Extracellular Matrix-Surrogate Advanced Functional Composite Biomaterials for Tissue Repair and Regeneration.

bone tissue cardiac tissue cartilage tissue composite biomaterials electrical conductivity magnetic stimulation nerve tissue

Journal

Advanced healthcare materials
ISSN: 2192-2659
Titre abrégé: Adv Healthc Mater
Pays: Germany
ID NLM: 101581613

Informations de publication

Date de publication:
22 Jul 2024
Historique:
revised: 13 06 2024
received: 01 04 2024
medline: 22 7 2024
pubmed: 22 7 2024
entrez: 22 7 2024
Statut: aheadofprint

Résumé

Native tissues, comprising multiple cell types and extracellular matrix components, are inherently composites. Mimicking the intricate structure, functionality, and dynamic properties of native composite tissues represents a significant frontier in biomaterials science and tissue engineering research. Biomimetic composite biomaterials combine the benefits of different components, such as polymers, ceramics, metals, and biomolecules, to create tissue-template materials that closely simulate the structure and functionality of native tissues. While the design of composite biomaterials and their in vitro testing are frequently reviewed, there is a considerable gap in whole animal studies that provides insight into the progress toward clinical translation. Herein, we provide an insightful critical review of advanced composite biomaterials applicable in several tissues. The incorporation of bioactive cues and signaling molecules into composite biomaterials to mimic the native microenvironment is discussed. Strategies for the spatiotemporal release of growth factors, cytokines, and extracellular matrix proteins are elucidated, highlighting their role in guiding cellular behavior, promoting tissue regeneration, and modulating immune responses. Advanced composite biomaterials design challenges, such as achieving optimal mechanical properties, improving long-term stability, and integrating multifunctionality into composite biomaterials and future directions, are discussed. We believe that this manuscript provides the reader with a timely perspective on composite biomaterials.

Identifiants

pubmed: 39036851
doi: 10.1002/adhm.202401218
doi:

Types de publication

Journal Article Review

Langues

eng

Sous-ensembles de citation

IM

Pagination

e2401218

Subventions

Organisme : Natural Sciences and Engineering Research Council of Canada (NSERC)
ID : RGPIN2018-06310

Informations de copyright

© 2024 The Author(s). Advanced Healthcare Materials published by Wiley‐VCH GmbH.

Références

A. Skorulska, P. Piszko, Z. Rybak, M. Szymonowicz, M. Dobrzyński, Materials 1592, 14, 2021.
S. Agarwala, G. L. Goh, G. D. Goh, V. Dikshit, W. Y. Yeong, 3D and 4D Printing of Polymer Nanocomposite Materials: Processes, Applications, and Challenges, pp. 297–324, 2020.
C. Ma, T. Du, X. Niu, Y. Fan, Bone Res. 2022, 10, https://doi.org/10.1038/s41413‐022‐00223‐y.
M. J. Olszta, X. Cheng, S. S. Jee, R. Kumar, Y.‐Y. Kim, M. J. Kaufman, E. P. Douglas, L. B. Gower, Mater. sci. eng. R: Reports 2007, 58, 77.
E. F. Morgan, G. U. Unnikrisnan, A. I. Hussein, Annu. Rev. Biomed. Eng. 2018, 20.
A. M. Bhosale, J. B. Richardson, Br. Med. Bull. 2008, 77, 87.
J. Eschweiler, N. Horn, B. Rath, M. Betsch, A. Baroncini, M. Tingart, F. Migliorini, Life 2021, 302, 11.
A. R. Poole, T. Kojima, T. Yasuda, F. Mwale, M. Kobayashi, S. Laverty, Clin. Orthop. Relat. Res. 2001, https://doi.org/10.1097/00003086‐200110001‐00004.
O. Bas, E. M. De‐Juan‐Pardo, C. Meinert, D. D'Angella, J. G. Baldwin, L. J. Bray, R. M. Wellard, S. Kollmannsberger, E. Rank, C. Werner, T. J. Klein, I. Catelas, D. W. Hutmacher, Biofabrication 2017, 9, 025014.
G. S. Kassab, J. R. Soc., Interface 2006, 719, 3.
A. J. Cocciolone, J. Z. Hawes, M. C. Staiculescu, E. O. Johnson, M. Murshed, J. E. Wagenseil, Am. J. Physiol. Heart Circ. Physiol. 2018. https://doi.org/10.1152/ajpheart.00087.2018.
T. Matsumoto, S. Sugita, T. Yaguchi, “Biomechanics of Blood Vessels: Structure, Mechanics, and Adaptation,” 2015. https://doi.org/10.1007/978‐3‐662‐46836‐4_4.
C. M. B. Ho, A. Mishra, P. T. P. Lin, S. H. Ng, W. Y. Yeong, Y.‐J. Kim, Y.‐J. Yoon, Macromol. Biosci. 2017, https://doi.org/10.1002/mabi.201600250.
R. Xie, H. Yao, A. S. Mao, Y. Zhu, D. Qi, Y. Jia, M. Gao, Y. Chen, L. Wang, D.‐A. Wang, K. Wang, S. Liu, L. Ren, C. Mao, Nat. Biomed. Eng. 2021, 5, 1189.
P. Ma, W. Wu, Y. Wei, L. Ren, S. Lin, J. Wu, Mater. Des. 2021, 207, 109865.
Y. Fang, T. Zhang, L. Zhang, W. Gong, W. Sun, Biofabrication 2019, 11, 035004.
Y. Li, L. Huang, G. Tai, F. Yan, L. Cai, C. Xin, S. Al Islam, Compos Part A Appl. Sci. Manuf. 2022, 152, 106672.
L. Benedini, J. Laiuppa, G. Santillán, M. Baldini, P. Messina, Mater. Sci. Eng., C 2020, 115, 111101.
A. Shapira, R. Feiner, T. Dvir, Int. Mater. Rev. 2016, 61, 1.
G. Turnbull, J. Clarke, F. Picard, P. Riches, L. Jia, F. Han, B. Li, W. Shu, Bioact. Mater. 2018, 3, 278.
E. Kon, F. Salamanna, G. Filardo, B. Di Matteo, N. Shabshin, J. Shani, M. Fini, F. Perdisa, A. Parrilli, S. Sprio, A. Ruffini, M. Marcacci, A. Tampieri, Front. Bioeng. Biotechnol. 2021, 9.
J. A. Nicholson, N. Makaram, A. H. R. W. Simpson, J. F. Keating, Injury 2021, 52, S3.
Sci. Transl. Med. 2016, 8.
N. Egge, S. L. B. Arneaud, R. S. Fonseca, K. R. Zuurbier, J. McClendon, P. M. Douglas, Nat. Commun. 2021, 12.
Z. Wang, L. P. Nogueira, H. J. Haugen, I. C. Van Der Geest, P. C. de Almeida Rodrigues, D. Janssen, T. Bitter, J. J. J. P. van den Beucken, S. C. Leeuwenburgh, Bioact. Mater. 2022, 15, 120.
K. Zhang, Y. Zhou, C. Xiao, W. Zhao, H. Wu, J. Tang, Z. Li, S. Yu, X. Li, L. Min, Z. Yu, G. Wang, L. Wang, K. Zhang, X. Yang, X. Zhu, C. Tu, X. Zhang, Sci. Adv. 2019, 5.
Y. Zhang, N. Sun, M. Zhu, Q. Qiu, P. Zhao, C. Zheng, Q. Bai, Q. Zeng, T. Lu, Biomater. Adv. 2022, 133, 112651.
J. Wieding, T. Lindner, P. Bergschmidt, R. Bader, Biomaterials 2015, 46, 35.
F. A. Shah, A. Snis, A. Matic, P. Thomsen, A. Palmquist, Acta Biomater. 2016, 30, 357.
J. S. Yerramshetty, O. Akkus, Bone 2008, 42, 476.
A. Bhattacharjee, S. Bose, Mater. Des. 2022, 221, 110903.
Z. Hussain, I. Ullah, X. Liu, W. Shen, P. Ding, Y. Zhang, T. Gao, M. Mansoorianfar, T. Gao, R. Pei, Chem. Eng. J. 2022, 438, 135611.
Y. Liu, Z. Qiao, J. Gao, F. Wu, B. Sun, M. Lian, J. Qian, Y. Su, X. Zhu, B. Zhu, Adv. Healthcare Mater. 2021, 10.
Y. Wang, J. Wang, H. Hao, M. Cai, S. Wang, J. Ma, Y. Li, C. Mao, S. Zhang, ACS Nano 2016, 9927, 10.
W. Ali, A. Mehboob, M. G. Han, S. H. Chang, Compos. Part A Appl. Sci. Manuf. 2019, 124, 105464.
H. Lee, D. Y. Shin, Y. Na, G. Han, J. Kim, N. Kim, S.‐J. Bang, H. S. Kang, S. Oh, C.‐B. Yoon, J. Park, H.‐E. Kim, H.‐D. Jung, M.‐H. Kang, Biomater. Adv. 2023, 152, 213523.
H. Lee, D. Y. Shin, S.‐J. Bang, G. Han, Y. Na, H. S. Kang, S. Oh, C.‐B. Yoon, S. Vijayavenkataraman, J. Song, H.‐E. Kim, H.‐D. Jung, M.‐H. Kang, Int. J. Biol. Macromol. 2024, 254, 127797.
W. Wang, B. Zhang, M. Li, J. Li, C. Zhang, Y. Han, L. Wang, K. Wang, C. Zhou, L. Liu, Y. Fan, X. Zhang, Composites, Part B 2021, 224, 109192.
H. Zhou, J. Lee, Acta Biomater. 2011, 7, 2769.
A. J. Wagoner Johnson, B. A. Herschler, Acta Biomater. 2011, 7, 16.
S. Bose, S. Tarafder, Acta Biomater. 2012, 8, 1401.
A. Hoppe, N. S. Güldal, A. R. Boccaccini, Biomaterials 2011, 32, 2757.
D. Ke, J. Yu, P. Liu, C. Niu, X. Yang, Materialia (Oxf) 2022, 21, 101339.
S. Bougioukli, A. Jain, O. Sugiyama, B. A. Tinsley, A. H. Tang, M. H. Tan, D. J. Adams, P. J. Kostenuik, J. R. Lieberman, Bone 2016, 84, 93.
B. Zhang, J. D. Skelly, J. R. Maalouf, D. C. Ayers, J. Song, Sci. Transl. Med. 2019, 11.
F. Senatov, A. Zimina, A. Chubrik, E. Kolesnikov, E. Permyakova, A. Voronin, M. Poponova, P. Orlova, T. Grunina, K. Nikitin, M. Krivozubov, N. Strukova, M. Generalova, A. Ryazanova, V. Manskikh, V. Lunin, A. Gromov, A. Karyagina, Biomater. Adv. 2022, 135, 112680.
J. Li, C. Wang, G. Gao, X. Yin, X. Pu, B. Shi, Y. Liu, Z. Huang, J. Wang, J. Li, G. Yin, Bioact. Mater. 2022, 15, 53.
L. Yang, X. Li, Y. Wu, P. Du, L. Sun, Z. Yu, S. Song, J. Yin, X. Ma, C. Jing, J. Zhao, H. Chen, Y. Dong, Q. Zhang, L. Zhao, Int. J. Nanomed. 2020, 15, 8697.
L. Yang, X. Li, D. Wang, S. Mu, W. Lv, Y. Hao, X. Lu, G. Zhang, W. Nan, H. Chen, L. Xie, Y. Zhang, Y. Dong, Q. Zhang, L. Zhao, J. Biomater. Sci., Polym. Ed. 2020, 31, 658.
J. Liu, G. Chen, H. Xu, K. Hu, J. Sun, M. Liu, F. Zhang, N. Gu, NPG Asia Mater. 2018, 10, 827.
Y. Gong, Y. Zhang, Z. Cao, F. Ye, Z. Lin, Y. Li, Biomater. Sci. 2019, 7, 3614.
W. L. Grayson, B. A. Bunnell, E. Martin, T. Frazier, B. P. Hung, J. M. Gimble, Nat. Rev. Endocrinol. 2015, 11, 140.
B. D. Smith, D. A. Grande, Nat Rev Rheumatol 2015, 11, 213.
S. Bersini, M. Gilardi, C. Arrigoni, G. Talò, M. Zamai, L. Zagra, V. Caiolfa, M. Moretti, Biomaterials 2016, 76, 157.
Z. Wu, J. Bai, G. Ge, T. Wang, S. Feng, Q. Ma, X. Liang, W. Li, W. Zhang, Y. Xu, K. Guo, W. Cui, G. Zha, D. Geng, Adv. Healthcare Mater. 2022, https://doi.org/10.1002/adhm.202200298.
D. F. Williams, Bioact. Mater. 2022, 10, 306.
X. Cui, Y. Zhang, J. Wang, C. Huang, Y. Wang, H. Yang, W. Liu, T. Wang, D. Wang, G. Wang, C. Ruan, D. Chen, W. W. Lu, W. Huang, M. N. Rahaman, H. Pan, Bioact. Mater. 2020, 5, 334.
B. Yuan, L. Wang, R. Zhao, X. Yang, X. Yang, X. Zhu, L. Liu, K. Zhang, Y. Song, X. Zhang, Sci. Adv. 2020, https://doi.org/10.1126/sciadv.abc4704.
Y. Xia, Y. Guo, Z. Yang, H. Chen, K. Ren, M. D. Weir, L. C. Chow, M. A. Reynolds, F. Zhang, N. Gu, H. H. K. Xu, Mater. Sci. Eng., C 2019, 104, 109955.
W. Liu, D. Chen, G. Jiang, Q. Li, Q. Wang, M. Cheng, G. He, X. Zhang, Nanomedicine 2018, 14, 153.
H. Wu, S. Yang, J. Xiao, Z. Ouyang, M. Yang, M. Zhang, D. Zhao, Q. Huang, Mater. Sci. Eng., C 2021, 130, 112442.
S. Rler, C. Heinemann, B. Kruppke, A. S. Wagner, S. Wenisch, H. P. Wiesmann, T. Hanke, Mater. Sci. Eng., C 2018, 93, 265.
T. Song, J. Yang, P. Liu, M. Liu, D. Li, Y. Xiao, Y. Wang, X. Zhang, Composites, Part B 2022, 235, 109759.
B. Ferrigno, R. Bordett, N. Duraisamy, J. Moskow, M. R. Arul, S. Rudraiah, S. P. Nukavarapu, A. T. Vella, S. G. Kumbar, Bioact. Mater. 2020, 5, 468.
A. Nain, S. Chakraborty, S. R. Barman, P. Gavit, S. Indrakumar, A. Agrawal, Z.‐H. Lin, K. Chatterjee, Biomaterials 2024, 307.
Y. Liu, G. Dzidotor, T. T. Le, T. Vinikoor, K. Morgan, E. J. Curry, R. Das, A. McClinton, E. Eisenberg, L. N. Apuzzo, K. T. M. Tran, P. Prasad, T. J. Flanagan, S.‐W. Lee, H.‐M. Kan, M. T. Chorsi, K. W. H. Lo, C. T. Laurencin, T. D. Nguyen, Sci. Transl. Med. 2022, 14, 122528.
B. P. Antunes, M. L. Vainieri, M. Alini, E. Monsonego‐Ornan, S. Grad, A. Yayon, Acta Biomater. 2020, 105, 170.
G. Zhen, Q. Guo, Y. Li, C. Wu, S. Zhu, R. Wang, X. E. Guo, B. C. Kim, J. Huang, Y. Hu, Y. Dan, M. Wan, T. Ha, S. An, X. Cao, Nat. Commun. 2021, https://doi.org/10.1038/s41467‐021‐21948‐0.
J. Liu, C. Tang, J. Huang, J. Gu, J. Yin, G. Xu, S. Yan, Adv. Healthcare Mater. 2023, https://doi.org/10.1002/adhm.202302293.
Y. Wang, X. Huang, X. Zhang, Nat. Commun. 2021, https://doi.org/10.1038/s41467‐021‐21577‐7.
W. J. C. M. Marijnissen, et al., Biomaterials 2002, https://doi.org/10.1016/S0142‐9612(01)00281‐2.
G. A. Ameer, T. A. Mahmood, R. Langer, J. Orthop. Res. 2002, https://doi.org/10.1016/S0736‐0266(01)00074‐2.
S. J. Hollister, Nat. Mater. 2005, 4, 518.
F. T. Moutos, L. E. Freed, F. Guilak, Nat. Mater. 2007, 6, 162.
D. Wang, H. Xu, J. Liu, Z. Chen, Y. Li, B. Hu, D. Zhang, J. Li, H. Chu, Composites, Part B 2020, 202, 108418.
X. Yu, Z. Deng, H. Li, Y. Ma, X. Ma, Q. Zheng, RSC Adv. 2022, 12, 28254.
G. Li, S. Liu, Y. Chen, J. Zhao, H. Xu, J. Weng, F. Yu, A. Xiong, A. Udduttula, D. Wang, P. Liu, Y. Chen, H. Zeng, Nat. Commun. 2023, 14, 11.
Y. Lei, Y. Wang, J. Shen, Z. Cai, C. Zhao, H. Chen, X. Luo, N. Hu, W. Cui, W. Huang, Sci. Adv. 2022, https://doi.org/10.1126/sciadv.abl6449.
H. Rogan, F. Ilagan, X. Tong, C. R. Chu, F. Yang, Biomaterials 2020, 228, 119579.
Y. Sun, Y. You, W. Jiang, B. Wang, Q. Wu, K. Dai, Sci. Adv. 2020, https://doi.org/10.1126/sciadv.aay1422.
L. Zheng, S. Zhao, Y. Li, J. Xu, W. Yan, B. Guo, J. Xu, L. Jiang, Y. Zhang, H. Wei, Q. Jiang, Sci. Adv. 2024, https://doi.org/10.1126/sciadv.adk6084.
S. E. Catheline, et al., Sci. Signaling 2022, 15.
Y. Deng, J. Lu, W. Li, A. Wu, X. Zhang, W. Tong, K. K. Ho, L. Qin, H. Song, K. K. Mak, Nat. Commun. 2018, https://doi.org/10.1038/s41467‐018‐07022‐2.
H. Iijima, G. Gilmer, K. Wang, A. C. Bean, Y. He, H. Lin, W.‐Y. Tang, D. Lamont, C. Tai, A. Ito, J. J. Jones, C. Evans, F. Ambrosio, Nat. Commun. 2023, https://doi.org/10.1038/s41467‐022‐35359‐2.
S. H. Chang, D. Mori, H. Kobayashi, Y. Mori, H. Nakamoto, K. Okada, Y. Taniguchi, S. Sugita, F. Yano, U.‐I. l. Chung, J.‐R. Kim‐Kaneyama, M. Yanagita, A. Economides, E. Canalis, D. Chen, S. Tanaka, T. Saito, Nat. Commun. 2019, https://doi.org/10.1038/s41467‐019‐09491‐5.
J. H. Tsui, A. Leonard, N. D. Camp, J. T. Long, Z. Y. Nawas, R. Chavanachat, A. S. T. Smith, J. S. Choi, Z. Dong, E. H. Ahn, A. Wolf‐Yadlin, C. E. Murry, N. J. Sniadecki, D.‐H. Kim, Biomaterials 2021, 272, 120764.
S. R. Shin, C. Zihlmann, M. Akbari, P. Assawes, L. Cheung, K. Zhang, V. Manoharan, Y. S. Zhang, M. Yüksekkaya, K.‐T. Wan, M. Nikkhah, M. R. Dokmeci, X. (.S.). Tang, A. Khademhosseini, Small 2016, 12, 3677.
A. E. Almada, A. J. Wagers, Nat. Rev. Mol. Cell Biol. 2016, 17, 267.
R. Alonaizan, C. Carr, Biochem. Soc. Trans. 2022, 50, 269.
M. Mao, H. Liang, J. He, A. Kasimu, Y. Zhang, L. Wang, X. Li, D. Li, Int. J. Bioprint. 2021, 7, 362.
W. Zhu, X. Qu, J. Zhu, X. Ma, S. Patel, J. Liu, P. Wang, C. S. E. Lai, M. Gou, Y. Xu, K. Zhang, S. Chen, Biomaterials 2017, 124, 106.
G. Basara, M. Saeidi‐Javash, X. Ren, G. Bahcecioglu, B. C. Wyatt, B. Anasori, Y. Zhang, P. Zorlutuna, Acta Biomater. 2022, 139, 179.
Z. Zheng, C. Lei, H. Liu, M. Jiang, Z. Zhou, Y. Zhao, C.‐Y. Yu, H. Wei, Adv. Healthcare Mater. 2022, https://doi.org/10.1002/adhm.202200990.
C. Wang, Y. Chai, X. Wen, Y. Ai, H. Zhao, W. Hu, X. Yang, M.‐Y. Ding, X. Shi, Q. Liu, Q. Liang, ACS Mater. Lett. 2021, 3, 1238.
L. Wang, Y. Liu, G. Ye, Y. He, B. Li, Y. Guan, B. Gong, K. Mequanint, M. M. Q. Xing, X. Qiu, Nat. Biomed. Eng. 2021, 5, 115710.
Y. He, Q. Li, P. Chen, Q. Duan, J. Zhan, X. Cai, L. Wang, H. Hou, X. Qiu, Nat. Commun. 2022, https://doi.org/10.1038/s41467‐022‐35437‐5.
S. Chen, J. Qi, S. Fan, Z. Qiao, J. C. Yeo, C. T. Lim, Adv. Healthcare Mater. 2021, https://doi.org/10.1002/adhm.202100116.
C. Huang, X. Wang, Q. Cao, D. Zhang, S. Ding, H. Xie, J.‐Z. Jiang, ACS Appl. Mater. Interfaces 2022, 14, 38196.
A. Bodys‐Pełka, M. Kusztal, M. Boszko, R. Główczyńska, M. Grabowski, J. Clin. Med. 2021, 4929.
A. Kamiŝalić, I. Fister, M. Turkanović, S. Karakatiĉ, Sensors (Switzerland) 2018, 18, 1714.
M. Elgendi, Curr. Cardiol. Rev. 2012, 8, 14.
H. Hu, H. Huang, M. Li, X. Gao, L. Yin, R. Qi, R. S. Wu, X. Chen, Y. Ma, K. Shi, C. Li, T. M. Maus, B. Huang, C. Lu, M. Lin, S. Zhou, Z. Lou, Y. Gu, Y. Chen, Y. Lei, X. Wang, R. Wang, W. Yue, X. Yang, Y. Bian, J. Mu, G. Park, S. Xiang, S. Cai, P. W. Corey, et al., Nature 2023, 613, 667.
S. Choi, S. I. Han, D. Jung, H. J. Hwang, C. Lim, S. Bae, O. K. Park, C. M. Tschabrunn, M. Lee, S. Y. Bae, J. W. Yu, J. H. Ryu, S.‐W. Lee, K. Park, P. M. Kang, W. B. Lee, R. Nezafat, T. Hyeon, D.‐H. Kim, Nat. Nanotechnol. 2018, 13, 1048.
B. Seelbinder, S. Ghosh, S. E. Schneider, A. K. Scott, A. G. Berman, C. J. Goergen, K. B. Margulies, K. C. Bedi, E. Casas, A. R. Swearingen, J. Brumbaugh, S. Calve, C. P. Neu, Nat. Biomed. Eng. 2021, 5, 1500.
R. Feiner, L. Engel, S. Fleischer, M. Malki, I. Gal, A. Shapira, Y. Shacham‐Diamand, T. Dvir, Nat. Mater. 2016, 15, 679.
M. Shi, R. Dong, J. Hu, B. Guo, Chem. Eng. J. 2023, 457, 141110.
M. H. Salehi, H. Golbaten‐Mofrad, S. H. Jafari, V. Goodarzi, M. Entezari, M. Hashemi, S. Zamanlui, Int. J. Biol. Macromol. 2021, 173, 467.
S. Noh, H. Y. Gong, H. J. Lee, W. G. Koh, “Electrically conductive micropatterned polyaniline‐poly(Ethylene glycol) composite hydrogel,” Materials, 2021, https://doi.org/10.3390/ma14020308.
B. Massoumi, M. Hatamzadeh, N. Firouzi, M. Jaymand, Mater. Sci. Eng., C 2019, 98, 300.
D. Su, J. Zhou, K. S. Ahmed, Q. Ma, G. Lv, J. Chen, Int. J. Biol. Macromol. 2019, 129, 895.
G. Zhao, H. Qing, G. Huang, G. M. Genin, T. J. Lu, Z. Luo, F. Xu, X. Zhang, NPG Asia Mater. 2018, 10, 982.
Y. Li, J. Wang, Y. Yang, J. Shi, H. Zhang, X. Yao, W. Chen, X. Zhang, Mater. Sci. Eng., C 2021, 118, 111447.
C. Zhang, J. Wang, R. Chi, J. Shi, Y. Yang, X. Zhang, Mater. Des. 2019, 183, 108166.
A. Serafin, C. Murphy, M. C. Rubio, M. N. Collins, Mater. Sci. Eng., C 2021, 122, 111927.
Y. Zhou, C. Wan, Y. Yang, H. Yang, S. Wang, Z. Dai, K. Ji, H. Jiang, X. Chen, Y. Long, Adv. Funct. Mater. 2019, https://doi.org/10.1002/adfm.201806220.
P. Deng, F. Chen, H. Zhang, Y. Chen, J. Zhou, Adv. Healthcare Mater. 2022, https://doi.org/10.1002/adhm.202200115.
M. Dong, B. Shi, D. Liu, J.‐H. Liu, D. Zhao, Z.‐H. Yu, X.‐Q. Shen, J.‐M. Gan, B.‐L. Shi, Y. Qiu, C.‐C. Wang, Z.‐Z. Zhu, Q.‐D. Shen, ACS Nano 2020, 14, 16565.
L. Sang, Y. Liu, W. Hua, K. Xu, G. Wang, W. Zhong, L. Wang, S. Xu, M. M. Q. Xing, X. Qiu, RSC Adv. 2016, 6, 26341.
L. Zhou, L. Fan, X. Yi, Z. Zhou, C. Liu, R. Fu, C. Dai, Z. Wang, X. Chen, P. Yu, D. Chen, G. Tan, Q. Wang, C. Ning, ACS Nano 2018, 12, 10957.
E. A. Kiyotake, E. E. Thomas, H. B. Homburg, C. K. Milton, A. D. Smitherman, N. D. Donahue, K.‐M. Fung, S. Wilhelm, M. D. Martin, M. S. Detamore, J. Biomed. Mater. Res., Part A 2022, 110, 365.
K. Zhang, J. Li, J. Jin, J. Dong, L. Li, B. Xue, W. Wang, Q. Jiang, Y. Cao, Mater. Des. 2020, 196, 109092.
B. Yang, C. Liang, D. Chen, F. Cheng, Y. Zhang, S. Wang, J. Shu, X. Huang, J. Wang, K. Xia, L. Ying, K. Shi, C. Wang, X. Wang, F. Li, Q. Zhao, Q. Chen, Bioact. Mater. 2022, 15, 103.
C. Xu, Y. Chang, P. Wu, K. Liu, X. Dong, A. Nie, C. Mu, Z. Liu, H. Dai, Z. Luo, Adv. Funct. Mater. 2021, https://doi.org/10.1002/adfm.202104440.
Y. Luo, L. Fan, C. Liu, H. Wen, S. Wang, P. Guan, D. Chen, C. Ning, L. Zhou, G. Tan, Bioact. Mater. 2022, 7, 98.
H. Liu, M. Li, C. Ouyang, T. J. Lu, F. Li, F. Xu, Small 2018, https://doi.org/10.1002/smll.201801711.
Q. Zhang, X. Liu, L. Duan, G. Gao, Chem. Eng. J. 2019, 365, 10.
Q. Wang, X. Pan, C. Lin, D. Lin, Y. Ni, L. Chen, L. Huang, S. Cao, X. Ma, Chem. Eng. J. 2019, 370, 1039.
M. Sasaki, B. C. Karikkineth, K. Nagamine, H. Kaji, K. Torimitsu, M. Nishizawa, Adv. Healthcare Mater. 2014, 3, 1919.
Y. Ye, Y. Zhang, Y. Chen, X. Han, F. Jiang, Adv. Funct. Mater. 2020, https://doi.org/10.1002/adfm.202003430.
J. Chen, Q. Peng, T. Thundat, H. Zeng, Chem. Mater. 2019, 31, 4553.
L. Han, L. Yan, M. Wang, K. Wang, L. Fang, J. Zhou, J. Fang, F. Ren, X. Lu, Chem. Mater. 2018, 30, 5561.
Z. Deng, T. Hu, Q. Lei, J. He, P. X. Ma, B. Guo, ACS Appl. Mater. Interfaces 2019, 11, 6796.
G. Ge, Y. Zhang, J. Shao, W. Wang, W. Si, W. Huang, X. Dong, Adv. Funct. Mater. 2018, https://doi.org/10.1002/adfm.201802576.
Y. J. Liu, W. T. Cao, M. G. Ma, P. Wan, ACS Appl. Mater. Interfaces 2017, 9, 25559.
Y. Zhou, C. Wan, Y. Yang, H. Yang, S. Wang, Z. Dai, K. Ji, H. Jiang, X. Chen, Y. Long, Adv. Funct. Mater. 2019, https://doi.org/10.1002/adfm.201806220.
C. Shao, M. Wang, L. Meng, H. Chang, B. Wang, F. Xu, J. Yang, P. Wan, Chem. Mater. 2018, 30, 3110.
G. Cai, J. Wang, K. Qian, J. Chen, S. Li, P. S. Lee, Adv. Sci. 2017, https://doi.org/10.1002/advs.201600190.
Y. Zhou, C. Wan, Y. Yang, H. Yang, S. Wang, Z. Dai, K. Ji, H. Jiang, X. Chen, Y. Long, Adv. Funct. Mater. 2019, https://doi.org/10.1002/adfm.201806220.
Z. Wang, H. Zhou, J. Lai, B. Yan, H. Liu, X. Jin, A. Ma, G. Zhang, W. Zhao, W. Chen, J. Mater. Chem. C Mater. 2018, 6, 9200.
X. Jin, H. Jiang, G. Li, B. Fu, X. Bao, Z. Wang, Q. Hu, Chem. Eng. J. 2020, 394, 124901.
C. Zheng, Y. Yue, L. Gan, X. Xu, C. Mei, J. Han, Nanomaterials 2019, 9, 937.
C. Zheng, K. Lu, Y. Lu, S. Zhu, Y. Yue, X. Xu, C. Mei, H. Xiao, Q. Wu, J. Han, Carbohydr. Polym. 2020, 250, 116905.
Y. Chen, K. Lu, Y. Song, J. Han, Y. Yue, S. K. Biswas, Q. Wu, H. Xiao, Nanomaterials 2019, 9, 1737.
H. Huang, L. Han, J. Li, X. Fu, Y. Wang, Z. Yang, X. Xu, L. Pan, M. Xu, J. Mater. Chem. A Mater. 2020, 8, 10291.
Y. Zhao, B. Zhang, B. Yao, Y. Qiu, Z. Peng, Y. Zhang, Y. Alsaid, I. Frenkel, K. Youssef, Q. Pei, X. He, Matter 2020, 3, 1196.
T. Distler, C. Polley, F. Shi, D. Schneidereit, M. D. Ashton, O. Friedrich, J. F. Kolb, J. G. Hardy, R. Detsch, H. Seitz, A. R. Boccaccini, Adv. Healthcare Mater. 2021, https://doi.org/10.1002/adhm.202001876.
M. Kashi, F. Baghbani, F. Moztarzadeh, H. Mobasheri, E. Kowsari, Int. J. Biol. Macromol. 2018, 107, 1567.
S. Liang, Y. Zhang, H. Wang, Z. Xu, J. Chen, R. Bao, B. Tan, Y. Cui, G. Fan, W. Wang, W. Wang, W. Liu, Adv. Mater. 2018, https://doi.org/10.1002/adma.201704235.
B. Guo, J. Qu, X. Zhao, M. Zhang, Acta Biomater. 2019, 84, 180.
J. Lee, V. Manoharan, L. Cheung, S. Lee, B.‐H. Cha, P. Newman, R. Farzad, S. Mehrotra, K. Zhang, F. Khan, M. Ghaderi, Y.‐D. Lin, S. Aftab, P. Mostafalu, M. Miscuglio, J. Li, B. B. Mandal, M. A. Hussain, K.‐T. Wan, X. S. Tang, A. Khademhosseini, S. R. Shin, ACS Nano 2019, 13, 12525.
B. Maharjan, D. Kumar, G. P. Awasthi, D. P. Bhattarai, J. Y. Kim, C. H. Park, C. S. Kim, Composites, Part B 2019, 177, 107415.
T. Wu, C. Cui, Y. Huang, Y. Liu, C. Fan, X. Han, Y. Yang, Z. Xu, B. Liu, G. Fan, W. Liu, ACS Appl. Mater. Interfaces 2020, 12, 2039.
J. Chen, X. Han, J. Deng, J. Zhang, L. Li, J. Ni, Y. Huang, X. Xie, S. Chen, L. Ke, X. Gao, W. Wang, G. Fan, Chem. Eng. J. 2021, 413, 127423.
L. Han, X. Lu, M. Wang, D. Gan, W. Deng, K. Wang, L. Fang, K. Liu, C. W. Chan, Y. Tang, L.‐T. Weng, H. Yuan, Small 2017, https://doi.org/10.1002/smll.201601916.
I. K. Han, K.‐I. l. Song, S.‐M. Jung, Y. Jo, J. Kwon, T. Chung, S. Yoo, J. Jang, Y.‐T. Kim, D. S. Hwang, Y. S. Kim, Adv. Mater. 2023, https://doi.org/10.1002/adma.202203431.
M. Taale, F. Schütt, K. Zheng, Y. K. Mishra, A. R. Boccaccini, R. Adelung, C. Selhuber‐Unkel, ACS Appl. Mater. Interfaces 2018, 10, 43874.
A. M. Martins, G. Eng, S. G. Caridade, J. F. Mano, R. L. Reis, G. Vunjak‐Novakovic, Biomacromolecules 2014, 15, 635.
A. Magaz, X. Li, J. E. Gough, J. J. Blaker, Mater. Sci. Eng., C 2021, 119, 111632.
J. S. Choi, J. S. Park, B. Kim, B. T. Lee, J. H. Yim, Polymer (Guildf) 2017, 124, 95.
J. Li, W. Fang, T. Hao, D. Dong, B. Yang, F. Yao, C. Wang, Composites, Part B 2020, 199, 108285.
I. Rajzer, M. Rom, E. Menaszek, P. Pasierb, Mater. Lett. 2015, 138, 60.
S. Wang, S. Guan, J. Wang, H. Liu, T. Liu, X. Ma, Z. Cui, J. Biosci. Bioeng. 2017, 123, 116.
S. Khan, M. Ul‐Islam, M. W. Ullah, Y. Kim, J. K. Park, Cellulose 2015, 22, 2141.
D. Naskar, P. Bhattacharjee, A. K. Ghosh, M. Mandal, S. C. Kundu, ACS Appl. Mater. Interfaces 2017, 19356, 9.
N. Maráková, Z. A. Boeva, P. Humpolcek, T. Lindfors, J. Pacherník, V. Kaspárková, K. A. Radaszkiewicz, Z. Capáková, A. Minark, M. Lehocký, Mater. Sci. Eng., C 2019, 105, 110029.
R. Kouser, A. Vashist, M. Zafaryab, M. A. Rizvi, S. Ahmad, Mater. Sci. Eng., C 2018, 84, 168.
M. Afifi, M. K. Ahmed, A. M. Fathi, V. Uskoković, Int. J. Pharm. 2020, 585, 119502.
S.‐M. Jeong, J. Ahn, Y. K. Choi, T. Lim, K. Seo, T. Hong, G. H. Choi, H. Kim, B. W. Lee, S. Y. Park, S. Ju, NPG Asia Mater. 2020, https://doi.org/10.1038/s41427‐020‐0213‐z.
J. Park, S. Choi, A. H. Janardhan, S.‐Y. Lee, S. Raut, J. Soares, K. Shin, S. Yang, C. Lee, K.‐W. Kang, H. R. Cho, S. J. Kim, P. Seo, W. Hyun, S. Jung, H.‐J. Lee, N. Lee, S. H. Choi, M. Sacks, N. Lu, M. E. Josephson, T. Hyeon, D.‐H. Kim, H. J. Hwang, Sci. Transl. Med. 2016, https://doi.org/10.1126/scitranslmed.aad8568.
Z. Zhang, Y. Wang, Z. Chen, D. Xu, D. Zhang, F. Wang, Y. Zhao, J. Nanobiotechnology 2022, https://doi.org/10.1186/s12951‐022‐01340‐w.
D. O. Adewole, M. D. Serruya, J. A. Wolf, D. K. Cullen, Front. Neurosci. 2019, https://doi.org/10.3389/fnins.2019.00269.
F. Lotti, F. Ranieri, G. Vadalà, L. Zollo, G. Di Pino, Front. Neurosci. 2017, https://doi.org/10.3389/fnins.2017.00497.
J. Maughan, P. J. Gouveia, J. G. Gonzalez, L. M. Leahy, I. Woods, C. O'Connor, T. McGuire, J. R. Garcia, D. G. O' Shea, S. F. McComish, O. D. Kennedy, M. A. Caldwell, A. Dervan, J. N. Coleman, F. J. O'Brien, Appl. Mater. Today 2022, 29, 101629.
A. Pardo, M. Gómez‐Florit, S. Barbosa, P. Taboada, R. M. A. Domingues, M. E. Gomes, ACS Nano 2021, 15, 175.
Y. Li, G. Huang, X. Zhang, B. Li, Y. Chen, T. Lu, T. J. Lu, F. Xu, Adv. Funct. Mater. 2013, 23, 660.
R. Tognato, A. R. Armiento, V. Bonfrate, R. Levato, J. Malda, M. Alini, D. Eglin, G. Giancane, T. Serra, Adv. Funct. Mater. 2019, https://doi.org/10.1002/adfm.201804647.
L. Zwi‐Dantsis, B. Wang, C. Marijon, S. Zonetti, A. Ferrini, L. Massi, D. J. Stuckey, C. M. Terracciano, M. M. Stevens, Adv. Mater. 2020, https://doi.org/10.1002/adma.201904598.
S. Liu, X. Chen, L. Bao, T. Liu, P. Yuan, X. Yang, X. Qiu, J. J. Gooding, Y. Bai, J. Xiao, F. Pu, Y. Jin, Nat. Biomed. Eng. 2020, 4, 1063.
H.‐F. Liang, Y.‐P. Zou, A.‐N. Hu, B. Wang, J. Li, L. Huang, W.‐S. Chen, D.‐H. Su, L. Xiao, Y. Xiao, Y.‐Q. Ma, X.‐L. Li, L.‐B. Jiang, J. Dong, Adv. Healthcare Mater. 2023, https://doi.org/10.1002/adhm.202301724.
W. J. Tyler, Nat. Rev. Neurosci. 2012, 13, 867.
A. Tay, A. Sohrabi, K. Poole, S. Seidlits, D. Di Carlo, Adv. Mater. 2018, https://doi.org/10.1002/adma.201800927.
M. Janmohammadi, Z. Nazemi, A. O. M. Salehi, A. Seyfoori, J. V. John, M. S. Nourbakhsh, M. Akbari, Bioact. Mater. 2023, 20.
N. Sarkar, S. Bose, ACS Appl. Mater. Interfaces 2019, 11, 17184.
S. Noreen, S. Hasan, S. A. Ghumman, S. Anwar, H. Y. Gondal, F. Batool, S. Noureen, ACS Omega 2023, 8, 5925.
M. M. Yahoum, S. Toumi, H. Tahraoui, S. Lefnaoui, M. Kebir, A. Amrane, A. A. Assadi, J. Zhang, L. Mouni, Micromachines (Basel) 14, 609 2023.
M. Liu, J. Zhang, X. Zhu, W. Shan, L. Li, J. Zhong, Z. Zhang, Y. Huang, J. Controlled Release 2016, 222, 67.
K. Liang, R. Ricco, C. M. Doherty, M. J. Styles, S. Bell, N. Kirby, S. Mudie, D. Haylock, A. J. Hill, C. J. Doonan, P. Falcaro, Nat. Commun. 2015, 6, 137.
X. Mo, D. Zhang, K. Liu, X. Zhao, X. Li, W. Wang, Int. J. Mol. Sci. 2023, 24, 1291.
K. Hasanbegloo, S. Banihashem, B. Faraji Dizaji, S. Bybordi, N. Farrokh‐Eslamlou, P. G.‐S. Abadi, F. S. Jazi, M. Irani, Int. J. Biol. Macromol. 2023, 230, 123380.
C. Huang, G. Yang, S. Zhou, E. Luo, J. Pan, C. Bao, X. Liu, ACS Biomater. Sci. Eng. 2020, 6, 5758.
C. Tipa, M. T. Cidade, T. Vieira, J. C. Silva, P. I. P. Soares, J. P. Borges, Nanomaterials 2021, 11, 25.
Y. Qu, B. Chu, K. Shi, X. Wei, P. Yang, M. Chen, M. Tang, S. Li, F. Wang, X. Yang, Y. Zheng, T. Niu, Z. Qian, Chem. Eng. J. 2023, 455, 140600.
N. Aslankoohi, K. Mequanint, ACS Appl. Bio. Mater. 2020, 3, 3621.
X. He, Y. Ding, S. Duan, S. Luo, J. Song, C. Peng, Y. Tan, Q. Zeng, Y. Liu, J. Biomed. Nanotechnol. 2019, 15, 2059.
M. Feng, G. Jiang, Y. Sun, U. E. Aharodnikau, K. E. Yunusov, T. Liu, Z. Zeng, S. O. Solomevich, Inorg. Chem. Commun. 2022, 144, 109896.
G. Jiang, B. Xu, J. Zhu, Y. Zhang, T. Liu, G. Song, Biomed. Phys. Eng. Express 2019, 5, 045038.
M. Gou, X. Qu, W. Zhu, M. Xiang, J. Yang, K. Zhang, Y. Wei, S. Chen, Nat. Commun. 2014, https://doi.org/10.1038/ncomms4774.
B. Xiao, E. Viennois, Q. Chen, L. Wang, M. K. Han, Y. Zhang, Z. Zhang, Y. Kang, Y. Wan, D. Merlin, ACS Nano 2018, 12, 5253.
Y. Zhang, J. Zhang, M. Chen, H. Gong, S. Thamphiwatana, L. Eckmann, W. Gao, L. Zhang, ACS Appl. Mater. Interfaces 2016, 8, 18367.
Y. guang Bi, Z. Ting Lin, S. Ting Deng, Mater. Sci. Eng., C 2019, 100, 576.
Z. Wang, Y. Wang, J. Yan, K. Zhang, F. Lin, L. Xiang, L. Deng, Z. Guan, W. Cui, H. Zhang, Adv. Drug Delivery Rev. 2021, 174, 504.

Auteurs

Milad Vahidi (M)

Department of Chemical and Biochemical Engineering, The University of Western Ontario, London, N6A5B9, Canada.

Amin S Rizkalla (AS)

Department of Chemical and Biochemical Engineering, The University of Western Ontario, London, N6A5B9, Canada.
School of Biomedical Engineering, The University of Western Ontario, London, N6A5B9, Canada.

Kibret Mequanint (K)

Department of Chemical and Biochemical Engineering, The University of Western Ontario, London, N6A5B9, Canada.
School of Biomedical Engineering, The University of Western Ontario, London, N6A5B9, Canada.

Classifications MeSH