Iron Biochemistry is Correlated with Amyloid Plaque Morphology in an Established Mouse Model of Alzheimer's Disease

Cell Chemical Biology

Volumn 24, Issue 10, 2017, Pages 1205-1215.e3

  Telling, Neil D ^a   Everett, James ^a   Collingwood, Joanna F ^b,c   Dobson, Jon ^c   van der Laan, Gerrit ^d   Gallagher, Joseph J ^e   Wang, Jian ^f   Hitchcock, Adam P ^g  

^a KEELE UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF WARWICK   (United Kingdom)

^c University of Florida   (United States)

^d DIAMOND LIGHT SOURCE LTD   (United Kingdom)

^e TRINITY COLLEGE DUBLIN   (Ireland)

^f CANADIAN LIGHT SOURCE INC   (Canada)

^g MCMASTER UNIVERSITY   (Canada)

Author keywords

Alzheimer's disease; amyloid beta; diffuse plaque; ferrous iron; magnetite; redox active iron; scanning transmission X ray microscopy; STXM; x ray magnetic circular dichroism; X ray spectromicroscopy

Indexed keywords

AMYLOID BETA PROTEIN; IRON; MAGNETITE;

ALZHEIMER DISEASE; AMYLOID PLAQUE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOCHEMISTRY; BIOMINERALIZATION; BRAIN CORTEX; BRAIN TISSUE; C57BL 6 MOUSE; CONTROLLED STUDY; FEMALE; IN VIVO STUDY; MORPHOLOGY; MOUSE; NONHUMAN; PRIORITY JOURNAL; REDUCTION (CHEMISTRY); ANIMAL; COMPLICATION; DIAGNOSTIC IMAGING; DISEASE MODEL; METABOLISM; OXIDATION REDUCTION REACTION; TRANSMISSION ELECTRON MICROSCOPY;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; DISEASE MODELS, ANIMAL; IRON; MICE; MICROSCOPY, ELECTRON, TRANSMISSION; OXIDATION-REDUCTION; PLAQUE, AMYLOID;

EID: 85030841047     PISSN: 24519456     EISSN: 24519448     Source Type: Journal    
DOI: 10.1016/j.chembiol.2017.07.014     Document Type: Article

References (49)

1. Acosta-Cabronero, J., Williams, G.B., Cardenas-Blanco, A., Arnold, R.J., Lupson, V., Nestor, P.J., In vivo quantitative susceptibility mapping (QSM) in Alzheimer's disease. PLoS One, 8, 2013, e81093.
2. Ahmad, S., Kitchin, K.T., Cullen, W.R., Arsenic species that cause release of iron from ferritin and generation of activated oxygen. Arch. Biochem. Biophys. 382 (2000), 195–202.
3. Antharam, V., Collingwood, J.F., Bullivant, J.P., Davidson, M., Chandra, S., Mikhaylova, A., Finnegan, M., Batich, C., Dobson, J., Relaxation properties of human hippocampus in Alzheimer's disease using high field MRI microscopy. Neuroimage 59 (2012), 1249–1260.
4. Coker, V.S., Byrne, J.M., Telling, N.D., Van Der Laan, G., Lloyd, J.R., Hitchcock, A.P., Wang, J., Pattrick, R.A.D., Characterisation of the dissimilatory reduction of Fe(III)-oxyhydroxide at the microbe – mineral interface: the application of STXM–XMCD. Geobiology 10 (2012), 347–354.
5. 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., et al. Three-dimensional tomographic imaging and characterization of iron compounds within Alzheimer's plaque core material. J. Alzheimers Dis. 14 (2008), 235–245.
6. Collingwood, J.F., Mikhaylova, A., Davidson, M., Batich, C., Streit, W.J., Terry, J., Dobson, J., In situ characterization and mapping of iron compounds in Alzheimer's disease tissue. J. Alzheimers Dis. 7 (2005), 267–272.
7. Collingwood, J.F., Telling, N.D., Iron oxides in the human brain. Faivre, D., (eds.) Iron Oxides: From Nature to Applications, 2016, Wiley-VCH Verlag, 143–176.
8. de Groot, F.M.F., de Smit, E., van Schooneveld, M.M., Aramburo, L.R., Weckhuysen, B.M., In-situ scanning transmission X-ray microscopy of catalytic solids and related nanomaterials. ChemPhysChem 11 (2010), 951–962.
9. Devos, D., Moreau, C., Devedjian, J.C., Kluza, J.R., Petrault, M., Laloux, C., Jonneaux, A.L., Ryckewaert, G., Garçon, G., Targeting chelatable iron as a therapeutic modality in Parkinson's disease. Antioxid. Redox Signal. 21 (2014), 195–210.
10. Dickson, T.C., Vickers, J.C., The morphological phenotype of beta-amyloid plaques and associated neuritic changes in Alzheimer's disease. Neuroscience 105 (2001), 99–107.
11. Dobson, J., Nanoscale biogenic iron oxides in neurodegenerative disease. FEBS Lett. 496 (2001), 1–5.
12. Dobson, J., Grassi, P., Magnetic properties of human hippocampal tissue: evaluation of artefact and contamination sources. Brain Res. Bull. 39 (1996), 255–259.
13. El Tannir El Tayara, N., Volk, A., Dhenain, M., Delatour, B., Transverse relaxation time reflects brain amyloidosis in young APP/PS1 transgenic mice. Magn. Reson. Med. 58 (2007), 179–184.
14. Everett, J., Céspedes, E., Shelford, L.R., Exley, C., Collingwood, J.F., Dobson, J., van der Laan, G., Jenkins, C.A., Arenholz, E., Telling, N.D., Evidence of redox-active iron formation following aggregation of ferrihydrite and the Alzheimer's disease peptide β-amyloid. Inorg. Chem. 53 (2014), 2803–2809.
15. Everett, J., Céspedes, E., Shelford, L.R., Exley, C., Collingwood, J.F., Dobson, J., van der Laan, G., Jenkins, C.A., Arenholz, E., Telling, N.D., Ferrous iron formation following the co-aggregation of ferric iron and the Alzheimer's disease peptide β-amyloid (1-42). J. R. Soc. Interface, 11, 2014, 20140165.
16. Fandrich, M., Schmidt, M., Grigorieff, N., Recent progress in understanding Alzheimer's beta-amyloid structures. Trends Biochem. Sci. 36 (2011), 338–345.
17. Gallagher, J.J., Finnegan, M.E., Grehana, B., Dobson, J., Modest amyloid deposition is associated with iron dysregulation, microglial activation, and oxidative stress. J. Alzheimers Dis. 28 (2012), 147–161.
18. Garvie, L.A.J., Buseck, P.R., Ratios of ferrous to ferric iron from nanometre-sized areas in minerals. Nature 396 (1998), 667–670.
19. Guo, C., Wang, T., Zheng, W., Shan, Z.-Y., Teng, W.-P., Wang, Z.-Y., Intranasal deferoamine reverses iron-induced memory deficits and inhibits amyloidogenic APP processing in a transgenic mouse model of Alzheimer's disease. Neurobiol. Aging 34 (2013), 562–575.
20. House, E., Collingwood, J.F., Khan, A., Korchazkina, O., Berthon, G., Exley, C., Aluminium, iron, zinc and copper influence the in vitro formation of amyloid fibrils of Aβ42 in a manner which may have consequences for metal chelation therapy in Alzheimer's disease. J. Alzheimers Dis. 6 (2004), 291–301.
21. Huang, X.D., Atwood, C.S., Hartshorn, M.A., Multhaup, G., Goldstein, L.E., Scarpa, R.C., Cuajungco, M.P., Gray, D.N., Lim, J., Moir, R.D., et al. The A beta peptide of Alzheimer's disease directly produces hydrogen peroxide through metal ion reduction. Biochemistry 38 (1999), 7609–7616.
22. Huang, X.D., Atwood, C.S., Moir, R.D., Hartshorn, M.A., Tanzi, R.E., Bush, A.I., Trace metal contamination initiates the apparent auto-aggregation, amyloidosis, and oligomerization of Alzheimer's A beta peptides. J. Biol. Inorg. Chem. 9 (2004), 954–960.
23. Hunter, R.C., Hitchcock, A.P., Dynes, J.J., Obst, M., Beveridge, T.J., Mapping the speciation of iron in Pseudomonas aeruginosa. Environ. Sci. Technol. 42 (2008), 8766–8772.
24. Khan, A., Dobson, J.P., Exley, C., Redox cycling of iron by A-beta42. Free Radic. Biol. Med. 40 (2006), 557–569.
25. Kirschvink, J.L., Kobayashi-Kirschvink, A., Woodford, B.J., Magnetite biomineralization in the human brain. Proc. Natl. Acad. Sci. USA 89 (1992), 7683–7687.
26. Leung, B.O., Brash, J.L., Hitchcock, A.P., Characterization of biomaterials by soft X-ray spectromicroscopy. Materials 3 (2010), 3911–3938.
27. Li, J., Hitchcock, A.P., Stöver, H.D.H., Shirley, I., A new approach to studying microcapsule wall growth mechanisms. Macromolecules 42 (2009), 2428–2432.
28. Liu, B., Moloney, A., Meehan, S., Morris, K., Thomas, S.E., Serpell, L.C., Hider, R., Marciniak, S.J., Lomas, D.A., Crowther, D.C., Iron promotes the toxicity of amyloid beta peptide by impeding its ordered aggregation. J. Biol. Chem. 286 (2011), 4248–4256.
29. Mantyh, P.W., Ghilardi, J.R., Rogers, S., Demaster, E., Allen, C.J., Stimson, E.R., Maggio, J.E., Aluminum, iron, and zinc ions promote aggregation of physiological concentrations of beta-amyloid peptide. J. Neurochem. 61 (1993), 1171–1174.
30. Meadowcroft, D.M., Connor, J.R., Smith, M.B., Yang, Q.X., Magnetic resonance imaging and histological analysis of beta-amyloid plaques in both human Alzheimer's disease and APP/PS1 transgenic mice. J. Magn. Reson. Imaging 29 (2009), 997–1007.
31. Meadowcroft, M.D., Peters, D.G., Dewal, R.P., Connor, J.R., Yang, Q.X., The effect of iron in MRI and transverse relaxation of amyloid-beta plaques in Alzheimer's disease. NMR Biomed. 28 (2014), 297–305.
32. Mikula, S., Trotts, I., Stone, J., Jones, E.G., Internet-enabled high-resolution brain mapping and virtual microscopy. Neuroimage 35 (2007), 9–15.
33. Plascencia-Villa, G., Ponce, A., Collingwood, J.F., Arellano-Jimenez, M.J., Zhu, X.W., Rogers, J.T., Betancourt, I., Jose-Yacaman, M., Perry, G., High-resolution analytical imaging and electron holography of magnetite particles in amyloid cores of Alzheimer's disease. Sci. Rep., 6, 2016, 24873.
34. Quintana, C., Cowley, J.M., Marhicc, C., Electron nanodiffraction and high-resolution electron microscopy studies of the structure and composition of physiological and pathological ferritin. J. Struct. Biol. 147 (2004), 166–178.
35. Regan, T.J., Ohldag, H., Stamm, C., Nolting, F., Lüning, J., Stöhr, J., White, R.L., Chemical effects at metal/oxide interfaces studied by X-ray-absorption spectroscopy. Phys. Rev. B, 64, 2001, 214422.
36. Rival, T., Page, R.M., Chandraratna, D.S., Sendall, T.J., Ryder, E., Liu, B., Lewis, H., Rosahl, T., Hider, R., Camargo, L.M., et al. Fenton chemistry and oxidative stress mediate the toxicity of the beta-amyloid peptide in a Drosophila model of Alzheimer's disease. Eur. J. Neurosci. 29 (2009), 1335–1347.
37. Rottkamp, C.A., Raina, A.K., Zhu, X., Gaier, E., Bush, A.I., Atwood, C.S., Chevion, M., Perry, G., Smith, M.A., Redox-active iron mediates amyloid-beta toxicity. Free Radic. Biol. Med. 30 (2001), 447–450.
38. Selkoe, D.J., Alzheimer's disease: a central role for amyloid. J. Neuropathol. Exp. Neurol. 53 (1994), 438–447.
39. Shirahama, T., Cohen, A.S., A Congo red staining method for epoxy-embedded amyloid. J. Histochem. Cytochem. 14 (1966), 725–729.
40. Smith, M.A., Harris, P.L., Sayre, L.M., Perry, G., Iron accumulation in Alzheimer disease is a source of redox-generated free radicals. Proc. Natl. Acad. Sci. USA 94 (1997), 9866–9868.
41. Telling, N.D., Coker, V.S., Cutting, R.S., van der Laan, G., Pearce, C.I., Pattrick, R.A.D., Arenholz, E., Lloyd, J.R., Remediation of Cr(VI) by biogenic magnetic nanoparticles: an X-ray magnetic circular dichroism study. App Phys. Lett. 95 (2009), 163701–163703.
42. Tone, B.M., Fakra, S.C., Manganini, S.J., Santelli, C.M., Marcus, M.A., Moffett, J.W., Rouxel, O., German, C.R., Edwards, K.J., Preservation of iron(II) by carbon-rich matrices in a hydrothermal plume. Nat. Geosci. 2 (2009), 197–201.
43. van der Laan, G., Kirkman, I.W., The 2p absorption-spectra of 3d transition-metal compounds in tetrahedral and octahedral symmetry. J. Phys. Condens. Matter 4 (1992), 4189–4204.
44. van der Laan, G., Applications of soft X-ray magnetic dichroism. J. Phys. Conf. Ser., 430, 2013, 012127.
45. van der Laan, G., Figueroa, A.I., X-ray magnetic circular dichroism - a versatile tool to study magnetism. Coord. Chem. Rev. 277 (2014), 95–129.
46. Wan, L., Nie, G., Zhang, J., Luo, Y., Zhang, P., Zhang, Z., Zhao, B., Beta-amyloid peptide increases levels of iron content and oxidative stress in human cell and Caenorhabditis elegans models of Alzheimer disease. Free Radic. Biol. Med. 50 (2011), 122–129.
47. Wang, D., Li, Y.-Y., Luo, J.-H., Li, Y.-H., Age-related iron deposition in the basal ganglia of controls and Alzheimer disease patients quantified using susceptibility weighted imaging. Arch. Gerontol. Geriatr. 59 (2014), 439–449.
48. Yanker, B.A., Lu, T., Amyloid β-protein toxicity and the pathogenesis of Alzheimer disease. J. Biol. Chem. 284 (2009), 4755–4759.
49. Zhu, X.H., Kalirai, S.S., Hitchcock, A.P., Bazylinski, D.A., What is the correct Fe L-23 X-ray absorption spectrum of magnetite?. J. Electron Spectrosc. 199 (2015), 19–26.