Photothermal therapeutic response of cancer cells to aptamer-gold nanoparticle-hybridized graphene oxide under NIR illumination

ACS Applied Materials and Interfaces

Volumn 7, Issue 9, 2015, Pages 5097-5106

  Yang, Lingyan ^a   Tseng, Yu Ting ^b   Suo, Guangli ^a   Chen, Liliang ^c   Yu, Jiantao ^a   Chiu, Wei Jane ^d   Huang, Chih Ching ^d,e   Lin, Chia Hua ^a  

^a SUZHOU INSTITUTE OF NANO TECH AND NANO BIONICS   (China)

^b NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^c RESEARCH CENTER OF LASER FUSION   (China)

^d NATIONAL TAIWAN OCEAN UNIVERSITY   (Taiwan)

^e KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

Author keywords

aptamers; cancer cells; gold nanoparticles; graphene oxides; HSP70; phototherapy

Indexed keywords

BIOCOMPATIBILITY; CYTOLOGY; DISEASES; GOLD NANOPARTICLES; GRAPHENE; GRAPHENE OXIDE; INFRARED DEVICES; METAL NANOPARTICLES; NANOCOMPOSITES; PROTEINS; SYNTHESIS (CHEMICAL); TUMORS;

APTAMERS; CANCER CELLS; HSP70; HUMAN BREAST CANCER CELLS; PHOTOTHERAPY; PHOTOTHERMAL THERAPY; SPECIFIC INTERACTION; TARGETING CAPABILITY;

CELLS;

APOPTOSIS REGULATORY PROTEIN; APTAMER; GOLD; GRAPHITE; HEAT SHOCK PROTEIN 70; METAL NANOPARTICLE; MUC1 PROTEIN, HUMAN; MUCIN 1; NANOCOMPOSITE; OXIDE; PURINE NUCLEOSIDE; RHODAMINE; RHODAMINE B; VER 155008;

ANTAGONISTS AND INHIBITORS; BREAST NEOPLASMS; CELL SURVIVAL; CHEMISTRY; DRUG EFFECTS; FEMALE; FLUORESCENCE MICROSCOPY; HUMAN; INFRARED RADIATION; MCF 7 CELL LINE; METABOLISM; PATHOLOGY; PHOTOTHERAPY; RADIATION RESPONSE; TEMPERATURE; UMBILICAL VEIN ENDOTHELIAL CELL;

APOPTOSIS REGULATORY PROTEINS; APTAMERS, NUCLEOTIDE; BREAST NEOPLASMS; CELL SURVIVAL; FEMALE; GOLD; GRAPHITE; HSP70 HEAT-SHOCK PROTEINS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; INFRARED RAYS; MCF-7 CELLS; METAL NANOPARTICLES; MICROSCOPY, FLUORESCENCE; MUCIN-1; NANOCOMPOSITES; OXIDES; PHOTOTHERAPY; PURINE NUCLEOSIDES; RHODAMINES; TEMPERATURE;

EID: 84924565724     PISSN: 19448244     EISSN: 19448252     Source Type: Journal    
DOI: 10.1021/am508117e     Document Type: Article

References (57)

1. Bray, F.; Ren, J. S.; Masuyer, E.; Ferlay, J. Global Estimates of Cancer Prevalence for 27 Sites in the Adult Population in 2008 Int. J. Cancer 2013, 132, 1133-1145
2. Ferlay, J.; Soerjomataram, I.; Ervik, M.; Dikshit, R.; Eser, S.; Mathers, C.; Rebelo, M.; Parkin, D. M.; Forman, D.; Bray, F.; GLOBOCAN 2012 v1.0: Cancer Incidence and Mortality Worldwide. CancerBase No. 11. International Agency for Research on Cancer, World Health Organization: Lyon, France; 2013.
3. Wu, P.; Gao, Y.; Zhang, H.; Cai, C. Aptamer-Guided Silver-Gold Bimetallic Nanostructures with Highly Active Surface-Enhanced Raman Scattering for Specific Detection and Near-Infrared Photothermal Therapy of Human Breast Cancer Cells Anal. Chem. 2012, 84, 7692-7699
4. Yin, D.; Li, Y.; Lin, H.; Guo, B.; Du, Y.; Li, X.; Jia, H.; Zhao, X.; Tang, J.; Zhang, L. Functional Graphene Oxide as a Plasmid-Based Stat3 SiRNA Carrier Inhibits Mouse Malignant Melanoma Growth in Vivo Nanotechnology 2013, 24, 105102
5. Chen, Y.-W.; Chen, P.-J.; Hu, S.-H.; Chen, I. W.; Chen, S.-Y. NIR-Triggered Synergic Photo-Chemothermal Therapy Delivered by Reduced Graphene Oxide/Carbon/Mesoporous Silica Nanocookies Adv. Funct. Mater. 2013, 24, 451-459
6. Xu, C.; Yang, D.; Mei, L.; Li, Q.; Zhu, H.; Wang, T. Targeting Chemophotothermal Therapy of Hepatoma by Gold Nanorods/Graphene Oxide Core/Shell Nanocomposites ACS Appl. Mater. Interfaces 2013, 5, 12911-12920
7. Zedan, A. F.; Moussa, S.; Terner, J.; Atkinson, G.; El-Shall, M. S. Ultrasmall Gold Nanoparticles Anchored to Graphene and Enhanced Photothermal Effects by Laser Irradiation of Gold Nanostructures in Graphene Oxide Solutions ACS Nano 2013, 7, 627-636
8. 2 Nanosheets as a Multifunctional Theranostic Agent for in Vivo Dual-Modal CT/Photoacoustic Imaging Guided Photothermal Therapy Adv. Mater. 2014, 26, 1886-1893
9. Wang, C.; Cheng, L.; Liu, Y.; Wang, X.; Ma, X.; Deng, Z.; Li, Y.; Liu, Z. Imaging-Guided pH-Sensitive Photodynamic Therapy Using Charge Reversible Upconversion Nanoparticles under Near-Infrared Light Adv. Funct. Mater. 2013, 23, 3077-3086
10. Lu, F.; Popa, A.; Zhou, S.; Zhu, J. J.; Samia, A. C. S. Iron Oxide-Loaded Hollow Mesoporous Silica Nanocapsules for Controlled Drug Release and Hyperthermia Chem. Commun. 2013, 49, 11436-11438
11. Zhang, F.; Braun, G. B.; Pallaoro, A.; Zhang, Y.; Shi, Y.; Cui, D.; Moskovits, M.; Zhao, D.; Stucky, G. D. Mesoporous Multifunctional Upconversion Luminescent and Magnetic "Nanorattle" Materials for Targeted Chemotherapy Nano Lett. 2012, 12, 61-67
12. Luo, Y.-L.; Shiao, Y.-S.; Huang, Y.-F. Release of Photoactivatable Drugs from Plasmonic Nanoparticles for Targeted Cancer Therapy ACS Nano 2011, 5, 7796-7804
13. Overgaard, J. The Current and Potential Role of Hyperthermia in Radiotherapy Int. J. Radiat. Oncol. Biol. Phys. 1989, 16, 535-549
14. Lepock, J. R. Cellular Effects of Hyperthermia: Relevance to the Minimum Dose for Thermal Damage Int. J. Hyperthermia 2003, 19, 252-266
15. Ke, H.; Yue, X.; Wang, J.; Xing, S.; Zhang, Q.; Dai, Z.; Tian, J.; Wang, S.; Jin, Y. Gold Nanoshelled Liquid Perfluorocarbon Nanocapsules for Combined Dual Modal Ultrasound/CT Imaging and Photothermal Therapy of Cancer Small 2014, 10, 1220-1227
16. 4 Particles with Extremely Low Toxicity as Highly Efficient Near-Infrared Photothermal Agents for in Vivo Tumor Ablation Nanoscale 2013, 5, 8056-8066
17. Akhavan, O.; Ghaderi, E. Graphene Nanomesh Promises Extremely Efficient in Vivo Photothermal Therapy Small 2013, 9, 3593-3601
18. Antaris, A. L.; Robinson, J. T.; Yaghi, O. K.; Hong, G.; Diao, S.; Luong, R.; Dai, H. Ultra-Low Doses of Chirality Sorted (6,5) Carbon Nanotubes for Simultaneous Tumor Imaging and Photothermal Therapy ACS Nano 2013, 7, 3644-3652
19. Cole, J. R.; Mirin, N. A.; Knight, M. W.; Goodrich, G. P.; Halas, N. J. Photothermal Efficiencies of Nanoshells and Nanorods for Clinical Therapeutic Applications J. Phys. Chem. C 2009, 113, 12090-12094
20. Dreaden, E. C.; Mackey, M. A.; Huang, X.; Kanga, B.; El-Sayed, M. A. Beating Cancer in Multiple Ways Using Nanogold Chem Soc. Rev. 2011, 40, 3391-3404
21. Robinson, J. T.; Tabakman, S. M.; Liang, Y.; Wang, H.; Sanchez Casalongue, H.; Vinh, D.; Dai, H. Ultrasmall Reduced Graphene Oxide with High Near-Infrared Absorbance for Photothermal Therapy J. Am. Chem. Soc. 2011, 133, 6825-6831
22. 4 Composites by a Solvothermal Reaction New J. Chem. 2010, 34, 2950-2955
23. Kakran, M.; Sahoo, N. G.; Bao, H.; Pan, Y.; Li, L. Functionalized Graphene Oxide as Nanocarrier for Loading and Delivery of Ellagic Acid Curr. Med. Chem. 2011, 18, 4503-4512
24. Shiang, Y. C.; Ou, C. M.; Chen, S. J.; Ou, T. Y.; Lin, H. J.; Huang, C. C.; Chang, H. T. Highly Efficient Inhibition of Human Immunodeficiency Virus Type 1 Reverse Transcriptase by Aptamers Functionalized Gold Nanoparticles Nanoscale 2013, 5, 2756-2764
25. Zhang, Z.; Ali, M. M.; Eckert, M. A.; Kang, D. K.; Chen, Y. Y.; Sender, L. S.; Fruman, D. A.; Zhao, W. A. Polyvalent Aptamer System for Targeted Drug Delivery Biomaterials 2013, 34, 9728-9735
26. Barbas, A. S.; Mi, J.; Clary, B. M.; White, R. R. Aptamer Applications for Targeted Cancer Therapy Future Oncol. 2010, 6, 1117-1126
27. Tan, L.; Neoh, K. G.; Kang, E. T.; Choe, W. S.; Su, X. Pegylated Anti-Muc1 Aptamer-Doxorubicin Complex for Targeted Drug Delivery to MCF7 Breast Cancer Cells Macromol. Biosci. 2011, 11, 1331-1335
28. Gaemers, I. C.; Vos, H. L.; Volders, H. H.; van der Valk, S. W.; Hilkens, J. A Stat-Responsive Element in the Promoter of the Episialin/MUC1 Gene Is Involved in Its Overexpression in Carcinoma Cells J. Biol. Chem. 2001, 276, 6191-6199
29. Walsh, M. D.; Luckie, S. M.; Cummings, M. C.; Antalis, T. M.; McGuckin, M. A. Heterogeneity of MUC1 Expression by Human Breast Carcinoma Cell Lines in Vivo and in Vitro Breast Cancer Res. Treat. 1999, 58, 255-266
30. Hattrup, C. L.; Gendler, S. J. MUC1 Alters Oncogenic Events and Transcription in Human Breast Cancer Cells Breast Cancer Res. 2006, 8, R37
31. Mosser, D. D.; Morimoto, R. I. Molecular Chaperones and the Stress of Oncogenesis Oncogene 2004, 23, 2907-2918
32. Kim, L. S.; Kim, J. H. Heat Shock Protein as Molecular Targets for Breast Cancer Therapeutics J. Breast Cancer 2011, 14, 167-174
33. Siebelt, M.; Jahr, H.; Groen, H. C.; Sandker, M.; Waarsing, J. H.; Kops, N.; Muller, C.; van Eden, W.; de Jong, M.; Weinans, H. HSP90 Inhibition Protects against Biomechanically Induced Osteoarthritis in Rats Arthritis Rheumatol. 2013, 65, 2102-2112
34. Jego, G.; Hazoume, A.; Seigneuric, R.; Garrido, C. Targeting Heat Shock Proteins in Cancer Cancer Lett. 2013, 332, 275-285
35. Mosser, D. D.; Caron, A. W.; Bourget, L.; Denis-Larose, C.; Massie, B. Role of the Human Heat Shock Protein HSP70 in Protection against Stress-Induced Apoptosis Mol. Cell. Biol. 1997, 17, 5317-5327
36. Moseley, P. L. Heat Shock Proteins and Heat Adaptation of the Whole Organism J. Appl. Physiol. 1997, 83, 1413-1417
37. Huang, H. C.; Yang, Y.; Nanda, A.; Koria, P.; Rege, K. Synergistic Administration of Photothermal Therapy and Chemotherapy to Cancer Cells Using Polypeptide-Based Degradable Plasmonic Matrices Nanomedicine (London, U. K.) 2011, 6, 459-473
38. Ito, A.; Saito, H.; Mitobe, K.; Minamiya, Y.; Takahashi, N.; Maruyama, K.; Motoyama, S.; Katayose, Y.; Ogawa, J. Inhibition of Heat Shock Protein 90 Sensitizes Melanoma Cells to Thermosensitive Ferromagnetic Particle-Mediated Hyperthermia with Low Curie Temperature Cancer Sci. 2009, 100, 558-564
39. Milanovic, D.; Firat, E.; Grosu, A. L.; Niedermann, G. Increased Radiosensitivity and Radiothermosensitivity of Human Pancreatic MIA PaCa-2 and U251 Glioblastoma Cell Lines Treated with the Novel HSP90 Inhibitor NVP-HSP990 Radiat. Oncol. 2013, 8, 42
40. Massey, A. J.; Williamson, D. S.; Browne, H.; Murray, J. B.; Dokurno, P.; Shaw, T.; Macias, A. T.; Daniels, Z.; Geoffroy, S.; Dopson, M.; Lavan, P.; Matassova, N.; Francis, G. L.; Graham, C. J.; Parsons, R.; Wang, Y.; Padfield, A.; Comer, M.; Drysdale, M. J.; Wood, M. A Novel, Small Molecule Inhibitor of HSC70/HSP70 Potentiates HSP90 Inhibitor Induced Apoptosis in HCT116 Colon Carcinoma Cells Cancer Chemother. Pharmacol. 2010, 66, 535-545
41. Chatterjee, M.; Andrulis, M.; Stuhmer, T.; Muller, E.; Hofmann, C.; Steinbrunn, T.; Heimberger, T.; Schraud, H.; Kressmann, S.; Einsele, H.; Bargou, R. C. The PI3K/Akt Signaling Pathway Regulates the Expression of HSP70, Which Critically Contributes to HSP90-Chaperone Function and Tumor Cell Survival in Multiple Myeloma Haematologica 2013, 98, 1132-1141
42. Guo, F.; Rocha, K.; Bali, P.; Pranpat, M.; Fiskus, W.; Boyapalle, S.; Kumaraswamy, S.; Balasis, M.; Greedy, B.; Armitage, E. S.; Lawrence, N.; Bhalla, K. Abrogation of Heat Shock Protein 70 Induction as a Strategy to Increase Antileukemia Activity of Heat Shock Protein 90 Inhibitor 17-Allylamino-Demethoxy Geldanamycin Cancer Res. 2005, 65, 10536-10544
43. Lanneau, D.; Brunet, M.; Frisan, E.; Solary, E.; Fontenay, M.; Garrido, C. Heat Shock Proteins: Essential Proteins for Apoptosis Regulation J. Cell. Mol. Med. 2008, 12, 743-761
44. Hummers, W. S.; Offeman, R. E. Preparation of Graphitic Oxide J. Am. Chem. Soc. 1958, 80, 1339-1339
45. Kudin, K. N.; Ozbas, B.; Schniepp, H. C.; Prudhomme, R. K.; Aksay, I. A.; Car, R. Raman Spectra of Graphite Oxide and Functionalized Graphene Sheets Nano Lett. 2008, 8, 36-41
46. Manani, G.; Morris, M.; Caudle, S.; Wanekaya, A.; Mugweru, A. Electrocatalytic Oxidation of Propranol Using Microwave Synthesized Graphene Decorated with Gold Nanoparticles and Single Walled Carbon Nanotubes. Chem Mater. Res. 2013, 3, 39-48
47. Marcano, D. C.; Kosynkin, D. V.; Berlin, J. M.; Sinitskii, A.; Sun, Z.; Slesarev, A.; Alemany, L. B.; Lu, W.; Tour, J. M. Improved Synthesis of Graphene Oxide ACS Nano 2010, 4, 4806-4814
48. Mucic, R. C.; Storhoff, J. J.; Mirkin, C. A.; Letsinger, R. L. DNA-Directed Synthesis of Binary Nanoparticle Network Materials J. Am. Chem. Soc. 1998, 120, 12674-12675
49. Liua, Y.; Liua, C. Y.; Liua, Y. Investigation on Fluorescence Quenching of Dyes by Graphite Oxide and Graphene Appl. Surf. Sci. 2011, 257, 5513-5518
50. Wang, Y.; Wang, H.; Liu, D.; Song, S.; Wang, X.; Zhang, H. Graphene Oxide Covalently Grafted Upconversion Nanoparticles for Combined NIR Mediated Imaging and Photothermal/Photodynamic Cancer Therapy Biomaterials 2013, 34, 7715-7724
51. Qin, X. C.; Guo, Z. Y.; Liu, Z. M.; Zhang, W.; Wan, M. M.; Yang, B. W. Folic Acid-Conjugated Graphene Oxide for Cancer Targeted Chemo-Photothermal Therapy J. Photochem. Photobiol., B 2013, 120, 156-162
52. Lim, D. K.; Barhoumi, A.; Wylie, R. G.; Reznor, G.; Langer, R. S.; Kohane, D. S. Enhanced Photothermal Effect of Plasmonic Nanoparticles Coated with Reduced Graphene Oxide Nano Lett. 2013, 13, 4075-4079
53. Abdelsayed, V.; Moussa, S.; Hassan, H. M.; Aluri, H. S.; Collinson, M. M.; El-Shall, M. S. Photothermal Deoxygenation of Graphite Oxide with Laser Excitation in Solution and Graphene-Aided Increase in Water Temperature J. Phys. Chem. Lett. 2010, 1, 2804-2809
54. Kroll, A.; Pillukat, M. H.; Hahn, D.; Schnekenburger, J. Interference of Engineered Nanoparticles with in Vitro Toxicity Assays Arch. Toxicol. 2012, 86, 1123-1136
55. Huang, J.; Zong, C.; Shen, H.; Liu, M.; Chen, B.; Ren, B.; Zhang, Z. Mechanism of Cellular Uptake of Graphene Oxide Studied by Surface-Enhanced Raman Spectroscopy Small 2012, 8, 2577-2584
56. Elmore, S. Apoptosis: A Review of Programmed Cell Death Toxicol. Pathol. 2007, 35, 495-516
57. Schmitt, E.; Gehrmann, M.; Brunet, M.; Multhoff, G.; Garrido, C. Intracellular and Extracellular Functions of Heat Shock Proteins: Repercussions in Cancer Therapy J. Leukocyte Biol. 2007, 81, 15-27