Enhanced proliferation and osteogenic differentiation of human mesenchymal stem cells on biomineralized three-dimensional graphene foams

Carbon

Volumn 105, Issue , 2016, Pages 233-243

  Zhang, Ting ^a   Li, Ning ^b   Li, Kunyang ^a   Gao, Ruifang ^a   Gu, Wei ^a   Wu, Chengcheng ^a   Su, Ruigong ^c   Liu, Liwei ^c   Zhang, Qi ^a   Liu, Jian ^a  

^a SOOCHOW UNIVERSITY   (China)

^b CHILDREN'S NATIONAL MEDICAL CENTER   (United States)

^c SUZHOU INSTITUTE OF NANO TECH AND NANO BIONICS   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BONE; CELL CULTURE; CELL PROLIFERATION; CELLS; CYTOLOGY; ELECTROPHORESIS; GRAPHENE; STEM CELLS;

BONE REGENERATION; HUMAN MESENCHYMAL STEM CELLS; HUMAN MESENCHYMAL STEM CELLS (HMSCS); NANO-STRUCTURED; OSTEOGENIC DIFFERENTIATION; SIMULATED BODY FLUIDS; THREE-DIMENSIONAL GRAPHENE; WESTERN-BLOT ANALYSIS;

SCAFFOLDS (BIOLOGY);

EID: 84964412973     PISSN: 00086223     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.carbon.2016.04.027     Document Type: Article

References (52)

1. P. Bianco, X. Cao, P.S. Frenette, J.J. Mao, P.G. Robey, P.J. Simmons, and et al. The meaning, the sense and the significance: translating the science of mesenchymal stem cells into medicine Nat. Med. 19 1 2013 35 42
2. A.F. Steinert, L. Rackwitz, F. Gilbert, U. Noth, and R.S. Tuan Concise review: the clinical application of mesenchymal stem cells for musculoskeletal regeneration: current status and perspectives Stem Cells Transl. Med. 1 3 2012 237 247
3. M. Guan, W. Yao, R. Liu, K.S. Lam, J. Nolta, J. Jia, and et al. Directing mesenchymal stem cells to bone to augment bone formation and increase bone mass Nat. Med. 18 3 2012 456 462
4. H.S. Dhowre, S. Rajput, N.A. Russell, and M. Zelzer Responsive cell-material interfaces Nanomedicine 10 5 2015 849 871
5. S.R. Ghaemi, F.J. Harding, B. Delalat, S. Gronthos, and N.H. Voelcker Exploring the mesenchymal stem cell niche using high throughput screening Biomaterials 34 31 2013 7601 7615
6. E. Bressan, L. Ferroni, C. Gardin, L. Sbricoli, L. Gobbato, F. Ludovichetti, and et al. Graphene based scaffolds effects on stem cells commitment J. Transl. Med. 12 1 2014 1 15
7. Y. Wang, Z. Li, J. Wang, J. Li, and Y. Lin Graphene and graphene oxide: biofunctionalization and applications in biotechnology Trends Biotechnol. 29 5 2011 205 212
8. Y. Wang, W.C. Lee, K.K. Manga, P.K. Ang, J. Lu, Y.P. Liu, and et al. Fluorinated graphene for promoting neuro-induction of stem cells Adv. Mater. 24 31 2012 4285 4290
9. G.Y. Chen, D.W. Pang, S.M. Hwang, H.Y. Tuan, and Y.C. Hu A graphene-based platform for induced pluripotent stem cells culture and differentiation Biomaterials 33 2 2012 418 427
10. A. Bendali, L.H. Hess, M. Seifert, V. Forster, A.-F. Stephan, J.A. Garrido, and et al. Purified neurons can survive on peptide-free graphene layers Adv. Healthc. Mater. 2 7 2013 929 933
11. O. Akhavan, E. Ghaderi, and M. Shahsavar Graphene nanogrids for selective and fast osteogenic differentiation of human mesenchymal stem cells Carbon 59 2013 200 211
12. M. Gu, Y. Liu, T. Chen, F. Du, X. Zhao, C. Xiong, and 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. 20 5 2014 477 491
13. Z. Fan, J. Wang, Z. Wang, H. Ran, Y. Li, L. Niu, and et al. One-pot synthesis of graphene/hydroxyapatite nanorod composite for tissue engineering Carbon 66 2014 407 416
14. Y.C. Shin, J.H. Lee, O.S. Jin, S.H. Kang, S.W. Hong, B. Kim, and et al. Synergistic effects of reduced graphene oxide and hydroxyapatite on osteogenic differentiation of MC3T3-E1 preosteoblasts Carbon 95 2015 1051 1060
15. T.R. Nayak, H. Andersen, V.S. Makam, C. Khaw, S. Bae, X. Xu, and et al. Graphene for controlled and accelerated osteogenic differentiation of human mesenchymal stem cells ACS Nano 5 6 2011 4670 4678
16. N. Li, Q. Zhang, S. Gao, Q. Song, R. Huang, L. Wang, and et al. Three-dimensional graphene foam as a biocompatible and conductive scaffold for neural stem cells Sci. Rep. 3 2013 1604
17. M.F. Brizzi, G. Tarone, and P. Defilippi Extracellular matrix, integrins, and growth factors as tailors of the stem cell niche Curr. Opin. Cell Biol. 24 5 2012 645 651
18. O. Akhavan, E. Ghaderi, S.A. Shirazian, and R. Rahighi Rolled graphene oxide foams as three-dimensional scaffolds for growth of neural fibers using electrical stimulation of stem cells Carbon 97 2016 71 77
19. S. Bose, M. Roy, and A. Bandyopadhyay Recent advances in bone tissue engineering scaffolds Trends Biotechnol. 30 10 2012 546 554
20. Y. Liu, Z. Dang, Y. Wang, J. Huang, and H. Li Hydroxyapatite/graphene-nanosheet composite coatings deposited by vacuum cold spraying for biomedical applications: inherited nanostructures and enhanced properties Carbon 67 2014 250 259
21. C. Wu, L. Xia, P. Han, M. Xu, B. Fang, J. Wang, and et al. Graphene-oxide-modified β-tricalcium phosphate bioceramics stimulate in vitro and in vivo osteogenesis Carbon 93 2015 116 129
22. W. Chen, J. Liu, N. Manuchehrabadi, M.D. Weir, Z. Zhu, and H.H. Xu Umbilical cord and bone marrow mesenchymal stem cell seeding on macroporous calcium phosphate for bone regeneration in rat cranial defects Biomaterials 34 38 2013 9917 9925
23. S.M. Zakaria, S.H. Sharif Zein, M.R. Othman, F. Yang, and J.A. Jansen Nanophase hydroxyapatite as a biomaterial in advanced hard tissue engineering: a review Tissue Eng. Part B Rev. 19 5 2013 431 441
24. W. Liu, J. Lipner, J. Xie, C.N. Manning, S. Thomopoulos, and Y. Xia Nanofiber scaffolds with gradients in mineral content for spatial control of osteogenesis ACS Appl. Mater. Interfaces 6 4 2014 2842 2849
25. K.S. Kim, Y. Zhao, H. Jang, S.Y. Lee, J.M. Kim, K.S. Kim, and et al. Large-scale pattern growth of graphene films for stretchable transparent electrodes Nature 457 7230 2009 706 710
26. X. Li, J. Xie, X. Yuan, and Y. Xia Coating electrospun poly(ϵ-caprolactone) fibers with gelatin and calcium phosphate and their use as biomimetic scaffolds for bone tissue engineering Langmuir 24 24 2008 14145 14150
27. W.C. Lee, C.H.Y.X. Lim, H. Shi, L.A.L. Tang, Y. Wang, C.T. Lim, and et al. Origin of enhanced stem cell growth and differentiation on graphene and graphene oxide ACS Nano 5 9 2011 7334 7341
28. Hsu S-h, and G.-S. Huang Substrate-dependent Wnt signaling in MSC differentiation within biomaterial-derived 3D spheroids Biomaterials 34 20 2013 4725 4738
29. S.W. Crowder, D. Prasai, R. Rath, D.A. Balikov, H. Bae, K.I. Bolotin, and et al. Three-dimensional graphene foams promote osteogenic differentiation of human mesenchymal stem cells Nanoscale 5 10 2013 4171 4176
30. N. Li, X. Zhang, Q. Song, R. Su, Q. Zhang, T. Kong, and et al. The promotion of neurite sprouting and outgrowth of mouse hippocampal cells in culture by graphene substrates Biomaterials 32 35 2011 9374 9382
31. E. Santos, R.M. Hernández, J.L. Pedraz, and G. Orive Novel advances in the design of three-dimensional bio-scaffolds to control cell fate: translation from 2D to 3D Trends Biotechnol. 30 6 2012 331 341
32. N.R. Gandavarapu, P.D. Mariner, M.P. Schwartz, and K.S. Anseth Extracellular matrix protein adsorption to phosphate-functionalized gels from serum promotes osteogenic differentiation of human mesenchymal stem cells Acta Biomater. 9 1 2013 4525 4534
33. Y.C. Chai, A. Carlier, J. Bolander, S.J. Roberts, L. Geris, J. Schrooten, and et al. Current views on calcium phosphate osteogenicity and the translation into effective bone regeneration strategies Acta Biomater. 8 11 2012 3876 3887
34. R.A. Surmenev, M.A. Surmeneva, and A.A. Ivanova Significance of calcium phosphate coatings for the enhancement of new bone osteogenesis - a review Acta Biomater. 10 2 2014 557 579
35. W. Liu, Y.-C. Yeh, J. Lipner, J. Xie, H.-W. Sung, S. Thomopoulos, and et al. Enhancing the stiffness of electrospun nanofiber scaffolds with a controlled surface coating and mineralization Langmuir 27 15 2011 9088 9093
36. C. Zhong, and C.C. Chu Biomimetic mineralization of acid polysaccharide-based hydrogels: towards porous 3-dimensional bone-like biocomposites J. Mater. Chem. 22 13 2012 6080 6087
37. S. Choi, and W.L. Murphy The effect of mineral coating morphology on mesenchymal stem cell attachment and expansion J. Mater. Chem. 22 48 2012 25288 25295
38. L. Zhao, S. Mei, P.K. Chu, Y. Zhang, and Z. Wu The influence of hierarchical hybrid micro/nano-textured titanium surface with titania nanotubes on osteoblast functions Biomaterials 31 19 2010 5072 5082
39. Z. Wang, D. Tonderys, S.E. Leggett, E.K. Williams, M.T. Kiani, R. Spitz Steinberg, and et al. Wrinkled, wavelength-tunable graphene-based surface topographies for directing cell alignment and morphology Carbon 97 2016 14 24
40. Z. Chen, W. Ren, L. Gao, B. Liu, S. Pei, and H.-M. Cheng Three-dimensional flexible and conductive interconnected graphene networks grown by chemical vapour deposition Nat. Mater. 10 6 2011 424 428
41. L. Chen, Z. Xiao, Y. Meng, Y. Zhao, J. Han, G. Su, and et al. The enhancement of cancer stem cell properties of MCF-7 cells in 3D collagen scaffolds for modeling of cancer and anti-cancer drugs Biomaterials 33 5 2012 1437 1444
42. K. Lin, M. Zhang, W. Zhai, H. Qu, and J. Chang Fabrication and characterization of hydroxyapatite/wollastonite composite bioceramics with controllable properties for hard tissue repair J. Am. Ceram. Soc. 94 1 2011 99 105
43. R. McBeath, D.M. Pirone, C.M. Nelson, K. Bhadriraju, and C.S. Chen Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment Dev. Cell 6 4 2004 483 495
44. M.K. Gheith, V.A. Sinani, J.P. Wicksted, R.L. Matts, and N.A. Kotov Single-walled carbon nanotube polyelectrolyte multilayers and freestanding films as a biocompatible platform for neuroprosthetic implants Adv. Mater. 17 22 2005 2663 2670
45. K.C. Koehler, D.L. Alge, K.S. Anseth, and C.N. Bowman A Diels-Alder modulated approach to control and sustain the release of dexamethasone and induce osteogenic differentiation of human mesenchymal stem cells Biomaterials 34 16 2013 4150 4158
46. X. Gao, A. Usas, Y. Tang, A. Lu, J. Tan, J. Schneppendahl, and et al. A comparison of bone regeneration with human mesenchymal stem cells and muscle-derived stem cells and the critical role of BMP Biomaterials 35 25 2014 6859 6870
47. D.M. Dohan Ehrenfest, P.G. Coelho, B.S. Kang, Y.T. Sul, and T. Albrektsson Classification of osseointegrated implant surfaces: materials, chemistry and topography Trends Biotechnol. 28 4 2010 198 206
48. K. Kolind, K.W. Leong, F. Besenbacher, and M. Foss Guidance of stem cell fate on 2D patterned surfaces Biomaterials 33 28 2012 6626 6633
49. T.D. Sargeant, C. Aparicio, J.E. Goldberger, H. Cui, and S.I. Stupp Mineralization of peptide amphiphile nanofibers and its effect on the differentiation of human mesenchymal stem cells Acta Biomater. 8 7 2012 2456 2465
50. D. Khang, J. Choi, Y.M. Im, Y.J. Kim, J.H. Jang, S.S. Kang, and et al. Role of subnano-, nano- and submicron-surface features on osteoblast differentiation of bone marrow mesenchymal stem cells Biomaterials 33 26 2012 5997 6007
51. L. Xia, K. Lin, X. Jiang, B. Fang, Y. Xu, J. Liu, and et al. Effect of nano-structured bioceramic surface on osteogenic differentiation of adipose derived stem cells Biomaterials 35 30 2014 8514 8527
52. A.B. Faia-Torres, S. Guimond-Lischer, M. Rottmar, M. Charnley, T. Goren, K. Maniura-Weber, and et al. Differential regulation of osteogenic differentiation of stem cells on surface roughness gradients Biomaterials 35 33 2014 9023 9032