Comparative in vivo assessment of some adverse bioeffects of equidimensional gold and silver nanoparticles and the attenuation of nanosilver's effects with a complex of innocuous bioprotectors

International Journal of Molecular Sciences

Volumn 14, Issue 2, 2013, Pages 2449-2483

  Katsnelson, Boris A ^a   Privalova, Larisa I ^a   Gurvich, Vladimir B ^a   Makeyev, Oleg H ^b   Shur, Vladimir Ya ^c   Beikin, Yakov B ^d   Sutunkova, Marina P ^a   Kireyeva, Ekaterina P ^a   Minigalieva, Ilzira A ^a   Loginova, Nadezhda V ^a   Vasilyeva, Marina S ^b   Korotkov, Artem V ^b   Shuman, Eugene A ^b   Vlasova, Larisa A ^b   Shishkina, Ekaterina V ^c   Tyurnina, Anastasia E ^c   Kozin, Roman V ^c   Valamina, Irene E ^b   Pichugova, Svetlana V ^d   Tulakina, Ludmila G ^d  

^a The Ekaterinburg Medical Research Center for Prophylaxis and Health Protection in Industrial Workers   (Russian Federation)

^b URAL STATE MEDICAL UNIVERSITY   (Russian Federation)

^c URAL FEDERAL UNIVERSITY   (Russian Federation)

^d City Clinical Diagnostics Centre   (Russian Federation)

Author keywords

Bioprotectors; Bronchoalveolar lavage; Genotoxicity; Nanogold; Nanosilver; Subchronic toxicity

Indexed keywords

ACETYLCYSTEINE; AMINO ACID; CALCIUM; FISH OIL; GLUTAMATE SODIUM; GLYCINE; GOLD NANOPARTICLE; MULTIVITAMIN; PECTIN; PROTECTIVE AGENT; SELENIUM; SILVER NANOPARTICLE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ATOMIC FORCE MICROSCOPY; CELL NUCLEUS; CELL SUSPENSION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DNA FRAGMENTATION; DRUG CYTOTOXICITY; ENDOCYTOSIS; FEMALE; GENOTOXICITY; HISTOPATHOLOGY; INTERNALIZATION; KIDNEY; LIVER; LUNG ALVEOLUS MACROPHAGE; MITOCHONDRION; NANOTOXICOLOGY; NEUTROPHIL; NONHUMAN; PHAGOCYTOSIS; RAT; SPLEEN; TOXICOKINETICS; TRANSMISSION ELECTRON MICROSCOPY;

EID: 84875109377     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms14022449     Document Type: Article

References (72)

1. 4) suspensions with different particle sizes in the nanometer and micrometer ranges: Are we defenseless against nanoparticles? Int. J. Occup. Environ. Health 2010, 16, 508-524.
2. 4 (magnetite) nanoparticles. Cent. Eur. J. Occup. Environ. Med. 2010, 16, 47-63.
3. 4 nano-and microparticles following repeated intraperitoneal administration to rats. Int. J. Toxicol. 2010, 30, 60-67.
4. 4 nanoparticles and alveolar macrophages. Bull. Exp. Biol. Med. 2012, 152, 627-631.
5. Katsnelson, B.A.; Privalova, L.I.; Sutunkova, M.P.; Khodos, M.Y.; Shur, V.Y.; Shishkina, E.V.; Tulakina, L.G.; Pichugova, S.V.; Beikin, J.B. Uptake of some metallic nanoparticles by, and their impact on pulmonary macrophages in vivo as viewed by optical, atomic force, and transmission electron microscopy. J. Nanomed. Nanotechnol. 2012, 3, 1-8.
6. 4. Nanotechnology 2012, doi:10.5402/2012/143613.
7. Arora, S.; Jain, J.; Rajwade, J.M.; Paknikar, K.M. Interactions of silver nanoparticles with primary mouse fibroblasts and liver cells. Toxicol. Appl. Pharmacol. 2009, 236, 310-318.
8. Ahamed, M.; AlSalhi, M.S.; Siddiqui, M.K.J. Silver nanoparticles applications and human health. Clin. Chim. Acta. 2010, 411, 1841-1184.
9. Trickler, W.J.; Lantz, S.M.; Murdock, R.C.; Schrand, A.M.; Robinson, B.L.; Newport, G.D.; Schlager, J.J.; Oldenburg, S.J.; Paule, M.G.; Slikker, W., Jr.; et al. Silver nanoparticle induced blood-brain barrier inflammation and increased permeability in primary rat brain micro vessel endothelial cells. Toxicol. Sci. 2010, 118, 160-170.
10. Park, E.-J.; Bae, E.; Yi, Y.; Yi, J.; Younghun, K.; Choi, K.; Lee, S.H.; Yoon, J.; Lee, C.; Park, K. Repeated-dose toxicity and inflammatory responses in mice by oral administration of silver nano-particles. Environ. Toxicol. Pharmacol. 2010, 30, 162-168.
11. Choi, J.E.; Kim, S.; Ahn, J.H.; Youn, P.; Kang, J.S.; Park, K.; Yi, J.; Ryu, D.Y. Induction of oxidative stress and apoptosis by silver nanoparticles in the liver of adult zebrafish. Aquat. Toxicol. 2010, 100, 151-159.
12. Kim, Y.S.; Song, M.Y.; Park, J.D.; Song, R.S.; Ryu, H.R.; Chung, Y.H.; Chang, H.K.; Lee, J.H.; Oh, K.H.; Kelman, B.J.; Hwang, I.K.; Yu, I.J. Subchronic oral toxicity of silver nanoparticles. Part. Fibre Toxicol. 2010, 7, 20.
13. Ahmadi, F.; Kordestany, A.H. Investigation on silver retention in different organs and oxidative stress enzymes in male broiler fed diet supplemented with powder of nano silver. Am-Euras. J. Toxicol. Sci. 2011, 3, 28-35.
14. Park, M.V.D.Z.; Neigh, A.M.; Vermeulen, J.P.; de la Fonteyne, L.J.J.; Verharen, H.W.; Biede, J.J.; van Loveren, H.; de Jong, W.H. The effect of particle size on the cytotoxicity, inflammation, developmental toxicity and genotoxicity of silver nanoparticles. J. Biomater. 2011, 32, 9810-9817.
15. Stebounova, L.V.; Adamcakova-Dodd, A.; Kim, J.S. Nanosilver induces minimal lung toxicity or inflammation in a subacute murine inhalation model. Part. Fibre Toxicol. 2011, 8, 5.
16. Srivastava, M.; Singh, S.; Self, W.T. Exposure to silver nanoparticles inhibits selenoprotein synthesis and the activity of thioredoxin reductase. Environ. Health Perspect. 2011, 120, 56-61.
17. Beer, C.; Foldbjerg, R.; Hayashi, Y.; Sutherland, D.S.; Autrup, H. Toxicity of silver nanoparticles-Nanoparticle or silver ion? Toxicol. Lett. 2012, 208, 286-292.
18. Bakri, S.J.; Pulido, J.S.; Mukerjee, P.; Marler, R.J.; Mukhopadhyay, D. Absence of histologic retinal toxicity of intravitreal nanogold in a rabbit model. Retina 2008, 28, 147-149.
19. Pan, Y.; Leifert, A.; Ruau, D.; Neuss, S.; Bornemann, J.; Schmid, G.; Brandau, W.; Simon, U.; Jahnen-Dechent, W. Gold nanoparticles of diameter 1.4 nm trigger necrosis by oxidative stress and mitochondrial damage. Small 2009, 5, 2067-2076.
20. Rudolf, R.; Friedrich, B.; Stopic, S.; Anzel, I.; Tomic, S.; C'Olic, M. Cytotoxicity of gold nanoparticles prepared by ultrasonic spray pyrolysis. J. Biomater. Appl. 2012, 26, 595-612.
21. Balasurbamanian, S.K.; Jittiwat, J.; Manikandan, J.; Ong, Ch.-N.; Yu, L.E.; Ong, W.-Y. Biodistribution of gold nanoparticles and gene expression changes in the liver and spleen after intravenous administration in rats. Biomaterials 2010, 31, 2034-2042.
22. Chen, Y.-Sh.; Hung, Y.-Ch.; Huang, G.S. Assessment of the in vivo toxicity of gold nanoparticles. Nanoscale Res. Lett. 2009, 4, 858-864.
23. Trickler, W.J.; Lantz, S.M.; Murdock, R.C.; Newport, G.D.; Oldenburg, S.J.; Paule, M.G.; Robinson, B.L.; Schlager, J.J.; Schrand, A.M.; Slikker, W.; Ali, S.F. Brain microvessel endothelial cells responses to gold microparticles: In vitro pro-inflammatory mediators and permeability. Nanotoxicology 2011, 5, 479-492.
24. Zhang, Q.; Hitchins, V.M.; Schrand, A.M.; Hussain, S.M.; Goering, P.L. Uptake of gold nanoparticles in murine macrophage cells without cytotoxicity or production of proinflammatory mediators. Nanotoxicology 2010, 5, 284-295.
25. Glazer, E.S.; Zhu, C.; Hamir, A.N.; Borne, A.; Thompson, C.S.; Curley, S.A. Biodistribution and acute toxicity of naked gold nanoparticles in a rabbit hepatic tumor model. Nanotoxicology 2011, 5, 459-468.
26. Mustafa, T.; Watanabe, F.; Monroe, W.; Mahmood, M.; Xu, Y.; Saeed, L.M.; Karmakar, A.; Casciano, D.; All, S.; Biris, A.S. Impact of gold nanoparticle concentration on their cellular uptake by MC3T3-E1 mouse osteoblastic cells as analyzed by transmission electron microscopy. J. Nanomed. Nanotechnol. 2011, 2, 1-8.
27. Dykman, L.; Khlebtsov, N. Gold nanoparticles in biomedical applications: Recent advances and perspectives. Chem. Soc. Rev. 2012, 41, 2256-2282.
28. Li, T.; Albee, B.; Alemayehu, M.; Diaz, R.; Ingham, L.; Kamal, S.; Rodriguez, M.; Bishnoi, S.W. Comparative toxicity study of Ag, Au, Ag-Au bimetallic nanoparticles on Daphnia magna. Anal. Bioanal. Chem. 2010, 398, 689-700.
29. Asharani, P.V.; Lianwu, Y.; Gong, Z.; Valiyaveettil, S. Comparison of the toxicity of silver, gold and platinum nanoparticles in developing zebrafish embryos. Nanotoxicology 2011, 5, 43-54.
30. 2) nanoparticles at two trophic levels: Plant and human lymphocytes. Chemosphere 2010, 81, 1253-1262.
31. Trouiller, B.; Reliene, R.; Westbrook, A.; Solaimani, P.; Schiestl, R.H. Titanium dioxide nanoparticles induce DNA damage and genetic instability in vivo in mice. Cancer Res. 2009, 69, 8784-8789.
32. Hackenberg, S.; Scherzed, A.; Kessler, M.; Hummel, S.; Technau, A.; Froelich, K.; Ginzkey, C.; Koehler, C.; Hangen, R.; Kleinsasser, N. Silver nanoparticles: Evaluation of DNA damage, toxicity and functional impairment in human mesenchymal stem cell. Toxicol. Lett. 2011, 201, 27-33.
33. Downs, T.R.; Crosby, M.E.; Hu, T.; Kumar, S.; Sullivan, A.; Sarlo, K.; Reeder, B.; Lynch, M.; Wagner, M.; Mills, T.; Pfuhler, S. Silica nanoparticles administered at the maximum tolerated dose induce genotoxic effect through an inflammatory reaction while gold nanoparticles do not. Mutat. Res. 2012, 745, 38-50.
34. Nabeshi, H.; Yoshikawa, T.; Matsuyama, K.; Nakazato, Y.; Tochigi. S.; Kondoh, S.; Hirai, T.; Akase, T.; Nagano, K.; Abe, Y.; et al. Amorphous nanosilica induce endocytosis-Dependent ROS generation and DNA damage in human keratinocytes. Toxicology 2011, 8, 1.
35. Bourdon, J.A.; Halappanavar, S.; Saber, A.T.; Jacobsen, N.R.; Williams, A.; Wallin, H.; Vogel, U.; Yauk, C.L. Hepatic and pulmonary toxicogenomic profiles in mice intratracheally instilled with carbon black nanoparticles reveal pulmonary inflammation, acute phase response, and alterations in lipid homeostasis. Toxicol. Sci. 2012, 127, 474-484.
36. Naya, M.; Kobayashi, N.; Ema, M.; Kasamoto, S.; Fukumuro, M.; Takami, S.; Nakajima, M.; Hayashi, M.; Nakanishi, J. In vivo genotoxicity study of titanium dioxide nanoparticles using Comet Assay following intratracheal instillation in rats. Regul. Toxicol. Pharmacol. 2012, 62, 1-6.
37. Ahamed, M.; Karns, M.; Goodson, M.; Rowe, J.; Hussain, S.M.; Schlager, J.J.; Hong, Y. DNA damage response to different surface chemistry of silver nanoparticles in mammalian cells. Toxicol. Appl. Pharmacol. 2008, 233, 404-410.
38. Foldbjerg, R.; Dang, D.A.; Autrup, H. Cytotoxicity and genotoxicity of silver nanoparticles in the human lung cancer cell line, A549. Arch. Toxicol. 2011, 85, 743-750.
39. Kim, H.R.; Kim, M.J.; Lee, S.Y.; Oh, S.M.; Chung, K.H. Genotoxic effects of silver nanoparticles stimulated by oxidative stress in human normal bronchial epithelial (BEAS-2B) cells. Mutat. Res. 2011, 726, 129-135.
40. Panda, K.K.; Achary, V.M.; Krishnaveni, R.; Pandhi, B.K.; Sarangi, S.N.; Sahu, S.N.; Panda, B.B. In vitro biosynthesis and genotoxicity bioassay of silver nanoparticles using plants. Toxicol. In Vitro 2011, 25, 1097-1105.
41. Li, Y.; Chen, D.H.; Yan, J.; Chen, Y.; Mittelststaedt, R.A.; Zhang, Y.; Biris, A.S.; Heflis, R.H.; Chen, T. Genotoxicity of silver nanoparticles evaluated using the Ames test and in vitro micronucleus assay. Mutat. Res. 2012, 745, 4-10.
42. Tavares, P.; Balbino, F.; martins de Oliveira, H.; Fugundes, G.E.; Vanancio, M.; Ronconi, J.V.V.; Merlini, A.; Streck, E.M.; Paula, M.M.S.; Andrade V.M. Evaluation of genotoxic effect of silver nanoparticles (Ag-NPs) in vitro and in vivo. J. Nanopart. Res. 2012, 14, 791.
43. Asare, N.; Instanes, C.; Sandberg, W.J.; Refsnes, M.; Schwarze, P.; Kruszewski, M.; Brunborg, G. Citotoxic and genotoxic effects of silver nanoparticles in testicular cell. Toxicology 2012, 291, 65-72.
44. Flower, N.A.L.; Brabu, B.; Revathy, M.; Gopalakrishnan, C.; Raja, S.V.K.; Murugan, S.S.; Kumaravel, T.S. Characterization of synthesized silver nanoparticles and assessment of its genotoxicity potentials using the alkaline comet assay. Mutat. Res. 2012, 742, 61-65.
45. Karlsson, H.; Gliga, A.R.; Kohonen, P.; Wallbergb, P.; Fadeel, B. Genotoxicity and epigenetic effects of silver nanoparticles. Toxicol. Lett. 2012, 211, S240.
46. Choi, S.Y.; Jeong, S.; Jang, S.H.; Park, J.; Ock, K.S.; Lee, S.Y.; Joo, S.-W. In vitro toxicity protein-adsorbed citrate-reduced gold nanoparticles in human lung adenocarcinoma cells. Toxicol. In Vitro 2012, 26, 229-237.
47. Li, J.J.; Lo, S.L.; Ng, C.T.; Gurung, R.L.; Hartono, D.; Hande, M.P.; Ong, C.N.; Bay, B.H.; Yung, L.Y. Genomic instability of gold nanoparticle treated human lung fibroblast cells. Biomaterials 2011, 32, 5515-5523.
48. Shulz, M.; Ma-Hock, L.; Brill, S.; Strauss, V.; Treumann, S.; Gröters, S.; Ravenzwaay, B.; Landsiedel, R. Investigation on the genotoxicity of different sizes of gold nanoparticles administered to the lungs of rats. Mutat. Res. 2012, 745, 51-57.
49. Singh, S.; D'Britto, V.; Prabhune, A.A.; Ramana, C.V.; Dhawan, A.; Prasad, B.L.V. Cytotoxic and genotoxic assessment of glycolipid-reduced and-capped gold and silver nanoparticles. New J. Chem. 2011, 34, 294-301.
50. Katsnelson, B.A.; Kuzmin, S. V; Degtyareva, T.D.; Privalova, L.I.; Soloboyeva, J.I. "Biological prophylaxis"-One of the ways to proceed from the analytical environmental epidemiology to the population health protection. Cent. Eur. J. Occup. Environ. Med. 2008, 14, 41-42.
51. Suttle, N.F. Control of hepatic copper retention in Texel ram lambs by dietary supplementation with copper antagonists followed by a copper depletion regimen. Anim. Food Sci. Techol. 2012, 11, 194-200.
52. Faddah, L.M.; Abdel Baky, N.A.; Al-Rasheed N.M.; Fatani A.U.; Atteya, M. Role of quercetin and arginine in ameliorating nano zinc oxide-induced nephrotoxicity in rats. BMC Complement. Altern. Med. 2012, 12, 60.
53. Ettinger, A. E.; Lamandid-Figueroa, H.; Tellez-Rojo, M.M. Effect of calcium supplementation on blood lead level in pregnancy: A randomized placebo-controlled trial. Environ. Health Perspect. 2009, 117, 26-31.
54. Privalova, L.I.; Katsnelson, B.A.; Osipenko, A.B.; Yushkov, B.H.; Babushkina, L.G. Response of a phagocyte cell system to products of macrophage breakdown as a probable mechanism of alveolar phagocytosis adaptation to deposition of particles of different cytotoxicity. Environ. Health Perspect. 1980, 35, 205-218.
55. Katsnelson, B.A.; Privalova, L.I. Recruitmant of pagocytizing cells into the respiratory tract as a response to the cytotoxic action of deposited particles. Environ. Health Perspect. 1984, 55, 313-325.
56. Privalova, L.I.; Katsnelson, B.A.; Yelnichnykh, L.N. Some peculiarities of the pulmonary phagocytotic response, dust kinetics, and silicosis development during long term exposure of rats to high quartz levels. Br. J. Ind. Med. 1987, 44, 228-235.
57. Privalova, L.I.; Katsnelson, B.A.; Sharapova, N.Y.; Kislitsina, N.S. On the relationship between activation and the breakdown of macrophages in pathogenesis of silicosis. Med. Lav. 1995, 86, 511-521.
58. Katsnelson, B.A.; Konysheva, L.K.; Privalova, L.Y.; Morosova, K.I. Development of a multicompartmental model of the kinetics of quartz dust in the pulmonary region of the lung during chronic inhalation exposure of rats. Br. J. Ind. Med. 1992, 49, 172-181.
59. Katsnelson, B.A.; Konyscheva, L.K.; Sharapova, N.; Privalova, L.I. Prediction of the comparative intensity of pneumoconiotic changes caused by chronic inhalation exposure to dusts of different cytotoxicity by means of a mathematical model. Occup. Environ. Med. 1994, 5, 173-180.
60. Katsnelson, B.A.; Konysheva, L.K.; Privalova, L.Y.; Sharapova, N.Y. Quartz dust retention in rat lungs under chronic exposure simulated by a multicompartmental model: Further evidence of the key role of the cytotoxicity of quartz particles. Inhalation Toxicol. 1997, 9, 703-715.
61. Sadauskas, E.; Wallin, H.; Stoltenberg, M.; Vogel, U.; Doering, P.; Larsen, A.; Danscher, G. Kupfer cells are central in the removal of nanoparticles from the organism. Part. Fibre Toxicol. 2007, 4, 10.
62. Lasagna-Reeves, C.; Gonzalez-Romero, D.; Barria, M.A.; Olmedo, I.; Clos, A.; Sadagopa Ramanujam, V.M.; Urayama, A.; Vergara, L.; Kogan, M.J.; Soto, C. Bioaccumulation and toxicity of gold nanoparticles after repeated administration in mice. Biochem. Biophys. Res. Commun. 2010, 393, 649-655.
63. Lau, C.; Outram, S.V.; Saldana, J.I.; Furmanski, A.L.; Dessens, J.T.; Cromton, T. Regulation of murine normal and stress-induced erythropoiesis by Desert Hedgehog. J. Blood 2012, 119, 4741-4751.
64. Li, N.; Xia, T.; Nel, A.E. The role of oxidative stress in ambient particulate matter-induced lung diseases and its implications in the toxicity of engineered nanoparticles. Free Radic. Biol. Med. 2008, 44, 1689-1699.
65. Privalova, L.I.; Katsnelson, B.A.; Sutunkova, M.P.; Valamina, I.E.; Beresneva, O.Y.; Degtyareva, T.D.; Yeremenko, O.S. Attenuation of some adverse health effects of chrysotile asbestos with a bioprotective complex in animal experiments. Cent. Eur. J. Occup. Environ. Med. 2007, 13, 265-276.
66. Katsnelson, B.A.; Makeev, O.H.; Kochneva, N.I.; Privalova, L.I.; Degtyareva, T.D.; Minin, V.V.; Bukhantsev, V.A.; Beresneva, O.Y.; Slyshkina, T.V.; Kostyukova, S.V.; Kulikov, E.S.; Dovzhenko, E.I. Testing a set of bioprotectors against the genotoxic effect of a combination of ecotoxicants. Cent. Eur. J. Occup. Environ. Med. 2007, 13, 251-264.
67. Katsnelson, B.A.; Yeremenko, O.S.; Privalova, L.I.; Makeyev, O.H.; Degtyareva, T.D.; Beresneva, O.Y.; Valamina, I.E.; Minihaliyeva, I.A.; Sutunkova, M.P.; Kireyeva, E.P.; et al. Toxicity of monazite particulate and its attenuation with a complex of bio-protectors. Med. Lav. 2009, 100, 455-470.
68. Gallyas, F. Chemical nature of the first products (nuclei) of the argyrophil stainig. A{cyrillic}s{cyrillic}ta Histochem. 1980, 67, 145-146.
69. Rylova, M.L. Methods of Investigating Long-Term Effects of Noxious Environmental Agents in Animal Experiments; Meditsina: Leningrad, Russia, 1964; p. 228.
70. Abeyemi, O.O.; Yemitan, O.K.; Taiwo, A.E. Neurosedative and muscle-relaxant activities of ethyl acetate extract of Baphianitida AFZEL. J. Ethnopharmacol. 2006, 106, 312-316.
71. Fernandez, S.P.; Wasowski, C.; Loscalzo, L.M.; Granger, R.E.; Johnston, G.A.R.; Paladini, A.C.; Marder, M. Central nervous system depressant action of flavonoid glycoside. Eur. J. Pharmacol. 2006, 539, 168-176.
72. Morozova, K.I.; Aronova, G.V.; Katsnelson, B.A.; Velichkovski, B.T.; Genkin, A.M.; Elnichnykh, L.N.; Privalova, L.I. On the defensive action of glutamate on the cytotoxicity and fibrogenicity of quartz dust. Br. J. Ind. Med. 1982, 39, 244-252.