Silver nanoparticles induced neurotoxicity through oxidative stress in rat cerebral astrocytes is distinct from the effects of silver ions

NeuroToxicology

Volumn 52, Issue , 2016, Pages 210-221

  Sun, Cheng ^a   Yin, Nuoya ^a   Wen, Ruoxi ^a,b   Liu, Wei ^a,c   Jia, Yanxia ^d   Hu, Ligang ^a   Zhou, Qunfang ^a   Jiang, Guibin ^a  

^a INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^b UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^c CHINESE ACADEMY OF INSPECTION AND QUARANTINE   (China)

^d INSTITUTE OF BIOPHYSICS   (China)

Author keywords

Astrocyte; Neurotoxicity; Particle effect; Silver ion release; Silver nanoparticle

Indexed keywords

CASPASE; CATION; REACTIVE OXYGEN METABOLITE; SILVER ION; SILVER NANOPARTICLE; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG; CYTOKINE; METAL NANOPARTICLE; SILVER;

ANIMAL CELL; APOPTOSIS; ARTICLE; ASTROCYTE; BRAIN CORTEX; CELL STIMULATION; COMPARATIVE STUDY; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOTOXICITY; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; INTERNALIZATION; NERVE CELL MEMBRANE; NERVE CELL NECROSIS; NERVOUS SYSTEM INFLAMMATION; NEUROTOXICITY; NEWBORN; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; RESAZURIN ASSAY; ANIMAL; CELL SURVIVAL; CHEMICALLY INDUCED; CYTOLOGY; DOSE RESPONSE; DRUG EFFECTS; METABOLISM; NECROSIS; PARTICLE SIZE; PATHOLOGY; PHOSPHORYLATION; PRIMARY CELL CULTURE;

ANIMALS; APOPTOSIS; ASTROCYTES; CELL SURVIVAL; CEREBRAL CORTEX; CYTOKINES; DOSE-RESPONSE RELATIONSHIP, DRUG; JNK MITOGEN-ACTIVATED PROTEIN KINASES; METAL NANOPARTICLES; NECROSIS; OXIDATIVE STRESS; PARTICLE SIZE; PHOSPHORYLATION; PRIMARY CELL CULTURE; RATS; REACTIVE OXYGEN SPECIES; SILVER;

EID: 84952664835     PISSN: 0161813X     EISSN: 18729711     Source Type: Journal    
DOI: 10.1016/j.neuro.2015.09.007     Document Type: Article

References (52)

1. AshaRani P.V., Low Kah Mun G., Hande M.P., Valiyaveettil S. Cytotoxicity and genotoxicity of silver nanoparticles in human cells. ACS Nano 2009, 3:279-290. http://dx.doi.org/10.1021/nn800596w.
2. Baharara J., Namvar F., Ramezani T., Mousavi M., Mohamad R. Silver nanoparticles biosynthesized using Achillea biebersteinii flower extract: apoptosis induction in MCF-7 cells via caspase activation and regulation of Bax and Bcl-2 gene expression. Molecules 2015, 20:2693-2706. http://dx.doi.org/10.3390/molecules20022693.
3. Bilberg K., Hovgaard M.B., Besenbacher F., Baatrup E. In vivo toxicity of silver nanoparticles and silver ions in zebrafish (Danio rerio). J. Toxicol. 2012, 293784:1-9. http://dx.doi.org/10.1155/2012/293784.
4. Bone A.J., Matson C.W., Colman B.P., Yang X., Meyer J.N., Di Giulio R.T. Silver nanoparticle toxicity to Atlantic killifish (Fundulus Heteroclitus) and Caenorhabditis elegans: a comparison of mesocosm, microcosm and conventional laboratory studies. Environ. Toxicol. Chem. 2015, 34:275-282.
5. Braat H., Rottiers P., Hommes D.W., Huyghebaert N., Remaut E., Remon J.P., van Deventer S.J., Neirynck S., Peppelenbosch M.P., Steidler L. A phase I trial with transgenic bacteria expressing interleukin-10 in Crohn's disease. Clin. Gastroenterol. Hepatol. 2006, 4:754-759. http://dx.doi.org/10.1016/j.cgh.2006.03.028.
6. Castranova V. Overview of current toxicological knowledge of engineered nanoparticles. J. Occup. Environ. Med. 2011, 53:S14-S17. http://dx.doi.org/10.1097/JOM.0b013e31821b1e5a.
7. Chae Y.J., Pham C.H., Lee J., Bae E., Yi J., Gu M.B. Evaluation of the toxic impact of silver nanoparticles on Japanese medaka (Oryzias latipes). Aqua Toxicol. 2009, 94:320-327. http://dx.doi.org/10.1016/j.aquatox.2009.07.019.
8. Chan F.K., Moriwaki K., De Rosa M.J. Detection of necrosis by release of lactate dehydrogenase (LDH) activity. Methods Mol. Biol. 2013, 979:65-70. http://dx.doi.org/10.1007/978-1-62703-290-2_7.
9. Chen X., Schluesener H.J. Nanosilver: a nanoproduct in medical application. Toxicol. Lett. 2008, 176:1-12. http://dx.doi.org/10.1016/j.toxlet.2007.10.004.
10. Chen Y., Swanson R.A. Astrocytes and brain injury. J. Cerebr. Blood F Met. 2003, 23:137-149. http://dx.doi.org 10.1097/01.WCB.0000044631.80210.3C.
11. Choi O., Hu Z. Size dependent and reactive oxygen species related nanosilver toxicity to nitrifying bacteria. Environ. Sci. Technol. 2008, 42:4583-4588. http://dx.doi.org/10.1021/es703238h.
12. Cortese-Krott M.M., Münchow M., Pirev E., Hessner F., Bozkurt A., Uciechowski P., Pallua N., Kröncke K.D., Suschek C.V. Silver ions induce oxidative stress and intracellular zinc release in human skin fibroblasts. Free Radic. Biol. Med. 2009, 47:1570-1577. http://dx.doi.org/10.1016/j.freeradbiomed.2009.08.023.
13. Danny N., Dhanasekaran E., Premkumar R. JNK signaling in apoptosis. Oncogene 2008, 27:6245-6251. http://dx.doi.org/10.1038/onc.2008.301.
14. Dufour J.H., Dziejman M., Liu M.T., Leung J.H., Lane T.E., Luster A.D. IFN-gamma-inducible protein 10 (IP-10; CXCL10)-deficient mice reveal a role for IP-10 in effector T cell generation and trafficking. J. Immunol. 2002, 168:3195-3204. http://dx.doi.org/10.4049/jimmunol.168.7.3195.
15. EPA State of the Science Literature Review 2010, Everything Nanosilver and More, US, Available from: http://www.epa.gov.
16. García-Alonso J., Khan F.R., Misra S.K., Turmaine M., Smith B.D., Rainbow P.S., Luoma S.N., Valsami-Jones E. Cellular internalization of silver nanoparticles in gut epithelia of the estuarine polychaete nereis diversicolor. Environ. Sci. Technol. 2011, 45:4630-4636. http://dx.doi.org/10.1021/es2005122.
17. Haase A., Rott S., Mantion A., Graf P., Plendl J., Thünemann A.F., Meier W.P., Taubert A., Luch A., Reiser G. Effects of silver nanoparticles on primary mixed neural cell cultures: uptake, oxidative stress and acute calcium responses. Toxicol. Sci. 2012, 126:457-468. http://dx.doi.org/10.1093/toxsci/kfs003.
18. Havelaar A.C., de Gast I.L., Snijders S., Beerens C.E.M.T., Mancini G.M.S., Verheijen F.W. Characterization of a heavy metal ion transporter in the lysosomal membrane. FEBS Lett. 1998, 436:223-227. http://dx.doi.org/10.1016/S0014-5793(98) 01133-8.
19. Herzog F., Clift M.J., Piccapietra F., Behra R., Schmid O., Petri-Fink A., Rothen-Rutishauser B. Exposure of silver-nanopartilces and silver-ions to lung cells in vitro at the air-liquid interface. Part Fibre Toxicol. 2013, 10:1-14. http://dx.doi.org/10.1186/1743-8977-10-11.
20. Hohnholt M.C., Geppert M., Luther E.M., Petters C., Bulcke F., Dringen R. Handling of iron oxide and silver nanoparticles by astrocytes. Neurochem. Res. 2013, 38:227-239. http://dx.doi.org/10.1007/s11064-012-0930-y.
21. Huang C.L., Hsiao I.L., Lin H.C., Wang C.F., Huang Y.J., Chuang C.Y. Silver nanoparticles affect on gene expression of inflammatory and neurodegenerative responses in mouse brain neural cells. Environ. Res. 2015, 136:253-263. http://dx.doi.org/10.1016/j.envres.2014.11.006.
22. Jayakumar A.R., Panickar K.S., Murthy ChR, Norenberg M.D. Oxidative stress and mitogen-activated protein kinase phosphorylation mediate ammonia-induced cell swelling and glutamate uptake inhibition in cultured astrocytes. J. Neurosci. 2006, 26:4774-4784. http://dx.doi.org/10.1523/JNEUROSCI.0120-06.2006.
23. Jones B.A., Beamer M., Ahmed S. Fractalkine/CX3CL1: a potential new target for inflammatory diseases. Mol. Interv. 2010, 10:263-270. http://dx.doi.org/10.1124/mi.10.5.3.
24. Kanna K., Jain S.K. Oxidative stress and apoptosis. Pathophysiology 2000, 7:153-163. http://dx.doi.org/10.1016/S0928-4680(00)00053-5.
25. Kathryn A.W., Robert W., Donnell O. Primary culture of rat cerebral astrocytes. Biol. Honor Thesis 2010, 1-20. http://josm.geneseo.edu/theses/Weiss-02.pdf.
26. Kawata K., Osawa M., Okabe S. In vitro toxicity of silver nanoparticles at noncytotoxic doses to HepG2 human hepatoma cells. Environ. Sci. Technol. 2009, 43:6046-6051. http://dx.doi.org/10.1021/es900754q.
27. Kohn L.A., Hao Q.L., Sasidharan R., Parekh C., Ge S., Zhu Y., Mikkola H.K., Crooks G.M. Lymphoid priming in human bone marrow begins before expression of CD10 with upregulation of l-selectin. Nat. Immunol. 2012, 13:963-971. http://dx.doi.org/10.1038/ni.2405.
28. Liu J., Lin A. Role of JNK activation in apoptosis: a double-edged sword. Cell Res. 2005, 15:36-42. http://dx.doi.org/10.1038/sj.cr.7290262.
29. Liu J., Sonshine D.A., Shervani S., Hurt R.H. Controlled release of biologically active silver from nanosilver surfaces. ACS Nano 2010, 4:6903-6913. http://dx.doi.org/10.1021/nn102272n.
30. Luther E.M., Koehler Y., Diendorf J., Epple M., Dringen R. Accumulation of silver nanoparticles by cultured primary brain astrocytes. Nanotechnology 2011, 22:1-11. http://dx.doi.org/10.1088/0957-4484/22/37/375101.
31. Luther E.M., Schmidt M.M., Diendorf J., Epple M., Dringen R. Upregulation of metallothioneins after exposure of cultured primary astrocytes to silver nanoparticles. Neurochem. Res. 2012, 37:1639-1648. http://dx.doi.org/10.1007/s11064-012-0767-4.
32. Mayer C.L., Huber B.R., Peskind E. Traumatic brain injury, neuroinflammation, and post-traumatic headaches. Headache 2013, 53:1523-1530. http://dx.doi.org/10.1111/head.12173.
33. McIlwain D.R., Berger T., Mak T.W. Caspase functions in cell death and disease. Cold Spring Harb. Perspect. Biol. 2013, 5:1-28. http://dx.doi.org/10.1101/cshperspect.a00865.
34. McShan D., Ray P.C., Yu H. Molecular toxicity mechanism of nanosilver. J. Food Drug Anal. 2014, 22:116-127. http://dx.doi.org/10.1016/j.jfda.2014.01.010.
35. Mytilineou C., Kramer B.C., Yabut J.A. Glutathione depletion and oxidative stress. Parkinsonism Relat. Disord. 2002, 8:385-387. http://dx.doi.org/10.1016/S1353-8020(02)00018-4.
36. Nakagawa H., Komorita N., Shibata F., Ikesue A., Konishi K., Fujioka M., Kato H. Identification of cytokine-induced neutrophil chemoattractants (CINC), rat GRO/CINC-2 alpha and CINC-2 beta, produced by granulation tissue in culture: purification, complete amino acid sequences and characterization. Biochem. J. 1994, 301:545-550. http://www.biochemj.org/bj/301/0545/3010545.pdf.
37. Nate S. Nanosilver: weighing the risks and benefits. Environ. Health Persp. 2013, 121. a220-5. http://dx.doi.org/10.1289/ehp.121-a220.
38. Rinna A., Magdolenova Z., Hudecova A., Kruszewski M., Refsnes M., Dusinska M. Effect of silver nanoparticles on mitogen-activated protein kinases activation: role of reactive oxygen species and implication in DNA damage. Mutagenesis 2015, 30:59-66. http://dx.doi.org/10.1093/mutage/geu057.
39. Sambale F., Wagner S., Stahl F., Khaydarov R.R., Scheper T., Bahnemann D. Investigations of the toxic effect of silver nanoparticles on mammalian cell lines. J. Nanomater. 2015, 136765:1-9. http://dx.doi.org/10.1155/2015/136765.
40. Sharma H.S., Ali S.F., Hussain S.M., Schlager J.J., Sharma A. Influence of engineered nanoparticles from metals on the blood-brain barrier permeability, cerebral blood flow, brain edema and neurotoxicity. An experimental study in the rat and mice using biochemical and morphological approaches. J. Nanosci. Nanotechnol. 2009, 9:5055-5072. http://dx.doi.org/10.1166/jnn.2009.GR09.
41. Siddiqi N., Abdelhalim M.A.K., El-Ansary A.K., Alhomida A.S., Ong W.Y. Identification of potential biomarkers of gold nanoparticle toxicity in rat brains. J. Neuroinflamm. 2012, 9:123-129. http://dx.doi.org/10.1186/1742-2094-9-123.
42. Solioz M., Odermatt A. Copper and silver transport by CopB-ATPase in membrane vesicles of Enterococcus hirae. J. Biol. Chem. 1995, 270:9217-9221. http://dx.doi.org/10.1074/jbc.270.16.9217.
43. Szydlowska K., Gozdz A., Dabrowski M., Zawadzka M., Kaminska B. Prolonged activation of ERK triggers glutamate-induced apoptosis of astrocytes: neuroprotective effect of FK506. J. Neurochem. 2010, 113:904-918. http://dx.doi.org/10.1111/j.1471-4159.2010.06656.x.
44. Tang J., Xiong L., Wang S., Wang J., Liu L., Li J., Yuan F., Xi T. Distribution, translocation and accumulation of silver nanoparticles in rats. J. Nanosci. Nanotechnol. 2009, 9:4924-4932. http://dx.doi.org/10.1166/jnn.2009.1269.
45. 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., Hussain S.M., Ali S.F. Silver nanoparticle induced blood-brain barrier inflammation and increased permeability in primary rat brain microvessel endothelial cells. Toxicol. Sci. 2010, 118:160-170. http://dx.doi.org/10.1093/toxsci/kfq244.
46. Vrček I.V., Zuntar I., Petlevski R., Pavičić I., Dutour Sikirić M., Curlin M., Goessler W. Comparison of in vitro toxicity of silver ions and silver nanoparticles on human hepatoma cells. Environ. Toxicol. 2014, 22081:1-14. http://dx.doi.org/10.1002/tox.22081.
47. Wilson center. Project on Emerging Nanotechnologies 2014, Consumer Products Inventory, Washington, DC, Available from: http://www.nanotechproject.org/cpi.
48. Win-Shwe T.T., Fujimaki H. Nanoparticles and neurotoxicity. Int. J. Mol. Sci. 2011, 12:6267-6280. http://dx.doi.org/10.3390/ijms12096267.
49. Wright P.C., Qin H., Choi M.M., Chiu N.H., Jia Z. Carbon nanodots interference with lactate dehydrogenase assay in human monocyte THP-1 cells. SpringerPlus 2014, 3:615-619. http://dx.doi.org/10.1186/2193-1801-3-615.
50. Xiu Z.M., Zhang Q.B., Puppala H.L., Colvin V.L., Alvarez P.J. Negligible particle-specific antibacterial activity of silver nanoparticles. Nano Lett. 2012, 12:4271-4275. http://dx.doi.org/10.1021/nl301934w.
51. Yin N., Liu Q., Liu J., He B., Cui L., Li Z., Yun Z., Qu G., Liu S., Zhou Q., Jiang G. Silver nanoparticle exposure attenuates the viability of rat cerebellum granule cells through apoptosis coupled to oxidative stress. Small 2013, 9:1831-1841. http://dx.doi.org/10.1002/smll.201202732.
52. Ziemińska E., Stafiej A., Struzyńska L. The role of the glutamatergic NMDA receptor in nanosilver-evoked neurotoxicity in primary cultures of cerebella granule cells. Toxicology 2014, 315:38-48. http://dx.doi.org/10.1016/j.tox.2013.11.008.