Issue

Vol. 11 (2019)

Comprehensive Application of Graphene: Emphasis on Biomedical Concerns

https://doi.org/10.1007/s40820-019-0237-5
S. Syama
Toxicology Division, Biomedical Technology Wing, Sree Chitra Tirunal Institute for Medical Sciences and Technology, Thiruvananthapuram, Kerala 695 012, India
P. V. Mohanan
Toxicology Division, Biomedical Technology Wing, Sree Chitra Tirunal Institute for Medical Sciences and Technology, Thiruvananthapuram, Kerala 695 012, India

Corresponding Author: P. V. Mohanan

mohanpv10@gmail.com

Nano-Micro Letters, Vol. 11 (2019), Article Number: 6

Abstract

Graphene, sp2 hybridized carbon framework of one atom thickness, is reputed as the strongest material to date. It has marked its impact in manifold applications including electronics, sensors, composites, and catalysis. Current state-of-the-art graphene research revolves around its biomedical applications. The two-dimensional (2D) planar structure of graphene provides a large surface area for loading drugs/biomolecules and the possibility of conjugating fluorescent dyes for bioimaging. The high near-infrared absorbance makes graphene ideal for photothermal therapy. Henceforth, graphene turns out to be a reliable multifunctional material for use in diagnosis and treatment. It exhibits antibacterial property by directly interacting with the cell membrane. Potential application of graphene as a scaffold for the attachment and proliferation of stem cells and neuronal cells is captivating in a tissue regeneration scenario. Fabrication of 2D graphene into a 3D structure is made possible with the help of 3D printing, a revolutionary technology having promising applications in tissue and organ engineering. However, apart from its advantageous application scope, use of graphene raises toxicity concerns. Several reports have confirmed the potential toxicity of graphene and its derivatives, and the inconsistency may be due to the lack of standardized consensus protocols. The present review focuses on the hidden facts of graphene and its biomedical application, with special emphasis on drug delivery, biosensing, bioimaging, antibacterial, tissue engineering, and 3D printing applications.


Highlights:


1 The introduction of graphene will certainly uncover new advanced materials, and many more future technologies will become realistic in the forthcoming years.
2 The present review article includes more recent publications about the biomedical application and cellular interaction of graphene. It is also updated with modern approaches such as use of graphene inks for 3D printing application.
3 Moreover, the importance of protein corona in modulating the cellular interaction, which was overlooked in previous review publications, is also included in this article.
4 The possible biological outcomes and toxicity when graphene is exposed to living organisms at the cellular and organ level are explained.

Keywords

Graphene Biomedical Bioprinting Toxicity Photothermal therapy
Syama, S., and P. V. Mohanan. 2019. “Comprehensive Application of Graphene: Emphasis on Biomedical Concerns”. Nano-Micro Letters 11 (January):6. https://doi.org/10.1007/s40820-019-0237-5.
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References
  1. J. Liu, L. Cui, D. Losic, Graphene and graphene oxide as new nanocarriers for drug delivery applications. Acta Biomater 9(12), 9243–9257 (2013). https://doi.org/10.1016/j.actbio.2013.08.016
  2. A. Lerf, J. Buchsteiner, J. Pieper, S. Schöttl, I. Dekany, T. Szabo, H.P. Boehm, Hydration behavior and dynamics of water molecules in graphite oxide. J. Phys. Chem. Solids 67(5–6), 1106–1110 (2006). https://doi.org/10.1016/j.jpcs.2006.01.031
  3. A. Buchsteiner, A. Lerf, J. Pieper, Water dynamics in graphite oxide investigated with neutron scattering. J. Phys. Chem. B 110(45), 22328–22338 (2006). https://doi.org/10.1021/jp0641132
  4. K.P. Loh, Q. Bao, G. Eda, M. Chhowalla, Graphene oxide as a chemically tunable platform for optical applications. Nat. Chem. 2(12), 1015–1024 (2010). https://doi.org/10.1038/nchem.907
  5. M. Konios, M. Stylianakis, E. Stratakis, E. Kymakis, Dispersion behaviour of graphene oxide and reduced graphene oxide. J. Colloid Interface Sci. 430, 108–112 (2014). https://doi.org/10.1016/j.jcis.2014.05.033
  6. S. Stankovich, D.A. Dikin, R.D. Piner, K.A. Kohlhaas, A. Kleinhammes, Y. Jia, Y. Wu, S.T. Nguyen, R.S. Ruoff, Synthesis of graphene-based nanosheets via chemical reduction of exfoliated graphite oxide. Carbon 45(7), 1558–1565 (2007). https://doi.org/10.1016/j.carbon.2007.02.034
  7. G. Wang, J. Yang, J. Park, X. Gou, B. Wang, H. Liu, J. Yao, Facile synthesis and characterization of graphene nanosheets. J. Phys. Chem. C 112(22), 8192–8195 (2008). https://doi.org/10.1021/jp710931h
  8. M.J. Fernández-Merino, L. Guardia, J.I. Paredes, S. Villar-Rodil, P. Solís-Fernández, A. Martínez-Alonso, J.M.D. Tascón, Vitamin C is an ideal substitute for hydrazine in the reduction of graphene oxide suspensions. J. Phys. Chem. C 114(14), 6426–6432 (2010). https://doi.org/10.1021/jp100603h
  9. H.J. Shin, K.K. Sim, A. Benayad, S.M. Yoon, H.K. Park et al., Efficient reduction of graphite oxide by sodium borohydride and its effect on electrical conductance. Adv. Funct. Mater. 19(12), 1987–1992 (2009). https://doi.org/10.1002/adfm.200900167
  10. X. Fan, W. Peng, Y. Li, X. Li, S. Wang, G. Zhang, F. Zhang, Deoxygenation of exfoliated graphite oxide under alkaline conditions: a green route to graphene preparation. Adv. Mater. 20(23), 4490–4493 (2008). https://doi.org/10.1002/adma.200801306
  11. H.P. Boehm, A. Clauss, G.O. Fischer, U.Z. Hofmann, The adsorption behavior of very thin carbon films. Anorg. Allg. Chem. 316, 119–127 (1962). https://doi.org/10.1002/zaac.19623160303
  12. K.S. Novoselov, A.K. Geim, S.V. Morozov, D. Jiang, Y. Zhang, S.V. Dubonos, I.V. Grigorieva, A.A. Firsov, Electric field effect in atomically thin carbon films. Science 306(5696), 666–669 (2004). https://doi.org/10.1126/science.1102896
  13. W.S. Hummers, R.E. Offeman, Preparation of graphitic oxide. J. Am. Chem. Soc. 80(6), 1339 (1958). https://doi.org/10.1021/ja01539a017
  14. K.R. Koch, Oxidation by Mn207: an impressive demonstration of the powerful oxidizing property of dimanganeseheptoxide. J. Chem. Educ. 59(11), 973 (1982). https://doi.org/10.1021/ed059p973.3
  15. B.C. Brodie, On the atomic weight of graphite. Proc. R. Soc. Lond. 10, 11–12 (1859)
  16. V. Kampars, M. Legzdina, Thermal deoxygenation of graphite oxide at low temperature. IOP Conf. Ser. Mater. Sci. Eng. 77, 012033 (2015). https://doi.org/10.1088/1757-899X/77/1/012033
  17. D.C. Marcano, D.V. Kosynkin, J.M. Berlin, A. Sinitskii, Z. Sun, A. Slesarev, L.B. Alemany, W. Lu, J.M. Tour, Improved synthesis of graphene oxide. ACS Nano 4(8), 4806–4814 (2010). https://doi.org/10.1021/nn1006368
  18. D.R. Dreyer, S. Park, C.W. Bielawski, R.S. Ruoff, The chemistry of graphene oxide. Chem. Soc. Rev. 39(1), 228–240 (2010). https://doi.org/10.1039/B917103G
  19. M.S. Khan, A. Shakoor, G.T. Khan, S. Sultana, A. Zia, A study of stable graphene oxide dispersions in various solvents. J. Chem. Soc. Pak. 37(01), 62–67 (2015)
  20. J. Paredes, S. Villar-Rodil, A. Martínez-Alonso, J. Tascón, Graphene oxide dispersions in organic solvents. Langmuir 24(19), 10560–10564 (2008). https://doi.org/10.1021/la801744a
  21. T.Y. Zhang, D. Zhang, Aqueous colloids of graphene oxide nanosheets by exfoliation of graphite oxide without ultrasonication. Bull. Mater. Sci. 34(1), 25–28 (2011). https://doi.org/10.1007/s12034-011-0048-x
  22. G. Gonçalves, M. Vila, I. Bdikin, A. de Andrés, N. Emami, R.A. Ferreira, L.D. Carlos, J. Gracio, P.A. Marques, Breakdown into nanoscale of graphene oxide: confined hot spot atomic reduction and fragmentation. Sci. Rep. 4, 6735 (2014). https://doi.org/10.1038/srep06735
  23. Z.S. Wu, W. Ren, L. Ago, B. Liu, C. Jiang, H.M. Cheng, Synthesis of high-quality graphene with a pre-determined number of layers. Carbon 47(2), 493–499 (2009). https://doi.org/10.1016/j.carbon.2008.10.031
  24. M. McAllister, J. Li, D. Adamson, H. Schniepp, H. Abdala et al., Single sheet functionalized graphene by oxidation and thermal expansion of graphite. Chem. Mater. 19(18), 4396–4404 (2007). https://doi.org/10.1021/cm0630800
  25. M. Zhou, Y. Wang, Y. Zhai, J. Zhai, W. Ren, F. Wang, S. Dong, Controlled synthesis of large-area and patterned electrochemically reduced graphene oxide films. Chemistry 15(25), 6116–6120 (2009). https://doi.org/10.1002/chem.200900596
  26. A. Kumar, C.H. Lee, in Advances in Graphene Science, ed. by M. Aliofkhazraei (InTech, Croatia, 2013), pp. 55–75
  27. J. Gao, F. Lui, Y. Lui, N. Ma, Z. Wang, X. Zhang, Environment-friendly method to produce graphene that employs Vitamin C and amino acid. Chem. Mater. 22(7), 2213–2218 (2010). https://doi.org/10.1021/cm902635j
  28. O. Akhavan, M. Kalaee, Z.S. Alavi, S.M.A. Ghiasi, A. Esfandiar, Increasing the antioxidant activity of green tea polyphenols in the presence of iron for the reduction of graphene oxide. Carbon 50(8), 3015–3025 (2012). https://doi.org/10.1016/j.carbon.2012.02.087
  29. Y. Wang, Z. Shi, J. Yin, Facile synthesis of soluble graphene via a green reduction of graphene oxide in tea solution and its biocomposites. ACS Appl. Mater. Interface 3(4), 1127–1133 (2011). https://doi.org/10.1021/am1012613
  30. A. Esfandiar, O. Akhavan, A. Irajizad, Melatonin as a powerful bio-antioxidant for reduction of graphene oxide. J. Mater. Chem. 21(29), 10907–10914 (2011). https://doi.org/10.1039/c1jm10151j
  31. O. Akhavan, E. Ghaderi, S. Aghayee, Y. Fereydooni, A. Talebi, The use of a glucose-reduced graphene oxide suspension for photothermal cancer therapy. J. Mater. Chem. 22(27), 13773–13781 (2012). https://doi.org/10.1039/c2jm31396k
  32. C. Zhu, S. Guo, Y. Fang, S. Dong, Reducing sugar: new functional molecules for the green synthesis of graphene nanosheets. ACS Nano 4(4), 2429–2437 (2010). https://doi.org/10.1021/nn1002387
  33. J. Liu, S. Fu, B. Yuan, Y. Li, Z. Deng, Toward a universal “Adhesive Nanosheet” for the assembly of multiple nanoparticles based on a protein-induced reduction/decoration of graphene oxide. J. Am. Chem. Soc. 132(21), 7279–7281 (2010). https://doi.org/10.1021/ja100938r
  34. E.C. Salas, Z. Sun, A. Luttge, J.M. Tour, Reduction of graphene oxide via bacterial respiration. ACS Nano 4(8), 4852–4856 (2010). https://doi.org/10.1021/nn101081t
  35. S. Thakur, N. Karak, Green reduction of graphene oxide by aqueous phytoextracts. Carbon 50(14), 5331–5339 (2012). https://doi.org/10.1016/j.carbon.2012.07.023
  36. Y. Hong, Z. Wang, X. Jin, Sulfuric acid intercalated graphite oxide for graphene preparation. Sci. Rep. 3(1), 3439 (2013). https://doi.org/10.1038/srep03439
  37. O. Jankovský, P. Marvan, M. Nováček, J. Luxa, V. Mazánek, K. Klímová, D. Sedmidubský, Z. Sofer, Synthesis procedure and type of graphite oxide strongly influence resulting graphene properties. Appl. Mater. Today 4, 45–53 (2016). https://doi.org/10.1016/j.apmt.2016.06.001
  38. T.D. Dao, H.M. Jeong, Graphene prepared by thermal reduction–exfoliation of graphite oxide: effect of raw graphite particle size on the properties of graphite oxide and graphene. Mater. Res. Bull. 70, 651–657 (2015). https://doi.org/10.1016/j.materresbull.2015.05.038
  39. C.H.A. Wong, O. Jankovský, Z. Sofer, M. Pumera, Vacuum-assisted microwave reduction/exfoliation of graphite oxide and the influence of precursor graphite oxide. Carbon 77, 508–517 (2014). https://doi.org/10.1016/j.carbon.2014.05.056
  40. Z. Lin, Y. Yao, Z. Li, Y. Liu, Z. Li, C.P. Wong, Solvent-assisted thermal reduction of graphite oxide. J. Phys. Chem. C 114(35), 14819–14825 (2010). https://doi.org/10.1021/jp1049843
  41. B. Yuan, C. Bao, X. Qian, P. Wen, W. Xing, L. Song, Y. Hu, A facile approach to prepare graphene via solvothermal reduction of graphite oxide. Mater. Res. Bull. 55, 48–52 (2014). https://doi.org/10.1016/j.materresbull.2014.04.016
  42. D.R. Dreyer, S. Murali, Y. Zhu, R.S. Ruoff, C.W. Bielawski, Reduction of graphite oxide using alcohols. J. Mater. Chem. 21(10), 3443–3447 (2011). https://doi.org/10.1039/C0JM02704A
  43. C. Cai, N. Sang, Z. Shen, X. Zhao, Facile and size-controllable preparation of graphene oxide nanosheets using high shear method and ultrasonic method. J. Exp. Nanosci. 12(1), 247–262 (2017). https://doi.org/10.1080/17458080.2017.1303853
  44. N. Blomquist, A.C. Engstrom, M. Hummelgard, B. Andres, S. Frosberg, H. Olin, Large-scale production of nanographite by tube-shear exfoliation in water. PLoS ONE 11(4), e0154686 (2016). https://doi.org/10.1371/journal.pone.0154686
  45. X. Sun, Z. Liu, K. Welsher, J. Robinson, A. Goodwin, S. Zaric, H. Dai, Nano-graphene oxide for cellular imaging and drug delivery. Nano Res. 1(3), 203–212 (2008). https://doi.org/10.1007/s12274-008-8021-8
  46. Z. Liu, J.T. Robinson, X.M. Sun, H. Dai, PEGylated nanographene oxide for delivery of water-insoluble cancer drugs. J. Am. Chem. Soc. 130(33), 10876–10877 (2008). https://doi.org/10.1021/ja803688x
  47. X. Yang, X. Zhang, Z. Liu, Y. Ma, Y. Huang, Y. Chen, High-efficiency loading and controlled release of doxorubicin hydrochloride on graphene oxide. J. Phys. Chem. C 112(45), 17554–17558 (2008). https://doi.org/10.1021/jp806751k
  48. C.S. Wang, J.Y. Li, C. Amatore, Y. Chen, H. Jiang, X.M. Wang, Gold nanoclusters and graphene nanocomposites for drug delivery and imaging of cancer cells. Angew. Chem. Int. Ed. 50(49), 11644–11648 (2011). https://doi.org/10.1002/anie.201105573
  49. M. de Sousa, L.A. Visani de Luna, L. Fonseca, S. Giorgio, O.L. Alves, Folic acid-functionalized graphene oxide nanocarrier: synthetic approaches, characterization, drug delivery study and anti-tumor screening. ACS Appl. Nano Mater. 1(2), 922–932 (2018). https://doi.org/10.1021/acsanm.7b00324
  50. B. Saifullah, K. Buskaran, R.B. Shaikh, F. Barahuie, S. Fakurazi, M.A. Mohd Moklas, M.Z. Hussein, Graphene oxide–PEG–protocatechuic acid nanocomposite formulation with improved anticancer properties. Nanomaterials 8(10), 8100820 (2018). https://doi.org/10.3390/nano8100820
  51. L.M. Zhang, J. Xia, Q. Zhao, L. Liu, Z. Zhang, Functional graphene oxide as a nanocarrier for controlled loading and targeted delivery of mixed anticancer drugs. Small 6(4), 537–544 (2010). https://doi.org/10.1002/smll.200901680
  52. Y. Tang, H. Hu, M.G. Zhang, J. Song, L. Nie et al., An aptamer-targeting photoresponsive drug delivery system using “off–on” graphene oxide wrapped mesoporous silica nanoparticles. Nanoscale 7(14), 6304–6310 (2015). https://doi.org/10.1039/C4NR07493A
  53. L.Z. Feng, S. Zhang, Z. Liu, Graphene based gene transfection. Nanoscale 3(3), 1252–1257 (2011). https://doi.org/10.1039/c0nr00680g
  54. L. Zhang, Z. Lu, Q. Zhao, J. Huang, H. Shen, Z. Zhang, Enhanced chemotherapy efficacy by sequential delivery of siRNA and anticancer drugs using PEI-grafted graphene oxide. Small 7(4), 460–464 (2011). https://doi.org/10.1002/smll.201001522
  55. K. Yang, L. Feng, X. Shi, Z. Liu, Nano-graphene in biomedicine: theranostic applications. Chem. Soc. Rev. 42(2), 530–547 (2013). https://doi.org/10.1039/C2CS35342C
  56. A. Paul, A. Hasan, H.A. Kindi, A.K. Gaharwar, V.T. Rao et al., Injectable graphene oxide/hydrogel-based angiogenic gene delivery system for vasculogenesis and cardiac repair. ACS Nano 8(8), 8050–8062 (2014). https://doi.org/10.1021/nn5020787
  57. W.G. La, M. Jin, S. Park, H.H. Yoon, G.J. Jeong, S.H. Bhang, H. Park, K. Char, B.S. Kim, Delivery of bone morphogenetic protein-2 and substance P using graphene oxide for bone regeneration. Int. J. Nanomedicine 9(1), 107–116 (2014). https://doi.org/10.2147/IJN.S50742
  58. F. Emadi, A. Amini, A. Gholami, Y. Ghasemi, Functionalized graphene oxide with chitosan for protein nanocarriers to protect against enzymatic cleavage and retain collagenase activity. Sci. Rep. 10(7), 42258 (2017). https://doi.org/10.1038/srep42258
  59. Y. Liu, Y. Qi, C. Yin, S. Wang, S. Zhang, A. Xu, W. Chen, S. Liu, Bio-transformation of graphene oxide in lung fluids significantly enhances its photothermal efficacy. Nanotheranostics 2(3), 222–232 (2018). https://doi.org/10.7150/ntno.25719
  60. A.M. Jastrzębska, P. Kurtycz, A.R. Olszyna, Recent advances in graphene family materials toxicity investigations. J. Nanopart. Res. 14(12), 1320 (2012). https://doi.org/10.1007/s11051-012-1320-8
  61. K. Yang, S. Zhang, G. Zhang, X. Sun, S.T. Lee, Z. Liu, Graphene in mice: ultrahigh in vivo tumor uptake and efficient photothermal therapy. Nano Lett. 10(9), 3318–3323 (2010). https://doi.org/10.1021/nl100996u
  62. X. Shi, H. Gong, Y. Li, C. Wang, L. Cheng, Z. Liu, Graphene-based magnetic plasmonic nanocomposite for dual bioimaging and photothermal therapy. Biomaterials 34(20), 4786–4793 (2013). https://doi.org/10.1016/j.biomaterials.2013.03.023
  63. J.L. Li, X.L. Hou, H.C. Bao, L. Sun, B. Tang, J.F. Wang, X.G. Wang, M. Gu, Graphene oxide nanoparticles for enhanced photothermal cancer cell therapy under the irradiation of a femtosecond laser beam. J. Biomed. Mater. Res. A 102(7), 2181–2188 (2014). https://doi.org/10.1002/jbm.a.34871
  64. X. Zhang, X. Nan, W. Shi, Y. Sun, H. Su, Y. He, X. Liu, Z. Zhang, D. Ge, Polydopamine-functionalized nanographene oxide: a versatile nanocarrier for chemotherapy and photothermal therapy. Nanotechnology 28(29), 295102 (2017). https://doi.org/10.1088/1361-6528/aa761b
  65. Y.A. Cheon, J.H. Bae, B.G. Chung, Reduced graphene oxide nanosheet for chemo-photothermal therapy. Langmuir 32(11), 2731–2736 (2016). https://doi.org/10.1021/acs.langmuir.6b00315
  66. P. Huang, C. Xu, J. Lin, C. Wang, X. Wang, C. Zhang, X. Zhou, S. Guo, D. Cui, Folic acid-conjugated graphene oxide loaded with photosensitizers for targeting photodynamic therapy. Theranostics 1, 240–250 (2011). https://doi.org/10.7150/thno/v01p0240
  67. S. Su, J. Wang, J. Wei, R. Martínez-Zaguilán, J. Qiu, S. Wang, Efficient photothermal therapy of brain cancer through porphyrin functionalized graphene oxide. New J. Chem. 39(7), 5743–5749 (2015). https://doi.org/10.1039/C5NJ00122F
  68. P. Rong, K. Yang, A. Srivastan, D.O. Kiesewetter, X. Yue et al., Photosensitizer loaded nano-graphene for multimodality imaging guided tumor photodynamic therapy. Theranostics 4(3), 229–239 (2014). https://doi.org/10.7150/thno.8070
  69. Y.W. Chen, Y.L. Su, S.H. Hu, S.Y. Chen, Functionalized graphene nanocomposites for enhancing photothermal therapy in tumor treatment. Adv. Drug Deliv. Rev. 105(Pt B), 190–204 (2016). https://doi.org/10.1016/j.addr.2016.05.022
  70. I. Ocsoy, N. Isiklan, S. Cansiz, N. Ozdemir, W. Tan, ICG-Conjugated magnetic graphene oxide for dual photothermal and photodynamic therapy. RSC Adv. 6(36), 30285–30292 (2016). https://doi.org/10.1039/C6RA06798K
  71. M.S.C. dos Santos, A.L. Gouvêa, L.D. de Moura, L.G. Paterno, P.E.N. de Souza et al., Nanographene oxide-methylene blue as phototherapies platform for breast tumor ablation and metastasis prevention in a syngeneic orthotopic murine model. J. Nanobiotechnology 16(9), 29382332 (2018). https://doi.org/10.1186/s12951-018-0333-6
  72. Q. Li, L. Hong, H. Li, C. Liu, Graphene oxide-fullerene C60 (GO-C60) hybrid for photodynamic and photothermal therapy triggered by near-infrared light. Biosens. Bioelectron. 89(1), 477–482 (2017). https://doi.org/10.1016/j.bios.2016.03.072
  73. D.Y. Zhang, Y. Zhang, C.P. Tan, J.H. Sun, W. Zhang, L.N. Ji, Z.W. Mao, Graphene oxide decorated with Ru(II)–polyethylene glycol complex for lysosome-targeted imaging and photodynamic/photothermal therapy. ACS Appl. Mater. Interfaces 9(8), 6761–6771 (2017). https://doi.org/10.1021/acsami.6b13808
  74. J.H. Lim, D.E. Kim, E.J. Kim, C.D. Ahrberg, B.G. Chung, Functional graphene oxide-based nanosheets for photothermal therapy. Macromol. Res. 26(6), 557–565 (2018). https://doi.org/10.1007/s13233-018-6067-3
  75. Y. Jang, S. Kim, S. Lee, C.M. Yoon, I. Lee, J. Jang, Graphene oxide wrapped SiO2/TiO2 hollow nanoparticles loaded with photosensitizer for photothermal and photodynamic combination therapy. Chem. Eur. J. 23, 3719–3727 (2017). https://doi.org/10.1002/chem.201605112
  76. A. Gulzar, J. Xu, D. Yang, L. Xu, F. He, S. Gai, P. Yang, Nano-graphene oxide-UCNP-Ce6 covalently constructed nanocomposites for NIR-mediated bioimaging and PTT/PDT combinatorial therapy. Dalton Trans. 47(11), 3931–3939 (2018). https://doi.org/10.1039/C7DT04141A
  77. X. Yan, G. Niu, J. Lin, A.J. Jin, H. Hu et al., Enhanced fluorescence imaging guided photodynamic therapy of sinoporphyrin sodium loaded graphene oxide. Biomaterials 42, 94–102 (2015). https://doi.org/10.1016/j.biomaterials.2014.11.040
  78. P. Huang, S. Wang, X. Wang, G. Shen, J. Lin et al., Surface functionalization of chemically reduced graphene oxide for targeted photodynamic therapy. J. Biomed. Nanotechnol. 11(1), 117–125 (2015). https://doi.org/10.1166/jbn.2015.2055
  79. Y. Wei, F. Zhou, D. Zhang, Q. Chen, D. Xing, A graphene oxide based smart drug delivery system for tumor mitochondria-targeting photodynamic therapy. Nanoscale 8(6), 3530–3538 (2016). https://doi.org/10.1039/C5NR07785K
  80. L. Hou, Y. Shi, G. Jiang, W. Liu, H. Han et al., Smart nanocomposite hydrogels based on azo crosslinked graphene oxide for oral colon-specific drug delivery. Nanotechnology 27(31), 315105 (2016). https://doi.org/10.1088/0957-4484/27/31/315105
  81. Z. Xu, S. Wang, Y. Li, M. Wang, P. Shi, X. Huang, Covalent functionalization of graphene oxide with biocompatible poly(ethylene glycol) for delivery of paclitaxel. ACS Appl. Mater. Interfaces 6(19), 17268–17276 (2014). https://doi.org/10.1021/am505308f
  82. H. Hu, J. Yu, Y. Li, J. Zhao, H. Dong, Engineering of a novel pluronic F127/graphene nanohybrid for pH responsive drug delivery. J. Biomed. Mater. Res. A 100(1), 141–148 (2012). https://doi.org/10.1002/jbm.a.33252
  83. H. Bao, Y. Pan, Y. Ping, N.G. Sahoo, T. Wu, L. Li, J. Li, L.H. Gan, Chitosan-functionalized graphene oxide as a nanocarrier for drug and gene delivery. Small 7(11), 1569–1578 (2011). https://doi.org/10.1002/smll.201100191
  84. M. Alibolandi, M. Mohammadi, S.M. Taghdisi, M. Ramezani, K. Abnous, Fabrication of aptamer decorated dextran coated nano-graphene oxide for targeted drug delivery. Carbohydr. Polym. 155, 218–229 (2017). https://doi.org/10.1016/j.carbpol.2016.08.046
  85. C. Wang, J. Li, C. Amatore, Y. Chen, H. Jiang, X.M. Wang, Gold nanoclusters and graphene nanocomposites for drug delivery and imaging of cancer cells. Angew. Chem. Int. Ed. 50(49), 11644–11648 (2011). https://doi.org/10.1002/anie.201105573
  86. X. Wang, X. Sun, J. Lao, H. He, T. Cheng, M. Wang, S. Wang, F. Huang, Multifunctional graphene quantum dots for simultaneous targeted cellular imaging and drug delivery. Colloids Surf. B 122, 638–644 (2014). https://doi.org/10.1016/j.colsurfb.2014.07.043
  87. G. Russel-Jones, K. McTavish, J. McEvan, J. Rice, D. Nowotnik, Vitamin-mediated targeting as a potential mechanism to increase drug uptake by tumors. J. Inorg. Biochem. 98(10), 1625–1633 (2004). https://doi.org/10.1016/j.jinorgbio.2004.07.009
  88. N.R. Ko, M. Nafiujjaman, J.S. Lee, H.N. Lim, Y.K. Lee, I.K. Kwon, Graphene quantum dot-based theranostic agents for active targeting of breast cancer. RSC Adv. 7(19), 11420–11427 (2017). https://doi.org/10.1039/C6RA25949A
  89. A. Jafarizad, A. Aghanejad, M. Sevim, Ö. Metin, J. Barar, Y. Omidi, D. Ekinci, Gold nanoparticles and reduced graphene oxide-gold nanoparticle composite materials as covalent drug delivery systems for breast cancer treatment. Chem. Sel. 2(23), 6663–6672 (2017). https://doi.org/10.1002/slct.201701178
  90. S.J. Zhen, T.T. Wang, Y.X. Liu, Z.L. Wu, H.Y. Zou, C.Z. Huang, Reduced graphene oxide coated Cu2−xSe nanoparticles for targeted chemo-photothermal therapy. J. Photochem. Photobiol., B 180, 9–16 (2018). https://doi.org/10.1016/j.jphotobiol.2018.01.020
  91. Y. Hu, D. Sun, J. Ding, L. Chen, X. Chen, Decorated reduced graphene oxide for photo-chemotherapy. J. Mater. Chem. B 4, 929–937 (2016). https://doi.org/10.1039/C5TB02359A
  92. G. Shim, J.Y. Kim, J. Han, S.W. Chung, S. Lee, Y. Byun, Y.K. Oh, Reduced graphene oxide nanosheets coated with an anti-angiogenic anticancer low-molecular-weight heparin derivative for delivery of anticancer drugs. J. Control. Release 189, 80–89 (2014). https://doi.org/10.1016/j.jconrel.2014.06.026
  93. W. Miao, G. Shim, S. Lee, Y.S. Choe, Y.K. Oh, Safety and tumor tissue accumulation of pegylated graphene oxide nanosheets for co-delivery of anticancer drug and photosensitizer. Biomaterials 34(13), 3402–3410 (2013). https://doi.org/10.1016/j.biomaterials.2013.01.010
  94. Y.J. Choi, S. Gurunathan, J.H. Kim, Graphene oxide–silver nanocomposite enhances cytotoxic and apoptotic potential of salinomycin in human ovarian cancer stem cells (OvCSCs): a novel approach for cancer therapy. Int. J. Mol. Sci. 19(3), 710 (2018). https://doi.org/10.3390/ijms19030710
  95. H. Shen, L. Zhang, M. Liu, Z. Zhang, Biomedical applications of graphene. Theranostics 2(3), 283–294 (2012). https://doi.org/10.7150/thno.3642
  96. O.S. Kwon, S.J. Park, J.Y. Hong, A.R. Han, J.S. Lee, J.S. Lee, J.H. Oh, J. Jang, Flexible FET-type VEGF aptasensor based on nitrogen-doped graphene converted from conducting polymer. ACS Nano 6(2), 1486–1493 (2012). https://doi.org/10.1021/nn204395n
  97. P. Suvarnaphaet, S. Pechprasarn, Graphene-based materials for biosensors: a Review. Sensors (Basel) 17(10), 2161 (2017). https://doi.org/10.3390/s17102161
  98. L.H. Hess, M. Jansen, V. Maybeck, M.V. Hauf, M. Seifert, M. Stutzmann, I.D. Sharp, A. Offenhausser, J. Garrido, Graphene transistor arrays for recording action potentials from electrogenic cells. Adv. Mater. 23, 5045–5049 (2011). https://doi.org/10.1002/adma.201102990
  99. C. Chung, Y.K. Kim, D. Shin, S.R. Ryoo, B.H. Hong, D.H. Min, Biomedical applications of graphene and graphene oxide. Acc. Chem. Res. 46(10), 2211–2224 (2013). https://doi.org/10.1021/ar300159f
  100. Y. Huang, X. Dong, Y. Liu, L.J. Li, P. Chen, Graphene-based biosensors for detection of bacteria and their metabolic activities. J. Mater. Chem. 21(33), 12358–12362 (2011). https://doi.org/10.1039/c1jm11436k
  101. F. Qu, T. Li, M. Yang, Colorimetric platform for visual detection of cancer biomarker based on intrinsic peroxidase activity of graphene oxide. Biosens. Bioelectron. 26(9), 3927–3931 (2011). https://doi.org/10.1016/j.bios.2011.03.013
  102. S.K. Lim, P. Chen, F.L. Lee, S. Moochhala, B. Liedberg, Peptide-assembled graphene oxide as a fluorescent turn-on sensor for lipopolysaccharide (endotoxin) detection. Anal. Chem. 87(18), 9408–9412 (2015). https://doi.org/10.1021/acs.analchem.5b02270
  103. L. Bai, Y. Chai, X. Pu, R. Yuan, A signal-on electrochemical aptasensor for ultrasensitive detection of endotoxin using three-way DNA junction-aided enzymatic recycling and graphene nanohybrid for amplification. Nanoscale 6(5), 2902–2908 (2014). https://doi.org/10.1039/c3nr05930h
  104. B. Jurado-Snchez, M. Pacheco, J. Rojo, A. Escarpa, Magnetocatalytic graphene quantum dots Janus micromotors for bacterial endotoxin detection. Angew. Chem. Int. Ed. 129(24), 7061–7065 (2017). https://doi.org/10.1002/ange.201701396
  105. S.J. Cheng, H.Y. Chiu, P.V. Kumar, K.Y. Hsieh, J.W. Yang, Y.-R. Lin, Y.C. Shen, G.Y. Chen, Simultaneous drug delivery and cellular imaging using graphene oxide. Biomater. Sci. 6(4), 813–819 (2018). https://doi.org/10.1039/C7BM01192J
  106. S. Jin, D. Kim, G. Jun, S. Hong, S. Jeon, Tuning the photoluminescence of graphene quantum dots through the charge transfer effect of functional groups. ACS Nano 7(2), 1239–1245 (2013). https://doi.org/10.1021/nn304675g
  107. J. Shen, Y. Zhu, C. Chen, X. Yang, C. Li, Facile preparation and upconversion luminescence of graphene quantum dots. Chem. Commun. 47(9), 2580–2582 (2011). https://doi.org/10.1039/C0CC04812G
  108. Y. Wang, Z. Li, D. Hu, C.T. Lin, J. Li, Y. Lin, Aptamer/graphene oxide nanocomplex for in situ molecular probing in living cells. J. Am. Chem. Soc. 132(27), 9274–9276 (2010). https://doi.org/10.1021/ja103169v
  109. W. Chen, P. Yi, Y. Zhang, L. Zhang, Z. Deng, Z. Zhang, Composites of aminodextran-coated Fe3O4 nanoparticles and graphene oxide for cellular magnetic resonance imaging. ACS Appl. Mater. Interfaces 3(10), 4085–4091 (2011). https://doi.org/10.1021/am2009647
  110. O. Akhavan, E. Ghaderi, Toxicity of graphene and graphene oxide nanowalls against bacteria. ACS Nano 4(10), 5731–5736 (2010). https://doi.org/10.1021/nn101390x
  111. S. Liu, T.H. Zeng, M. Hofmann, E. Burcombe, J. Wei, R. Jiang, J. Kong, Y. Chen, Antibacterial activity of graphite, graphite oxide, graphene oxide, and reduced graphene oxide: membrane and oxidative stress. ACS Nano 5(9), 6971–6980 (2011). https://doi.org/10.1021/nn202451x
  112. X. Guo, N. Mei, Assessment of the toxic potential of graphene family nanomaterials. J. Food Drug Anal. 22(1), 105–115 (2014). https://doi.org/10.1016/j.jfda.2014.01.009
  113. K. Krishnamoorthy, M. Veerapandian, L.H. Zhang, K. Yun, S.J. Kim, Antibacterial efficiency of graphene nanosheets against pathogenic bacteria via lipid peroxidation. J. Phys. Chem. C 116(32), 17280–17287 (2012). https://doi.org/10.1021/jp3047054
  114. I. Zarafu, I. Turcu, D.C. Culită, S. Petrescu, M. Popa, M.C. Chifiriuc, C. Limban, A. Telehoiu, P. Ionit, Antimicrobial features of organic functionalized graphene-oxide with selected amines. Materials 11(9), 1704 (2018). https://doi.org/10.3390/ma11091704
  115. M. Cao, W. Zhao, L. Wang, R. Li, H. Gong, Y. Zhang, H. Xu, J.R. Lu, Graphene oxide-assisted accumulation and layer-by-layer assembly of antibacterial peptide for sustained release applications. ACS Appl. Mater. Interfaces 10(29), 24937–24946 (2018). https://doi.org/10.1021/acsami.8b07417
  116. O.N. Ruiz, K.A.S. Fernando, B. Wang, N.A. Brown, P.G. Luo, N.D. McNamara, M. Vangsness, Y.P. Sun, C.E. Bunker, Graphene oxide: a nonspecific enhancer of cellular growth. ACS Nano 5(10), 8100–8107 (2011). https://doi.org/10.1021/nn202699t
  117. M.D. Giulio, R. Zappacosta, S.D. Lodovico, E.D. Campli, G. Siani, A. Fontana, L. Cellini, Antimicrobial and antibiofilm efficacy of graphene oxide against chronic wound microorganisms. Antimicrob. Agents Chemother. 62(7), e00547-18 (2018). https://doi.org/10.1128/AAC.00547-18
  118. H.E. Karahan, C. Wiraja, C. Xu, J. Wei, Y. Wang, L. Wang, F. Liu, Y. Chen, Graphene materials in antimicrobial nanomedicine: current status and future perspectives. Adv. Healthc. Mater. 7(13), 1701406 (2018). https://doi.org/10.1002/adhm.201701406
  119. M. Kalbacova, A. Broz, J. Kong, M. Kalbac, Graphene substrates promote adherence of human osteoblasts and mesenchymal stromal cells. Carbon 48(15), 4323–4329 (2010). https://doi.org/10.1016/j.carbon.2010.07.045
  120. S.R. Ryoo, Y.K. Kim, M.H. Kim, D.H. Min, Behaviors of NIH-3T3 fibroblasts on graphene/carbon nanotubes: proliferation, focal adhesion, and gene transfection studies. ACS Nano 4(11), 6587–6598 (2010). https://doi.org/10.1021/nn1018279
  121. C.X. Guo, X.T. Zheng, Z.S. Lu, X.W. Lou, C.M. Li, Biointerface by cell growth on layered graphene–artificial peroxidase–protein nanostructure for in situ quantitative molecular detection. Adv. Mater. 22(45), 5164–5167 (2010). https://doi.org/10.1002/adma.201001699
  122. W.C. Lee, C.H.Y.X. Lim, H. Shi, L.A.L. Tang, Y. Wang, C.T. Lim, K.P. Loh, Origin of enhanced stem cell growth and differentiation on graphene and graphene oxide. ACS Nano 5(9), 7334–7341 (2011). https://doi.org/10.1021/nn202190c
  123. N. Li, X. Zhang, Q. Song, R. Su, Q. Zhang, T. Kong, L. Liu, G. Jin, M. Tang, G. Cheng, The promotion of neurite sprouting and outgrowth of mouse hippocampal cells in culture by graphene substrates. Biomaterials 32(35), 9374–9382 (2011). https://doi.org/10.1016/j.biomaterials.2011.08.065
  124. S. Sayyar, E. Murray, B. Thompson, S. Gambhir, D. Officer, G. Wallace, Covalently linked biocompatible graphene/polycaprolactone composites for tissue engineering. Carbon 52, 296–304 (2013). https://doi.org/10.1016/j.carbon.2012.09.031
  125. H.L. Fan, L.L. Wang, K.K. Zhao, N. Li, Z.J. Shi, Z.G. Ge, Z.X. Jin, Fabrication, mechanical properties and biocompatibility of graphene-reinforced chitosan composites. Biomacromol 11(9), 2345–2351 (2010). https://doi.org/10.1021/bm100470q
  126. H.N. Lim, N.M. Huang, S.S. Lim, I. Harrison, C.H. Chia, Fabrication and characterization of graphene hydrogel via hydrothermal approach as a scaffold for preliminary study of cell growth. Int. J. Nanomedicine 6, 1817–1823 (2011). https://doi.org/10.2147/IJN.S23392
  127. G. Yang, J. Su, J. Gao, X. Hu, C. Geng, Q. Fu, Fabrication of well-controlled porous foams of graphene oxide modified poly(propylene-carbonate) using supercritical carbon dioxide and its potential tissue engineering applications. J. Supercrit. Fluids 73, 1–9 (2013). https://doi.org/10.1016/j.supflu.2012.11.004
  128. S. Shah, P.T. Yin, T.M. Uehara, S.D. Chueng, L. Yang, K. Lee, Guiding stem cell differentiation into oligodendrocytes using graphene-nanofiber hybrid scaffolds. Adv. Mater. 26(22), 3673–3680 (2014). https://doi.org/10.1002/adma.201400523
  129. S. Saravanan, N. Sareen, E. Abu-El-Rub, H. Ashour, G.L. Sequiera et al., Graphene oxide-gold nanosheets containing chitosan scaffold improves ventricular contractility and function after implantation into infarcted heart. Sci. Rep. 8, 15069 (2018). https://doi.org/10.1038/s41598-018-33144-0
  130. S.R. Shin, C.Z.M. Akbari, P. Assawes, L. Cheung, K. Zhang et al., Reduced graphene oxide-GelMA hybrid hydrogels as scaffolds for cardiac tissue engineering. Small 12(27), 3677–3689 (2016). https://doi.org/10.1002/smll.201600178
  131. G. Zhao, H. Qing, G. Huang, G.M. Genin, T.J. Lu, Z. Luo, F. Xu, X. Zhang, Reduced graphene oxide functionalized nanofibrous silk fibroin matrices for engineering excitable tissues. NPG Asia Mater. 10, 982–994 (2018). https://doi.org/10.1038/s41427-018-0092-8
  132. M.H. Norahan, M. Amroon, R. Ghahremanzadeh, M. Mahmoodi, N. Baheiraei, Electroactive graphene oxide-incorporated collagen assisting vascularization for cardiac tissue engineering. J. Biomed. Mater. Res. A 107A(1), 204–219 (2018). https://doi.org/10.1002/jbm.a.36555
  133. P. Hitscherich, A. Aphale, R. Gordan, R. Whitaker, P. Singh, L.H. Xie, P. Patra, E.J. Lee, Electroactive graphene composite scaffolds for cardiac tissue engineering. J. Biomed. Mater. Res. A 106(11), 2923–2933 (2018). https://doi.org/10.1002/jbm.a.36481
  134. S. Malik, F.M. Ruddock, A.H. Dowling, K. Byrne, W. Schmitt et al., Graphene composites with dental and biomedical applicability. Beilstein J. Nanotechnol. 9, 801–808 (2018). https://doi.org/10.3762/bjnano.9.73
  135. V. Rosa, H. Xie, N. Dubey, T.T. Madanagopal, S.S. Rajan, J.L.P. Morin, I. Islam, A.H.C. Neto, Graphene oxide-based substrate: physical and surface characterization, cytocompatibility and differentiation potential of dental pulp stem cells. Dent. Mater. 32, 1019–1025 (2016). https://doi.org/10.1016/j.dental.2016.05.008
  136. G.Y. Chen, D.W.P. Pang, S.M. Hwang, H.Y. Tuan, Y.C. Hu, A graphene-based platform for induced pluripotent stem cells culture and differentiation. Biomaterials 33(2), 418–427 (2012). https://doi.org/10.1016/j.biomaterials.2011.09.071
  137. A.E. Jakus, E.B. Secor, A.L. Rutz, S.W. Jordan, M.C. Hersam, R.N. Shah, Three-dimensional printing of high-content graphene scaffolds for electronic and biomedical applications. ACS Nano 9(4), 4636–4648 (2015). https://doi.org/10.1021/acsnano.5b01179
  138. Q. Chen, J.D. Mangadlao, J. Wallat, A.D. Leon, J.K. Pokorski, R.C. Advincula, 3D printing biocompatible polyurethane/poly(lactic acid)/graphene oxide nanocomposites: anisotropic properties. ACS Appl. Mater. Interfaces 9(4), 4015–4023 (2017). https://doi.org/10.1021/acsami.6b11793
  139. A.E. Jakus, R.N. Shah, Multi and mixed 3D-printing of graphene-hydroxyapatite hybrid materials for complex tissue engineering. J. Biomed. Mater. Res. A 105(1), 274–283 (2017). https://doi.org/10.1002/jbm.a.35684
  140. Z. Gu, Z. Yang, L. Wang, H. Zhou, C.A. Jimenez-Cruz, R. Zhou, The role of basic residues in the adsorption of blood proteins onto the graphene surface. Sci. Rep. 5, 10873 (2015). https://doi.org/10.1038/srep10873
  141. Y. Chong, C. Ge, Z. Yang, J.A. Garate, Z. Gu, J.K. Weber, J. Liu, R. Zhou, Reduced cytotoxicity of graphene nanosheets mediated by blood-protein coating. ACS Nano 9(6), 5713–5724 (2015). https://doi.org/10.1021/nn5066606
  142. W. Hu, C. Peng, M. Lv, X. Li, Y. Zhang, N. Chen, C. Fan, Q. Huang, Protein corona-mediated mitigation of cytotoxicity of graphene oxide. ACS Nano 5(5), 3693–3700 (2011). https://doi.org/10.1021/nn200021j
  143. G. Duan, S. Kang, X. Tian, J.A. Garate, L. Zhao, C. Ge, R. Zhou, Protein corona mitigates the cytotoxicity of graphene oxide by reducing its physical interaction with cell membrane. Nanoscale 7(37), 15214–15224 (2015). https://doi.org/10.1039/C5NR01839K
  144. F. Zhou, D. Xing, B. Wu, S. Wu, Z. Ou, W. Chen, New insights of transmembranal mechanism and subcellular localization of noncovalently modified single-walled carbon nanotubes. Nano Lett. 10(5), 1677–1681 (2010). https://doi.org/10.1021/nl100004m
  145. Y. Li, Y. Liu, Y. Fu, T. Wei, L.L. Guyader, G. Gao, R. Liu, Y. Chang, C. Chen, The triggering of apoptosis in macrophages by pristine graphene through the MAPK and TGF-beta signaling pathways. Biomaterials 33(2), 402–411 (2012). https://doi.org/10.1016/j.biomaterials.2011.09.091
  146. A. Sasidharan, L. Panchakarla, P. Chandran, D. Menon, S. Nair, C. Rao, M. Koyakutty, Differential nano-bio interactions and toxicity effects of pristine versus functionalized graphene. Nanoscale 3(6), 2461–2464 (2011). https://doi.org/10.1039/c1nr10172b
  147. S.P. Mukherjee, N. Lozano, M. Kucki, A.E. Del Rio-Castillo, L. Newman, E. Vázquez, K. Kostarelos, P. Wick, B. Fadeel, Detection of endotoxin contamination of graphene based materials using the TNF-α expression test and guidelines for endotoxin-free graphene oxide production. PLoS ONE 11(11), e0166816 (2016). https://doi.org/10.1371/journal.pone.0166816
  148. M.H. Lahiani, K. Gokulan, K. Williams, M.V. Khodakovskaya, S. Khare, Graphene and carbon nanotubes activate different cell surface receptors on macrophages before and after deactivation of endotoxins. J. Appl. Toxicol. 37(11), 1305–1316 (2017). https://doi.org/10.1002/jat.3477
  149. A. Jarosz, M. Skoda, I. Dudek, D. Szukiewicz, Oxidative stress and mitochondrial activation as the main mechanisms underlying graphene toxicity against human cancer cells. Oxid. Med. Cell Longev. (2016). https://doi.org/10.1155/2016/5851035
  150. Y. Kang, J. Liu, J. Wu, Q. Yin, H. Liang, A. Chen, L. Shao, Graphene oxide and reduced graphene oxide induced neural pheochromocytoma-derived PC12 cell lines apoptosis and cell cycle alterations via the ERK signaling pathways. Int. J. Nanomedicine 12, 5501–5510 (2017). https://doi.org/10.2147/IJN.S141032
  151. X. Tian, Z. Yang, G. Duan, A. Wu, Z. Gu et al., Graphene oxide nanosheets retard cellular migration via disruption of actin cytoskeleton. Small (2017). https://doi.org/10.1002/smll.201602133
  152. G. Chen, H. Yang, C. Lu, Y. Chao, S. Hwang et al., Simultaneous induction of autophagy and toll-like receptor signaling pathways by graphene oxide. Biomaterials 33(27), 6559–6569 (2012). https://doi.org/10.1016/j.biomaterials.2012.05.064
  153. A. Wang, K. Pu, B. Dong, Y. Liu, L. Zhang, Z. Zhang, W. Duan, Y. Zhu, Role of surface charge and oxidative stress in cytotoxicity and genotoxicity of graphene oxide towards human lung fibroblast cells. J. Appl. Toxicol. 33(10), 1156–1164 (2013). https://doi.org/10.1002/jat.2877
  154. K.H. Liao, Y.S. Lin, C.W. Macosko, C.L. Haynes, Cytotoxicity of graphene oxide and graphene in human erythrocytes and skin fibroblasts. ACS Appl. Mater. Interfaces 3(7), 2607–2615 (2011). https://doi.org/10.1021/am200428v
  155. D. Wang, L. Zhu, J.F. Chen, L. Dai, Can graphene quantum dots cause DNA damage in cells? Nanoscale 7(21), 9894–9901 (2015). https://doi.org/10.1039/C5NR01734C
  156. Z.M. Markovic, B.Z. Ristic, K.M. Arsikin, D.G. Klisic, L.M. Harhaji-Trajkovic et al., Graphene quantum dots as autophagy-inducing photodynamic agents. Biomaterials 33(29), 7084–7092 (2012). https://doi.org/10.1016/j.biomaterials.2012.06.060
  157. X. Tian, B. Xiao, A. Wu, L. Yu, J. Zhou, Y. Wang, N. Wang, H. Guan, Z. Shang, Hydroxylated-graphene quantum dots induce cells senescence in both p53-dependent and -independent manner. Toxicol. Res. 5(6), 1639–1648 (2016). https://doi.org/10.1039/C6TX00209A
  158. L. Mao, M. Hu, B. Pan, Y. Xie, E.J. Petersen, Biodistribution and toxicity of radio-labeled few layer graphene in mice after intratracheal instillation. Part. Fibre Toxicol. 13, 7 (2016). https://doi.org/10.1186/s12989-016-0120-1
  159. S. Syama, W. Paul, A. Sabareeswaran, P.V. Mohanan, Raman spectroscopy for the detection of organ distribution and clearance of PEGylated reduced graphene oxide and biological consequences. Biomaterials 131, 121–130 (2017). https://doi.org/10.1016/j.biomaterials.2017.03.043
  160. M.C.P. Mendonça, E.S. Soares, M.B. de Jesus, H.J. Ceragioli, M.S. Ferreira, R.R. Catharino, M.A. da Cruz-Hofling, Reduced graphene oxide induces transient blood–brain barrier opening: an in vivo study. J. Nanobiotechnology 13(1), 78 (2015). https://doi.org/10.1186/s12951-015-0143-z
  161. S. Xu, Z. Zhang, M. Chu, Long-term toxicity of reduced graphene oxide nanosheets: effects on female mouse reproductive ability and offspring development. Biomaterials 54, 188–200 (2015). https://doi.org/10.1016/j.biomaterials.2015.03.015
  162. S.K. Singh, M.K. Singh, M.K. Nayak, S. Kumari, S. Shrivastava, J.J.A. Grácio, D. Dash, Thrombus inducing property of atomically thin graphene oxide sheets. ACS Nano 5(6), 4987–4996 (2011). https://doi.org/10.1021/nn201092p
  163. H. Yue, W. Wei, Z. Yue, B. Wang, N. Luo, Y. Gao, D. Ma, G. Ma, Z. Su, The role of the lateral dimension of graphene oxide in the regulation of cellular responses. Biomaterials 33(16), 4013–4021 (2012). https://doi.org/10.1016/j.biomaterials.2012.02.021
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