Graphene oxide: A carrier for pharmaceuticals and a scaffold for cell interactions

Current Topics in Medicinal Chemistry

Volumn 15, Issue 4, 2015, Pages 309-327

  Durán, Nelson ^a   Martinez, Diego Stéfani T ^b   Silveira, Camila P ^a   Durán, Marcela ^a   de Moraes, Ana C M ^a   Simões, Mateus B ^a   Alves, Oswaldo L ^a   Fávaro, Wagner J ^a  

^a UNIVERSITY OF CAMPINAS   (Brazil)

^b BRAZILIAN CENTER FOR RESEARCH IN ENERGY AND MATERIALS CNPEM   (Brazil)

Author keywords

Doxorubicin; Graphene oxide; Nanocarrier; Protein corona; Stem cells

Indexed keywords

DOXORUBICIN; EPIRUBICIN; GRAPHENE OXIDE; MOLECULAR SCAFFOLD; SILVER NANOPARTICLE; DRUG; DRUG CARRIER; GRAPHITE; OXIDE;

ADSORPTION KINETICS; ARTICLE; BIOCOMPATIBILITY; CELL INTERACTION; CELL VIABILITY ASSAY; CHEMICAL STRUCTURE; CYSTECTOMY; DRUG DELIVERY SYSTEM; DRUG INDUSTRY; GENE EXPRESSION; HUMAN; HYDROPHOBICITY; MESENCHYMAL STEM CELL; MORPHOLOGICAL ADAPTATION; NONHUMAN; OXIDATION; PUBLICATION; SIGNAL TRANSDUCTION; THERMODYNAMICS; TRANSMISSION ELECTRON MICROSCOPY; CELL ADHESION; CHEMISTRY; DRUG EFFECTS; NEOPLASMS; PATHOLOGY;

CELL ADHESION; DRUG CARRIERS; GRAPHITE; HUMANS; NEOPLASMS; OXIDES; PHARMACEUTICAL PREPARATIONS;

EID: 84940394950     PISSN: 15680266     EISSN: 18734294     Source Type: Journal    
DOI: 10.2174/1568026615666150108144217     Document Type: Article

References (167)

1. Novoselov, K.S.; Geim, A.K.; Morozov, S.V.; Jiang, D.; Zhang, Y.; Dubonos, S.V.; Grigorieva, I.V.; Firsov, A.A. Electric field effect in atomically thin carbon films. Science, 2004, 306, 666-669.
2. Park, S.; Ruoff, R. S. Chemical methods for the production of graphenes. Nat. Nanotechnol., 2009, 4, 217-224.
3. Dreyer, D.R.; Todd, A.D.; Bielawski, C.W. Harnessing the chemistry of graphene oxide. Chem. Soc. Rev., 2014, 43, 5288-5301.
4. Goenka S.; Sant V.; Sant S. Graphene-based nanomaterials for drug delivery and tissue engineering. J. Control. Release, 2014, 173, 75–88.
5. Dreyer, D.R.; Park, S.; Bielawski, C.W.; Ruoff, R.S. The chemistry of graphene oxide. Chem. Soc. Rev. 2010, 39, 228-240.
6. Bai, H.; Li, C.; Shi, G.Q. Functional Composite Materials Based on Chemically Converted Graphene. Adv. Mater. 2011, 23, 1089-1115.
7. Brodie, B.C. On the atomic weight of graphite. Philos. Trans. R. Soc. London, 1859, 149, 249–259.
8. Soldano, C.; Mahmood, A.; Dujardin, E. Production, properties and potential of graphene. Carbon, 2010, 48, 2127-2150.
9. Staudenmaier, L., Verfahren zur darstellung der graphitsaure. Ber. Dtsch. Chem. Ges. 1898, 31, 1481–1487.
10. Hummers, W.S.; Offeman, R.E. Preparation of graphitic oxide. J. Am. Chem. Soc., 1958, 80, 1339-1339.
11. Kovtyukhova, N.I.; Ollivier, P.J.; Martin, B.R.; Mallouk, T.E.; Chizhik, S.A.; Buzaneva, E. V.; Gorchinskiy, A. D. Layer-by-layer assembly of ultrathin composite films from micron-sized graphite oxide sheets and polycations. Chem. Mater. 1999, 11, 771-778.
12. Marcano D. C.; Kosynkin, D. V.; Berlin, J. M.; Sinitskii, A.; Sun, Z.; Slesarev, A., Alemany, LB.; Lu, W.; Tour, J. M. Improved synthesis of graphene oxide. ACS Nano, 2010, 4, 4806–4814.
13. Park S.; An, J.; Jung, I.; Piner, R. D.; An, S. J.; Li, X.; Velamakanni, A.; Ruoff, R. S. Colloidal suspensions of highly reduced graphene oxide in a wide variety of organic solvents. Nano Lett. 2009, 9, 1593-1597.
14. Lerf, A.; He, H. Y.; Forster, M.; Klinowski, J. Structure of graphite oxide revisited. J. Phys. Chem. B, 1998, 102, 4477-4482.
15. Verdejo, R.; Lamoriniere, S.; Cottam, B.; Bismarck, A.; Shaffer, M. Removal of oxidation debris from multi-walled carbon nanotubes. Chem. Commun., 2007, 513-515.
16. Stefani, D.; Paula, A.J.; Vaz, B.G.; Silva, R. A.; Andrade, N. F.; Justo, G. Z.; Ferreira, C. V.; Souza Filho, A. G.; Eberlin, M. N.; Alves, O. L. Structural and proactive safety aspects of oxidation debris from multiwalled carbon nanotubes. J. Hazard. Mater., 2011, 189, 391–396.
17. Faria, A.F.; Martinez, D.S.T.; Moraes, A.C.M.; Maia da Costa, M. E. H.; Barros, E. B.; Souza Filho, A. G.; Paula, A. J.; Alves, O. L. Unveiling the role of oxidation debris on the surface chemistry of graphene through the anchoring of Ag nanoparticles. Chem. Mater., 2012, 24, 4080–4087.
18. Rourke, J. P.; Pandey, P. A.; Moore, J. J.; Bates, M.; Kinloch, I. A.; Young R. J.; Wilson, N. R. The real graphene oxide revealed: stripping the oxidative debris from the graphene-like sheets. Angew. Chem. Int. Ed., 2011, 50, 3173–3177.
19. Coluci, V.R.; Martinez, D.S.T.; Honorio, J.G.; de Faria, A.F.; Morales, D.A.; Skaf, M.S.; Alves, O.L.; Umbuzeiro, G.A. Noncovalent interaction with graphene oxide: The crucial role of oxidative debris. J. Phys. Chem. C., 2014, 118, 2187–2193.
20. Bao, H.Q.; Pan, Y.Z.; Ping, Y.; Sahoo, N.G.; Wu, T.; Li, L.; Gan, L.H. Chitosan-functionalized graphene oxide as a nanocarrier for drug and gene delivery. Small, 2011,7, 1569–1578.
21. Shen, J.; Shi, M.; Yan, B.; Ma, H.; Li, N.; Hu, Y.; Ye, M. Covalent attaching protein to graphene oxide via diimide-activated amidation. Colloids Surf., B, 2010, 81, 434-438.
22. Lu, C-H.; Yang, H-H.; Zhu, C-L.; Chen, X.; Chen, G.N. A Graphene platform for sensing biomolecules. Angew. Chem. Int. Ed. Engl., 2009, 48, 4785-4787.
23. Mertens, R., The Graphene Handbook, 2013, Lulu Press, USA.
24. Wespanick, K.A.; Smith, B.A.; Bitter, J.L.; Fairbrother, H. Chemical and structural characterization of carbon nanotube surfaces. Anal Bional Chem, 2010, 396, 1003-1014.
25. Yang, D.; Velamakanni, A.; Bozoklu, G.; Park, S.; Stoller, M.; Piner, R. D.; Stankovich, S.; Jung, I.; Field, D.A.; Ventrice Jr, C.A.; Ruoff, R.S. Chemical analysis of graphene oxide films after heat and chemical treatments by X-ray photoelectron and Micro-Raman spectroscopy. Carbon 2009, 47, 145-152.
26. Gengler, R.Y.N.; Spyrou, K.; Rudolf, P. A roadmap to high quality chemically prepared graphene. J. Phys. D: Appl. Phys. 2010, 43, 374015-374019.
27. Allen, M.J.; Tung, V.C.; Kaner, R.B. Honeycomb carbon: a review of graphene. Chem. Rev. 2010, 110, 132-145.
28. Sharma, P.; Darabdhara, G.; Reddy, T.M.; Borah, A.; Bezboruah, P.; Gogoi, P.; Hussain, N.; Sengupta, P.; Das, M.R. Synthesis, characterization and catalytic application of Au NPs-reduced graphene oxide composites material: an eco-friendly approach. Catal. Commun., 2013, 40, 139-144.
29. Paredes, J. I.; Villar-Rodil, S.; Martínez-Alonso, A.; Tascón, J.M.D. Graphene oxide dispersions in organic solvents. Langmuir, 2008, 24, 10560-10564.
30. Liu, Z.; Robinson, J.T.; Sun, X.M.; Dai, H. PEGylated nanographene oxide for delivery of water-insoluble cancer drugs. J. Am. Chem. Soc., 2008, 130, 10876–19877.
31. Sun, X.; Liu, Z.; Welsher, K.; Robinson, J.T.; Goodwin, A.; Zaric, S.; Dai, H. Nano-graphene oxide for cellular imaging and drug delivery. Nano Res., 2008, 1, 203-212.
32. Pan, Y.; Sahoo, N.G.; Li, L. The application of graphene oxide in drug delivery. Exp. Opin. Drug Deliv., 2012, 12, 13265–13276.
33. Feng, L.; Wu, L.; Qu, X. New horizons for diagnostics and therapeutic applications of graphene and graphene oxide. Adv. Mater., 2013, 25, 168–186.
34. Yang, K.; Feng, L.; Shi, X.; Liu, Z. Nano-graphene in biomedicine: theranostic applications. Chem. Soc. Rev., 2013, 42, 530–547.
35. Liu J.; Cui, L.; Losic, D. Graphene and graphene oxide as new nanocarriers for drug delivery applications. Acta Biomaterialia, 2013, 9, 9243–9257.
36. Jin, S.E.; Jin, H.E.; Hong, S.S. Targeted delivery system of nanobiomaterials in anticancer therapy: from cells to clinics. BioMed. Res. Intern., 2014, Art. ID 814208.
37. Bonanni, A.; Ambrosi, A.; Chua, C.K.; Pumera, M. Oxidation debris in graphene oxide is responsible for its inherent electroactivity. ACS Nano, 2014, 8, 4197-4204.
38. Yang, K.; Zhang, S.A.; Zhang, G.X.; 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.
39. Jing, Y.; Zhu, Y.; Yang, X.; Shen, J.; Li, C. Ultrasound-triggered smart drug release from multifunctional core_shell capsules onestep fabricated by coaxial electrospray method. Langmuir, 2010, 27, 1175–1180.
40. 4 composites by a solvothermal reaction. New J. Chem., 2010, 34, 2950–2955.
41. Liu, J-H.; Yang, S-T.; Wang, H.; Chang, Y.; Cao, A.; Liu, Y. Effect of size and dose on the biodistribution of graphene oxide in mice. Nanomedicine, 2012, 7, 1801-1812.
42. Wen, H.; Dong, C.; Dong, H.; Shen A.; Xia, W.; Cai, X.; Song, Y.; Li, X.; Li, Y.; Shi, D. Engineered redox-responsive PEG detachment mechanism in PEGylated nano-graphene oxide for intracellular drug delivery. Small, 2012, 8, 760-769.
43. Bai, H.; Li, C.; Wang, X.L.; Shi, G. A pH-sensitive graphene oxide composite hydrogel. Chem. Commun., 2010, 46, 2376–2378.
44. 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.
45. Wu, J.; Wang, Y.S., Yang, X.Y.; Liu, Y.Y.; Yang, J.R.; Yang, R.; Zhang, N. Graphene oxide used as a carrier for adriamycin can reverse drug resistance in breast cancer cells. Nanotechnology, 2012, 23, 355101.
46. Lu, Y.J.; Yang, H.W.; Hung, S.C.; Li S.M.; Ma, C.C.; Chen, P.Y.; Tsai, H.C.; Wei, K.C.; Chen, J.P. Improving thermal stability and efficacy of BCNU in treating glioma cells using PAA functionalized graphene oxide. Int. J. Nanomed., 2012, 7, 1737–1747.
47. Ma, D.; Lin, J.T.; Chen, Y.Y.; Xue, W.; Zhang, L-M. In situ gelation and sustained release of an antitumor drug by graphene oxide nanosheets. Carbon, 2012, 50, 3001–3007.
48. Zhang, L.; Xia, J.; Zhao, Q.; Liu, L.; Zhang, Z. Functional graphene oxide as a nanocarrier for controlled loading and targeted delivery of mixed anticancer drugs. Small, 2010, 6, 537-544.
49. Zhang, L.M.; Lu, Z.X.; Zhao, Q.H.; Huang, J.; Shen, H.; Zhang, Z. Enhanced chemotherapy efficacy by sequential delivery of siRNA and anticancer drugs using PEI-grafted graphene oxide. Small, 2011, 7, 460–464.
50. Zhou, T.; Zhou, X.; Xing, D. Controlled release of doxorubicin from graphene oxide based charge-reversal nanocarrier. Biomaterials, 2014, 35, 4185-4194.
51. Wang, H.; Gu, W.; Xiao, N.; Ye, L.; Xu, Q. Chlorotoxinconjugated graphene oxide for targeted delivery of an anticancer drug. Inter. J. Nanomed., 2014, 9, 1433–1442.
52. Wu, S.; Zhao, X.; Li, Y.; Du, Q.; Sun, J.; Wang, Y.; Wang, X.; Xia, Y.; Wang, Z.; Xia, L. Adsorption properties of doxorubicin hydrochloride onto graphene oxide: equilibrium, kinetic and thermodynamic studies. Materials, 2013, 6, 2026-2042.
53. Zhang, Q.; Li, W.; Kong, T.; Su, R.; Li, N.; Song, Q.; Tang, M.; Liu, L.; Cheng, G. Tailoring the interlayer interaction between doxorubicin-loaded graphene oxide nanosheets by controlling the drug content. Carbon, 2013, 51, 164-172.
54. Wojtoniszak, M.; Urbas, K.; Perużyńska, M.; Kurzawski, M.; Drozdzik, M.; Mijowska, E. Covalent conjugation of graphene oxide with methotrexate and its antitumor activity. Chem. Phys. Let., 2013, 568-569, 151-156.
55. Wu, H.; Shi, H.; Wang, Y.; Jia, X.; Tang, C.; Zhang, J.; Yang, S. Hyaluronic acid conjugated graphene oxide for targeted drug delivery. Carbon, 2014, 69, 379-389.
56. Hong, B.J.; Compton, O.C.; An, Z.; Eryazici, I.; Nguyen, S-B.T. Successful stabilization of graphene oxide in electrolyte solutions: enhancement of biofuncionalization and cellular uptake. ACS Nano, 2012, 6, 63-73.
57. Bai, H.; Xu, Y.; Zhao, L.; Li, C.; Shi, G. Non-covalent functionalization of graphene sheets by sulfonated polyaniline. Chem. Commun., 2009, 1667-1669.
58. Pérez-Arnaiz, C.; Busto, N.; Leal, J.M.; García, B. New insights into the mechanism of the DNA/doxorubicin interaction. J. Phys. Chem. B, 2014, 119, 1288-95.
59. Yang, Y.; Zhang, Y.M.; Chen, Y.; Zhao, D.; Chen, J.T.; Liu, Y. Construction of a graphene oxide based noncovalent multiple nanosupramolecular assembly as a scaffold for drug delivery. Chem. Eur. J., 2012, 18, 4208-4215.
60. Makharza, S.; Cirillo, G.; Bachmatiuk, A.; Vittorio, O.; Mendes, R.G.; Oswald, S.; Hampel, S.; Rummeli, M.H. Size-dependent nanographene oxide as a platform for efficient carboplatin release. J. Mater. Chem. B, 2013, 1, 6107-6114.
61. Kavitha, T.; Abd, S.I.H.; Park, S.Y. pH-sensitive nanocargo based on smart polymer functionalized graphene oxide for site-specific drug delivery. Phys. Chem. Chem. Phys., 2013, 15, 5176-5185.
62. Stein, W.D.; Bates, S.E. Fojo, T. Intractable cancers: the many faces of multidrug resistance and the many targets it presents for therapeutic attack. Curr. Drug Targets, 2004, 5, 333-346.
63. Gottesman, M.M.; Fojo, T.; Bates, S.E. Multidrug resistance in cancer: role of ATP-dependent transporters. Nat. Rev. Cancer, 2002, 2, 48-58.
64. Cao, X.; Feng, F.; Wang, Y.; Yang, X.; Duan, H.; Chen, Y. Folic acid-conjugated graphene oxide as a transporter of chemotherapeutic drug and siRNA for reversal of cancer drug resistance. J. Nanopart. Res., 2013, 15, 1-12.
65. Zhi, F.; Dong, H.; Jia, X.; Guo, W.; Lu, H.; Yang, Y.; Ju, H.; Zhang, X.; Hu, Y. Functionalized graphene oxide mediated adriamycin delivery and miR-21 gene silencing to overcome tumor multidrug resistance in vitro. Plos One, 2013, 8, 1-9.
66. Xing, Z.; Li, D.; Yang, L.; Xi, Y.; Su, X. MicroRNAs and anticancer drugs. Acta Biochim. Biophys. Sin., 2014, 46, 233-239.
67. Zheng, T.; Wang, J.; Chen, X.; Liu, L. Role of microRNA in anticancer drug resistance. Int. J. Cancer, 2010, 126, 2-10.
68. Zhi, X.; Fang, H.L.; Bao, C.; Shen, G.; Zhang, J.; Wang, K.; Guo, S.; Wan, T.; Cui, D. The immunotoxicity of graphene oxides and the effect of PVP-coating. Biomaterials, 2013, 34, 5254-5261.
69. Qin, S.Y.; Feng, J.; Rong, L.; Jia, H.Z.; Chen, S.; Liu, X.J.; Luo, G.F.; Zhuo, R.X.; Zhang, X.Z. Theranostic GO-based nanohybrid for tumor induced imaging and potential combinatorial tumor therapy. Small, 2014, 10, 599-608.
70. Jung, H.S.; Kong, W.H.; Sung, D.K.; Lee, M-Y.; Beack, S.E.; Keum, D.H.; Kim, K.S.; Yun, S.H.; Hahn, S.K. Nanographene oxide-hyaluronic acid conjugate for photothermal ablation therapy of skin cancer. ACS Nano, 2014, 8, 260-268.
71. Markovic, Z.M.; Harhaji-Trajovic, L.M.; Todorovic-Markovic, B.M.; Kepic, D.P.; Arsikin, K.M.; Jovanovic, S.P.; Pantovic, A.C.; Dramicanin, M.D.; Trajkovic, V.S. In vitro comparison of the photothermal anticancer activity of graphene nanoparticles and carbon nanotubes. Biomaterials, 2011, 32, 1121-1129.
72. Tian, B.; Wang, C.; Zhang, S.; Feng, L.; Liu, Z. Photothermally enhanced photodynamic therapy delivered by nano-graphene oxide. ACS Nano, 2011, 5, 7000-7009.
73. Son, S.J.; Bai, X.; Lee, S.B. Inorganic hollow nanoparticles and nanotubes in nanomedicine part 2: imaging, diagnostic, and therapeutic applications. Drug Discov. Today, 2007, 12, 657-663.
74. Miao, W.; Shim, G.; Lee, S.; Lee, S.; Choe, Y.S.; Oh, Y.K. Safety and tumor tissue accumulation of pegylated graphene oxide nanosheets for co-delivery of anticancer drug and photosensitizer. Biomaterials, 2013, 34, 3402-3410.
75. Zhang, W.; Guo, Z.; Huang, D.; Liu, Z.; Guo, X.; Zhong, H. Synergistic effect of chemo-photothermal therapy using PEGylated graphene oxide. Biomaterials, 2011, 32, 8555-8561.
76. Yang, S.T.; Liu, Y.; Wang, Y.W.; Cao, A. Biosafety and bioapplication of nanomaterials by designing protein-nanoparticle interactions. Small, 2013, 9, 1635-1653.
77. Yang, H.W.; Lu, Y.J.; Lin, K.J.; Hsu, S.C.; Huang, C.Y.; She, S.H.; Liu, H.L.; Lin, C.W.; Xiao, M.C.; Wey, S.P.; Chen, P.Y.; Yen, T.C.; Wei, K.C.; Ma, C.C. EGRF conjugated PEGylated nanographene oxide for targeted chemotherapy and photothermal therapy. Biomaterials, 2013, 34, 7204-7214.
78. Meirelles, L.S.; Chagastelles, P.C.; Nardi, N.B. Mesenchymal stem cells reside in virtually all post-natal organs and tissues. J. Cell Sci., 2006, 119, 2204-2213.
79. Pittenger, M.F.; Mackay, A.M.; Beck, S.C.; Jaiswal, R.K.; Douglas, R.; Mosca, J.D.; Moorman, M.A.; Simonetti, D.W.; Craig, S.; Marshak, D.R. Multilineage potential of adult human mesenchymal stem cells. Science, 1999, 284, 143-147.
80. Timper, K.; Seboek, D.; Eberhardt, M. Human adipose tissuederived mesenchymal stem cells differentiate into insulin, somatostatin, and glucagon expressing cells. Biochem. Biophys. Res. Commun., 2006, 341, 1135-1140.
81. Chamberlain, G.; Fox, J.; Ashton, B.; Middleton, J. Concise review: mesenchymal stem cells: their phenotype, differentiation capacity, immunological features, and potential for homing. Stem Cells., 2007, 25, 2739-49.
82. Chang, C.; Niu, D.; Zhou, H.; Li, F.; Gong, F. Mesenchymal stem cells contribute to insulin-producing cells upon microenvironmental manipulation in vitro. Transp. Proces., 2007, 39, 3363-3368.
83. Nasef, A.; Ashammakhi, N.; Fouillard, L. Immunomodulatory effect of mesenchymal stromal cells: possible mechanisms. Regen. Med., 2008, 3, 531-546.
84. Frenette, P.S.; Pinho, S.; Lucas, D.; Scheiermann, C. Mesenchymal Stem Cell: keystone of the hematopoietic stem cell niche and a stepping-stone for regenerative. Med. Annu. Rev. Immunol., 2012, 12, 285-316.
85. Menaa, F.; Abdelghani, A.; Menaa, B. Graphene nanomaterials as biocompatible and conductive scaffolds for stem cells: impact for tissue engineering and regenerative medicine. J. Tissue Eng. Regen. Med., 2014, DOI: 10.1002/term.1910.
86. Shi, J.G.; Fu, W.J.; Wang, X.X.; Wu, Y.D.; Li, G.; Hong, B.F.; Wang, Y.; Du, Z.Y.; Zhang, X. Tissue engineering of ureteral grafts by seeding urothelial differentiated hADSCs onto biodegradable ureteral scaffolds. J. Biomed. Mater. Res. Part A., 2012, 100A, 2612–2622.
87. Yuan, H.; Liu, L.; Zheng, S.; Liu, Z.; Yang, L.; Pu, C.; Li, J.; Long, D.; Wei, Q.; Han, P. Experimental study of differentiation of umbilical cord mesenchymal stem cells into smooth muscle cells induced by bladder smooth muscle cells conditioned medium. Zhongguo Xiu Fu Chong Jian Wai Ke Za Zhi. 2013, 27, 1506-11.
88. Kumar, S.; Poojan, S.; Verma, V.; Verma, M.K.; Lohani, M. Rapid isolation of integrin rich multipotent stem cell pool and reconstruction of mouse epidermis equivalent. Am. J. Stem Cells., 2014, 3, 27-36.
89. Lee, W.C.; Lim, C.H.Y.X.; Shi, H.; Tang, L.A.L.; Wang, Y.; Lim, C.T.; Loh, K.P. Origin of enhanced stem cell growth and differentiation on graphene and graphene oxide. ASC Nano., 2011, 5, 7334–7341.
90. Akhavan, O.; Ghaderi, E.; Akhavan, A. Size-dependent genotoxicity of graphene nanoplatelets in human stem cells. Biomaterials, 2012, 33, 8017-8025.
91. Shen, H.; Liu, M.; He, H.; Zhang, L.; Huang, J.; Chong, Y.; Dai, J.; Zhang, Z. PEGylated graphene oxide-Mediated protein delivery for cell function regulation. Appl. Mater. Interfaces., 2012, 4, 6317−6323.
92. Kim, J.; Kim, R.Y.; Kim, Y.; Lim, K.T.; Seonwoo, H.; Park, S.; Cho, S.P.; Hong, B.H.; Choung, P.H.; Chung, T.D.; Choung, Y.H.; Chung, J.H. Graphene-incorporated chitosan substrata for adhesion and differentiation of human mesenchymal stem cells. J. Mater. Chem. B., 2013a, 1, 933–938.
93. Lee, M.S.; Lee, K.; Kim, S.Y.; Lee, H.; Park, J.; Choi, K.H.; Kim, H.K.; Kim, D.G.; Lee, D.Y.; Nam, S.; Park, J.U. Highperformance, transparent, and stretchable electrodes using graphene-metal nanowire hybrid structures. Nano Lett., 2013, 13, 2814-2821.
94. Justin, R.; Chen, B. Characterization and drug release performance of biodegradable chitosan-graphene oxide nanocomposites. Carbohydr. Polym., 2014, 103, 70-80.
95. Tsuchiya, T.; Terabe, K.; Aono, M. Graphene: in situ and nonvolatile bandgap tuning of multilayer graphene oxide in an allsolid-state electric double-layer transistor. Adv. Mater., 2014, 26, 1143-1145.
96. Ku, S.H.; Park, C.B. Myoblast differentiation on graphene oxide. Biomaterials, 2013, 34, 2017-2023.
97. Kim, J.; Choi, K.S.; Kim, Y.; Lim, K.T.; Seonwoo, H.; Park, Y.; Kim, D.H.; Choung, P.H.; Cho, C.S.; Kim, S.Y.; Choung, Y.H.; Chung, J.H. Bioactive effects of grapheme oxide cell culture substratum on structure and function of human adipose-derived stem cells. J. Biomed. Mat. Res. A., 2013b, 101, 3520-3530.
98. Paul, W.; Sharma, C.P. Blood compatibility and biomedical applications of graphene. Trends Biomater. Artif. Organs, 2011, 25, 91-94.
99. Paula, A.J.; Araujo Júnior, R.T.; Martinez, D.S.T.; Gamero, E.J.P.; Nader, H.B., Durán, N.; Justo, G.Z.; Alves, O.L. Influence of protein corona on the transport of molecules into cells by mesoporous silica nanoparticles. ACS Appl. Mater. Interfaces, 2013, 5, 8387-8393.
100. Paula, A.J.; Martinez, D.S.; Júnior R.T.A.; Souza Filho, A.G.; Alves, O.L. Suppression of the hemolytic effect of mesoporous silica nanoparticles after protein corona interaction: independence of the surface microchemical environment. J. Braz. Chem. Soc., 2012; 23, 1807-1814.
101. Zuo, P.P.; Feng, H.F.; Xu, Z.Z.; Zhang, L.F.; Zhang, Y.L.; Xia, W.; Zhang, W.Q. Fabrication of biocompatible and mechanically reinforced graphene oxide-chitosan nanocomposite films. Chem. Cent., 2013, 7, 1-11.
102. Seabra, A.B.; Paula, A.J., de Lima, R.; Alves, O.L.; Durán, N. Nanotoxicity of graphene and graphene oxide. Chem. Res. Toxicol., 2014, 27, 159-168.
103. Durán, N.; Guterres, S.S.; Alves, O.L. (Eds). Nanotoxicology: Materials, methodologies, and assessments. Springer, pp 412 (2014). ISBN 978-1-4614-8992-4.
104. Luna, L.A.V.; Martinez, D.S.T.; Alves, O.L. Assessing the erythrocyte toxicity of nanomaterials: from current methods to biomolecular surface chemistry interactions. In: Nanotoxicoloy: Materials, Methodologies and Assessments. Durán, N.; Guterres, S.S.; Alves, O.L. (Editors). Nanomedicine and Nanotoxicology series, Springer, 2013, Chapter 16, 347-361.
105. ASTM. Standard test method for analysis of hemolytic properties of nanoparticles. E2524-08, 2008.
106. Singh, K.S.; Singh, M.K.; Kulkarni, P.P.; Sonkar, V.K.; Grácio, J.J.A.; Dash, D. Amine-modified graphene: Thrombo-protective safer alternative to graphene oxide for biomedical applications. ACS Nano, 2012, 6, 2731-2740.
107. Guo, M.; Li, M.; Liu, X.; Zhao, M.; Li, D.; Geng, D.; Sun, X.; Gu, H. N-containing functional groups induced superior cytocompatible and hemocompatible graphene by NH2 ion implantation. J. Mater Sci: Mater. Med., 2013, 24, 2741-2748.
108. Liao, K-H.; Lin, Y-S.; Macosko, C.W.; Haynes, C.L. Cytotoxicity of graphene oxide and graphene in human erythrocytes and skin fibroblasts. ACS Appl. Mater. Interfaces, 2011, 3, 2607-2615.
109. Love, S.A.; Thompson, J.W.; Haynes, C.L. Development of screening assays for nanoparticle toxicity assessment n human blood: preliminary studies with charged Au nanoparticles. Nanomedicine, 2012, 7, 1355-1364.
110. Kim, H-M.; Kim, K-M.; Lee, K.; Kim, Y.S.; Oh, J-M. Nano-Bio interactions between graphite oxide nanoparticles and human blood components. Eur. J. Inorg. Chem., 2012, 5343-5349.
111. Laloy, J.; Mullier, F.; Alpan, L.; Mejia, J.; Lucas, S.; Chatelain, B.; Toussaint, O.; Masereel, B.; Rolin, S.; Dogné, J.M. A comparison of six major platelet functional tests to assess the impact of carbon nanomaterials on platelet function: A practical guide. Nanotoxicology, 2014, 8, 220-232.
112. Li, H-C.; Hsieh, F-J.; Chen, C-P.; Chang, M-Y.; Hsieh, P.C.H.; Chen, C-C.; Hung, S-U.; Wu, C-C.; Chang, H-C. The hemocompatibility of oxidized diamond nanocrystals for biomedical applications. Scientific Reports, 2013, 3, 1-8.
113. Qu, G.B.; Liu, S.J.; Zhang, S.; Wang, L.; Wang, W.; Sun, B.; Yin, N.; Gao, X.; Xia, T.; Chen, J-J.; Jiang, G-B. Graphene oxide induces toll-like receptor 4 (TLR-4)-dependent necrosis in macrophages. ACS Nano, 2013, 7, 5732-5745.
114. Podila, R.; Moore, T.; Alexis, F.; Rao, A.M. Graphene coatings for enhanced hemo-compatibility of nitinol stents. RSC Adv., 2013, 3, 1660-1665.
115. Sasidharan, A.; Panchakarla, L.S.; Sadanandan, A.R.; Ashokan, A.; Chandran, P.; Girish, C.M.; Menon, D.; Nair, S.V.; Rao, C.N.; Koyakutty, M. Hemocompatibility and macrophage response of pristine and functionalized graphene. Small, 2012, 8, 1251-1263.
116. Zhou, N-L.; Gu, H.; Tang, F-F.; Li, W-X.; Chen, Y-Y.; Yuan, J. Biocompatibility of novel carboxylated graphene oxide-glutamic acid complexes. J. Mater. Sci., 2013, 48, 7097-7103.
117. Cheng, C.; Li, S.; Nie, S.; Zhao, W.; Yang, H.; Sun, S.; Zhao, C. General and biomimetic approach to biopolymer-functionalized graphene oxide nanosheets through adhesive dopamine. Biomacromolecules, 2012, 13, 4236-4246.
118. Monopoli, M.P.; Aberg, C.; Salvati, A.; Dawson, K.A. Biomolecular coronas provide the biological identity of nanosized materials. Nat. Nanotechnol., 2012, 7, 779-786.
119. Paula, A.J.; Silveira, C. P.; Martinez, D.S.T.; Souza Filho, A.G.; Romero, F.V.; Fonseca, L.C.; Tasic, L.; Alves, O.L.; Durán, N. Topography-driven bionano-interactions on coloidal sílica nanoparticles. ACS Appl. Mater. Interfaces, 2014, 6, 3437-3447.
120. Lundqvist, M.; Stigler, J.; Elia, G.; Lynch, I.; Cedervall, T. Nanoparticle size and surface properties determine the protein corona with possible implications for biological impacts. Proc. Natl. Acad. Sci. USA, 2008, 105, 14264-14270.
121. Casey, A.; Davoren, M.; Herzog, E.; Lyng, F.M.; Byrne, H.J.; Chambers, G. Probing the interaction of single walled carbon nanotube within cell culture medium as a precursor to toxicity testing. Carbon, 2007, 45, 34-40.
122. Lynch, I.; Salvati, A.; Dawson, K.A. Protein-nanoparticle interactions: what does the cell see? Nat. Nanotechnol. 2009, 4, 546-547.
123. Hu, W.; Peng, C.; Lv, M.; Li, X.; Zhang, Y.; Chen, N.; Fan, C.; Huang, Q. Protein-corona mediated mitigation of cytotoxicity of graphene oxide. ACS Nano, 2011, 5, 3693-3700.
124. Pearson, R.M.; Hsu, H-J.; Bugno, J.; Hong, S. Understanding nanobio interactions to improve nanocarriers for drug delivery. MRS Bulletin, 2014, 39, 227-237.
125. Barran-Berdon, A.L.; Pozzi, D.; Caracciolo, G.; Capriotti, A.L.; Caruso, G.; Cavaliere, C.; Riccioli, A.; Palchetti, S.; Laganà, A. Time evolution of nanoparticle-protein corona in human plasma: Relevance for targeted drug delivery. Langmuir, 2013, 29, 6485-6494.
126. Salvati, A.; Pitek, A.; Monopoli, M.P.; Prapainop, K.; Bombelli, F.B.; Hristov, D.R.; Kelly, P.M.; Aberg, C.; Mahon, E.; Dawson, K.A. Transferrin-functionalized nanoparticles lose their targeting capabilities when a biomolecule corona adsorbs on the surface. Nat. Nanotechnol., 2013, 8, 137-143.
127. Amiri, H.; Bordonali, L.; Lascialfari, A.; Wan S, Monopoli, M.P.; Lynch, I.; Laurent, S.; Mahmoudi, M. Protein corona affects the relaxivity and MRI contrast efficiency of magnetic nanoparticles. Nanoscale, 2013, 5, 8656-8665.
128. Mu, Q.; Su, G.; Li, L.; Gilbertson, B.O.; Yu, L.H.; Zhang, Q.; Sun, Y-P., Yan, B. Size-dependent cell uptake of protein-coated graphene oxide nanosheets. ACS Appl. Mater. Interfaces, 2012, 4, 2259-2266.
129. Chang, Y.L.; Yang, S.T.; Liu, J-H.; Dong, E.; Wang, Y.; Cao, A.; Liu, Y.; Wang, H. In vitro toxicity evaluation of graphene oxide on A549 cells. Toxicol. Lett., 2011, 200, 201-210.
130. Liu, J.; Guo, S.; Han, L.; Wang, T.; Hong, W.; Liu, Y.; Wang, E. Synthesis of phospholipid monolayer membrane functionalized graphene for drug delivery. J. Mater. Chem., 2012, 22, 20634–20640.
131. Mao, H.; Chen, W.; Laurent, S.; Thirifays, C.; Burtea, C.; Rezaee, F.; Mahmoudi, M. Hard corona composition and cellular toxicities of the graphene sheets. Colloids Surf., B, 2013, 109, 212-218.
132. Mahmoudi, M.; Saeedi-Eslami, S.N.; Shokrgozar, M.; Azadmanesh, K.; Hassanlou, M.; Kalhor, H.R.; Burtea, C.; Rothen-Rutishauser, B.; Laurent, S.; Sheibani, S.; Vali, H. Cell “vision”: complementary factor of protein corona in nanotoxicology. Nanoscale, 2012, 4, 5461-5468.
133. Hajipour, M.J.; Laurent, S.; Aghaie, A.; Rezaee, F.; Mahmoudi, M. Personalized protein coronas: a “key” factor at the nanobiointerface. Biomat. Sci., 2014, 2, 1210-1221.
134. Goebell, P.J.; Knowles, M.A. Bladder cancer or bladder cancers? Genetic, ally distinct malignant conditions of the urothelium. Urol. Oncol., 2010, 28, 409-428.
135. Miyamoto, H.; Brimo, F; Schultz, L.; Ye, H.; Miller, J.S.; Fajardo, D.A.; Lee, T.K.; Epstein, J.I.; Netto, G.J. Low-grade papillary urothelial carcinoma of the urinary bladder: a clinicopathologic analysis of a post-World Health Organization/International Society of Urological Pathology classification cohort from a single academic center. Arch. Pathol. Lab. Med, 2010, 134, 1160-1163.
136. Siegel, R.; Naishadham, D.; Jemal, A. Cancer statistics 2013. Cancer. J. Clin, 2013, 63, 11-30.
137. Shimada, K.; Fuji, T.; Anai, S.; Fujimoto, K.; Konishi, N. ROS generation via NOX4 and its utility in the cytological diagnosis of urothelial carcinoma of the urinary bladder. BMC Urol., 2011, 11, 22.
138. Epstein, J.L.; Amin, M.B.; Reuter, V.R. The World Health Organization / International Society of Urological Pathology consensus classification of urothelial (tranticional cell) neoplasms of the urinary bladder. Bladder Consensus Conference Committee. Am. J. Surg. Pathol., 1998, 22, 1435-1448.
139. Askeland, E.J.; Newton, M.R.; O’Donnel, M.A.; Luo, Y. Bladder cancer immunotherapy: BCG and beyond. Adv. Urol., 2012, 212, 181987.
140. Zeegers, M.P.; Tan, F.E.; Dorant, E.; van Den Brandt, P.A. The impact of characteristics of cigarette smoking on urinary tract cancer risk: a meta analysis of epidemiologic studies. Cancer, 2000, 89, 630–639.
141. Grimmer, G.; Dettbarn, G.; Seidel, A.; Jacob, J. Detection of carcinogenic aromatic amines in the urine of non-smokers. Sci. Total Environ., 2000, 247, 81–90.
142. Kemp, T.J.; Ludwig, A.T.; Earel, J.K.; Moore, J.M.; Vanoosten, R.L.; Moses, B.; Leidal, K.; Nauseef, W.M.; Griffith, T.S. Neutrophil stimulation with Mycobacterium bovis bacillus Calmette-Guerin (BCG) results in the release of functional soluble TRAIL/Apo-2L. Blood., 2005, 106, 3474-3482, 2005.
143. Hall, M.C.; Chang, S.S.; Dalbagni, G.; Pruthi, R.S.; Schellhammer, P.F.; Seigne, J.D.; Skinner, E.C.; Wolf Jr, J.S. Guideline for the management of nonmuscle invasive bladder cancer (stages Ta, T1, and Tis): 2007 update. J Urol., 2007, 178, 2314-2330.
144. Morales, A.; Eidinger, D.; Bruce, A.W. Bacillus Calmette-Guerin in the treatment of adenocarcinoma of the kidney. J. Urol., 1976, 115, 377-380.
145. Bhöle, A.; Brandau, S. Immune mechanisms in Bacillus Calmette Guerin imunotherapy for superficial bladder cancer. J. Urol., 2003, 170, 964–969.
146. O’Donnell, M.A. Practical applications of intravesical chemotherapy and immunotherapy in high-risk patients with superficial bladder cancer. Urol. Clin. North Am., 2005, 32, 121-131.
147. DiPaola, R.S.; Lattime, E.C. Bacillus Calmette-Guerin mechanism of action: the role of immunity, apoptosis, necrosis and autophagy. J. Urol., 2007, 178, 1840-1841.
148. Simons, M.P.; O'Donnell, M.A.; Griffith, T.S. Role of neutrophils in BCG immunotherapy for bladder cancer. Urol. Oncol., 2008, 26, 341-345.
149. Ludwig, A.T.; Moore, J.M.; Luo, Y.; Chen, X.; Saltsgaver, N.A.; O'Donnell, M.A.; Griffith, T.S. Tumor necrosis factor-related apoptosis-inducing ligand: A novel mechanism for Bacillus Calmette-Guerin-induced antitumor activity. Cancer Res., 2004, 64, 338–3390.
150. Reis, L.O.; Ferreira, U.; Billis, A.; Cagnon, V.H.; Fávaro, W.J. Anti-angiogenic effects of the superantigen staphylococcal enterotoxin B and bacillus Calmette-Guérin immunotherapy for nonmuscle invasive bladder cancer. J. Urol., 2012, 2, 438-445.
151. Seow, S.W.; Rahmat, J.N.; Mohamed, A.A.; Mahendran, R.; Lee, Y.K.; Bay, B.H. Lactobacillus species is more cytotoxic to human bladder cancer cells than Mycobacterium Bovis (bacillus Calmette-Guerin). J. Urol., 2002, 168, 2236-2239.
152. Heldwein, K.A.; Liang, M.D.; Andresen, T.K.; Thomas, K.E.; Marty, A.M.; Cuesta, N.; Vogel, S.N.; Fenton, M.J. TLR2 and TLR4 serve distinct roles in the host immune response against Mycobacterium bovis BCG. J. Leukoc. Biol., 2003, 74, 277–286.
153. Hennessy, E.J.; Parker, A.E.; O'Neill, L.A. Targeting Toll-like receptors: emerging therapeutics? Nat. Rev. Drug Discov., 2010, 9, 293–307.
154. So, E.Y.; Ouchi, T. The application of Toll like receptors for cancer therapy. Int. J. Biol. Sci., 2010, 6, 675–681.
155. Goutagny, N.; Estornes, Y.; Hasan, U.; Lebecque, S.; Caux, C. Targeting pattern recognition receptors in cancer immunotherapy. Target. Oncol., 2012, 7, 29–54.
156. LaRue, H.; Ayari, C.; Bergeron, A.; Fradet, Y. Toll-like receptors in urothelial cells--targets for cancer immunotherapy. Nat Rev Urol., 2013, 10, 537-545.
157. Fávaro, W.J.; Nunes, O.S.; Seiva, F.R.; Nunes, I.S.; Woolhiser, L.K.; Durán, N.; Lenaerts, A.J. Effects of P-MAPA Immunomodulator on Toll-Like Receptors and p53: Potential Therapeutic Strategies for Infectious Diseases and Cancer. Infect. Agent Cancer., 2012, 7, 14.
158. McKiernan, J.M.; Barlow, L.J.; Laudano, M.A.; Mann, M.J.; Petrylak, D.P.; Benson, M.C. A phase I trial of intravesical nanoparticle albumin-bound paclitaxel in the treatment of bacillus Calmette-Guérin refractory nonmuscle invasive bladder cancer. J. Urol., 2011, 186, 448-451.
159. Perabo, F.G.; Willert, P.L.; Wirger, A. Superantigen-activated mononuclear cells induce apoptosis in transitional cell carcinoma. Anticancer Res., 2005, 25, 3565-3573.
160. van der Meijden, A.P.; Sylvester, R.J.; Oosterlinck, W.; Hoeltl, W.; Bono, A.V. Maintenance Bacillus Calmette-Guerin for Ta T1 bladder tumors is not associated with increased toxicity: results from a European Organisation for Research and Treatment of Cancer Genito-Urinary Group Phase III Trial. Eur. Urol., 2003, 44, 429-434.
161. Tyagi, P.; Wu, P.C.; Chancellor, M.; Yoshimura, N.; Huang, L. Recent Advances in Intravesical Drug/Gene Delivery. Mol. Pharm., 2006, 3, 369−379.
162. Carvalho, F.C.; Bruschi, M.L.; Evangelista, R.C.; Gremião, M.P.D. Mucoadhesive drug delivery systems. Braz. J. Pharm. Sci., 2010, 46, 1−17.
163. Zhou, H.; Zhang, B.; Zheng, J.; Yu, M.; Zhou, T.; Zhao, K.; Jia, Y.; Gao, X.; Chen, C.; Wei, T. The inhibition of migration and invasion of cancer cells by graphene via the impairment of mitochondrial respiration. Biomaterials., 2013, 30, 1-11.
164. Hong, H.; Yang, K.; Zhang, Y.; Engle, J.W.; Feng, L.; Yang, Y.; Nayak, T.R.; Goel, S.; Bean, J.; Theuer, C.P.; Barnhart, T.E.; Liu, Z.; Cai, W. In vivo targeting and imaging of tumor vasculature with radiolabeled, antibody-conjugated nanographene. ACS Nano., 2012, 6, 2361-2370.
165. Castilho, J.J.; Syvendsen, W.E.; Rozlosnik, N.; Escobar, P.; Martínez, F.; Castillo-León, J. Detection of cancer cells using a peptide nanotube-folic acid modified graphene electrode. Analyst, 2013, 138, 1026-1031.
166. Chen, M.L.; He, Y.J.; Chen, X.W.; Wang, J-H. Quantum-dotconjugated graphene as a probe for simultaneous cancer-targeted fluorescent imaging, tracking, and monitoring drug delivery. Bioconjug. Chem., 2013, 24, 387-397.
167. Liu Z.; Guo, Z.; Zhong, H.; Qin, X.; Wan, M.; Yang, B. Graphene oxide based surface enhanced Raman scattering probes for cancer cell imaging. Phys. Chem., 2013, 15, 2961-2966.