Production of Functional Materials Derived from Regenerated Silk Fibroin by Utilizing 3D Printing and Biomimetic Enzyme-induced Mineralization

Ni Chen; Fei-Yu Luo; Gong-Wen Yang; Jin-Rong Yao; Xin Chen; Zheng-Zhong Shao

doi:10.1007/s10118-023-3059-3

Your Location：

Home >

Browse articles >

Production of Functional Materials Derived from Regenerated Silk Fibroin by Utilizing 3D Printing and Biomimetic Enzyme-induced Mineralization

RESEARCH ARTICLE | Updated：2024-02-20

- Production of Functional Materials Derived from Regenerated Silk Fibroin by Utilizing 3D Printing and Biomimetic Enzyme-induced Mineralization
- Chinese Journal of Polymer Science Vol. 42, Issue 3, Pages: 299-310(2024)
- Affiliations：
  
  State Key Laboratory of Molecular Engineering of Polymers, Laboratory of Advanced Materials and Department of Macromolecular Science, Fudan University, Shanghai 200433, China
- Author bio：
  
  zzshao@fudan.edu.cn
- Funds：
- DOI：10.1007/s10118-023-3059-3
  CLC：
- Received：23 August 2023，
  
  Revised：2023-10-11，
  
  Accepted：12 October 2023，
  
  Online First：15 November 2023，
  
  Published：01 March 2024
- Accepted：
Scan QR Code
Chen, N.; Luo, F. Y.; Yang, G. W.; Yao, J. R.; Chen, X.; Shao, Z. Z. Production of functional materials derived from regenerated silk fibroin by utilizing 3D printing and biomimetic enzyme-induced mineralization. Chinese J. Polym. Sci. 2024, 42, 299–310

Ni Chen, Fei-Yu Luo, Gong-Wen Yang, et al. Production of Functional Materials Derived from Regenerated Silk Fibroin by Utilizing 3D Printing and Biomimetic Enzyme-induced Mineralization[J]. Chinese Journal of Polymer Science, 2024, 42(3): 299-310.
Chen, N.; Luo, F. Y.; Yang, G. W.; Yao, J. R.; Chen, X.; Shao, Z. Z. Production of functional materials derived from regenerated silk fibroin by utilizing 3D printing and biomimetic enzyme-induced mineralization. Chinese J. Polym. Sci. 2024, 42, 299–310 DOI： 10.1007/s10118-023-3059-3.

Ni Chen, Fei-Yu Luo, Gong-Wen Yang, et al. Production of Functional Materials Derived from Regenerated Silk Fibroin by Utilizing 3D Printing and Biomimetic Enzyme-induced Mineralization[J]. Chinese Journal of Polymer Science, 2024, 42(3): 299-310. DOI： 10.1007/s10118-023-3059-3.

摘要

The 3D-printed RSF-hydroxyapatite composite materials that were prepared through a two-step technique by integrating 3D printing technology and ALP-induced biomimetic mineralization

demonstrated a promising bone substitute material with intricate structure

adjustable compression modulus of megapascal grade and variable hydroxyapatite content.

Abstract

Critical-sized bone defects

commonly encountered in clinical orthopedic surgery

present a significant challenge. One of the promising solutions is to prepare synthetic bone substitute materials with precise structural control

mechanical compatibility

and enhanced osteogenic induction performance

nevertheless the successful preparation of such materials remains difficult. In this study

a two-step technique

integrating an extrusion-based printing process with biomimetic mineralization induced by alkaline phosphatase (ALP)

was developed. Initially

a pre-cured hydrogel of regenerated silk fibroin (RSF) with a small quantity of hydroxypropyl cellulose (HPC) and ALP was prepared through heating the mixed aqueous solution. This pre-cured hydrogel demonstrated thixotropic property and could be directly extruded into predetermined structures through a 3D-printer. Subsequently

the 3D-printed RSF-based materials with ALP underwent biomimetic

in situ

mineralization in calcium glycerophosphate (Ca-GP) mineralizing solution

utilizing the polymer chains of RSF as templates and ALP as a trigger for cleaving phosphate bonds of Ca-GP. The resulting 3D-printed RSF-mineral composites including hydrogel and sponge possessed adjustable compression modulus of megapascal grade and variable hydroxyapatite content

which could be controlled by manipulating the duration of the mineralization process. Moreover

these 3D-printed RSF-mineral composites demonstrated non-cytotoxicity towards rat bone marrow mesenchymal stem cells. Therefore

they may hold great potential for applications involving the replacement of tissues characterized by osteoinductivity and intricate structures.

关键词

Keywords

references

Chen,H.;Liu,Y.;Wang,C.;Zhang,A.;Chen,B.;Han,Q.;Wang,J.Designandpropertiesofbiomimeticirregularscaffoldsforbonetissueengineering. Comput. Biol. Med. 2021 , 130 ,104241..

Zhang,M.;Matinlinna,J.P.;Tsoi,J.K.H.;Liu,W.;Cui,X.;Lu,W.W.;Pan,H.Recentdevelopmentsinbiomaterialsforlong-bonesegmentaldefectreconstruction:anarrativeoverview. J. Orthop. Translat. 2020 , 22 ,26−33..

Liu,Y.H.;Liu,W.;Zheng,Z.L.;Wei,X.;Shah,N.A.;Lin,H.;Zhao,B.S.;Huang,S.S.;Xu,J.Z.;Li,Z.M.Fabricationofhighlyanisotropicandinterconnectedporousscaffoldstopromotepreosteoblastproliferationforbonetissueengineering. Chinese J. Polym. Sci. 2021 , 39 ,1191−1199..

Neovius,E.;Engstrand,T.Craniofacialreconstructionwithboneandbiomaterials:reviewoverthelast11years. J. Plast. Reconstr. Aesthet. Surg. 2010 , 63 ,1615−1623..

Lauthe,O.;Soubeyrand,M.;Babinet,A.;Dumaine,V.;Anract,P.;Biau,D.J.Theindicationsanddonor-sitemorbidityoftibialcorticalstrutautograftsinthemanagementofdefectsinlongbones. Bone Joint J . 2018 , 100-B ,67−674..

Han,J.;Wu,J.;Xiang,X.;Xie,L.;Chen,R.;Li,L.;Ma,K.;Sun,Q.;Yang,R.;Huang,T.;Tong,L.;Zhu,L.;Wang,H.;Wen,C.;Zhao,Y.;Wang,J.BiodegradableBBG/PCLcompositescaffoldsfabricatedbyselectivelasersinteringfordirectedregenerationofcritical-sizedbonedefects. Mater. Des. 2023 , 225 ,111543..

Stevens,M.M.Biomaterialsforbonetissueengineering. Mater. Today 2008 , 11 ,18−25..

Kumar,A.;Kargozar,S.;Baino,F.;Han,S.S.Additivemanufacturingmethodsforproducinghydroxyapatiteandhydroxyapatite-basedcompositescaffolds:areview. Front. Mater. 2019 , 6 ,313..

Ehret,C.;Aid,R.;DosSantos,B.P.;Rey,S.;Letourneur,D.;AmedeeVilamitjana,J.;deMones,E.Boneregenerationinsmallandlargesegmentalbonedefectmodelsafterradiotherapyusinginjectablepolymer-basedbiodegradablematerialscontainingstrontium-dopedhydroxyapatiteparticles. Int. J. Mol. Sci. 2023 , 24 ,5429..

Hu,J.;Cai,X.;Mo,S.B.;Chen,L.;Shen,X.Y.;Tong,H.Fabricationandcharacterizationofchitosan-silkfibroin/hydroxyapatitecomposites via in situ precipitationforbonetissueengineering. Chinese J. Polym. Sci. 2015 , 33 ,1661−1671..

Zhou,H.;Lee,J.Nanoscalehydroxyapatiteparticlesforbonetissueengineering. Acta Biomater. 2011 , 7 ,2769−2781..

Ma,P.X.Biomimeticmaterialsfortissueengineering. Adv. Drug Deliv. Rev. 2008 , 60 ,184−198..

Trakoolwannachai,V.;Kheolamai,P.;Ummartyotin,S.Characterizationofhydroxyapatitefromeggshellwasteandpolycaprolactone(PCL)compositeforscaffoldmaterial. Compos. B Eng. 2019 , 173 ,106974..

Yan,H.;Wang,Z.;Li,L.;Shi,X.;Jia,E.;Ji,Q.;Wang,Y.;Ito,Y.;Wei,Y.;Zhang,P.DOPA-derivedelectroactivecopolymerandIGF-1immobilizedpoly(lactic- co -glycolicacid)/hydroxyapatitebiodegradablemicrospheresforsynergisticbonerepair. Chem. Eng. J. 2021 , 416 ,129129..

Abouzeid,R.E.;Khiari,R.;Salama,A.;Diab,M.;Beneventi,D.;Dufresne,A.Insitumineralizationofnano-hydroxyapatiteonbifunctionalcellulosenanofiber/polyvinylalcohol/sodiumalginatehydrogelusing3Dprinting. Int. J. Biol. Macromol. 2020 , 160 ,538−547..

Chen,P.;Liu,L.;Pan,J.;Mei,J.;Li,C.;Zheng,Y.Biomimeticcompositescaffoldofhydroxyapatite/gelatin-chitosancore-shellnanofibersforbonetissueengineering. Mater. Sci. Eng. C Mater. Biol. Appl. 2019 , 97 ,325−335..

Kaushik,S.;Thungon,P.D.;Goswami,P.Silkfibroin:anemergingbiocompatiblematerialforapplicationofenzymesandwholecellsinbioelectronicsandbioanalyticalsciences. ACS Biomater. Sci. Eng. 2020 , 6 ,4337−4355..

Fang,G.;Huang,Y.;Tang,Y.;Qi,Z.;Yao,J.;Shao,Z.;Chen,X.Insightsintosilkformationprocess:correlationofmechanicalpropertiesandstructuralevolutionduringartificialspinningofsilkfibers. ACS Biomater. Sci. Eng. 2016 , 2 ,1992−2000..

Yang,G.;Gu,K.;Shao,Z.Theinvestigationfromanimalsilkstosilkprotein-basedmaterials. Acta Polymerica Sinica (inChinese) 2021 , 52 ,16−28..

Kim,H.;Che,L.;Ha,Y.;Ryu,W.Mechanically-reinforcedelectrospuncompositesilkfibroinnanofiberscontaininghydroxyapatitenanoparticles. Mater. Sci. Eng. C Mater. Biol. Appl. 2014 , 40 ,324−335..

Mi,R.;Liu,Y.;Chen,X.;Shao,Z.Structureandpropertiesofvarioushybridsfabricatedbysilknanofibrilsandnanohydroxyapatite. Nanoscale 2016 , 8 ,20096−20102..

Yan,Z.;Chen,W.;Jin,W.;Sun,Y.;Cai,J.;Gu,K.;Mi,R.;Chen,N.;Chen,S.;Shao,Z.Aninterferencescrewmadeusingasilkfibroin-basedbulkmaterialwithhighcontentofhydroxyapatiteforanteriorcruciateligamentreconstructioninarabbitmodel. J. Mater. Chem. B 2021 , 9 ,5352−5364..

Liu,X.;Yuk,H.;Lin,S.;Parada,G.A.;Tang,T.C.;Tham,E.;delaFuente-Nunez,C.;Lu,T.K.;Zhao,X.3Dprintingoflivingresponsivematerialsanddevices. Adv. Mater . 2018 , 30 ,1704821..

Xin,A.;Su,Y.;Feng,S.;Yan,M.;Yu,K.;Feng,Z.;HoonLee,K.;Sun,L.;Wang,Q.Growinglivingcompositeswithorderedmicrostructuresandexceptionalmechanicalproperties. Adv. Mater. 2021 , 33 ,e2006946..

Heveran,C.M.;Williams,S.L.;Qiu,J.;Artier,J.;Hubler,M.H.;Cook,S.M.;Cameron,J.C.;Srubar,W.V.Biomineralizationandsuccessiveregenerationofengineeredlivingbuildingmaterials. Matter 2020 , 2 ,481−494..

Hoffmann,C.;Zollfrank,C.;Ziegler,G.Enzyme-catalysedsynthesisofcalciumphosphates. J. Mater. Sci. Mater. Med. 2008 , 19 ,907−915..

Rauner,N.;Meuris,M.;Zoric,M.;Tiller,J.C.Enzymaticmineralizationgeneratesultrastiffandtoughhydrogelswithtunablemechanics. Nature 2017 , 543 ,407−410..

Douglas,T.E.;Messersmith,P.B.;Chasan,S.;Mikos,A.G.;deMulder,E.L.;Dickson,G.;Schaubroeck,D.;Balcaen,L.;Vanhaecke,F.;Dubruel,P.;Jasen,A.J.;Leeuwenburgh,S.C.G.Enzymaticmineralizationofhydrogelsforbonetissueengineeringbyincorporationofalkalinephosphatase. Macromol. Biosci. 2012 , 12 ,1077−1089..

Yao,R.;Zhang,B.;Gao,T.;Zhang,N.;Wang,Y.;Meng,G.;He,J.;Wu,F.Dopamineenhancesthemechanicalandbiologicalpropertiesofenzyme-inducedmineralizedhydrogels. J. Mater. Chem. B 2020 , 8 ,9052−9061..

Bose,S.;Vahabzadeh,S.;Bandyopadhyay,A.Bonetissueengineeringusing3Dprinting. Mater. Today 2013 , 16 ,496−504..

Gong,Z.;Huang,L.;Yang,Y.;Chen,X.;Shao,Z.Twodistinctbeta-sheetfibrilsfromsilkprotein. Chem. Commun . 2009 ,7506−7508..

Chen,G.;Liang,X.;Zhang,P.;Lin,S.;Cai,C.;Yu,Z.;Liu,J.Bioinspired3Dprintingoffunctionalmaterialsbyharnessingenzyme-inducedbiomineralization. Adv. Funct. Mater. 2022 , 32 ,2113262..

Gong,Z.;Yang,Y.;Ren,Q.;Chen,X.;Shao,Z.Injectablethixotropichydrogelcomprisingregeneratedsilkfibroinandhydroxypropylcellulose. Soft Matter 2012 , 8 ,2875−2883..

Dong,T.;Mi,R.;Wu,M.;Zhong,N.;Zhao,X.;Chen,X.;Shao,Z.Theregeneratedsilkfibroinhydrogelwithdesignedarchitecturebioprintedbyitsmicrohydrogel. J. Mater. Chem. B 2019 , 7 ,4328−4337..

Chen,N.;Zhang,X.;Lyu,J.;Zhao,G.;Gu,K.;Xia,J.;Chen,Z.;Shao,Z.Preparationofanovelregeneratedsilkfibroin-basedhydrogelforextrusionbioprinting. Soft Matter 2022 , 18 ,7360−7368..

Samal,S.K.;Dash,M.;Declercq,H.A.;Gheysens,T.;Dendooven,J.;VanDerVoort,P.;Cornelissen,R.;Dubruel,P.;Kaplan,D.L.Enzymaticmineralizationofsilkscaffolds. Macromol. Biosci. 2014 , 14 ,991−1003..

Su,D.;Yao,M.;Liu,J.;Zhong,Y.;Chen,X.;Shao,Z.EnhancingMechanicalPropertiesofSilkFibroinHydrogelthroughRestrictingtheGrowthofbeta-SheetDomains. ACS Appl. Mater. Interfaces 2017 , 9 ,17489−17498..

Rapacz-Kmita,A.;Paluszkiewicz,C.;Ślósarczyk,A.;Paszkiewicz,Z.FTIRandXRDinvestigationsonthethermalstabilityofhydroxyapatiteduringhotpressingandpressurelesssinteringprocesses. J. Mol. Struct . 2005 , 744−747 ,653−656..

Chen,X.;Shao,Z.;Marinkovic,N.S.;Miller,L.M.;Zhou,P.;Chance,M.R.Conformationtransitionkineticsofregenerated Bombyx morisilkfibroinmembranemonitoredbytime-resolvedFTIRspectroscopy. Biophys. Chem. 2001 , 89 ,25−34..

Li,Z.;Zheng,Z.;Yang,Y.;Fang,G.;Yao,J.;Shao,Z.;Chen,X.Robustproteinhydrogelsfromsilkwormsilk. ACS Sustainable Chem. Eng. 2016 , 4 ,1500−1506..

Rehman,I.;Bonfield,W.CharacterizationofhydroxyapatiteandcarbonatedapatitebyphotoacousticFTIRspectroscopy. J. Mater. Sci. Mater. Med. 1997 , 8 ,1−4..

Shepherd,D.E.;Seedhom,B.B.The'instantaneous'compressivemodulusofhumanarticularcartilageinjointsofthelowerlimb. Rheumatology 1999 , 38 ,124−132..

Gao,F.;Xu,Z.;Liang,Q.;Li,H.;Peng,L.;Wu,M.;Zhao,X.;Cui,X.;Ruan,C.;Liu,W.Osteochondralregenerationwith3D-printedbiodegradablehigh-strengthsupramolecularpolymerreinforced-gelatinhydrogelscaffolds. Adv. Sci. 2019 , 6 ,1900867..

Lujerdean,C.;Baci,G.M.;Cucu,A.A.;Dezmirean,D.S.Thecontributionofsilkfibroininbiomedicalengineering. Insects 2022 , 13 ,286..

Holland,C.;Numata,K.;Rnjak-Kovacina,J.;Seib,F.P.Thebiomedicaluseofsilk:past,present,future. Adv. Healthc. Mater. 2019 , 8 ,e1800465..

Da,G.;Ma,Y.;Lin,Q.;Shao,Z.Regeneratedsilkfibroinhydrogelwithlaponite/polydopaminecompositenanoparticles. Acta Polymerica Sinica (inChinese) 2023 , 54 ,95−105..

Chen,L.;Sun,L.;Liu,W.;Yao,J.;Shao,Z.;Zhao,B.;Chen,X.Long-lastingthixotropicnaturalpolymerichydrogelbasedonsilknanofibrils. ACS Biomater. Sci. Eng. 2023 , 9 ,4168−4177..

Saleem,M.;Rasheed,S.;Yougen,C.Silkfibroin/hydroxyapatitescaffold:ahighlycompatiblematerialforboneregeneration. Sci. Technol. Adv. Mater. 2020 , 21 ,242−266..

Bharadwaz,A.;Jayasuriya,A.C.Recenttrendsintheapplicationofwidelyusednaturalandsyntheticpolymernanocompositesinbonetissueregeneration. Mater. Sci. Eng. C Mater. Biol. Appl. 2020 , 110 ,110698..

Zhang,H.;You,R.;Yan,K.;Lu,Z.;Fan,Q.;Li,X.;Wang,D.Silkastemplatesforhydroxyapatitebiomineralization:acomparativestudyof Bombyx mori and Antheraea pernyi silkwormsilks. Int. J. Biol. Macromol. 2020 , 164 ,2842−2850..

Sotome,S.;Uemura,T.;Kikuchi,M.;Chen,J.;Itoh,S.;Tanaka,J.;Tateishi,T.;Shinomiya,K.Synthesisand in vivo evaluationofanovelhydroxyapatite/collagen-alginateasabonefillerandadrugdeliverycarrierofbonemorphogeneticprotein. Mater. Sci. Eng. C. 2004 , 24 ,341−347..

Views

343

Downloads

CSCD

Alert me when the article has been cited

Submit

Tools

Publicity Resources

The Silk Textile Embedded in Silk Fibroin Composite: Preparation and Properties

In Vivo Degradation Behavior of Porous Composite Scaffolds of Poly(lactide-co-glycolide) and Nano-hydroxyapatite Surface Grafted with Poly(L-lactide)

2026-9 Contents

Experimental Investigation of Graphene and TiO2 Reinforced Poly(vinyl alcohol)-based Fiber Metal Laminates

Squaramide-directed Cooperative One-dimensional Assembly in Telechelic Polydimethylsiloxane for Hierarchical Network Formation

Related Author

Xin Chen

Zheng-Zhong Shao

Yu Duan

Li-guo Cui

Pei-biao Zhang

Xue-si Chen

Yu Wang

Zong-liang Wang

Related Institution

State Key Laboratory of Molecular Engineering of Polymers, Department of Macromolecular Science, Laboratory of Advanced Materials, Fudan University

First Hospital, Jilin University

Key Laboratory of Polymer Ecobiomaterials, Changchun Institute of Applied Chemistry, Graduate School of Chinese Academy of Sciences, Chinese Academy of Sciences

⁰