Hostname: page-component-cd9895bd7-jkksz Total loading time: 0 Render date: 2024-12-28T03:07:54.290Z Has data issue: false hasContentIssue false
  • English
  • Français

Multiple Morphologies of Gold–Magnetite Heterostructure Nanoparticles are Effectively Functionalized with Protein for Cell Targeting

Published online by Cambridge University Press:  07 June 2013

Evan S. Krystofiak ,
Eric C. Mattson ,
Paul M. Voyles ,
Carol J. Hirschmugl ,
Ralph M. Albrecht ,
Marija Gajdardziska-Josifovska  and
Julie A. Oliver
Evan S. Krystofiak
Affiliation:
Department of Biological Sciences, University of Wisconsin–Milwaukee, P.O. Box 413, Milwaukee, WI 53201-0413, USA
Eric C. Mattson
Affiliation:
Department of Physics, University of Wisconsin–Milwaukee, P.O. Box 413, Milwaukee, WI 53201-0413, USA
Paul M. Voyles
Affiliation:
Department of Materials Science and Engineering, University of Wisconsin, Madison, WI 53706, USA
Carol J. Hirschmugl
Affiliation:
Department of Physics, University of Wisconsin–Milwaukee, P.O. Box 413, Milwaukee, WI 53201-0413, USA
Ralph M. Albrecht
Affiliation:
Department of Animal Sciences, University of Wisconsin, Madison, WI 53706, USA Department of Pharmaceutical Sciences, University of Wisconsin, Madison, WI 53706, USA Department of Pediatrics, University of Wisconsin, Madison, WI 53706, USA
Marija Gajdardziska-Josifovska
Affiliation:
Department of Physics, University of Wisconsin–Milwaukee, P.O. Box 413, Milwaukee, WI 53201-0413, USA
Julie A. Oliver*
Affiliation:
Department of Biological Sciences, University of Wisconsin–Milwaukee, P.O. Box 413, Milwaukee, WI 53201-0413, USA Department of Animal Sciences, University of Wisconsin, Madison, WI 53706, USA
*
*Corresponding author. E-mail: [email protected]
Get access

Abstract

Nanoparticles composed of a magnetic iron oxide core surrounded by a metal shell have utility in a broad range of biomedical applications. However, the presence of surface energy differences between the two components makes wetting of oxide with metal unfavorable, precluding a “core–shell” structure of an oxide core completely surrounded by a thin metal shell. Three-dimensional island growth followed by island coalescence into thick shells is favored over the two-dimensional layer-by-layer growth of a thin, continuous metal coating of a true core–shell. Aqueous synthesis of gold-coated magnetite nanoparticles with analysis by infrared, energy-dispersive X-ray, and electron energy loss spectroscopies; high-resolution transmission electron microscopy; selected area electron diffraction; and high-angle annular dark-field scanning transmission electron microscopy showed two distinct morphologies that are inconsistent with an idealized core–shell. The majority were isolated ~16–22-nm-diameter nanoparticles consisting of ~7-nm-diameter magnetite and a thick deposition of gold, most often discontinuous, with some potentially “sandwiched” morphologies. A minority were aggregates of agglomerated magnetite decorated with gold but displaying significant bare magnetite. Both populations were successfully conjugated to fibrinogen and targeted to surface-activated platelets, demonstrating that iron oxide–gold nanoparticles produced by aqueous synthesis do not require an ideal core–shell structure for biological activity in cell labeling and targeting applications.

Keywords

analytical electron microscopycell targetingdiffractioninfrared spectroscopyplateletsfibrinogen
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 19 , Issue 4 , August 2013 , pp. 821 - 834
Copyright
Copyright © Microscopy Society of America 2013 

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.)

Footnotes

†

These authors contributed equally to this work and thus share first authorship.

References

Akamatsu, K., Kimura, M., Shibata, Y., Nakano, S., Miyoshi, D., Nawafune, H. & Sugimoto, N. (2006). A DNA duplex with extremely enhanced thermal stability based on controlled immobilization on gold nanoparticles. Nano Lett 6, 491–495.Google Scholar
Albrecht, R.M., Goodman, S.L. & Simmons, S.R. (1989). Distribution and movement of membrane-associated platelet glycoproteins: Use of colloidal gold with correlative video-enhanced light microscopy, low-voltage high-resolution scanning electron microscopy, and high-voltage transmission electron microscopy. Am J Anat 185, 149–164.CrossRefGoogle ScholarPubMed
Bao, J., Chen, W., Liu, T., Zhu, Y., Jin, P., Wang, L., Liu, J., Wei, Y. & Li, Y. (2007). Bifunctional Au-Fe3O4 nanoparticles for protein separation. ACS Nano 1, 293–298.CrossRefGoogle ScholarPubMed
Caruntu, D., Cushing, B.L., Caruntu, G. & O'Conner, C.J. (2005). Attachment of gold nanograins onto colloidal magnetite nanocrystals. Chem Mater 17, 3398–3402.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. Google Scholar
Cho, S.-J., Idrobo, J.-C., Olamit, J., Liu, K., Browning, N.D. & Kauzlarich, S.M. (2005). Growth mechanisms and oxidation resistance of gold-coated iron nanoparticles. Chem Mater 17, 3181–3186.Google Scholar
Colliex, C., Manoubi, T. & Ortiz, C. (1991). Electron-energy-loss-spectroscopy near-edge fine structures in the iron-oxygen system. Phys Rev B 44, 11402–11411.Google Scholar
Cui, Y.-R., Hong, C., Zhou, Y.-L., Li, Y., Gao, X.-M. & Zhang, X.-X. (2011). Synthesis of orientedly bioconjugated core/shell Fe3O4@Au magnetic nanoparticles for cell separation. Talanta 85, 1246–1252.Google Scholar
Fan, Z., Shelton, M., Singh, A.K., Senapati, D., Khan, S.A. & Ray, P.C. (2012). Multifunctional plasmonic shell-magnetic core nanoparticles for targeted diagnostics, isolation, and photothermal destruction of tumor cells. ACS Nano 6, 1065–1073.Google Scholar
Finnis, M.W. (1996). The theory of metal-ceramic interfaces. J Phys: Condens Matter 8, 5811–5836.Google Scholar
Gangopadhyay, P., Gallet, S., Franz, E., Persoons, A. & Verbiest, T. (2005). Novel superparamagnetic core(shell) nanoparticles for magnetic targeted drug delivery and hyperthermia treatment. IEEE Trans Magn 41, 4194–4196.Google Scholar
Gatel, C. & Snoeck, E. (2006). Comparative study of Pt, Au and Ag growth on Fe3O4(0 0 1) surface. Surf Sci 600, 2650–2662.Google Scholar
Gatel, C. & Snoeck, E. (2007). Epitaxial growth of Au and Pt on Fe3O4(1 1 1) surface. Surf Sci 601, 1031–1039.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
Gole, A., Dash, C., Ramakrishnan, V., Sainkar, S.R., Mandale, A.B., Rao, M. & Sastry, M. (2001). Pepsin-gold colloid conjugates: Preparation, characterization, and enzymatic activity. Langmuir 17, 1674–1679.Google Scholar
Gole, A., Vyas, S., Phadtare, S., Lachke, A. & Sastry, M. (2002). Studies on the formation of bioconjugates of Endoglucanase with colloidal gold. Colloid Surf B Biointerfaces 25, 129–138.Google Scholar
Goodman, S.L., Hodges, G.M. & Livingston, D.C. (1980). A review of the colloidal gold marker system. Scan Electron Microsc 1980/II, 133–146.Google Scholar
Goon, I.Y., Lai, L.M.H., Lim, M., Munroe, P., Gooding, J.J. & Amal, R. (2009). Fabrication and dispersion of gold-shell-protected magnetite nanoparticles: Systematic control using polyethyleneimine. Chem Mater 21, 673–681.Google Scholar
Haiss, W., Thanh, N.T.K., Aveyard, J. & Fernig, D.G. (2007). Determination of size and concentration of gold nanoparticles from UV-Vis spectra. Anal Chem 79, 4215–4221.Google Scholar
Hu, J.-D., Zevi, Y., Kou, X.-M., Xiao, J., Wang, X.-J. & Jin, Y. (2010). Effect of dissolved organic matter on the stability of magnetite nanoparticles under different pH and ionic strength conditions. Sci Total Environ 408, 3477–3489.CrossRefGoogle ScholarPubMed
Jeong, J.-R., Lee, S.-J., Kim, J.-D. & Shin, S.-C. (2004). Magnetic properties of γ-Fe2O3 nanoparticles made by coprecipitation method. Phys Status Solidi B 241, 1593–1596.Google Scholar
Johannsen, M., Thiesen, B., Jordan, A., Taymoorian, K., Gneveckow, U., Waldöfner, N., Scholz, R., Koch, M., Lein, M., Jung, K. & Loening, S.A. (2005). Magnetic fluid hyperthermia (MFH) reduces prostate cancer growth in the orthotopic Dunning R3327 rat model. Prostate 64, 283–292.Google Scholar
Krystofiak, E.S., Matson, V.Z., Steeber, D.A. & Oliver, J.A. (2012). Elimination of tumor cells using folate receptor targeting by antibody-conjugted, gold-coated magnetite nanoparticles in a murine breast cancer model. J Nanomater 2012, 431012. Google Scholar
Lee, H.S., Lee, W.C. & Furubayashi, T. (1999). A comparison of coprecipitation with microemulsion methods in the preparation of magnetite. J Appl Phys 85, 5231–5233.Google Scholar
Lim, I.-I.S., Njoki, P.N., Park, H.-Y., Wang, X., Wang, L., Mott, D. & Zhong, C.-J. (2008). Gold and magnetic oxide/gold core/shell nanoparticles as bio-functional nanoprobes. Nanotechnology 19, 305102. Google Scholar
Liu, H.L., Sonn, C.H., Wu, J.H., Lee, K.-M. & Kim, Y.K. (2008). Synthesis of streptavidin-FITC-conjugated core-shell Fe3O4-Au nanocrystals and their application for the purification of CD4+ lymphocytes. Biomaterials 29, 4003–4011.Google Scholar
Loftus, J.C. & Albrecht, R.M. (1984). Redistribution of the fibrinogen receptor of human platelets after surface activation. J Cell Biol 99, 822–829.Google Scholar
Lu, Q.H., Yao, K.L., Xi, D., Liu, Z.L., Luo, X.P. & Ning, Q. (2006). Synthesis and characterization of composite nanoparticles comprised of gold shell and magnetic core/cores. J Magn Magn Mater 301, 44–49.Google Scholar
Lyon, J.L., Fleming, D.A., Stone, M.B., Schiffer, P. & Williams, M.E. (2004). Synthesis of Fe oxide core/Au shell nanoparticles by iterative hydroxylamine seeding. Nano Lett 4, 719–723.Google Scholar
Mandal, M., Kundu, S., Ghosh, S.K., Panigrahi, S., Sau, T.K., Yusuf, S.M. & Pal, T. (2005). Magnetite nanoparticles with tunable gold or silver shell. J Colloid Interface Sci 286, 187–194.Google Scholar
Massart, R. (1981). Preparation of aqueous magnetic liquids in alkaline and acidic media. IEEE Trans Magn 17, 1247–1248.CrossRefGoogle Scholar
Mazzucchelli, S., Colombo, M., De Palma, C., Salvadè, A., Verderio, P., Coghi, M.D., Clementi, E., Tortora, P., Corsi, F. & Prosperi, D. (2010). Single-domain protein A-engineered magnetic nanoparticles: Toward a universal strategy to site-specific labeling of antibodies for targeted detection of tumor cells. ACS Nano 4, 5693–5702.Google Scholar
Meyer, D.A., Oliver, J.A. & Albrecht, R.M. (2010). Colloidal palladium particles of different shapes for electron microscopy labeling. Microsc Microanal 16, 33–42.Google Scholar
Mornet, S., Vasseur, S., Grasset, F. & Duguet, E. (2004). Magnetic nanoparticle design for medical diagnosis and therapy. J Mater Chem 14, 2161–2175.Google Scholar
Oliver, J.A. & Albrecht, R.M. (1987). Colloidal gold labelling of fibrinogen receptors in epinephrine- and ADP-activated platelet suspensions. Scanning Microsc 1, 745–756.Google ScholarPubMed
Pal, S., Morales, M., Mukherjee, P. & Srikanth, H. (2009). Synthesis and magnetic properties of gold coated iron oxide nanoparticles. J Appl Phys 105, 07B504. Google Scholar
Pankhurst, Q.A., Connolly, J., Jones, S.K. & Dobson, J. (2003). Applications of magnetic nanoparticles in biomedicine. J Phys D: Appl Phys 36, R167–R181.Google Scholar
Pham, T.T.H., Cao, C. & Sim, S.J. (2008). Application of citrate-stabilized gold-coated ferric oxide composite nanoparticles for biological separations. J Magn Magn Mater 320, 2049–2055.CrossRefGoogle Scholar
Robinson, I., Tung, L.D., Maenosono, S., Wälti, C. & Thanh, N.T.K. (2010). Synthesis of core-shell gold coated magnetic nanoparticles and their interaction with thiolated DNA. Nanoscale 2, 2624–2630.Google Scholar
Signorini, L., Pasquini, L., Savini, L., Carboni, R., Boscherini, F. & Bonetti, E. (2003). Site-dependent oxidation in iron/iron oxide core-shell nanoparticles. Phys Rev B 68, 195423. Google Scholar
Simmons, S.R. & Albrecht, R.M. (1996). Self-association of bound fibrinogen on platelet surfaces. J Lab Clin Med 128, 39–50.Google Scholar
Simmons, S.R., Sims, P.A. & Albrecht, R.M. (1997). αIIbβ3 redistribution triggered by receptor cross-linking. Arterioscler Thromb Vasc Biol 17, 3311–3320.CrossRefGoogle Scholar
Tseng, H.-Y., Lee, C.-Y., Shih, Y.-H., Lin, X.-Z. & Lee, G.-B. (2007). Hyperthermia cancer therapy utilizing superparamagnetic nanoparticles. In 2007 2nd IEEE International Conference on Nano/Micro Engineered and Molecular Systems, pp. 163–166. Bangkok, Thailand: Institute of Electrical and Electronics Engineers.Google Scholar
Wang, L., Luo, J., Fan, Q., Suzuki, M., Suzuki, I.S., Engelhard, M.H., Lin, Y., Kim, N., Wang, J.Q. & Zhong, C.-J. (2005a). Monodispersed core-shell Fe3O4@Au nanoparticles. J Phys Chem B 109, 21593–21601.Google Scholar
Wang, L., Luo, J., Maye, M.M., Fan, Q., Rendeng, Q., Engelhard, M.H., Wang, C., Lin, Y. & Zhong, C.-J. (2005b). Iron oxide-gold core-shell nanoparticles and thin film assembly. J Mater Chem 15, 1821–1832.Google Scholar
Wu, W., He, Q., Chen, H., Tang, J. & Nie, L. (2007). Sonochemical synthesis, structure and magnetic properties of air-stable Fe3O4/Au nanoparticles. Nanotechnology 18, 145609. CrossRefGoogle Scholar
Zhang, H., Zhong, X., Xu, J.-J. & Chen, H.-Y. (2008). Fe3O4/polypyrrole/Au nanocomposites with core/shell/shell structure: Synthesis, characterization, and their electrochemical properties. Langmuir 24, 13748–13752.Google Scholar
Zhao, D.-L., Zhang, H.-L., Zeng, X.-W., Xia, Q.-S. & Tang, J.-T. (2006). Inductive heat property of Fe3O4/polymer composite nanoparticles in an AC magnetic field for localized hyperthermia. Biomed Mater 1, 198–201.Google Scholar
Zook, J.M., Rastogi, V., Maccuspie, R.I., Keene, A.M. & Fagan, J. (2011). Measuring agglomerate size distribution and dependence of localized surface plasmon resonance absorbance on gold nanoparticle agglomerate size using analytical ultracentrifugation. ACS Nano 5, 8070–8079.CrossRefGoogle Scholar