Electrospun Icariin-Loaded Core-Shell Collagen, Polycaprolactone, Hydroxyapatite Composite Scaffolds for the Repair of Rabbit Tibia Bone Defects

References

• Fernandez de Grado G, Keller L, Idoux-Gillet Y, et al. Bone substitutes: a review of their characteristics, clinical use, and perspectives for large bone defects management. J Tissue Eng. 2018;9:2041731418776819. doi:10.1177/204173141877681929899969
   PubMed Web of Science ®Google Scholar
• Stevenson S. Enhancement of fracture healing with autogenous and allogeneic bone grafts. Clin Orthop Relat Res. 1998;355S(355 Suppl):S239–246. doi:10.1097/00003086-199810001-00024
   Google Scholar
• Ghayor C, Weber FE. Osteoconductive microarchitecture of bone substitutes for bone regeneration revisited. Front Physiol. 2018;9:960. doi:10.3389/fphys.2018.0096030072920
   PubMed Web of Science ®Google Scholar
• Salgado AJ, Coutinho OP, Reis RL. Bone tissue engineering: state of the art and future trends. Macromol Biosci. 2004;4(8):743–765. doi:10.1002/mabi.20040002615468269
   PubMed Web of Science ®Google Scholar
• Jimi E, Hirata S, Osawa K, Terashita M, Kitamura C, Fukushima H. The current and future therapies of bone regeneration to repair bone defects. Int J Dent. 2012;2012:148261. doi:10.1155/2012/14826122505894
   PubMedGoogle Scholar
• Heydari Z, Mohebbi-Kalhori D, Afarani MS. Engineered electrospun polycaprolactone (PCL)/octacalcium phosphate (OCP) scaffold for bone tissue engineering. Mater Sci Eng C Mater Biol Appl. 2017;81:127–132. doi:10.1016/j.msec.2017.07.04128887955
   PubMed Web of Science ®Google Scholar
• Luo W, Zhang S, Lan Y, et al. 3D printed porous polycaprolactone/oyster shell powder (PCL/OSP) scaffolds for bone tissue engineering. Mater Res Express. 2018;5(4):045403. doi:10.1088/2053-1591/aab916
   Web of Science ®Google Scholar
• Cunniffe GM, Curtin CM, Thompson EM, Dickson GR, O’Brien FJ. Content-dependent osteogenic response of nanohydroxyapatite: an in vitro and in vivo assessment within collagen-based scaffolds. ACS Appl Mater Interfaces. 2016;8(36):23477–23488. doi:10.1021/acsami.6b0659627537605
   PubMed Web of Science ®Google Scholar
• Xu T, Miszuk JM, Zhao Y, Sun H, Fong H. Electrospun polycaprolactone 3D nanofibrous scaffold with interconnected and hierarchically structured pores for bone tissue engineering. Adv Healthc Mater. 2015;4(15):2238–2246. doi:10.1002/adhm.20150034526332611
   PubMed Web of Science ®Google Scholar
• Shkarina S, Shkarin R, Weinhardt V, et al. 3D biodegradable scaffolds of polycaprolactone with silicate-containing hydroxyapatite microparticles for bone tissue engineering: high-resolution tomography and in vitro study. Sci Rep. 2018;8(1):8907. doi:10.1038/s41598-018-27097-729891842
   PubMedGoogle Scholar
• Zou L, Zhang Y, Liu X, Chen J, Zhang Q. Biomimetic mineralization on natural and synthetic polymers to prepare hybrid scaffolds for bone tissue engineering. Colloids Surf B Biointerfaces. 2019;178:222–229. doi:10.1016/j.colsurfb.2019.03.00430870789
   PubMed Web of Science ®Google Scholar
• Clarke B. Normal bone anatomy and physiology. Clin J Am Soc Nephrol. 2008;3(Suppl 3):S131–139. doi:10.2215/CJN.0415120618988698
   PubMed Web of Science ®Google Scholar
• Tierney CM, Haugh MG, Liedl J, Mulcahy F, Hayes B, O’Brien FJ. The effects of collagen concentration and crosslink density on the biological, structural and mechanical properties of collagen-GAG scaffolds for bone tissue engineering. J Mech Behav Biomed Mater. 2009;2(2):202–209. doi:10.1016/j.jmbbm.2008.08.00719627824
   PubMed Web of Science ®Google Scholar
• Filardo G, Kon E, Tampieri A, et al. New bio-ceramization processes applied to vegetable hierarchical structures for bone regeneration: an experimental model in sheep. Tissue Eng Part A. 2014;20(3–4):763–773. doi:10.1089/ten.TEA.2013.010824099033
   PubMed Web of Science ®Google Scholar
• Hayrapetyan A, Bongio M, Leeuwenburgh SC, Jansen JA, van den Beucken JJ. Effect of nano-HA/collagen composite hydrogels on osteogenic behavior of mesenchymal stromal cells. Stem Cell Rev. 2016;12(3):352–364. doi:10.1007/s12015-016-9644-x
   Web of Science ®Google Scholar
• Wang C, Zhao Q, Wang M. Cryogenic 3D printing for producing hierarchical porous and rhBMP-2-loaded Ca-P/PLLA nanocomposite scaffolds for bone tissue engineering. Biofabrication. 2017;9(2):025031. doi:10.1088/1758-5090/aa71c928589918
   PubMed Web of Science ®Google Scholar
• Cao H, Kuboyama N. A biodegradable porous composite scaffold of PGA/beta-TCP for bone tissue engineering. Bone. 2010;46(2):386–395. doi:10.1016/j.bone.2009.09.03119800045
   PubMed Web of Science ®Google Scholar
• Yao Q, Cosme JG, Xu T, et al. Three dimensional electrospun PCL/PLA blend nanofibrous scaffolds with significantly improved stem cells osteogenic differentiation and cranial bone formation. Biomaterials. 2017;115:115–127. doi:10.1016/j.biomaterials.2016.11.01827886552
   PubMed Web of Science ®Google Scholar
• Lai Y, Li Y, Cao H, et al. Osteogenic magnesium incorporated into PLGA/TCP porous scaffold by 3D printing for repairing challenging bone defect. Biomaterials. 2019;197:207–219. doi:10.1016/j.biomaterials.2019.01.01330660996
   PubMed Web of Science ®Google Scholar
• Luo JW, Liu C, Wu JH, et al. In situ forming gelatin/hyaluronic acid hydrogel for tissue sealing and hemostasis. J Biomed Mater Res B Appl Biomater. 2019.
   Web of Science ®Google Scholar
• Zein I, Hutmacher DW, Tan KC, Teoh SH. Fused deposition modeling of novel scaffold architectures for tissue engineering applications. Biomaterials. 2002;23(4):1169–1185. doi:10.1016/S0142-9612(01)00232-011791921
   PubMed Web of Science ®Google Scholar
• Jung MR, Shim IK, Chung HJ, et al. Local BMP-7 release from a PLGA scaffolding-matrix for the repair of osteochondral defects in rabbits. J Controlled Release. 2012;162(3):485–491. doi:10.1016/j.jconrel.2012.07.040
   PubMed Web of Science ®Google Scholar
• Nielsen EO, Chen L, Hansen JO, Degn M, Overgaard S, Ding M. Optimizing osteogenic differentiation of ovine adipose-derived stem cells by osteogenic induction medium and FGFb, BMP2, or NELL1 in vitro. Stem Cells Int. 2018;2018:9781393. doi:10.1155/2018/978139330356449
   PubMed Web of Science ®Google Scholar
• Eap S, Keller L, Schiavi J, et al. A living thick nanofibrous implant bifunctionalized with active growth factor and stem cells for bone regeneration. Int J Nanomedicine. 2015;10:1061–1075. doi:10.2147/IJN.S7267025709432
   PubMed Web of Science ®Google Scholar
• Mitsak AG, Kemppainen JM, Harris MT, Hollister SJ. Effect of polycaprolactone scaffold permeability on bone regeneration in vivo. Tissue Eng Part A. 2011;17(13–14):1831–1839. doi:10.1089/ten.tea.2010.056021395465
   PubMed Web of Science ®Google Scholar
• Rashad A, Mohamed-Ahmed S, Ojansivu M, et al. Coating 3D printed polycaprolactone scaffolds with nanocellulose promotes growth and differentiation of mesenchymal stem cells. Biomacromolecules. 2018;19(11):4307–4319. doi:10.1021/acs.biomac.8b0119430296827
   PubMed Web of Science ®Google Scholar
• Martino S, D’Angelo F, Armentano I, Kenny JM, Orlacchio A. Stem cell-biomaterial interactions for regenerative medicine. Biotechnol Adv. 2012;30(1):338–351. doi:10.1016/j.biotechadv.2011.06.01521740963
   PubMed Web of Science ®Google Scholar
• Zhang D, Wu X, Chen J, Lin K. The development of collagen based composite scaffolds for bone regeneration. Bioactive Mater. 2018;3(1):129–138. doi:10.1016/j.bioactmat.2017.08.004
   PubMed Web of Science ®Google Scholar
• Zhang L, Zhang X, Li KF, et al. Icariin promotes extracellular matrix synthesis and gene expression of chondrocytes in vitro. Phytother Res. 2012;26(9):1385–1392. doi:10.1002/ptr.373322308065
   PubMed Web of Science ®Google Scholar
• Xie X, Pei F, Wang H, Tan Z, Yang Z, Kang P. Icariin: a promising osteoinductive compound for repairing bone defect and osteonecrosis. J Biomater Appl. 2015;30(3):290–299. doi:10.1177/088532821558155125876888
   PubMed Web of Science ®Google Scholar
• He J-P, Feng X, Wang J-F, et al. Icariin prevents bone loss by inhibiting bone resorption and stabilizing bone biological apatite in a hindlimb suspension rodent model. Acta Pharmacol Sin. 2018;39(11):1760–1767. doi:10.1038/s41401-018-0040-829891857
   PubMed Web of Science ®Google Scholar
• Wang Z, Li K, Sun H, Wang J, Fu Z, Liu M. Icariin promotes stable chondrogenic differentiation of bone marrow mesenchymal stem cells in selfassembling peptide nanofiber hydrogel scaffolds. Mol Med Rep. 2018;17(6):8237–8243. doi:10.3892/mmr.2018.891329693145
   PubMed Web of Science ®Google Scholar
• Venkatesan J, Kim SK. Chitosan composites for bone tissue engineering–an overview. Mar Drugs. 2010;8(8):2252–2266. doi:10.3390/md808225220948907
   PubMed Web of Science ®Google Scholar
• Thein-Han WW, Misra RD. Biomimetic chitosan-nanohydroxyapatite composite scaffolds for bone tissue engineering. Acta Biomater. 2009;5(4):1182–1197. doi:10.1016/j.actbio.2008.11.02519121983
   PubMed Web of Science ®Google Scholar
• Sinha VR, Singla AK, Wadhawan S, et al. Chitosan microspheres as a potential carrier for drugs. Int J Pharm. 2004;274(1–2):1–33. doi:10.1016/j.ijpharm.2003.12.02615072779
   PubMed Web of Science ®Google Scholar
• Liu H, Zhu J, Bao P, et al. Construction and in vivo/in vitro evaluation of a nanoporous ion-responsive targeted drug delivery system for recombinant human interferon alpha-2b delivery. Int J Nanomedicine. 2019;14:5339–5353. doi:10.2147/IJN.S20964631409991
   PubMed Web of Science ®Google Scholar
• Feng C, Wang Z, Jiang C, et al. Chitosan/o-carboxymethyl chitosan nanoparticles for efficient and safe oral anticancer drug delivery: in vitro and in vivo evaluation. Int J Pharm. 2013;457(1):158–167. doi:10.1016/j.ijpharm.2013.07.07924029170
   PubMed Web of Science ®Google Scholar
• Zhang H, Fu QW, Sun TW, et al. Amorphous calcium phosphate, hydroxyapatite and poly(d,l-lactic acid) composite nanofibers: electrospinning preparation, mineralization and in vivo bone defect repair. Colloids Surf B Biointerfaces. 2015;136:27–36. doi:10.1016/j.colsurfb.2015.08.01526350803
   PubMed Web of Science ®Google Scholar
• Wu J, Hong Y. Enhancing cell infiltration of electrospun fibrous scaffolds in tissue regeneration. Bioactive Mater. 2016;1(1):56–64. doi:10.1016/j.bioactmat.2016.07.001
   PubMed Web of Science ®Google Scholar
• Zhou Y, Chyu J, Zumwalt M. Recent progress of fabrication of cell scaffold by electrospinning technique for articular cartilage tissue engineering. Int J Biomater. 2018;2018:1953636. doi:10.1155/2018/195363629765405
   PubMed Web of Science ®Google Scholar
• Xin X, Hussain M, Mao JJ. Continuing differentiation of human mesenchymal stem cells and induced chondrogenic and osteogenic lineages in electrospun PLGA nanofiber scaffold. Biomaterials. 2007;28(2):316–325. doi:10.1016/j.biomaterials.2006.08.04217010425
   PubMed Web of Science ®Google Scholar
• Zafar M, Najeeb S, Khurshid Z, et al. Potential of electrospun nanofibers for biomedical and dental applications. Materials (Basel). 2016;9:2. doi:10.3390/ma9020073
   Web of Science ®Google Scholar
• Nerurkar NL, Sen S, Baker BM, Elliott DM, Mauck RL. Dynamic culture enhances stem cell infiltration and modulates extracellular matrix production on aligned electrospun nanofibrous scaffolds. Acta Biomater. 2011;7(2):485–491. doi:10.1016/j.actbio.2010.08.01120728589
   PubMed Web of Science ®Google Scholar
• Milleret V, Simona B, Neuenschwander P, Hall H. Tuning electrospinning parameters for production of 3D-fiber-fleeces with increased porosity for soft tissue engineering applications. Eur Cell Mater. 2011;21:286–303. doi:10.22203/eCM.v021a2221432783
   PubMed Web of Science ®Google Scholar
• Ekaputra AK, Prestwich GD, Cool SM, Hutmacher DW. Combining electrospun scaffolds with electrosprayed hydrogels leads to three-dimensional cellularization of hybrid constructs. Biomacromolecules. 2008;9(8):2097–2103. doi:10.1021/bm800565u18646822
   PubMed Web of Science ®Google Scholar
• Lewandowska-Lancucka J, Gilarska A, Bula A, Horak W, Latkiewicz A, Nowakowska M. Genipin crosslinked bioactive collagen/chitosan/hyaluronic acid injectable hydrogels structurally amended via covalent attachment of surface-modified silica particles. Int J Biol Macromol. 2019;136:1196–1208. doi:10.1016/j.ijbiomac.2019.06.18431252014
   PubMed Web of Science ®Google Scholar
• Mahmood SK, Zakaria M, Razak I, et al. Preparation and characterization of cockle shell aragonite nanocomposite porous 3D scaffolds for bone repair. Biochem Biophys Rep. 2017;10:237–251. doi:10.1016/j.bbrep.2017.04.00828955752
   PubMedGoogle Scholar
• Xiao H, Huang W, Xiong K, et al. Osteochondral repair using scaffolds with gradient pore sizes constructed with silk fibroin, chitosan, and nano-hydroxyapatite. Int J Nanomedicine. 2019;14:2011–2027. doi:10.2147/IJN.S19162730962685
   PubMed Web of Science ®Google Scholar
• Diaz E, Puerto I, Ribeiro S, Lanceros-Mendez S, Barandiaran JM. The influence of copolymer composition on PLGA/nHA scaffolds’ cytotoxicity and in vitro degradation. Nanomaterials (Basel, Switzerland). 2017;7:7. doi:10.3390/nano7120458
   PubMedGoogle Scholar
• Chen D, Zhu T, Fu W, Zhang H. Electrospun polycaprolactone/collagen nanofibers cross-linked with 1-ethyl-3-(3-dimethylaminopropyl) carbodiimide/N-hydroxysuccinimide and genipin facilitate endothelial cell regeneration and may be a promising candidate for vascular scaffolds. Int J Nanomedicine. 2019;14:2127–2144. doi:10.2147/IJN.S19269930988613
   PubMed Web of Science ®Google Scholar
• Yang A, Yu C, Lu Q, Li H, Li Z, He C. Mechanism of action of icariin in bone marrow mesenchymal stem cells. Stem Cells Int. 2019;2019:5747298. doi:10.1155/2019/574729831089330
   PubMed Web of Science ®Google Scholar
• Fan JJ, Cao LG, Wu T, et al. The dose-effect of icariin on the proliferation and osteogenic differentiation of human bone mesenchymal stem cells. Molecules. 2011;16(12):10123–10133. doi:10.3390/molecules16121012322146373
   PubMed Web of Science ®Google Scholar
• Zhang X, Xu M, Song L, et al. Effects of compatibility of deproteinized antler cancellous bone with various bioactive factors on their osteogenic potential. Biomaterials. 2013;34(36):9103–9114. doi:10.1016/j.biomaterials.2013.08.02424008040
   PubMed Web of Science ®Google Scholar
• De Becker A, Riet IV. Homing and migration of mesenchymal stromal cells: how to improve the efficacy of cell therapy? World J Stem Cells. 2016;8(3):73–87. doi:10.4252/wjsc.v8.i3.7327022438
   PubMed Web of Science ®Google Scholar
• Sprio S, Fricia M, Maddalena GF, Nataloni A, Tampieri A. Osteointegration in cranial bone reconstruction: a goal to achieve. J Appl Biomater Funct Mater. 2016;14(4):e470–e476. doi:10.5301/jabfm.500029327311430
   PubMed Web of Science ®Google Scholar
• Dennis SC, Berkland CJ, Bonewald LF, Detamore MS. Endochondral ossification for enhancing bone regeneration: converging native extracellular matrix biomaterials and developmental engineering in vivo. Tissue Eng Part B Rev. 2015;21(3):247–266. doi:10.1089/ten.teb.2014.041925336144
   PubMed Web of Science ®Google Scholar
• Delgado LM, Fuller K, Zeugolis DI. Collagen cross-linking: biophysical, biochemical, and biological response analysis. Tissue Eng Part A. 2017;23(19–20):1064–1077. doi:10.1089/ten.tea.2016.041528071973
   PubMed Web of Science ®Google Scholar
• Hutmacher DW, Schantz T, Zein I, Ng KW, Teoh SH, Tan KC. Mechanical properties and cell cultural response of polycaprolactone scaffolds designed and fabricated via fused deposition modeling. J Biomed Mater Res. 2001;55(2):203–216. doi:10.1002/1097-4636(200105)55:2<203::AID-JBM1007>3.0.CO;2-711255172
   PubMed Web of Science ®Google Scholar
• A A, Menon D, BS T, et al. Bioinspired composite matrix containing hydroxyapatite-silica core-shell nanorods for bone tissue engineering. ACS Appl Mater Interfaces. 2017;9(32):26707–26718. doi:10.1021/acsami.7b0713128741921
   PubMed Web of Science ®Google Scholar
• Na K, Kim SW, Sun BK, et al. Osteogenic differentiation of rabbit mesenchymal stem cells in thermo-reversible hydrogel constructs containing hydroxyapatite and bone morphogenic protein-2 (BMP-2). Biomaterials. 2007;28(16):2631–2637. doi:10.1016/j.biomaterials.2007.02.00817331575
   PubMed Web of Science ®Google Scholar
• Fu S, Ni P, Wang B, et al. In vivo biocompatibility and osteogenesis of electrospun poly(epsilon-caprolactone)-poly(ethylene glycol)-poly(epsilon-caprolactone)/nano-hydroxyapatite composite scaffold. Biomaterials. 2012;33(33):8363–8371. doi:10.1016/j.biomaterials.2012.08.02322921926
   PubMed Web of Science ®Google Scholar
• Phipps MC, Clem WC, Catledge SA, et al. Mesenchymal stem cell responses to bone-mimetic electrospun matrices composed of polycaprolactone, collagen I and nanoparticulate hydroxyapatite. PLoS One. 2011;6(2):e16813. doi:10.1371/journal.pone.001681321346817
   PubMed Web of Science ®Google Scholar
• Pham QP, Sharma U, Mikos AG. Electrospun poly(epsilon-caprolactone) microfiber and multilayer nanofiber/microfiber scaffolds: characterization of scaffolds and measurement of cellular infiltration. Biomacromolecules. 2006;7(10):2796–2805. doi:10.1021/bm060680j17025355
   PubMed Web of Science ®Google Scholar
• Nam J, Huang Y, Agarwal S, Lannutti J. Improved cellular infiltration in electrospun fiber via engineered porosity. Tissue Eng. 2007;13(9):2249–2257. doi:10.1089/ten.2006.030617536926
   PubMedGoogle Scholar
• Leong MF, Rasheed MZ, Lim TC, Chian KS. In vitro cell infiltration and in vivo cell infiltration and vascularization in a fibrous, highly porous poly(D,L-lactide) scaffold fabricated by cryogenic electrospinning technique. J Biomed Mater Res A. 2009;91(1):231–240. doi:10.1002/jbm.a.3220818814222
   PubMedGoogle Scholar
• Phipps MC, Clem WC, Grunda JM, Clines GA, Bellis SL. Increasing the pore sizes of bone-mimetic electrospun scaffolds comprised of polycaprolactone, collagen I and hydroxyapatite to enhance cell infiltration. Biomaterials. 2012;33(2):524–534. doi:10.1016/j.biomaterials.2011.09.08022014462
   PubMed Web of Science ®Google Scholar
• Chen P, Liu L, Pan J, Mei J, Li C, Zheng Y. Biomimetic composite scaffold of hydroxyapatite/gelatin-chitosan core-shell nanofibers for bone tissue engineering. Mater Sci Eng C Mater Biol Appl. 2019;97:325–335. doi:10.1016/j.msec.2018.12.02730678918
   PubMed Web of Science ®Google Scholar
• Temenoff JS, Mikos AG. Review: tissue engineering for regeneration of articular cartilage. Biomaterials. 2000;21(5):431–440. doi:10.1016/S0142-9612(99)00213-610674807
   PubMed Web of Science ®Google Scholar
• Hutmacher DW. Scaffolds in tissue engineering bone and cartilage. Biomaterials. 2000;21(24):2529–2543. doi:10.1016/S0142-9612(00)00121-611071603
   PubMed Web of Science ®Google Scholar
• Lu H-T, Lu T-W, Chen C-H, Mi F-L. Development of genipin-crosslinked and fucoidan-adsorbed nano-hydroxyapatite/hydroxypropyl chitosan composite scaffolds for bone tissue engineering. Int J Biol Macromol. 2019;128:973–984. doi:10.1016/j.ijbiomac.2019.02.01030738901
   PubMed Web of Science ®Google Scholar
• Mountziaris PM, Mikos AG. Modulation of the inflammatory response for enhanced bone tissue regeneration. Tissue Eng Part B Rev. 2008;14(2):179–186. doi:10.1089/ten.teb.2008.003818544015
   PubMed Web of Science ®Google Scholar
• Karageorgiou V, Kaplan D. Porosity of 3D biomaterial scaffolds and osteogenesis. Biomaterials. 2005;26(27):5474–5491. doi:10.1016/j.biomaterials.2005.02.00215860204
   PubMed Web of Science ®Google Scholar
• Song W, Yu X, Markel DC, Shi T, Ren W. Coaxial PCL/PVA electrospun nanofibers: osseointegration enhancer and controlled drug release device. Biofabrication. 2013;5(3):035006. doi:10.1088/1758-5082/5/3/03500623799653
   PubMed Web of Science ®Google Scholar
• Zhang X, Chang W, Lee P, et al. Polymer-ceramic spiral structured scaffolds for bone tissue engineering: effect of hydroxyapatite composition on human fetal osteoblasts. PLoS One. 2014;9(1):e85871. doi:10.1371/journal.pone.008587124475056
   PubMed Web of Science ®Google Scholar
• Yang J, Liu Y, He L, et al. Icariin conjugated hyaluronic acid/collagen hydrogel for osteochondral interface restoration. Acta Biomater. 2018;74:156–167. doi:10.1016/j.actbio.2018.05.00529734010
   PubMed Web of Science ®Google Scholar
• Huang Y, Shi R, Gong M, et al. Icariin-loaded electrospun PCL/gelatin sub-microfiber mat for preventing epidural adhesions after laminectomy. Int J Nanomedicine. 2018;13:4831–4844. doi:10.2147/IJN.S16942730214191
   PubMed Web of Science ®Google Scholar
• Shirazi RN, Ronan W, Rochev Y, McHugh P. Modelling the degradation and elastic properties of poly(lactic-co-glycolic acid) films and regular open-cell tissue engineering scaffolds. J Mech Behav Biomed Mater. 2016;54:48–59. doi:10.1016/j.jmbbm.2015.08.03026414516
   PubMed Web of Science ®Google Scholar