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Graphene-Functionalized Biomimetic Scaffolds for Tissue Regeneration

  • Yong Cheol Shin
  • Su-Jin Song
  • Suck Won Hong
  • Jin-Woo Oh
  • Yu-Shik Hwang
  • Yu Suk Choi
  • Dong-Wook HanEmail author
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1064)

Abstract

Graphene is a two-dimensional atomic layer of graphite, where carbon atoms are assembled in a honeycombed lattice structure. Recently, graphene family nanomaterials, including pristine graphene, graphene oxide and reduced graphene oxide, have increasingly attracted a great deal of interest from researchers in a variety of science, engineering and industrial fields because of their unique structural and functional features. In particular, extensive studies have been actively conducted in the biomedical and related fields, including multidisciplinary and emerging areas, as their stimulating effects on cell behaviors have been becoming an increasing concern. Herein, we are attempting to summarize some of recent findings in the fields of tissue regeneration concerning the graphene family nanomaterial-functionalized biomimetic scaffolds, and to provide the promising perspectives for the possible applications of graphene family nanomaterial.

Keywords

Graphene Graphene family nanomaterial Tissue regeneration Biomimetic scaffold 

References

  1. Ahadian S, Ramón-Azcón J, Chang H, Liang X, Kaji H, Shiku H, Nakajima K, Ramalingam M, Wu H, Matsue T (2014) Electrically regulated differentiation of skeletal muscle cells on ultrathin graphene-based films. RSC Adv 4(19):9534–9541CrossRefGoogle Scholar
  2. Akhavan O, Ghaderi E (2010) Toxicity of graphene and graphene oxide nanowalls against bacteria. ACS Nano 4(10):5731–5736PubMedCrossRefPubMedCentralGoogle Scholar
  3. Akhavan O, Ghaderi E (2013) Differentiation of human neural stem cells into neural networks on graphene nanogrids. J Mater Chem B 1(45):6291–6301CrossRefGoogle Scholar
  4. Akhavan O, Ghaderi E, Esfandiar A (2011) Wrapping bacteria by graphene nanosheets for isolation from environment, reactivation by sonication, and inactivation by near-infrared irradiation. J Phys Chem B 115(19):6279–6288PubMedCrossRefPubMedCentralGoogle Scholar
  5. Akhavan O, Ghaderi E, Akhavan A (2012) Size-dependent genotoxicity of graphene nanoplatelets in human stem cells. Biomaterials 33(32):8017–8025PubMedCrossRefPubMedCentralGoogle Scholar
  6. Akhavan O, Ghaderi E, Shahsavar M (2013) Graphene nanogrids for selective and fast osteogenic differentiation of human mesenchymal stem cells. Carbon 59:200–211CrossRefGoogle Scholar
  7. Akhavan O, Ghaderi E, Abouei E, Hatamie S, Ghasemi E (2014) Accelerated differentiation of neural stem cells into neurons on ginseng-reduced graphene oxide sheets. Carbon 66:395–406CrossRefGoogle Scholar
  8. Akhavan O, Ghaderi E, Shirazian SA, Rahighi R (2016) Rolled graphene oxide foams as three-dimensional scaffolds for growth of neural fibers using electrical stimulation of stem cells. Carbon 97:71–77CrossRefGoogle Scholar
  9. Bajaj P, Rivera JA, Marchwiany D, Solovyeva V, Bashir R (2014) Graphene-based patterning and differentiation of C2C12 myoblasts. Adv Healthc Mater 3(7):995–1000PubMedCrossRefPubMedCentralGoogle Scholar
  10. Baniasadi H, Sa AR, Mashayekhan S (2015) Fabrication and characterization of conductive chitosan/gelatin-based scaffolds for nerve tissue engineering. Int J Biol Macromol 74:360–366PubMedCrossRefPubMedCentralGoogle Scholar
  11. Baweja L, Dhawan A (2018) Chapter 12 Computational approaches for predicting nanotoxicity at the molecular level. In: Dhawan A, Anderson D, Shanker R (eds) Nanotoxicology: experimental and computational perspectives, vol 35. Royal Society of Chemistry, CambrIdge, pp 304–327.  https://doi.org/10.1039/9781782623922-00304 CrossRefGoogle Scholar
  12. Cellot G, Toma FM, Varley ZK, Laishram J, Villari A, Quintana M, Cipollone S, Prato M, Ballerini L (2011) Carbon nanotube scaffolds tune synaptic strength in cultured neural circuits: novel frontiers in nanomaterial–tissue interactions. J Neurosci 31(36):12945–12953PubMedCrossRefPubMedCentralGoogle Scholar
  13. Cha C, Shin SR, Gao X, Annabi N, Dokmeci MR, Tang XS, Khademhosseini A (2014) Controlling mechanical properties of cell-laden hydrogels by covalent incorporation of graphene oxide. Small 10(3):514–523PubMedCrossRefPubMedCentralGoogle Scholar
  14. Chang Y, Yang S-T, Liu J-H, Dong E, Wang Y, Cao A, Liu Y, Wang H (2011) In vitro toxicity evaluation of graphene oxide on A549 cells. Toxicol Lett 200(3):201–210PubMedCrossRefPubMedCentralGoogle Scholar
  15. Chaudhari AA, Vig K, Baganizi DR, Sahu R, Dixit S, Dennis V, Singh SR, Pillai SR (2016) Future prospects for scaffolding methods and biomaterials in skin tissue engineering: a review. Int J Mol Sci 17(12):1974PubMedCentralCrossRefGoogle Scholar
  16. Chaudhuri B, Bhadra D, Mondal B, Pramanik K (2014) Biocompatibility of electrospun graphene oxide–poly (ε-caprolactone) fibrous scaffolds with human cord blood mesenchymal stem cells derived skeletal myoblast. Mater Lett 126:109–112CrossRefGoogle Scholar
  17. Chaudhuri B, Bhadra D, Moroni L, Pramanik K (2015) Myoblast differentiation of human mesenchymal stem cells on graphene oxide and electrospun graphene oxide–polymer composite fibrous meshes: importance of graphene oxide conductivity and dielectric constant on their biocompatibility. Biofabrication 7(1):015009PubMedCrossRefPubMedCentralGoogle Scholar
  18. Chaudhuri B, Mondal B, Kumar S, Sarkar SC (2016) Myoblast differentiation and protein expression in electrospun graphene oxide (GO)-poly (ε-caprolactone, PCL) composite meshes. Mater Lett 182:194–197CrossRefGoogle Scholar
  19. Chen G-Y, Pang D-P, Hwang S-M, Tuan H-Y, Hu Y-C (2012a) A graphene-based platform for induced pluripotent stem cells culture and differentiation. Biomaterials 33(2):418–427PubMedCrossRefPubMedCentralGoogle Scholar
  20. Chen Y, Qi Y, Tai Z, Yan X, Zhu F, Xue Q (2012b) Preparation, mechanical properties and biocompatibility of graphene oxide/ultrahigh molecular weight polyethylene composites. Eur Polym J 48(6):1026–1033CrossRefGoogle Scholar
  21. Cherukula K, Manickavasagam Lekshmi K, Uthaman S, Cho K, Cho C-S, Park I-K (2016) Multifunctional inorganic nanoparticles: Recent progress in thermal therapy and imaging. Nanomaterials 6(4):76PubMedCentralCrossRefGoogle Scholar
  22. Ciriza J, del Burgo LS, Virumbrales-Muñoz M, Ochoa I, Fernandez LJ, Orive G, Hernandez RM, Pedraz JL (2015) Graphene oxide increases the viability of C2C12 myoblasts microencapsulated in alginate. Int J Pharm 493(1):260–270PubMedCrossRefPubMedCentralGoogle Scholar
  23. Collins MN, Birkinshaw C (2013) Hyaluronic acid based scaffolds for tissue engineering – a review. Carbohydr Polym 92(2):1262–1279PubMedCrossRefPubMedCentralGoogle Scholar
  24. Depan D, Girase B, Shah JS, Misra RDK (2011) Structure–process–property relationship of the polar graphene oxide-mediated cellular response and stimulated growth of osteoblasts on hybrid chitosan network structure nanocomposite scaffolds. Acta Biomater 7(9):3432–3445PubMedCrossRefPubMedCentralGoogle Scholar
  25. Díez-Pascual AM, Díez-Vicente AL (2016) Poly (propylene fumarate)/polyethylene glycol-modified graphene oxide nanocomposites for tissue engineering. ACS Appl Mater Interfaces 8(28):17902–17914PubMedCrossRefPubMedCentralGoogle Scholar
  26. Dobrovolskaia MA, McNeil SE (2007) Immunological properties of engineered nanomaterials. Nat Nanotechnol 2(8):469–478PubMedCrossRefPubMedCentralGoogle Scholar
  27. Drury JL, Mooney DJ (2003) Hydrogels for tissue engineering: scaffold design variables and applications. Biomaterials 24(24):4337–4351PubMedCrossRefPubMedCentralGoogle Scholar
  28. Dvir T, Timko BP, Kohane DS, Langer R (2011) Nanotechnological strategies for engineering complex tissues. Nat Nanotechnol 6(1):13–22PubMedCrossRefPubMedCentralGoogle Scholar
  29. Elkhenany H, Amelse L, Lafont A, Bourdo S, Caldwell M, Neilsen N, Dervishi E, Derek O, Biris AS, Anderson D (2015) Graphene supports in vitro proliferation and osteogenic differentiation of goat adult mesenchymal stem cells: potential for bone tissue engineering. J Appl Toxicol 35(4):367–374PubMedCrossRefPubMedCentralGoogle Scholar
  30. Engler AJ, Sen S, Sweeney HL, Discher DE (2006) Matrix elasticity directs stem cell lineage specification. Cell 126(4):677–689PubMedCrossRefGoogle Scholar
  31. Fan H, Wang L, Zhao K, Li N, Shi Z, Ge Z, Jin Z (2010) Fabrication, mechanical properties, and biocompatibility of graphene-reinforced chitosan composites. Biomacromolecules 11(9):2345–2351PubMedCrossRefPubMedCentralGoogle Scholar
  32. Golafshan N, Kharaziha M, Fathi M (2017) Tough and conductive hybrid graphene-PVA: alginate fibrous scaffolds for engineering neural construct. Carbon 111:752–763CrossRefGoogle Scholar
  33. Gómez-Navarro C, Burghard M, Kern K (2008) Elastic properties of chemically derived single graphene sheets. Nano Lett 8(7):2045–2049PubMedCrossRefPubMedCentralGoogle Scholar
  34. Guo B, Lei B, Li P, Ma PX (2015) Functionalized scaffolds to enhance tissue regeneration. Regen Biomater 2(1):47–57PubMedPubMedCentralCrossRefGoogle Scholar
  35. Ho J, Walsh C, Yue D, Dardik A, Cheema U (2017) Current advancements and strategies in tissue engineering for wound healing: a comprehensive review. Adv Wound Care 6(6):191–209CrossRefGoogle Scholar
  36. Hood E (2004) Nanotechnology: looking as we leap. Environ Health Perspect 112(13):A740PubMedPubMedCentralCrossRefGoogle Scholar
  37. Hussain SM, Javorina AK, Schrand AM, Duhart HM, Ali SF, Schlager JJ (2006) The interaction of manganese nanoparticles with PC-12 cells induces dopamine depletion. Toxicol Sci 92(2):456–463PubMedCrossRefPubMedCentralGoogle Scholar
  38. Ionita M, Pandele MA, Iovu H (2013) Sodium alginate/graphene oxide composite films with enhanced thermal and mechanical properties. Carbohydr Polym 94(1):339–344PubMedCrossRefGoogle Scholar
  39. Jakus AE, Secor EB, Rutz AL, Jordan SW, Hersam MC, Shah RN (2015) Three-dimensional printing of high-content graphene scaffolds for electronic and biomedical applications. ACS Nano 9(4):4636–4648PubMedCrossRefPubMedCentralGoogle Scholar
  40. Jo H, Sim M, Kim S, Yang S, Yoo Y, Park J-H, Yoon TH, Kim M-G, Lee JY (2016) Electrically conductive graphene/polyacrylamide hydrogels produced by mild chemical reduction for enhanced myoblast growth and differentiation. Acta Biomater 48:100–109PubMedCrossRefPubMedCentralGoogle Scholar
  41. Kalbacova M, Broz A, Kong J, Kalbac M (2010) Graphene substrates promote adherence of human osteoblasts and mesenchymal stromal cells. Carbon 48(15):4323–4329CrossRefGoogle Scholar
  42. Kim MJ, Lee JH, Shin YC, Jin L, Hong SW, Han D-W, Kim Y-J, Kim B (2015a) Stimulated myogenic differentiation of C2C12 murine myoblasts by using graphene oxide. J Korean Phys Soc 67(11):1910–1914CrossRefGoogle Scholar
  43. Kim T-H, Shah S, Yang L, Yin PT, Hossain MK, Conley B, Choi J-W, Lee K-B (2015b) Controlling differentiation of adipose-derived stem cells using combinatorial graphene hybrid-pattern arrays. ACS Nano 9(4):3780–3790PubMedPubMedCentralCrossRefGoogle Scholar
  44. Kim J-W, Shin YC, Lee J-J, Bae E-B, Jeon Y-C, Jeong C-M, Yun M-J, Lee S-H, Han D-W, Huh J-B (2017) The effect of reduced graphene oxide-coated biphasic calcium phosphate bone graft material on osteogenesis. Int J Mol Sci 18(8):1725PubMedCentralCrossRefGoogle Scholar
  45. Krueger E, Chang AN, Brown D, Eixenberger J, Brown R, Rastegar S, Yocham KM, Cantley KD, Estrada D (2016) Graphene foam as a three-dimensional platform for myotube growth. ACS Biomater Sci Eng 2(8):1234–1241PubMedPubMedCentralCrossRefGoogle Scholar
  46. Ku SH, Park CB (2013) Myoblast differentiation on graphene oxide. Biomaterials 34(8):2017–2023PubMedCrossRefPubMedCentralGoogle Scholar
  47. Kumar S, Chatterjee K (2015) Strontium eluting graphene hybrid nanoparticles augment osteogenesis in a 3D tissue scaffold. Nanoscale 7(5):2023–2033PubMedCrossRefPubMedCentralGoogle Scholar
  48. Lalwani G, D’Agati M, Gopalan A, Rao M, Schneller J, Sitharaman B (2017) Three-dimensional macroporous graphene scaffolds for tissue engineering. J Biomed Mater Res A 105(1):73–83PubMedCrossRefPubMedCentralGoogle Scholar
  49. Lam C-W, James JT, McCluskey R, Hunter RL (2004) Pulmonary toxicity of single-wall carbon nanotubes in mice 7 and 90 days after intratracheal instillation. Toxicol Sci 77(1):126–134PubMedCrossRefPubMedCentralGoogle Scholar
  50. Langer R, Vacanti JP (1993) Tissue engineering. Science 260(5110):920–926CrossRefGoogle Scholar
  51. Lee WC, Lim CHY, Shi H, Tang LA, Wang Y, Lim CT, Loh KP (2011) Origin of enhanced stem cell growth and differentiation on graphene and graphene oxide. ACS Nano 5(9):7334–7341PubMedCrossRefPubMedCentralGoogle Scholar
  52. Lee JH, Shin YC, Jin OS, Han D-W, Kang SH, Hong SW, Kim JM (2012a) Enhanced neurite outgrowth of PC-12 cells on graphene-monolayer-coated substrates as biomimetic cues. J Korean Phys Soc 61(10):1696–1699CrossRefGoogle Scholar
  53. Lee JH, Shin YC, Jin OS, Lee EJ, Han D-W, Kang SH, Hong SW, Ahn JY, Kim SH (2012b) Cytotoxicity evaluations of pristine graphene and carbon nanotubes in fibroblastic cells. J Korean Phys Soc 61(6):873–877CrossRefGoogle Scholar
  54. Lee EJ, Lee JH, Shin YC, Hwang D-G, Kim JS, Jin OS, Jin L, Hong SW, Han D-W (2014) Graphene oxide-decorated PLGA/collagen hybrid fiber sheets for application to tissue engineering scaffolds. Biomater Res 18 (1):18-24.Google Scholar
  55. Lee JH, Shin YC, Jin OS, Kang SH, Hwang Y-S, Park J-C, Hong SW, Han D-W (2015a) Reduced graphene oxide-coated hydroxyapatite composites stimulate spontaneous osteogenic differentiation of human mesenchymal stem cells. Nanoscale 7(27):11642–11651PubMedCrossRefPubMedCentralGoogle Scholar
  56. Lee JH, Shin YC, Lee S-M, Jin OS, Kang SH, Hong SW, Jeong C-M, Huh JB, Han D-W (2015b) Enhanced osteogenesis by reduced graphene oxide/hydroxyapatite nanocomposites. Sci Rep 5:18833PubMedPubMedCentralCrossRefGoogle Scholar
  57. Lee WC, Lim CH, Su C, Loh KP, Lim CT (2015c) Cell-assembled graphene biocomposite for enhanced chondrogenic differentiation. Small 11(8):963–969PubMedCrossRefPubMedCentralGoogle Scholar
  58. Lee JH, Lee S-M, Shin YC, Park JH, Hong SW, Kim B, Lee JJ, Lim D, Lim Y-J, Huh JB (2016a) Spontaneous osteodifferentiation of bone marrow-derived mesenchymal stem cells by hydroxyapatite covered with graphene nanosheets. J Biomater Tissue Eng 6(10):818–825CrossRefGoogle Scholar
  59. Lee JH, Lee Y, Shin YC, Kim MJ, Park JH, Hong SW, Kim B, Oh J-W, Park KD, Han D-W (2016b) In situ forming gelatin/graphene oxide hydrogels for facilitated C2C12 myoblast differentiation. Appl Spectrosc Rev 51(7-9):527–539CrossRefGoogle Scholar
  60. Li D, Xia Y (2004) Electrospinning of nanofibers: reinventing the wheel? Adv Mater 16(14):1151–1170CrossRefGoogle Scholar
  61. Li WJ, Laurencin CT, Caterson EJ, Tuan RS, Ko FK (2002) Electrospun nanofibrous structure: a novel scaffold for tissue engineering. J Biomed Mater Res 60(4):613–621PubMedCrossRefPubMedCentralGoogle Scholar
  62. Li X, MacEwan MR, Xie J, Siewe D, Yuan X, Xia Y (2010) Fabrication of density gradients of biodegradable polymer microparticles and their use in guiding neurite outgrowth. Adv Funct Mater 20(10):1632–1637PubMedPubMedCentralCrossRefGoogle Scholar
  63. Li N, Zhang Q, Gao S, Song Q, Huang R, Wang L, Liu L, Dai J, Tang M, Cheng G (2013) Three-dimensional graphene foam as a biocompatible and conductive scaffold for neural stem cells. Sci Rep 3:1604PubMedPubMedCentralCrossRefGoogle Scholar
  64. Liao J, Qu Y, Chu B, Zhang X, Qian Z (2015) Biodegradable CSMA/PECA/graphene porous hybrid scaffold for cartilage tissue engineering. Sci Rep 5:9879PubMedPubMedCentralCrossRefGoogle Scholar
  65. Lin N, Huang J, Dufresne A (2012) Preparation, properties and applications of polysaccharide nanocrystals in advanced functional nanomaterials: a review. Nanoscale 4(11):3274–3294PubMedCrossRefPubMedCentralGoogle Scholar
  66. Liu H, Webster TJ (2007) Nanomedicine for implants: a review of studies and necessary experimental tools. Biomaterials 28(2):354–369PubMedCrossRefPubMedCentralGoogle Scholar
  67. Liu W, Thomopoulos S, Xia Y (2012) Electrospun nanofibers for regenerative medicine. Adv Healthc Mater 1(1):10–25PubMedCrossRefPubMedCentralGoogle Scholar
  68. Liu Y, Dang Z, Wang Y, Huang J, Li H (2014) Hydroxyapatite/graphene-nanosheet composite coatings deposited by vacuum cold spraying for biomedical applications: Inherited nanostructures and enhanced properties. Carbon 67:250–259CrossRefGoogle Scholar
  69. Lu B, Li T, Zhao H, Li X, Gao C, Zhang S, Xie E (2012) Graphene-based composite materials beneficial to wound healing. Nanoscale 4(9):2978–2982PubMedCrossRefPubMedCentralGoogle Scholar
  70. MacDiarmid AG (2001) “Synthetic metals”: a novel role for organic polymers (Nobel lecture). Angew Chem Int Ed 40(14):2581–2590CrossRefGoogle Scholar
  71. Marrella A, Lagazzo A, Barberis F, Catelani T, Quarto R, Scaglione S (2017) Enhanced mechanical performances and bioactivity of cell laden-graphene oxide/alginate hydrogels open new scenario for articular tissue engineering applications. Carbon 115:608–616CrossRefGoogle Scholar
  72. Martín C, Merino S, González-Domínguez JM, Rauti R, Ballerini L, Prato M, Vázquez E (2017) Graphene improves the biocompatibility of polyacrylamide hydrogels: 3D polymeric scaffolds for neuronal growth. Sci Rep 7:10942PubMedPubMedCentralCrossRefGoogle Scholar
  73. Murray E, Thompson BC, Sayyar S, Wallace GG (2015) Enzymatic degradation of graphene/polycaprolactone materials for tissue engineering. Polym Degrad Stab 111:71–77CrossRefGoogle Scholar
  74. Murugan R, Ramakrishna S (2006) Nano-featured scaffolds for tissue engineering: a review of spinning methodologies. Tissue Eng 12(3):435–447PubMedCrossRefPubMedCentralGoogle Scholar
  75. Nayak TR, Andersen H, Makam VS, Khaw C, Bae S, Xu X, Ee P-LR, Ahn J-H, Hong BH, Pastorin G (2011) Graphene for controlled and accelerated osteogenic differentiation of human mesenchymal stem cells. ACS Nano 5(6):4670–4678PubMedCrossRefPubMedCentralGoogle Scholar
  76. Nichol JW, Koshy ST, Bae H, Hwang CM, Yamanlar S, Khademhosseini A (2010) Cell-laden microengineered gelatin methacrylate hydrogels. Biomaterials 31(21):5536–5544PubMedPubMedCentralCrossRefGoogle Scholar
  77. Nie W, Peng C, Zhou X, Chen L, Wang W, Zhang Y, Ma PX, He C (2017) Three-dimensional porous scaffold by self-assembly of reduced graphene oxide and nano-hydroxyapatite composites for bone tissue engineering. Carbon 116:325–337CrossRefGoogle Scholar
  78. Nishida E, Miyaji H, Takita H, Kanayama I, Tsuji M, Akasaka T, Sugaya T, Sakagami R, Kawanami M (2014) Graphene oxide coating facilitates the bioactivity of scaffold material for tissue engineering. Jpn J Appl Phys 53(6S):06JD04CrossRefGoogle Scholar
  79. Norouzi M, Boroujeni SM, Omidvarkordshouli N, Soleimani M (2015) Advances in skin regeneration: application of electrospun scaffolds. Adv Healthc Mater 4(8):1114–1133PubMedCrossRefPubMedCentralGoogle Scholar
  80. O’Brien FJ (2011) Biomaterials & scaffolds for tissue engineering. Mater Today 14(3):88–95CrossRefGoogle Scholar
  81. Papageorgiou DG, Kinloch IA, Young RJ (2017) Mechanical properties of graphene and graphene-based nanocomposites. Prog Mater Sci 90:75–127CrossRefGoogle Scholar
  82. Parak WJ, George M, Kudera M, Gaub HE, Behrends JC (2001) Effects of semiconductor substrate and glia-free culture on the development of voltage-dependent currents in rat striatal neurones. Eur Biophys J 29(8):607–620PubMedCrossRefPubMedCentralGoogle Scholar
  83. Park SY, Park J, Sim SH, Sung MG, Kim KS, Hong BH, Hong S (2011) Enhanced differentiation of human neural stem cells into neurons on graphene. Adv Mater 23(36):H263–H267PubMedCrossRefPubMedCentralGoogle Scholar
  84. Park J, Park S, Ryu S, Bhang SH, Kim J, Yoon JK, Park YH, Cho SP, Lee S, Hong BH (2014) Graphene–regulated cardiomyogenic differentiation process of mesenchymal stem cells by enhancing the expression of extracellular matrix proteins and cell signaling molecules. Adv Healthc Mater 3(2):176–181PubMedCrossRefPubMedCentralGoogle Scholar
  85. Park E-J, Lee G-H, Han BS, Lee B-S, Lee S, Cho M-H, Kim J-H, Kim D-W (2015a) Toxic response of graphene nanoplatelets in vivo and in vitro. Arch Toxicol 89(9):1557–1568PubMedCrossRefPubMedCentralGoogle Scholar
  86. Park J, Kim B, Han J, Oh J, Park S, Ryu S, Jung S, Shin J-Y, Lee BS, Hong BH (2015b) Graphene oxide flakes as a cellular adhesive: prevention of reactive oxygen species mediated death of implanted cells for cardiac repair. ACS Nano 9(5):4987–4999PubMedCrossRefPubMedCentralGoogle Scholar
  87. Park KO, Lee JH, Park JH, Shin YC, Huh JB, Bae J-H, Kang SH, Hong SW, Kim B, Yang DJ (2016) Graphene oxide-coated guided bone regeneration membranes with enhanced osteogenesis: spectroscopic analysis and animal study. Appl Spectrosc Rev 51(7-9):540–551CrossRefGoogle Scholar
  88. Patel A, Mukundan S, Wang W, Karumuri A, Sant V, Mukhopadhyay SM, Sant S (2016a) Carbon-based hierarchical scaffolds for myoblast differentiation: Synergy between nano-functionalization and alignment. Acta Biomater 32:77–88PubMedCrossRefPubMedCentralGoogle Scholar
  89. Patel M, Moon HJ, Ko DY, Jeong B (2016b) Composite system of graphene oxide and polypeptide thermogel as an injectable 3D scaffold for adipogenic differentiation of tonsil-derived mesenchymal stem cells. ACS Appl Mater Interfaces 8(8):5160–5169PubMedCrossRefPubMedCentralGoogle Scholar
  90. Peng S, Feng P, Wu P, Huang W, Yang Y, Guo W, Gao C, Shuai C (2017) Graphene oxide as an interface phase between polyetheretherketone and hydroxyapatite for tissue engineering scaffolds. Sci Rep 7:46604PubMedPubMedCentralCrossRefGoogle Scholar
  91. Qiu C, Bennet KE, Khan T, Ciubuc JD, Manciu FS (2016) Raman and conductivity analysis of graphene for biomedical applications. Materials 9(11):897PubMedCentralCrossRefGoogle Scholar
  92. Ray PC (2010) Size and shape dependent second order nonlinear optical properties of nanomaterials and their application in biological and chemical sensing. Chem Rev 110(9):5332–5365PubMedPubMedCentralCrossRefGoogle Scholar
  93. Ruiz ON, Fernando KS, Wang B, Brown NA, Luo PG, McNamara ND, Vangsness M, Sun Y-P, Bunker CE (2011) Graphene oxide: a nonspecific enhancer of cellular growth. ACS Nano 5(10):8100–8107PubMedCrossRefPubMedCentralGoogle Scholar
  94. Sanchez VC, Jachak A, Hurt RH, Kane AB (2011) Biological interactions of graphene-family nanomaterials: an interdisciplinary review. Chem Res Toxicol 25(1):15–34PubMedPubMedCentralCrossRefGoogle Scholar
  95. Sayyar S, Murray E, Thompson BC, Chung J, Officer DL, Gambhir S, Spinks GM, Wallace GG (2015) Processable conducting graphene/chitosan hydrogels for tissue engineering. J Mater Chem B 3(3):481–490CrossRefGoogle Scholar
  96. Schmidt CE, Shastri VR, Vacanti JP, Langer R (1997) Stimulation of neurite outgrowth using an electrically conducting polymer. Proc Natl Acad Sci U S A 94(17):8948–8953PubMedPubMedCentralCrossRefGoogle Scholar
  97. Seong JM, Kim B-C, Park J-H, Kwon IK, Mantalaris A, Hwang Y-S (2010) Stem cells in bone tissue engineering. Biomed Mater 5(6):062001PubMedCrossRefPubMedCentralGoogle Scholar
  98. Serrano MC, Patiño J, García-Rama C, Ferrer ML, Fierro JLG, Tamayo A, Collazos-Castro JE, del Monte F, Gutierrez MC (2014) 3D free-standing porous scaffolds made of graphene oxide as substrates for neural cell growth. J Mater Chem B 2(34):5698–5706CrossRefGoogle Scholar
  99. Shah S, Yin PT, Uehara TM, Chueng STD, Yang L, Lee KB (2014) Guiding stem cell differentiation into oligodendrocytes using graphene-nanofiber hybrid scaffolds. Adv Mater 26(22):3673–3680PubMedPubMedCentralCrossRefGoogle Scholar
  100. Sharma G, Thakur B, Naushad M, Kumar A, Stadler FJ, Alfadul SM, Mola GT (2017) Applications of nanocomposite hydrogels for biomedical engineering and environmental protection. Environ Chem Lett.  https://doi.org/10.1007/s10311-017-0671-x CrossRefGoogle Scholar
  101. Shin SR, Aghaei-Ghareh-Bolagh B, Dang TT, Topkaya SN, Gao X, Yang SY, Jung SM, Oh JH, Dokmeci MR, Tang XS (2013) Cell-laden microengineered and mechanically tunable hybrid hydrogels of gelatin and graphene oxide. Adv Mater 25(44):6385–6391PubMedPubMedCentralCrossRefGoogle Scholar
  102. Shin YC, Lee JH, Jin L, Kim MJ, Kim YJ, Hyun JK, Jung TG, Hong SW, Han DW (2015a) Stimulated myoblast differentiation on graphene oxide-impregnated PLGA-collagen hybrid fibre matrices. J Nanobiotechnol 13:21CrossRefGoogle Scholar
  103. Shin YC, Lee JH, Jin OS, Kang SH, Hong SW, Kim B, Park J-C, Han D-W (2015b) Synergistic effects of reduced graphene oxide and hydroxyapatite on osteogenic differentiation of MC3T3-E1 preosteoblasts. Carbon 95:1051–1060CrossRefGoogle Scholar
  104. Shin YC, Lee JH, Kim MJ, Hong SW, Kim B, Hyun JK, Choi YS, Park J-C, Han D-W (2015c) Stimulating effect of graphene oxide on myogenesis of C2C12 myoblasts on RGD peptide-decorated PLGA nanofiber matrices. J Biol Eng 9(1):22PubMedPubMedCentralCrossRefGoogle Scholar
  105. Shin SR, Zihlmann C, Akbari M, Assawes P, Cheung L, Zhang K, Manoharan V, Zhang YS, Yüksekkaya M, Kt W (2016a) Reduced graphene oxide-GelMA hybrid hydrogels as scaffolds for cardiac tissue engineering. Small 12(27):3677–3689PubMedPubMedCentralCrossRefGoogle Scholar
  106. Shin YC, Shin DM, Lee EJ, Lee JH, Kim JE, Song SH, Hwang DY, Lee JJ, Kim B, Lim D, Hyon S-H, Lim Y-J, Han D-W (2016b) Hyaluronic acid/PLGA core/shell fiber matrices loaded with EGCG beneficial to diabetic wound healing. Adv Healthc Mater 5(23):3035–3045PubMedCrossRefPubMedCentralGoogle Scholar
  107. Shin YC, Jin L, Lee JH, Jun S, Hong SW, Kim C-S, Kim Y-J, Hyun JK, Han D-W (2017a) Graphene oxide-incorporated PLGA-collagen fibrous matrices as biomimetic scaffolds for vascular smooth muscle cells. Sci Adv Mater 9(2):232–237CrossRefGoogle Scholar
  108. Shin YC, Kang SH, Lee JH, Kim B, Hong SW, Han D-W (2017b) Three-dimensional graphene oxide-coated polyurethane foams beneficial to myogenesis. J Biomater Sci Polym Ed.  https://doi.org/10.1080/09205063.09202017.01348738
  109. Shin YC, Kim J, Kim SE, Song S-J, Hong SW, Oh J-W, Lee J, Park J-C, Hyon S-H, Han D-W (2017c) RGD peptide and graphene oxide co-functionalized PLGA nanofiber scaffolds for vascular tissue engineering. Regen Biomater 4(3):159–166PubMedPubMedCentralCrossRefGoogle Scholar
  110. Shin YC, Song S-J, Hong SW, Jeong SJ, Chrzanowski W, Lee J-C, Han D-W (2017d) Multifaceted biomedical applications of functional graphene nanomaterials to coated substrates, patterned arrays and hybrid scaffolds. Nanomaterials 7(11):369PubMedCentralCrossRefGoogle Scholar
  111. Shuai C, Feng P, Gao C, Shuai X, Xiao T, Peng S (2015) Graphene oxide reinforced poly (vinyl alcohol): nanocomposite scaffolds for tissue engineering applications. RSC Adv 5(32):25416–25423CrossRefGoogle Scholar
  112. Song H, Stevens CF, Gage FH (2002) Astroglia induce neurogenesis from adult neural stem cells. Nature 417(6884):39–44PubMedPubMedCentralCrossRefGoogle Scholar
  113. Song J, Gao H, Zhu G, Cao X, Shi X, Wang Y (2015) The preparation and characterization of polycaprolactone/graphene oxide biocomposite nanofiber scaffolds and their application for directing cell behaviors. Carbon 95:1039–1050CrossRefGoogle Scholar
  114. Tang L, Wang Y, Li Y, Feng H, Lu J, Li J (2009) Preparation, structure, and electrochemical properties of reduced graphene sheet films. Adv Funct Mater 19(17):2782–2789CrossRefGoogle Scholar
  115. Tang M, Song Q, Li N, Jiang Z, Huang R, Cheng G (2013) Enhancement of electrical signaling in neural networks on graphene films. Biomaterials 34(27):6402–6411PubMedCrossRefPubMedCentralGoogle Scholar
  116. Teo WE, Ramakrishna S (2006) A review on electrospinning design and nanofibre assemblies. Nanotechnology 17(14):R89PubMedCrossRefPubMedCentralGoogle Scholar
  117. Unnithan AR, Park CH, Kim CS (2016) Nanoengineered bioactive 3D composite scaffold: a unique combination of graphene oxide and nanotopography for tissue engineering applications. Compos Part B 90:503–511CrossRefGoogle Scholar
  118. Valiev R (2002) Materials science: nanomaterial advantage. Nature 419(6910):887–889PubMedCrossRefPubMedCentralGoogle Scholar
  119. Vasita R, Katti DS (2006) Nanofibers and their applications in tissue engineering. Int J Nanomedicine 1(1):15PubMedPubMedCentralCrossRefGoogle Scholar
  120. Wan C, Frydrych M, Chen B (2011) Strong and bioactive gelatin-graphene oxide nanocomposites. Soft Matter 7(13):6159–6166CrossRefGoogle Scholar
  121. Wang Y, Li Z, Wang J, Li J, Lin Y (2011) Graphene and graphene oxide: biofunctionalization and applications in biotechnology. Trends Biotechnol 29(5):205–212PubMedCrossRefPubMedCentralGoogle Scholar
  122. Wang L, Lu C, Li Y, Wu F, Zhao B, Dong X (2015) Green fabrication of porous silk fibroin/graphene oxide hybrid scaffolds for bone tissue engineering. RSC Adv 5(96):78660–78668CrossRefGoogle Scholar
  123. Wolf MT, Dearth CL, Sonnenberg SB, Loboa EG, Badylak SF (2015) Naturally derived and synthetic scaffolds for skeletal muscle reconstruction. Adv Drug Deliv Rev 84:208–221PubMedCrossRefPubMedCentralGoogle Scholar
  124. Yin H, Ding G, Shi X, Guo W, Ni Z, Fu H, Fu Z (2016) A bioengineered drug-eluting scaffold accelerated cutaneous wound healing in diabetic mice. Colloids Surf B-Biointerfaces 145:226–231PubMedCrossRefPubMedCentralGoogle Scholar
  125. Yoon OJ, Sohn IY, Kim DJ, Lee N-E (2012) Enhancement of thermomechanical properties of poly (D, L-lactic-co-glycolic acid) and graphene oxide composite films for scaffolds. Macromol Res 20(8):789–794CrossRefGoogle Scholar
  126. Yue H, Wei W, Yue Z, Wang B, Luo N, Gao Y, Ma D, Ma G, Su Z (2012) The role of the lateral dimension of graphene oxide in the regulation of cellular responses. Biomaterials 33(16):4013–4021PubMedCrossRefPubMedCentralGoogle Scholar
  127. Zhang H-B, Zheng W-G, Yan Q, Yang Y, Wang J-W, Lu Z-H, Ji G-Y, Yu Z-Z (2010a) Electrically conductive polyethylene terephthalate/graphene nanocomposites prepared by melt compounding. Polymer 51(5):1191–1196CrossRefGoogle Scholar
  128. Zhang Y, Ali SF, Dervishi E, Xu Y, Li Z, Casciano D, Biris AS (2010b) Cytotoxicity effects of graphene and single-wall carbon nanotubes in neural phaeochromocytoma-derived PC12 cells. ACS Nano 4(6):3181–3186PubMedCrossRefPubMedCentralGoogle Scholar
  129. Zhang C, Wang L, Zhai T, Wang X, Dan Y, Turng L-S (2016a) 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 53:403–413PubMedCrossRefPubMedCentralGoogle Scholar
  130. Zhang K, Zheng H, Liang S, Gao C (2016b) Aligned PLLA nanofibrous scaffolds coated with graphene oxide for promoting neural cell growth. Acta Biomater 37:131–142PubMedCrossRefPubMedCentralGoogle Scholar
  131. Zhao C, Tan A, Pastorin G, Ho HK (2013) Nanomaterial scaffolds for stem cell proliferation and differentiation in tissue engineering. Biotechnol Adv 31(5):654–668PubMedCrossRefPubMedCentralGoogle Scholar
  132. Zhou Z-Y, Tian N, Li J-T, Broadwell I, Sun S-G (2011) Nanomaterials of high surface energy with exceptional properties in catalysis and energy storage. Chem Soc Rev 40(7):4167–4185PubMedCrossRefPubMedCentralGoogle Scholar
  133. Zhou K, Motamed S, Thouas GA, Bernard CC, Li D, Parkington HC, Coleman HA, Finkelstein DI, Forsythe JS (2016a) Graphene functionalized scaffolds reduce the inflammatory response and supports endogenous neuroblast migration when implanted in the adult brain. PLoS One 11(3):e0151589PubMedPubMedCentralCrossRefGoogle Scholar
  134. Zhou T, Wang N, Xue Y, Ding T, Liu X, Mo X, Sun J (2016b) Electrospun tilapia collagen nanofibers accelerating wound healing via inducing keratinocytes proliferation and differentiation. Colloids Surf B-Biointerfaces 143:415–422PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  • Yong Cheol Shin
    • 1
  • Su-Jin Song
    • 2
  • Suck Won Hong
    • 2
  • Jin-Woo Oh
    • 3
  • Yu-Shik Hwang
    • 4
  • Yu Suk Choi
    • 5
  • Dong-Wook Han
    • 2
    Email author
  1. 1.Research Center for Energy Convergence TechnologyPusan National UniversityBusanSouth Korea
  2. 2.Department of Cogno-Mechatronics Engineering, College of Nanoscience & NanotechnologyPusan National UniversityBusanSouth Korea
  3. 3.Department of Nanoenergy Engineering, College of Nanoscience & NanotechnologyPusan National UniversityBusanSouth Korea
  4. 4.Department of Maxillofacial Biomedical Engineering, School of DentistryKyung Hee UniversitySeoulSouth Korea
  5. 5.School of Human SciencesUniversity of Western AustraliaCrawleyAustralia

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