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Graphene: an emerging material for biological tissue engineering
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  • Journal title : Carbon letters
  • Volume 14, Issue 2,  2013, pp.63-75
  • Publisher : Korean Carbon Society
  • DOI : 10.5714/CL.2013.14.2.063
 Title & Authors
Graphene: an emerging material for biological tissue engineering
Lee, Sang Kyu; Kim, Hyun; Shim, Bong Sup;
  PDF(new window)
 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.
 Keywords
graphene;graphene oxide;carbon nanomaterials;tissue engineering;cell scaffolds;drug delivery;neural interface;biomaterials;biocompatibility;
 Language
English
 Cited by
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Bioelectronics with two-dimensional materials, Microelectronic Engineering, 2016, 161, 18  crossref(new windwow)
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Electrostatic self-assembled graphene oxide-collagen scaffolds towards a three-dimensional microenvironment for biomimetic applications, RSC Adv., 2016, 6, 54, 49039  crossref(new windwow)
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 References
1.
Stolyarova E, Rim KT, Ryu S, Maultzsch J, Kim P, Brus LE, Heinz TF, Hybertsen MS, Flynn GW. High-resolution scanning tunneling microscopy imaging of mesoscopic graphene sheets on an insulating surface. Proc Natl Acad Sci USA, 104, 9209 (2007). http:// dx.doi.org/10.1073/pnas.0703337104. crossref(new window)

2.
Emtsev KV, Bostwick A, Horn K, Jobst J, Kellogg GL, Ley L, McChesney JL, Ohta T, Reshanov SA, Rohrl J, Rotenberg E, Schmid AK, Waldmann D, Weber HB, Seyller T. Towards wafersize graphene layers by atmospheric pressure graphitization of silicon carbide. Nat Mater, 8, 203 (2009). http://dx.doi.org/10.1038/nmat2382. crossref(new window)

3.
Kim KS, Zhao Y, Jang H, Lee SY, Kim JM, Ahn JH, Kim P, Choi JY, Hong BH. Large-scale pattern growth of graphene films for stretchable transparent electrodes. Nature, 457, 706 (2009). http:// dx.doi.org/10.1038/nature07719. crossref(new window)

4.
Li D, Muller MB, Gilje S, Kaner RB, Wallace GG. Processable aqueous dispersions of graphene nanosheets. Nat Nanotechnol, 3, 101 (2008). http://dx.doi.org/10.1038/nnano.2007.451. crossref(new window)

5.
He HY, Klinowski J, Forster M, Lerf A. A new structural model for graphite oxide. Chem Phys Lett, 287, 53 (1998). http://dx.doi. org/10.1016/s0009-2614(98)00144-4. crossref(new window)

6.
Singh V, Joung D, Zhai L, Das S, Khondaker SI, Seal S. Graphene based materials: past, present and future. Prog Mater Sci, 56, 1178 (2011). http://dx.doi.org/10.1016/j.pmatsci.2011.03.003. crossref(new window)

7.
Guo SJ, Dong SJ. Graphene nanosheet: synthesis, molecular engineering, thin film, hybrids, and energy and analytical applications. Chem Soc Rev, 40, 2644 (2011). http://dx.doi.org/10.1039/c0cs00079e. crossref(new window)

8.
Shao YY, Wang J, Wu H, Liu J, Aksay IA, Lin YH. Graphene based electrochemical sensors and biosensors: a review. Electroanalysis, 22, 1027 (2010). http://dx.doi.org/10.1002/elan.200900571. crossref(new window)

9.
Wassei JK, Kaner RB. Graphene, a promising transparent conductor. Mater Today, 13, 52 (2010). http://dx.doi.org/10.1016/S1369-7021(10)70034-1. crossref(new window)

10.
Wan XJ, Long GK, Huang L, Chen YS. Graphene: a promising material for organic photovoltaic cells. Adv Mater, 23, 5342 (2011). http://dx.doi.org/10.1002/adma.201102735. crossref(new window)

11.
Pang SP, Hernandez Y, Feng XL, Mullen K. Graphene as transparent electrode material for organic electronics. Adv Mater, 23, 2779 (2011). http://dx.doi.org/10.1002/adma.201100304. crossref(new window)

12.
Moon JS, Antcliffe M, Seo HC, Lin SC, Schmitz A, Milosavljevic I, McCalla K, Wong D, Gaskill DK, Campbell PM, Lee KM, Asbeck P. Graphene review: an emerging RF technology. Proceedings of the IEEE 12th Topical Meeting on Silicon Monolithic Integrated Circuits in RF Systems, Santa Clara, CA, 199 (2012). http://dx.doi. org/10.1109/SiRF.2012.6160170. crossref(new window)

13.
Dreyer DR, Park S, Bielawski CW, Ruoff RS. The chemistry of graphene oxide. Chem Soc Rev, 39, 228 (2010). http://dx.doi. org/10.1039/b917103g. crossref(new window)

14.
Zhang XY, Yin JL, Peng C, Hu WQ, Zhu ZY, Li WX, Fan CH, Huang Q. Distribution and biocompatibility studies of graphene oxide in mice after intravenous administration. Carbon, 49, 986 (2011). http://dx.doi.org/10.1016/j.carbon.2010.11.005. crossref(new window)

15.
Mutlu GkM, Budinger GRS, Green AA, Urich D, Soberanes S, Chiarella SE, Alheid GF, McCrimmon DR, Szleifer I, Hersam MC. Biocompatible nanoscale dispersion of single-walled carbon nanotubes minimizes in vivo pulmonary toxicity. Nano Lett, 10, 1664 (2010). http://dx.doi.org/10.1021/nl9042483. crossref(new window)

16.
Poland CA, Duffin R, Kinloch I, Maynard A, Wallace WAH, Seaton A, Stone V, Brown S, MacNee W, Donaldson K. Carbon nanotubes introduced into the abdominal cavity of mice show as-bestos-like pathogenicity in a pilot study. Nat Nanotechnol, 3, 423 (2008). http://dx.doi.org/10.1038/nnano.2008.111. crossref(new window)

17.
Yang K, Wan J, Zhang S, Zhang Y, Lee ST, Liu Z. In vivo pharmacokinetics, long-term biodistribution, and toxicology of PEGylated graphene in mice. ACS Nano, 5, 516 (2010). http://dx.doi. org/10.1021/nn1024303. crossref(new window)

18.
Park S, Mohanty N, Suk JW, Nagaraja A, An JH, Piner RD, Cai WW, Dreyer DR, Berry V, Ruoff RS. Biocompatible, robust free-standing paper composed of a TWEEN/graphene composite. Adv Mater, 22, 1736 (2010). http://dx.doi.org/10.1002/adma.200903611. crossref(new window)

19.
Kalbacova M, Broz A, Kong J, Kalbac M. Graphene substrates promote adherence of human osteoblasts and mesenchymal stromal cells. Carbon, 48, 4323 (2010). http://dx.doi.org/10.1016/j.carbon.2010.07.045. crossref(new window)

20.
Guo CX, Zheng XT, Lu ZS, Lou XW, Li CM. Biointerface by cell growth on layered graphene-artificial peroxidase-protein nanostructure for in situ quantitative molecular detection. Adv Mater, 22, 5164 (2010). http://dx.doi.org/10.1002/adma.201001699. crossref(new window)

21.
Ryoo SR, Kim YK, Kim MH, Min DH. Behaviors of NIH-3T3 fibroblasts on graphene/carbon nanotubes: proliferation, focal adhesion, and gene transfection studies. ACS Nano, 4, 6587 (2010). http://dx.doi.org/10.1021/nn1018279. crossref(new window)

22.
Hu W, Peng C, Luo W, Lv M, Li X, Li D, Huang Q, Fan C. Graphene-based antibacterial paper. ACS Nano, 4, 4317 (2010). http:// dx.doi.org/10.1021/nn101097v. crossref(new window)

23.
Chang Y, Yang ST, Liu JH, Dong E, Wang Y, Cao A, Liu Y, Wang H. In vitro toxicity evaluation of graphene oxide on A549 cells. Toxicol Lett, 200, 201 (2011). http://dx.doi.org/10.1016/j.toxlet.2010.11.016 crossref(new window)

24.
Park SY, Park J, Sim SH, Sung MG, Kim KS, Hong BH, Hong S. Enhanced differentiation of human neural stem cells into neurons on graphene. Adv Mater, 23, H263 (2011). http://dx.doi. org/10.1002/adma.201101503. crossref(new window)

25.
Li N, Zhang X, Song Q, Su R, Zhang Q, Kong T, Liu L, Jin G, Tang M, Cheng G. The promotion of neurite sprouting and outgrowth of mouse hippocampal cells in culture by graphene substrates. Biomaterials, 32, 9374 (2011). http://dx.doi.org/http://dx.doi.org/ 10.1016/j.biomaterials.2011.08.065. crossref(new window)

26.
Sayyar S, Murray E, Thompson BC, Gambhir S, Officer DL, Wallace GG. Covalently linked biocompatible graphene/polycaprolactone composites for tissue engineering. Carbon, 52, 296 (2013). http://dx.doi.org/10.1016/j.carbon.2012.09.031. crossref(new window)

27.
Fan HL, Wang LL, Zhao KK, Li N, Shi ZJ, Ge ZG, Jin ZX. Fabrication, mechanical properties, and biocompatibility of graphenereinforced chitosan composites. Biomacromolecules, 11, 2345 (2010). http://dx.doi.org/10.1021/bm100470q. crossref(new window)

28.
Lim HN, Huang NM, Lim SS, Harrison I, Chia CH. Fabrication and characterization of graphene hydrogel via hydrothermal approach as a scaffold for preliminary study of cell growth. Int J Nanomed, 6, 1817 (2011). http://dx.doi.org/10.2147/ijn.s23392. crossref(new window)

29.
Yang G, Su J, Gao J, Hu X, Geng C, Fu Q. Fabrication of well-controlled porous foams of graphene oxide modified poly(propylenecarbonate) using supercritical carbon dioxide and its potential tissue engineering applications. J Supercrit Fluids, 73, 1 (2013). http://dx.doi.org/10.1016/j.supflu.2012.11.004. crossref(new window)

30.
Chen GY, Pang DWP, Hwang SM, Tuan HY, Hu YC. A graphene-based platform for induced pluripotent stem cells culture and differentiation. Biomaterials, 33, 418 (2012). http://dx.doi.org/10.1016/j.biomaterials.2011.09.071. crossref(new window)

31.
Wang Y, Lee WC, Manga KK, Ang PK, Lu J, Liu YP, Lim CT, Loh KP. Fluorinated graphene for promoting neuro-induction of stem cells. Adv Mater, 24, 4285 (2012). http://dx.doi.org/10.1002/adma.201200846. crossref(new window)

32.
Ku SH, Park CB. Myoblast differentiation on graphene oxide. Biomaterials, 34, 2017 (2013). http://dx.doi.org/10.1016/j.biomaterials.2012.11.052. crossref(new window)

33.
Sebaa M, Nguyen TY, Paul RK, Mulchandani A, Liu H. Graphene and carbon nanotube-graphene hybrid nanomaterials for human embryonic stem cell culture. Mater Lett, 92, 122 (2013). http:// dx.doi.org/10.1016/j.matlet.2012.10.035. crossref(new window)

34.
Park HB, Nam HG, Oh HG, Kim JH, Kim CM, Song KS, Jhee KH. Effect of graphene on growth of neuroblastoma cells. J Microbiol Biotechnol, 23, 274 (2013). crossref(new window)

35.
Orive G, Anitua E, Pedraz JL, Emerich DF. Biomaterials for promoting brain protection, repair and regeneration. Nat Rev Neurosci, 10, 682 (2009). http://dx.doi.org/10.1038/nrn2685. crossref(new window)

36.
Allen TM, Cullis PR. Drug delivery systems: Entering the mainstream. Science, 303, 1818 (2004). http://dx.doi.org/10.1126/science.1095833. crossref(new window)

37.
Liu Z, Robinson JT, Sun X, Dai H. PEGylated nanographene oxide for delivery of water-insoluble cancer drugs. J Am Chem Soc, 130, 10876 (2008). http://dx.doi.org/10.1021/ja803688x. crossref(new window)

38.
Yang X, Zhang X, Ma Y, Huang Y, Wang Y, Chen Y. Superparamagnetic graphene oxide-Fe3O4 nanoparticles hybrid for controlled targeted drug carriers. J Mater Chem, 19, 2710 (2009). http:// dx.doi.org/10.1039/B821416F. crossref(new window)

39.
Depan D, Shah J, Misra RDK. Controlled release of drug from folate-decorated and graphene mediated drug delivery system: synthesis, loading efficiency, and drug release response. Mater Sci Eng C, 31, 1305 (2011). http://dx.doi.org/10.1016/j.msec.2011.04.010. crossref(new window)

40.
Liu K, Zhang JJ, Cheng FF, Zheng TT, Wang C, Zhu JJ. Green and facile synthesis of highly biocompatible graphene nanosheets and its application for cellular imaging and drug delivery. J Mater Chem, 21, 12034 (2011). http://dx.doi.org/10.1039/C1JM10749. crossref(new window)

41.
Bao H, Pan Y, Ping Y, Sahoo NG, Wu T, Li L, Li J, Gan LH. Chitosan-functionalized graphene oxide as a nanocarrier for drug and gene delivery. Small, 7, 1569 (2011). http://dx.doi.org/10.1002/smll.201100191. crossref(new window)

42.
Cogan SF. Neural stimulation and recording electrodes. Annu Rev Biomed Eng, 10, 275 (2008). http://dx.doi.org/10.1146/annurev.bioeng.10.061807.160518. crossref(new window)

43.
Nam Y. Material considerations for in vitro neural interface technology. MRS Bull, 37, 566 (2012). http://dx.doi.org/10.1557/mrs.2012.98. crossref(new window)

44.
Ordonez J, Schuettler M, Boehler C, Boretius T, Stieglitz T. Thin films and microelectrode arrays for neuroprosthetics. MRS Bull, 37, 590 (2012). http://dx.doi.org/doi:10.1557/mrs.2012.117. crossref(new window)

45.
Wallace G, Spinks G. Conducting polymers--bridging the bionic interface. Soft Matter, 3, 665 (2007). http://dx.doi.org/10.1039/b618204f. crossref(new window)

46.
Wallace GG, Spinks GM. Conducting polymers--a bridge across the bionic interface. Chem Eng Prog, 103, S18 (2007).

47.
Green RA, Lovell NH, Wallace GG, Poole-Warren LA. Conducting polymers for neural interfaces: challenges in developing an effective long-term implant. Biomaterials, 29, 3393 (2008). http:// dx.doi.org/10.1016/j.biomaterials.2008.04.047. crossref(new window)

48.
Keefer EW, Botterman BR, Romero MI, Rossi AF, Gross GW. Carbon nanotube coating improves neuronal recordings. Nat Nanotechnol, 3, 434 (2008). http://dx.doi.org/10.1038/nnano.2008.174. crossref(new window)

49.
Nguyen P, Berry V. Graphene interfaced with biological cells: opportunities and challenges. J Phys Chem Lett, 3, 1024 (2012). http://dx.doi.org/10.1021/jz300033g. crossref(new window)

50.
Zhou K, Thouas GA, Bernard CC, Nisbet DR, Finkelstein DI, Li D, Forsythe JS. Method to impart electro-and biofunctionality to neural scaffolds using graphene-polyelectrolyte multilayers. ACS Appl Mater Interfaces, 4, 4524 (2012). http://dx.doi.org/10.1021/am3007565. crossref(new window)

51.
Bendali A, Hess LH, Seifert M, Forster V, Stephan AF, Garrido JA, Picaud S. Purified neurons can survive on peptide-free graphene layers. Adv Healthc Mater, in press (2013). http://dx.doi. org/10.1002/adhm.201200347. crossref(new window)

52.
Chen CH, Lin CT, Hsu WL, Chang YC, Yeh SR, Li LJ, Yao DJ. A flexible hydrophilic-modified graphene microprobe for neural and cardiac recording. Nanomedicine, in press (2013). http://dx.doi. org/10.1016/j.nano.2012.12.004. crossref(new window)

53.
Hess LH, Jansen M, Maybeck V, Hauf MV, Seifert M, Stutzmann M, Sharp ID, Offenhausser A, Garrido JA. Graphene transistor arrays for recording action potentials from electrogenic cells. Adv Mater, 23, 5045 (2011). http://dx.doi.org/10.1002/adma.201102990. crossref(new window)

54.
Cohen-Karni T, Qing Q, Li Q, Fang Y, Lieber CM. Graphene and nanowire transistors for cellular interfaces and electrical recording. Nano Lett, 10, 1098 (2010). http://dx.doi.org/10.1021/nl1002608. crossref(new window)

55.
Luo X, Weaver CL, Tan S, Cui XT. Pure graphene oxide doped conducting polymer nanocomposite for bio-interfacing. J Mater Chem B, 1, 1340 (2013). http://dx.doi.org/10.1039/C3TB00006K. crossref(new window)