Biodegradable Zn–Sr alloy for bone regeneration in rat femoral condyle defect model: In vitro and in vivo studies

Montazerolghaem, 2016, Simvastatin-doped pre-mixed calcium phosphate cement inhibits osteoclast differentiation and resorption, J. Mater. Sci. Mater. Med., 27, 83, 10.1007/s10856-016-5692-7 Nabiyouni, 2018, Magnesium-based bioceramics in orthopedic applications, Acta Biomater., 66, 23, 10.1016/j.actbio.2017.11.033 Ishack, 2017, Bone regeneration in critical bone defects using three-dimensionally printed beta-tricalcium phosphate/hydroxyapatite scaffolds is enhanced by coating scaffolds with either dipyridamole or BMP-2, J. Biomed. Mater. Res. B Appl. Biomater., 105, 366, 10.1002/jbm.b.33561 Bian, 2014, A model for facilitating translational research and development in China: call for establishing a Hong Kong branch of the Chinese national engineering research centre for biomaterials, J. Orthop. Transl., 2, 170 Zhou, 2017, Improving osteogenesis of three-dimensional porous scaffold based on mineralized recombinant human-like collagen via mussel-inspired polydopamine and effective immobilization of BMP-2-derived peptide, Colloids Surf. B Biointerfaces, 152, 124, 10.1016/j.colsurfb.2016.12.041 Webber, 2015, Supramolecular biomaterials, Nat. Mater., 15, 13, 10.1038/nmat4474 Dellavia, 2016, Iliac crest fresh-frozen allografts versus autografts in oral pre-prosthetic bone reconstructive surgery: histologic and histomorphometric study, Implant Dent., 25, 731, 10.1097/ID.0000000000000451 Rice, 2010, Safety and feasibility of autologous bone marrow cellular therapy in relapsing-progressive multiple sclerosis, Clin. Pharmacol. Ther., 87, 679, 10.1038/clpt.2010.44 He, 2014, Hydroxyapatite bioceramic coatings prepared by hydrothermal-electrochemical deposition method, J. Wuhan Univ. Technol.-Materials Sci. Ed., 29, 398, 10.1007/s11595-014-0928-1 Zheng, 2014, Biodegradable metals, Mater. Sci. Eng. R Rep., 77, 1, 10.1016/j.mser.2014.01.001 Glenske, 2018, Applications of metals for bone regeneration, Int. J. Mol. Sci., 19, 826, 10.3390/ijms19030826 Ching, 2014, Effects of surface coating on reducing friction and wear of orthopaedic implants, Sci. Technol. Adv. Mater., 15, 10.1088/1468-6996/15/1/014402 Li, 2012, Designing superhard, self-toughening CrAlN coatings through grain boundary engineering, Acta Mater., 60, 5735, 10.1016/j.actamat.2012.06.049 Bauer, 2000, Bone graft materials. An overview of the basic science, Clin. Orthop. Relat. Res., 371, 10, 10.1097/00003086-200002000-00003 Pederson, 2007, Long bone reconstruction with vascularized bone grafts, Orthop. Clin., 38, 23, 10.1016/j.ocl.2006.10.006 Tong, 2018, Microstructure, mechanical properties, biocompatibility, and in vitro corrosion and degradation behavior of a new Zn-5Ge alloy for biodegradable implant materials, Acta Biomater., 82, 197, 10.1016/j.actbio.2018.10.015 Kafri, 2019, The effects of 4%Fe on the performance of pure zinc as biodegradable implant material, Ann. Biomed. Eng., 47, 1400, 10.1007/s10439-019-02245-w Qu, 2020, Serum zinc levels and multiple health outcomes: implications for zinc-based biomaterials, Bioact. Mater., 5, 410, 10.1016/j.bioactmat.2020.03.006 McCall, 2000, Function and mechanism of zinc metalloenzymes, J. Nutr., 130, 1437S, 10.1093/jn/130.5.1437S Yamaguchi, 2010, Role of nutritional zinc in the prevention of osteoporosis, Mol. Cell. Biochem., 338, 241, 10.1007/s11010-009-0358-0 Yamaguchi, 1987, Stimulatory effect of zinc on bone formation in tissue culture, Biochem. Pharmacol., 36, 4007, 10.1016/0006-2952(87)90471-0 Chen, 1999, In vitro effects of zinc on markers of bone formation, Biol. Trace Elem. Res., 68, 225, 10.1007/BF02783905 Yamaguchi, 1996, Stimulatory effect of zinc-chelating dipeptide on deoxyribonucleic acid synthesis in osteoblastic MC3T3-E1 cells, Peptides, 17, 1207, 10.1016/S0196-9781(96)00114-3 Fu, 2018, Runx2/Osterix and zinc uptake synergize to orchestrate osteogenic differentiation and citrate containing bone apatite formation, Adv. Sci., 5, 1700755, 10.1002/advs.201700755 Seo, 2010, Zinc may increase bone formation through stimulating cell proliferation, alkaline phosphatase activity and collagen synthesis in osteoblastic MC3T3-E1 cells, Nutr. Res. Pract., 4, 356, 10.4162/nrp.2010.4.5.356 Yusa, 2011, In vitro prominent bone regeneration by release zinc ion from Zn-modified implant, Biochem. Biophys. Res. Commun., 412, 273, 10.1016/j.bbrc.2011.07.082 Bowen, 2013, Zinc exhibits ideal physiological corrosion behavior for bioabsorbable stents, Adv. Mater., 25, 2577, 10.1002/adma.201300226 Yang, 2018, In vitro and in vivo studies on zinc-hydroxyapatite composites as novel biodegradable metal matrix composite for orthopedic applications, Acta Biomater., 71, 200, 10.1016/j.actbio.2018.03.007 Li, 2019, Additive manufacturing of high-strength CrMnFeCoNi high-entropy alloys-based composites with WC addition, J. Mater. Sci. Technol., 35, 2430, 10.1016/j.jmst.2019.05.062 Chao, 2016, Mechanical properties: in vitro degradation behavior, hemocompatibility and cytotoxicity evaluation of Zn-1.2Mg alloy for biodegradable implants, RSC Adv., 6, 86410, 10.1039/C6RA14300H Li, 2015, Development of biodegradable Zn-1X binary alloys with nutrient alloying elements Mg, Ca and Sr, Sci. Rep., 5, 10719, 10.1038/srep10719 Jia, 2020, In vitro and in vivo studies of Zn-Mn biodegradable metals designed for orthopedic applications, Acta Biomater., 108, 358, 10.1016/j.actbio.2020.03.009 Yang, 2020, Alloying design of biodegradable zinc as promising bone implants for load-bearing applications, Nat. Commun., 11, 401, 10.1038/s41467-019-14153-7 Zhu, 2007, Induction of a program gene expression during osteoblast differentiation with strontium ranelate, Biochem. Biophys. Res. Commun., 355, 307, 10.1016/j.bbrc.2007.01.120 Yang, 2018, Enhanced osseointegration of Zn-Mg composites by tuning the release of Zn ions with sacrificial Mg-rich anode design, ACS Biomater. Sci. Eng., 5, 453, 10.1021/acsbiomaterials.8b01137 Dimitriou, 2005, Current concepts of molecular aspects of bone healing, Injury, 36, 1392, 10.1016/j.injury.2005.07.019 Houschyar, 2018, Wnt pathway in bone repair and regeneration – what do we know so far, Front. Cell Dev. Biol., 6, 170, 10.3389/fcell.2018.00170 Cho, 2002, Differential temporal expression of members of the transforming growth factor beta superfamily during murine fracture healing, J. Bone Miner. Res., 17, 513, 10.1359/jbmr.2002.17.3.513 Wang, 2013, Role of mesenchymal stem cells in bone regeneration and fracture repair: a review, Int. Orthop., 37, 2491, 10.1007/s00264-013-2059-2 Fazzalari, 2011, Bone fracture and bone fracture repair, Osteoporos. Int., 22, 2003, 10.1007/s00198-011-1611-4 Lieberman, 2002, The role of growth factors in the repair of bone, J. Bone Joint Surg., 84, 1032, 10.2106/00004623-200206000-00022 Cho, 2002, Differential temporal expression of members of the transforming growth factor β superfamily during murine fracture healing, J. Bone Joint Surg., 17, 513 Fayaz, 2011, vol. 35, 1587 Marsell, 2011, The biology of fracture healing, Injury, 42, 551, 10.1016/j.injury.2011.03.031 Kloen, 2012, Management of forearm nonunions: current concepts, Strat, Trauma Limb Reconstr, 7, 1, 10.1007/s11751-011-0125-0 Ducy, 1997, Osf2/Cbfa1: a transcriptional activator of osteoblast differentiation, Cell, 89, 747, 10.1016/S0092-8674(00)80257-3 Krishnan, 2006, Regulation of bone mass by Wnt signaling, J. Clin. Invest., 116, 1202, 10.1172/JCI28551 Martini, 2014, PI3K/AKT signaling pathway and cancer: an updated review, Ann. Med., 46, 372, 10.3109/07853890.2014.912836 Majidinia, 2018, The roles of signaling pathways in bone repair and regeneration, J. Cell. Physiol., 233, 2937, 10.1002/jcp.26042 C. Ge, G. Xiao, D. Jiang, R.T. Franceschi, Critical role of the extracellular signal-regulated kinase-MAPK pathway in osteoblast differentiation and skeletal development, J. Cell Biol. 176 709-718. Gong, 2017, A novel nano-sized bioactive glass stimulates osteogenesis via the MAPK pathway, RSC Adv., 7, 13760, 10.1039/C6RA26713K Rajabi, 2017, The role of angiogenesis in cancer treatment, Biomedicines, 5, 34, 10.3390/biomedicines5020034 Mao, 2017, The synergistic effects of Sr and Si bioactive ions on osteogenesis, osteoclastogenesis and angiogenesis for osteoporotic bone regeneration, Acta Biomater., 61, 217, 10.1016/j.actbio.2017.08.015 Lin, 2013, Strontium substituted hydroxyapatite porous microspheres: surfactant-free hydrothermal synthesis, enhanced biological response and sustained drug release, Chem. Eng. J., 222, 49, 10.1016/j.cej.2013.02.037 Zhang, 2016, A strontium-incorporated nanoporous titanium implant surface for rapid osseointegration, Nanoscale, 8, 5291, 10.1039/C5NR08580B Ma, 2015, Endothelial cellular responses to biodegradable metal zinc, ACS Biomater. Sci. Eng., 1, 1174, 10.1021/acsbiomaterials.5b00319 Yamaguchi, 2004, Bioavailability of zinc yeast in rats: stimulatory effect on bone calcification in vivo, J. Health Sci., 50, 75, 10.1248/jhs.50.75 Prabha, 2019, Strontium functionalized scaffold for bone tissue engineering, Mater. Sci. Eng. C Mater. Biol. Appl., 94, 509, 10.1016/j.msec.2018.09.054 Rybchyn, 2011, An Akt-dependent increase in canonical Wnt signaling and a decrease in sclerostin protein levels are involved in strontium ranelate-induced osteogenic effects in human osteoblasts, J. Biol. Chem., 286, 23771, 10.1074/jbc.M111.251116 Peng, 2009, Strontium promotes osteogenic differentiation of mesenchymal stem cells through the Ras/MAPK signaling pathway, Cell. Physiol. Biochem., 23, 165, 10.1159/000204105 Saidak, 2012, Strontium signaling: molecular mechanisms and therapeutic implications in osteoporosis, Pharmacol. Ther., 136, 216, 10.1016/j.pharmthera.2012.07.009 Zhang, 2016, Strontium attenuates rhBMP-2-induced osteogenic differentiation via formation of Sr-rhBMP-2 complex and suppression of Smad-dependent signaling pathway, Acta Biomater., 33, 290, 10.1016/j.actbio.2016.01.042 Fielding, 2014, Effects of SiO2, SrO, MgO, and ZnO dopants in tricalcium phosphates on osteoblastic Runx2 expression, J. Biomed. Mater. Res., 102, 2417, 10.1002/jbm.a.34909 Naruphontjirakul, 2018, In vitro osteogenesis by intracellular uptake of strontium containing bioactive glass nanoparticles, Acta Biomater., 66, 67, 10.1016/j.actbio.2017.11.008 Zhu, 2017, Biological responses and mechanisms of human bone marrow mesenchymal stem cells to Zn and Mg biomaterials, ACS Appl. Mater. Interfaces, 9, 27453, 10.1021/acsami.7b06654 Zhou, 2020, Zinc L-aspartate enhances intestinal stem cell activity to protect the integrity of the intestinal mucosa against deoxynivalenol through activation of the Wnt/β-catenin signaling pathway, Environ. Pollut., 262, 114290, 10.1016/j.envpol.2020.114290 Zhang, 2015, Effects of bioactive cements incorporating zinc-bioglass nanoparticles on odontogenic and angiogenic potential of human dental pulp cells, J. Biomater. Appl., 29, 954, 10.1177/0885328214550896 Zhang, 2016, Zinc attenuates tubulointerstitial fibrosis in diabetic nephropathy via inhibition of HIF through PI-3K signaling, Biol. Trace Elem. Res., 173, 372, 10.1007/s12011-016-0661-z Dong, 2016, GPR39 activates proliferation and differentiation of porcine intramuscular preadipocytes through targeting the PI3K/AKT cell signaling pathway, J. Recept. Signal Transduct. Res., 36, 130, 10.3109/10799893.2015.1056308 Akbari, 2020, Role of zinc supplementation on ischemia/reperfusion injury in various organs, Biol. Trace Elem. Res., 196, 1, 10.1007/s12011-019-01892-3