Silica-coated magnetic nanoparticles impair proteasome activity and increase the formation of cytoplasmic inclusion bodies in vitro

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Phukan, Geetika ^a   Shin, Tae Hwan ^a,b   Shim, Jeom Soon ^a   Paik, Man Jeong ^c   Lee, Jin Kyu ^d   Choi, Sangdun ^b   Kim, Yong Man ^e   Kang, Seong Ho ^f   Kim, Hyung Sik ^g   Kang, Yup ^a   Lee, Soo Hwan ^a   Mouradian, M Maral ^h   Lee, Gwang ^a  

^a Ajou University School of Medicine   (South Korea)

^b Ajou University   (South Korea)

^c Sunchon National University   (South Korea)

^d Seoul National University   (South Korea)

^e Pharmicell Co Ltd   (South Korea)

^f Kyung Hee University   (South Korea)

^g Sungkyunkwan University   (South Korea)

^h RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SYNUCLEIN; MAGNETITE NANOPARTICLE; PROTEASOME; RHODAMINE; RHODAMINE ISOTHIOCYANATE; SILICON DIOXIDE;

ANIMAL; CELL INCLUSION; CHEMICALLY INDUCED; CHEMISTRY; DOPAMINERGIC NERVE CELL; DRUG EFFECT; GENETICS; HEK293 CELL LINE; HUMAN; PATHOLOGY; PRIMARY CELL CULTURE; PROTEINOSIS; RAT;

ALPHA-SYNUCLEIN; ANIMALS; DOPAMINERGIC NEURONS; HEK293 CELLS; HUMANS; INCLUSION BODIES; MAGNETITE NANOPARTICLES; PRIMARY CELL CULTURE; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN AGGREGATION, PATHOLOGICAL; RATS; RHODAMINES; SILICON DIOXIDE;

EID: 84977263551     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep29095     Document Type: Article

References (50)

1. Krug, H. F. & Wick, P. Nanotoxicology: an interdisciplinary challenge. Angew Chem Int Ed Engl 50, 1260-1278 (2011).
2. Larsen, B. A., Haag, M. A., Serkova, N. J., Shroyer, K. R. & Stoldt, C. R. Controlled aggregation of superparamagnetic iron oxide nanoparticles for the development of molecular magnetic resonance imaging probes. Nanotechnology 19, 265102 (2008).
3. Park, K. S. et al. Characterization, in vitro cytotoxicity assessment, and in vivo visualization of multimodal, RITC-labeled, silicacoated magnetic nanoparticles for labeling human cord blood-derived mesenchymal stem cells. Nanomedicine 6, 263-276 (2010).
4. Wu, J., Wang, C., Sun, J. & Xue, Y. Neurotoxicity of silica nanoparticles: brain localization and dopaminergic neurons damage pathways. ACS Nano 5, 4476-4489 (2011).
5. Kim, J. S. et al. Toxicity and tissue distribution of magnetic nanoparticles in mice. Toxicol Sci 89, 338-347 (2006).
6. Elder, A. et al. Translocation of inhaled ultrafine manganese oxide particles to the central nervous system. Environ Health Perspect 114, 1172-1178 (2006).
7. Liu, D. et al. In vitro and in vivo studies on the transport of PEGylated silica nanoparticles across the blood-brain barrier. ACS Appl Mater Interfaces 6, 2131-2136 (2014).
8. Linse, S. et al. Nucleation of protein fibrillation by nanoparticles. Proc Natl Acad Sci USA 104, 8691-8696 (2007).
9. Chen, M. & von Mikecz, A. Nanoparticle-induced cell culture models for degenerative protein aggregation diseases. Inhal Toxicol 21 Suppl 1, 110-114 (2009).
10. Zhang, D. et al. Gold nanoparticles can induce the formation of protein-based aggregates at physiological pH. Nano Lett 9, 666-671 (2009).
11. Fink, A. L. Protein aggregation: folding aggregates, inclusion bodies and amyloid. Fold Des 3, R9-23 (1998).
12. Shim, W. et al. Analysis of changes in gene expression and metabolic profiles induced by silica-coated magnetic nanoparticles. ACS Nano 6, 7665-7680 (2012).
13. Falaschetti, C. A. et al. Negatively charged metal oxide nanoparticles interact with the 20S proteasome and differentially modulate its biologic functional effects. ACS Nano 7, 7759-7772 (2013).
14. Wu, J. & Xie, H. Effects of titanium dioxide nanoparticles on alpha-synuclein aggregation and the ubiquitin-proteasome system in dopaminergic neurons. Artif Cells Nanomed Biotechnol 44, 690-694 (2016).
15. Menendez-Benito, V., Verhoef, L. G., Masucci, M. G. & Dantuma, N. P. Endoplasmic reticulum stress compromises the ubiquitinproteasome system. Hum Mol Genet 14, 2787-2799 (2005).
16. Rutkowski, D. T. et al. Adaptation to ER stress is mediated by differential stabilities of pro-survival and pro-apoptotic mRNAs and proteins. PLoS Biol 4, e374 (2006).
17. Galvin, J. E. et al. Pathobiology of the Lewy body. Adv Neurol 80, 313-324 (1999).
18. Gomez-Tortosa, E., Newell, K., Irizarry, M. C., Sanders, J. L. & Hyman, B. T. alpha-Synuclein immunoreactivity in dementia with Lewy bodies: morphological staging and comparison with ubiquitin immunostaining. Acta Neuropathol 99, 352-357 (2000).
19. Chung, K. K. et al. Parkin ubiquitinates the alpha-synuclein-interacting protein, synphilin-1: implications for Lewy-body formation in Parkinson disease. Nat Med 7, 1144-1150 (2001).
20. Engelender, S. et al. Synphilin-1 associates with alpha-synuclein and promotes the formation of cytosolic inclusions. Nat Genet 22, 110-114 (1999).
21. Kim, Y. S. et al. Multiple ligand interaction of alpha-synuclein produced various forms of protein aggregates in the presence of Abeta25-35, copper, and eosin. Brain Res 908, 93-98 (2001).
22. Jellinger, K. A. Recent developments in the pathology of Parkinson's disease. J Neural Transm Suppl. 347-376 (2002).
23. Fujisawa, S. & Kadoma, Y. Kinetic evaluation of polyamines as radical scavengers. Anticancer Res 25, 965-969 (2005).
24. Antony, T. et al. Cellular polyamines promote the aggregation of alpha-synuclein. J Biol Chem 278, 3235-3240 (2003).
25. Paik, M. J. et al. Polyamine patterns in the cerebrospinal fluid of patients with Parkinson's disease and multiple system atrophy. Clin Chim Acta 411, 1532-1535 (2010).
26. Wong, E. et al. Molecular determinants of selective clearance of protein inclusions by autophagy. Nat Commun 3, 1240 (2012).
27. Malvindi, M. A. et al. Toxicity assessment of silica coated iron oxide nanoparticles and biocompatibility improvement by surface engineering. PLoS One 9, e85835 (2014).
28. Maharjan, S., Oku, M., Tsuda, M., Hoseki, J. & Sakai, Y. Mitochondrial impairment triggers cytosolic oxidative stress and cell death following proteasome inhibition. Sci Rep 4, 5896 (2014).
29. Rhee, S. G. Cell signaling. H2O2, a necessary evil for cell signaling. Science 312, 1882-1883 (2006).
30. Wu, J. & Xie, H. Effects of titanium dioxide nanoparticles on alpha-synuclein aggregation and the ubiquitin-proteasome system in dopaminergic neurons. Artif Cells Nanomed Biotechnol, 1-5 (2014).
31. Yang, M. H. et al. Activation of the ubiquitin proteasome pathway by silk fibroin modified chitosan nanoparticles in hepatic cancer cells. Int J Mol Sci 16, 1657-1676 (2015).
32. Droge, W. Free radicals in the physiological control of cell function. Physiol Rev 82, 47-95 (2002).
33. Izumi, Y. et al. p-Quinone mediates 6-hydroxydopamine-induced dopaminergic neuronal death and ferrous iron accelerates the conversion of p-quinone into melanin extracellularly. J Neurosci Res 79, 849-860 (2005).
34. Wang, X. & Michaelis, E. K. Selective neuronal vulnerability to oxidative stress in the brain. Front Aging Neurosci 2, 12 (2010).
35. Agrawal, L. et al. Dopaminergic neurotoxicity of HIV-1 gp120: reactive oxygen species as signaling intermediates. Brain Res 1306, 116-130 (2010).
36. Liang, C. L., Wang, T. T., Luby-Phelps, K. & German, D. C. Mitochondria mass is low in mouse substantia nigra dopamine neurons: implications for Parkinson's disease. Exp Neurol 203, 370-380 (2007).
37. Sun, F. et al. Proteasome inhibitor MG-132 induces dopaminergic degeneration in cell culture and animal models. Neurotoxicology 27, 807-815 (2006).
38. Geiser, M. Update on macrophage clearance of inhaled micro- and nanoparticles. J Aerosol Med Pulm Drug Deliv 23, 207-217 (2010).
39. Wang, Z., Tiruppathi, C., Minshall, R. D. & Malik, A. B. Size and dynamics of caveolae studied using nanoparticles in living endothelial cells. ACS Nano 3, 4110-4116 (2009).
40. Vacha, R., Martinez-Veracoechea, F. J. & Frenkel, D. Receptor-mediated endocytosis of nanoparticles of various shapes. Nano Lett 11, 5391-5395 (2011).
41. Bohmer, N. & Jordan, A. Caveolin-1 and CDC42 mediated endocytosis of silica-coated iron oxide nanoparticles in HeLa cells. Beilstein J Nanotechnol 6, 167-176 (2015).
42. Blechinger, J. et al. Uptake kinetics and nanotoxicity of silica nanoparticles are cell type dependent. Small 9, 3970-3980, 3906 (2013).
43. Doherty, G. J. & McMahon, H. T. Mechanisms of endocytosis. Annu Rev Biochem 78, 857-902 (2009).
44. Bright, G. R., Fisher, G. W., Rogowska, J. & Taylor, D. L. Fluorescence ratio imaging microscopy: temporal and spatial measurements of cytoplasmic pH. J Cell Biol 104, 1019-1033 (1987).
45. Malhotra, J. D. & Kaufman, R. J. Endoplasmic reticulum stress and oxidative stress: a vicious cycle or a double-edged sword? Antioxid Redox Signal 9, 2277-2293 (2007).
46. Lee, G. et al. Casein kinase II-mediated phosphorylation regulates alpha-synuclein/synphilin-1 interaction and inclusion body formation. J Biol Chem 279, 6834-6839 (2004).
47. Shaw, G., Morse, S., Ararat, M. & Graham, F. L. Preferential transformation of human neuronal cells by human adenoviruses and the origin of HEK 293 cells. FASEB J 16, 869-871 (2002).
48. Block, M. L. et al. Nanometer size diesel exhaust particles are selectively toxic to dopaminergic neurons: the role of microglia, phagocytosis, and NADPH oxidase. FASEB J 18, 1618-1620 (2004).
49. Yoon, T. J. et al. Multifunctional nanoparticles possessing a "magnetic motor effect" for drug or gene delivery. Angew Chem Int Ed Engl 44, 1068-1071 (2005).
50. Beck, G. R. Jr. et al. Bioactive silica-based nanoparticles stimulate bone-forming osteoblasts, suppress bone-resorbing osteoclasts, and enhance bone mineral density in vivo. Nanomedicine 8, 793-803 (2012).