Graphene-Based Materials for Stem Cell Applications

Materials

Volumn 8, Issue 12, 2015, Pages 8674-8690

  Kim, Tae Hyung ^a   Lee, Taek ^b   El Said, Waleed A ^b,c   Choi, Jeong Woo ^b  

^a Chung Ang University   (South Korea)

^b Sogang University   (South Korea)

^c Assiut University   (Egypt)

Author keywords

biomedical applications; detection; differentiation; Graphene; graphene hybrid materials; graphene oxide; graphene scaffolds; stem cell engineering; stem cells; transplantation

Indexed keywords

BIOCOMPATIBILITY; CELLS; CYTOLOGY; DIFFERENTIATION (CALCULUS); DISEASE CONTROL; DISEASES; ERROR DETECTION; GRAPHENE; HYBRID MATERIALS; MEDICAL APPLICATIONS; NEURODEGENERATIVE DISEASES; SCAFFOLDS (BIOLOGY); STEM CELLS; TRANSPLANTATION (SURGICAL);

ALZHEIMER'S DISEASE; BIOMEDICAL APPLICATIONS; CARDIO-VASCULAR DISEASE; GRAPHENE OXIDES; NEUROLOGICAL DISEASE; PARKINSON'S DISEASE; SPINAL CORD INJURIES (SCI); STEM CELL DIFFERENTIATION;

CELL ENGINEERING;

EID: 84952315602     PISSN: None     EISSN: 19961944     Source Type: Journal    
DOI: 10.3390/ma8125481     Document Type: Article

References (85)

1. Geim, A.K.; Novoselov, K.S. The rise of graphene. Nat. Mater. 2007, 6, 183-191. [CrossRef] [PubMed]
2. Li, J.H.; Niu, L.Y.; Zheng, Z.J.; Yan, F. Photosensitive graphene transistors. Adv. Mater. 2014, 26, 5239-5273. [CrossRef] [PubMed]
3. Stankovich, S.; Dikin, D.A.; Dommett, G.H.B.; Kohlhaas, K.M.; Zimney, E.J.; Stach, E.A.; Piner, R.D.; Nguyen, S.T.; Ruoff, R.S. Graphene-based composite materials. Nature 2006, 442, 282-286. [CrossRef] [PubMed]
4. Balandin, A.A.; Ghosh, S.; Bao, W.Z.; Calizo, I.; Teweldebrhan, D.; Miao, F.; Lau, C.N. Superior thermal conductivity of single-layer graphene. Nano Lett. 2008, 8, 902-907. [CrossRef] [PubMed]
5. Gomez-Navarro, C.; Weitz, R.T.; Bittner, A.M.; Scolari, M.; Mews, A.; Burghard, M.; Kern, K. Electronic transport properties of individual chemically reduced graphene oxide sheets. Nano Lett 2007, 7, 3499-3503. [CrossRef] [PubMed]
6. Lee, C.; Wei, X.D.; Kysar, J.W.; Hone, J. Measurement of the elastic properties and intrinsic strength of monolayer graphene. Science 2008, 321, 385-388. [CrossRef] [PubMed]
7. Parlak, O.; Turner, A.P.F.; Tiwari, A. On/off-switchable zipper-like bioelectronics on a graphene interface. Adv. Mater. 2014, 26, 482-486. [CrossRef] [PubMed]
8. Stoller, M.D.; Park, S.J.; Zhu, Y.W.; An, J.H.; Ruoff, R.S. Graphene-based ultracapacitors. Nano Lett. 2008, 8, 3498-3502. [CrossRef] [PubMed] 9. Chung, C.; Kim, Y.K.; Shin, D.; Ryoo, S.R.; Hong, B.H.; Min, D.H. Biomedical applications of graphene and graphene oxide. Acc. Chem. Res. 2013, 46, 2211-2224. [CrossRef] [PubMed]
9. Chung, C.; Kim, Y.K.; Shin, D.; Ryoo, S.R.; Hong, B.H.; Min, D.H. Biomedical applications of graphene and graphene oxide. Acc. Chem. Res. 2013, 46, 2211-2224. [CrossRef] [PubMed]
10. Dong, H.Q.; Li, Y.Y.; Yu, J.H.; Song, Y.Y.; Cai, X.J.; Liu, J.Q.; Zhang, J.M.; Ewing, R.C.; Shi, D.L. A versatile multicomponent assembly via-cyclodextrin hostguest chemistry on graphene for biomedical applications. Small 2013, 9, 446-456. [CrossRef] [PubMed]
11. He, C.; Shi, Z.Q.; Ma, L.; Cheng, C.; Nie, C.X.; Zhou, M.; Zhao, C.S. Graphene oxide based heparin-mimicking and hemocompatible polymeric hydrogels for versatile biomedical applications. J. Mater. Chem. B 2015, 3, 592-602. [CrossRef]
12. Lee, Y.; Bae, J.W.; Thi, T.T.H.; Park, K.M.; Park, K.D. Injectable and mechanically robust 4-arm PPO-PEO/graphene oxide composite hydrogels for biomedical applications. Chem. Commun. 2015, 51, 8876-8879. [CrossRef] [PubMed]
13. Liu, Y.; Dang, Z.H.; Wang, Y.Y.; Huang, J.; Li, H. Hydroxyapatite/graphene-nanosheet composite coatings deposited by vacuum cold spraying for biomedical applications: Inherited nanostructures and enhanced properties. Carbon 2014, 67, 250-259. [CrossRef]
14. Singh, S.K.; Singh, M.K.; Kulkarni, P.P.; Sonkar, V.K.; Gracio, J.J.A.; Dash, D. Amine-modified graphene. Thrombo-protective safer alternative to graphene oxide for biomedical applications. ACS Nano 2012, 6, 2731-2740. [CrossRef] [PubMed]
15. Turcheniuk, K.; Boukherroub, R.; Szunerits, S. Gold-graphene nanocomposites for sensing and biomedical applications. J. Mater. Chem. B 2015, 3, 4301-4324. [CrossRef]
16. Zhang, Y.; Nayak, T.R.; Hong, H.; Cai, W.B. Graphene: A versatile nanoplatform for biomedical applications. Nanoscale 2012, 4, 3833-3842. [CrossRef] [PubMed]
17. Xie, H.; Cao, T.; Gomes, J.V.; Neto, A.H.C.; Rosa, V. Two and three-dimensional graphene substrates to magnify osteogenic differentiation of periodontal ligament stem cells. Carbon 2015, 93, 266-275. [CrossRef]
18. Kang, S.; Park, J.B.; Lee, T.J.; Ryu, S.; Bhang, S.H.; La, W.G.; Noh, M.K.; Hong, B.H.; Kim, B.S. Covalent conjugation of mechanically stiffgraphene oxide flakes to three-dimensional collagen scaffolds for osteogenic differentiation of human mesenchymal stem cells. Carbon 2015, 83, 162-172. [CrossRef]
19. Yoon, H.H.; Bhang, S.H.; Kim, T.; Yu, T.; Hyeon, T.; Kim, B.S. Dual roles of graphene oxide in chondrogenic differentiation of adult stem cells: Cell-adhesion substrate and growth factor-delivery carrier. Adv. Funct. Mater. 2014, 24, 6455-6464. [CrossRef]
20. Tatavarty, R.; Ding, H.; Lu, G.J.; Taylor, R.J.; Bi, X.H. Synergistic acceleration in the osteogenesis of human mesenchymal stem cells by graphene oxide-calcium phosphate nanocomposites. Chem. Commun. 2014, 50, 8484-8487. [CrossRef] [PubMed]
21. Akhavan, O.; Ghaderi, E.; Abouei, E.; Hatamie, S.; Ghasemi, E. Accelerated differentiation of neural stem cells into neurons on ginseng-reduced graphene oxide sheets. Carbon 2014, 66, 395-406. [CrossRef]
22. Ryu, S.; Kim, B.S. Culture of neural cells and stem cells on graphene. Tissue Eng. Regen. Med. 2013, 10, 39-46. [CrossRef]
23. Kim, J.; Kim, Y.R.; Kim, Y.; Lim, K.T.; Seonwoo, H.; Park, S.; Cho, S.P.; Hong, B.H.; Choung, P.H.; Chung, T.D.; et al. Graphene-incorporated chitosan substrata for adhesion and differentiation of human mesenchymal stem cells. J. Mater. Chem. B 2013, 1, 933-938. [CrossRef]
24. Sharma, M.; Afrin, F.; Tripathi, R.P.; Gangenahalli, G. Transgene expression study of CXCR4 active mutants potential prospects in up-modulation of homing and engraftment efficiency of hematopoietic stem/progenitor cells. Cell Adhes. Migr. 2014, 8, 384-388. [CrossRef] [PubMed]
25. Shetty, P.; Thakur, A.M.; Viswanathan, C. Dopaminergic cells, derived from a high efficiency differentiation protocol from umbilical cord derived mesenchymal stem cells, alleviate symptoms in a parkinson's disease rodent model. Cell Biol. Int. 2013, 37, 167-180. [CrossRef] [PubMed]
26. Parte, S.; Bhartiya, D.; Telang, J.; Daithankar, V.; Salvi, V.; Zaveri, K.; Hinduja, I. Detection, characterization, and spontaneous differentiation in vitro of very small embryonic-like putative stem cells in adult mammalian ovary. Stem Cells Dev. 2011, 20, 1451-1464. [CrossRef] [PubMed]
27. Lequeux, C.; Oni, G.; Mojallal, A.; Damour, O.; Brown, S.A. Adipose derived stem cells: Efficiency, toxicity, stability of brdu labeling and effects on self-renewal and adipose differentiation. Mol. Cell Biochem. 2011, 351, 65-75. [CrossRef] [PubMed]
28. He, H.A.; Emmert, M.R.; Marshall, A.G.; Ji, Y.J.; Conrad, C.A.; Priebe, W.; Colman, H.; Lang, F.F.; Madden, T.L. Induced phenotypic differentiation of glioblastoma stem cells revisited-detection of glycomic response based on metabolic labeling. Neuro Oncol. 2010, 12, 119-127.
29. La Rocca, G.; Anzalone, R.; Corrao, S.; Magno, F.; Loria, T.; Lo Iacono, M.; Di Stefano, A.; Giannuzzi, P.; Marasa, L.; Cappello, F.; et al. Isolation and characterization of Oct-4+/HLA-G+ mesenchymal stem cells from human umbilical cord matrix: Differentiation potential and detection of new markers. Histochem. Cell Biol. 2009, 131, 267-282. [CrossRef] [PubMed]
30. Brenner, S.; Whiting-Theobald, N.L.; Malech, H.L. Relationship between length of cell culture, cell division, transduction efficiency and engraftment in NOD/SCID mice of human mobilized CD34+ peripheral blood stem cells. Blood 2002, 100, 184A.
31. Reubinoff, B.E.; Pera, M.F.; Fong, C.Y.; Trounson, A.; Bongso, A. Embryonic stem cell lines from human blastocysts: Somatic differentiation in vitro. Nat. Biotechnol. 2000, 18, 399-404. [PubMed]
32. Lowell, S.; Jones, P.; Le Roux, I.; Dunne, J.; Watt, F.M. Stimulation of human epidermal differentiation by delta-notch signalling at the boundaries of stem-cell clusters. Curr. Biol. 2000, 10, 491-500. [CrossRef]
33. Yao, X.; Peng, R.; Ding, J.D. Cell-material interactions revealed via material techniques of surface patterning. Adv. Mater. 2013, 25, 5257-5286. [CrossRef] [PubMed]
34. Wang, X.; Song, W.; Kawazoe, N.; Chen, G. The osteogenic differentiation of mesenchymal stem cells by controlled cell-cell interaction on micropatterned surfaces. J. Biomed. Mater. Res. A 2013, 101, 3388-3395. [CrossRef] [PubMed]
35. Song, W.; Kawazoe, N.; Chen, G.P. Dependence of spreading and differentiation of mesenchymal stem cells on micropatterned surface area. J. Nanomater. 2011, 2011. [CrossRef]
36. Tay, C.Y.; Yu, H.Y.; Pal, M.; Leong, W.S.; Tan, N.S.; Ng, K.W.; Leong, D.T.; Tan, L.P. Micropatterned matrix directs differentiation of human mesenchymal stem cells towards myocardial lineage. Exp. Cell Res. 2010, 316, 1159-1168. [CrossRef] [PubMed]
37. Solanki, A.; Shah, S.; Memoli, K.A.; Park, S.Y.; Hong, S.; Lee, K.B. Controlling differentiation of neural stem cells using extracellular matrix protein patterns. Small 2010, 6, 2509-2513. [CrossRef] [PubMed] 38. Kilian, K.A.; Bugarija, B.; Lahn, B.T.; Mrksich, M. Geometric cues for directing the differentiation of mesenchymal stem cells. Proc. Natl. Acad. Sci. USA 2010, 107, 4872-4877. [CrossRef] [PubMed]
38. Kilian, K.A.; Bugarija, B.; Lahn, B.T.; Mrksich, M. Geometric cues for directing the differentiation of mesenchymal stem cells. Proc. Natl. Acad. Sci. USA 2010, 107, 4872-4877. [CrossRef] [PubMed]
39. Gao, L.; McBeath, R.; Chen, C.S. Stem cell shape regulates a chondrogenic versus myogenic fate through RAC1 and n-cadherin. Stem Cells 2010, 28, 564-572. [CrossRef] [PubMed]
40. McBeath, R.; Pirone, D.M.; Nelson, C.M.; Bhadriraju, K.; Chen, C.S. Cell shape, cytoskeletal tension, and rhoa regulate stem cell lineage commitment. Dev. Cell 2004, 6, 483-495. [CrossRef]
41. Nayak, T.R.; Andersen, H.; Makam, V.S.; Khaw, C.; Bae, S.; Xu, X.F.; Ee, P.L.R.; Ahn, J.H.; Hong, B.H.; Pastorin, G.; et al. Graphene for controlled and accelerated osteogenic differentiation of human mesenchymal stem cells. ACS Nano 2011, 5, 4670-4678. [CrossRef] [PubMed] 42. Lee, W.C.; Lim, C.H.Y.X.; Shi, H.; Tang, L.A.L.; Wang, Y.; Lim, C.T.; Loh, K.P. Origin of enhanced stem cell growth and differentiation on graphene and graphene oxide. ACS Nano 2011, 5, 7334-7341. [CrossRef] [PubMed]
42. Lee, W.C.; Lim, C.H.Y.X.; Shi, H.; Tang, L.A.L.; Wang, Y.; Lim, C.T.; Loh, K.P. Origin of enhanced stem cell growth and differentiation on graphene and graphene oxide. ACS Nano 2011, 5, 7334-7341. [CrossRef] [PubMed]
43. Talukdar, Y.; Rashkow, J.T.; Lalwani, G.; Kanakia, S.; Sitharaman, B. The effects of graphene nanostructures on mesenchymal stem cells. Biomaterials 2014, 35, 4863-4877. [CrossRef] [PubMed]
44. Kim, J.; Park, S.; Kim, Y.J.; Jeon, C.S.; Lim, K.T.; Seonwoo, H.; Cho, S.-P.; Chung, T.D.; Choung, P.-H.; Choung, Y.-H.; et al. Monolayer graphene-directed growth and neuronal differentiation of mesenchymal stem cells. J. Biomed. Nanotechnol. 2015, 11, 2024-2033. [CrossRef] [PubMed]
45. Park, S.Y.; Park, J.; Sim, S.H.; Sung, M.G.; Kim, K.S.; Hong, B.H.; Hong, S. Enhanced differentiation of human neural stem cells into neurons on graphene. Adv. Mater. 2011, 23, H263-H267. [CrossRef] [PubMed]
46. Shah, S.; Yin, P.T.; Uehara, T.M.; Chueng, S.T.D.; Yang, L.T.; Lee, K.B. Guiding stem cell differentiation into oligodendrocytes using graphene-nanofiber hybrid scaffolds. Adv. Mater. 2014, 26, 3673-3680. [CrossRef] [PubMed]
47. Li, N.; Zhang, Q.; Gao, S.; Song, Q.; Huang, R.; Wang, L.; Liu, L.W.; Dai, J.W.; Tang, M.L.; Cheng, G.S. Three-dimensional graphene foam as a biocompatible and conductive scaffold for neural stem cells. Sci. Rep. 2013, 3. [CrossRef] [PubMed]
48. Park, J.; Kim, I.Y.; Patel, M.; Moon, H.J.; Hwang, S.J.; Jeong, B. 2D and 3D hybrid systems for enhancement of chondrogenic differentiation of tonsil-derived mesenchymal stem cells. Adv. Funct. Mater. 2015, 25, 2573-2582. [CrossRef]
49. Park, J.; Kim, B.; Han, J.; Oh, J.; Park, S.; Ryu, S.; Jung, S.; Shin, J.Y.; Lee, B.S.; Hong, B.H.; et al. Graphene oxide flakes as a cellular adhesive: Prevention of reactive oxygen species mediated death of implanted cells for cardiac repair. ACS Nano 2015, 9, 4987-4999. [CrossRef] [PubMed]
50. Kim, T.H.; Lee, K.B.; Choi, J.W. 3D graphene oxide-encapsulated gold nanoparticles to detect neural stem cell differentiation. Biomaterials 2013, 34, 8660-8670. [CrossRef] [PubMed]
51. Menaa, F. 2-D graphene and derivatives-based scaffolds in regenerative medicine: Innovative boosters mimicking 3-D cell microenvironment. J. Regen. Med. 2013, 2. [CrossRef]
52. 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. 2014. [CrossRef] [PubMed]
53. Nair, M.; Nancy, D.; Krishnan, A.G.; Anjusree, G.S.; Vadukumpully, S.; Nair, S.V. Graphene oxide nanoflakes incorporated gelatin-hydroxyapatite scaffolds enhance osteogenic differentiation of human mesenchymal stem cells. Nanotechnology 2015, 26. [CrossRef] [PubMed]
54. Park, J.; Park, S.; Ryu, S.; Bhang, S.H.; Kim, J.; Yoon, J.K.; Park, Y.H.; Cho, S.P.; Lee, S.; Hong, B.H.; et al. Graphene-regulated cardiomyogenic differentiation process of mesenchymal stem cells by enhancing the expression of extracellular matrix proteins and cell signaling molecules. Adv. Healthc. Mater. 2014, 3, 176-181. [CrossRef] [PubMed]
55. Chaudhuri, B.; Bhadra, D.; Mondal, B.; Pramanik, K. Biocompatibility of electrospun graphene oxide poly(epsilon-caprolactone) fibrous scaffolds with human cord blood mesenchymal stem cells derived skeletal myoblast. Mater. Lett. 2014, 126, 109-112. [CrossRef]
56. Shang, Y.; Zhang, D.; Liu, Y.Y.; Liu, Y. Simultaneous synthesis of diverse graphene via electrochemical reduction of graphene oxide. J. Appl. Electrochem. 2015, 45, 453-462. [CrossRef]
57. Hayes, W.I.; Joseph, P.; Mughal, M.Z.; Papakonstantinou, P. Production of reduced graphene oxide via hydrothermal reduction in an aqueous sulphuric acid suspension and its electrochemical behaviour. J. Solid State Electrochem. 2015, 19, 361-380. [CrossRef]
58. Kauppila, J.; Kunnas, P.; Damlin, P.; Viinikanoja, A.; Kvarnstrom, C. Electrochemical reduction of graphene oxide films in aqueous and organic solutions. Electrochim. Acta 2013, 89, 84-89. [CrossRef]
59. Sasidharan, A.; Panchakarla, L.S.; Chandran, P.; Menon, D.; Nair, S.; Rao, C.N.R.; Koyakutty, M. Differential nano-bio interactions and toxicity effects of pristine versus functionalized graphene. Nanoscale 2011, 3, 2461-2464. [CrossRef] [PubMed]
60. Lv, M.; Zhang, Y.J.; Liang, L.; Wei, M.; Hu, W.B.; Li, X.M.; Huang, Q. Effect of graphene oxide on undifferentiated and retinoic acid-differentiated SH-SY5Y cells line. Nanoscale 2012, 4, 3861-3866. [CrossRef] [PubMed]
61. Yan, L.; Wang, Y.; Xu, X.; Zeng, C.; Hou, J.; Lin, M.; Xu, J.; Sun, F.; Huang, X.; Dai, L.; et al. Can graphene oxide cause damage to eyesight? Chem. Res. Toxicol. 2012, 25, 1265-1270. [CrossRef] [PubMed]
62. Sasidharan, A.; Panchakarla, L.S.; Sadanandan, A.R.; Ashokan, A.; Chandran, P.; Girish, C.M.; Menon, D.; Nair, S.V.; Rao, C.N.R.; Koyakutty, M. Hemocompatibility and macrophage response of pristine and functionalized graphene. Small 2012, 8, 1251-1263. [CrossRef] [PubMed]
63. Wang, K.; Ruan, J.; Song, H.; Zhang, J.L.; Wo, Y.; Guo, S.W.; Cui, D.X. Biocompatibility of graphene oxide. Nanoscale Res. Lett. 2011, 6, 1-8. [CrossRef]
64. Chang, Y.L.; Yang, S.T.; Liu, J.H.; Dong, E.; Wang, Y.W.; Cao, A.N.; Liu, Y.F.; Wang, H.F. In vitro toxicity evaluation of graphene oxide on A549 cells. Toxicol. Lett. 2011, 200, 201-210. [CrossRef] [PubMed]
65. Carpio, I.E.M.; Santos, C.M.; Wei, X.; Rodrigues, D.F. Toxicity of a polymer-graphene oxide composite against bacterial planktonic cells, biofilms, and mammalian cells. Nanoscale 2012, 4, 4746-4756. [CrossRef] [PubMed]
66. Alzhavan, O.; Ghaderi, E.; Shahsavar, M. Graphene nanogrids for selective and fast osteogenic differentiation of human mesenchymal stem cells. Carbon 2013, 59, 200-211.
67. Orive, G.; Anitua, E.; Pedraz, J.L.; Emerich, D.F. Biomaterials for promoting brain protection, repair and regeneration. Nat. Rev. Neurosci. 2009, 10, 682-692. [CrossRef] [PubMed]
68. Ellis-Behnke, R.G.; Liang, Y.X.; You, S.W.; Tay, D.K.C.; Zhang, S.G.; So, K.F.; Schneider, G.E. Nano neuro knitting: Peptide nanofiber scaffold for brain repair and axon regeneration with functional return of vision. Proc. Natl. Acad. Sci. USA 2006, 103, 5054-5059. [CrossRef] [PubMed]
69. Silva, G.A.; Czeisler, C.; Niece, K.L.; Beniash, E.; Harrington, D.A.; Kessler, J.A.; Stupp, S.I. Selective differentiation of neural progenitor cells by high-epitope density nanofibers. Science 2004, 303, 1352-1355. [CrossRef] [PubMed]
70. Akhavan, O.; Ghaderi, E. Differentiation of human neural stem cells into neural networks on graphene nanogrids. J. Mater. Chem. B 2013, 1, 6291-6301. [CrossRef]
71. Yang, D.H.; Li, T.; Xu, M.H.; Gao, F.; Yang, J.; Yang, Z.; Le, W.D. Graphene oxide promotes the differentiation of mouse embryonic stem cells to dopamine neurons. Nanomedicine 2014, 9, 2445-2455. [CrossRef] [PubMed]
72. Pezeshki-Modaress, M.; Mirzadeh, H.; Zandi, M. Gelatin-gag electrospun nanofibrous scaffold for skin tissue engineering: Fabrication and modeling of process parameters. Mater. Sci. Eng. C 2015, 48, 704-712. [CrossRef] [PubMed]
73. Xue, J.J.; He, M.; Liu, H.; Niu, Y.Z.; Crawford, A.; Coates, P.D.; Chen, D.F.; Shi, R.; Zhang, L.Q. Drug loaded homogeneous electrospun PCL/gelatin hybrid nanofiber structures for anti-infective tissue regeneration membranes. Biomaterials 2014, 35, 9395-9405. [CrossRef] [PubMed]
74. Sulong, A.F.; Hassan, N.H.; Hwei, N.M.; Lokanathan, Y.; Naicker, A.S.; Abdullah, S.; Yusof, M.R.; Htwe, O.; Idrus, R.B.H.; Haflah, N.H.M. Collagen-coated polylactic-glycolic acid (PLGA) seeded with neural-differentiated human mesenchymal stem cells as a potential nerve conduit. Adv. Clin. Exp. Med. 2014, 23, 353-362. [CrossRef] [PubMed]
75. Iafisco, M.; Quirici, N.; Foltran, I.; Rimondini, L. Electrospun collagen mimicking the reconstituted extracellular matrix improves osteoblastic differentiation onto titanium surfaces. J. Nanosci. Nanotechnol. 2013, 13, 4720-4726. [CrossRef]
76. Crowder, S.W.; Prasai, D.; Rath, R.; Balikov, D.A.; Bae, H.; Bolotin, K.I.; Sung, H.J. Three-dimensional graphene foams promote osteogenic differentiation of human mesenchymal stem cells. Nanoscale 2013, 5, 4171-4176. [CrossRef] [PubMed]
77. Serrano, M.C.; Patino, J.; Garcia-Rama, C.; Ferrer, M.L.; Fierro, J.L.G.; Tamayo, A.; Collazos-Castro, J.E.; del Monte, F.; Gutierrez, M.C. 3D free-standing porous scaffolds made of graphene oxide as substrates for neural cell growth. J. Mater. Chem. B 2014, 2, 5698-5706. [CrossRef]
78. Guilak, F.; Cohen, D.M.; Estes, B.T.; Gimble, J.M.; Liedtke, W.; Chen, C.S. Control of stem cell fate by physical interactions with the extracellular matrix. Cell Stem Cell 2009, 5, 17-26. [CrossRef] [PubMed] 79. Pelham, R.J.; Wang, Y.L. Cell locomotion and focal adhesions are regulated by substrate flexibility. Proc. Natl. Acad. Sci. USA 1997, 94, 13661-13665. [CrossRef] [PubMed]
79. Pelham, R.J.; Wang, Y.L. Cell locomotion and focal adhesions are regulated by substrate flexibility. Proc. Natl. Acad. Sci. USA 1997, 94, 13661-13665. [CrossRef] [PubMed]
80. Yan, C.; Sun, J.G.; Ding, J.D. Critical areas of cell adhesion on micropatterned surfaces. Biomaterials 2011, 32, 3931-3938. [CrossRef] [PubMed]
81. Peng, R.; Yao, X.; Ding, J.D. Effect of cell anisotropy on differentiation of stem cells on micropatterned surfaces through the controlled single cell adhesion. Biomaterials 2011, 32, 8048-8057. [CrossRef] [PubMed]
82. Kim, T.H.; Shah, S.; Yang, L.T.; Yin, P.T.; Hossain, M.K.; Conley, B.; Choi, J.W.; Lee, K.B. Controlling differentiation of adipose-derived stem cells using combinatorial graphene hybrid-pattern arrays. ACS Nano 2015, 9, 3780-3790. [CrossRef] [PubMed]
83. Bajaj, P.; Rivera, J.A.; Marchwiany, D.; Solovyeva, V.; Bashir, R. Graphene-based patterning and differentiation of C2C12 myoblasts. Adv. Healthc. Mater. 2014, 3, 995-1000. [CrossRef] [PubMed]
84. Yin, P.T.; Shah, S.; Chhowalla, M.; Lee, K.B. Design, synthesis, and characterization of graphene-nanoparticle hybrid materials for bioapplications. Chem. Rev. 2015, 115, 2483-2531. [CrossRef] [PubMed]
85. Solanki, A.; Chueng, S.T.D.; Yin, P.T.; Kappera, R.; Chhowalla, M.; Lee, K.B. Axonal alignment and enhanced neuronal differentiation of neural stem cells on graphene-nanoparticle hybrid structures. Adv. Mater. 2013, 25, 5477-5482. [CrossRef] [PubMed]