Hostname: page-component-745bb68f8f-hvd4g Total loading time: 0 Render date: 2025-01-27T23:50:51.576Z Has data issue: false hasContentIssue false
  • English
  • Français

Investigation of the redox state of magnetite upon Aβ-fibril formation or proton irradiation; implication of iron redox inactivation and β-amyloidolysis

Published online by Cambridge University Press:  14 June 2018

Younshick Choi  and
Jong-Ki Kim
Younshick Choi
Affiliation:
Department of Biomedical Engineering & Radiology, School of Medicine, Catholic University of Daegu, Daegu 42472, Korea
Jong-Ki Kim*
Affiliation:
Department of Biomedical Engineering & Radiology, School of Medicine, Catholic University of Daegu, Daegu 42472, Korea
*
Address all correspondence to Jong-Ki Kim at jkkim@cu.ac.kr
Get access

Abstract

In in vitro separate compartment model of neuronal cells and extracellular iron oxide nanoparticles (IONs)–amyloid complexes, a traversing proton-induced Coulomb nanoradiator effect (CNR) was found to break up the ION–amyloid fibrils and to induce redox changes in the IONs. We found that the CNR effect caused the conversion of redox-active iron (II) into redox-inactive iron (III) as well as the disruption of the ION–amyloid fibrils without significantly damaging normal neuronal cells. Our observations suggest a non-invasive redox inactivation and β-amyloidolyis-based therapy of neurotoxic Aβ plaque involving a traversing proton Coulomb nanochelator that would not substantially impact normal neuronal cells.

Type
Research Letters
Information
MRS Communications , Volume 8 , Issue 3 , September 2018 , pp. 955 - 960
Check for updates
Copyright
Copyright © Materials Research Society 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1.Bolt, H.M. and Marchan, R.: Iron dysregulation: an important aspect in toxicology. Arch. Toxicol. 84, 823 (2010).Google Scholar
2.Savelieff, M.G., Lee, S., Liu, Y., and Lim, M.-H.: Untangling amyloid-β, tau, and metals in Alzheimer's disease ACS Chem. Biol. 8, 856–865 (2013).Google Scholar
3.Zecca, L., Youdim, M.B.H., Riederer, P., Connor, J.R., and Crichton, R.R.: Iron, brain ageing and neurodegenerative disorders. Nat. Rev. Neurosci. 5, 863 (2004).Google Scholar
4.Collingwood, J.F., Chong, R.K.K., Kasama, T., Cervera-Gontard, L., Dunin-Borkowski, R.E., Perry, G., Pósfai, M., Siedlak, S.L., Simpson, E.T., Smith, M.A., and Dobson, J.: Three-dimensional tomographic imaging and characterization of iron compounds within Alzheimer's plaque core material. J. Alzheimers Dis. 14, 235 (2008).Google Scholar
5.Kirschvink, J.L., Kobayashi-Kirschvink, A., and Woodford, B.J.: Magnetite biomineralization in the human brain. Proc. Natl. Acad. Sci. USA 89, 7683 (1992).Google Scholar
6.Gallagher, J.J., Finnegan, M.E., Grehana, B., and Dobson, J.: Modest amyloid deposition is associated with iron dysregulation, microglial activation, and oxidative stress. J. Alzheimers Dis. 28, 147 (2012).Google Scholar
7.Smith, M.A., Harris, P.L.R., Sayre, L.M., and Perry, G.: Iron accumulation in Alzheimer disease is a source of redox-generated free radicals. Proc. Natl. Acad. Sci. USA 94, 9866 (1997).Google Scholar
8.Honda, K., Moreira, P.I., Liu, Q., Siedlak, S.L., Zhu, X.W., Smith, M.A., and Perry, G.: Redox active iron at the center of oxidative stress in Alzheimer disease. Lett. Drug Des. Disc. 2, 479 (2005).Google Scholar
9.Everett, J., Céspedes, E., Shelford, L.R., Exley, C., Collingwood, J.F., Dobson, J., van der Laan, G., Jenkins, C.A., Arenholz, E., and Telling, N.D.: Ferrous iron formation following the co-aggregation of ferric iron and the Alzheimer's disease peptide b-amyloid (1–42). J. R. Soc. Interface 11, 20140165 (2014).Google Scholar
10.Teller, S., Tahirbegi, I.B., Mir, M., Samitier, J., and Soriano, J.: Magnetite-Amyloid-β deteriorates activity and functional organization in an in vitro model for Alzheimer's disease. Sci. Rep. 5, 17261 (2015).Google Scholar
11.Mirsadeghi, S., Shanehsazzadeh, S., Atyabi, F., and Dinarvand, R.: Effect of PEGylated superparamagnetic iron oxide nanoparticles (SPIONs) under magnetic field on amyloid beta fibrillation process. Mater. Sci. Eng. C 59, 390 (2016).Google Scholar
12.Mahmoudi, M., Quinlan-Pluck, F., Monopoli, M.P., Sheibani, S., Vali, H., Dawson, K.A., and Lynch, I., Influence of the physiochemical properties of superparamagnetic iron oxide nanoparticles on amyloid β protein fibrillation in solution. ACS Chem. Neurosci. 4, 475 (2013).Google Scholar
13.Telling, N.D., Everett, J, Collingwood, J.F., Dobson, J., van der Laan, G., Gallagher, J.J., Wang, J, and Hitchcock, A.P.: Iron biochemistry is correlated with amyloid plaque morphology in an established mouse model of Alzheimer's disease. Cell Chem. Biol. 24, 1205 (2017).Google Scholar
14.Kim, J.-K., Seo, S.-J., Kim, H.-T., Kim, K.-H., Chung, M.-H., Kim, K.-R., and Ye, S.-J.: Enhanced proton treatment in mouse tumors through proton irradiated nanoradiator effects on metallic nanoparticles. Phys. Med. Biol. 57, 8309 (2012).Google Scholar
15.Schuemann, J., Berbeco, R., Chithrani, D.B., Cho, S.H., Kumar, R., McMahon, S.J., Sridhar, S., and Krishnan, S.: Roadmap to clinical use of gold nanoparticles for radiation sensitization. Int. J. Radiat. Oncol. Biol. Phys. 94, 189 (2016).Google Scholar
16.Porcel, E., Tillement, O., Lux, F., Mowat, P., Usami, N., Kobayashi, K., Furusawa, Y., Le Sech, C., Li, S., and Lacombe, S.: Gadolinium-based nanoparticles to improve the hadrontherapy performances. Nanomed.: Nanotechnol. Biol. Med. 10, 1601 (2014).Google Scholar
17.Kim, H-K., Titze, J., Schöffler, M., Trinter, F., Waitz, M., Voigtsberger, J., Sann, H., Meckel, M., Stuck, C., Lenz, U., Odenweller, M., Neumann, N., Schössler, S., Ullmann-Pfleger, K., Ulrich, B., Costa Fraga, R., Petridis, N., Metz, D., Jung, A., Grisenti, R., Czasch, A., Jagutzki, O., Schmidt, L., Jahnke, T., Schmidt-Böcking, H., and Dörner, R.: Enhanced production of low energy electrons by alpha particle impact. Proc. Natl. Acad. Sci. USA 108, 11821 (2011).Google Scholar
18.Gokhberg, K., Kolorenč, P., Kuleff, A.I., and Cederbaum, L.S.: Site- and energy-selective slow-electron production through intermolecular Coulombic decay. Nature 505, 661 (2014).Google Scholar
19.Trinter, F., Schoeffler, M.S., Kim, H.K., Sturm, F.P., Cole, K., Neumann, N., Vredenborg, A., Williams, J., Bocharova, I., Guillemin, R., Simon, M., Belkacem, A., Landers, A.L., Weber, Th, Schmidt-Böcking, H., Dörner, R., and Jahnke, T.: Resonant Auger decay driving intermolecular Coulombic decay in molecular dimers. Nature 505, 664 (2014).Google Scholar
20.Wolfe, T., Chatterjee, D., Lee, J., Grant, J.D., Bhattarai, S., Tailor, R., Goodrich, G., Nicolucci, P., and Krishnan, S.: Targeted gold nanoparticles enhance sensitization of prostate tumors to megavoltage radiation therapy in vivo. Nanomedicine 11, 1277 (2015).Google Scholar
21.Hainfeld, J.F., Dilmanian, F.A., Zhong, Z., Slatkin, D.N., Kalef-Ezra, J.A., and Smilowitz, H.M.: Gold nanoparticles enhance the radiation therapy of a murine squamous cell carcinoma. Phys. Med. Biol. 55, 3045 (2010).Google Scholar
22.Taggart, L.E., McMahon, S.J., Currell, F.J., Prise, K.M., and Butterworth, K.T.: The role of mitochondrial function in gold nanoparticle mediated radiosensitisation. Cancer Nanotechnol. 7, 8 (2016).Google Scholar
23.Shmatov, M.L.: Importance of electric fields from ionized nanoparticles for radiation therapy. Phys. Part. Nucl. Lett. 14, 533 (2017).Google Scholar
24.Seo, S.-J., Jeon, J.-K., Han, S.-M., and Kim, J.-K.: Reactive oxygen species-based measurement of the dependence of the Coulomb nanoradiator effect on proton energy and atomic Z value. Int. J. Radiat. Biol. 93, 1239 (2017).Google Scholar
25.Jeon, J.-K., Han, S.-M., Min, S.-K., Seo, S.-J., Ihm, K, Chang, W.-S., and Kim, J.-K.: Coulomb nanoradiator-mediated, site-specific thrombolytic proton treatment with a traversing pristine Bragg peak. Sci. Rep. 6, 37848 (2016).Google Scholar
26.Cabrera, E., Mathews, P., Mezherichera, E., Beach, T.G., Deng, J., Neubert, T.A., Rostagnoa, A., and Ghiso, J.: Aβ truncated species: Implications for brain clearance mechanisms and amyloid plaque deposition. Biochim. Biophys. – Mol. Basis Dis. 1864, 208 (2018).Google Scholar
27.Boudaiffa, B., Cloutier, P., Hunting, D., Huels, M.A., and Sanche, L.: Resonant formation of DNA strand breaks by low-energy (3 to 20 eV) electrons. Science 287, 1658 (2000).Google Scholar
28.Abdoul-Carime, H., Cecchini, S., and Sanche, L.: Alteration of protein structure induced by low-energy (<18 eV) electrons. I. The peptide and disulfide bridges. Radiat. Res. 158, 23 (2002).Google Scholar
29.Sanchea, L.: Low energy electron-driven damage in biomolecules. Eur. Phys. J. D 35, 367 (2005).Google Scholar
30.Rezaee, M., Hill, R.P., and Jaffray, D.A.: The exploitation of low-energy electrons in cancer treatment. Radiat. Res. 188, 123 (2017).Google Scholar
31.McMahon, S.J., Hyland, W.B., Muir, M.F., Coulter, J.A., Jain, S., Butterworth, K.T., Schettino, G., Dickson, G.R., Hounsell, A.R., O'Sullivan, J.M., Prise, K.M., Hirst, D.G., and Currell, F.J.: Biological consequences of nanoscale energy deposition near irradiated heavy atom nanoparticles. Sci. Rep. 1, 18 (2011).Google Scholar
32.Jeon, J.-K., and Kim, J.-K.: Fluorescence imaging of reactive oxygen species by confocal laser scanning microscopy for track analysis of synchrotron X-ray photoelectric nanoradiator dose: X-ray pump–optical probe. J. Synchrotron Rad. 23, 1191 (2016).Google Scholar
33.Monje, M.L., Mizumatsu, S., Fike, J.R., and Palmer, T.D.: Irradiation induces neural precursor-cell dysfunction. Nat. Med. 8, 955 (2002).Google Scholar
34.Robbins, M.E., Bourland, J.D., Cline, J.M., Wheeler, K.T., and Deadwyler, S.A.: A model for assessing cognitive impairment after fractionated whole-brain irradiation in nonhuman primates. Radiat. Res. 175, 519 (2011).Google Scholar
35.Greene-Schloesser, D., Moore, E., and Robbins, M.E.: Molecular pathways: radiation-induced cognitive impairment. Clin Cancer Res. 19, 2294 (2013).Google Scholar
Supplementary material: File

Choi and Kim supplementary material 1

Choi and Kim supplementary material

Download Choi and Kim supplementary material 1(File)
File 1.5 MB