Localized Co-delivery of Doxorubicin, Cisplatin, and Methotrexate by Thermosensitive Hydrogels for Enhanced Osteosarcoma Treatment

ACS Applied Materials and Interfaces

Volumn 7, Issue 49, 2015, Pages 27040-27048

  Ma, Hecheng ^a,b   He, Chaoliang ^a   Cheng, Yilong ^a   Yang, Zhiming ^b   Zang, Junting ^b   Liu, Jianguo ^b   Chen, Xuesi ^a  

^a CHANGCHUN INSTITUTE OF APPLIED CHEMISTRY   (China)

^b THE FIRST HOSPITAL OF JILIN UNIVERSITY   (China)

Author keywords

combination therapy; injectable hydrogels; localized delivery; multidrug co delivery; osteosarcoma treatment; synergistic therapy

Indexed keywords

CELL DEATH; GENE EXPRESSION; GENE EXPRESSION REGULATION; MAMMALS; PLATINUM COMPOUNDS; TUMORS;

CO DELIVERIES; COMBINATION THERAPY; INJECTABLE HYDROGELS; LOCALIZED DELIVERY; OSTEOSARCOMA; SYNERGISTIC THERAPY;

HYDROGELS;

ANTINEOPLASTIC AGENT; CISPLATIN; DOXORUBICIN; HYDROGEL; METHOTREXATE;

ANIMAL; APOPTOSIS; CHEMISTRY; DRUG EFFECTS; DRUG SCREENING; HUMAN; HYDROGEL; MOUSE; NUDE MOUSE; OSTEOSARCOMA;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; CISPLATIN; DOXORUBICIN; HUMANS; HYDROGELS; METHOTREXATE; MICE; MICE, NUDE; OSTEOSARCOMA; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84950157408     PISSN: 19448244     EISSN: 19448252     Source Type: Journal    
DOI: 10.1021/acsami.5b09112     Document Type: Article

References (54)

1. Ward, E.; DeSantis, C.; Robbins, A.; Kohler, B.; Jemal, A. Childhood and Adolescent Cancer Statistics Ca-Cancer J. Clin. 2014, 64, 83-103 10.3322/caac.21219
2. Hogendoorn, P. C. W. Bone Sarcomas: ESMO Clinical Practice Guidelines for Diagnosis, Treatment and Follow-up Ann. Oncol. 2010, 21, v204-v213 10.1093/annonc/mdq223
3. Kaatsch, P. Epidemiology of Childhood Cancer Cancer Treat. Rev. 2010, 36, 277-285 10.1016/j.ctrv.2010.02.003
4. Bielack, S. S.; Kempf-Bielack, B.; Delling, G.; Exner, G. U.; Flege, S.; Helmke, K.; Kotz, R.; Salzer-Kuntschik, M.; Werner, M.; Winkelmann, W. Prognostic Factors in High-Grade Osteosarcoma of the Extremities or Trunk: An Analysis of 1,702 Patients Treated on Neoadjuvant Cooperative Osteosarcoma Study Group Protocols J. Clin. Oncol. 2002, 20, 776-790 10.1200/JCO.20.3.776
5. Bielack, S.; Jürgens, H.; Jundt, G.; Kevric, M.; Kühne, T.; Reichardt, P.; Zoubek, A.; Werner, M.; Winkelmann, W.; Kotz, R. Osteosarcoma: The COSS Experience. In Pediatric and Adolescent Osteosarcoma; Jaffe, N.; Bruland, O. S.; Bielack, S.; Eds.; Springer: New York, 2010; pp 289-308.
6. Kempf-Bielack, B.; Bielack, S. S.; Jürgens, H.; Branscheid, D.; Berdel, W. E.; Exner, G. U.; Göbel, U.; Helmke, K.; Jundt, G.; Kabisch, H. Osteosarcoma Relapse After Combined Modality Therapy: An Analysis of Unselected Patients in the Cooperative Osteosarcoma Study Group (COSS) J. Clin. Oncol. 2005, 23, 559-568 10.1200/JCO.2005.04.063
7. Kager, L.; Zoubek, A.; Pötschger, U.; Kastner, U.; Flege, S.; Kempf-Bielack, B.; Branscheid, D.; Kotz, R.; Salzer-Kuntschik, M.; Winkelmann, W. Primary Metastatic Osteosarcoma: Presentation and Outcome of Patients Treated on Neoadjuvant Cooperative Osteosarcoma Study Group Protocols J. Clin. Oncol. 2003, 21, 2011-2018 10.1200/JCO.2003.08.132
8. Gatta, G.; Botta, L.; Rossi, S.; Aareleid, T.; Bielska-Lasota, M.; Clavel, J.; Dimitrova, N.; Jakab, Z.; Kaatsch, P.; Lacour, B.; Mallone, S.; Marcos-Gragera, R.; Minicozzi, P.; Sanchez-Perez, M. J.; Sant, M.; Santaquilani, M.; Stiller, C.; Tavilla, A.; Trama, A.; Visser, O.; Peris-Bonet, R. Childhood Cancer Survival in Europe 1999-2007: Results of EUROCARE-5-A Population-Based Study Lancet Oncol. 2014, 15, 35-47 10.1016/S1470-2045(13)70548-5
9. Stiller, C. A.; Trama, A.; Serraino, D.; Rossi, S.; Navarro, C.; Chirlaque, M. D.; Casali, P. G. Descriptive Epidemiology of Sarcomas in Europe: Report From the RARECARE Project Eur. J. Cancer 2013, 49, 684-695 10.1016/j.ejca.2012.09.011
10. Anninga, J. K.; Gelderblom, H.; Fiocco, M.; Kroep, J. R.; Taminiau, A. H. M.; Hogendoorn, P. C. W.; Egeler, R. M. Chemotherapeutic Adjuvant Treatment for Osteosarcoma: Where Do We Stand? Eur. J. Cancer 2011, 47, 2431-2445 10.1016/j.ejca.2011.05.030
11. Luetke, A.; Meyers, P. A.; Lewis, I.; Juergens, H. Osteosarcoma Treatment-Where Do We Stand? A State of the Art Review Cancer Treat. Rev. 2014, 40, 523-532 10.1016/j.ctrv.2013.11.006
12. McTiernan, A.; Jinks, R. C.; Sydes, M. R.; Uscinska, B.; Hook, J. M.; van Glabbeke, M.; Bramwell, V.; Lewis, I. J.; Taminiau, A. H. M.; Nooij, M. A.; Hogendoorn, P. C. W.; Gelderblom, H.; Whelan, J. S. Presence of Chemotherapy-Induced Toxicity Predicts Improved Survival in Patients with Localised Extremity Osteosarcoma Treated with Doxorubicin and Cisplatin: A Report from the European Osteosarcoma Intergroup Eur. J. Cancer 2012, 48, 703-712 10.1016/j.ejca.2011.09.012
13. Marina, N.; Bielack, S.; Whelan, J.; Smeland, S.; Krailo, M.; Sydes, M.; Butterfass-Bahloul, T.; Calaminus, G.; Bernstein, M. International Collaboration Is Feasible in Trials for Rare Conditions: The EURAMOS Experience. In Pediatric and Adolescent Osteosarcoma; Jaffe, N.; Bruland, O. S.; Bielack, S.; Eds.; Springer: New York, 2010; pp 339-353.
14. Cortes, E. P.; Holland, J. F.; Wang, J. J.; Sinks, L. F.; Blom, J.; Senn, H.; Bank, A.; Glidewell, O. Amputation and Adriamycin in Primary Osteosarcoma N. Engl. J. Med. 1974, 291 (19) 998-1000 10.1056/NEJM197411072911903
15. Carter, S. K.; Blum, R. H. New Chemotherapeutic Agents··· Bleomycin and Adriamycin Ca-Cancer J. Clin. 1974, 24 (6) 322-331 10.3322/canjclin.24.6.322
16. Pang, B.; Qiao, X.; Janssen, L.; Velds, A.; Groothuis, T.; Kerkhoven, R.; Nieuwland, M.; Ovaa, H.; Rottenberg, S.; van Tellingen, O. et al. Drug-Induced Histone Eviction from Open Chromatin Contributes to the Chemotherapeutic Effects of Doxorubicin Nat. Commun. 2013, 4, 1908 10.1038/ncomms2921
17. Swift, L. P.; Rephaeli, A.; Nudelman, A.; Phillips, D. R.; Cutts, S. M. Doxorubicin-DNA Adducts Induce a Non-topoisomerase II-Mediated Form of Cell Death Cancer Res. 2006, 66, 4863-4871 10.1158/0008-5472.CAN-05-3410
18. Jolivet, J.; Cowan, K. H.; Curt, G. A.; Clendeninn, N. J.; Chabner, B. A. The Pharmacology and Clinical Use of Methotrexate N. Engl. J. Med. 1983, 309, 1094-1104 10.1056/NEJM198311033091805
19. Janeway, K. A.; Grier, H. E. Sequelae of Osteosarcoma Medical Therapy: A Review of Rare AcuteToxicities and Late Effects Lancet Oncol. 2010, 11 (7) 670-678 10.1016/S1470-2045(10)70062-0
20. Hayek, E. R.; Speakman, E.; Rehmus, E. Acute Doxorubicin Cardiotoxicity N. Engl. J. Med. 2005, 352, 2456-2457 10.1056/NEJM200506093522321
21. Widemann, B. C.; Adamson, P. C. Understanding and Managing Methotrexate Nephrotoxicity Oncologist 2006, 11, 694-703 10.1634/theoncologist.11-6-694
22. Park, S. B.; Goldstein, D.; Krishnan, A. V.; Lin, C. S. Y.; Friedlander, M. L.; Cassidy, J.; Koltzenburg, M.; Kiernan, M. C. Chemotherapy-Induced Peripheral Neurotoxicity: A Critical Analysis Ca-Cancer J. Clin. 2013, 63, 419-437 10.3322/caac.21204
23. Berrino, F.; De Angelis, R.; Sant, M.; Rosso, S.; Lasota, M. B.; Coebergh, J. W.; Santaquilani, M. Survival for Eight Major Cancers and All Cancers Combined for European Adults Diagnosed in 1995-99: Results of the EUROCARE-4 Study Lancet Oncol. 2007, 8, 773-783 10.1016/S1470-2045(07)70245-0
24. Kim, S.; Nishimoto, S. K.; Bumgardner, J. D.; Haggard, W. O.; Gaber, M. W.; Yang, Y. A Chitosan/β-Glycerophosphate Thermosensitive Gel for the Delivery of Ellagic Acid for the Treatment of Brain Cancer Biomaterials 2010, 31, 4157-4166 10.1016/j.biomaterials.2010.01.139
25. Yu, L.; Ding, J. Injectable Hydrogels as Unique Biomedical Materials Chem. Soc. Rev. 2008, 37, 1473-1481 10.1039/b713009k
26. He, C.; Kim, S. W.; Lee, D. S. In Situ Gelling Stimuli-Sensitive Block Copolymer Hydrogels for Drug Delivery J. Controlled Release 2008, 127, 189-207 10.1016/j.jconrel.2008.01.005
27. Park, M. H.; Joo, M. K.; Choi, B. G.; Jeong, B. Biodegradable Thermogels Acc. Chem. Res. 2012, 45, 424-33 10.1021/ar200162j
28. Alexander, A.; Ajazuddin; Khan, J.; Saraf, S.; Saraf, S. Poly(Ethylene Glycol)-Poly(Lactic-co-Glycolic Acid) Based Thermosensitive Injectable Hydrogels for Biomedical Applications J. Controlled Release 2013, 172, 715-729 10.1016/j.jconrel.2013.10.006
29. Guo, D. D.; Hong, S. H.; Jiang, H. L.; Kim, J. H.; Minai-Tehrani, A.; Kim, J. E.; Shin, J. Y.; Jiang, T.; Kim, Y.-K.; Choi, Y.-J. et al. Synergistic Effects of Akt1 shRNA and Paclitaxel-Incorporated Conjugated Linoleic Acid-Coupled Poloxamer Thermosensitive Hydrogel on Breast Cancer Biomaterials 2012, 33, 2272-2281 10.1016/j.biomaterials.2011.12.011
30. Ta, H. T.; Dass, C. R.; Larson, I.; Choong, P. F.; Dunstan, D. E. A Chitosan Hydrogel Delivery System for Osteosarcoma Gene Therapy with Pigment Epithelium-Derived Factor Combined with Chemotherapy Biomaterials 2009, 30, 4815-4823 10.1016/j.biomaterials.2009.05.035
31. Narayani, R.; Panduranga Rao, K. Collagen-Poly(HEMA) Hydrogels for the Controlled Delivery of Methotrexate and Cisplatin Int. J. Pharm. 1996, 138, 121-124 10.1016/0378-5173(96)04527-9
32. Bouhadir, K. H.; Alsberg, E.; Mooney, D. J. Hydrogels for Combination Delivery of Antineoplastic Agents Biomaterials 2001, 22, 2625-2633 10.1016/S0142-9612(01)00003-5
33. Konishi, M.; Tabata, Y.; Kariya, M.; Hosseinkhani, H.; Suzuki, A.; Fukuhara, K.; Mandai, M.; Takakura, K.; Fujii, S. In Vivo Anti-Tumor Effect of Dual Release of Cisplatin and Adriamycin from Biodegradable Gelatin Hydrogel J. Controlled Release 2005, 103, 7-19 10.1016/j.jconrel.2004.11.014
34. Miao, B.; Song, C.; Ma, G. Injectable Thermosensitive Hydrogels for Intra-Articular Delivery of Methotrexate J. Appl. Polym. Sci. 2011, 122, 2139-2145 10.1002/app.34332
35. Zhu, W.; Li, Y.; Liu, L.; Chen, Y.; Xi, F. Supramolecular Hydrogels as a Universal Scaffold for Stepwise Delivering Dox and Dox/cisplatin Loaded Block Copolymer Micelles Int. J. Pharm. 2012, 437, 11-19 10.1016/j.ijpharm.2012.08.007
36. Chen, Y. Y.; Wu, H. C.; Sun, J. S.; Dong, G. C.; Wang, T. W. Injectable and Thermoresponsive Self-Assembled Nanocomposite Hydrogel for Long-Term Anticancer Drug Delivery Langmuir 2013, 29, 3721-3729 10.1021/la400268p
37. Yu, L.; Ci, T.; Zhou, S.; Zeng, W.; Ding, J. The Thermogelling PLGA-PEG-PLGA Block Copolymer as a Sustained Release Matrix of Doxorubicin Biomater. Sci. 2013, 1, 411-420 10.1039/c2bm00159d
38. Ma, H.; He, C.; Cheng, Y.; Li, D.; Gong, Y.; Liu, J.; Tian, H.; Chen, X. PLK1shRNA and Doxorubicin Co-Loaded Thermosensitive PLGA-PEG-PLGA Hydrogels for Osteosarcoma Treatment Biomaterials 2014, 35, 8723-8734 10.1016/j.biomaterials.2014.06.045
39. Cho, H.; Kwon, G. S. Thermosensitive Poly-(D,L-Lactide-co-Glycolide)- block-Poly(Ethylene Glycol)-block-Poly-(D,L-Lactide-co-Glycolide) Hydrogels for Multi-Drug Delivery J. Drug Targeting 2014, 22, 669-77 10.3109/1061186X.2014.931406
40. Xu, S.; Wang, W.; Li, X.; Liu, J.; Dong, A.; Deng, L. Sustained Release of PTX-Incorporated Nanoparticles Synergized by Burst Release of DOX•HCl from Thermosensitive Modified PEG/PCL Hydrogel to Improve Anti-Tumor Efficiency Eur. J. Pharm. Sci. 2014, 62, 267-273 10.1016/j.ejps.2014.06.002
41. Shen, W.; Luan, J.; Cao, L.; Sun, J.; Yu, L.; Ding, J. Thermogelling Polymer-Platinum(IV) Conjugates for Long-Term Delivery of Cisplatin Biomacromolecules 2015, 16, 105-115 10.1021/bm501220a
42. Nair, L. S.; Laurencin, C. T. Biodegradable Polymers as Biomaterials Prog. Polym. Sci. 2007, 32, 762-798 10.1016/j.progpolymsci.2007.05.017
43. Berenbaum, M. C. A Method for Testing for Synergy with Any Number of Agents J. Infect. Dis. 1978, 137, 122-130 10.1093/infdis/137.2.122
44. Song, W.; Tang, Z.; Li, M.; Lv, S.; Sun, H.; Deng, M.; Liu, H.; Chen, X. Polypeptide-Based Combination of Paclitaxel and Cisplatin for Enhanced Chemotherapy Efficacy and Reduced Side-Effects Acta Biomater. 2014, 10, 1392-1402 10.1016/j.actbio.2013.11.026
45. Ci, T.; Chen, L.; Yu, L.; Ding, J. Tumor Regression Achieved by Encapsulating a Moderately Soluble Drug into a Polymeric Thermogel Sci. Rep. 2014, 4, 5473 10.1038/srep05473
46. Jeong, B.; Bae, Y. H.; Kim, S. W. Drug Release from Biodegradable Injectable Thermosensitive Hydrogel of PEG-PLGA-PEG Triblock Copolymers J. Controlled Release 2000, 63, 155-163 10.1016/S0168-3659(99)00194-7
47. Zentner, G. M.; Rathi, R.; Shih, C.; McRea, J. C.; Seo, M.-H.; Oh, H.; Rhee, B. G.; Mestecky, J.; Moldoveanu, Z.; Morgan, M.; Weitman, S. Biodegradable Block Copolymers for Delivery of Proteins and Water-Insoluble Drugs J. Controlled Release 2001, 72, 203-215 10.1016/S0168-3659(01)00276-0
48. Nishioka, Y.; Kyotani, S.; Kusunose, M.; Mimoto, H.; Hamada, T.; Asai, M.; Sagara, Y. Cisplatin Suppository: Preparation, Release Characteristics and Clinical Evaluation Chem. Pharm. Bull. 1991, 39, 1518-1521 10.1248/cpb.39.1518
49. Jhaveri, A.; Deshpande, P.; Torchilin, V. Stimuli-Sensitive Nanopreparations for Combination Cancer Therapy J. Controlled Release 2014, 190, 352-370 10.1016/j.jconrel.2014.05.002
50. Lowe, S. W.; Lin, A. W. Apoptosis in Cancer Carcinogenesis 2000, 21, 485-495 10.1093/carcin/21.3.485
51. García-Sáez, A. The Secrets of the Bcl-2 Family Cell Death Differ. 2012, 19, 1733-1740 10.1038/cdd.2012.105
52. Devarajan, E.; Sahin, A. A.; Chen, J. S.; Krishnamurthy, R. R.; Aggarwal, N.; Brun, A.-M.; Sapino, A.; Zhang, F.; Sharma, D.; Yang, X.-H. et al. Down-Regulation of Caspase 3 in Breast Cancer: A Possible Mechanism for Chemoresistance Oncogene 2002, 21, 8843-8851 10.1038/sj.onc.1206044
53. Hockenbery, D.; Nuñez, G.; Milliman, C.; Schreiber, R. D.; Korsmeyer, S. J. Bcl-2 Is an Inner Mitochondrial Membrane Protein That Blocks Programmed Cell Death Nature 1990, 348, 334-336 10.1038/348334a0
54. Srinivasula, S. M.; Hegde, R.; Saleh, A.; Datta, P.; Shiozaki, E.; Chai, J.; Lee, R.-A.; Robbins, P. D.; Fernandes-Alnemri, T.; Shi, Y. et al. A Conserved XIAP-Interaction Motif in Caspase-9 and Smac/DIABLO Regulates Caspase Activity and Apoptosis Nature 2001, 410, 112-116 10.1038/35065125