Please wait a minute...
Frontiers of Materials Science

ISSN 2095-025X

ISSN 2095-0268(Online)

CN 11-5985/TB

Postal Subscription Code 80-974

2018 Impact Factor: 1.701

Front. Mater. Sci.    2014, Vol. 8 Issue (2) : 107-122    https://doi.org/10.1007/s11706-014-0228-x
REVIEW ARTICLE
The development of graphene-based devices for cell biology research
Zhi-Qin YAN1,Wei ZHANG2,*()
1. School of Mechanical, Jinzhong University, Yuci, Jinzhong 030600, China
2. CAS Key Laboratory for Biomedical Effects of Nanomaterials and Nanosafety, National Center for Nanoscience and Technology, 11 Beiyitiao, Zhongguancun, Beijing 100190, China
 Download: PDF(1656 KB)   HTML
 Export: BibTeX | EndNote | Reference Manager | ProCite | RefWorks
Abstract

Graphene has emerged as a new carbon nanoform with great potential in many applications due to its exceptional physical and chemical properties. Especially, graphene and its derivatives are also gaining a lot of interest in the biomedical field as new components for biosensors, tissue engineering, and drug delivery. This review presents unique properties of graphene, the bio-effects of graphene and its derivatives, especially their interactions with cells and the development of graphene-based biosensors and nanomedicines for cancer diagnosis and treatment.

Keywords graphene      graphene oxide (GO)      cell      sensor      cancer     
Corresponding Author(s): Wei ZHANG   
Issue Date: 24 June 2014
 Cite this article:   
Zhi-Qin YAN,Wei ZHANG. The development of graphene-based devices for cell biology research[J]. Front. Mater. Sci., 2014, 8(2): 107-122.
 URL:  
https://academic.hep.com.cn/foms/EN/10.1007/s11706-014-0228-x
https://academic.hep.com.cn/foms/EN/Y2014/V8/I2/107
Fig.1  SGS internalization within Hep3B cancer cells. (a)(b)(c)(d)(e)(f) Transmission electron microscopy (TEM) images of internalized carbonaceous material and SGSs within Hep3B liver cancer cells. (Reproduced with permission from Ref. [28]).
Fig.2  (a) The differentiation of NSCs on 3D-glial fibrillary (GF) scaffold. Left, Western blot analysis of nestin, Tuj1, glial fibrillary acidic protein (GFAP) and receptor-interacting protein (RIP) protein expression of differentiated NSCs on 2D graphene films and 3D-GFs; Right, relative optical densities of nestin, Tuj1, GFAP and RIP bands. (Reproduced with permission from Ref. [39]). (b) Fluorescence images of hNSCs differentiated on glass (left) and graphene (right) after one month differentiation. The differentiated hNSCs were immunostained with GFAP (red) for astroglial cells, class III β-tubulin (TUJ1) (green) for neural cells, and 4′,6-diamidino-2-phenylindole (DAPI) (blue) for nuclei. Note that more hNSCs were adhered to graphene than to glass. Scale bars= 200 μm. (Reproduced with permission from Ref. [41]).
Fig.3  GO chip and functionalization/characterization of GO. (a) Schematic of the GO chip. (b) Schematic showing the conjugation chemistry between functionalized GO nanosheets and EpCAM antibodies. GO nanosheets are adsorbed onto the gold pattern. The N-(g-maleimidobutyryloxy) succinimide ester (GMBS) cross-linker binds to PL-PEG-NH2 on the GO nanosheets. The NeutrAvidin is connected to the GMBS and biotinylated EpCAM. (c) Preparation procedures for the functionalized GO. (Reproduced with permission from Ref. [57]).
Fig.4  Top, fluorescence images of the MCF-7/ADR cells after the incubation with GQDs, DOX and DOX/GQDs: (a) bright-field, (b) nuclei stained by Hoechst, (c) fluorescence of DOX excited at 510 nm, and (d) overlays of (a), (b), and (c). Scale bars= 50 μm. Bottom, cell viability of the MCF-7/ADR cells exposed to different concentrations of DOX alone (dark bars) and DOX with GQDs for 24 h (grey bars). The control samples are the untreated cells and the cells with GQDs only (gray bar). (Reproduced with permission from Ref. [<CitationRef CitationID="cit68"></CitationRef>]).
Fig.5  (a) Schematic illustration of the synthetic procedure for UCNPs-NGO: Numbers of core-shell structured UCNPs being covalently grafted with NGO via bifunctional polyethylene glycol. (b) Schematic illustration of UCNPs-NGO/ZnPc as a multifunctional theranostic nanoplatform for cancer treatment. (Reproduced with permission from Ref. [73]).
1 Novoselov K S, Geim A K, Morozov S V, . Electric field effect in atomically thin carbon films. Science, 2004, 306(5696): 666–669
2 Huang X, Qi X Y, Boey F, . Graphene-based composites. Chemical Society Reviews, 2012, 41(2): 666–686
3 Gunlycke D, Lawler H M, White C T. Room-temperature ballistic transport in narrow graphene strips. Physical Review B: Condensed Matter and Materials Physics, 2007, 75(8): 085418 (5 pages)
4 Novoselov K S, Jiang Z, Zhang Y, . Room-temperature quantum Hall effect in graphene. Science, 2007, 315(5817): 1379
5 Zhang Y B, Tan Y W, Stormer H L, . Experimental observation of the quantum Hall effect and Berry’s phase in graphene. Nature, 2005, 438(7065): 201–204
6 Nair R R, Blake P, Grigorenko A N, . Fine structure constant defines visual transparency of graphene. Science, 2008, 320(5881): 1308
7 Xia F N, Mueller T, Lin Y M, . Ultrafast graphene photodetector. Nature Nanotechnology, 2009, 4(12): 839–843
8 Gómez-Navarro C, Burghard M, Kern K. Elastic properties of chemically derived single graphene sheets. Nano Letters, 2008, 8(7): 2045–2049
9 Dikin D A, Stankovich S, Zimney E J, . Preparation and characterization of graphene oxide paper. Nature, 2007, 448(7152): 457–460
10 Balandin A A, Ghosh S, Bao W Z, . Superior thermal conductivity of single-layer graphene. Nano Letters, 2008, 8(3): 902–907
11 Wang Y, Li Z H, Wang J, . Graphene and graphene oxide: biofunctionalization and applications in biotechnology. Trends in Biotechnology, 2011, 29(5): 205–212
12 Ryoo S R, Kim Y K, Kim M H, . Behaviors of NIH-3T3 fibroblasts on graphene/carbon nanotubes: proliferation, focal adhesion, and gene transfection studies. ACS Nano, 2010, 4(11): 6587–6598
13 Chang Y, Yang S T, Liu J H, . In vitro toxicity evaluation of graphene oxide on A549 cells. Toxicology Letters, 2011, 200(3): 201–210
14 Gurunathan S, Han J W, Eppakayala V, . Biocompatibility of microbially reduced graphene oxide in primary mouse embryonic fibroblast cells. Colloids and surfaces B: Biointerfaces, 2013, 105: 58–66
15 Zhang H, Peng C, Yang J Z, . Uniform ultrasmall graphene oxide nanosheets with low cytotoxicity and high cellular uptake. ACS Applied Materials & Interfaces, 2013, 5(5): 1761–1767
16 Waiwijit U, Kandhavivorn W, Oonkhanond B, . Cytotoxicity assessment of MDA-MB-231 breast cancer cells on screen-printed graphene–carbon paste substrate. Colloids and surfaces B: Biointerfaces, 2014, 113: 190–197
17 Zhang Y, Ali S F, Dervishi E, . Cytotoxicity effects of graphene and single-wall carbon nanotubes in neural phaeochromocytoma-derived PC12 cells. ACS Nano, 2010, 4(6): 3181–3186
18 Wang K, Ruan J, Song H, . Biocompatibility of graphene oxide. Nanoscale Research Letters, 2011, 6: 8
19 Gurunathan S, Han J W, Eppakayala V, . Green synthesis of graphene and its cytotoxic effects in human breast cancer cells. International Journal of Nanomedicine, 2013, 8: 1015–1027
20 Jaworski S, Sawosz E, Grodzik M, . In vitro evaluation of the effects of graphene platelets on glioblastoma multiforme cells. International Journal of Nanomedicine, 2013, 8: 413–420
21 Horvath L, Magrez A, Burghard M, . Evaluation of the toxicity of graphene derivatives on cells of the lung luminal surface. Carbon, 2013, 64: 45–60
22 Qu G B, Liu S J, Zhang S P, . Graphene oxide induces toll-like receptor 4 (TLR4)-dependent necrosis in macrophages. ACS Nano, 2013, 7(7): 5732–5745
23 Das S, Singh S, Singh V, . Oxygenated functional group density on graphene oxide: its effect on cell toxicity. Particle & Particle Systems Characterization, 2013, 30(2): 148–157
24 Kim J A, ?berg C, Salvati A, . Role of cell cycle on the cellular uptake and dilution of nanoparticles in a cell population. Nature Nanotechnology, 2012, 7(1): 62–68
25 Yue H, Wei W, Yue Z G, . The role of the lateral dimension of graphene oxide in the regulation of cellular responses. Biomaterials, 2012, 33(16): 4013–4021
26 Makharza S, Cirillo G, Bachmatiuk A, . Size-dependent nanographene oxide as a platform for efficient carboplatin release. Journal of Materials Chemistry B, 2013, 1: 6107–6114
27 Lammel T, Boisseaux P, Fernandez-Cruz M-L, . Internalization and cytotoxicity of graphene oxide and carboxyl graphene nanoplatelets in the human hepatocellular carcinoma cell line Hep G2. Particle and Fibre Toxicology, 2013, 10: 27
28 Corr S J, Raoof M, Cisneros B T, . Cytotoxicity and variant cellular internalization behavior of water-soluble sulfonated nanographene sheets in liver cancer cells. Nanoscale Research Letters, 2013, 8: 208
29 Wu C, Wang C, Han T, . Insight into the cellular internalization and cytotoxicity of graphene quantum dots. Advanced Healthcare Materials, 2013
doi: 10.1002/adhm.201300066
30 Na H K, Kim M H, Lee J, . Cytoprotective effects of graphene oxide for mammalian cells against internalization of exogenous materials. Nanoscale, 2013, 5(4): 1669–1677
31 Marconi E, Nieus T, Maccione A, . Emergent functional properties of neuronal networks with controlled topology. PLoS ONE, 2012, 7(4): e34648
32 Strong V, Dubin S, El-Kady M F, . Patterning and electronic tuning of laser scribed graphene for flexible all-carbon devices. ACS Nano, 2012, 6(2): 1395–1403
33 Lorenzoni M, Brandi F, Dante S, . Simple and effective graphene laser processing for neuron patterning application. Scientific Reports, 2013, 3: 1954
34 Tu Q, Pang L, Chen Y, . Effects of surface charges of graphene oxide on neuronal outgrowth and branching. Analyst, 2014, 139(1): 105–115
35 Crowder S W, Prasai D, Rath R, . Three-dimensional graphene foams promote osteogenic differentiation of human mesenchymal stem cells. Nanoscale, 2013, 5(10): 4171–4176
36 Akhavan O, Ghaderi E, Shahsavar M. Graphene nanogrids for selective and fast osteogenic differentiation of human mesenchy-mal stem cells. Carbon, 2013, 59: 200–211
37 Ku S H, Park C B. Myoblast differentiation on graphene oxide. Biomaterials, 2013, 34(8): 2017–2023
38 Lv M, Zhang Y, Liang L, . Effect of graphene oxide on undifferentiated and retinoic acid-differentiated SH-SY5Y cells line. Nanoscale, 2012, 4(13): 3861–3866
39 Li N, Zhang Q, Gao S, . Three-dimensional graphene foam as a biocompatible and conductive scaffold for neural stem cells. Scientific Reports, 2013, 3: 1604
40 Akhavan O, Ghaderia E. Differentiation of human neural stem cells into neural networks on graphene nanogrids. Journal of Materials Chemistry B, 2013, 1(45): 6291–6301
41 Park S Y, Park J, Sim S H, . Enhanced differentiation of human neural stem cells into neurons on graphene. Advanced Materials, 2011, 23(36): H263–H267
42 Castillo J J, Svendsen W E, Rozlosnik N, . Detection of cancer cells using a peptide nanotube-folic acid modified graphene electrode. Analyst, 2013, 138(4): 1026–1031
43 Guo C X, Ng S R, Khoo S Y, . RGD-peptide functionalized graphene biomimetic live-cell sensor for real-time detection of nitric oxide molecules. ACS Nano, 2012, 6(8): 6944–6951
44 Zhang B, Li Q, Cui T H. Ultra-sensitive suspended graphene nanocomposite cancer sensors with strong suppression of electrical noise. Biosensors & Bioelectronics, 2012, 31(1): 105–109
45 Cohen-Karni T, Qing Q, Li Q, . Graphene and nanowire transistors for cellular interfaces and electrical recording. Nano Letters, 2010, 10(3): 1098–1102
46 He Q Y, Sudibya H G, Yin Z Y, . Centimeter-long and large-scale micropatterns of reduced graphene oxide films: fabrication and sensing applications. ACS Nano, 2010, 4(6): 3201–3208
47 Kim D J, Sohn I Y, Jung J H, . Reduced graphene oxide field-effect transistor for label-free femtomolar protein detection. Biosensors and Bioelectronics, 2013, 41: 621–626
48 Liu Z M, Guo Z Y, Zhong H Q, . Graphene oxide based surface-enhanced Raman scattering probes for cancer cell imaging. Physical Chemistry Chemical Physics, 2013, 15(8): 2961–2966
49 Hu C F, Liu Y L, Qin J L, . Fabrication of reduced graphene oxide and sliver nanoparticle hybrids for Raman detection of absorbed folic acid: a potential cancer diagnostic probe. ACS Applied Materials & Interfaces, 2013, 5(11): 4760–4768
50 Liu Q H, Wei L, Wang J Y, . Cell imaging by graphene oxide based on surface enhanced Raman scattering. Nanoscale, 2012, 4(22): 7084–7089
51 Pan D, Zhang J, Li Z, . Hydrothermal route for cutting graphene sheets into blue-luminescent graphene quantum dots. Advanced Materials, 2010, 22(6): 734–738
52 Zhu S, Tang S, Zhang J, . Control the size and surface chemistry of graphene for the rising fluorescent materials. Chemical Communications, 2012, 48(38): 4527–4539
53 Zhang X, Wang S, Liu M, . Size tunable fluorescent nano-graphite oxides: preparation and cell imaging applications. Physical Chemistry Chemical Physics, 2013, 15(43): 19013–19018
54 Sheng Y, Tang X S, Peng E W, . Graphene oxide based fluorescent nanocomposites for cellular imaging. Journal of Materials Chemistry B, 2013, 1(4): 512–521
55 Chen M L, He Y J, Chen X W, . Quantum-dot-conjugated graphene as a probe for simultaneous cancer-targeted fluorescent imaging, tracking, and monitoring drug delivery. Bioconjugate Chemistry, 2013, 24(3): 387–397
56 Yue Z G, Lv P P, Yue H, . Inducible graphene oxide probe for high-specific tumor diagnosis. Chemical Communications, 2013, 49(37): 3902–3904
57 Yoon H J, Kim T H, Zhang Z, . Sensitive capture of circulating tumour cells by functionalized graphene oxide nanosheets. Nature Nanotechnology, 2013, 8: 735–741
58 Sheng Z H, Song L, Zheng J X, . Protein-assisted fabrication of nano-reduced graphene oxide for combined in vivo photoacoustic imaging and photothermal therapy. Biomaterials, 2013, 34(21): 5236–5243
59 Tang L A L, Wang J Z, Lim T K, . High-performance graphene–titania platform for detection of phosphopeptides in cancer cells. Analytical Chemistry, 2012, 84(15): 6693–6700
60 Mao X W, Li H B. Chiral imaging in living cells with functionalized graphene oxide. Journal of Materials Chemistry B, 2013, 1(34): 4267–4272
61 Liu Z, Robinson J T, Sun X M, . PEGylated nanographene oxide for delivery of water-insoluble cancer drugs. Journal of the American Chemical Society, 2008, 130(33): 10876–10877
62 Yang X Y, Zhang X Y, Liu Z F, . High-efficiency loading and controlled release of doxorubicin hydrochloride on graphene oxide. Journal of Physical Chemistry C, 2008, 112(45): 17554–17558
63 Wu J, Wang Y S, Yang X Y, . Graphene oxide used as a carrier for adriamycin can reverse drug resistance in breast cancer cells. Nanotechnology, 2012, 23(35): 355101
64 Zhi F, Dong H F, Jia X F, . Functionalized graphene oxide mediated adriamycin delivery and miR-21 gene silencing to overcome tumor multidrug resistance in vitro. PLoS ONE, 2013, 8(3): e60034
65 Chang Y L, Yang S T, Liu J H, . In vitro toxicity evaluation of graphene oxide on A549 cells. Toxicology Letters, 2011, 200(3): 201–210
66 Liu J-H, Yang S-T, Wang H-F, . Effect of size and dose on the biodistribution of graphene oxide in mice. Nanomedicine, 2012, 7(12): 1801–1812
67 Jin R, Ji X J, Yang Y X, . Self-assembled graphene-dextran nanohybrid for killing drug-resistant cancer cells. ACS Applied Materials & Interfaces, 2013, 5(15): 7181–7189
68 Wang C, Wu C Y, Zhou X J, . Enhancing cell nucleus accumulation and DNA cleavage activity of anti-cancer drug via graphene quantum dots. Scientific Reports, 2013, 3: 2852
69 Qin X C, Guo Z Y, Liu Z M, . Folic acid-conjugated graphene oxide for cancer targeted chemo-photothermal therapy. Journal of Photochemistry and Photobiology B: Biology, 2013, 120: 156–162
70 Wang Y W, Fu Y Y, Peng Q L, . Dye-enhanced graphene oxide for photothermal therapy and photoacoustic imaging. Journal of Materials Chemistry B, 2013, 1(42): 5762–5767
71 Wu S W, Han G, Milliron D J, . Non-blinking and photostable upconverted luminescence from single lanthanide-doped nanocrystals. Proceedings of the National Academy of Sciences of the United States of America, 2009, 106(27): 10917–10921
72 Zhou J, Liu Z, Li F Y. Upconversion nanophosphors for small-animal imaging. Chemical Society Reviews, 2012, 41(3): 1323–1349
73 Wang Y, Wang H, Liu D, . Graphene oxide covalently grafted upconversion nanoparticles for combined NIR mediated imaging and photothermal/photodynamic cancer therapy. Biomaterials, 2013, 34(31): 7715–7724
[1] Shalmali BASU, Kamalika SEN. A review on graphene-based materials as versatile cancer biomarker sensors[J]. Front. Mater. Sci., 2020, 14(4): 353-372.
[2] Biyu ZHOU, Junbo LI, Binzhong LU, Wenlan WU, Leitao ZHANG, Ju LIANG, Junpeng YI, Xin LI. Novel polyzwitterion shell with adaptable surface chemistry engineered to enhance anti-fouling and intracellular imaging of detonation nanodiamonds under tumor pHe[J]. Front. Mater. Sci., 2020, 14(4): 402-412.
[3] Zhenxiao LU, Wenxian WANG, Jun ZHOU, Zhongchao BAI. FeS2@C nanorods embedded in three-dimensional graphene as high-performance anode for sodium-ion batteries[J]. Front. Mater. Sci., 2020, 14(3): 255-265.
[4] Kun YANG, Jinghuan TIAN, Wei QU, Bo LUAN, Ke LIU, Jun LIU, Likui WANG, Junhui JI, Wei ZHANG. Host-mediated biofilm forming promotes post-graphene pathogen expansion via graphene micron-sheet[J]. Front. Mater. Sci., 2020, 14(2): 221-231.
[5] Huan-Yan XU, Dan LU, Xu HAN. Graphene-induced enhanced anticorrosion performance of waterborne epoxy resin coating[J]. Front. Mater. Sci., 2020, 14(2): 211-220.
[6] Jinxing ZHANG, Kexing HU, Qi OUYANG, Qilin GUI, Xiaonong CHEN. One-step functionalization of graphene via Diels--Alder reaction for improvement of dispersibility[J]. Front. Mater. Sci., 2020, 14(2): 198-210.
[7] Rui ZHU, Feiyang LIU, Zixing WANG, Bin WEI, Guo CHEN. Investigation of post-thermal annealing-induced enhancement in photovoltaic performance for squaraine-based organic solar cells[J]. Front. Mater. Sci., 2020, 14(1): 81-88.
[8] Wei SUN, Rui ZHAO, Tian WANG, Ke ZHAN, Zheng YANG, Bin ZHAO, Ya YAN. An approach to prepare uniform graphene oxide/aluminum composite powders by simple electrostatic interaction in water/alcohol solution[J]. Front. Mater. Sci., 2019, 13(4): 375-381.
[9] Xia HE, Qingchun LIU, Jiajun WANG, Huiling CHEN. Wearable gas/strain sensors based on reduced graphene oxide/linen fabrics[J]. Front. Mater. Sci., 2019, 13(3): 305-313.
[10] Ram Sevak SINGH, Anurag GAUTAM, Varun RAI. Graphene-based bipolar plates for polymer electrolyte membrane fuel cells[J]. Front. Mater. Sci., 2019, 13(3): 217-241.
[11] Chaoyuan LIU, Zhongbing HUANG, Ximing PU, Lei SHANG, Guangfu YIN, Xianchun CHEN, Shuang CHENG. Fabrication of carboxylic graphene oxide-composited polypyrrole film for neurite growth under electrical stimulation[J]. Front. Mater. Sci., 2019, 13(3): 258-269.
[12] Bin CAI, Changxiang SHAO, Liangti QU, Yuning MENG, Lin JIN. Preparation of sulfur-doped graphene fibers and their application in flexible fibriform micro-supercapacitors[J]. Front. Mater. Sci., 2019, 13(2): 145-155.
[13] Ruiping LIU, Ning ZHANG, Xinyu WANG, Chenhui YANG, Hui CHENG, Hanqing ZHAO. SnO2 nanoparticles anchored on graphene oxide as advanced anode materials for high-performance lithium-ion batteries[J]. Front. Mater. Sci., 2019, 13(2): 186-192.
[14] Chao WANG, Wu WANG, Ke HE, Shantang LIU. Pr-doped In2O3 nanocubes induce oxygen vacancies for enhancing triethylamine gas-sensing performance[J]. Front. Mater. Sci., 2019, 13(2): 174-185.
[15] Maria COROŞ, Florina POGĂCEAN, Lidia MĂGERUŞAN, Crina SOCACI, Stela PRUNEANU. A brief overview on synthesis and applications of graphene and graphene-based nanomaterials[J]. Front. Mater. Sci., 2019, 13(1): 23-32.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed