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Cited by 365Hydrogels: synthesis, properties, applicationsBone Tissue Engineering Materials3D Printing in Biomedical Research

Osteochondral Regeneration with 3D‐Printed Biodegradable High‐Strength Supramolecular Polymer Reinforced‐Gelatin Hydrogel Scaffolds

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Gao, Fei, Xu, Ziyang, Liang, Qingfei, Li, Haofei, Peng, Liuqi, Wu, Mingming, Zhao, Xiaoli, Cui, Xu +2 more·2019·Advanced Science
DOI 10.1002/advs.201900867PMC PMC6685475
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Abstract

Abstract Biomacromolecules with poor mechanical properties cannot satisfy the stringent requirement for load‐bearing as bioscaffolds. Herein, a biodegradable high‐strength supramolecular polymer strengthened hydrogel composed of cleavable poly( N ‐acryloyl 2‐glycine) (PACG) and methacrylated gelatin (GelMA) (PACG‐GelMA) is successfully constructed by photo‐initiated polymerization. Introducing hydrogen bond‐strengthened PACG contributes to a significant increase in the mechanical strengths of gelatin hydrogel with a high tensile strength (up to 1.1 MPa), outstanding compressive strength (up to 12.4 MPa), large Young's modulus (up to 320 kPa), and high compression modulus (up to 837 kPa). In turn, the GelMA chemical crosslinking could stabilize the temporary PACG network, showing tunable biodegradability by adjusting ACG/GelMA ratios. Further, a biohybrid gradient scaffold consisting of top layer of PACG‐GelMA hydrogel‐Mn 2+ and bottom layer of PACG‐GelMA hydrogel‐bioactive glass is fabricated for repair of osteochondral defects by a 3D printing technique. In vitro biological experiments demonstrate that the biohybrid gradient hydrogel scaffold not only supports cell attachment and spreading but also enhances gene expression of chondrogenic‐related and osteogenic‐related differentiation of human bone marrow stem cells. Around 12 weeks after in vivo implantation, the biohybrid gradient hydrogel scaffold significantly facilitates concurrent regeneration of cartilage and subchondral bone in a rat model.

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  1. [1]H. J. Huang, X. Zhang, X. Q. Hu, Z. X. Shao, J. X. Zhu, L. H. Dai, Z. T. Man, L. Yuan, H. F. Chen, C. Y. Zhou, Y. F. Ao, Biomaterials 2014, 35, 9608. 25176065
  2. [2]L. Li, J. Y. Li, J. M. Guo, H. K. Zhang, X. Zhang, C. Y. Yin, L. M. Wang, Y. S. Zhu, Q. Q. Yao, Adv. Funct. Mater. 2019, 29, 1807356.
  3. [3]W. L. Shi, M. Y. Sun, X. Q. Hu, B. Ren, J. Cheng, C. X. Li, X. N. Duan, X. Fu, J. Y. Zhang, H. F. Chen, Y. F. Ao, Adv. Mater. 2017, 29, 1701089.
  4. [4]W. Wang, L. Sun, P. F. Zhang, J. F. Song, W. G. Liu, Acta Biomater. 2014, 10, 4983. 25169257
  5. [5]D. J. Huey, J. C. Hu, K. A. Athanasiou, Science 2012, 338, 917. 23161992 PMC4327988
  6. [6]R. Dorotka, U. Windberger, K. Macfelda, U. Bindreiter, C. Toma, S. Nehrer, Biomaterials 2005, 26, 3617. 15621252
  7. [7]J. Z. Yang, Y. S. Zhang, K. Yue, A. Khademhosseini, Acta Biomater. 2017, 57, 1. 28088667 PMC5545789
  8. [8]Y. Y. Du, H. M. Liu, Q. Yang, S. Wang, J. L. Wang, J. Ma, I. Noh, A. G. Mikos, S. M. Zhang, Biomaterials 2017, 137, 37. 28528301 PMC5544967
  9. [9]D. Seliktar, Science 2012, 336, 1124. 22654050
  10. [10]R. Jin, L. S. M. Teixeira, P. J. Dijkstra, C. A. V. Blitterswijk, M. Karperien, J. Feijen, Biomaterials 2010, 31, 3103. 20116847
  11. [11]T. Nonoyama, S. Wada, R. Kiyama, N. Kitamura, M. I. Mredha, X. Zhang, T. Kurokawa, T. Nakajima, Y. Takagi, K. Yasuda, J. P. Gong, Adv. Mater. 2016, 28, 6740. 27184968
  12. [12]I. C. Liao, F. T. Moutos, B. T. Estes, X. H. Zhao, F. Guilak, Adv. Funct. Mater. 2013, 23, 5833. 24578679 PMC3933181
  13. [13]C. Qi, J. Liu, Y. Jin, L. M. Xu, G. B. Wang, Z. Wang, L. Wang, Biomaterials 2018, 163, 89. 29455069
  14. [14]F. You, X. B. Chen, D. M. L. Cooper, T. J. Chang, B. F. Eames, Biofabrication 2019, 11, 015015. 30524110
  15. [15]X. F. Ji, H. Zhu, L. M. Zhao, J. Xiao, Regener. Med. 2018, 13, 73.
  16. [16]K. Markstedt, A. Mantas, I. Tournier, H. M. Ávila, D. Hägg, P. Gatenholm, Biomacromolecules 2015, 16, 1489. 25806996
  17. [17]S. Das, F. Pati, Y. J. Choi, G. Rijal, J. H. Shim, S. W. Kim, A. R. Ray, D. W. Cho, S. Ghosh, Acta Biomater. 2015, 11, 233. 25242654
  18. [18]N. A. Peppas, Y. Huang, M. T. Lugo, J. H. Ward, J. Zhang, Annu. Rev. Biomed. Eng. 2000, 2, 9. 11701505
  19. [19]E. Hoch, C. Schuh, T. Hirth, G. E. M. Tovar, K. Borchers, J. Mater. Sci.: Mater. Med. 2012, 23, 2607. 22890515
  20. [20]Z. F. Wang, G. An, Y. Zhu, X. M. Liu, Y. H. Chen, H. K. Wu, Y. J. Wang, X. T. Shi, C. B. Mao, Mater. Horiz. 2019, 6, 733. PMC6768557 31572613
  21. [21]Q. Feng, K. C. Wei, S. Lin, Z. Xu, Y. X. Sun, P. Shi, G. Li, L. M. Bian, Biomaterials 2016, 101, 217. 27294539
  22. [22]Q. Feng, K. C. Wei, K. Y. Zhang, B. G. Yang, F. Tian, G. X. Wang, L. M. Bian, NPG Asia Mater. 2018, 10, 455.
  23. [23]D. H. Lee, E. J. Choi, S. E. Lee, K. L. Kang, H. J. Moon, H. J. Kim, Y. H. Youn, D. N. Heo, S. J. Lee, H. Nah, Y. S. H. Wang, Y. H. Lee, J. Seong, S. H. Do, I. K. Kwon, Chem. Eng. J. 2019, 365, 30.
  24. [24]F. Gao, Z. Y. Xu, Q. F. Liang, B. Liu, H. F. Li, Y. H. Wu, Y. Y. Zhang, Z. F. Lin, M. M. Wu, C. S. Ruan, W. G. Liu, Adv. Funct. Mater. 2018, 28, 1706644.
  25. [25]X. Y. Zhai, Y. F. Ma, C. Y. Hou, F. Gao, Y. Y. Zhang, C. S. Ruan, H. B. Pan, W. W. J. Lu, W. G. Liu, ACS Biomater. Sci. Eng. 2017, 3, 1109. 33429585
  26. [26]F. Gao, Y. Y. Zhang, Y. M. Li, B. Xu, Z. Q. Cao, W. G. Liu, ACS Appl. Mater. Interfaces 2016, 8, 8956. 27014865
  27. [27]Z. Y. Xu, W. G. Liu, Chem. Commun. 2018, 54, 10540. 30152822
  28. [28]W. Wang, Y. Y. Zhang, W. G. Liu, Prog. Polym. Sci. 2017, 71, 1.
  29. [29]A. I. V. D. Bulcke, B. Bogdanov, N. D. Rooze, E. H. Schacht, M. Cornelissen, H. Berghmans, Biomacromolecules 2000, 1, 31. 11709840
  30. [30]X. Q. Yan, Q. Chen, L. Zhu, H. Chen, D. D. Wei, F. Chen, Z. Q. Tang, J. Yang, J. Zheng, J. Mater. Chem. B 2017, 5, 7683. 32264369
  31. [31]C. Y. Cui, T. L. Wu, F. Gao, C. C. Fan, Z. Y. Xu, H. B. Wang, B. Liu, W. G. Liu, Adv. Funct. Mater. 2018, 28, 1804925.
  32. [32]J. Liu, H. Y. Zheng, P. S. P. Poh, H. G. Machens, A. F. Schilling, Int. J. Mol. Sci. 2015, 16, 15997. 26184185 PMC4519935
  33. [33]F. T. Moutos, L. E. Freed, F. Guilak, Nat. Commun. 2007, 6, 162. 17237789
  34. [34]L. Han, J. L. Xu, X. Lu, D. L. Gan, Z. X. Wang, K. F. Wang, H. P. Zhang, H. P. Yuan, J. Weng, J. Mater. Chem. B 2017, 5, 731. 32263841
  35. [35]C. J. Deng, Q. Q. Yao, C. Feng, J. Y. Li, L. M. Wang, G. F. Cheng, M. C. Shi, L. Chen, J. Chang, C. T. Wu, Adv. Funct. Mater. 2017, 27, 1703117.
  36. [36]J. R. Jones, Acta Biomater. 2013, 9, 4457. 22922331
  37. [37]L. Chen, C. J. Deng, J. Y. Li, Q. Q. Yao, J. Chang, L. M. Wang, C. T. Wu, Biomaterials 2019, 196, 138. 29643002
  38. [38]F. B. Li, G. Z. Zhang, Y. H. Xia, Z. S. Wang, H. Y. Jiang, X. Q. Feng, Y. Q. Zhang, M. J. Liu, H. J. Li, Compos. Sci. Technol. 2018, 165, 339.
  39. [39]J. Y. Sun, X. H. Zhao, W. R. K. Illeperuma, O. Chaudhuri, K. H. Oh, D. J. Mooney, J. J. Vlassak, Z. G. Suo, Nature 2012, 489, 133. 22955625 PMC3642868
  40. [40]J. Yang, X. M. Zhang, M. G. Ma, F. Xu, ACS Macro Lett. 2015, 4, 829. 35596504
  41. [41]G. H. Deng, F. Y. Li, H. X. Yu, F. Y. Liu, C. Y. Liu, W. X. Sun, H. F. Jiang, Y. M. Chen, ACS Macro Lett. 2012, 1, 275. 35578522
  42. [42]Z. Wei, J. H. Yang, Z. Q. Liu, F. Xu, J. X. Zhou, M. Zrínyi, Y. Osada, Y. M. Chen, Adv. Funct. Mater. 2015, 25, 1352.
  43. [43]Z. J. Wei, J. He, T. Liang, H. Oh, J. Athas, Z. Tong, C. Y. Wang, Z. H. Nie, Polym. Chem. 2013, 4, 4601.
  44. [44]J. Malda, J. Visser, F. P. Melchels, T. Jüngst, W. E. Hennink, W. J. A. Dhert, J. Groll, D. W. Hutmacher, Adv. Mater. 2013, 25, 5011. 24038336
  45. [45]W. J. Liu, M. A. Heinrich, Y. X. Zhou, A. Akpek, N. Hu, X. Liu, X. F. Guan, Z. Zhong, X. Y. Jin, A. Khademhosseini, Y. S. Zhang, Adv. Healthcare Mater. 2017, 6, 1601451. PMC5545786 28464555

Authors
Gao, F., Xu, Z., Liang, Q., Li, H., Peng, L., Wu, M., Zhao, X., Cui, X., Ruan, C., & Liu, W.
Affiliations
  • Tianjin University (CN)
  • Chinese Academy of Sciences (CN)
Corresponding author
  • Ruan, Changshun
  • Liu, Wenguang
ORCID
Venue
Advanced Science
Publisher
Wiley
Published
2019-06-11
Volume
6
Issue
15
Pages
1900867-1900867
ISSN
2198-3844 (ISSN-L)
DOI
10.1002/advs.201900867
PMC
PMC6685475
OpenAlex
W2952891779
Cited by
365
References
47
Citations by year
2026: 37 · 2025: 46 · 2024: 53 · 2023: 73 · 2022: 72 · 2021: 51 · 2020: 29 · 2019: 3 · 2015: 1
FWCI
13.40
Type
journal article
Language
en
Open access
Licence
Locations
  • Advanced Science (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • National Natural Science Foundation of China (51733006, 31771041)
  • National Basic Research Program of China (2016YFC1101301, 2018YFB1105600)
  • Youth Innovation Promotion Association of the Chinese Academy of Sciences (2019350)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Medicine › Hydrogels: synthesis, properties, applications
  • Physical Sciences › Engineering › Biomedical Engineering › Bone Tissue Engineering Materials
  • Physical Sciences › Engineering › Biomedical Engineering › 3D Printing in Biomedical Research
Keywords
osteochondral regeneration, supramolecular polymers, gelatin methacryloyl, hydrogen bonding, hydrogel mechanical properties, biodegradable hydrogels, 3D-printed scaffolds, bioactive glass, manganese ions, chondrogenic differentiation, osteogenic differentiation, bone marrow-derived stem cells, cartilage repair, subchondral bone regeneration

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