Silver nanoparticles activate endoplasmic reticulum stress signaling pathway in cell and mouse models: The role in toxicity evaluation

Biomaterials

Volumn 61, Issue , 2015, Pages 307-315

  Huo, Lingling ^a,b   Chen, Rui ^b   Zhao, Lin ^b,c   Shi, Xiaofei ^b,c   Bai, Ru ^b   Long, Dingxin ^c   Chen, Feng ^c   Zhao, Yuliang ^b   Chang, Yan Zhong ^a   Chen, Chunying ^b  

^a HEBEI NORMAL UNIVERSITY   (China)

^b NATIONAL CENTER FOR NANOSCIENCE AND TECHNOLOGY   (China)

^c UNIVERSITY OF SOUTH CHINA   (China)

Author keywords

Apoptosis; Cytotoxicity; Intratracheal instillation; Signaling pathway; Silver

Indexed keywords

BIOLOGICAL ORGANS; CELL CULTURE; CELL DEATH; CYTOTOXICITY; HISTOLOGY; MAMMALS; METAL NANOPARTICLES; SIGNALING; SILVER; SILVER NANOPARTICLES; TISSUE; TOXICITY;

ANTI-MICROBIAL PROPERTIES; BIOLOGICAL IMPACTS; EFFECT CONCENTRATION; ENDOPLASMIC RETICULUM STRESS; INTRATRACHEAL INSTILLATION; SIGNALING PATHWAYS; SILVER NANOPARTICLES (AGNPS); UPREGULATED EXPRESSION;

CELL SIGNALING;

ASPARTATE AMMONIA LIGASE; BIOLOGICAL MARKER; CASPASE 12; CASPASE 3; GLUCOSE REGULATED PROTEIN 78; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; HEAT SHOCK PROTEIN 70; INITIATION FACTOR 2ALPHA; MESSENGER RNA; PROTEIN IRE1; SILVER NANOPARTICLE; X BOX BINDING PROTEIN 1; METAL NANOPARTICLE; REACTIVE OXYGEN METABOLITE; SILVER;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CELL VIABILITY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYTOTOXICITY; ENDOPLASMIC RETICULUM STRESS; GENE EXPRESSION PROFILING; HEPG2 CELL LINE; HUMAN; HUMAN CELL; HYDRODYNAMICS; IN VITRO STUDY; IN VIVO STUDY; KIDNEY; LIVER; LUNG; MALE; MOUSE; NANOTOXICOLOGY; NONHUMAN; PARTICLE SIZE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TUNEL ASSAY; UMBILICAL VEIN ENDOTHELIAL CELL; UNFOLDED PROTEIN RESPONSE; UPREGULATION; ZETA POTENTIAL; ANIMAL; CELL LINE; CELL SURVIVAL; DOSE RESPONSE; DRUG EFFECTS; ENDOPLASMIC RETICULUM; INSTITUTE FOR CANCER RESEARCH MOUSE; MATERIALS TESTING; METABOLISM; OXIDATIVE STRESS; PHYSIOLOGY;

MUS;

ANIMALS; CELL LINE; CELL SURVIVAL; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOPLASMIC RETICULUM; HEP G2 CELLS; HUMANS; MALE; MATERIALS TESTING; METAL NANOPARTICLES; MICE; MICE, INBRED ICR; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; SILVER;

EID: 84937557682     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2015.05.029     Document Type: Article

References (38)

1. Bidgoli S.A., Mahdavi M., Rezayat S.M., Korani M., Amani A., Ziarati P. Toxicity assessment of nanosilver wound dressing in Wistar rat. Acta Med. Iran 2013, 51:203-208.
2. Mitrano D.M., Rimmele E., Wichser A., Erni R., Height M., Nowack B. Presence of nanoparticles in wash water from conventional silver and nano-silver textiles. ACS Nano 2014, 8:7208-7219.
3. 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.
4. Jiang X., Miclaus T., Wang L., Foldbjerg R., Sutherland D.S., Autrup H., et al. Fast intracellular dissolution and persistent cellular uptake of silver nanoparticles in CHO-K1 cells: implication for cytotoxicity. Nanotoxicology 2015, 9(2):181-189.
5. Vandebriel R.J., Tonk E.C., de la Fonteyne-Blankestijn L.J., Gremmer E.R., Verharen H.W., van der Ven L.T., et al. Immunotoxicity of silver nanoparticles in an intravenous 28-day repeated-dose toxicity study in rats. Part Fibre Toxicol. 2014, 11:21.
6. Jiang X., Foldbjerg R., Miclaus T., Wang L., Singh R., Hayashi Y., et al. Multi-platform genotoxicity analysis of silver nanoparticles in the model cell line CHO-K1. Toxicol. Lett. 2013, 222:55-63.
7. Kim J.S., Kuk E., Yu K.N., Kim J.H., Park S.J., Lee H.J., et al. Antimicrobial effects of silver nanoparticles. Nanomed. Nanotechnol. Biol. Med. 2007, 3:95-101.
8. Ahamed M., Karns M., Goodson M., Rowe J., Hussain S.M., Schlager J.J., et al. DNA damage response to different surface chemistry of silver nanoparticles in mammalian cells. Toxicol. Appl. Pharmacol. 2008, 233:404-410.
9. 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.
10. de Lima R., Seabra A.B., Duran N. Silver nanoparticles: a brief review of cytotoxicity and genotoxicity of chemically and biogenically synthesized nanoparticles. J. Appl. Toxicol. 2012, 32:867-879.
11. Jena P., Mohanty S., Mallick R., Jacob B., Sonawane A. Toxicity and antibacterial assessment of chitosan-coated silver nanoparticles on human pathogens and macrophage cells. Int. J. Nanomed. 2012, 7:1805-1818.
12. Panda K.K., Achary V.M., Krishnaveni R., Padhi B.K., Sarangi S.N., Sahu S.N., et al. In vitro biosynthesis and genotoxicity bioassay of silver nanoparticles using plants. Toxicol. In Vitro 2011, 25:1097-1105.
13. Chen R., Huo L., Shi X., Bai R., Zhang Z., Zhao Y., et al. Endoplasmic reticulum stress induced by zinc oxide nanoparticles is an earlier biomarker for nanotoxicological evaluation. ACS Nano 2014, 8:2562-2574.
14. van Schadewijk A., van't Wout E.F., Stolk J., Hiemstra P.S. A quantitative method for detection of spliced X-box binding protein-1 (XBP1) mRNA as a measure of endoplasmic reticulum (ER) stress. Cell Stress Chaperones 2012, 17:275-279.
15. Zhang R., Piao M.J., Kim K.C., Kim A.D., Choi J.Y., Choi J., et al. Endoplasmic reticulum stress signaling is involved in silver nanoparticles-induced apoptosis. Int. J. Biochem. Cell Biol. 2012, 44:224-232.
16. Christen V., Capelle M., Fent K. Silver nanoparticles induce endoplasmatic reticulum stress response in zebrafish. Toxicol. Appl. Pharmacol. 2013, 272:519-528.
17. Srivastava M., Singh S., Self W.T. Exposure to silver nanoparticles inhibits selenoprotein synthesis and the activity of thioredoxin reductase. Environ. Health Persp. 2012, 120:56-61.
18. Bai R., Zhang L., Liu Y., Meng L., Wang L., Wu Y., et al. Pulmonary responses to printer toner particles in mice after intratracheal instillation. Toxicol. Lett. 2010, 199:288-300.
19. Hengartner M.O. The biochemistry of apoptosis. Nature 2000, 407:770-776.
20. Klein C.L., Comero S., Stahlmecke B., Romazanov J., Kuhlbusch T.A.J., Doren E.V., et al. NM-series of Representative Manufactured Nanomaterials NM-300 Silver Characterisation, Stability, Homogeneity 2011, 1-86. JRC Scientific and Technical Reports. Italy.
21. Hinderliter P.M., Minard K.R., Orr G., Chrisler W.B., Thrall B.D., Pounds J.G., et al. ISDD: A computational model of particle sedimentation, diffusion and target cell dosimetry for in vitro toxicity studies. Part Fibre Toxicol. 2010, 7:36.
22. de Virgilio M., Kitzmuller C., Schwaiger E., Klein M., Kreibich G., Ivessa N.E. Degradation of a short-lived glycoprotein from the lumen of the endoplasmic reticulum: the role of N-linked glycans and the unfolded protein response. Mol. Biol. Cell 1999, 10:4059-4073.
23. Nakagawa T., Zhu H., Morishima N., Li E., Xu J., Yankner B.A., et al. Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta. Nature 2000, 403:98-103.
24. Budihardjo I., Oliver H., Lutter M., Luo X., Wang X. Biochemical pathways of caspase activation during apoptosis. Ann. Rev. Cell Dev. Biol. 1999, 15:269-290.
25. dos Santos C.A., Seckler M.M., Ingle A.P., Gupta I., Galdiero S., Galdiero M., et al. Silver nanoparticles: therapeutical uses, toxicity, and safety issues. J. Pharm. Sci. 2014, 103:1931-1944.
26. Ivask A., Juganson K., Bondarenko O., Mortimer M., Aruoja V., Kasemets K., et al. Mechanisms of toxic action of Ag, ZnO and CuO nanoparticles to selected ecotoxicological test organisms and mammalian cells in vitro: a comparative review. Nanotoxicology 2014, 8:57-71.
27. De Matteis V., Malvindi M.A., Galeone A., Brunetti V., De Luca E., Kote S., et al. Negligible particle-specific toxicity mechanism of silver nanoparticles: the role of Ag+ ion release in the cytosol. Nanomed. Nanotechnol. Biol. Med. 2015, 11:731-739.
28. Berger B.J., Muller T.S., Buschmann I.R., Peters K., Kirsch M., Christ B., et al. High levels of the molecular chaperone Mdg1/ERdj4 reflect the activation state of endothelial cells. Exp. Cell Res. 2003, 290:82-92.
29. 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, 179:130-139.
30. Kamata H., Honda S., Maeda S., Chang L., Hirata H., Karin M. Reactive oxygen species promote TNFalpha-induced death and sustained JNK activation by inhibiting MAP kinase phosphatases. Cell 2005, 120:649-661.
31. Lao F., Chen L., Li W., Ge C., Qu Y., Sun Q., et al. Fullerene nanoparticles selectively enter oxidation-damaged cerebral microvessel endothelial cells and inhibit JNK-related apoptosis. ACS Nano 2009, 3:3358-3368.
32. Andersen M.E., Dennison J.E., Thomas R.S., Conolly R.B. New directions in incidence-dose modeling. Trends Biotech. 2005, 23:122-127.
33. Huk A., Izak-Nau E., Reidy B., Boyles M., Duschl A., Lynch I., et al. Is the toxic potential of nanosilver dependent on its size?. Part Fibre Toxicol. 2014, 11:65.
34. Kaewamatawong T., Banlunara W., Maneewattanapinyo P., Thammachareon C., Ekgasit S. Acute and subacute pulmonary toxicity caused by a single intratracheal instillation of colloidal silver nanoparticles in mice: pathobiological changes and metallothionein responses. J. Environ. Pathol. Toxicol. Oncol 2014, 33:59-68.
35. Park E.J., Choi K., Park K. Induction of inflammatory responses and gene expression by intratracheal instillation of silver nanoparticles in mice. Arch. Pharm. Res. 2011, 34:299-307.
36. Jun E.A., Lim K.M., Kim K., Bae O.N., Noh J.Y., Chung K.H., et al. Silver nanoparticles enhance thrombus formation through increased platelet aggregation and procoagulant activity. Nanotoxicology 2011, 5:157-167.
37. Katsnelson B.A., Privalova L.I., Gurvich V.B., Makeyev O.H., Shur V.Y., Beikin Y.B., et al. 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. Intern. J. Mol. Sci. 2013, 14:2449-2483.
38. 2 nanoparticle inhalation: nanotoxicity has susceptible population. Environ. Sci. Technol. 2008, 42:8985-8992.