Enhanced osteogenesis and angiogenesis by PCL/chitosan/Sr-doped calcium phosphate electrospun nanocomposite membrane for guided bone regeneration

References

• Clementini M, Morlupi A, Canullo L, et al. Success rate of dental implants inserted in horizontal and vertical guided bone regenerated areas: a systematic review. Int J Oral Maxillofac Surg. 2012;41:847–852.
   PubMed Web of Science ®Google Scholar
• Winkler T, Sass FA, Duda GN, et al. A review of biomaterials in bone defect healing, remaining shortcomings and future opportunities for bone tissue engineering: the unsolved challenge. Bone Joint Surg. 2018;7:232–243.
   Google Scholar
• Qu Y, Wang Y, Kong X, et al. Heat-treated membranes with bioelectricity promote bone regeneration. J Biomater Sci Polym Ed. 2014;25:211–223.
   PubMed Web of Science ®Google Scholar
• Ezati M, Safavipour H, Houshmand B, et al. Development of a PCL/gelatin/chitosan/beta-TCP electrospun composite for guided bone regeneration. Prog Biomater. 2018;7:225–237.
   PubMed Web of Science ®Google Scholar
• Li J, Zuo Y, Man Y, et al. Fabrication and biocompatibility of an antimicrobial composite membrane with an asymmetric porous structure. J Biomater Sci Polym Ed. 2012;23:81–96.
   PubMed Web of Science ®Google Scholar
• Agarwal S, Wendorff JH, Greiner A. Use of electrospinning technique for biomedical applications. Polymer. 2008;49:5603–5621.
   Web of Science ®Google Scholar
• Jin S, Sun F, Zou Q, et al. Fish collagen and hydroxyapatite reinforced poly(lactide-co-glycolide) fibrous membrane for guided bone regeneration. Biomacromolecules. 2019;20:2058–2067.
   PubMed Web of Science ®Google Scholar
• Surucu S, Turkoglu Sasmazel H. DBD atmospheric plasma-modified, electrospun, layer-by-layer polymeric scaffolds for L929 fibroblast cell cultivation. J Biomater Sci Polym Ed. 2016;27:111–132.
   PubMed Web of Science ®Google Scholar
• Fadaie M, Mirzaei E, Geramizadeh B, et al. Incorporation of nanofibrillated chitosan into electrospun PCL nanofibers makes scaffolds with enhanced mechanical and biological properties. Carbohydr Polym. 2018;199:628–640.
   PubMed Web of Science ®Google Scholar
• Ren K, Wang Y, Sun T, et al. Electrospun PCL/gelatin composite nanofiber structures for effective guided bone regeneration membranes. Mater Sci Eng C Mater Biol Appl. 2017;78:324–332.
   PubMed Web of Science ®Google Scholar
• Sharifi F, Atyabi SM, Norouzian D, et al. Polycaprolactone/carboxymethyl chitosan nanofibrous scaffolds for bone tissue engineering application. Int J Biol Macromol. 2018;115:243–248.
   PubMed Web of Science ®Google Scholar
• Islam MT, Felfel RM, Abou Neel EA, et al. Bioactive calcium phosphate-based glasses and ceramics and their biomedical applications: a review. J Tissue Eng. 2017;8:204173141771917.
   Web of Science ®Google Scholar
• Yar M, Farooq A, Shahzadi L, et al. Novel meloxicam releasing electrospun polymer/ceramic reinforced biodegradable membranes for periodontal regeneration applications. Mater Sci Eng C Mater Biol Appl. 2016;64:148–156.
   PubMed Web of Science ®Google Scholar
• Bhattacharjee A, Gupta A, Verma M, et al. Site-specific antibacterial efficacy and cyto/hemo-compatibility of zinc substituted hydroxyapatite. Ceram Int. 2019;45:12225–12233.
   Web of Science ®Google Scholar
• Lim PN, Konishi T, Wang Z, et al. Enhancing osteoconductivity and biocompatibility of silver-substituted apatite in vivo through silicon co-substitution. Mater Lett. 2018;212:90–93.
   Web of Science ®Google Scholar
• Sanyal V, Raja CR. Synthesis, characterization and in-vitro studies of strontium-zinc co-substituted fluorohydroxyapatite for biomedical applications. J Non-Cryst Solids. 2016;445-446:81–87.
   Web of Science ®Google Scholar
• Fereshteh Z, Mallakpour F, Fathi M, et al. Surface modification of Mg-doped fluoridated hydroxyapatite nanoparticles using bioactive amino acids as the coupling agent for biomedical applications. Ceram Int. 2015;41:10079–10086.
   Web of Science ®Google Scholar
• Lourenco AH, Torres AL, Vasconcelos DP, et al. Osteogenic, anti-osteoclastogenic and immunomodulatory properties of a strontium-releasing hybrid scaffold for bone repair. Mater Sci Eng C Mater Biol Appl. 2019;99:1289–1303.
   PubMed Web of Science ®Google Scholar
• Lode A, Heiss C, Knapp G, et al. Strontium-modified premixed calcium phosphate cements for the therapy of osteoporotic bone defects. Acta Biomater. 2018;65:475–485.
   PubMed Web of Science ®Google Scholar
• Li J, Yang L, Guo X, et al. Osteogenesis effects of strontium-substituted hydroxyapatite coatings on true bone ceramic surfaces in vitro and in vivo. Biomed Mater. 2017;13:015018.
   PubMed Web of Science ®Google Scholar
• Li S, Li L, Guo C, et al. A promising wound dressing material with excellent cytocompatibility and proangiogenesis action for wound healing: strontium loaded Silk fibroin/Sodium alginate (SF/SA) blend films. Int J Biol Macromol. 2017;104(Pt A):969–978.
   Web of Science ®Google Scholar
• Verrier S, Alini M, Alsberg E, et al. Tissue engineering and regenerative approaches to improving the healing of large bone defects. Eur Cell Mater. 2016;32:87–110.
   PubMed Web of Science ®Google Scholar
• Shie MY, Chiang WH, Chen IP, et al. Synergistic acceleration in the osteogenic and angiogenic differentiation of human mesenchymal stem cells by calcium silicate-graphene composites. Mater Sci Eng C Mater Biol Appl. 2017;73:726–735.
   PubMed Web of Science ®Google Scholar
• Chen Y, Gao A, Bai L, et al. Antibacterial, osteogenic, and angiogenic activities of SrTiO3 nanotubes embedded with Ag2O nanoparticles. Mater Sci Eng C Mater Biol Appl. 2017;75:1049–1058.
   PubMed Web of Science ®Google Scholar
• Li L, Zuo Y, Zou Q, et al. Hierarchical structure and mechanical improvement of an n-HA/GCO-PU composite scaffold for bone regeneration. ACS Appl Mater Interfaces. 2015;7:22618–22629.
   PubMed Web of Science ®Google Scholar
• Shuai C, Guo W, Wu P, et al. A graphene oxide-Ag co-dispersing nanosystem: dual synergistic effects on antibacterial activities and mechanical properties of polymer scaffolds. Chem Eng J. 2018;347:322–333.
   Web of Science ®Google Scholar
• Bagchi A, Meka SR, Rao BN, et al. Perovskite ceramic nanoparticles in polymer composites for augmenting bone tissue regeneration. Nanotechnology. 2014;25:485101.
   PubMed Web of Science ®Google Scholar
• Kouhi M, Prabhakaran MP, Shamanian M, et al. Electrospun PHBV nanofibers containing HA and bredigite nanoparticles: fabrication, characterization and evaluation of mechanical properties and bioactivity. Compos Sci Technol. 2015;121:115–122.
   Web of Science ®Google Scholar
• Gupta D, Venugopal J, Mitra S, et al. Nanostructured biocomposite substrates by electrospinning and electrospraying for the mineralization of osteoblasts. Biomaterials. 2009;30:2085–2094.
   PubMed Web of Science ®Google Scholar
• Li L, Qian Y, Jiang C, et al. The use of hyaluronan to regulate protein adsorption and cell infiltration in nanofibrous scaffolds. Biomaterials. 2012;33:3428–3445.
   PubMed Web of Science ®Google Scholar
• Lee J-H, Kim Y-J. Hydroxyapatite nanofibers fabricated through electrospinning and sol–gel process. Ceram Int. 2014;40:3361–3369.
   Web of Science ®Google Scholar
• Weng L, Boda SK, Teusink MJ, et al. Binary doping of strontium and copper enhancing osteogenesis and angiogenesis of bioactive glass nanofibers while suppressing osteoclast activity. ACS Appl Mater Interfaces. 2017;9:24484–24496.
   PubMed Web of Science ®Google Scholar
• Fridrikh SV, Yu JH, Brenner MP, et al. Controlling the fiber diameter during electrospinning. Phys Rev Lett. 2003;90:144502.
   PubMed Web of Science ®Google Scholar
• Surmenev RA, Shkarina S, Syromotina DS, et al. Characterization of biomimetic silicate- and strontium-containing hydroxyapatite microparticles embedded in biodegradable electrospun polycaprolactone scaffolds for bone regeneration. Eur Polym J. 2019;113:67–77.
   Web of Science ®Google Scholar
• Feng P, Wu P, Gao C, et al. A Multimaterial scaffold with tunable properties: toward bone tissue repair. Adv Sci. 2018;5:1700817.
   Web of Science ®Google Scholar
• Cheng G, Zhang Y, Yin H, et al. Effects of strontium substitution on the structural distortion of hydroxyapatite by rietveld refinement and Raman Spectroscopy. Ceram Int. 2019;45:11073–11078.
   Web of Science ®Google Scholar
• Ehret C, Aid-Launais R, Sagardoy T, et al. Strontium-doped hydroxyapatite polysaccharide materials effect on ectopic bone formation. PLoS One. 2017;12:e0184663.
   PubMed Web of Science ®Google Scholar
• Edwin N, Saranya S, Wilson P. Strontium incorporated hydroxyapatite/hydrothermally reduced graphene oxide nanocomposite as a cytocompatible material. Ceram Int. 2019;45:5475–5485.
   Web of Science ®Google Scholar
• Zhang H, Luo X, Lin X, et al. Polycaprolactone/chitosan blends: simulation and experimental design. Mater Des. 2016;90:396–402.
   Web of Science ®Google Scholar
• Ning CQ, Greish Y, El-Ghannam A. Crystallization behavior of silica-calcium phosphate biocomposites: XRD and FTIR studies. J Mater Sci: Mater Med. 2004;15:1227–1235.
   PubMed Web of Science ®Google Scholar
• Jin S, Li J, Wang J, et al. Electrospun silver ion-loaded calcium phosphate/chitosan antibacterial composite fibrous membranes for guided bone regeneration. Int J Nanomedicine. 2018;13:4591–4605.
   PubMed Web of Science ®Google Scholar
• Li X, Wang C, Yang S, et al. Electrospun PCL/mupirocin and chitosan/lidocaine hydrochloride multifunctional double layer nanofibrous scaffolds for wound dressing applications. Int J Nanomedicine. 2018; 13:5287–5299.
   PubMed Web of Science ®Google Scholar
• Wang J, Planz V, Vukosavljevic B, et al. Multifunctional electrospun nanofibers for wound application - Novel insights into the control of drug release and antimicrobial activity. Eur J Pharm Biopharm. 2018;129:175–183.
   PubMed Web of Science ®Google Scholar
• Xiong X, Chu C, Zeng X, et al. Effect of substrate temperature on CaHPO4 coating on HT-C/C composites prepared by ultrasonic induction heating method. Rare Metal Mat Eng. 2014;43:1594–1599.
   Web of Science ®Google Scholar
• Gomes S, Rodrigues G, Martins G, et al. Evaluation of nanofibrous scaffolds obtained from blends of chitosan, gelatin and polycaprolactone for skin tissue engineering. Int J Biol Macromol. 2017;102:1174–1185.
   PubMed Web of Science ®Google Scholar
• Poon L, Wilson LD, Headley JV. Chitosan-glutaraldehyde copolymers and their sorption properties. Carbohydr Polym. 2014;109:92–101.
   PubMed Web of Science ®Google Scholar
• Chan BP, Leong KW. Scaffolding in tissue engineering: general approaches and tissue-specific considerations. Eur Spine J. 2008;17:467–479.
   PubMed Web of Science ®Google Scholar
• Hao J, Acharya A, Chen K, et al. Novel bioresorbable strontium hydroxyapatite membrane for guided bone regeneration. Clin Oral Impl Res. 2015;26:1–7.
   PubMed Web of Science ®Google Scholar
• Mahoney C, Conklin D, Waterman J, et al. Electrospun nanofibers of poly(epsilon-caprolactone)/depolymerized chitosan for respiratory tissue engineering applications. J Biomater Sci Polym Ed. 2016;27:611–625.
   PubMed Web of Science ®Google Scholar
• Calamak S, Aksoy EA, Ertas N, et al. Ag/silk fibroin nanofibers: effect of fibroin morphology on Ag + release and antibacterial activity. Eur Polym J. 2015;67:99–112.
   Web of Science ®Google Scholar
• Meka SR, Jain S, Chatterjee K. Strontium eluting nanofibers augment stem cell osteogenesis for bone tissue regeneration. Colloids Surf B Biointerfaces. 2016;146:649–656.
   PubMed Web of Science ®Google Scholar
• Schumacher M, Lode A, Helth A, et al. A novel strontium(II)-modified calcium phosphate bone cement stimulates human-bone-marrow-derived mesenchymal stem cell proliferation and osteogenic differentiation in vitro. Acta Biomater. 2013;9:9547–9557.
   PubMed Web of Science ®Google Scholar
• Sila-Asna M, Bunyaratvej A, Maeda S, et al. Osteoblast differentiation and bone formation gene expression in strontium-inducing bone marrow mesenchymal stem cell. Kobe J Med Sci. 2007;53:25–35.
   PubMedGoogle Scholar
• Tian M, Chen F, Song W, et al. In vivo study of porous strontium-doped calcium polyphosphate scaffolds for bone substitute applications. J Mater Sci: Mater Med. 2009;20:1505–1512.
   PubMed Web of Science ®Google Scholar
• Peng S, Zhou G, Luk KD, et al. Strontium promotes osteogenic differentiation of mesenchymal stem cells through the Ras/MAPK signaling pathway. Cell Physiol Biochem. 2009;23:165–174.
   PubMed Web of Science ®Google Scholar
• Liu F, Zhang X, Yu X, et al. In vitro study in stimulating the secretion of angiogenic growth factors of strontium-doped calcium polyphosphate for bone tissue engineering. J Mater Sci: Mater Med. 2011;22:683–692.
   PubMed Web of Science ®Google Scholar
• Lei Y, Xu Z, Ke Q, et al. Strontium hydroxyapatite/chitosan nanohybrid scaffolds with enhanced osteoinductivity for bone tissue engineering. Mater Sci Eng C Mater Biol Appl. 2017;72:134–142.
   PubMed Web of Science ®Google Scholar
• Naruphontjirakul P, Porter AE, Jones JR. In vitro osteogenesis by intracellular uptake of strontium containing bioactive glass nanoparticles. Acta Biomater. 2018;66:67–80.
   PubMed Web of Science ®Google Scholar
• Chattopadhyay N, Quinn SJ, Kifor O, et al. The calcium-sensing receptor (CaR) is involved in strontium ranelate-induced osteoblast proliferation. Biochem Pharmacol. 2007;74:438–447.
   PubMed Web of Science ®Google Scholar
• Xing M, Wang X, Wang E, et al. Bone tissue engineering strategy based on the synergistic effects of silicon and strontium ions. Acta Biomater. 2018;72:381–395.
   PubMed Web of Science ®Google Scholar
• Ohara N, Hayashi Y, Yamada S, et al. Early gene expression analyzed by cDNA microarray and RT-PCR in osteoblasts cultured with water-soluble and low molecular chitooligosaccharide. Biomaterials. 2004;25:1749–1754.
   PubMed Web of Science ®Google Scholar
• Tsigkou O, Jones JR, Polak JM, et al. Differentiation of fetal osteoblasts and formation of mineralized bone nodules by 45S5 Bioglass® conditioned medium in the absence of osteogenic supplements. Biomaterials. 2009;30:3542–3550.
   PubMed Web of Science ®Google Scholar
• Ni P, Fu S, Fan M, et al. Preparation of poly(ethylene glycol)/polylactide hybrid fibrous scaffolds for bone tissue engineering. Int J Nanomedicine. 2011;6:3065–3075.
   PubMed Web of Science ®Google Scholar
• Pittenger MF, Mackay AM, Beck SC, et al. Multilineage potential of adult human mesenchymal stem cells. Science. 1999;284:143–147.
   PubMed Web of Science ®Google Scholar
• Barry FP, Murphy JM. Mesenchymal stem cells: clinical applications and biological characterization. Int J Biochem Cell Biol. 2004;36:568–584.
   PubMed Web of Science ®Google Scholar
• Naruphontjirakul P, Tsigkou O, Li S, et al. Human mesenchymal stem cells differentiate into an osteogenic lineage in presence of strontium containing bioactive glass nanoparticles. Acta Biomater. 2019;90:373–392.
   PubMed Web of Science ®Google Scholar
• Shams M, Karimi M, Ghollasi M, et al. Electrospun poly-l-lactic acid nanofibers decorated with melt-derived S53P4 bioactive glass nanoparticles: the effect of nanoparticles on proliferation and osteogenic differentiation of human bone marrow mesenchymal stem cells in vitro. Ceram Int. 2018;44:20211.
   Web of Science ®Google Scholar
• Jimenez M, Abradelo C, San Roman J, et al. Bibliographic review on the state of the art of strontium and zinc based regenerative therapies. Recent developments and clinical applications. J Mater Chem B. 2019;7:1974–1985.
   Web of Science ®Google Scholar
• Zhang W, Cao H, Zhang X, et al. A strontium-incorporated nanoporous titanium implant surface for rapid osseointegration. Nanoscale. 2016;8:5291–5301.
   PubMed Web of Science ®Google Scholar
• Wang G, Roohani-Esfahani SI, Zhang W, et al. Effects of Sr-HT-Gahnite on osteogenesis and angiogenesis by adipose derived stem cells for critical-sized calvarial defect repair. Sci Rep. 2017;7:41135.
   PubMed Web of Science ®Google Scholar
• Balasubramanian P, Salinas AJ, Sanchez-Salcedo S, et al. Induction of VEGF secretion from bone marrow stromal cell line (ST-2) by the dissolution products of mesoporous silica glass particles containing CuO and SrO. J Non-Cryst Solids. 2018;500:217–224.
   Web of Science ®Google Scholar