1,245
Views
100
CrossRef citations to date
0
Altmetric
Review

Graphene-based 3D scaffolds in tissue engineering: fabrication, applications, and future scope in liver tissue engineering

, , &
Pages 5753-5783 | Published online: 24 Jul 2019

References

  • Lavik E, Langer R. Tissue engineering: current state and perspectives. Appl Microbiol Biotechnol. 2004;65(1):1–8. doi:10.1007/s00253-004-1580-z15221227
  • Atala A. Engineering tissues, organs and cells. J Tissue Eng Regen Med. 2007;1(2):83–96. doi:10.1002/term.1818038397
  • Lanza R, Langer R, Vacanti JP. Principles of Tissue Engineering. London: Academic press; 2011.
  • Minuth WW, Sittinger M, Kloth S. Tissue engineering: generation of differentiated artificial tissues for biomedical applications. Cell Tissue Res. 1997;291(1):1–11.
  • Nerem RM, Sambanis A. Tissue engineering: from biology to biological substitutes. Tissue Eng. 1995;1(1):3–13.19877911
  • Mao AS, Mooney DJ. Regenerative medicine: current therapies and future directions. Proc Natl Acad Sci USA. 2015;112(47):14452–14459.26598661
  • Atala A. Engineering organs. Curr Opin Biotechnol. 2009;20(5):575–592.19896823
  • Marx V. Tissue engineering: organs from the lab. Nature. 2015;522(7556):373–377.26085275
  • Adachi T, Osako Y, Tanaka M, Hojo M, Hollister SJ. Framework for optimal design of porous scaffold microstructure by computational simulation of bone regeneration. Biomaterials. 2006;27(21):3964–3972.16584771
  • Chen Y, Zhou S, Li Q. Microstructure design of biodegradable scaffold and its effect on tissue regeneration. Biomaterials. 2011;32(22):5003–5014. doi:10.1016/j.biomaterials.2011.03.06421529933
  • Hollister SJ, Maddox R, Taboas JM. Optimal design and fabrication of scaffolds to mimic tissue properties and satisfy biological constraints. Biomaterials. 2002;23(20):4095–4103.12182311
  • Velasco MA, Narváez-Tovar CA, Garzón-Alvarado DA. Design, materials, and mechanobiology of biodegradable scaffolds for bone tissue engineering. Biomed Res Int. 2015;2015:729076.
  • Khoruzhenko A. 2D-and 3D-cell culture. Biopolym Cell. 2011;27(1):17–24. doi:10.7124/bc.00007D
  • Baharvand H, Hashemi SM, Ashtiani SK, Farrokhi A. Differentiation of human embryonic stem cells into hepatocytes in 2D and 3D culture systems in vitro. Int J Deve Biol. 2004;50(7):645–652. doi:10.1387/ijdb.052072hb
  • Pampaloni F, Reynaud EG, Stelzer EH. The third dimension bridges the gap between cell culture and live tissue. Nat Rev Mol Cell Biol. 2007;8(10):839–845. doi:10.1038/nrm223617684528
  • Ravi M, Paramesh V, Kaviya S, Anuradha E, Solomon F. 3D cell culture systems: advantages and applications. J Cell Physiol. 2015;230(1):16–26. doi:10.1002/jcp.2468324912145
  • Kim JB, Stein R, O’hare MJ. Three-dimensional in vitro tissue culture models of breast cancer – a review. Breast Cancer Res Treat. 2004;85(3):281–291. doi:10.1023/B:BREA.0000025418.88785.2b15111767
  • Sun T, Jackson S, Haycock JW, MacNeil S. Culture of skin cells in 3D rather than 2D improves their ability to survive exposure to cytotoxic agents. J Biotechnol. 2006;122(3):372–381. doi:10.1016/j.jbiotec.2005.12.02116446003
  • Breslin S, O’Driscoll L. Three-dimensional cell culture: the missing link in drug discovery. Drug Discov Today. 2013;18(5):240–249. doi:10.1016/j.drudis.2012.10.00323073387
  • Thoma CR, Zimmermann M, Agarkova I, Kelm JM, Krek W. 3D cell culture systems modeling tumor growth determinants in cancer target discovery. Adv Drug Deliv Rev. 2014;69:29–41. doi:10.1016/j.addr.2014.03.00124636868
  • Hartung T. 3D-A new dimension of in vitro research. Adv Drug Deliv Rev. 2014;69:vi. doi:10.1016/j.addr.2014.04.00324721291
  • Dhandayuthapani B, Yoshida Y, Maekawa T, Kumar DS. Polymeric scaffolds in tissue engineering application: a review. Int J Polym Sci. 2011;2011:290602.
  • Carletti E, Motta A, Migliaresi C. Scaffolds for tissue engineering and 3D cell culture. 3D Cell Cult Methods Protoc. 2011;695:17–39.
  • Wei G, Ma PX. Partially nanofibrous architecture of 3D tissue engineering scaffolds. Biomaterials. 2009;30(32):6426–6434.19699518
  • Mandal BB, Kundu SC. Cell proliferation and migration in silk fibroin 3D scaffolds. Biomaterials. 2009;30(15):2956–2965.19249094
  • Amann A, Zwierzina M, Kern J, et al. Establishment of a multicellular 3D cell culture model for tumor-endothelial cell interaction. AACR. 2016;76:1–13.
  • Randle DH, Fang Y, Eglen RM. 3D Cell culture and dish based organogenesis: optimizing in vitro cellular physiology. In: Bittker JA, Ross NT, editors. High Throughput Screening Methods. Cambridge: Royal Society of Chemistry; 2016;239–251.
  • Lima PAL, Resende CX, de Almeida Soares GD, Anselme K, Almeida LE. Preparation, characterization and biological test of 3D-scaffolds based on chitosan, fibroin and hydroxyapatite for bone tissue engineering. Mater Sci Eng C. 2013;33(6):3389–3395.
  • Liang M, Yao J, Chen X, Huang L, Shao Z. Silk fibroin immobilization on poly (ethylene terephthalate) films: comparison of two surface modification methods and their effect on mesenchymal stem cells culture. Mater Sci Eng C. 2013;33(3):1409–1416.
  • Kavya K, Jayakumar R, Nair S, Chennazhi KP. Fabrication and characterization of chitosan/gelatin/nSiO 2 composite scaffold for bone tissue engineering. Int J Biol Macromol. 2013;59:255–263.23591473
  • Martins AM, Eng G, Caridade SG, JoF M, Reis RL, Vunjak-Novakovic G. Electrically conductive chitosan/carbon scaffolds for cardiac tissue engineering. Biomacromolecules. 2014;15(2):635–643.24417502
  • Ayaz HGŞ, Perets A, Ayaz H, et al. Textile-templated electrospun anisotropic scaffolds for regenerative cardiac tissue engineering. Biomaterials. 2014;35(30):8540–8552.25017096
  • Liu Q, Tian S, Zhao C, et al. Porous nanofibrous poly (L-lactic acid) scaffolds supporting cardiovascular progenitor cells for cardiac tissue engineering. Acta Biomater. 2015;26:105–114.26283164
  • Billiet T, Gevaert E, De Schryver T, Cornelissen M, Dubruel P. The 3D printing of gelatin methacrylamide cell-laden tissue-engineered constructs with high cell viability. Biomaterials. 2014;35(1):49–62.24112804
  • Mihic A, Li J, Miyagi Y, et al. The effect of cyclic stretch on maturation and 3D tissue formation of human embryonic stem cell-derived cardiomyocytes. Biomaterials. 2014;35(9):2798–2808.24424206
  • Beaumont M, Kondor A, Plappert S, et al. Surface properties and porosity of highly porous, nanostructured cellulose II particles. Cellulose. 2017;24(1):435–440.
  • Möllers S, Heschel I, Damink LHO, et al. Cytocompatibility of a novel, longitudinally microstructured collagen scaffold intended for nerve tissue repair. Tissue Eng Part A. 2008;15(3):461–472.
  • Ma L, Gao C, Mao Z, et al. Collagen/chitosan porous scaffolds with improved biostability for skin tissue engineering. Biomaterials. 2003;24(26):4833–4841.14530080
  • Bhardwaj N, Sow WT, Devi D, Ng KW, Mandal BB, Cho N-J. Silk fibroin–keratin based 3D scaffolds as a dermal substitute for skin tissue engineering. Integr Biol. 2014;7(1):53–63.
  • Yooyod M, Ross G, Limpeanchob N, Suphrom N, Mahasaranon S, Ross S. Investigation of silk sericin conformational structure for fabrication into porous scaffolds with poly (vinyl alcohol) for skin tissue reconstruction. Eur Polym J. 2016;81:43–52.
  • Yu P, Bao R-Y, Shi X-J, Yang W, Yang M-B. Self-assembled high-strength hydroxyapatite/graphene oxide/chitosan composite hydrogel for bone tissue engineering. Carbohydr Polym. 2017;155:507–515.27702542
  • Simon KA, Mosadegh B, Minn KT, et al. Metabolic response of lung cancer cells to radiation in a paper-based 3D cell culture system. Biomaterials. 2016;95:47–59.27116031
  • van Duinen V, Trietsch SJ, Joore J, Vulto P, Hankemeier T. Microfluidic 3D cell culture: from tools to tissue models. Curr Opin Biotechnol. 2015;35:118–126.26094109
  • Chang C-H, Chen C-H, Liu H-W, et al. Bioengineered periosteal progenitor cell sheets to enhance tendon-bone healing in a bone tunnel. Biomed J. 2012;35(6):473–480.23442360
  • DuRaine GD, Brown WE, Hu JC, Athanasiou KA. Emergence of scaffold-free approaches for tissue engineering musculoskeletal cartilages. Ann Biomed Eng. 2015;43(3):543–554.25331099
  • Liu Y, Luo H, Wang X, et al. In vitro construction of scaffold-free bilayered tissue-engineered skin containing capillary networks. Biomed Res Int. 2013;2013:561410.
  • Masuda S, Shimizu T. Three-dimensional cardiac tissue fabrication based on cell sheet technology. Adv Drug Deliv Rev. 2016;96:103–109.25980939
  • Na S, Zhang H, Huang F, et al. Regeneration of dental pulp/dentine complex with a three‐dimensional and scaffold‐free stem‐cell sheet‐derived pellet. J Tissue Eng Regen Med. 2016;10(3):261–270.23365018
  • Owaki T, Shimizu T, Yamato M, Okano T. Cell sheet engineering for regenerative medicine: current challenges and strategies. Biotechnol J. 2014;9(7):904–914.24964041
  • See EY-S, Toh SL, Goh JCH. Multilineage potential of bone-marrow-derived mesenchymal stem cell cell sheets: implications for tissue engineering. Tissue Eng Part A. 2010;16(4):1421–1431.19951089
  • Syed‐Picard FN, Du Y, Hertsenberg AJ, et al. Scaffold‐free tissue engineering of functional corneal stromal tissue. J Tissue Eng Regen Med. 2018;12(1):59–69.27863068
  • Truby RL, Lewis JA. Printing soft matter in three dimensions. Nature. 2016;540(7633):371.27974748
  • Sellaro TL, Ranade A, Faulk DM, et al. Maintenance of human hepatocyte function in vitro by liver-derived extracellular matrix gels. Tissue Eng Part A. 2009;16(3):1075–1082.
  • Frantz C, Stewart KM, Weaver VM. The extracellular matrix at a glance. J Cell Sci. 2010;123(24):4195–4200.21123617
  • Pati F, Jang J, Ha D-H, et al. Printing three-dimensional tissue analogues with decellularized extracellular matrix bioink. Nat Commun. 2014;5:3935.24887553
  • Lock J, Liu H. Nanomaterials enhance osteogenic differentiation of human mesenchymal stem cells similar to a short peptide of BMP-7. Int J Nanomedicine. 2011;6:2769–2777.22114505
  • Ovsianikov A, Khademhosseini A, Mironov V. The synergy of scaffold-based and scaffold-free tissue engineering strategies. Trends Biotechnol. 2018;36:348–357.
  • Bettinger CJ, Langer R, Borenstein JT. Engineering substrate topography at the micro‐and nanoscale to control cell function. Angew Chem Int Ed. 2009;48(30):5406–5415.
  • Binulal N, Deepthy M, Selvamurugan N, et al. Role of nanofibrous poly (caprolactone) scaffolds in human mesenchymal stem cell attachment and spreading for in vitro bone tissue engineering – response to osteogenic regulators. Tissue Eng Part A. 2010;16(2):393–404.19772455
  • Cheng K, Kisaalita WS. Exploring cellular adhesion and differentiation in a micro‐/nano‐hybrid polymer scaffold. Biotechnol Prog. 2010;26(3):838–846.20196160
  • Zhao C, Tan A, Pastorin G, Ho HK. Nanomaterial scaffolds for stem cell proliferation and differentiation in tissue engineering. Biotechnol Adv. 2013;31(5):654–668.22902273
  • Kim J, Choi KS, Kim Y, et al. Bioactive effects of graphene oxide cell culture substratum on structure and function of human adipose‐derived stem cells. J Biomed Mater Res B Appl Biomater. 2013;101(12):3520–3530.
  • Rifai A, Pirogova E, Fox K. Encyclopedia of Biomedical Engineering, Volume 1- Biomaterials: Science and Engineering. Narayan RJ, editor. Cambridge: Elsevier, Oliver Walter; 2019.
  • Martinelli V, Bosi S, Peña B, et al. 3D Carbon-nanotube-based composites for cardiac tissue engineering. ACS Appl Biomater. 2018;1(5):1530–1537.
  • Minami K, Kasuya Y, Yamazaki T, et al. Highly ordered 1d fullerene crystals for concurrent control of macroscopic cellular orientation and differentiation toward large‐scale tissue engineering. Adv Mater. 2015;27(27):4020–4026.26033774
  • Cheng Q, Rutledge K, Jabbarzadeh E. Carbon nanotube–poly (lactide-co-glycolide) composite scaffolds for bone tissue engineering applications. Ann Biomed Eng. 2013;41(5):904–916.23283475
  • Starý V, Bačáková L, Horník J, Chmelík V. Bio-compatibility of the surface layer of pyrolytic graphite. Thin Solid Films. 2003;433(1):191–198.
  • Bolotin KI, Sikes K, Jiang Z, et al. Ultrahigh electron mobility in suspended graphene. Solid State Commun. 2008;146(9):351–355.
  • Morozov S, Novoselov K, Katsnelson M, et al. Giant intrinsic carrier mobilities in graphene and its bilayer. Phys Rev Lett. 2008;100(1):016602.18232798
  • Lee C, Wei X, Kysar JW, Hone J. Measurement of the elastic properties and intrinsic strength of monolayer graphene. Science. 2008;321(5887):385–388.18635798
  • Balandin AA, Ghosh S, Bao W, et al. Superior thermal conductivity of single-layer graphene. Nano Lett. 2008;8(3):902–907.18284217
  • Cai W, Zhu Y, Li X, Piner RD, Ruoff RS. Large area few-layer graphene/graphite films as transparent thin conducting electrodes. Appl Phys Lett. 2009;95(12):123115.
  • Feng L, Liu Z. Graphene in biomedicine: opportunities and challenges. Nanomedicine. 2011;6(2):317–324.21385134
  • Shen H, Zhang L, Liu M, Zhang Z. Biomedical applications of graphene. Theranostics. 2012;2(3):283–294.22448195
  • Edirisinghe M. The biomedical applications of graphene. R Soc. 2018;8:1–2.
  • Terse-Thakoor T, Badhulika S, Mulchandani A. Graphene based biosensors for healthcare. J Mater Res. 2017;32(15):2905–2929.
  • Bai RG, Ninan N, Muthoosamy K, Manickam S. Graphene: a versatile platform for nanotheranostics and tissue engineering. Prog Mater Sci. 2017;91:24–69.
  • Huang X, Yin Z, Wu S, et al. Graphene‐based materials: synthesis, characterization, properties, and applications. Small. 2011;7(14):1876–1902.21630440
  • Muthoosamy K. G Bai R, Manickam S. Graphene and graphene oxide as a docking station for modern drug delivery system. Curr Drug Deliv. 2014;11(6):701–718.24909150
  • Guo S, Dong S. Graphene nanosheet: synthesis, molecular engineering, thin film, hybrids, and energy and analytical applications. Chem Soc Rev. 2011;40(5):2644–2672.21283849
  • Zhang Y, Nayak TR, Hong H, Cai W. Graphene: a versatile nanoplatform for biomedical applications. Nanoscale. 2012;4(13):3833–3842.22653227
  • Abbasi E, Akbarzadeh A, Kouhi M, Milani M. Graphene: synthesis, bio-applications, and properties. Artif Cells Nanomed Biotechnol. 2016;44(1):150–156.24978443
  • Bai RG, Muthoosamy K, Shipton FN, et al. The biogenic synthesis of a reduced graphene oxide–silver (RGO–ag) nanocomposite and its dual applications as an antibacterial agent and cancer biomarker sensor. RSC Adv. 2016;6(43):36576–36587.
  • Chung C, Kim Y-K, Shin D, Ryoo S-R, Hong BH, Min D-H. Biomedical applications of graphene and graphene oxide. Acc Chem Res. 2013;46(10):2211–2224.23480658
  • Dreyer DR, Park S, Bielawski CW, Ruoff RS. The chemistry of graphene oxide. Chem Soc Rev. 2010;39(1):228–240.20023850
  • Pei S, Cheng H-M. The reduction of graphene oxide. Carbon. 2012;50(9):3210–3228.
  • Bai RG, Muthoosamy K, Zhou M, Ashokkumar M, Huang NM, Manickam S. Sonochemical and sustainable synthesis of graphene-gold (G-Au) nanocomposites for enzymeless and selective electrochemical detection of nitric oxide. Biosens Bioelectron. 2017;87:622–629.27616288
  • Thakur S, Karak N. Green reduction of graphene oxide by aqueous phytoextracts. Carbon. 2012;50(14):5331–5339.
  • Veetil JV, Ye K. Tailored carbon nanotubes for tissue engineering applications. Biotechnol Prog. 2009;25(3):709–721.19496152
  • Ku SH, Lee M, Park CB. Carbon‐based nanomaterials for tissue engineering. Adv Healthc Mater. 2013;2(2):244–260.23184559
  • Lin Y, Taylor S, Li H, et al. Advances toward bioapplications of carbon nanotubes. J Mater Chem. 2004;14(4):527–541.
  • Kuila T, Bose S, Mishra AK, Khanra P, Kim NH, Lee JH. Chemical functionalization of graphene and its applications. Prog Mater Sci. 2012;57(7):1061–1105.
  • Liao J, Li Q, Wen J, et al. Graphene nanoparticles-based self-healing hydrogel in preventing post-operative recurrence of breast cancer. ACS Biomater Sci Eng. 2019;5:768–779.
  • Eswaraiah V, Aravind SSJ, Ramaprabhu S. Top down method for synthesis of highly conducting graphene by exfoliation of graphite oxide using focused solar radiation. J Mater Chem. 2011;21(19):6800–6803.
  • Chen Y-C, Cao T, Chen C, et al. Molecular bandgap engineering of bottom-up synthesized graphene nanoribbon heterojunctions. Nat Nanotechnol. 2015;10(2):156–160.25581888
  • Jung HS, Choi Y-J, Jeong J, et al. Nanoscale graphene coating on commercially pure titanium for accelerated bone regeneration. RSC Adv. 2016;6(32):26719–26724.
  • Mokkapati V, Tasli NP, Khan Z, et al. NaB integrated graphene oxide membranes for enhanced cell viability and stem cell properties of human adipose stem cells. RSC Adv. 2016;6(61):56159–56165.
  • Akhavan O, Ghaderi E. Flash photo stimulation of human neural stem cells on graphene/TiO2 heterojunction for differentiation into neurons. Nanoscale. 2013;5(21):10316–10326.24056702
  • Paul A, Hasan A, Kindi HA, et al. Injectable graphene oxide/hydrogel-based angiogenic gene delivery system for vasculogenesis and cardiac repair. ACS Nano. 2014;8(8):8050–8062.24988275
  • Zhao W, Fang M, Wu F, Wu H, Wang L, Chen G. Preparation of graphene by exfoliation of graphite using wet ball milling. J Mater Chem. 2010;20(28):5817–5819. doi:10.1039/c0jm01354d
  • Chen Z, Ren W, Gao L, Liu B, Pei S, Cheng H-M. Three-dimensional flexible and conductive interconnected graphene networks grown by chemical vapour deposition. Nat Mater. 2011;10(6):424–428. doi:10.1038/nmat300121478883
  • Muthoosamy K, Bai RG, Abubakar IB, et al. Exceedingly biocompatible and thin-layered reduced graphene oxide nanosheets using an eco-friendly mushroom extract strategy. Int J Nanomedicine. 2015;10:1505.25759577
  • Qian Y, Song J, Zhao X, et al. Tissue engineering: 3D fabrication with integration molding of a graphene oxide/polycaprolactone nanoscaffold for neurite regeneration and angiogenesis. Adv Sci. 2018;5(4):1870020. doi:10.1002/advs.201870020
  • Nyambat B, Chen C-H, Wong P-C, Chiang C-W, Satapathy MK, Chuang E-Y. Genipin-crosslinked adipose stem cell derived extracellular matrix-nano graphene oxide composite sponge for skin tissue engineering. J Mater Chem B. 2018;6(6):979–990. doi:10.1039/C7TB02480K
  • Wu D, Samanta A, Srivastava RK, Hakkarainen M. Starch derived nano-graphene oxide paves the way for electrospinnable and bioactive starch scaffolds for bone tissue engineering. Biomacromolecules. 2017;18:1582–1591. doi:10.1021/acs.biomac.7b0019528350456
  • Akhavan O. Graphene scaffolds in progressive nanotechnology/stem cell-based tissue engineering of the nervous system. J Mater Chem B. 2016;4(19):3169–3190. doi:10.1039/C6TB00152A
  • Jakus AE, Shah R. Multi and mixed 3D‐printing of graphene‐hydroxyapatite hybrid materials for complex tissue engineering. J Biomed Mater Res B Appl Biomater. 2017;105(1):274–283. doi:10.1002/jbm.a.35684
  • Liu Y, Chen T, Du F, et al. Single-layer graphene enhances the osteogenic differentiation of human mesenchymal stem cells in vitro and in vivo. J Biomed Nanotechnol. 2016;12(6):1270–1284.27319220
  • Akhavan O, Ghaderi E, Shirazian SA. Near infrared laser stimulation of human neural stem cells into neurons on graphene nanomesh semiconductors. Colloids Surf B Biointerfaces. 2015;126:313–321. doi:10.1016/j.colsurfb.2014.12.02725578421
  • Jo H, Sim M, Kim S, et al. Electrically conductive graphene/polyacrylamide hydrogels produced by mild chemical reduction for enhanced myoblast growth and differentiation. Acta Biomater. 2017;48:100–109. doi:10.1016/j.actbio.2016.10.03527989919
  • Liu C, Wong HM, Yeung KWK, Tjong SC. Novel electrospun polylactic acid nanocomposite fiber mats with hybrid graphene oxide and nanohydroxyapatite reinforcements having enhanced biocompatibility. Polymers. 2016;8(8):287. doi:10.3390/polym8080287
  • Shin SR, Zihlmann C, Akbari M, et al. Reduced graphene oxide‐gelMA hybrid hydrogels as scaffolds for cardiac tissue engineering. Small. 2016;12(27):3677–3689. doi:10.1002/smll.20160017827254107
  • Mondal MK, Mukherjee S, Saha SK, Chowdhury P, Babu SPS. Design and synthesis of reduced graphene oxide based supramolecular scaffold: a benign microbial resistant network for enzyme immobilization and cell growth. Mater Sci Eng C. 2017;75:1168–1177. doi:10.1016/j.msec.2017.02.136
  • Holt BD, Arnold AM, Sydlik SA. Peptide‐functionalized reduced graphene oxide as a bioactive mechanically robust tissue regeneration scaffold. Polym Int. 2017. doi:10.1002/pi.5375
  • Sacks R, Schein G, Isseroff R, Ricotta V, Simon M, Rafailovich M. The influence of metalized graphene oxide/reduced graphene oxide and sulfonated polystyrene on dental pulp stem cell differentiation and protein adsorption. MRS Adv. 2017;20:1059–1070.
  • Ameri S, Singh P, D’Angelo R, Stoppel W, Black L, Sonkusale S Three dimensional graphene scaffold for cardiac tissue engineering and in-situ electrical recording. Paper presented at: Engineering in medicine and biology society (embc), 2016 IEEE 38th annual international conference of the 2016;  Orlando, FL, USA.
  • Lamprecht C, Taale M, Paulowicz I, et al. A tunable scaffold of microtubular graphite for 3D cell growth. ACS Appl Mater Interfaces. 2016;8(24):14980. doi:10.1021/acsami.6b0077827258400
  • Xie H, Chua M, Islam I, et al. CVD-grown monolayer graphene induces osteogenic but not odontoblastic differentiation of dental pulp stem cells. Dent Mater. 2017;33(1):e13–e21. doi:10.1016/j.dental.2016.09.03027692439
  • Golafshan N, Kharaziha M, Fathi M. Tough and conductive hybrid graphene-PVA: alginate fibrous scaffolds for engineering neural construct. Carbon. 2017;111:752–763. doi:10.1016/j.carbon.2016.10.042
  • Li N, Zhang Q, Gao S, et al. Three-dimensional graphene foam as a biocompatible and conductive scaffold for neural stem cells. Sci Rep. 2013;3:1604. doi:10.1038/srep0160423549373
  • Li C, Shi G. Three-dimensional graphene architectures. Nanoscale. 2012;4(18):5549–5563. doi:10.1039/c2nr31467c22895734
  • Bhardwaj N, Chouhan D, Mandal BB. 3D functional scaffolds for skin tissue engineering In: Deng Y, Jordan Kuiper J, editors. Functional 3D Tissue Engineering Scaffolds. Duxford: Woodhead Publishing, Elsevier; 2018:345–365.
  • Li X, Ye X, Qi J, et al. EGF and curcumin co-encapsulated nanoparticle/hydrogel system as potent skin regeneration agent. Int J Nanomedicine. 2016;11:3993. doi:10.2147/IJN.S10435027574428
  • Kumar S, Chatterjee K. Strontium eluting graphene hybrid nanoparticles augment osteogenesis in a 3D tissue scaffold. Nanoscale. 2015;7(5):2023–2033. doi:10.1039/c4nr05060f25553731
  • Jiang L, Fan Z. Design of advanced porous graphene materials: from graphene nanomesh to 3D architectures. Nanoscale. 2014;6(4):1922–1945. doi:10.1039/c3nr04555b24301688
  • Kelly CN, Miller AT, Hollister SJ, Guldberg RE, Gall K. Design and structure–function characterization of 3D printed synthetic porous biomaterials for tissue engineering. Adv Healthc Mater. 2018;7(7):1701095. doi:10.1002/adhm.201701095
  • Trautmann A, Rüth M, Lemke H-D, Walther T, Hellmann R Large 3D direct laser written scaffolds for tissue engineering applications. Paper presented at: Nanophotonics australasia2017; Melbourne, VIC, Australia; 2017.
  • Feiner R, Fleischer S, Shapira A, Kalish O, Dvir T. Multifunctional degradable electronic scaffolds for cardiac tissue engineering. J Control Release. 2018;281:189–195. doi:10.1016/j.jconrel.2018.05.02329782947
  • Seunarine K, Gadegaard N, Tormen M, Meredith D, Riehle M, Wilkinson C. 3D polymer scaffolds for tissue engineering. Nanomedicine. 2006;1:281–296. doi:10.2217/17435889.1.3.28117716159
  • Hu S, Chen H, Zhou X, et al. Thermally induced self-agglomeration 3D scaffolds with BMP-2-loaded core–shell fibers for enhanced osteogenic differentiation of rat adipose-derived stem cells. Int J Nanomedicine. 2018;13:4145. doi:10.2147/IJN.S17762730046239
  • Mikos AG, Thorsen AJ, Czerwonka LA, et al. Preparation and characterization of poly (L-lactic acid) foams. Polymer. 1994;35(5):1068–1077. doi:10.1016/0032-3861(94)90953-9
  • Pinto AM, Moreira S, Gonçalves IC, Gama FM, Mendes AM, Magalhães FD. Biocompatibility of poly (lactic acid) with incorporated graphene-based materials. Colloids Surf B Biointerfaces. 2013;104:229–238. doi:10.1016/j.colsurfb.2012.12.00623333912
  • Joshi MK, Pant HR, Tiwari AP, Park CH, Kim CS. Multi-layered macroporous three-dimensional nanofibrous scaffold via a novel gas foaming technique. Chem Eng J. 2015;275:79–88. doi:10.1016/j.cej.2015.03.121
  • Yang G, Su J, Gao J, Hu X, Geng C, Fu Q. Fabrication of well-controlled porous foams of graphene oxide modified poly (propylene-carbonate) using supercritical carbon dioxide and its potential tissue engineering applications. J Supercrit Fluids. 2013;73:1–9. doi:10.1016/j.supflu.2012.11.004
  • Jing X, Mi HY, Salick MR, Peng XF, Turng LS. Preparation of thermoplastic polyurethane/graphene oxide composite scaffolds by thermally induced phase separation. Polym Compos. 2014;35(7):1408–1417. doi:10.1002/pc.22793
  • Sayyar S, Cornock R, Murray E, Beirne S, Officer DL, Wallace GG. Extrusion Printed Graphene/Polycaprolactone/Composites for Tissue Engineering. Materials Science Forum. 2014;773–774:496–502.
  • Kumar S, Azam M, Raj S, et al. 3D scaffold alters cellular response to graphene in a polymer composite for orthopedic applications. J Biomed Mater Res B Appl Biomater. 2015;104:732–749.
  • Zhu J, Marchant RE. Design properties of hydrogel tissue-engineering scaffolds. Expert Rev Med Devices. 2011;8(5):607–626. doi:10.1586/erd.11.2722026626
  • Yi W, Wu H, Wang H, Du Q. Interconnectivity of macroporous hydrogels prepared via graphene oxide-stabilized pickering high internal phase emulsions. Langmuir. 2016;32(4):982–990. doi:10.1021/acs.langmuir.5b0447726752516
  • Chen Y, Wang Y, Shi X, et al. Hierarchical and reversible assembly of graphene oxide/polyvinyl alcohol hybrid stabilized pickering emulsions and their templating for macroporous composite hydrogels. Carbon. 2017;111:38–47. doi:10.1016/j.carbon.2016.09.059
  • O’Brien FJ, Harley BA, Yannas IV, Gibson L. Influence of freezing rate on pore structure in freeze-dried collagen-GAG scaffolds. Biomaterials. 2004;25(6):1077–1086.14615173
  • Murphy CM, Haugh MG, O’Brien FJ. The effect of mean pore size on cell attachment, proliferation and migration in collagen–glycosaminoglycan scaffolds for bone tissue engineering. Biomaterials. 2010;31(3):461–466. doi:10.1016/j.biomaterials.2009.09.06319819008
  • Mohandes F, Salavati-Niasari M. Freeze-drying synthesis, characterization and in vitro bioactivity of chitosan/graphene oxide/hydroxyapatite nanocomposite. RSC Adv. 2014;4(49):25993–26001. doi:10.1039/c4ra03534h
  • Unnithan AR, Park CH, Kim CS. Nanoengineered bioactive 3D composite scaffold: a unique combination of graphene oxide and nanotopography for tissue engineering applications. Compos Part B Eng. 2016;90:503–511. doi:10.1016/j.compositesb.2016.01.012
  • Zhang C, Wang L, Zhai T, Wang X, Dan Y, Turng L-S. The surface grafting of graphene oxide with poly (ethylene glycol) as a reinforcement for poly (lactic acid) nanocomposite scaffolds for potential tissue engineering applications. J Mech Behav Biomed Mater. 2016;53:403–413. doi:10.1016/j.jmbbm.2015.08.04326409231
  • Jing X, Mi H-Y, Salick MR, Cordie TM, Peng X-F, Turng L-S. Electrospinning thermoplastic polyurethane/graphene oxide scaffolds for small diameter vascular graft applications. Mater Sci Eng C. 2015;49:40–50. doi:10.1016/j.msec.2014.12.060
  • Murphy SV, Atala A. 3D bioprinting of tissues and organs. Nat Biotechnol. 2014;32(8):773–785. doi:10.1038/nbt.295825093879
  • Do A-V, Smith R, Acri TM, Geary SM, Salem AK. 3D printing technologies for 3D scaffold engineering In: Ahmad N, Gopinath P, Dutta R, editors. Functional 3D Tissue Engineering Scaffolds. St. Louis: Elsevier; 2018:203–234.
  • Wang W, Caetano G, Ambler WS, et al. Enhancing the hydrophilicity and cell attachment of 3D printed PCL/graphene scaffolds for bone tissue engineering. Materials. 2016;9(12):992. doi:10.3390/ma9120992
  • Vijayavenkataraman S, Thaharah S, Zhang S, Lu WF, Fuh JYH. 3D‐printed PCL/rGO conductive scaffolds for peripheral nerve injury repair. Artif Organs. 2018;43:515-523.
  • Geckil H, Xu F, Zhang X, Moon S, Demirci U. Engineering hydrogels as extracellular matrix mimics. Nanomedicine. 2010;5(3):469–484. doi:10.2217/nnm.10.1220394538
  • Shen H, Lin H, Sun AX, et al. Chondroinductive factor-free chondrogenic differentiation of human mesenchymal stem cells in graphene oxide-incorporated hydrogels. J Mater Chem B. 2018;6(6):908–917. doi:10.1039/C7TB02172K
  • Saravanan S, Vimalraj S, Anuradha D. Chitosan based thermoresponsive hydrogel containing graphene oxide for bone tissue repair. Biomed Pharmacother. 2018;107:908–917. doi:10.1016/j.biopha.2018.08.07230257403
  • Qian Y, Zhao X, Han Q, Chen W, Li H, Yuan W. An integrated multi-layer 3D-fabrication of PDA/RGD coated graphene loaded PCL nanoscaffold for peripheral nerve restoration. Nat Commun. 2018;9(1):323. doi:10.1038/s41467-017-02598-729358641
  • Tasnim N, Thakur V, Chattopadhyay M, Joddar B. The efficacy of graphene foams for culturing mesenchymal stem cells and their differentiation into dopaminergic neurons. Stem Cells Int. 2018;2018:3410168.
  • Valencia C, Valencia C, Zuluaga F, Valencia M, Mina J, Grande-Tovar C. Synthesis and application of scaffolds of chitosan-graphene oxide by the freeze-drying method for tissue regeneration. Molecules. 2018;23(10):2651. doi:10.3390/molecules23102651
  • Hermenean A, Codreanu A, Herman H, et al. Chitosan-graphene oxide 3D scaffolds as promising tools for bone regeneration in critical-size mouse calvarial defects. Sci Rep. 2017;7(1):16641. doi:10.1038/s41598-017-16599-529192253
  • Domínguez-Bajo A, González-Mayorga A, López-Dolado E, Serrano MC. Graphene-derived materials interfacing the spinal cord: outstanding in vitro and in vivo findings. Front Syst Neurosci. 2017;11:71. doi:10.3389/fnsys.2017.0007129085285
  • Nguyen AT, Mattiassi S, Loeblein M, et al. Human Rett-derived neuronal progenitor cells in 3D graphene scaffold as an in vitro platform to study the effect of electrical stimulation on neuronal differentiation. Biomedical Mater. 2018;13(3):034111. doi:10.1088/1748-605X/aaaf2b
  • Liu P, Chen W, Jia Y, Bai S, Wang Q. Fabrication of poly (vinyl alcohol)/graphene nanocomposite foam based on solid state shearing milling and supercritical fluid technology. Mater Des. 2017;134:121–131. doi:10.1016/j.matdes.2017.08.045
  • Bayer IS. Thermomechanical properties of polylactic acid-graphene composites: a state-of-the-art review for biomedical applications. Materials. 2017;10(7):748. doi:10.3390/ma10070748
  • Han L, Sun H, Tang P, et al. Mussel-inspired graphene oxide nanosheet-enwrapped Ti scaffolds with drug-encapsulated gelatin microspheres for bone regeneration. Biomater Sci. 2018;6(3):538–549. doi:10.1039/c7bm01060e29376156
  • Patel A, Xue Y, Hartley R, et al. Hierarchically aligned fibrous hydrogel films through microfluidic self‐assembly of graphene and polysaccharides. Biotechnol Bioeng. 2018;115(10):2654–2667. doi:10.1002/bit.2680130011077
  • Girão AF, Semitela Â, Ramalho G, Completo A, Marques PA. Mimicking nature: fabrication of 3D anisotropic electrospun polycaprolactone scaffolds for cartilage tissue engineering applications. Compos Part B-Eng. 2018;154:99–107. doi:10.1016/j.compositesb.2018.08.001
  • Hutmacher DW. Scaffold design and fabrication technologies for engineering tissues – state of the art and future perspectives. J Biomater Sci Polym Ed. 2001;12(1):107–124. doi:10.1163/15685620174448911334185
  • Sachlos E, Czernuszka J. Making tissue engineering scaffolds work. Review: the application of solid freeform fabrication technology to the production of tissue engineering scaffolds. Eur Cell Mater. 2003;5(29):39–40. doi:10.22203/eCM.v005a03
  • Crowder SW, Prasai D, Rath R, et al. Three-dimensional graphene foams promote osteogenic differentiation of human mesenchymal stem cells. Nanoscale. 2013;5(10):4171–4176. doi:10.1039/c3nr00803g23592029
  • Tang M, Song Q, Li N, Jiang Z, Huang R, Cheng G. Enhancement of electrical signaling in neural networks on graphene films. Biomaterials. 2013;34(27):6402–6411. doi:10.1016/j.biomaterials.2013.05.02423755830
  • Wang Y, Lee WC, Manga KK, et al. Fluorinated graphene for promoting neuro‐induction of stem cells. Adv Mater. 2012;24(31):4285–4290. doi:10.1002/adma.20120084622689093
  • Kazantseva J, Ivanov R, Gasik M, Neuman T, Hussainova I. Graphene-augmented nanofiber scaffolds demonstrate new features in cells behaviour. Sci Rep. 2016;6:1–8.28442741
  • Kalbacova M, Broz A, Kong J, Kalbac M. Graphene substrates promote adherence of human osteoblasts and mesenchymal stromal cells. Carbon. 2010;48(15):4323–4329. doi:10.1016/j.carbon.2010.07.045
  • Mattox DM. Handbook of Physical Vapor Deposition (PVD) Processing. Amsterdam: Elsevier; 2010.
  • Wasalathilake KC, Galpaya DG, Ayoko GA, Yan C. Understanding the structure-property relationships in hydrothermally reduced graphene oxide hydrogels. Carbon. 2018;137:282–290. doi:10.1016/j.carbon.2018.05.036
  • Zhai L, Li L, Zhang Q. Fabrication of capsaicin functionalized reduced graphene oxide and its effect on proliferation and differentiation of osteoblasts. Environ Toxicol Pharmacol. 2018;57:41–45. doi:10.1016/j.etap.2017.11.01229175712
  • Park SY, Park J, Sim SH, et al. Enhanced differentiation of human neural stem cells into neurons on graphene. Adv Mater. 2011;23:36. doi:10.1002/adma.201103379
  • Nayak TR, Andersen H, Makam VS, et al. Graphene for controlled and accelerated osteogenic differentiation of human mesenchymal stem cells. ACS Nano. 2011;5(6):4670–4678. doi:10.1021/nn200500h21528849
  • Nakayama KH, Hou L, Huang NF. Role of extracellular matrix signaling cues in modulating cell fate commitment for cardiovascular tissue engineering. Adv Healthc Mater. 2014;3(5):628–641. doi:10.1002/adhm.20130062024443420
  • Berg EL, Hsu Y-C, Lee JA. Consideration of the cellular microenvironment: physiologically relevant co-culture systems in drug discovery. Adv Drug Deliv Rev. 2014;69:190–204. doi:10.1016/j.addr.2014.01.01324524933
  • Montanez-Sauri SI, Beebe DJ, Sung KE. Microscale screening systems for 3D cellular microenvironments: platforms, advances, and challenges. Cell Mol Life Sci. 2015;72(2):237–249. doi:10.1007/s00018-014-1738-525274061
  • Wanjare M, Huang NF. Regulation of the microenvironment for cardiac tissue engineering. Regen Med. 2017;12(2):187–201. doi:10.2217/rme-2016-013228244821
  • Zlotorynski E. Mechanotransduction: stretching chromatin promotes transcription. Nat Rev Mol Cell Biol. 2016;17(10):610. doi:10.1038/nrm.2016.11927580843
  • Li Z, Lee H, Zhu C. Molecular mechanisms of mechanotransduction in integrin-mediated cell-matrix adhesion. Exp Cell Res. 2016;349(1):85–94. doi:10.1016/j.yexcr.2016.10.00127720950
  • Polacheck WJ, German AE, Mammoto A, Ingber DE, Kamm RD. Mechanotransduction of fluid stresses governs 3D cell migration. Proc Natl Acad Sci USA. 2014;111(7):2447–2452. doi:10.1073/pnas.131684811124550267
  • Baker BM, Chen CS. Deconstructing the third dimension–how 3D culture microenvironments alter cellular cues. J Cell Sci. 2012;125(13):3015–3024. doi:10.1242/jcs.07950922797912
  • Goenka S, Sant V, Sant S. Graphene-based nanomaterials for drug delivery and tissue engineering. J Control Release. 2014;173:75–88. doi:10.1016/j.jconrel.2013.10.01724161530
  • Shin SR, Li Y-C, Jang HL, et al. Graphene-based materials for tissue engineering. Adv Drug Deliv Rev. 2016;105:255–274. doi:10.1016/j.addr.2016.03.00727037064
  • Pinto AM, Gonçalves IC, Magalhães FD. Graphene-based materials biocompatibility: a review. Colloids Surf B Biointerfaces. 2013;111:188–202. doi:10.1016/j.colsurfb.2013.05.02223810824
  • Yang Y, Asiri AM, Tang Z, Du D, Lin Y. Graphene based materials for biomedical applications. Mater Today. 2013;16(10):365–373. doi:10.1016/j.mattod.2013.09.004
  • Ding X, Liu H, Fan Y. Graphene‐based materials in regenerative medicine. Adv Healthc Mater. 2015;4(10):1451–1468. doi:10.1002/adhm.20150020326037920
  • Lee SK, Kim H, Shim BS. Graphene: an emerging material for biological tissue engineering. Carbon Lett. 2013;14(2):63–75. doi:10.5714/CL.2013.14.2.063
  • Zhu W, Qu X, Zhu J, et al. Direct 3D bioprinting of prevascularized tissue constructs with complex microarchitecture. Biomaterials. 2017;124:106–115. doi:10.1016/j.biomaterials.2017.01.04228192772
  • Datta P, Ayan B, Ozbolat IT. Bioprinting for vascular and vascularized tissue biofabrication. Acta Biomater. 2017;51:1–20. doi:10.1016/j.actbio.2017.01.03528087487
  • Zhang X, Zhang Y. Tissue engineering applications of three-dimensional bioprinting. Cell Biochem Biophys. 2015;72(3):777–782. doi:10.1007/s12013-015-0531-x25663505
  • Aphale A, Hitscherich P, Narula R, et al. Biocompatibility of PCL-graphene nanostructured scaffolds with mouse embryonic stem cell-derived cardiomyocytes. Materials. 2015;8:12. doi:10.3390/ma8125486
  • Shadjou N, Hasanzadeh M. Graphene and its nanostructure derivatives for use in bone tissue engineering: recent advances. J Biomed Mater Res B Appl Biomater. 2016;104:1250–1275. doi:10.1002/jbm.a.v104.5
  • Gu M, Liu Y, Chen T, et al. Is graphene a promising nano-material for promoting surface modification of implants or scaffold materials in bone tissue engineering? Tissue Eng Part B Rev. 2014;20(5):477–491. doi:10.1089/ten.teb.2013.063824447041
  • Nie W, Peng C, Zhou X, et al. Three-dimensional porous scaffold by self-assembly of reduced graphene oxide and nano-hydroxyapatite composites for bone tissue engineering. Carbon. 2017;116:325–337. doi:10.1016/j.carbon.2017.02.013
  • Dinescu S, Ionita M, Pandele AM, et al. In vitro cytocompatibility evaluation of chitosan/graphene oxide 3D scaffold composites designed for bone tissue engineering. Biomed Mater Eng. 2014;24(6):2249–2256. doi:10.3233/BME-14103725226924
  • Saravanan S, Anjali C, Vairamani M, Sastry T, Subramanian K, Selvamurugan N. Scaffolds containing chitosan, gelatin and graphene oxide for bone tissue regeneration in vitro and in vivo. Int J Biol Macromol. 2017;104:1975–1985. doi:10.1016/j.ijbiomac.2017.01.03428089930
  • Liao J, Qu Y, Chu B, Zhang X, Qian Z. Biodegradable CSMA/PECA/graphene porous hybrid scaffold for cartilage tissue engineering. Sci Rep. 2015;5:9879. doi:10.1038/srep0987925961959
  • Frueh FS, Menger MD, Lindenblatt N, Giovanoli P, Laschke MW. Current and emerging vascularization strategies in skin tissue engineering. Crit Rev Biotechnol. 2016;371–13.23883073
  • Lee EJ, Lee JH, Shin YC, et al. Graphene oxide-decorated PLGA/collagen hybrid fiber sheets for application to tissue engineering scaffolds. Biomater Res. 2014;18:18–24. doi:10.1186/2055-7124-18-1826331069
  • Li Z, Wang H, Yang B, Sun Y, Huo R. Three-dimensional graphene foams loaded with bone marrow derived mesenchymal stem cells promote skin wound healing with reduced scarring. Mater Sci Eng C. 2015;57:181–188. doi:10.1016/j.msec.2015.07.062
  • Shin SR, Aghaei‐Ghareh‐Bolagh B, Dang TT, et al. Cell‐laden microengineered and mechanically tunable hybrid hydrogels of gelatin and graphene oxide. Adv Mater. 2013;25(44):6385–6391. doi:10.1002/adma.20130108223996513
  • Guo W, Wang S, Yu X, et al. Construction of a 3D rGO–collagen hybrid scaffold for enhancement of the neural differentiation of mesenchymal stem cells. Nanoscale. 2016;8(4):1897–1904. doi:10.1039/c5nr06602f26750302
  • López‐Dolado E, González‐Mayorga A, Portolés MT, et al. Subacute tissue response to 3D graphene oxide scaffolds implanted in the injured rat spinal cord. Adv Healthc Mater. 2015;4(12):1861–1868. doi:10.1002/adhm.20150033326115359
  • Jiang Z, Song Q, Tang M, et al. Enhanced migration of neural stem cells by microglia grown on a three-dimensional graphene scaffold. ACS Appl Mater Interfaces. 2016;8(38):25069–25077. doi:10.1021/acsami.6b0678027589088
  • López-Dolado E, González-Mayorga A, Gutiérrez MC, Serrano MC. Immunomodulatory and angiogenic responses induced by graphene oxide scaffolds in chronic spinal hemisected rats. Biomaterials. 2016;99:72–81. doi:10.1016/j.biomaterials.2016.05.01227214651
  • Guo W, Zhang X, Yu X, et al. Self-powered electrical stimulation for enhancing neural differentiation of mesenchymal stem cells on graphene–poly (3, 4-ethylenedioxythiophene) hybrid microfibers. ACS Nano. 2016;10(5):5086–5095. doi:10.1021/acsnano.6b0020027144593
  • Barrilleaux B, Phinney DG, Prockop DJ, O’connor KC. Review: ex vivo engineering of living tissues with adult stem cells. Tissue Eng. 2006;12(11):3007–3019. doi:10.1089/ten.2006.12.300717518617
  • Menaa F, Abdelghani A, Menaa B. Graphene nanomaterials as biocompatible and conductive scaffolds for stem cells: impact for tissue engineering and regenerative medicine. J Tissue Eng Regen Med. 2015;9(12):1321–1338. doi:10.1002/term.191024917559
  • Bressan E, Ferroni L, Gardin C, et al. Graphene based scaffolds effects on stem cells commitment. J Transl Med. 2014;12(1):296. doi:10.1186/s12967-014-0296-925344443
  • Gardin C, Piattelli A, Zavan B. Graphene in regenerative medicine: focus on stem cells and neuronal differentiation. Trends Biotechnol. 2016;34(6):435–437. doi:10.1016/j.tibtech.2016.01.00626879187
  • Sayyar S, Bjorninen M, Haimi S, et al. UV Cross-linkable graphene/poly (trimethylene carbonate) composites for 3D printing of electrically conductive scaffolds. ACS Appl Mater Interfaces. 2016;8(46):31916–31925. doi:10.1021/acsami.6b0996227782383
  • Akhavan O, Ghaderi E, Shirazian SA, Rahighi R. Rolled graphene oxide foams as three-dimensional scaffolds for growth of neural fibers using electrical stimulation of stem cells. Carbon. 2016;97:71–77. doi:10.1016/j.carbon.2015.06.079
  • Hassanein TI, Schade RR, Hepburn IS. Acute-on-chronic liver failure: extracorporeal liver assist devices. Curr Opin Crit Care. 2011;17(2):195–203. doi:10.1097/MCC.0b013e328344b3aa21346566
  • Bhatia SN, Underhill GH, Zaret KS, Fox IJ. Cell and tissue engineering for liver disease. Sci Transl Med. 2014;6(245):245sr242–245sr242. doi:10.1126/scitranslmed.3005975
  • Taub R. Liver regeneration: from myth to mechanism. Nat Rev Mol Cell Biol. 2004;5(10):836. doi:10.1038/nrm148915459664
  • Michalopoulos GK, DeFrances MC. Liver regeneration. Science. 1997;276(5309):60–66. doi:10.1126/science.276.5309.609082986
  • Lee SY, Kim HJ, Choi D. Cell sources, liver support systems and liver tissue engineering: alternatives to liver transplantation. Int J Stem Cells. 2015;8(1):36. doi:10.15283/ijsc.2015.8.1.3626019753
  • Palakkan AA, Hay DC, Kumary T, Ross JA. Liver tissue engineering and cell sources: issues and challenges. Liver Int. 2013;33(5):666–676. doi:10.1111/liv.1213423490085
  • Hammond JS, Beckingham IJ, Shakesheff KM. Scaffolds for liver tissue engineering. Expert Rev Med Devices. 2006;3(1):21–27. doi:10.1586/17434440.3.1.2116359250
  • Chan C, Berthiaume F, Nath BD, Tilles AW, Toner M, Yarmush ML. Hepatic tissue engineering for adjunct and temporary liver support: critical technologies. Liver Transpl. 2004;10(11):1331–1342. doi:10.1002/lt.2022915497161
  • Kaihara S, Borenstein J, Koka R, et al. Silicon micromachining to tissue engineer branched vascular channels for liver fabrication. Tissue Eng. 2000;6(2):105–117. doi:10.1089/10763270032073910941206
  • Bhandari RN, Riccalton LA, Lewis AL, et al. Liver tissue engineering: a role for co-culture systems in modifying hepatocyte function and viability. Tissue Eng. 2001;7(3):345–357. doi:10.1089/1076327015204420611429154
  • Dvir-Ginzberg M, Gamlieli-Bonshtein I, Agbaria R, Cohen S. Liver tissue engineering within alginate scaffolds: effects of cell-seeding density on hepatocyte viability, morphology, and function. Tissue Eng. 2003;9(4):757–766. doi:10.1089/10763270376824743013678452
  • Shirakigawa N, Ijima H, Takei T. Decellularized liver as a practical scaffold with a vascular network template for liver tissue engineering. J Biosci Bioeng. 2012;114(5):546–551. doi:10.1016/j.jbiosc.2012.05.02222717723
  • Mayer J, Karamuk E, Akaike T, Wintermantel E. Matrices for tissue engineering-scaffold structure for a bioartificial liver support system. J Control Release. 2000;64(1–3):81–90.10640647
  • Ohashi K, Yokoyama T, Yamato M, et al. Engineering functional two-and three-dimensional liver systems in vivo using hepatic tissue sheets. Nat Med. 2007;13(7):880. doi:10.1038/nm157617572687
  • Cho C, Seo S, Park I, et al. Galactose-carrying polymers as extracellular matrices for liver tissue engineering. Biomaterials. 2006;27(4):576–585. doi:10.1016/j.biomaterials.2005.06.00816084586
  • Lin P, Chan WC, Badylak SF, Bhatia SN. Assessing porcine liver-derived biomatrix for hepatic tissue engineering. Tissue Eng. 2004;10(7–8):1046–1053. doi:10.1089/ten.2004.10.104615363162
  • Jiankang H, Dichen L, Yaxiong L, et al. Preparation of chitosan–gelatin hybrid scaffolds with well-organized microstructures for hepatic tissue engineering. Acta Biomater. 2009;5(1):453–461. doi:10.1016/j.actbio.2008.07.00218675601
  • Wang X, Yan Y, Pan Y, et al. Generation of three-dimensional hepatocyte/gelatin structures with rapid prototyping system. Tissue Eng. 2006;12(1):83–90. doi:10.1089/ten.2006.12.8316499445
  • Risbud MV, Karamuk E, Schlosser V, Mayer J. Hydrogel-coated textile scaffolds as candidate in liver tissue engineering: II. Evaluation of spheroid formation and viability of hepatocytes. J Biomater Sci Polym Ed. 2003;14(7):719–731.12903739
  • Zhu XH, Gan SK, Wang CH, Tong YW. Proteins combination on PHBV microsphere scaffold to regulate Hep3B cells activity and functionality: a model of liver tissue engineering system. J Biomed Mater Res A. 2007;83(3):606–616.17503536
  • Yang Z, Xu LS, Yin F, et al. In vitro and in vivo characterization of silk fibroin/gelatin composite scaffolds for liver tissue engineering. J Dig Dis. 2012;13(3):168–178.22356312
  • Fiegel HC, Kaufmann PM, Bruns H, et al. Hepatic tissue engineering: from transplantation to customized cell‐based liver directed therapies from the laboratory. J Cell Mol Med. 2008;12(1):56–66.18021311
  • Kulig KM, Vacanti JP. Hepatic tissue engineering. Transpl Immunol. 2004;12(3–4):303–310.15157923
  • Jiang J, Kojima N, Guo L, et al. Efficacy of engineered liver tissue based on poly-L-lactic acid scaffolds and fetal mouse liver cells cultured with oncostatin M, nicotinamide, and dimethyl sulfoxide. Tissue Eng. 2004;10(9–10):1577–1586.15588417
  • Powers MJ, Domansky K, Kaazempur‐Mofrad MR, et al. A microfabricated array bioreactor for perfused 3D liver culture. Biotechnol Bioeng. 2002;78(3):257–269.11920442
  • Sabetkish S, Kajbafzadeh AM, Sabetkish N, et al. Whole‐organ tissue engineering: decellularization and recellularization of three‐dimensional matrix liver scaffolds. J Biomed Mater Res Part A. 2015;103(4):1498–1508.
  • Kim SS, Utsunomiya H, Koski JA, et al. Survival and function of hepatocytes on a novel three-dimensional synthetic biodegradable polymer scaffold with an intrinsic network of channels. Ann Surg. 1998;228(1):8.9671060
  • Ohashi K, Waugh JM, Dake MD, et al. Liver tissue engineering at extrahepatic sites in mice as a potential new therapy for genetic liver diseases. Hepatology. 2005;41(1):132–140.15619229
  • Dash A, Inman W, Hoffmaster K, et al. Liver tissue engineering in the evaluation of drug safety. Expert Opin Drug Metab Toxicol. 2009;5(10):1159–1174.19637986
  • Mazza G, Al‐Akkad W, Rombouts K, Pinzani M. Liver tissue engineering: from implantable tissue to whole organ engineering. Hepatol Commun. 2018;2(2):131–141.29404520
  • Nicolas CT, Hickey RD, Chen HS, et al. Concise review: liver regenerative medicine: from hepatocyte transplantation to bioartificial livers and bioengineered grafts. Stem Cells. 2017;35(1):42–50.27641427
  • Fiegel HC, Kneser U, Kluth D, Metzger R, Till H, Rolle U. Development of hepatic tissue engineering. Pediatr Surg Int. 2009;25(8):667–673.19488762
  • Tong XF, Zhao FQ, Ren YZ, Zhang Y, Cui YL, Wang QS. Injectable hydrogels based on glycyrrhizin, alginate, and calcium for three‐dimensional cell culture in liver tissue engineering. J Biomed Mater Res B Appl Biomater. 2018;106:3292–3302.
  • Lewis PL, Green RM, Shah RN. 3D-printed gelatin scaffolds of differing pore geometry modulate hepatocyte function and gene expression. Acta Biomater. 2018;69:63–70.29317370
  • Lee JW, Choi Y-J, Yong W-J, et al. Development of a 3D cell printed construct considering angiogenesis for liver tissue engineering. Biofabrication. 2016;8(1):015007.26756962
  • Song W, Lu Y-C, Frankel AS, An D, Schwartz RE, Ma M. Engraftment of human induced pluripotent stem cell-derived hepatocytes in immunocompetent mice via 3D co-aggregation and encapsulation. Sci Rep. 2015;5:16884.26592180
  • Ozbolat IT, Hospodiuk M. Current advances and future perspectives in extrusion-based bioprinting. Biomaterials. 2016;76:321–343.26561931
  • Jeon H, Kang K, Park SA, et al. Generation of multilayered 3D structures of HepG2 cells using a bio-printing technique. Gut Liver. 2017;11(1):121.27559001
  • Kang K, Kim Y, Jeon H, et al. Three-dimensional bioprinting of hepatic structures with directly converted hepatocyte-like cells. Tissue Eng Part A. 2018;24(7–8):576–583.28726547
  • Lee JS, Shin J, Park H-M, et al. Liver extracellular matrix providing dual functions of two-dimensional substrate coating and three-dimensional injectable hydrogel platform for liver tissue engineering. Biomacromolecules. 2013;15(1):206–218.24350561
  • Uygun BE, Yarmush ML, Uygun K. Application of whole-organ tissue engineering in hepatology. Nat Rev Gastroenterol Hepatol. 2012;9(12):738.22890112
  • Mazza G, Al-Akkad W, Rombouts K. Engineering in vitro models of hepatofibrogenesis. Adv Drug Deliv Rev. 2017;121:147–157.28578016
  • Bianco A. Graphene: safe or toxic? The two faces of the medal. Angew Chem Int Ed. 2013;52(19):4986–4997.
  • Li Y, Wang Y, Tu L, et al. Sub-acute toxicity study of graphene oxide in the Sprague-Dawley rat. Int J Environ Res Public Health. 2016;13(11):1149.
  • Horvath L, Magrez A, Burghard M, Kern K, Forró L, Schwaller B. Evaluation of the toxicity of graphene derivatives on cells of the lung luminal surface. Carbon. 2013;64:45–60.
  • Liu J-H, Yang S-T, Wang H, Chang Y, Cao A, Liu Y. Effect of size and dose on the biodistribution of graphene oxide in mice. Nanomedicine. 2012;7(12):1801–1812.22830500
  • Zhou H, Cheng C, Qin H, et al. Self-assembled 3D biocompatible and bioactive layer at the macro-interface via graphene-based supermolecules. Polym Chem. 2014;5(11):3563–3575.
  • Song SH, Jang M-H, Jeong J-M, et al. Primary hepatocyte imaging by multiphoton luminescent graphene quantum dots. Chem Commun. 2015;51(38):8041–8043.
  • Loeblein M, Perry G, Tsang SH, et al. Three‐dimensional graphene: a biocompatible and biodegradable scaffold with enhanced oxygenation. Adv Healthcare Mater. 2016:1177–1191.
  • Mohamed WNAEM, El Din TAS, Tohamy AAE-M, El-yamany NA, Amin AS. Evaluation of genotoxic and hepatotoxic effects of graphene oxide nanosheets in male albino mice. Egypt J Exp Biol (Zoo). 2017;13(1):43–53.
  • Starokozhko V, Hemmingsen M, Larsen L, et al. Differentiation of human‐induced pluripotent stem cell under flow conditions to mature hepatocytes for liver tissue engineering. J Tissue Eng Regen Med. 2018;12(5):1273–1284.29499107
  • Grant R, Hay D, Callanan A. From scaffold to structure: the synthetic production of cell derived extracellular matrix for liver tissue engineering. Biomed Phys Eng Express. 2018;4:1–13.
  • Fu J, Wang D-A. In situ organ-specific vascularization in tissue engineering. Trends Biotechnol. 2018;36:834-849.
  • Jastrzębska AM, Kurtycz P, Olszyna AR. Recent advances in graphene family materials toxicity investigations. J Nanopart Res. 2012;14(12):1320.23239936
  • Liu J, Tang J, Gooding JJ. Strategies for chemical modification of graphene and applications of chemically modified graphene. J Mater Chem. 2012;22(25):12435–12452.
  • Caffo M, Merlo L, Marino D, Caruso G. Biomedical applications of graphene In: Aliofkhazraei M, Ali N, Milne WI, Ozkan CS, Stanislaw Mitura S, Gervasoni JL, editors. Graphene Science Handbook: Applications and Industrialization. Boca Raton: CRC Press, Taylor & Francis; 2016:41–56.
  • Holmes B, Bulusu K, Plesniak M, Zhang LG. A synergistic approach to the design, fabrication and evaluation of 3D printed micro and nano featured scaffolds for vascularized bone tissue repair. Nanotechnology. 2016;27(6):064001.26758780