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Identification of Ferrous-Ferric Fe3O4 Nanoparticles in Recombinant Human Ferritin Cages

Published online by Cambridge University Press:  26 June 2013

Michael G. Walls ,
Changqian Cao ,
Kui Yu-Zhang ,
Jinhua Li ,
Renchao Che  and
Yongxin Pan
Michael G. Walls
Affiliation:
Laboratoire de Physiques des Solides, UMR CNRS 8502, Bât. 510, 91405 Orsay, France
Changqian Cao
Affiliation:
Franco-Chinese Bio-Mineralization and Nano-Structures Laboratory, Key Laboratory of the Earth's Deep Interior, Institute of Geology and Geophysics, Chinese Academy of Sciences, Beijing 100029, China
Kui Yu-Zhang*
Affiliation:
Dépt. Physique, Université de Reims, B.P. 1039, 51687 Reims, France
Jinhua Li
Affiliation:
Franco-Chinese Bio-Mineralization and Nano-Structures Laboratory, Key Laboratory of the Earth's Deep Interior, Institute of Geology and Geophysics, Chinese Academy of Sciences, Beijing 100029, China
Renchao Che
Affiliation:
Laboratory of Advanced Materials, Fudan University, 2205 Songhu Road, Shanghai 200438, China
Yongxin Pan
Affiliation:
Franco-Chinese Bio-Mineralization and Nano-Structures Laboratory, Key Laboratory of the Earth's Deep Interior, Institute of Geology and Geophysics, Chinese Academy of Sciences, Beijing 100029, China
*
*Corresponding author. E-mail: kui.yu@univ-reims.fr
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Abstract

Recombinant ferritin is an excellent template for the synthesis of magnetic nanoparticles. This paper describes carefully performed experiments both to identify ironoxides within nanoparticles and to measure the number of iron atoms in the cores of recombinant human H-chain ferritin (HFn), based on spectroscopy techniques. Using electron energy-loss spectroscopy (EELS) analysis, magnetite (Fe3O4) has been unequivocally identified as the ironoxide formed within HFn cores under special preparation conditions. Atom counting analysis by EELS and high-angle annular dark-field imaging further allowed the correlation of the particle sizes to the real Fe atom numbers in a quantitative manner. These results help clarify some structural confusion between magnetite and maghemite (γ-Fe2O3), and also provide standard data for the number of Fe atoms within Fe3O4 particles of a given size, whose use is not limited to cases of magnetite synthesized in the cores of recombinant human ferritin.

Keywords

ferritinironoxidesnanoparticleTEMEELSHAADF
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 19 , Issue 4 , August 2013 , pp. 835 - 841
Copyright
Copyright © Microscopy Society of America 2013 

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References

Brice-Profeta, S., Arrio, M.A., Tronc, E., Menguy, N., Letard, I., Cartier dit Moulin, C., Nogues, M., Chanéac, C., Jolivet, J.P. & Sainctavit, P. (2005). Magnetic order in γ-Fe2O3 nanoparticles: A XMCD study. J Magn Magn Mater 288, 354–365.Google Scholar
Cao, C., Tian, L., Liu, Q., Liu, W., Chen, G. & Pan, Y. (2010). Magnetic characterization of noninteracting, randomly oriented, nanometer-scale ferrimagnetic particles. J Geophys Res 115, B07103. Google Scholar
Chen, J., Huang, D.J., Tanaka, A., Chang, C.F., Chung, S.C., Wu, W.B. & Chen, C.T. (2004). Magnetic circular dichroism in Fe 2p resonant photoemission of magnetite. Phys Rev B 69, 085107. Google Scholar
Chen, S.-Y., Gloter, A., Zobelli, A., Wang, L., Chen, C.-H. & Colliex, C. (2009). Electron energy loss spectroscopy and ab initio investigation of iron oxide nanomaterials grown by a hydrothermal process. Phys Rev B 79, 104103-1–10.Google Scholar
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. & Dobson, J. (2008). Three-dimensional tomographic imaging and characterization of iron compounds within Alzheimer's plaque core material. J Alzheimers Dis 14, 235–245.Google Scholar
Cornell, R.M. & Schwertmann, U. (2003). The Iron Oxides: Structure, Properties, Reactions, Occurrences and Uses, 2nd completely revised and extended edition. Weinheim, Germany: Wiley-VCH.Google Scholar
Cowley, J.M., Janney, D.E., Gerkin, R.C. & Buseck, P.R. (2000). The structure of ferritin cores determined by electron nanodiffraction. J Struct Biol 131, 210–216.Google Scholar
Crocombette, J., Pollak, M., Jollet, F., Thromat, N. & Gautier-Soyer, M. (1995). X-ray-absorption spectroscopy at the Fe L2,3 threshold in iron oxides. Phys Rev B 52, 3143. Google Scholar
Dobson, J. (2001a). Nanoscale biogenic iron oxides and neurodegenerative disease. FEBS Lett 496, 1–5.Google Scholar
Dobson, J. (2001b). On the structural form of iron in ferritin cores associated with progressive supranuclear palsy and Alzheimer's disease. Cell Mol Biol (Noisy-le-grand) 47, OL49–50.Google Scholar
Douglas, T., Strable, E., Willits, D., Aitouchen, A., Libera, M. & Young, M. (2002). Protein engineering of a viral cage for constrained nanomaterials synthesis. Adv Mater 14, 415–418.Google Scholar
Egerton, R.F. (2011). Electron Energy-Loss Spectroscopy in the Electron Microscope. New York, Dordrecht, Heidelberg, London: Springer.CrossRefGoogle Scholar
Fan, K., Cao, C., Pan, Y., Lu, D., Yang, D., Feng, J., Song, L., Liang, M. & Yan, X. (2012). Magnetoferritin nanoparticles for targeting and visualizing tumour tissues. Nat Nanotechnol 7, 459–464.Google Scholar
Farrant, J.L. (1954). An electron microscopic study of ferritin. Biochim Biophys Acta 13, 569–576.Google Scholar
Fischbach, F.A. & Anderegg, J.W. (1965). An X-ray scattering study of ferritin and apoferritin. J Mol Biol 14, 458–473.CrossRefGoogle Scholar
Gálvez, N., Fernández, B., Sánchez, P., Cuesta, R., Ceolín, M., Clemente-León, M., Trasobares, S., López-Haro, M., Calvino, J.J., Stéphan, O. & Domínguez-Vera, J.M. (2008). Comparative structural and chemical studies of ferritin cores with gradual removal of their iron contents. J Am Chem Soc 130, 8062–8068.Google Scholar
Gloter, A., Douiri, A., Tencé, M. & Colliex, C. (2003). Improving energy resolution of EELS spectra: An alternative to the monochromator solution. Ultramicroscopy 96, 385–400.Google Scholar
Gloter, A., Zbinden, M., Guyot, F., Gaill, F. & Colliex, C. (2004). TEM-EELS study of natural ferrihydrite from geological-biological interactions in hydrothermal systems. Earth Planet Sci Lett 222, 947–957.Google Scholar
Goering, E. (2011). Large hidden orbital moments in magnetite. Phys Status Solidi B 248, 2345–2351.Google Scholar
Haggis, G.H. (1965). The iron oxide core of the ferritin molecule. J Mol Biol 14, 598–602.Google Scholar
Harrison, P.M. (1963). The structure of apoferritin: Molecular size, shape and symmetry from X-ray data. J Mol Biol 6, 404–422.Google Scholar
Harrison, P.M., Andrews, S.C., Artymiuk, P.J., Ford, G.C., Guest, J.R., Hirzmann, J., Lawson, D.M., Livingstone, J.C., Smith, J.M.A., Treffry, A. & Yewdall, S.J. (1991). Probing structure-function relations in ferritin and bacterioferritin. Adv Inorg Chem 36, 449–486.Google Scholar
Harrison, P.M. & Arosio, P. (1996). The ferritins: Molecular properties, iron storage function and cellular regulation. Biochim Biophys Acta 1275, 161–203.Google Scholar
Harrison, P.M., Fischbach, F.A., Hoy, T.G. & Haggis, G.H. (1967). Ferric oxyhydroxide core of ferritin. Nature 216, 1188–1190.Google Scholar
Harrison, P.M., Hoy, T.G., Macara, I.G. & Hoare, R.J. (1974). Ferritin iron uptake and release. Structure–function relationships. Biochem J 143, 445–451.Google Scholar
Hoy, T.G., Harrison, P.M., Shabbir, M. & Macara, I.G. (1974). The release of iron from horse spleen ferritin to 1,10-phenanthroline. Biochem J 137, 67–70.Google Scholar
Kirschvink, J.L., Kobayashi-Kirschvink, A. & Woodford, B.J. (1992). Magnetite biomineralization in the human brain. Proc Natl Acad Sci 89, 7683–7687.Google Scholar
Leapman, R.D. & Aronova, M.A. (2007). Localizing specific elements bound to macromolecules by EFTEM. In Cellular Electron Microscopy, McIntosh, J.R. (Ed.), vol. 79, pp. 593–613. Waltham, MA: Academic Press.CrossRefGoogle Scholar
Li, Z.Y., Young, N.P., Di Vece, M., Palomba, S., Palmer, R.E., Bleloch, A.L., Curley, B.C., Johnston, R.L., Jiang, J. & Yuan, J. (2008). Three-dimensional atomic-scale structure of size-selected gold nanoclusters. Nature 451, 46–48.CrossRefGoogle ScholarPubMed
Lovell, M.A., Robertson, J.D., Teesdale, W.J., Campbell, J.L. & Markesbery, W.R. (1998). Copper, iron and zinc in Alzheimer's disease senile plaques. J Neurol Sci 158, 47–52.CrossRefGoogle ScholarPubMed
Meldrum, F.C., Wade, V.J., Nimmo, D.L., Heywood, B.R. & Mann, S. (1991). Synthesis of inorganic nanophase materials in supramolecular protein cages. Nature 349, 684–687.CrossRefGoogle Scholar
Michel, F.M., Ehm, L., Antao, S.M., Lee, P.L., Chupas, P.J., Liu, G., Strongin, D.R., Schoonen, M.A.A., Phillips, B.L. & Parise, J.B. (2007). The structure of ferrihydrite, a nanocrystalline material. Science 316, 1726–1729.CrossRefGoogle ScholarPubMed
Pan, Y., Brown, A., Brydson, R., Warley, A., Li, A. & Powell, J. (2006). Electron beam damage studies of synthetic 6-line ferrihydrite and ferritin molecule cores within a human liver biopsy. Micron 37, 403–411.CrossRefGoogle ScholarPubMed
Pan, Y.-H., Vaughan, G., Brydson, R., Bleloch, A., Gass, M., Sader, K. & Brown, A. (2010). Electron-beam-induced reduction of Fe3+ in iron phosphate dihydrate, ferrihydrite, haemosiderin and ferritin as revealed by electron energy-loss spectroscopy. Ultramicroscopy 110, 1020–1032.Google Scholar
Pellegrain, E., Hagelstein, M., Doyle, S., Moser, H.O., Fuchs, J., Vollath, D., Schuppler, S., James, M.A., Saxena, S.S., Niesen, L., Rogojanu, O., Sawatzky, G.A., Ferrero, C., Borowski, M., Tjernberg, O. & Brookes, N.B. (1999). Characterization of nanocrystalline γ-Fe2O3 with synchrotron radiation techniques. Phys Status Solidi B 215, 797–801.Google Scholar
Quintana, C., Cowley, J.M. & Marhic, C. (2004). Electron nanodiffraction and high-resolution electron microscopy studies of the structure and composition of physiological and pathological ferritin. J Struct Biol 147, 166–178.Google Scholar
Rez, P. (1982). Cross-sections for energy loss spectrometry. Ultramicroscopy 9, 283–287.Google Scholar
Santambrogio, P., Cozzi, A., Levi, S., Rovida, E., Magni, F., Albertini, A. & Arosio, P. (2000). Functional and immunological analysis of recombinant mouse h- and l-ferritins from Escherichia coli . Protein Expres Purif 19, 212–218.CrossRefGoogle Scholar
Treffry, A., Bauminger, E.R., Hechel, D., Hodson, N.W., Nowik, I., Yewdall, S.J. & Harrison, P.M. (1993). Defining the roles of the threefold channels in iron uptake, iron oxidation and iron-core formation in ferritin: A study aided by site-directed mutagenesis. Biochem J 296, 721–728.Google Scholar
Uchida, M., Terashima, M., Cunningham, C.H., Suzuki, Y., Willits, D.A., Willis, A.F., Yang, P.C., Tsao, P.S., McConnell, M.V., Young, M.J. & Douglas, T. (2008). A human ferritin iron oxide nano-composite magnetic resonance contrast agent. Magn Reson Med 60, 1073–1081.Google Scholar
Zhang, P., Land, W., Lee, S., Juliani, J., Lefman, J., Smith, S.R., Germain, D., Kessel, M., Leapman, R., Rouault, T.A. & Subramaniam, S. (2005). Electron tomography of degenerating neurons in mice with abnormal regulation of iron metabolism. J Struct Biol 150, 144–153.Google Scholar
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