stürzenbaum, S. R.; Georgiev, O.; Morgan, A. J.; Kille, P. Cadmium detoxification in earthworms: From genes to cells Environ. Sci. Technol. 2004, 38 (23) 6283-6289
12. Bihari, P.; Vippola, M.; Schultes, S.; Praetner, M.; Khandoga, A.; Reichel, C.; Coester, C.; Tuomi, T.; Rehberg, M.; Krombach, F. Optimized dispersion of nanoparticles for biological in vitro and in vivo studies Part. Fibre Toxicol. 2008, 5 (1) 14
13. Casals, E.; Pfaller, T.; Duschl, A.; Oostingh, G. J.; Puntes, V. Time evolution of the nanoparticle protein corona ACS Nano 2010, 4 (7) 3623-3632
14. Beer, C.; Foldbjerg, R.; Hayashi, Y.; Sutherland, D. S.; Autrup, H. Toxicity of silver nanoparticles-Nanoparticle or silver ion? Toxicol. Lett. 2012, 208 (3) 286-292
15. Engelmann, P.; Pálinkás, L.; Cooper, E. L.; Németh, P. Monoclonal antibodies identify four distinct annelid leukocyte markers Dev. Comp. Immunol. 2005, 29 (7) 599-614
16. Park, E.; Jung, H.; Yang, H.; Yoo, M.; Kim, C.; Kim, K. Optimized THP-1 differentiation is required for the detection of responses to weak stimuli Inflamm. Res. 2007, 56 (1) 45-50
17. Foldbjerg, R.; Olesen, P.; Hougaard, M.; Dang, D. A.; Hoffmann, H. J.; Autrup, H. PVP-coated silver nanoparticles and silver ions induce reactive oxygen species, apoptosis and necrosis in THP-1 monocytes Toxicol. Lett. 2009, 190 (2) 156-162
18. Krejsa, C. M.; Schieven, G. L. Detection of oxidative stress in lymphocytes using dichlorodihydrofluorescein diacetate. In Stress Response; Walker, J. M.; Keyse, S. M., Eds.; Humana Press, 2000; Vol. 99, pp 35-47.
19. Peirson, S. N.; Butler, J. N.; Foster, R. G. Experimental validation of novel and conventional approaches to quantitative real-time PCR data analysis Nucleic Acids Res. 2003, 31 (14) e73
20. Heckmann, L.-H.; Sorensen, P.; Krogh, P.; Sorensen, J. NORMA-Gene: A simple and robust method for qPCR normalization based on target gene data BMC Bioinf. 2011, 12 (1) 250
21. Suzuki, H.; Toyooka, T.; Ibuki, Y. Simple and easy method to evaluate uptake potential of nanoparticles in mammalian cells using a flow cytometric light scatter analysis Environ. Sci. Technol. 2007, 41 (8) 3018-3024
22. Lundqvist, M.; Stigler, J.; Elia, G.; Lynch, I.; Cedervall, T.; Dawson, K. A. Nanoparticle size and surface properties determine the protein corona with possible implications for biological impacts Proc. Natl. Acad. Sci. U. S. A. 2008, 105 (38) 14265-14270
23. Walczyk, D.; Bombelli, F. B.; Monopoli, M. P.; Lynch, I.; Dawson, K. A. What the cell "sees" in bionanoscience J. Am. Chem. Soc. 2010, 132 (16) 5761-5768
24. Hollinger, M. A. Toxicological Aspects of Topical Silver Pharmaceuticals Crit. Rev. Toxicol. 1996, 26 (3) 255-260
25. Lunov, O.; Syrovets, T.; Loos, C.; Beil, J.; Delacher, M.; Tron, K.; Nienhaus, G. U.; Musyanovych, A.; Mailänder, V.; Landfester, K.; Simmet, T. Differential uptake of functionalized polystyrene nanoparticles by human macrophages and a monocytic cell line ACS Nano 2011, 5 (3) 1657-1669
26. 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 Environ. Sci. Technol. 2007, 41 (11) 4158-4163
27. Navarro, E.; Piccapietra, F.; Wagner, B.; Marconi, F.; Kaegi, R.; Odzak, N.; Sigg, L.; Behra, R. Toxicity of silver nanoparticles to Chlamydomonas reinhardtii Environ. Sci. Technol. 2008, 42 (23) 8959-8964
28. Liu, J.; Hurt, R. H. Ion release kinetics and particle persistence in aqueous nano-silver colloids Environ. Sci. Technol. 2010, 44 (6) 2169-2175
29. Locht, L.; Larsen, A.; Stoltenberg, M.; Danscher, G. Cultured macrophages cause dissolucytosis of metallic silver Histol. Histopathol. 2009, 24, 167-173
30. Reinecke, F.; Levanets, O.; Olivier, Y.; Louw, R.; Semete, B.; Grobler, A.; Hidalgo, J.; Smeitink, J.; Olckers, A.; Van der Westhuizen, F. H. Metallothionein isoform 2A expression is inducible and protects against ROS-mediated cell death in rotenone-treated HeLa cells Biochem. J. 2006, 395 (2) 405-415
31. Eom, H.-J.; Choi, J. p38 MAPK activation, DNA damage, cell cycle arrest and apoptosis as mechanisms of toxicity of silver nanoparticles in jurkat T cells Environ. Sci. Technol. 2010, 44 (21) 8337-8342
32. Hsin, Y. H.; Chen, 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 (3) 130-139
33. Ahamed, M.; Posgai, R.; Gorey, T. J.; Nielsen, M.; Hussain, S. M.; Rowe, J. J. Silver nanoparticles induced heat shock protein 70, oxidative stress and apoptosis in Drosophila melanogaster Toxicol. Appl. Pharmacol. 2010, 242 (3) 263-269
34. Olchawa, E.; Bzowska, M.; Stürzenbaum, S. R.; Morgan, A. J.; Plytycz, B. Heavy metals affect the coelomocyte-bacteria balance in earthworms: Environmental interactions between abiotic and biotic stressors Environ. Pollut. 2006, 142 (2) 373-381
35. Aksoy, E.; Goldman, M.; Willems, F. Protein kinase C epsilon: A new target to control inflammation and immune-mediated disorders Int. J. Biochem. Cell Biol. 2004, 36 (2) 183-188
36. Larsen, E. C.; Ueyama, T.; Brannock, P. M.; Shirai, Y.; Saito, N.; Larsson, C.; Loegering, D.; Weber, P. B.; Lennartz, M. R. A role for PKC-ε in FcγR-mediated phagocytosis by RAW 264.7 cells J. Cell Biol. 2002, 159 (6) 939-944
37. Wong, C. K.; Li, P. W.; Lam, C. W. K. Intracellular JNK, p38 MAPK and NF-κB regulate IL-25 induced release of cytokines and chemokines from costimulated T helper lymphocytes Immunol. Lett. 2007, 112 (2) 82-91
38. Shin, S. H.; Ye, M. K.; Kim, H. S.; Kang, H. S. The effects of nano-silver on the proliferation and cytokine expression by peripheral blood mononuclear cells Int. Immunopharmacol. 2007, 7 (13) 1813-1818
39. Castillo, P. M.; Herrera, J. L.; Fernandez-Montesinos, R.; Caro, C.; Zaderenko, A. P.; Mejías, J. A.; Pozo, D. Tiopronin monolayer-protected silver nanoparticles modulate IL-6 secretion mediated by Toll-like receptor ligands Nanomedicine 2008, 3 (5) 627-635
40. 2) on Mytilus hemocytes Aquat. Toxicol. 2010, 96 (2) 151-158