Biosynthesizing lignin dehydrogenation polymer to fabricate hybrid hydrogel composite with hyaluronic acid for cartilage repair
Tóm tắt
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. Bioenzymatically synthesized lignin dehydrogenation polymers to hybridize with hyaluronic acid to prepare hydrogel composites for promoting cartilage defect repair.
Tài liệu tham khảo
Yang S, Shi C, Qu K, Sun Z, Li H, Xu B, Huang Z, Guo Z (2023) Electrostatic self-assembly cellulose nanofibers/MXene/nickel chains for highly stable and efficient seawater evaporation and purification. Carbon Lett. https://doi.org/10.1007/s42823-023-00540-0
Ruan J, Chang Z, Rong H, Alomar TS, Zhu D, AlMasoud N, Liao Y, Zhao R, Zhao X, Li Y, Xu B, Guo Z, El-Bahy ZM, Li H, Zhang X, Ge S (2023) High-conductivity nickel shells encapsulated wood-derived porous carbon for improved electromagnetic interference shielding. Carbon 213:118208. https://doi.org/10.1016/j.carbon.2023.118208
Lian M, Huang Y, Liu Y, Jiang D, Wu Z, Li B, Xu Q, Murugadoss V, Jiang Q, Huang M, Guo Z (2022) An overview of regenerable wood-based composites: preparation and applications for flame retardancy, enhanced mechanical properties, biomimicry, and transparency energy saving. Adv Compos Hybrid Mater 5:1612–1657. https://doi.org/10.1007/s42114-022-00475-6
Wang X, Shen Y, Xu S, Huang C, Lai C, Yong Q, Chu F, Algadi H, Zhang D, Lu C, Wang J (2023) Lignin in situ self-assembly facilitates biomimetic multiphase structure for fabricating ultra-strong and tough ionic conductors for wearable pressure and strain sensors. Adv Compos Hybrid Mater 6(3):84. https://doi.org/10.1007/s42114-023-00658-9
Lai C, Jia Y, Yang C, Chen L, Shi H, Yong Q (2020) Incorporating lignin into polyethylene glycol enhanced its performance for promoting enzymatic hydrolysis of hardwood. ACS Sustain Chem Eng 8(4):1797–1804. https://doi.org/10.1021/acssuschemeng.9b05724
Zheng L, Lu G, Pei W, Yan W, Li Y, Zhang L, Huang C, Jiang Q (2021) Understanding the relationship between the structural properties of lignin and their biological activities. Int J Biol Macromol 190:291–300. https://doi.org/10.1016/j.ijbiomac.2021.08.168
Deng J, Gu J, Zhao X, Yan B, Wang L, Ji G, Huang C (2023) Improving the protective ability of lignin against vascular and neurological development in BPAF-induced zebrafish by high-pressure homogenization technology. Int J Biol Macromol 231:123356. https://doi.org/10.1016/j.ijbiomac.2023.123356
Pei W, Deng J, Wang P, Wang X, Zheng L, Zhang Y, Huang C (2022) Sustainable lignin and lignin-derived compounds as potential therapeutic agents for degenerative orthopaedic diseases: A systemic review. Int J Biol Macromol 212:547–560. https://doi.org/10.1016/j.ijbiomac.2022.05.152
Lu Z, Liu S, Le Y, Qin Z, He M, Xu F, Zhu Y, Zhao J, Mao C, Zheng L (2019) An injectable collagen-genipin-carbon dot hydrogel combined with photodynamic therapy to enhance chondrogenesis. Biomaterials 218:119190. https://doi.org/10.1016/j.biomaterials.2019.05.001
Abbina S, Vappala S, Kumar P, Siren EMJ, La CC, Abbasi U, Brooks DE, Kizhakkedathu JN (2017) Hyperbranched polyglycerols: recent advances in synthesis, biocompatibility and biomedical applications. J Mater Chem B 5:9249–9277. https://doi.org/10.1039/c7tb02515g
Wei X, Cui S, Xie Y (2022) Synthesis and antibacterial properties of oligomeric dehydrogenation polymer from lignin precursors. Molecules 27(5):1466. https://doi.org/10.3390/molecules27051466
Ullah I, Chen Z, Xie Y, Khan SS, Singh S, Yu C, Cheng G (2022) Recent advances in biological activities of lignin and emerging biomedical applications: a short review. Int J Biol Macromol 208:819–832. https://doi.org/10.1016/j.ijbiomac.2022.03.182
Xie Y, Jiang C, Chen X, Wu H, Bi S (2020) Preparation of oligomeric phenolic compounds (DHPs) from coniferin and syringin and characterization of their anticancer properties. Bioresources 15:1791–1809. https://doi.org/10.15376/biores.15.1.1791-1809
Liang R, Zhao J, Li B, Cai P, Loh XJ, Xu C, Cheng P, Kai D, Zheng L (2020) Implantable and degradable antioxidant poly (ε-caprolactone)-lignin nanofiber membrane for effective osteoarthritis treatment. Biomaterials 230:119601. https://doi.org/10.1016/j.biomaterials.2019.119601
Guo X, Ma Y, Min Y, Sun J, Shi X, Gao G, Sun L, Wang J (2023) Progress and prospect of technical and regulatory challenges on tissue-engineered cartilage as therapeutic combination product. Bioact Mater 20:501–518. https://doi.org/10.1016/j.bioactmat.2022.06.015
Liu J, Chen E, Wu Y, Yang H, Huang K, Chang G, Pan X, Huang K, He Z, Lei M (2022) Silver nanosheets doped polyvinyl alcohol hydrogel piezoresistive bifunctional sensor with a wide range and high resolution for human motion detection. Adv Compos Hybrid Mater 5:1196–1205. https://doi.org/10.1007/s42114-022-00472-9
Wu Y, Chen E, Weng X, He Z, Chang G, Pan X, Liu J, Huang K, Huang K, Lei M (2022) Conductive polyvinyl alcohol/silver nanoparticles hydrogel sensor with large draw ratio, high sensitivity and high stability for human behavior monitoring. Eng Sci 18:113–120. https://doi.org/10.30919/es8d659
Cheng K, Zou L, Chang B, Liu X, Shi H, Li T, Yang Q, Guo Z, Liu C, Shen C (2022) Mechanically robust and conductive poly(acrylamide) nanocomposite hydrogel by the synergistic effect of vinyl hybrid silica nanoparticle and polypyrrole for human motion sensing. Adv Compos Hybrid Mater 5:2834–2846. https://doi.org/10.1007/s42114-022-00465-8
Sidheekha MP, Shabeeba A, Rajan L, Thayyil MS, Ismail YA (2023) Conducting polymer/hydrogel hybrid free-standing electrodes for flexible supercapacitors capable of self-sensing working conditions: large-scale fabrication through facile and low-cost route. Eng Sci 23:890. https://doi.org/10.30919/es890
Li T, Wei H, Zhang Y, Wan T, Cui D, Zhao S, Zhang T, Ji Y, Algadi H, Guo Z, Chu L, Cheng B (2023) Sodium alginate reinforced polyacrylamide/xanthan gum double network ionic hydrogels for stress sensing and self-powered wearable device applications. Carbohydr Polym 309:120678. https://doi.org/10.1016/j.carbpol.2023.120678
Tang S, Chi K, Xu H, Yong Q, Yang J, Catchmark JM (2021) A covalently cross-linked hyaluronic acid/bacterial cellulose composite hydrogel for potential biological applications. Carbohydr Polym 252:117123. https://doi.org/10.1016/j.carbpol.2020.117123
Huang C, He J, Narron R, Wang Y, Yong Q (2017) Characterization of kraft lignin fractions obtained by sequential ultrafiltration and their potential application as a biobased component in blends with polyethylene. ACS Sustain Chem Eng 5:11770–11779. https://doi.org/10.1021/acssuschemeng.7b03415
Guerra A, Filpponen I, Lucia LA, Argyropoulos DS (2006) Comparative evaluation of three lignin isolation protocols for various wood species. J Agric Food Chem 54(26):9696–9705. https://doi.org/10.1021/jf062433c
Wei X, Liu Y, Luo Y, Shen Z, Wang S, Li M, Zhang L (2021) Effect of organosolv extraction on the structure and antioxidant activity of eucalyptus kraft lignin. Int J Biol Macromol 187:462–470. https://doi.org/10.1016/j.ijbiomac.2021.07.082
Wang S, Shen Q, Su S, Lin J, Song G (2022) The temptation from homogeneous linear catechyl lignin. Trends Chem 4:948–961. https://doi.org/10.1016/j.trechm.2022.07.008
Yang G, An X, Yang S (2021) The effect of ball milling time on the isolation of lignin in the cell wall of different biomass. Front Bioeng Biotechnol 9:807625. https://doi.org/10.3389/fbioe.2021.807625
Ran F, Li C, Hao Z, Zhang X, Dai L, Si C, Shen Z, Qiu Z, Wang J (2022) Combined bactericidal process of lignin and silver in a hybrid nanoparticle on E. coli. Adv Compos Hybrid Mater 5:1841–1851. https://doi.org/10.1007/s42114-022-00460-z
Mu L, Dong Y, Li L, Gu X, Shi Y (2021) Achieving high value utilization of bio-oil from lignin targeting for advanced lubrication. Eng Sci 11:72–80. https://doi.org/10.30919/esmm5f1146
Culebras M, Collins GA, Beaucamp A, Geaney H, Collins MN (2022) Lignin/Si hybrid carbon nanofibers towards highly efficient sustainable Li-ion anode materials. Eng Sci 17:195–203. https://doi.org/10.30919/es8d608
Yang W, Fortunati E, Gao D, Balestra GM, Giovanale G, He X, Torre L, Kenny JM, Puglia D (2018) Valorization of acid isolated high yield lignin nanoparticles as innovative antioxidant/antimicrobial organic materials. ACS Sustain Chem Eng 6:3502–3514. https://doi.org/10.1021/acssuschemeng.7b03782
Mendes L, de Freitas V, Baptista P, Carvalho M (2011) Comparative antihemolytic and radical scavenging activities of strawberry tree (Arbutus unedo L.) leaf and fruit. Food Chem Toxicol 49:2285–2291. https://doi.org/10.1016/j.fct.2011.06.028
Dandona P, Ghanim H, Brooks DP (2007) Antioxidant activity of carvedilol in cardiovascular disease. J Hypertens 25:731–741. https://doi.org/10.1097/HJH.0b013e3280127948
Sun Y, Yuan Y, Wu W, Lei L, Zhang L (2021) The effects of locomotion on bone marrow mesenchymal stem cell fate: insight into mechanical regulation and bone formation. Cell Biosci 11:88. https://doi.org/10.1186/s13578-021-00601-9
Toosi S, Naderi-Meshkin H, Kalalinia F, Peivandi MT, Khani HH, Bahrami AR, Heirani-Tabasi A, Mirahmadi M, Behravan J (2016) Comparative characteristics of mesenchymal stem cells derived from reamer-irrigator-aspirator, iliac crest bone marrow, and adipose tissue. Cell Mol Biol 62:68–74. https://doi.org/10.14715/cmb/2016.62.10.11
Irawan V, Sung TC, Higuchi A, Ikoma T (2018) Collagen scaffolds in cartilage tissue engineering and relevant approaches for future development. Tissue Eng Regen Med 15:673–697. https://doi.org/10.1007/s13770-018-0135-9
Bai Y, Gong X, Dou C, Cao Z, Dong S (2019) Redox control of chondrocyte differentiation and chondrogenesis. Free Radic Biol Med 132:83–89. https://doi.org/10.1016/j.freeradbiomed.2018.10.443
Heywood HK, Lee DA (2017) Bioenergetic reprogramming of articular chondrocytes by exposure to exogenous and endogenous reactive oxygen species and its role in the anabolic response to low oxygen. J Tissue Eng Regen Med 11:2286–2294. https://doi.org/10.1002/term.2126
Kim KS, Choi HW, Yoon HE, Kim IY (2010) Reactive oxygen species generated by NADPH oxidase 2 and 4 are required for chondrogenic differentiation. J Biol Chem 285:40294–40302. https://doi.org/10.1074/jbc.M110.126821
He S, Liu A, Zhang J, Liu J, Shao W (2022) Preparation of ε-polylysine and hyaluronic acid self-assembled microspheres loaded bacterial cellulose aerogels with excellent antibacterial activity. Colloid Surface A 654:130114. https://doi.org/10.1016/j.colsurfa.2022.130114
Serafin A, Culebras M, Oliveira JM, Koffler J, Collins MN (2023) 3D printable electroconductive gelatin-hyaluronic acid materials containing polypyrrole nanoparticles for electroactive tissue engineering. Adv Compos Hybrid Mater 6:109. https://doi.org/10.1007/s42114-023-00665-w
Liu K, Liu W, Li W, Duan Y, Zhou K, Zhang S, Ni S, Xu T, Si C (2022) Strong and highly conductive cellulose nanofibril/silver nanowires nanopaper for high performance electromagnetic interference shielding. Adv Compos Hybrid Mater 5(2):1078–1089. https://doi.org/10.1007/s42114-022-00425-2
Zhu EQ, Xu GF, Sun SF, Yang J, Yang HY, Wang DW, Guo ZH, Shi ZJ, Deng J (2021) Rosin acid modification of bamboo powder and thermoplasticity of its products based on hydrothermal pretreatment. Adv Compos Hybrid Mater 4:584–590. https://doi.org/10.1007/s42114-021-00266-5
Li Q, Gao Z, Chen Y, Guan MX (2017) The role of mitochondria in osteogenic, adipogenic and chondrogenic differentiation of mesenchymal stem cells. Protein Cell 8:439–445. https://doi.org/10.1007/s13238-017-0385-7
Maceda A, Terrazas T (2022) Fluorescence microscopy methods for the analysis and characterization of lignin. Polymers 14(5):961. https://doi.org/10.3390/polym14050961
Wang X, Zhang Y, Luo J, Xu T, Si C, Oscanoa AJC, Tang D, Zhu L, Wang P, Huang C (2023) Printability of hybridized composite from maleic acid-treated bacterial cellulose with gelatin for bone tissue regeneration. Adv Compos Hybrid Mater 6:134. https://doi.org/10.1007/s42114-023-00711-7
Liu L, Bai L, Tripathi A, Yu J, Wang Z, Borghei M, Fan Y, Rojas OJ (2019) High axial ratio nanochitins for ultrastrong and shape-recoverable hydrogels and cryogels via ice templating. ACS Nano 13:2927–2935. https://doi.org/10.1021/acsnano.8b07235
Pan P, Geng Y, Hu L, Liu Q, Liu M, Cheng M, Chen L, Chen J (2022) Biologically enhanced 3D printed micro-nano hybrid scaffolds doped with abalone shell for bone regeneration. Adv Compos Hybrid Mater 6:10. https://doi.org/10.1007/s42114-022-00593-1
Bian L, Zhai DY, Mauck RL, Burdick JA (2011) Coculture of human mesenchymal stem cells and articular chondrocytes reduces hypertrophy and enhances functional properties of engineered cartilage. Tissue Eng Part A 17:1137–1145. https://doi.org/10.1089/ten.TEA.2010.0531
Korhonen RK, Laasanen MS, Toyras J, Rieppo J, Hirvonen J, Helminen HJ, Jurvelin JS (2002) Comparison of the equilibrium response of articular cartilage in unconfined compression, confined compression and indentation. J Biomech 35:903–909. https://doi.org/10.1016/S0021-9290(02)00052-0
Lee F, Chung JE, Kurisawa M (2009) An injectable hyaluronic acid-tyramine hydrogel system for protein delivery. J Control Release 134:186–193. https://doi.org/10.1016/j.jconrel.2008.11.028
Chen K, Chen X, Han X, Fu Y (2020) A comparison study on the release kinetics and mechanism of bovine serum albumin and nanoencapsulated albumin from hydrogel networks. Int J Biol Macromol 163:1291–1300. https://doi.org/10.1016/j.ijbiomac.2020.07.043
Qiao Z, Tang J, Yue B, Wang J, Zhang J, Xuan L, Dai C, Li S, Li M, Xu C, Dai K, Wang Y (2020) Human adipose-derived mesenchymal progenitor cells plus microfracture and hyaluronic acid for cartilage repair: a Phase IIa trial. Future Med 15:1193–1214. https://doi.org/10.2217/rme-2019-0068
Yan L, Liu G, Wu X (2021) The umbilical cord mesenchymal stem cell-derived exosomal lncRNA H19 improves osteochondral activity through miR-29b-3p/FoxO3 axis. Clin Transl Med 11:e255. https://doi.org/10.1002/ctm2.255
Liang R, Yang X, Yew PYM, Sugiarto S, Zhu Q, Zhao J, Loh XJ, Zheng L, Kai D (2022) PLA-lignin nanofibers as antioxidant biomaterials for cartilage regeneration and osteoarthritis treatment. J Nanobiotechnology 20:327. https://doi.org/10.1186/s12951-022-01534-2