Strategies to direct vascularisation using mesoporous bioactive glass-based biomaterials for bone regeneration

References

• Jain RK, Au P, Tam J, et al. Engineering vascularized tissue. Nat Biotechnol. 2005;23(7):821–823.
   PubMed Web of Science ®Google Scholar
• Santos MI, Reis RL. Vascularization in bone tissue engineering: physiology, current strategies, major hurdles and future challenges. Macromol Biosci. 2010;10(1):12–27.
   PubMed Web of Science ®Google Scholar
• Amini AR, Laurencin CT, Nukavarapu SP. Bone tissue engineering: recent advances and challenges. Crit Rev Biomed Eng. 2012;40(5):363–408.
   PubMedGoogle Scholar
• Stevens MM. Biomaterial for bone tissue engineering. Materials Today. 2008;11(5):18–25.
   Web of Science ®Google Scholar
• Hench LL, Polak JM. Third-generation biomedical materials. Science. 2002;295(5557):1014.
   PubMed Web of Science ®Google Scholar
• Hench LL, Jones JR. Bioactive glasses: frontiers and challenges. Front Bioeng Biotechnol. 2015;3:156.
   PubMedGoogle Scholar
• Hench LL. Opening paper 2015-Some comments on Bioglass: Four Eras of Discovery and Development. Biomed Glasses. 2015;1(1).
   Google Scholar
• Jones JR. Review of bioactive glass: from Hench to hybrids. Acta Biomater. 2013;9(1):4457–4486.
   PubMed Web of Science ®Google Scholar
• Jones JR, Ehrenfried LM, Hench LL. Optimising bioactive glass scaffolds for bone tissue engineering. Biomaterials. 2006;27(7):964–973.
   PubMed Web of Science ®Google Scholar
• Chen QZ, Thompson ID, Boccaccini AR. 45S5 Bioglass-derived glass-ceramic scaffolds for bone tissue engineering. Biomaterials. 2006;27(11):2414–2425.
   PubMed Web of Science ®Google Scholar
• Wu ZY, Hill RG, Yue S, et al. Melt-derived bioactive glass scaffolds produced by a gel-cast foaming technique. Acta Biomater. 2011;7(4):1807–1816.
   PubMed Web of Science ®Google Scholar
• Fu Q, Saiz E, Tomsia AP. Bioinspired strong and highly porous glass scaffolds. Adv Funct Mater. 2011;21(6):1058–1063.
   PubMed Web of Science ®Google Scholar
• Gorustovich AA, Roether JA, Boccaccini AR. Effect of bioactive glasses on angiogenesis: a review of in vitro and in vivo evidences. Tissue Eng Part B Rev. 2010;16(2):199–207.
   PubMed Web of Science ®Google Scholar
• Izquierdo-Barba I, Vallet-Regí M. Mesoporous bioactive glasses: relevance of their porous structure compared to that of classical bioglasses. Biomed Glasses. 2015;1(1):140–150.
   Google Scholar
• Wu C, Chang J. Mesoporous bioactive glasses: structure characteristics, drug/growth factor delivery and bone regeneration application. Interface Focus. 2012;2(3):292–306.
   PubMed Web of Science ®Google Scholar
• Taylor D, Hazenberg JG, Lee TC. Living with cracks: damage and repair in human bone. Nat Mater. 2007;6(4):263–268.
   PubMed Web of Science ®Google Scholar
• Roberts TT, Rosenbaum AJ. Bone grafts, bone substitutes and orthobiologics: the bridge between basic science and clinical advancements in fracture healing. Organogenesis. 2012;8(4):114–124.
   PubMed Web of Science ®Google Scholar
• Schwartz CE, Martha JF, Kowalski P, et al. Prospective evaluation of chronic pain associated with posterior autologous iliac crest bone graft harvest and its effect on postoperative outcome. Health Qual Life Outcomes. 2009;7:49.
   PubMed Web of Science ®Google Scholar
• Dimitriou R, Mataliotakis GI, Angoules AG, et al. Complications following autologous bone graft harvesting from the iliac crest and using the RIA: a systematic review. Injury. 2011;42(Suppl 2):S3–S15.
   PubMed Web of Science ®Google Scholar
• Zimmermann G, Moghaddam A. Allograft bone matrix versus synthetic bone graft substitutes. Injury. 2011;42(Suppl 2):S16–S21.
   PubMed Web of Science ®Google Scholar
• Nguyen LH, Annabi N, Nikkhah M, et al. Vascularized bone tissue engineering: approaches for potential improvement. Tissue Eng Part B Rev. 2012;18(5):363–382.
   PubMed Web of Science ®Google Scholar
• Liu Y, Chan JK, Teoh SH. Review of vascularised bone tissue-engineering strategies with a focus on co-culture systems. J Tissue Eng Regen Med. 2015;9(2):85–105.
   PubMed Web of Science ®Google Scholar
• Chen FM, Shelton RM, Jin Y, et al. Localized delivery of growth factors for periodontal tissue regeneration: role, strategies, and perspectives. Med Res Rev. 2009;29(3):472–513.
   PubMed Web of Science ®Google Scholar
• Zisch AH, Lutolf MP, Hubbell JA. Biopolymeric delivery matrices for angiogenic growth factors. Cardiovasc Pathol. 2003;12(6):295–310.
   PubMed Web of Science ®Google Scholar
• Yang P, Gai S, Lin J. Functionalized mesoporous silica materials for controlled drug delivery. Chem Soc Rev. 2012;41(9):3679.
   PubMed Web of Science ®Google Scholar
• Hench LL, Splinter RJ, Allen WC, et al. Bonding mechanisms at the interface of ceramic prosthetic materials. J Biomed Mater Res A. 1971;5(6):117–141.
   Google Scholar
• Hench LL. Bioceramics: from concept to clinic. J Am Ceram Soc. 1991;74(7):1487–1510.
   Web of Science ®Google Scholar
• Rahaman MN, Day DE, Sonny Bal B, et al. Bioactive glass in tissue engineering. Acta Biomater. 2011;7(6):2355–2373.
   PubMed Web of Science ®Google Scholar
• Oonishi H, Hench LL, Wilson J, et al. Quantitative comparison of bone growth behavior in granules of Bioglass, A-W glass-ceramic, and hydroxyapatite. J Biomed Mater Res. 2000;51(1):37–46.
   PubMed Web of Science ®Google Scholar
• Xynos ID, Hukkanen MVJ, Batten JJ, et al. Bioglass 45S5 stimulates osteoblast turnover and enhances bone formation in vitro: implications and applications for bone tissue engineering. Calcif Tissue Int. 2000;67(4):321–329.
   PubMed Web of Science ®Google Scholar
• Hamadouche M, Meunier A, Greenspan DC, et al. Long-term in vivo bioactivity and degradability of bulk sol-gel bioactive glasses. J Biomed Mater Res. 2001;54(4):560–566.
   PubMed Web of Science ®Google Scholar
• Ajita J, Saravanan S, Selvamurugan N. Effect of size of bioactive glass nanoparticles on mesenchymal stem cell proliferation for dental and orthopedic applications. Mater Sci Eng C Mater Biol Appl. 2015;53:142–149.
   PubMed Web of Science ®Google Scholar
• Brink M. The influence of alkali and alkaline earths on the working range for bioactive glasses. J Biomed Mater Res. 1997;36(1):109–117.
   PubMed Web of Science ®Google Scholar
• Liang W, Rahaman MN, Day DE, et al. Bioactive borate glass scaffold for bone tissue engineering. J Non-Cryst Solids. 2008;354(15–16):1690–1696.
   Web of Science ®Google Scholar
• Fu H, Fu Q, Zhou N, et al. In vitro evaluation of borate-based bioactive glass scaffolds prepared by a polymer foam replication method. Mat Sci Eng C-Mater. 2009;29(7):2275–2281.
   Web of Science ®Google Scholar
• Gao H, Tan T, Wang D. Dissolution mechanism and release kinetics of phosphate controlled release glasses in aqueous medium. J Control Release. 2004;96(1):29–36.
   PubMed Web of Science ®Google Scholar
• Kaur G, Pandey OP, Singh K, et al. A review of bioactive glasses: their structure, properties, fabrication and apatite formation. J Biomed Mater Res A. 2014;102(1):254–274.
   PubMed Web of Science ®Google Scholar
• Sitarz M, Bulat K, Olejniczak Z. Structure and microstructure of glasses from a NaCaPO4-SiO2-BPO4 system. Vib Spectrosc. 2012;61:72–77.
   Web of Science ®Google Scholar
• Dayanand C, Bhikshamaiah G, Tyagaraju VJ, et al. Structural investigations of phosphate glasses: a detailed infrared study of the x(PbO)-(1-x)P2O5 vitreous system. J Mater Sci. 1996;31(8):1945–1967.
   Web of Science ®Google Scholar
• Martin SW. Ionic conduction in phosphate glasses. J Am Ceram Soc. 1991;74(8):1767–1784.
   Web of Science ®Google Scholar
• Li R, Clark AE, Hench LL. An investigation of bioactive glass powders by sol-gel processing. J Appl Biomater. 1991;2(4):231–239.
   PubMedGoogle Scholar
• Izquierdo-Barba I, Salinas AJ, Vallet-Regí M. Bioactive glasses: from Macro to Nano. Int J Appl Glass Sci. 2013;4(2):149–161.
   Web of Science ®Google Scholar
• Sepulveda P, Jones JR, Hench LL. Bioactive sol-gel foams for tissue repair. J Biomed Mater Res. 2002;59(2):340–348.
   PubMed Web of Science ®Google Scholar
• Hulbert SF, Morrison SJ, Klawitter JJ. Compatibility of porous ceramics with soft tissue; application to tracheal prostheses. J Biomed Mater Res. 1971;5(6):269–279.
   Google Scholar
• Vallet-Regí M, Salinas AJ, Arcos D. Tailoring the structure of bioactive glasses: from the Nanoscale to Macroporous scaffolds. Int J Appl Glass Sci. 2016;7(2):195–205.
   Web of Science ®Google Scholar
• Sepulveda P, Jones JR, Hench LL. Characterization of melt-derived 45S5 and sol-gel-derived 58S bioactive glasses. J Biomed Mater Res. 2001;58(6):734–740.
   PubMed Web of Science ®Google Scholar
• Yan X, Yu C, Zhou X, et al. Highly ordered mesoporous bioactive glasses with superior in vitro bone-forming bioactivities. Angew Chem Int Ed Engl. 2004;43(44):5980–5984.
   PubMed Web of Science ®Google Scholar
• Lin S, Ionescu C, Pike KJ, et al. Nanostructure evolution and calcium distribution in sol–gel derived bioactive glass. J Mater Chem. 2009;19(9):1276–1282.
   Web of Science ®Google Scholar
• Wu C, Fan W, Chang J. Functional mesoporous bioactive glass nanospheres: synthesis, high loading efficiency, controllable delivery of doxorubicin and inhibitory effect on bone cancer cells. J Mater Chem B. 2013;1(21):2710.
   PubMed Web of Science ®Google Scholar
• Greasley SL, Page SJ, Sirovica S, et al. Controlling particle size in the Stöber process and incorporation of calcium. J Colloid Interf Sci. 2016;469:213–223.
   PubMed Web of Science ®Google Scholar
• FitzGerald V, Martin RA, Jones JR, et al. Bioactive glass sol-gel foam scaffolds: evolution of nanoporosity during processing and in situ monitoring of apatite layer formation using small- and wide-angle X-ray scattering. J Biomed Mater Res A. 2009;91A(1):76–83.
   Web of Science ®Google Scholar
• Jung SB, et al. Treatment of non-healing diabetic venous stasis ulcers with bioactive glass nanofibers. Wound Repair Regen. 2011;19(2):A30–A30.
   Web of Science ®Google Scholar
• Poologasundarampillai G, Wang D, Li S, et al. Cotton-wool-like bioactive glasses for bone regeneration. Acta Biomater. 2014;10(8):3733–3746.
   PubMed Web of Science ®Google Scholar
• Hsu FY, Weng RC, Lin HM, et al. A biomimetic extracellular matrix composed of mesoporous bioactive glass as a bone graft material. Micropor Mesopor Mat. 2015;212:56–65.
   Web of Science ®Google Scholar
• Hong Y, Chen X, Jing X, et al. Fabrication and drug delivery of ultrathin Mesoporous bioactive glass hollow fibers. Adv Funct Mater. 2010;20(9):1503–1510.
   Web of Science ®Google Scholar
• Yun HS, Kim S, Hyun Y, et al. Hierarchically Mesoporous-Macroporous bioactive glasses scaffolds for bone tissue regeneration. J Biomed Mater Res B. 2008;87B(2):374–380.
   Web of Science ®Google Scholar
• Wu C, Zhou Y, Chang J, et al. Delivery of dimethyloxallyl glycine in mesoporous bioactive glass scaffolds to improve angiogenesis and osteogenesis of human bone marrow stromal cells. Acta Biomater. 2013;9(11):9159–9168.
   PubMed Web of Science ®Google Scholar
• Wu C, Luo Y, Cuniberti G, et al. Three-dimensional printing of hierarchical and tough mesoporous bioactive glass scaffolds with a controllable pore architecture, excellent mechanical strength and mineralization ability. Acta Biomater. 2011;7(6):2644–2650.
   PubMed Web of Science ®Google Scholar
• Rodrigues M, Griffith LG, Wells A. Growth factor regulation of proliferation and survival of multipotential stromal cells. Stem Cell Res Ther. 2010;1(4):32.
   PubMed Web of Science ®Google Scholar
• Honnami M, Choi S, Liu I, et al. Repair of rabbit segmental femoral defects by using a combination of tetrapod-shaped calcium phosphate granules and basic fibroblast growth factor-binding ion complex gel. Biomaterials. 2013;34(36):9056–9062.
   PubMed Web of Science ®Google Scholar
• Kim IG, Hwang MP, Du P, et al. Bioactive cell-derived matrices combined with polymer mesh scaffold for osteogenesis and bone healing. Biomaterials. 2015;50:75–86.
   PubMed Web of Science ®Google Scholar
• Nevins M, Kao RT, McGuire MK, et al. Platelet-derived growth factor promotes periodontal regeneration in localized osseous defects: 36-month extension results from a randomized, controlled, double-masked clinical trial. J Periodontol. 2013;84(4):456–464.
   PubMed Web of Science ®Google Scholar
• Gao C, et al. MSC-seeded dense collagen scaffolds with a bolus dose of VEGF promote healing of large bone defects. Eur Cell Mater. 2013;26:195–207.
   PubMed Web of Science ®Google Scholar
• Weiss S., Zimmermann G, Pufe T, et al. The systemic angiogenic response during bone healing. Arch Orthop Trauma Surg. 2009;129(7):989–997.
   PubMed Web of Science ®Google Scholar
• Salinas AJ, Esbrit P, Vallet-Regí M. A tissue engineering approach based on the use of bioceramics for bone repair. Biomater Sci. 2013;1:40–51.
   Web of Science ®Google Scholar
• Gerber HP, Ferrara N, Vu TH, et al. VEGF couples hypertrophic cartilage remodeling, ossification and angiogenesis during endochondral bone formation. Nat Med. 1999;5(6):623–628.
   PubMed Web of Science ®Google Scholar
• Rocha FG, Sundback CA, Krebs NJ, et al. The effect of sustained delivery of vascular endothelial growth factor on angiogenesis in tissue-engineered intestine. Biomaterials. 2008;29(19):2884–2890.
   PubMed Web of Science ®Google Scholar
• Bautch VL. VEGF-directed blood vessel patterning: from cells to organism. Cold Spring Harb Perspect Med. 2012;2(9):a006452.
   PubMed Web of Science ®Google Scholar
• Liu B, et al. VEGF expression in mesenchymal stem cells promotes bone formation of tissue-engineered bones. Mol Med Rep. 2011;4(6):1121–1126.
   PubMed Web of Science ®Google Scholar
• Fischerauer E, Heidari N, Neumayer B, et al. The spatial and temporal expression of VEGF and its receptors 1 and 2 in post-traumatic bone bridge formation of the growth plate. J Mol Histol. 2011;42(6):513–522.
   PubMed Web of Science ®Google Scholar
• Orlandini M, Spreafico A, Bardelli M, et al. Vascular endothelial growth factor-D activates VEGFR-3 expressed in osteoblasts inducing their differentiation. J Biol Chem. 2006;281(26):17961–17967.
   PubMed Web of Science ®Google Scholar
• Grellier M, Ferreira-Tojais N, Bourget C, et al. Role of vascular endothelial growth factor in the communication between human osteoprogenitors and endothelial cells. J Cell Biochem. 2009;106(3):390–398.
   PubMed Web of Science ®Google Scholar
• Street J, Bao M, deGuzman L, et al. Vascular endothelial growth factor stimulates bone repair by promoting angiogenesis and bone turnover. Proc Natl Acad Sci U S A. 2002;99(15):9656–9661.
   PubMed Web of Science ®Google Scholar
• Deckers MM, Karperien M, van der Bent C, et al. Expression of vascular endothelial growth factors and their receptors during osteoblast differentiation. Endocrinology. 2000;141(5):1667–1674.
   PubMed Web of Science ®Google Scholar
• Furumatsu T. Vascular endothelial growth factor principally acts as the main angiogenic factor in the early stage of human osteoblastogenesis. J Biochem. 2003;133(5):633–639.
   PubMed Web of Science ®Google Scholar
• Percival CJ, Richtsmeier JT. Angiogenesis and intramembranous osteogenesis. Dev Dyn. 2013;242(8):909–922.
   PubMed Web of Science ®Google Scholar
• Koch S, Claesson-Welsh L. Signal transduction by vascular endothelial growth factor receptors. Cold Spring Harb Perspect Med. 2012;2(7):a006502.
   PubMed Web of Science ®Google Scholar
• Ellis LM, Hicklin DJ. VEGF-targeted therapy: mechanisms of anti-tumour activity. Nat Rev Cancer. 2008;8(8):579–591.
   PubMed Web of Science ®Google Scholar
• Koch S, Tugues S, Li X, et al. Signal transduction by vascular endothelial growth factor receptors. Biochem J. 2011;437(2):169–183.
   PubMed Web of Science ®Google Scholar
• Nazarenko I, Hede SM, He X, et al. PDGF and PDGF receptors in glioma. Ups J Med Sci. 2012;117(2):99–112.
   PubMed Web of Science ®Google Scholar
• Xie H, Cui Z, Wang L, et al. PDGF-BB secreted by preosteoclasts induces angiogenesis during coupling with osteogenesis. Nat Med. 2014;20(11):1270–1278.
   PubMed Web of Science ®Google Scholar
• Li X, Tjwa M, Moons L, et al. Revascularization of ischemic tissues by PDGF-CC via effects on endothelial cells and their progenitors. J Clin Invest. 2005;115(1):118–127.
   PubMed Web of Science ®Google Scholar
• Heldin CH, Lennartsson J. Structural and functional properties of platelet-derived growth factor and stem cell factor receptors. Cold Spring Harb Perspect Biol. 2013;5(8):a009100.
   PubMed Web of Science ®Google Scholar
• Demoulin JB, Essaghir A. PDGF receptor signaling networks in normal and cancer cells. Cytokine Growth Factor Rev. 2014;25(3):273–283.
   PubMed Web of Science ®Google Scholar
• Andrae J, Gallini R, Betsholtz C. Role of platelet-derived growth factors in physiology and medicine. Genes Dev. 2008;22(10):1276–1312.
   PubMed Web of Science ®Google Scholar
• Carrasco-Garcia E, Saceda M, Martinez-Lacaci I. Role of receptor tyrosine kinases and their ligands in glioblastoma. Cells. 2014;3(2):199–235.
   PubMedGoogle Scholar
• Ornitz DM, Itoh N. Fibroblast growth factors. Genome Biol. 2001;2(3):reviews3005.1.
   Web of Science ®Google Scholar
• Werner S, Grose R. Regulation of wound healing by growth factors and cytokines. Physiol Rev. 2003;83(3):835–870.
   PubMed Web of Science ®Google Scholar
• Kottakis F, Polytarchou C, Foltopoulou P, et al. FGF-2 regulates cell proliferation, migration, and angiogenesis through an NDY1/KDM2B-miR-101-EZH2 pathway. Mol Cell. 2011;43(2):285–298.
   PubMed Web of Science ®Google Scholar
• Lai WT, Krishnappa V, Phinney DG. Fibroblast growth factor 2 (Fgf2) inhibits differentiation of mesenchymal stem cells by inducing Twist2 and Spry4, blocking extracellular regulated kinase activation, and altering Fgf receptor expression levels. Stem Cells. 2011;29(7):1102–1111.
   PubMed Web of Science ®Google Scholar
• Braun S, auf dem Keller U, Steiling H, et al. Fibroblast growth factors in epithelial repair and cytoprotection. Philos Trans R Soc Lond B Biol Sci. 2004;359(1445):753–757.
   PubMed Web of Science ®Google Scholar
• Turner N, Grose R. Fibroblast growth factor signalling: from development to cancer. Nat Rev Cancer. 2010;10(2):116–129.
   PubMed Web of Science ®Google Scholar
• Yun YR, Won JE, Jeon E, et al. Fibroblast growth factors: biology, function, and application for tissue regeneration. J Tissue Eng. 2010;1:218142.
   Google Scholar
• Stavri GT, et al. Basic fibroblast growth factor upregulates the expression of vascular endothelial growth factor in vascular smooth muscle cells. Synergistic interaction with hypoxia. Circulation. 1995;92(1):11–14.
   PubMed Web of Science ®Google Scholar
• Esser JS, Rahner S, Deckler M, et al. Fibroblast growth factor signaling pathway in endothelial cells is activated by BMPER to promote angiogenesis. Arterioscler Thromb Vasc Biol. 2015;35(2):358–367.
   PubMed Web of Science ®Google Scholar
• Hardikar AA, Marcus-Samuels B, Geras-Raaka E, et al. Human pancreatic precursor cells secrete FGF2 to stimulate clustering into hormone-expressing islet-like cell aggregates. Proc Natl Acad Sci U S A. 2003;100(12):7117–7122.
   PubMed Web of Science ®Google Scholar
• Presta M, Dell’Era P, Mitola S, et al. Fibroblast growth factor/fibroblast growth factor receptor system in angiogenesis. Cytokine Growth Factor Rev. 2005;16(2):159–178.
   PubMed Web of Science ®Google Scholar
• Kim BG, Kim HJ, Park HJ, et al. Runx2 phosphorylation induced by fibroblast growth factor-2/protein kinase C pathways. Proteomics. 2006;6(4):1166–1174.
   PubMed Web of Science ®Google Scholar
• Ito T, Sawada R, Fujiwara Y, et al. FGF-2 increases osteogenic and chondrogenic differentiation potentials of human mesenchymal stem cells by inactivation of TGF-beta signaling. Cytotechnology. 2008;56(1):1–7.
   PubMed Web of Science ®Google Scholar
• Santana RB, Trackman PC. Controlled release of fibroblast growth factor 2 stimulates bone healing in an animal model of diabetes mellitus. Int J Oral Maxillofac Implants. 2006;21(5):711–718.
   PubMed Web of Science ®Google Scholar
• Kawaguchi H, Oka H, Jingushi S, et al. A local application of recombinant human fibroblast growth factor 2 for tibial shaft fractures: a randomized, placebo-controlled trial. J Bone Miner Res. 2010;25(12):2735–2743.
   PubMed Web of Science ®Google Scholar
• Nakamura Y, Tensho K, Nakaya H, et al. Low dose fibroblast growth factor-2 (FGF-2) enhances bone morphogenetic protein-2 (BMP-2)-induced ectopic bone formation in mice. Bone. 2005;36(3):399–407.
   PubMed Web of Science ®Google Scholar
• Naderi H, Matin MM, Bahrami AR. Review paper: critical issues in tissue engineering: biomaterials, cell sources, angiogenesis, and drug delivery systems. J Biomater Appl. 2011;26(4):383–417.
   PubMed Web of Science ®Google Scholar
• Bajpai VK, Andreadis ST. Stem cell sources for vascular tissue engineering and regeneration. Tissue Eng Part B Rev. 2012;18(5):405–425.
   PubMed Web of Science ®Google Scholar
• Wang L, Ott L, Seshareddy K, et al. Musculoskeletal tissue engineering with human umbilical cord mesenchymal stromal cells. Regen Med. 2011;6(1):95–109.
   PubMed Web of Science ®Google Scholar
• Atesok K, et al. Endothelial progenitor cells promote fracture healing in a segmental bone defect model. J Orthop Res. 2010;28(8):1007–1014.
   PubMed Web of Science ®Google Scholar
• Rozen N, Bick T, Bajayo A, et al. Transplanted blood-derived endothelial progenitor cells (EPC) enhance bridging of sheep tibia critical size defects. Bone. 2009;45(5):918–924.
   PubMed Web of Science ®Google Scholar
• Duttenhoefer F, et al. 3D scaffolds co-seeded with human endothelial progenitor and mesenchymal stem cells: evidence of prevascularisation within 7 days. Eur Cell Mater. 2013;26:49–64.
   PubMed Web of Science ®Google Scholar
• Kriehuber E, Breiteneder-Geleff S, Groeger M, et al. Isolation and characterization of dermal lymphatic and blood endothelial cells reveal stable and functionally specialized cell lineages. J Exp Med. 2001;194(6):797–808.
   PubMed Web of Science ®Google Scholar
• Boyer M, Townsend LE, Vogel LM, et al. Isolation of endothelial cells and their progenitor cells from human peripheral blood. J Vasc Surg. 2000;31(1 Pt 1):181–189.
   PubMed Web of Science ®Google Scholar
• Thebaud NB, et al. Human progenitor-derived endothelial cells vs. venous endothelial cells for vascular tissue engineering: an in vitro study. J Tissue Eng Regen Med. 2010;4(6):473–484.
   PubMed Web of Science ®Google Scholar
• Balconi G, Spagnuolo R, Dejana E. Development of endothelial cell lines from embryonic stem cells: a tool for studying genetically manipulated endothelial cells in vitro. Arterioscler Thromb Vasc Biol. 2000;20(6):1443–1451.
   PubMed Web of Science ®Google Scholar
• Ni CW, Kumar S, Ankeny CJ, et al. Development of immortalized mouse aortic endothelial cell lines. Vasc Cell. 2014;6(1):7.
   PubMedGoogle Scholar
• Fu WL, Xiang Z, Huang FG, et al. Coculture of peripheral blood-derived mesenchymal stem cells and endothelial progenitor cells on strontium-doped calcium polyphosphate scaffolds to generate vascularized engineered bone. Tissue Eng Part A. 2015;21(5–6):948–959.
   PubMed Web of Science ®Google Scholar
• Wang Z, He Y, Yu X, et al. Rapid vascularization of tissue-engineered vascular grafts in vivo by endothelial cells in co-culture with smooth muscle cells. J Mater Sci Mater Med. 2012;23(4):1109–1017.
   PubMed Web of Science ®Google Scholar
• Correia C, Grayson WL, Park M, et al. In vitro model of vascularized bone: synergizing vascular development and osteogenesis. PLoS One. 2011;6(12):e28352.
   PubMed Web of Science ®Google Scholar
• Huang DM, Chung TH, Hung Y, et al. Internalization of mesoporous silica nanoparticles induces transient but not sufficient osteogenic signals in human mesenchymal stem cells. Toxicol Appl Pharm. 2008;231(2):208–215.
   PubMed Web of Science ®Google Scholar
• Duffy GP, Ahsan T, O'Brien T, et al. Bone marrow-derived mesenchymal stem cells promote angiogenic processes in a time- and dose-dependent manner in vitro. Tissue Eng Part A. 2009;15(9):2459–2470.
   PubMed Web of Science ®Google Scholar
• Ando Y, Matsubara K, Ishikawa J, et al. Stem cell-conditioned medium accelerates distraction osteogenesis through multiple regenerative mechanisms. Bone. 2014;61:82–90.
   PubMed Web of Science ®Google Scholar
• Krock BL, Skuli N, Simon MC. Hypoxia-induced angiogenesis: good and evil. Genes Cancer. 2011;2(12):1117–1133.
   PubMedGoogle Scholar
• Schipani E, Maes C, Carmeliet G, et al. Regulation of osteogenesis-angiogenesis coupling by HIFs and VEGF. J Bone Miner Res. 2009;24(8):1347–1353.
   PubMed Web of Science ®Google Scholar
• Webb JD, Coleman ML, Pugh CW. Hypoxia, hypoxia-inducible factors (HIF), HIF hydroxylases and oxygen sensing. Cell Mol Life Sci. 2009;66(22):3539–3554.
   PubMed Web of Science ®Google Scholar
• Kotch LE, Iyer NV, Laughner E, et al. Defective vascularization of HIF-1alpha-null embryos is not associated with VEGF deficiency but with mesenchymal cell death. Dev Biol. 1999;209(2):254–267.
   PubMed Web of Science ®Google Scholar
• Wan C, Gilbert SR, Wang Y, et al. Activation of the hypoxia-inducible factor-1alpha pathway accelerates bone regeneration. Proc Natl Acad Sci U S A. 2008;105(2):686–691.
   PubMed Web of Science ®Google Scholar
• Liu W, et al. Targeted genes and interacting proteins of hypoxia inducible factor-1. Int J Biochem Mol Biol. 2012;3(2):165–178.
   PubMedGoogle Scholar
• Kelly BD. Cell type-specific regulation of angiogenic growth factor gene expression and induction of angiogenesis in nonischemic tissue by a constitutively active form of hypoxia-inducible factor 1. Circ Res. 2003;93(11):1074–1081.
   PubMed Web of Science ®Google Scholar
• Hadjipanayi E, Schilling AF. Hypoxia-based strategies for angiogenic induction: the dawn of a new era for ischemia therapy and tissue regeneration. Organogenesis. 2013;9(4):261–272.
   PubMed Web of Science ®Google Scholar
• Wei L, Fraser JL, Lu ZY, et al. Transplantation of hypoxia preconditioned bone marrow mesenchymal stem cells enhances angiogenesis and neurogenesis after cerebral ischemia in rats. Neurobiol Dis. 2012;46(3):635–645.
   PubMed Web of Science ®Google Scholar
• Lee JS, Park JC, Kim TW, et al. Human bone marrow stem cells cultured under hypoxic conditions present altered characteristics and enhanced in vivo tissue regeneration. Bone. 2015;78:34–45.
   PubMed Web of Science ®Google Scholar
• Zou D, et al. Repair of critical-sized rat calvarial defects using genetically engineered bone marrow-derived mesenchymal stem cells overexpressing hypoxia-inducible factor-1alpha. Stem Cells. 2011;29(9):1380–1390.
   PubMed Web of Science ®Google Scholar
• Kuchler U, Keibl C, Fügl A, et al. Dimethyloxalylglycine lyophilized onto bone substitutes increase vessel area in rat calvarial defects. Clin Oral Implants Res. 2015;26(5):485–491.
   PubMed Web of Science ®Google Scholar
• Wu C, Zhou Y, Fan W, et al. Hypoxia-mimicking mesoporous bioactive glass scaffolds with controllable cobalt ion release for bone tissue engineering. Biomaterials. 2012;33(7):2076–2085.
   PubMed Web of Science ®Google Scholar
• Azevedo MM, Tsigkou O, Nair R, et al. Hypoxia inducible factor-stabilizing bioactive glasses for directing mesenchymal stem cell behavior. Tissue Eng Part A. 2015;21(1–2):382–389.
   PubMed Web of Science ®Google Scholar
• Wu CT, Chang J. Silicate bioceramics for bone tissue regeneration. J Inorg Mater. 2013;28(1):29–39.
   Web of Science ®Google Scholar
• Whitman M, Kaplan DR, Schaffhausen B, et al. Association of phosphatidylinositol kinase activity with polyoma middle-T competent for transformation. Nature. 1985;315(6016):239–242.
   PubMed Web of Science ®Google Scholar
• Jiang BH, Liu LZ. PI3K/PTEN signaling in angiogenesis and tumorigenesis. Adv Cancer Res. 2009;102:19–65.
   PubMed Web of Science ®Google Scholar
• Ferguson GJ, Milne L, Kulkarni S, et al. PI(3)Kgamma has an important context-dependent role in neutrophil chemokinesis. Nat Cell Biol. 2007;9(1):86–91.
   PubMed Web of Science ®Google Scholar
• Yoo SK, Deng Q, Cavnar PJ, et al. Differential regulation of protrusion and polarity by PI3 K during neutrophil motility in live zebrafish. Dev Cell. 2010;18(2):226–236.
   PubMed Web of Science ®Google Scholar
• Xue G, Hemmings BA. PKB/Akt-dependent regulation of cell motility. J Natl Cancer Inst. 2013;105(6):393–404.
   PubMedGoogle Scholar
• Li S, Deng L, Gong L, et al. Upregulation of CXCR4 favoring neural-like cells migration via AKT activation. Neurosci Res. 2010;67(4):293–299.
   PubMed Web of Science ®Google Scholar
• Vanhaesebroeck B, Leevers SJ, Ahmadi K, et al. Synthesis and function of 3-phosphorylated inositol lipids. Annu Rev Biochem. 2001;70:535–602.
   PubMed Web of Science ®Google Scholar
• Thi EP, Reiner NE. Phosphatidylinositol 3-kinases and their roles in phagosome maturation. J Leukoc Biol. 2012;92(3):553–566.
   PubMed Web of Science ®Google Scholar
• Suire S, Coadwell J, Ferguson GJ, et al. p84, a new Gbetagamma-activated regulatory subunit of the type IB phosphoinositide 3-kinase p110gamma. Curr Biol. 2005;15(6):566–570.
   PubMed Web of Science ®Google Scholar
• Voigt P, Brock C, Nürnberg B, et al. Assigning functional domains within the p101 regulatory subunit of phosphoinositide 3-kinase gamma. J Biol Chem. 2005;280(6):5121–5127.
   PubMed Web of Science ®Google Scholar
• Bunney TD, Katan M. Phosphoinositide signalling in cancer: beyond PI3K and PTEN. Nat Rev Cancer. 2010;10(5):342–352.
   PubMed Web of Science ®Google Scholar
• Backer JM. The regulation and function of Class III PI3Ks: novel roles for Vps34. Biochem J. 2008;410(1):1–17.
   PubMed Web of Science ®Google Scholar
• Graupera M, Potente M. Regulation of angiogenesis by PI3K signaling networks. Exp Cell Res. 2013;319(9):1348–1355.
   PubMed Web of Science ®Google Scholar
• Yoeli-Lerner M, Toker A. Akt/PKB signaling in cancer: a function in cell motility and invasion. Cell Cycle. 2006;5(6):603–605.
   PubMed Web of Science ®Google Scholar
• Dimitriou R, Tsiridis E, Giannoudis PV. Current concepts of molecular aspects of bone healing. Injury. 2005;36(12):1392–1404.
   PubMed Web of Science ®Google Scholar
• Xia W, Chang J. Well-ordered mesoporous bioactive glasses (MBG): a promising bioactive drug delivery system. J Control Release. 2006;110(3):522–530.
   PubMed Web of Science ®Google Scholar
• Wu C, Zhu Y, Chang J, et al. Bioactive inorganic-materials/alginate composite microspheres with controllable drug-delivery ability. J Biomed Mater Res B. 2010;94(1):32–43.
   Google Scholar
• Kang MS, Kim JH, Singh RK, et al. Therapeutic-designed electrospun bone scaffolds: mesoporous bioactive nanocarriers in hollow fiber composites to sequentially deliver dual growth factors. Acta Biomater. 2015;16:103–116.
   PubMed Web of Science ®Google Scholar
• Chen S, et al. Mesoporous bioactive glass surface modified poly(lactic-co-glycolic acid) electrospun fibrous scaffold for bone regeneration. Int J Nanomed. 2015;10:3815–3827.
   PubMed Web of Science ®Google Scholar
• El-Fiqi A, Kim JH, Kim HW. Osteoinductive fibrous scaffolds of biopolymer/mesoporous bioactive glass nanocarriers with excellent bioactivity and long-term delivery of osteogenic drug. ACS Appl Mater Inter. 2015;7(2):1140–1152.
   PubMed Web of Science ®Google Scholar
• Kanczler JM, Oreffo RO. Osteogenesis and angiogenesis: the potential for engineering bone. Eur Cell Mater. 2008;15:100–114.
   PubMed Web of Science ®Google Scholar
• Wu C, Fan W, Chang J, et al. Mesoporous bioactive glass scaffolds for efficient delivery of vascular endothelial growth factor. J Biomater Appl. 2013;28(3):367–374.
   PubMed Web of Science ®Google Scholar
• Mourino V, Boccaccini AR. Bone tissue engineering therapeutics: controlled drug delivery in three-dimensional scaffolds. J R Soc Interface. 2010;7(43):209–227.
   PubMed Web of Science ®Google Scholar
• Li Y, Liu YZ, Long T, et al. Mesoporous bioactive glass as a drug delivery system: fabrication, bactericidal properties and biocompatibility. J Mater Sci Mater Med. 2013;24(8):1951–1961.
   PubMed Web of Science ®Google Scholar
• Franz S, Rammelt S, Scharnweber D, et al. Immune responses to implants – a review of the implications for the design of immunomodulatory biomaterials. Biomaterials. 2011;32(28):6692–6709.
   PubMed Web of Science ®Google Scholar
• Min Z, Shichang Z, Chen X, et al. 3D-printed dimethyloxallyl glycine delivery scaffolds to improve angiogenesis and osteogenesis. Biomater Sci. 2015;3:1236–1244.
   PubMed Web of Science ®Google Scholar
• Jaakkola P, Mole DR, Tian YM, et al. Targeting of HIF-alpha to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science. 2001;292(5516):468–472.
   PubMed Web of Science ®Google Scholar
• Bruick RK, McKnight SL. A conserved family of prolyl-4-hydroxylases that modify HIF. Science. 2001;294(5545):1337–1340.
   PubMed Web of Science ®Google Scholar
• Day RM, Boccaccini AR, Shurey S, et al. Assessment of polyglycolic acid mesh and bioactive glass for soft-tissue engineering scaffolds. Biomaterials. 2004;25(27):5857–5866.
   PubMed Web of Science ®Google Scholar
• Hoppe A, Guldal NS, Boccaccini AR. A review of the biological response to ionic dissolution products from bioactive glasses and glass-ceramics. Biomaterials. 2011;32(11):2757–2774.
   PubMed Web of Science ®Google Scholar
• Haro Durand LA, Vargas GE, Romero NM, et al. Angiogenic effects of ionic dissolution products released from a boron-doped 45S5 bioactive glass. J Mater Chem B. 2015;3(6):1142–1148.
   Web of Science ®Google Scholar
• Han P, Wu C, Chang J, et al. The cementogenic differentiation of periodontal ligament cells via the activation of Wnt/β-catenin signalling pathway by Li+ ions released from bioactive scaffolds. Biomaterials. 2012;33(27):6370–6379.
   PubMed Web of Science ®Google Scholar
• Zhu Y, Li X, Yang J, et al. Composition-structure-property relationships of the CaO-MxOy-SiO2-P2O5 (M = Zr, Mg, Sr) mesoporous bioactive glass (MBG) scaffolds. J Mater Chem. 2011;21(25):9208–9218.
   Web of Science ®Google Scholar
• Rabiee SM, Nazparvar N, Azizian M, et al. Effect of ion substitution on properties of bioactive glasses: a review. Ceram Int. 2015;41(6):7241–7251.
   Web of Science ®Google Scholar
• Wu C, Zhou Y, Xu M, et al. Copper-containing mesoporous bioactive glass scaffolds with multifunctional properties of angiogenesis capacity, osteostimulation and antibacterial activity. Biomaterials. 2013;34(2):422–433.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Liu Y, Li M, et al. The effect of iron incorporation on the in vitro bioactivity and drug release of mesoporous bioactive glasses. Ceram Int. 2013;39(6):6591–6598.
   Web of Science ®Google Scholar
• Wu C, Chang J. Multifunctional mesoporous bioactive glasses for effective delivery of therapeutic ions and drug/growth factors. J Control Release. 2014;193:282–295.
   PubMed Web of Science ®Google Scholar
• Tang F, Li L, Chen D. Mesoporous silica nanoparticles: synthesis, biocompatibility and drug delivery. Adv Mater. 2012;24(12):1504–1534.
   PubMed Web of Science ®Google Scholar
• Li X, He Q, Shi J. Global gene expression analysis of cellular death mechanisms induced by mesoporous silica nanoparticle-based drug delivery system. ACS Nano. 2014;8(2):1309–1320.
   PubMed Web of Science ®Google Scholar
• Slowing I, Viveroescoto J, Wu C, et al. Mesoporous silica nanoparticles as controlled release drug delivery and gene transfection carriers. Adv Drug Deliv Rev. 2008;60(11):1278–1288.
   PubMed Web of Science ®Google Scholar
• Ha SW, Weitzmann MN, Beck GR Jr. Bioactive silica nanoparticles promote osteoblast differentiation through stimulation of autophagy and direct association with LC3 and p62. ACS Nano. 2014;8(6):5898–5910.
   PubMed Web of Science ®Google Scholar
• Vallet-Regi M, Rámila A, del Real RP, et al. A new property of MCM-41: drug delivery system. Chem Mater. 2001;13(2):308–311.
   Web of Science ®Google Scholar
• Vallet-Regi M, Colilla M, Izquierdo-Barba I. Bioactive mesoporous silicas as controlled delivery systems: application in bone tissue regeneration. J Biomed Nanotechnol. 2008;4(1):1–15.
   Web of Science ®Google Scholar
• Wang J, Yang M, Zhu Y, et al. Phage nanofibers induce vascularized osteogenesis in 3D printed bone scaffolds. Adv Mater. 2014;26(29):4961–4966.
   PubMed Web of Science ®Google Scholar
• Vallet-Regí M, Ruiz-Hernández E, González B, et al. Design of Smart Nanomaterials for Drug and Gene Delivery. J Biomater Tissue Eng. 2011;1(1):6–29.
   Web of Science ®Google Scholar
• Shi M, Zhou Y, Shao J, et al. Stimulation of osteogenesis and angiogenesis of hBMSCs by delivering Si ions and functional drug from mesoporous silica nanospheres. Acta Biomater. 2015;21:178–189.
   PubMed Web of Science ®Google Scholar
• Chen Z, Yuen J, Crawford R, et al. The effect of osteoimmunomodulation on the osteogenic effects of cobalt incorporated beta-tricalcium phosphate. Biomaterials. 2015;61:126–138.
   PubMed Web of Science ®Google Scholar
• Roch T, et al. The influence of polystyrene and poly(ether imide) inserts with different roughness, on the activation of dendritic cells. Clin Hemorheol Microcirc. 2013;55(1):157–168.
   PubMed Web of Science ®Google Scholar
• Look M, Saltzman WM, Craft J, et al. The nanomaterial-dependent modulation of dendritic cells and its potential influence on therapeutic immunosuppression in lupus. Biomaterials. 2014;35(3):1089–1095.
   PubMed Web of Science ®Google Scholar
• Chen Z, Klein T, Murray RZ, et al. Osteoimmunomodulation for the development of advanced bone biomaterials. Mater Today. 2016;19(6):304–321.
   Web of Science ®Google Scholar
• Williams DF. On the nature of biomaterials. Biomaterials. 2009;30(30):5897–5909.
   PubMed Web of Science ®Google Scholar
• Mokarram N, Bellamkonda RV. A perspective on immunomodulation and tissue repair. Ann Biomed Eng. 2014;42(2):338–351.
   PubMed Web of Science ®Google Scholar
• Mundy GR, Raisz LG, Cooper RA, et al. Evidence for the secretion of an osteoclast stimulating factor in myeloma. New Engl J Med. 1974;291(20):1041–1046.
   PubMed Web of Science ®Google Scholar
• Horton JE, Raisz LG, Simmons HA, et al. Bone resorbing activity in supernatant fluid from cultured human peripheral blood leukocytes. Science. 1972;177(4051):793–795.
   PubMed Web of Science ®Google Scholar
• Takayanagi H. Osteoimmunology: shared mechanisms and crosstalk between the immune and bone systems. Nature reviews. Immunology. 2007;7(4):292–304.
   PubMed Web of Science ®Google Scholar
• Walsh MC, Kim N, Kadono Y, et al. Osteoimmunology: interplay between the immune system and bone metabolism. Annu Rev Immunol. 2006;24:33–63.
   PubMed Web of Science ®Google Scholar
• Takayanagi H. Inflammatory bone destruction and osteoimmunology. J Periodontal Res. 2005;40(4):287–293.
   PubMed Web of Science ®Google Scholar
• Lorenzo J. Interactions between immune and bone cells: new insights with many remaining questions. J Clin Invest. 2000;106(6):749–752.
   PubMed Web of Science ®Google Scholar
• Li Y, Toraldo G, Li A, et al. B cells and T cells are critical for the preservation of bone homeostasis and attainment of peak bone mass in vivo. Blood. 2007;109(9):3839–3848.
   PubMed Web of Science ®Google Scholar
• Pacifici R. The immune system and bone. Arch Biochem Biophys. 2010;503(1):41–53.
   PubMed Web of Science ®Google Scholar
• Chen Z, Mao X, Tan L, et al. Osteoimmunomodulatory properties of magnesium scaffolds coated with beta-tricalcium phosphate. Biomaterials. 2014;35(30):8553–8565.
   PubMed Web of Science ®Google Scholar
• Chen Z, Yi D, Zheng X, et al. Nutrient element-based bioceramic coatings on titanium alloy stimulating osteogenesis by inducing beneficial osteoimmmunomodulation. J Mater Chem B. 2014;2(36):6030–6043.
   Web of Science ®Google Scholar
• Chen Z, Wu C, Gu W, et al. Osteogenic differentiation of bone marrow MSCs by beta-tricalcium phosphate stimulating macrophages via BMP2 signalling pathway. Biomaterials. 2014;35(5):1507–1518.
   PubMed Web of Science ®Google Scholar
• Shweiki D, Itin A, Soffer D, et al. Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nature. 1992;359(6398):843–845.
   PubMed Web of Science ®Google Scholar
• Li TS, Hamano K, Suzuki K, et al. Improved angiogenic potency by implantation of ex vivo hypoxia prestimulated bone marrow cells in rats. Am J Physiol Heart C Physiol. 2002;283(2):H468–H473.
   PubMed Web of Science ®Google Scholar
• Cramer T, Yamanishi Y, Clausen BE, et al. HIF-1alpha is essential for myeloid cell-mediated inflammation. Cell. 2003;112(5):645–657.
   PubMed Web of Science ®Google Scholar
• Oda T. Activation of hypoxia-inducible factor 1 during macrophage differentiation. Am J Physiol Cell Physiol. 2006;291(1):C104–C113.
   PubMed Web of Science ®Google Scholar
• Blouin CC. Hypoxic gene activation by lipopolysaccharide in macrophages: implication of hypoxia-inducible factor 1alpha. Blood. 2003;103(3):1124–1130.
   PubMed Web of Science ®Google Scholar
• Hellwig-Burgel T, et al. Interleukin-1beta and tumor necrosis factor-alpha stimulate DNA binding of hypoxia-inducible factor-1. Blood. 1999;94(5):1561–1567.
   PubMed Web of Science ®Google Scholar