Volume 9 Issue 2
May  2024
Turn off MathJax
Article Contents
Zongpu Xu, Fang He, Jing Yu, Zhangze Yang, Yu Zhu, Rong Liao, Ruyin Lyu, Mei Yang, Liangjun Zhu, Mingying Yang. From common biomass materials to high-performance tissue engineering scaffold: Biomimetic preparation, properties characterization, in vitro and in vivo evaluations[J]. Journal of Bioresources and Bioproducts, 2024, 9(2): 185-196. doi: 10.1016/j.jobab.2024.03.004
Citation: Zongpu Xu, Fang He, Jing Yu, Zhangze Yang, Yu Zhu, Rong Liao, Ruyin Lyu, Mei Yang, Liangjun Zhu, Mingying Yang. From common biomass materials to high-performance tissue engineering scaffold: Biomimetic preparation, properties characterization, in vitro and in vivo evaluations[J]. Journal of Bioresources and Bioproducts, 2024, 9(2): 185-196. doi: 10.1016/j.jobab.2024.03.004

From common biomass materials to high-performance tissue engineering scaffold: Biomimetic preparation, properties characterization, in vitro and in vivo evaluations

doi: 10.1016/j.jobab.2024.03.004
More Information
  • Corresponding author: E-mail address: xuzongpu@zju.edu.cn (Z. Xu)
  • Available Online: 2024-03-26
  • Publish Date: 2024-05-01
  • Converting common biomass materials to high-performance biomedical products could not only reduce the environmental pressure associated with the large-scale use of synthetic materials, but also increase the economic value. Chitosan as a very promising candidate has drawn considerable attention owing to its abundant sources and remarkable bioactivities. However, pure chitosan materials usually exhibit insufficient mechanical properties and excessive swelling ratio, which seriously affected their in vivo stability and integrity when applied as tissue engineering scaffolds. Thus, simultaneously improving the mechanical strength and biological compatibility of pure chitosan (CS) scaffolds becomes very important. Here, inspired by the fiber-reinforced construction of natural extracellular matrix and the porous structure of cancellous bone, we built silk microfibers/chitosan composite scaffolds via ice-templating technique. This biomimetic strategy achieved 500% of mechanical improvement to pure chitosan, and meanwhile still maintaining high porosity (> 87%). In addition, the increased roughness of chitosan pore walls by embedded silk microfibers significantly promoted cell adhesion and proliferation. More importantly, after subcutaneous implantation in mice for four weeks, the composite scaffold showed greater structural integrity, as well as better collagenation, angiogenesis, and osteogenesis abilities, suggesting its great potential in biomedicine.

     

  • Ethical statement
    All animal experiments in this study were performed in accordance with the guidelines and approval (ZJU20160383) of the Laboratory Animal Welfare Ethics Committee of Zhejiang University.
    Declaration of Competing Interest
    The authors declare no conflicts of interest.
    Supplementary materials
    Supplementary material associated with this article can be found, in the online version, at doi:10.1016/j.jobab.2024.03.004
  • loading
  • Ahmad Zamri, M.F.M., Bahru, R., Amin, R., Aslam Khan, M.U., Razak, S.I.A., Abu Hassan, S., Kadir, M.R.A., Nayan, N.H.M., 2021. Waste to health: a review of waste derived materials for tissue engineering. J. Clean. Prod. 290, 125792. doi: 10.1016/j.jclepro.2021.125792
    Ali Soliman, E., Furuta, M., 2014. Influence of phase behavior and miscibility on mechanical, thermal and micro-structure of soluble starch-gelatin thermoplastic biodegradable blend films. Food Nutr. Sci. 5, 1040–1055. http://www.cqvip.com/QK/72853X/201411/HS728532014011009.html
    Bojedla, S.S.R., Chameettachal, S., Yeleswarapu, S., Nikzad, M., Masood, S.H., Pati, F., 2022. Silk fibroin microfiber-reinforced polycaprolactone composites with enhanced biodegradation and biological characteristics. J. Biomed. Mater. Res. A 110, 1386–1400. doi: 10.1002/jbm.a.37380
    Bou-Francis, A., Piercey, M., Al-Qatami, O., Mazzanti, G., Khattab, R., Ghanem, A., 2020. Polycaprolactone blends for fracture fixation in low load-bearing applications. J. Appl. Polym. Sci. 137, 48940. doi: 10.1002/app.48940
    Cheng, N., Wang, Y.Q., Zhang, Y.F., Shi, B., 2013. The osteogenic potential of mesoporous bioglasses/silk and non-mesoporous bioglasses/silk scaffolds in ovariectomized rats: in vitro and in vivo evaluation. PLoS ONE 8, e81014. doi: 10.1371/journal.pone.0081014
    Collins, M.N., Ren, G., Young, K., Pina, S., Reis, R.L., Oliveira, J.M., 2021. Scaffold fabrication technologies and structure/function properties in bone tissue engineering. Adv. Funct. Mater. 31, 2010609. doi: 10.1002/adfm.202010609
    Costa-Pinto, A.R., Reis, R.L., Neves, N.M., 2011. Scaffolds based bone tissue engineering: the role of chitosan. Tissue Eng. Part B Rev. 17, 331–347. doi: 10.1089/ten.teb.2010.0704
    Cywar, R.M., Rorrer, N.A., Hoyt, C.B., Beckham, G.T., Chen, E.Y.X., 2022. Bio-based polymers with performance-advantaged properties. Nat. Rev. Mater. 7, 83–103. doi: 10.1038/s41578-021-00363-3
    Deepthi, S., Venkatesan, J., Kim, S.K., Bumgardner, J.D., Jayakumar, R., 2016. An overview of chitin or chitosan/nano ceramic composite scaffolds for bone tissue engineering. Int. J. Biol. Macromol. 93, 1338–1353. doi: 10.1016/j.ijbiomac.2016.03.041
    Demeyer, S., Athipornchai, A., Pabunrueang, P., Trakulsujaritchok, T., 2021. Development of mangiferin loaded chitosan-silica hybrid scaffolds: physicochemical and bioactivity characterization. Carbohydr. Polym. 261, 117905. doi: 10.1016/j.carbpol.2021.117905
    Doustdar, F., Olad, A., Ghorbani, M., 2022. Effect of glutaraldehyde and calcium chloride as different crosslinking agents on the characteristics of chitosan/cellulose nanocrystals scaffold. Int. J. Biol. Macromol. 208, 912–924. doi: 10.1016/j.ijbiomac.2022.03.193
    Fang, Y.C., Zhang, T., Song, Y., Sun, W., 2020. Assessment of various crosslinking agents on collagen/chitosan scaffolds for myocardial tissue engineering. Biomed. Mater. 15, 045003. doi: 10.1088/1748-605x/ab452d
    Felfel, R.M., Gideon-Adeniyi, M.J., Zakir Hossain, K.M., Roberts, G.A.F., Grant, D.M., 2019. Structural, mechanical and swelling characteristics of 3D scaffolds from chitosan-agarose blends. Carbohydr. Polym. 204, 59–67. doi: 10.1016/j.carbpol.2018.10.002
    Fernandez-Yague, M.A., Abbah, S.A., McNamara, L., Zeugolis, D.I., Pandit, A., Biggs, M.J., 2015. Biomimetic approaches in bone tissue engineering: integrating biological and physicomechanical strategies. Adv. Drug Deliv. Rev. 84, 1–29. doi: 10.1016/j.addr.2014.09.005
    Filippi, M., Born, G., Chaaban, M., Scherberich, A., 2020. Natural polymeric scaffolds in bone regeneration. Front. Bioeng. Biotechnol. 8, 474. doi: 10.3389/fbioe.2020.00474
    Geyer, R., Jambeck, J.R., Law, K.L., 2017. Production, use, and fate of all plastics ever made. Sci. Adv. 3, e1700782. doi: 10.1126/sciadv.1700782
    Gholap, A.D., Rojekar, S., Kapare, H.S., Vishwakarma, N., Raikwar, S., Garkal, A., Mehta, T.A., Jadhav, H., Prajapati, M.K., Annapure, U., 2024. Chitosan scaffolds: expanding horizons in biomedical applications. Carbohydr. Polym. 323, 121394. doi: 10.1016/j.carbpol.2023.121394
    Gu, Z.P., Xie, H.X., Huang, C.C., Li, L., Yu, X.X., 2013. Preparation of chitosan/silk fibroin blending membrane fixed with alginate dialdehyde for wound dressing. Int. J. Biol. Macromol. 58, 121–126. doi: 10.1016/j.ijbiomac.2013.03.059
    Guo, L.Q., Liang, Z.H., Yang, L., Du, W.Y., Yu, T., Tang, H.Y., Li, C.D., Qiu, H.B., 2021. The role of natural polymers in bone tissue engineering. J. Control. Release 338, 571–582. doi: 10.1016/j.jconrel.2021.08.055
    He, Y., Mu, C.Y., Shen, X.K., Yuan, Z., Liu, J., Chen, W.Z., Lin, C.C., Tao, B.L., Liu, B., Cai, K.Y., 2018. Peptide LL-37 coating on micro-structured titanium implants to facilitate bone formation in vivo via mesenchymal stem cell recruitment. Acta Biomater. 80, 412–424. doi: 10.1016/j.actbio.2018.09.036
    Islam, M.M., Shahruzzaman, M., Biswas, S., Nurus Sakib, M., Rashid, T.U., 2020. Chitosan based bioactive materials in tissue engineering applications-a review. Bioact. Mater. 5, 164–183. http://www.sciengine.com/doi/pdf/89FC411AABA7402C964C2B6925E8FB49
    Jambeck, J.R., Geyer, R., Wilcox, C., Siegler, T.R., Perryman, M., Andrady, A., Narayan, R., Law, K.L., 2015. Plastic waste inputs from land into the ocean. Science 347, 768–771. doi: 10.1126/science.1260352
    Jia, Z.R., Gong, J.L., Zeng, Y., Ran, J.H., Liu, J., Wang, K.F., Xie, C.M., Lu, X., Wang, J., 2021. Bioinspired conductive silk microfiber integrated bioelectronic for diagnosis and wound healing in diabetes. Adv. Funct. Mater. 31, 2010461. doi: 10.1002/adfm.202010461
    Kandelousi, P.S., Rabiee, S.M., Jahanshahi, M., Nasiri, F., 2019. The effect of bioactive glass nanoparticles on polycaprolactone/chitosan scaffold: melting enthalpy and cell viability. J. Bioact. Compat. Polym. 34, 97-111. doi: 10.1177/0883911518819109
    Kandil, H., Ekram, B., Abo-Zeid, M.A.M., 2023. Cytocompatibility of MG-63 osteosarcoma cells on chitosan/hydroxyapatite/lignin hybrid composite scaffold in vitro. Biomed. Mater. 18, 015002. doi: 10.1088/1748-605x/ac9f92
    Kim, I.Y., Seo, S.J., Moon, H.S., Yoo, M.K., Park, I.Y., Kim, B.C., Cho, C.S., 2008. Chitosan and its derivatives for tissue engineering applications. Biotechnol. Adv. 26, 1–21. doi: 10.1016/j.biotechadv.2007.07.009
    Levengood, S.L., Zhang, M.Q., 2014. Chitosan-based scaffolds for bone tissue engineering. J. Mater. Chem. B 2, 3161–3184. doi: 10.1039/c4tb00027g
    Li, D.W., Lei, X.H., He, F.L., He, J., Liu, Y.L., Ye, Y.J., Deng, X.D., Duan, E.K., Yin, D.C., 2017. Silk fibroin/chitosan scaffold with tunable properties and low inflammatory response assists the differentiation of bone marrow mesenchymal stem cells. Int. J. Biol. Macromol. 105, 584–597. doi: 10.1016/j.ijbiomac.2017.07.080
    Liu, H.R., Sun, Z.Y., Guo, C.C., 2022. Chemical modification of silk proteins: current status and future prospects. Adv. Fiber Mater. 4, 705–719. doi: 10.1007/s42765-022-00144-9
    Logith Kumar, R., KeshavNarayan, A., Dhivya, S., Chawla, A., Saravanan, S., Selvamurugan, N., 2016. A review of chitosan and its derivatives in bone tissue engineering. Carbohydr. Polym. 151, 172–188. doi: 10.1016/j.carbpol.2016.05.049
    Madni, A., Kousar, R., Naeem, N., Wahid, F., 2021. Recent advancements in applications of chitosan-based biomaterials for skin tissue engineering. J. Bioresour. Bioprod. 6, 11–25. doi: 10.1016/j.jobab.2021.01.002
    Maharjan, B., Park, J., Kaliannagounder, V.K., Awasthi, G.P., Joshi, M.K., Park, C.H., Kim, C.S., 2021. Regenerated cellulose nanofiber reinforced chitosan hydrogel scaffolds for bone tissue engineering. Carbohydr. Polym. 251, 117023. doi: 10.1016/j.carbpol.2020.117023
    Mandal, B.B., Grinberg, A., Gil, E.S., Panilaitis, B., Kaplan, D.L., 2012. High-strength silk protein scaffolds for bone repair. Proc. Natl. Acad. Sci. USA 109, 7699–7704. doi: 10.1073/pnas.1119474109
    Matsiko, A., Gleeson, J.P., O'Brien, F.J., 2015. Scaffold mean pore size influences mesenchymal stem cell chondrogenic differentiation and matrix deposition. Tissue Eng. Part A 21, 486–497. doi: 10.1089/ten.tea.2013.0545
    Melchels, F.P.W., Tonnarelli, B., Olivares, A.L., Martin, I., Lacroix, D., Feijen, J., Wendt, D.J., Grijpma, D.W., 2011. The influence of the scaffold design on the distribution of adhering cells after perfusion cell seeding. Biomaterials 32, 2878–2884. doi: 10.1016/j.biomaterials.2011.01.023
    Melke, J., Midha, S., Ghosh, S., Ito, K., Hofmann, S., 2016. Silk fibroin as biomaterial for bone tissue engineering. Acta Biomater. 31, 1–16. doi: 10.1016/j.actbio.2015.09.005
    Mirjalili, F., Mahmoodi, M., Khazali, S., 2024. Characterization and in vitro bioactivity evaluation of polyvinyl alcohol incorporated electro spun chitosan/fluor apatite nanofibrous scaffold for bone tissue engineering. J. Mech. Behav. Biomed. Mater. 150, 106322. doi: 10.1016/j.jmbbm.2023.106322
    Mohammadi, Z., Mesgar, A.S.M., Rasouli-Disfani, F., 2016. Reinforcement of freeze-dried chitosan scaffolds with Multiphasic calcium phosphate short fibers. J. Mech. Behav. Biomed. Mater. 61, 590–599. doi: 10.1016/j.jmbbm.2016.04.022
    Mohanty, A.K., Vivekanandhan, S., Pin, J.M., Misra, M., 2018. Composites from renewable and sustainable resources: challenges and innovations. Science 362, 536–542. doi: 10.1126/science.aat9072
    Mohebbi, S., Nezhad, M.N., Zarrintaj, P., Jafari, S.H., Gholizadeh, S.S., Saeb, M.R., Mozafari, M., 2019. Chitosan in biomedical engineering: a critical review. Curr. Stem Cell Res. Ther. 14, 93–116. doi: 10.2174/1574888x13666180912142028
    Pina, S., Oliveira, J.M., Reis, R.L., 2015. Natural-based nanocomposites for bone tissue engineering and regenerative medicine: a review. Adv. Mater. 27, 1143–1169. doi: 10.1002/adma.201403354
    Pohling, J., Hawboldt, K., Dave, D., 2022. Comprehensive review on pre-treatment of native, crystalline chitin using non-toxic and mechanical processes in preparation for biomaterial applications. Green Chem. 24, 6790–6809. doi: 10.1039/d2gc01968j
    Preethi Soundarya, S., Haritha Menon, A., Viji Chandran, S., Selvamurugan, N., 2018. Bone tissue engineering: scaffold preparation using chitosan and other biomaterials with different design and fabrication techniques. Int. J. Biol. Macromol. 119, 1228–1239. doi: 10.1016/j.ijbiomac.2018.08.056
    Qiao, Z.G., Lian, M.F., Han, Y., Sun, B.B., Zhang, X., Jiang, W.B., Li, H.W., Hao, Y.Q., Dai, K.R., 2021. Bioinspired stratified electrowritten fiber-reinforced hydrogel constructs with layer-specific induction capacity for functional osteochondral regeneration. Biomaterials 266, 120385. doi: 10.1016/j.biomaterials.2020.120385
    Rajabi, M., McConnell, M., Cabral, J., Ali, M.A., 2021. Chitosan hydrogels in 3D printing for biomedical applications. Carbohydr. Polym. 260, 117768. doi: 10.1016/j.carbpol.2021.117768
    Sánchez-Cardona, Y., Echeverri-Cuartas, C.E., Londoño López, M.E., Moreno-Castellanos, N., 2021. Chitosan/gelatin/PVA scaffolds for beta pancreatic cell culture. Polymers 13, 2372. doi: 10.3390/polym13142372
    Sanz-Fraile, H., Amoros, S., Mendizabal, I., Galvez-Monton, C., Prat-Vidal, C., Bayes-Genis, A., Navajas, D., Farre, R., Otero, J., 2020. Silk-reinforced collagen hydrogels with raised multiscale stiffness for mesenchymal cells 3D culture. Tissue Eng. Part A 26, 358–370. doi: 10.1089/ten.tea.2019.0199
    Saravanan, S., Leena, R.S., Selvamurugan, N., 2016. Chitosan based biocomposite scaffolds for bone tissue engineering. Int. J. Biol. Macromol. 93, 1354–1365. doi: 10.1016/j.ijbiomac.2016.01.112
    Shao, G.F., Hanaor, D.A.H., Shen, X.D., Gurlo, A., 2020. Freeze casting: from low-dimensional building blocks to aligned porous structures-a review of novel materials, methods, and applications. Adv. Mater. 32, e1907176. doi: 10.1002/adma.201907176
    Shi, L.Y., Wang, F.L., Zhu, W., Xu, Z.P., Fuchs, S., Hilborn, J., Zhu, L.J., Ma, Q., Wang, Y.J., Weng, X.S., Ossipov, D.A., 2017. Self-healing silk fibroin-based hydrogel for bone regeneration: dynamic metal-ligand self-assembly approach. Adv. Funct. Mater. 27, 1700591. doi: 10.1002/adfm.201700591
    Shuai, Y.J., Lu, H., Lv, R.Y., Wang, J., Wan, Q., Mao, C.B., Yang, M.Y., 2021. Biomineralization directed by prenucleated calcium and phosphorus nanoclusters improving mechanical properties and osteogenic potential of Antheraea pernyi silk fibroin-based artificial periosteum. Adv. Healthc. Mater. 10, e2001695. doi: 10.1002/adhm.202001695
    Sionkowska, A., Płanecka, A., 2013. Preparation and characterization of silk fibroin/chitosan composite sponges for tissue engineering. J. Mol. Liq. 178, 5–14. doi: 10.1016/j.molliq.2012.10.042
    Sultankulov, B., Berillo, D., Sultankulova, K., Tokay, T., Saparov, A., 2019. Progress in the development of chitosan-based biomaterials for tissue engineering and regenerative medicine. Biomolecules 9, 470. doi: 10.3390/biom9090470
    Tuwalska, A., Grabska-Zielińska, S., Sionkowska, A., 2022. Chitosan/silk fibroin materials for biomedical applications-a review. Polymers 14, 1343. doi: 10.3390/polym14071343
    Vinod, A., Sanjay, M.R., Suchart, S., Jyotishkumar, P., 2020. Renewable and sustainable biobased materials: an assessment on biofibers, biofilms, biopolymers and biocomposites. J. Clean. Prod. 258, 120978. doi: 10.1016/j.jclepro.2020.120978
    Vishwanath, V., Pramanik, K., Biswas, A., 2016. Optimization and evaluation of silk fibroin-chitosan freeze-dried porous scaffolds for cartilage tissue engineering application. J. Biomater. Sci. Polym. Ed. 27, 657–674. doi: 10.1080/09205063.2016.1148303
    Xiao, W.Q., Tan, Y.F., Li, J.L., Gu, C.F., Li, H., Li, B., Liao, X.L., 2018. Fabrication and characterization of silk microfiber-reinforced methacrylated gelatin hydrogel with turnable properties. J. Biomater. Sci. Polym. Ed. 29, 2068–2082. doi: 10.1080/09205063.2018.1493022
    Xu, H., Ge, Y.W., Lu, J.W., Ke, Q.F., Liu, Z.Q., Zhu, Z.N., Guo, Y.P., 2018. Icariin loaded-hollow bioglass/chitosan therapeutic scaffolds promote osteogenic differentiation and bone regeneration. Chem. Eng. J. 354, 285–294. doi: 10.1016/j.cej.2018.08.022
    Xu, Y.X., Xia, D.D., Han, J.M., Yuan, S.P., Lin, H., Zhao, C., 2017. Design and fabrication of porous chitosan scaffolds with tunable structures and mechanical properties. Carbohydr. Polym. 177, 210–216. doi: 10.1080/02670844.2016.1202672
    Xu, Z.P., Shi, L.Y., Hu, D.D., Hu, B.H., Yang, M.Y., Zhu, L.J., 2016. Formation of hierarchical bone-like apatites on silk microfiber templates via biomineralization. RSC Adv. 6, 76426–76433. doi: 10.1039/C6RA17199K
    Xu, Z.P., Shi, L.Y., Yang, M.Y., Zhang, H.P., Zhu, L.J., 2015. Fabrication of a novel blended membrane with chitosan and silk microfibers for wound healing: characterization, in vitro and in vivo studies. J. Mater. Chem. B 3, 3634–3642.
    Yang, M.Y., Shuai, Y.J., Sunderland, K.S., Mao, C.B., 2017. Ice-templated protein nanoridges induce bone tissue formation. Adv. Funct. Mater. 27, 1703726. http://pubmed.ncbi.nlm.nih.gov/29657571/
    Yang, Y.T., Du, Y.Z., Zhang, J., Zhang, H.L., Guo, B.L., 2022. Structural and functional design of electrospun nanofibers for hemostasis and wound healing. Adv. Fiber Mater. 4, 1027–1057. doi: 10.1007/s42765-022-00178-z
    Younes, I., Rinaudo, M., 2015. Chitin and chitosan preparation from marine sources. Structure, properties and applications. Mar. Drugs 13, 1133–1174. doi: 10.3390/md13031133
    Zhang, R.J., Chang, S.J., Jing, Y.Z., Wang, L.Y., Chen, C.J., Liu, J.T., 2023. Application of chitosan with different molecular weights in cartilage tissue engineering. Carbohydr. Polym. 314, 120890. doi: 10.1016/j.carbpol.2023.120890
    Zhao, W.G., Cao, S.Y., Cai, H.X., Wu, Y., Pan, Q., Lin, H., Fang, J., He, Y.Y., Deng, H.B., Liu, Z.H., 2022. Chitosan/silk fibroin biomimic scaffolds reinforced by cellulose acetate nanofibers for smooth muscle tissue engineering. Carbohydr. Polym. 298, 120056.
    Zhou, C.Z., Confalonieri, F., Jacquet, M., Perasso, R., Li, Z.G., Janin, J., 2001. Silk fibroin: structural implications of a remarkable amino acid sequence. Proteins 44, 119–122.
    Zhou, M.L., Wu, X.L., Luo, J.X., Yang, G.Z., Lu, Y.Z., Lin, S.H., Jiang, F., Zhang, W.J., Jiang, X.Q., 2021. Copper peptide-incorporated 3D-printed silk-based scaffolds promote vascularized bone regeneration. Chem. Eng. J. 422, 130147. http://www.sciencedirect.com/science/article/pii/S1385894721017320
    Zhou, X.J., Wang, Z.J., Li, T., Liu, Z.L., Sun, X., Wang, W.Z., Chen, L., He, C.L., 2023. Enhanced tissue infiltration and bone regeneration through spatiotemporal delivery of bioactive factors from polyelectrolytes modified biomimetic scaffold. Mater. Today Bio 20, 100681. doi: 10.1016/j.mtbio.2023.100681
  • 加载中

Catalog

    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Figures(7)

    Article Metrics

    Article views (208) PDF downloads(5) Cited by()
    Proportional views
    Related

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return