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ORIGINAL RESEARCH

Sericin/Nano-Hydroxyapatite Hydrogels Based on Graphene Oxide for Effective Bone Regeneration via Immunomodulation and Osteoinduction

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Pages 1875-1895 | Received 07 Dec 2022, Accepted 05 Apr 2023, Published online: 06 Apr 2023

References

  • Zhao C, Liu W, Zhu M, Wu C, Zhu Y. Bioceramic-based scaffolds with antibacterial function for bone tissue engineering: a review. Bioact Mater. 2022;18:383–398.
  • Niu Y, Wang Z, Shi Y, Dong L, Wang C. Modulating macrophage activities to promote endogenous bone regeneration: biological mechanisms and engineering approaches. Bioact Mater. 2021;6:244–261. doi:10.1016/j.bioactmat.2020.08.012
  • Bose S, Sarkar N. Natural medicinal compounds in bone tissue engineering. Trends Biotechnol. 2020;38:404–417. doi:10.1016/j.tibtech.2019.11.005
  • Zhang L, Yang G, Johnson BN, Jia X. Three-dimensional (3D) printed scaffold and material selection for bone repair. Acta Biomater. 2019;84:16–33. doi:10.1016/j.actbio.2018.11.039
  • Hao Z, Li H, Wang Y, et al. Supramolecular peptide nanofiber hydrogels for bone tissue engineering: from multihierarchical fabrications to comprehensive applications. Adv Sci. 2022;9:e2103820. doi:10.1002/advs.202103820
  • Martin KE, García AJ. Macrophage phenotypes in tissue repair and the foreign body response: implications for biomaterial-based regenerative medicine strategies. Acta Biomater. 2021;133:4–16. doi:10.1016/j.actbio.2021.03.038
  • Mestres G, Carter SD, Hailer NP, Diez-Escudero A. A practical guide for evaluating the osteoimmunomodulatory properties of biomaterials. Acta Biomater. 2021;130:115–137. doi:10.1016/j.actbio.2021.05.038
  • Xie Y, Hu C, Feng Y, et al. Osteoimmunomodulatory effects of biomaterial modification strategies on macrophage polarization and bone regeneration. Regener Biomater. 2020;7:233–245. doi:10.1093/rb/rbaa006
  • Zhu Y, Liang H, Liu X, et al. Regulation of macrophage polarization through surface topography design to facilitate implant-to-bone osteointegration. Sci Adv. 2021;7:eabf6654. doi:10.1126/sciadv.abf6654
  • Sadowska JM, Ginebra MP. Inflammation and biomaterials: role of the immune response in bone regeneration by inorganic scaffolds. J Mater Chem B. 2020;8:9404–9427. doi:10.1039/D0TB01379J
  • Fan L, Guan P, Xiao C, et al. Exosome-functionalized polyetheretherketone-based implant with immunomodulatory property for enhancing osseointegration. Bioact Mater. 2021;6:2754–2766. doi:10.1016/j.bioactmat.2021.02.005
  • Patel DK, Dutta SD, Hexiu J, Ganguly K, Lim KT. 3D-printable chitosan/silk fibroin/cellulose nanoparticle scaffolds for bone regeneration via M2 macrophage polarization. Carbohydr Polym. 2022;281:119077. doi:10.1016/j.carbpol.2021.119077
  • Wang T, Bai J, Lu M, et al. Engineering immunomodulatory and osteoinductive implant surfaces via mussel adhesion-mediated ion coordination and molecular clicking. Nat Commun. 2022;13:160. doi:10.1038/s41467-021-27816-1
  • Wu Z, Bai J, Ge G, et al. Regulating macrophage polarization in high glucose microenvironment using lithium-modified bioglass-hydrogel for diabetic bone regeneration. Adv Healthcare Mater. 2022;11:e2200298. doi:10.1002/adhm.202200298
  • He J, Chen G, Liu M, et al. Scaffold strategies for modulating immune microenvironment during bone regeneration. Mater Sci Eng C. 2020;108:110411. doi:10.1016/j.msec.2019.110411
  • Chouhan D, Mandal BB. Silk biomaterials in wound healing and skin regeneration therapeutics: from bench to bedside. Acta Biomater. 2020;103:24–51. doi:10.1016/j.actbio.2019.11.050
  • Zhang D, Chen Q, Zhang W, et al. Silk-inspired β-peptide materials resist fouling and the foreign-body response. Angew Chem Int Ed Engl. 2020;59:9586–9593. doi:10.1002/anie.202000416
  • Lamboni L, Gauthier M, Yang G, Wang Q. Silk sericin: a versatile material for tissue engineering and drug delivery. Biotechnol Adv. 2015;33:1855–1867. doi:10.1016/j.biotechadv.2015.10.014
  • Zhang D, Chen Q, Bi Y, et al. Bio-inspired poly-DL-serine materials resist the foreign-body response. Nat Commun. 2021;12:5327. doi:10.1038/s41467-021-25581-9
  • Das G, Shin HS, Campos EV, et al. Sericin based nanoformulations: a comprehensive review on molecular mechanisms of interaction with organisms to biological applications. J Nanobiotechnol. 2021;19:30. doi:10.1186/s12951-021-00774-y
  • Farokhi M, Mottaghitalab F, Samani S, et al. Silk fibroin/hydroxyapatite composites for bone tissue engineering. Biotechnol Adv. 2018;36:68–91. doi:10.1016/j.biotechadv.2017.10.001
  • Cho YS, Quan ML, Kang NU, et al. Strategy for enhancing mechanical properties and bone regeneration of 3D polycaprolactone kagome scaffold: nano hydroxyapatite composite and its exposure. Eur Polym J. 2020;134:12. doi:10.1016/j.eurpolymj.2020.109814
  • Hernández-González AC, Téllez-Jurado L, Rodríguez-Lorenzo LM. Alginate hydrogels for bone tissue engineering, from injectables to bioprinting: a review. Carbohydr Polym. 2020;229:115514. doi:10.1016/j.carbpol.2019.115514
  • Bressan E, Ferroni L, Gardin C, et al. Graphene based scaffolds effects on stem cells commitment. J Transl Med. 2014;12:296. doi:10.1186/s12967-014-0296-9
  • Lee WC, Lim CH, Shi H, et al. Origin of enhanced stem cell growth and differentiation on graphene and graphene oxide. ACS nano. 2011;5:7334–7341. doi:10.1021/nn202190c
  • Liu W, Li J, Cheng M, et al. A surface-engineered polyetheretherketone biomaterial implant with direct and immunoregulatory antibacterial activity against methicillin-resistant Staphylococcus aureus. Biomaterials. 2019;208:8–20. doi:10.1016/j.biomaterials.2019.04.008
  • Anderson JM, Rodriguez A, Chang DT. Foreign body reaction to biomaterials. Semin Immunol. 2008;20:86–100. doi:10.1016/j.smim.2007.11.004
  • Jiang LB, Ding SL, Ding W, et al. Injectable sericin based nanocomposite hydrogel for multi-modal imaging-guided immunomodulatory bone regeneration. Chem Eng J. 2021;418:19.
  • Cao L, Lu W, Mata A, Nishinari K, Fang Y. Egg-box model-based gelation of alginate and pectin: a review. Carbohydr Polym. 2020;242:116389. doi:10.1016/j.carbpol.2020.116389
  • Lee KY, Mooney DJ. Alginate: properties and biomedical applications. Prog Polym Sci. 2012;37:106–126. doi:10.1016/j.progpolymsci.2011.06.003
  • Li Z, Du T, Ruan C, Niu X. Bioinspired mineralized collagen scaffolds for bone tissue engineering. Bioact Mater. 2021;6:1491–1511. doi:10.1016/j.bioactmat.2020.11.004
  • Palacio-Mancheno PE, Larriera AI, Doty SB, et al. 3D assessment of cortical bone porosity and tissue mineral density using high-resolution µCT: effects of resolution and threshold method. J Bone Miner Res. 2014;29:142–150. doi:10.1002/jbmr.2012
  • Collins MN, Ren G, Young K, et al. Scaffold fabrication technologies and structure/function properties in bone tissue engineering. Adv Funct Mater. 2021;31:2010609.
  • Wang C, Huang W, Zhou Y, et al. 3D printing of bone tissue engineering scaffolds. Bioact Mater. 2020;5:82–91. doi:10.1016/j.bioactmat.2020.01.004
  • KhorramiN K, Radi M, Amiri S, McClements DJ. Fabrication and characterization of alginate-based films functionalized with nanostructured lipid carriers. Int J Biol Macromol. 2021;182:373–384. doi:10.1016/j.ijbiomac.2021.03.159
  • Lawrie G, Keen I, Drew B, et al. Interactions between alginate and chitosan biopolymers characterized using FTIR and XPS. Biomacromolecules. 2007;8:2533–2541. doi:10.1021/bm070014y
  • Wang X, Tang J, Huang J, Hui M. Production and characterization of bacterial cellulose membranes with hyaluronic acid and silk sericin. Colloids Surf B. 2020;195:111273. doi:10.1016/j.colsurfb.2020.111273
  • Alicka M, Sobierajska P, Kornicka K, Wiglusz RJ, Marycz K. Lithium ions (Li (+)) and nanohydroxyapatite (nHAp) doped with Li (+) enhance expression of late osteogenic markers in adipose-derived stem cells. Potential theranostic application of nHAp doped with Li (+) and co-doped with europium (III) and samarium (III) ions. Mater Sci Eng C. 2019;99:1257–1273.
  • Santana-Melo GF, Rodrigues BVM, da Silva E, et al. Electrospun ultrathin PBAT/nHAp fibers influenced the in vitro and in vivo osteogenesis and improved the mechanical properties of neoformed bone. Colloids Surf B. 2017;155:544–552. doi:10.1016/j.colsurfb.2017.04.053
  • Zhang Y, Zhang H, Zou Q, Xing R, Jiao T, Yan X. An injectable dipeptide-fullerene supramolecular hydrogel for photodynamic antibacterial therapy. J Mater Chem B. 2018;6:7335–7342. doi:10.1039/C8TB01487F
  • Shahbazarab Z, Teimouri A, Chermahini AN, Azadi M. Fabrication and characterization of nanobiocomposite scaffold of zein/chitosan/nanohydroxyapatite prepared by freeze-drying method for bone tissue engineering. Int J Biol Macromol. 2018;108:1017–1027. doi:10.1016/j.ijbiomac.2017.11.017
  • Ji C, Khademhosseini A, Dehghani F. Enhancing cell penetration and proliferation in chitosan hydrogels for tissue engineering applications. Biomaterials. 2011;32:9719–9729. doi:10.1016/j.biomaterials.2011.09.003
  • Felfel RM, Gideon-Adeniyi MJ, Zakir Hossain K, Roberts GAF, Grant DM. Structural, mechanical and swelling characteristics of 3D scaffolds from chitosan-agarose blends. Carbohydr Polym. 2019;204:59–67. doi:10.1016/j.carbpol.2018.10.002
  • Patel S, Srivastava S, Singh MR, Singh D. Preparation and optimization of chitosan-gelatin films for sustained delivery of lupeol for wound healing. Int J Biol Macromol. 2018;107:1888–1897.
  • Mahato A, Sandy Z, Bysakh S, et al. Development of nano-porous hydroxyapatite coated e-glass for potential bone-tissue engineering application: an in vitro approach. Mater Sci Eng C. 2020;111:110764. doi:10.1016/j.msec.2020.110764
  • Yang D, Xiao J, Wang B, Li L, Kong X, Liao J. The immune reaction and degradation fate of scaffold in cartilage/bone tissue engineering. Mater Sci Eng C. 2019;104:109927.
  • Zhu G, Zhang T, Chen M, et al. Bone physiological microenvironment and healing mechanism: basis for future bone-tissue engineering scaffolds. Bioact Mater. 2021;6:4110–4140. doi:10.1016/j.bioactmat.2021.03.043
  • Selvaraj S, Fathima NN. Fenugreek incorporated silk fibroin Nanofibers-A potential antioxidant scaffold for enhanced wound healing. ACS Appl Mater Interfaces. 2017;9:5916–5926. doi:10.1021/acsami.6b16306
  • Sathiyavimal S, Vasantharaj S, LewisOscar F, Pugazhendhi A, Subashkumar R. Biosynthesis and characterization of hydroxyapatite and its composite (hydroxyapatite-gelatin-chitosan-fibrin-bone ash) for bone tissue engineering applications. Int J Biol Macromol. 2019;129:844–852. doi:10.1016/j.ijbiomac.2019.02.058
  • Ruiz ON, Fernando KA, Wang B, et al. Graphene oxide: a nonspecific enhancer of cellular growth. ACS nano. 2011;5:8100–8107. doi:10.1021/nn202699t
  • Singh DP, Herrera CE, Singh B, Singh S, Singh RK, Kumar R. Graphene oxide: an efficient material and recent approach for biotechnological and biomedical applications. Mater Sci Eng C. 2018;86:173–197.
  • Reina G, González-Domínguez JM, Criado A, Vázquez E, Bianco A, Prato M. Promises, facts and challenges for graphene in biomedical applications. Chem Soc Rev. 2017;46:4400–4416. doi:10.1039/C7CS00363C
  • Balabiyev A, Podolnikova NP, Kilbourne JA, et al. Fibrin polymer on the surface of biomaterial implants drives the foreign body reaction. Biomaterials. 2021;277:121087.
  • Ding C, Yang C, Cheng T, et al. Macrophage-biomimetic porous Se@SiO(2) nanocomposites for dual modal immunotherapy against inflammatory osteolysis. J Nanobiotechnol. 2021;19:382. doi:10.1186/s12951-021-01128-4
  • Antonios JK, Yao Z, Li C, Rao AJ, Goodman SB. Macrophage polarization in response to wear particles in vitro. Cell Mol Immunol. 2013;10:471–482. doi:10.1038/cmi.2013.39
  • Chachlioutaki K, Karavasili C, Adamoudi E, et al. Silk sericin/PLGA electrospun scaffolds with anti-inflammatory drug-eluting properties for periodontal tissue engineering. Mater Sci Eng C. 2022;133:112723.
  • Huang W, Ling S, Li C, Omenetto FG, Kaplan DL. Silkworm silk-based materials and devices generated using bio-nanotechnology. Chem Soc Rev. 2018;47:6486–6504. doi:10.1039/C8CS00187A
  • Okamoto K, Nakashima T, Shinohara M, et al. Osteoimmunology: the conceptual framework unifying the immune and skeletal systems. Physiol Rev. 2017;97:1295–1349.
  • Kim H, Hwangbo H, Koo Y, Kim G. Fabrication of mechanically reinforced gelatin/hydroxyapatite bio-composite scaffolds by core/shell nozzle printing for bone tissue engineering. Int J Mol Sci. 2020;21:3401. doi:10.3390/ijms21093401
  • Zou Z, Wang L, Zhou Z, et al. Simultaneous incorporation of PTH (1-34) and nano-hydroxyapatite into Chitosan/Alginate Hydrogels for efficient bone regeneration. Bioact Mater. 2021;6:1839–1851. doi:10.1016/j.bioactmat.2020.11.021
  • Boller LA, Shiels SM, Florian DC, et al. Effects of nanocrystalline hydroxyapatite concentration and skeletal site on bone and cartilage formation in rats. Acta Biomater. 2021;130:485–496. doi:10.1016/j.actbio.2021.05.056
  • Newby SD, Masi T, Griffin CD, et al. Functionalized graphene nanoparticles induce human mesenchymal stem cells to express distinct extracellular matrix proteins mediating osteogenesis. Int J Nanomed. 2020;15:2501–2513. doi:10.2147/IJN.S245801
  • Wu X, Zheng S, Ye Y, Wu Y, Lin K, Su J. Enhanced osteogenic differentiation and bone regeneration of poly (lactic-co-glycolic acid) by graphene via activation of PI3K/Akt/GSK-3β/β-catenin signal circuit. Biomater Sci. 2018;6:1147–1158. doi:10.1039/C8BM00127H
  • Bordoni V, Reina G, Orecchioni M, et al. Stimulation of bone formation by monocyte-activator functionalized graphene oxide in vivo. Nanoscale. 2019;11:19408–19421. doi:10.1039/C9NR03975A
  • Wu J, Zheng A, Liu Y, et al. Enhanced bone regeneration of the silk fibroin electrospun scaffolds through the modification of the graphene oxide functionalized by BMP-2 peptide. Int J Nanomed. 2019;14:733–751. doi:10.2147/IJN.S187664
  • Pajarinen J, Lin T, Gibon E, et al. Mesenchymal stem cell-macrophage crosstalk and bone healing. Biomaterials. 2019;196:80–89. doi:10.1016/j.biomaterials.2017.12.025
  • Chen M, Zhang Y, Zhou P, et al. Substrate stiffness modulates bone marrow-derived macrophage polarization through NF-κB signaling pathway. Bioact Mater. 2020;5:880–890. doi:10.1016/j.bioactmat.2020.05.004
  • Hao S, Meng J, Zhang Y, et al. Macrophage phenotypic mechanomodulation of enhancing bone regeneration by superparamagnetic scaffold upon magnetization. Biomaterials. 2017;140:16–25. doi:10.1016/j.biomaterials.2017.06.013
  • Jin SS, He DQ, Luo D, et al. A biomimetic hierarchical nanointerface orchestrates macrophage polarization and mesenchymal stem cell recruitment to promote endogenous bone regeneration. ACS nano. 2019;13:6581–6595. doi:10.1021/acsnano.9b00489
  • Kazimierczak P, Koziol M, Przekora A. The chitosan/Agarose/NanoHA bone scaffold-induced M2 macrophage polarization and its effect on osteogenic differentiation in vitro. Int J Mol Sci. 2021;22:1109. doi:10.3390/ijms22031109
  • Zheng ZW, Chen YH, Wu DY, et al. Development of an accurate and proactive immunomodulatory strategy to improve bone substitute material-mediated osteogenesis and angiogenesis. Theranostics. 2018;8:5482–5500. doi:10.7150/thno.28315
  • Spiller KL, Nassiri S, Witherel CE, et al. Sequential delivery of immunomodulatory cytokines to facilitate the M1-to-M2 transition of macrophages and enhance vascularization of bone scaffolds. Biomaterials. 2015;37:194–207. doi:10.1016/j.biomaterials.2014.10.017
  • Zou M, Sun J, Xiang Z. Induction of M2-type macrophage differentiation for bone defect repair via an interpenetration network hydrogel with a GO-based controlled release system. Adv Healthcare Mater. 2021;10:e2001502. doi:10.1002/adhm.202001502
  • Chen R, Hao Z, Wang Y, et al. Mesenchymal stem cell-immune cell interaction and related modulations for bone tissue engineering. Stem Cells Int. 2022;2022:7153584. doi:10.1155/2022/7153584
  • Zhang HJ, Li FS, Wang F, et al. Transgenic PDGF-BB sericin hydrogel potentiates bone regeneration of BMP9-stimulated mesenchymal stem cells through a crosstalk of the Smad-STAT pathways. Regener Biomater. 2023;10:rbac095. doi:10.1093/rb/rbac095
  • Qi C, Deng Y, Xu L, et al. A sericin/ graphene oxide composite scaffold as a biomimetic extracellular matrix for structural and functional repair of calvarial bone. Theranostics. 2020;10:741–756. doi:10.7150/thno.39502
  • Sun J, Li L, Xing F, et al. Graphene oxide-modified silk fibroin/nanohydroxyapatite scaffold loaded with urine-derived stem cells for immunomodulation and bone regeneration. Stem Cell Res Ther. 2021;12:591. doi:10.1186/s13287-021-02634-w
  • Liu Y, Zhang Y, Zheng Z, et al. Incorporation of NGR1 promotes bone regeneration of injectable HA/nHAp hydrogels by anti-inflammation regulation via a MAPK/ERK signaling pathway. Front Bioeng Biotechnol. 2022;10:992961. doi:10.3389/fbioe.2022.992961