Hypoxia-mimicking cobalt-doped multi-walled carbon nanotube nanocomposites enhance the angiogenic capacity of stem cells from apical papilla

Dammaschke, 2003, Long-term survival of root-canal-treated teeth: a retrospective study over 10 years, J. Endod., 29, 638, 10.1097/00004770-200310000-00006 Dissanayaka, 2017, The role of vasculature engineering in dental pulp regeneration, J. Endod., 43, S102, 10.1016/j.joen.2017.09.003 Goncalves, 2012, Mesenchymal stem cell recruitment by stromal derived factor-1-delivery systems based on chitosan/poly (gamma-glutamic acid) polyelectrolyte complexes, Eur. Cell Mater., 23, 249, 10.22203/eCM.v023a19 Gholobova, 2020, Vascularization of tissue-engineered skeletal muscle constructs, Biomaterials., 235, 119708, 10.1016/j.biomaterials.2019.119708 Silva, 2018, Injectable and tunable hyaluronic acid hydrogels releasing chemotactic and angiogenic growth factors for endodontic regeneration, Acta Biomater., 77, 155, 10.1016/j.actbio.2018.07.035 Zhu, 2019, Dental pulp stem cells overexpressing stromal-derived factor-1α and vascular endothelial growth factor in dental pulp regeneration, Clin. Oral Investig., 23, 2497, 10.1007/s00784-018-2699-0 Dissanayaka, 2014, Scaffold-free prevascularized microtissue spheroids for pulp regeneration, J. Dent. Res., 93, 1296, 10.1177/0022034514550040 Han, 2020, HIF-1α stabilization enhances angio-/vasculogenic properties of shed, J. Dent. Res., 99, 804, 10.1177/0022034520912190 Aranha, 2010, Hypoxia enhances the angiogenic potential of human dental pulp cells, J. Endod., 36, 1633, 10.1016/j.joen.2010.05.013 Tamama, 2011, Differential roles of hypoxia inducible factor subunits in multipotential stromal cells under hypoxic condition, J. Cell. Biochem., 112, 804, 10.1002/jcb.22961 Kelly, 2003, 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., 93, 1074, 10.1161/01.RES.0000102937.50486.1B Yamakawa, 2003, Hypoxia-inducible factor-1 mediates activation of cultured vascular endothelial cells by inducing multiple angiogenic factors, Circ. Res., 93, 664, 10.1161/01.RES.0000093984.48643.D7 Stegen, 2016, HIF-1α promotes glutamine-mediated redox homeostasis and glycogen-dependent bioenergetics to support postimplantation bone cell survival, Cell Metab., 23, 265, 10.1016/j.cmet.2016.01.002 Chen, 2017, Metabolic reprogramming by HIF-1 activation enhances survivability of human adipose-derived stem cells in ischaemic microenvironments, Cell Prolif., 50, 10.1111/cpr.12363 Mouriño, 2012, Metallic ions as therapeutic agents in tissue engineering scaffolds: an overview of their biological applications and strategies for new developments, J. R. Soc. Interface, 9, 401, 10.1098/rsif.2011.0611 Fan, 2010, Enhancing in vivo vascularized bone formation by cobalt chloride-treated bone marrow stromal cells in a tissue engineered periosteum model, Biomaterials., 31, 3580, 10.1016/j.biomaterials.2010.01.083 Kim, 2002, Stabilization of hypoxia-inducible factor-1alpha is involved in the hypoxic stimuli-induced expression of vascular endothelial growth factor in osteoblastic cells, Cytokine., 17, 14, 10.1006/cyto.2001.0985 Yuan, 2003, Cobalt inhibits the interaction between hypoxia-inducible factor-alpha and von Hippel-Lindau protein by direct binding to hypoxia-inducible factor-alpha, J. Biol. Chem., 278, 15911, 10.1074/jbc.M300463200 Wu, 2012, Hypoxia-mimicking mesoporous bioactive glass scaffolds with controllable cobalt ion release for bone tissue engineering, Biomaterials., 33, 2076, 10.1016/j.biomaterials.2011.11.042 Kulanthaivel, 2015, Improving the osteogenic and angiogenic properties of synthetic hydroxyapatite by dual doping of bivalent cobalt and magnesium ion, Ceram. Int., 41, 11323, 10.1016/j.ceramint.2015.05.090 Quinlan, 2015, Hypoxia-mimicking bioactive glass/collagen glycosaminoglycan composite scaffolds to enhance angiogenesis and bone repair, Biomaterials., 52, 358, 10.1016/j.biomaterials.2015.02.006 Liu, 2014, Carbon nanotubes as VEGF carriers to improve the early vascularization of porcine small intestinal submucosa in abdominal wall defect repair, Int. J. Nanomedicine, 9, 1275 Abarrategi, 2008, Multiwall carbon nanotube scaffolds for tissue engineering purposes, Biomaterials., 29, 94, 10.1016/j.biomaterials.2007.09.021 Zhou, 2018, Effective nerve cell modulation by electrical stimulation of carbon nanotube embedded conductive polymeric scaffolds, Biomater Sci., 6, 2375, 10.1039/C8BM00553B Sun, 2017, Carbon nanotube-composite hydrogels promote intercalated disc assembly in engineered cardiac tissues through β1-integrin mediated FAK and RhoA pathway, Acta Biomater., 48, 88, 10.1016/j.actbio.2016.10.025 Zhu, 2013, Immobilizing metal nanoparticles to metal-organic frameworks with size and location control for optimizing catalytic performance, J. Am. Chem. Soc., 135, 10210, 10.1021/ja403330m Huang, 2014, Bimetallic alloy nanocrystals encapsulated in zif-8 for synergistic catalysis of ethylene oxidative degradation, Chem. Commun. (Camb.), 50, 10115, 10.1039/C4CC04479G Huxford, 2010, Metal-organic frameworks as potential drug carriers, Curr. Opin. Chem. Biol., 14, 262, 10.1016/j.cbpa.2009.12.012 Ju, 2013, An unprecedented dynamic porous metal-organic framework assembled from fivefold interlocked closed nanotubes with selective gas adsorption behaviors, Chem. Commun. (Camb.), 49, 1820, 10.1039/c3cc38519a Choi, 2014, Supercapacitors of nanocrystalline metal-organic frameworks, ACS Nano, 8, 7451, 10.1021/nn5027092 Hu, 2014, Hollow/porous nanostructures derived from nanoscale metal-organic frameworks towards high performance anodes for lithium-ion batteries, Nanoscale., 6, 1236, 10.1039/C3NR05192G Yuan, 2015, Coculture of stem cells from apical papilla and human umbilical vein endothelial cell under hypoxia increases the formation of three-dimensional vessel-like structures in vitro, Tissue Eng. Part A, 21, 1163, 10.1089/ten.tea.2014.0058 Lee, 2017, Hypoxic preconditioning promotes the bioactivities of mesenchymal stem cells via the HIF-1α-GRP78-Akt axis, Int. J. Mol. Sci., 18, 1320, 10.3390/ijms18061320 Roitbak, 2011, Continuous expression of HIF-1α in neural stem/progenitor cells, Cell. Mol. Neurobiol., 31, 119, 10.1007/s10571-010-9561-5 Yu, 2019, Cellular hypoxia promotes osteogenic differentiation of mesenchymal stem cells and bone defect healing via STAT3 signaling, Cell. Mol. Biol. Lett., 24, 64, 10.1186/s11658-019-0191-8 Cecil, 2017, Immunization against HIF-1α inhibits the growth of basal mammary tumors and targets mammary stem cells, Clin. Cancer Res., 23, 3396, 10.1158/1078-0432.CCR-16-1678 Cervia, 2018, Current progress in electrotransfection as a nonviral method for gene delivery, Mol. Pharm., 15, 3617, 10.1021/acs.molpharmaceut.8b00207 Piret, 2002, CoCl2, a chemical inducer of hypoxia-inducible factor-1, and hypoxia reduce apoptotic cell death in hepatoma cell line HepG2, Ann. N. Y. Acad. Sci., 973, 443, 10.1111/j.1749-6632.2002.tb04680.x Martin, 2005, Copper-dependent activation of hypoxia-inducible factor (HIF)-1: implications for ceruloplasmin regulation, Blood, 105, 4613, 10.1182/blood-2004-10-3980 Salnikow, 2004, Depletion of intracellular ascorbate by the carcinogenic metals nickel and cobalt results in the induction of hypoxic stress, J. Biol. Chem., 279, 40337, 10.1074/jbc.M403057200 He, 2013, Disturbance of aerobic metabolism accompanies neurobehavioral changes induced by nickel in mice, Neurotoxicology., 38, 9, 10.1016/j.neuro.2013.05.011 Wu, 2013, Copper-containing mesoporous bioactive glass scaffolds with multifunctional properties of angiogenesis capacity, osteostimulation and antibacterial activity, Biomaterials., 34, 422, 10.1016/j.biomaterials.2012.09.066 Birgani, 2016, Combinatorial incorporation of fluoride and cobalt ions into calcium phosphates to stimulate osteogenesis and angiogenesis, Biomed. Mater., 11, 10.1088/1748-6041/11/1/015020 Wong, 2013, Carbon nanotubes for delivery of small molecule drugs, Adv. Drug Deliv. Rev., 65, 1964, 10.1016/j.addr.2013.08.005 Li, 2014, In vivo biodistribution of platinum-based drugs encapsulated into multi-walled carbon nanotubes, Nanomedicine, 10, 1465, 10.1016/j.nano.2014.01.004 Pantarotto, 2003, Synthesis, structural characterization, and immunological properties of carbon nanotubes functionalized with peptides, J. Am. Chem. Soc., 125, 6160, 10.1021/ja034342r Peters, 2001, Induction of apoptosis in human microvascular endothelial cells by divalent cobalt ions. Evidence for integrin-mediated signaling via the cytoskeleton, J. Mater. Sci. Mater. Med., 12, 955, 10.1023/A:1012852814570 Huang, 2015, Metal organic frameworks route to in situ insertion of multiwalled carbon nanotubes in Co3O4 polyhedra as anode materials for lithium-ion batteries, ACS Nano, 9, 1592, 10.1021/nn506252u Lee, 2011, The HIF pathway and erythrocytosis, Annu. Rev. Pathol., 6, 165, 10.1146/annurev-pathol-011110-130321 Zhou, 2016, Hypoxia-mimicking Co doped TiO2 microporous coating on titanium with enhanced angiogenic and osteogenic activities, Acta Biomater., 43, 358, 10.1016/j.actbio.2016.07.045 Deng, 2019, Hypoxia-mimicking cobalt-doped borosilicate bioactive glass scaffolds with enhanced angiogenic and osteogenic capacity for bone regeneration, Int. J. Biol. Sci., 15, 1113, 10.7150/ijbs.32358 Ferrara, 1997, The biology of vascular endothelial growth factor, Endocr. Rev., 18, 4, 10.1210/edrv.18.1.0287 Soker, 2000, Systems for therapeutic angiogenesis in tissue engineering, World J. Urol., 18, 10, 10.1007/PL00007070 ten Freyhaus, 2011, Hypoxia enhances platelet-derived growth factor signaling in the pulmonary vasculature by down-regulation of protein tyrosine phosphatases, Am. J. Respir. Crit. Care Med., 183, 1092, 10.1164/rccm.200911-1663OC Meng, 2015, Carbon nanotubes activate macrophages into a m1/m2 mixed status: recruiting naгїve macrophages and supporting angiogenesis, ACS Appl. Mater. Interfaces, 7, 3180, 10.1021/am507649n Wierzbicki, 2013, Comparison of anti-angiogenic properties of pristine carbon nanoparticles, Nanoscale Res. Lett., 8, 195, 10.1186/1556-276X-8-195 Eldridge, 2017, Evaluation of multiwalled carbon nanotube cytotoxicity in cultures of human brain microvascular endothelial cells grown on plastic or basement membrane, Toxicol. in Vitro, 41, 223, 10.1016/j.tiv.2017.03.002 Wu, 2011, Induction and testing of hypoxia in cell culture, J. Vis. Exp., 12, 2899 McKeon-Fischer, 2014, In vivo skeletal muscle biocompatibility of composite, coaxial electrospun, and microfibrous scaffolds, Tissue Eng. Part A, 20, 1961, 10.1089/ten.tea.2013.0283