Cyclic RGD-linked polymeric micelles for targeted delivery of platinum anticancer drugs to glioblastoma through the blood-brain tumor barrier

ACS Nano

Volumn 7, Issue 10, 2013, Pages 8583-8592

  Miura, Yutaka ^a,b   Takenaka, Tomoya ^a   Toh, Kazuko ^b   Wu, Shourong ^b   Nishihara, Hiroshi ^c   Kano, Mitsunobu R ^d   Ino, Yasushi ^a   Nomoto, Takahiro ^a   Matsumoto, Yu ^b   Koyama, Hiroyuki ^b   Cabral, Horacio ^a   Nishiyama, Nobuhiro ^e   Kataoka, Kazunori ^a,b  

^a UNIVERSITY OF TOKYO   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d OKAYAMA UNIVERSITY   (Japan)

^e TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

Author keywords

block copolymer; cancer therapy; cRGD; drug delivery; integrin; polymeric micelle

Indexed keywords

CANCER THERAPY; CONFOCAL LASER SCANNING MICROSCOPY; CRGD; DRUG DELIVERY SYSTEM; EFFICIENT DRUG DELIVERY; INTEGRINS; PLATINUM ANTICANCER DRUGS; POLYMERIC MICELLE;

BLOCK COPOLYMERS; DRUG DELIVERY; DRUG PRODUCTS; LIGANDS; MICELLES; MOLECULES; PLATINUM; TUMORS;

POLYMERS;

ANTINEOPLASTIC AGENT; CYCLIC ARGININE GLYCINE ASPARTIC ACID PEPTIDE; CYCLIC ARGININE-GLYCINE-ASPARTIC ACID PEPTIDE; CYCLOPEPTIDE; INTEGRIN; PLATINUM COMPLEX; POLYMER;

ANIMAL; ARTICLE; BAGG ALBINO MOUSE; BLOOD BRAIN BARRIER; BRAIN TUMOR; CHEMISTRY; FLOW CYTOMETRY; GLIOBLASTOMA; HUMAN; METABOLISM; MICELLE; MOUSE; TUMOR CELL LINE;

ANIMALS; ANTINEOPLASTIC AGENTS; BLOOD-BRAIN BARRIER; BRAIN NEOPLASMS; CELL LINE, TUMOR; FLOW CYTOMETRY; GLIOBLASTOMA; HUMANS; INTEGRINS; MICE; MICE, INBRED BALB C; MICELLES; ORGANOPLATINUM COMPOUNDS; PEPTIDES, CYCLIC; POLYMERS;

EID: 84887013087     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/nn402662d     Document Type: Article

References (50)

1. Rat, J. S. Molecular Mechanisms of Glioma Invasiveness: The Role of Proteases Nat. Rev. Cancer 2003, 3, 489-501
2. Arko, L.; Katsyv, I.; Park, G. E.; Luan, W. P.; Park, J. K. Experimental Approaches for the Treatment of Malignant Gliomas Pharmacol. Ther. 2010, 128, 1-36
3. Mangiola, A.; Anile, C.; Pompucci, A.; Capone, G.; Rigante, L.; De Bonis, P. Glioblastoma Therapy: Going Beyond Hercules Columns Expert Rev. Neurother. 2010, 10, 507-514
4. Jain, R. K.; Tomaso, di E.; Duda, D. G.; Loeffler, J. S.; Sorensen, A. G.; Batchelor, T. T. Angiogenesis in Brain Tumours Nat. Rev. Neurosci. 2008, 8, 610-622
5. Wen, P. Y.; Kesari, S. Malignant Gliomas in Adults N. Engl. J. Med. 2008, 359, 492-507
6. Avgeropoulos, N. G.; Batchelor, T. T. New Treatment Strategies for Malignant Gliomas Oncologist 1999, 4, 209-224
7. Jones, T. S.; Holland, E. C. Standard of Care Therapy for Malignant Glioma and Its Effect on Tumor and Stromal Cells Oncogene 2012, 31, 1995-2006
8. Rich, J. N.; Bigner, D. D. Development of Novel Targeted Therapies in the Treatment of Malignant Glioma Nat. Rev. Drug Discovery 2004, 3, 430-446
9. Reardon, D. A.; Perry, J. R.; Brandes, A. A.; Jalali, R.; Wick, W. Advances in Malignant Glioma Drug Discovery Expert Opin. Drug Discovery 2011, 6, 739-753
10. Groothuis, D. R. The Blood-Brain and Blood-Tumor Barriers: A Review of Strategies for Increasing Drug Delivery Neuro-Oncology 2000, 2, 45-59
11. Ningaraj, N. S. Drug Delivery to Brain Tumours: Challenges and Progress Expert Opin. Drug Delivery 2006, 3, 499-509
12. Sarin, H. Recent Progress towards Development of Effective Systemic Chemotherapy for the Treatment of Malignant Brain Tumors J. Transl. Med. 2009, 7, 77
13. He, H.; Li, Y.; Jia, X. R.; Du, J.; Ying, X.; Lu, W. L.; Lou, J. N.; Wei, Y. PEGylated Poly(amidoamine) Dendrimer-Based Dual-Targeting Carrier for Treating Brain Tumors Biomaterials 2011, 32, 478-487
14. Xin, H.; Jiang, X.; Gu, J.; Sha, X.; Chen, L.; Law, K.; Chen, Y.; Wang, X.; Jiang, Y.; Fang, X. Angiopep-Conjugated Poly(ethylene glycol)-co- Poly(ε-caprolactone) Nanoparticles as Dual-Targeting Drug Delivery System for Brain Glioma Biomaterials 2011, 32, 4293-4305
15. Pardridge, W. M. Drug and Gene Delivery to the Brain: The Vascular Route Neuron 2002, 36, 555-558
16. Muldoon, L. L.; Soussain, C.; Jahnke, K.; Johanson, C.; Siegal, T.; Smith, Q. R.; Hall, W. A.; Hynynen, K.; Senter, P. D.; Peereboom, D. M. et al. Chemotherapy Delivery Issues in Central Nervous System Malignancy: A Reality Check J. Clin. Oncol. 2007, 25, 2295-2305
17. Liu, Y.; Lu, W. Recent Advances in Brain Tumor-Targeted Nano-Drug Delivery Systems Expert Opin. Drug Delivery 2012, 9, 671-686
18. Chen, C.; Xu, T.; Lu, Y.; Chen, J.; Wu, S. The Efficacy of Temozolomide for Recurrent Glioblastoma Multiforme Eur. J. Neurol. 2013, 20, 223-230
19. Duncan, R. The Dawning Era of Polymer Therapeutics Nat. Rev. Drug Discovery 2003, 2, 347-360
20. Ferrari, M. Cancer Nanotechnology: Opportunities and Challenges Nat. Rev. Cancer 2005, 5, 161-171
21. Torchilin, V. P. Recent Advances with Liposomes as Pharmaceutical Carriers Nat. Rev. Drug Discovery 2005, 4, 145-160
22. Davis, M. E.; Chen, Z.; Shin, D. Nanoparticle Therapeutics: An Emerging Treatment Modality for Cancer Nat. Rev. Drug Discovery 2008, 7, 771-782
23. Kataoka, K.; Harada, A.; Nagasaki, Y. Block Copolymer Micelles for Drug Delivery: Design, Characterization and Biological Significance Adv. Drug Delivery Rev. 2001, 47, 113-131
24. Nishiyama, N.; Kataoka, K. Current State, Achievements, and Future Prospects of Polymeric Micelles as Nanocarriers for Drug and Gene Delivery Pharmacol. Ther. 2006, 112, 630-648
25. Danhier, F.; Breton, A. L.; Préat, V. RGD-Based Strategies to Target Alpha(v) Beta(3) Integrin in Cancer Therapy and Diagnosis Mol. Pharmaceutics 2012, 9, 2961-2973
26. Matsumura, Y.; Maeda, H. A New Concept for Macromolecular Therapeutics in Cancer Chemotherapy: Mechanism of Tumouritropic Accumulation of Proteins and the Antitumour Agent SMANCS Cancer Res. 1986, 46, 6387-6392
27. Hobbs, S. K.; Monsky, W. L.; Yuan, F.; Roberts, W. G.; Griffith, L.; Torchilin, V. P.; Jain, R. K. Regulation of Transport Pathways in Tumor Vessels: Role of Tumor Type and Microenvironment Proc. Natl. Acad. Sci. U.S.A. 1998, 95, 4607-4612
28. Hynes, R. O. A Reevaluation of Integrins as Regulators of Angiogenesis Nat. Med. 2001, 8, 918-912
29. Hood, J. D.; Cheresh, D. A. Role of Integrins in Cell Invasion and Migration Nat. Rev. Cancer 2002, 2, 91-100
30. Desgrosellier, J. S.; Cheresh, D. A. Integrins in Cancer: Biological Implications and Therapeutic Opportunities Nat. Rev. Cancer 2010, 10, 9-22
31. Taga, T.; Suzuki, A.; Gonzalez-Gomez, I.; Gilles, F. H.; Stins, M.; Shimada, H.; Barsky, L.; Weinberg, K. I.; Laug, W. E. αv-Integrin Antagonist EMD 121974 Induces Apoptosis in Brain Tumor Cells Growing on Vitronectin and Tenascin Int. J. Cancer 2002, 98, 690-697
32. Sheldrake, H. M.; Patterson, L. H. Function and Antagonism of Beta3 Integrins in the Development of Cancer Therapy Curr. Cancer Drug Targets 2009, 9, 519-540
33. Zhan, C.; Gu, B.; Xie, C.; Li, J.; Liu, Y.; Lu, W. Cyclic RGD Conjugated Poly(ethylene glycol)-co-Poly(lactic acid) Micelle Enhances Paclitaxel Anti-Glioblastoma Effect J. Controlled Release 2010, 143, 136-142
34. Zhan, C.; Wei, X.; Qian, J.; Feng, L.; Zhu, J.; Lu, W. Co-Delivery of TRAIL Gene Enhances the Anti-Glioblastoma Effect of Paclitaxel in Vitro and in Vivo J. Controlled Release 2012, 160, 630-636
35. Cabral, H.; Matsumoto, Y.; Mizuno, K.; Chen, Q.; Murakami, M.; Kimura, M.; Terada, Y.; Kano, M. R.; Miyazono, K.; Uesaka, M. et al. Accumulation of Sub-100 nm Polymeric Micelles in Poorly Permeable Tumours Depends on Size Nat. Nanotechnol. 2011, 6, 815-823
36. Murakami, M.; Cabral, H.; Matsumoto, Y.; Wu, S.; Kano, M. R.; Yamori, T.; Nishiyama, N.; Kataoka, K. Improving Drug Potency and Efficacy by Nanocarrier-Mediated Subcellular Targeting Sci. Transl. Med. 2011, 3, 64ra2
37. Matsumoto, Y.; Nomoto, T.; Cabral, H.; Matsumoto, Y.; Watanabe, S.; Christie, R. J.; Miyata, K.; Oba, M.; Ogura, T.; Yamasaki, Y. et al. Direct and Instantaneous Observation of Intravenously Injected Substances using Intravital Confocal Micro-Videography Biomed. Opt. Express 2010, 1, 1209-1216
38. Nomoto, T.; Matsumoto, Y.; Miyata, K.; Oba, M.; Fukushima, S.; Nishiyama, N.; Yamasoba, T.; Kataoka, K. In Situ Quantitative Monitoring of Polyplexes and Polyplex Micelles in the Blood Circulation Using Intravital Real-Time Confocal Laser Scanning Microscopy J. Controlled Release 2011, 151, 104-109
39. Cabral, H.; Nishiyama, N.; Okazaki, S.; Kato, Y.; Kataoka, K. Preparation and Biological Properties of Dichloro(1,2-diaminocyclohexane)platinum(II) (DACHPt)-Loaded Polymeric Micelles J. Controlled Release 2005, 101, 223-232
40. Cabral, H.; Nishiyama, N.; Kataoka, K. Optimization of (1,2-Diaminocyclohexane)platinum(II)-Loaded Polymeric Micelles Directed to Improved Tumour Targeting and Enhanced Antitumour Activity J. Controlled Release 2007, 121, 146-155
41. Yamada, S.; Bu, X. Y.; Khankaldyyan, V.; Gonzales-Gomez, I.; McComb, J. G.; Laug, W. E. Effect of the Angiogenesis Inhibitor Cilengitide (EMD 121974) on Glioblastoma Growth in Nude Mice Neurosurgery 2006, 59, 1304-1312
42. Carter, A. Integrins as Target: First Phase III Trial Launches, But Questions Remain J. Natl. Cancer Inst. 2010, 102, 675-677
43. Fink, K.; Mikkelsen, T.; Nabors, L. B.; Ravin, P.; Plotkin, S. R.; Schiff, D.; Hicking, C.; Picard, M.; Reardon, D. A. Long-Term Effects of Cilengitide, a Novel Integrin Inhibitor, in Recurrent Glioblastoma: A Randomized Phase IIa Study J. Clin. Oncol. 2010, 28, 182s
44. Mikkelsen, T.; Brodie, C.; Finniss, S.; Berens, M. E.; Rennert, J. L.; Nelson, K.; Lemke, N.; Brown, S. L.; Hahn, D.; Neuteboom, B. et al. Radiation Sensitization of Glioblastoma by Cilengitide Has Unanticipated Schedule-Dependency Int. J. Cancer 2009, 124, 2719-2727
45. Nabors, L. B.; Mikkelsen, T.; Rosenfeld, S. S.; Hochberg, F.; Akella, N. S.; Fisher, J. D.; Cloud, G. A.; Zhang, Y.; Carson, K.; Wittemer, S. M. et al. Phase I and Correlative Biology Study of Cilengitide in Patients with Recurrent Malignant Glioma J. Clin. Oncol. 2007, 25, 1651-1657
46. Morita, K.; Sasaki, H.; Furuse, K.; Furuse, M.; Tsukita, S.; Miyachi, Y. Expression of Claudin-5 in Dermal Vascular Endothelia Exp. Dermatol. 2003, 12, 289-295
47. Cooper, I.; Cohen-Kashi-Malina, K.; Teichberq, V. I. Claudin-5 Expression in in Vitro Models of the Blood-Brain Barrier Methods Mol. Biol. 2011, 762, 347-354
48. Jiao, H.; Wang, Z.; Liu, Y.; Wang, P.; Xue, Y. Specific Role of Tight Junction Proteins Claudin-5, Occludin, and ZO-1 of the Blood-Brain Barrier in a Focal Cerebral Ischemic Insult J. Mol. Neurosci. 2011, 44, 130-139
49. Stewart, P. A.; Hayakawa, K.; Farrell, C. L.; Del Maestro, R. F. Quantitative Study of Microvessel Ultrastructure in Human Peritumoral Brain Tissue. Evidence for a Blood-Brain Barrier Defect J. Neurosurg. 1987, 67, 697-705
50. Stewart, P. A. Endothelial Vesicles in the Blood-Brain Barrier: Are They Related to Permeability? Cell. Mol. Neurobiol. 2000, 20, 149-163