Promoting vascularization for tissue engineering constructs: current strategies focusing on HIF-regulating scaffolds

References

• Jawoniyi O, Gormley K, McGleenan E, et al. Organ donation and transplantation: awareness and roles of healthcare professionals-A systematic literature review. J Clin Nurs. 2018 Mar;27(5–6):e726–e738.
   PubMed Web of Science ®Google Scholar
• Acuna SA. Etiology of increased cancer incidence after solid organ transplantation. Transplant Rev (Orlando). 2018 Oct;32(4):218–224.
   PubMedGoogle Scholar
• Fischer SA. Is this organ donor safe?: donor-derived infections in solid organ transplantation. Infect Dis Clin North Am. 2018 Sep;32(3):495–506.
   PubMed Web of Science ®Google Scholar
• Thirumavalavan N, Scovell JM, Link RE, et al. Does solid organ transplantation affect male reproduction? Eur Urol Focus. 2018 Apr;4(3):307–310.
   PubMedGoogle Scholar
• Atala A, Bauer SB, Soker S, et al. Tissue-engineered autologous bladders for patients needing cystoplasty. Lancet. 2006 Apr 15;367(9518):1241–1246.
   PubMed Web of Science ®Google Scholar
• Gonfiotti A, Jaus MO, Barale D, et al. The first tissue-engineered airway transplantation: 5-year follow-up results. Lancet. 2014 Jan 18;383(9913):238–244.
   PubMed Web of Science ®Google Scholar
• Korecky B, Hai CM, Rakusan K. Functional capillary density in normal and transplanted rat hearts. Can J Physiol Pharmacol. 1982 Jan;60(1):23–32.
   PubMed Web of Science ®Google Scholar
• Rakusan K, Flanagan MF, Geva T, et al. Morphometry of human coronary capillaries during normal growth and the effect of age in left ventricular pressure-overload hypertrophy. Circulation. 1992 Jul;86(1):38–46.
   PubMed Web of Science ®Google Scholar
• Potente M, Gerhardt H, Carmeliet P. Basic and therapeutic aspects of angiogenesis. Cell. 2011 Sep 16;146(6):873–887.
   PubMed Web of Science ®Google Scholar
• Armulik A, Abramsson A, Betsholtz C. Endothelial/pericyte interactions. Circ Res. 2005 Sep 16;97(6):512–523.
   PubMed Web of Science ®Google Scholar
• Augustin HG, Koh GY, Thurston G, et al. Control of vascular morphogenesis and homeostasis through the angiopoietin-tie system. Nat Rev Mol Cell Biol. 2009 Mar;10(3):165–177.
   PubMed Web of Science ®Google Scholar
• Liu J, Hilderink J, Groothuis TA, et al. Monitoring nutrient transport in tissue-engineered grafts. J Tissue Eng Regen Med. 2015 Aug;9(8):952–960.
   PubMed Web of Science ®Google Scholar
• Radisic M, Deen W, Langer R, et al. Mathematical model of oxygen distribution in engineered cardiac tissue with parallel channel array perfused with culture medium containing oxygen carriers. Am J Physiol Heart Circ Physiol. 2005 Mar;288(3):H1278–H1289.
   PubMed Web of Science ®Google Scholar
• Shimizu T, Sekine H, Yang J, et al. Polysurgery of cell sheet grafts overcomes diffusion limits to produce thick, vascularized myocardial tissues. FASEB J. 2006 Apr;20(6):708–710.
   PubMed Web of Science ®Google Scholar
• Riegler J, Tiburcy M, Ebert A, et al. Human engineered heart muscles engraft and survive long term in a rodent myocardial infarction model. Circ Res. 2015 Sep 25;117(8):720–730.
   PubMed Web of Science ®Google Scholar
• Tiburcy M, Hudson JE, Balfanz P, et al. Defined engineered human myocardium with advanced maturation for applications in heart failure modeling and repair. Circulation. 2017 May 9;135(19):1832–1847.
   PubMed Web of Science ®Google Scholar
• Zhang M, Methot D, Poppa V, et al. Cardiomyocyte grafting for cardiac repair: graft cell death and anti-death strategies. J Mol Cell Cardiol. 2001 May;33(5):907–921.
   PubMed Web of Science ®Google Scholar
• Kainuma S, Miyagawa S, Fukushima S, et al. Cell-sheet therapy with omentopexy promotes arteriogenesis and improves coronary circulation physiology in failing heart. Mol Ther. 2015 Feb;23(2):374–386.
   PubMed Web of Science ®Google Scholar
• Zhang C, Hou J, Zheng S, et al. Vascularized atrial tissue patch cardiomyoplasty with omentopexy improves cardiac performance after myocardial infarction. Ann Thorac Surg. 2011 Oct;92(4):1435–1442.
   PubMed Web of Science ®Google Scholar
• Kawamura M, Miyagawa S, Fukushima S, et al. Enhanced survival of transplanted human induced pluripotent stem cell-derived cardiomyocytes by the combination of cell sheets with the pedicled omental flap technique in a porcine heart. Circulation. 2013 Sep 10;128(11 Suppl 1):S87–S94.
   PubMed Web of Science ®Google Scholar
• Panaro F, Bouyabrine H, Carabalona JP, et al. Omental flap for hepatic artery coverage during liver transplantation. J Gastrointest Surg. 2014 Aug;18(8):1518–1522.
   PubMed Web of Science ®Google Scholar
• Hudon V, Berthod F, Black AF, et al. A tissue-engineered endothelialized dermis to study the modulation of angiogenic and angiostatic molecules on capillary-like tube formation in vitro. Br J Dermatol. 2003 Jun;148(6):1094–1104.
   PubMed Web of Science ®Google Scholar
• Tremblay PL, Hudon V, Berthod F, et al. Inosculation of tissue-engineered capillaries with the host’s vasculature in a reconstructed skin transplanted on mice. Am J Transplant. 2005 5;May(5):1002–1010.
   Google Scholar
• Stoehr A, Hirt MN, Hansen A, et al. Spontaneous formation of extensive vessel-like structures in murine engineered heart tissue. Tissue Eng Part A. 2016 Feb;22(3–4):326–335.
   PubMed Web of Science ®Google Scholar
• Yang M, Baranov E, Li XM, et al. Whole-body and intravital optical imaging of angiogenesis in orthotopically implanted tumors. Proc Natl Acad Sci U S A. 2001 Feb 27;98(5):2616–2621.
   PubMed Web of Science ®Google Scholar
• Hellstrom M, Gerhardt H, Kalen M, et al. Lack of pericytes leads to endothelial hyperplasia and abnormal vascular morphogenesis. J Cell Biol. 2001 Apr 30;153(3):543–553.
   PubMed Web of Science ®Google Scholar
• Thurston G, Suri C, Smith K, et al. Leakage-resistant blood vessels in mice transgenically overexpressing angiopoietin-1. Science. 1999 Dec 24;286(5449):2511–2514.
   PubMed Web of Science ®Google Scholar
• Perry L, Landau S, Flugelman MY, et al. Genetically engineered human muscle transplant enhances murine host neovascularization and myogenesis. Commun Biol. 2018;1:161.
   PubMed Web of Science ®Google Scholar
• Anisimov A, Tvorogov D, Alitalo A, et al. Vascular endothelial growth factor-angiopoietin chimera with improved properties for therapeutic angiogenesis. Circulation. 2013 Jan 29;127(4):424–434.
   PubMed Web of Science ®Google Scholar
• Chen RR, Silva EA, Yuen WW, et al. Spatio-temporal VEGF and PDGF delivery patterns blood vessel formation and maturation. Pharm Res. 2007 Feb;24(2):258–264.
   PubMed Web of Science ®Google Scholar
• Davies NH, Schmidt C, Bezuidenhout D, et al. Sustaining neovascularization of a scaffold through staged release of vascular endothelial growth factor-A and platelet-derived growth factor-BB. Tissue Eng Part A. 2012 Jan;18(1–2):26–34.
   PubMed Web of Science ®Google Scholar
• Brudno Y, Ennett-Shepard AB, Chen RR, et al. Enhancing microvascular formation and vessel maturation through temporal control over multiple pro-angiogenic and pro-maturation factors. Biomaterials. 2013 Dec;34(36):9201–9209.
   PubMed Web of Science ®Google Scholar
• Engel FB, Hsieh PC, Lee RT, et al. FGF1/p38 MAP kinase inhibitor therapy induces cardiomyocyte mitosis, reduces scarring, and rescues function after myocardial infarction. Proc Natl Acad Sci USA. 2006 Oct 17;103(42):15546–15551.
   PubMed Web of Science ®Google Scholar
• Kitrou P, Karnabatidis D, Brountzos E, et al. Gene-based therapies in patients with critical limb ischemia. Expert Opin Biol Ther. 2017 Apr;17(4):449–456.
   PubMed Web of Science ®Google Scholar
• Veith AP, Henderson K, Spencer A, et al. Therapeutic strategies for enhancing angiogenesis in wound healing. Adv Drug Deliv Rev. 2018 Sep 26. DOI:10.1016/j.addr.2018.09.010.
   PubMed Web of Science ®Google Scholar
• Elson DA, Thurston G, Huang LE, et al. Induction of hypervascularity without leakage or inflammation in transgenic mice overexpressing hypoxia-inducible factor-1alpha. Genes Dev. 2001 Oct 1;15(19):2520–2532.
   PubMed Web of Science ®Google Scholar
• Don CW, Murry CE. Improving survival and efficacy of pluripotent stem cell-derived cardiac grafts. J Cell Mol Med. 2013 Nov;17(11):1355–1362.
   PubMed Web of Science ®Google Scholar
• Chong JJ, Yang X, Don CW, et al. Human embryonic-stem-cell-derived cardiomyocytes regenerate non-human primate hearts. Nature. 2014 Jun 12;510(7504):273–277.
   PubMed Web of Science ®Google Scholar
• Laflamme MA, Chen KY, Naumova AV, et al. Cardiomyocytes derived from human embryonic stem cells in pro-survival factors enhance function of infarcted rat hearts. Nat Biotechnol. 2007 Sep;25(9):1015–1024.
   PubMed Web of Science ®Google Scholar
• Lee AS, Inayathullah M, Lijkwan MA, et al. Prolonged survival of transplanted stem cells after ischaemic injury via the slow release of pro-survival peptides from a collagen matrix. Nat Biomed Eng. 2018 Feb;2(2):104–113.
   PubMed Web of Science ®Google Scholar
• Mehrhof FB, Muller FU, Bergmann MW, et al. In cardiomyocyte hypoxia, insulin-like growth factor-I-induced antiapoptotic signaling requires phosphatidylinositol-3-OH-kinase-dependent and mitogen-activated protein kinase-dependent activation of the transcription factor cAMP response element-binding protein. Circulation. 2001 Oct 23;104(17):2088–2094.
   PubMed Web of Science ®Google Scholar
• Rosova I, Dao M, Capoccia B, et al. Hypoxic preconditioning results in increased motility and improved therapeutic potential of human mesenchymal stem cells. Stem Cells. 2008 Aug;26(8):2173–2182.
   PubMed Web of Science ®Google Scholar
• Tang YL, Zhu W, Cheng M, et al. Hypoxic preconditioning enhances the benefit of cardiac progenitor cell therapy for treatment of myocardial infarction by inducing CXCR4 expression. Circ Res. 2009 May 22;104(10):1209–1216.
   PubMed Web of Science ®Google Scholar
• Wakai T, Narasimhan P, Sakata H, et al. Hypoxic preconditioning enhances neural stem cell transplantation therapy after intracerebral hemorrhage in mice. J Cereb Blood Flow Metab. 2016 Dec;36(12):2134–2145.
   PubMed Web of Science ®Google Scholar
• Cai Z, Luo W, Zhan H, et al. Hypoxia-inducible factor 1 is required for remote ischemic preconditioning of the heart. Proc Natl Acad Sci U S A. 2013 Oct 22;110(43):17462–17467.
   PubMed Web of Science ®Google Scholar
• Eckle T, Kohler D, Lehmann R, et al. Hypoxia-inducible factor-1 is central to cardioprotection: a new paradigm for ischemic preconditioning. Circulation. 2008 Jul 8;118(2):166–175.
   PubMed Web of Science ®Google Scholar
• Hahn JY, Song YB, Kim EK, et al. Ischemic postconditioning during primary percutaneous coronary intervention: the effects of postconditioning on myocardial reperfusion in patients with ST-segment elevation myocardial infarction (POST) randomized trial. Circulation. 2013 Oct 22;128(17):1889–1896.
   PubMed Web of Science ®Google Scholar
• Meybohm P, Bein B, Brosteanu O, et al. A multicenter trial of remote ischemic preconditioning for heart surgery. N Engl J Med. 2015 Oct 8;373(15):1397–1407.
   PubMed Web of Science ®Google Scholar
• Sloth AD, Schmidt MR, Munk K, et al. Improved long-term clinical outcomes in patients with ST-elevation myocardial infarction undergoing remote ischaemic conditioning as an adjunct to primary percutaneous coronary intervention. Eur Heart J. 2014 Jan;35(3):168–175.
   PubMed Web of Science ®Google Scholar
• Thielmann M, Kottenberg E, Kleinbongard P, et al. Cardioprotective and prognostic effects of remote ischaemic preconditioning in patients undergoing coronary artery bypass surgery: a single-centre randomised, double-blind, controlled trial. Lancet. 2013 Aug 17;382(9892):597–604.
   PubMed Web of Science ®Google Scholar
• Radisic M, Park H, Chen F, et al. Biomimetic approach to cardiac tissue engineering: oxygen carriers and channeled scaffolds. Tissue Eng. 2006 Aug;12(8):2077–2091.
   PubMedGoogle Scholar
• Lee HY, Kim HW, Lee JH, et al. Controlling oxygen release from hollow microparticles for prolonged cell survival under hypoxic environment. Biomaterials. 2015;53:583–591.
   PubMed Web of Science ®Google Scholar
• Patil PS, Fountas-Davis N, Huang H, et al. Fluorinated methacrylamide chitosan hydrogels enhance collagen synthesis in wound healing through increased oxygen availability. Acta Biomater. 2016 May;36:164–174.
   PubMed Web of Science ®Google Scholar
• Seekell RP, Lock AT, Peng Y, et al. Oxygen delivery using engineered microparticles. Proc Natl Acad Sci USA. 2016 Nov 1;113(44):12380–12385.
   PubMed Web of Science ®Google Scholar
• Harrison BS, Eberli D, Lee SJ, et al. Oxygen producing biomaterials for tissue regeneration. Biomaterials. 2007 Nov;28(31):4628–4634.
   PubMed Web of Science ®Google Scholar
• Oh SH, Ward CL, Atala A, et al. Oxygen generating scaffolds for enhancing engineered tissue survival. Biomaterials. 2009 Feb;30(5):757–762.
   PubMed Web of Science ®Google Scholar
• Fan Z, Xu Z, Niu H, et al. An injectable oxygen release system to augment cell survival and promote cardiac repair following myocardial infarction. Sci Rep. 2018 Jan 22;8(1):1371.
   PubMedGoogle Scholar
• Hirt MN, Boeddinghaus J, Mitchell A, et al. Functional improvement and maturation of rat and human engineered heart tissue by chronic electrical stimulation. J Mol Cell Cardiol. 2014 Sep;74:151–161.
   PubMed Web of Science ®Google Scholar
• Yang X, Pabon L, Murry CE. Engineering adolescence: maturation of human pluripotent stem cell-derived cardiomyocytes. Circ Res. 2014 Jan 31;114(3):511–523.
   PubMed Web of Science ®Google Scholar
• Ott HC, Matthiesen TS, Goh SK, et al. Perfusion-decellularized matrix: using nature’s platform to engineer a bioartificial heart. Nat Med. 2008 Feb;14(2):213–221. .
   PubMed Web of Science ®Google Scholar
• Ren X, Moser PT, Gilpin SE, et al. Engineering pulmonary vasculature in decellularized rat and human lungs. Nat Biotechnol. 2015 Oct;33(10):1097–1102.
   PubMed Web of Science ®Google Scholar
• Hooper RC, Hernandez KA, Boyko T, et al. Fabrication and in vivo microanastomosis of vascularized tissue-engineered constructs. Tissue Eng Part A. 2014 Oct;20(19–20):2711–2719.
   PubMed Web of Science ®Google Scholar
• Norotte C, Marga FS, Niklason LE, et al. Scaffold-free vascular tissue engineering using bioprinting. Biomaterials. 2009 Oct;30(30):5910–5917.
   PubMed Web of Science ®Google Scholar
• Schoneberg J, De Lorenzi F, Theek B, et al. Engineering biofunctional in vitro vessel models using a multilayer bioprinting technique. Sci Rep. 2018 Jul 11;8(1):10430.
   PubMedGoogle Scholar
• Miller JS, Stevens KR, Yang MT, et al. Rapid casting of patterned vascular networks for perfusable engineered three-dimensional tissues. Nat Mater. 2012 Sep;11(9):768–774.
   PubMed Web of Science ®Google Scholar
• Jia W, Gungor-Ozkerim PS, Zhang YS, et al. Direct 3D bioprinting of perfusable vascular constructs using a blend bioink. Biomaterials. 2016 Nov;106:58–68.
   PubMed Web of Science ®Google Scholar
• Zhang YS, Arneri A, Bersini S, et al. Bioprinting 3D microfibrous scaffolds for engineering endothelialized myocardium and heart-on-a-chip. Biomaterials. 2016 Dec;110:45–59.
   PubMed Web of Science ®Google Scholar
• Zhu W, Qu X, Zhu J, et al. Direct 3D bioprinting of prevascularized tissue constructs with complex microarchitecture. Biomaterials. 2017 Apr;124:106–115.
   PubMed Web of Science ®Google Scholar
• Zhang B, Montgomery M, Chamberlain MD, et al. Biodegradable scaffold with built-in vasculature for organ-on-a-chip engineering and direct surgical anastomosis. Nat Mater. 2016 Jun;15(6):669–678.
   PubMed Web of Science ®Google Scholar
• Lai BFL, Huyer LD, Lu RXZ, et al. InVADE: integrated Vasculature for Assessing Dynamic Events. Adv Funct Mater. 2017 Dec 8;27(46). English. DOI:10.1002/Adfm.201703524
   Web of Science ®Google Scholar
• Semenza GL. Regulation of oxygen homeostasis by hypoxia-inducible factor 1. Physiology (Bethesda). 2009 Apr;24:97–106.
   PubMed Web of Science ®Google Scholar
• Dengler VL, Galbraith M, Espinosa JM. Transcriptional regulation by hypoxia inducible factors. Crit Rev Biochem Mol Biol. 2014 Jan–Feb;49(1):1–15.
   PubMed Web of Science ®Google Scholar
• Manalo DJ, Rowan A, Lavoie T, et al. Transcriptional regulation of vascular endothelial cell responses to hypoxia by HIF-1. Blood. 2005 Jan 15;105(2):659–669.
   PubMed Web of Science ®Google Scholar
• Bruick RK, McKnight SL. A conserved family of prolyl-4-hydroxylases that modify HIF. Science. 2001 Nov 9;294(5545):1337–1340.
   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 Apr 20;292(5516):468–472.
   PubMed Web of Science ®Google Scholar
• Mahon PC, Hirota K, Semenza GL. FIH-1: a novel protein that interacts with HIF-1alpha and VHL to mediate repression of HIF-1 transcriptional activity. Genes Dev. 2001 Oct 15;15(20):2675–2686.
   PubMed Web of Science ®Google Scholar
• Lando D, Peet DJ, Gorman JJ, et al. FIH-1 is an asparaginyl hydroxylase enzyme that regulates the transcriptional activity of hypoxia-inducible factor. Genes Dev. 2002 Jun 15;16(12):1466–1471.
   PubMed Web of Science ®Google Scholar
• Hu CJ, Wang LY, Chodosh LA, et al. Differential roles of hypoxia-inducible factor 1alpha (HIF-1alpha) and HIF-2alpha in hypoxic gene regulation. Mol Cell Biol. 2003 Dec;23(24):9361–9374.
   PubMed Web of Science ®Google Scholar
• Warnecke C, Zaborowska Z, Kurreck J, et al. Differentiating the functional role of hypoxia-inducible factor (HIF)-1alpha and HIF-2alpha (EPAS-1) by the use of RNA interference: erythropoietin is a HIF-2alpha target gene in Hep3B and Kelly cells. FASEB J. 2004 Sep;18(12):1462–1464.
   PubMedGoogle Scholar
• Kelly BD, Hackett SF, Hirota K, et al. 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 Nov 28;93(11):1074–1081.
   PubMed Web of Science ®Google Scholar
• Koyasu S, Kobayashi M, Goto Y, et al. Regulatory mechanisms of hypoxia-inducible factor 1 activity: two decades of knowledge. Cancer Sci. 2018 Mar;109(3):560–571.
   PubMed Web of Science ®Google Scholar
• Wang Y, Wan C, Deng L, et al. The hypoxia-inducible factor alpha pathway couples angiogenesis to osteogenesis during skeletal development. J Clin Invest. 2007 Jun;117(6):1616–1626.
   PubMed Web of Science ®Google Scholar
• Zou D, Zhang Z, He J, et al. Blood vessel formation in the tissue-engineered bone with the constitutively active form of HIF-1alpha mediated BMSCs. Biomaterials. 2012 Mar;33(7):2097–2108.
   PubMed Web of Science ®Google Scholar
• HoWangYin KY, Loinard C, Bakker W, et al. HIF-prolyl hydroxylase 2 inhibition enhances the efficiency of mesenchymal stem cell-based therapies for the treatment of critical limb ischemia. Stem Cells. 2014 Jan;32(1):231–243.
   PubMed Web of Science ®Google Scholar
• Botusan IR, Sunkari VG, Savu O, et al. Stabilization of HIF-1alpha is critical to improve wound healing in diabetic mice. Proc Natl Acad Sci USA. 2008 Dec 9;105(49):19426–19431.
   PubMed Web of Science ®Google Scholar
• Holscher M, Schafer K, Krull S, et al. Unfavourable consequences of chronic cardiac HIF-1alpha stabilization. Cardiovasc Res. 2012 Apr 1;94(1):77–86.
   PubMed Web of Science ®Google Scholar
• Huang M, Chan DA, Jia F, et al. Short hairpin RNA interference therapy for ischemic heart disease. Circulation. 2008 Sep 30;118(14 Suppl):S226–33.
   PubMed Web of Science ®Google Scholar
• Bao W, Qin P, Needle S, et al. Chronic inhibition of hypoxia-inducible factor prolyl 4-hydroxylase improves ventricular performance, remodeling, and vascularity after myocardial infarction in the rat. J Cardiovasc Pharmacol. 2010 Aug;56(2):147–155.
   PubMed Web of Science ®Google Scholar
• Li Q, Chen H, Huang X, et al. Effects of 12 metal ions on iron regulatory protein 1 (IRP-1) and hypoxia-inducible factor-1 alpha (HIF-1alpha) and HIF-regulated genes. Toxicol Appl Pharmacol. 2006 Jun 15;213(3):245–255.
   PubMed Web of Science ®Google Scholar
• Martin F, Linden T, Katschinski DM, et al. Copper-dependent activation of hypoxia-inducible factor (HIF)-1: implications for ceruloplasmin regulation. Blood. 2005 Jun 15;105(12):4613–4619.
   PubMed Web of Science ®Google Scholar
• Goldberg MA, Dunning SP, Bunn HF. Regulation of the erythropoietin gene: evidence that the oxygen sensor is a heme protein. Science. 1988 Dec 9;242(4884):1412–1415.
   PubMed Web of Science ®Google Scholar
• Ho VT, Bunn HF. Effects of transition metals on the expression of the erythropoietin gene: further evidence that the oxygen sensor is a heme protein. Biochem Biophys Res Commun. 1996 Jun 5;223(1):175–180.
   PubMed Web of Science ®Google Scholar
• Triantafyllou A, Liakos P, Tsakalof A, et al. Cobalt induces hypoxia-inducible factor-1alpha (HIF-1alpha) in HeLa cells by an iron-independent, but ROS-, PI-3K- and MAPK-dependent mechanism. Free Radic Res. 2006 Aug;40(8):847–856.
   PubMed Web of Science ®Google Scholar
• Yuan Y, Beitner-Johnson D, Millhorn DE. Hypoxia-inducible factor 2alpha binds to cobalt in vitro. Biochem Biophys Res Commun. 2001 Nov 9;288(4):849–854.
   PubMed Web of Science ®Google Scholar
• Yuan Y, Hilliard G, Ferguson T, et al. 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. 2003 May 2;278(18):15911–15916.
   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 Jan;21(1–2):382–389.
   PubMed Web of Science ®Google Scholar
• Quinlan E, Partap S, Azevedo MM, et al. Hypoxia-mimicking bioactive glass/collagen glycosaminoglycan composite scaffolds to enhance angiogenesis and bone repair. Biomaterials. 2015 Jun;52:358–366.
   PubMed Web of Science ®Google Scholar
• Kargozar S, Lotfibakhshaiesh N, Ai J, et al. Strontium- and cobalt-substituted bioactive glasses seeded with human umbilical cord perivascular cells to promote bone regeneration via enhanced osteogenic and angiogenic activities. Acta Biomater. 2017 Aug;58:502–514.
   PubMed Web of Science ®Google Scholar
• Zhang ML, Wu CT, Li HY, et al. Preparation, characterization and in vitro angiogenic capacity of cobalt substituted beta-tricalcium phosphate ceramics. J Mater Chem. 2012 Oct 28;22(40):21686–21694. English.
   Web of Science ®Google Scholar
• Tahmasebi Birgani Z, Fennema E, Gijbels MJ, et al. Stimulatory effect of cobalt ions incorporated into calcium phosphate coatings on neovascularization in an in vivo intramuscular model in goats. Acta Biomater. 2016 May;36:267–276.
   PubMed Web of Science ®Google Scholar
• Liu X, Zhang W, Wu Z, et al. Copper levels affect targeting of hypoxia-inducible factor 1alpha to the promoters of hypoxia-regulated genes. J Biol Chem. 2018 Sep 21;293(38):14669–14677.
   PubMed Web of Science ®Google Scholar
• Feng W, Ye F, Xue W, et al. Copper regulation of hypoxia-inducible factor-1 activity. Mol Pharmacol. 2009 Jan;75(1):174–182.
   PubMed Web of Science ®Google Scholar
• Li S, Zhang J, Yang H, et al. Copper depletion inhibits CoCl2-induced aggressive phenotype of MCF-7 cells via downregulation of HIF-1 and inhibition of snail/twist-mediated epithelial-mesenchymal transition. Sci Rep. 2015 Jul 15;5:12410.
   PubMed 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 Jan;34(2):422–433.
   PubMed Web of Science ®Google Scholar
• Lin Y, Xiao W, Bal BS, et al. Effect of copper-doped silicate 13-93 bioactive glass scaffolds on the response of MC3T3-E1 cells in vitro and on bone regeneration and angiogenesis in rat calvarial defects in vivo. Mater Sci Eng C Mater Biol Appl. 2016;67:440–452.
   PubMed Web of Science ®Google Scholar
• Zhang W, Chang Q, Xu L, et al. Graphene oxide-copper nanocomposite-coated porous cap scaffold for vascularized bone regeneration via activation of Hif-1alpha. Adv Healthc Mater. 2016 Jun;5(11):1299–1309.
   PubMed Web of Science ®Google Scholar
• Barralet J, Gbureck U, Habibovic P, et al. Angiogenesis in calcium phosphate scaffolds by inorganic copper ion release. Tissue Eng Part A. 2009 Jul;15(7):1601–1609.
   PubMed Web of Science ®Google Scholar
• Gbureck U, Hölzel T, Doillon CJ, et al. Direct printing of bioceramic implants with spatially localized angiogenic factors. Adv Mater. 2007;19(6):795–800.
   Web of Science ®Google Scholar
• Zhao S, Li L, Wang H, et al. Wound dressings composed of copper-doped borate bioactive glass microfibers stimulate angiogenesis and heal full-thickness skin defects in a rodent model. Biomaterials. 2015;53:379–391.
   PubMed Web of Science ®Google Scholar
• Li J, Zhai D, Lv F, et al. Preparation of copper-containing bioactive glass/eggshell membrane nanocomposites for improving angiogenesis, antibacterial activity and wound healing. Acta Biomater. 2016 May;36:254–266.
   PubMed Web of Science ®Google Scholar
• Li H, Li J, Jiang J, et al. An osteogenesis/angiogenesis-stimulation artificial ligament for anterior cruciate ligament reconstruction. Acta Biomater. 2017 May;54:399–410.
   PubMed Web of Science ®Google Scholar
• Wang GL, Semenza GL. Desferrioxamine induces erythropoietin gene expression and hypoxia-inducible factor 1 DNA-binding activity: implications for models of hypoxia signal transduction. Blood. 1993 Dec 15;82(12):3610–3615.
   PubMed Web of Science ®Google Scholar
• Wang C, Cai Y, Zhang Y, et al. Local injection of deferoxamine improves neovascularization in ischemic diabetic random flap by increasing HIF-1alpha and VEGF expression. PLoS One. 2014;9(6):e100818.
   PubMed Web of Science ®Google Scholar
• Zhang C, Li Y, Cornelia R, et al. Regulation of VEGF expression by HIF-1alpha in the femoral head cartilage following ischemia osteonecrosis. Sci Rep. 2012;2:650.
   PubMed Web of Science ®Google Scholar
• Dongiovanni P, Valenti L, Ludovica Fracanzani A, et al. Iron depletion by deferoxamine up-regulates glucose uptake and insulin signaling in hepatoma cells and in rat liver. Am J Pathol. 2008 Mar;172(3):738–747.
   PubMed Web of Science ®Google Scholar
• Jiang X, Malkovskiy AV, Tian W, et al. Promotion of airway anastomotic microvascular regeneration and alleviation of airway ischemia by deferoxamine nanoparticles. Biomaterials. 2014 Jan;35(2):803–813.
   PubMed Web of Science ®Google Scholar
• Vignesh S, Sivashanmugam A, Mohandas A, et al. Injectable deferoxamine nanoparticles loaded chitosan-hyaluronic acid coacervate hydrogel for therapeutic angiogenesis. Colloids Surf B Biointerfaces. 2018;161:129–138.
   PubMed Web of Science ®Google Scholar
• Duscher D, Neofytou E, Wong VW, et al. Transdermal deferoxamine prevents pressure-induced diabetic ulcers. Proc Natl Acad Sci USA. 2015 Jan 6;112(1):94–99.
   PubMed Web of Science ®Google Scholar
• Yao Q, Liu Y, Selvaratnam B, et al. Mesoporous silicate nanoparticles/3D nanofibrous scaffold-mediated dual-drug delivery for bone tissue engineering. J Control Release. 2018;279:69–78.
   PubMed Web of Science ®Google Scholar
• Jia P, Chen H, Kang H, et al. Deferoxamine released from poly(lactic-co-glycolic acid) promotes healing of osteoporotic bone defect via enhanced angiogenesis and osteogenesis. J Biomed Mater Res A. 2016 Oct;104(10):2515–2527.
   PubMed Web of Science ®Google Scholar
• Li J, Fan L, Yu Z, et al. The effect of deferoxamine on angiogenesis and bone repair in steroid-induced osteonecrosis of rabbit femoral heads. Exp Biol Med (Maywood). 2015 Feb;240(2):273–280.
   PubMed Web of Science ®Google Scholar
• Saito T, Tabata Y. Hypoxia-induced angiogenesis is increased by the controlled release of deferoxiamine from gelatin hydrogels. Acta Biomater. 2014 Aug;10(8):3641–3649.
   PubMed Web of Science ®Google Scholar
• Wahl EA, Schenck TL, Machens HG, et al. VEGF released by deferoxamine preconditioned mesenchymal stem cells seeded on collagen-GAG substrates enhances neovascularization. Sci Rep. 2016;6:36879.
   PubMed Web of Science ®Google Scholar
• Schley G, Klanke B, Schodel J, et al. Selective stabilization of HIF-1alpha in renal tubular cells by 2-oxoglutarate analogues. Am J Pathol. 2012 Nov;181(5):1595–1606.
   PubMed Web of Science ®Google Scholar
• Shafighi M, Olariu R, Fathi AR, et al. Dimethyloxalylglycine stabilizes HIF-1alpha in cultured human endothelial cells and increases random-pattern skin flap survival in vivo. Plast Reconstr Surg. 2011 Aug;128(2):415–422.
   PubMed Web of Science ®Google Scholar
• Sham A, Martinez EC, Beyer S, et al. Incorporation of a prolyl hydroxylase inhibitor into scaffolds: a strategy for stimulating vascularization. Tissue Eng Part A. 2015 Mar;21(5–6):1106–1115.
   PubMed Web of Science ®Google Scholar
• Zhang J, Feng Z, Wei J, et al. Repair of critical-sized mandible defects in aged rat using hypoxia preconditioned BMSCs with up-regulation of Hif-1alpha. Int J Biol Sci. 2018;14(4):449–460.
   PubMed Web of Science ®Google Scholar
• Ding H, Chen S, Song WQ, et al. Dimethyloxaloylglycine improves angiogenic activity of bone marrow stromal cells in the tissue-engineered bone. Int J Biol Sci. 2014;10(7):746–756.
   PubMed 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 Nov;9(11):9159–9168.
   PubMed Web of Science ®Google Scholar
• Gao W, Sun L, Fu X, et al. Enhanced diabetic wound healing by electrospun core–sheath fibers loaded with dimethyloxalylglycine. J Mater Chem B. 2018;6(2):277–288.
   Web of Science ®Google Scholar
• Kuchler U, Keibl C, Fugl A, et al. Dimethyloxalylglycine lyophilized onto bone substitutes increase vessel area in rat calvarial defects. Clin Oral Implants Res. 2015 May;26(5):485–491.
   PubMed Web of Science ®Google Scholar
• Woo KM, Jung HM, Oh JH, et al. Synergistic effects of dimethyloxalylglycine and butyrate incorporated into alpha-calcium sulfate on bone regeneration. Biomaterials. 2015 Jan;39:1–14.
   PubMed Web of Science ®Google Scholar
• Zhdanov AV, Okkelman IA, Collins FW, et al. A novel effect of DMOG on cell metabolism: direct inhibition of mitochondrial function precedes HIF target gene expression. Biochim Biophys Acta. 2015 Oct;1847(10):1254–1266.
   PubMed Web of Science ®Google Scholar
• Isaacs JS, Jung YJ, Mole DR, et al. HIF overexpression correlates with biallelic loss of fumarate hydratase in renal cancer: novel role of fumarate in regulation of HIF stability. Cancer Cell. 2005 8;Aug(2):143–153.
   Google Scholar
• Nishimoto-Hazuku A, Hirase T, Ide N, et al. Simvastatin stimulates vascular endothelial growth factor production by hypoxia-inducible factor-1alpha upregulation in endothelial cells. J Cardiovasc Pharmacol. 2008 Mar;51(3):267–273.
   PubMed Web of Science ®Google Scholar
• Thirunavukkarasu M, Selvaraju V, Dunna NR, et al. Simvastatin treatment inhibits hypoxia inducible factor 1-alpha-(HIF-1alpha)-prolyl-4-hydroxylase 3 (PHD-3) and increases angiogenesis after myocardial infarction in streptozotocin-induced diabetic rat. Int J Cardiol. 2013 Oct 3;168(3):2474–2480.
   PubMed Web of Science ®Google Scholar
• Pullisaar H, Tiainen H, Landin MA, et al. Enhanced in vitro osteoblast differentiation on TiO2 scaffold coated with alginate hydrogel containing simvastatin. J Tissue Eng. 2013;4:2041731413515670.
   Google Scholar
• Yu WL, Sun TW, Qi C, et al. Enhanced osteogenesis and angiogenesis by mesoporous hydroxyapatite microspheres-derived simvastatin sustained release system for superior bone regeneration. Sci Rep. 2017;7:44129.
   PubMed Web of Science ®Google Scholar
• Liu H, Li W, Liu C, et al. Incorporating simvastatin/poloxamer 407 hydrogel into 3D-printed porous Ti6Al4V scaffolds for the promotion of angiogenesis, osseointegration and bone ingrowth. Biofabrication. 2016 Oct 27;8(4):045012.
   PubMed Web of Science ®Google Scholar
• Ariazi JL, Duffy KJ, Adams DF, et al. Discovery and preclinical characterization of GSK1278863 (Daprodustat), a small molecule hypoxia inducible factor-prolyl hydroxylase inhibitor for anemia. J Pharmacol Exp Ther. 2017 Dec;363(3):336–347.
   PubMed Web of Science ®Google Scholar
• Beck H, Jeske M, Thede K, et al. Discovery of molidustat (BAY 85–3934): a small-molecule oral HIF-Prolyl Hydroxylase (HIF-PH) inhibitor for the treatment of renal anemia. ChemMedChem. 2018 May 23;13(10):988–1003.
   PubMed Web of Science ®Google Scholar
• Gupta N, Wish JB. Hypoxia-inducible factor prolyl hydroxylase inhibitors: a potential new treatment for anemia in patients with CKD. Am J Kidney Dis. 2017 Jun;69(6):815–826.
   PubMed Web of Science ®Google Scholar
• Provenzano R, Besarab A, Wright S, et al. Roxadustat (FG-4592) versus epoetin alfa for anemia in patients receiving maintenance hemodialysis: a phase 2, randomized, 6- to 19-Week, open-label, active-comparator, dose-ranging, safety and exploratory efficacy study. Am J Kidney Dis. 2016 Jun;67(6):912–924.
   PubMed Web of Science ®Google Scholar
• Akizawa T, Tsubakihara Y, Nangaku M, et al. Effects of daprodustat, a novel hypoxia-inducible factor prolyl hydroxylase inhibitor on anemia management in Japanese hemodialysis subjects. Am J Nephrol. 2017;45(2):127–135.
   PubMed Web of Science ®Google Scholar
• Martin ER, Smith MT, Maroni BJ, et al. Clinical trial of vadadustat in patients with anemia secondary to stage 3 or 4 chronic kidney disease. Am J Nephrol. 2017;45(5):380–388.
   PubMed Web of Science ®Google Scholar
• Griffith CK, Miller C, Sainson RC, et al. Diffusion limits of an in vitro thick prevascularized tissue. Tissue Eng. 2005 Jan-Feb;11(1–2):257–266.
   PubMedGoogle Scholar
• Brem H, Folkman J. Inhibition of tumor angiogenesis mediated by cartilage. J Exp Med. 1975;1412:427–439. English.
   PubMed Web of Science ®Google Scholar