European Biophysics Journal

, Volume 37, Issue 2, pp 223–228 | Cite as

Intracellular heating of living cells through Néel relaxation of magnetic nanoparticles

  • Jean-Paul Fortin
  • Florence Gazeau
  • Claire Wilhelm
Biophysics Letter


Maghemite and cobalt ferrite anionic magnetic nanoparticles enter tumor cells and can be used as heat sources when exposed to a high-frequency magnetic field. Comparative studies of the two particles enable to unravel the magnetic heating mechanisms (Néel relaxation vs. Brown relaxation) responsible for the cellular temperature rise, and also to establish a simple model, adjusted to the experimental results, allowing to predict the intracellular heating efficiency of iron oxide nanoparticles. Hence, we are able to derive the best nanoparticle design for a given material with a view to intracellular hyperthermia-based applications.


  1. Alexiou C, Schmid RJ, Jurgons R, Kremer M, Wanner G, Bergemann C, Huenges E, Nawroth T, Arnold W, Parak FG (2006) Targeting cancer cells: magnetic nanoparticles as drug carriers. Eur Biophys J 35:446–450CrossRefGoogle Scholar
  2. Billotey C, Wilhelm C, Devaud M, Bacri JC, Bittoun J, Gazeau F (2003) Cell internalization of anionic maghemite nanoparticles: quantitative effect on magnetic resonance imaging. Magn Reson Med 49:646–654CrossRefGoogle Scholar
  3. Bulte JW, Zhang S, van Gelderen P, Herynek V, Jordan EK, Duncan ID, Frank JA (1999) Neurotransplantation of magnetically labeled oligodendrocyte progenitors: magnetic resonance tracking of cell migration and myelination. Proc Natl Acad Sci USA 96:15256–15261CrossRefADSGoogle Scholar
  4. DeNardo SJ, DeNardo GL, Miers LA, Natarajan A, Foreman AR, Gruettner C, Adamson GN, Ivkov R (2005) Development of tumor targeting bioprobes ((111)In-chimeric L6 monoclonal antibody nanoparticles) for alternating magnetic field cancer therapy. Clin Cancer Res 11:7087s–7092sCrossRefGoogle Scholar
  5. Dodd SJ, Williams M, Suhan JP, Williams DS, Koretsky AP, Ho C (1999) Detection of single mammalian cells by high-resolution magnetic resonance imaging. Biophys J 76:103–109CrossRefGoogle Scholar
  6. Fortin-Ripoche JP, Martina MS, Gazeau F, Menager C, Wilhelm C, Bacri JC, Lesieur S, Clement O (2006) Magnetic targeting of magnetoliposomes to solid tumors with MR imaging monitoring in mice: feasibility. Radiology 239:415–424CrossRefGoogle Scholar
  7. Fortin JP, Wilhelm C, Servais J, Ménager C, Bacri JC, Gazeau F (2007) Size-sorted anionic iron oxide nanomagnets as colloidal mediators for magnetic hyperthermia. JACS 129:2628–2635CrossRefGoogle Scholar
  8. Hafeli UO (2004) Magnetically modulated therapeutic systems. Int J Pharm 277:19–24CrossRefGoogle Scholar
  9. Hergt R, Hiergeist R, Hilger I, Kaiser WA, Lapatnikov Y, Margel S, Richter U (2004) Maghemite nanoparticles with very high AC-losses for application in RF-magnetic hyperthermia. J Magn Magn Mater 270:345–357CrossRefADSGoogle Scholar
  10. Hilger I, Andra W, Hergt R, Hiergeist R, Schubert H, Kaiser WA (2001) Electromagnetic heating of breast tumors in interventional radiology: in vitro and in vivo studies in human cadavers and mice. Radiology 218:570–575Google Scholar
  11. Hogemann D, Ntziachristos V, Josephson L, Weissleder R (2002) High throughput magnetic resonance imaging for evaluating targeted nanoparticle probes. Bioconjug Chem 13:116–121CrossRefGoogle Scholar
  12. Ito A, Tanaka K, Honda H, Abe S, Yamaguchi H, Kobayashi T (2003) Complete regression of mouse mammary carcinoma with a size greater than 15 mm by frequent repeated hyperthermia using magnetite nanoparticles. J Biosci Bioeng 96:364–369Google Scholar
  13. Ito A, Shinkai M, Honda H, Kobayashi T (2005) Medical application of functionalized magnetic nanoparticles. J Biosci Bioeng 100:1–11CrossRefGoogle Scholar
  14. Ito A, Kuga Y, Honda H, Kikkawa H, Horiuchi A, Watanabe Y, Kobayashi T (2004) Magnetite nanoparticle-loaded anti-HER2 immunoliposomes for combination of antibody therapy with hyperthermia. Cancer Lett 212:167–175CrossRefGoogle Scholar
  15. Jordan A, Wust P, Fahling H, John W, Hinz A, Felix R (1993) Inductive heating of ferrimagnetic particles and magnetic fluids: physical evaluation of their potential for hyperthermia. Int J Hyperthermia 9:51–68CrossRefGoogle Scholar
  16. Jordan A, Scholz R, Wust P, Fahling H, Krause J, Wlodarczyk W, Sander B, Vogl T, Felix R (1997) Effects of magnetic fluid hyperthermia (MFH) on C3H mammary carcinoma in vivo. Int J Hyperthermia 13:587–605CrossRefGoogle Scholar
  17. Jordan A, Scholz R, Wust P, Fakhling R, Felix R (1999a) Magnetic fluid hyperthermia (MFH): cancer treatment with AC magnetic field induced excitation of biocompatible superparamagnetic nanoparticles. J Mag Mag Mat 201:413–419CrossRefADSGoogle Scholar
  18. Jordan A, Scholz R, Wust P, Schirra H, Schiestel T, Schmidt H, Felix R (1999b) Endocytosis of dextran and silan-coated magnetite nanoparticles and the effect of intracellular hyperthermia on human mammary carcinoma cells in vitro. J Mag Mag Mat 194:185–196CrossRefADSGoogle Scholar
  19. Massart R (1981) Preparation of aqueous magnetic liquids in alkaline and acidic media. IEEE Trans Magn 17:1247–1248CrossRefADSGoogle Scholar
  20. Montet X, Montet-Abou K, Reynolds F, Weissleder R, Josephson L (2006) Nanoparticle imaging of integrins on tumor cells. Neoplasia 8:214–222CrossRefGoogle Scholar
  21. Moroz P, Jones SK, Gray BN (2002) Magnetically mediated hyperthermia: current status and future directions. Int J Hyperthermia 18:267–84CrossRefGoogle Scholar
  22. Rosensweig RE (2002) Heating magnetic fluid with alternating magnetic field. J Magn Magn Mater 252:370–374CrossRefADSGoogle Scholar
  23. Sun EY, Josephson L, Kelly KA, Weissleder R (2006) Development of nanoparticle libraries for biosensing. Bioconjug Chem 17:109–113CrossRefGoogle Scholar
  24. Thiel A, Scheffold A, Radbruch A (1998) Immunomagnetic cell sorting–pushing the limits. Immunotechnology 4:89–96CrossRefGoogle Scholar
  25. Wang X, Gu H, Yang Z (2005) The heating effect of magnetic fluids in an alternating magnetic field. J Magn Magn Mater 293:334–340CrossRefADSGoogle Scholar
  26. Whitesides GM (2003) The ‘right’ size in nanobiotechnology. Nat Biotechnol 21:1161–1165CrossRefGoogle Scholar
  27. Wilhelm C, Gazeau F, Bacri JC (2002a) Magnetophoresis and ferromagnetic resonance of magnetically labeled cells. Eur Biophys J 31:118–125CrossRefGoogle Scholar
  28. Wilhelm C, Gazeau F, Roger J, Pons JN, Bacri JC (2002b) Interaction of anionic superparamagnetic nanoparticles with cells: kinetic analyses of membrane adsorption and subsequent internalization. Langmuir 18:8148–8155CrossRefGoogle Scholar
  29. Wilhelm C, Cebers A, Bacri JC, Gazeau F (2003) Deformation of intracellular endosomes under a magnetic field. Eur Biophys J 32:655–660CrossRefGoogle Scholar
  30. Zhang Y, Kohler N, Zhang M (2002) Surface modification of superparamagnetic magnetite nanoparticles and their intracellular uptake. Biomaterials 23:1553–1561CrossRefGoogle Scholar

Copyright information

© EBSA 2007

Authors and Affiliations

  • Jean-Paul Fortin
    • 1
  • Florence Gazeau
    • 1
  • Claire Wilhelm
    • 1
  1. 1.Laboratoire Matière et Systèmes Complexes, CNRS UMR 7057Université Paris 7ParisFrance

Personalised recommendations