Graphene Family of Nanomaterials: Reviewing Advanced Applications in Drug delivery and Medicine

Author(s): Kumud Joshi*, Bhaskar Mazumder, Pronobesh Chattopadhyay, Nilutpal Sharma Bora, Danswrang Goyary, Sanjeev Karmakar.

Journal Name: Current Drug Delivery

Volume 16 , Issue 3 , 2019

Become EABM
Become Reviewer

Graphical Abstract:


Abstract:

Graphene in nano form has proven to be one of the most remarkable materials. It has a single atom thick molecular structure and it possesses exceptional physical strength, electrical and electronic properties. Applications of the Graphene Family of Nanomaterials (GFNs) in different fields of therapy have emerged, including for targeted drug delivery in cancer, gene delivery, antimicrobial therapy, tissue engineering and more recently in more diseases including HIV. This review seeks to analyze current advances of potential applications of graphene and its family of nano-materials for drug delivery and other major biomedical purposes. Moreover, safety and toxicity are the major roadblocks preventing the use of GFNs in therapeutics. This review intends to analyze the safety and biocompatibility of GFNs along with the discussion on the latest techniques developed for toxicity reduction and biocompatibility enhancement of GFNs. This review seeks to evaluate how GFNs in future will serve as biocompatible and useful biomaterials in therapeutics.

Keywords: Graphene, graphene nanoplatelets, graphene nanoribbons, drug delivery, antimicrobial therapy, tissue engineering, graphene biocompatibility.

[1]
Pierson, H.O. Handbook of Carbon, Graphite, Diamonds and Fullerenes: Processing, Properties and Applications (Materials Science and Process Technology); William Andrew, 2012.
[2]
Novoselov, K.S.; Geim, A.K.; Morozov, S.V.; Jiang, D.; Katsnelson, M.I.; Grigorieva, I.V.; Dubonos, S.V.; Firsov, A.A. Two-dimensional gas of massless dirac fermions in graphene. Nature, 2005, 438, 197-200.
[3]
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.
[4]
Balandin, A.A. Thermal properties of graphene and nanostructured carbon materials. Nat. Mater., 2011, 10, 569.
[5]
Novoselov, K.S.; Fal’ko, V.I.; Colombo, L.; Gellert, P.R.; Schwab, M.G.; Kim, K. A roadmap for graphene. Nature, 2012, 490, 192-200.
[6]
Malik, S.; Ruddock, F.M.; Dowling, A.H.; Byrne, K.; Schmitt, W.; Khalakhan, I.; Nemoto, Y.; Guo, H.; Shrestha, L.K.; Ariga, K.; Hill, J.P. Graphene composites with dental and biomedical applicability. Beilstein J. Nanotechnol., 2018, 9, 801.
[7]
Huang, C.T.; Shrestha, L.K.; Ariga, K.; Hsu, S.H. A graphene-polyurethane composite hydrogel as a potential bioink for 3D bioprinting and differentiation of neural stem cells. J. Mater. Chem. B, 2017, 5, 8854-8864.
[8]
Nakamura, M.; Tahara, Y.; Fukata, S.; Zhang, M.; Yang, M.; Iijima, S.; Yudasaka, M. Significance of optimization of phospholipid poly (ethylene glycol) quantity for coating carbon nanohorns to achieve low cytotoxicity. Bull. Chem. Soc. Jpn., 2017, 90, 662-666.
[9]
Liu, J.; Cui, L.; Losic, D. Graphene and graphene oxide as new nanocarriers for drug delivery applications. Acta Biomater., 2013, 9, 9243-9257.
[10]
Kim, H.; Kim, W.J. Photothermally controlled gene delivery by reduced graphene oxide-polyethylenimine nanocomposite. Small, 2014, 10, 117-126.
[11]
Feng, L.; Zhang, S.; Liu, Z. Graphene based gene transfection. Nanoscale, 2011, 3, 1252-1257.
[12]
Zhang, L.; Lu, Z.; Zhao, Q.; 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.
[13]
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. ACS Appl. Mater. Interfaces, 2012, 4, 6317-6323.
[14]
Zhang, B.; Wang, Y.; Liu, J.; Zhai, G. Recent developments of phototherapy based on graphene family nanomaterials. Curr. Med. Chem., 2017, 24, 268-291.
[15]
Krishna, K.V.; Ménard-Moyon, C.; Verma, S.; Bianco, A. Graphene-based nanomaterials for nanobiotechnology and biomedical applications. Nanomedicine, 2013, 8, 1669-1688.
[16]
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.
[17]
Yue, H.; Zhou, X.; Cheng, M.; Xing, D. Graphene oxide-mediated cas9/sgRNA delivery for efficient genome editing. Nanoscale, 2018, 10(3), 1063-1071.
[18]
Ghafary, S.M.; Nikkhah, M.; Hatamie, S.; Hosseinkhani, S. Simultaneous gene delivery and tracking through preparation of photo-luminescent nanoparticles based on graphene quantum dots and chimeric peptides. Sci. Rep., 2017, 7, 9552.
[19]
Ni, G.; Wang, Y.; Wu, X.; Wang, X.; Chen, S.; Liu, X. Graphene oxide absorbed anti-IL10R antibodies enhance LPS induced immune responses in vitro and in vivo. Immunol. Lett., 2012, 148, 126-132.
[20]
Palmieri, V.; Bugli, F.; Lauriola, M.C.; Cacaci, M.; Torelli, R.; Ciasca, G.; Conti, C.; Sanguinetti, M.; Papi, M.; De Spirito, M. Bacteria meet graphene: Modulation of graphene oxide nanosheet interaction with human pathogens for effective antimicrobial therapy. ACS Biomater. Sci. Eng., 2017, 3, 619-627.
[21]
Kim, E.S.; Ahn, E.H.; Dvir, T.; Kim, D.H. Emerging nanotechnology approaches in tissue engineering and regenerative medicine. Int. J. Nanomedicine, 2014, 9, 1-5.
[22]
Hummers, W.S.; Offeman, R.E. Preparation of graphitic oxide. J. Am. Chem. Soc., 1958, 80, 1339-1339.
[23]
Ambrosi, A.; Chua, C.K.; Bonanni, A.; Pumera, M. Electrochemistry of graphene and related materials. Chem. Rev., 2014, 114, 7150-7188.
[24]
Mattevi, C.; Kim, H.; Chhowalla, M. A review of chemical vapour deposition of graphene on copper. J. Mater. Chem., 2011, 21, 3324-3334.
[25]
Pollard, B. Growing graphene via chemical vapor deposition. Ph. D. Thesis, 2011, 1-47.
[26]
Abdolhosseinzadeh, S.; Asgharzadeh, H.; Seop, K.H. Fast and fully-scalable synthesis of reduced graphene oxide. Sci. Rep., 2015, 5, 10160.
[27]
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.
[28]
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.
[29]
Xu, Z.; Wang, S.; Li, Y.; Wang, M.; Shi, P.; Huang, X. Covalent functionalization of graphene oxide with biocompatible Poly(ethylene Glycol) for delivery of paclitaxel. ACS Appl. Mater. Interfaces, 2014, 6, 17268-17276.
[30]
Bianco, A. Graphene: Safe or toxic? The Two Faces of the Medal. Angew. Chem. Int. Ed., 2013, 52, 4986-4997.
[31]
Chen, F.; Gao, W.; Qiu, X.; Zhang, H.; Liu, L.; Liao, P.; Fu, W.; Luo, Y. Graphene quantum dots in biomedical applications: Recent advances and future challenges. Front. Lab. Med, 2017, 1(4), 192-199.
[32]
Chowdhury, S.M.; Zafar, S.; Tellez, V.; Sitharaman, B. Graphene nanoribbon-based platform for highly efficacious nuclear gene delivery. ACS Biomater. Sci. Eng., 2016, 2, 798-808.
[33]
Chang, D.W.; Baek, J-B. Eco-friendly synthesis of graphene nanoplatelets. J. Mater. Chem. A Mater. Energy Sustain., 2016, 4, 15281-15293.
[34]
Shen, J.; Hu, Y.; Li, C.; Qin, C.; Ye, M. Synthesis of amphiphilic graphene nanoplatelets. Small, 2009, 5, 82-85.
[35]
Lin, H.A.; Sato, Y.; Segawa, Y.; Nishihara, T.; Sugimoto, N.; Scott, L.T.; Higashiyama, T.; Itami, K. A water-soluble warped nanographene: Synthesis and applications for photoinduced cell death. angew. Chemie - Int. Ed., 2018, 57, 2874-2878.
[36]
Thapa1, R.K.; Byeon, J.H.; Choi, H.-G.; Yong, C.S.; Kim, J.O. No PEGylated lipid bilayer-wrapped nano-graphene oxides for synergistic co-delivery of doxorubicin and rapamycin to prevent drug resistance in cancers. Nanotechnology, 2017, 28(29), 295101.
[37]
Debbage, P. Targeted drugs and nanomedicine: Present and future. Curr. Pharm. Des., 2009, 15, 153-172.
[38]
Yang, X.; Zhang, X.; Liu, Z.; Ma, Y.; Huang, Y.; Chen, Y. High-efficiency loading and controlled release of doxorubicin hydrochloride on graphene oxide. J. Phys. Chem. C, 2008, 112, 17554-17558.
[39]
Iannazzo, D.; Pistone, A.; Salamò, M.; Galvagno, S.; Romeo, R.; Giofré, S.V.; Branca, C.; Visalli, G.; Di Pietro, A. Graphene quantum dots for cancer targeted drug delivery. Int. J. Pharm., 2017, 518, 185-192.
[40]
Zhao, X.; Yang, L.; Li, X.; Jia, X.; Liu, L.; Zeng, J.; Guo, J.; Liu, P. Functionalized graphene oxide nanoparticles for cancer cell-specific delivery of antitumor drug. Bioconjug. Chem., 2015, 26, 128-136.
[41]
Liu, L.; Wei, Y.; Zhai, S.; Chen, Q.; Xing, D. Dihydroartemisinin and transferrin dual-dressed nano-graphene oxide for a pH-triggered chemotherapy. Biomaterials, 2015, 62, 35-46.
[42]
Rao, Z.; Ge, H.; Liu, L.; Zhu, C.; Min, L.; Liu, M.; Fan, L.; Li, D. Carboxymethyl cellulose modified graphene oxide as ph-sensitive drug delivery system. Int. J. Biol. Macromol., 2017, 107, 1184-1192.
[43]
Hussien, N.A.; Işıklan, N.; Türk, M. Pectin-conjugated magnetic graphene oxide nanohybrid as a novel drug carrier for paclitaxel delivery. Artif. Cells Nanomed. Biotechnol., 2018, 1-10.
[http://dx.doi.org/10.1080/21691401.2017]
[44]
Xu, X.; Wang, J.; Wang, Y.; Zhao, L.; Li, Y.; Liu, C. Formation of graphene oxide-hybridized nanogels for combinative anticancer therapy. Nanomedicine, 2018, 14(7), 2387-2395.
[45]
Lu, Y.J.; Yang, H.W.; Hung, S.C.; Huang, C.Y.; Li, S.M.; Ma, C.C.M.; 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. Nanomedicine, 2012, 7, 1737-1747.
[46]
Hashemi, M.; Omidi, M.; Muralidharan, B.; Smyth, H.; Mohagheghi, M.A.; Mohammadi, J.; Milner, T.E. Evaluation of the photothermal properties of a reduced graphene oxide/arginine nanostructure for near-infrared absorption. ACS Appl. Mater. Interfaces, 2017, 9, 32607-32620.
[47]
Yin, F.; Hu, K.; Chen, Y.; Yu, M.; Wang, D.; Wang, Q.; Yong, K.T.; Lu, F.; Liang, Y.; Li, Z. SiRNA delivery with PEGylated graphene oxide nanosheets for combined photothermal and genetherapy for pancreatic cancer. Theranostics, 2017, 7, 1133-1148.
[48]
Jiang, W.; Mo, F.; Lin, Y.; Wang, X.; Xu, L.; Fu, F. Tumor targeting dual stimuli responsive controllable release nanoplatform based on DNA-conjugated reduced graphene oxide for chemo-photothermal synergetic cancer therapy. J. Mater. Chem. B, 2018, 6, 4360-4367.
[49]
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.
[50]
Deb, A.; Andrews, N.G.; Raghavan, V. Natural polymer functionalized graphene oxide for co-delivery of anticancer drugs: In-vitro and in-vivo. Int. J. Biol. Macromol., 2018, 113, 515-525.
[51]
Gurunathan, S.; Kim, J.H. Graphene oxide-silver nanoparticles nanocomposite stimulates differentiation in human neuroblastoma cancer cells (SH-SY5Y). Int. J. Mol. Sci., 2017, 18, 2549.
[52]
Zhang, X.F.; Huang, F.H.; Zhang, G.L.; Bai, D.P.; de Felici, M.; Huang, Y.F.; Gurunathan, S. Novel biomolecule lycopene-reduced graphene oxide-silver nanoparticle enhances apoptotic potential of trichostatin a in human ovarian cancer cells (SKOV3). Int. J. Nanomedicine, 2017, 12, 7551-7575.
[53]
Yuan, Y.G.; Wang, Y.H.; Xing, H.H.; Gurunathan, S. Quercetin-mediated synthesis of graphene oxide-silver nanoparticle nanocomposites: A suitable alternative nanotherapy for neuroblastoma. Int. J. Nanomedicine, 2017, 12, 5819-5839.
[54]
Tian, J.; Luo, Y.; Huang, L.; Feng, Y.; Ju, H.; Yu, B.Y. Pegylated folate and peptide-decorated graphene oxide nanovehicle for in vivo targeted delivery of anticancer drugs and therapeutic self-monitoring. Biosens. Bioelectron., 2016, 80, 519-524.
[55]
Tang, Y.; Hu, H.; Zhang, M.G.; Song, J.; Nie, L.; Wang, S.; Niu, G.; Huang, P.; Lu, G.; Chen, X. An aptamer-targeting photoresponsive drug delivery system using “off-on” graphene oxide wrapped mesoporous silica nanoparticles. Nanoscale, 2015, 7, 6304-6310.
[56]
Ou, J.; Wang, F.; Huang, Y.; Li, D.; Jiang, Y.; Qin, Q.H.; Stachurski, Z.H.; Tricoli, A.; Zhang, T. fabrication and cyto-compatibility of Fe3O4/SiO2/graphene-CdTe QDs/CS nanocomposites for drug delivery. Colloids Surf. B Biointerfaces, 2014, 117, 466-472.
[57]
Wang, X.; Sun, X.; Lao, J.; He, H.; Cheng, T.; Wang, M.; Wang, S.; Huang, F. Multifunctional graphene quantum dots for simultaneous targeted cellular imaging and drug delivery. Colloids Surf. B Biointerfaces, 2014, 122, 638-644.
[58]
Dong, J.; Wang, K.; Sun, L.; Sun, B.; Yang, M.; Chen, H.; Wang, Y.; Sun, J.; Dong, L. Application of graphene quantum dots for simultaneous fluorescence imaging and tumor-targeted drug delivery. Sens. Actuators B Chem., 2018, 256, 616-623.
[59]
Justin, R.; Tao, K.; Román, S.; Chen, D.; Xu, Y.; Geng, X.; Ross, I.M.; Grant, R.T.; Pearson, A.; Zhou, G.; Neil, S.M.; Sun, K.; Chen, B. Photoluminescent and superparamagnetic reduced graphene oxide-iron oxide quantum dots for dual-modality imaging, drug delivery and photothermal therapy. Carbon N.Y., 2016, 97, 54-70.
[60]
Nafiujjaman, M.; Lee, Y.K.; Joon, H.; Kwak, K.S. Synthesis of nitrogen-and chlorine-doped graphene quantum dots for cancer cell imaging. J. Nanosci. Nanotechnol., 2018, 18, 3793-3799.
[61]
Sun, J.; Xin, Q.; Yang, Y.; Shah, H.; Cao, H.; Qi, Y.; Gong, J.R.; Li, J. Nitrogen-doped graphene quantum dots coupled with photosensitizers for one-/two-photon activated photodynamic therapy based on a FRET mechanism. Chem. Commun., 2018, 54, 715-718.
[62]
Zhang, D.; Wen, L.; Huang, R.; Wang, H.; Hu, X.; Xing, D. Mitochondrial specific photodynamic therapy by rare-earth nanoparticles mediated near-infrared graphene quantum dots. Biomaterials, 2018, 153, 14-26.
[63]
Choi, S.Y.; Baek, S.H.; Chang, S.J.; Song, Y.; Rafique, R.; Lee, K.T.; Park, T.J. Synthesis of upconversion nanoparticles conjugated with graphene oxide quantum dots and their use against cancer cell imaging and photodynamic therapy. Biosens. Bioelectron., 2017, 93, 267-273.
[64]
Wu, C.; Wang, L.; Tian, Y.; Guan, X.; Liu, Q.; Li, S.; Qin, X.; Yang, H.; Liu, Y. “triple-Punch” anticancer strategy mediated by near-infrared photosensitizer/CpG oligonucleotides dual-dressed and mitochondria-targeted nanographene. ACS Appl. Mater. Interfaces, 2018, 10, 6942-6955.
[65]
Akhavan, O.; Ghaderi, E.; Emamy, H. Nontoxic concentrations of PEGylated graphene nanoribbons for selective cancer cell imaging and photothermal therapy. J. Mater. Chem., 2012, 22, 20626-20633.
[66]
Chowdhury, S.M.; Surhland, C.; Sanchez, Z.; Chaudhary, P.; Suresh Kumar, M.A.; Lee, S.; Peña, L.A.; Waring, M.; Sitharaman, B.; Naidu, M. Graphene nanoribbons as a drug delivery agent for lucanthone mediated therapy of glioblastoma multiforme. Nanomedicine, 2015, 11, 109-118.
[67]
Kim, J.; Jay, M. Neutron-activatable radionuclide cancer therapy using graphene oxide nanoplatelets. Nucl. Med. Biol., 2017, 52, 42-48.
[68]
Lammel, T.; Boisseaux, P.; Fernández-Cruz, M.L.; Navas, J.M. Internalization and cytotoxicity of graphene oxide and carboxyl graphene nanoplatelets in the human hepatocellular carcinoma cell line hep G2. Part. Fibre Toxicol., 2013, 10, 27.
[69]
Yang, L.; Wang, F.; Han, H.; Yang, L.; Zhang, G.; Fan, Z. Functionalized graphene oxide as a drug carrier for loading pirfenidone in treatment of subarachnoid hemorrhage. Colloids Surf. B Biointerfaces, 2015, 129, 21-29.
[70]
Volarevic, V.; Paunovic, V.; Markovic, Z.; Simovic Markovic, B.; Misirkic-Marjanovic, M.; Todorovic-Markovic, B.; Bojic, S.; Vucicevic, L.; Jovanovic, S.; Arsenijevic, N.; Holclajtner-Antunovic, I.; Milosavljevic, M.; Dramicanin, M.; Kravic-Stevovic, T.; Ciric, D.; Lukic, M.L.; Trajkovic, V. Large graphene quantum dots alleviate immune- mediated liver damage. ACS Nano, 2014, 8(12), 12098-12109.
[71]
Jafarzadeh, F.; McManus, D.; Barbolina, I.; Malik, N.; Casiraghi, C.; Holt, C. Application of graphene based coating on coronary artery stents. Heart, 2017, 103, A108.
[72]
Iannazzo, D.; Pistone, A.; Ferro, S.; De Luca, L.; Monforte, A.M.; Romeo, R.; Buemi, M.R.; Pannecouque, C. Graphene quantum dots based systems as HIV inhibitors. Bioconjug. Chem., 2018, 29, 3084-3093.
[73]
Deb, A.; Vimala, R. Camptothecin loaded graphene oxide nanoparticle functionalized with polyethylene glycol and folic acid for anticancer drug delivery. J. Drug Deliv. Sci. Technol., 2018, 43, 333-342.
[74]
Xu, Z.; Zhu, S.; Wang, M.; Li, Y.; Shi, P.; Huang, X. Delivery of paclitaxel using PEGylated graphene oxide as a nanocarrier. ACS Appl. Mater. Interfaces, 2015, 7, 1355-1363.
[75]
Tian, L.; Pei, X.; Zeng, Y.; He, R.; Li, Z.; Wang, J.; Wan, Q.; Li, X. Functionalized nanoscale graphene oxide for high efficient drug delivery of cisplatin. J. Nanopart. Res., 2014, 16, 2709.
[76]
Makharza, S.; Vittorio, O.; Cirillo, G.; Oswald, S.; Hinde, E.; Kavallaris, M.; Büchner, B.; Mertig, M.; Hampel, S. Graphene oxide - gelatin nanohybrids as functional tools for enhanced carboplatin activity in neuroblastoma cells. Pharm. Res., 2015, 32, 2132-2143.
[77]
Fan, X.; Jiao, G.; Zhao, W.; Jin, P.; Li, X. Magnetic Fe3O4-graphene composites as targeted drug nanocarriers for pH-activated release. Nanoscale, 2013, 5, 1143.
[78]
Khoee, S.; Karimi, M.R. Dual-drug loaded janus graphene oxide-based thermoresponsive nanoparticles for targeted therapy. Polymer (Guildf.), 2018, 142, 80-98.
[79]
Chen, M.L.; He, Y.J.; Chen, X.W.; Wang, J.H. Quantum-dot-conjugated graphene as a probe for simultaneous cancer-targeted fluorescent imaging, tracking, and monitoring drug delivery. Bioconjug. Chem., 2013, 24, 387-397.
[80]
McDonald, L.C. Trends in antimicrobial resistance in health care-associated pathogens and effect on treatment. Clin. Infect. Dis., 2006, 42, S65-S71.
[81]
Carlet, J.; Jarlier, V.; Harbarth, S.; Voss, A.; Goossens, H.; Pittet, D. Ready for a world without antibiotics? The pensières antibiotic resistance call to action. Antimicrob. Resist. Infect. Control, 2012, 1, 1-13.
[82]
Rossolini, G.M.; Arena, F.; Pecile, P.; Pollini, S. Update on the antibiotic resistance crisis. Curr. Opin. Pharmacol., 2014, 18, 56-60.
[83]
Kang, S.; Herzberg, M.; Rodrigues, D.F.; Elimelech, M. Antibacterial effects of carbon nanotubes: size does matter! Langmuir, 2008, 24, 6409-6413.
[84]
Krishnamoorthy, K.; Veerapandian, M.; Zhang, L.H.; Yun, K.; Kim, S.J. Antibacterial efficiency of graphene nanosheets against pathogenic bacteria via lipid peroxidation. J. Phys. Chem. C, 2012, 116, 17280-17287.
[85]
Wu, X.; Tan, S.; Xing, Y.; Pu, Q.; Wu, M.; Zhao, J.X. Graphene oxide as an efficient antimicrobial nanomaterial for eradicating multi-drug resistant bacteria in vitro and in vivo. Colloids Surf. B Biointerfaces, 2017, 157, 1-9.
[86]
Gurunathan, S.; Han, J.W.; Dayem, A.A.; Eppakayala, V.; Kim, J.H. Oxidative stress-mediated antibacterial activity of graphene oxide and reduced graphene oxide in Pseudomonas aeruginosa. Int. J. Nanomedicine, 2012, 7, 5901-5914.
[87]
Akhavan, O.; Ghaderi, E. Toxicity of graphene and graphene oxide nanowalls against bacteria. ACS Nano, 2010, 4, 5731-5736.
[88]
Vecitis, C.D.; Zodrow, K.R.; Kang, S.; Elimelech, M. Electronic-structure-dependent bacterial cytotoxicity of single-walled carbon nanotubes. ACS Nano, 2010, 4, 5471-5479.
[89]
Li, J.; Wang, G.; Zhu, H.; Zhang, M.; Zheng, X.; Di, Z.; Liu, X.; Wang, X. Antibacterial activity of large-area monolayer graphene film manipulated by charge transfer. Sci. Rep., 2014, 4, 4359.
[90]
Hui, L.; Piao, J.G.; Auletta, J.; Hu, K.; Zhu, Y.; Meyer, T.; Liu, H.; Yang, L. Availability of the basal planes of graphene oxide determines whether it is antibacterial. ACS Appl. Mater. Interfaces, 2014, 6, 13183-13190.
[91]
Karahan, H.E.; Wang, Y.; Li, W.; Liu, F.; Wang, L.; Sui, X.; Riaz, M.A.; Chen, Y. Antimicrobial graphene materials: The interplay of complex materials characteristics and competing mechanisms. Biomater. Sci., 2018, 6, 766-773.
[92]
Barbolina, I.; Woods, C.R.; Lozano, N.; Kostarelos, K.; Novoselov, K.S.; Roberts, I.S. Purity of graphene oxide determines its antibacterial activity. 2D Mater., 2016, 3, 025025.
[93]
Zheng, H.; Ma, R.; Gao, M.; Tian, X.; Li, Y-Q.; Zeng, L.; Li, R. Antibacterial applications of graphene oxides: Structure-activity relationships, molecular initiating events and biosafety. Sci. Bull., 2018, 63, 133-142.
[94]
Posa, V.R.; Annavaram, V.; Koduru, J.R.; Bobbala, P. V.M.; Somala, A.R. Preparation of graphene? TiO2 nanocomposite and photocatalytic degradation of rhodamine-B under solar light irradiation. J. Exp. Nanosci., 2016, 11, 722-736.
[95]
Scaffaro, R.; Botta, L.; Maio, A.; Gallo, G. PLA graphene nanoplatelets nanocomposites: Physical properties and release kinetics of an antimicrobial agent. Compos., Part B Eng., 2017, 109, 138-146.
[96]
Xu, L.Q.; Liao, Y.B.; Li, N.N.; Li, Y.J.; Zhang, J.Y.; Wang, Y.B.; Hu, X.F.; Li, C.M. Vancomycin-assisted green synthesis of reduced graphene oxide for antimicrobial applications. J. Colloid Interface Sci., 2018, 514, 733-739.
[97]
Kooti, M.; Sedeh, A.N.; Motamedi, H.; Rezatofighi, S.E. Magnetic graphene oxide inlaid with silver nanoparticles as antibacterial and drug delivery composite. Appl. Microbiol. Biotechnol., 2018, 102, 3607-3621.
[98]
Dadashi, F.M.; Arabi, S.A.; Sharifian, G.M.; Rahimpour, A.; Soroush, M. A novel nanocomposite with superior antibacterial activity: A silver-based metal organic framework embellished with graphene oxide. Adv. Mater. Interfaces, 2018, 5(11), 1701365.
[99]
Peng, J.M.; Lin, J.C.; Chen, Z.Y.; Wei, M.C.; Fu, Y.X.; Lu, S.S.; Yu, D.S.; Zhao, W. Enhanced antimicrobial activities of silver-nanoparticle-decorated reduced graphene nanocomposites against oral pathogens. Mater. Sci. Eng. C, 2017, 71, 10-16.
[100]
Whitehead, K.A.; Vaidya, M.; Liauw, C.M.; Brownson, D.A.C.; Ramalingam, P.; Kamieniak, J.; Rowley-Neale, S.J.; Tetlow, L.A.; Wilson-Nieuwenhuis, J.S.T.; Brown, D.; McBaind, A.J.; Kulandaivel, J.; Banks, C.E. Antimicrobial activity of graphene oxide-metal hybrids. Int. Biodeterior. Biodegradation, 2017, 123, 182-190.
[101]
Zhu, J.; Wang, J.; Hou, J.; Zhang, Y.; Liu, J.; Van der Bruggen, B. Graphene-based antimicrobial polymeric membranes: A review. J. Mater. Chem. A, 2017, 5, 6776-6793.
[102]
Lim, H.N.; Huang, N.M.; Loo, C.H. Facile preparation of graphene-based chitosan films: Enhanced thermal, mechanical and antibacterial properties. J. Non-Cryst. Solids, 2012, 358, 525-530.
[103]
Dhanasekar, M.; Jenefer, V.; Nambiar, R.B.; Babu, S.G.; Selvam, S.P.; Neppolian, B.; Bhat, S.V. ambient light antimicrobial activity of reduced graphene oxide supported metal doped TiO2 nanoparticles and their PVA based polymer nanocomposite films. Mater. Res. Bull., 2018, 97, 238-243.
[104]
Silva, M.; Caridade, S.G.; Vale, A.C.; Cunha, E.; Sousa, M.P.; Mano, J.F.; Paiva, M.C.; Alves, N.M. Biomedical films of graphene nanoribbons and nanoflakes with natural polymers. RSC Adv, 2017, 7, 27578-27594.
[105]
Ye, S.; Shao, K.; Li, Z.; Guo, N.; Zuo, Y.; Li, Q.; Lu, Z.; Chen, L.; He, Q.; Han, H. Antiviral activity of graphene oxide: How sharp edged structure and charge matter. ACS Appl. Mater. Interfaces, 2015, 7, 21578-21579.
[106]
Deokar, A.R.; Nagvenkar, A.P.; Kalt, I.; Shani, L.; Yeshurun, Y.; Gedanken, A.; Sarid, R. Graphene-based “hot plate” for the capture and destruction of the herpes simplex virus type 1. Bioconjug. Chem., 2017, 28, 1115-1122.
[107]
Karimi, L.; Yazdanshenas, M.E.; Khajavi, R.; Rashidi, A.; Mirjalili, M. Using graphene/TiO nanocomposite as a new route for preparation of electroconductive, self-cleaning, antibacterial and antifungal cotton fabric without toxicity. Cellulose, 2014, 21(5), 3813-3827.
[108]
Li, R.; Mansukhani, N.D.; Guiney, L.M.; Ji, Z.; Zhao, Y.; Chang, C.H.; French, C.T.; Miller, J.F.; Hersam, M.C.; Nel, A.E. Identification and optimization of carbon radicals on hydrated graphene oxide for ubiquitous antibacterial coatings. ACS Nano, 2016, 10, 10966-10980.
[109]
Dybowska-Sarapuk, Ł.; Kotela, A.; Krzemiński, J.; Wróblewska, M.; Marchel, H.; Romaniec, M.; Łȩgosz, P.; Jakubowska, M. Graphene nanolayers as a new method for bacterial biofilm prevention: Preliminary results. J. AOAC Int., 2017, 100, 900-904.
[110]
Nguyen, H.N.; Nadres, E.T.; Alamani, B.G.; Rodrigues, D.F. Designing polymeric adhesives for antimicrobial materials: Poly(ethylene imine) polymer, graphene, graphene oxide and molybdenum trioxide - a biomimetic approach. J. Mater. Chem. B, 2017, 5, 6616-6628.
[111]
de Moraes, A.C.M.; Lima, B.A.; de Faria, A.F.; Brocchi, M.; Alves, O.L. Graphene oxide-silver nanocomposite as a promising biocidal agent against methicillin-resistant staphylococcus aureus. Int. J. Nanomedicine, 2015, 10, 6847-6861.
[112]
Bugli, F.; Cacaci, M.; Palmieri, V.; Di Santo, R.; Torelli, R.; Ciasca, G.; Di Vito, M.; Vitali, A.; Conti, C.; Sanguinetti, M.; De Spirito, M.; Papi, M. Curcumin-loaded graphene oxide flakes as an effective antibacterial system against methicillin-resistant staphylococcus aureus. Interface Focus, 2018, 8, 20170059.
[113]
Zanni, E.; Chandraiahgari, C.; De Bellis, G.; Montereali, M.; Armiento, G.; Ballirano, P.; Polimeni, A.; Sarto, M.; Uccelletti, D. Zinc oxide nanorods-decorated graphene nanoplatelets: A promising antimicrobial agent against the cariogenic bacterium streptococcus mutans. Nanomaterials, 2016, 6, 179.
[114]
Yu, W.; Zhan, S.; Shen, Z.; Zhou, Q. A newly synthesized Au/GO-Co3O4 composite effectively inhibits the replication of tetracycline resistance gene in water. Chem. Eng. J., 2018, 345, 462-470.
[115]
Sun, H.; Gao, N.; Dong, K.; Ren, J.; Qu, X. Graphene quantum dots-band-aids used for wound disinfection. ACS Nano, 2014, 8, 6202-6210.
[116]
Wu, P.C.; Chen, H.H.; Chen, S.Y.; Wang, W.L.; Yang, K.L.; Huang, C.H.; Kao, H.F.; Chang, J.C.; Hsu, C.L.L.; Wang, J.Y.; Chou, T.M.; Kuo, W.S. Graphene oxide conjugated with polymers: a study of culture condition to determine whether a bacterial growth stimulant or an antimicrobial agent? J. Nanobiotechnology, 2018, 16, 1.
[117]
Al-Dosari, M.S.; Gao, X. Nonviral gene delivery: Principle, limitations, and recent progress. AAPS J., 2009, 11, 671-681.
[118]
Ren, T.; Li, L.; Cai, X.; Dong, H.; Liu, S.; Li, Y. Engineered Polyethylenimine/graphene oxide nanocomposite for nuclear localized gene delivery. Polym. Chem., 2012, 3, 2561.
[119]
Yin, H.; Kanasty, R.L.; Eltoukhy, A.A.; Vegas, A.J.; Dorkin, J.R.; Anderson, D.G. Non-viral vectors for gene-based therapy. Nat. Rev. Genet., 2014, 15, 541-555.
[120]
Ramamoorth, M.; Narvekar, A. Non viral vectors in gene therapy- an overview. J. Clin. Diagn. Res., 2015, 9, GE01-GE06.
[121]
Whitehead, K.A.; Langer, R.; Anderson, D.G. Knocking down Barriers: Advances in siRNA delivery. Nat. Rev. Drug Discov., 2009, 8, 129-138.
[122]
Yao, C.; Tu, Y.; Ding, L.; Li, C.; Wang, J.; Fang, H.; Huang, Y.; Zhang, K.; Lu, Q.; Wu, M. Tumor cell-specific nuclear targeting of functionalized graphene quantum dots in vivo. Bioconjug. Chem., 2017, 28, 2608-2619.
[123]
Teimouri, M.; Nia, A.H.; Abnous, K.; Eshghi, H.; Ramezani, M. Graphene oxide-cationic polymer conjugates: synthesis and application as gene delivery vectors. Plasmid, 2016, 84-85, 51-60.
[124]
Jäger, M.; Schubert, S.; Ochrimenko, S.; Fischer, D.; Schubert, U.S. Branched and linear poly(ethylene imine)-based conjugates: Synthetic modification, characterization, and application. Chem. Soc. Rev., 2012, 41, 4755-4767.
[125]
Chen, B.; Liu, M.; Zhang, L.; Huang, J.; Yao, J.; Zhang, Z. Polyethylenimine-functionalized graphene oxide as an efficient gene delivery vector. J. Mater. Chem., 2011, 21, 7736.
[126]
Mo, R.; Jiang, T.; Sun, W.; Gu, Z. ATP-Responsive DNA-graphene hybrid nanoaggregates for anticancer drug delivery. Biomaterials, 2015, 50, 67-74.
[127]
Huang, Y-P.; Hung, C-M.; Hsu, Y-C.; Zhong, C-Y.; Wang, W-R.; Chang, C-C.; Lee, M-J. Suppression of breast cancer cell migration by small interfering RNA delivered by polyethylenimine-functionalized graphene oxide. Nanoscale Res. Lett., 2016, 11, 247.
[128]
Wang, F.; Zhang, B.; Zhou, L.; Shi, Y.; Li, Z.; Xia, Y.; Tian, J. Imaging dendrimer-grafted graphene oxide mediated anti-mir-21 delivery with an activatable luciferase reporter. ACS Appl. Mater. Interfaces, 2016, 8, 9014-9021.
[129]
Li, Y.T.; Chua, M.J.; Kunnath, A.P.; Chowdhury, E.H. Reversing multidrug resistance in breast cancer cells by silencing ABC transporter genes with nanoparticle-facilitated delivery of target siRNAs. Int. J. Nanomedicine, 2012, 7, 2473-2481.
[130]
Zeng, X.; Yuan, Y.; Wang, T.; Wang, H.; Hu, X.; Fu, Z.; Zhang, G.; Liu, B.; Lu, G. Targeted imaging and induction of apoptosis of drug-resistant hepatoma cells by miR-122-loaded graphene-InP nanocompounds. J. Nanobiotechnology, 2017, 15, 9.
[131]
Foreman, H-C.C.; Lalwani, G.; Kalra, J.; Krug, L.T.; Sitharaman, B. Gene delivery to mammalian cells using a graphene nanoribbon platform. J. Mater. Chem. B, 2017, 5, 2347-2354.
[132]
Hsieh, C.J.; Chen, Y.C.; Hsieh, P.Y.; Liu, S.R.; Wu, S.P.; Hsieh, Y.Z.; Hsu, H.Y. Graphene oxide based nanocarrier combined with a pH-sensitive tracer: A vehicle for concurrent pH sensing and pH-responsive oligonucleotide delivery. ACS Appl. Mater. Interfaces, 2015, 7, 11467-11475.
[133]
Arayachukiat, S.; Seemork, J.; Pan-In, P.; Amornwachirabodee, K.; Sangphech, N.; Sansureerungsikul, T.; Sathornsantikun, K.; Vilaivan, C.; Shigyou, K.; Pienpinijtham, P.; Vilaivan, T.; Palaga, T.; Banlunara, W.; Hamada, T.; Wanichwecharungruang, S. Bringing macromolecules into cells and evading endosomes by oxidized carbon nanoparticles. Nano Lett., 2015, 15, 3370-3376.
[134]
Baek, A.; Baek, Y.M.; Kim, H.M.; Jun, B.H.; Kim, D.E. Polyethylene glycol-engrafted graphene oxide as biocompatible materials for peptide nucleic acid delivery into cells. Bioconjug. Chem., 2018, 29, 528-537.
[135]
Adibi-Motlagh, B.; Lotfi, A.S.; Rezaei, A.; Hashemi, E. Cell attachment evaluation of the immobilized bioactive peptide on a nanographene oxide composite. Mater. Sci. Eng. C, 2018, 82, 323-329.
[136]
Yu, Q.; Zhang, B.; Li, J.; Li, M. The design of peptide-grafted graphene oxide targeting the actin cytoskeleton for efficient cancer therapy. Chem. Commun., 2017, 53, 11433-11436.
[137]
Zhou, X.; Laroche, F.; Lamers, G.E.M.; Torraca, V.; Voskamp, P.; Lu, T.; Chu, F.; Spaink, H.P.; Abrahams, J.P.; Liu, Z. Ultra-small graphene oxide functionalized with polyethylenimine (PEI) for very efficient gene delivery in cell and zebrafish embryos. Nano Res., 2012, 5, 703-709.
[138]
Ren, L.; Zhang, Y.; Cui, C.; Bi, Y.; Ge, X. Functionalized graphene oxide for anti-VEGF siRNA delivery: Preparation, characterization and evaluation in vitro and in vivo. RSC Adv, 2017, 7(33), 20553-20566.
[139]
Zhang, L.; Zhou, Q.; Song, W.; Wu, K.; Zhang, Y.; Zhao, Y. Dual-functionalized graphene oxide based siRNA delivery system for implant surface biomodification with enhanced osteogenesis. ACS Appl. Mater. Interfaces, 2017, 9, 34722-34735.
[140]
Yang, H.W.; Huang, C.Y.; Lin, C.W.; Liu, H.L.; Huang, C.W.; Liao, S.S.; Chen, P.Y.; Lu, Y.J.; Wei, K.C.; Ma, C.C.M. Gadolinium-functionalized nanographene oxide for combined drug and microRNA delivery and magnetic resonance imaging. Biomaterials, 2014, 35, 6534-6542.
[141]
Dou, C.; Ding, N.; Luo, F.; Hou, T.; Cao, Z.; Bai, Y.; Liu, C.; Xu, J.; Dong, S. Graphene-based microRNA transfection blocks preosteoclast fusion to increase bone formation and vascularization. Adv. Sci., 2018, 5, 1700578.
[142]
Chen, G-Y.; Pang, D.W-P.; Hwang, S-M.; Tuan, H-Y.; Hu, Y-C. A graphene-based platform for induced pluripotent stem cells culture and differentiation. Biomaterials, 2012, 33, 418-427.
[143]
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. ACS Nano, 2011, 5, 7334-7341.
[144]
Solanki, A.; Chueng, S.T.D.; Yin, P.T.; Kappera, R.; Chhowalla, M.; Lee, K.B. Axonal alignment and enhanced neuronal differentiation of neural stem cells on graphene-nanoparticle hybrid structures. Adv. Mater., 2013, 25, 5477-5482.
[145]
Ryu, S.; Kim, B-S. culture of neural cells and stem cells on graphene. Tissue Eng. Regen. Med., 2013, 10, 39-46.
[146]
Yang, D.; Li, T.; Xu, M.; Gao, F.; Yang, J.; Yang, Z.; Le, W. Graphene oxide promotes the differentiation of mouse embryonic stem cells to dopamine neurons. Nanomedicine (Lond.), 2014, 9, 2445-2455.
[147]
Park, S.Y.; Park, J.; Sim, S.H.; Sung, M.G.; Kim, K.S.; Hong, B.H.; Hong, S. Enhanced differentiation of human neural stem cells into neurons on graphene. Adv. Mater., 2011, 23, H263-H267.
[148]
Qian, Y.; Zhao, X.; Han, Q.; Chen, W.; Li, H.; Yuan, W. An integrated multi-layer 3D-fabrication of PDA/RGD coated graphene loaded PCL nanoscaffold for peripheral nerve restoration. Nat. Commun., 2018, 9, 323.
[149]
Qian, Y.; Song, J.; Zhao, X.; Chen, W.; Ouyang, Y.; Yuan, W.; Fan, C. 3D fabrication with integration molding of a graphene oxide/polycaprolactone nanoscaffold for neurite regeneration and angiogenesis. Adv. Sci., 2018, 5, 1700499.
[150]
Palejwala, A.H.; Fridley, J.S.; Mata, J.A.; Samuel, E.L.G.; Luerssen, T.G.; Perlaky, L.; Kent, T.A.; Tour, J.M.; Jea, A. Biocompatibility of reduced graphene oxide nanoscaffolds following acute spinal cord injury in rats. Surg. Neurol. Int., 2016, 7, 75.
[151]
Abaco, G.M.D.; Mattei, C.; Hudson, E.J.; Alshawaf, A.J.; Chana, G.; Everall, I.P.; Nayagam, B.; Dottori, M.; Skafidas, E. Graphene foam as a biocompatible scaffold for culturing human neurons subject. RSC Open Sci, 2018, 5, 171364.
[152]
Correa-Duarte, M.A.; Wagner, N.; Rojas-Chapana, J.; Morsczeck, C.; Thie, M.; Giersig, M. Fabrication and biocompatibility of carbon nanotube-based 3D networks as scaffolds for cell seeding and growth. Nano Lett., 2004, 4, 2233-2236.
[153]
Zhu, W.; Harris, B.T.; Zhang, L.G. Gelatin methacrylamide hydrogel with graphene nanoplatelets for neural cell-laden 3D bioprinting. Conf. Proc. IEEE Eng. Med. Biol. Soc., 2016, 2016, 4185-4188.
[154]
Zhu, W.; George, J.K.; Sorger, V.J.; Grace Zhang, L. 3D printing scaffold coupled with low level light therapy for neural tissue regeneration. Biofabrication, 2017, 9, 025002.
[155]
Kumar, S.; Raj, S.; Sarkar, K.; Chatterjee, K. Engineering a multi-biofunctional composite using poly(ethylenimine) decorated graphene oxide for bone tissue regeneration. Nanoscale, 2016, 8, 6820-6836.
[156]
Lim, H.N.; Huang, N.M.; Lim, S.S.; Harrison, I.; Chia, C.H. Fabrication and characterization of graphene hydrogel via hydrothermal approach as a scaffold for preliminary study of cell growth. Int. J. Nanomedicine, 2011, 6, 1817-1823.
[157]
Zhou, X.; Nowicki, M.; Cui, H.; Zhu, W.; Fang, X.; Miao, S.; Lee, S.J.; Keidar, M.; Zhang, L.G. 3D bioprinted graphene oxide-incorporated matrix for promoting chondrogenic differentiation of human bone marrow mesenchymal stem cells. Carbon N.Y., 2017, 116, 615-624.
[158]
Kaur, T.; Thirugnanam, A.; Pramanik, K. Effect of carboxylated graphene nanoplatelets on mechanical and in-vitro biological properties of polyvinyl alcohol nanocomposite scaffolds for bone tissue engineering. Mater. Today Commun, 2017, 12, 34-42.
[159]
Nalvuran, H.; Elçin, A.E.; Elçin, Y.M. Nanofibrous silk fibroin/reduced graphene oxide scaffolds for tissue engineering and cell culture applications. Int. J. Biol. Macromol., 2018, 114, 77-84.
[160]
Rodríguez-Lozano, F.J.; García-Bernal, D.; Aznar-Cervantes, S.; Ros-Roca, M.A.; Algueró, M.C.; Atucha, N.M.; Lozano-García, A.A.; Moraleda, J.M.; Cenis, J.L. Effects of composite films of silk fibroin and graphene oxide on the proliferation, cell viability and mesenchymal phenotype of periodontal ligament stem cells. J. Mater. Sci. Mater. Med., 2014, 25, 2731-2741.
[161]
Bressan, E.; Ferroni, L.; Gardin, C.; Sbricoli, L.; Gobbato, L.; Ludovichetti, F.; Tocco, I.; Carraro, A.; Piattelli, A.; Zavan, B. Graphene based scaffolds effects on stem cells commitment. J. Transl. Med., 2014, 12, 296.
[162]
Du, Y.; Ge, J.; Li, Y.; Ma, P.X.; Lei, B. Biomimetic elastomeric, conductive and biodegradable polycitrate-based nanocomposites for guiding myogenic differentiation and skeletal muscle regeneration. Biomaterials, 2018, 157, 40-50.
[163]
Nair, M.; Nancy, D.; Krishnan, A.G.; Anjusree, G.S.; Vadukumpully, S.; Nair, S.V. Graphene oxide nanoflakes incorporated gelatin-hydroxyapatite scaffolds enhance osteogenic differentiation of human mesenchymal stem cells. Nanotechnology, 2015, 26, 161001.
[164]
Lu, S.; Wang, J.; Ye, J.; Zou, Y.; Zhu, Y.; Wei, Q.; Wang, X.; Tang, S.; Liu, H.; Fan, J.; Zhang, F.; Farina, E.M.; Mohammed, M.M.; Song, D.; Liao, J.; Huang, J.; Guo, D.; Lu, M.; Liu, F.; Liu, J.; Li, L.; Ma, C.; Hu, X.; Lee, M.J.; Reid, R.R.; Ameer, G.A.; Zhou, D.; He, T. Bone morphogenetic protein 9 (BMP9) induces effective bone formation from reversibly immortalized multipotent adipose-derived (iMAD) mesenchymal stem cells. Am. J. Transl. Res., 2016, 8, 3710-3730.
[165]
Rashkow, J.T.; Lalwani, G.; Sitharaman, B. In vitro bioactivity of one- and two-dimensional nanoparticle-incorporated bone tissue engineering scaffolds. Tissue Eng. Part A, 2018, 24, 641-652.
[166]
Shin, S.R.; Zihlmann, C.; Akbari, M.; Assawes, P.; Cheung, L.; Zhang, K.; Manoharan, V.; Zhang, Y.S.; Yüksekkaya, M.; Wan, K.T.; Nikkhah, M.; Dokmeci, M.R.; Tang, X.S.; Khademhosseini, A. Reduced graphene oxide-gelMA hybrid hydrogels as scaffolds for cardiac tissue engineering. Small, 2016, 12, 3677-3689.
[167]
Zhang, X.; Yin, J.; Peng, C.; Hu, W.; Zhu, Z.; Li, W.; Fan, C.; Huang, Q. Distribution and biocompatibility studies of graphene oxide in mice after intravenous administration. Carbon N.Y., 2011, 49, 986-995.
[168]
Wang, K.; Ruan, J.; Song, H.; Zhang, J.; Wo, Y.; Guo, S.; Cui, D. Biocompatibility of graphene oxide. Nanoscale Res. Lett., 2011, 6, 1-8.
[169]
Syama, S.; Mohanan, P.V. Safety and biocompatibility of graphene: A new generation nanomaterial for biomedical application. Int. J. Biol. Macromol., 2016, 86, 546-555.
[170]
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.
[171]
Akhavan, O.; Ghaderi, E.; Akhavan, A. Size-dependent genotoxicity of graphene nanoplatelets in human stem cells. Biomaterials, 2012, 33, 8017-8025.
[172]
Vila, M.; Portolés, M.T.; Marques, P.A.A.P.; Feito, M.J.; Matesanz, M.C.; Ramírez-Santillán, C.; Gonçalves, G.; Cruz, S.M.A.; Nieto, A.; Vallet-Regi, M. Cell uptake survey of pegylated nanographene oxide. Nanotechnology, 2012, 23, 465103.
[173]
Champion, J.A.; Mitragotri, S. Role of target geometry in phagocytosis. Proc. Natl. Acad. Sci. USA, 2006, 103, 4930-4934.
[174]
Zhang, Y.; Ali, S.F.; Dervishi, E.; Xu, Y.; Li, Z.; Casciano, D.; Biris, A.S. Cytotoxicity effects of graphene and single-wall carbon nanotubes in neural phaeochromocytoma-derived pc12 cells. ACS Nano, 2010, 4, 3181-3186.
[175]
Jaworski, S.; Sawosz, E.; Grodzik, M.; Winnicka, A.; Prasek, M.; Wierzbicki, M.; Chwalibog, A. In vitro evaluation of the effects of graphene platelets on glioblastoma multiforme cells. Int. J. Nanomedicine, 2013, 8, 413-420.
[176]
Park, E.J.; Lee, S.J.; Lee, K.; Choi, Y.C.; Lee, B.S.; Lee, G.H.; Kim, D.W. Pulmonary persistence of graphene nanoplatelets may disturb physiological and immunological homeostasis. J. Appl. Toxicol., 2017, 37, 296-309.
[177]
Chowdhury, S.M.; Dasgupta, S.; Mcelroy, A.E.; Sitharaman, B. Structural disruption increases toxicity of graphene nanoribbons. J. Appl. Toxicol., 2014, 34, 1235-1246.
[178]
Khim Chng, E.L.; Chua, C.K.; Pumera, M. graphene oxide nanoribbons exhibit significantly greater toxicity than graphene oxide nanoplatelets. Nanoscale, 2014, 6, 10792-10797.
[179]
Liu, K.; Zhang, J-J.; Cheng, F-F.; Zheng, T-T.; Wang, C.; Zhu, J-J. Green and facile synthesis of highly biocompatible graphene nanosheets and its application for cellular imaging and drug delivery. J. Mater. Chem., 2011, 21, 12034-12040.
[180]
Zhu, C.; Guo, S.; Fang, Y.; Dong, S. Reducing sugar: New functional molecules for the green synthesis of graphene nanosheets. ACS Nano, 2010, 4, 2429-2437.
[181]
Fernández-Merino, M.J.; Guardia, L.; Paredes, J.I.; Villar-Rodil, S.; Solís-Fernández, P.; Martínez-Alonso, A.; Tascón, J.M.D.; Vitamin, C. Is an ideal substitute for hydrazine in the reduction of graphene oxide suspensions. J. Phys. Chem. C, 2010, 114, 6426-6432.
[182]
Gurunathan, S.; Han, J.W.; Kim, E.S.; Park, J.H.; Kim, J.H. Reduction of graphene oxide by resveratrol: A novel and simple biological method for the synthesis of an effective anticancer nanotherapeutic molecule. Int. J. Nanomedicine, 2015, 10, 2951-2969.
[183]
Gurunathan, S.; Han, J.W.; Eppakayala, V.; Kim, J-H. Green synthesis of graphene and its cytotoxic effects in human breast cancer cells. Int. J. Nanomedicine, 2013, 8, 1015-1027.
[184]
Cheng, C.; Nie, S.; Li, S.; Peng, H.; Yang, H.; Ma, L.; Sun, S.; Zhao, C. Biopolymer functionalized reduced graphene oxide with enhanced biocompatibility via mussel inspired coatings/anchors. J. Mater. Chem. B, 2013, 1, 265-275.
[185]
Khodadadei, F.; Safarian, S.; Ghanbari, N. Methotrexate-loaded nitrogen-doped graphene quantum dots nanocarriers as an efficient anticancer drug delivery system. Mater. Sci. Eng. C Mater. Biol. Appl., 2017, 79, 280-285.
[186]
Cheng, S-J.; Chiu, H-Y.; Kumar, P.V.; Hsieh, K.Y.; Yang, J-W.; Lin, Y-R.; Shen, Y-C.; Chen, G-Y. Simultaneous drug delivery and cellular imaging using graphene oxide. Biomater. Sci., 2018, 6, 813-819.
[187]
Chen, M.L.; Gao, Z.W.; Chen, X.M.; Pang, S.C.; Zhang, Y. Laser-assisted in situ synthesis of graphene-based magnetic-responsive hybrids for multimodal imaging-guided chemo/photothermal synergistic therapy. Talanta, 2018, 182, 433-442.
[188]
Bani, F.; Bodaghi, A.; Dadkhah, A.; Movahedi, S.; Bodaghabadi, N.; Sadeghizadeh, M.; Adeli, M. One-pot exfoliation, functionalization, and size manipulation of graphene sheets: Efficient system for biomedical applications. Lasers Med. Sci., 2018, 33, 795-802.
[189]
Liu, Y.; Peng, J.; Wang, S.; Xu, M.; Gao, M.; Xia, T.; Weng, J.; Xu, A.; Liu, S. Molybdenum disulfide/graphene oxide nanocomposites show favorable lung targeting and enhanced drug loading/tumor-killing efficacy with improved biocompatibility. NPG Asia Mater., 2018, 10, e458.
[190]
Gao, J.; Liu, F.; Liu, Y.; Ma, N.; Wang, Z.; Zhang, X. Environment-friendly method to produce graphene that employs vitamin c and amino acid. Chem. Mater., 2010, 22, 2213-2218.
[191]
Thakur, S.; Karak, N. Green reduction of graphene oxide by aqueous phytoextracts. Carbon N.Y., 2012, 50, 5331-5339.
[192]
Salas, E.C.; Sun, Z.; Lüttge, A.; Tour, J.M. Reduction of graphene oxide via bacterial respiration. ACS Nano, 2010, 4, 4852-4856.
[193]
Liu, M.; Zeng, X.; Ma, C.; Yi, H.; Ali, Z.; Mou, X.; Li, S.; Deng, Y.; He, N. Injectable hydrogels for cartilage and bone tissue engineering. Bone Res., 2017, 30, 17014.


Rights & PermissionsPrintExport Cite as


Article Details

VOLUME: 16
ISSUE: 3
Year: 2019
Page: [195 - 214]
Pages: 20
DOI: 10.2174/1567201815666181031162208
Price: $58

Article Metrics

PDF: 33
HTML: 2
EPUB: 1
PRC: 1