Potential of Magnetic Hyperthermia to Stimulate Localized Immune Activation.
biological response
heat-shock protein 70
immune stimulation
magnetic hyperthermia
superparamagnetic iron oxide nanoparticles
Journal
Small (Weinheim an der Bergstrasse, Germany)
ISSN: 1613-6829
Titre abrégé: Small
Pays: Germany
ID NLM: 101235338
Informations de publication
Date de publication:
04 2021
04 2021
Historique:
revised:
20
01
2021
received:
25
08
2020
pubmed:
19
3
2021
medline:
15
7
2021
entrez:
18
3
2021
Statut:
ppublish
Résumé
Magnetic hyperthermia (MH) harnesses the heat-releasing properties of superparamagnetic iron oxide nanoparticles (SPIONs) and has potential to stimulate immune activation in the tumor microenvironment whilst sparing surrounding normal tissues. To assess feasibility of localized MH in vivo, SPIONs are injected intratumorally and their fate tracked by Zirconium-89-positron emission tomography, histological analysis, and electron microscopy. Experiments show that an average of 49% (21-87%, n = 9) of SPIONs are retained within the tumor or immediately surrounding tissue. In situ heating is subsequently generated by exposure to an externally applied alternating magnetic field and monitored by thermal imaging. Tissue response to hyperthermia, measured by immunohistochemical image analysis, reveals specific and localized heat-shock protein expression following treatment. Tumor growth inhibition is also observed. To evaluate the potential effects of MH on the immune landscape, flow cytometry is used to characterize immune cells from excised tumors and draining lymph nodes. Results show an influx of activated cytotoxic T cells, alongside an increase in proliferating regulatory T cells, following treatment. Complementary changes are found in draining lymph nodes. In conclusion, results indicate that biologically reactive MH is achievable in vivo and can generate localized changes consistent with an anti-tumor immune response.
Identifiants
pubmed: 33734595
doi: 10.1002/smll.202005241
doi:
Substances chimiques
Ferric Compounds
0
Magnetite Nanoparticles
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e2005241Subventions
Organisme : Medical Research Council
ID : G1001497
Pays : United Kingdom
Organisme : Wellcome Trust
ID : WT 088641/Z/09/Z
Pays : United Kingdom
Organisme : Cancer Research UK Accelerator
ID : Cl 15121 A 20256
Informations de copyright
© 2021 The Authors. Small published by Wiley-VCH GmbH.
Références
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, X.-J. Liang, Theranostics 2020, 10, 3793.
P. Wust, B. Hildebrandt, G. Sreenivasa, B. Rau, J. Gellermann, H. Riess, R. Felix, P. M. Schlag, Lancet Oncol. 2002, 3, 487.
M. Hurwitz, P. Stauffer, Semin. Oncol. 2014, 41, 714.
R. D. Issels, Eur. J. Cancer 2008, 44, 2546.
V. Bücklein, C. Limmroth, E. Kampmann, G. Schuebbe, R. Issels, F. Roeder, M. Angele, H. Roland Dürr, T. Knösel, S. Abdel-Rahman, D. Di Gioia, L. H. Lindner, Sarcoma 2020, 2020, 6901678.
R. D. Issels, L. H. Lindner, J. Verweij, R. Wessalowski, P. Reichardt, P. Wust, P. Ghadjar, P. Hohenberger, M. Angele, C. Salat, Z. Vujaskovic, S. Daugaard, O. Mella, U. Mansmann, H. R. Dürr, T. Knösel, S. Abdel-Rahman, M. Schmidt, W. Hiddemann, K.-W. Jauch, C. Belka, A. Gronchi, JAMA Oncol. 2018, 4, 483.
V. Vilas-Boas, F. Carvalho, B. Espiña, Molecules 2020, 25, 2874.
S. K. Sharma, N. Shrivastava, F. Rossi, L. D. Tung, N. T. K. Thanh, Nano Today 2019, 29, 100795.
D. Haemmerich, P. F. Laeseke, Int. J. Hyperthermia 2005, 21, 755.
K. F. Chu, D. E. Dupuy, Nat. Rev. Cancer 2014, 14, 199.
P.-y Pu, Y.-z. Zhang, D.-h. Jiang, Chin. J. Cancer Res. 2000, 12, 257.
S. S. Evans, E. A. Repasky, D. T. Fisher, Nat. Rev. Immunol. 2015, 15, 335.
E. A. Repasky, S. S. Evans, M. W. Dewhirst, Cancer Immunol. Res. 2013, 1, 210.
D. T. Fisher, Q. Chen, J. J. Skitzki, J. B. Muhitch, L. Zhou, M. M. Appenheimer, T. D. Vardam, E. L. Weis, J. Passanese, W.-C. Wang, S. O. Gollnick, M. W. Dewhirst, S. Rose-John, E. A. Repasky, H. Baumann, S. S. Evans, J. Clin. Invest. 2011, 121, 3846.
R. D. Issels, L. H. Lindner, M. Von Bergwelt-Baildon, P. Lang, C. Rischpler, H. Diem, B. Mosetter, J. Eckl, D. J. Schendel, C. Salat, O. Stötzer, S. Burdach, I. Von Luettichau-Teichert, R. Handgretinger, J. Neumann, T. Kirchner, K. Steiger, M. Boxberg, U. Mansmann, G. Multhoff, E. Noessner, Int. J. Hyperthermia 2020, 37, 55.
T. Carter, P. Mulholland, K. Chester, Immunotherapy 2016, 8, 941.
I. Elsayed, X. Huang, M. Elsayed, Cancer Lett. 2006, 239, 129.
X. Huang, I. H. El-Sayed, W. Qian, M. A. El-Sayed, J. Am. Chem. Soc. 2006, 128, 2115.
C. Fabbro, H. Ali-Boucetta, T. D. Ros, K. Kostarelos, A. Bianco, M. Prato, Chem. Commun. 2012, 48, 3911.
M. Shevtsov, G. Multhoff, Curr. Drug Metab. 2016, 17, 737.
M. Shevtsov, S. Stangl, B. Nikolaev, L. Yakovleva, Y. Marchenko, R. Tagaeva, W. Sievert, E. Pitkin, A. Mazur, P. Tolstoy, O. Galibin, V. Ryzhov, K. Steiger, O. Smirnov, W. Khachatryan, K. Chester, G. Multhoff, Small 2019, 15, 1900205.
A. K. Gupta, M. Gupta, Biomaterials 2005, 26, 3995.
R. Weissleder, M. Nahrendorf, M. J. Pittet, Nat. Mater. 2014, 13, 125.
T. Y. Tang, S. P. S. Howarth, S. R. Miller, M. J. Graves, A. J. Patterson, J.-M. U-King-Im, Z. Y. Li, S. R. Walsh, A. P. Brown, P. J. Kirkpatrick, E. A. Warburton, P. D. Hayes, K. Varty, J. R. Boyle, M. E. Gaunt, A. Zalewski, J. H. Gillard, J. Am. Coll. Cardiol. 2009, 53, 2039.
M. E. Kooi, V. C. Cappendijk, K. B. J. M. Cleutjens, A. G. H. Kessels, P. J. E. H. M. Kitslaar, M. Borgers, P. M. Frederik, M. J. A. P. Daemen, J. M. A. van Engelshoven, Circulation 2003, 107, 2453.
J. M. Richards, S. I. Semple, T. J. MacGillivray, C. Gray, J. P. Langrish, M. Williams, M. Dweck, W. Wallace, G. McKillop, R. T. A. Chalmers, O. J. Garden, D. E. Newby, Circ.: Cardiovasc. Imaging 2011, 4, 274.
J. L. Gaglia, M. Harisinghani, I. Aganj, G. R. Wojtkiewicz, S. Hedgire, C. Benoist, D. Mathis, R. Weissleder, Proc. Natl. Acad. Sci. U. S. A. 2015, 112, 2139.
V. Weissig, T. Pettinger, N. Murdock, Int. J. Nanomed. 2014, 9, 4357.
D. Ortega, Q. A. Pankhurst, in Nanoscience, Vol. 1, (Ed: P. O'Brien), RSC Publishing, London 2012, pp. 60-68.
M. R. A. Abdollah, T. J. Carter, C. Jones, T. L. Kalber, V. Rajkumar, B. Tolner, C. Gruettner, M. Zaw-Thin, J. Baguña Torres, M. Ellis, M. Robson, R. B. Pedley, P. Mulholland, R. T. M. De Rosales, K. A. Chester, ACS Nano 2018, 12, 1156.
R. Goldstein, J. Sosabowski, M. Livanos, J. Leyton, K. Vigor, G. Bhavsar, G. Nagy-Davidescu, M. Rashid, E. Miranda, J. Yeung, B. Tolner, A. Plückthun, S. Mather, T. Meyer, K. Chester, Eur. J. Nucl. Med. Mol. Imaging 2014, 41, 1.
J. Echevarria-Uraga, García-Alonso, Plazaola, Insausti, Etxebarria, Saiz-Lopez, Fernández-Ruanova, Int. J. Nanomed. 2012, 7, 2399.
S. Wilhelm, A. J. Tavares, Q. Dai, S. Ohta, J. Audet, H. F. Dvorak, W. C. W. Chan, Nat. Rev. Mater. 2016, 1, 16014.
M. Torrice, ACS Cent. Sci. 2016, 2, 434.
A. Jordan, R. Scholz, K. Maier-Hauff , F. K. H. van Landeghem, N. Waldoefner, U. Teichgraeber, J. Pinkernelle, H. Bruhn, F. Neumann, B. Thiesen, A. Von Deimling, R. Felix, J. Neuro-Oncol. 2006, 78, 7.
K. Maier-Hauff, F. Ulrich, D. Nestler, H. Niehoff, P. Wust, B. Thiesen, H. Orawa, V. Budach, A. Jordan, J. Neuro-Oncol. 2011, 103, 317.
K. Maier-Hauff, R. Rothe, R. Scholz, U. Gneveckow, P. Wust, B. Thiesen, A. Feussner, A. Von Deimling, N. Waldoefner, R. Felix, A. Jordan, J. Neuro-Oncol. 2007, 81, 53.
F. K. H. van Landeghem, K. Maier-Hauff, A. Jordan, K.-T. Hoffmann, U. Gneveckow, R. Scholz, B. Thiesen, W. Brück, A. Von Deimling, Biomaterials 2009, 30, 52.
T. Kobayashi, K. Kakimi, E. Nakayama, K. Jimbow, Nanomedicine 2014, 9, 1715.
A. Mukhopadhaya, J. Mendecki, X. Dong, L. Liu, S. Kalnicki, M. Garg, A. Alfieri, C. Guha, Cancer Res. 2007, 67, 7798.
C. Garrido, M. Brunet, C. Didelot, Y. Zermati, E. Schmitt, G. Kroemer, Cell Cycle 2006, 5, 2592.
J. R. Ostberg, E. Kabingu, E. A. Repasky, Int. J. Hyperthermia 2003, 19, 520.
M. Nishikawa, S. Takemoto, Y. Takakura, Int. J. Pharm. 2008, 354, 23.
P. Li, J. L. Gregg, N. Wang, D. Zhou, P. O'donnell, J. S. Blum, V. L. Crotzer, Immunol. Rev. 2005, 207, 206.
T. Chen, J. Guo, C. Han, M. Yang, X. Cao, J. Immunol. 2009, 182, 1449.
M. Shevtsov, G. Multhoff, Front. Immunol. 2016, 7, 171.
M. Muthana, G. Multhoff, A. Graham Pockley, Int. J. Hyperthermia 2010, 26, 247.
I. Sato, M. Umemura, K. Mitsudo, M. Kioi, H. Nakashima, T. Iwai, X. Feng, K. Oda, A. Miyajima, A. Makino, M. Iwai, T. Fujita, U. Yokoyama, S. Okumura, M. Sato, H. Eguchi, I. Tohnai, Y. Ishikawa, J. Physiol. Sci. 2014, 64, 177.
A. J. Giustini, R. Ivkov, P. J. Hoopes, Nanotechnology 2011, 22, 345101.
E. Boros, A. M. Bowen, L. Josephson, N. Vasdev, J. P. Holland, Chem. Sci. 2015, 6, 225.
B. M. Skinner, E. E. P. Johnson, Chromosoma 2017, 126, 195.
M. A. Shevtsov, B. P. Nikolaev, V. A. Ryzhov, L. Y. Yakovleva, A. V. Dobrodumov, Y. Y. Marchenko, B. A. Margulis, E. Pitkin, I. V. Guzhova, J. Magn. Magn. Mater. 2015, 388, 123.
V. Ryzhov, I. Larionov, V. Fomichev, J. Tech. Phys. 1996, 41, 620.
V. Ryzhov, V. A. Ryzhov, I. A. Kiselev, O. P. Smirnov, Y. P. Chernenkov, V. V. Deriglazov, Y. Y. Marchenko, L. Y. Yakovleva, B. P. Nikolaev, Y. V. Bogachev, arXiv preprint arXiv:1712.07534 2017.
E. K. Schlachter, H. R. Widmer, A. Bregy, T. Lönnfors-Weitzel, I. Vajtai, N. Corazza, V. J. P. Bernau, T. Weitzel, P. Mordasini, J. Slotboom, G. Herrmann, S. Bogni, H. Hofmann, M. Frenz, M. Reinert, Int. J. Nanomed. 2011, 6, 1793.
L.i Li, W. Jiang, K. Luo, H. Song, F. Lan, Y. Wu, Z. Gu, Theranostics 2013, 3, 595.
C. Xu, D. Miranda-Nieves, J. A. Ankrum, M. E. Matthiesen, J. A. Phillips, I. Roes, G. R. Wojtkiewicz, V. Juneja, J. R. Kultima, W. Zhao, P. K. Vemula, C. P. Lin, M. Nahrendorf, J. M. Karp, Nano Lett. 2012, 12, 4131.
J. W. M. Bulte, D. L. Kraitchman, NMR Biomed. 2004, 17, 484.
S. Balivada, R. S. Rachakatla, H. Wang, T. N. Samarakoon, R. K. Dani, M. Pyle, F. O. Kroh, B. Walker, X. Leaym, O. B. Koper, M. Tamura, V. Chikan, S. H. Bossmann, D. L. Troyer, BMC Cancer 2010, 10, 119.
M. Johannsen, B. Thiesen, A. Jordan, K. Taymoorian, U. Gneveckow, N. Waldöfner, R. Scholz, M. Koch, M. Lein, K. Jung, S. A. Loening, Prostate 2005, 64, 283.
A. Jordan, R. Scholz, P. Wust, H. Fähling, J. Krause, W. Wlodarczyk, B. Sander, T.h. Vogl, R. Felix, Int. J. Hyperthermia 1997, 13, 587.
S. J. DeNardo, G. L. DeNardo, A. Natarajan, L. A. Miers, A. R. Foreman, C. Gruettner, G. N. Adamson, R. Ivkov, J. Nucl. Med. 2007, 48, 437.
G. D. Lianos, G. A. Alexiou, A. Mangano, A. Mangano, S. Rausei, L. Boni, G. Dionigi, D. H. Roukos, Cancer Lett. 2015, 360, 114.
M. Nishikawa, S. Takemoto, Y. Takakura, Int. J. Pharm. 2008, 354, 23.
Y. Delneste, V. Larochette, P. Jeannin, in HSP70 in Human Diseases and Disorders, Springer, Berlin 2018, pp. 173-203.
H. M. Beere, B. B. Wolf, K. Cain, D. D. Mosser, A. Mahboubi, T. Kuwana, P. Tailor, R. I. Morimoto, G. M. Cohen, D. R. Green, Nat. Cell Biol. 2000, 2, 469.
N. R. Datta, S. Krishnan, D. E. Speiser, E. Neufeld, N. Kuster, S. Bodis, H. Hofmann, Cancer Treat. Rev. 2016, 50, 217.
M. W. Dewhirst, C.-T. Lee, K. A. Ashcraft, Int. J. Hyperthermia 2016, 32, 4.
T. Weiss, M. Weller, P. Roth, Expert Rev. Anticancer Ther. 2016, 16, 1087.
N. D. Pennock, J. T. White, E. W. Cross, E. E. Cheney, B. A. Tamburini, R. M. Kedl, Adv. Physiol. Educ. 2013, 37, 273.
J. Yang, M. Hou, W. Sun, Q. Wu, J. Xu, L. Xiong, Y. Chai, Y. Liu, M. Yu, H. Wang, Z. P. Xu, X. Liang, C. Zhang, Adv. Sci. 2020, 7, 2001088.
R. C. Mould, A. W. K. Auyeung, J. P. Van Vloten, L. Susta, A. J. Mutsaers, J. J. Petrik, G. A. Wood, S. K. Wootton, K. Karimi, B. W. Bridle, Sci. Rep. 2017, 7, 8322.
T. F. Gajewski, H. Schreiber, Y.-X. Fu, Nat. Immunol. 2013, 14, 1014.
S. Spranger, R. M. Spaapen, Y. Zha, J. Williams, Y. Meng, T. T. Ha, T. F. Gajewski, Sci. Transl. Med. 2013, 5, 200ra116.
K. Catakovic, E. Klieser, D. Neureiter, R. Geisberger, Cell Commun. Signaling 2017, 15, 1.
M. Ahmadzadeh, L. A. Johnson, B. Heemskerk, J. R. Wunderlich, M. E. Dudley, D. E. White, S. A. Rosenberg, Blood 2009, 114, 1537.
N. S. Joshi, E. H. Akama-Garren, Y. Lu, D.-Y. Lee, G. P. Chang, A. Li, M. Dupage, T. Tammela, N. R. Kerper, A. F. Farago, R. Robbins, D. M. Crowley, R. T. Bronson, T. Jacks, Immunity 2015, 43, 579.
L. Zou, H. Wang, B. He, L. Zeng, T. Tan, H. Cao, X. He, Z. Zhang, S. Guo, Y. Li, Theranostics 2016, 6, 762.
K. P. Tamarov, L. A. Osminkina, S. V. Zinovyev, K. A. Maximova, J. V. Kargina, M. B. Gongalsky, Y. Ryabchikov, A. Al-Kattan, A. P. Sviridov, M. Sentis, A. V. Ivanov, V. N. Nikiforov, A. V. Kabashin, V. Y. Timoshenko, Sci. Rep. 2014, 4, 7034.
K. Mahmoudi, A. Bouras, D. Bozec, R. Ivkov, C. Hadjipanayis, Int. J. Hyperthermia 2018, 34, 1316.
P. Walter, D. Ron, Science 2011, 334, 1081.
B. Frey, E.-M. Weiss, Y. Rubner, R. Wunderlich, O. J. Ott, R. Sauer, R. Fietkau, U. S. Gaipl, Int. J. Hyperthermia 2012, 28, 528.
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, S. Fiering, Nanomed.: Nanotechnol., Biol. Med. 2014, 10, 1273.
A. J. Moy, J. W. Tunnell, Adv. Drug Delivery Rev. 2017, 114, 175.
C. Wang, L. Xu, C. Liang, J. Xiang, R. Peng, Z. Liu, Adv. Mater. 2014, 26, 8154.
J. Cano-Mejia, R. A. Burga, E. E. Sweeney, J. P. Fisher, C. M. Bollard, A. D. Sandler, C. R. Y. Cruz, R. Fernandes, Nanomed.: Nanotechnol., Biol. Med. 2017, 13, 771.
Q. Chen, L. Xu, C. Liang, C. Wang, R. Peng, Z. Liu, Nat. Commun. 2016, 7, 13193.
Q. Chen, Q. Hu, E. Dukhovlinova, G. Chen, S. Ahn, C. Wang, E. A. Ogunnaike, F. S. Ligler, G. Dotti, Z. Gu, Adv. Mater. 2019, 31, 1900192.
A. Mantovani, F. Marchesi, A. Malesci, L. Laghi, P. Allavena, Nat. Rev. Clin. Oncol. 2017, 14, 399.
P.-L. Loyher, J. Rochefort, C. Baudesson De Chanville, P. Hamon, G. Lescaille, C. Bertolus, M. Guillot-Delost, M. F. Krummel, F. M. Lemoine, C. Combadière, A. Boissonnas, Cancer Res. 2016, 76, 6483.
S. Dimeloe, C. Frick, M. Fischer, P. M. Gubser, L. Razik, G. R. Bantug, M. Ravon, A. Langenkamp, C. Hess, Eur. J. Immunol. 2014, 44, 3614.
D. J. Huss, A. F. Pellerin, B. P. Collette, A. K. Kannan, L. Peng, A. Datta, B. T. Wipke, J. D. Fontenot, Immunology 2016, 148, 276.
A. El Andaloussi, Y. Han, M. S. Lesniak, J. Neurosurg. 2006, 105, 430.