Horizon of exosome-mediated bone tissue regeneration: The all-rounder role in biomaterial engineering

Materials Today Bio - Tập 16 - Trang 100355 - 2022
Wentao Wang1, Xiaolong Liang1, Kai Zheng1, Gaoran Ge1, Xu Chen2, Yaozeng Xu1, Jiaxiang Bai1, Guoqing Pan2, Dechun Geng1
1Department of Orthopaedics, The First Affiliated Hospital of Soochow University, 188 Shizi Street, Suzhou, 215006, Jiangsu, China
2Institute for Advanced Materials, School of Materials Science and Engineering, Jiangsu University, 301 Xuefu Road, Zhenjiang, 212013, Jiangsu, China

Tài liệu tham khảo

Kostenuik, 2017, Fracture healing physiology and the quest for therapies for delayed healing and nonunion, J. Orthop. Res., 35, 213, 10.1002/jor.23460 Zhang, 2022, Emerging biomimetic nanotechnology in orthopedic diseases: progress, challenges, and opportunities, Trends Chem., 4, 420, 10.1016/j.trechm.2022.02.002 Schmal, 2020, Orthopaedic trauma, nonunion - consensus from the 4th annual meeting of the Danish orthopaedic trauma society, EFORT Open Rev., 5, 46, 10.1302/2058-5241.5.190037 Zhou, 2021, Biomaterials and nanomedicine for bone regeneration: progress and future prospects, Explorations, 1 Lee, 2019, Current advances in immunomodulatory biomaterials for bone regeneration, Adv. Healthc. Mater., 8, 10.1002/adhm.201801106 Schwartz, 2009, Prospective evaluation of chronic pain associated with posterior autologous iliac crest bone graft harvest and its effect on postoperative outcome, Health Qual. Life Outcome, 7, 49, 10.1186/1477-7525-7-49 van Griensven, 2015, Preclinical testing of drug delivery systems to bone, Adv. Drug Deliv. Rev., 94, 151, 10.1016/j.addr.2015.07.006 Li, 2022, Non-Invasive thermal therapy for tissue engineering and regenerative medicine, Small Pelissier, 2003, Influences of vascularization and osteogenic cells on heterotopic bone formation within a madreporic ceramic in rats, Plast. Reconstr. Surg., 111, 1932, 10.1097/01.PRS.0000055044.14093.EA Rouwkema, 2016, Vascularization and angiogenesis in tissue engineering: beyond creating static networks, Trends Biotechnol., 34, 733, 10.1016/j.tibtech.2016.03.002 Phinney, 2017, Concise review: MSC-derived exosomes for cell-free therapy, Stem Cell., 35, 851, 10.1002/stem.2575 Minciacchi, 2015, Extracellular vesicles in cancer: exosomes, microvesicles and the emerging role of large oncosomes, Semin. Cell Dev. Biol., 40, 41, 10.1016/j.semcdb.2015.02.010 Schneider, 2013, Exosomes: vesicular carriers for intercellular communication in neurodegenerative disorders, Cell Tissue Res., 352, 33, 10.1007/s00441-012-1428-2 Eggenhofer, 2014, The life and fate of mesenchymal stem cells, Front. Immunol., 5, 148, 10.3389/fimmu.2014.00148 Pan, 1983, Fate of the transferrin receptor during maturation of sheep reticulocytes in vitro: selective externalization of the receptor, Cell, 33, 967, 10.1016/0092-8674(83)90040-5 Ratajczak, 2006, Embryonic stem cell-derived microvesicles reprogram hematopoietic progenitors: evidence for horizontal transfer of mRNA and protein delivery, Leukemia, 20, 847, 10.1038/sj.leu.2404132 Valadi, 2007, Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells, Nat. Cell Biol., 9, 654, 10.1038/ncb1596 Mittelbrunn, 2011, Unidirectional transfer of microRNA-loaded exosomes from T cells to antigen-presenting cells, Nat. Commun., 2, 282, 10.1038/ncomms1285 Greening, 2015, Exosomes and their roles in immune regulation and cancer, Semin. Cell Dev. Biol., 40, 72, 10.1016/j.semcdb.2015.02.009 Zhu, 2019, Exosomes from nicotine-stimulated macrophages accelerate atherosclerosis through miR-21-3p/PTEN-mediated VSMC migration and proliferation, Theranostics, 9, 6901, 10.7150/thno.37357 Zhang, 2015, Exosome and exosomal microRNA: trafficking, sorting, and function, Dev. Reprod. Biol., 13, 17 Bobrie, 2011, Exosome secretion: molecular mechanisms and roles in immune responses, Traffic, 12, 1659, 10.1111/j.1600-0854.2011.01225.x Zakharova, 2007, T cell exosomes induce cholesterol accumulation in human monocytes via phosphatidylserine receptor, J. Cell. Physiol., 212, 174, 10.1002/jcp.21013 Yellon, 2014, Exosomes: nanoparticles involved in cardioprotection?, Circ. Res., 114, 325, 10.1161/CIRCRESAHA.113.300636 Zhang, 2019, Exosomes: biogenesis, biologic function and clinical potential, Cell Biosci., 9, 19, 10.1186/s13578-019-0282-2 Vlassov, 2012, Exosomes: current knowledge of their composition, biological functions, and diagnostic and therapeutic potentials, Biochim. Biophys. Acta, 1820, 940, 10.1016/j.bbagen.2012.03.017 Waldenstrom, 2014, Role of exosomes in myocardial remodeling, Circ. Res., 114, 315, 10.1161/CIRCRESAHA.114.300584 Skog, 2008, Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers, Nat. Cell Biol., 10, 1470, 10.1038/ncb1800 Valadi, 2007, Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells, Nat. Cell Biol., 9, 654, 10.1038/ncb1596 Kogure, 2013, Extracellular vesicle-mediated transfer of a novel long noncoding RNA TUC339: a mechanism of intercellular signaling in human hepatocellular cancer, Genes Cancer, 4, 261, 10.1177/1947601913499020 Conigliaro, 2015, CD90+ liver cancer cells modulate endothelial cell phenotype through the release of exosomes containing H19 lncRNA, Mol. Cancer, 14, 155, 10.1186/s12943-015-0426-x Li, 2015, Circular RNA is enriched and stable in exosomes: a promising biomarker for cancer diagnosis, Cell Res., 25, 981, 10.1038/cr.2015.82 Kedjouar, 2004, Molecular characterization of the microsomal tamoxifen binding site, J. Biol. Chem., 279, 34048, 10.1074/jbc.M405230200 de Medina, 2011, Importance of cholesterol and oxysterols metabolism in the pharmacology of tamoxifen and other AEBS ligands, Chem. Phys. Lipids, 164, 432, 10.1016/j.chemphyslip.2011.05.005 Bradley, 2015, Histone deacetylases in bone development and skeletal disorders, Physiol. Rev., 95, 1359, 10.1152/physrev.00004.2015 Qin, 2016, Exosome: a novel approach to stimulate bone regeneration through regulation of osteogenesis and angiogenesis, Int. J. Mol. Sci., 17, 10.3390/ijms17050712 Gerber, 1999, VEGF couples hypertrophic cartilage remodeling, ossification and angiogenesis during endochondral bone formation, Nat. Med., 5, 623, 10.1038/9467 Qin, 2016, Bone marrow stromal/stem cell-derived extracellular vesicles regulate osteoblast activity and differentiation in vitro and promote bone regeneration in vivo, Sci. Rep., 6 Lu, 2017, Priming adipose stem cells with tumor necrosis factor-alpha preconditioning potentiates their exosome efficacy for bone regeneration, Tissue Eng., 23, 1212, 10.1089/ten.tea.2016.0548 Zhao, 2018, Exosomes derived from bone marrow mesenchymal stem cells improve osteoporosis through promoting osteoblast proliferation via MAPK pathway, Eur. Rev. Med. Pharmacol. Sci., 22, 3962 Cui, 2016, Exosomes derived from mineralizing osteoblasts promote ST2 cell osteogenic differentiation by alteration of microRNA expression, FEBS Lett., 590, 185, 10.1002/1873-3468.12024 Narayanan, 2016, Hijacking the cellular mail: exosome mediated differentiation of mesenchymal stem cells, Stem Cell. Int., 2016 Xu, 2014, Altered microRNA expression profile in exosomes during osteogenic differentiation of human bone marrow-derived mesenchymal stem cells, PLoS One, 9, 10.1371/journal.pone.0114627 Wei, 2014, let-7 enhances osteogenesis and bone formation while repressing adipogenesis of human stromal/mesenchymal stem cells by regulating HMGA2, Stem Cell. Dev., 23, 1452, 10.1089/scd.2013.0600 Zhang, 2014, A signal-amplification circuit between miR-218 and Wnt/β-catenin signal promotes human adipose tissue-derived stem cells osteogenic differentiation, Bone, 58, 59, 10.1016/j.bone.2013.09.015 Schaap-Oziemlak, 2010, MicroRNA hsa-miR-135b regulates mineralization in osteogenic differentiation of human unrestricted somatic stem cells, Stem Cell. Dev., 19, 877, 10.1089/scd.2009.0112 Bakhshandeh, 2012, Down-regulation of miRNA-221 triggers osteogenic differentiation in human stem cells, Biotechnol. Lett., 34, 1579, 10.1007/s10529-012-0934-3 Xu, 2018, Exosomes from C2C12 myoblasts enhance osteogenic differentiation of MC3T3-E1 pre-osteoblasts by delivering miR-27a-3p, Biochem. Biophys. Res. Commun., 498, 32, 10.1016/j.bbrc.2018.02.144 Qi, 2016, Exosomes secreted by human-induced pluripotent stem cell-derived mesenchymal stem cells repair critical-sized bone defects through enhanced angiogenesis and osteogenesis in osteoporotic rats, Int. J. Biol. Sci., 12, 836, 10.7150/ijbs.14809 O'Sullivan, 2011, Mesenchymal chondroprogenitor cell origin and therapeutic potential, Stem Cell Res. Ther., 2, 8, 10.1186/scrt49 Zou, 2018, Progress of co-culture systems in cartilage regeneration, Expet Opin. Biol. Ther., 18, 1151, 10.1080/14712598.2018.1533116 Zhang, 2014, Regeneration of human-ear-shaped cartilage by co-culturing human microtia chondrocytes with BMSCs, Biomaterials, 35, 4878, 10.1016/j.biomaterials.2014.02.043 Cosenza, 2017, Mesenchymal stem cells derived exosomes and microparticles protect cartilage and bone from degradation in osteoarthritis, Sci. Rep., 7, 10.1038/s41598-017-15376-8 Zhu, 2017, Comparison of exosomes secreted by induced pluripotent stem cell-derived mesenchymal stem cells and synovial membrane-derived mesenchymal stem cells for the treatment of osteoarthritis, Stem Cell Res. Ther., 8, 64, 10.1186/s13287-017-0510-9 Wu, 2019, miR-100-5p-abundant exosomes derived from infrapatellar fat pad MSCs protect articular cartilage and ameliorate gait abnormalities via inhibition of mTOR in osteoarthritis, Biomaterials, 206, 87, 10.1016/j.biomaterials.2019.03.022 Mao, 2018, Exosomal miR-95-5p regulates chondrogenesis and cartilage degradation via histone deacetylase 2/8, J. Cell Mol. Med., 22, 5354, 10.1111/jcmm.13808 Li, 2020, Chondrocytes-derived exosomal miR-8485 regulated the Wnt/beta-catenin pathways to promote chondrogenic differentiation of BMSCs, Biochem. Biophys. Res. Commun., 523, 506, 10.1016/j.bbrc.2019.12.065 Yan, 2019, Vascularized 3D printed scaffolds for promoting bone regeneration, Biomaterials, 190–191, 97, 10.1016/j.biomaterials.2018.10.033 Xie, 2017, Extracellular vesicle-functionalized decalcified bone matrix scaffolds with enhanced pro-angiogenic and pro-bone regeneration activities, Sci. Rep., 7 Liu, 2017, Exosomes secreted from human-induced pluripotent stem cell-derived mesenchymal stem cells prevent osteonecrosis of the femoral head by promoting angiogenesis, Int. J. Biol. Sci., 13, 232, 10.7150/ijbs.16951 Zhang, 2019, Exosomes from human umbilical cord mesenchymal stem cells enhance fracture healing through HIF-1alpha-mediated promotion of angiogenesis in a rat model of stabilized fracture, Cell Prolif, 52, 10.1111/cpr.12570 Chen, 2016, Upregulating hif-1α by hydrogel nanofibrous scaffolds for rapidly recruiting angiogenesis relative cells in diabetic wound, Adv. Healthc. Mater., 5, 907, 10.1002/adhm.201501018 Walsh, 2018, Updating osteoimmunology: regulation of bone cells by innate and adaptive immunity, Nat. Rev. Rheumatol., 14, 146, 10.1038/nrrheum.2017.213 Bai, 2020, Biomimetic osteogenic peptide with mussel adhesion and osteoimmunomodulatory functions to ameliorate interfacial osseointegration under chronic inflammation, Biomaterials, 255, 10.1016/j.biomaterials.2020.120197 Jin, 2019, A biomimetic hierarchical nanointerface orchestrates macrophage polarization and mesenchymal stem cell recruitment to promote endogenous bone regeneration, ACS Nano, 13, 6581, 10.1021/acsnano.9b00489 Horwood, 2016, Macrophage polarization and bone formation: a review, Clin. Rev. Allergy Immunol., 51, 79, 10.1007/s12016-015-8519-2 Chen, 2015, The effect of osteoimmunomodulation on the osteogenic effects of cobalt incorporated beta-tricalcium phosphate, Biomaterials, 61, 126, 10.1016/j.biomaterials.2015.04.044 Gu, 2017, Macrophages and bone inflammation, J. Orthop. Translat., 10, 86, 10.1016/j.jot.2017.05.002 Liu, 2021, A novel delivery nanobiotechnology: engineered miR-181b exosomes improved osteointegration by regulating macrophage polarization, J. Nanobiotechnol., 19, 269, 10.1186/s12951-021-01015-y Zhao, 2020, Tumor-derived exosomal miR-934 induces macrophage M2 polarization to promote liver metastasis of colorectal cancer, J. Hematol. Oncol., 13, 156, 10.1186/s13045-020-00991-2 Nakao, 2021, Exosomes from TNF-α-treated human gingiva-derived MSCs enhance M2 macrophage polarization and inhibit periodontal bone loss, Acta Biomater., 122, 306, 10.1016/j.actbio.2020.12.046 Fan, 2020, Generation of small RNA-modulated exosome mimetics for bone regeneration, ACS Nano, 14, 11973, 10.1021/acsnano.0c05122 DeCastro, 2021, The microfluidic toolbox for analyzing exosome biomarkers of aging, Molecules, 26, 10.3390/molecules26030535 MacNeil, 2007, Progress and opportunities for tissue-engineered skin, Nature, 445, 874, 10.1038/nature05664 Germain, 2000, Can we produce a human corneal equivalent by tissue engineering?, Prog. Retin. Eye Res., 19, 497, 10.1016/S1350-9462(00)00005-7 Roseti, 2017, Scaffolds for bone tissue engineering: state of the art and new perspectives, Mater. Sci. Eng. C Mater. Biol. Appl., 78, 1246, 10.1016/j.msec.2017.05.017 Sacks, 2009, Bioengineering challenges for heart valve tissue engineering, Annu. Rev. Biomed. Eng., 11, 289, 10.1146/annurev-bioeng-061008-124903 Ouyang, 2022, Minimally invasive nanomedicine: nanotechnology in photo-/ultrasound-/radiation-/magnetism-mediated therapy and imaging, Chem. Soc. Rev., 51, 4996, 10.1039/D1CS01148K Zhang, 2021, Electroactive electrospun nanofibers for tissue engineering, Nano Today, 39, 10.1016/j.nantod.2021.101196 Hosseini, 2019, Current progress in hepatic tissue regeneration by tissue engineering, J. Transl. Med., 17, 383, 10.1186/s12967-019-02137-6 Amiel, 2000, Renal therapy using tissue-engineered constructs and gene delivery, World J. Urol., 18, 71, 10.1007/s003450050013 Zhang, 2021, Micro/nano-textured hierarchical titanium topography promotes exosome biogenesis and secretion to improve osseointegration, J. Nanobiotechnol., 19, 78, 10.1186/s12951-021-00826-3 Zhai, 2020, Human mesenchymal stem cell derived exosomes enhance cell-free bone regeneration by altering their miRNAs profiles, Adv. Sci. (Weinh), 7 Wu, 2020, Schwann Cell-derived exosomes promote bone regeneration and repair by enhancing the biological activity of porous Ti6Al4V scaffolds, Biochem. Biophys. Res. Commun., 531, 559, 10.1016/j.bbrc.2020.07.094 Wei, 2019, Exosome-integrated titanium oxide nanotubes for targeted bone regeneration, Acta Biomater., 86, 480, 10.1016/j.actbio.2019.01.006 Kang, 2022, Exosome-functionalized magnesium-organic framework-based scaffolds with osteogenic, angiogenic and anti-inflammatory properties for accelerated bone regeneration, Bioact. Mater., 18, 26, 10.1016/j.bioactmat.2022.02.012 Zhang, 2016, Exosomes/tricalcium phosphate combination scaffolds can enhance bone regeneration by activating the PI3K/Akt signaling pathway, Stem Cell Res. Ther., 7, 136, 10.1186/s13287-016-0391-3 Wu, 2019, Exosomes secreted by stem cells from human exfoliated deciduous teeth promote alveolar bone defect repair through the regulation of angiogenesis and osteogenesis, ACS Biomater. Sci. Eng., 5, 3561, 10.1021/acsbiomaterials.9b00607 Liang, 2019, Dimethyloxaloylglycine-stimulated human bone marrow mesenchymal stem cell-derived exosomes enhance bone regeneration through angiogenesis by targeting the AKT/mTOR pathway, Stem Cell Res. Ther., 10, 335, 10.1186/s13287-019-1410-y Liu, 2021, Optimized BMSC-derived osteoinductive exosomes immobilized in hierarchical scaffold via lyophilization for bone repair through Bmpr2/Acvr2b competitive receptor-activated Smad pathway, Biomaterials, 272, 10.1016/j.biomaterials.2021.120718 Jiang, 2021, Enhancement of acellular cartilage matrix scaffold by Wharton's jelly mesenchymal stem cell-derived exosomes to promote osteochondral regeneration, Bioact. Mater., 6, 2711, 10.1016/j.bioactmat.2021.01.031 Hu, 2021, Exosome-guided bone targeted delivery of Antagomir-188 as an anabolic therapy for bone loss, Bioact. Mater., 6, 2905, 10.1016/j.bioactmat.2021.02.014 Zha, 2021, Progenitor cell-derived exosomes endowed with VEGF plasmids enhance osteogenic induction and vascular remodeling in large segmental bone defects, Theranostics, 11, 397, 10.7150/thno.50741 Lu, 2021, Modulatory role of silver nanoparticles and mesenchymal stem cell-derived exosome-modified barrier membrane on macrophages and osteogenesis, Front. Chem., 9, 10.3389/fchem.2021.699802 Diomede, 2018, Three-dimensional printed PLA scaffold and human gingival stem cell-derived extracellular vesicles: a new tool for bone defect repair, Stem Cell Res. Ther., 9, 104, 10.1186/s13287-018-0850-0 Gandolfi, 2020, Mineral-doped poly(L-lactide) acid scaffolds enriched with exosomes improve osteogenic commitment of human adipose-derived mesenchymal stem cells, Nanomaterials (Basel), 10, 10.3390/nano10030432 Li, 2018, Tissue-engineered bone immobilized with human adipose stem cells-derived exosomes promotes bone regeneration, ACS Appl. Mater. Interfaces, 10, 5240, 10.1021/acsami.7b17620 Gao, 2022, Bioinspired porous microspheres for sustained hypoxic exosomes release and vascularized bone regeneration, Bioact. Mater., 14, 377, 10.1016/j.bioactmat.2022.01.041 Fan, 2021, Exosome-functionalized polyetheretherketone-based implant with immunomodulatory property for enhancing osseointegration, Bioact. Mater., 6, 2754, 10.1016/j.bioactmat.2021.02.005 Swanson, 2020, Scaffolds with controlled release of pro-mineralization exosomes to promote craniofacial bone healing without cell transplantation, Acta Biomater., 118, 215, 10.1016/j.actbio.2020.09.052 Chen, 2019, Exosomes derived from miR-375-overexpressing human adipose mesenchymal stem cells promote bone regeneration, Cell Prolif., 52, 10.1111/cpr.12669 Zhang, 2021, Umbilical mesenchymal stem cell-derived exosome-encapsulated hydrogels accelerate bone repair by enhancing angiogenesis, ACS Appl. Mater. Interfaces, 13, 18472, 10.1021/acsami.0c22671 Li, 2022, Exosomes from adipose-derived stem cells regulate M1/M2 macrophage phenotypic polarization to promote bone healing via miR-451a/MIF, Stem Cell Res. Ther., 13, 149, 10.1186/s13287-022-02823-1 Yang, 2020, Integration of human umbilical cord mesenchymal stem cells-derived exosomes with hydroxyapatite-embedded hyaluronic acid-alginate hydrogel for bone regeneration, ACS Biomater. Sci. Eng., 6, 1590, 10.1021/acsbiomaterials.9b01363 Wang, 2020, A new self-healing hydrogel containing hucMSC-derived exosomes promotes bone regeneration, Front. Bioeng. Biotechnol., 8, 10.3389/fbioe.2020.564731 Liu, 2017, Integration of stem cell-derived exosomes with in situ hydrogel glue as a promising tissue patch for articular cartilage regeneration, Nanoscale, 9, 4430, 10.1039/C7NR00352H Zhang, 2021, Injectable Mussel-Inspired highly adhesive hydrogel with exosomes for endogenous cell recruitment and cartilage defect regeneration, Biomaterials, 278, 10.1016/j.biomaterials.2021.121169 Chen, 2019, Desktop-stereolithography 3D printing of a radially oriented extracellular matrix/mesenchymal stem cell exosome bioink for osteochondral defect regeneration, Theranostics, 9, 2439, 10.7150/thno.31017 Tao, 2021, Small extracellular vesicles in combination with sleep-related circRNA3503: a targeted therapeutic agent with injectable thermosensitive hydrogel to prevent osteoarthritis, Bioact. Mater., 6, 4455, 10.1016/j.bioactmat.2021.04.031 Ma, 2022, Smart μ-fiber hydrogels with macro-porous structure for sequentially promoting multiple phases of articular cartilage regeneration, Adv. Funct. Mater., 32, 10.1002/adfm.202113380 Kapanen, 2001, Effect of nickel-titanium shape memory metal alloy on bone formation, Biomaterials, 22, 2475, 10.1016/S0142-9612(00)00435-X Long, 1998, Titanium alloys in total joint replacement--a materials science perspective, Biomaterials, 19, 1621, 10.1016/S0142-9612(97)00146-4 Yazdimamaghani, 2017, Porous magnesium-based scaffolds for tissue engineering, Mater. Sci. Eng. C Mater. Biol. Appl., 71, 1253, 10.1016/j.msec.2016.11.027 Liao, 2013, Novel polypropylene biocomposites reinforced with carbon nanotubes and hydroxyapatite nanorods for bone replacements, Mater. Sci. Eng. C Mater. Biol. Appl., 33, 1380, 10.1016/j.msec.2012.12.039 Chang, 1996, Significance of interstitial bone ingrowth under load-bearing conditions: a comparison between solid and porous implant materials, Biomaterials, 17, 1141, 10.1016/0142-9612(96)85917-5 Hu, 2020, Enhanced interfacial adhesion and osseointegration of anodic TiO(2) nanotube arrays on ultra-fine-grained titanium and underlying mechanisms, Acta Biomater., 106, 360, 10.1016/j.actbio.2020.02.009 Mei, 2014, Antibacterial effects and biocompatibility of titanium surfaces with graded silver incorporation in titania nanotubes, Biomaterials, 35, 4255, 10.1016/j.biomaterials.2014.02.005 Liu, 2021, Pnictogens in medicinal chemistry: evolution from erstwhile drugs to emerging layered photonic nanomedicine, Chem. Soc. Rev., 50, 2260, 10.1039/D0CS01175D Zhang, 2021, Nanoscale materials-based platforms for the treatment of bone-related diseases, Matter, 4, 2727, 10.1016/j.matt.2021.05.019 Okuda, 2007, The effect of the microstructure of beta-tricalcium phosphate on the metabolism of subsequently formed bone tissue, Biomaterials, 28, 2612, 10.1016/j.biomaterials.2007.01.040 Wang, 1998, Biological evaluation of biphasic calcium phosphate ceramic vertebral laminae, Biomaterials, 19, 1387, 10.1016/S0142-9612(98)00014-3 Le Nihouannen, 2007, Interactions of total bone marrow cells with increasing quantities of macroporous calcium phosphate ceramic granules, J. Mater. Sci. Mater. Med., 18, 1983, 10.1007/s10856-007-3098-2 Horch, 2006, Synthetic, pure-phase beta-tricalcium phosphate ceramic granules (Cerasorb) for bone regeneration in the reconstructive surgery of the jaws, Int. J. Oral Maxillofac. Surg., 35, 708, 10.1016/j.ijom.2006.03.017 Handschel, 2002, TCP is hardly resorbed and not osteoconductive in a non-loading calvarial model, Biomaterials, 23, 1689, 10.1016/S0142-9612(01)00296-4 Fu, 2018, Runx2/Osterix and zinc uptake synergize to orchestrate osteogenic differentiation and citrate containing bone apatite formation, Adv. Sci. (Weinh), 5 Chen, 2011, The role of surface charge on the uptake and biocompatibility of hydroxyapatite nanoparticles with osteoblast cells, Nanotechnology, 22, 10.1088/0957-4484/22/10/105708 Kumar Saini, 2019, Nano-silver hydroxyapatite based antibacterial 3D scaffolds of gelatin/alginate/poly (vinyl alcohol) for bone tissue engineering applications, Colloids Surf. B Biointerfaces, 177, 211, 10.1016/j.colsurfb.2019.01.064 Ji, 2020, Mesenchymal stem cell-loaded thermosensitive hydroxypropyl chitin hydrogel combined with a three-dimensional-printed poly(epsilon-caprolactone)/nano-hydroxyapatite scaffold to repair bone defects via osteogenesis, angiogenesis and immunomodulation, Theranostics, 10, 725, 10.7150/thno.39167 Morishita, 2006, Tissue engineering approach to the treatment of bone tumors: three cases of cultured bone grafts derived from patients' mesenchymal stem cells, Artif. Organs, 30, 115, 10.1111/j.1525-1594.2006.00190.x Liao, 2018, Preparation, bioactivity and mechanism of nano-hydroxyapatite/sodium alginate/chitosan bone repair material, J. Appl. Biomater. Funct. Mater., 16, 28 Zhou, 2019, Hierarchically porous hydroxyapatite hybrid scaffold incorporated with reduced graphene oxide for rapid bone ingrowth and repair, ACS Nano, 13, 9595, 10.1021/acsnano.9b04723 Ducheyne, 1999, Bioactive ceramics: the effect of surface reactivity on bone formation and bone cell function, Biomaterials, 20, 2287, 10.1016/S0142-9612(99)00181-7 Montazerian, 2016, History and trends of bioactive glass-ceramics, J. Biomed. Mater. Res., 104, 1231, 10.1002/jbm.a.35639 Fu, 2010, Silicate, borosilicate, and borate bioactive glass scaffolds with controllable degradation rate for bone tissue engineering applications. I. Preparation and in vitro degradation, J. Biomed. Mater. Res., 95, 164, 10.1002/jbm.a.32824 Brown, 2009, Effect of borate glass composition on its conversion to hydroxyapatite and on the proliferation of MC3T3-E1 cells, J. Biomed. Mater. Res., 88, 392, 10.1002/jbm.a.31679 Huang, 2006, Kinetics and mechanisms of the conversion of silicate (45S5), borate, and borosilicate glasses to hydroxyapatite in dilute phosphate solutions, J. Mater. Sci. Mater. Med., 17, 583, 10.1007/s10856-006-9220-z Delahaye, 1999, Dissolution of (50-x)Na2O-xCaO-50P(2)O(5) metaphosphate glasses in different saline solutions: mechanism and kinetic control, Glass Sci. Technol.-Glastechnische Berichte, 72, 161 Abou Neel, 2009, Structure and properties of strontium-doped phosphate-based glasses, J. R. Soc. Interface, 6, 435, 10.1098/rsif.2008.0348 Salih, 2000, Development of soluble glasses for biomedical use Part II: the biological response of human osteoblast cell lines to phosphate-based soluble glasses, J. Mater. Sci. Mater. Med., 11, 615, 10.1023/A:1008901612674 da Silva, 2003, Electrochemical oxidation of biological molecules at carbon paste electrodes pre-treated in guanine solutions, J. Pharm. Biomed. Anal., 33, 735, 10.1016/S0731-7085(03)00296-6 Zhu, 2019, In vivo engineered extracellular matrix scaffolds with instructive niches for oriented tissue regeneration, Nat. Commun., 10, 4620, 10.1038/s41467-019-12545-3 Font Tellado, 2015, Strategies to engineer tendon/ligament-to-bone interface: biomaterials, cells and growth factors, Adv. Drug Deliv. Rev., 94, 126, 10.1016/j.addr.2015.03.004 Gabizon, 1989, Pharmacokinetics and tissue distribution of doxorubicin encapsulated in stable liposomes with long circulation times, J. Natl. Cancer Inst., 81, 1484, 10.1093/jnci/81.19.1484 Cheng, 2020, Advanced liposome-loaded scaffolds for therapeutic and tissue engineering applications, Biomaterials, 232, 10.1016/j.biomaterials.2019.119706 Perumal, 2020, Synthesis of magnesium phosphate nanoflakes and its PCL composite electrospun nanofiber scaffolds for bone tissue regeneration, Mater. Sci. Eng. C Mater. Biol. Appl., 109, 10.1016/j.msec.2019.110527 Constantinides, 2018, Vivo tracking and (1)H/(19)F magnetic resonance imaging of biodegradable polyhydroxyalkanoate/polycaprolactone blend scaffolds seeded with labeled cardiac stem cells, ACS Appl. Mater. Interfaces, 10, 25056, 10.1021/acsami.8b06096 Fu, 2014, Electrospun gelatin/PCL and collagen/PLCL scaffolds for vascular tissue engineering, Int. J. Nanomed., 9, 2335, 10.2147/IJN.S61375 Shafei, 2017, Electroactive nanostructured scaffold produced by controlled deposition of PPy on electrospun PCL fibres, Res. Chem. Intermed., 43, 1235, 10.1007/s11164-016-2695-4 Hassanajili, 2019, Preparation and characterization of PLA/PCL/HA composite scaffolds using indirect 3D printing for bone tissue engineering, Mater. Sci. Eng. C Mater. Biol. Appl., 104, 10.1016/j.msec.2019.109960 Xue, 2017, Polycaprolactone nanofiber scaffold enhances the osteogenic differentiation potency of various human tissue-derived mesenchymal stem cells, Stem Cell Res. Ther., 8, 148, 10.1186/s13287-017-0588-0 Dorozhkin, 2015, Calcium orthophosphate-containing biocomposites and hybrid biomaterials for biomedical applications, J. Funct. Biomater., 6, 708, 10.3390/jfb6030708 Larsen, 2005, Fixation of osteochondritis dissecans lesions using poly(l-lactic acid)/poly(glycolic acid) copolymer bioabsorbable screws, Am. J. Sports Med., 33, 68, 10.1177/0363546504265927 Athanasiou, 1998, Orthopaedic applications for PLA-PGA biodegradable polymers, Arthroscopy, 14, 726, 10.1016/S0749-8063(98)70099-4 Baptista, 2021, Morphological and mechanical characterization of 3D printed PLA scaffolds with controlled porosity for trabecular bone tissue replacement, Mater. Sci. Eng. C Mater. Biol. Appl., 118, 10.1016/j.msec.2020.111528 Singhvi, 2019, Polylactic acid: synthesis and biomedical applications, J. Appl. Microbiol., 127, 1612, 10.1111/jam.14290 Tyler, 2016, Polylactic acid (PLA) controlled delivery carriers for biomedical applications, Adv. Drug Deliv. Rev., 107, 163, 10.1016/j.addr.2016.06.018 Mooney, 1996, Stabilized polyglycolic acid fibre-based tubes for tissue engineering, Biomaterials, 17, 115, 10.1016/0142-9612(96)85756-5 Martin, 1996, Acidity near eroding polylactide-polyglycolide in vitro and in vivo in rabbit tibial bone chambers, Biomaterials, 17, 2373, 10.1016/S0142-9612(96)00075-0 Rezwan, 2006, Biodegradable and bioactive porous polymer/inorganic composite scaffolds for bone tissue engineering, Biomaterials, 27, 3413, 10.1016/j.biomaterials.2006.01.039 Felix Lanao, 2013, Physicochemical properties and applications of poly(lactic-co-glycolic acid) for use in bone regeneration, Tissue Eng. B Rev., 19, 380, 10.1089/ten.teb.2012.0443 Gentile, 2014, An overview of poly(lactic-co-glycolic) acid (PLGA)-based biomaterials for bone tissue engineering, Int. J. Mol. Sci., 15, 3640, 10.3390/ijms15033640 Wu, 2006, Bone tissue engineering evaluation based on rat calvaria stromal cells cultured on modified PLGA scaffolds, Biomaterials, 27, 896, 10.1016/j.biomaterials.2005.07.002 Thomson, 1998, Hydroxyapatite fiber reinforced poly(alpha-hydroxy ester) foams for bone regeneration, Biomaterials, 19, 1935, 10.1016/S0142-9612(98)00097-0 Wu, 2009, The effect of mesoporous bioactive glass on the physiochemical, biological and drug-release properties of poly(DL-lactide-co-glycolide) films, Biomaterials, 30, 2199, 10.1016/j.biomaterials.2009.01.029 Gu, 2020, Bioinspired modifications of PEEK implants for bone tissue engineering, Front. Bioeng. Biotechnol., 8 Lee, 2001, Hydrogels for tissue engineering, Chem. Rev., 101, 1869, 10.1021/cr000108x Peppas, 2006, Hydrogels in biology and medicine: from molecular principles to bionanotechnology, Adv. Mater., 18, 1345, 10.1002/adma.200501612 Liu, 2018, Cardiac recovery via extended cell-free delivery of extracellular vesicles secreted by cardiomyocytes derived from induced pluripotent stem cells, Nat Biomed Eng, 2, 293, 10.1038/s41551-018-0229-7 Zhang, 2011, Synthesis of multiresponsive and dynamic chitosan-based hydrogels for controlled release of bioactive molecules, Biomacromolecules, 12, 2894, 10.1021/bm200423f Guan, 2022, Exosome-loaded extracellular matrix-mimic hydrogel with anti-inflammatory property Facilitates/promotes growth plate injury repair, Bioact. Mater., 10, 145, 10.1016/j.bioactmat.2021.09.010 Hosseinzadeh, 2016, Apoptosis signaling pathways in osteoarthritis and possible protective role of melatonin, J. Pineal Res., 61, 411, 10.1111/jpi.12362