Physical and Cellular Basis of Oncologic Magnetic Thermotherapy
Fiorela Ghilini, Mariana Tasso and Marcela. B. Fernández van Raap
Magnetic thermotherapy (MT) for treating solid tumors employs magnetic hyperthermia (MH) protocols. Superparamagnetic iron oxide nanoparticles -nowadays considered nanomedicines- are delivered to the tumor to induce temperature elevations upon the application of an external alternating magnetic field in the radiofrequency range. This treatment activates cell death pathways and sensitizes cells to other cancer therapies. Much information is available on magnetic materials preparation and functionalization, physical relaxation mechanisms behind magnetic heating, and designed devices for field generation and magnetic material tracking, but further insight is still needed about the nature and characteristics of the cellular response to MH. In this chapter, the physical foundations of MT are thoroughly discussed and complemented by a general overview of the cellular responses induced to counteract the various sources of stress associated with this technology.
Keywords
Magnetic Hyperthermia, Superparamagnetic Iron Oxide Nanoparticles, Nanomedicines, Cell-Nanoparticle Interactions, Cell Response to Heat Shock, Heat Shock Proteins
Published online , 39 pages
Citation: Fiorela Ghilini, Mariana Tasso and Marcela. B. Fernández van Raap, Physical and Cellular Basis of Oncologic Magnetic Thermotherapy, Materials Research Foundations, Vol. 143, pp 102-139, 2023
DOI: https://doi.org/10.21741/9781644902332-4
Part of the book on Magnetic Nanoparticles for Biomedical Applications
References
[1] M. C. Garnett and P. Kallinteri, Occupational Medicine 56, 307 (2006). https://doi.org/10.1093/occmed/kql052
[2] Q. A. Pankhurst, J. Connolly, S. K. Jones, and J. Dobson, J. Phys. D: Appl. Phys 36, 167 (2003). https://doi.org/10.1088/0022-3727/36/13/201
[3] R. Banerjee, Y. Katsenovich, L. Lagos, M. Mciintosh, X. Zhang, and C.-Z. Li, Current Medicinal Chemistry 17, 3120 (2010). https://doi.org/10.2174/092986710791959765
[4] K. Wu, D. Su, J. Liu, R. Saha, and J. P. Wang, Nanotechnology 30, 502003 (2019). https://doi.org/10.1088/1361-6528/ab4241
[5] H. Kang, S. Hu, M. H. Cho, S. H. Hong, Y. Choi, and H. S. Choi, Nano Today 23, 59 (2018). https://doi.org/10.1016/j.nantod.2018.11.001
[6] I. Rubia-Rodríguez, A. Santana-Otero, S. Spassov, E. Tombácz, C. Johansson, P. de La Presa, F. J. Teran, M. del P. Morales, S. Veintemillas-Verdaguer, N. T. K. Thanh, M. O. Besenhard, C. Wilhelm, F. Gazeau, Q. Harmer, E. Mayes, B. B. Manshian, S. J. Soenen, Y. Gu, Á. Millán, E. K. Efthimiadou, J. Gaudet, P. Goodwill, J. Mansfield, U. Steinhoff, J. Wells, F. Wiekhorst, and D. Ortega, Materials 14, 706 (2021). https://doi.org/10.3390/ma14040706
[7] Z. Zhou, Z. Shen, and X. Chen, ACS Nano 14, 7 (2020). https://doi.org/10.1021/acsnano.9b06842
[8] P. A. Soto, M. Vence, G. M. Piñero, D. F. Coral, V. Usach, D. Muraca, A. Cueto, A. Roig, M. B. F. van Raap, and C. P. Setton-Avruj, Acta Biomaterialia 130, 234 (2021). https://doi.org/10.1016/j.actbio.2021.05.050
[9] M. E. de Sousa, M. B. Fernández van Raap, P. C. Rivas, P. Mendoza Zélis, P. Girardin, G. A. Pasquevich, J. L. Alessandrini, D. Muraca, and F. H. Sánchez, The Journal of Physical Chemistry C 117, 5436 (2013). https://doi.org/10.1021/jp311556b
[10] W. Cai and J. Wan, Journal of Colloid and Interface Science 305, 366 (2007). https://doi.org/10.1016/j.jcis.2006.10.023
[11] J. G. Ovejero, F. Spizzo, M. P. Morales, and L. del Bianco, Materials 14, 6416 (2021). https://doi.org/10.3390/ma14216416
[12] G. Cotin, C. Kiefer, F. Perton, D. Ihiawakrim, C. Blanco-Andujar, S. Moldovan, C. Lefevre, O. Ersen, B. Pichon, D. Mertz, and S. Bégin-Colin, Nanomaterials 8, 881 (2018). https://doi.org/10.3390/nano8110881
[13] P. M. Zélis, G. A. Pasquevich, S. J. Stewart, M. B. F. van Raap, J. Aphesteguy, I. J. Bruvera, C. Laborde, B. Pianciola, S. Jacobo, and F. H. Sánchez, Journal of Physics D: Applied Physics 46, 125006 (2013). https://doi.org/10.1088/0022-3727/46/12/125006
[14] A. Makridis, K. Topouridou, M. Tziomaki, D. Sakellari, K. Simeonidis, M. Angelakeris, M. P. Yavropoulou, J. G. Yovos, and O. Kalogirou, J. Mater. Chem. B 2, 8390 (2014). https://doi.org/10.1039/C4TB01017E
[15] Q. Lu, X. Dai, P. Zhang, X. Tan, Y. Zhong, C. Yao, M. Song, G. Song, Z. Zhang, G. Peng, Z. Guo, Y. Ge, K. Zhang, and Y. Li, International Journal of Nanomedicine Volume 13, 2491 (2018). https://doi.org/10.2147/IJN.S157935
[16] C. Caro, F. Gámez, P. Quaresma, J. M. Páez-Muñoz, A. Domínguez, J. R. Pearson, M. Pernía Leal, A. M. Beltrán, Y. Fernandez-Afonso, J. M. de la Fuente, R. Franco, E. Pereira, and M. L. García-Martín, Pharmaceutics 13, 416 (2021). https://doi.org/10.3390/pharmaceutics13030416
[17] K. Dukenbayev, I. Korolkov, D. Tishkevich, A. Kozlovskiy, S. Trukhanov, Y. Gorin, E. Shumskaya, E. Kaniukov, D. Vinnik, M. Zdorovets, M. Anisovich, A. Trukhanov, D. Tosi, and C. Molardi, Nanomaterials 9, 494 (2019). https://doi.org/10.3390/nano9040494
[18] V. Torresan, A. Guadagnini, D. Badocco, P. Pastore, G. A. Muñoz Medina, M. B. Fernàndez van Raap, I. Postuma, S. Bortolussi, M. Bekić, M. Čolić, M. Gerosa, A. Busato, P. Marzola, and V. Amendola, Advanced Healthcare Materials 10, 2001632 (2021). https://doi.org/10.1002/adhm.202001632
[19] M. Auffan, J. Rose, J.-Y. Bottero, G. v. Lowry, J.-P. Jolivet, and M. R. Wiesner, Nature Nanotechnology 4, 634 (2009). https://doi.org/10.1038/nnano.2009.242
[20] A. Pietroiusti, L. Campagnolo, and B. Fadeel, Small 9, 1557 (2013). https://doi.org/10.1002/smll.201201463
[21] N. Oh and J. H. Park, International Journal of Nanomedicine 9, 51 (2014). https://doi.org/10.2147/IJN.S26592
[22] A. A. Shvedova, V. E. Kagan, and B. Fadeel, Annual Review of Pharmacology and Toxicology 50, 63 (2010). https://doi.org/10.1146/annurev.pharmtox.010909.105819
[23] N. Oh and J. H. Park, International Journal of Nanomedicine 9, 51 (2014). https://doi.org/10.2147/IJN.S26592
[24] S. C. Sahu and A. W. Hayes, Toxicology Research and Application 1, 239784731772635 (2017). https://doi.org/10.1177/2397847317726352
[25] T. Xia, N. Li, and A. E. Nel, Annual Review of Public Health 30, 137 (2009). https://doi.org/10.1146/annurev.publhealth.031308.100155
[26] G. Oberdörster, Z. Sharp, V. Atudorei, A. Elder, R. Gelein, W. Kreyling, and C. Cox, Inhalation Toxicology 16, 437 (2004). https://doi.org/10.1080/08958370490439597
[27] V. Torresan, D. Forrer, A. Guadagnini, D. Badocco, P. Pastore, M. Casarin, A. Selloni, D. Coral, M. Ceolin, M. B. Fernández van Raap, A. Busato, P. Marzola, A. E. Spinelli, and V. Amendola, ACS Nano 14, 12840 (2020). https://doi.org/10.1021/acsnano.0c03614
[28] C. Buzea, I. I. Pacheco, and K. Robbie, Biointerphases 2, MR17 (2007). https://doi.org/10.1116/1.2815690
[29] V. de Matteis, Toxics 5, 29 (2017). https://doi.org/10.3390/toxics5040029
[30] H. Arami, A. Khandhar, D. Liggitt, and K. M. Krishnan, Chemical Society Reviews 44, 8576 (2015). https://doi.org/10.1039/C5CS00541H
[31] D. A. Hume, K. M. Irvine, and C. Pridans, Trends in Immunology 40, 98 (2019). https://doi.org/10.1016/j.it.2018.11.007
[32] A. Chow, B. D. Brown, and M. Merad, Nature Reviews Immunology 11, 788 (2011). https://doi.org/10.1038/nri3087
[33] W. Poon, Y.-N. Zhang, B. Ouyang, B. R. Kingston, J. L. Y. Wu, S. Wilhelm, and W. C. W. Chan, ACS Nano 13, 5785 (2019). https://doi.org/10.1021/acsnano.9b01383
[34] R. Gref, Y. Minamitake, M. T. Peracchia, V. Trubetskoy, V. Torchilin, and R. Langer, Science 263, 1600 (1994). https://doi.org/10.1126/science.8128245
[35] H. Soo Choi, W. Liu, P. Misra, E. Tanaka, J. P. Zimmer, B. Itty Ipe, M. G. Bawendi, and J. V. Frangioni, Nature Biotechnology 25, 1165 (2007). https://doi.org/10.1038/nbt1340
[36] H. H. Gustafson, D. Holt-Casper, D. W. Grainger, and H. Ghandehari, Nano Today 10, 487 (2015). https://doi.org/10.1016/j.nantod.2015.06.006
[37] D. E. Owens III and N. A. Peppas, International Journal of Pharmaceutics 307, 93 (2006). https://doi.org/10.1016/j.ijpharm.2005.10.010
[38] T. U. Wani, S. N. Raza, and N. A. Khan, Polymer Bulletin 77, 3865 (2020). https://doi.org/10.1007/s00289-019-02924-7
[39] P. Aggarwal, J. B. Hall, C. B. McLeland, M. A. Dobrovolskaia, and S. E. McNeil, Advanced Drug Delivery Reviews 61, 428 (2009). https://doi.org/10.1016/j.addr.2009.03.009
[40] S.-D. Li and L. Huang, Biochimica et Biophysica Acta (BBA) – Biomembranes 1788, 2259 (2009). https://doi.org/10.1016/j.bbamem.2009.06.022
[41] S. Guo and L. Huang, Journal of Nanomaterials 2011, 1 (2011). https://doi.org/10.1155/2011/742895
[42] K. Greish, In: S. Grobmyer, B. Moudgil (eds). Cancer Nanotechnology. Methods in Molecular Biology, vol. 624. Humana Press (2010). https://doi.org/10.1007/978-1-60761-609-2_3
[43] P. Foroozandeh and A. A. Aziz, Nanoscale Research Letters 13, 339 (2018). https://doi.org/10.1186/s11671-018-2728-6
[44] A. B. Engin, D. Nikitovic, M. Neagu, P. Henrich-Noack, A. O. Docea, M. I. Shtilman, K. Golokhvast, and A. M. Tsatsakis, Particle and Fibre Toxicology 14, 22 (2017). https://doi.org/10.1186/s12989-017-0199-z
[45] S. E. A. Gratton, P. A. Ropp, P. D. Pohlhaus, J. C. Luft, V. J. Madden, M. E. Napier, and J. M. DeSimone, Proceedings of the National Academy of Sciences 105, 11613 (2008). https://doi.org/10.1073/pnas.0801763105
[46] K. Maier-Hauff, F. Ulrich, D. Nestler, H. Niehoff, P. Wust, B. Thiesen, H. Orawa, V. Budach, and A. Jordan, J Neurooncol 103, 317 (2011). https://doi.org/10.1007/s11060-010-0389-0
[47] K. Mahmoudi, A. Bouras, D. Bozec, R. Ivkov, and C. Hadjipanayis, International Journal of Hyperthermia 34, 1316 (2018). https://doi.org/10.1080/02656736.2018.1430867
[48] M. Johannsen, B. Thiesen, P. Wust, A. Jordan, International J of Hyperthermia 26, 790 (2010). https://doi.org/10.3109/02656731003745740
[49] F. Brero, M. Albino, A. Antoccia, P. Arosio, M. Avolio, F. Berardinelli, D. Bettega, P. Calzolari, M. Ciocca, M. Corti, A. Facoetti, S. Gallo, F. Groppi, A. Guerrini, C. Innocenti, C. Lenardi, S. Locarno, S. Manenti, R. Marchesini, M. Mariani, F. Orsini, E. Pignoli, C. Sangregorio, I. Veronese, and A. Lascialfari, Nanomaterials 10, 1 (2020). https://doi.org/10.3390/nano10101919
[50] I. Hilger, International Journal of Hyperthermia 29, 828 (2013). https://doi.org/10.3109/02656736.2013.832815
[51] M. Tasso, F. Ghilini, M. Cathcarth, and A. S. Picco, In: S. K. Sharma (eds). Toxicity Assessment of Nanoferrites. Spinel Nanoferrites. Topics in Mining, Metallurgy and Materials Engineering. Springer, Cham. (2021). https://doi.org/10.1007/978-3-030-79960-1_9
[52] R. Vakili-Ghartavol, A. A. Momtazi-Borojeni, Z. Vakili-Ghartavol, H. T. Aiyelabegan, M. R. Jaafari, S. M. Rezayat, and S. Arbabi Bidgoli, Artificial Cells, Nanomedicine, and Biotechnology 48, 443 (2020). https://doi.org/10.1080/21691401.2019.1709855
[53] S. Alarifi, D. Ali, S. Alkahtani, and M. S. Alhader, Biological Trace Element Research 159, 416 (2014). https://doi.org/10.1007/s12011-014-9972-0
[54] A. Hanini, A. Schmitt, K. Kacem, F. Chau, S. Ammar, J. Gavard, International Journal of Nanomedicine 2011:6, 787 (2011). https://doi.org/10.2147/IJN.S17574
[55] V. Valdiglesias, N. Fernández-Bertólez, G. Kiliç, C. Costa, S. Costa, S. Fraga, M. J. Bessa, E. Pásaro, J. P. Teixeira, and B. Laffon, Journal of Trace Elements in Medicine and Biology 38, 53 (2016). https://doi.org/10.1016/j.jtemb.2016.03.017
[56] J. Shaw, S. O. Raja, and A. K. Dasgupta, Cancer Nanotechnology 5, 2 (2014). https://doi.org/10.1186/s12645-014-0002-x
[57] B. Hajipour Verdom, P. Abdolmaleki, and M. Behmanesh, Scientific Reports 8, 990 (2018). https://doi.org/10.1038/s41598-018-19247-8
[58] X. Tian, D. Wang, M. Zha, X. Yang, X. Ji, L. Zhang, and X. Zhang, Electromagnetic Biology and Medicine 37, 114 (2018). https://doi.org/10.1080/15368378.2018.1458627
[59] M. E. Feder and G. E. Hofmann, Annual Review of Physiology 61, 243 (1999). https://doi.org/10.1146/annurev.physiol.61.1.243
[60] D. Przepiorka and P. K. Srivastava, Molecular Medicine Today 4, 478 (1998). https://doi.org/10.1016/S1357-4310(98)01345-8
[61] S. K. Calderwood, J. R. Theriault, and J. Gong, European Journal of Immunology 35, 2518 (2005). https://doi.org/10.1002/eji.200535002
[62] K. C. Kregel, Journal of Applied Physiology 92, 2177 (2002). https://doi.org/10.1152/japplphysiol.01267.2001
[63] V. Reichel, A. Kovács, M. Kumari, É. Bereczk-Tompa, E. Schneck, P. Diehle, M. Pósfai, A. M. Hirt, M. Duchamp, R. E. Dunin-Borkowski, and D. Faivre, Scientific Reports 7, 45484 (2017). https://doi.org/10.1038/srep45484
[64] Yu. L. Raikher and V. I. Stepanov, Journal of Experimental and Theoretical Physics 112, 173 (2011). https://doi.org/10.1134/S1063776110061160
[65] R. K. Gilchrist, R. Medal, W. D. Shorey, R. C. Hanselman, J. C. Parrott, and C. B. Taylor, Annals of Surgery 146, 596 (1957). https://doi.org/10.1097/00000658-195710000-00007
[66] A. Jordan, P. Wust, R. Scholz, B. Tesche, H. Fähling, T. Mitrovics, T. Vogl, J. Cervós-navarro, and R. Felix, International Journal of Hyperthermia 12, 705 (1996). https://doi.org/10.3109/02656739609027678
[67] D. Bobo, K. J. Robinson, J. Islam, K. J. Thurecht, and S. R. Corrie, Pharmaceutical Research 33, 2373 (2016). https://doi.org/10.1007/s11095-016-1958-5
[68] J. L. Dormann, L. Bessais, and D. Fiorani, Journal of Physics C: Solid State Physics 21, 2015 (1988). https://doi.org/10.1088/0022-3719/21/10/019
[69] D. F. Coral, P. Mendoza Zélis, M. E. de Sousa, D. Muraca, V. Lassalle, P. Nicolás, M. L. Ferreira, and M. B. Fernández van Raap, Journal of Applied Physics 115, 043907 (2014). https://doi.org/10.1063/1.4862647
[70] J. Dieckhoff, D. Eberbeck, M. Schilling, and F. Ludwig, Journal of Applied Physics 119, 043903 (2016). https://doi.org/10.1063/1.4940724
[71] M. I. Shliomis and V. I. Stepanov, In: W. Coffey (ed.). Advances in Chemical Physics. Theory of the Dynamic Susceptibility of Magnetic Fluids (1994). https://doi.org/10.1002/9780470141465.ch1
[72] Z. Li, D. Li, Y. Chen, and H. Cui, Soft Matter 14, 3858 (2018). https://doi.org/10.1039/C8SM00478A
[73] R. E. Rosensweig, Journal of Magnetism and Magnetic Materials 252, 370 (2002). https://doi.org/10.1016/S0304-8853(02)00706-0
[74] C. Tannous and J. Gieraltowski, European Journal of Physics 29, 475 (2008). https://doi.org/10.1088/0143-0807/29/3/008
[75] J. Carrey, B. Mehdaoui, and M. Respaud, Journal of Applied Physics 109, 083921 (2011). https://doi.org/10.1063/1.3551582
[76] M. Colombo, S. Carregal-Romero, M. F. Casula, L. Gutiérrez, M. P. Morales, I. B. Böhm, J. T. Heverhagen, D. Prosperi, and W. J. Parak, Chemical Society Reviews 41, 4306 (2012). https://doi.org/10.1039/c2cs15337h
[77] W. J. Atkinson, I. A. Brezovich, and D. P. Chakraborty, IEEE Transactions on Biomedical Engineering BME-31, 70 (1984). https://doi.org/10.1109/TBME.1984.325372
[78] R. Hergt and S. Dutz, Journal of Magnetism and Magnetic Materials 311, 187 (2007). https://doi.org/10.1016/j.jmmm.2006.10.1156
[79] I. A. Brezovich, In: B. Paliwal, F. W. Hetzel, and M. W. Dewhirst (eds.). Medical Physics Monograph No. 6: Biological, Physical, and Clinical Aspects of Hyperthermia. Medical Physics Publishing (1988).
[80] R. Hergt, S. Dutz, R. Müller, and M. Zeisberger, Journal of Physics: Condensed Matter 18, S2919 (2006). https://doi.org/10.1088/0953-8984/18/38/S26
[81] M. L. Etheridge and J. C. Bischof, Annals of Biomedical Engineering 41, 78 (2013). https://doi.org/10.1007/s10439-012-0633-1
[82] R. Yanes, O. Chubykalo-Fesenko, H. Kachkachi, D. A. Garanin, R. Evans, and R. W. Chantrell, Physical Review B 76, 064416 (2007). https://doi.org/10.1103/PhysRevB.76.064416
[83] F. Luis, J. M. Torres, L. M. García, J. Bartolomé, J. Stankiewicz, F. Petroff, F. Fettar, J.-L. Maurice, and A. Vaurè, and A. Vaurè, Phys. Rev. B 65, 094409 (2002). https://doi.org/10.1103/PhysRevB.65.094409
[84] J. L. Dormann, D. Fiorani, and E. Tronc, In: I. Prigogine and S.A. Rice (eds.). Advances in Chemical Physics, Magnetic Relaxation in Fine-Particle Systems (1997). https://doi.org/10.1002/9780470141571.ch4
[85] F. H. Sánchez, P. Mendoza Zélis, M. L. Arciniegas, G. A. Pasquevich, and M. B. Fernández van Raap, Physical Review B 95, 134421 (2017). https://doi.org/10.1103/PhysRevB.95.134421
[86] M. B. Fernández van Raap, P. Mendoza Zélis, D. F. Coral, T. E. Torres, C. Marquina, G. F. Goya, and F. H. Sánchez, Journal of Nanoparticle Research 14, 1072 (2012). https://doi.org/10.1007/s11051-012-1072-5
[87] G. T. Landi, Physical Review B 89, 014403 (2014). https://doi.org/10.1103/PhysRevB.89.014403
[88] G. T. Landi, Journal of Applied Physics 113, 163908 (2013). https://doi.org/10.1063/1.4802583
[89] R. P. Tan, J. Carrey, and M. Respaud, Physical Review B 90, 214421 (2014). https://doi.org/10.1103/PhysRevB.90.214421
[90] D. F. Coral, P. Mendoza Zélis, M. Marciello, M. del P. Morales, A. Craievich, F. H. Sánchez, and M. B. Fernández van Raap, Langmuir 32, 1201 (2016). https://doi.org/10.1021/acs.langmuir.5b03559
[91] I. Conde-Leboran, D. Baldomir, C. Martinez-Boubeta, O. Chubykalo-Fesenko, M. del Puerto Morales, G. Salas, D. Cabrera, J. Camarero, F. J. Teran, and D. Serantes, The Journal of Physical Chemistry C 119, 15698 (2015). https://doi.org/10.1021/acs.jpcc.5b02555
[92] C. Papadopoulos, A. Kolokithas‐Ntoukas, R. Moreno, D. Fuentes, G. Loudos, V. C. Loukopoulos, and G. C. Kagadis, Medical Physics 49, 547 (2022). https://doi.org/10.1002/mp.15317
[93] K. Gilmore, Y. U. Idzerda, M. T. Klem, M. Allen, T. Douglas, and M. Young, Journal of Applied Physics 97, 10B301 (2005). https://doi.org/10.1063/1.1845973
[94] A. I. Figueroa, J. Bartolomé, L. M. García, F. Bartolomé, A. Arauzo, A. Millán, and F. Palacio, Physics Procedia 75, 1050 (2015). https://doi.org/10.1016/j.phpro.2015.12.174
[95] M. B. Fernández van Raap, D. F. Coral, S. Yu, G. A. Muñoz, F. H. Sánchez, and A. Roig, Physical Chemistry Chemical Physics 19, 7176 (2017). https://doi.org/10.1039/C6CP08059F
[96] M. Kallumadil, M. Tada, T. Nakagawa, M. Abe, P. Southern, and Q. A. Pankhurst, Journal of Magnetism and Magnetic Materials 321, 1509 (2009). https://doi.org/10.1016/j.jmmm.2009.02.075
[97] J. Wells, D. Ortega, U. Steinhoff, S. Dutz, E. Garaio, O. Sandre, E. Natividad, M. M. Cruz, F. Brero, P. Southern, Q. A. Pankhurst, and S. Spassov, International Journal of Hyperthermia 38, 447 (2021). https://doi.org/10.1080/02656736.2021.1892837
[98] H. Gavilán, S. K. Avugadda, T. Fernández-Cabada, N. Soni, M. Cassani, B. T. Mai, R. Chantrell, and T. Pellegrino, Chemical Society Reviews 50, 11614 (2021). https://doi.org/10.1039/D1CS00427A
[99] J. M. Orozco-Henao, D. Muraca, F. H. Sánchez, and P. Mendoza Zélis, Journal of Physics D: Applied Physics 53, 385001 (2020). https://doi.org/10.1088/1361-6463/ab9264
[100] A. Gallo-Cordova, J. G. Ovejero, A. M. Pablo-Sainz-Ezquerra, J. Cuya, B. Jeyadevan, S. Veintemillas-Verdaguer, P. Tartaj, and M. del P. Morales, Journal of Colloid and Interface Science 608, 1585 (2022). https://doi.org/10.1016/j.jcis.2021.10.111
[101] D. Niculaes, A. Lak, G. C. Anyfantis, S. Marras, O. Laslett, S. K. Avugadda, M. Cassani, D. Serantes, O. Hovorka, R. Chantrell, and T. Pellegrino, ACS Nano 11, 12121 (2017). https://doi.org/10.1021/acsnano.7b05182
[102] B. Sanz, M. P. Calatayud, E. de Biasi, E. Lima, M. V. Mansilla, R. D. Zysler, M. R. Ibarra, and G. F. Goya, Scientific Reports 6, 38733 (2016). https://doi.org/10.1038/srep38733
[103] R. di Corato, A. Espinosa, L. Lartigue, M. Tharaud, S. Chat, T. Pellegrino, C. Ménager, F. Gazeau, and C. Wilhelm, Biomaterials 35, 6400 (2014). https://doi.org/10.1016/j.biomaterials.2014.04.036
[104] U. M. Engelmann, J. Seifert, B. Mues, S. Roitsch, C. Ménager, A. M. Schmidt, and I. Slabu, Journal of Magnetism and Magnetic Materials 471, 486 (2019). https://doi.org/10.1016/j.jmmm.2018.09.113
[105] S. Dutz, M. Kettering, I. Hilger, R. Müller, and M. Zeisberger, Nanotechnology 22, 265102 (2011). https://doi.org/10.1088/0957-4484/22/26/265102
[106] D. Cabrera, A. Lak, T. Yoshida, M. E. Materia, D. Ortega, F. Ludwig, P. Guardia, A. Sathya, T. Pellegrino, and F. J. Teran, Nanoscale 9, 5094 (2017). https://doi.org/10.1039/C7NR00810D
[107] M. Avolio, A. Guerrini, F. Brero, C. Innocenti, C. Sangregorio, M. Cobianchi, M. Mariani, F. Orsini, P. Arosio, and A. Lascialfari, Journal of Magnetism and Magnetic Materials 471, 504 (2019). https://doi.org/10.1016/j.jmmm.2018.09.111
[108] D. F. Coral, P. A. Soto, V. Blank, A. Veiga, E. Spinelli, S. Gonzalez, G. P. Saracco, M. A. Bab, D. Muraca, P. C. Setton-Avruj, A. Roig, L. Roguin, and M. B. Fernández van Raap, Nanoscale 10, 21262 (2018). https://doi.org/10.1039/C8NR07453D
[109] E. Garaio, J. M. Collantes, J. A. Garcia, F. Plazaola, S. Mornet, F. Couillaud, and O. Sandre, Journal of Magnetism and Magnetic Materials 368, 432 (2014). https://doi.org/10.1016/j.jmmm.2013.11.021
[110] V. Connord, B. Mehdaoui, R. P. Tan, J. Carrey, and M. Respaud, Review of Scientific Instruments 85, 093904 (2014). https://doi.org/10.1063/1.4895656
[111] I. J. Bruvera, D. G. Actis, M. P. Calatayud, and P. Mendoza Zélis, Journal of Magnetism and Magnetic Materials 491, 165563 (2019). https://doi.org/10.1016/j.jmmm.2019.165563
[112] I. Malaescu, P. C. Fannin, C. N. Marin, and D. Lazic, Medical Hypotheses 110, 76 (2018). https://doi.org/10.1016/j.mehy.2017.11.004
[113] M. Beković, M. Trlep, M. Jesenik, and A. Hamler, Journal of Magnetism and Magnetic Materials 355, 12 (2014). https://doi.org/10.1016/j.jmmm.2013.11.045
[114] M. E. Cano, A. Barrera, J. C. Estrada, A. Hernandez, and T. Cordova, Review of Scientific Instruments 82, 114904 (2011). https://doi.org/10.1063/1.3658818
[115] S. Dürr, W. Schmidt, C. Janko, H. P. Kraemer, P. Tripal, F. Eiermann, R. Tietze, S. Lyer, and C. Alexiou, Biomedical Engineering / Biomedizinische Technik (2013). https://doi.org/10.1515/bmt-2013-4129
[116] V. Connord, B. Mehdaoui, R. P. Tan, J. Carrey, and M. Respaud, Review of Scientific Instruments 85, 093904 (2014). https://doi.org/10.1063/1.4895656
[117] L.-M. Lacroix, J. Carrey, and M. Respaud, Review of Scientific Instruments 79, 093909 (2008). https://doi.org/10.1063/1.2972172
[118] S. A. Gonzalez, E. M. Spinelli, A. L. Veiga, D. F. Coral, M. B. F. van Raap, P. M. Zelis, G. A. Pasquevich, and F. H. Sanchez, in 2017 IEEE 8th Latin American Symposium on Circuits & Systems (LASCAS) (IEEE, 2017), pp. 1-4. https://doi.org/10.1109/LASCAS.2017.7948091
[119] U. Gneveckow, A. Jordan, R. Scholz, V. Brüß, N. Waldöfner, J. Ricke, A. Feussner, B. Hildebrandt, B. Rau, and P. Wust, Medical Physics 31, 1444 (2004). https://doi.org/10.1118/1.1748629
[120] G. Oberdörster, E. Oberdörster, and J. Oberdörster, Environmental Health Perspectives 113, 823 (2005). https://doi.org/10.1289/ehp.7339
[121] P. Khanna, C. Ong, B. Bay, and G. Baeg, Nanomaterials 5, 1163 (2015). https://doi.org/10.3390/nano5031163
[122] R. Vakili-Ghartavol, A. A. Momtazi-Borojeni, Z. Vakili-Ghartavol, H. T. Aiyelabegan, M. R. Jaafari, S. M. Rezayat, and S. Arbabi Bidgoli, Artificial Cells, Nanomedicine, and Biotechnology 48, 443 (2020). https://doi.org/10.1080/21691401.2019.1709855
[123] M. Tasso, M. A. Lago Huvelle, I. Diaz Bessone, and A. S. Picco, In: S. K. Sharma, Y. Javed (eds). Toxicity Assessment of Nanomaterials. Magnetic Nanoheterostructures. Nanomedicine and Nanotoxicology. Springer, Cham. (2020). https://doi.org/10.1007/978-3-030-39923-8_13
[124] S. T. Stern, P. P. Adiseshaiah, and R. M. Crist, Particle and Fibre Toxicology 9, 20 (2012). https://doi.org/10.1186/1743-8977-9-20
[125] E. A. K. Warren and C. K. Payne, RSC Advances 5, 13660 (2015). https://doi.org/10.1039/C4RA15727C
[126] D. C. Pan, J. W. Myerson, J. S. Brenner, P. N. Patel, A. C. Anselmo, S. Mitragotri, and V. Muzykantov, Scientific Reports 8, 1615 (2018). https://doi.org/10.1038/s41598-018-19897-8
[127] A. Kurtz-Chalot, J. P. Klein, J. Pourchez, D. Boudard, V. Bin, G. B. Alcantara, M. Martini, M. Cottier, and V. Forest, Journal of Nanoparticle Research 16, 2738 (2014). https://doi.org/10.1007/s11051-014-2738-y
[128] S. Xu, B. Z. Olenyuk, C. T. Okamoto, and S. F. Hamm-Alvarez, Advanced Drug Delivery Reviews 65, 121 (2013). https://doi.org/10.1016/j.addr.2012.09.041
[129] A. Manke, L. Wang, and Y. Rojanasakul, BioMed Research International 2013, 1 (2013). https://doi.org/10.1155/2013/942916
[130] D. Ling and T. Hyeon, Small 9, 1450 (2013). https://doi.org/10.1002/smll.201202111
[131] N. Fernández-Bertólez, C. Costa, M. J. Bessa, M. Park, M. Carriere, F. Dussert, J. P. Teixeira, E. Pásaro, B. Laffon, and V. Valdiglesias, Mutation Research/Genetic Toxicology and Environmental Mutagenesis 845, 402989 (2019). https://doi.org/10.1016/j.mrgentox.2018.11.013
[132] M. Mahmoudi, H. Hofmann, B. Rothen-Rutishauser, and A. Petri-Fink, Chemical Reviews 112, 2323 (2012). https://doi.org/10.1021/cr2002596
[133] Q. Feng, Y. Liu, J. Huang, K. Chen, J. Huang, and K. Xiao, Scientific Reports 8, 2082 (2018). https://doi.org/10.1038/s41598-018-19628-z
[134] L. C. Davies, S. J. Jenkins, J. E. Allen, and P. R. Taylor, Nature Immunology 14, 986 (2013). https://doi.org/10.1038/ni.2705
[135] R. Stevenson, A. J. Hueber, A. Hutton, I. B. McInnes, and D. Graham, The Scientific World Journal 11, 1300 (2011). https://doi.org/10.1100/tsw.2011.106
[136] D. Reichel, M. Tripathi, and J. M. Perez, Nanotheranostics 3, 66 (2019). https://doi.org/10.7150/ntno.30052
[137] B. B. Manshian, J. Poelmans, S. Saini, S. Pokhrel, J. J. Grez, U. Himmelreich, L. Mädler, and S. J. Soenen, Acta Biomaterialia 68, 99 (2018). https://doi.org/10.1016/j.actbio.2017.12.020
[138] A. Gojova, B. Guo, R. S. Kota, J. C. Rutledge, I. M. Kennedy, and A. I. Barakat, Environmental Health Perspectives 115, 403 (2007). https://doi.org/10.1289/ehp.8497
[139] M.-T. Zhu, B. Wang, Y. Wang, L. Yuan, H.-J. Wang, M. Wang, H. Ouyang, Z.-F. Chai, W.-Y. Feng, and Y.-L. Zhao, Toxicology Letters 203, 162 (2011). https://doi.org/10.1016/j.toxlet.2011.03.021
[140] P. R. Leroueil, S. Hong, A. Mecke, J. R. Baker, B. G. Orr, and M. M. Banaszak Holl, Accounts of Chemical Research 40, 335 (2007). https://doi.org/10.1021/ar600012y
[141] C. Contini, M. Schneemilch, S. Gaisford, and N. Quirke, Journal of Experimental Nanoscience 13, 62 (2018). https://doi.org/10.1080/17458080.2017.1413253
[142] J. Chen, J. A. Hessler, K. Putchakayala, B. K. Panama, D. P. Khan, S. Hong, D. G. Mullen, S. C. DiMaggio, A. Som, G. N. Tew, A. N. Lopatin, J. R. Baker, M. M. B. Holl, and B. G. Orr, The Journal of Physical Chemistry B 113, 11179 (2009). https://doi.org/10.1021/jp9033936
[143] H. Nakamura and S. Watano, KONA Powder and Particle Journal 35, 49 (2018). https://doi.org/10.14356/kona.2018011
[144] T. Decker and M.-L. Lohmann-Matthes, Journal of Immunological Methods 115, 61 (1988). https://doi.org/10.1016/0022-1759(88)90310-9
[145] N. Singh, B. Nelson, L. Scanlan, E. Coskun, P. Jaruga, and S. Doak, International Journal of Molecular Sciences 18, 1515 (2017). https://doi.org/10.3390/ijms18071515
[146] K. Kansara, P. Patel, D. Shah, R. K. Shukla, S. Singh, A. Kumar, and A. Dhawan, Environmental and Molecular Mutagenesis 56, 204 (2015). https://doi.org/10.1002/em.21925
[147] D. Y. Seo, M. Jin, J.-C. Ryu, and Y.-J. Kim, Toxicology and Environmental Health Sciences 9, 23 (2017). https://doi.org/10.1007/s13530-017-0299-z
[148] R. Wan, Y. Mo, L. Feng, S. Chien, D. J. Tollerud, and Q. Zhang, Chemical Research in Toxicology 25, 1402 (2012). https://doi.org/10.1021/tx200513t
[149] M. Ahamed, H. A. Alhadlaq, J. Alam, M. A. Majeed Khan, D. Ali, and S. Alarafi, Current Pharmaceutical Design 19, 6681 (2013). https://doi.org/10.2174/1381612811319370011
[150] S. Alarifi, D. Ali, S. Alkahtani, and M. S. Alhader, Biological Trace Element Research 159, 416 (2014). https://doi.org/10.1007/s12011-014-9972-0
[151] X.-Q. Zhang, X. Xu, N. Bertrand, E. Pridgen, A. Swami, and O. C. Farokhzad, Advanced Drug Delivery Reviews 64, 1363 (2012). https://doi.org/10.1016/j.addr.2012.08.005
[152] M. A. Malvindi, V. de Matteis, A. Galeone, V. Brunetti, G. C. Anyfantis, A. Athanassiou, R. Cingolani, and P. P. Pompa, PLoS ONE 9, e85835 (2014). https://doi.org/10.1371/journal.pone.0085835
[153] G. Crisponi, V. M. Nurchi, J. I. Lachowicz, M. Peana, S. Medici, and M. A. Zoroddu, In: A. M. Grumezescu (eds). Toxicity of Nanoparticles: Etiology and Mechanisms. Antimicrobial Nanoarchitectonics. Elsevier (2017). https://doi.org/10.1016/B978-0-323-52733-0.00018-5
[154] P. Rivera Gil, G. Oberdörster, A. Elder, V. Puntes, and W. J. Parak, ACS Nano 4, 5527 (2010). https://doi.org/10.1021/nn1025687
[155] A. Laszlo, Cell Proliferation 25, 59 (1992). https://doi.org/10.1111/j.1365-2184.1992.tb01482.x
[156] J.R. Lepock, in: Advances in Molecular and Cell Biology, Elsevier, 1997, pp. 223–259.
[157] J. L. Roti, International Journal of Hyperthermia 24, 3 (2008). https://doi.org/10.1080/02656730701769841
[158] C. M. Neophytou, I. P. Trougakos, N. Erin, and P. Papageorgis, Cancers 13, 4363 (2021). doi: 10.3390/cancers13174363
[159] M. Sefidgar, E. Bashooki, and P. Shojaee, Journal of Thermal Biology 94, 102742 (2020). https://doi.org/10.1016/j.jtherbio.2020.102742
[160] N. CM, T. IP, E. N, and P. P, Cancers (Basel) 13, (2021).
[161] F. H. Igney and P. H. Krammer, Nature Reviews Cancer 2002 2:4 2, 277 (2002). https://doi.org/10.1038/nrc776
[162] A. Murshid, J. Gong, and S. K. Calderwood, Frontiers in Immunology 3, (2012). https://doi.org/10.3389/fimmu.2012.00063
[163] B. Perillo, M. Di Donato, A. Pezone, E. Di Zazzo, P. Giovannelli, G. Galasso, G. Castoria, and A. Migliaccio, Experimental and Molecular Medicine 52, 192 (2020). https://doi.org/10.1038/s12276-020-0384-2
[164] Y. Huang, S. Wu, L. Zhang, Q. Deng, J. Ren, and X. Qu, ACS Nano 16, 4228 (2022). https://doi.org/10.1021/acsnano.1c10231
[165] X. Cheng, H.-D. Xu, H.-H. Ran, G. Liang, and F.-G. Wu, ACS Nano 15, 8039 (2021). https://doi.org/10.1021/acsnano.1c00498
[166] S. J. Dixon, K. M. Lemberg, M. R. Lamprecht, R. Skouta, E. M. Zaitsev, C. E. Gleason, D. N. Patel, A. J. Bauer, A. M. Cantley, W. S. Yang, B. Morrison, and B. R. Stockwell, Cell 149, 1060 (2012). https://doi.org/10.1016/j.cell.2012.03.042
[167] M. R. Sepand, S. Ranjbar, I. M. Kempson, M. Akbariani, W. C. A. Muganda, M. Müller, M. H. Ghahremani, and M. Raoufi, Nanomedicine 29, 102243 (2020). https://doi.org/10.1016/j.nano.2020.102243
[168] J. Y. Cao and S. J. Dixon, Cellular and Molecular Life Sciences 73, 2195 (2016). https://doi.org/10.1007/s00018-016-2194-1
[169] S. Zanganeh, G. Hutter, R. Spitler, O. Lenkov, M. Mahmoudi, A. Shaw, J. S. Pajarinen, H. Nejadnik, S. Goodman, M. Moseley, L. M. Coussens, and H. E. Daldrup-Link, Nature Nanotechnology 11, 986 (2016). https://doi.org/10.1038/nnano.2016.168
[170] L. Yue, J. Wang, Z. Dai, Z. Hu, X. Chen, Y. Qi, X. Zheng, and D. Yu, Bioconjugate Chemistry 28, 400 (2017). https://doi.org/10.1021/acs.bioconjchem.6b00562
[171] C. Hu, X. Chen, Y. Huang, and Y. Chen, Scientific Reports 8, 2274 (2018). https://doi.org/10.1038/s41598-018-20715-4
[172] Z. Zhou, J. Song, R. Tian, Z. Yang, G. Yu, L. Lin, G. Zhang, W. Fan, F. Zhang, G. Niu, L. Nie, and X. Chen, Angewandte Chemie – International Edition 56, 6492 (2017). https://doi.org/10.1002/anie.201701181
[173] W. P. Li, C. H. Su, Y. C. Chang, Y. J. Lin, and C. S. Yeh, ACS Nano 10, 2017 (2016). https://doi.org/10.1021/acsnano.5b06175
[174] Z. Shen, J. Song, B. C. Yung, Z. Zhou, A. Wu, and X. Chen, Advanced Materials 30, 1704007 (2018). https://doi.org/10.1002/adma.201704007
[175] J. Li, F. Cao, H.-L. Yin, Z.-J. Huang, Z.-T. Lin, N. Mao, B. Sun, and G. Wang, Cell Death and Disease 11, 88 (2020). https://doi.org/10.1038/s41419-020-2298-2
[176] X. Chen, C. Yu, R. Kang, and D. Tang, Frontiers in Cell and Developmental Biology 8, 1 (2020). https://doi.org/10.3389/fcell.2020.590226
[177] P. K. Srivastava, Advances in Cancer Research 62, 153 (1993). https://doi.org/10.1016/S0065-230X(08)60318-8
[178] R. J. Binder, The Journal of Immunology 193, 5765 (2014). https://doi.org/10.4049/jimmunol.1401417
[179] C. Wood, P. Srivastava, R. Bukowski, L. Lacombe, A. I. Gorelov, S. Gorelov, P. Mulders, H. Zielinski, A. Hoos, F. Teofilovici, L. Isakov, R. Flanigan, R. Figlin, R. Gupta, and B. Escudier, The Lancet 372, 145 (2008). https://doi.org/10.1016/S0140-6736(08)60697-2
[180] F. Gong, N. Yang, X. Wang, Q. Zhao, Q. Chen, Z. Liu, and L. Cheng, Nano Today 32, 100851 (2020). https://doi.org/10.1016/j.nantod.2020.100851
[181] S. K. Calderwood, M. A. Khaleque, D. B. Sawyer, and D. R. Ciocca, Trends in Biochemical Sciences 31, 164 (2006). https://doi.org/10.1016/j.tibs.2006.01.006
[182] B. Frey, E. M. Weiss, Y. Rubner, R. Wunderlich, O. J. Ott, R. Sauer, R. Fietkau, and U. S. Gaipl, International Journal of Hyperthermia 28, 528 (2012). https://doi.org/10.3109/02656736.2012.677933
[183] A. Murshid, T. J. Borges, C. Bonorino, B. J. Lang, and S. K. Calderwood, Front Immunol 10, 3035 (2019). https://doi.org/10.3389/fimmu.2019.03035
[184] J. Gong, B. Zhu, A. Murshid, H. Adachi, B. Song, A. Lee, C. Liu, and S. K. Calderwood, The Journal of Immunology 183, 3092 (2009). https://doi.org/10.4049/jimmunol.0901235
[185] J. R. Thériault, H. Adachi, and S. K. Calderwood, The Journal of Immunology 177, 8604 (2006). https://doi.org/10.4049/jimmunol.177.12.8604
[186] S. Persano, P. Das, and T. Pellegrino, Cancers (Basel) 13, (2021). https://doi.org/10.3390/cancers13112735
[187] S. Toraya-Brown, M. R. Sheen, P. Zhang, L. Chen, J. R. Baird, E. Demidenko, M. J. Turk, P. J. Hoopes, J. R. Conejo-Garcia, and S. Fiering, Nanomedicine: Nanotechnology, Biology, and Medicine 10, 1273 (2014). https://doi.org/10.1016/j.nano.2014.01.011
[188] K.-G. Tranberg, Frontiers in Oncology 11, (2021). https://doi.org/10.3389/fonc.2021.708810
[189] E. M. Scutigliani, Y. Liang, H. Crezee, R. Kanaar, and P. M. Krawczyk, Cancers (Basel) 13, 1 (2021). https://doi.org/10.3390/cancers13061243
[190] K. Ohnishi, A. Takahashi, S. Yokota, and T. Ohnishi, International Journal of Radiation Biology 80, 607 (2004). https://doi.org/10.1080/09553000412331283470
[191] K. Ohnishi, In: S. Kokura, T. Yoshikawa, T. Ohnishi (eds). Thermo-Tolerance. Hyperthermic Oncology from Bench to Bedside. Springer, Singapore (2016). https://doi.org/10.1007/978-981-10-0719-4_7
[192] J. H. Wang, M. Z. Yao, J. F. Gu, L. Y. Sun, X. Y. Liu, and Y. F. Shen, Biochemical and Biophysical Research Communications 290, 1454 (2002). https://doi.org/10.1006/bbrc.2002.6373
[193] Y. Nakamura, M. Fujimoto, N. Hayashida, R. Takii, A. Nakai, and M. Muto, J Dermatol Sci 60, 187 (2010). https://doi.org/10.1016/j.jdermsci.2010.09.009
[194] E. Sahin, M. Sahin, A. D. Sanlioǧlu, and S. Gümüslü, Int J Hyperthermia 27, 63 (2011). https://doi.org/10.3109/02656736.2010.528139
[195] L. E. M. Vriend, N. van den Tempel, A. L. Oei, M. L’Acosta, F. J. Pieterson, N. A. P. Franken, R. Kanaar, and P. M. Krawczyk, Oncotarget 8, 97490 (2017). https://doi.org/10.18632/oncotarget.22142
[196] T. Miyagawa, H. Saito, Y. Minamiya, K. Mitobe, S. Takashima, N. Takahashi, A. Ito, K. Imai, S. Motoyama, and J. Ogawa, Int J Clin Oncol 19, 722 (2014). https://doi.org/10.1007/s10147-013-0606-x
[197] D. Egea-Benavente, J. G. Ovejero, M. D. P. Morales, and D. F. Barber, Cancers (Basel) 13, (2021). https://doi.org/10.3390/cancers13184583
[198] M. Asgari, T. Miri, M. Soleymani, and A. Barati, Journal of Molecular Liquids 324, 114731 (2021). https://doi.org/10.1016/j.molliq.2020.114731
[199] J. R. Lepock, International Journal of Hyperthermia 19, 252 (2003). https://doi.org/10.1080/0265673031000065042
[200] G. C. van Rhoon, M. Franckena, and T. L. M. ten Hagen, Advanced Drug Delivery Reviews 163-164, 145 (2020). https://doi.org/10.1016/j.addr.2020.03.006
[201] M. Chang, Z. Hou, M. Wang, C. Li, and J. Lin, Advanced Materials 33, 2004788 (2021). https://doi.org/10.1002/adma.202004788
[202] X. Liu, Y. Zhang, Y. Wang, W. Zhu, G. Li, X. Ma, Y. Zhang, S. Chen, S. Tiwari, K. Shi, S. Zhang, H. M. Fan, Y. X. Zhao, and X. J. Liang, Theranostics 10, 3793 (2020). https://doi.org/10.7150/thno.40805
