Combining magnetic hyperthermia and photodynamic therapy for tumor ablation with photoresponsive magnetic liposomes

ACS Nano

Volumn 9, Issue 3, 2015, Pages 2904-2916

  Di Corato, Riccardo ^a   Béalle, Gaëlle ^b   Kolosnjaj Tabi, Jelena ^a,c   Espinosa, Ana ^a   Clément, Olivier ^c   Silva, Amanda K A ^a   Ménager, Christine ^b   Wilhelm, Claire ^a  

^a UNIVERSITÉ PARIS DIDEROT   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c PARIS CARDIOVASCULAR RESEARCH CENTER   (France)

Author keywords

cancer combined therapy; liposomes; magnetic hyperthermia; magnetic nanoparticles; photodynamic therapy; photosensitizer

Indexed keywords

ABLATION; CELL DEATH; CHEMOTHERAPY; DIAGNOSIS; DISEASES; HYPERTHERMIA THERAPY; IRON OXIDES; LASER EXCITATION; LIPID BILAYERS; LIPOSOMES; MAGNETIC NANOPARTICLES; MAGNETISM; PHOTOSENSITIZERS; TUMORS;

ALTERNATING MAGNETIC FIELD; COMBINED THERAPY; IRON OXIDE NANOPARTICLE; MAGNETIC HYPERTHERMIA; MAGNETIC LIPOSOMES; PHOTODYNAMIC THERAPY (PDT); THERAPEUTIC AGENTS; THERAPEUTIC METHOD;

PHOTODYNAMIC THERAPY;

LIPOSOME; MESOPORPHYRIN; NANOPARTICLE; PHOTOSENSITIZING AGENT; SINGLET OXYGEN; TEMOPORFIN;

ABLATION THERAPY; ANIMAL; CARCINOMA, SQUAMOUS CELL; CELL DEATH; CHEMICAL STRUCTURE; CHEMISTRY; CONFORMATION; DRUG EFFECTS; DRUG RELEASE; FEMALE; HUMAN; HYPERTHERMIC THERAPY; MAGNET; METABOLISM; MOUSE; MULTIMODALITY CANCER THERAPY; NANOMEDICINE; PATHOLOGY; PHOTOCHEMOTHERAPY; PROCEDURES; RADIATION RESPONSE; TRANSPORT AT THE CELLULAR LEVEL; TUMOR CELL LINE;

ABLATION TECHNIQUES; ANIMALS; BIOLOGICAL TRANSPORT; CARCINOMA, SQUAMOUS CELL; CELL DEATH; CELL LINE, TUMOR; COMBINED MODALITY THERAPY; DRUG LIBERATION; FEMALE; HUMANS; HYPERTHERMIA, INDUCED; LIPOSOMES; MAGNETS; MESOPORPHYRINS; MICE; MODELS, MOLECULAR; MOLECULAR CONFORMATION; NANOMEDICINE; NANOPARTICLES; PHOTOCHEMOTHERAPY; PHOTOSENSITIZING AGENTS; SINGLET OXYGEN;

EID: 84925624106     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/nn506949t     Document Type: Article

References (52)

1. Pavet, V.; Portal, M.; Moulin, J.; Herbrecht, R.; Gronemeyer, H. Towards Novel Paradigms for Cancer Therapy Oncogene 2011, 30, 1-20
2. Lee, P. Y.; Wong, K. K. Nanomedicine: A New Frontier in Cancer Therapeutics Curr. Drug Delivery 2011, 8, 245-253
3. Albini, A.; Pennesi, G.; Donatelli, F.; Cammarota, R.; De Flora, S.; Noonan, D. M. Cardiotoxicity of Anticancer Drugs: The Need for Cardio-oncology and Cardio-oncological Prevention J. Natl. Cancer Inst. 2010, 102, 14-25
4. Bertrand, N.; Wu, J.; Xu, X.; Kamaly, N.; Farokhzad, O. C. Cancer Nanotechnology: The Impact of Passive and Active Targeting in the Era of Modern Cancer Biology Adv. Drug Delivery Rev. 2014, 66, 2-25
5. Maherani, B.; Arab-Tehrany, E.; Mozafari, M.; Gaiani, C.; Linder, M. Liposomes: A Review of Manufacturing Techniques and Targeting Strategies Curr. Nanosci. 2011, 7, 436-452
6. Torchilin, V. P.; Omelyanenko, V. G.; Papisov, M. I.; Bogdanov, A. A., Jr.; Trubetskoy, V. S.; Herron, J. N.; Gentry, C. A. Poly(ethylene glycol) on the Liposome Surface: On the Mechanism of Polymer-Coated Liposome Longevity Biochim. Biophys. Acta, Biomembr. 1994, 1195, 11-20
7. Martina, M. S.; Nicolas, V.; Wilhelm, C.; Ménager, C.; Barratt, G.; Lesieur, S. The In Vitro Kinetics of the Interactions between PEG-ylated Magnetic-Fluid-Loaded Liposomes and Macrophages Biomaterials 2007, 28, 4143-4153
8. Sawant, R. R.; Torchilin, V. P. Challenges in Development of Targeted Liposomal Therapeutics AAPS J. 2012, 14, 303-315
9. Peer, D.; Karp, J. M.; Hong, S.; Farokhzad, O. C.; Margalit, R.; Langer, R. Nanocarriers as an Emerging Platform for Cancer Therapy Nat. Nanotechnol. 2007, 2, 751-760
10. Chang, H. I.; Yeh, M. K. Clinical Development of Liposome-Based Drugs: Formulation, Characterization, and Therapeutic Efficacy Int. J. Nanomed. 2012, 7, 49-60
11. Ganta, S.; Devalapally, H.; Shahiwala, A.; Amiji, M. A Review of Stimuli-Responsive Nanocarriers for Drug and Gene Delivery J. Controlled Release 2008, 126, 187-204
12. Brown, S. B.; Brown, E. A.; Walker, I. The Present and Future Role of Photodynamic Therapy in Cancer Treatment Lancet Oncol. 2004, 5, 497-508
13. Tu, H. L.; Lin, Y. S.; Lin, H. Y.; Hung, Y.; Lo, L. W.; Chen, Y. F.; Mou, C. Y. In Vitro Studies of Functionalized Mesoporous Silica Nanoparticles for Photodynamic Therapy Adv. Mater. 2009, 21, 172-177
14. Taillefer, J.; Brasseur, N.; van Lier, J. E.; Lenaerts, V.; Garrec, D. L.; Leroux, J. C. In-Vitro and In-Vivo Evaluation of pH-Responsive Polymeric Micelles in a Photodynamic Cancer Therapy Model J. Pharm. Pharmacol. 2001, 53, 155-166
15. Fowley, C.; Nomikou, N.; McHale, A. P.; McCaughan, B.; Callan, J. F. Extending the Tissue Penetration Capability of Conventional Photosensitisers: A Carbon Quantum Dot-Protoporphyrin IX Conjugate for Use in Two-Photon Excited Photodynamic Therapy Chem. Commun. 2013, 49, 8934-8936
16. Choi, W. I.; Kim, J. Y.; Kang, C.; Byeon, C. C.; Kim, Y. H.; Tae, G. Tumor Regression in Vivo by Photothermal Therapy Based on Gold-Nanorod-Loaded, Functional Nanocarriers ACS Nano 2011, 5, 1995-2003
17. Cole, J. R.; Mirin, N. A.; Knight, M. W.; Goodrich, G. P.; Halas, N. J. Photothermal Efficiencies of Nanoshells and Nanorods for Clinical Therapeutic Applications J. Phys. Chem. C 2009, 113, 12090-12094
18. Zhang, Z.; Wang, J.; Chen, C. Near-Infrared Light-Mediated Nanoplatforms for Cancer Thermo-Chemotherapy and Optical Imaging Adv. Mater. 2013, 25, 3869-3880
19. Schnarr, K.; Mooney, R.; Weng, Y. M.; Zhao, D. H.; Garcia, E.; Armstrong, B.; Annala, A. J.; Kim, S. U.; Aboody, K. S.; Berlin, J. M. Gold Nanoparticle-Loaded Neural Stem Cells for Photothermal Ablation of Cancer Adv. Healthcare Mater. 2013, 2, 976-982
20. Shen, H. F.; You, J.; Zhang, G. D.; Ziemys, A.; Li, Q. P.; Bai, L. T.; Deng, X. Y.; Erm, D. R.; Liu, X. W.; Li, C. Cooperative, Nanoparticle-Enabled Thermal Therapy of Breast Cancer Adv. Healthcare Mater. 2012, 1, 84-89
21. Johannsen, M.; Gneveckow, U.; Eckelt, L.; Feussner, A.; Waldöfner, N.; Scholz, R.; Deger, S.; Wust, P.; Loening, S.; Jordan, A. Clinical Hyperthermia of Prostate Cancer Using Magnetic Nanoparticles: Presentation of a New Interstitial Technique Int. J. Hyperthermia 2005, 21, 637-647
22. 4 Composite Nanospheres for In Vivo Imaging and Hyperthermia Adv. Mater. 2009, 21, 2170-2173
23. Brulé, S.; Levy, M.; Wilhelm, C.; Letourneur, D.; Gazeau, F.; Ménager, C.; Le Visage, C. Doxorubicin Release Triggered by Alginate Embedded Magnetic Nanoheaters: A Combined Therapy Adv. Mater. 2011, 23, 787-790
24. Lopez-Noriega, A.; Hastings, C. L.; Ozbakir, B.; ODonnell, K. E.; OBrien, F. J.; Storm, G.; Hennink, W. E.; Duffy, G. P.; Ruiz-Hernandez, E. Hyperthermia-Induced Drug Delivery from Thermosensitive Liposomes Encapsulated in an Injectable Hydrogel for Local Chemotherapy Adv. Healthcare Mater. 2014, 3, 854-859
25. Kolosnjaj-Tabi, J.; Di Corato, R.; Lartigue, L.; Marangon, I.; Guardia, P.; Silva, A. K. A.; Luciani, N.; Clement, O.; Flaud, P.; Singh, J. V. Heat-Generating Iron Oxide Nanocubes: Subtle "Destructurators" of the Tumoral Microenvironment ACS Nano 2014, 8, 4268-4283
26. Bovis, M. J.; Woodhams, J. H.; Loizidou, M.; Scheglmann, D.; Bown, S. G.; MacRobert, A. J. Improved In Vivo Delivery of M-Thpc via Pegylated Liposomes for Use in Photodynamic Therapy J. Controlled Release 2012, 157, 196-205
27. Amstad, E.; Kohlbrecher, J.; Müller, E.; Schweizer, T.; Textor, M.; Reimhult, E. Triggered Release from Liposomes through Magnetic Actuation of Iron Oxide Nanoparticle Containing Membranes Nano Lett. 2011, 11, 1664-1670
28. Soenen, S. J.; Velde, G. V.; Ketkar-Atre, A.; Himmelreich, U.; De Cuyper, M. Magnetoliposomes as Magnetic Resonance Imaging Contrast Agents Wiley Interdiscip. Rev.: Nanomed. Nanobiotechnol. 2011, 3, 197-211
29. Mikhaylov, G.; Mikac, U.; Magaeva, A. A.; Itin, V. I.; Naiden, E. P.; Psakhye, I.; Babes, L.; Reinheckel, T.; Peters, C.; Zeiser, R. Ferri-liposomes as an MRI-Visible Drug-Delivery System for Targeting Tumours and Their Microenvironment Nat. Nanotechnol. 2011, 6, 594-602
30. Béalle, G.; Di Corato, R.; Kolosnjaj-Tabi, J.; Dupuis, V.; Clément, O.; Gazeau, F.; Wilhelm, C.; Ménager, C. Ultra Magnetic Liposomes for MR Imaging, Targeting, and Hyperthermia Langmuir 2012, 28, 11834-11842
31. Yanase, M.; Shinkai, M.; Honda, H.; Wakabayashi, T.; Yoshida, J.; Kobayashi, T. Intracellular Hyperthermia for Cancer Using Magnetite Cationic Liposomes: An In Vivo Study Cancer Sci. 1998, 89, 463-470
32. Pradhan, P.; Giri, J.; Rieken, F.; Koch, C.; Mykhaylyk, O.; Döblinger, M.; Banerjee, R.; Bahadur, D.; Plank, C. Targeted Temperature Sensitive Magnetic Liposomes for Thermo-Chemotherapy J. Controlled Release 2010, 142, 108-121
33. Senge, M. O.; Brandt, J. C. Temoporfin (Foscan®, 5,10,15,20-Tetra(m-hydroxyphenyl)chlorin)-A Second-Generation Photosensitizer Photochem. Photobiol. 2011, 87, 1240-1296
34. Karakullukcu, B.; Nyst, H. J.; van Veen, R. L.; Hoebers, F. J.; Hamming-Vrieze, O.; Witjes, M. J.; de Visscher, S. A.; Burlage, F. R.; Levendag, P. C.; Sterenborg, H. J. mTHPC Mediated Interstitial Photodynamic Therapy of Recurrent Nonmetastatic Base of Tongue Cancers: Development of a New Method Head Neck 2012, 34, 1597-1606
35. Fayol, D.; Luciani, N.; Lartigue, L.; Gazeau, F.; Wilhelm, C. Managing Magnetic Nanoparticle Aggregation and Cellular Uptake: A Precondition for Efficient Stem-Cell Differentiation and MRI Tracking Adv. Healthcare Mater. 2013, 2, 313-325
36. Aubertin, K.; Bonneau, S.; Silva, A. K. A.; Bacri, J.-C.; Gallet, F.; Wilhelm, C. Impact of Photosensitizers Activation on Intracellular Trafficking and Viscosity PLoS One 2013, 8, e84850
37. Das, K.; Dube, A.; Gupta, P. A Spectroscopic Study of Photobleaching of Chlorin P6 in Different Environments Dyes Pigm. 2005, 64, 201-205
38. Busch, T. M.; Hahn, S. M.; Evans, S. M.; Koch, C. J. Depletion of Tumor Oxygenation during Photodynamic Therapy: Detection by the Hypoxia Marker Ef3 [2-(2-Nitroimidazol-1[H]-Yl)- N -(3,3,3-trifluoropropyl)acetamide] Cancer Res. 2000, 60, 2636-2642
39. Orenstein, A.; Kostenich, G.; Kopolovic, Y.; Babushkina, T.; Malik, Z. Enhancement of Ala-PDT Damage by IR-Induced Hyperthermia on a Colon Carcinoma Model Photochem. Photobiol. 1999, 69, 703-707
40. Yanase, S.; Nomura, J.; Matsumura, Y.; Nagata, T.; Fujii, T.; Tagawa, T. Synergistic Interaction of 5-Aminolevulinic Acid-Based Photodynamic Therapy with Simultaneous Hyperthermia in an Osteosarcoma Tumor Model Int. J. Oncol. 2006, 29, 365-373
41. Frank, J.; Lambert, C.; Biesalski, H. K.; Thews, O.; Vaupel, P.; Kelleher, D. K. Intensified Oxidative and Nitrosative Stress Following Combined Ala-Based Photodynamic Therapy and Local Hyperthermia in Rat Tumors Int. J. Cancer 2003, 107, 941-948
42. Lin, J.; Wang, S.; Huang, P.; Wang, Z.; Chen, S.; Niu, G.; Li, W.; He, J.; Cui, D.; Lu, G. Photosensitizer-Loaded Gold Vesicles with Strong Plasmonic Coupling Effect for Imaging-Guided Photothermal/Photodynamic Therapy ACS Nano 2013, 7, 5320-5329
43. Jang, B.; Park, J.-Y.; Tung, C.-H.; Kim, I.-H.; Choi, Y. Gold Nanorod-Photosensitizer Complex for Near-Infrared Fluorescence Imaging and Photodynamic/Photothermal Therapy in Vivo ACS Nano 2011, 5, 1086-1094
44. Wang, J.; Zhu, G.; You, M.; Song, E.; Shukoor, M. I.; Zhang, K.; Altman, M. B.; Chen, Y.; Zhu, Z.; Huang, C. Z. Assembly of Aptamer Switch Probes and Photosensitizer on Gold Nanorods for Targeted Photothermal and Photodynamic Cancer Therapy ACS Nano 2012, 6, 5070-5077
45. Wang, S.; Huang, P.; Nie, L.; Xing, R.; Liu, D.; Wang, Z.; Lin, J.; Chen, S.; Niu, G.; Lu, G. Single Continuous Wave Laser Induced Photodynamic/Plasmonic Photothermal Therapy Using Photosensitizer-Functionalized Gold Nanostars Adv. Mater. 2013, 25, 3055-3061
46. Oliveira, D. M.; Macaroff, P. P.; Ribeiro, K. F.; Lacava, Z. G. M.; Azevedo, R. B.; Lima, E. C. D.; Morais, P. C.; Tedesco, A. C. Studies of Zinc Phthalocyanine/Magnetic Fluid Complex as a Bifunctional Agent for Cancer Treatment J. Magn. Magn. Mater. 2005, 289, 476-479
47. Corr, S. A.; OByrne, A.; Gunko, Y. K.; Ghosh, S.; Brougham, D. F.; Mitchell, S.; Volkov, Y.; Prina-Mello, A. Magnetic-Fluorescent Nanocomposites for Biomedical Multitasking Chem. Commun. 2006, 43, 4474-4476
48. de Paula, L. B.; Primo, F. L.; Jardim, D. R.; Morais, P. C.; Tedesco, A. C. Development, Characterization, and In Vitro Trials of Chloroaluminum Phthalocyanine-Magnetic Nanoemulsion to Hyperthermia and Photodynamic Therapies on Glioblastoma as a Biological Model J. Appl. Phys. 2012, 111, 07B307
49. Bolfarini, G. C.; Siqueira-Moura, M. P.; Demets, G. J. F.; Morais, P. C.; Tedesco, A. C. In Vitro Evaluation of Combined Hyperthermia and Photodynamic Effects Using Magnetoliposomes Loaded with Cucurbit 7 Uril Zinc Phthalocyanine Complex on Melanoma J. Photochem. Photobiol., B 2012, 115, 1-4
50. Massart, R. Preparation of Aqueous Magnetic Liquids in Alkaline and Acidic Media IEEE Trans. Magn. 1981, 17, 1247-1248
51. Szoka, F.; Papahadjopoulos, D. Procedure for Preparation of Liposomes with Large Internal Aqueous Space and High Capture by Reverse-Phase Evaporation Proc. Natl. Acad. Sci. U.S.A. 1978, 75, 4194-4198
52. Rouser, G.; Fleischer, S.; Yamamoto, A. Two Dimensional Thin Layer Chromatographic Separation of Polar Lipids and Determination of Phospholipids by Phosphorus Analysis of Spots Lipids 1970, 5, 494-496