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Biosynthesizing lignin dehydrogenation polymer to fabricate hybrid hydrogel composite with hyaluronic acid for cartilage repair

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Abstract

Lignin possesses a number of functional groups including phenolic hydroxyl and methoxy groups, which grant its bioactivity for the fabrication of bio-polymer-based composites in bone tissue engineering applications. However, the heterogeneity of natural lignin limits its use in biomedicine. In the present study, a bio-enzyme approach was proposed to synthesize lignin-dehydrogenated polymers from the precursors of arabinogalactan (DHP-A) and xylose (DHP-X), which possess more homogeneous substructures with appropriate functional groups. Both DHP-A and DHP-X showed excellent in vitro abilities for regulating biocompatibility, “pre-oxidation,” and chondrogenic differentiation, in which DHP-A possessed cartilage repair ability due to its abundant content of phenolic hydroxyl groups (3.00 mmol g−1). Hence, DHP-A was hybridized with hyaluronic acid (HA) to prepare a hydrogel (DHP-HA) composite, which exhibited the compressive strength and modulus of 810 kPa and 310 kPa, respectively. Notably, these properties closely resemble those of articular cartilage, which typically ranges from 320 to 810 kPa. The application of DHP-HA hydrogel composite in a rat cartilage defect model in vivo revealed that it promoted the regeneration of hyaline cartilage rather than hypertrophic cartilage, which could heal 66.22–79.26% of the cartilage defects compared to the control group. Pre-oxidation of DHP-A elicits a mechanism that activates the oxidative stress system, leading to an augmented stress response and consequent increase in stress resistance. This study introduces a pioneering enzymatic synthesis technique to prepare the biologically active lignin for creating bio-polymer-based composites, demonstrating its potential as an innovative avenue for therapeutic cartilage regeneration.

Graphical Abstract

Bioenzymatically synthesized lignin dehydrogenation polymers to hybridize with hyaluronic acid to prepare hydrogel composites for promoting cartilage defect repair.

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Data availability

The data that support the findings of this study are available from the corresponding author, Prof. Caoxing Huang upon reasonable request.

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Funding

This work was funded by the China Postdoctoral Science Foundation (Grant No. 2022M722769) for Dr. Liming Zheng. Prof. Caoxing Huang thanks Alexander von Humboldt Foundation for supporting his research stay in University of Göttingen. Yifei Zhan thanks CSC for financial support of his PhD study in University of Göttingen.

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  1. Wenhui Pei, Yalikun Yusufu, and Yifei Zhan contributed equally to this work, regarding as the first author.

Authors and Affiliations

  1. Jiangsu Co-Innovation Center for Efficient Processing and Utilization of Forest Resources, Nanjing Forestry University, Nanjing, 210037, China

    Wenhui Pei, Xucai Wang, Jian Gan & Caoxing Huang

  2. State Key Laboratory of Pharmaceutical Biotechnology, Department of Sports Medicine and Adult Reconstructive Surgery, Nanjing Drum Tower Hospital, The Affiliated Hospital of Nanjing University Medical School, Nanjing, 210008, China

    Yalikun Yusufu, Liming Zheng & Peng Wang

  3. Department Wood Technology and Wood-Based Composites, Sustainable Materials and Chemistry, University of Göttingen, Göttingen, Germany

    Yifei Zhan & Kai Zhang

  4. Department of Orthopedic Surgery, the Second Affiliated Hospital, Zhejiang University School of Medicine, Zhejiang Province, Hangzhou City, 310000, People’s Republic of China

    Liming Zheng

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  1. Wenhui Pei
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Contributions

Wenhui Pei, Yalikun Yusufu, and Yifei Zhan wrote the main manuscript text. Peng Wang, Liming Zheng, Kai Zhang, and Caoxing Huang conceived the idea and designed the research. Xucai Wang revised the manuscript. Jian Gan designed all the schematic diagram in this works. All authors reviewed the manuscript.

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Correspondence to Liming Zheng, Peng Wang, Kai Zhang or Caoxing Huang.

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Pei, W., Yusufu, Y., Zhan, Y. et al. Biosynthesizing lignin dehydrogenation polymer to fabricate hybrid hydrogel composite with hyaluronic acid for cartilage repair. Adv Compos Hybrid Mater 6, 180 (2023). https://doi.org/10.1007/s42114-023-00758-6

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