Photothermally triggered cytosolic drug delivery via endosome disruption using a functionalized reduced graphene oxide

ACS Nano

Volumn 7, Issue 8, 2013, Pages 6735-6746

  Kim, Hyunwoo ^a,b   Lee, Duhwan ^a,b   Kim, Jinhwan ^a,b   Kim, Tae Il ^c   Kim, Won Jong ^a,b  

^a Institute for Basic Science   (South Korea)

^b Pohang University of Science and Technology (POSTECH)   (South Korea)

^c Seoul National University   (South Korea)

Author keywords

controlled drug delivery; endosome disruption; functionalized reduced graphene oxide; near infrared stimuli responsive; photothermal effect

Indexed keywords

BIOMEDICAL APPLICATIONS; ENDOSOMAL DISRUPTION; ENDOSOMES; HYDROPHOBIC INTERACTIONS; PHOTOTHERMAL EFFECTS; PHYSIO-CHEMICAL PROPERTIES; REDUCED GRAPHENE OXIDES; STIMULI-RESPONSIVE;

CELL DEATH; CONTROLLED DRUG DELIVERY; ENZYME INHIBITION; INFRARED DEVICES; IRRADIATION; MEDICAL APPLICATIONS;

GRAPHENE;

ANTINEOPLASTIC AGENT; BRANCHED POLYETHYLENEIMINE BLOCK POLYETHYLENE GLYCOL; BRANCHED POLYETHYLENEIMINE-BLOCK-POLYETHYLENE GLYCOL; DOXORUBICIN; DRUG CARRIER; DRUG DERIVATIVE; GLUTATHIONE; GRAPHITE; MACROGOL DERIVATIVE; OXIDE; POLYETHYLENEIMINE;

ARTICLE; CHEMISTRY; CONFOCAL MICROSCOPY; CYTOSOL; ENDOSOME; HELA CELL; HUMAN; INFRARED RADIATION; METABOLISM; METHODOLOGY; NANOTECHNOLOGY; NEAR INFRARED SPECTROSCOPY; NEOPLASM; PHOTOCHEMISTRY; TIME; TUMOR CELL LINE; ANALOGS AND DERIVATIVES; HELA CELL LINE; NEOPLASMS; PROCEDURES;

ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; CYTOSOL; DOXORUBICIN; DRUG CARRIERS; ENDOSOMES; GLUTATHIONE; GRAPHITE; HELA CELLS; HUMANS; INFRARED RAYS; MICROSCOPY, CONFOCAL; NANOTECHNOLOGY; NEOPLASMS; OXIDES; PHOTOCHEMISTRY; POLYETHYLENE GLYCOLS; POLYETHYLENEIMINE; SPECTROSCOPY, NEAR-INFRARED; TIME FACTORS;

EID: 84883260857     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/nn403096s     Document Type: Article

References (45)

1. Fleige, E.; Quadir, M. A.; Haag, R. Stimuli-Responsive Polymeric Nanocarriers for the Controlled Transport of Active Compounds: Concepts and Applications Adv. Drug Delivery Rev. 2012, 64, 866-884
2. Timko, B. P.; Dvir, T.; Kohane, D. S. Remotely Triggerable Drug Delivery Systems Adv. Mater. 2010, 22, 4925-4943
3. 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
4. Ochs, M.; Carregal-Romero, S.; Rejman, J.; Braeckmans, K.; De Smedt, S. C.; Parak, W. J. Light-Addressable Capsules as Caged Compound Matrix for Controlled Triggering of Cytosolic Reactions Angew. Chem., Int. Ed. 2013, 52, 695-699
5. Aathimanikandan, S. V.; Savariar, E. N.; Thayumanavan, S. Temperature-Sensitive Dendritic Micelles J. Am. Chem. Soc. 2005, 127, 14922-14929
6. Hoare, T.; Santamaria, J.; Goya, G. F.; Irusta, S.; Lin, D.; Lau, S.; Padera, R.; Langer, R.; Kohane, D. S. A Magnetically Triggered Composite Membrane for On-Demand Drug Delivery Nano Lett. 2009, 9, 3651-3657
7. Hernot, S.; Klibanov, A. L. Microbubbles in Ultrasound-Triggered Drug and Gene Delivery Adv. Drug Delivery Rev. 2008, 60, 1153-1166
8. Geers, B.; Lentacker, I.; Cool, S.; Demeester, J.; De Smedt, S. C.; Sanders, N. N. Ultrasound Responsive Doxorubicin-Loaded Microbubbles; Towards an Easy Applicable Drug Delivery Platform J. Controlled Release 2010, 148, e59-e60
9. Weissleder, R. A Clearer Vision for in Vivo Imaging Nat. Biotechnol. 2001, 19, 316-317
10. Kuo, T.-R.; Hovhannisyan, V. A.; Chao, Y.-C.; Chao, S.-L.; Chiang, S.-J.; Lin, S.-J.; Dong, C.-Y.; Chen, C.-C. Multiple Release Kinetics of Targeted Drug from Gold Nanorod Embedded Polyelectrolyte Conjugates Induced by Near-Infrared Laser Irradiation J. Am. Chem. Soc. 2010, 132, 14163-14171
11. Carregal-Romero, S.; Ochs, M.; Rivera-Gil, P.; Ganas, C.; Pavlov, A. M.; Sukhorukov, G. B.; Parak, W. J. NIR-Light Triggered Delivery of Macromolecules into the Cytosol J. Controlled Release 2012, 159, 120-127
12. Yavuz, M. S.; Cheng, Y.; Chen, J.; Cobley, C. M.; Zhang, Q.; Rycenga, M.; Xie, J.; Kim, C.; Wang, L. V.; Xia, Y. et al. Gold Nanocages Covered by Smart Polymers for Controlled Release with Near-Infrared Light Nat. Mater. 2009, 8, 935-939
13. Moon, G. D.; Choi, S. W.; Cai, X.; Li, W.; Cho, E. C.; Jeong, U.; Wang, L. V.; Xia, Y. A New Theranostic System Based on Gold Nanocages and Phase-Change Materials with Unique Features for Photoacoustic Imaging and Controlled Release J. Am. Chem. Soc. 2011, 133, 4762-4765
14. Chang, Y.-T.; Liao, P.-Y.; Sheu, H.-S.; Tseng, Y.-J.; Cheng, F.-Y.; Yeh, C.-S. Near-Infrared Light-Responsive Intracellular Drug and siRNA Release Using Au Nanoensembles with Oligonucleotide-Capped Silica Shell Adv. Mater. 2012, 24, 3309-3314
15. Qin, Z.; Bischof, J. C. Thermophysical and Biological Responses of Gold Nanoparticle Laser Heating Chem. Soc. Rev. 2012, 41, 1191-1217
16. Wu, G.; Mikhailovsky, A.; Khant, H. A.; Fu, C.; Chiu, W.; Zasadzinski, J. A. Remotely Triggered Liposome Release by Near-Infrared Light Absorption via Hollow Gold Nanoshells J. Am. Chem. Soc. 2008, 130, 8175-8177
17. Krpetic, Z.; Nativo, P.; See, V.; Prior, I. A.; Brust, M.; Volk, M. Inflicting Controlled Nonthermal Damage to Subcellular Structures by Laser-Activated Gold Nanoparticles Nano Lett. 2010, 10, 4549-4554
18. Liu, Z.; Sun, X.; Nakayama-Ratchford, N.; Dai, H. Supramolecular Chemistry on Water-Soluble Carbon Nanotubes for Drug Loading and Delivery ACS Nano 2007, 1, 50-56
19. Liu, Z.; Robinson, J. T.; Sun, X.; Dai, H. PEGylated Nanographene Oxide for Delivery of Water-Insoluble Cancer Drugs J. Am. Chem. Soc. 2008, 130, 10876-10877
20. Sherlock, S. P.; Tabakman, S. M.; Xie, L.; Dai, H. Photothermally Enhanced Drug Delivery by Ultrasmall Multifunctional FeCo/Graphitic Shell Nanocrystals ACS Nano 2011, 5, 1505-1512
21. Zhang, L. M.; Xia, J. G.; Zhao, Q. H.; Liu, L. W.; Zhang, Z. J. Functional Graphene Oxide as a Nanocarrier for Controlled Loading and Targeted Delivery of Mixed Anticancer Drugs Small 2010, 6, 537-544
22. Bao, H. Q.; Pan, Y. Z.; Ping, Y.; Sahoo, N. G.; Wu, T. F.; Li, L.; Li, J.; Gan, L. H. Chitosan-Functionalized Graphene Oxide as a Nanocarrier for Drug and Gene Delivery Small 2011, 7, 1569-1578
23. Robinson, J. T.; Tabakman, S. M.; Liang, Y. Y.; Wang, H. L.; Casalongue, H. S.; Vinh, D.; Dai, H. J. Ultrasmall Reduced Graphene Oxide with High Near-Infrared Absorbance for Photothermal Therapy J. Am. Chem. Soc. 2011, 133, 6825-6831
24. Kim, H.; Namgung, R.; Singha, K.; Oh, I. K.; Kim, W. J. Graphene Oxide-Polyethylenimine Nanoconstruct as a Gene Delivery Vector and Bioimaging Tool Bioconjugate Chem. 2011, 22, 2558-2567
25. Kim, H.; Kim, W. J. Photothermally Controlled Gene Delivery by Reduced Graphene Oxide-Polyethylenimine Nanocomposite Small 2013, 10.1002/smll.201202636
26. Zhang, L. M.; Lu, Z. X.; Zhao, Q. H.; Huang, J.; Shen, H.; Zhang, Z. J. Enhanced Chemotherapy Efficacy by Sequential Delivery of siRNA and Anticancer Drugs Using PEI-Grafted Graphene Oxide Small 2011, 7, 460-464
27. Zhang, W.; Guo, Z. Y.; Huang, D. Q.; Liu, Z. M.; Guo, X.; Zhong, H. Q. Synergistic Effect of Chemo-Photothermal Therapy Using PEGylated Graphene Oxide Biomaterials 2011, 32, 8555-8561
28. Yang, K.; Zhang, S.; Zhang, G.; Sun, X.; Lee, S. T.; Liu, Z. Graphene in Mice: Ultrahigh in Vivo Tumor Uptake and Efficient Photothermal Therapy Nano Lett. 2010, 10, 3318-3323
29. Li, M.; Yang, X.; Ren, J.; Qu, K.; Qu, X. Using Graphene Oxide High Near-Infrared Absorbance for Photothermal Treatment of Alzheimer's Disease Adv. Mater. 2012, 24, 1722-1728
30. Tian, B.; Wang, C.; Zhang, S.; Feng, L. Z.; Liu, Z. Photothermally Enhanced Photodynamic Therapy Delivered by Nano-Graphene Oxide ACS Nano 2011, 5, 7000-7009
31. Sahu, A.; Choi, W. I.; Tae, G. A Stimuli-Sensitive Injectable Graphene Oxide Composite Hydrogel Chem Commun. 2012, 48, 5820-5822
32. Akhavan, O.; Ghaderi, E.; Aghayee, S.; Fereydooni, Y.; Talebi, A. The Use of a Glucose-Reduced Graphene Oxide Suspension for Photothermal Cancer Therapy J. Mater. Chem. 2012, 22, 13773-13781
33. Hu, S. H.; Chen, Y. W.; Hung, W. T.; Chen, I. W.; Chen, S. Y. Quantum-Dot-Tagged Reduced Graphene Oxide Nanocomposites for Bright Fluorescence Bioimaging and Photothermal Therapy Monitored in Situ Adv. Mater. 2012, 24, 1748-1754
34. Kiyomiya, K.-i.; Matsuo, S.; Kurebe, M. Mechanism of Specific Nuclear Transport of Adriamycin: The Mode of Nuclear Translocation of Adriamycin-Proteasome Complex Cancer Res. 2001, 61, 2467-2471
35. Son, S.; Namgung, R.; Kim, J.; Singha, K.; Kim, W. J. Bioreducible Polymers for Gene Silencing and Delivery Acc. Chem. Res. 2011, 45, 1100-1112
36. Dembereldorj, U.; Kim, M.; Kim, S.; Ganbold, E.-O.; Lee, S. Y.; Joo, S.-W. A Spatiotemporal Anticancer Drug Release Platform of PEGylated Graphene Oxide Triggered by Glutathione in Vitro and in Vivo J. Mater. Chem. 2012, 22, 23845-23851
37. Szabó, T.; Berkesi, O.; Forgó, P.; Josepovits, K.; Sanakis, Y.; Petridis, D.; Dékány, I. Evolution of Surface Functional Groups in a Series of Progressively Oxidized Graphite Oxides Chem. Mater. 2006, 18, 2740-2749
38. Moon, I. K.; Lee, J.; Ruoff, R. S.; Lee, H. Reduced Graphene Oxide by Chemical Graphitization Nat. Commun. 2010, 1, 73-78
39. Moon, H. K.; Lee, S. H.; Choi, H. C. In Vivo Near-Infrared Mediated Tumor Destruction by Photothermal Effect of Carbon Nanotubes ACS Nano 2009, 3, 3707-3713
40. Kim, J.; Cote, L. J.; Kim, F.; Huang, J. Visualizing Graphene Based Sheets by Fluorescence Quenching Microscopy J. Am. Chem. Soc. 2009, 132, 260-267
41. Yang, K.; Wan, J.; Zhang, S.; Tian, B.; Zhang, Y.; Liu, Z. The Influence of Surface Chemistry and Size of Nanoscale Graphene Oxide on Photothermal Therapy of Cancer Using Ultra-Low Laser Power Biomaterials 2012, 33, 2206-2214
42. Wu, M.; Kempaiah, R.; Huang, P. J.; Maheshwari, V.; Liu, J. Adsorption and Desorption of DNA on Graphene Oxide Studied by Fluorescently Labeled Oligonucleotides Langmuir 2011, 27, 2731-2738
43. Zhang, R. Y.; Olin, H. Carbon Nanomaterials as Drug Carriers: Real Time Drug Release Investigation Mater. Sci. Eng. C 2012, 32, 1247-1252
44. Zhang, C.; Gao, S.; Jiang, W.; Lin, S.; Du, F.; Li, Z.; Huang, W. Targeted Minicircle DNA Delivery Using Folate-Poly(ethylene glycol)- Polyethylenimine as Non-Viral Carrier Biomaterials 2010, 31, 6075-6086
45. You, J.-O.; Auguste, D. T. The Effect of Swelling and Cationic Character on Gene Transfection by pH-Sensitive Nanocarriers Biomaterials 2010, 31, 6859-6866