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Vol. 10 No. 3 (2018)

Nanostructured Graphene Surfaces Promote Different Stages of Bone Cell Differentiation

https://doi.org/10.1007/s40820-018-0198-0
F. F. Borghi
Plasma Nanoscience, School of Physics, The University of Sydney, Sydney, NSW 2006, Australia
P. A. Bean
CSIRO Manufacturing, P.O. Box 52, North Ryde, NSW 2113, Australia
M. D. M. Evans
CSIRO Manufacturing, P.O. Box 52, North Ryde, NSW 2113, Australia
T. van der Laan
School of Chemistry, Physics and Mechanical Engineering, Queensland University of Technology, Brisbane, QLD 4000, Australia
S. Kumar
School of Chemistry, Physics and Mechanical Engineering, Queensland University of Technology, Brisbane, QLD 4000, Australia
K. Ostrikov
Plasma Nanoscience, School of Physics, The University of Sydney, Sydney, NSW 2006, Australia

Corresponding Author: K. Ostrikov

Kostya.Ostrikov@qut.edu.au

Nano-Micro Letters, Vol. 10 No. 3 (2018), Article Number: 47

Abstract

Nanostructured graphene films were used as platforms for the differentiation of Saos-2 cells into bone-like cells. The films were grown using the plasma-enhanced chemical vapor deposition method, which allowed the production of both vertically and horizontally aligned carbon nanowalls (CNWs). Modifications of the technique allowed control of the density of the CNWs and their orientation after the transfer process. The influence of two different topographies on cell attachment, proliferation, and differentiation was investigated. First, the transferred graphene surfaces were shown to be noncytotoxic and were able to support cell adhesion and growth for over 7 days. Second, early cell differentiation (identified by cellular alkaline phosphatase release) was found to be enhanced on the horizontally aligned CNW surfaces, whereas mineralization (identified by cellular calcium production), a later stage of bone cell differentiation, was stimulated by the presence of the vertical CNWs on the surfaces. These results show that the graphene coatings, grown using the presented method, are biocompatible. And their topographies have an impact on cell behavior, which can be useful in tissue engineering applications.


Highlights:


1 Horizontally and vertically oriented carbon nanowalls (CNWs) have diverse influences on cell behavior.
2 The graphene-based topographies are nontoxic and support cell adhesion and growth.
3 Early cell differentiation was observed on the hybrid graphene layer surfaces. Later cell differentiation was stimulated by the CNW films.
4 The synergy between the CNWs and differentiation medium provides enhanced mineralization.

Keywords

Carbon nanowalls Graphene films Bone cell Cell differentiation Plasma nanoscience
Borghi, F. F., P. A. Bean, M. D. M. Evans, T. van der Laan, S. Kumar, and K. Ostrikov. 2018. “Nanostructured Graphene Surfaces Promote Different Stages of Bone Cell Differentiation”. Nano-Micro Letters 10 (3):47. https://doi.org/10.1007/s40820-018-0198-0.
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References
  1. L.M. Cross, A. Thakur, N.A. Jalili, M. Detamore, A.K. Gaharwar, Nanoengineered biomaterials for repair and regeneration of orthopedic tissue interfaces. Acta Biomater. 42, 2–17 (2016). https://doi.org/10.1016/j.actbio.2016.06.023
  2. R.G. Flemming, C.J. Murphy, G.A. Abrams, S.L. Goodman, P.F. Nealey, Effects of synthetic micro- and nano-structured surfaces on cell behavior. Biomaterials 20(6), 573–588 (1999). https://doi.org/10.1016/S0142-9612(98)00209-9
  3. M.J. Dalby, N. Gadegaard, M.O. Riehle, C.D.W. Wilkinson, A.S.G. Curtis, Investigating filopodia sensing using arrays of defined nano-pits down to 35 nm diameter in size. Int. J. Biochem. Cell Biol. 36(10), 2005–2015 (2004). https://doi.org/10.1016/j.biocel.2004.03.001
  4. A.S.G. Curtis, N. Gadegaard, M.J. Dalby, M.O. Riehle, C.D.W. Wilkinson, G. Aitchison, Cells react to nanoscale order and symmetry in their surroundings. IEEE Trans. Nanobiosci. 3(1), 61–65 (2004). https://doi.org/10.1109/TNB.2004.824276
  5. F.F. Borghi, A.E. Rider, S. Kumar, Z.J. Han, D. Haylock, K. Ostrikov, Emerging stem cell controls: nanomaterials and plasma effects. J. Nanomater. 2013, 329139 (2013). https://doi.org/10.1155/2013/329139
  6. T. Limongi, L. Tirinato, F. Pagliari, A. Giugni, M. Allione, G. Perozziello, P. Candeloro, E. di Fabrizio, Fabrication and applications of micro/nanostructured devices for tissue engineering. Nano-Micro Lett. 9(1), 1 (2017). https://doi.org/10.1007/s40820-016-0103-7
  7. Y. Chen, J. Ni, H. Wu, R. Zhang, C. Zhao, W. Chen, F. Zhang, S. Zhang, X. Zhang, Study of cell behaviors on anodized TiO2 nanotube arrays with coexisting multi-size diameters. Nano-Micro Lett. 8(1), 61–69 (2016). https://doi.org/10.1007/s40820-015-0062-4
  8. C.D. Bandara, S. Singh, I.O. Afara, A. Wolff, T. Tesfamichael, K. Ostrikov, A. Oloyede, Bactericidal effects of natural nanotopography of dragonfly wing on Escherichia coli. ACS Appl. Mater. Interfaces 9(8), 6746–6760 (2017). https://doi.org/10.1021/acsami.6b13666
  9. K. Saha, J.F. Pollock, D.V. Schaffer, K.E. Healy, Designing synthetic materials to control stem cell phenotype. Curr. Opin. Chem. Biol. 11(4), 381–387 (2007). https://doi.org/10.1016/j.cbpa.2007.05.030
  10. G.H. Altman, R.L. Horan, I. Martin, J. Farhadi, P.R.H. Stark, V. Volloch, J.C. Richmond, G. Vunjak-Novakovic, D.L. Kaplan, Cell differentiation by mechanical stress. FASEB J. 16(2), 270–272 (2002). https://doi.org/10.1096/fj.01-0656fje
  11. M.J. Dalby, N. Gadegaard, C.D.W. Wilkinson, The response of fibroblasts to hexagonal nanotopography fabricated by electron beam lithography. J. Biomed. Mater. Res. Part A 84(4), 973–979 (2008). https://doi.org/10.1002/jbm.a.31409
  12. S. Ryoo, Y. Kim, M. Kim, D. Min, Behaviors of NIH-3T3 fibroblasts on graphene/carbon nanotubes: proliferation, focal adhesion, and gene transfection studies. ACS Nano 4(11), 6587–6598 (2010). https://doi.org/10.1021/nn1018279
  13. G.-Y. Chen, D.W.-P. Pang, S.-M. Hwang, H.-Y. Tuan, Y.-C. Hu, A graphene-based platform for induced pluripotent stem cells culture and differentiation. Biomaterials 33(2), 418–427 (2012). https://doi.org/10.1016/j.biomaterials.2011.09.071
  14. H. Shen, L. Zhang, M. Liu, Z. Zhang, Biomedical applications of graphene. Theranostics 2(3), 283–294 (2012). https://doi.org/10.7150/thno.3642
  15. A.M. Pinto, I.C. Gonçalves, F.D. Magalhães, Graphene-based materials biocompatibility: a review. Colloid Surf. B Biointerfaces 111, 188–202 (2013). https://doi.org/10.1016/j.colsurfb.2013.05.022
  16. Z. Zhu, An overview of carbon nanotubes and graphene for biosensing applications. Nano-Micro Lett. 9(3), 25 (2017). https://doi.org/10.1007/s40820-017-0128-6
  17. Z.Q. Yan, W. Zhang, The development of graphene-based devices for cell biology research. Front. Mater. Sci. 8(2), 107–122 (2014). https://doi.org/10.1007/s11706-014-0228-x
  18. K. Kostarelos, K.S. Novoselov, Exploring the interface of graphene and biology. Science 344(6181), 261–263 (2014). https://doi.org/10.1126/science.1246736
  19. N. Dubey, R. Bentini, I. Islam, T. Cao, A.H. Castro Neto, V. Rosa, Graphene: a versatile carbon-based material for bone tissue engineering. Stem Cells Int. 2015, 804213 (2015). https://doi.org/10.1155/2015/804213
  20. A. Sasidharan, L.S. Panchakarla, P. Chandran, D. Menon, S. Nair, C.N.R. Rao et al., Differential nano-bio interactions and toxicity effects of pristine versus functionalized graphene. Nanoscale 3, 2461–2464 (2011). https://doi.org/10.1039/c1nr10172b
  21. W.C. Lee, C.H. Lim, H. Shi, L.A. Tang, Y. Wang, C.T. Lim, K.P. Loh, Origin of enhanced stem cell growth and differentiation on graphene and graphene oxide. ACS Nano 5(9), 7334–7341 (2011). https://doi.org/10.1021/nn202190c
  22. O. Akhavan, E. Ghaderi, Differentiation of human neural stem cells into neural networks on graphene nanogrids. J. Mater. Chem. B 1, 6291–6301 (2013). https://doi.org/10.1039/c3tb21085e
  23. O. Akhavan, E. Ghaderi, M. Shahsavar, Graphene nanogrids for selective and fast osteogenic differentiation of human mesenchymal stem cells. Carbon 59, 200–211 (2013). https://doi.org/10.1016/j.carbon.2013.03.010
  24. M. Kalbacova, A. Broz, J. Kong, M. Kalbac, Graphene substrates promote adherence of human osteoblasts and mesenchymal stromal cells. Carbon 48(15), 4323–4329 (2010). https://doi.org/10.1016/j.carbon.2010.07.045
  25. T.R. Nayak, H. Andersen, V.S. Makam, C. Khaw, S. Bae et al., Graphene for controlled and accelerated osteogenic differentiation of human mesenchymal stem cells. ACS Nano 5(6), 4670–4678 (2011). https://doi.org/10.1021/nn200500h
  26. W. Qi, W. Yuan, J. Yan, H. Wang, Growth and accelerated differentiation of mesenchymal stem cells on graphene oxide/poly-l-lysine composite films. J. Mater. Chem. B 2(33), 5461–5467 (2014). https://doi.org/10.1039/C4TB00856A
  27. A. Solanki, S.T.D. Chueng, P.T. Yin, R. Kappera, M. Chhowalla, K.B. Lee, Axonal alignment and enhanced neuronal differentiation of neural stem cells on graphene-nanoparticle hybrid structures. Adv. Mater. 25(38), 5477–5482 (2013). https://doi.org/10.1002/adma.201302219
  28. S.Y. Park, J. Park, S.H. Sim, M.G. Sung, K.S. Kim, B.H. Hong, S. Hong, Enhanced differentiation of human neural stem cells into neurons on graphene. Adv. Mater. 23(36), 263–267 (2011). https://doi.org/10.1002/adma.201101503
  29. J. Kim, W.-G. Bae, S. Park, Y.J. Kim, I. Jo et al., Engineering structures and functions of mesenchymal stem cells by suspended large-area graphene nanopatterns. 2D Mater. 3(3), 035013 (2016). https://doi.org/10.1088/2053-1583/3/3/035013
  30. O. Akhavan, E. Ghaderi, E. Abouei, S. Hatamie, E. Ghasemi, Accelerated differentiation of neural stem cells into neurons on ginseng-reduced graphene oxide sheets. Carbon 66, 395–406 (2014). https://doi.org/10.1016/j.carbon.2013.09.015
  31. T.C.O. Marsi, T.G. Santos, C. Pacheco-Soares, E.J. Corat, F.R. Marciano, A.O. Lobo, Biomineralization of superhydrophilic vertically aligned carbon nanotubes. Langmuir 28(9), 4413–4424 (2012). https://doi.org/10.1021/la300111k
  32. H. Watanabe, H. Kondo, Y. Okamoto, M. Hiramatsu, M. Sekine, Y. Baba, H. Masaru, Carbon nanowall scaffold to control culturing of cervical cancer cells. Appl. Phys. Lett. 105(24), 244105 (2014). https://doi.org/10.1063/1.4902054
  33. Y. Wu, P. Qiao, T. Chong, Z. Shen, Carbon nanowalls grown by microwave plasma enhanced chemical vapor deposition. Adv. Mater. 14(1), 64–67 (2002). https://doi.org/10.1002/1521-4095(20020104)14:1<64::AID-ADMA64>3.0.CO;2-G
  34. M. Hiramatsu, K. Shiji, H. Amano, M. Hori, Fabrication of vertically aligned carbon nanowalls using capacitively coupled plasma-enhanced chemical vapor deposition assisted by hydrogen radical injection. Appl. Phys. Lett. 84, 4708 (2004). https://doi.org/10.1063/1.1762702
  35. D.H. Seo, S. Kumar, K. Ostrikov, Thinning vertical graphenes, tuning electrical response: from semiconducting to metallic. J. Mater. Chem. 21, 16339–16343 (2011). https://doi.org/10.1039/c1jm13835a
  36. D.H. Seo, S. Kumar, A.E. Rider, Z. Han, K. Ostrikov, Deterministic control of structural and optical properties of plasma-grown vertical graphene nanosheet networks via nitrogen gas variation. Opt. Mater. Express 2(6), 700–707 (2012). https://doi.org/10.1364/OME.2.000700
  37. S. Kumar, I. Levchenko, M. Keidar, K. Ostrikov, Plasma-enabled growth of separated, vertically aligned copper-capped carbon nanocones on silicon. Appl. Phys. Lett. 97, 151503 (2010). https://doi.org/10.1063/1.3502562
  38. T. van der Laan, S. Kumar, K. Ostrikov, Water-mediated and instantaneous transfer of graphene grown at 220 °C enabled by a plasma. Nanoscale 7, 20564–20570 (2015). https://doi.org/10.1039/C5NR06365E
  39. Y. Qi, B. Deng, X. Guo, S. Chen, J. Gao et al., Switching vertical to horizontal graphene growth using faraday cage-assisted PECVD approach for high-performance transparent heating device. Adv. Mater. 30(8), 1704839 (2018). https://doi.org/10.1002/adma.201704839
  40. S. Pineda, F.F. Borghi, D.H. Seo, S. Yick, M. Lawn, T. van der Laan, Z.J. Han, K.K. Ostrikov, Multifunctional graphene micro-islands: rapid, low-temperature plasma-enabled synthesis and facile integration for bioengineering and genosensing applications. Biosens. Bioelectron. 89, 437–443 (2017). https://doi.org/10.1016/j.bios.2016.04.072
  41. M. Prideaux, A.R. Wijenayaka, D.D. Kumarasinghe, R.T. Ormsby, A. Evdokiou, D.M. Findlay, G.J. Atkins, SaOS2 osteosarcoma cells as an in vitro model for studying the transition of human osteoblasts to osteocytes. Calcif. Tissue Int. 95(2), 183–193 (2014). https://doi.org/10.1007/s00223-014-9879-y
  42. E.M. Czekanska, M.J. Stoddart, J.R. Ralphs, R.G. Richards, J.S. Hayes, A phenotypic comparison of osteoblast cell lines versus human primary osteoblasts for biomaterials testing. J. Biomed. Mater. Res. Part A 102(8), 2636–2643 (2014). https://doi.org/10.1002/jbm.a.34937
  43. H.J. Princ, A.K. Braat, D. Gawlitta, W.J. Dhert, D.A. Egan et al., In vitro induction of alkaline phosphatase levels predicts in vivo bone forming capacity of human bone marrow stromal cells. Stem Cell Res. 12(2), 428–440 (2014). https://doi.org/10.1016/j.scr.2013.12.001
  44. S. Ghosh, S.R. Polaki, N. Kumar, S. Amirthapandian, M. Kamruddin, K. Ostrikov, Process-specific mechanisms of vertically oriented graphene growth in plasmas. Beilstein J. Nanotechnol. 8, 1658–1670 (2017). https://doi.org/10.3762/bjnano.8.166
  45. A. Cuesta, P. Dhamelincourt, J. Laureyns, A. Martínez-Alonso, J.M.D. Tascón, Comparative performance of X-ray diffraction and Raman microprobe techniques for the study of carbon materials. J. Mater. Chem. 8, 2875–2879 (1998). https://doi.org/10.1039/a805841e
  46. P. Lespade, R. Al-Jishi, M.S. Dresselhaus, Model for Raman scattering from incompletely graphitized carbons. Carbon 20(5), 427–431 (1982). https://doi.org/10.1016/0008-6223(82)90043-4
  47. Y. Wang, D.C. Alsmeyer, R.L. Mccreery, Raman spectroscopy of carbon materials: structural basis of observed spectra. Chem. Mater. 2(5), 557–563 (1990). https://doi.org/10.1021/cm00011a018
  48. S. Niyogi, E. Bekyarova, M.E. Itkis, H. Zhang, K. Shepperd et al., Spectroscopy of covalently functionalized graphene. Nano Lett. 10(10), 406–4066 (2010). https://doi.org/10.1021/nl1021128
  49. E.C. Stancu, A.-M. Stanciuc, S. Vizireanu, C. Luculescu, L. Moldovan, A. Achour, G. Dinescu, Plasma functionalization of carbon nanowalls and its effect on attachment of fibroblast-like cells. J. Phys D-Appl. Phys. 47, 265203 (2014). https://doi.org/10.1088/0022-3727/47/26/265203
  50. E.C. Stancu, M.D. Ionita, S. Vizireanu, A.M. Stanciuc, L. Moldovan, G. Dinescu, Wettability properties of carbon nanowalls layers deposited by a radiofrequency plasma beam discharge. Mater. Sci. Eng. B 169(1–3), 119–122 (2010). https://doi.org/10.1016/j.mseb.2010.01.062
  51. Z. Bo, Y. Tian, Z. Han, S. Wu, S. Zhang, J. Yan, K. Cen, K. Ostrikov, Tuneable fluidics within graphene nanogaps for water purification and energy storage. Nanoscale Horizons 2, 89–98 (2017). https://doi.org/10.1039/C6NH00167J
  52. J.M. Schakenraad, H.J. Busscher, C.R. Wildevuur, J. Arends, Thermodynamic aspects of cell spreading on solid substrata. Cell Biophys. 13(1), 75–91 (1988). https://doi.org/10.1007/BF02797367
  53. T.A. Horbett, M.B. Schway, Correlations between mouse 3T3 cell spreading and serum fibronectin adsorption on glass and hydroxyethylmethacrylate–ethylmethacrylate copolymers. J. Biomed. Mater. Res. 22(9), 763–793 (1988). https://doi.org/10.1002/jbm.820220903
  54. S. Ghosh, G. Xiong, T.S. Fisher, B. Han, Guidance of cell adhesion and migration by graphitic nanopetals on carbon fibers. Mater. Lett. 184, 211–215 (2016). https://doi.org/10.1016/j.matlet.2016.08.077
  55. R. Ion, S. Vizireanu, C.E. Stancu, C. Luculescu, A. Cimpean, G. Dinescu, Surface plasma functionalization influences macrophage behavior on carbon nanowalls. Mater. Sci. Eng. C 48, 118–125 (2015). https://doi.org/10.1016/j.msec.2014.11.064
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