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Biomimetic scaffold development for bone tissue engineering: Crosslinking graphene with collagen to enhance mechanical strength, conductivity, and porous structure

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Abstract

In this study, we extract type I collagen from fish scales and employ an electrostatic self-assembly technique to crosslink it with negatively charged graphene. By incorporating 0%, 1%, 5%, and 10% weight of graphene with collagen, we significantly enhance the mechanical strength, conductivity, and 3D porous structure of the scaffolds. The incorporation of graphene increases the Young’s modulus of the scaffolds threefold compared to pure collagen scaffolds. Impedance measurements reveal values of 4 kΩ, 2.5 kΩ, and 1 kΩ for scaffolds containing 1%, 5%, and 10% weight of graphene with collagen, respectively. The scaffolds demonstrate cell viability above 90%, and the osteogenic differentiation potential, as determined by ALP assay, confirms successful osteogenesis. Moreover, the eco-friendly synthesis route establishes the hybrid 3D graphene-collagen nanocomposite scaffold as a stable material with excellent biocompatible properties in a biological medium.

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References

  1. B.S. Kim, I.K. Park, T. Hoshiba, H.L. Jiang, Y.J. Choi, T. Akaike, C.S. Cho, Prog. Polym. Sci. 36, 238 (2011)

    Article  CAS  Google Scholar 

  2. C. Dong, Y. Lv, Polymers 8, 42 (2016)

    Article  Google Scholar 

  3. L. Cen, W. Liu, L. Cui, W. Zhang, Y. Cao, Pediatr. Res. 63, 492 (2008)

    Article  CAS  Google Scholar 

  4. K. Gelse, E. Pöschl, T. Aigner, Adv. Drug Deliv. Rev. 55, 1531 (2003)

    Article  CAS  Google Scholar 

  5. Y. Li, Y. Liu, R. Li, H. Bai, Z. Zhu, L. Zhu, C. Zhu, Z. Che, H. Liu, J. Wang, L. Huang, Mater. Des. 210, 110049 (2021)

    Article  CAS  Google Scholar 

  6. G.A. Rico-Llanos, S.B. Gonzalez, M.M. Donos, J. Becerra, R. Visser, Polymers 13, 599 (2021)

    Article  CAS  Google Scholar 

  7. U. Cheema, M. Ananta, V. Mudera, Regenerative Medicine and Tissue Engineering Cells and Biomaterials (Intechopen, London, 2011)

    Google Scholar 

  8. K. Silvipriya, K.K. Kumar, A. Bhat, B.D. Kumar, A. John, P. Lakshmanan, J. Appl. Pharm. 5, 123 (2015)

    Google Scholar 

  9. S.F. Badylak, Transpl. Immunol. 12, 367 (2004)

    Article  CAS  Google Scholar 

  10. A. Shavandi, Y. Hou, A. Carne, M. McConnell, A.E.-D.A. Bekhit, Adv. Food Nutr. Res. 87, 187 (2019)

    Article  CAS  Google Scholar 

  11. S. Liu, C. Lau, K. Liang, F. Wen, S. Teoh, Curr. Opin. Biotechmol. 74, 92 (2022)

    Article  CAS  Google Scholar 

  12. H. Jafari, A. Lista, M.M. Siekapen, P. Ghaffari-Bohlouli, L. Nie, H. Alimoradi, A. Shavandi, Polymers 12, 2230 (2020)

    Article  CAS  Google Scholar 

  13. S. Yamada, K. Yamamoto, T. Ikeda, K. Yanagiguchi, Y. Hayashi, Biomed. Res. Int. 2014, 302932 (2014)

    Article  Google Scholar 

  14. S. Dinescu, M. Albu Kaya, L. Chitoiu, S. Ignat, D.A. Kaya, M. Costache, Cellulose-Based Superabsorbent Hydrogels (Springer, Cham, 2019), p.1643

    Book  Google Scholar 

  15. D. Durgalakshmi, S. Vimalraj, R.A. Rakkesh, S. Sekaran, P. Bargavi, S. Balakumar, Mater. Sci. Eng. C 126, 111856 (2012)

    Google Scholar 

  16. C. Zhou, S. Liu, J. Li, K. Guo, Q. Yuan, A. Zhong, J. Yang, J. Wang, J. Sun, Z. Wang, A.C.S. Appl, Mater. Interfaces 10, 44080 (2018)

    Article  CAS  Google Scholar 

  17. R. Pavithra, R.A. Rakkesh, D. Durgalakshmi, S. Balakumar, Graphene 2, 113 (2014)

    Article  Google Scholar 

  18. Y. Zhang, T.R. Nayak, H. Hong, W. Cai, Nanoscale 4, 3833 (2012)

    Article  CAS  Google Scholar 

  19. S. Tharani, D. Durgalakshmi, S. Balakumar, R.A. Rakkesh, ChemistrySelect 7, e202203603 (2022)

    Article  CAS  Google Scholar 

  20. A.K. Geim, Science 324, 1530 (2009)

    Article  CAS  Google Scholar 

  21. R. Ajay Rakkesh, D. Durgalakshmi, S. Balakumar, Nanotechnology 33, 495703 (2022)

    Article  Google Scholar 

  22. M.H. Norahan, M. Amroon, R. Ghahremanzadeh, M. Mahmoodi, N. Baheiraei, J. Biomed. Mater. Res. A 107, 204 (2018)

    Article  Google Scholar 

  23. A.F. Girão, G. Gonçalves, K.S. Bhangra, J.B. Phillips, J. Knowles, G. Irurueta, M.K. Singh, I. Badkin, A. Completo, P.A.A.P. Marques, RSC Adv. 6, 49039 (2016)

    Article  Google Scholar 

  24. S. Bahrami, N. Baheiraei, M. Shahrezaee, Biomimetic reduced graphene oxide coated collagen scaffold for in situ bone regeneration. Sci. Rep. 11, 16783 (2021)

    Article  CAS  Google Scholar 

  25. P.N.B. Rebecca, D. Durgalakshmi, S. Balakumar, R.A. Rakkesh, ChemistrySelect 7, e202104013 (2022)

    Article  Google Scholar 

  26. H. Fang, C. Luo, S. Liu, M. Zhou, Y. Zeng, J. Hou, L. Chen, S. Mou, J. Sun, Z. Wang, Theranostics 10, 2759 (2020)

    Article  CAS  Google Scholar 

  27. S. Liu, C. Zhou, S. Mou, J. Li, M. Zhou, Y. Zeng, C. Luo, J. Sun, Z. Wang, W. Xu, Mater. Sci. Eng. C 105, 110137 (2019)

    Article  CAS  Google Scholar 

  28. B.H. León-Mancilla, M.A. Araiza-Téllez, J.O. Flores-Flores, M.C. Piña-Barba, J. Appl. Res. Tech. 14, 77 (2016)

    Article  Google Scholar 

  29. C. Liu, Z. Han, J.T. Czernuszka, Acta Biomater. 5, 661 (2009)

    Article  CAS  Google Scholar 

  30. I.V. Antoniac, A. Antoniac, E. Vasile, C. Tecu, M. Fosca, V.G. Yankova, J.V. Rau, Bioact. Mater. 6, 3383 (2021)

    Article  CAS  Google Scholar 

  31. J. Gu, K. Jiao, J. Li, J. Yan, K. Wang, F. Wang, Y. Liu, F.R. Tay, J. Chen, L. Niu, Bioact. Mater. 15, 68 (2022)

    Article  CAS  Google Scholar 

  32. N.S. Kumar, S. Das, C. Bernhard, G.D. Varma, Supercond. Sci. Tech. 26, 095008 (2013)

    Article  Google Scholar 

  33. C. Gullekson, L. Lucas, K. Hewitt, L. Kreplak, Biophys. J. 100, 1837 (2011)

    Article  CAS  Google Scholar 

  34. T. Ikoma, H. Kobayashi, J. Tanaka, D. Walsh, S. Mann, Int. J. Biol. Macromol. 32, 199 (2003)

    Article  CAS  Google Scholar 

  35. E. Brauchle, J. Kasper, R. Daum, N. Schierbaum, C. Falch, A. Kirschniak, T.E. Schäffer, K. Schenke-Layland, Matrix Biol. 68, 180 (2018)

    Article  Google Scholar 

  36. M.G. Martinez, A.J. Bullock, S. MacNeil, I.U. Rehman, Appl. Spectrosc. Rev. 54, 509 (2019)

    Article  CAS  Google Scholar 

  37. S. Li, C. Tian, M. Li, X. Meng, L. Wang, R. Wang, J. Yin, H. Fu, J. Mater. Chem. A 1, 6462 (2013)

    Article  Google Scholar 

  38. G. Wang, J. Yang, J. Park, X. Gou, B. Wang, H. Liu, J. Yao, J. Phys. Chem. C 112, 8192 (2008)

    Article  CAS  Google Scholar 

  39. Y. Zeng, M. Zhou, L. Chen, H. Fang, S. Liu, C. Zhou, J. Sun, Z. Wang, Bioact. Mater. 5, 859 (2020)

    Article  Google Scholar 

  40. G. Agarwal, N. Kumar, S. Akshay, Mater. Sci. Eng. C 118, 111518 (2021)

    Article  CAS  Google Scholar 

  41. V. Karageorgiou, D. Kaplan, Biomaterials 26, 5474 (2005)

    Article  CAS  Google Scholar 

  42. N. Abbasi, S. Hamlet, R.M. Love, N. Nguyen, J. Sci. Adv. Mater. Dev. 5, 1 (2020)

    Google Scholar 

  43. H. Qu, H. Fu, Z. Han, Y. Sun, RSC Adv. 9, 26252 (2019)

    Article  CAS  Google Scholar 

  44. T. Zheng, Y. Huang, X. Zhang, Q. Cai, X. Deng, X. Yang, J. Mater. Chem. B 8, 10221 (2020)

    Article  CAS  Google Scholar 

  45. H. Yu, H. Zhao, C. Huang, Y. Du, A.C.S. Biomater, Sci. Eng. 3, 3017 (2017)

    CAS  Google Scholar 

  46. N. Abzan, M. Kharaziha, S. Labbaf, Mater. Des. 167, 107636 (2019)

    Article  CAS  Google Scholar 

  47. D.T. Dixon, C.T. Gomillion, J. Funct. Biomater. 13, 1 (2021)

    Article  Google Scholar 

  48. E. Kolanthai, P.A. Sindu, D.K. Khajuria, S.C. Veerla, D. Kuppuswamy, L.H. Catalani, D.R. Mahapatra, A.C.S. Appl, Mater. Interface 10, 12441 (2018)

    Article  CAS  Google Scholar 

  49. F.J. O’Brien, B.A. Harley, M.A. Waller, I.V. Yannas, L.J. Gibson, P.J. Prendergast, Technol. Health Care 15, 3 (2007)

    Article  Google Scholar 

  50. V.C. Dumont, H.S. Mansur, A.A.P. Mansur, S.M. Carvalho, N.S.V. Capanema, B.R. Barrioni, R. Breno, Inter. J. Bio. Macromol. 93, 1465 (2016)

    Article  CAS  Google Scholar 

  51. T. Shalini, R. Ajay Rakkesh, S. Balakumar, Biomed. Mater. Res. Part B Appl. Biomater. 111, 858 (2022)

    Google Scholar 

  52. S. Kale, S. Bermann, C. Edwards, C. Tarnowski, M. Morris, M.W. Long, Nat. Biotehnol. 18, 954 (2000)

    Article  CAS  Google Scholar 

  53. Y. Zhang, L. Ye, J. Cui, B. Yang, H. Sun, J. Li, F. Yao, A.C.S. Biomater, Sci. Eng. 2, 544 (2016)

    CAS  Google Scholar 

  54. A. Deng, Y. Yang, S. Du, S. Yang, Biomater. Sci. 5, 2197 (2018)

    Article  Google Scholar 

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Acknowledgments

The author acknowledges the University Grant Commission—Dr D. S. Kothari Postdoctoral fellowship (EN/16-17/0030) to carry out this research work.

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Authors and Affiliations

  1. Functional Nano-Materials (FuN) Laboratory, Department of Physics and Nanotechnology, Faculty of Engineering and Technology, SRM Institute of Science and Technology, Kattankulathur, 603203, India

    P. N. Blessy Rebecca & R. Ajay Rakkesh

  2. Department of Medical Physics, Anna University, Chennai, 600 025, India

    D. Durgalakshmi

  3. National Centre for Nanoscience and Nanotechnology, University of Madras, Chennai, 600 025, India

    S. Balakumar

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  1. P. N. Blessy Rebecca
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  2. D. Durgalakshmi
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  3. S. Balakumar
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Contributions

PNBR—Experimental design and carrying out measurements; DD—manuscript composition and RAR—conception and manuscript composition.

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Correspondence to R. Ajay Rakkesh.

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Rebecca, P.N.B., Durgalakshmi, D., Balakumar, S. et al. Biomimetic scaffold development for bone tissue engineering: Crosslinking graphene with collagen to enhance mechanical strength, conductivity, and porous structure. Journal of Materials Research 38, 4314–4323 (2023). https://doi.org/10.1557/s43578-023-01145-z

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