Synergistic effects of reduced graphene oxide and hydroxyapatite on osteogenic differentiation of MC3T3-E1 preosteoblasts

Carbon

Volumn 95, Issue , 2015, Pages 1051-1060

  Shin, Yong Cheol ^a   Lee, Jong Ho ^a   Jin, Oh Seong ^a   Kang, Seok Hee ^a   Hong, Suck Won ^a   Kim, Bongju ^b   Park, Jong Chul ^c   Han, Dong Wook ^a  

^a Pusan National University   (South Korea)

^b UNIVERSITY OF TOKUSHIMA   (Japan)

^c Yonsei University College of Medicine   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ALKALINITY; BIOCOMPATIBILITY; BIOLOGICAL MATERIALS; BONE; CELL CULTURE; CELL ENGINEERING; CELLS; CYTOLOGY; HYBRID MATERIALS; HYDROXYAPATITE; PHOSPHATASES; STEM CELLS; TISSUE ENGINEERING;

ALKALINE PHOSPHATASE ACTIVITY; BONE TISSUE ENGINEERING; GRAPHENE-BASED COMPOSITES; MESENCHYMAL STEM CELL; OSTEOGENIC DIFFERENTIATION; OSTEOPROGENITOR CELLS; REDUCED GRAPHENE OXIDES; REDUCED GRAPHENE OXIDES (RGO);

GRAPHENE;

EID: 84943560706     PISSN: 00086223     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.carbon.2015.09.028     Document Type: Article

References (68)

1. I. Rocchietta, F. Fontana, and M. Simion Clinical outcomes of vertical bone augmentation to enable dental implant placement: a systematic review J. Clin. Periodontol. 35 s8 2008 203 215
2. T.J. Blokhuis, and J.J. Chris Arts Bioactive and osteoinductive bone graft substitutes: definitions, facts and myths Injury 42 2011 S26 S29
3. E. Nkenke, V. Weisbach, E. Winckler, P. Kessler, S. Schultze-Mosgau, J. Wiltfang, and F.W. Neukam Morbidity of harvesting of bone grafts from the iliac crest for preprosthetic augmentation procedures: a prospective study Int. J. Oral Maxillofac. Surg. 33 2 2004 157 163
4. G.M. Raghoebar, L. Meijndert, W.W.I. Kalk, and A. Vissink Morbidity of mandibular bone harvesting: a comparative study Int. J. Oral Maxillofac. Implants 22 3 2001 359 365
5. L. Wang, H. Fan, Z.Y. Zhang, A.J. Lou, G.X. Pei, S. Jiang, T.W. Mu, J.J. Qin, S.Y. Chen, and D. Jin Osteogenesis and angiogenesis of tissue-engineered bone constructed by prevascularized β-tricalcium phosphate scaffold and mesenchymal stem cells Biomaterials 31 36 2010 9452 9461
6. M. Bashoor-Zadeh, G. Baroud, and M. Bohner Simulation of the in vivo resorption rate of β-tricalcium phosphate bone graft substitutes implanted in a sheep model Biomaterials 32 27 2011 6362 6373
7. L.G. Galea, M. Bohner, J. Lemaître, T. Kohler, and R. Müller Bone substitute: transforming beta-tricalcium phosphate porous scaffolds into monetite Biomaterials 29 24 2008 3400 3407
8. M. Esposito, M.G. Grusovin, S. Kwan, H.V. Worthington, and P. Coulthard Interventions for replacing missing teeth: Bone augmentation techniques for dental implant treatment Aust. Dent. J. 54 1 2009 70 71
9. P. Amerio, G. Vianale, M. Reale, R. Muraro, A. Tulli, and A. Piattelli The effect of deproteinized bovine bone on osteoblast growth factors and proinflammatory cytokine production Clin. Oral Implants Res. 21 6 2010 650 655
10. ® bone ceramic: histomorphometric results from a randomized controlled multicenter clinical trial Clin. Oral Implants Res. 19 8 2008 796 803
11. D. Turhani, M. Weissenbock, E. Watzinger, K. Yerit, B. Cvikl, R. Ewers, and D. Thurnher In vitro study of adherent mandibular osteoblast-like cells on carrier materials Int. J. Oral Maxillofac. Surg. 34 5 2005 543 550
12. U. Ripamonti, and A.H. Reddi Periodontal regeneration: potential role of bone morphogenetic proteins J. Periodontal Res. 29 4 1994 225 235
13. P.J. Boyne, L.C. Lilly, R.E. Marx, P.K. Moy, M. Nevins, D.B. Spagnoli, and R.G. Triplett De novo bone induction by recombinant human bone morphogenetic protein-2 (rhBMP-2) in maxillary sinus floor augmentation J. Oral Maxillofac. Surg. 63 12 2005 1693 1707
14. R.E. Jung, S.I. Windisch, A.M. Eggenschwiler, D.S. Thoma, F.E. Weber, and C.H.F. Hämmerle A randomized-controlled clinical trial evaluating clinical and radiological outcomes after 3 and 5 years of dental implants placed in bone regenerated by means of GBR techniques with or without the addition of BMP-2 Clin. Oral Implants Res. 20 7 2009 660 666
15. E.A. Wang, V. Rosen, J.S. D'Alessandro, M. Bauduy, P. Cordes, T. Harada, D.I. Israel, R.M. Hewick, K.M. Kerns, P. Lapan, D.P. Luxenberg, D. Mcquaid, I.K. Moutsatsos, J. Nove, and J.M. Wozney Recombinant human bone morphogenetic protein induces bone formation Prac. Natl. Acad. Sci. U. S. A. 87 6 1990 2220 2224
16. R. Lutz, J. Park, E. Felszeghy, J. Wiltfang, E. Nkenke, and K.A. Schlegel Bone regeneration after topical BMP-2-gene delivery in circumferential peri-implant bone defects Clin. Oral Implants Res. 19 6 2008 590 599
17. J.N. Zara, R.K. Siu, X. Zhang, J. Shen, R. Ngo, M. Lee, W. Li, M. Chiang, J. Chung, J. Kwak, B.M. Wu, K. Ting, and C. Soo High doses of bone morphogenetic protein 2 induce structurally abnormal bone and inflammation in vivo Tissue Eng. Part A 17 9-10 2011 1389 1399
18. 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
19. M. Li, Q. Liu, Z. Jia, X. Xu, Y. Cheng, Y. Zheng, T. Xi, and S. Wei Graphene oxide/hydroxyapatite composite coatings fabricated by electrophoretic nanotechnology for biological applications Carbon 67 2014 185 197
20. S. Baradaran, E. Moghaddam, W.J. Basirun, M. Mehrali, M. Sookhakian, M. Hamdi, M.R. Nakhaei Moghaddam, and Y. Alias Mechanical properties and biomedical applications of a nanotube hydroxyapatite-reduced graphene oxide composite Carbon 69 2014 32 45
21. J.D. Núñez, A.M. Benito, R. González, J. Aragón, R. Arenal, and W.K. Maser Integration and bioactivity of hydroxyapatite grown on carbon nanotubes and graphene oxide Carbon 79 2014 590 604
22. J. Wang, Z. Ouyang, Z. Ren, J. Li, P. Zhang, G. Wei, and Z. Su Self-assembled peptide nanofibers on graphene oxide as a novel nanohybrid for biomimetic mineralization of hydroxyapatite Carbon 89 2015 20 30
23. L. Zhang, W. Liu, C. Yue, T. Zhang, P. Li, Z. Xing, and Y. Chen A tough graphene nanosheet/hydroxyapatite composite with improved in vitro biocompatibility Carbon 61 2013 105 115
24. Z. Fan, J. Wang, Z. Wang, H. Ran, Y. Li, L. Niu, P. Gong, B. Liu, and S. Yang One-pot synthesis of graphene/hydroxyapatite nanorod composite for tissue engineering Carbon 66 2014 407 416
25. Y. Zhang, T.R. Nayak, H. Hong, and W. Cai Graphene: a versatile nanoplatform for biomedical applications Nanoscale 4 13 2012 3833 3842
26. L. Feng, L. Wu, and X. Qu New horizons for diagnostics and therapeutic applications of graphene and graphene oxide Adv. Mater 25 2 2013 168 186
27. V. Biju Chemical modifications and bioconjugate reactions of nanomaterials for sensing, imaging, drug delivery and therapy Chem. Soc. Rev. 43 3 2014 744 764
28. T.R. Nayak, H. Andersen, V.S. Makam, C. Khaw, S. Bae, X. Xu, P.L.R. Ee, J.H. Ahn, B.H. Hong, G. Pastorin, and B. Özyilmaz Graphene for controlled and accelerated osteogenic differentiation of human mesenchymal stem cells ACS Nano 5 6 2011 4670 4678
29. W.C. Lee, C.H.Y. Lim, H. Shi, L.A. Tang, Y. Wang, C.T. Lim, and K.P. Loh Origin of enhanced stem cell growth and differentiation on graphene and graphene oxide ACS Nano 5 9 2011 7334 7341
30. S.Y. Park, J. Park, S.H. Sim, M.G. Sung, K.S. Kim, B.H. Hong, and S. Hong Enhanced differentiation of human neural stem cells into neurons on graphene Adv. Mater 23 36 2011 H263 H267
31. N. Li, Q. Zhang, S. Gao, Q. Song, R. Huang, L. Wang, L. Liu, J. Dai, M. Tang, and G. Cheng Three-dimensional graphene foam as a biocompatible and conductive scaffold for neural stem cells Sci. Rep. 3 2013 1604
32. S.H. Ku, and C.B. Park Myoblast differentiation on graphene oxide Biomaterials 34 8 2013 2017 2023
33. W.C. Lee, C.H. Lim, Su C. Kenry, K.P. Loh, and C.T. Lim Cell-assembled graphene biocomposite for enhanced chondrogenic differentiation Small 11 8 2015 963 969
34. S. Park, and R.S. Ruoff Chemical methods for the production of graphenes Nat. Nanotechnol. 4 4 2009 217 224
35. S. Das, S. Singh, V. Singh, D. Joung, J.M. Dowding, D. Reid, J. Anderson, L. Zhai, S.I. Khondaker, W.T. Self, and S. Seal Oxygenated functional group density on graphene oxide: Its effect on cell toxicity Part Part Syst. Charact. 30 2 2013 148 157
36. H. Zanin, E. Saito, F.R. Marciano, H.J. Ceragioli, A.E.C. Granato, M. Porcionattod, and A.O. Lobo Fast preparation of nano-hydroxyapatite/superhydrophilic reduced graphene oxide composites for bioactive applications J. Mater Chem. B 1 38 2013 4947 4955
37. W.S. Hummers, and R.E. Offeman Preparation of graphitic oxide J. Am. Chem. Soc. 80 6 1958 1339
38. S. Park, J. An, I. Jung, R.D. Piner, S.J. An, X. Li, A. Velamakanni, and R.S. Ruoff Colloidal suspensions of highly reduced graphene oxide in a wide variety of organic solvents Nano Lett. 9 4 2009 1593 1597
39. B.K. Lim, F. Sun, S.C. Ryu, K. Koh, D.W. Han, and J. Lee Hydroxyapatite coating on damaged tooth surfaces by immersion Biomed. Mater 4 2 2009 025017
40. D.A. Dikin, S. Stankovich, E.J. Zimney, R.D. Piner, G.H.B. Dommett, G. Evmenenko, S.T. Nguyen, and R.S. Ruoff Preparation and characterization of graphene oxide paper Nature 448 7152 2007 457 460
41. W. Cui, M. Li, J. Liu, B. Wang, C. Zhang, L. Jiang, and Q. Cheng A strong integrated strength and toughness artificial nacre based on dopamine cross-linked graphene oxide ACS Nano 8 9 2014 9511 9517
42. O.C. Compton, B. Jain, D.A. Dikin, A. Abouimrane, K. Amine, and S.T. Nguyen Chemically active reduced graphene oxide with tunable C/O ratios ACS Nano 5 6 2011 4380 4391
43. Y. Sanguansak, P. Srimuk, A. Krittayavathananon, S. Luanwuthi, N. Chinvipas, P. Chiochan, J. Khuntilo, P. Klunbud, T. Mungcharoen, and M. Sawangphruk Permselective properties of graphene oxide and reduced graphene oxide electrodes Carbon 68 2014 662 669
44. G. Bharath, R. Madhu, S.M. Chen, V. Veeramani, A. Balamurugan, D. Mangalaraj, C. Viswanathan, and N. Ponpandian Enzymatic electrochemical glucose biosensors by mesoporous 1D hydroxyapatite-on-2D reduced graphene oxide J. Mater Chem. B 3 7 2015 1360 1370
45. E.J. Gudiña, J.A. Teixeira, and L.R. Rodrigues Biosurfactant-producing lactobacilli: Screening, production profiles, and effect of medium composition Appl. Environ. Soil Sci. 2011 2011 201254
46. H. Mohammadi, M. Hafezi, N. Nezafati, S. Heasarki, A. Nadernezhad, S.M.H. Ghazanfari, and M. Sepantafar Bioinorganics in bioactive calcium silicate ceramics for bone tissue repair: Bioactivity and biological properties J. Ceram. Sci. Technol. 5 2014 1 12
47. L. Wang, G. Zhou, H. Liu, X. Niu, J. Han, L. Zheng, and Y. Fan Nano-hydroxyapatite particles induce apoptosis on MC3T3-E1 cells and tissue cells in SD rats Nanoscale 4 9 2012 2894 2899
48. J. Xu, P. Xu, Z. Li, J. Huang, and Z. Yang Oxidative stress and apoptosis induced by hydroxyapatite nanoparticles in C6 cells J. Biomed. Mater Res. A 100 3 2012 738 745
49. X. Zhao, S. Ng, B.C. Heng, J. Guo, L. Ma, T.T.Y. Tan, K.W. Ng, and S.C.J. Loo Cytotoxicity of hydroxyapatite nanoparticles is shape and cell dependent Arch. Toxicol. 87 6 2013 1037 1052
50. Y. Zhu, W. Li, Q. Li, Y. Li, Y. Li, X. Zhang, and Q. Huang Effects of serum proteins on intracellular uptake and cytotoxicity of carbon nanoparticles Carbon 47 5 2009 1351 1358
51. W. Hu, C. Peng, M. Lv, X. Li, Y. Zhang, N. Chen, C. Fan, and Q. Huang Protein corona-mediated mitigation of cytotoxicity of graphene oxide ACS Nano 5 5 2011 3693 3700
52. H.S. Jung, T. Lee, I.K. Kwon, H.S. Kim, S.K. Hahn, and C.S. Lee Surface modification of multipass caliber-rolled Ti alloy with dexamethasone-loaded graphene for dental applications ACS Appl. Mater. Interfaces 7 2015 9598 9607
53. E. Birmingham, G.L. Niebur, P.E. McHugh, G. Shaw, F.P. Barry, and L.M. McNamara Osteogenic differentiation of mesenchymal stem cells is regulated by osteocyte and osteoblast cells in a simplified bone niche Eur. Cell Mater. 23 2012 13 27
54. L. Kyllönen, S. Haimi, B. Mannerström, H. Huhtala, K.M. Rajala, H. Skottman, G.K. Sándor, and S. Miettinen Effects of different serum conditions on osteogenic differentiation of human adipose stem cells in vitro Stem Cell Res. Ther. 4 1 2013 17
55. G.S. Stein, and J.B. Lian Molecular mechanisms mediating proliferation/differentiation interrelationships during progressive development of the osteoblast phenotype Endocr. Rev. 14 4 1993 424 442
56. M. Li, Y. Wang, Q. Liu, Q. Li, Y. Cheng, Y. Zheng, T. Xi, and S. Wei In situ synthesis and biocompatibility of nano hydroxyapatite on pristine and chitosan functionalized graphene oxide J. Mater. Chem. B 1 4 2013 475 484
57. Y. Liu, J. Huang, and H. Li Synthesis of hydroxyapatite-reduced graphite oxide nanocomposites for biomedical applications: oriented nucleation and epitaxial growth of hydroxyapatite J. Mater. Chem. B 1 2013 1826 1834
58. 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
59. M.J. Dalby, D. McCloy, M. Robertson, H. Agheli, D. Sutherland, S. Affrossman, and R.O.C. Oreffo Osteoprogenitor response to semi-ordered and random nanotopographies Biomaterials 27 15 2006 2980 2987
60. M.J. Dalby, N. Gadegaard, R. Tare, A. Andar, M.O. Riehle, P. Herzyk, C.D.W. Wilkinson, and R.O.C. Oreffo The control of human mesenchymal cell differentiation using nanoscale symmetry and disorder Nat. Mater. 6 12 2007 997 1003
61. S. Kumar, and K. Chatterjee Strontium eluting graphene hybrid nanoparticles augment osteogenesis in a 3D tissue scaffold Nanoscale 7 5 2015 2023 2033
62. J. Cheng, H. Liu, B. Zhao, R. Shen, D. Liu, J. Hong, H. Wei, P. Xi, F. Chen, and D. Bai MC3T3-E1 preosteoblast cell-mediated mineralization of hydroxyapatite by polydopamine-functionalized graphene oxide J. Bioact. Compat. Pol. 30 3 2015 289 301
63. M. Nair, D. Nancy, A.G. Krishnan, G.S. Anjusree, S. Vadukumpully, and S.V. Nair Graphene oxide nanoflakes incorporated gelatin-hydroxyapatite scaffolds enhance osteogenic differentiation of human mesenchymal stem cells Nanotechnology 26 16 2015 161001
64. J.H. Lee, Y.C. Shin, O.S. Jin, S.H. Kang, Y.S. Hwang, J.C. Park, S.W. Hong, and D.W. Han Reduced graphene oxide-coated hydroxyapatite composites stimulate spontaneous osteogenic differentiation of human mesenchymal stem cells Nanoscale 7 27 2015 11642 11651
65. H. Liu, J. Cheng, F. Chen, D. Bai, C. Shao, J. Wang, P. Xi, and Z. Zeng Gelatin functionalized graphene oxide for mineralization of hydroxyapatite: biomimetic and in vitro evaluation Nanoscale 6 10 2014 5315 5322
66. J. Kim, Y.R. Kim, Y. Kim, K.T. Lim, H. Seonwoo, S. Park, S.P. Cho, B.H. Hong, P.H. Choung, T.D. Chung, Y.H. Choung, and J.H. Chung Graphene-incorporated chitosan substrata for adhesion and differentiation of human mesenchymal stem cells J. Mater. Chem. B 1 7 2013 933 938
67. M. Mehrali, M. Mehrali, E. Moghaddam, S.F. Shirazi, S. Baradaran, M. Mehrali, S.T. Latibari, H.S. Metselaar, N.A. Kadri, K. Zandi, and N.A. Osman Synthesis, mechanical properties, and in vitro biocompatibility with osteoblasts of calcium silicate-reduced graphene oxide composites ACS Appl. Mater. Interfaces 6 6 2014 3947 3962
68. R. Tatavarty, H. Ding, G. Lu, R.J. Taylor, and X. Bi Synergistic acceleration in the osteogenesis of human mesenchymal stem cells by graphene oxide-calcium phosphate nanocomposites Chem. Commun. 50 62 2015 8484 8487