Review
The Application of Biomaterial-Based Spinal Cord Tissue Engineering
Liang Ma,
Zhen Zhang,
Yulei Mu,
Bangheng Liu,
Huiqun Zhou,
Dong-An Wang,
Liang Ma
Department of Biomedical Engineering, City University of Hong Kong, 83 Tat Chee Avenue, Kowloon, Hong Kong, 999077 China
Search for more papers by this authorZhen Zhang
Department of Biomedical Engineering, City University of Hong Kong, 83 Tat Chee Avenue, Kowloon, Hong Kong, 999077 China
Search for more papers by this authorYulei Mu
Department of Biomedical Engineering, City University of Hong Kong, 83 Tat Chee Avenue, Kowloon, Hong Kong, 999077 China
Search for more papers by this authorBangheng Liu
Department of Biomedical Engineering, City University of Hong Kong, 83 Tat Chee Avenue, Kowloon, Hong Kong, 999077 China
Search for more papers by this authorHuiqun Zhou
Department of Biomedical Engineering, City University of Hong Kong, 83 Tat Chee Avenue, Kowloon, Hong Kong, 999077 China
Search for more papers by this authorCorresponding Author
Dong-An Wang
Department of Biomedical Engineering, City University of Hong Kong, 83 Tat Chee Avenue, Kowloon, Hong Kong, 999077 China
Centre for Neuromusculoskeletal Restorative Medicine, InnoHK HKSTP, Sha Tin, Hong Kong, 999077 China
Tung Biomedical Sciences Centre, City University of Hong Kong, 83 Tat Chee Avenue, Kowloon, Hong Kong, 999077 China
E-mail: [email protected]
Search for more papers by this authorLiang Ma,
Zhen Zhang,
Yulei Mu,
Bangheng Liu,
Huiqun Zhou,
Dong-An Wang,
Liang Ma
Department of Biomedical Engineering, City University of Hong Kong, 83 Tat Chee Avenue, Kowloon, Hong Kong, 999077 China
Search for more papers by this authorZhen Zhang
Department of Biomedical Engineering, City University of Hong Kong, 83 Tat Chee Avenue, Kowloon, Hong Kong, 999077 China
Search for more papers by this authorYulei Mu
Department of Biomedical Engineering, City University of Hong Kong, 83 Tat Chee Avenue, Kowloon, Hong Kong, 999077 China
Search for more papers by this authorBangheng Liu
Department of Biomedical Engineering, City University of Hong Kong, 83 Tat Chee Avenue, Kowloon, Hong Kong, 999077 China
Search for more papers by this authorHuiqun Zhou
Department of Biomedical Engineering, City University of Hong Kong, 83 Tat Chee Avenue, Kowloon, Hong Kong, 999077 China
Search for more papers by this authorCorresponding Author
Dong-An Wang
Department of Biomedical Engineering, City University of Hong Kong, 83 Tat Chee Avenue, Kowloon, Hong Kong, 999077 China
Centre for Neuromusculoskeletal Restorative Medicine, InnoHK HKSTP, Sha Tin, Hong Kong, 999077 China
Tung Biomedical Sciences Centre, City University of Hong Kong, 83 Tat Chee Avenue, Kowloon, Hong Kong, 999077 China
E-mail: [email protected]
Search for more papers by this authorFirst published: 29 October 2024
Abstract
Advancements in biomaterial-based spinal cord tissue engineering technology have profoundly influenced regenerative medicine, providing innovative solutions for both spinal cord organoid development and engineered spinal cord injury (SCI) repair. In spinal cord organoids, biomaterials offer a supportive microenvironment that mimics the natural extracellular matrix, facilitating cell differentiation and organization and advancing the understanding of spinal cord development and pathophysiology. Furthermore, biomaterials are essential in constructing engineered spinal cords for SCI repair. The incorporation of biomaterials with growth factors, fabrication of ordered scaffold structures, and artificial spinal cord assemblies are critical insights for SCI to ensure structural integrity, enhance cell viability, and promote neural regeneration in transplantation. In summary, this review summarizes the contribution of biomaterials to the spinal cord organoids progression and discusses strategies for biomaterial-based spinal cord engineering in SCI therapy. These achievements underscore the transformative potential of biomaterials to improve treatment options for SCI and accelerate future clinical applications.
Conflict of Interest
The authors declare no conflict of interest.
References
- 1Y. Tanabe, T. M. Jessell, Science 1996, 274, 1115.
- 2J. W. McDonald, C. Sadowsky, Lancet 2002, 359, 417.
- 3M. G. Fehlings, L. A. Tetreault, J. R. Wilson, B. K. Kwon, A. S. Burns, A. R. Martin, G. Hawryluk, J. S. Harrop, “A clinical practice guideline for the management of acute spinal cord injury: introduction, rationale, and scope”, SAGE Publications Sage CA, Los Angeles, CA 2017, p. 7/84S.
- 4G. Courtine, M. V. Sofroniew, Nat. Med. 2019, 25, 898.
- 5J. Fawcett, A. Curt, J. Steeves, W. Coleman, M. Tuszynski, D. Lammertse, P. Bartlett, A. Blight, V. Dietz, J. Ditunno, Spinal cord 2007, 45, 190.
- 6M. Tsintou, K. Dalamagkas, A. M. Seifalian, Neural Regen. Res. 2015, 10, 726.
- 7M. A. Anderson, J. E. Burda, Y. Ren, Y. Ao, T. M. O'Shea, R. Kawaguchi, G. Coppola, B. S. Khakh, T. J. Deming, M. V. Sofroniew, Nature 2016, 532, 195.
- 8M. A. Anwar, T. S. Al Shehabi, A. H. Eid, Front. Cell. Neurosci. 2016, 10, 98.
- 9Tissue Eng., Part B 2019, 25, 471.
- 10Stem Cells Dev. 2009, 18, 683.
- 11S. Nishimura, A. Yasuda, H. Iwai, M. Takano, Y. Kobayashi, S. Nori, O. Tsuji, K. Fujiyoshi, H. Ebise, Y. Toyama, H. Okano, M. Nakamura, Mol. Brain 2013, 6, 3.
- 12P. Arlotta, Nat. Methods 2018, 15, 27.
- 13H. Clevers, Cell 2016, 165, 1586.
- 14Z. Zhao, X. Chen, A. M. Dowbaj, A. Sljukic, K. Bratlie, L. Lin, E. L. S. Fong, G. M. Balachander, Z. Chen, A. Soragni, Nat. Rev. Methods Primers 2022, 2, 94.
- 15S. Bian, M. Repic, Z. Guo, A. Kavirayani, T. Burkard, J. A. Bagley, C. Krauditsch, J. A. Knoblich, Nat. Methods 2018, 15, 631.
- 16A.-N. Cho, Y. Jin, S. Kim, S. Kumar, H. Shin, H.-C. Kang, S.-W. Cho, ACS Appl. Mater. Interfaces 2019, 11, 15344.
- 17F. Z. Volpato, T. Führmann, C. Migliaresi, D. W. Hutmacher, P. D. Dalton, Biomaterials 2013, 34, 4945.
- 18H.-J. Jeong, Y. Yun, S.-J. Lee, Y. Ha, S.-J. Gwak, Neurochem. Int. 2021, 144, 104973.
- 19B. Kaplan, S. Levenberg, Int. J. Mol. Sci. 2022, 23, 1244.
- 20S. Liu, Y.-Y. Xie, B. Wang, Neural Regener. Res. 2019, 14, 1352.
- 21R. D. Bartlett, D. Eleftheriadou, R. Evans, D. Choi, J. B. Phillips, Biomaterials 2020, 258, 120303.
- 22R. D. Bartlett, D. Choi, J. B. Phillips, Regener. Med. 2016, 11, 659.
- 23A. J. Engler, S. Sen, H. L. Sweeney, D. E. Discher, Cell 2006, 126, 677.
- 24K. C. Clause, L. J. Liu, K. Tobita, Cell Commun. Adhes. 2010, 17, 48.
- 25X. Lin, Y. Shi, Y. Cao, W. Liu, Biomed. Mater. 2016, 11, 014109.
- 26H. Uwamori, T. Higuchi, K. Arai, R. Sudo, Sci. Rep. 2017, 7, 17349.
- 27T. Führmann, P. N. Anandakumaran, M. S. Shoichet, Adv. Healthcare Mater. 2017, 6, 1601130.
- 28E. Moeendarbary, I. P. Weber, G. K. Sheridan, D. E. Koser, S. Soleman, B. Haenzi, E. J. Bradbury, J. Fawcett, K. Franze, Nat. Commun. 2017, 8, 14787.
- 29Q. Han, W. Jin, Z. Xiao, H. Ni, J. Wang, J. Kong, J. Wu, W. Liang, L. Chen, Y. Zhao, Biomaterials 2010, 31, 9212.
- 30D. Joung, N. S. Lavoie, S. Z. Guo, S. H. Park, A. M. Parr, M. C. McAlpine, Adv. Funct. Mater. 2020, 30, 1906237.
- 31Q. Han, Y. Xie, J. D. Ordaz, A. J. Huh, N. Huang, W. Wu, N. Liu, K. A. Chamberlain, Z.-H. Sheng, X.-M. Xu, Cell Metab. 2020, 31, 623.
- 32M. A. Lancaster, M. Renner, C.-A. Martin, D. Wenzel, L. S. Bicknell, M. E. Hurles, T. Homfray, J. M. Penninger, A. P. Jackson, J. A. Knoblich, Nature 2013, 501, 373.
- 33S. L. Giandomenico, M. Sutcliffe, M. A. Lancaster, Nat. Protoc. 2021, 16, 579.
- 34W. A. Alaynick, T. M. Jessell, S. L. Pfaff, Cell 2011, 146, 178.
- 35P. Tripathi, F. Sieber, Essentials of Neurosurgical Anesthesia & Critical Care: Strategies for Prevention, Early Detection, and Successful Management of Perioperative Complications, 2020, p. 3, https://doi.org/10.1007/978-3-030-17410-1_1.
- 36D. B. Choi, G. Nam, D. M. Groh, S. Syed, J. S. Fridley, Z. L. Gokaslan, Spinal Cord Tumors, 2019, p. 43, https://doi.org/10.1007/978-3-319-99438-3_3.
10.1007/978-3-319-99438-3_3 Google Scholar
- 37A. Nógrádi, G. Vrbová, in Transplantation of Neural Tissue into the Spinal Cord, Springer US, Boston, MA 2006, p. 1.
10.1007/0-387-32633-2 Google Scholar
- 38S. Wiese, A. Faissner, Exp. Neurol. 2015, 274, 90.
- 39T. Ogura, H. Sakaguchi, S. Miyamoto, J. Takahashi, Development 2018, 145, dev162214.
- 40J.-H. Hor, S.-Y. Ng, in Methods in Cell Biology 2020 (Ed.: J. R. Spence), Academic Press, Cambridge, MA 2020, p. 257.
- 41T. M. Jessell, Nat. Rev. Genet. 2000, 1, 20.
- 42M. E. Dickinson, M. A. J. Selleck, A. P. McMahon, M. Bronner-Fraser, Development 1995, 121, 2099.
- 43M. n. I. Garcı́a-Castro, C. Marcelle, M. Bronner-Fraser, Science 2002, 297, 848.
- 44M. Goulding, Nat. Rev. Neurosci. 2009, 10, 507.
- 45J. S. Dasen, T. M. Jessell, in Current Topics in Developmental Biology, Academic Press, Cambridge MA 2009, p. 169.
- 46T. Caspary, K. V. Anderson, Nat. Rev. Neurosci. 2003, 4, 289.
- 47W. Xue, B. Li, H. Liu, Y. Xiao, B. Li, L. Ren, H. Li, Z. Shao, iScience 2023, 26, 105898.
- 48J. Andersen, O. Revah, Y. Miura, N. Thom, N. D. Amin, K. W. Kelley, M. Singh, X. Chen, M. V. Thete, E. M. Walczak, H. Vogel, H. C. Fan, S. P. Paşca, Cell 2020, 183, 1913.
- 49N. Duval, C. Vaslin, T. C. Barata, Y. Frarma, V. Contremoulins, X. Baudin, S. p. Nedelec, V. C. Ribes, Development 2019, 146, dev175430.
- 50S. Sances, L. I. Bruijn, S. Chandran, K. Eggan, R. Ho, J. R. Klim, M. R. Livesey, E. Lowry, J. D. Macklis, D. Rushton, Nat. Neurosci. 2016, 19, 542.
- 51S. A. Sloan, J. Andersen, A. M. Pașca, F. Birey, S. P. Pașca, Nat. Protoc. 2018, 13, 2062.
- 52Y. Miura, M.-Y. Li, F. Birey, K. Ikeda, O. Revah, M. V. Thete, J.-Y. Park, A. Puno, S. H. Lee, M. H. Porteus, Nat. Biotechnol. 2020, 38, 1421.
- 53J.-M. F. Martins, C. Fischer, A. Urzi, R. Vidal, S. Kunz, P.-L. Ruffault, L. Kabuss, I. Hube, E. Gazzerro, C. Birchmeier, Cell Stem Cell 2020, 26, 172.
- 54G. Mattei, C. Magliaro, S. Giusti, S. D. Ramachandran, S. Heinz, J. Braspenning, A. Ahluwalia, PLoS One 2017, 12, e0173206.
- 55P. A. Mollica, E. N. Booth-Creech, J. A. Reid, M. Zamponi, S. M. Sullivan, X.-L. Palmer, P. C. Sachs, R. D. Bruno, Acta Biomater. 2019, 95, 201.
- 56M. Hao, W. Wang, A. Kumar, W. H. A. Kamaruddin, S. Saidin, N. A. N. N. Malek, J. Claverie, H. Liu, BMEMat 2024, 2, e12059.
- 57C. Rathnam, L. Yang, S. Castro-Pedrido, J. Luo, L. Cai, K.-B. Lee, Sci. Adv. 2021, 7, eabj2281.
- 58J. Xu, S. Fang, S. Deng, H. Li, X. Lin, Y. Huang, S. Chung, Y. Shu, Z. Shao, Nat. Biomed. Eng. 2023, 7, 253.
- 59Y. Han, M. King, E. Tikhomirov, P. Barasa, C. D. S. Souza, J. Lindh, D. Baltriukiene, L. Ferraiuolo, M. Azzouz, M. R. Gullo, E. N. Kozlova, Int. J. Mol. Sci. 2022, 23, 5788.
- 60Z. Wang, H. Zhao, X. Tang, T. Meng, D. Khutsishvili, B. Xu, S. Ma, Research.4 2022, 2022, 9832128.
- 61J.-H. Lee, H. Shin, M. R. Shaker, H. J. Kim, S.-H. Park, J. H. Kim, N. Lee, M. Kang, S. Cho, T. H. Kwak, J. W. Kim, M.-R. Song, S.-H. Kwon, D. W. Han, S. Lee, S.-Y. Choi, I. J. Rhyu, H. Kim, D. Geum, I.-J. Cho, W. Sun, Nat. Biomed. Eng. 2022, 6, 435.
- 62S. Gribaudo, R. Robert, B. van Sambeek, C. Mirdass, A. Lyubimova, K. Bouhali, J. Ferent, X. Morin, A. van Oudenaarden, S. Nedelec, Nat. Biotechnol. 2023, 42, 1243.
- 63J. Huang, Y. Jiang, Y. Ren, Y. Liu, X. Wu, Z. Li, J. Ren, J. Biomed. Mater. Res., Part A 2020, 108, 1501.
- 64S. Vukicevic, H. K. Kleinman, F. P. Luyten, A. B. Roberts, N. S. Roche, A. H. Reddi, Exp. Cell Res. 1992, 202, 1.
- 65H. K. Kleinman, G. R. Martin, in Seminars in cancer biology, Elsevier, Amsterdam, Netherlands 2005, p. 15/378.
- 66Z. J. Khong, J. H. Hor, S. Y. Ng, Neural Regener. Res. 2019, 14, 1515.
- 67T. J. Rowland, L. M. Miller, A. J. Blaschke, E. L. Doss, A. J. Bonham, S. T. Hikita, L. V. Johnson, D. O. Clegg, Stem Cells Dev. 2010, 19, 1231.
- 68I. P. S. Fernando, W. Lee, E. J. Han, G. Ahn, Chem. Eng. J. 2020, 391, 123823.
- 69W. H. Chooi, C. Y. Ng, V. Ow, J. Harley, W. Ng, J.-H. Hor, K. E. Low, B. Malleret, K. Xue, S.-Y. Ng, Adv. Healthcare Mater. 2023, 12, 2202342.
- 70D. A. C. Walma, K. M. Yamada, Development 2020, 147, dev175596.
- 71S. A. Yi, Y. Zhang, C. Rathnam, T. Pongkulapa, K.-B. Lee, Adv. Mater. 2021, 33, 2007949.
- 72W. Zhang, A. Du, S. Liu, M. Lv, S. Chen, Regener. Ther. 2021, 18, 88.
- 73S. Kim, S. Min, Y. S. Choi, S.-H. Jo, J. H. Jung, K. Han, J. Kim, S. An, Y. W. Ji, Y.-G. Kim, Nat. Commun. 2022, 13, 1692.
- 74B. Yaldiz, P. Saglam-Metiner, O. Yesil-Celiktas, Expert Rev. Mol. Med. 2021, 23, e25.
- 75G. G. Giobbe, C. Crowley, C. Luni, S. Campinoti, M. Khedr, K. Kretzschmar, M. M. De Santis, E. Zambaiti, F. Michielin, L. Meran, Q. Hu, G. van Son, L. Urbani, A. Manfredi, M. Giomo, S. Eaton, D. Cacchiarelli, V. S. W. Li, H. Clevers, P. Bonfanti, N. Elvassore, P. De Coppi, Nat. Commun. 2019, 10, 5658.
- 76Z. Wang, R. Liu, Y. Liu, Y. Zhao, Y. Wang, B. Lu, H. Li, C. Ju, W. Wu, X. Gao, H. Xu, S. Cheng, Y. Cao, S. Jia, C. Hu, L. Zhu, D. Hao, ACS Biomater. Sci. Eng. 2024, 10, 3218.
- 77W. Wu, Y. Liu, R. Liu, Y. Wang, Y. Zhao, H. Li, B. Lu, C. Ju, X. Gao, H. Xu, Y. Cao, S. Cheng, Z. Wang, S. Jia, C. Hu, L. Zhu, D. Hao, ACS Biomater. Sci. Eng. 2024, 10, 3203.
- 78K. Zhang, Z. Rao, H. Zuo, H. Chu, J. Chen, R. Cui, S. Zhu, X. Guo, Y. Hu, D. Quan, Y. Bai, Adv. Funct. Mater. 2024, 34, 2407097.
- 79Z. Sun, Z. Chen, M. Yin, X. Wu, B. Guo, X. Cheng, R. Quan, Y. Sun, Q. Zhang, Y. Fan, C. Jin, Y. Yin, X. Hou, W. Liu, M. Shu, X. Xue, Y. Shi, B. Chen, Z. Xiao, J. Dai, Y. Zhao, Cell Stem Cell 2024, 31, 772.
- 80R. J. Dumont, D. O. Okonkwo, S. Verma, R. J. Hurlbert, P. T. Boulos, D. B. Ellegala, A. S. Dumont, Clin. Neuropharmacol. 2001, 24, 254.
- 81K. V. Ambrozaitis, E. Kontautas, B. Spakauskas, D. Vaitkaitis, Medicina 2006, 42, 255.
- 82A. Anjum, M. D. i. Yazid, M. Fauzi Daud, J. Idris, A. M. H. Ng, A. Selvi Naicker, O. H. R. Ismail, R. K. Athi Kumar, Y. Lokanathan, Int. J. Mol. Sci. 2020, 21, 7533.
- 83C. S. Ahuja, M. Fehlings, Stem Cells Transl. Med. 2016, 5, 914.
- 84C. S. Ahuja, A. Mothe, M. Khazaei, J. H. Badhiwala, E. A. Gilbert, D. Kooy, C. M. Morshead, C. Tator, M. G. Fehlings, Stem Cells Transl. Med. 2020, 9, 1509.
- 85H. L. Weiner, J. Neurol. 2008, 255, 3.
- 86S. Li, G. A. Mealing, P. Morley, P. K. Stys, J. Neurosci. 1999, 19, RC16.
- 87S. Li, P. K. Stys, J. Neurosci. 2000, 20, 1190.
- 88M. Dizdaroglu, P. Jaruga, M. Birincioglu, H. Rodriguez, Free Radical Biol. Med. 2002, 32, 1102.
- 89M. Liu, W. Wu, H. Li, S. Li, L.-t. Huang, Y.-q. Yang, Q. Sun, C.-x. Wang, Z. Yu, C.-h. Hang, J. Spinal Cord Med. 2015, 38, 745.
- 90S. David, A. Kroner, Nat. Rev. Neurosci. 2011, 12, 388.
- 91S. Dolma, H. Kumar, Mol. Neurobiol. 2021, 58, 4652.
- 92J. Mao, L. Chen, Z. Cai, S. Qian, Z. Liu, B. Zhao, Y. Zhang, X. Sun, W. Cui, Adv. Funct. Mater. 2022, 32, 2111003.
- 93C. Iannotti, Y. P. Zhang, L. B. Shields, Y. Han, D. A. Burke, X.-M. Xu, C. B. Shields, J. Neurotrauma 2006, 23, 853.
- 94E. J. Bradbury, E. R. Burnside, Nat. Commun. 2019, 10, 3879.
- 95A. T. Mneimneh, M. M. Mehanna, Int. J. Pharm. 2021, 601, 120559.
- 96X. Zhao, R. Gu, Y. Zhao, F. Wei, X. Gao, Y. Zhuang, Z. Xiao, H. Shen, J. Dai, Cell Proliferation 2023, 56, e13451.
- 97Y. Yang, Y. Fan, H. Zhang, Q. Zhang, Y. Zhao, Z. Xiao, W. Liu, B. Chen, L. Gao, Z. Sun, Biomaterials 2021, 269, 120479.
- 98Y. Sun, C. Yang, X. Zhu, J. J. Wang, X. Y. Liu, X. P. Yang, X. W. An, J. Liang, H. J. Dong, W. Jiang, J. Biomed. Mater. Res., Part A 2019, 107, 1898.
- 99M. H. Spilker, I. Yannas, H.-P. Hsu, T. Norregaard, S. Kostyk, M. Spector, Tissue Eng. 1997, 3, 309.
- 100N. J. Schaub, C. D. Johnson, B. Cooper, R. J. Gilbert, J. Neurotrauma 2016, 33, 1405.
- 101M. W. MOSESSON, J. Thromb. Haemostasis 2005, 3, 1894.
- 102A. R. Bento, P. Quelhas, M. J. Oliveira, A. P. Pêgo, I. F. Amaral, J. Tissue Eng. Regener. Med. 2017, 11, 3494.
- 103Z.-a. Yao, F.-j. Chen, H.-l. Cui, T. Lin, N. Guo, ( H.-g. Wu), Neural regeneration research, 2018, 13, 502.
- 104X. Hu, X. Zhou, Y. Li, Q. Jin, W. Tang, Q. Chen, D. Aili, H. Qian, Int. J. Dev. Neurosci. 2019, 76, 80.
- 105M. I. Günther, N. Weidner, R. Müller, A. Blesch, Acta Biomater. 2015, 27, 140.
- 106S. A. Geissler, A. L. Sabin, R. R. Besser, O. M. Gooden, B. D. Shirk, Q. M. Nguyen, Z. Z. Khaing, C. E. Schmidt, J. Neural Eng. 2018, 15, 025004.
- 107S. V. Kushchayev, M. B. Giers, D. H. Eng, N. L. Martirosyan, J. M. Eschbacher, M. M. Mortazavi, N. Theodore, A. Panitch, M. C. Preul, J. Neurosurg. Spine 2016, 25, 114.
- 108T. Gros, J. S. Sakamoto, A. Blesch, L. A. Havton, M. H. Tuszynski, Biomaterials 2010, 31, 6719.
- 109L. Fan, C. Liu, X. Chen, Y. Zou, Z. Zhou, C. Lin, G. Tan, L. Zhou, C. Ning, Q. Wang, ACS Appl. Mater. Interfaces 2018, 10, 17742.
- 110C. M. Walsh, J. K. Wychowaniec, L. Costello, D. F. Brougham, D. Dooley, Adv. Healthcare Mater. 2023, 12, 2300951.
- 111H. Liu, X. Xu, Y. Tu, K. Chen, L. Song, J. Zhai, S. Chen, L. Rong, L. Zhou, W. Wu, ACS Appl. Mater. Interfaces 2020, 12, 17207.
- 112X.-b. Kong, Q.-y. Tang, X.-y. Chen, Y. Tu, S.-z. Sun, Z.-l. Sun, Neural Regener. Res. 2017, 12, 1003.
- 113H. Ren, M. Han, J. Zhou, Z.-F. Zheng, P. Lu, J.-J. Wang, J.-Q. Wang, Q.-J. Mao, J.-Q. Gao, H. W. Ouyang, Biomaterials 2014, 35, 6585.
- 114E. A. Kiyotake, M. D. Martin, M. S. Detamore, Acta Biomater. 2022, 139, 43.
- 115J. Rosner, P. Avalos, F. Acosta, J. Liu, D. Drazin, Stem cells international 2012, 2012, 826754.
- 116E. J. Huang, L. F. Reichardt, Annu. Rev. Neurosci. 2001, 24, 677.
- 117K. M. Keefe, I. S. Sheikh, G. M. Smith, Int. J. Mol. Sci. 2017, 18, 548.
- 118S. Morcuende, R. Muñoz-Hernández, B. Benítez-Temiño, A. M. Pastor, R. R. de la Cruz, Neuroscience 2013, 250, 31.
- 119L. Schnell, R. Schneider, R. Kolbeck, Y.-A. Barde, M. E. Schwab, Nature 1994, 367, 170.
- 120L. T. Alto, L. A. Havton, J. M. Conner, E. R. Hollis II, A. Blesch, M. H. Tuszynski, Nat. Neurosci. 2009, 12, 1106.
- 121X. Sun, C. Zhang, J. Xu, H. Zhai, S. Liu, Y. Xu, Y. Hu, H. Long, Y. Bai, D. Quan, ACS Biomater. Sci. Eng. 2020, 6, 1228.
- 122G. Li, B. Zhang, J.-h. Sun, L.-y. Shi, M.-y. Huang, L.-j. Huang, Z.-j. Lin, Q.-y. Lin, B.-q. Lai, Y.-h. Ma, Bioact. Mater. 2021, 6, 3766.
- 123G. Li, M.-T. Che, K. Zhang, L.-N. Qin, Y.-T. Zhang, R.-Q. Chen, L.-M. Rong, S. Liu, Y. Ding, H.-Y. Shen, S.-M. Long, J.-L. Wu, E.-A. Ling, Y.-S. Zeng, Biomaterials 2016, 83, 233.
- 124A. Jain, Y.-T. Kim, R. J. McKeon, R. V. Bellamkonda, Biomaterials 2006, 27, 497.
- 125S. Han, B. Wang, W. Jin, Z. Xiao, X. Li, W. Ding, M. Kapur, B. Chen, B. Yuan, T. Zhu, Biomaterials 2015, 41, 89.
- 126Z. Hassannejad, S. A. Zadegan, A. R. Vaccaro, V. Rahimi-Movaghar, O. Sabzevari, Injury 2019, 50, 278.
- 127H.-L. Xu, F.-R. Tian, C.-T. Lu, J. Xu, Z.-L. Fan, J.-J. Yang, P.-P. Chen, Y.-D. Huang, J. Xiao, Y.-Z. Zhao, Sci. Rep. 2016, 6, 38332.
- 128Q. Shi, W. Gao, X. Han, X. Zhu, J. Sun, F. Xie, X. Hou, H. Yang, J. Dai, L. Chen, Sci. China Life Sci. 2014, 57, 232.
- 129G. Balbinot, G. Li, S. Kalsi-Ryan, R. Abel, D. Maier, Y.-B. Kalke, N. Weidner, R. Rupp, M. Schubert, A. Curt, Nat. Commun. 2023, 14, 723.
- 130B. Shi, S. Lu, H. Yang, S. Mahmood, C. Sun, N. A. N. N. Malek, W. H. A. Kamaruddin, S. Saidin, C. Zhang, BMEMat 2024, 2, e12111.
- 131S. Stokols, M. H. Tuszynski, Biomaterials 2004, 25, 5839.
- 132B. Vigani, S. Rossi, G. Sandri, M. C. Bonferoni, F. Ferrari, Neural Regener. Res. 2017, 12, 1786.
- 133N. Shahrubudin, T. C. Lee, R. Ramlan, Procedia Manuf. 2019, 35, 1286.
10.1016/j.promfg.2019.06.089 Google Scholar
- 134S. Chen, J. V. John, A. McCarthy, J. Xie, J. Mater. Chem. B 2020, 8, 3733.
- 135S. Stokols, M. H. Tuszynski, Biomaterials 2006, 27, 443.
- 136S. Chen, J. V. John, A. McCarthy, M. A. Carlson, X. Li, J. Xie, Appl. Phys. Rev. 2020, 8, 3733.
- 137S. M. S. Shahriar, N. S. Polavoram, S. M. Andrabi, Y. Su, D. Lee, H. Q. Tran, S. J. Schindler, J. Xie, BMEMat 2024, 2, e12065.
- 138S. Wu, Y. Wang, P. N. Streubel, B. Duan, Acta Biomater. 2017, 62, 102.
- 139Z. Chen, Z. Sun, Y. Fan, M. Yin, C. Jin, B. Guo, Y. Yin, R. Quan, S. Zhao, S. Han, X. Cheng, W. Liu, B. Chen, Z. Xiao, J. Dai, Y. Zhao, ACS Nano 2023, 17, 25591.
- 140F.-Y. Hsieh, S.-h. Hsu, Organogenesis 2015, 11, 153.
- 141A. C. Fonseca, F. P. Melchels, M. J. Ferreira, S. R. Moxon, G. Potjewyd, T. R. Dargaville, S. J. Kimber, M. Domingos, Chem. Rev. 2020, 120, 11093.
- 142V. M. Gaspar, P. Lavrador, J. Borges, M. B. Oliveira, J. F. Mano, Adv. Mater. 2020, 32, 1903975.
- 143T. Bedir, S. Ulag, C. B. Ustundag, O. Gunduz, Mater. Sci. Eng., C 2020, 110, 110741.
- 144J. Yang, K. Yang, W. Man, J. Zheng, Z. Cao, C.-Y. Yang, K. Kim, S. Yang, Z. Hou, G. Wang, X. Wang, Bioact. Mater. 2023, 25, 160.
- 145J. Koffler, W. Zhu, X. Qu, O. Platoshyn, J. N. Dulin, J. Brock, L. Graham, P. Lu, J. Sakamoto, M. Marsala, S. Chen, M. H. Tuszynski, Nat. Med. 2019, 25, 263.
- 146B.-Q. Lai, J.-M. Wang, J.-J. Duan, Y.-F. Chen, H.-Y. Gu, E.-A. Ling, J.-L. Wu, Y.-S. Zeng, Biomaterials 2013, 34, 2888.
- 147B.-Q. Lai, M.-T. Che, B. Feng, Y.-R. Bai, G. Li, Y.-H. Ma, L.-J. Wang, M.-Y. Huang, Y.-Q. Wang, B. Jiang, Y. Ding, X. Zeng, Y.-S. Zeng, Adv. Sci. 2019, 6, 1901240.
- 148G.-H. Wu, H.-J. Shi, M.-T. Che, M.-Y. Huang, Q.-S. Wei, B. Feng, Y.-H. Ma, L.-J. Wang, B. Jiang, Y.-Q. Wang, I. Han, E.-A. Ling, X. Zeng, Y.-S. Zeng, Biomaterials 2018, 181, 15.
- 149M. Abematsu, K. Tsujimura, M. Yamano, M. Saito, K. Kohno, J. Kohyama, M. Namihira, S. Komiya, K. Nakashima, J. Clin. Invest. 2010, 120, 3255.
- 150J. F. Bonner, O. Steward, Brain Res. 2015, 1619, 115.
- 151C. Haas, I. Fischer, Neural Regen. Res. 2014, 9, 1173.
- 152B.-Q. Lai, M.-T. Che, B.-L. Du, X. Zeng, Y.-H. Ma, B. Feng, X.-C. Qiu, K. Zhang, S. Liu, H.-Y. Shen, Biomaterials 2016, 109, 40.
- 153B.-Q. Lai, B. Feng, M.-T. Che, L.-J. Wang, S. Cai, M.-Y. Huang, H.-Y. Gu, B. Jiang, E.-A. Ling, M. Li, X. Zeng, Y.-S. Zeng, Adv. Sci. 2018, 5, 1800261.
- 154I. Kelava, M. A. Lancaster, Dev. Biol. 2016, 420, 199.
- 155X. Qian, H. N. Nguyen, M. M. Song, C. Hadiono, S. C. Ogden, C. Hammack, B. Yao, G. R. Hamersky, F. Jacob, C. Zhong, Cell 2016, 165, 1238.
- 156K. Muguruma, A. Nishiyama, H. Kawakami, K. Hashimoto, Y. Sasai, Cell Rep. 2015, 10, 537.
- 157H. Sakaguchi, Y. Ozaki, T. Ashida, T. Matsubara, N. Oishi, S. Kihara, J. Takahashi, Stem Cell Rep. 2019, 13, 458.
- 158X. Liu, M. Hao, Z. Chen, T. Zhang, J. Huang, J. Dai, Z. Zhang, Biomaterials 2021, 272, 120771.
- 159C. Mandrycky, Z. Wang, K. Kim, D.-H. Kim, Biotechnol. Adv. 2016, 34, 422.
