10.1007/s40097-018-0265-6

Graphene and graphene oxide as nanomaterials for medicine and biology application

HTML PDF
  • Subhashree Priyadarsini1,
  • Swaraj Mohanty2,
  • Sumit Mukherjee1,
  • Srirupa Basu1,
  • Monalisa Mishra*1,
  1. Neural Developmental Biology Laboratory, Department of Life Science, National Institute of Technology (NIT), Rourkela, Odisha, 769008, IN
  2. Bachelor of Technology (B. Tech), Department of Biotechnology, Gandhi Institute of Engineering and Technology (GIET), Biju Patnaik University of Technology (BPUT), Rourkela, Odisha, 769015, IN
Cover Image

Published in Issue 07-06-2018

How to Cite

Priyadarsini, S., Mohanty, S., Mukherjee, S., Basu, S., & Mishra, M. (2018). Graphene and graphene oxide as nanomaterials for medicine and biology application. Journal of Nanostructure in Chemistry, 8(2 (June 2018). https://doi.org/10.1007/s40097-018-0265-6
Crossref
Scopus
Google Scholar
Europe PMC

HTML views: 82

PDF views: 217

Abstract

Abstract Graphene- and graphene oxide-based nanomaterials have gained broad interests in research because of their unique physiochemical properties. The 2D allotropic structure allows it to be used in various biological fields. The biomedical applications of graphene and its composite include its use in gene and small molecular drug delivery. It is further used for biofunctionalization of protein, in anticancer therapy, as an antimicrobial agent for bone and teeth implantation. The biocompatibility of the newly synthesized nanomaterials allows its substantial use in medicine and biology. The current review summarizes the chemical structure and biological application of graphene in various fields. Graphical abstract

Keywords

  • Graphene,
  • Graphene oxide,
  • Reduced graphene,
  • Nanoparticles,
  • Biomedical application
HTML PDF

References

  1. Chen et al. (2008) Intrinsic and extrinsic performance limits of graphene devices on SiO2 3(4) https://doi.org/10.1038/nnano.2008.58
  2. Choi et al. (2010) Synthesis of graphene and its applications: a review 35(1) (pp. 52-71) https://doi.org/10.1080/10408430903505036
  3. Geim and Novoselov (2007) The rise of graphene 6(3) https://doi.org/10.1038/nmat1849
  4. Allen et al. (2009) Honeycomb carbon: a review of graphene 110(1) (pp. 132-145) https://doi.org/10.1021/cr900070d
  5. Compton and Nguyen (2010) Graphene oxide, highly reduced graphene oxide, and graphene: versatile building blocks for carbon-based materials 6(6) (pp. 711-723) https://doi.org/10.1002/smll.200901934
  6. Acik et al. (2010) The role of intercalated water in multilayered graphene oxide 4(10) (pp. 5861-5868) https://doi.org/10.1021/nn101844t
  7. Sanchez et al. (2011) Biological interactions of graphene-family nanomaterials: an interdisciplinary review 25(1) (pp. 15-34) https://doi.org/10.1021/tx200339h
  8. Edwards and Coleman (2013) Graphene synthesis: relationship to applications 5(1) (pp. 38-51) https://doi.org/10.1039/C2NR32629A
  9. Warner, J.H., Schaffel, F., Rummeli, M., Bachmatiuk, A.:
  10. Graphene: fundamentals and emergent applications
  11. . Newnes (2012)
  12. Novoselov et al. (2004) Electric field effect in atomically thin carbon films 306(5696) (pp. 666-669) https://doi.org/10.1126/science.1102896
  13. Reina et al. (2008) Large area, few-layer graphene films on arbitrary substrates by chemical vapor deposition 9(1) (pp. 30-35) https://doi.org/10.1021/nl801827v
  14. Dato et al. (2008) Substrate-free gas-phase synthesis of graphene sheets 8(7) (pp. 2012-2016) https://doi.org/10.1021/nl8011566
  15. Verdejo et al. (2011) Graphene filled polymer nanocomposites 21(10) (pp. 3301-3310) https://doi.org/10.1039/C0JM02708A
  16. Park and Ruoff (2009) Chemical methods for the production of graphenes 4(4) (pp. 217-224) https://doi.org/10.1038/nnano.2009.58
  17. Chung et al. (2013) Biomedical applications of graphene and graphene oxide 46(10) (pp. 2211-2224) https://doi.org/10.1021/ar300159f
  18. Loh et al. (2010) Graphene oxide as a chemically tunable platform for optical applications 2(12) https://doi.org/10.1038/nchem.907
  19. Gao (2015) (pp. 61-95) Springer https://doi.org/10.1007/978-3-319-15500-5
  20. Li et al. (2010) All-carbon electronic devices fabricated by directly grown single-walled carbon nanotubes on reduced graphene oxide electrodes 22(28) (pp. 3058-3061) https://doi.org/10.1002/adma.201000736
  21. Liu et al. (2011) Carbon materials for drug delivery and cancer therapy 14(7–8) (pp. 316-323) https://doi.org/10.1016/S1369-7021(11)70161-4
  22. Jiang et al. (2007) Quantum Hall states near the charge-neutral Dirac point in graphene 99(10) https://doi.org/10.1103/PhysRevLett.99.106802
  23. Rao et al. (2009) Graphene: the new two-dimensional nanomaterial 48(42) (pp. 7752-7777) https://doi.org/10.1002/anie.200901678
  24. Marcano et al. (2010) Improved synthesis of graphene oxide 4(8) (pp. 4806-4814) https://doi.org/10.1021/nn1006368
  25. Kulshrestha et al. (2014) A graphene/zinc oxide nanocomposite film protects dental implant surfaces against cariogenic Streptococcus mutans 30(10) (pp. 1281-1294) https://doi.org/10.1080/08927014.2014.983093
  26. Goenka et al. (2014) Graphene-based nanomaterials for drug delivery and tissue engineering (pp. 75-88) https://doi.org/10.1016/j.jconrel.2013.10.017
  27. Wang et al. (2011) Graphene and graphene oxide: biofunctionalization and applications in biotechnology 29(5) (pp. 205-212) https://doi.org/10.1016/j.tibtech.2011.01.008
  28. Kuila et al. (2011) Recent advances in graphene-based biosensors 26(12) (pp. 4637-4648) https://doi.org/10.1016/j.bios.2011.05.039
  29. Shen et al. (2012) Graphene quantum dots: emergent nanolights for bioimaging, sensors, catalysis and photovoltaic devices 48(31) (pp. 3686-3699) https://doi.org/10.1039/c2cc00110a
  30. Nayak et al. (2011) Graphene for controlled and accelerated osteogenic differentiation of human mesenchymal stem cells 5(6) (pp. 4670-4678) https://doi.org/10.1021/nn200500h
  31. Crowder et al. (2013) Three-dimensional graphene foams promote osteogenic differentiation of human mesenchymal stem cells 5(10) (pp. 4171-4176) https://doi.org/10.1039/c3nr00803g
  32. Lee et al. (2011) Origin of enhanced stem cell growth and differentiation on graphene and graphene oxide 5(9) (pp. 7334-7341) https://doi.org/10.1021/nn202190c
  33. Yoon et al. (2014) Dual roles of graphene oxide in chondrogenic differentiation of adult stem cells: cell-adhesion substrate and growth factor-delivery carrier 24(41) (pp. 6455-6464) https://doi.org/10.1002/adfm.201400793
  34. Kim et al. (2013) Bioactive effects of graphene oxide cell culture substratum on structure and function of human adipose-derived stem cells 101(12) (pp. 3520-3530) https://doi.org/10.1002/jbm.a.34659
  35. Lee et al. (2014) Graphene enhances the cardiomyogenic differentiation of human embryonic stem cells 452(1) (pp. 174-180) https://doi.org/10.1016/j.bbrc.2014.08.062
  36. Park et al. (2014) Graphene-regulated cardiomyogenic differentiation process of mesenchymal stem cells by enhancing the expression of extracellular matrix proteins and cell signaling molecules 3(2) (pp. 176-181) https://doi.org/10.1002/adhm.201300177
  37. Li et al. (2013) Three-dimensional graphene foam as a biocompatible and conductive scaffold for neural stem cells https://doi.org/10.1038/srep01604
  38. Ghuge et al. (2017) Graphene: a comprehensive review 18(6) (pp. 724-733) https://doi.org/10.2174/1389450117666160709023425
  39. Sun et al. (2008) Nano-graphene oxide for cellular imaging and drug delivery 1(3) (pp. 203-212) https://doi.org/10.1007/s12274-008-8021-8
  40. Akhavan and Ghaderi (2010) Toxicity of graphene and graphene oxide nanowalls against bacteria 4(10) (pp. 5731-5736) https://doi.org/10.1021/nn101390x
  41. Perreault et al. (2015) Antimicrobial properties of graphene oxide nanosheets: why size matters 9(7) (pp. 7226-7236) https://doi.org/10.1021/acsnano.5b02067
  42. Lu et al. (2009) A graphene platform for sensing biomolecules 121(26) (pp. 4879-4881) https://doi.org/10.1002/ange.200901479
  43. Wang et al. (2009) Graphene oxide as an ideal substrate for hydrogen storage 3(10) (pp. 2995-3000) https://doi.org/10.1021/nn900667s
  44. Song et al. (2010) Graphene oxide: intrinsic peroxidase catalytic activity and its application to glucose detection 22(19) (pp. 2206-2210) https://doi.org/10.1002/adma.200903783
  45. Zhang et al. (2010) Graphene oxide as a matrix for enzyme immobilization 26(9) (pp. 6083-6085) https://doi.org/10.1021/la904014z
  46. Zhang et al. (2013) A novel surface plasmon resonance biosensor based on graphene oxide decorated with gold nanorod–antibody conjugates for determination of transferrin (pp. 230-236) https://doi.org/10.1016/j.bios.2013.02.008
  47. Dong et al. (2010) Fluorescence resonance energy transfer between quantum dots and graphene oxide for sensing biomolecules 82(13) (pp. 5511-5517) https://doi.org/10.1021/ac100852z
  48. Shao et al. (2010) Graphene based electrochemical sensors and biosensors: a review 22(10) (pp. 1027-1036) https://doi.org/10.1002/elan.200900571
  49. Zhang et al. (2011) Interaction of peptides with graphene oxide and its application for real-time monitoring of protease activity 47(8) (pp. 2399-2401) https://doi.org/10.1039/C0CC04887A
  50. Takahashi et al. (2000) Catalytic activity in organic solvents and stability of immobilized enzymes depend on the pore size and surface characteristics of mesoporous silica 12(11) (pp. 3301-3305) https://doi.org/10.1021/cm000487a
  51. Chen et al. (2017) Enhanced performance of magnetic graphene oxide-immobilized laccase and its application for the decolorization of dyes 22(2) https://doi.org/10.3390/molecules22020221
  52. Gong et al. (2017) Moving and unsinkable graphene sheets immobilized enzyme for microfluidic biocatalysis 7(1) https://doi.org/10.1038/s41598-017-04216-4
  53. Srivastava et al. (2014) Functionalized graphene sheets as immobilization matrix for fenugreek β-amylase: enzyme kinetics and stability studies 9(11) https://doi.org/10.1371/journal.pone.0113408
  54. Grigorenko et al. (2017) Molecular modeling clarifies the mechanism of chromophore maturation in the green fluorescent protein 139(30) (pp. 10239-10249) https://doi.org/10.1021/jacs.7b00676
  55. Rafat et al. (2010) PEG–PLA microparticles for encapsulation and delivery of Tat-EGFP to retinal cells 31(12) (pp. 3414-3421) https://doi.org/10.1016/j.biomaterials.2010.01.031
  56. Bindels et al. (2017) mScarlet: a bright monomeric red fluorescent protein for cellular imaging 14(1) https://doi.org/10.1038/nmeth.4074
  57. Tschopp and Duboule (2014) (pp. 89-102) Springer
  58. Hong, S.W., Lee, J.H., Kang, S.H., Hwang, E.Y., Hwang, Y.-S., Lee, M.H., Han, D.-W., Park, J.-C:
  59. Enhanced neural cell adhesion and neurite outgrowth on graphene
  60. -
  61. based biomimetic substrates.
  62. BioMed Res. Int.
  63. 2014
  64. (2014)
  65. Gurunathan et al. (2014) Enhanced green fluorescent protein-mediated synthesis of biocompatible graphene 12(1) https://doi.org/10.1186/s12951-014-0041-9
  66. Feng et al. (2011) Graphene based gene transfection 3(3) (pp. 1252-1257) https://doi.org/10.1039/c0nr00680g
  67. Rana et al. (2011) Synthesis and drug-delivery behavior of chitosan-functionalized graphene oxide hybrid nanosheets 296(2) (pp. 131-140) https://doi.org/10.1002/mame.201000307
  68. Bao et al. (2011) Chitosan-functionalized graphene oxide as a nanocarrier for drug and gene delivery 7(11) (pp. 1569-1578) https://doi.org/10.1002/smll.201100191
  69. Jaeger et al. (2012) Branched and linear poly (ethylene imine)-based conjugates: synthetic modification, characterization, and application 41(13) (pp. 4755-4767) https://doi.org/10.1039/c2cs35146c
  70. Kim and Kim (2014) Photothermally controlled gene delivery by reduced graphene oxide–polyethylenimine nanocomposite 10(1) (pp. 117-126) https://doi.org/10.1002/smll.201202636
  71. Chen et al. (2011) Polyethylenimine-functionalized graphene oxide as an efficient gene delivery vector 21(21) (pp. 7736-7741) https://doi.org/10.1039/c1jm10341e
  72. Pan et al. (2011) Water-soluble poly (N-isopropylacrylamide)–graphene sheets synthesized via click chemistry for drug delivery 21(14) (pp. 2754-2763) https://doi.org/10.1002/adfm.201100078
  73. Yang et al. (2008) High-efficiency loading and controlled release of doxorubicin hydrochloride on graphene oxide 112(45) (pp. 17554-17558) https://doi.org/10.1021/jp806751k
  74. Tang et al. (2009) Preparation, structure, and electrochemical properties of reduced graphene sheet films 19(17) (pp. 2782-2789) https://doi.org/10.1002/adfm.200900377
  75. Chang et al. (2010) Graphene fluorescence resonance energy transfer aptasensor for the thrombin detection 82(6) (pp. 2341-2346) https://doi.org/10.1021/ac9025384
  76. Tang et al. (2011) DNA-directed self-assembly of graphene oxide with applications to ultrasensitive oligonucleotide assay 5(5) (pp. 3817-3822) https://doi.org/10.1021/nn200147n
  77. Dong et al. (2010) Graphene as a novel matrix for the analysis of small molecules by MALDI-TOF MS 82(14) (pp. 6208-6214) https://doi.org/10.1021/ac101022m
  78. Wang et al. (2009) Application of graphene-modified electrode for selective detection of dopamine 11(4) (pp. 889-892) https://doi.org/10.1016/j.elecom.2009.02.013
  79. Chen et al. (2005) Self-assembly of synthetic hydroxyapatite nanorods into an enamel prism-like structure 288(1) (pp. 97-103) https://doi.org/10.1016/j.jcis.2005.02.064
  80. Zeng et al. (2010) Self-assembled graphene-enzyme hierarchical nanostructures for electrochemical biosensing 20(19) (pp. 3366-3372) https://doi.org/10.1002/adfm.201000540
  81. Shen et al. (2012) Biomedical applications of graphene 2(3) https://doi.org/10.7150/thno.3642
  82. Wan et al. (2010) Graphene oxide sheet-mediated silver enhancement for application to electrochemical biosensors 83(3) (pp. 648-653) https://doi.org/10.1021/ac103047c
  83. Khalil et al. (2017) Graphene metal nanocomposites—Recent progress in electrochemical biosensing applications (pp. 425-439) https://doi.org/10.1016/j.jiec.2017.11.001
  84. Ma et al. (2013) The layer-by-layer assembly of polyelectrolyte functionalized graphene sheets: a potential tool for biosensing (pp. 6-11) https://doi.org/10.1016/j.colsurfa.2013.02.039
  85. Fiorillo et al. (2015) Graphene oxide selectively targets cancer stem cells, across multiple tumor types: implications for non-toxic cancer treatment, via “differentiation-based nano-therapy” 6(6) https://doi.org/10.18632/oncotarget.3348
  86. Michaud et al. (2011) Autophagy-dependent anticancer immune responses induced by chemotherapeutic agents in mice 334(6062) (pp. 1573-1577) https://doi.org/10.1126/science.1208347
  87. Xu et al. (2007) Toll-like receptor 4 is a sensor for autophagy associated with innate immunity 27(1) (pp. 135-144) https://doi.org/10.1016/j.immuni.2007.05.022
  88. Levine (2005) Eating oneself and uninvited guests: autophagy-related pathways in cellular defense 120(2) (pp. 159-162)
  89. Chen et al. (2014) Graphene oxide triggers toll-like receptors/autophagy responses in vitro and inhibits tumor growth in vivo 3(9) (pp. 1486-1495) https://doi.org/10.1002/adhm.201300591
  90. Liu et al. (2008) PEGylated nanographene oxide for delivery of water-insoluble cancer drugs 130(33) (pp. 10876-10877) https://doi.org/10.1021/ja803688x
  91. Yang et al. (2010) Graphene in mice: ultrahigh in vivo tumor uptake and efficient photothermal therapy 10(9) (pp. 3318-3323) https://doi.org/10.1021/nl100996u
  92. Markovic et al. (2011) In vitro comparison of the photothermal anticancer activity of graphene nanoparticles and carbon nanotubes 32(4) (pp. 1121-1129) https://doi.org/10.1016/j.biomaterials.2010.10.030
  93. Kang et al. (2017) Gold nanoparticle/graphene oxide hybrid sheets attached on mesenchymal stem cells for effective photothermal cancer therapy 29(8) (pp. 3461-3476) https://doi.org/10.1021/acs.chemmater.6b05164
  94. Tian et al. (2011) Photothermally enhanced photodynamic therapy delivered by nano-graphene oxide 5(9) (pp. 7000-7009) https://doi.org/10.1021/nn201560b
  95. de Faria et al. (2014) Anti-adhesion and antibacterial activity of silver nanoparticles supported on graphene oxide sheets (pp. 115-124) https://doi.org/10.1016/j.colsurfb.2013.08.006
  96. Das et al. (2011) Synthesis of silver nanoparticles in an aqueous suspension of graphene oxide sheets and its antimicrobial activity 83(z) (pp. 16-22) https://doi.org/10.1016/j.colsurfb.2010.10.033
  97. Bao et al. (2011) Synthesis and characterization of silver nanoparticle and graphene oxide nanosheet composites as a bactericidal agent for water disinfection 360(2) (pp. 463-470) https://doi.org/10.1016/j.jcis.2011.05.009
  98. Huang et al. (2015) An ultrasensitive electrochemical DNA biosensor based on graphene/Au nanorod/polythionine for human papillomavirus DNA detection (pp. 442-446) https://doi.org/10.1016/j.bios.2015.01.039
  99. Gulbakan et al. (2010) A dual platform for selective analyte enrichment and ionization in mass spectrometry using aptamer-conjugated graphene oxide 132(49) (pp. 17408-17410) https://doi.org/10.1021/ja109042w
  100. Geim (2009) Graphene: status and prospects 324(5934) (pp. 1530-1534) https://doi.org/10.1126/science.1158877
  101. Hu et al. (2018) Biomimetic graphene-based 3D scaffold for long-term cell culture and real-time electrochemical monitoring 90(2) (pp. 1136-1141) https://doi.org/10.1021/acs.analchem.7b03324
  102. Kalbacova et al. (2010) Graphene substrates promote adherence of human osteoblasts and mesenchymal stromal cells 48(15) (pp. 4323-4329) https://doi.org/10.1016/j.carbon.2010.07.045
  103. Lee et al. (2018) When stem cells meet graphene: opportunities and challenges in regenerative medicine (pp. 236-250) https://doi.org/10.1016/j.biomaterials.2017.10.004
  104. Jasim et al. (2016) Synthesis of few-layered, high-purity graphene oxide sheets from different graphite sources for biology 3(1) https://doi.org/10.1088/2053-1583/3/1/014006
  105. Sasidharan et al. (2011) Differential nano-bio interactions and toxicity effects of pristine versus functionalized graphene 3(6) (pp. 2461-2464) https://doi.org/10.1039/c1nr10172b
  106. Li et al. (2013) Graphene microsheets enter cells through spontaneous membrane penetration at edge asperities and corner sites 110(30) (pp. 12295-12300) https://doi.org/10.1073/pnas.1222276110
  107. Ryoo et al. (2010) Behaviors of NIH-3T3 fibroblasts on graphene/carbon nanotubes: proliferation, focal adhesion, and gene transfection studies 4(11) (pp. 6587-6598) https://doi.org/10.1021/nn1018279
  108. Fan et al. (2010) Fabrication, mechanical properties, and biocompatibility of graphene-reinforced chitosan composites 11(9) (pp. 2345-2351) https://doi.org/10.1021/bm100470q
  109. Qi et al. (2014) Layer-by-layer assembled graphene oxide composite films for enhanced mechanical properties and fibroblast cell affinity 2(3) (pp. 325-331) https://doi.org/10.1039/C3TB21387K
  110. Park et al. (2011) Enhanced differentiation of human neural stem cells into neurons on graphene
  111. Kim et al. (2015) Monolayer graphene-directed growth and neuronal differentiation of mesenchymal stem cells 11(11) (pp. 2024-2033) https://doi.org/10.1166/jbn.2015.2137
  112. Garcia-Alegria et al. (2016) Graphene oxide promotes embryonic stem cell differentiation to haematopoietic lineage https://doi.org/10.1038/srep25917
  113. Tyagi et al. (2013) Graphene nanomaterials and applications in bio-medical sciences 3(1) (pp. 339-345)
  114. Roy and Lee (2007) Biomedical applications of diamond-like carbon coatings: a review 83(1) (pp. 72-84) https://doi.org/10.1002/jbm.b.30768
  115. Huang et al. (2003) Hemocompatibility of titanium oxide films 24(13) (pp. 2177-2187) https://doi.org/10.1016/S0142-9612(03)00046-2
  116. Gillespie et al. (1988) The incidence of cancer following total hip replacement 70(4) (pp. 539-542) https://doi.org/10.1302/0301-620X.70B4.3403594
  117. Oryan et al. (2013) Current concerns regarding healing of bone defects 2(2) (pp. 1-12) https://doi.org/10.13172/2050-2303-2-2-374
  118. Rosa et al. (2012) Tissue engineering: from research to dental clinics 28(4) (pp. 341-348) https://doi.org/10.1016/j.dental.2011.11.025
  119. Amini et al. (2012) Bone tissue engineering: recent advances and challenges https://doi.org/10.1615/CritRevBiomedEng.v40.i5.10
  120. Stevens (2008) Biomaterials for bone tissue engineering 11(5) (pp. 18-25) https://doi.org/10.1016/S1369-7021(08)70086-5
  121. Lin et al. (2009) Study of hydroxyapatite osteoinductivity with an osteogenic differentiation of mesenchymal stem cells 89(2) (pp. 326-335) https://doi.org/10.1002/jbm.a.31994
  122. Mohandes and Salavati-Niasari (2014) In vitro comparative study of pure hydroxyapatite nanorods and novel polyethylene glycol/graphene oxide/hydroxyapatite nanocomposite 16(9) https://doi.org/10.1007/s11051-014-2604-y
  123. Mohandes and Salavati-Niasari (2014) Freeze-drying synthesis, characterization and in vitro bioactivity of chitosan/graphene oxide/hydroxyapatite nanocomposite 4(49) (pp. 25993-26001) https://doi.org/10.1039/c4ra03534h
  124. Liu et al. (2014) Biomimetic and cell-mediated mineralization of hydroxyapatite by carrageenan functionalized graphene oxide 6(5) (pp. 3132-3140) https://doi.org/10.1021/am4057826
  125. Liu et al. (2013) Synthesis of hydroxyapatite–reduced graphite oxide nanocomposites for biomedical applications: oriented nucleation and epitaxial growth of hydroxyapatite 1(13) (pp. 1826-1834) https://doi.org/10.1039/c3tb00531c
  126. Baradaran et al. (2014) Mechanical properties and biomedical applications of a nanotube hydroxyapatite-reduced graphene oxide composite (pp. 32-45) https://doi.org/10.1016/j.carbon.2013.11.054
  127. Nair et al. (2015) Graphene oxide nanoflakes incorporated gelatin–hydroxyapatite scaffolds enhance osteogenic differentiation of human mesenchymal stem cells 26(16) https://doi.org/10.1088/0957-4484/26/16/161001
  128. Xie et al. (2017) Graphene for the development of the next-generation of biocomposites for dental and medical applications 33(7) (pp. 765-774) https://doi.org/10.1016/j.dental.2017.04.008
  129. Gao et al. (2014) Enhancement mechanisms of graphene in nano-58S bioactive glass scaffold: mechanical and biological performance https://doi.org/10.1038/srep04712
  130. Li et al. (2017) Mechanical, tribological and biological properties of novel 45S5 Bioglass® composites reinforced with in situ reduced graphene oxide (pp. 77-89) https://doi.org/10.1016/j.jmbbm.2016.08.007
  131. Walker et al. (2011) Toughening in graphene ceramic composites 5(4) (pp. 3182-3190) https://doi.org/10.1021/nn200319d
  132. Lee et al. (2015) Reduced graphene oxide-coated hydroxyapatite composites stimulate spontaneous osteogenic differentiation of human mesenchymal stem cells 7(27) (pp. 11642-11651) https://doi.org/10.1039/C5NR01580D
  133. Xie et al. (2015) Two and three-dimensional graphene substrates to magnify osteogenic differentiation of periodontal ligament stem cells (pp. 266-275) https://doi.org/10.1016/j.carbon.2015.05.071
  134. Wu et al. (2015) Graphene-oxide-modified β-tricalcium phosphate bioceramics stimulate in vitro and in vivo osteogenesis (pp. 116-129) https://doi.org/10.1016/j.carbon.2015.04.048
  135. Lee et al. (2015) Enhanced osteogenesis by reduced graphene oxide/hydroxyapatite nanocomposites https://doi.org/10.1038/srep18833
  136. Rosa et al. (2013) Dental pulp tissue engineering in full-length human root canals 92(11) (pp. 970-975) https://doi.org/10.1177/0022034513505772
  137. Gunatillake and Adhikari (2003) Biodegradable synthetic polymers for tissue engineering 5(1) (pp. 1-16)
  138. Agrawal and Ray (2001) Biodegradable polymeric scaffolds for musculoskeletal tissue engineering 55(2) (pp. 141-150) https://doi.org/10.1002/1097-4636(200105)55:2<141::AID-JBM1000>3.0.CO;2-J
  139. Podila et al. (2013) Graphene coatings for biomedical implants
  140. Shradhanjali et al. (2017) Graphene for dental implant applications 7(36) (pp. 19876-19881)
  141. Segerström and Ruyter (2009) Adhesion properties in systems of laminated pigmented polymers, carbon–graphite fiber composite framework and titanium surfaces in implant suprastructures 25(9) (pp. 1169-1177) https://doi.org/10.1016/j.dental.2009.04.009
  142. Bartolo et al. (2012) Biomedical production of implants by additive electro-chemical and physical processes 61(2) (pp. 635-655) https://doi.org/10.1016/j.cirp.2012.05.005
  143. Yang et al. (2013) Nano-graphene in biomedicine: theranostic applications 42(2) (pp. 530-547) https://doi.org/10.1039/C2CS35342C
  144. Li et al. (2012) Using graphene oxide high near-infrared absorbance for photothermal treatment of Alzheimer’s disease 24(13) (pp. 1722-1728) https://doi.org/10.1002/adma.201104864
  145. Yao et al. (2016) Partially reduced graphene oxide based FRET on fiber-optic interferometer for biochemical detection https://doi.org/10.1038/srep23706
  146. Zhang et al. (2011) Synergistic effect of chemo-photothermal therapy using PEGylated graphene oxide 32(33) (pp. 8555-8561) https://doi.org/10.1016/j.biomaterials.2011.07.071
  147. Su et al. (2015) Efficient photothermal therapy of brain cancer through porphyrin functionalized graphene oxide 39(7) (pp. 5743-5749) https://doi.org/10.1039/C5NJ00122F
  148. You et al. (2012) Effective photothermal chemotherapy using doxorubicin-loaded gold nanospheres that target EphB4 receptors in tumors 72(18) (pp. 4777-4786) https://doi.org/10.1158/0008-5472.CAN-12-1003
  149. Yang et al. (2013) Graphene based materials for biomedical applications 16(10) (pp. 365-373) https://doi.org/10.1016/j.mattod.2013.09.004
  150. Zhou et al. (2011) Graphene oxide noncovalent photosensitizer and its anticancer activity in vitro 17(43) (pp. 12084-12091) https://doi.org/10.1002/chem.201003078
  151. Kong and Huang (2014) Applications of graphene in mass spectrometry 14(7) (pp. 4719-4732) https://doi.org/10.1166/jnn.2014.9503
  152. Tang et al. (2010) Graphene-based SELDI probe with ultrahigh extraction and sensitivity for DNA oligomer 132(32) (pp. 10976-10977) https://doi.org/10.1021/ja104017y
  153. Zhou et al. (2010) Reduced graphene oxide films used as matrix of MALDI-TOF-MS for detection of octachlorodibenzo-p-dioxin 46(37) (pp. 6974-6976) https://doi.org/10.1039/c0cc01681k
  154. Lu et al. (2011) Matrix interference-free method for the analysis of small molecules by using negative ion laser desorption/ionization on graphene flakes 83(8) (pp. 3161-3169) https://doi.org/10.1021/ac2002559
  155. Zhang et al. (2013) Use of graphene as a matrix to minimize reduction in the process of matrix-assisted laser desorption/ionization 27(11) (pp. 1278-1282) https://doi.org/10.1002/rcm.6561
  156. Luo et al. (2011) Magnetic retrieval of graphene: extraction of sulfonamide antibiotics from environmental water samples 1218(10) (pp. 1353-1358) https://doi.org/10.1016/j.chroma.2011.01.022
  157. Lu et al. (2012) Facile synthesis of TiO2/graphene composites for selective enrichment of phosphopeptides 4(5) (pp. 1577-1580) https://doi.org/10.1039/c2nr11791f
  158. Kim and Min (2009) Durable large-area thin films of graphene/carbon nanotube double layers as a transparent electrode 25(19) (pp. 11302-11306) https://doi.org/10.1021/la9029744
  159. Kim and Min (2012) Preparation of the hybrid film of poly (allylamine hydrochloride)-functionalized graphene oxide and gold nanoparticle and its application for laser-induced desorption/ionization of small molecules 28(9) (pp. 4453-4458) https://doi.org/10.1021/la204185p
  160. Lee et al. (2010) Laser desorption/ionization mass spectrometric assay for phospholipase activity based on graphene oxide/carbon nanotube double-layer films 132(42) (pp. 14714-14717) https://doi.org/10.1021/ja106276j
  161. Kim et al. (2011) Synergistic effect of graphene oxide/MWCNT films in laser desorption/ionization mass spectrometry of small molecules and tissue imaging 5(6) (pp. 4550-4561) https://doi.org/10.1021/nn200245v
  162. Kim and Min (2012) Fabrication of alternating multilayer films of graphene oxide and carbon nanotube and its application in mechanistic study of laser desorption/ionization of small molecules 4(4) (pp. 2088-2095) https://doi.org/10.1021/am300054z
  163. Qian et al. (2013) Laser engineered graphene paper for mass spectrometry imaging https://doi.org/10.1038/srep01415
  164. Cheng et al. (2012) A graphene-based multifunctional affinity probe for selective capture and sequential identification of different biomarkers from biosamples 48(82) (pp. 10240-10242) https://doi.org/10.1039/c2cc35483g
  165. Liu et al. (2011) Graphene and graphene oxide sheets supported on silica as versatile and high-performance adsorbents for solid-phase extraction 123(26) (pp. 6035-6039) https://doi.org/10.1002/ange.201007138
  166. Shi et al. (2012) Enrichment and detection of small molecules using magnetic graphene as an adsorbent and a novel matrix of MALDI-TOF-MS 48(18) (pp. 2418-2420) https://doi.org/10.1039/c2cc17696c
  167. Zou et al. (2016) Mechanisms of the antimicrobial activities of graphene materials 138(7) (pp. 2064-2077) https://doi.org/10.1021/jacs.5b11411
  168. Chen et al. (2014) Graphene oxide exhibits broad-spectrum antimicrobial activity against bacterial phytopathogens and fungal conidia by intertwining and membrane perturbation 6(3) (pp. 1879-1889) https://doi.org/10.1039/C3NR04941H
  169. Solís-Fernández et al. (2017) Synthesis, structure and applications of graphene-based 2D heterostructures 46(15) (pp. 4572-4613) https://doi.org/10.1039/C7CS00160F