Graphene: an emerging material for biological tissue engineering

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  • ABSTRACT

    Graphene, a carbon crystal sheet of molecular thickness, shows diverse and exceptional properties ranging from electrical and thermal conductivities, to optical and mechanical qualities. Thus, its potential applications include not only physicochemical materials but also extends to biological uses. Here, we review recent experimental studies about graphene for such bioapplications. As a prerequisite to the search to determine the potential of graphene for bioapplications, the essential qualities of graphene that support biocompatibility, were briefly summarized. Then, direct examples of tissue regeneration and tissue engineering utilizing graphenes, were discussed, including uses for cell scaffolds, cell modulating interfaces, drug delivery, and neural interfaces.


  • KEYWORD

    graphene , graphene oxide , carbon nanomaterials , tissue engineering , cell scaffolds , drug delivery , neural interface , biomaterials , biocompatibility

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  • [Table 1.] Unique physical properties of graphene as materials
    Unique physical properties of graphene as materials
  • [Fig. 1.] Examples of several different graphene forms [5].
    Examples of several different graphene forms [5].
  • [Fig. 2.] Schematics of one method of typical tissue engineering approaches.
    Schematics of one method of typical tissue engineering approaches.
  • [Fig. 3.] Scanning electron microscope images of TWEEN/RGO paper (a-c) composite confocal microscopy images of the three kinds of mammalian cells grown for 48 h on TWEEN-paper for the standard live-dead test (scale bars, 20 mm), (d) photos of a TWEEN paper sample, (e-f ) optical microscopy images of the TWEEN paper before and after treatment with mature Bacillus cereus cells. The TWEEN paper shows no bacterial attachment [18]. TWEEN: polyoxyethylene sorbitan laurate, RGO: reduced graphene oxide.
    Scanning electron microscope images of TWEEN/RGO paper (a-c) composite confocal microscopy images of the three kinds of mammalian cells grown for 48 h on TWEEN-paper for the standard live-dead test (scale bars, 20 mm), (d) photos of a TWEEN paper sample, (e-f ) optical microscopy images of the TWEEN paper before and after treatment with mature Bacillus cereus cells. The TWEEN paper shows no bacterial attachment [18]. TWEEN: polyoxyethylene sorbitan laurate, RGO: reduced graphene oxide.
  • [Fig. 4.] Scanning electron microscope images of MCF-7 cells cultured for 12 h on (a) ITO/(AP)10 and (b) ITO/(graphene-AP)10?the scale bar is 5 μm for both, (c) proliferation curves of cells cultured on films with different compositions: 1) ITO/(AP)10 , 2) ITO/ (graphene)10 , 3) ITO/(graphene-AP)10 , 4) ITO/(graphene- AP)10?one laminin layer on top, and 5) ITO/(graphene-AP-laminin)10 [20]. ITO: indium tin oxide.
    Scanning electron microscope images of MCF-7 cells cultured for 12 h on (a) ITO/(AP)10 and (b) ITO/(graphene-AP)10?the scale bar is 5 μm for both, (c) proliferation curves of cells cultured on films with different compositions: 1) ITO/(AP)10 , 2) ITO/ (graphene)10 , 3) ITO/(graphene-AP)10 , 4) ITO/(graphene- AP)10?one laminin layer on top, and 5) ITO/(graphene-AP-laminin)10 [20]. ITO: indium tin oxide.
  • [Fig. 5.] Live and dead staining of NIH-3T3 cells after incubation on each substrate for 48 h?live cells are stained fluorescent green, and dead cells appear red (left side)?substrates: (i) glass; (ii) multi-walled carbon nanotube (MWCNT); (iii) graphene oxide (GO); (iv) GO/MWCNT; (v) reduced GO (RGO); and (vi) RGO/MWCNT?Scale bars all represent 100 μm. For the proliferation assay (right side), the number of cells on each substrate was evaluated at 24 and 48 h, and the percentage increase was calculated [21].
    Live and dead staining of NIH-3T3 cells after incubation on each substrate for 48 h?live cells are stained fluorescent green, and dead cells appear red (left side)?substrates: (i) glass; (ii) multi-walled carbon nanotube (MWCNT); (iii) graphene oxide (GO); (iv) GO/MWCNT; (v) reduced GO (RGO); and (vi) RGO/MWCNT?Scale bars all represent 100 μm. For the proliferation assay (right side), the number of cells on each substrate was evaluated at 24 and 48 h, and the percentage increase was calculated [21].
  • [Fig. 6.] (a) Viability of A549 cells incubated with 20 and 85 μg/mL graphene oxide (GO) nanosheets for 2 h and 24 h, (b) metabolic activity of Escherichia coli incubation with 20 and 85 μg/mL GO nanosheets at 37℃ for 2 h, (c) viability of A549 cell incubated with 20 and 85 μg/mL reduced GO (RGO) nanosheets, (d) metabolic activity of E. coli treated with 85 μg/mL GO and RGO nano-sheets [22].
    (a) Viability of A549 cells incubated with 20 and 85 μg/mL graphene oxide (GO) nanosheets for 2 h and 24 h, (b) metabolic activity of Escherichia coli incubation with 20 and 85 μg/mL GO nanosheets at 37℃ for 2 h, (c) viability of A549 cell incubated with 20 and 85 μg/mL reduced GO (RGO) nanosheets, (d) metabolic activity of E. coli treated with 85 μg/mL GO and RGO nano-sheets [22].
  • [Fig. 7.] Enhanced neural-differentiation of human neural stem cells (hNSCs) on graphene films?all scale bars represent 200 μm. (a) Bright-field images of the hNSCs differentiated for three days (left), two weeks (middle), and three weeks (right), (b) bright-field (top row) and fluorescence (bottom row) images of hNSCs differentiated on glass (left) and graphene (right) after one month of differentiation?the differentiated hNSCs were immunostained with GFAP (red) for astroglial cells, TUJ1 (green) for neural cells, and DAPI (blue) for nuclei. c) Cell counts per area (0.64 mm2) on graphene and glass regions after onemonth differentiation, d) percentage of immunoreactive cells for GFAP (red) and TUJ1 (green) on glass and grapheme [24].
    Enhanced neural-differentiation of human neural stem cells (hNSCs) on graphene films?all scale bars represent 200 μm. (a) Bright-field images of the hNSCs differentiated for three days (left), two weeks (middle), and three weeks (right), (b) bright-field (top row) and fluorescence (bottom row) images of hNSCs differentiated on glass (left) and graphene (right) after one month of differentiation?the differentiated hNSCs were immunostained with GFAP (red) for astroglial cells, TUJ1 (green) for neural cells, and DAPI (blue) for nuclei. c) Cell counts per area (0.64 mm2) on graphene and glass regions after onemonth differentiation, d) percentage of immunoreactive cells for GFAP (red) and TUJ1 (green) on glass and grapheme [24].
  • [Fig. 8.] Graphene-based composite scaffolds. (i) TWEEN/graphene paper [18]. (ii) Graphene hydrogels [28]. TWEEN: polyoxyethylene sorbitan laurate.
    Graphene-based composite scaffolds. (i) TWEEN/graphene paper [18]. (ii) Graphene hydrogels [28]. TWEEN: polyoxyethylene sorbitan laurate.
  • [Fig. 9.] Scanning electron microscope images of PPC/GO foams without cells (a), and cell-seeded PPC/GO foam after culturing 24 h in vitro (b, c)?the white arrows indicate the cell-to-cell communications. In vitro cell cytotoxicities of PPC-GO foams according to the MTT assay (d) for three days [29]. PPC: propylene carbonate, GO: graphene oxide.
    Scanning electron microscope images of PPC/GO foams without cells (a), and cell-seeded PPC/GO foam after culturing 24 h in vitro (b, c)?the white arrows indicate the cell-to-cell communications. In vitro cell cytotoxicities of PPC-GO foams according to the MTT assay (d) for three days [29]. PPC: propylene carbonate, GO: graphene oxide.
  • [Fig. 10.] (a-c) Fluorescent images of the actin cytoskeleton of mesenchymal stromal cells (MSCs) cultured on graphene, partillay fluorinated grapheme (FG) and FG stained with rhodamine-phalloidin at day 7 (scale bar = 100 μm), (d) proliferation of MSCs cultured on the graphene films, showing the controlled growth of MSCs on fluorinated graphene with different coverage of fluorine, (e) MSCs preferentially attached and highly aligned on the FG strips (scale bar = 50 μm), (h) percentage of immune-reactive cells for TUJ1 and MAP2 on unpatterned and patterned FG strips [31].
    (a-c) Fluorescent images of the actin cytoskeleton of mesenchymal stromal cells (MSCs) cultured on graphene, partillay fluorinated grapheme (FG) and FG stained with rhodamine-phalloidin at day 7 (scale bar = 100 μm), (d) proliferation of MSCs cultured on the graphene films, showing the controlled growth of MSCs on fluorinated graphene with different coverage of fluorine, (e) MSCs preferentially attached and highly aligned on the FG strips (scale bar = 50 μm), (h) percentage of immune-reactive cells for TUJ1 and MAP2 on unpatterned and patterned FG strips [31].
  • [Fig. 11.] (A) aspect ratio quantification of C2C12 cells on unmodified, graphene oxide (GO)-, and reduced GO (rGO)-modified glass substrates?cells were cultured in GM for 1 day, (B) quantification of fusion index and maturation index?quantification of (C) cell area, (D) length of multinucleate myotubes [32].
    (A) aspect ratio quantification of C2C12 cells on unmodified, graphene oxide (GO)-, and reduced GO (rGO)-modified glass substrates?cells were cultured in GM for 1 day, (B) quantification of fusion index and maturation index?quantification of (C) cell area, (D) length of multinucleate myotubes [32].
  • [Fig. 12.] Fluorescence images of H9 human embryonic stem cells cultured on graphene, multi-walled carbon nanotube (MWCNT)-graphene hybrid, glass, control tissue culture polystyrene substrates for 9 days [33].
    Fluorescence images of H9 human embryonic stem cells cultured on graphene, multi-walled carbon nanotube (MWCNT)-graphene hybrid, glass, control tissue culture polystyrene substrates for 9 days [33].
  • [Table 2.] Graphene-based cell modulations
    Graphene-based cell modulations
  • [Fig. 13.] Schematic illustration of a drug delivery system [37,38].
    Schematic illustration of a drug delivery system [37,38].
  • [Fig. 14.] Overview of neural electrode arrays applied to different sections of the nervous system [44].
    Overview of neural electrode arrays applied to different sections of the nervous system [44].
  • [Fig. 15.] (a) Schematic view of a G-SGFET with a cell on the gate area, (b) optical microscopy image showing eight transistors in the central area of a GSGFET, (c) transistor current vs. electrolytic gate voltage measured in HL-1 cell on the array, and (d) transconductance vs. gate voltage for the transistor [53]. SGFET: solution- gated field-effect transistors.
    (a) Schematic view of a G-SGFET with a cell on the gate area, (b) optical microscopy image showing eight transistors in the central area of a GSGFET, (c) transistor current vs. electrolytic gate voltage measured in HL-1 cell on the array, and (d) transconductance vs. gate voltage for the transistor [53]. SGFET: solution- gated field-effect transistors.
  • [Fig. 16.] (A) Representation of the relative size of a cardiomyocyte cell interfaced to a typical graphene and silicon nanowire-FET device, (B) gate effect on graphene-FET recorded signals from cardiomyocytes?recorded traces at different applied water gate potentials [54]. FET: field-effect transistor.
    (A) Representation of the relative size of a cardiomyocyte cell interfaced to a typical graphene and silicon nanowire-FET device, (B) gate effect on graphene-FET recorded signals from cardiomyocytes?recorded traces at different applied water gate potentials [54]. FET: field-effect transistor.
  • [Fig. 17.] (A) Scanning electron microscope image of a neuron growing on the PEDOT/GO surface at 1 d, (B) bode and nyquist plots of the electrochemical impedance behavior of platinum iridium microwires uncoated, coated with PEDOT/GO and coated with PEDOT-GO covalently modified with p20, (C) average neurite length of cells growing on the polymer surfaces, (D) average neurite length of neurons growing on the p20 modified PEDOT-GO surfaces [55]. PEDOT: poly(3,4-ethylenedioxythiophene, GO: graphene oxide.
    (A) Scanning electron microscope image of a neuron growing on the PEDOT/GO surface at 1 d, (B) bode and nyquist plots of the electrochemical impedance behavior of platinum iridium microwires uncoated, coated with PEDOT/GO and coated with PEDOT-GO covalently modified with p20, (C) average neurite length of cells growing on the polymer surfaces, (D) average neurite length of neurons growing on the p20 modified PEDOT-GO surfaces [55]. PEDOT: poly(3,4-ethylenedioxythiophene, GO: graphene oxide.
  • [Fig. 18.] Adult retinal ganglion cells on graphene either (A) bare, or (C) coated with poly-D-lysine and laminin?new-born retinal ganglion cells on graphene either (B) bare, or (D) coated with poly-D-lysine and laminin [51].
    Adult retinal ganglion cells on graphene either (A) bare, or (C) coated with poly-D-lysine and laminin?new-born retinal ganglion cells on graphene either (B) bare, or (D) coated with poly-D-lysine and laminin [51].