Nanohybrid liposomal cerasomes with good physiological stability and rapid temperature responsiveness for high intensity focused ultrasound triggered local chemotherapy of cancer

ACS Nano

Volumn 9, Issue 2, 2015, Pages 1280-1293

  Liang, Xiaolong ^a   Gao, Jing ^b   Jiang, Lingdong ^c   Luo, Jianwen ^b   Jing, Lijia ^c   Li, Xiaoda ^c   Jin, Yushen ^c   Dai, Zhifei ^a  

^a PEKING UNIVERSITY   (China)

^b Tsinghua University   (China)

^c HARBIN INSTITUTE OF TECHNOLOGY   (China)

Author keywords

cerasomes; high intensity focused ultrasound; local chemotherapy; thermosensitive liposome; triggered drug release

Indexed keywords

BIOCOMPATIBILITY; CARDIOVASCULAR SYSTEM; CHEMOTHERAPY; DISEASES; DRUG INTERACTIONS; HYDROPHILICITY; LIPOSOMES; MAMMALS; MOLAR RATIO; TARGETED DRUG DELIVERY; TEMPERATURE; TUMORS; ULTRASONICS;

1 ,2-DIPALMITOYL-SN-GLYCERO-3-PHOSPHOCHOLINE; CERASOMES; HIGH INTENSITY FOCUSED ULTRASOUND; INTRAVENOUS INJECTIONS; SYSTEMIC ADMINISTRATION; THERAPEUTIC EFFICACY; THERMOSENSITIVE LIPOSOMES; TRIGGERED DRUG RELEASE;

CONTROLLED DRUG DELIVERY;

ANTINEOPLASTIC AGENT; BIOMATERIAL; DOXORUBICIN; GLYCEROPHOSPHOLIPID; LIPID BILAYER; LIPOSOME; NANOMATERIAL;

ANIMAL; CELL SURVIVAL; CHEMICAL PHENOMENA; CHEMICAL STRUCTURE; CHEMISTRY; CONFORMATION; DRUG EFFECTS; DRUG RELEASE; DRUG STABILITY; FEMALE; HUMAN; LIPID BILAYER; MOUSE; NEOPLASMS; PATHOLOGY; RAT; TEMPERATURE; TUMOR CELL LINE; ULTRASOUND;

ANIMALS; ANTINEOPLASTIC AGENTS; BIOCOMPATIBLE MATERIALS; CELL LINE, TUMOR; CELL SURVIVAL; DOXORUBICIN; DRUG LIBERATION; DRUG STABILITY; FEMALE; GLYCEROPHOSPHOLIPIDS; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; LIPID BILAYERS; LIPOSOMES; MICE; MODELS, MOLECULAR; MOLECULAR CONFORMATION; NANOSTRUCTURES; NEOPLASMS; RATS; TEMPERATURE; ULTRASONIC WAVES;

EID: 84923478202     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/nn507482w     Document Type: Article

References (79)

1. Singal, P. K.; Iliskovic, N. Doxorubicin-Induced Cardiomyopathy N. Engl. J. Med. 1998, 339, 900-905
2. Slamon, D. J.; Leyland-Jones, B.; Shak, S.; Fuchs, H.; Paton, V.; Bajamonde, A.; Fleming, T.; Eiermann, W.; Wolter, J.; Pegram, M. Use of Chemotherapy Plus Amonoclonal Antibody Against HER2 Formetastatic Breast Cancer that Overexpresses HER2 N. Engl. J. Med. 2001, 344, 783-792
3. Kessler, D. A.; Austin, R. H.; Levine, H. Resistance to Chemotherapy: Patient Variability and Cellular Heterogeneity Cancer Res. 2014, 74, 4663-4670
4. Moitra, K.; Lou, H.; Dean, M. Multidrug Efflux Pumps and Cancer Stem Cells: Insights into Multidrug Resistance and Therapeutic Development Clin. Pharmacol. Ther. 2011, 89, 491-502
5. Tan, G. R.; Feng, S. S.; Leong, D. T. The Reduction of Anti-cancer Drug Antagonism by the Spatial Protection of Drugs with PLA-TPGS Nanoparticles Biomaterials 2014, 35, 3044-3051
6. 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
7. Torchilin, V. P. Multifunctional Nanocarriers Adv. Drug Delivery Rev. 2006, 58, 1532-1555
8. Allen, T. M.; Cullis, P. R. Drug Delivery Systems: Entering the Mainstream Science 2004, 303, 1818-1822
9. Liang, X.; Yue, X.; Dai, Z.; Kikuchi, J. Photoresponsive Liposomal Nanohybrid Cerasomes Chem. Commun. 2011, 47, 4751-4753
10. Weinstein, J. N.; Magin, R. L.; Yatvin, M. B.; Zaharko, D. S. Liposomes and Local Hyperthermia: Selective Delivery of Methotrexate to Heated Tumors Sciences 1979, 204, 188-191
11. Alvarez-Lorenzo, C.; Bromberg, L.; Concheiro, A. Light-Sensitive Intelligent Drug Delivery Systems Photochem. Photobiol. 2009, 85, 848-860
12. Tay, C. Y.; Setyawati, M. I.; Xie, J.; Parak, W. J.; Leong, D. T. Back to Basics: Exploiting the Innate Physico-Chemical Characteristics of Nanomaterials for Biomedical Applications Adv. Funct. Mater. 2014, 24, 5936-5955
13. Matsumura, Y.; Maeda, H. A New Concept for Macromolecular Therapeutics in Cancer Chemotherapy: Mechanism of Tumoritropic Accumulation of Proteins and the Antitumor Agent SMANCS Cancer Res. 1986, 46, 6387-6392
14. Maeda, H.; Wu, J.; Sawa, T.; Matsumura, Y.; Hori, K. Tumor Vascular Permeability and the EPR Effect in Macromolecular Therapeutics: A Review J. Controlled Release 2000, 65, 271-284
15. Yu, B.; Tai, H. C.; Xue, W.; Lee, L. J.; Lee, R. J. Receptor Targeted Nanocarriers for Therapeutic Delivery to Cancer Mol. Membr. Biol. 2010, 27, 286-298
16. Setyawati, M. I.; Tay, C. Y.; Chia, S. L.; Goh, S. L.; Fang, W.; Neo, M. J.; Chong, H. C.; Tan, S. M.; Loo, S. C.; Ng, K. W. Titanium Dioxide Nanomaterials Cause Endothelial Cell Leakiness by Disrupting the Homophilic Interaction of VE-Cadherin Nat. Commun. 2013, 4, 1673
17. Setyawati, M. I.; Tay, C. Y.; Leong, D. T. The Gap between Endothelial Cells: Key to the Quick Escape of Nanomaterials? Nanomedicine 2014, 9, 1591-1594
18. Carpentier, A.; Chauvet, D.; Reina, V.; Beccaria, K.; Leclerq, D.; McNichols, R. J.; Gowda, A.; Cornu, P.; Delattre, J. MR-Guided Laser-Induced Thermal Therapy (LITT) for Recurrent Glioblastomas Lasers Surg. Med. 2012, 44, 361-368
19. Fatehi, D.; van der Zee, J.; de Bruijne, M.; Franckena, M.; van Rhoon, G. C. RF-Power and Temperature Data Analysis of 444 Patients With Primary Cervical Cancer: Deep Hyperthermia Using the Sigma-60 Applicator is Reproducible Int. J. Hyperthermia 2007, 23, 623-643
20. Johnson, J. E.; Neuman, D. G.; Maccarini, P. F.; Juang, T.; Stauffer, P. R.; Turner, P. Evaluation of a Dual-Arm Archimedean Spiral Array Formicrowave Hyperthermia Int. J. Hyperthermia 2006, 22, 475-490
21. Salomir, R.; Palussiere, J.; Vimeux, F. C.; de Zwart, J. A.; Quesson, B.; Gauchet, M.; Lelong, P.; Pergrale, J.; Grenier, N.; Moonen, C. T. Local Hyperthermia with MR-guided Focused Ultrasound: Spiral Trajectory of the Focal Point Optimized for Temperature Uniformity in the Target Region J. Magn. Reson. Imaging 2000, 12, 571-583
22. Hamano, N.; Negishi, Y.; Takatori, K.; Endo-Takahashi, Y.; Suzuki, R.; Maruyama, K.; Niidome, T.; Aramaki, Y. Combination Of Bubble Liposomes and High-Intensity Focused Ultrasound (HIFU) Enhanced Antitumor Effect by Tumor Ablation Biol. Pharm. Bull. 2014, 37, 174-177
23. Morawski, A. M.; Lanza, G. A.; Wickline, S. A. Targeted Contrast Agents for Magnetic Resonance Imaging and Ultrasound Curr. Opin. Biotechnol. 2005, 16, 89-92
24. Unezaki, S.; Maruyama, K.; Takahashi, N.; Koyama, M.; Yuda, T.; Suginaka, A.; Iwatsuru, M. Enhanced Delivery and Antitumor Activity of Doxorubicin Using Long Circulating Thermosensitive Liposomes Containing Amphipathic Polyethylene Glycol in Combination with Local Hyperthermia Pharm. Res. 1994, 11, 1180-1185
25. Gaber, M. H.; Wu, N. Z.; Hong, K.; Huang, S. K.; Dewhirst, M. W.; Papahadjopoulos, D. Thermosensitive Liposomes: Extravasation and Release of Contents in Tumor Microvascular Networks Int. J. Radiat. Oncol. Biol. Phys. 1996, 36, 1177-1187
26. Yatvin, M. B.; Weinstein, J. N.; Dennis, W. H.; Blumenthal, R. Design of Liposomes for Enhanced Local Release of Drugs by Hyperthermia Science 1978, 202, 1290-1293
27. Needham, D.; Anyarambhatla, G.; Kong, G.; Dewhirst, M. W. A New Temperature Sensitive Liposome for Use with Mild Hyperthermia: Characterization and Testing in a Human Tumor Xenograft Model Cancer Res. 2000, 60, 1197-1201
28. Kong, G.; Anyarambhatla, G.; Petros, W. P.; Braun, R. D.; Colvin, O. M.; Needham, D.; Dewhirst, M. W. Efficacy of Liposomes and Hyperthermia in a Human Tumor Xenograft Model: Importance of Triggered Drug Release Cancer Res. 2000, 60, 6950-6957
29. Dromi, S.; Frenkel, V.; Luk, A.; Traughber, B.; Angstadt, M.; Bur, M.; Poff, J.; Xie, J.; Libutti, S. K.; Li, K. C. Pulsed-High Intensity Focused Ultrasound and Low Temperature-Sensitive Liposomes for Enhanced Targeted Drug Delivery and Antitumor Effect Clin. Cancer Res. 2007, 13, 2722-2727
30. Ponce, A. M.; Vujaskovic, Z.; Yuan, F.; Needham, D.; Dewhirst, M. W. Hyperthermia Mediated Liposomal Drug Delivery Int. J. Hyperthermia 2006, 22, 205-213
31. Koning, G. A.; Eggermont, A. M.; Lindner, L. H.; ten Hagen, T. L. Hyperthermia and Thermosensitive Liposomes for Improved Delivery of Chemotherapeutic Drugs to Solid Tumors Pharm. Res. 2010, 27, 1750-1754
32. Li, L.; ten Hagen, T. L.; Hossann, M.; Süss, R.; van Rhoon, G. C.; Eggermont, A. M.; Haemmerich, D.; Koning, G. A. Mild Hyperthermia Triggered Doxorubicin Release from Optimized Stealth Thermosensitive Liposomes Improves Intratumoral Drug Delivery and Efficacy J. Controlled Release 2013, 168, 142-150
33. Banno, B.; Ickenstein, L. M.; Chiu, G. N.; Bally, M. B.; Thewalt, J.; Brief, E.; Wasan, E. K. The Functional Roles of Poly(Ethylene Glycol)-Lipid and Lysolipid in the Drug Retention and Release from Lysolipid-Containing Thermosensitive Liposomes in Vitro and in Vivo J. Pharm. Sci. 2010, 99, 2295-2308
34. Mills, J. K.; Needham, D. Lysolipid Incorporation in Dipalmitoylphosphatidylcholine Bilayer Membranes Enhances the Ion Permeability and Drug Release Rates at the Membrane Phase Transition Biochim. Biophys. Acta 2005, 1716, 77-96
35. Ponce, A. M.; Viglianti, B. L.; Yu, D.; Yarmolenko, P. S.; Michelich, C. R.; Woo, J.; Bally, M. B.; Dewhirst, M. W. Magnetic Resonance Imaging of Temperature-Sensitive Liposome Release: Drug Dose Painting and Antitumor Effects J. Natl. Cancer Inst. 2007, 99, 53-63
36. Landon, C. D.; Park, J. Y.; Needham, D.; Dewhirst, M. W. Nanoscale Drug Delivery and Hyperthermia: the Materials Design and Preclinical and Clinical Testing of Low Temperature-Sensitive Liposomes Used in Combination with Mild Hyperthermia in the Treatment of Local Cancer Open Nanomed. J. 2011, 3, 38-64
37. Needham, D.; Park, J. Y.; Wright, A. M.; Tong, J. Materials Characterization of the Low Temperature Sensitive Liposome (LTSL): Effects of the Lipid Composition (Lysolipid and DSPE-PEG-2000) on the Thermal Transition and Release of Doxorubicin Faraday Discuss. 2013, 161, 515-534
38. de Smet, M.; Langereis, S.; van den Bosch, S.; Grull, H. Temperature-Sensitive Liposomes for Doxorubicin Delivery under MRI Guidance J. Controlled Release 2010, 143, 120-127
39. Woo, J.; Chiu, G. N.; Karlsson, G.; Wasan, E.; Ickenstein, L.; Edwards, K.; Bally, M. B. Use of a Passive Equilibration Methodology to Encapsulate Cisplatin into Preformed Thermosensitive Liposomes Int. J. Pharm. 2008, 349, 38-46
40. Kennedy, J. High-Intensity Focused Ultrasound in the Treatment of Solid Tumours Nat. Rev. Cancer 2005, 5, 321-327
41. Wu, J.; Nyborg, W. L. Ultrasound, Cavitation Bubbles and Their Interaction with Cells Adv. Drug Delivery Rev. 2008, 60, 1103-1116
42. Ranjan, A.; Jacobs, G. C.; Woods, D. L.; Negussie, A. H.; Partanen, A.; Yarmolenko, P. S.; Gacchina, C. E.; Sharma, K. V.; Frenkel, V.; Wood, B. J. Image-Guided Drug Delivery with Magnetic Resonance Guided High Intensity Focused Ultrasound and Temperature Sensitive Liposomes in a Rabbit Vx2 Tumor Model J. Controlled Release 2012, 158, 487-494
43. Gasselhuber, A.; Dreher, M. R.; Partanen, A.; Yarmolenko, P. S.; Woods, D.; Wood, B. J.; Haemmerich, D. Targeted Drug Delivery by High Intensity Focused Ultrasound Mediated Hyperthermia Combined with Temperature-Sensitive Liposomes: Computational Modelling and Preliminary in Vivo Validation Int. J. Hyperthermia 2012, 28, 337-348
44. de Smet, M.; Heijman, E.; Langereis, S.; Hijnen, N. M.; Grüll, H. Magnetic Resonance Imaging of High Intensity Focused Ultrasound Mediated Drug Delivery from Temperature-Sensitive Liposomes: An in Vivo Proof-of-Concept Study J. Controlled Release 2011, 150, 102-110
45. Partanen, A.; Yarmolenko, P. S.; Viitala, A.; Appanaboyina, S.; Haemmerich, D.; Ranjan, A.; Jacobs, G.; Woods, D.; Enholm, J.; Wood, B. J. Mild Hyperthermia with Magnetic Resonance-Guided High-Intensity Focused Ultrasound for Applications in Drug Delivery Int. J. Hyperthermia 2012, 28, 320-336
46. Grüll, H.; Langereis, S. Hyperthermia-Triggered Drug Delivery from Temperature Sensitive Liposomes Using MRI-Guided High Intensity Focused Ultrasound J. Controlled Release 2012, 161, 317-327
47. Staruch, R.; Chopra, R.; Hynynen, K. Localised Drug Release Using MRI-Controlled Focused Ultrasound Hyperthermia Int. J. Hyperthermia 2011, 27, 156-171
48. Park, S. M.; Kim, M. S.; Park, S. J.; Park, E. S.; Choi, K. S.; Kim, Y. S.; Kim, H. R. Novel Temperature-Triggered Liposome with High Stability: Formulation, in Vitro Evaluation, and in Vivo Study Combined with High-Intensity Focused Ultrasound (HIFU) J. Controlled Release 2013, 170, 373-379
49. Changsan, N.; Chan, H.-K.; Separovic, F.; Srichana, T. Physicochemical Characterization and Stability of Rifampicin Liposome Dry Powder Formulations for Inhalation J. Pharm. Sci. 2009, 98, 628-639
50. Behera, T.; Swain, P.; Sahoo, S. K. Antigen in Chitosan Coated Liposomes Enhances Immune Responses Through Parenteral Immunization Int. Immunopharmacol. 2011, 11, 907-914
51. Poon, R. T.; Borys, N. Lyso-Thermosensitive Liposomal Doxorubicin: a Novel Approach to Enhance Efficacy of Thermal Ablation of Liver Cancer Expert Opin. Pharmacother. 2009, 10, 333-343
52. Gasselhuber, A.; Dreher, M. R.; Negussie, A.; Wood, B. J.; Rattay, F.; Haemmerich, D. Mathematical Spatio-Temporal Model of Drug Delivery from Low Temperature Sensitive Liposomes During Radiofrequency Tumour Ablation Int. J. Hyperthermia 2010, 26, 499-513
53. Negussie, A. H.; Yarmolenko, P. S.; Partanen, A.; Ranjan, A.; Jacobs, G.; Woods, D.; Bryant, H.; Thomasson, D.; Dewhirst, M. W.; Wood, B. J. Formulation and Characterisation of Magnetic Resonance Imageable Thermally Sensitive Liposomes for Use With magnetic Resonance-Guided High Intensity Focused Ultrasound Int. J. Hyperthermia 2011, 27, 140-155
54. Cao, Z.; Ma, Y.; Yue, X.; Li, S.; Dai, Z.; Kikuchi, J. Stabilized Liposomal Nanohybrid Cerasomes for Drug Delivery Applications Chem. Commun. 2010, 46, 5265-5267
55. Kawataki, T.; Yasuhara, K.; Kikuchi, J. Remarkable Long-Term Stability of Cerasome as an Organicinorganic Hybrid Nanocontainer for Water-Soluble Macromolecules Chem. Lett. 2011, 40, 461-463
56. Ma, Y.; Dai, Z.; Gao, Y.; Cao, Z.; Zha, Z.; Yue, X.; Kikuchi, J. Liposomal Architecture Boosts Biocompatibility of Nanohybrid Cerasomes Nanotoxicology 2011, 5, 622-635
57. Jin, Y.; Yue, X.; Zhang, Q.; Wu, X.; Cao, Z.; Dai, Z. Cerasomal Doxorubicin With Long-Term Storage Stability and Controllable Sustained Release Acta Biomater. 2012, 8, 3372-3380
58. Cao, Z.; Yue, X.; Jin, Y.; Wu, X.; Dai, Z. Modulation of Release of Paclitaxel from Composite Cerasomes Colloids Surf., B 2012, 98, 97-104
59. Liang, X.; Li, X.; Jing, L.; Xue, P.; Jiang, L.; Ren, Q.; Dai, Z. Design and Synthesis of Lipidic Organoalkoxysilane for Self-assembly of Liposomal Nanohybrid Cerasomes with Controlled Drug Release Properties Chem.-Eur. J. 2013, 19, 16113-16121
60. Yue, X.; Dai, Z. Recent Advances in Liposomal Nanohybrid Cerasomes as Promising Drug Nanocarriers Adv. Colloid Interface Sci. 2014, 207, 32-42
61. Mills, J. K.; Needham, D. The Materials Engineering of Temperature-Sensitive Liposomes Methods Enzymol. 2004, 387, 82-113
62. Hristova, K. A. D. N. Influence of Bilayer Fluctuations on the Steric Interactions Between Polymer-Grafted Bilayers Liq. Cryst. 1995, 18, 423-430
63. May, J. P.; Li, S. D. Hyperthermia-Induced Drug Targeting Expert Opin. Drug Delivery 2013, 10, 511-527
64. Park, C.; Lim, J.; Yun, M.; Kim, C. Photoinduced Release of Guest Molecules by Supramolecular Transformation of Self-Assembled Aggregates Derived from Dendrons Angew. Chem., Int. Ed. 2008, 47, 2959-2963
65. Chen, D.; Wu, J. An in Vitro Feasibility Study of Controlled Drug Release from Encapsulated Nanometer Liposomes Using High Intensity Focused Ultrasound Ultrasonics 2010, 50, 744-749
66. Juliano, R. L.; Stamp, D. The Effect of Particle Size and Charge on the Clearance Rates of Liposomes and Liposome Encapsulated Drugs Biochem. Biophys. Res. Commun. 1975, 63, 651-658
67. Sheng, Y.; Liu, C.; Yuan, Y.; Tao, X.; Yang, F.; Shan, X.; Zhou, H.; Xu, F. Long-Circulating Polymeric Nanoparticles Bearing a Combinatorial Coating of PEG and Water-Soluble Chitosan Biomaterials 2009, 30, 2340-2348
68. He, C.; Hu, Y.; Yin, L.; Tang, C.; Yin, C. Effects of Particle Size and Surface Charge on Cellular Uptake and Biodistribution of Polymeric Nanoparticles Biomaterials 2010, 31, 3657-3666
69. Roser, M.; Fischer, D.; Kissel, T. Surface-Modified Biodegradable Albumin Nano and Microspheres. II: Effect of Surface Charges on in Vitro Phagocytosis and Biodistribution in Rats Eur. J. Pharm. Biopharm. 1998, 46, 255-263
70. Hu, C. S.; Chiang, C. H.; Hong, P. D.; Yeh, M. K. Influence of Charge on FITC-BSA-Loaded Chondroitin Sulfate-chitosan Nanoparticles upon Cell Uptake in Human Caco-2 Cell Monolayers Int. J. Nanomed. 2012, 7, 4861-4872
71. Xiao, K.; Li, Y.; Luo, J.; Lee, J. S.; Xiao, W.; Gonik, A. M.; Agarwal, R. G.; Lam, K. S. The Effect of Surface Charge on in Vivo Biodistribution of PEG-oligocholic Acid Based Micellar Nanoparticles Biomaterials 2011, 32, 3435-3446
72. Dobrovolskaia, M. A.; Aggarwal, P.; Hall, J. B.; McNeil, S. E. Preclinical Studies To Understand Nanoparticle Interaction with the Immune System and Its Potential Effects on Nanoparticle Biodistribution Mol. Pharmaceutics 2008, 5, 487-495
73. Liberman, A.; Wu, Z.; Barback, C. V.; Viveros, R. D.; Wang, J.; Ellies, L. G.; Mattrey, R. F.; Trogler, W. C.; Kummel, A. C.; Blair, S. L. Hollow Iron-Silica Nanoshells for Enhanced High Intensity Focused Ultrasound J. Surg. Res. 2014, 190, 391-398
74. Wang, X.; Chen, H.; Zheng, Y.; Ma, M.; Chen, Y.; Zhang, K.; Zeng, D.; Shi, J. Au-Nanoparticle Coated Mesoporous Silica Nanocapsule-Based Multifunctional Platform for Ultrasound Mediated Imaging, Cytoclasis and Tumor Ablation Biomaterials 2013, 34, 2057-2068
75. Setyawati, M. I.; Kutty, R. V.; Tay, C. Y.; Yuan, X.; Xie, J.; Leong, D. T. Novel Theranostic DNA Nanoscaffolds for the Simultaneous Detection and Killing of Escherichia coli and Staphylococcus aureus ACS Appl. Mater. Interfaces 2014, 6, 21822-21831
76. Phillips, L. C.; Puett, C.; Sheeran, P. S.; Wilson Miller, G.; Matsunaga, T. O.; Dayton, P. A. Phase-Shift Perfluorocarbon Agents Enhance High Intensity Focused Ultrasound Thermal Delivery with Reduced Near-field Heating J. Acoust. Soc. Am. 2013, 134, 1473-1482
77. Chen, K. J.; Liang, H. F.; Chen, H. L.; Wang, Y.; Cheng, P. Y.; Liu, H. L.; Xia, Y.; Sung, H. W. A Thermoresponsive Bubble-Generating Liposomal System for Triggering Localized Extracellular Drug Delivery ACS Nano 2013, 7, 438-446
78. Ma, Y.; Liang, X.; Tong, S.; Bao, G.; Ren, Q.; Dai, Z. Gold Nanoshelled Nanomicelles for Potential MRI Imaging, Light-Triggered Drug Release and Photothermal Therapy Adv. Funct. Mater. 2013, 23, 815-822
79. - To Make Bone Substitutes More Osteointegrative Mater. Sci. Eng., C 2008, 28, 129-140