164
Views
3
CrossRef citations to date
0
Altmetric
Review

Optimizing the host substrate environment for cardiac angiogenesis, arteriogenesis, and myogenesis

, , &
Pages 435-447 | Received 13 Oct 2016, Accepted 06 Feb 2017, Published online: 17 Feb 2017

References

  • Asahara T, Kawamoto A, Masuda H. Concise review: circulating endothelial progenitor cells for vascular medicine. Stem Cells. 2011;29(11):1650–1655.
  • Resch T, Pircher A, Kahler CM, et al. Endothelial progenitor cells: current issues on characterization and challenging clinical applications. Stem Cell Rev. 2012;8(3):926–939.
  • Giordano C, Kuraitis D, Beanlands RS, et al. Cell-based vasculogenic studies in preclinical models of chronic myocardial ischaemia and hibernation. Expert Opin Biol Ther. 2013;13(3):411–428.
  • Borselli C, Storrie H, Benesch-Lee F, et al. Functional muscle regeneration with combined delivery of angiogenesis and myogenesis factors. Proc Natl Acad Sci U S A. 2010;107(8):3287–3292.
  • Kuraitis D, Ebadi D, Zhang P, et al. Injected matrix stimulates myogenesis and regeneration of mouse skeletal muscle after ischaemic injury. Eur Cell Mater. 2012;24:175–195.
  • Murohara T, Asahara T, Silver M, et al. Nitric oxide synthase modulates angiogenesis in response to tissue ischemia. J Clin Invest. 1998;101(11):2567–2578.
  • Duan J, Murohara T, Ikeda H, et al. Hypercholesterolemia inhibits angiogenesis in response to hindlimb ischemia: nitric oxide-dependent mechanism. Circulation. 2000;102(19Suppl 3):Iii370–6.
  • Voisine P, Bianchi C, Ruel M, et al. Inhibition of the cardiac angiogenic response to exogenous vascular endothelial growth factor. Surgery. 2004;136(2):407–415.
  • Sellke FW, Lassaletta AD, Robich MP, et al. Regenerative therapies for improving myocardial perfusion in patients with cardiovascular disease: failure to meet expectations but optimism for the future. Curr Vasc Pharmacol. 2012;10(3):300–309.
  • Kuraitis D, Giordano C, Ruel M, et al. Exploiting extracellular matrix-stem cell interactions: a review of natural materials for therapeutic muscle regeneration. Biomaterials. 2012;33(2):428–443.
  • Segers VF, Lee RT. Biomaterials to enhance stem cell function in the heart. Circ Res. 2011;109(8):910–922.
  • Hirata Y, Nagata D, Suzuki E, et al. Diagnosis and treatment of endothelial dysfunction in cardiovascular disease. Int Heart J. 2010;51(1):1–6.
  • Park KH, Park WJ. Endothelial dysfunction: clinical implications in cardiovascular disease and therapeutic approaches. J Korean Med Sci. 2015;30(9):1213–1225.
  • Costa ED, Rezende BA, Cortes SF, et al. Neuronal nitric oxide synthase in vascular physiology and diseases. Front Physiol. 2016;7:206.
  • Yang G, Lucas R, Caldwell R, et al. Novel mechanisms of endothelial dysfunction in diabetes. J Cardiovasc Dis Res. 2010;1(2):59–63.
  • Ku DD. Coronary vascular reactivity after acute myocardial ischemia. Science. 1982;218(4572):576–578.
  • Kaeffer N, Richard V, Thuillez C. Delayed coronary endothelial protection 24 hours after preconditioning: role of free radicals. Circulation. 1997;96(7):2311–2316.
  • Ebrahimian TG, Heymes C, You D, et al. NADPH oxidase-derived overproduction of reactive oxygen species impairs postischemic neovascularization in mice with type 1 diabetes. Am J Pathol. 2006;169(2):719–728.
  • Capettini LS, Cortes SF, Silva JF, et al. Decreased production of neuronal NOS-derived hydrogen peroxide contributes to endothelial dysfunction in atherosclerosis. Br J Pharmacol. 2011;164(6):1738–1748.
  • Silva GC, Silva JF, Diniz TF, et al. Endothelial dysfunction in DOCA-salt-hypertensive mice: role of neuronal nitric oxide synthase-derived hydrogen peroxide. Clin Sci (Lond). 2016;130(11):895–906.
  • Laude K, Thuillez C, Richard V. Coronary endothelial dysfunction after ischemia and reperfusion: a new therapeutic target? Braz J Med Biol Res. 2001;34(1):1–7.
  • Chen Q, Varga M, Wang X, et al. Overexpression of nitric oxide synthase restores circulating angiogenic cell function in patients with coronary artery disease: implications for autologous cell therapy for myocardial infarction. J Am Heart Assoc. 2016; 5(1):e002257.
  • Tagawa S, Nakanishi C, Mori M, et al. Determination of early and late endothelial progenitor cells in peripheral circulation and their clinical association with coronary artery disease. Int J Vasc Med. 2015;v2015:674213.
  • Molgat AS, Tilokee EL, Rafatian G, et al. Hyperglycemia inhibits cardiac stem cell-mediated cardiac repair and angiogenic capacity. Circulation. 2014;130(11 Suppl 1):S70–6.
  • Peng J, Liu B, Ma QL, et al. Dysfunctional endothelial progenitor cells in cardiovascular diseases: role of NADPH oxidase. J Cardiovasc Pharmacol. 2015;65(1):80–87.
  • Hill JM, Zalos G, Halcox JP, et al. Circulating endothelial progenitor cells, vascular function, and cardiovascular risk. N Engl J Med. 2003;348(7):593–600.
  • Kumar D, Branch BG, Pattillo CB, et al. Chronic sodium nitrite therapy augments ischemia-induced angiogenesis and arteriogenesis. Proc Natl Acad Sci U S A. 2008;105(21):7540–7545.
  • Yang B, Cai B, Deng P, et al. Nitric oxide increases arterial endotheial permeability through mediating VE-cadherin expression during arteriogenesis. PLoS One. 2015;10(7):e0127931.
  • Lasch M, Caballero-Martinez A, Troidl K, et al. Arginase inhibition attenuates arteriogenesis and interferes with M2 macrophage accumulation. Lab Invest. 2016;96(8):830–838.
  • Silvestre JS, Tamarat R, Ebrahimian TG, et al. Vascular endothelial growth factor-B promotes in vivo angiogenesis. Circ Res. 2003;93(2):114–123.
  • Cui X, Chopp M, Zacharek A, et al. Role of endothelial nitric oxide synthetase in arteriogenesis after stroke in mice. Neuroscience. 2009;159(2):744–750.
  • Faber JE, Chilian WM, Deindl E, et al. A brief etymology of the collateral circulation. Arterioscler Thromb Vasc Biol. 2014;34(9):1854–1859.
  • Wahlberg E. Angiogenesis and arteriogenesis in limb ischemia. J Vasc Surg. 2003;38(1):198–203.
  • Semenza GL. Vasculogenesis, angiogenesis, and arteriogenesis: mechanisms of blood vessel formation and remodeling. J Cell Biochem. 2007;102(4):840–847.
  • Carmeliet P, Jain RK. Molecular mechanisms and clinical applications of angiogenesis. Nature. 2011;473(7347):298–307.
  • Hoeben A, Landuyt B, Highley MS, et al. Vascular endothelial growth factor and angiogenesis. Pharmacol Rev. 2004;56(4):549–580.
  • Kofler NM, Simons M. Angiogenesis versus arteriogenesis: neuropilin 1 modulation of VEGF signaling. F1000Prime Rep. 2015;7:26.
  • Helisch A, Ware JA. Therapeutic angiogenesis for ischemic heart disease. Adv Exp Med Biol. 2000;476:327–350.
  • Gerber HP, McMurtrey A, Kowalski J, et al. Vascular endothelial growth factor regulates endothelial cell survival through the phosphatidylinositol 3ʹ-kinase/Akt signal transduction pathway. Requirement for Flk-1/KDR activation. J Biol Chem. 1998;273(46):30336–30343.
  • Lahteenvuo JE, Lahteenvuo MT, Kivela A, et al. Vascular endothelial growth factor-B induces myocardium-specific angiogenesis and arteriogenesis via vascular endothelial growth factor receptor-1- and neuropilin receptor-1-dependent mechanisms. Circulation. 2009;119(6):845–856.
  • Li GH, Luo B, Lv YX, et al. Dual effects of VEGF-B on activating cardiomyocytes and cardiac stem cells to protect the heart against short- and long-term ischemia-reperfusion injury. J Transl Med. 2016;14(1):116.
  • Witzenbichler B, Asahara T, Murohara T, et al. Vascular endothelial growth factor-C (VEGF-C/VEGF-2) promotes angiogenesis in the setting of tissue ischemia. Am J Pathol. 1998;153(2):381–394.
  • Patila T, Ikonen T, Rutanen J, et al. Vascular endothelial growth factor C-induced collateral formation in a model of myocardial ischemia. J Heart Lung Transplant. 2006;25(2):206–213.
  • Murakami M, Nguyen LT, Zhuang ZW, et al. The FGF system has a key role in regulating vascular integrity. J Clin Invest. 2008;118(10):3355–3366.
  • Kardami E, Liu L, Pasumarthi SK, et al. Regulation of basic fibroblast growth factor (bFGF) and FGF receptors in the heart. Ann N Y Acad Sci. 1995;752:(–⋂353-69.
  • Seghezzi G, Patel S, Ren CJ, et al. Fibroblast growth factor-2 (FGF-2) induces vascular endothelial growth factor (VEGF) expression in the endothelial cells of forming capillaries: an autocrine mechanism contributing to angiogenesis. J Cell Biol. 1998;141(7):1659–1673.
  • Harada K, Grossman W, Friedman M, et al. Basic fibroblast growth factor improves myocardial function in chronically ischemic porcine hearts. J Clin Invest. 1994;94(2):623–630.
  • Horrigan MC, Malycky JL, Ellis SG, et al. Reduction in myocardial infarct size by basic fibroblast growth factor following coronary occlusion in a canine model. Int J Cardiol. 1999;68(Suppl 1):S85–91.
  • Iwatate M, Miura T, Ikeda Y, et al. Effects of in vivo gene transfer of fibroblast growth factor-2 on cardiac function and collateral vessel formation in the microembolized rabbit heart. Jpn Circ J. 2001;65(3):226–231.
  • Goetz R, Mohammadi M. Exploring mechanisms of FGF signalling through the lens of structural biology. Nat Rev Mol Cell Biol. 2013;14(3):166–180.
  • Detillieux KA, Sheikh F, Kardami E, et al. Biological activities of fibroblast growth factor-2 in the adult myocardium. Cardiovasc Res. 2003;57(1):8–19.
  • Asahara T, Bauters C, Zheng LP, et al. Synergistic effect of vascular endothelial growth factor and basic fibroblast growth factor on angiogenesis in vivo. Circulation. 1995;92(9 Suppl):Ii365–71.
  • Nillesen ST, Geutjes PJ, Wismans R, et al. Increased angiogenesis and blood vessel maturation in acellular collagen-heparin scaffolds containing both FGF2 and VEGF. Biomaterials. 2007;28(6):1123–1131.
  • Gerthoffer WT. Mechanisms of vascular smooth muscle cell migration. Circ Res. 2007;100(5):607–621.
  • Kupatt C, Hinkel R, Pfosser A, et al. Cotransfection of vascular endothelial growth factor-A and platelet-derived growth factor-B via recombinant adeno-associated virus resolves chronic ischemic malperfusion role of vessel maturation. J Am Coll Cardiol. 2010;56(5):414–422.
  • Cao R, Brakenhielm E, Pawliuk R, et al. Angiogenic synergism, vascular stability and improvement of hind-limb ischemia by a combination of PDGF-BB and FGF-2. Nat Med. 2003;9(5):604–613.
  • Ruel M, Wu GF, Khan TA, et al. Inhibition of the cardiac angiogenic response to surgical FGF-2 therapy in a Swine endothelial dysfunction model. Circulation. 2003;108(Suppl 1):Ii335–40.
  • Boodhwani M, Voisine P, Ruel M, et al. Comparison of vascular endothelial growth factor and fibroblast growth factor-2 in a swine model of endothelial dysfunction. Eur J Cardiothorac Surg. 2008;33(4):645–650. discussion 251-2.
  • Messina S, Mazzeo A, Bitto A, et al. VEGF overexpression via adeno-associated virus gene transfer promotes skeletal muscle regeneration and enhances muscle function in mdx mice. Faseb J. 2007;21(13):3737–3746.
  • Deasy BM, Feduska JM, Payne TR, et al. Effect of VEGF on the regenerative capacity of muscle stem cells in dystrophic skeletal muscle. Mol Ther. 2009;17(10):1788–1798.
  • Pelosi L, Giacinti C, Nardis C, et al. Local expression of IGF-1 accelerates muscle regeneration by rapidly modulating inflammatory cytokines and chemokines. Faseb J. 2007;21(7):1393–1402.
  • Kothapalli CR, Ramamurthi A. Benefits of concurrent delivery of hyaluronan and IGF-1 cues to regeneration of crosslinked elastin matrices by adult rat vascular cells. J Tissue Eng Regen Med. 2008;2(2–3):106–116.
  • Suuronen EJ, Zhang P, Kuraitis D, et al. An acellular matrix-bound ligand enhances the mobilization, recruitment and therapeutic effects of circulating progenitor cells in a hindlimb ischemia model. Faseb J. 2009;23(5):1447–1458.
  • Suuronen EJ, Hazra S, Zhang P, et al. Impairment of human cell-based vasculogenesis in rats by hypercholesterolemia-induced endothelial dysfunction and rescue with L-arginine supplementation. J Thorac Cardiovasc Surg. 2010;139(1):209–16.e2.
  • Nematbakhsh M, Haghjooyjavanmard S, Mahmoodi F, et al. The prevention of endothelial dysfunction through endothelial cell apoptosis inhibition in a hypercholesterolemic rabbit model: the effect of L-arginine supplementation. Lipids Health Dis. 2008;7:27.
  • Martinez-Romero R, Canuelo A, Siles E, et al. Nitric oxide modulates hypoxia-inducible factor-1 and poly (ADP-ribose) polymerase-1 cross talk in response to hypobaric hypoxia. J Appl Physiol. (1985).2012;112(5):816–823.
  • Saleh AI, Abdel Maksoud SM, El-Maraghy SA, et al. Protective effect of L-arginine in experimentally induced myocardial ischemia: comparison with aspirin. J Cardiovasc Pharmacol Ther. 2011;16(1):53–62.
  • Voisine P, Bianchi C, Khan TA, et al. Normalization of coronary microvascular reactivity and improvement in myocardial perfusion by surgical vascular endothelial growth factor therapy combined with oral supplementation of l-arginine in a porcine model of endothelial dysfunction. J Thorac Cardiovasc Surg. 2005;129(6):1414–1420.
  • Voisine P, Li J, Bianchi C, et al. Effects of L-arginine on fibroblast growth factor 2-induced angiogenesis in a model of endothelial dysfunction. Circulation. 2005;112(9 Suppl):I202–7.
  • Javanmard SH, Gheisari Y, Soleimani M, et al. Effect of L-arginine on circulating endothelial progenitor cells in hypercholesterolemic rabbits. Int J Cardiol. 2010;143(2):213–216.
  • Luo L, Chen B, Huang Y, et al. Cardioprotective activity of placental growth factor combined with oral supplementation of l-arginine in a rat model of acute myocardial infarction. Drug Des Devel Ther. 2016;10:3483–3492.
  • Ruel M, Beanlands RS, Lortie M, et al. Concomitant treatment with oral L-arginine improves the efficacy of surgical angiogenesis in patients with severe diffuse coronary artery disease: the endothelial modulation in angiogenic therapy randomized controlled trial. J Thorac Cardiovasc Surg. 2008;135(4):762–770. .
  • Wang X, Liang F, Jiao X, et al. Diverse effects of L-arginine on cardiac function of rats subjected to myocardial ischemia and reperfusion in vivo. Acta Biochim Biophys Sin (Shanghai). 2007;39(3):201–207.
  • Schulman SP, Becker LC, Kass DA, et al. L-arginine therapy in acute myocardial infarction: the vascular interaction with age n myocardial infarction (VINTAGE MI) randomized clinical trial. Jama. 2006;295(1):58–64.
  • Marzo F, Lavorgna A, Coluzzi G, et al. Erythropoietin in heart and vessels: focus on transcription and signalling pathways. J Thromb Thrombolysis. 2008;26(3):183–187.
  • Burger DE, Xiang FL, Hammoud L, et al. Erythropoietin protects the heart from ventricular arrhythmia during ischemia and reperfusion via neuronal nitric-oxide synthase. J Pharmacol Exp Ther. 2009;329(3):900–907.
  • Kawachi K, Iso Y, Sato T, et al. Effects of erythropoietin on angiogenesis after myocardial infarction in porcine. Heart Vessels. 2012;27(1):79–88.
  • Westenbrink BD, Lipsic E, van der Meer P, et al. Erythropoietin improves cardiac function through endothelial progenitor cell and vascular endothelial growth factor mediated neovascularization. Eur Heart J. 2007;28(16):2018–2027.
  • Ott I, Schulz S, Mehilli J, et al. Erythropoietin in patients with acute ST-segment elevation myocardial infarction undergoing primary percutaneous coronary intervention: a randomized, double-blind trial. Circ Cardiovasc Interv. 2010;3(5):408–413.
  • Deng B, Shen L, Wu Y, et al. Delivery of alginate-chitosan hydrogel promotes endogenous repair and preserves cardiac function in rats with myocardial infarction. J Biomed Mater Res A. 2015;103(3):907–918.
  • Seif-Naraghi SB, Singelyn JM, Salvatore MA, et al. Safety and efficacy of an injectable extracellular matrix hydrogel for treating myocardial infarction. Sci Transl Med. 2013;5(173):173ra25.
  • Grotenhuis N, Bayon Y, Lange JF, et al. A culture model to analyze the acute biomaterial-dependent reaction of human primary macrophages. Biochem Biophys Res Commun. 2013;433(1):115–120.
  • Wang Z, Cui Y, Wang J, et al. The effect of thick fibers and large pores of electrospun poly(epsilon-caprolactone) vascular grafts on macrophage polarization and arterial regeneration. Biomaterials. 2014;35(22):5700–5710.
  • Sarig U, Sarig H, de-Berardinis E, et al. Natural myocardial ECM patch drives cardiac progenitor based restoration even after scarring. Acta Biomater. 2016;44:209–220.
  • Vaz CM, Van Tuijl S, Bouten CV, et al. Design of scaffolds for blood vessel tissue engineering using a multi-layering electrospinning technique. Acta Biomater. 2005;1(5):575–582.
  • Johnson TD, Christman KL. Injectable hydrogel therapies and their delivery strategies for treating myocardial infarction. Expert Opin Drug Deliv. 2013;10(1):59–72.
  • Bott K, Upton Z, Schrobback K, et al. The effect of matrix characteristics on fibroblast proliferation in 3D gels. Biomaterials. 2010;31(32):8454–8464.
  • Yao X, Liu Y, Gao J, et al. Nitric oxide releasing hydrogel enhances the therapeutic efficacy of mesenchymal stem cells for myocardial infarction. Biomaterials. 2015;60:130–140.
  • Dixit P, Katare R. Challenges in identifying the best source of stem cells for cardiac regeneration therapy. Stem Cell Res Ther. 2015;6(1):26.
  • Hare JM, Fishman JE, Gerstenblith G, et al. Comparison of allogeneic vs autologous bone marrow-derived mesenchymal stem cells delivered by transendocardial injection in patients with ischemic cardiomyopathy: the POSEIDON randomized trial. Jama. 2012;308(22):2369–2379.
  • Yoon YS, Park JS, Tkebuchava T, et al. Unexpected severe calcification after transplantation of bone marrow cells in acute myocardial infarction. Circulation. 2004;109(25):3154–3157.
  • Cheng CC, Chang SJ, Chueh YN, et al. Distinct angiogenesis roles and surface markers of early and late endothelial progenitor cells revealed by functional group analyses. BMC Genomics. 2013;14:182.
  • Urbich C, Aicher A, Heeschen C, et al. Soluble factors released by endothelial progenitor cells promote migration of endothelial cells and cardiac resident progenitor cells. J Mol Cell Cardiol. 2005;39(5):733–742.
  • Suuronen EJ, Price J, Veinot JP, et al. Comparative effects of mesenchymal progenitor cells, endothelial progenitor cells, or their combination on myocardial infarct regeneration and cardiac function. J Thorac Cardiovasc Surg. 2007;134(5):1249–1258.
  • Hirschi KK, Ingram DA, Yoder MC. Assessing identity, phenotype, and fate of endothelial progenitor cells. Arterioscler Thromb Vasc Biol. 2008;28(9):1584–1595.
  • Ahmadi A, McNeill B, Vulesevic B, et al. The role of integrin A2 in cell and matrix therapy that improves perfusion, viability and function of infarcted myocardium. Biomaterials. 2014;35(17):4749–4758.
  • Giordano C, Thorn SL, Renaud JM, et al. Preclinical evaluation of biopolymer-delivered circulating angiogenic cells in a swine model of hibernating myocardium. Circ Cardiovasc Imaging. 2013;6(6):982–991.
  • Garbern JC, Lee RT. Cardiac stem cell therapy and the promise of heart regeneration. Cell Stem Cell. 2013;12(6):689–698.
  • Smith RR, Barile L, Cho HC, et al. Regenerative potential of cardiosphere-derived cells expanded from percutaneous endomyocardial biopsy specimens. Circulation. 2007;115(7):896–908.
  • Davis DR, Kizana E, Terrovitis J, et al. Isolation and expansion of functionally-competent cardiac progenitor cells directly from heart biopsies. J Mol Cell Cardiol. 2010;49(2):312–321.
  • Latham N, Ye B, Jackson R, et al. Human blood and cardiac stem cells synergize to enhance cardiac repair when cotransplanted into ischemic myocardium. Circulation. 2013;128(11 Suppl 1):S105–12.
  • Fadini GP, Agostini C, Sartore S, et al. Endothelial progenitor cells in the natural history of atherosclerosis. Atherosclerosis. 2007;194(1):46–54.
  • Ward MR, Thompson KA, Isaac K, et al. Nitric oxide synthase gene transfer restores activity of circulating angiogenic cells from patients with coronary artery disease. Mol Ther. 2011;19(7):1323–1330.
  • Mayfield AE, Tilokee EL, Latham N, et al. The effect of encapsulation of cardiac stem cells within matrix-enriched hydrogel capsules on cell survival, post-ischemic cell retention and cardiac function. Biomaterials. 2014;35(1):133–142.
  • McNeill B, Vulesevic B, Ostojic A, et al. Collagen matrix-induced expression of integrin alphaVbeta3 in circulating angiogenic cells can be targeted by matricellular protein CCN1 to enhance their function. Faseb J. 2015;29(4):1198–1207.
  • Valarmathi MT, Goodwin RL, Fuseler JW, et al. A 3-D cardiac muscle construct for exploring adult marrow stem cell based myocardial regeneration. Biomaterials. 2010;31(12):3185–3200.
  • Chun YW, Balikov DA, Feaster TK, et al. Combinatorial polymer matrices enhance in vitro maturation of human induced pluripotent stem cell-derived cardiomyocytes. Biomaterials. 2015;67:52–64.
  • Sun JS, Tsuang YH, Chang WH, et al. Effect of hydroxyapatite particle size on myoblasts and fibroblasts. Biomaterials. 1997;18(9):683–690.
  • He Q, Zhao Y, Chen B, et al. Improved cellularization and angiogenesis using collagen scaffolds chemically conjugated with vascular endothelial growth factor. Acta Biomater. 2011;7(3):1084–1093.
  • Miyagi Y, Chiu LL, Cimini M, et al. Biodegradable collagen patch with covalently immobilized VEGF for myocardial repair. Biomaterials. 2011;32(5):1280–1290.
  • Garbern JC, Minami E, Stayton PS, et al. Delivery of basic fibroblast growth factor with a pH-responsive, injectable hydrogel to improve angiogenesis in infarcted myocardium. Biomaterials. 2011;32(9):2407–2416.
  • You J-O, Rafat M, Ye GJC, et al. Nanoengineering the heart: conductive scaffolds enhance connexin 43 expression. Nano Letters. 2011;11(9):3643–3648.
  • Shin SR, Jung SM, Zalabany M, et al. Carbon-nanotube-embedded hydrogel sheets for engineering cardiac constructs and bioactuators. ACS Nano. 2013;7(3):2369–2380.
  • Dvir T, Timko BP, Brigham MD, et al. Nanowired three-dimensional cardiac patches. Nat Nanotechnol. 2011;6(11):720–725.
  • Tian B, Liu J, Dvir T, et al. Macroporous nanowire nanoelectronic scaffolds for synthetic tissues. Nat Mater. 2012;11(11):986–994.
  • Mooney E, Mackle JN, Blond DJ, et al. The electrical stimulation of carbon nanotubes to provide a cardiomimetic cue to MSCs. Biomaterials. 2012;33(26):6132–6139.
  • Im AR, Kim JY, Kim HS, et al. Wound healing and antibacterial activities of chondroitin sulfate- and acharan sulfate-reduced silver nanoparticles. Nanotechnology. 2013;24(39):395102.
  • Zhang S, Liu X, Wang H, et al. Silver nanoparticle-coated suture effectively reduces inflammation and improves mechanical strength at intestinal anastomosis in mice. J Pediatr Surg. 2014;49(4):606–613.
  • Alarcon EI, Udekwu K, Skog M, et al. The biocompatibility and antibacterial properties of collagen-stabilized, photochemically prepared silver nanoparticles. Biomaterials. 2012;33(19):4947–4956.
  • Alarcon EI, Udekwu KI, Noel CW, et al. Safety and efficacy of composite collagen-silver nanoparticle hydrogels as tissue engineering scaffolds. Nanoscale. 2015;7(44):18789–18798.
  • Wen Y, Xu J, Ma X, et al. High-dose erythropoietin in acute ST-segment elevation myocardial infarction: a meta-analysis of randomized controlled trials. Am J Cardiovasc Drugs. 2013;13(6):435–442.
  • Prunier F, Biere L, Gilard M, et al. Single high-dose erythropoietin administration immediately after reperfusion in patients with ST-segment elevation myocardial infarction: results of the erythropoietin in myocardial infarction trial. Am Heart J. 2012;163(2):200–7.e1.
  • Erbs S, Beck EB, Linke A, et al. High-dose rosuvastatin in chronic heart failure promotes vasculogenesis, corrects endothelial function, and improves cardiac remodeling–results from a randomized, double-blind, and placebo-controlled study. Int J Cardiol. 2011;146(1):56–63.
  • Cangiano E, Marchesini J, Campo G, et al. ACE inhibition modulates endothelial apoptosis and renewal via endothelial progenitor cells in patients with acute coronary syndromes. Am J Cardiovasc Drugs. 2011;11(3):189–198.
  • Xiaozhen H, Yun Z, Mei Z, et al. Effect of carvedilol on coronary flow reserve in patients with hypertensive left-ventricular hypertrophy. Blood Press. 2010;19(1):40–47.
  • Kayaalti F, Kalay N, Basar E, et al. Effects of nebivolol therapy on endothelial functions in cardiac syndrome X. Heart Vessels. 2010;25(2):92–96.
  • Tripathi P, Chandra M, Misra MK. Protective role of l-Arginine against free-radical mediated oxidative damage in patients with unstable angina. Indian J Clin Biochem. 2010;25(3):302–306.
  • Taniguchi N, Nakamura T, Sawada T, et al. Erythropoietin prevention trial of coronary restenosis and cardiac remodeling after ST-elevated acute myocardial infarction (EPOC-AMI): a pilot, randomized, placebo-controlled study. Circ J. 2010;74(11):2365–2371.
  • Povsic TJ, Najjar SS, Prather K, et al. EPC mobilization after erythropoietin treatment in acute ST-elevation myocardial infarction: the REVEAL EPC substudy. J Thromb Thrombolysis. 2013;36(4):375–383.
  • Lister Z, Rayner KJ, Suuronen EJ. How biomaterials can influence various cell types in the repair and regeneration of the heart after myocardial infarction. Front Bioeng Biotechnol. 2016;4:62.
  • Blackburn NJ, Sofrenovic T, Kuraitis D, et al. Timing underpins the benefits associated with injectable collagen biomaterial therapy for the treatment of myocardial infarction. Biomaterials. 2015;39:182–192.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.