Strong, tough, rapid-recovery, and fatigue-resistant hydrogels made of picot peptide fibres

Bin Xue; Zoobia Bashir; Yachong Guo; WenTing Yu; Wenxu Sun; Yiran Li; Yiyang Zhang; Meng Qin; Wei Wang; Yi Cao

doi:10.1038/s41467-023-38280-4

journal article Open Access May 04, 2023

Strong, tough, rapid-recovery, and fatigue-resistant hydrogels made of picot peptide fibres

Bin Xue

Zoobia Bashir Yachong Guo WenTing Yu Wenxu Sun

Yiran Li

Yiyang Zhang Meng Qin

Wei Wang

Yi Cao

Nature Communications Vol. 14 No. 1 · Springer Science and Business Media LLC

View at Publisher Save 10.1038/s41467-023-38280-4

Abstract

AbstractHydrogels are promising soft materials as tissue engineering scaffolds, stretchable sensors, and soft robotics. Yet, it remains challenging to develop synthetic hydrogels with mechanical stability and durability similar to those of the connective tissues. Many of the necessary mechanical properties, such as high strength, high toughness, rapid recovery, and high fatigue resistance, generally cannot be established together using conventional polymer networks. Here we present a type of hydrogels comprising hierarchical structures of picot fibres made of copper-bound self-assembling peptide strands with zipped flexible hidden length. The redundant hidden lengths allow the fibres to be extended to dissipate mechanical load without reducing network connectivity, making the hydrogels robust against damage. The hydrogels possess high strength, good toughness, high fatigue threshold, and rapid recovery, comparable to or even outperforming those of articular cartilage. Our study highlights the unique possibility of tailoring hydrogel network structures at the molecular level to improve their mechanical performance.

Topics

No keywords indexed for this article. Browse by subject →

References

66

[1]

Huey, D. J., Hu, J. C. & Athanasiou, K. A. Unlike bone, cartilage regeneration remains elusive. Science 338, 917–921 (2012). 10.1126/science.1222454

[2]

Thambyah, A., Nather, A. & Goh, J. Mechanical properties of articular cartilage covered by the meniscus. Osteoarthr. Cartil. 14, 580–588 (2006). 10.1016/j.joca.2006.01.015

[3]

Robinson, D. L. et al. Mechanical properties of normal and osteoarthritic human articular cartilage. J. Mech. Behav. Biomed. Mater. 61, 96–109 (2016). 10.1016/j.jmbbm.2016.01.015

[4]

Burgin, L. V., Edelsten, L. & Aspden, R. M. The mechanical and material properties of elderly human articular cartilage subject to impact and slow loading. Med. Eng. Phys. 36, 226–232 (2014). 10.1016/j.medengphy.2013.11.002

[5]

Hydrogels for tissue engineering: scaffold design variables and applications

Jeanie L. Drury, David J. Mooney

Biomaterials 2003 10.1016/s0142-9612(03)00340-5

[6]

Bodugoz-Senturk, H., Macias, C. E., Kung, J. H. & Muratoglu, O. K. Poly(vinyl alcohol)–acrylamide hydrogels as load-bearing cartilage substitute. Biomaterials 30, 589–596 (2009). 10.1016/j.biomaterials.2008.10.010

[7]

Moutos, F. T., Freed, L. E. & Guilak, F. A biomimetic three-dimensional woven composite scaffold for functional tissue engineering of cartilage. Nat. Mater. 6, 162–167 (2007). 10.1038/nmat1822

[8]

Creton, C. 50th Anniversary perspective: networks and gels: soft but dynamic and tough. Macromolecules 50, 8297–8316 (2017). 10.1021/acs.macromol.7b01698

[9]

Mayumi, K., Guo, J., Narita, T., Hui, C. Y. & Creton, C. Fracture of dual crosslink gels with permanent and transient crosslinks. Extrem. Mech. Lett. 6, 52–59 (2016). 10.1016/j.eml.2015.12.002

[10]

Zhang, H. J. et al. Tough physical double-network hydrogels based on amphiphilic triblock copolymers. Adv. Mater. 28, 4884–4890 (2016). 10.1002/adma.201600466

[11]

Gonzalez, M. A. et al. Strong, tough, stretchable, and self-adhesive hydrogels from intrinsically unstructured proteins. Adv. Mater. 29, 1604743 (2017). 10.1002/adma.201604743

[12]

Wang, T. et al. Regulating mechanical properties of polymer-supramolecular double-network hydrogel by supramolecular self-assembling structures. Chin. J. Chem. 39, 2711–2717 (2021). 10.1002/cjoc.202100370

[13]

Sun, J.-Y. et al. Highly stretchable and tough hydrogels. Nature 489, 133 (2012). 10.1038/nature11409

[14]

Yang, Y., Wang, X., Yang, F., Wang, L. & Wu, D. Highly elastic and ultratough hybrid ionic–covalent hydrogels with tunable structures and mechanics. Adv. Mater. 30, 1707071 (2018). 10.1002/adma.201707071

[15]

Long, T., Li, Y., Fang, X. & Sun, J. Salt-mediated polyampholyte hydrogels with high mechanical strength, excellent self-healing property, and satisfactory electrical conductivity. Adv. Funct. Mater. 28, 1804416 (2018). 10.1002/adfm.201804416

[16]

Chen, Q., Zhu, L., Zhao, C., Wang, Q. & Zheng, J. A robust, one-pot synthesis of highly mechanical and recoverable double network hydrogels using thermoreversible sol-gel polysaccharide. Adv. Mater. 25, 4171–4176 (2013). 10.1002/adma.201300817

[17]

Hu, X. et al. Dynamics of dual networks: strain rate and temperature effects in hydrogels with reversible H-bonds. Macromolecules 50, 652–659 (2017). 10.1021/acs.macromol.6b02422

[18]

Lin, P., Ma, S., Wang, X. & Zhou, F. Molecularly engineered dual-crosslinked hydrogel with ultrahigh mechanical strength, toughness, and good self-recovery. Adv. Mater. 27, 2054–2059 (2015). 10.1002/adma.201405022

[19]

Sun, W. et al. Molecular engineering of metal coordination interactions for strong, tough, and fast-recovery hydrogels. Sci. Adv. 6, eaaz9531 (2020). 10.1126/sciadv.aaz9531

[20]

Liu, J. et al. Tough supramolecular polymer networks with extreme stretchability and fast room-temperature self-healing. Adv. Mater. 29, 1605325 (2017). 10.1002/adma.201605325

[21]

Li, J., Suo, Z. & Vlassak, J. J. Stiff, strong, and tough hydrogels with good chemical stability. J. Mater. Chem. B 2, 6708–6713 (2014). 10.1039/c4tb01194e

[22]

Wang, W., Zhang, Y. & Liu, W. Bioinspired fabrication of high strength hydrogels from non-covalent interactions. Prog. Polym. Sci. 71, 1–25 (2017). 10.1016/j.progpolymsci.2017.04.001

[23]

The conflicts between strength and toughness

Robert O. Ritchie

Nature Materials 2011 10.1038/nmat3115

[24]

Zhu, H. et al. Anomalous scaling law of strength and toughness of cellulose nanopaper. Proc. Natl Acad. Sci. USA 112, 8971–8976 (2015). 10.1073/pnas.1502870112

[25]

High strength in combination with high toughness in robust and sustainable polymeric materials

Xiaojian Liao, Martin Dulle, Juliana Martins de Souza e Silva et al.

Science 2019 10.1126/science.aay9033

[26]

Sun, J.-Y. et al. Highly stretchable and tough hydrogels. Nature 489, 133–136 (2012). 10.1038/nature11409

[27]

Yu, A. C. et al. Physical networks from entropy-driven non-covalent interactions. Nat. Commun. 12, 746 (2021). 10.1038/s41467-021-21024-7

[28]

Zhang, D. et al. Multiple physical bonds to realize highly tough and self-adhesive double-network hydrogels. ACS Appl. Polym. Mater. 2, 1031–1042 (2020). 10.1021/acsapm.9b00889

[29]

Physical hydrogels composed of polyampholytes demonstrate high toughness and viscoelasticity

Tao Lin Sun, Takayuki Kurokawa, Shinya Kuroda et al.

Nature Materials 2013 10.1038/nmat3713

[30]

Li, X. & Gong, J. P. Role of dynamic bonds on fatigue threshold of tough hydrogels. Proc Natl Acad. Sci. USA 119, e2200678119 (2022). 10.1073/pnas.2200678119

[31]

Liu, C. et al. Tough hydrogels with rapid self-reinforcement. Science 372, 1078–1081 (2021). 10.1126/science.aaz6694

[32]

Fracture, fatigue, and friction of polymers in which entanglements greatly outnumber cross-links

Junsoo Kim, Guogao Zhang, Meixuanzi Shi et al.

Science 2021 10.1126/science.abg6320

[33]

Wang, Z. et al. Toughening hydrogels through force-triggered chemical reactions that lengthen polymer strands. Science 374, 193–196 (2021). 10.1126/science.abg2689

[34]

Smith, B. L. et al. Molecular mechanistic origin of the toughness of natural adhesives, fibres and composites. Nature 399, 761–763 (1999). 10.1038/21607

[35]

Fantner, G. E. et al. Sacrificial bonds and hidden length: unraveling molecular mesostructures in tough materials. Biophys. J. 90, 1411–1418 (2006). 10.1529/biophysj.105.069344

[36]

Fantner, G. E. et al. Sacrificial bonds and hidden length dissipate energy as mineralized fibrils separate during bone fracture. Nat. Mater. 4, 612–616 (2005). 10.1038/nmat1428

[37]

Zhao, H. & Waite, J. H. Proteins in load-bearing junctions:the histidine-rich metal-binding protein of mussel byssus. Biochemistry 45, 14223–14231 (2006). 10.1021/bi061677n

[38]

Boschetti, F. & Peretti, G. M. Mechanical properties of normal and osteoarthritic human articular cartilage. J. Biomech. 41, S171 (2008). 10.1016/s0021-9290(08)70171-4

[39]

Hua, M. et al. Strong tough hydrogels via the synergy of freeze-casting and salting out. Nature 590, 594–599 (2021). 10.1038/s41586-021-03212-z

[40]

Liang, X. et al. Anisotropically fatigue-resistant hydrogels. Adv. Mater. 33, 2102011 (2021). 10.1002/adma.202102011

[41]

Harrington, M. J. & Fratzl, P. Natural load-bearing protein materials. Prog. Mater. Sci. 120, 100767 (2021). 10.1016/j.pmatsci.2020.100767

[42]

Burla, F., Mulla, Y., Vos, B. E., Aufderhorst-Roberts, A. & Koenderink, G. H. From mechanical resilience to active material properties in biopolymer networks. Nat. Rev. Phys. 1, 249–263 (2019). 10.1038/s42254-019-0036-4

[43]

Highly accurate protein structure prediction with AlphaFold

John Jumper, Richard Evans, Alexander Pritzel et al.

Nature 2021 10.1038/s41586-021-03819-2

[44]

Sheu, S.-Y., Yang, D.-Y., Selzle, H. L. & Schlag, E. W. Energetics of hydrogen bonds in peptides. Proc. Natl Acad. Sci. USA 100, 12683–12687 (2003). 10.1073/pnas.2133366100

[45]

Williams, D. H., Searle, M. S., Mackay, J. P., Gerhard, U. & Maplestone, R. A. Toward an estimation of binding constants in aqueous solution: studies of associations of vancomycin group antibiotics. Proc. Natl Acad. Sci. USA 90, 1172–1178 (1993). 10.1073/pnas.90.4.1172

[46]

Micsonai, A. et al. Accurate secondary structure prediction and fold recognition for circular dichroism spectroscopy. Proc. Natl Acad. Sci. USA 112, E3095–E3103 (2015). 10.1073/pnas.1500851112

[47]

Guterman, T. et al. Formation of bacterial pilus-like nanofibres by designed minimalistic self-assembling peptides. Nat. Commun. 7, 13482 (2016). 10.1038/ncomms13482

[48]

Matsuda, T. et al. Yielding criteria of double network hydrogels. Macromolecules 49, 1865–1872 (2016). 10.1021/acs.macromol.5b02592

[49]

Zhang, W. et al. Fracture toughness and fatigue threshold of tough hydrogels. ACS Macro Lett. 8, 17–23 (2019). 10.1021/acsmacrolett.8b00788

[50]

Paul, J. Flory. principles of polymer chemistry. Science 119, 555–556 (1954).

Showing 50 of 66 references

Cited By

131

Fatigue threshold of dual-crosslinking hydrogels

Yijian Zheng, Yang Gao · 2026

Extreme Mechanics Letters

A bio-based supramolecular hydrogel with gel-sol transition for intelligent and sustainable agro-chemical delivery

Ling Li, Ke Li · 2026

Chemical Engineering Journal

Molecular self-assembly strategy tuning a dry crosslinking protein patch for biocompatible and biodegradable haemostatic sealing

Lisha Yu, Zhaodi Liu · 2025

Nature Communications

Mechanically robust eutectogels enabled by precisely engineered crystalline domains

Yujia Jiang, Ning Tang · 2025

Nature Communications

Refinement of Crystalline Domains: A Strategy To Toughen Conductive Hydrogels

Teng Fei, Haowen Zheng · 2025

ACS Nano

Hydrogels for Long‐Term Moisture Retention under Ambient Conditions: Inhibiting the Evaporation of Free Water from Macroscopic to Molecular Scales

Yong Liu, Shihong Shen · 2025

Advanced Functional Materials

Hierarchical Engineering of Amphiphilic Peptides Nanofibrous Crosslinkers toward Mechanically Robust, Functionally Customable, and Sustainable Supramolecular Hydrogels

Yifan Zheng, Shuang Zhang · 2025

Advanced Materials

Proteins for Hyperelastic Materials

Rui Su, Chao Ma · 2025

Small

Peptide-based rigid nanorod-reinforced gelatin methacryloyl hydrogels for osteochondral regeneration and additive manufacturing

Junjin Zhu, Yueting Wei · 2025

Nature Communications

Biodegradable photosensitive antimicrobial hydrogel film based on curcumin-carbon dots for raw meat preservation

Shan Xiao, Yanxue Cai · 2025

Food Chemistry: X

Mechanochemistry: Fundamental Principles and Applications

Liang Dong, Luofei Li · 2024

Advanced Science

A Bio‐Inspired Multifunctional Hydrogel Network with Toughly Interfacial Chemistry for Dendrite‐Free Flexible Zinc Ion Battery

Song Yang, Qing Wu · 2024

Angewandte Chemie International Edi...

Self-regulated reversal deformation and locomotion of structurally homogenous hydrogels subjected to constant light illumination

Kexin Guo, Xuehan Yang · 2024

Nature Communications

Metrics

131

Citations

66

References

Details

Published: May 04, 2023
Vol/Issue: 14(1)
License: View

Authors

Wenzhou University

Hong Kong University of Science and Technology

Y

Yi Cao

School of Psychological and Cognitive Sciences, Peking University, Beijing 100871, China

Funding

National Natural Science Foundation of China Award: T2225016,11934008 and 12002149

Natural Science Foundation of Jiangsu Province Award: BK20220120

Cite This Article

Bin Xue, Zoobia Bashir, Yachong Guo, et al. (2023). Strong, tough, rapid-recovery, and fatigue-resistant hydrogels made of picot peptide fibres. Nature Communications, 14(1). https://doi.org/10.1038/s41467-023-38280-4

Strong, tough, rapid-recovery, and fatigue-resistant hydrogels made of picot peptide fibres

You May Also Like