Investigating the immunomodulatory nature of zinc oxide nanoparticles at sub-cytotoxic levels in vitro and after intranasal instillation in vivo

Journal of Nanobiotechnology

Volumn 13, Issue 1, 2015, Pages

  Saptarshi, Shruti R ^a   Feltis, Bryce N ^b,c   Wright, Paul F A ^b   Lopata, Andreas L ^a  

^a JAMES COOK UNIVERSITY   (Australia)

^b RMIT UNIVERSITY   (Australia)

^c MONASH UNIVERSITY   (Australia)

Author keywords

A549 cells; Heme oxygenase 1; IL 8; Intranasal instillation; Reactive oxygen species

Indexed keywords

AMINO ACIDS; ANTIOXIDANTS; BIOLOGICAL ORGANS; CELLS; CYTOLOGY; CYTOTOXICITY; MACHINERY; MOBILE SECURITY; NANOPARTICLES; OXYGEN; PORPHYRINS; TOXICITY; ZINC;

A549 CELLS; HEME OXYGENASE-1; IL-8; INTRANASAL; REACTIVE OXYGEN SPECIES;

ZINC OXIDE;

EOTAXIN; GAMMA INTERFERON INDUCIBLE PROTEIN 10; HEME OXYGENASE 1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 8; LACTATE DEHYDROGENASE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE P38; MONOCYTE CHEMOTACTIC PROTEIN 1; RANTES; REACTIVE OXYGEN METABOLITE; SYNAPTOTAGMIN I; TUMOR NECROSIS FACTOR ALPHA; ZINC OXIDE NANOPARTICLE; ACETYLCYSTEINE; HMOX1 PROTEIN, HUMAN; IMMUNOLOGIC FACTOR; METAL NANOPARTICLE; ZINC OXIDE;

A549 CELL LINE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DEATH; CELL VIABILITY; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOTOXICITY; FEMALE; HUMAN; HUMAN CELL; IMMUNOMODULATION; IN VITRO STUDY; IN VIVO STUDY; LUNG TOXICITY; MOUSE; NANOTOXICOLOGY; NONHUMAN; PARTICLE SIZE; PNEUMONIA; PROTEIN PHOSPHORYLATION; REDOX STRESS; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; BAGG ALBINO MOUSE; CELL LINE; DOSE RESPONSE; DRUG EFFECTS; EPITHELIUM CELL; GENETICS; IMMUNOLOGY; INFLAMMATION; INTRANASAL DRUG ADMINISTRATION; METABOLISM; PROCEDURES; TOXICITY TESTING;

MURINAE; MUS;

ACETYLCYSTEINE; ADMINISTRATION, INTRANASAL; ANIMALS; CELL LINE; DOSE-RESPONSE RELATIONSHIP, DRUG; EPITHELIAL CELLS; FEMALE; HEME OXYGENASE-1; HUMANS; IMMUNOLOGIC FACTORS; INFLAMMATION; INTERLEUKIN-8; MAP KINASE SIGNALING SYSTEM; METAL NANOPARTICLES; MICE, INBRED BALB C; NF-KAPPA B; TOXICITY TESTS; ZINC OXIDE;

EID: 84924428407     PISSN: None     EISSN: 14773155     Source Type: Journal    
DOI: 10.1186/s12951-015-0067-7     Document Type: Article

References (50)

1. Wang ZL. Zinc oxide nanostructures: growth, properties and applications. J Phys Condens Matter. 2004;16:R829-58.
2. Saptarshi S, Duschl A, Lopata A. Interaction of nanoparticles with proteins: relation to bio-reactivity of the nanoparticle. J Nanobiotechnol. 2013;11:26.
3. Wu W, Samet JM, Peden DB, Bromberg PA. Phosphorylation of p65 is required for zinc oxide nanoparticle-induced interleukin 8 expression in human bronchial epithelial cells. Environ Health Perspect. 2010;118:982-7.
4. Karlsson HL, Cronholm P, Gustafsson J, Möller L. Copper oxide nanoparticles are highly toxic: a comparison between metal oxide nanoparticles and carbon nanotubes. Chem Res Toxicol. 2008;21:1726-32.
5. Lin W, Xu Y, Huang C-C, Ma Y, Shannon K, Chen D-R, et al. Toxicity of nano- and micro-sized ZnO particles in human lung epithelial cells. J Nanoparticle Res. 2009;11:25-39.
6. Feltis BN, O'Keefe SJ, Harford AJ, Piva TJ, Turney TW, Wright PFA. Independent cytotoxic and inflammatory responses to zinc oxide nanoparticles in human monocytes and macrophages. Nanotoxicology. 2012;6:757-65.
7. Kang TS, Guan RF, Chen XQ, Song YJ, Jiang H, Zhao J. In vitro toxicity of different-sized ZnO nanoparticles in Caco-2 cells. Nanoscale Res Lett. 2013;8:496.
8. Prach M, Stone V, Proudfoot L. Zinc oxide nanoparticles and monocytes: Impact of size, charge and solubility on activation status. Toxicol Appl Pharmacol. 2013;266:19-26.
9. Ahamed M, Akhtar MJ, Raja M, Ahmad I, Siddiqui MKJ, AlSalhi MS, et al. ZnO nanorod-induced apoptosis in human alveolar adenocarcinoma cells via p53, survivin and bax/bcl-2 pathways: role of oxidative stress. Nanomedicine. 2011;7:904-13.
10. Akhtar MJ, Ahamed M, Kumar S, Khan MAM, Ahmad J, Alrokayan SA. Zinc oxide nanoparticles selectively induce apoptosis in human cancer cells through reactive oxygen species. Int J Nanomedicine. 2012;7:845-57.
11. Andersson-Willman B, Gehrmann U, Cansu Z, Buerki-Thurnherr T, Krug HF, Gabrielsson S, et al. Effects of subtoxic concentrations of TiO2 and ZnO nanoparticles on human lymphocytes, dendritic cells and exosome production. Toxicol Appl Pharmacol. 2012;264:94-103.
12. Guo D, Bi H, Liu B, Wu Q, Wang D, Cui Y. Reactive oxygen species-induced cytotoxic effects of zinc oxide nanoparticles in rat retinal ganglion cells. Toxicol In Vitro. 2013;27:731-8.
13. Yang H, Liu C, Yang D, Zhang H, Xi Z. Comparative study of cytotoxicity, oxidative stress and genotoxicity induced by four typical nanomaterials: the role of particle size, shape and composition. J Appl Toxicol. 2009;29:69-78.
14. Hackenberg S, Zimmermann F-Z, Scherzed A, Friehs G, Froelich K, Ginzkey C, et al. Repetitive exposure to zinc oxide nanoparticles induces dna damage in human nasal mucosa mini organ cultures. Environ Mol Mutagen. 2011;52:582-9.
15. Wilhelmi V, Fischer U, Weighardt H, Schulze-Osthoff K, Nickel C, Stahlmecke B, et al. Zinc oxide nanoparticles induce necrosis and apoptosis in macrophages in a p47phox- and Nrf2-independent manner. PLoS ONE. 2013;8:e65704.
16. Xia T, Kovochich M, Liong M, Mädler L, Gilbert B, Shi H, et al. Comparison of the mechanism of toxicity of zinc oxide and cerium oxide nanoparticles based on dissolution and oxidative stress properties. ACS Nano. 2008;2:2121-34.
17. Buerki-Thurnherr T, Xiao L, Diener L, Arslan O, Hirsch C, Maeder-Althaus X, et al. In vitro mechanistic study towards a better understanding of ZnO nanoparticle toxicity. Nanotoxicology. 2013;7:402-16.
18. Song W, Zhang J, Guo J, Zhang J, Ding F, Li L, et al. Role of the dissolved zinc ion and reactive oxygen species in cytotoxicity of ZnO nanoparticles. Toxicol Lett. 2010;199:389-97.
19. Kim YH, Fazlollahi F, Kennedy IM, Yacobi NR, Hamm-Alvarez SF, Borok Z, et al. Alveolar epithelial cell injury due to zinc oxide nanoparticle exposure. Am J Respir Crit Care Med. 2010;182:1398-409.
20. Turney TW, Duriska MB, Jayaratne V, Elbaz A, O'Keefe SJ, Hastings AS, et al. Formation of zinc-containing nanoparticles from Zn2+ Ions in cell culture media: implications for the nanotoxicology of ZnO. Chem Res Toxicol. 2012;25:2057-66.
21. Luo M, Shen C, Feltis BN, Martin LL, Hughes AE, Wright PFA, et al. Reducing ZnO nanoparticle cytotoxicity by surface modification. Nanoscale. 2014;6:5791-8.
22. Shen C, James SA, de Jonge MD, Turney TW, Wright PFA, Feltis BN. Relating cytotoxicity, zinc ions, and reactive oxygen in ZnO nanoparticle-exposed human immune cells. Toxicol Sci. 2013;136:120-30.
23. Cho WS, Duffin R, Howie SEM, Scotton CJ, Wallace WAH, MacNee W, et al. Progressive severe lung injury by zinc oxide nanoparticles; the role of Zn2+ dissolution inside lysosomes. Particle Fibre Toxicol. 2011;8:1-16.
24. Huang C-C, Aronstam RS, Chen D-R, Huang Y-W. Oxidative stress, calcium homeostasis, and altered gene expression in human lung epithelial cells exposed to ZnO nanoparticles. Toxicol In Vitro. 2010;24:45-55.
25. Yu K-N, Yoon T-J, Minai-Tehrani A, Kim J-E, Park SJ, Jeong MS, et al. Zinc oxide nanoparticle induced autophagic cell death and mitochondrial damage via reactive oxygen species generation. Toxicol In Vitro. 2013;27:1187-95.
26. Shrivastava R, Raza S, Yadav A, Kushwaha P, Flora SJS. Effects of sub-acute exposure to TiO2, ZnO and Al2O3 nanoparticles on oxidative stress and histological changes in mouse liver and brain. Drug Chem Toxicol. 2014;37:336-47.
27. Gojova A, Guo B, Kota RS, Rutledge JC, Kennedy IM, Barakat AI. Induction of inflammation in vascular endothelial cells by metal oxide nanoparticles: Effect of particle composition. Environ Health Perspect. 2007;115:403-9.
28. Prasad A. Zinc and immunity. Mol Cell Biochem. 1998;188:63-9.
29. Fraker PJ, King LE, Laakko T, Vollmer TL. The dynamic link between the integrity of the immune system and zinc status. J Nutr. 2000;130:1399S-406.
30. Cho W-S, Duffin R, Poland CA, Duschl A, Oostingh GJ, MacNee W, et al. Differential pro-inflammatory effects of metal oxide nanoparticles and their soluble ions in vitro and in vivo; zinc and copper nanoparticles, but not their ions, recruit eosinophils to the lungs. Nanotoxicology. 2012;6:22-35.
31. Chuang H-C, Juan H-T, Chang C-N, Yan Y-H, Yuan T-H, Wang J-S, et al. Cardiopulmonary toxicity of pulmonary exposure to occupationally relevant zinc oxide nanoparticles. Nanotoxicology. 2014;8:593-604.
32. Fukui H, Horie M, Endoh S, Kato H, Fujita K, Nishio K, et al. Association of zinc ion release and oxidative stress induced by intratracheal instillation of ZnO nanoparticles to rat lung. Chem Biol Interact. 2012;198:29-37.
33. Kao Y-Y, Chen Y-C, Cheng T-J, Chiung Y-M, Liu P-S. Zinc oxide nanoparticles interfere with zinc Ion homeostasis to cause cytotoxicity. Toxicol Sci. 2012;125:462-72.
34. Kao Y-Y, Cheng T-J, Yang D-M, Wang C-T, Chiung Y-M, Liu P-S. Demonstration of an olfactory bulb-brain translocation pathway for ZnO nanoparticles in rodent cells in vitro and in vivo. J Mol Neurosci. 2012;48:464-71.
35. Gao L, Yang S-T, Li S, Meng Y, Wang H, Lei H. Acute toxicity of zinc oxide nanoparticles to the rat olfactory system after intranasal instillation. J Appl Toxicol. 2013;33:1079-88.
36. Rob J, Vandebriel WHDJ. A review of mammalian toxicity of ZnO nanoparticles. Nanotechnol Sci Appl. 2012;5:61-71.
37. Avalos A, Haza AI, Mateo D, Morales P. Cytotoxicity and ROS production of manufactured silver nanoparticles of different sizes in hepatoma and leukemia cells. J Appl Toxicol. 2014;34:413-23.
38. Nel A, Xia T, Madler L, Li N. Toxic potential of materials at the nanolevel. Science. 2006;311:622-7.
39. Gozzelino R, Jeney V, Soares MP. Mechanisms of cell protection by heme oxygenase-1. Annu Rev Pharmacol Toxicol. 2010;50:323-54.
40. Napierska D, Thomassen LCJ, Rabolli V, Lison D, Gonzalez L, Kirsch-Volders M, et al. Size-dependent cytotoxicity of monodisperse silica nanoparticles in human endothelial cells. Small. 2009;5:846-53.
41. Watanabe M, Yoneda M, Morohashi A, Hori Y, Okamoto D, Sato A, et al. Effects of Fe3O4 magnetic nanoparticles on A549 cells. Int J Mol Sci. 2013;14:15546-60.
42. Herzog E, Byrne HJ, Davoren M, Casey A, Duschl A, Oostingh GJ. Dispersion medium modulates oxidative stress response of human lung epithelial cells upon exposure to carbon nanomaterial samples. Toxicol Appl Pharmacol. 2009;236:276-81.
43. Hoffmann E, Dittrich-Breiholz O, Holtmann H, Kracht M. Multiple control of interleukin-8 gene expression. J Leukoc Biol. 2002;72:847-55.
44. Moos PJ, Olszewski K, Honeggar M, Cassidy P, Leachman S, Woessner D, et al. Responses of human cells to ZnO nanoparticles: a gene transcription study. Metallomics. 2011;3:1199-211.
45. Bae H, Ryu H, Jeong S, Lee E, Park Y-H, Lee K, et al. Oxidative stress and apoptosis induced by ZnO nanoparticles in HaCaT cells. Molecular & Cellular Toxicology. 2011;7:333-7.
46. Yan Z, Xu L, Han J, Wu Y-J, Wang W, Yao W, et al. Transcriptional and posttranscriptional regulation and endocytosis were involved in zinc oxide nanoparticle-induced interleukin-8 overexpression in human bronchial epithelial cells. Cell Biol Toxicol. 2014;30:79-88.
47. James SA, Feltis BN, de Jonge MD, Sridhar M, Kimpton JA, Altissimo M, et al. Quantification of ZnO Nanoparticle Uptake, Distribution, and Dissolution within Individual Human Macrophages. ACS Nano. 2013;7:10621-35.
48. Cho W-S, Duffin R, Howie S, Scotton C, Wallace W, MacNee W, et al. Progressive severe lung injury by zinc oxide nanoparticles; the role of Zn2+ dissolution inside lysosomes. Particle and Fibre Toxicology. 2011;8:1-16.
49. Adamcakova-Dodd A, Stebounova L, Kim J, Vorrink S, Ault A, O'Shaughnessy P, et al. Toxicity assessment of zinc oxide nanoparticles using sub-acute and sub-chronic murine inhalation models. Particle and Fibre Toxicology. 2014;11:15.
50. Baisch B, Corson N, Wade-Mercer P, Gelein R, Kennell A, Oberdorster G, et al. Equivalent titanium dioxide nanoparticle deposition by intratracheal instillation and whole body inhalation: the effect of dose rate on acute respiratory tract inflammation. Particle and Fibre Toxicology. 2014;11:5.