An Organic–Inorganic Hydrogel with Exceptional Mechanical Properties via Anion-Induced Synergistic Toughening for Accelerating Osteogenic Differentiation
Hongmei Luo
College of Polymer Science and Engineering, Sichuan University, Chengdu, 610065 China
Search for more papers by this authorQifeng Mu
RIKEN Center for Emergent Matter Science, 2-1 Hirosawa, Wako, Saitama, 351-0198 Japan
Search for more papers by this authorRuijie Zhu
Faculty of Engineering, Hokkaido University, Sapporo, 060–8628 Japan
Search for more papers by this authorMin Li
College of Polymer Science and Engineering, Sichuan University, Chengdu, 610065 China
Search for more papers by this authorHuanwei Shen
College of Polymer Science and Engineering, Sichuan University, Chengdu, 610065 China
Search for more papers by this authorHonglang Lu
College of Polymer Science and Engineering, Sichuan University, Chengdu, 610065 China
Search for more papers by this authorLongyu Hu
College of Polymer Science and Engineering, Sichuan University, Chengdu, 610065 China
Search for more papers by this authorJiajun Tian
College of Polymer Science and Engineering, Sichuan University, Chengdu, 610065 China
Search for more papers by this authorCorresponding Author
Wei Cui
College of Polymer Science and Engineering, Sichuan University, Chengdu, 610065 China
E-mail: [email protected]; [email protected]
Search for more papers by this authorCorresponding Author
Rong Ran
College of Polymer Science and Engineering, Sichuan University, Chengdu, 610065 China
E-mail: [email protected]; [email protected]
Search for more papers by this authorHongmei Luo
College of Polymer Science and Engineering, Sichuan University, Chengdu, 610065 China
Search for more papers by this authorQifeng Mu
RIKEN Center for Emergent Matter Science, 2-1 Hirosawa, Wako, Saitama, 351-0198 Japan
Search for more papers by this authorRuijie Zhu
Faculty of Engineering, Hokkaido University, Sapporo, 060–8628 Japan
Search for more papers by this authorMin Li
College of Polymer Science and Engineering, Sichuan University, Chengdu, 610065 China
Search for more papers by this authorHuanwei Shen
College of Polymer Science and Engineering, Sichuan University, Chengdu, 610065 China
Search for more papers by this authorHonglang Lu
College of Polymer Science and Engineering, Sichuan University, Chengdu, 610065 China
Search for more papers by this authorLongyu Hu
College of Polymer Science and Engineering, Sichuan University, Chengdu, 610065 China
Search for more papers by this authorJiajun Tian
College of Polymer Science and Engineering, Sichuan University, Chengdu, 610065 China
Search for more papers by this authorCorresponding Author
Wei Cui
College of Polymer Science and Engineering, Sichuan University, Chengdu, 610065 China
E-mail: [email protected]; [email protected]
Search for more papers by this authorCorresponding Author
Rong Ran
College of Polymer Science and Engineering, Sichuan University, Chengdu, 610065 China
E-mail: [email protected]; [email protected]
Search for more papers by this authorAbstract
Mineralized bio-tissues achieve exceptional mechanical properties through the assembly of rigid inorganic minerals and soft organic matrices, providing abundant inspiration for synthetic materials. Hydrogels, serving as an ideal candidate to mimic the organic matrix in bio-tissues, can be strengthened by the direct introduction of minerals. However, this enhancement often comes at the expense of toughness due to interfacial mismatch. This study reveals that extreme toughening of hydrogels can be realized through simultaneous in situ mineralization and salting-out, without the need for special chemical modification or additional reinforcements. The key to this strategy lies in harnessing the kosmotropic and precipitation behavior of specific anions as they penetrate a hydrogel system containing both anion-sensitive polymers and multivalent cations. The resulting mineralized hydrogels demonstrate significant improvements in fracture stress, fracture energy, and fatigue threshold due to a multiscale energy dissipation mechanism, with optimal values reaching 12 MPa, 49 kJ m−2, and 2.98 kJ m−2. This simple strategy also proves to be generalizable to other anions, resulting in tough hydrogels with osteoconductivity for promoting in vitro mineralization of human adipose-derived mesenchymal stem cells. This work introduces a universal route to toughen hydrogels without compromising other parameters, holding promise for biological applications demanding integrated mechanical properties.
Conflict of Interest
The authors declare no conflict of interest.
Open Research
Data Availability Statement
The data that support the findings of this study are available from the corresponding author upon reasonable request.
Supporting Information
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References
- 1J. Li, D. J. Mooney, Nat. Rev. Mater. 2016, 1, 1.
- 2B. Balakrishnan, R. Banerjee, Chem. Rev. 2011, 111, 4453.
- 3H. Yuk, C. E. Varela, C. S. Nabzdyk, X. Mao, R. F. Padera, E. T. Roche, X. Zhao, Nature 2019, 575, 169.
- 4X. Wang, X. Sun, D. Gan, M. Soubrier, H.-Y. Chiang, L. Yan, Y. Li, J. Li, S. Yu, Y. Xia, Matter 2022, 5, 1204.
- 5M. Sun, H. Li, Y. Hou, N. Huang, X. Xia, H. Zhu, Q. Xu, Y. Lin, L. Xu, Sci. Adv. 2023, 9, eade6973.
- 6C. Yang, T. Yin, Z. Suo, J. Mech. Phys. Solids 2019, 131, 43.
- 7J. P. Gong, Y. Katsuyama, T. Kurokawa, Y. Osada, Adv. Mater. 2003, 15, 1155.
- 8W. Cui, R. Zhu, Y. Zheng, Q. Mu, M. Pi, Q. Chen, R. Ran, J. Mater. Chem. A 2021, 9, 9706.
- 9G. Shao, D. A. Hanaor, X. Shen, A. Gurlo, Adv. Mater. 2020, 32, 1907176.
- 10C. Yang, Z. Suo, Nat. Rev. Mater. 2018, 3, 125.
- 11K. Haraguchi, T. Takehisa, Adv. Mater. 2002, 14, 1120.
- 12H.-P. Cong, P. Wang, S.-H. Yu, Chem. Mater. 2013, 25, 3357.
- 13Y.-Z. Zhang, J. K. El-Demellawi, Q. Jiang, G. Ge, H. Liang, K. Lee, X. Dong, H. N. Alshareef, Chem. Sco. Rev. 2020, 49, 7229.
- 14T. Nonoyama, H. Ogasawara, M. Tanaka, M. Higuchi, T. Kinoshita, Soft Matter 2012, 8, 11531.
- 15Y. Tan, L. Ma, X. Chen, Y. Ran, Q. Tong, L. Tang, X. Li, Int. J. Biol. Macromol. 2022, 216, 547.
- 16T. Nonoyama, Polym. J. 2020, 52, 709.
- 17K. Fukao, T. Nonoyama, R. Kiyama, K. Furusawa, T. Kurokawa, T. Nakajima, J. P. Gong, ACS Nano 2017, 11, 12103.
- 18K. Fukao, K. Tanaka, R. Kiyama, T. Nonoyama, J. P. Gong, J. Mater. Chem. B 2020, 8, 5184.
- 19H. Du, T. Yuan, R. Zhao, M. Hirsch, M. Kessler, E. Amstad, Biomater. Sci. 2022, 10, 4949.
- 20J.-Y. Sun, X. Zhao, W. R. Illeperuma, O. Chaudhuri, K. H. Oh, D. J. Mooney, J. J. Vlassak, Z. Suo, Nature 2012, 489, 133.
- 21W. Cui, D. R. King, Y. Huang, L. Chen, T. L. Sun, Y. Guo, Y. Saruwatari, C. Y. Hui, T. Kurokawa, J. P. Gong, Adv. Mater. 2020, 32, 1907180.
- 22W. Cui, Y. Huang, L. Chen, Y. Zheng, Y. Saruwatari, C.-Y. Hui, T. Kurokawa, D. R. King, J. P. Gong, Matter 2021, 4, 3646.
- 23C.-Y. Hui, Z. Liu, S. L. Phoenix, D. R. King, W. Cui, Y. Huang, J. P. Gong, Extreme Mech. Lett. 2020, 35, 100642.
- 24S. Wu, M. Hua, Y. Alsaid, Y. Du, Y. Ma, Y. Zhao, C. Y. Lo, C. Wang, D. Wu, B. Yao, Adv. Mater. 2021, 33, 2007829.
- 25Q. He, Y. Huang, S. Wang, Adv. Funct. Mater. 2018, 28, 1705069.
- 26Y. Huang, Y. Xiao, J. Zhou, T. Liu, Y. Yan, S. Long, X. Li, Adv. Funct. Mater. 2021, 31, 2103917.
- 27H. C. Yu, S. Y. Zheng, L. Fang, Z. Ying, M. Du, J. Wang, K. F. Ren, Z. L. Wu, Q. Zheng, Adv. Mater. 2020, 32, 2005171.
- 28R. S. Carnegie, C. L. Gibb, B. C. Gibb, Angew. Chem., Int. Ed. 2014, 53, 11498.
- 29N. Rauner, M. Meuris, M. Zoric, J. C. Tiller, Nature 2017, 543, 407.
- 30S. Sun, L. B. Mao, Z. Lei, S. H. Yu, H. Cölfen, Angew. Chem., Int. Ed. 2016, 55, 11765.
- 31J. Fang, P. Li, X. Lu, L. Fang, X. Lü, F. Ren, Acta Biomater. 2019, 88, 503.
- 32N. Kashimura, Y. Suzuki, T. Nonoyama, J. P. Gong, Chem. Mater. 2024, 36, 2944.
- 33S. Wu, M. Hua, Y. Alsaid, Y. Du, Y. Ma, Y. Zhao, C. Y. Lo, C. Wang, D. Wu, B. Yao, J. Strzalka, H. Zhou, X. Zhu, X. He, Adv. Mater. 2021, 33, 2007829.
- 34J. L. Arias, M. a. S. Fernández, Chem. Rev. 2008, 108, 4475.
- 35A. W. Xu, M. Antonietti, H. Cölfen, Y. P. Fang, Adv. Funct. Mater. 2006, 16, 903.
- 36M. A. Levenstein, C. Anduix-Canto, Y. Y. Kim, M. A. Holden, C. González Niño, D. C. Green, S. E. Foster, A. N. Kulak, L. Govada, N. E. Chayen, Adv. Funct. Mater. 2019, 29, 1808172.
- 37D. R. Baer, J. Moulder, Surf. Sci. Spectra 1993, 2, 1.
- 38F. B. Reig, J. G. Adelantado, M. M. Moreno, Talanta 2002, 58, 811.
- 39W. Cui, Y. Zheng, R. Zhu, Q. Mu, X. Wang, Z. Wang, S. Liu, M. Li, R. Ran, Adv. Funct. Mater. 2022, 32, 2204823.
- 40M. Hua, S. Wu, Y. Ma, Y. Zhao, Z. Chen, I. Frenkel, J. Strzalka, H. Zhou, X. Zhu, X. He, Nature 2021, 590, 594.
- 41O. Karabiyik Acar, A. B. Kayitmazer, G. Torun Kose, Biomacromolecules 2018, 19, 1198.
- 42R. Long, C.-Y. Hui, Soft Matter 2016, 12, 8069.
- 43X. Li, K. Cui, T. L. Sun, L. Meng, C. Yu, L. Li, C. Creton, T. Kurokawa, J. P. Gong, Proc. Natl. Acad. Sci. USA 2020, 117, 7606.
- 44X. Zhao, X. Chen, H. Yuk, S. Lin, X. Liu, G. Parada, Chem. Rev. 2021, 121, 4309.
- 45L. Xu, S. Gao, Q. Guo, C. Wang, Y. Qiao, D. Qiu, Adv. Mater. 2020, 32, 2004579.
- 46Y. Wu, Y. Zhang, H. Wu, J. Wen, S. Zhang, W. Xing, H. Zhang, H. Xue, J. Gao, Y. Mai, Adv. Mater. 2023, 35, 2210624.
- 47L. Xu, X. Zhao, C. Xu, N. A. Kotov, Adv. Mater. 2018, 30, 1703343.
- 48J. Xiong, X. Wang, L. Li, Q. Li, S. Zheng, Z. Liu, W. Li, F. Yan, Angew. Chem., Int. Ed. 2024, 63, 202316375.
- 49J.-H. Liu, Z. Mao, Y. Chen, Y. Long, H. Wu, J. Shen, R. Zhang, O. W. Yeung, B. Zhou, C. Zhi, Chem. Eng. J. 2023, 468, 143735.
- 50S. Lin, X. Liu, J. Liu, H. Yuk, H.-C. Loh, G. A. Parada, C. Settens, J. Song, A. Masic, G. H. McKinley, Sci. Adv. 2019, 5, eaau8528.
- 51J. Ma, X. Zhang, D. Yin, Y. Cai, Z. Shen, Z. Sheng, J. Bai, S. Qu, S. Zhu, Z. Jia, Adv. Mater. 2024, 36, 2311795.
- 52Y. Ma, J. Gong, Q. Li, X. Liu, C. Qiao, J. Zhang, S. Zhang, Z. Li, Small 2024, 2310046, https://doi.org/10.1002/smll.202310046.
10.1002/smll.202310046 Google Scholar
- 53X. P. Morelle, W. R. Illeperuma, K. Tian, R. Bai, Z. Suo, J. J. Vlassak, Adv. Mater. 2018, 30, 1801541.
- 54B. Xu, P. Zheng, F. Gao, W. Wang, H. Zhang, X. Zhang, X. Feng, W. Liu, Adv. Funct. Mater. 2017, 27, 1604327.
- 55L. Zhang, J. Zhao, J. Zhu, C. He, H. Wang, Soft Matter 2012, 8, 10439.
- 56J. Kim, G. Zhang, M. Shi, Z. Suo, Science 2021, 374, 212.
- 57C. Fan, B. Liu, Z. Xu, C. Cui, T. Wu, Y. Yang, D. Zhang, M. Xiao, Z. Zhang, W. Liu, Mater. Horiz. 2020, 7, 1160.
- 58T. Li, H. Qi, Y. Zhao, P. Kumar, C. Zhao, Z. Li, X. Dong, X. Guo, M. Zhao, X. Li, Sci. Adv. 2024, 10, eadk6643.
- 59Y. Zhou, J. Hu, P. Zhao, W. Zhang, Z. Suo, T. Lu, J. Mech. Phys. Solids 2021, 153, 104483.
- 60Z. Zou, X. Yang, M. Alberic, T. Heil, Q. Wang, B. Pokroy, Y. Politi, L. Bertinetti, Adv. Funct. Mater. 2020, 30, 2000003.
- 61E. Loste, R. M. Wilson, R. Seshadri, F. C. Meldrum, J. Cryst. Growth 2003, 254, 206.