Self-assembled hybrids of fluorescent carbon dots and PAMAM dendrimers for epirubicin delivery and intracellular imaging

ACS Applied Materials and Interfaces

Volumn 7, Issue 21, 2015, Pages 11423-11435

  Matai, Ishita ^a   Sachdev, Abhay ^a   Gopinath, P ^a  

^a INDIAN INSTITUTE OF TECHNOLOGY ROORKEE   (India)

Author keywords

bioimaging; carbon dots; dendrimers; drug delivery; epirubicin; hybrids

Indexed keywords

CARBON; CELL DEATH; CELL SIGNALING; CELLS; CYTOLOGY; CYTOTOXICITY; DENDRIMERS; DISEASES; DRUG DELIVERY; ENAMELS; FIELD EMISSION MICROSCOPES; FLUORESCENCE; IONS; MOBILE SECURITY; SCANNING ELECTRON MICROSCOPY;

BIO-IMAGING; CARBON DOTS; EPIRUBICIN; FIELD EMISSION SCANNING ELECTRON MICROSCOPY; HYBRIDS; INTRACELLULAR DISTRIBUTION; NON-COVALENT INTERACTION; REACTIVE OXYGEN SPECIES;

FUNCTIONAL POLYMERS;

ANTINEOPLASTIC ANTIBIOTIC; CARBON; DENDRIMER; EPIRUBICIN; FLUORESCENT DYE; NANOCAPSULE; NANOCONJUGATE; PAMAM STARBURST;

CELL SURVIVAL; CHEMISTRY; DIFFUSION; DRUG EFFECTS; FLUORESCENCE MICROSCOPY; HUMAN; MATERIALS TESTING; MCF 7 CELL LINE; PROCEDURES; THERANOSTIC NANOMEDICINE; ULTRASTRUCTURE;

ANTIBIOTICS, ANTINEOPLASTIC; CARBON; CELL SURVIVAL; DENDRIMERS; DIFFUSION; EPIRUBICIN; FLUORESCENT DYES; HUMANS; MATERIALS TESTING; MCF-7 CELLS; MICROSCOPY, FLUORESCENCE; NANOCAPSULES; NANOCONJUGATES; THERANOSTIC NANOMEDICINE;

EID: 84930652762     PISSN: 19448244     EISSN: 19448252     Source Type: Journal    
DOI: 10.1021/acsami.5b02095     Document Type: Article

References (69)

1. Xie, J.; Lee, S.; Chen, X. Nanoparticle-Based Theranostic Agents Adv. Drug Delivery Rev. 2010, 62, 1064-1079
2. Janib, S. M.; Moses, A. S.; MacKay, J. A. Imaging and Drug Delivery using Theranostic Nanoparticles Adv. Drug Delivery Rev. 2010, 62, 1052-1063
3. Wang, Z.; Niu, G.; Chen, X. Polymeric Materials for Theranostic Applications Pharm. Res. 2014, 31, 1358-1376
4. Wang, D.; Lin, B.; Ai, H. Theranostic Nanoparticles for Cancer and Cardiovascular Applications Pharm. Res. 2014, 31, 1390-1406
5. Lee, C. C.; MacKay, J. A.; Frechet, J. M. J.; Szoka, F. C. Designing Dendrimers for Biological Applications Nat. Biotechnol. 2005, 23, 1517-26
6. Stiriba, S. E.; Frey, H.; Haag, R. Dendritic Polymers in Biomedical Applications: From Potential to Clinical Use in Diagnostics and Therapy Angew. Chem., Int. Ed. 2002, 41, 1329-1334
7. Svenson, S.; Tomalia, D. A. Dendrimers in Biomedical Applications - Reflections on the Field Adv. Drug Delivery Rev. 2005, 57, 2106-2129
8. Wolinsky, J. B.; Grinstaff, M. W. Therapeutic and Diagnostic Applications of Dendrimers for Cancer Treatment Adv. Drug Delivery Rev. 2008, 60, 1037-1055
9. Meijer, E. W.; Jansen, J.; Brabander-van den Berg, E. Encapsulation of Guest Molecules into a Dendritic Box Science 1994, 266, 1226-1229
10. Morgan, M. T.; Carnahan, M. A.; Immoos, C. E.; Ribeiro, A. A.; Finkelstein, S.; Lee, S. J.; Grinstaff, M. W. Dendritic Molecular Capsules for Hydrophobic Compounds J. Am. Chem. Soc. 2003, 125, 15485-15489
11. Wang, Y.; Guo, R.; Cao, X.; Shen, M.; Shi, X. Encapsulation of 2-Methoxyestradiol within Multifunctional Poly (amidoamine) Dendrimers for Targeted Cancer Therapy Biomaterials 2011, 32, 3322-3329
12. Zheng, Y.; Fu, F.; Zhang, M.; Shen, M.; Zhu, M.; Shi, X. Multifunctional Dendrimers Modified with Alpha-Tocopheryl Succinate for Targeted Cancer Therapy Med. Chem. Commun. 2014, 5, 879-885
13. Zhu, J.; Shi, X. Dendrimer-Based Nanodevices for Targeted Drug Delivery Applications J. Mater. Chem. B 2013, 1, 4199-4211
14. Zhu, J.; Zheng, L.; Wen, S.; Tang, Y.; Shen, M.; Zhang, G.; Shi, X. Targeted Cancer Theranostics Using Alpha Tocopheryl Succinate-Conjugated Multifunctional Dendrimer-Entrapped Gold Nanoparticles Biomaterials 2014, 35, 7635-7646
15. Tsai, Y. J.; Hu, C. C.; Chu, C. C.; Imae, T. Intrinsically Fluorescent PAMAM Dendrimer as Gene Carrier and Nanoprobe for Nucleic Acids Delivery: Bioimaging and Transfection Study Biomacromolecules 2011, 12, 4283-4290
16. Kong, L.; Alves, C. S.; Hou, W.; Qiu, J.; Mohwald, H.; Tomas, H.; Shi, X. RGD Peptide-Modified Dendrimer-Entrapped Gold Nanoparticles Enable Highly Efficient and Specific Gene Delivery to Stem Cells ACS Appl. Mater. Interfaces 2015, 7, 4833-4843
17. Xiao, T.; Hou, W.; Cao, X.; Wen, S.; Shen, M.; Shi, X. Dendrimer-Entrapped Gold Nanoparticles Modified with Folic Acid for Targeted Gene Delivery Applications Biomater. Sci. 2013, 1, 1172-1180
18. Dufès, C.; Uchegbu, L. F.; Schätzlein, A. G. Dendrimers in Gene Delivery Adv. Drug Delivery Rev. 2005, 57, 2177-2202
19. Shi, X.; Sun, Kai.; Baker, J. R. Spontaneous Formation of Functionalized Dendrimer-Stabilized Gold Nanoparticles J. Phys. Chem. C 2009, 112, 8251-8258
20. Matai, I.; Sachdev, A.; Gopinath, P. Multicomponent 5-fluorouracil loaded PAMAM Stabilized-Silver Nanocomposites Synergistically Induce Apoptosis in Human Cancer Cells Biomater. Sci. 2015, 3, 457-468
21. Naha, P. C.; Davoren, M.; Lyng, F. M.; Byrne, H. J. Reactive Oxygen Species (ROS) Induced Cytokine Production and Cytotoxicity of PAMAM Dendrimers in J774A.1 cells Toxicol. Appl. Pharmacol. 2010, 246, 91-99
22. Naha, P. C.; Byrne, H. J. Generation of Intracellular Reactive Oxygen Species and Genotoxicity Effect to Exposure of Nanosized Polyamidoamine (PAMAM) Dendrimers in PLHC-1 cells In Vitro Aquat. Toxicol. 2013, 132-133, 61-72
23. Naha, P. C.; Davoren, M.; Casey, A.; Byrne, H. J. An Ecotoxicological Study of Poly(amidoamine) Dendrimers-Toward Quantitative Structure Activity Relationships Environ. Sci. Technol. 2009, 43, 6864-6869
24. Mukherjee, S. P.; Lyng, F. M.; Garcia, A.; Davoren, M.; Byrne, H. J. Mechanistic Studies of In Vitro Cytotoxicity of Poly(amidoamine) Dendrimers in Mammalian Cells Toxicol. Appl. Pharmacol. 2010, 248, 259-268
25. Hong, S.; Bielinska, A. U.; Mecke, A.; Keszler, B.; Beals, J. L.; Shi, X.; Balogh, L.; Orr, B. G.; Baker, J. R. Interaction of Poly(amidoamine) Dendrimers with Supported Lipid Bilayers and Cells: Hole Formation and the Relation to Transport Bioconjugate Chem. 2004, 15, 774-782
26. Mecke, A.; Majoros, I. J.; Patri, A. K.; Baker, J. R., Jr.; Banaszak Holl, M. M.; Orr, B. G. Lipid Bilayer Disruption by Polyamidoamine Dendrimers: The Role of Generation and Capping Group Langmuir 2005, 21, 10348-10354
27. Lee, H.; Larson, R. G. Lipid Bilayer Curvature and Pore Formation Induced by Charged Linear Polymers and Dendrimers: The Effect of Molecular Shape J. Phys. Chem. B 2008, 112, 12279-12285
28. Wang, W.; Xiong, W.; Wan, J. L.; Sun, X. H.; Xu, H. B.; Yang, X. L. The Decrease of PAMAM Dendrimer-Induced Cytotoxicity by PEGylation via Attenuation of Oxidative Stress Nanotechnology 2009, 20, 105-103
29. Liu, H.; Wang, H.; Xu, Y.; Guo, R.; Wen, S.; Huang, Y.; Liu, W.; Shen, M.; Zhao, J.; Zhang, G.; Shi, X. Lactobionic Acid-Modified Dendrimer-Entrapped Gold Nanoparticles for Targeted Computed Tomography Imaging of Human Hepatocellular Carcinoma ACS Appl. Mater. Interfaces 2014, 6, 6944-6953
30. Liu, H.; Wang, H.; Xu, Y.; Shen, M.; Zhao, J.; Zhang, G.; Shi, X. Synthesis of PEGylated Low Generation Dendrimer-Entrapped Gold Nanoparticles for CT Imaging Applications Nanoscale 2014, 6, 4521-4526
31. Majoros, I. J.; Keszler, B.; Woehler, S.; Bull, T.; Baker, J. R. Acetylation of Poly(amidoamine) Dendrimers Macromolecules 2003, 36, 5526-5529
32. Hu, J.; Su, Y.; Zhang, H.; Xu, T.; Cheng, Y. Design of Interior-Functionalized Fully Acetylated Dendrimers for Anticancer Drug Delivery Biomaterials 2011, 32, 9950-9959
33. Minotti, G.; Menna, P.; Salvatorelli, E.; Cairo, G.; Gianni, L. Anthracyclines: Molecular Advances and Pharmacologic Developments in Antitumor Activity and Cardiotoxicity Pharmacol. Rev. 2004, 56, 185-229
34. Torti, F. M.; Bristow, M. M.; Lum, B. L.; Carter, S. K.; Howes, A. E.; Aston, D. A.; Brown, B. W., Jr.; Hannigan, J. F., Jr.; Meyers, F. J.; Mitchell, E. P.; Billingham, M. E. Cardiotoxicity of Epirubicin and Doxorubicin: Assessment by Endomyocardial Biopsy Cancer Res. 1986, 46, 3722-3727
35. Xu, X. Y.; Ray, R.; Gu, Y. L.; Ploehn, H. J.; Gearheart, L.; Raker, K.; Scrivens, W. A. Electrophoretic Analysis and Purification of Fluorescent Single-Walled Carbon Nanotube Fragments J. Am. Chem. Soc. 2004, 126, 12736-12737
36. Sun, Y. P.; Zhou, B.; Lin, Y.; Wang, W.; Fernando, K. A. S.; Pathak, P.; Meziani, M. J.; Harruff, B. A.; Wang, X.; Wang, H.; Luo, P. G.; Yang, H.; Kose, M. E.; Chen, B.; Veca, L. M.; Xie, S. Y. Quantum Sized Carbon Dots for Bright and Colorful Photoluminescence J. Am. Chem. Soc. 2006, 128, 7756-7757
37. Ma, Z.; Zhang, Y. L.; Wang, L.; Ming, H.; Li, H. T.; Zhang, X.; Wang, F.; Liu, Y.; Kang, Z. H.; Lee, S. T. Bioinspired Photoelectric Conversion System Based on Carbon Quantum Dot Doped Dye-Semiconductor Complex ACS Appl. Mater. Interfaces 2013, 5, 5080-5084
38. Sachdev, A.; Matai, I.; Kumar, S. U.; Bhushan, B.; Dubey, P.; Gopinath, P. A Novel One-Step Synthesis of PEG Passivated Multicolour Fluorescent Carbon Dots for Potential Biolabeling Application RSC Adv. 2013, 3, 16958-16961
39. Sachdev, A.; Matai, I.; Gopinath, P. Implications of Surface Passivation on Physicochemical and Bioimaging Properties of Carbon Dots RSC Adv. 2014, 4, 20915-20921
40. Sachdev, A.; Matai, I.; Gopinath, P. Dual-Functional Carbon Dots-Silver@Zinc Oxide Nanocomposite: In Vitro Evaluation of Cellular Uptake and Induction of Apoptosis J. Mater. Chem. B 2015, 3, 1217-1229
41. Datta, K. K. R.; Kozak, O.; Ranc, V.; Havrdová, M.; Bourlinos, A. B.; Šafářová, K.; Holá, K.; Tománková, K.; Zoppellaro, G.; Otyepkaa, M.; Zbořil, R. Quaternized Carbon Dot-Modified Graphene Oxide for Selective Cell Labelling-Controlled Nucleus and Cytoplasm Imaging Chem. Commun. 2014, 50, 10782-10785
42. Zhou, L.; Li, Z.; Liu, Z.; Ren, J.; Qu, X. Luminescent Carbon Dot-Gated Nanovehicles for pH-Triggered Intracellular Controlled Release and Imaging Langmuir 2013, 29, 6396-6403
43. Zong, J.; Yang, X.; Trinchi, A.; Hardin, S.; Cole, I.; Zhu, Y.; Li, C.; Muster, T.; Wei, G. Photoluminescence Enhancement of Carbon Dots by Gold Nanoparticles Conjugated via PAMAM dendrimers Nanoscale 2013, 5, 11200-11206
44. Dong, W.; Zhou, S.; Dong, Y.; Wang, J.; Ge, X.; Sui, L. The Preparation of Ethylenediamine-Modified Fluorescent Carbon Dots and their use in Imaging of Cells Luminescence 2015, 10.1002/bio.2834
45. Liu, C.; Zhang, P.; Zhai, X.; Tian, F.; Li, W.; Yang, J.; Liu, Y.; Wang, H.; Wang, W.; Liu, W. Nano-carrier for Gene Delivery and Bioimaging based on Carbon Dots with PEI-Passivation Enhanced Fluorescence Biomaterials 2012, 33, 3604-3613
46. Wang, Q.; Huang, X.; Long, Y.; Wang, X.; Zhang, H.; Zhu, R.; Liang, L.; Teng, P.; Zheng, H. Hollow Luminescent Carbon Dots for Drug Delivery Carbon 2013, 59, 192-199
47. Majoros, I. J.; Myc, A.; Thomas, T.; Mehta, C. B.; Baker, J. R., Jr. PAMAM Dendrimer-based Multifunctional Conjugate for Cancer Therapy: Synthesis, Characterization, and Functionality Biomacromolecules 2006, 7, 572-579
48. Li, X.; Gao, C.; Wu, Y.; Cheng, C. Y.; Xiac, W.; Zhang, Z. Combination Delivery of Adjudin and Doxorubicin via Integrating Drug Conjugation and Nanocarrier Approaches for the Treatment of Drug-resistant Cancer Cells J. Mater. Chem. B 2015, 3, 1556-1564
49. Huang, R.; Ke, W.; Liu, Y.; Jiang, C.; Pei, Y. The Use of Lactoferrin as a Ligand for Targeting the Polyamidoamine-based Gene Delivery System to the Brain Biomaterials 2008, 29, 238-246
50. Tong, G.; Wang, J.; Wang, R.; Guo, X.; He, L.; Qiu, F.; Wang, Ge.; Zhu, B.; Zhu, X.; Liu, T. Amorphous Carbon Dots with High two-photon Fluorescence for Cellular Imaging Passivated by Hyperbranched Poly(amino amine) J. Mater. Chem. B 2015, 3, 700-706
51. Maiti, P. K.; Cagin, T.; Lin, S. T.; Goddard, W. A. Effect of Solvent and pH on the Structure of PAMAM Dendrimers Macromolecules 2005, 38, 979-991
52. Dong, Y.; Wang, R.; Li, H.; Shao, J.; Chi, Y.; Lin, X.; Chen, G. Polyamine-Functionalized Carbon Quantum Dots for Chemical Sensing Carbon 2012, 50, 2810-2815
53. Yordanov, G.; Evangelatov, A.; Skrobanska, R. Epirubicin Loaded to Pre-Polymerized Poly(butyl cyanoacrylate) Nanoparticles: Preparation and In Vitro Evaluation in Human Lung Adenocarcinoma Cells Colloids Surf., B 2013, 107, 115-123
54. Sahay, G.; Alakhova, D. Y.; Kabanov, A. V. Endocytosis of Nanomedicines J. Controlled Release 2010, 145, 182-195
55. Kitchens, K. M.; Foraker, A. B.; Kolhatkar, R. B.; Swaan, P. W.; Ghandehari, H. Endocytosis and Interaction of Poly (amidoamine) Dendrimers with Caco-2 cells Pharm. Res. 2007, 24, 2138-2145
56. Kitchens, K. M.; Kolhatkar, R. B.; Swaan, P. W.; Ghandehari, H. Endocytosis Inhibitors prevent Poly(amidoamine) Dendrimer Internalization and Permeability across Caco-2 cells Mol. Pharmaceutics. 2008, 5, 364-369
57. Fornari, F. A.; Randolph, J. K.; Yalowich, J. C.; Ritke, M. K.; Gewirtz, D. A. Interference by Doxorubicin with DNA Unwinding in MCF-7 Breast Tumor Cells Mol. Pharmacol. 1994, 45, 649-656
58. Olinski, R.; Gackowski, D.; Foksinski, M.; Rozalski, R.; Roszkowski, K.; Jaruga, P. Oxidative DNA damage: Assessment of the Role in Carcinogenesis, Atherosclerosis, and Acquired Immunodeficiency Syndrome Free Radical Biol. Med. 2002, 33, 192-200
59. Lo, Y. L.; Wang, W. Formononetin Potentiates Epirubicin-Induced Apoptosis via ROS Production in HeLa cells In Vitro Chem. Biol. Interact. 2013, 205, 188-197
60. Riccardi, C.; Nicoletti, I. Analysis of Apoptosis by Propidium Iodide Staining and Flow Cytometry Nat. Protoc. 2006, 1, 1458-1461
61. Darzynkiewicz, Z.; Bruno, S.; Del, B. G.; Gorczyca, W.; Hotz, M. A.; Lassota, P.; Traganos, F. Features of Apoptotic cells Measured by Flow Cytometry Cytometry 1992, 13, 795-808
62. Rello, S.; Stockert, J. C.; Moreno, V.; Gámez, A.; Pacheco, M.; Juarranz, A.; Caete, M.; Villanueva, A. Morphological Criteria to Distinguish Cell Death Induced by Apoptotic and Necrotic Treatments Apoptosis 2005, 10, 201-208
63. Hu, D. G.; Rogers, A.; Mackenzie, P. I. Epirubicin Upregulates UDP glucuronosyltransferase 2B7 Expression in Liver Cancer cells via the p53 pathway Mol. Pharmacol. 2014, 85, 887-897
64. Millour, J.; de Olano, N.; Horimoto, Y.; Monteiro, L. J.; Langer, J. K.; Aligue, R.; Hajji, N.; Lam, E. W. ATM and p53 Regulate FOXM1 Expression via E2F in Breast Cancer Epirubicin Treatment and Resistance Mol. Cancer Ther. 2011, 10, 1046-1058
65. Chao, D. T.; Korsmeyer, S. J. BCL-2 family: Regulators of Cell Death Annu. Rev. Immunol. 1998, 16, 395-419
66. Wolter, K. G.; Hsu, Y. T.; Smith, C. L.; Nechushtan, A.; Xi, X. G.; Youle, R. J. Movement of Bax from the Cytosol to Mitochondria During Apoptosis J. Cell Biol. 1997, 139, 1281-1292
67. Liu, X.; Kim, C. N.; Yang, J.; Jemmerson, R.; Wang, X. Induction of Apoptotic Program in Cell-Free Extracts: Requirement for dATP and cytochrome c Cell 1996, 86, 147-157
68. Porter, A. G.; Jänicke, R. U. Emerging Roles of Caspase-3 in Apoptosis Cell Death Differ. 1999, 6, 99-104
69. Lee, Y. K.; Lin, T. H.; Chang, C. F.; Lo, Y. L. Galectin-3 Silencing Inhibits Epirubicin-Induced ATP Binding Cassette Transporters and Activates the Mitochondrial Apoptosis Pathway via β-catenin/GSK-3β Modulation in Colorectal Carcinoma PLoS One 2013, 8, 82478