Amphiphilic polymer-mediated formation of laponite-based nanohybrids with robust stability and pH sensitivity for anticancer drug delivery

ACS Applied Materials and Interfaces

Volumn 6, Issue 19, 2014, Pages 16687-16695

  Wang, Guoying ^a   Maciel, Dina ^a   Wu, Yilun ^c   Rodrigues, Joaío ^a   Shi, Xiangyang ^a,c   Yuan, Yuan ^b   Liu, Changsheng ^b   Tomás, Helena ^a   Li, Yulin ^a,b  

^a UNIVERSITY OF MADEIRA   (Portugal)

^b EAST CHINA UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^c DONGHUA UNIVERSITY   (China)

Author keywords

amphiphilic polymer; anticancer; doxorubicin; Laponite; pH sensitive

Indexed keywords

CELL CULTURE; ENCAPSULATION; NANOSTRUCTURED MATERIALS; PH; PH SENSORS; PHYSIOLOGY; POLYETHYLENE GLYCOLS; POLYETHYLENE OXIDES; SELF ASSEMBLY; SILICATES;

AMPHIPHILIC POLYMERS; ANTICANCER; DOXORUBICIN; LAPONITES; PH SENSITIVE;

STABILITY;

ANTINEOPLASTIC AGENT; DOXORUBICIN; LAPONITE; NANOPARTICLE; POLYMER; SILICATE; SURFACTANT;

3T3 CELL LINE; ANIMAL; CELL DEATH; CELL SHAPE; CELL SURVIVAL; CHEMISTRY; DRUG DELIVERY SYSTEM; DRUG EFFECTS; DRUG RELEASE; ENDOCYTOSIS; FLUORESCENCE MICROSCOPY; HUMAN; INFRARED SPECTROSCOPY; MOUSE; PH; TUMOR CELL LINE; ULTRASTRUCTURE; ULTRAVIOLET SPECTROPHOTOMETRY;

ANIMALS; ANTINEOPLASTIC AGENTS; CELL DEATH; CELL LINE, TUMOR; CELL SHAPE; CELL SURVIVAL; DOXORUBICIN; DRUG DELIVERY SYSTEMS; DRUG LIBERATION; ENDOCYTOSIS; HUMANS; HYDROGEN-ION CONCENTRATION; MICE; MICROSCOPY, FLUORESCENCE; NANOPARTICLES; NIH 3T3 CELLS; POLYMERS; SILICATES; SPECTROPHOTOMETRY, ULTRAVIOLET; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; SURFACE-ACTIVE AGENTS;

EID: 84907893482     PISSN: 19448244     EISSN: 19448252     Source Type: Journal    
DOI: 10.1021/am5032874     Document Type: Article

References (57)

1. Happell, B.; Scott, D.; Platania-Phung, C. Provision of Preventive Services for Cancer and Infectious Diseases Among Individuals with Serious Mental Illness Arch. Psychiat. Nurs. 2012, 26, 192-201
2. Tacar, O.; Sriamornsak, P.; Dass, C. R. Doxorubicin: an Update on Anticancer Molecular Action, Toxicity and Novel Drug Delivery Systems J. Pharm. Pharmacol. 2013, 65, 157-170
3. Yin, Q.; Shen, J.; Zhang, Z.; Yu, H.; Li, Y. Reversal of Multidrug Resistance by Stimuli-Responsive Drug Delivery Systems for Therapy of Tumor Adv. Drug Delivery Rev. 2013, 65, 1699-715
4. MacKay, J. A.; Chen, M.; McDaniel, J. R.; Liu, W.; Simnick, A. J.; Chilkoti, A. Self-assembling Chimeric Polypeptide-Doxorubicin Conjugate Nanoparticles that Abolish Tumours after a Single Injection Nat. Mater. 2009, 8, 993-999
5. Yang, J.; Lee, C. H.; Park, J.; Seo, S.; Lim, E. K.; Song, Y. J.; Suh, J. S.; Yoon, H. G.; Huh, Y. M.; Haam, S. Antibody Conjugated Magnetic PLGA Nanoparticles for Diagnosis and Treatment of Breast Cancer J. Mater. Chem. 2007, 17, 2695-2699
6. Yu, M. K.; Jeong, Y. Y.; Park, J.; Park, S.; Kim, J. W.; Min, J. J.; Kim, K.; Jon, S. Drug-Loaded Superparamagnetic Iron Oxide Nanoparticles for Combined Cancer Imaging and Therapy in vivo Angew. Chem., Int. Ed. 2008, 47, 5362-5365
7. Barraud, L.; Merle, P.; Soma, E.; Lefrancíois, L.; Guerret, S.; Chevallier, M.; Dubernet, C.; Couvreur, P.; Trépo, C.; Vitvitski, L. Increase of Doxorubicin Sensitivity by Doxorubicin-Loading into Nanoparticles for Hepatocellular Carcinoma Cells in vitro and in vivo J. Hepatol. 2005, 42, 736-743
8. Goncíalves, M.; Figueira, P.; Maciel, D.; Rodrigues, J.; Shi, X.; Tomás, H.; Li, Y. Antitumor Efficacy of Doxorubicin-Loaded Laponite/Alginate Hybrid Hydrogels Macromol. Biosci. 2013, 14, 110-120
9. Swain, S. M.; Whaley, F. S.; Ewer, M. S. Congestive Heart Failure in Patients Treated with Doxorubicin Cancer 2003, 97, 2869-2879
10. Lee, C. C.; Gillies, E. R.; Fox, M. E.; Guillaudeu, S. J.; Fréchet, J. M.; Dy, E. E.; Szoka, F. C. A Single Dose of Doxorubicin-Functionalized Bow-Tie Dendrimer Cures Mice Bearing C-26 Colon Carcinomas Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 16649-16654
11. Batist, G.; Ramakrishnan, G.; Rao, C. S.; Chandrasekharan, A.; Gutheil, J.; Guthrie, T.; Shah, P.; Khojasteh, A.; Nair, M. K.; Hoelzer, K. Reduced Cardiotoxicity and Preserved Antitumor Efficacy of Liposome-Encapsulated Doxorubicin and Cyclophosphamide Compared with Conventional Doxorubicin and Cyclophosphamide in a Randomized, Multicenter Trial of Metastatic Breast Cancer J. Clin. Oncol. 2001, 19, 1444-1454
12. Yoo, H. S.; Park, T. G. Folate Receptor Targeted Biodegradable Polymeric Doxorubicin Micelles J. Controlled Release 2004, 96, 273-283
13. Wang, S.; Wu, Y.; Guo, R.; Huang, Y.; Wen, S.; Shen, M.; Wang, J.; Shi, X. Laponite Nanodisks as an Efficient Platform for Doxorubicin Delivery to Cancer Cells Langmuir 2013, 29, 5030-5036
14. Zhang, X.; Meng, L.; Lu, Q.; Fei, Z.; Dyson, P. J. Targeted Delivery and Controlled Release of Doxorubicin to Cancer Cells Using Modified Single Wall Carbon Nanotubes Biomaterials 2009, 30, 6041-6047
15. Yu, S. Y.; Hu, J. H.; Pan, X. Y.; Yao, P.; Jiang, M. Stable and pH-Sensitive Nanogels Prepared by Self-Assembly of Chitosan and Ovalbumin Langmuir 2006, 22, 2754-2759
16. Cheng, R.; Meng, F. H.; Deng, C.; Klok, H. A.; Zhong, Z. Y. Dual and Multi-Stimuli Responsive Polymeric Nanoparticles for Programmed Site-Specific Drug Delivery Biomaterials 2013, 34, 3647-3657
17. Brannon-Peppas, L.; Blanchette, J. O. Nanoparticle and Targeted Systems for Cancer Therapy Adv. Drug Delivery Rev. 2012, 64, 206-212
18. Viseras, C.; Cerezo, P.; Sanchez, R.; Salcedo, I.; Aguzzi, C. Current Challenges in Clay Minerals for Drug Delivery Appl..Clay Sci. 2010, 48, 291-295
19. Thompson, D. W.; Butterworth, J. T. The Nature of Laponite and Its Aqueous Dispersions J. Colloid Interface Sci. 1992, 151, 236-243
20. Li, Y.; Santos, J.; Maciel, D.; Tomás, H.; Rodrigues, J. Injectable Hybrid Laponite/Alginate Hydrogels for Sustained Release of Methylene Blue J. Controlled Release 2011, 152 (Suppl 1) e55-57
21. Gaharwar, A. K.; Mihaila, S. M.; Swami, A.; Patel, A.; Sant, S.; Reis, R. L.; Marques, A. P.; Gomes, M. E.; Khademhosseini, A. Bioactive Silicate Nanoplatelets for Osteogenic Differentiation of Human Mesenchymal Stem Cells Adv. Mater. 2013, 25, 3329-3336
22. Dawson, J. I.; Oreffo, R. O. Clay: New Opportunities for Tissue Regeneration and Biomaterial Design Adv. Mater. 2013, 25, 4069-4086
23. Okada, A.; Usuki, A. Twenty Years of Polymer-Clay Nanocomposites Macromol. Mater. Eng. 2006, 291, 1449-1476
24. Goncalves, M.; Figueira, P.; Maciel, D.; Rodrigues, J.; Qu, X.; Liu, C.; Tomás, H.; Li, Y. pH-sensitive Laponite®/Doxorubicin/Alginate Nanohybrids with Improved Anticancer Efficacy Acta Biomater. 2014, 10, 300-307
25. Jung, H.; Kim, H. M.; Bin Choy, Y.; Hwang, S. J.; Choy, J. H. Laponite-Based Nanohybrid for Enhanced Solubility and Controlled Release of Itraconazole Int. J. Pharm. 2008, 349, 283-290
26. Takahashi, T.; Yamada, Y.; Kataoka, K.; Nagasaki, Y. Preparation of a Novel PEG-Clay Hybrid as a DDS Material: Dispersion Sability and Sustained Release Profiles J. Controlled Release 2005, 107, 408-416
27. Fang, J.; Nakamura, H.; Maeda, H. The EPR effect: Unique Features of Tumor Blood Vessels for Drug Delivery, Factors Involved, and Limitations and Augmentation of the Effect Adv. Drug Delivery Rev. 2011, 63, 136-151
28. Moghimi, S. M.; Davis, S. S. Innovations in Avoiding Particle Clearance from Blood by Kupffer Cells-Cause for Reflection Crit. Rev. Ther. Drug Carrier Syst. 1994, 11, 31-59
29. Li, Y. H.; Wang, J.; Wientjes, M. G.; Au, J. L. S. Delivery of Nanomedicines to Extracellular and Intracellular Compartments of a Solid Tumor Adv. Drug Deliver. Rev. 2012, 64, 29-39
30. Delair, T. Colloidal Polyelectrolyte Complexes of Chitosan and Dextran Sulfate Towards Versatile Nanocarriers of Bioactive Molecules Eur. J. Pharm. Biopharm. 2011, 78, 10-18
31. Douglas, K. L.; Piecirillo, C. A.; Tabrizian, M. Effects of Alginate Inclusion on the Vector Properties of Chitosan-Based Nanoparticles J. Controlled Release 2006, 115, 354-361
32. Li, Y. L.; Rodrigues, J.; Tomás, H. Injectable and Biodegradable Hydrogels: Gelation, Biodegradation and Biomedical Applications Chem. Soc. Rev. 2012, 41, 2193-2221
33. Parveen, S.; S, S. K. Evaluation of Cytotoxicity and Mechanism of Apoptosis of Doxorubicin Using Folate-decorated Chitosan Nanoparticles for Targeted Delivery to Retinoblastoma Cancer Nanotechnol. 2010, 1, 47-62
34. Kayal, S.; Ramanujan, R. V. Doxorubicin Loaded PVA Coated Iron Oxide Nanoparticles for Targeted Drug Delivery Mater. Sci. Eng., C 2010, 30, 484-490
35. Wang, S. G.; Zheng, F. Y.; Huang, Y. P.; Fang, Y. T.; Shen, M. W.; Zhu, M. F.; Shi, X. Y. Encapsulation of Amoxicillin within Laponite-Doped Poly(lactic-co-glycolic acid) Nanofibers: Preparation, Characterization, and Antibacterial Activity ACS Appl. Mater. Interfaces 2012, 4, 6393-6401
36. Wang, D. K.; Varanasi, S.; Fredericks, P. M.; Hill, D. J.; Symons, A. L.; Whittaker, A. K.; Rasoul, F. FT-IR Characterization and Hydrolysis of PLA-PEG-PLA Based Copolyester Hydrogels with Short PLA Segments and a Cytocompatibility Study J. Polym. Sci., Part A: Polym. Chem. 2013, 51, 5163-5176
37. Knop, K.; Hoogenboom, R.; Fischer, D.; Schubert, U. S. Poly(ethylene glycol) in Drug Delivery: Pros and Cons as Well as Potential Alternatives Angew. Chem., Int. Ed. 2010, 49, 6288-6308
38. Rosenholm, J. M.; Sahlgren, C.; Linden, M. Towards Multifunctional, Targeted Drug Delivery Systems Using Mesoporous Silica Nanoparticles-Opportunities & Challenges Nanoscale 2010, 2, 1870-1883
39. Bertrand, N.; Leroux, J. C. The journey of a drug-carrier in the body: an anatomo-physiological perspective J. Controlled Release 2012, 161, 152-63
40. Mangoni, A. A.; Jackson, S. H. D. Age-Related Changes in Pharmacokinetics and Pharmacodynamics: Basic Principles and Practical Applications Br. J. Clin. Pharmacol. 2004, 57, 6-14
41. Ernsting, M. J.; Tang, W. L.; MacCallum, N. W.; Li, S. D. Preclinical Pharmacokinetic, Biodistribution, and Anti-Cancer Efficacy Studies of a Docetaxel-Carboxymethylcellulose Nanoparticle in Mouse Models Biomaterials 2012, 33, 1445-1454
42. Zhang, X. D.; Wu, D.; Shen, X.; Chen, J.; Sun, Y. M.; Liu, P. X.; Liang, X. J. Size-Dependent Radiosensitization of PEG-Coated Gold Nanoparticles for Cancer Radiation Therapy Biomaterials 2012, 33, 6408-19
43. Vonarbourg, A.; Passirani, C.; Saulnier, P.; Simard, P.; Leroux, J. C.; Benoit, J. P. Evaluation of Pegylated Lipid Nanocapsules Versus Complement System Activation and Macrophage Uptake J. Biomed. Mater. Res., Part A 2006, 78A, 620-628
44. Hamad, I.; Al-Hanbali, O.; Hunter, A. C.; Rutt, K. J.; Andresen, T. L.; Moghimi, S. M. Distinct Polymer Architecture Mediates Switching of Complement Activation Pathways at the Nanosphere-Serum Interface: Implications for Stealth Nanoparticle Engineering ACS Nano 2010, 4, 6629-6638
45. Cho, H. J.; Yoon, I. S.; Yoon, H. Y.; Koo, H.; Jin, Y. J.; Ko, S. H.; Shim, J. S.; Kim, K.; Kwon, I. C.; Kim, D. D. Polyethylene Glycol-Conjugated Hyaluronic Acid-Ceramide Self-Assembled Nanoparticles for Targeted Delivery of Doxorubicin Biomaterials 2012, 33, 1190-1200
46. Naeye, B.; Raemdonck, K.; Demeester, J.; De Smedt, S. C. Interactions of siRNA Loaded Dextran Nanogel with Blood Cells J. Controlled Release 2010, 148, E90-E91
47. Bhadra, D.; Bhadra, S.; Jain, S.; Jain, N. K. A PEGylated Dendritic Nanoparticulate Carrier of Fluorouracil Int. J. Pharm. 2003, 257, 111-124
48. Mahoney, B. P.; Raghunand, N.; Baggett, B.; Gillies, R. J. Tumor Acidity, Ion Trapping and Chemotherapeutics I. Acid pH Affects the Distribution of Chemotherapeutic Agents in vitro Biochem. Pharmacol. 2003, 66, 1207-1218
49. Wojtkowiak, J. W.; Verduzco, D.; Schramm, K. J.; Gillies, R. J. Drug Resistance and Cellular Adaptation to Tumor Acidic pH Microenvironment Mol. Pharm. 2011, 8, 2032-2038
50. Maciel, D.; Figueira, P.; Xiao, S. L.; Hu, D. M.; Shi, X. Y.; Rodrigues, J.; Tomás, H.; Li, Y. L. Redox-Responsive Alginate Nanogels with Enhanced Anticancer Cytotoxicity Biomacromolecules 2013, 14, 3140-3146
51. Oishi, M.; Sumitani, S.; Nagasaki, Y. On-off Regulation of F-19 Magnetic Resonance Signals Based on pH-Sensitive PEGylated Nanogels for Potential Tumor-Specific Smart F-19 MRI Probes Bioconjugate Chem. 2007, 18, 1379-1382
52. Yang, J.; Chen, H. T.; Vlahov, I. R.; Cheng, J. X.; Low, P. S. Characterization of the pH of Folate Receptor-Containing Endosomes and the Rate of Hydrolysis of Internalized Acid-Labile Folate-Drug Conjugates J. Pharmacol. Exp. Ther. 2007, 321, 462-468
53. Santos, J. L.; Oliveira, H.; Pandita, D.; Rodrigues, J.; Pego, A. P.; Granja, P. L.; Tomás, H. Functionalization of Poly(amidoamine) Dendrimers with Hydrophobic Chains for Improved Gene Delivery in Mesenchymal Stem Cells J. Controlled Release 2010, 144, 55-64
54. Harush-Frenkel, O.; Debotton, N.; Benita, S.; Altschuler, Y. Targeting of Nanoparticles to the Clathrin-Mediated Endocytic Pathway Biochem. Biophys. Res. Commun. 2007, 353, 26-32
55. Dawson, J. I.; Oreffo, R. O. C. Clay: New Opportunities for Tissue Regeneration and Biomaterial Design Adv. Mater. 2013, 25, 4069-4086
56. Zhang, X. K.; Meng, L. J.; Lu, Q. H.; Fei, Z. F.; Dyson, P. J. Targeted Delivery and Controlled Release of Doxorubicin to Cancer Cells Using Modified Single Wall Carbon Nanotubes Biomaterials 2009, 30, 6041-6047
57. Goncalves, M.; Figueira, P.; Maciel, D.; Capelo, D.; Xiao, S.; Sun, W.; Rodrigues, J.; Shi, X.; Tomás, H.; Li, Y. Dendrimer-Assisted Formation of Fluorescent Nanogels for Drug Delivery and Intracellular Imaging Biomacromolecules 2014, 15, 492-499