COMMUNICATION
Surface Coatings
Vertically Aligned Graphene Coating is Bactericidal
and Prevents the Formation of Bacterial Biofilms
Santosh Pandit, Zhejian Cao, Venkata R. S. S. Mokkapati, Emanuele Celauro, Avgust
Yurgens, Martin Lovmar, Fredrik Westerlund, Jie Sun,* and Ivan Mijakovic*
The key first step in developing bacterial infections related to implants and
medical devices is the attachment of planktonic bacterial cells, and sub-
sequent formation of biofilms. Herein, it is reported that graphene, a 2D
carbon-based material, can be effectively used to prevent bacterial attach-
ment. The key parameter for this effect is the orientation of graphene with
respect to the coated surface. Chemical vapor deposition (CVD) graphene,
deposited horizontally on the surface, exhibits no antibacterial effect. By con-
trast, an array of graphene flakes grown perpendicularly to the surface by a
plasma-enhanced CVD (PECVD) process prevent biofilm formation. Electron
microscopy reveals that the exposed edges of vertically aligned graphene
flakes penetrate the bacterial membrane and drain the cytosolic content.
Bacteria are not able to develop resistance to this killing mechanism during
multiple exposures. By keeping the height of the vertical graphene coating
between 60 and 100 nm, the coating is able to effectively kill bacteria, while
being completely harmless to mammalian cells.
Graphene is a 2D material consisting of carbon atoms arranged
in a honeycomb-like hexagonal lattice.[1] Due to its remark-
able mechanical and electrical properties, graphene has been
exploited in various applications.[2,3] The interaction of graphene
with bacterial cells has been extensively studied, but there
remains some controversy in this field.[4] There are a number
of reports describing bactericidal effects of graphene flakes,
Dr. S. Pandit, Dr. V. R. S. S. Mokkapati, Dr. E. Celauro,
Prof. F. Westerlund, Prof. I. Mijakovic
Department of Biology and Biological Engineering
Chalmers University of Technology
Kemivägen 10, 41296 Göteborg, Sweden
E-mail: ivan.mijakovic@chalmers.se
Z. Cao, Prof. A. Yurgens, Prof. J. Sun
Department of Microtechnology and Nanoscience
Chalmers University of Technology
Kemivägen 9, 41296 Göteborg, Sweden
E-mail: jie.sun@chalmers.se
Dr. M. Lovmar
Wellspect Healthcare
Aminogatan 1, 43121 Mölndal, Sweden
Prof. J. Sun
Key Laboratory of Optoelectronics Technology
Beijing University of Technology
Pingleyuan 100, 100124 Beijing, China
The ORCID identification number(s) for the author(s) of this article
can be found under https://doi.org/10.1002/admi.201701331.
DOI: 10.1002/admi.201701331
Adv. Mater. Interfaces 2018, 1701331 1701331  (1 of 9)
www.advmatinterfaces.de
but they are not unanimous with regard
to the mechanism of killing. Physical dis-
ruption of the bacterial membrane is often
cited as the cause of death,[5–8] and here it
has been demonstrated that the density of
graphene flakes plays an important role.[9]
Other reports claim that bacteria can be
killed by oxidative stress, caused by the
reactive oxygen species (ROS) generated
by graphene derivatives.[10,11] In this case,
the size of graphene and graphene oxide
flakes seems to be important, since larger
flakes can wrap around bacterial cells and
deliver more severe oxidative stress.[10,11]
By contrast, there are also studies demon-
strating that graphene and graphene oxide
are not harmful to bacteria, and can rather
stimulate bacterial growth or metabolic
functions.[12–14]
A major reason for these apparently
controversial results is the heterogeneity
of graphene flakes used in previous experiments. Depending
on the production method, graphene can have various degrees
of crystallinity, doping, orientation, layer numbers, impurities,
and additional functional groups. In the large majority of ear-
lier reports, solution processed graphene flakes graphene oxide
(GO), reduced graphene oxide (rGO) were used.[15,16] These
low-cost flakes are freely suspended in solution, with little con-
trol over flake orientation, thickness, and geometry, and are also
associated with a large number of defects and impurities.[6,15,16]
Here, we address a hypothesis that the relative orientation of
graphene with respect to bacteria could be the key parameter
in defining the outcome of their interaction. A recent study
suggested that vertically oriented graphene oxide nanosheets
exhibited a significantly higher degree of activity against gram-
negative bacteria, compared to randomly oriented and hori-
zontally coated graphene oxide.[8] The toxicity of such vertically
oriented graphene oxide nanosheets was due to both mechan-
ical disruption and generation of oxidative stress.[8] To further
examine this, we used a new format of graphene, namely, ver-
tically oriented graphene grown by plasma-enhanced chemical
vapor deposition (PECVD). The vertical graphene is much more
controllable in terms of all the parameters mentioned above.
The as-grown vertical graphene is of high quality in terms of
its chemical purity, crystallinity, and electrical properties, as
compared with typical liquid phase derived graphene that is
the dominant format of graphene in the biology sector. Most
importantly, all the graphene flakes are “rooted” on a substrate
© 2018 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim
www.advancedsciencenews.com
www.advmatinterfaces.de

Figure 1.  Preparation of surfaces coated with vertically aligned graphene flakes. a) Photograph of the uncoated and coated 6 mm × 6 mm SiO2 and
Au samples. b) Optical microscopy image of the graphene coating on the Au surface. c) High magnification (top) and low magnification (bottom)
SEM images of the graphene nanoflakes grown on silicon dioxide (SiO2) and gold (Au) surfaces, viewed from above. Because the graphene is quasi-
suspended, a small acceleration voltage (5 kV) was used for observation of surface features.

with their sharp edges pointing outward. Our vertical graphene
coating is very reproducible, and the flake geometry is well con-
trolled. Furthermore, the coating is patternable by lithography
(with micrometer precision) and compatible with existing elec-
tronics processing.
In order to achieve well-defined interaction conditions
between bacteria and graphene, we coated two supporting sur-
faces, SiO2 and gold (Au), with graphene in the two distinct and
controlled geometries, but with equal quality and purity. The
horizontal coating was a single sheet of monolayer CVD gra-
phene,[17] deposited on the surface. The vertical coating was a
dense array of PECVD graphene flakes grown perpendicularly to
the basal plane, with a typical height of 60–100 nm. These two
arrangements of graphene had diametrically opposite effects
on bacteria. The horizontal monolayer graphene did not harm
either the bacterial cells or mouse fibroblasts, suggesting low
risk of cytotoxicity. By contrast, vertically grown graphene caused
extensive structural damage to bacterial cells and effectively pre-
vented biofilm attachment to the coated surfaces. The damage to
the bacterial cells was mechanical (loss of membrane integrity)
and was not due to generation of oxidative stress. During a pro-
longed incubation, bacteria did not develop any resistance to the
killing effect of vertically deposited graphene. Interestingly, verti-
cally deposited graphene did not harm mouse fibroblasts, so the
killing effect seems to be confined to microbes. To the best of
our knowledge, this is the first study reporting and clarifying the
mechanism of bactericidal effect of PECVD vertical graphene.
Based on a definite morphology and high quality of graphene
used, our study also contributes to clarifying the general contro-
versy regarding the mechanism of graphene–bacteria interaction.

Adv. Mater. Interfaces 2018, 1701331 1701331  (2 of 9) © 2018 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim
www.advancedsciencenews.com
www.advmatinterfaces.de

In order to examine the importance of relative orientation
between graphene and bacteria, we devised experimental sys-
tems with a defined interaction geometry and controlled gra-
phene quality and size. The first experimental setup contained
horizontal monolayer CVD graphene, interacting with bacteria
via its flat and uniform surface, and the second contained verti-
cally aligned graphene flakes, interacting with bacteria via the
exposed sharp edges. We used two reference surfaces to be
coated with graphene: the insulating SiO2 and the conductive
Au. The rationale behind this choice was to test whether con-
ductivity of the coated surface could be a relevant parameter
for bactericidal effect. Gram-negative Escherichia coli (E. coli)
(UTI89) and Gram-positive Staphylococcus epidermidis (S. epider-
midis) (ATCC 35984), causative agents of urinary tract infections
and infections related to implants and catheters, were used to
test the antibacterial properties of the coatings. For the hori-
zontal coating, a single layer of CVD graphene was synthesized
on copper foil,[17] and transferred onto SiO2 and Au surfaces
(6 × 6 mm plates), using poly-methyl methacrylate as support
during transfer (Figure S1, Supporting Information). Previous
studies have examined the effect of graphene on planktonic
bacteria, which is not the most common condition for bacte-
rial cells in their natural environment. We opted to examine
the effect on bacterial biofilms, since these protected, multicel-
lular structures are more relevant for bacterial infections and
biofouling.[18] To test the impact of graphene, we grew bacterial
biofilms directly on the analyzed surfaces. Bacterial inoculum
(2 × 105 colony forming units (CFUs) per milliliter of overnight
culture) was deposited on top of the coated surfaces, where it
was left to form a biofilm. The biofilm was incubated for 1–72 h,
harvested, and sonicated, and the surviving bacteria were
counted as CFUs on agar plates. Monolayer graphene horizon-
tally deposited on either SiO2 or Au surfaces had no measurable
effect on the CFU counts of E. coli or S. epidermidis in the 72 h
biofilm (Figure S2a, Supporting Information). To verify this
with an independent method, we visualized live/dead bacterial
cells with propidium iodide staining. Propidium iodide perme-
ates and stains specifically the dead cells (red), while the living
cells are not stained (green). The result of this experiment con-
firmed the finding obtained by the CFU counts (Figure S2b,
Supporting Information), i.e., no dead cells. To assess whether
the coating had any destabilizing effect on the mechanical sta-
bility of the biofilm, we carried out the CFU counting with the
old culture medium fractions, performed on the biofilm sam-
ples every 24 h to replenish the medium. The numbers of bac-
teria in the old culture medium were identical in the coated and
the noncoated control samples (Figure S3, Supporting Informa-
tion). We concluded that the horizontally deposited monolayer
graphene had no impact on either bacterial survival or mechan-
ical stability of the biofilms on the coated surfaces.
Next, we tested SiO2 and Au samples coated with PECVD
graphene flakes aligned perpendicularly to the surface.[19] Due
to diffuse reflection, the graphene-coated samples appear black
(Figure 1a) and the coating is very uniform (Figure 1b). Scan-
ning electron microscopy (SEM) images of the surface reveal
the regular structure of the vertically aligned graphene nano-
flakes (Figure 1c). The dimensions of the nanoflakes were
characterized using atomic force microscopy (AFM), and
this indicated that the vertical flakes had an average size of
100 nm on the Au substrate and 60 nm on the SiO2 substrate

Figure 2.  Vertically aligned graphene coating is bactericidal. a) Loss of viability measured for E. coli and S. epidermidis. Both strains were cultured for
1 h (light gray bars), 4 h (white bars), and 72 h (dark gray bars) on SiO2 and Au substrate with or without vertically aligned graphene. The data for
horizontal monolayer coating in the same setup are shown in Figure S2 (Supporting Information). b) Live and dead staining of E. coli and S. epidermidis
on control and vertically aligned graphene-coated surfaces. Green color represents live cells, while dead cells are stained red. Both experiments were
performed in three biological replicates. *P < 0.001.

Adv. Mater. Interfaces 2018, 1701331 1701331  (3 of 9) © 2018 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim
www.advancedsciencenews.com
www.advmatinterfaces.de

Adv. Mater. Interfaces 2018, 1701331 1701331  (4 of 9) © 2018 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim
www.advancedsciencenews.com
www.advmatinterfaces.de

Figure 3.  Mechanical damage to the cellular envelope caused by vertically aligned graphene. a) SEM images of E. coli (two top rows) and S. epidermidis
(two bottom rows) on the control SiO2 and Au surfaces and samples coated with vertically aligned graphene samples. The right-most images show
coated samples with higher magnification. The experiment was performed in three biological replicates and representative images are shown.
b) A high magnification illustrative image of E. coli cells on the coated surface, showing a completely disintegrated cell, and several partially damaged
cells. c) Bacterial resistance development to vertically aligned graphene evaluated with S. epidermidis. Twenty four hour old biofilm cells grown on SiO2
and Au surfaces coated with vertically aligned graphene were homogenized and recultured on respective new substrates, and the viability of bacteria
was analyzed. d) Four and seventy two hour old biofilms were stained with CellRox and DAPI for the detection of ROS formation in the biofilm cells.
ROS was not detected in gold (Au) and vertical graphene coated gold substrate. ROS was detected in the positive control where biofilms were exposed
with H2O2. Error bars represent the standard deviation from three independent biological replicates. *P < 0.001.

(Figure S4, Supporting Information). The vertical graphene
flakes are generally longer on Au than on SiO2, which is due to
the catalytic effect of the transition metal Au on the carbon pre-
cursor decomposition and the subsequent graphitization. Apart
from AFM characterization, we also carried out additional SEM
characterization. In the tilted angle SEM of vertical graphene,
the quasi side view of the material is shown. It is seen that
the graphene flakes are not lying on the substrate, but rather
sticking out vertically (Figure S5a, Supporting Information).
We have also grown the vertical graphene by PECVD on SiO2
particles, which have round surfaces (Figure S5b, Supporting
Information). In the SEM micrographs, it is very clear that the
graphene flakes are vertical to the tangent plane of the local sur-
face (Figure S5a–c, Supporting Information). Raman spectros-
copy confirmed the graphitic structure of the samples and their
comparably good quality (Figure S6, Supporting Information).
Results obtained from contact angle measurement showed
the higher hydrophobicity of graphene-coated substrates com-
pared to noncoated surfaces (Figure S7, Supporting Informa-
tion). Contact angles with graphene coated SiO2 and Au were

Adv. Mater. Interfaces 2018, 1701331 1701331  (5 of 9) © 2018 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim
www.advancedsciencenews.com
117.2° and 107.9°, respectively, whereas contact angles with
noncoated SiO2 and Au were 87.3° and 80.3°, respectively. Verti-
cally aligned graphene exhibited a strong inhibitory effect on
adhesion of E. coli and S. epidermidis biofilms (Figure 2a). The
effect was strongest with the shortest incubation interval (1 h),
with close to 100% loss of bacterial viability. The antibacterial
effect became progressively weaker toward 72 h. The loss of
viability was similar for the SiO2 and Au surfaces, suggesting
that the bactericidal effect of vertically grown graphene was
not related to the conductivity of the coated surface. The pro-
pidium iodide staining of the biofilms confirmed the results of
the CFU counts (Figure 2b), revealing a large fraction of dead
cells. The measured loss of bacterial viability was not caused by
mechanical destabilization of the biofilm, since the old culture
medium fractions contained the same CFU counts for coated
and uncoated surfaces (Figure S3, Supporting Information).
We therefore concluded that vertically aligned graphene coating
exhibits bactericidal effects and prevents growth of bacterial
biofilms.
In order to explore the mechanism by which bacterial via-
bility is reduced on the vertically aligned graphene surfaces, we
examined the morphology of the cells with SEM (Figure 3a).
The E. coli and S. epidermidis cells maintained full envelope
integrity on the noncoated SiO2 and Au controls. Morpholog-
ical changes consistent with cell disintegration were observed
on surfaces coated with vertically aligned graphene (Figure 3a).
The zoomed-out images show a heterogeneous picture, with
some cells entirely disintegrated, some damaged, and some
seemingly intact. The zoomed-in images of E. coli cells reveal
large surfaces of broken cellular envelopes stretched on the gra-
phene surface. For S. epidermidis, which was more resistant to
graphene in loss of viability and propidium iodide assays, the
damage of the envelope appeared to be more contained, and on
average fewer cells were affected. Theoretical simulations have
predicted that graphene edges can penetrate the lipid bilayer via
strong van der Waals attraction with the hydrophobic tails of
membrane lipids.[7,20] Our experimental results are consistent
with this prediction.
Observed loss of DNA from the bacterial cells grown on
vertically aligned graphene confirmed the leakage of cytosolic
content (Figure S8, Supporting Information). This killing
mechanism requires that an exposed sharp graphene edge
penetrates the membrane. This is obviously facilitated by the
90° angle between graphene and the membrane surface. The
killing mechanism is also consistent with the observation that
prolonged incubation of the bacterial biofilm on the coated
surface reduces the killing effect (Figure 2a): since direct con-
tact between the graphene edge and the bacterial membrane is
required, dead cells that accumulate on the surface are likely to
offer protection to fresh cells attaching from the liquid phase. A
completely disintegrated cell covering a large graphene surface
can be seen in Figure 3b. Disintegrated cells like this one could
be expected to cover large portions of the surface, and reduce
the bactericidal effect. It must be emphasized that the starting
inoculum we used (5 × 104 CFU mL−1) highly surpasses the
actual bacterial density encountered in biofouling or early
infection. Therefore the protection levels (in terms of loss of
viability) in those applications can be expected to be higher
than reported here. While our SEM analyses clearly pointed
Adv. Mater. Interfaces 2018, 1701331 1701331  (6 of 9)
www.advmatinterfaces.de
to structural damage to the membrane, the generation of ROS
by graphene derivatives has also been cited as a bactericidal
mechanism in the literature.[11,21] To check for potential genera-
tion of ROS by the graphene coatings used in our experiments,
biofilms were stained with cellRox ROS sensor and observed
under a fluorescence microscope. As shown in Figure 3d, ROS
were not detected in biofilms grown on either gold or vertical
graphene-coated gold substrates. However, ROS generation
was clearly observed in biofilms that were exposed to H2O2 as
a positive control for our assay. This indicated that the bacteri-
cidal effect of vertical PECVD graphene is not due to genera-
tion of oxidative stress. Next, we examined whether bacteria
can develop resistance against the effect of the vertically aligned
graphene. Since S. epidermidis showed a higher initial tolerance
to the vertical graphene coating, we selected this strain for the
assay. We first incubated the bacterial biofilm for 24 h on SiO2
and Au substrate, with or without vertical coating. The bacte-
rial biofilms were then resuspended in a fresh medium to allow
survivors to recover. The cells were subsequently recultured for
24 h on new samples of the respective coated surfaces for two
more times. The loss of viability was consistently the same in
all recultured batches (Figure 3c), indicating that no resistance
to the killing effect of vertical graphene had developed.
The observed differences in loss of viability between
E. coli and S. epidermidis are most likely related to the dif-
ferent envelope composition of Gram-negative and Gram-
positive bacteria, and difference in probability of graphene
reaching the membrane lipids. The cell wall of Gram-nega-
tive bacteria (E. coli) is 8–12 nm thick and contains around
20–30% of murein, which maintains the structural integrity.
In Gram-positive bacteria (S. epidermidis), the cell wall is
≈20–80 nm thick, with 70–80% of murein, which makes it
comparatively more robust.[22,23] The stretched-out membrane
surfaces projected from partly disintegrated E. coli cells prob-
ably correspond to fragments of the outer lipid membrane,
not contained in the cell wall, and absent in S. epidermidis.
The round shape of cocci may also contribute to its resistance
to graphene penetration, because this shape reduces the bacte-
rial surface available for interaction with a flat surface, com-
pared to a rod-like E. coli cell. A qualitative examination of a
large number of SEM images suggests a positive correlation
between the vertical orientation, density and sharpness of the
nanoflake edges on the one side and the severity of damage to
the bacterial cells on the other.
We finally examined the effect of vertically aligned graphene
on eukaryal cells, using a cell culture of mouse fibroblasts,
NIH3T3 (Figure 4) and human neuroblastoma, SH-SY5Y
(Figure S9, Supporting Information). Surfaces coated with
vertical graphene had no observable effect on both fibroblast
and neuroblastoma cell viability, detected with the dead/live
staining (Figure 4a and Figure S9, Supporting Information).
This finding was also supported by the SEM images (Figure
4b), where no mechanical damage was visible on mammalian
cells. These mammalian cells are ≈20 µm in size, an order of
magnitude larger than the bacterial cells (1–2 µm). The lipid
composition of the mammalian cell membrane is significantly
different from that of bacterial cells.[7,24,25] Either the size, the
membrane composition, or the protective matrix secreted by
the fibroblasts and neuroblastoma cells made them resistant
© 2018 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim
www.advancedsciencenews.com
www.advmatinterfaces.de

Figure 4.  Graphene coatings show no toxicity toward the mouse embryo derived fibroblast cell line NIH3T3. a) Laser scanning confocal microscopic
images of mouse fibroblast cells. Cells were cultured for 48 h on horizontally and vertically graphene coated SiO2 and Au substrates, as well as on
uncoated controls. Cells were fixed and stained with Live/Dead viability stain. Forty eight hour cultured cells were treated with 20% ethanol for 10 min as
a control for cell death. b) SEM images of cells grown on vertical graphene coated SiO2 and Au substrates and respective control. c) High magnification
SEM image of a cell on the coated surface, with a clear view of filopodia. All experiments were performed in three biological replicates and representative
images are shown.

to the effects of vertical graphene. In addition to not harming
the NIH3T3 cells, vertical graphene seemed to enhance their
formation of filopodia (Figure 4c). These actin filament-based
structures are involved in cell attachment, sensing the envi-
ronment, and migration.[26] Thus, our results are in line with
previous observations that graphene and graphene derivatives
enhance the adherence, differentiation, and proliferation of
mammalian cells,[27–29] and our special vertical coating did
not seem to diminish this beneficial interaction.
Our results demonstrate that by controlling the orientation
of graphene coatings, it is possible to achieve two very distinct
outcomes: bactericidal and neutral. The continuous horizontal
CVD monolayer graphene coating consistently had no del-
eterious effects on attachment or survival of either bacterial or

Adv. Mater. Interfaces 2018, 1701331 1701331  (7 of 9) © 2018 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim
www.advancedsciencenews.com
mammalian cells. This highlights the possibility to use such
surfaces for fabrication of bioelectrodes[30] or biosensors,[31]
where conductivity properties of graphene can be exploited
without harming the cells. By contrast, PECVD-grown, vertically
aligned graphene coating had a pronounced killing effect and
effectively prevented attachment of bacteria to the coated sur-
faces while being harmless to mammalian cells. The penetra-
tion of graphene into the bacterial cells depended crucially on
the angle between the membrane and the graphene flakes. It
has previously been documented that graphene oxide flakes in
suspension have a higher potential to penetrate biological mem-
branes compared to their counterparts attached to a surface.[32]
In the experimental setup employed by Li et al.,[32] the flakes
were mostly in contact with the basal plane, resulting in a flat
assembly with a reduced contact of the sharp edges with the bio-
logical membrane. In our experimental setup, a large majority
of the graphene flakes point away from the plane (Figure 1c).
Therefore, an opposite effect was achieved: high loss of viability,
comparable to that observed with flakes in solution and plank-
tonic bacteria.[6] The method we used for producing vertically
coated surfaces[22] provides a uniform array of vertically aligned
nanoflakes (Figure 1). Depending on the application, as long as
a predominantly vertical alignment of the flakes can be achieved
on the surface, sufficient antibacterial effects can probably be
attained with a simpler coating method. The potential of gra-
phene in biomedicine is far from being fully realized, due to the
unexplored potential risks linked to the use of graphene and its
derivatives.[33–35] Graphene flakes in solution mainly represent
an environmental and health hazard associated with free diffu-
sion. Graphene vertically attached to the surface of a substrate,
as a stable coating, could represent a viable alternative for a
broad spectrum of antibacterial applications.
Supporting Information
Supporting Information is available from the Wiley Online Library or
from the author.
Acknowledgements
S.P. and Z.C. contributed equally to this work. This work was funded
by grants from the Chalmers Areas of Advance in Nanoscience
and Nanotechnology and Life Science Engineering to I.M., F.W.,
and A.Y.; SIO-Grafen, a joint investment of VINNOVA, Formas,
and Energimyndigheten, to M.L., I.M., and F.W.; NSFC 11674016,
NKRDPC 2017YFB0403102, BMSTP Z161100002116032, BMCE
PXM2017_014204_500034, and STINT to J.S.; and ÅForsk to I.M.
Conflict of Interest
The authors declare no conflict of interest.
Keywords
adhesion, antibacterial activity, biofilm, mouse fibroblast cell, vertical
graphene
Adv. Mater. Interfaces 2018, 1701331 1701331  (8 of 9)
www.advmatinterfaces.de
Received: October 16, 2017
Revised: January 7, 2018
Published online:
[1] A. K. Geim, K. S. Novoselov, Nat. Mater. 2007, 6, 183.
[2] C. Lee, X. Wei, J. W. Kysar, J. Hone, Science 2008, 321, 385.
[3] K. S. Novoselov, A. K. Geim, S. V. Morozov, D. Jiang, Y. Zhang,
S. V. Dubonos, I. V. Grigorieva, A. A. Firsov, Science 2004, 306,
666.
[4] H. M. Hegab, A. ElMekawy, L. D. Zou, D. Mulcahy, C. P. Saint,
M. Ginic-Markovic, Carbon 2016, 105, 362.
[5] W. B. Hu, C. Peng, W. J. Luo, M. Lv, X. M. Li, D. Li, Q. Huang,
C. H. Fan, ACS Nano 2010, 4, 4317.
[6] S. Liu, T. H. Zeng, M. Hofmann, E. Burcombe, J. Wei, R. Jiang,
J. Kong, Y. Chen, ACS Nano 2011, 5, 6971.
[7] Y. S. Tu, M. Lv, P. Xiu, T. Huynh, M. Zhang, M. Castelli, Z. R. Liu,
Q. Huang, C. H. Fan, H. P. Fang, R. H. Zhou, Nat. Nanotechnol.
2013, 8, 594.
[8] X. Lu, X. Feng, J. R. Werber, C. Chu, I. Zucker, J. H. Kim, C. O. Osuji,
M. Elimelech, Proc. Natl. Acad. Sci. USA 2017, 114, E9793.
[9] V. T. H. Pham, V. K. Truong, M. D. J. Quinn, S. M. Notley, Y. Guo,
V. A. Baulin, M. AI Kobaisi, R. J. Crawford, E. P. Ivanova, ACS Nano
2015, 9, 8458.
[10] S. B. Liu, M. Hu, T. H. Zeng, R. Wu, R. R. Jiang, J. Wei, L. Wang,
J. Kong, Y. Chen, Langmuir 2012, 28, 12364.
[11] F. Perreault, A. F. de Faria, S. Nejati, M. Elimelech, ACS Nano 2015,
9, 7226.
[12] O. N. Ruiz, K. A. Fernando, B. Wang, N. A. Brown, P. G. Luo,
N. D. McNamara, M. Vangsness, Y. P. Sun, C. E. Bunker, ACS Nano
2011, 5, 8100.
[13] W. Ren, G. Ren, Y. Teng, Z. Li, L. Li, J. Hazard. Mater. 2015, 297,
286.
[14] D. Wang, G. Wang, G. Zhang, X. Xu, F. Yang, Bioresour. Technol.
2013, 131, 527.
[15] O. Akhavan, E. Ghaderi, ACS Nano 2010, 4, 5731.
[16] J. Chen, H. Peng, X. Wang, F. Shao, Z. Yuan, H. Han, Nanoscale
2014, 6, 1879.
[17] X. Li, W. Cai, J. An, S. Kim, J. Nah, D. Yang, R. Piner, A. Velamakanni,
I. Jung, E. Tutuc, Science 2009, 324, 1312.
[18] M. M. Mihai, A. M. Holban, C. Giurcaneanu, L. G. Popa,
R. M. Oanea, V. Lazar, M. C. Chifiriuc, M. Popa, M. I. Popa, Curr.
Top. Med. Chem. 2015, 15, 1552.
[19] L. Liu, X. Liu, Z. Zhan, W. Guo, C. Xu, J. Deng, D. Chakarov,
P. Hyldgaard, E. Schröder, A. Yurgens, J. Sun, Adv. Mater. Interfaces
2016, 3, 1500492.
[20] B. Luan, T. Huynhb, R. Zhou, Nanoscale 2016, 8, 5750.
[21] X. Zou, L. Zhang, Z. Wang, Y. Luo, J. Am. Chem. Soc. 2016, 138,
2064.
[22] H. Nikaido, Science 1994, 264, 382.
[23] L. Brown, J. M. Wolf, R. Prados-Rosales, A. Casadevall, Nat. Rev.
Microbiol. 2015, 13, 620.
[24] C. Sohlenkamp, O. Geiger, FEMS Microbiol Rev. 2016, 40, 133.
[25] G. van Meer, A. I. de Kroon. J. Cell Sci. 2011, 124, 5.
[26] G. Jacquemet, H. Hamidi, J. Ivaska, Curr. Opin. Cell Biol. 2015, 36,
23.
[27] W. C. Lee, C. H. Lim, H. Shi, L. A. Tang, Y. Wang, C. T. Lim,
K. P. Loh, ACS Nano 2011, 5, 7334.
[28] T. R. Nayak, H. Andersen, V. S. Makam, C. Khaw, S. Bae, X. Xu,
P. L. Ee, J. H. Ahn, B. H. Hong, G. Pastorin, B. Özyilmaz, ACS Nano
2011, 5, 4670.
[29] B. Zhang, P. Wei, Z. Zhou, T. Wei, Adv. Drug Delivery Rev. 2016, 105,
145.
© 2018 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim
www.advancedsciencenews.com
www.advmatinterfaces.de

[30] R. B. Song, C. E. Zhao, L. P. Jiang, E. S. Abdel-Halim, J. R. Zhang,
J. J. Zhu, ACS Appl. Mater. Interfaces 2016, 8, 16170.
[31] E. Akbari, Z. Buntat, A. Afroozeh, A. Zeinalinezhad, I. E. T. Nikoukar,
Nanobiotechnology 2015, 9, 273.
[32] Y. Li, H. Yuan, A. von dem Bussche, M. Creighton, R. H. Hurt,
A. B. Kane, H. Gao, Proc. Natl. Acad. Sci. USA 2013, 110, 12295.
[33] C. Xu, J. Wang, Y. Xu, G. Shang, R. Wang, Y. Lin, Curr. Drug Metab.
2013, 14, 863.
[34] N. Chatterjee, H. J. Eom, J. Choi, Biomaterials 2014, 35, 1109.
[35] P. Choudhary, T. Parandhaman, B. Ramalingam, N. Duraipandy,
M. S. Kiran, S. K. Das, ACS Appl. Mater. Interfaces 2017, 9,
38255.

Adv. Mater. Interfaces 2018, 1701331 1701331  (9 of 9) © 2018 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim