Intracellular accumulation dynamics and fate of zinc ions in alveolar epithelial cells exposed to airborne ZnO nanoparticles at the air-liquid interface

Nanotoxicology

Volumn 9, Issue 1, 2015, Pages 9-22

  Mihai, Cosmin ^a   Chrisler, William B ^b   Xie, Yumei ^a   Hu, Dehong ^a   Szymanski, Craig J ^a   Tolic, Ana ^a   Klein, Jessica A ^b   Smith, Jordan N ^b   Tarasevich, Barbara J ^c   Orr, Galya ^a  

^a PACIFIC NORTHWEST NATIONAL LABORATORY   (United States)

^b Fundamental and Computational Sciences Direct ^*  (Canada)

^c PACIFIC NORTHWEST NATIONAL LABORATORY   (United States)

Author keywords

Air liquid interface; Airborne nanoparticles; Endosomes; FluoZin 3; Intracellular Zn2+; Lysosomes

Indexed keywords

ZINC ION; ZINC OXIDE NANOPARTICLE; METAL NANOPARTICLE; ZINC; ZINC OXIDE;

AIRBORNE PARTICLE; ARTICLE; CELL LEVEL; CELL VACUOLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOTOXICITY; ENDOSOME; HUMAN; HUMAN CELL; LUNG ALVEOLUS EPITHELIUM CELL; LYSOSOME; PRIORITY JOURNAL; ANALYSIS; ANIMAL; CELL CULTURE TECHNIQUE; CELL LINE; CHEMISTRY; CYTOLOGY; DOSE RESPONSE; DRUG EFFECTS; EPITHELIUM CELL; EXPOSURE; INTRACELLULAR SPACE; LUNG ALVEOLUS; METABOLISM; MOUSE; OXIDATIVE STRESS;

ANIMALS; CELL CULTURE TECHNIQUES; CELL LINE; DOSE-RESPONSE RELATIONSHIP, DRUG; EPITHELIAL CELLS; INHALATION EXPOSURE; INTRACELLULAR SPACE; METAL NANOPARTICLES; MICE; OXIDATIVE STRESS; PULMONARY ALVEOLI; ZINC; ZINC OXIDE;

EID: 84925335188     PISSN: 17435390     EISSN: 17435404     Source Type: Journal    
DOI: 10.3109/17435390.2013.859319     Document Type: Article

References (54)

1. AshaRani PV, Low Kah Mun G, Hande MP, Valiyaveettil S. 2009. Cytotoxicity and genotoxicity of silver nanoparticles in human cells. ACS Nano 3:279-90.
2. Auld DS. 2001. Zinc coordination sphere in biochemical zinc sites. Biometals 14:271-313.
3. Bar-Ilan O, Albrecht RM, Fako VE, Furgeson DY. 2009. Toxicity assessments of multisized gold and silver nanoparticles in zebrafish embryos. Small 5:1897-910.
4. Buerki-Thurnherr T, Xiao L, Diener L, Arslan O, Hirsch C, Maeder-Althaus X, et al. 2013. In vitro mechanistic study towards a better understanding of ZnO nanoparticle toxicity. Nanotoxicology 7:402-16.
5. Cho WS, Duffin R, Howie SEM, Scotton CJ, Wallace WAH, MacNee W, et al. 2011. Progressive severe lung injury by zinc oxide nanoparticles; the role of Zn2 dissolution inside lysosomes. Part Fibre Toxicol 8: 1-16.
6. Cho WS, Duffin R, Poland CA, Duschl A, Oostingh GJ, Macnee W, et al. 2012a. Differential pro-inflammatory effects of metal oxide nanopar-ticles and their soluble ions in vitro and in vivo; zinc and copper nanoparticles, but not their ions, recruit eosinophils to the lungs. Nanotoxicology 6:22-35.
7. Cho WS, Duffin R, Poland CA, Howie SEM, MacNee W, Bradley M, et al. 2010. Metal oxide nanoparticles induce unique inflammatory footprints in the lung: important implications for nanoparticle testing. Environ Health Persp 118:1699-1706.
8. Cho WS, Duffin R, Thielbeer F, Bradley M, Megson IL, Macnee W, et al. 2012b. Zeta potential and solubility to toxic ions as mechanisms of lung inflammation caused by metal/metal oxide nanoparticles. Toxicol Sci 126:469-77.
9. Cousins RJ, Liuzzi JP, Lichten LA. 2006. Mammalian zinc transport, trafficking, and signals. J Biol Chem 281:24085-9.
10. de Duve C. 1983. Lysosomes revisited. Eur J Biochem 137:391-7.
11. Donaldson K, Borm PJA, Oberdorster G, Pinkerton KE, Stone V, Tran CL. 2008. Concordance between in vitro and in vivo dosimetry in the proinflammatory effects of low-toxicity, low-solubility particles: the key role of the proximal alveolar region. Inhal Toxicol 20:53-62.
12. Eide DJ. 2006. Zinc transporters and the cellular trafficking of zinc. Biochim Biophys Acta 1763:711-22.
13. Franklin NM, Rogers NJ, Apte SC, Batley GE, Gadd GE, Casey PS. 2007. Comparative toxicity of nanoparticulate ZnO, bulk ZnO, and ZnCl2 to a freshwater microalga (Pseudokirchneriella subcapitata): the importance of particle solubility. Environ Sci Technol 41:8484-90.
14. George S, Pokhrel S, Xia T, Gilbert B, Ji ZX, Schowalter M, et al. 2010. Use of a rapid cytotoxicity screening approach to engineer a safer zinc oxide nanoparticle through iron doping. ACS Nano 4:15-29.
15. Gilbert B, Fakra SC, Xia T, Pokhrel S, Madler L, Nel AE. 2012. The fate of ZnO nanoparticles administered to human bronchial epithelial cells. ACS Nano 6:4921-30.
16. Horie M, Nishio K, Endoh S, Kato H, Fujita K, Miyauchi A, et al. 2013. Chromium(III) oxide nanoparticles induced remarkable oxidative stress and apoptosis on culture cells. Environ Toxicol 28:61-75.
17. Horie M, Nishio K, Fujita K, Kato H, Nakamura A, Kinugasa S, et al. 2009. Ultrafine NiO particles induce cytotoxicity in vitro by cellular uptake and subsequent Ni(II) release. Chem Res Toxicol 22:1415-26.
18. Hsiao IL, Huang YJ. 2011. Effects of various physicochemical characteristics on the toxicities of ZnO and TiO2 nanoparticles toward human lung epithelial cells. Sci Total Environ 409:1219-28.
19. Huang CC, Aronstam RS, Chen DR, Huang YW. 2010. Oxidative stress, calcium homeostasis, and altered gene expression in human lung epithelial cells exposed to ZnO nanoparticles. Toxicol in Vitro 24: 45-55.
20. Hwang JJ, Lee SJ, Kim TY, Cho JH, Koh JY. 2008. Zinc and 4-hydroxy-2-nonenal mediate lysosomal membrane permeabilization induced by H2O2 in cultured hippocampal neurons. J Neurosci 28:3114-22.
21. Ji SL, Ye CH. 2008. Synthesis, growth mechanism, and applications of zinc oxide nanomaterials. J Mater Sci Technol 24:457-72.
22. Johansson AC, Appelqvist H, Nilsson C, Kagedal K, Roberg K, Ollinger K. 2010. Regulation of apoptosis-associated lysosomal membrane permeabilization. Apoptosis 15:527-40.
23. Karlsson HL, Cronholm P, Gustafsson J, Moller L. 2008. Copper oxide nanoparticles are highly toxic: a comparison between metal oxide nanoparticles and carbon nanotubes. Chem Res Toxicol 21:1726-32.
24. Kawata K, Osawa M, Okabe S. 2009. In vitro toxicity of silver nanoparticles at noncytotoxic doses to HepG2 human hepatoma cells. Environ Sci Technol 43:6046-51.
25. Kim YH, Fazlollahi F, Kennedy IM, Yacobi NR, Hamm-Alvarez SF, Borok Z, et al. 2010. Alveolar epithelial cell injury due to zinc oxide nanoparticle exposure. Am J Resp Crit Care 182:1398-409.
26. Kittler S, Greulich C, Koller M, Epple M. 2009. Synthesis of PVP-coated silver nanoparticles and their biological activity towards human mesenchymal stem cells. Materialwiss Werkst 40:258-64.
27. Könczöl M, Goldenberg E, Ebeling S, Schäfer B, Garcia-Käufer M, Gminski R, et al. 2012. Cellular uptake and toxic effects of fine and ultrafine metal-sulfate particles in human a549 lung epithelial cells. Chem Res Toxicol 25:2687-703.
28. Krezel A, Maret W. 2007. Dual nanomolar and picomolar Zn(II) binding properties of metallothionein. J Am Chem Soc 129:10911-21.
29. Kroemer G, Jaattela M. 2005. Lysosomes and autophagy in cell death control. Nat Rev Cancer 5:886-97.
30. Kuschner WG, Dalessandro A, Wintermeyer SF, Wong H, Boushey HA, Blanc PD. 1995. Pulmonary responses to purified zinc-oxide fume. J Invest Med 43:371-8.
31. Laity JH, Andrews GK. 2007. Understanding the mechanisms of zinc-sensing by metal-response element binding transcription factor-1 (MTF-1). Arch Biochem Biophys 463:201-10.
32. Lee SJ, Koh JY. 2010. Roles of zinc and metallothionein-3 in oxidative stress-induced lysosomal dysfunction, cell death, and autophagy in neurons and astrocytes. Mol Brain 3:1-9.
33. Lenz AG, Karg E, Lentner B, Dittrich V, Brandenberger C, Rothen-Rutishauser B, et al. 2009. A dose-controlled system for air-liquid interface cell exposure and application to zinc oxide nanoparticles. Part Fibre Toxicol 6:1-19.
34. Lin WS, Xu Y, Huang CC, Ma YF, Shannon KB, Chen DR, Huang YW. 2009. Toxicity of nano-and micro-sized ZnO particles in human lung epithelial cells. J Nanopart Res 11:25-39.
35. Lucarelli D, Russo S, Garman E, Milano A, Meyer-Klaucke W, Pohl E. 2007. Crystal structure and function of the zinc uptake regulator FurB from Mycobacterium tuberculosis. J Biol Chem 282:9914-22.
36. Mercer RR, Hubbs AF, Scabilloni JF, Wang LY, Battelli LA, Schwegler-Berry D, et al. 2010. Distribution and persistence of pleural penetrations by multi-walled carbon nanotubes. Part Fibre Toxicol 7:1-11.
37. Moos PJ, Chung K, Woessner D, Honeggar M, Cutler NS, Veranth JM. 2010. ZnO particulate matter requires cell contact for toxicity in human colon cancer cells. Chem Res Toxicol 23:733-9.
38. Oberdorster G, Oberdorster E, Oberdorster J. 2005. Nanotoxicology: an emerging discipline evolving from studies of ultrafine particles. Environ Health Persp 113:823-39.
39. Orr G, Panther DJ, Cassens KJ, Phillips JL, Tarasevich BJ, Pounds JG. 2009. Syndecan-1 mediates the coupling of positively charged submicrometer amorphous silica particles with actin filaments across the alveolar epithelial cell membrane. Toxicol Appl Pharmacol 236: 210-20.
40. Orr G, Panther DJ, Phillips JL, Tarasevich BJ, Dohnalkova A, Hu D, et al. 2007. Submicrometer and nanoscale inorganic particles exploit the actin machinery to be propelled along microvilli-like structures into alveolar cells. ACS Nano 1:463-75.
41. Rink L, Haase H. 2007. Zinc homeostasis and immunity. Trends Immunol 28:1-4.
42. Sayes CM, Reed KL, Warheit DB. 2007. Assessing toxicity of fine and nanoparticles: comparing in vitro measurements to in vivo pulmonary toxicity profiles. Toxicol Sci 97:163-80.
43. Sharma V, Anderson D, Dhawan A. 2012. Zinc oxide nanoparticles induce oxidative DNA damage and ROS-triggered mitochondria mediated apoptosis in human liver cells (HepG2). Apoptosis 17:852-70.
44. Soura V, Stewart-Parker M, Williams TL, Ratnayaka A, Atherton J, Gorringe K, et al. 2012. Visualization of co-localization in Abeta42-administered neuroblastoma cells reveals lysosome damage and autophagosome accumulation related to cell death. Biochem J 441: 579-90.
45. Wang XD, Song JH, Wang ZL. 2007. Nanowire and nanobelt arrays of zinc oxide from synthesis to properties and to novel devices. J Mater Chem 17:711-20.
46. Wang ZL. 2004. Zinc oxide nanostructures: growth, properties and applications. J Phys-Condens Mater 16:R829-58.
47. Warheit DB, Sayes CM, Reed KL. 2009. Nanoscale and fine zinc oxide particles: can in vitro assays accurately forecast lung hazards following inhalation exposures? Environ Sci Technol 43:7939-45.
48. Wellenreuther G, Cianci M, Tucoulou R, Meyer-Klaucke W, Haase H. 2009. The ligand environment of zinc stored in vesicles. Biochem Biophys Res Commun 380:198-203.
49. Wu WD, Samet JM, Peden DB, Bromberg PA. 2010. Phosphorylation of p65 is required for zinc oxide nanoparticle-induced interleukin 8 expression in human bronchial epithelial cells. Environ Health Persp 118:982-7.
50. Xia T, Hamilton RF, Bonner JC, Crandall ED, Elder A, Fazlollahi F, et al. 2013. Interlaboratory evaluation of in vitro cytotoxicity and inflammatory responses to engineered nanomaterials: The NIEHS Nano GO Consortium. Environ Health Perspect 121:683-90.
51. Xia T, Kovochich M, Liong M, Madler L, Gilbert B, Shi H, et al. 2008. Comparison of the mechanism of toxicity of zinc oxide and cerium oxide nanoparticles based on dissolution and oxidative stress properties. ACS Nano 2:2121-34.
52. Xia T, Zhao Y, Sager T, George S, Pokhrel S, Li N, et al. 2011. Decreased dissolution of ZnO by iron doping yields nanoparticles with reduced toxicity in the rodent lung and zebrafish embryos. ACS Nano 5: 1223-35.
53. Xie Y, Williams NG, Tolic A, Chrisler WB, Teeguarden JG, Maddux BL, et al. 2012. Aerosolized ZnO nanoparticles induce toxicity in alveolar type II epithelial cells at the air-liquid interface. Toxicol Sci 125: 450-61.
54. Xiu ZM, Ma J, Alvarez PJJ. 2011. Differential effect of common ligands and molecular oxygen on antimicrobial activity of silver nanoparticles versus silver ions. Environ Sci Technol 45: 9003-8.