Generic placeholder image

Current Medicinal Chemistry

Author(s): Mohammad Omaish Ansari, Kalamegam Gauthaman, Abdurahman Essa, Sidi A. Bencherif and Adnan Memic*

DOI: 10.2174/0929867326666190705155854

DownloadDownload PDF Flyer Cite As
Graphene and Graphene-Based Materials in Biomedical Applications

Page: [6834 - 6850] Pages: 17

  • * (Excluding Mailing and Handling)

Abstract

Nanobiotechnology has huge potential in the field of regenerative medicine. One of the main drivers has been the development of novel nanomaterials. One developing class of materials is graphene and its derivatives recognized for their novel properties present on the nanoscale. In particular, graphene and graphene-based nanomaterials have been shown to have excellent electrical, mechanical, optical and thermal properties. Due to these unique properties coupled with the ability to tune their biocompatibility, these nanomaterials have been propelled for various applications. Most recently, these two-dimensional nanomaterials have been widely recognized for their utility in biomedical research. In this review, a brief overview of the strategies to synthesize graphene and its derivatives are discussed. Next, the biocompatibility profile of these nanomaterials as a precursor to their biomedical application is reviewed. Finally, recent applications of graphene-based nanomaterials in various biomedical fields including tissue engineering, drug and gene delivery, biosensing and bioimaging as well as other biorelated studies are highlighted.

Keywords: GN oxide, tissue engineering, drug delivery, biomedical applications, biocompatibility, nanomaterials.

[1]
Geim, A.K.; Novoselov, K.S. The rise of graphene. Nat. Mater., 2007, 6(3), 183-191.
[http://dx.doi.org/10.1038/nmat1849] [PMID: 17330084]
[2]
Chimene, D.; Alge, D.L.; Gaharwar, A.K. Two-dimensional nanomaterials for biomedical applications: emerging trends and future prospects. Adv. Mater., 2015, 27(45), 7261-7284.
[http://dx.doi.org/10.1002/adma.201502422] [PMID: 26459239]
[3]
Cha, C.; Shin, S.R.; Annabi, N.; Dokmeci, M.R.; Khademhosseini, A. Carbon-based nanomaterials: multifunctional materials for biomedical engineering. ACS Nano, 2013, 7(4), 2891-2897.
[http://dx.doi.org/10.1021/nn401196a] [PMID: 23560817]
[4]
Iijima, S. Helical microtubules of graphitic carbon. Nature, 1991, 354, 56.
[http://dx.doi.org/10.1038/354056a0]
[5]
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(5696), 666-669.
[http://dx.doi.org/10.1126/science.1102896]
[6]
Ruoff, R. Graphene: calling all chemists. Nat. Nanotechnol., 2008, 3(1), 10-11.
[http://dx.doi.org/10.1038/nnano.2007.432] [PMID: 18654440]
[7]
Stankovich, S.; Dikin, D.A.; Dommett, G.H.; Kohlhaas, K.M.; Zimney, E.J.; Stach, E.A.; Piner, R.D.; Nguyen, S.T.; Ruoff, R.S. Graphene-based composite materials. Nature, 2006, 442(7100), 282-286.
[http://dx.doi.org/10.1038/nature04969] [PMID: 16855586]
[8]
Dikin, D.A.; Stankovich, S.; Zimney, E.J.; Piner, R.D.; Dommett, G.H.; Evmenenko, G.; Nguyen, S.T.; Ruoff, R.S. Preparation and characterization of graphene oxide paper. Nature, 2007, 448(7152), 457-460.
[http://dx.doi.org/10.1038/nature06016] [PMID: 17653188]
[9]
Wang, S.; Ang, P.K.; Wang, Z.; Tang, A.L.L.; Thong, J.T.; Loh, K.P. High mobility, printable, and solution-processed graphene electronics. Nano Lett., 2010, 10(1), 92-98.
[http://dx.doi.org/10.1021/nl9028736] [PMID: 20025234]
[10]
Feng, L.; Liu, Z. Graphene in biomedicine: opportunities and challenges. Nanomedicine (Lond.), 2011, 6(2), 317-324.
[http://dx.doi.org/10.2217/nnm.10.158] [PMID: 21385134]
[11]
Sanchez, V.C.; Jachak, A.; Hurt, R.H.; Kane, A.B. Biological interactions of graphene-family nanomaterials: an interdisciplinary review. Chem. Res. Toxicol., 2012, 25(1), 15-34.
[http://dx.doi.org/10.1021/tx200339h] [PMID: 21954945]
[12]
Wee, A.T.S. Graphene: the game changer? ACS Nano, 2012, 6(7), 5739-5741.
[http://dx.doi.org/10.1021/nn302799p] [PMID: 22823276]
[13]
Lee, C.; Wei, X.; Kysar, J.W.; Hone, J. Measurement of the elastic properties and intrinsic strength of monolayer graphene. Science, 2008, 321(5887), 385-388.
[http://dx.doi.org/10.1126/science.1157996] [PMID: 18635798]
[14]
Lau, C.N.; Bao, W.; Velasco, J., Jr Properties of suspended graphene membranes. Mater. Today, 2012, 15(6), 238-245.
[http://dx.doi.org/10.1016/S1369-7021(12)70114-1]
[15]
Butko, A.V.; Butko, V.Y. Electrical transport in graphene with different interface conditions. Phys. Solid State, 2015, 57(5), 1048-1050.
[http://dx.doi.org/10.1134/S1063783415050066]
[16]
Papageorgiou, D.G.; Kinloch, I.A.; Young, R.J. Mechanical properties of graphene and graphene-based nanocomposites. Prog. Mater. Sci., 2017, 90, 75-127.
[http://dx.doi.org/10.1016/j.pmatsci.2017.07.004]
[17]
Li, X.; Yu, J.; Wageh, S.; Al-Ghamdi, A.A.; Xie, J. Graphene in photocatalysis: a review. Small, 2016, 12(48), 6640-6696.
[http://dx.doi.org/10.1002/smll.201600382] [PMID: 27805773]
[18]
Yang, T.; Jiang, X.; Zhong, Y.; Zhao, X.; Lin, S.; Li, J.; Li, X.; Xu, J.; Li, Z.; Zhu, H. A wearable and highly sensitive graphene strain sensor for precise home-based pulse wave monitoring. ACS Sens., 2017, 2(7), 967-974.
[http://dx.doi.org/10.1021/acssensors.7b00230] [PMID: 28750520]
[19]
Shiraz, H.G.; Tavakoli, O. Investigation of graphene-based systems for hydrogen storage. Renew. Sustain. Energy Rev., 2017, 74, 104-109.
[http://dx.doi.org/10.1016/j.rser.2017.02.052]
[20]
Lin, X-F.; Zhang, Z-Y.; Yuan, Z-K.; Li, J.; Xiao, X-F.; Hong, W.; Chen, X-D.; Yu, D-S. Graphene-based materials for polymer solar cells. Chin. Chem. Lett., 2016, 27(8), 1259-1270.
[http://dx.doi.org/10.1016/j.cclet.2016.06.041]
[21]
Zhao, H.; Ding, R.; Zhao, X.; Li, Y.; Qu, L.; Pei, H.; Yildirimer, L.; Wu, Z.; Zhang, W. Graphene-based nanomaterials for drug and/or gene delivery, bioimaging, and tissue engineering. Drug Discov. Today, 2017, 22(9), 1302-1317.
[http://dx.doi.org/10.1016/j.drudis.2017.04.002] [PMID: 28869820]
[22]
Suvarnaphaet, P.; Pechprasarn, S. Graphene-based materials for biosensors: a review. Sensors (Basel), 2017, 17(10)E2161
[http://dx.doi.org/10.3390/s17102161] [PMID: 28934118]
[23]
Karahan, H.E.; Wiraja, C.; Xu, C.; Wei, J.; Wang, Y.; Wang, L.; Liu, F.; Chen, Y. Graphene materials in antimicrobial nanomedicine: current status and future perspectives. Adv. Healthc. Mater., 2018, 7(13)e1701406
[http://dx.doi.org/10.1002/adhm.201701406] [PMID: 29504283]
[24]
Singh, D.P.; Herrera, C.E.; Singh, B.; Singh, S.; Singh, R.K.; Kumar, R. Graphene oxide: an efficient material and recent approach for biotechnological and biomedical applications. Mater. Sci. Eng. C, 2018, 86, 173-197.
[http://dx.doi.org/10.1016/j.msec.2018.01.004] [PMID: 29525091]
[25]
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(4), 1593-1597.
[http://dx.doi.org/10.1021/nl803798y] [PMID: 19265429]
[26]
Xie, W.; Zhu, X.; Xu, S.; Yi, S.; Guo, Z.; Kuang, J.; Deng, Y. Cost-effective fabrication of graphene-like nanosheets from natural microcrystalline graphite minerals by liquid oxidation-reduction method. RSC Advances, 2017, 7(51), 32008-32019.
[http://dx.doi.org/10.1039/C7RA02171B]
[27]
Balan, A.; Kumar, R.; Boukhicha, M.; Beyssac, O.; Bouillard, J-C.; Taverna, D.; Sacks, W.; Marangolo, M.; Lacaze, E.; Gohler, R. Anodic bonded graphene. J. Phys. D Appl. Phys., 2010, 43(37)374013
[http://dx.doi.org/10.1088/0022-3727/43/37/374013]
[28]
Kazemizadeh, F.; Malekfar, R. One step synthesis of porous graphene by laser ablation: a new and facile approach. Physica B, 2018, 530, 236-241.
[http://dx.doi.org/10.1016/j.physb.2017.11.052]
[29]
Lin, W-C.; Chuang, M-K.; Keshtov, M.L.; Sharma, G.D.; Chen, F-C. Photoexfoliation of two-dimensional materials through continuous UV irradiation. Nanotechnology, 2017, 28(12)125604
[http://dx.doi.org/10.1088/1361-6528/aa5c79] [PMID: 28220757]
[30]
Hummers, W.S., Jr; Offeman, R.E. Preparation of graphitic oxide. J. Am. Chem. Soc., 1958, 80(6), 1339-1339.
[http://dx.doi.org/10.1021/ja01539a017]
[31]
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(8), 4806-4814.
[http://dx.doi.org/10.1021/nn1006368] [PMID: 20731455]
[32]
Alam, S.N.; Sharma, N.; Kumar, L. Synthesis of graphene oxide (GO) by modified hummers method and its thermal reduction to obtain reduced graphene oxide (rGO). Graphene, 2017, 6(1), 1-18.
[http://dx.doi.org/10.4236/graphene.2017.61001]
[33]
Parveen, N.; Ansari, M.O.; Cho, M.H. Simple route for gram synthesis of less defective few layered graphene and its electrochemical performance. RSC Advances, 2015, 5(56), 44920-44927.
[http://dx.doi.org/10.1039/C5RA06404J]
[34]
Ciesielski, A.; Samorì, P. Graphene via sonication assisted liquid-phase exfoliation. Chem. Soc. Rev., 2014, 43(1), 381-398.
[http://dx.doi.org/10.1039/C3CS60217F] [PMID: 24002478]
[35]
Zhang, Y.; Zhang, L.; Zhou, C. Review of chemical vapor deposition of graphene and related applications. Acc. Chem. Res., 2013, 46(10), 2329-2339.
[http://dx.doi.org/10.1021/ar300203n] [PMID: 23480816]
[36]
Yu, Q.; Lian, J.; Siriponglert, S.; Li, H.; Chen, Y.P.; Pei, S-S. Graphene segregated on Ni surfaces and transferred to insulators. Appl. Phys. Lett., 2008, 93(11)113103
[http://dx.doi.org/10.1063/1.2982585]
[37]
Li, X.; Cai, W.; An, J.; Kim, S.; Nah, J.; Yang, D.; Piner, R.; Velamakanni, A.; Jung, I.; Tutuc, E.; Banerjee, S.K.; Colombo, L.; Ruoff, R.S. Large-area synthesis of high-quality and uniform graphene films on copper foils. Science, 2009, 324(5932), 1312-1314.
[http://dx.doi.org/10.1126/science.1171245] [PMID: 19423775]
[38]
Sutter, P.W.; Flege, J-I.; Sutter, E.A. Epitaxial graphene on ruthenium. Nat. Mater., 2008, 7(5), 406-411.
[http://dx.doi.org/10.1038/nmat2166] [PMID: 18391956]
[39]
Walt, A.H.; Claire, B. Epitaxial graphene. J. Phys. D Appl. Phys., 2012, 45(15)150301
[http://dx.doi.org/10.1088/0022-3727/45/15/150301]
[40]
Sun, Z.; Yan, Z.; Yao, J.; Beitler, E.; Zhu, Y.; Tour, J.M. Growth of graphene from solid carbon sources. Nature, 2010, 468(7323), 549-552.
[http://dx.doi.org/10.1038/nature09579] [PMID: 21068724]
[41]
Kim, W.; Oh, H-S.; Shon, I-J. The effect of graphene reinforcement on the mechanical properties of Al2O3 ceramics rapidly sintered by high-frequency induction heating. Int. J. Refract. Met. Hard Mater., 2015, 48, 376-381.
[http://dx.doi.org/10.1016/j.ijrmhm.2014.10.011]
[42]
Kumar, H.G.P.; Xavior, M.A. Graphene reinforced metal matrix composite (GRMMC): a review. Procedia Eng., 2014, 97, 1033-1040.
[http://dx.doi.org/10.1016/j.proeng.2014.12.381]
[43]
Gao, Y. Graphene and polymer composites for supercapacitor applications: a review. Nanoscale Res. Lett., 2017, 12(1), 387.
[http://dx.doi.org/10.1186/s11671-017-2150-5] [PMID: 28582964]
[44]
Yan, J.; Wei, T.; Shao, B.; Fan, Z.; Qian, W.; Zhang, M.; Wei, F. Preparation of a graphene nanosheet/polyaniline composite with high specific capacitance. Carbon, 2010, 48(2), 487-493.
[http://dx.doi.org/10.1016/j.carbon.2009.09.066]
[45]
Lingappan, N.; Gal, Y-S.; Lim, K.T. Synthesis of reduced graphene oxide/polypyrrole conductive composites. Mol. Cryst. Liq. Cryst. (Phila. Pa.), 2013, 585(1), 60-66.
[http://dx.doi.org/10.1080/15421406.2013.849510]
[46]
Mitra, M.; Kulsi, C.; Chatterjee, K.; Kargupta, K.; Ganguly, S.; Banerjee, D.; Goswami, S. Reduced graphene oxide-polyaniline composites-synthesis, characterization and optimization for thermoelectric applications. RSC Advances, 2015, 5(39), 31039-31048.
[http://dx.doi.org/10.1039/C5RA01794G]
[47]
Zheng, X.; Peng, Y.; Yang, Y.; Chen, J.; Tian, H.; Cui, X.; Zheng, W. Hydrothermal reduction of graphene oxide; effect on surface-enhanced Raman scattering. J. Raman Spectrosc., 2017, 48(1), 97-103.
[http://dx.doi.org/10.1002/jrs.4998]
[48]
Donaldson, K.; Aitken, R.; Tran, L.; Stone, V.; Duffin, R.; Forrest, G.; Alexander, A. Carbon nanotubes: a review of their properties in relation to pulmonary toxicology and workplace safety. Toxicol. Sci., 2006, 92(1), 5-22.
[http://dx.doi.org/10.1093/toxsci/kfj130] [PMID: 16484287]
[49]
Bianco, A. Graphene: safe or toxic? The two faces of the medal. Angew. Chem. Int. Ed. Engl., 2013, 52(19), 4986-4997.
[http://dx.doi.org/10.1002/anie.201209099] [PMID: 23580235]
[50]
Alshehri, R.; Ilyas, A.M.; Hasan, A.; Arnaout, A.; Ahmed, F.; Memic, A. Carbon nanotubes in biomedical applications: factors, mechanisms, and remedies of toxicity. J. Med. Chem., 2016, 59(18), 8149-8167.
[http://dx.doi.org/10.1021/acs.jmedchem.5b01770] [PMID: 27142556]
[51]
Ren, H.; Wang, C.; Zhang, J.; Zhou, X.; Xu, D.; Zheng, J.; Guo, S.; Zhang, J. DNA cleavage system of nanosized graphene oxide sheets and copper ions. ACS Nano, 2010, 4(12), 7169-7174.
[http://dx.doi.org/10.1021/nn101696r] [PMID: 21082807]
[52]
Chandra, V.; Park, J.; Chun, Y.; Lee, J.W.; Hwang, I-C.; Kim, K.S. Water-dispersible magnetite-reduced graphene oxide composites for arsenic removal. ACS Nano, 2010, 4(7), 3979-3986.
[http://dx.doi.org/10.1021/nn1008897] [PMID: 20552997]
[53]
Wilczek, P.; Major, R.; Lipinska, L.; Lackner, J.; Mzyk, A. Thrombogenicity and biocompatibility studies of reduced graphene oxide modified acellular pulmonary valve tissue. Mater. Sci. Eng. C, 2015, 53, 310-321.
[http://dx.doi.org/10.1016/j.msec.2015.04.044] [PMID: 26042719]
[54]
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,, 2011, 49(3), 986-995.
[http://dx.doi.org/10.1016/j.carbon.2010.11.005]
[55]
Wang, L.; Wang, Y.; Xu, T.; Liao, H.; Yao, C.; Liu, Y.; Li, Z.; Chen, Z.; Pan, D.; Sun, L.; Wu, M. Gram-scale synthesis of single-crystalline graphene quantum dots with superior optical properties. Nat. Commun., 2014, 5, 5357.
[http://dx.doi.org/10.1038/ncomms6357] [PMID: 25348348]
[56]
Murray, E.; Sayyar, S.; Thompson, B.C.; Gorkin, R., III; Officer, D.L.; Wallace, G.G. A bio-friendly, green route to processable, biocompatible graphene/polymer composites. RSC Advances, 2015, 5(56), 45284-45290.
[http://dx.doi.org/10.1039/C5RA07210G]
[57]
Xu, Y.; Wu, Q.; Sun, Y.; Bai, H.; Shi, G. Three-dimensional self-assembly of graphene oxide and DNA into multifunctional hydrogels. ACS Nano, 2010, 4(12), 7358-7362.
[http://dx.doi.org/10.1021/nn1027104] [PMID: 21080682]
[58]
Yang, K.; Wan, J.; Zhang, S.; Zhang, Y.; Lee, S-T.; Liu, Z. In vivo pharmacokinetics, long-term biodistribution, and toxicology of PEGylated graphene in mice. ACS Nano, 2011, 5(1), 516-522.
[http://dx.doi.org/10.1021/nn1024303] [PMID: 21162527]
[59]
Nel, A.E.; Mädler, L.; Velegol, D.; Xia, T.; Hoek, E.M.; Somasundaran, P.; Klaessig, F.; Castranova, V.; Thompson, M. Understanding biophysicochemical interactions at the nano-bio interface. Nat. Mater., 2009, 8(7), 543-557.
[http://dx.doi.org/10.1038/nmat2442] [PMID: 19525947]
[60]
Hu, W.; Peng, C.; Luo, W.; Lv, M.; Li, X.; Li, D.; Huang, Q.; Fan, C. Graphene-based antibacterial paper. ACS Nano, 2010, 4(7), 4317-4323.
[http://dx.doi.org/10.1021/nn101097v] [PMID: 20593851]
[61]
Memic, A.; Navaei, A.; Mirani, B.; Cordova, J.A.V.; Aldhahri, M.; Dolatshahi-Pirouz, A.; Akbari, M.; Nikkhah, M. Bioprinting technologies for disease modeling. Biotechnol. Lett., 2017, 39(9), 1279-1290.
[http://dx.doi.org/10.1007/s10529-017-2360-z] [PMID: 28550360]
[62]
Kharaziha, M.; Memic, A.; Akbari, M.; Brafman, D.A.; Nikkhah, M. Nano-enabled approaches for stem cell-based cardiac tissue engineering. Adv. Healthc. Mater., 2016, 5(13), 1533-1553.
[http://dx.doi.org/10.1002/adhm.201600088] [PMID: 27199266]
[63]
Memic, A.; Alhadrami, H.A.; Hussain, M.A.; Aldhahri, M.; Al Nowaiser, F.; Al-Hazmi, F.; Oklu, R.; Khademhosseini, A. Hydrogels 2.0: improved properties with nanomaterial composites for biomedical applications. Biomed. Mater., 2015, 11(1)014104
[http://dx.doi.org/10.1088/1748-6041/11/1/014104] [PMID: 26694229]
[64]
Ding, X.; Liu, H.; Fan, Y. Graphene‐based materials in regenerative medicine. Adv. Healthc. Mater., 2015, 4(10), 1451-1468.
[http://dx.doi.org/10.1002/adhm.201500203] [PMID: 26037920]
[65]
Kobolak, J.; Dinnyes, A.; Memic, A.; Khademhosseini, A.; Mobasheri, A. Mesenchymal stem cells: Identification, phenotypic characterization, biological properties and potential for regenerative medicine through biomaterial micro-engineering of their niche. Methods, 2016, 99, 62-68.
[http://dx.doi.org/10.1016/j.ymeth.2015.09.016] [PMID: 26384580]
[66]
Paul, A.; Manoharan, V.; Krafft, D.; Assmann, A.; Uquillas, J.A.; Shin, S.R.; Hasan, A.; Hussain, M.A.; Memic, A.; Gaharwar, A.K.; Khademhosseini, A. Nanoengineered biomimetic hydrogels for guiding human stem cell osteogenesis in three dimensional microenvironments. J. Mater. Chem. B Mater. Biol. Med., 2016, 4(20), 3544-3554.
[http://dx.doi.org/10.1039/C5TB02745D] [PMID: 27525102]
[67]
Memic, A.; Khademhosseini, A. Finding the winning combination. Combinatorial screening of three dimensional niches to guide stem cell osteogenesis. Organogenesis, 2014, 10(3), 299-302.
[http://dx.doi.org/10.4161/org.29646] [PMID: 25482315]
[68]
Kenry; Lee, W.C.; Loh, K.P.; Lim, C.T. When stem cells meet graphene: opportunities and challenges in regenerative medicine. Biomaterials, 2018, 155, 236-250.
[http://dx.doi.org/10.1016/j.biomaterials.2017.10.004] [PMID: 29195230]
[69]
Ramos, A.P.; Cruz, M.A.E.; Tovani, C.B.; Ciancaglini, P. Biomedical applications of nanotechnology. Biophys. Rev., 2017, 9(2), 79-89.
[http://dx.doi.org/10.1007/s12551-016-0246-2] [PMID: 28510082]
[70]
Teradal, N.L.; Jelinek, R. Carbon nanomaterials in biological studies and biomedicine. Adv. Healthc. Mater., 2017, 6(17)
[http://dx.doi.org/10.1002/adhm.201700574] [PMID: 28777502]
[71]
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(16)161001
[http://dx.doi.org/10.1088/0957-4484/26/16/161001] [PMID: 25824014]
[72]
Fu, C.; Bai, H.; Zhu, J.; Niu, Z.; Wang, Y.; Li, J.; Yang, X.; Bai, Y. Enhanced cell proliferation and osteogenic differentiation in electrospun PLGA/hydroxyapatite nanofibre scaffolds incorporated with graphene oxide. PLoS One, 2017, 12(11)e0188352
[http://dx.doi.org/10.1371/journal.pone.0188352] [PMID: 29186202]
[73]
Kim, J.; Kim, H.D.; Park, J.; Lee, E.S.; Kim, E.; Lee, S.S.; Yang, J-K.; Lee, Y-S.; Hwang, N.S. Enhanced osteogenic commitment of murine mesenchymal stem cells on graphene oxide substrate. Biomater. Res., 2018, 22(1), 1.
[http://dx.doi.org/10.1186/s40824-017-0112-8] [PMID: 29308274]
[74]
Niu, Y.; Chen, K.C.; He, T.; Yu, W.; Huang, S.; Xu, K. Scaffolds from block polyurethanes based on poly(ɛ-caprolactone) (PCL) and poly(ethylene glycol) (PEG) for peripheral nerve regeneration. Biomaterials, 2014, 35(14), 4266-4277.
[http://dx.doi.org/10.1016/j.biomaterials.2014.02.013] [PMID: 24582378]
[75]
Li, D.; Luo, L.; Pang, Z.; Ding, L.; Wang, Q.; Ke, H.; Huang, F.; Wei, Q. Novel phenolic biosensor based on a magnetic polydopamine-laccase-nickel nanoparticle loaded carbon nanofiber composite. ACS Appl. Mater. Interfaces, 2014, 6(7), 5144-5151.
[http://dx.doi.org/10.1021/am500375n] [PMID: 24606719]
[76]
Muszanska, A.K.; Rochford, E.T.; Gruszka, A.; Bastian, A.A.; Busscher, H.J.; Norde, W.; van der Mei, H.C.; Herrmann, A. Antiadhesive polymer brush coating functionalized with antimicrobial and RGD peptides to reduce biofilm formation and enhance tissue integration. Biomacromolecules, 2014, 15(6), 2019-2026.
[http://dx.doi.org/10.1021/bm500168s] [PMID: 24833130]
[77]
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(1), 323.
[http://dx.doi.org/10.1038/s41467-017-02598-7] [PMID: 29358641]
[78]
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(33), 10876-10877.
[http://dx.doi.org/10.1021/ja803688x] [PMID: 18661992]
[79]
Wang, L.; Zhang, Y.; Wu, A.; Wei, G. Designed graphene-peptide nanocomposites for biosensor applications: a review. Anal. Chim. Acta, 2017, 985, 24-40.
[http://dx.doi.org/10.1016/j.aca.2017.06.054] [PMID: 28864192]
[80]
Li, D.; Zhang, W.; Yu, X.; Wang, Z.; Su, Z.; Wei, G. When biomolecules meet graphene: from molecular level interactions to material design and applications. Nanoscale, 2016, 8(47), 19491-19509.
[http://dx.doi.org/10.1039/C6NR07249F] [PMID: 27878179]
[81]
Kim, H.; Lee, D.; Kim, J.; Kim, T.I.; Kim, W.J. Photothermally triggered cytosolic drug delivery via endosome disruption using a functionalized reduced graphene oxide. ACS Nano, 2013, 7(8), 6735-6746.
[http://dx.doi.org/10.1021/nn403096s] [PMID: 23829596]
[82]
Song, Z.; Xu, Y.; Yang, W.; Cui, L.; Zhang, J.; Liu, J. Graphene/tri-block copolymer composites prepared via RAFT polymerizations for dual controlled drug delivery via pH stimulation and biodegradation. Eur. Polym. J., 2015, 69, 559-572.
[http://dx.doi.org/10.1016/j.eurpolymj.2015.02.014]
[83]
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 (Lond.), 2015, 11(1), 109-118.
[http://dx.doi.org/10.1016/j.nano.2014.08.001] [PMID: 25131339]
[84]
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(19), 17268-17276.
[http://dx.doi.org/10.1021/am505308f] [PMID: 25216036]
[85]
Park, Y.H.; Park, S.Y.; In, I. Direct noncovalent conjugation of folic acid on reduced graphene oxide as anticancer drug carrier. J. Ind. Eng. Chem., 2015, 30, 190-196.
[http://dx.doi.org/10.1016/j.jiec.2015.05.021]
[86]
Wang, Y.; Polavarapu, L.; Liz-Marzán, L.M. Reduced graphene oxide-supported gold nanostars for improved SERS sensing and drug delivery. ACS Appl. Mater. Interfaces, 2014, 6(24), 21798-21805.
[http://dx.doi.org/10.1021/am501382y] [PMID: 24827538]
[87]
Song, J.; Yang, X.; Jacobson, O.; Lin, L.; Huang, P.; Niu, G.; Ma, Q.; Chen, X. Sequential drug release and enhanced photothermal and photoacoustic effect of hybrid reduced graphene oxide-loaded ultrasmall gold nanorod vesicles for cancer therapy. ACS Nano, 2015, 9(9), 9199-9209.
[http://dx.doi.org/10.1021/acsnano.5b03804] [PMID: 26308265]
[88]
Chen, H.; Wang, Z.; Zong, S.; Wu, L.; Chen, P.; Zhu, D.; Wang, C.; Xu, S.; Cui, Y. SERS-fluorescence monitored drug release of a redox-responsive nanocarrier based on graphene oxide in tumor cells. ACS Appl. Mater. Interfaces, 2014, 6(20), 17526-17533.
[http://dx.doi.org/10.1021/am505160v] [PMID: 25272041]
[89]
Shi, J.; Wang, L.; Zhang, J.; Ma, R.; Gao, J.; Liu, Y.; Zhang, C.; Zhang, Z. A tumor-targeting near-infrared laser-triggered drug delivery system based on GO@Ag nanoparticles for chemo-photothermal therapy and X-ray imaging. Biomaterials, 2014, 35(22), 5847-5861.
[http://dx.doi.org/10.1016/j.biomaterials.2014.03.042] [PMID: 24746963]
[90]
Ma, X.; Qu, Q.; Zhao, Y.; Luo, Z.; Zhao, Y.; Ng, K.W.; Zhao, Y. Graphene oxide wrapped gold nanoparticles for intracellular Raman imaging and drug delivery. J. Mater. Chem. B Mater. Biol. Med., 2013, 1(47), 6495-6500.
[http://dx.doi.org/10.1039/c3tb21385d]
[91]
Yang, X.; Wang, Y.; Huang, X.; Ma, Y.; Huang, Y.; Yang, R.; Duan, H.; Chen, Y. Multi-functionalized graphene oxide based anticancer drug-carrier with dual-targeting function and pH-sensitivity. J. Mater. Chem., 2011, 21(10), 3448-3454.
[http://dx.doi.org/10.1039/C0JM02494E]
[92]
Mo, R.; Jiang, T.; Sun, W.; Gu, Z. ATP-responsive DNA-graphene hybrid nanoaggregates for anticancer drug delivery. Biomaterials, 2015, 50, 67-74.
[http://dx.doi.org/10.1016/j.biomaterials.2015.01.053] [PMID: 25736497]
[93]
Wu, J.; Chen, A.; Qin, M.; Huang, R.; Zhang, G.; Xue, B.; Wei, J.; Li, Y.; Cao, Y.; Wang, W. Hierarchical construction of a mechanically stable peptide-graphene oxide hybrid hydrogel for drug delivery and pulsatile triggered release in vivo. Nanoscale, 2015, 7(5), 1655-1660.
[http://dx.doi.org/10.1039/C4NR05798H] [PMID: 25559308]
[94]
Wang, H.; Gu, W.; Xiao, N.; Ye, L.; Xu, Q. Chlorotoxin-conjugated graphene oxide for targeted delivery of an anticancer drug. Int. J. Nanomedicine, 2014, 9, 1433-1442.
[http://dx.doi.org/10.2147/IJN.S58783] [PMID: 24672236]
[95]
Hu, S.H.; Fang, R.H.; Chen, Y.W.; Liao, B.J.; Chen, I.W.; Chen, S.Y. Photoresponsive protein–graphene–protein hybrid capsules with dual targeted heat‐triggered drug delivery approach for enhanced tumor therapy. Adv. Funct. Mater., 2014, 24(26), 4144-4155.
[http://dx.doi.org/10.1002/adfm.201400080]
[96]
Rana, V.K.; Choi, M.C.; Kong, J.Y.; Kim, G.Y.; Kim, M.J.; Kim, S.H.; Mishra, S.; Singh, R.P.; Ha, C.S. Synthesis and drug‐delivery behavior of chitosan‐functionalized graphene oxide hybrid nanosheets. Macromol. Mater. Eng., 2011, 296(2), 131-140.
[http://dx.doi.org/10.1002/mame.201000307]
[97]
Riley, M.K.; Vermerris, W. Recent advances in nanomaterials for gene delivery-a review. Nanomaterials (Basel), 2017, 7(5), 94.
[http://dx.doi.org/10.3390/nano7050094] [PMID: 28452950]
[98]
Yang, Z.R.; Wang, H.F.; Zhao, J.; Peng, Y.Y.; Wang, J.; Guinn, B.A.; Huang, L.Q. Recent developments in the use of adenoviruses and immunotoxins in cancer gene therapy. Cancer Gene Ther., 2007, 14(7), 599-615.
[http://dx.doi.org/10.1038/sj.cgt.7701054] [PMID: 17479105]
[99]
Mintzer, M.A.; Simanek, E.E. Nonviral vectors for gene delivery. Chem. Rev., 2009, 109(2), 259-302.
[http://dx.doi.org/10.1021/cr800409e] [PMID: 19053809]
[100]
Whitehead, K.A.; Langer, R.; Anderson, D.G. Knocking down barriers: advances in siRNA delivery. Nat. Rev. Drug Discov., 2009, 8(2), 129-138.
[http://dx.doi.org/10.1038/nrd2742] [PMID: 19180106]
[101]
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(21), 7736-7741.
[http://dx.doi.org/10.1039/c1jm10341e]
[102]
Feng, L.; Zhang, S.; Liu, Z. Graphene based gene transfection. Nanoscale, 2011, 3(3), 1252-1257.
[http://dx.doi.org/10.1039/c0nr00680g] [PMID: 21270989]
[103]
Sun, Y.; Zhou, J.; Cheng, Q.; Lin, D.; Jiang, Q.; Dong, A.; Liang, Z.; Deng, L. Fabrication of mPEGylated graphene oxide/poly (2‐dimethyl aminoethyl methacrylate) nanohybrids and their primary application for small interfering RNA delivery. J. Appl. Polym. Sci., 2016, 133(16)
[http://dx.doi.org/10.1002/app.43303]
[104]
Liu, X.; Ma, D.; Tang, H.; Tan, L.; Xie, Q.; Zhang, Y.; Ma, M.; Yao, S. Polyamidoamine dendrimer and oleic acid-functionalized graphene as biocompatible and efficient gene delivery vectors. ACS Appl. Mater. Interfaces, 2014, 6(11), 8173-8183.
[http://dx.doi.org/10.1021/am500812h] [PMID: 24836601]
[105]
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(24), 6534-6542.
[http://dx.doi.org/10.1016/j.biomaterials.2014.04.057] [PMID: 24811259]
[106]
Bao, H.; Pan, Y.; Ping, Y.; Sahoo, N.G.; Wu, T.; Li, L.; Li, J.; Gan, L.H. Chitosan-functionalized graphene oxide as a nanocarrier for drug and gene delivery. Small, 2011, 7(11), 1569-1578.
[http://dx.doi.org/10.1002/smll.201100191] [PMID: 21538871]
[107]
Hu, H.; Tang, C.; Yin, C. Folate conjugated trimethyl chitosan/graphene oxide nanocomplexes as potential carriers for drug and gene delivery. Mater. Lett., 2014, 125, 82-85.
[http://dx.doi.org/10.1016/j.matlet.2014.03.133]
[108]
Li, H.; Fierens, K.; Zhang, Z.; Vanparijs, N.; Schuijs, M.J.; Van Steendam, K.; Feiner Gracia, N.; De Rycke, R.; De Beer, T.; De Beuckelaer, A.; De Koker, S.; Deforce, D.; Albertazzi, L.; Grooten, J.; Lambrecht, B.N.; De Geest, B.G. Spontaneous protein adsorption on graphene oxide nanosheets allowing efficient intracellular vaccine protein delivery. ACS Appl. Mater. Interfaces, 2016, 8(2), 1147-1155.
[http://dx.doi.org/10.1021/acsami.5b08963] [PMID: 26694764]
[109]
La, W.G.; Park, S.; Yoon, H.H.; Jeong, G.J.; Lee, T.J.; Bhang, S.H.; Han, J.Y.; Char, K.; Kim, B.S. Delivery of a therapeutic protein for bone regeneration from a substrate coated with graphene oxide. Small, 2013, 9(23), 4051-4060.
[http://dx.doi.org/10.1002/smll.201300571] [PMID: 23839958]
[110]
Choi, M.; Kim, K-G.; Heo, J.; Jeong, H.; Kim, S.Y.; Hong, J. Multilayered graphene nano-film for controlled protein delivery by desired electro-stimuli. Sci. Rep., 2015, 5, 17631.
[http://dx.doi.org/10.1038/srep17631] [PMID: 26621344]
[111]
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(11), 6317-6323.
[http://dx.doi.org/10.1021/am3019367] [PMID: 23106794]
[112]
Cao, X.; Zheng, S.; Zhang, S.; Wang, Y.; Yang, X.; Duan, H.; Huang, Y.; Chen, Y. Functionalized graphene oxide with hepatocyte targeting as anti-tumor drug and gene intracellular transporters. J. Nanosci. Nanotechnol., 2015, 15(3), 2052-2059.
[http://dx.doi.org/10.1166/jnn.2015.9145] [PMID: 26413620]
[113]
Kang, P.; Wang, M.C.; Knapp, P.M.; Nam, S. Crumpled graphene photodetector with enhanced, strain-tunable, and wavelength-selective photoresponsivity. Adv. Mater., 2016, 28(23), 4639-4645.
[http://dx.doi.org/10.1002/adma.201600482] [PMID: 27061899]
[114]
Chang, H-Y.; Yang, S.; Lee, J.; Tao, L.; Hwang, W-S.; Jena, D.; Lu, N.; Akinwande, D. High-performance, highly bendable MoS2 transistors with high-k dielectrics for flexible low-power systems. ACS Nano, 2013, 7(6), 5446-5452.
[http://dx.doi.org/10.1021/nn401429w] [PMID: 23668386]
[115]
Akinwande, D.; Petrone, N.; Hone, J. Two-dimensional flexible nanoelectronics. Nat. Commun., 2014, 5, 5678.
[http://dx.doi.org/10.1038/ncomms6678] [PMID: 25517105]
[116]
Amani, M.; Lien, D-H.; Kiriya, D.; Xiao, J.; Azcatl, A.; Noh, J.; Madhvapathy, S.R.; Addou, R.; Kc, S.; Dubey, M.; Cho, K.; Wallace, R.M.; Lee, S.C.; He, J.H.; Ager, J.W., III; Zhang, X.; Yablonovitch, E.; Javey, A. Near-unity photoluminescence quantum yield in MoS2. Science, 2015, 350(6264), 1065-1068.
[http://dx.doi.org/10.1126/science.aad2114] [PMID: 26612948]
[117]
Choi, C.; Choi, M.K.; Liu, S.; Kim, M.S.; Park, O.K.; Im, C.; Kim, J.; Qin, X.; Lee, G.J.; Cho, K.W.; Kim, M.; Joh, E.; Lee, J.; Son, D.; Kwon, S.H.; Jeon, N.L.; Song, Y.M.; Lu, N.; Kim, D.H. Human eye-inspired soft optoelectronic device using high-density MoS2-graphene curved image sensor array. Nat. Commun., 2017, 8(1), 1664.
[http://dx.doi.org/10.1038/s41467-017-01824-6] [PMID: 29162854]
[118]
Beik, J.; Abed, Z.; Ghoreishi, F.S.; Hosseini-Nami, S.; Mehrzadi, S.; Shakeri-Zadeh, A.; Kamrava, S.K. Nanotechnology in hyperthermia cancer therapy: from fundamental principles to advanced applications. J. Control. Release, 2016, 235, 205-221.
[http://dx.doi.org/10.1016/j.jconrel.2016.05.062] [PMID: 27264551]
[119]
Dos Santos, M.S.C.; Gouvêa, A.L.; de Moura, L.D.; Paterno, L.G.; de Souza, P.E.N.; Bastos, A.P.; Damasceno, E.A.M.; Veiga-Souza, F.H.; de Azevedo, R.B.; Báo, S.N. Nanographene oxide-methylene blue as phototherapies platform for breast tumor ablation and metastasis prevention in a syngeneic orthotopic murine model. J. Nanobiotechnology, 2018, 16(1), 9.
[http://dx.doi.org/10.1186/s12951-018-0333-6] [PMID: 29382332]
[120]
Taratula, O.; Patel, M.; Schumann, C.; Naleway, M.A.; Pang, A.J.; He, H.; Taratula, O. Phthalocyanine-loaded graphene nanoplatform for imaging-guided combinatorial phototherapy. Int. J. Nanomedicine, 2015, 10, 2347-2362.
[http://dx.doi.org/10.2147/IJN.S81097] [PMID: 25848255]
[121]
Antoci, A.; Galeotti, M.; Sordi, S. Environmental pollution as engine of industrialization. Commun. Nonlinear Sci. Numer. Simul., 2018, 58, 262-273.
[http://dx.doi.org/10.1016/j.cnsns.2017.06.016]
[122]
Xu, C.; Zhu, J.; Yuan, R.; Fu, X. More effective use of graphene in photocatalysis by conformal attachment of small sheets to TiO2 spheres. Carbon, 2016, 96, 394-402.
[http://dx.doi.org/10.1016/j.carbon.2015.09.088]
[123]
Peng, W.; Li, H.; Liu, Y.; Song, S. A review on heavy metal ions adsorption from water by graphene oxide and its composites. J. Mol. Liq., 2017, 230, 496-504.
[http://dx.doi.org/10.1016/j.molliq.2017.01.064]
[124]
Huang, Z-H.; Zheng, X.; Lv, W.; Wang, M.; Yang, Q-H.; Kang, F. Adsorption of lead(II) ions from aqueous solution on low-temperature exfoliated graphene nanosheets. Langmuir, 2011, 27(12), 7558-7562.
[http://dx.doi.org/10.1021/la200606r] [PMID: 21591809]
[125]
Chandra, V.; Kim, K.S. Highly selective adsorption of Hg2+ by a polypyrrole-reduced graphene oxide composite. Chem. Commun. (Camb.), 2011, 47(13), 3942-3944.
[http://dx.doi.org/10.1039/c1cc00005e] [PMID: 21350767]
[126]
Wan, W.; Zhang, R.; Li, W.; Liu, H.; Lin, Y.; Li, L.; Zhou, Y. Graphene-carbon nanotube aerogel as an ultra-light, compressible and recyclable highly efficient absorbent for oil and dyes. Environ. Sci. Nano, 2016, 3(1), 107-113.
[http://dx.doi.org/10.1039/C5EN00125K]
[127]
Liu, J.; Liu, L.; Bai, H.; Wang, Y.; Sun, D.D. Gram-scale production of graphene oxide-TiO2 nanorod composites: towards high-activity photocatalytic materials. Appl. Catal. B, 2011, 106(1), 76-82.
[http://dx.doi.org/10.1016/j.apcatb.2011.05.007]
[128]
Akhavan, O.; Ghaderi, E. Photocatalytic reduction of graphene oxide nanosheets on TiO2 thin film for photoinactivation of bacteria in solar light irradiation. J. Phys. Chem. C, 2009, 113(47), 20214-20220.
[http://dx.doi.org/10.1021/jp906325q]
[129]
Akhavan, O.; Choobtashani, M.; Ghaderi, E. Protein degradation and RNA efflux of viruses photocatalyzed by graphene–tungsten oxide composite under visible light irradiation. J. Phys. Chem. C, 2012, 116(17), 9653-9659.
[http://dx.doi.org/10.1021/jp301707m]