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Journal of Nanomaterials
Volume 2017, Article ID 1564634, 13 pages
https://doi.org/10.1155/2017/1564634
Review Article

Mechanisms of Cellular Effects Directly Induced by Magnetic Nanoparticles under Magnetic Fields

1Beijing Key Laboratory of Bioelectromagnetism, Institute of Electrical Engineering, Chinese Academy of Sciences, Beijing, China
2University of Chinese Academy of Sciences, Beijing, China
3France-China Bio-Mineralization and Nano-Structures Laboratory, Beijing, China

Correspondence should be addressed to Tao Song; nc.ca.eei.liam@oatgnos

Received 13 February 2017; Revised 6 April 2017; Accepted 26 April 2017; Published 13 June 2017

Academic Editor: Paulo Cesar Morais

Copyright © 2017 Linjie Chen et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. A. Sobczak-Kupiec, J. Venkatesan, A. Alhathal AlAnezi et al., “Magnetic nanomaterials and sensors for biological detection,” Nanomedicine: Nanotechnology, Biology and Medicine, vol. 12, no. 8, pp. 2459–2473, 2016. View at Publisher · View at Google Scholar
  2. S. Behrens and I. Appel, “Magnetic nanocomposites,” Current Opinion in Biotechnology, vol. 39, pp. 89–96, 2016. View at Publisher · View at Google Scholar · View at Scopus
  3. X. Sun and S. Sun, “Preparation of magnetic nanoparticles for biomedical applications,” in Biomedical Nanotechnology, vol. 1570 of Methods in Molecular Biology, pp. 73–89, Springer New York, New York, NY, 2017. View at Publisher · View at Google Scholar
  4. K. Strojan, J. Lojk, V. B. Bregar, P. Veranič, and M. Pavlin, “Glutathione reduces cytotoxicity of polyethyleneimine coated magnetic nanoparticles in CHO cells,” Toxicology in Vitro, vol. 41, pp. 12–20, 2017. View at Publisher · View at Google Scholar
  5. S. Rana, N. G. Shetake, K. C. Barick, B. N. Pandey, H. G. Salunke, and P. A. Hassan, “Folic acid conjugated Fe,” Dalton Trans., vol. 45, no. 43, pp. 17401–17408, 2016. View at Publisher · View at Google Scholar
  6. K. H. Bae, M. Park, M. J. Do et al., “Chitosan oligosaccharide-stabilized ferrimagnetic iron oxide nanocubes for magnetically modulated cancer hyperthermia,” ACS Nano, vol. 6, no. 6, pp. 5266–5273, 2012. View at Publisher · View at Google Scholar · View at Scopus
  7. M. Creixell, A. C. Bohórquez, M. Torres-Lugo, and C. Rinaldi, “EGFR-targeted magnetic nanoparticle heaters kill cancer cells without a perceptible temperature rise,” ACS Nano, vol. 5, no. 9, pp. 7124–7129, 2011. View at Publisher · View at Google Scholar · View at Scopus
  8. Z. Wang, R. Qiao, N. Tang et al., “Active targeting theranostic iron oxide nanoparticles for MRI and magnetic resonance-guided focused ultrasound ablation of lung cancer,” Biomaterials, vol. 127, pp. 25–35, 2017. View at Publisher · View at Google Scholar
  9. H. Chen, L. Wang, Q. Yu et al., “Anti-HER2 antibody and ScFvEGFR-conjugated antifouling magnetic iron oxide nanoparticles for targeting and magnetic resonance imaging of breast cancer,” International Journal of Nanomedicine, vol. 8, pp. 3781–3794, 2013. View at Publisher · View at Google Scholar · View at Scopus
  10. R. P. Blakemore, “Magnetotactic bacteria,” Annual Review of Microbiology, vol. 36, pp. 217–238, 1982. View at Publisher · View at Google Scholar · View at Scopus
  11. D. A. Bazylinski and R. B. Frankel, “Magnetosome formation in prokaryotes,” Nature Reviews Microbiology, vol. 2, no. 3, pp. 217–230, 2004. View at Publisher · View at Google Scholar · View at Scopus
  12. R. B. Frankel and D. A. Bazylinski, “Magnetosomes and magneto-aerotaxis,” Contributions to Microbiology, vol. 16, pp. 182–193, 2009. View at Publisher · View at Google Scholar · View at Scopus
  13. R. Qiao, C. Yang, and M. Gao, “Erratum: superparamagnetic iron oxide nanoparticles: from preparations to in vivo MRI applications,” Journal of Materials Chemistry, vol. 19, no. 48, p. 9286, 2009. View at Google Scholar · View at Scopus
  14. T. Kubik, K. Bogunia-Kubik, and M. Sugisaka, “Nanotechnology on duty in medical applications,” Current Pharmaceutical Biotechnology, vol. 6, no. 1, pp. 17–33, 2005. View at Publisher · View at Google Scholar · View at Scopus
  15. Wahajuddin and S. Arora, “Superparamagnetic iron oxide nanoparticles: magnetic nanoplatforms as drug carriers,” International Journal of Nanomedicine, vol. 7, pp. 3445–3471, 2012. View at Publisher · View at Google Scholar
  16. Y. W. Chu, D. A. Engebretson, and J. R. Carey, “Bioconjugated magnetic nanoparticles for the detection of bacteria,” Journal of Biomedical Nanotechnology, vol. 9, no. 12, pp. 1951–1961, 2013. View at Publisher · View at Google Scholar · View at Scopus
  17. R. Ivkov, “Magnetic nanoparticle hyperthermia: a new frontier in biology and medicine?” International Journal of Hyperthermia, vol. 29, no. 8, pp. 703–705, 2013. View at Publisher · View at Google Scholar · View at Scopus
  18. A. Singh and S. K. Sahoo, “Magnetic nanoparticles: a novel platform for cancer theranostics,” Drug Discovery Today, vol. 19, no. 4, pp. 474–481, 2014. View at Publisher · View at Google Scholar · View at Scopus
  19. R. Hergt, S. Dutz, R. Müller, and M. Zeisberger, “Magnetic particle hyperthermia: nanoparticle magnetism and materials development for cancer therapy,” Journal of Physics Condensed Matter, vol. 18, no. 38, pp. S2919–S2934, 2006. View at Publisher · View at Google Scholar · View at Scopus
  20. N. J. Sniadecki, “A tiny touch: activation of cell signaling pathways with magnetic nanoparticles,” Endocrinology, vol. 151, no. 2, pp. 451–457, 2010. View at Publisher · View at Google Scholar · View at Scopus
  21. D. Kilinc, C. L. Dennis, and G. U. Lee, “Bio-nano-magnetic materials for localized mechanochemical stimulation of cell growth and death,” Advanced Materials, vol. 28, no. 27, pp. 5672–5680, 2016. View at Publisher · View at Google Scholar · View at Scopus
  22. G. Vallejo-Fernandez, O. Whear, A. G. Roca et al., “Mechanisms of hyperthermia in magnetic nanoparticles,” Journal of Physics D: Applied Physics, vol. 46, no. 31, Article ID 312001, 2013. View at Publisher · View at Google Scholar · View at Scopus
  23. A. E. Deatsch and B. A. Evans, “Heating efficiency in magnetic nanoparticle hyperthermia,” Journal of Magnetism and Magnetic Materials, vol. 354, pp. 163–172, 2014. View at Publisher · View at Google Scholar · View at Scopus
  24. Q. A. Pankhurst, J. Connolly, S. K. Jones, and J. Dobson, “Applications of magnetic nanoparticles in biomedicine,” Journal of Physics D: Applied Physics, vol. 36, no. 13, pp. R167–R181, 2003. View at Publisher · View at Google Scholar · View at Scopus
  25. M. Latorre and C. Rinaldi, “Applications of magnetic nanoparticles in medicine: magnetic fluid hyperthermia,” Puerto Rico Health Sciences Journal, vol. 28, no. 3, pp. 227–238, 2009. View at Google Scholar · View at Scopus
  26. A. Jordan, “Hyperthermia classic commentary: 'inductive heating of ferrimagnetic particles and magnetic fluids: physical evaluation of their potential for hyperthermia' by Andreas Jordan et al., International Journal of Hyperthermia, 1993;9:51–68,” International Journal of Hyperthermia, vol. 25, no. 7, pp. 512–516, 2009. View at Publisher · View at Google Scholar
  27. S. Dutz and R. Hergt, “Magnetic particle hyperthermia—a promising tumour therapy?” Nanotechnology, vol. 25, no. 45, Article ID 452001, 2014. View at Publisher · View at Google Scholar · View at Scopus
  28. F. K. Storm, H. W. Baker, E. F. Scanlon et al., “Magnetic‐induction hyperthermia. Results of a 5‐year multi‐institutional national cooperative trial in advanced cancer patients,” Cancer, vol. 55, no. 11, pp. 2677–2687, 1985. View at Publisher · View at Google Scholar · View at Scopus
  29. R. T. Pettigrew, C. M. Ludgate, and A. N. Smith, “Proceedings: The effect of whole body hyperthermia in advanced cancer,” British Journal of Cancer, vol. 30, no. 2, p. 179, 1974. View at Publisher · View at Google Scholar · View at Scopus
  30. T. Sadhukha, L. Niu, T. S. Wiedmann, and J. Panyam, “Effective elimination of cancer stem cells by magnetic hyperthermia,” Molecular Pharmaceutics, vol. 10, no. 4, pp. 1432–1441, 2013. View at Publisher · View at Google Scholar · View at Scopus
  31. S. Balivada, R. S. Rachakatla, H. Wang et al., “A/C magnetic hyperthermia of melanoma mediated by iron(0)/iron oxide core/shell magnetic nanoparticles: a mouse study,” BMC Cancer, vol. 10, article 119, 2010. View at Publisher · View at Google Scholar · View at Scopus
  32. S. Ota, N. Yamazaki, A. Tomitaka, T. Yamada, and Y. Takemura, “Hyperthermia using antibody-conjugated magnetic nanoparticles and its enhanced effect with cryptotanshinone,” Nanomaterials, vol. 4, no. 2, pp. 319–330, 2014. View at Publisher · View at Google Scholar
  33. T. Kikumori, T. Kobayashi, M. Sawaki, and T. Imai, “Anti-cancer effect of hyperthermia on breast cancer by magnetite nanoparticle-loaded anti-HER2 immunoliposomes,” Breast Cancer Research and Treatment, vol. 113, no. 3, pp. 435–441, 2009. View at Publisher · View at Google Scholar · View at Scopus
  34. A. Chalkidou, K. Simeonidis, M. Angelakeris et al., “In vitro application of Fe/MgO nanoparticles as magnetically mediated hyperthermia agents for cancer treatment,” Journal of Magnetism and Magnetic Materials, vol. 323, no. 6, pp. 775–780, 2011. View at Publisher · View at Google Scholar · View at Scopus
  35. H. L. Rodríguez-Luccioni, M. Latorre-Esteves, J. Méndez-Vega et al., “Enhanced reduction in cell viability by hyperthermia induced by magnetic nanoparticles,” International Journal of Nanomedicine, vol. 6, pp. 373–380, 2011. View at Google Scholar · View at Scopus
  36. R. Ghosh, L. Pradhan, Y. P. Devi et al., “Induction heating studies of Fe3O4 magnetic nanoparticles capped with oleic acid and polyethylene glycol for hyperthermia,” Journal of Materials Chemistry, vol. 21, no. 35, pp. 13388–13398, 2011. View at Publisher · View at Google Scholar · View at Scopus
  37. G. Wang, D. Xu, Q. Chai et al., “Magnetic fluid hyperthermia inhibits the growth of breast carcinoma and downregulates vascular endothelial growth factor expression,” Oncology Letters, vol. 7, no. 5, pp. 1370–1374, 2014. View at Publisher · View at Google Scholar · View at Scopus
  38. Y. Du, D. Zhang, H. Liu, and R. Lai, “Thermochemotherapy effect of nanosized As2O3/Fe3O4 complex on experimental mouse tumors and its influence on the expression of CD44v6, VEGF-C and MMP-9,” BMC Biotechnology, vol. 9, article no. 1472, p. 84, 2009. View at Publisher · View at Google Scholar · View at Scopus
  39. J.-H. Lee, J.-T. Jang, J.-S. Choi et al., “Exchange-coupled magnetic nanoparticles for efficient heat induction,” Nature Nanotechnology, vol. 6, no. 7, pp. 418–422, 2011. View at Publisher · View at Google Scholar · View at Scopus
  40. D. Cheng, X. Li, G. Zhang, and H. Shi, “Morphological effect of oscillating magnetic nanoparticles in killing tumor cells,” Nanoscale Research Letters, vol. 9, no. 1, pp. 1–8, 2014. View at Publisher · View at Google Scholar · View at Scopus
  41. E. Zhang, M. F. Kircher, M. Koch, L. Eliasson, S. N. Goldberg, and E. Renström, “Dynamic magnetic fields remote-control apoptosis via nanoparticle rotation,” ACS Nano, vol. 8, no. 4, pp. 3192–3201, 2014. View at Publisher · View at Google Scholar · View at Scopus
  42. D.-H. Kim, E. A. Rozhkova, I. V. Ulasov et al., “Biofunctionalized magnetic-vortex microdiscs for targeted cancer-cell destruction,” Nature Materials, vol. 9, no. 2, pp. 165–171, 2010. View at Publisher · View at Google Scholar · View at Scopus
  43. Y. Cheng, M. E. Muroski, D. C. M. C. Petit et al., “Rotating magnetic field induced oscillation of magnetic particles for in vivo mechanical destruction of malignant glioma,” Journal of Controlled Release, vol. 223, pp. 75–84, 2016. View at Publisher · View at Google Scholar · View at Scopus
  44. C. Chen, L. Chen, P. Wang, L. Wu, and T. Song, “Magnetically-induced elimination of Staphylococcus aureus by magnetotactic bacteria under a swing magnetic field,” Nanomedicine: Nanotechnology, Biology and Medicine, vol. 13, no. 2, pp. 363–370, 2017. View at Publisher · View at Google Scholar
  45. S. Hughes, S. McBain, J. Dobson, and A. J. El Haj, “Selective activation of mechanosensitive ion channels using magnetic particles,” Journal of the Royal Society Interface, vol. 5, no. 25, pp. 855–863, 2008. View at Publisher · View at Google Scholar · View at Scopus
  46. J.-H. Lee, J.-W. Kim, M. Levy et al., “Magnetic nanoparticles for ultrafast mechanical control of inner ear hair cells,” ACS Nano, vol. 8, no. 7, pp. 6590–6598, 2014. View at Publisher · View at Google Scholar · View at Scopus
  47. A. Tay, A. Kunze, C. Murray, and D. Di Carlo, “Induction of calcium influx in cortical neural networks by nanomagnetic forces,” ACS Nano, vol. 10, no. 2, pp. 2331–2341, 2016. View at Publisher · View at Google Scholar · View at Scopus
  48. N. Wang, J. P. Butler, and D. E. Ingber, “Mechanotransduction across the cell surface and through the cytoskeleton,” Science, vol. 260, no. 5111, pp. 1124–1127, 1993. View at Publisher · View at Google Scholar · View at Scopus
  49. F. Chowdhury, S. Na, D. Li et al., “Material properties of the cell dictate stress-induced spreading and differentiation in embryonic stem cells,” Nature Materials, vol. 9, pp. 82–88, 2010. View at Publisher · View at Google Scholar · View at Scopus
  50. M. H. Cho, E. J. Lee, M. Son et al., “A magnetic switch for the control of cell death signalling in in vitro and in vivo systems,” Nature Materials, vol. 11, no. 12, pp. 1038–1043, 2012. View at Publisher · View at Google Scholar · View at Scopus
  51. K. Perica, A. Tu, A. Richter, J. G. Bieler, M. Edidin, and J. P. Schneck, “Magnetic field-induced t cell receptor clustering by nanoparticles enhances t cell activation and stimulates antitumor activity,” ACS Nano, vol. 8, no. 3, pp. 2252–2260, 2014. View at Publisher · View at Google Scholar · View at Scopus
  52. J. Lee, E. Kim, M. Cho et al., “Artificial control of cell signaling and growth by magnetic nanoparticles,” Angewandte Chemie, vol. 122, no. 33, pp. 5834–5838, 2010. View at Publisher · View at Google Scholar
  53. R. J. Mannix, S. Kumar, F. Cassiola et al., “Nanomagnetic actuation of receptor-mediated signal transduction,” Nature Nanotechnology, vol. 3, no. 1, pp. 36–40, 2008. View at Publisher · View at Google Scholar · View at Scopus
  54. K. Maier-Hauff, R. Rothe, R. Scholz et al., “Intracranial thermotherapy using magnetic nanoparticles combined with external beam radiotherapy: results of a feasibility study on patients with glioblastoma multiforme,” Journal of Neuro-Oncology, vol. 81, no. 1, pp. 53–60, 2007. View at Publisher · View at Google Scholar · View at Scopus
  55. K. Maier-Hauff, F. Ulrich, D. Nestler et al., “Efficacy and safety of intratumoral thermotherapy using magnetic iron-oxide nanoparticles combined with external beam radiotherapy on patients with recurrent glioblastoma multiforme,” Journal of Neuro-Oncology, vol. 103, no. 2, pp. 317–324, 2011. View at Publisher · View at Google Scholar · View at Scopus
  56. M. Johannsen, U. Gneveckow, L. Eckelt et al., “Clinical hyperthermia of prostate cancer using magnetic nanoparticles: presentation of a new interstitial technique,” International Journal of Hyperthermia, vol. 21, no. 7, pp. 637–647, 2005. View at Publisher · View at Google Scholar · View at Scopus
  57. M.-H. Kim, I. Yamayoshi, S. Mathew, H. Lin, J. Nayfach, and S. I. Simon, “Magnetic nanoparticle targeted hyperthermia of cutaneous Staphylococcus aureus infection,” Annals of Biomedical Engineering, vol. 41, no. 3, pp. 598–609, 2013. View at Publisher · View at Google Scholar · View at Scopus
  58. D. Rodrigues, M. Bañobre-López, B. Espiña, J. Rivas, and J. Azeredo, “Effect of magnetic hyperthermia on the structure of biofilm and cellular viability of a food spoilage bacterium,” Biofouling, vol. 29, no. 10, pp. 1225–1232, 2013. View at Publisher · View at Google Scholar · View at Scopus
  59. R. Hergt, R. Hiergeist, M. Zeisberger et al., “Magnetic properties of bacterial magnetosomes as potential diagnostic and therapeutic tools,” Journal of Magnetism and Magnetic Materials, vol. 293, no. 1, pp. 80–86, 2005. View at Publisher · View at Google Scholar · View at Scopus
  60. R.-T. Liu, J. Liu, J.-Q. Tong et al., “Heating effect and biocompatibility of bacterial magnetosomes as potential materials used in magnetic fluid hyperthermia,” Progress in Natural Science: Materials International, vol. 22, no. 1, pp. 31–39, 2012. View at Publisher · View at Google Scholar · View at Scopus
  61. S. Mannucci, L. Ghin, G. Conti et al., “Magnetic nanoparticles from Magnetospirillum gryphiswaldense increase the efficacy of thermotherapy in a model of Colon Carcinoma,” PLoS ONE, vol. 9, no. 10, Article ID 0108959, 2014. View at Publisher · View at Google Scholar · View at Scopus
  62. E. Alphandéry, S. Faure, O. Seksek, F. Guyot, and I. Chebbi, “Chains of magnetosomes extracted from AMB-1 magnetotactic bacteria for application in alternative magnetic field cancer therapy,” ACS Nano, vol. 5, no. 8, pp. 6279–6296, 2011. View at Publisher · View at Google Scholar · View at Scopus
  63. E. Alphandéry, F. Guyot, and I. Chebbi, “Preparation of chains of magnetosomes, isolated from Magnetospirillum magneticum strain AMB-1 magnetotactic bacteria, yielding efficient treatment of tumors using magnetic hyperthermia,” International Journal of Pharmaceutics, vol. 434, no. 1-2, pp. 444–452, 2012. View at Publisher · View at Google Scholar · View at Scopus
  64. C. Chen, L. Chen, Y. Yi, C. Chen, L.-F. Wu, and T. Song, “Killing of Staphylococcus aureus via magnetic hyperthermia mediated by magnetotactic bacteria,” Applied and Environmental Microbiology, vol. 82, no. 7, pp. 2219–2226, 2016. View at Publisher · View at Google Scholar · View at Scopus
  65. R. Yang, Q. Tang, F. Miao et al., “Inhibition of heat-shock protein 90 sensitizes liver cancer stem-like cells to magnetic hyperthermia and enhances anti-tumor effect on hepatocellular carcinoma-burdened nude mice,” International Journal of Nanomedicine, vol. 10, pp. 7345–7358, 2015. View at Publisher · View at Google Scholar · View at Scopus
  66. K. A. Court, H. Hatakeyama, S. Y. Wu et al., “HSP70 inhibition synergistically enhances the effects of magnetic fluid hyperthermia in ovarian cancer,” Molecular Cancer Therapeutics, vol. 16, no. 5, pp. 966–976, 2017. View at Publisher · View at Google Scholar
  67. R. Hergt and S. Dutz, “Magnetic particle hyperthermia—biophysical limitations of a visionary tumour therapy,” Journal of Magnetism and Magnetic Materials, vol. 311, no. 1, pp. 187–192, 2007. View at Publisher · View at Google Scholar · View at Scopus
  68. C. Sanchez, D. El Hajj Diab, V. Connord et al., “Targeting a G-protein-coupled receptor overexpressed in endocrine tumors by magnetic nanoparticles to induce cell death,” ACS Nano, vol. 8, no. 2, pp. 1350–1363, 2014. View at Publisher · View at Google Scholar · View at Scopus
  69. L. Asín, M. R. Ibarra, A. Tres, and G. F. Goya, “Controlled cell death by magnetic hyperthermia: Effects of exposure time, field amplitude, and nanoparticle concentration,” Pharmaceutical Research, vol. 29, no. 5, pp. 1319–1327, 2012. View at Publisher · View at Google Scholar · View at Scopus
  70. M. Domenech, I. Marrero-Berrios, M. Torres-Lugo, and C. Rinaldi, “Lysosomal membrane permeabilization by targeted magnetic nanoparticles in alternating magnetic fields,” ACS Nano, vol. 7, no. 6, pp. 5091–5101, 2013. View at Publisher · View at Google Scholar · View at Scopus
  71. A. Villanueva, P. De La Presa, J. M. Alonso et al., “Hyperthermia hela cell treatment with silica-coated manganese oxide nanoparticles,” Journal of Physical Chemistry C, vol. 114, no. 5, pp. 1976–1981, 2010. View at Publisher · View at Google Scholar · View at Scopus
  72. V. Grazú, A. M. Silber, M. Moros et al., “Application of magnetically induced hyperthermia in the model protozoan Crithidia fasciculata as a potential therapy against parasitic infections,” International Journal of Nanomedicine, vol. 7, pp. 5351–5360, 2012. View at Publisher · View at Google Scholar · View at Scopus
  73. A. Riedinger, P. Guardia, A. Curcio et al., “Subnanometer local temperature probing and remotely controlled drug release based on Azo-functionalized iron oxide nanoparticles,” Nano Letters, vol. 13, no. 6, pp. 2399–2406, 2013. View at Publisher · View at Google Scholar · View at Scopus
  74. J. T. Dias, M. Moros, P. Del Pino, S. Rivera, V. Grazú, and J. M. De La Fuente, “DNA as a molecular local thermal probe for the analysis of magnetic hyperthermia,” Angewandte Chemie - International Edition, vol. 52, no. 44, pp. 11526–11529, 2013. View at Publisher · View at Google Scholar · View at Scopus
  75. H. Huang, S. Delikanli, H. Zeng, D. M. Ferkey, and A. Pralle, “Remote control of ion channels and neurons through magnetic-field heating of nanoparticles,” Nature Nanotechnology, vol. 5, no. 8, pp. 602–606, 2010. View at Publisher · View at Google Scholar · View at Scopus
  76. R. Chen, G. Romero, M. G. Christiansen, A. Mohr, and P. Anikeeva, “Wireless magnetothermal deep brain stimulation,” Science, vol. 347, no. 6229, pp. 1477–1480, 2015. View at Publisher · View at Google Scholar · View at Scopus
  77. S. A. Stanley, J. E. Gagner, S. Damanpour, M. Yoshida, J. S. Dordick, and J. M. Friedman, “Radio-wave heating of iron oxide nanoparticles can regulate plasma glucose in mice,” Science, vol. 336, no. 6081, pp. 604–608, 2012. View at Publisher · View at Google Scholar · View at Scopus
  78. S. A. Stanley, J. Sauer, R. S. Kane, J. S. Dordick, and J. M. Friedman, “Remote regulation of glucose homeostasis in mice using genetically encoded nanoparticles,” Nature Medicine, vol. 21, no. 1, pp. 92–98, 2015. View at Publisher · View at Google Scholar · View at Scopus
  79. S. A. Stanley, L. Kelly, K. N. Latcha et al., “Bidirectional electromagnetic control of the hypothalamus regulates feeding and metabolism,” Nature, vol. 531, no. 7596, pp. 647–650, 2016. View at Publisher · View at Google Scholar · View at Scopus
  80. A. Gupta, R. S. Kane, and D.-A. Borca-Tasciuc, “Local temperature measurement in the vicinity of electromagnetically heated magnetite and gold nanoparticles,” Journal of Applied Physics, vol. 108, no. 6, Article ID 064901, 2010. View at Publisher · View at Google Scholar · View at Scopus
  81. R. Hergt, W. Andrae, C. G. d'Ambly et al., “Physical limits of hyperthermia using magnetite fine particles,” IEEE Transactions on Magnetics, vol. 34, no. 5, pp. 3745–3754, 1998. View at Publisher · View at Google Scholar · View at Scopus
  82. P. Keblinski, D. G. Cahill, A. Bodapati, C. R. Sullivan, and T. A. Taton, “Limits of localized heating by electromagnetically excited nanoparticles,” Journal of Applied Physics, vol. 100, no. 5, Article ID 054305, 2006. View at Publisher · View at Google Scholar · View at Scopus
  83. M. Meister, “Physical limits to magnetogenetics,” eLife, vol. 5, 2016. View at Publisher · View at Google Scholar
  84. C. L. Dennis and R. Ivkov, “Physics of heat generation using magnetic nanoparticles for hyperthermia,” International Journal of Hyperthermia, vol. 29, no. 8, pp. 715–729, 2013. View at Publisher · View at Google Scholar · View at Scopus
  85. J. Carrey, V. Connord, and M. Respaud, “Ultrasound generation and high-frequency motion of magnetic nanoparticles in an alternating magnetic field: toward intracellular ultrasound therapy?” Applied Physics Letters, vol. 102, no. 23, Article ID 232404, 2013. View at Publisher · View at Google Scholar · View at Scopus
  86. T. Saliev, L. B. Feril Jr., K. Ogawa et al., “Induction of apoptosis in U937 cells by using a combination of bortezomib and low-intensity ultrasound,” Medical Science Monitor, vol. 22, pp. 5049–5057, 2016. View at Publisher · View at Google Scholar
  87. M. Ivone, C. Pappalettere, A. Watanabe, and K. Tachibana, “Study of cellular response induced by low intensity ultrasound frequency sweep pattern on myelomonocytic lymphoma U937 cells,” Journal of Ultrasound, vol. 19, no. 3, pp. 167–174, 2016. View at Publisher · View at Google Scholar
  88. N. Hallali, P. Clerc, D. Fourmy, V. Gigoux, and J. Carrey, “Influence on cell death of high frequency motion of magnetic nanoparticles during magnetic hyperthermia experiments,” Applied Physics Letters, vol. 109, no. 3, Article ID 032402, 2016. View at Publisher · View at Google Scholar · View at Scopus
  89. T. Yue, X. Zhang, and F. Huang, “Molecular modeling of membrane responses to the adsorption of rotating nanoparticles: promoted cell uptake and mechanical membrane rupture,” Soft Matter, vol. 11, no. 3, pp. 456–465, 2015. View at Publisher · View at Google Scholar · View at Scopus
  90. S. Bulut, W. M. Waites, and J. R. Mitchell, “Effects of combined shear and thermal forces on destruction of Microbacterium lacticum,” Applied and Environmental Microbiology, vol. 65, no. 10, pp. 4464–4469, 1999. View at Google Scholar · View at Scopus
  91. S. Sahoo, K. K. Rao, and G. K. Suraishkumar, “Reactive oxygen species induced by shear stress mediate cell death in Bacillus subtilis,” Biotechnology and Bioengineering, vol. 94, no. 1, pp. 118–127, 2006. View at Publisher · View at Google Scholar · View at Scopus
  92. X. Long, J. Ye, D. Zhao, and S.-J. Zhang, “Magnetogenetics: remote non-invasive magnetic activation of neuronal activity with a magnetoreceptor,” Science Bulletin, vol. 60, no. 24, pp. 2107–2119, 2015. View at Publisher · View at Google Scholar · View at Scopus
  93. M. A. Wheeler, C. J. Smith, M. Ottolini et al., “Genetically targeted magnetic control of the nervous system,” Nature Neuroscience, vol. 19, no. 5, pp. 756–761, 2016. View at Publisher · View at Google Scholar · View at Scopus
  94. M. Bernardini, A. Fiorio Pla, N. Prevarskaya, and D. Gkika, “Human transient receptor potential (TRP) channels expression profiling in carcinogenesis,” International Journal of Developmental Biology, vol. 59, no. 7-9, pp. 399–406, 2015. View at Publisher · View at Google Scholar · View at Scopus
  95. A. Kondratskyi, K. Kondratska, R. Skryma, and N. Prevarskaya, “Ion channels in the regulation of apoptosis,” Biochimica et Biophysica Acta - Biomembranes, vol. 1848, no. 10, pp. 2532–2546, 2015. View at Publisher · View at Google Scholar · View at Scopus
  96. K. Kunzelmann, “Ion channels in regulated cell death,” Cellular and Molecular Life Sciences, vol. 73, no. 11-12, pp. 2387–2403, 2016. View at Publisher · View at Google Scholar · View at Scopus
  97. S. Dwivedi, M. A. Siddiqui, N. N. Farshori, M. Ahamed, J. Musarrat, and A. A. Al-Khedhairy, “Synthesis, characterization and toxicological evaluation of iron oxide nanoparticles in human lung alveolar epithelial cells,” Colloids and Surfaces B: Biointerfaces, vol. 122, pp. 209–215, 2014. View at Publisher · View at Google Scholar · View at Scopus
  98. P. Wang, C. Chen, K. Zeng, W. Pan, and T. Song, “Magnetic nanoparticles trigger cell proliferation arrest of neuro-2a cells and ROS-mediated endoplasmic reticulum stress response,” Journal of Nanoparticle Research, vol. 16, no. 11, 2014. View at Publisher · View at Google Scholar · View at Scopus
  99. S. Naqvi, M. Samim, M. Z. Abdin et al., “Concentration-dependent toxicity of iron oxide nanoparticles mediated by increased oxidative stress,” International Journal of Nanomedicine, vol. 5, no. 1, pp. 983–989, 2010. View at Publisher · View at Google Scholar · View at Scopus
  100. L. Gao, J. Zhuang, L. Nie et al., “Intrinsic peroxidase-like activity of ferromagnetic nanoparticles,” Nature Nanotechnology, vol. 2, no. 9, pp. 577–583, 2007. View at Publisher · View at Google Scholar · View at Scopus
  101. Z. Chen, J.-J. Yin, Y.-T. Zhou et al., “Dual enzyme-like activities of iron oxide nanoparticles and their implication for diminishing cytotoxicity,” ACS Nano, vol. 6, no. 5, pp. 4001–4012, 2012. View at Publisher · View at Google Scholar · View at Scopus
  102. D.-M. Huang, J.-K. Hsiao, Y.-C. Chen et al., “The promotion of human mesenchymal stem cell proliferation by superparamagnetic iron oxide nanoparticles,” Biomaterials, vol. 30, no. 22, pp. 3645–3651, 2009. View at Publisher · View at Google Scholar · View at Scopus
  103. M. Yu, S. Huang, K. J. Yu, and A. M. Clyne, “Dextran and polymer polyethylene glycol (PEG) coating reduce both 5 and 30 nm iron oxide nanoparticle cytotoxicity in 2D and 3D cell culture,” International Journal of Molecular Sciences, vol. 13, no. 5, pp. 5554–5570, 2012. View at Publisher · View at Google Scholar · View at Scopus
  104. V. Connord, P. Clerc, N. Hallali et al., “Real-time analysis of magnetic hyperthermia experiments on living cells under a confocal microscope,” Small, vol. 11, no. 20, pp. 2437–2445, 2015. View at Publisher · View at Google Scholar · View at Scopus
  105. J.-E. Bae, M.-I. Huh, B.-K. Ryu et al., “The effect of static magnetic fields on the aggregation and cytotoxicity of magnetic nanoparticles,” Biomaterials, vol. 32, no. 35, pp. 9401–9414, 2011. View at Publisher · View at Google Scholar · View at Scopus
  106. H. L. Jia, C. Wang, Y. Li et al., “Combined effects of 50 Hz magnetic field and magnetic nanoparticles on the proliferation and apoptosis of PC12 cells,” Biomedical and Environmental Sciences, vol. 27, no. 2, pp. 97–105, 2014. View at Publisher · View at Google Scholar · View at Scopus
  107. A. Pal, A. Singh, T. C. Nag, P. Chattopadhyay, R. Mathur, and S. Jain, “Iron oxide nanoparticles and magnetic field exposure promote functional recovery by attenuating free radical-induced damage in rats with spinal cord transection,” International Journal of Nanomedicine, vol. 8, pp. 2259–2272, 2013. View at Publisher · View at Google Scholar · View at Scopus
  108. J. Shin, C.-H. Yoo, J. Lee, and M. Cha, “Cell response induced by internalized bacterial magnetic nanoparticles under an external static magnetic field,” Biomaterials, vol. 33, no. 22, pp. 5650–5657, 2012. View at Publisher · View at Google Scholar · View at Scopus
  109. R. J. Wydra, C. E. Oliver, K. W. Anderson, T. D. Dziubla, and J. Z. Hilt, “Accelerated generation of free radicals by iron oxide nanoparticles in the presence of an alternating magnetic field,” RSC Advances, vol. 5, no. 24, pp. 18888–18893, 2015. View at Publisher · View at Google Scholar · View at Scopus
  110. V. Binhi, “Do naturally occurring magnetic nanoparticles in the human body mediate increased risk of childhood leukaemia with EMF exposure?” International Journal of Radiation Biology, vol. 84, no. 7, pp. 569–579, 2008. View at Publisher · View at Google Scholar · View at Scopus
  111. V. N. Binhi and D. S. Chernavskii, “Stochastic dynamics of magnetosomes in cytoskeleton,” Europhysics Letters, vol. 70, no. 6, pp. 850–856, 2005. View at Publisher · View at Google Scholar · View at Scopus
  112. R. D. Montoya, “Magnetic fields, radicals and cellular activity,” Electromagnetic Biology and Medicine, pp. 1–12, 2016. View at Publisher · View at Google Scholar
  113. Q. L. Zhao, Y. Fujiwara, and T. Kondo, “Mechanism of cell death induction by nitroxide and hyperthermia,” Free Radical Biology & Medicine, vol. 40, no. 7, pp. 1131–1143, 2006. View at Publisher · View at Google Scholar
  114. T. Yoshikawa, S. Kokura, K. Tainaka et al., “The role of active oxygen species and lipid peroxidation in the antitumor effect of hyperthermi,” Cancer Research, vol. 53, no. 10, pp. 2326–2329, 1993. View at Google Scholar · View at Scopus