Biomaterial strategies to improve the efficacy of bone marrow cell therapy for myocardial infarction

References

• The 10 leading causes of death in the world, 2000 and 2012. World Health Organization; 2014. Available from http://www.who.int/mediacentre/factsheets/fs310/en
   Google Scholar
• Alpert JS, Thygesen K, Antman E, et al. Myocardial infarction redefined–a consensus document of The Joint European Society of Cardiology/American College of Cardiology Committee for the redefinition of myocardial infarction. J Am Coll Cardiol. 2000;36:959–969.
   PubMed Web of Science ®Google Scholar
• Nian M, Lee P, Khaper N, et al. Inflammatory cytokines and postmyocardial infarction remodeling. Circ Res. 2004;94:1543–1553. DOI:10.1161/01.RES.0000130526.20854.fa
   PubMed Web of Science ®Google Scholar
• Boudoulas KD, Hatzopoulos AK. Cardiac repair and regeneration: the Rubik’s cube of cell therapy for heart disease. Dis Model Mech. 2009;2:344–358. DOI:10.1242/dmm.000240
   PubMed Web of Science ®Google Scholar
• Kucia M, Dawn B, Hunt G, et al. Cells expressing early cardiac markers reside in the bone marrow and are mobilized into the peripheral blood after myocardial infarction. Circ Res. 2004;95:1191–1199. DOI:10.1161/01.RES.0000150856.47324.5b
   PubMed Web of Science ®Google Scholar
• Schächinger V, Aicher A, Döbert N, et al. Pilot trial on determinants of progenitor cell recruitment to the infarcted human myocardium. Circulation. 2008;118:1425–1432. DOI:10.1161/CIRCULATIONAHA.108.777102
   PubMed Web of Science ®Google Scholar
• Shi M, Li J, Liao L, et al. Regulation of CXCR4 expression in human mesenchymal stem cells by cytokine treatment: role in homing efficiency in NOD/SCID mice. Haematologica. 2007;92:897–904.
   PubMed Web of Science ®Google Scholar
• Hu X, Dai S, Wu W-J, et al. Stromal cell derived factor-1 alpha confers protection against myocardial ischemia/reperfusion injury: role of the cardiac stromal cell derived factor-1 alpha CXCR4 axis. Circulation. 2007;116:654–663. DOI:10.1161/CIRCULATIONAHA.106.672451
   PubMed Web of Science ®Google Scholar
• Cheng C, Li P, Wang Y-G, et al. Study on the expression of VEGF and HIF-1α in infarct area of rats with AMI. Eur Rev Med Pharmacol Sci. 2016;20:115–119.
   PubMed Web of Science ®Google Scholar
• Yoon Y-S, Wecker A, Heyd L, et al. Clonally expanded novel multipotent stem cells from human bone marrow regenerate myocardium after myocardial infarction. J Clin Invest. 2005;115:326–338. DOI:10.1172/JCI22326
   PubMed Web of Science ®Google Scholar
• Fazel S, Cimini M, Chen L, et al. Cardioprotective c-kit+ cells are from the bone marrow and regulate the myocardial balance of angiogenic cytokines. J Clin Invest. 2006;116:1865–1877. DOI:10.1172/JCI27019
   PubMed Web of Science ®Google Scholar
• Wojakowski W, Tendera M, Michałowska A, et al. Mobilization of CD34/CXCR4+, CD34/CD117+, c-met+ stem cells, and mononuclear cells expressing early cardiac, muscle, and endothelial markers into peripheral blood in patients with acute myocardial infarction. Circulation. 2004;110:3213–3220. DOI:10.1161/01.CIR.0000147609.39780.02
   PubMed Web of Science ®Google Scholar
• Wojakowski W, Landmesser U, Bachowski R, et al. Mobilization of stem and progenitor cells in cardiovascular diseases. Leukemia. 2012;26:23–33. DOI:10.1038/leu.2011.184
   PubMed Web of Science ®Google Scholar
• Schmidt-Lucke C, Rössig L, Fichtlscherer S, et al. Reduced number of circulating endothelial progenitor cells predicts future cardiovascular events: proof of concept for the clinical importance of endogenous vascular repair. Circulation. 2005;111:2981–2987. DOI:10.1161/CIRCULATIONAHA.104.504340
   PubMed Web of Science ®Google Scholar
• Fortunato O, Spinetti G, Specchia C, et al. Migratory activity of circulating progenitor cells and serum SDF-1α predict adverse events in patients with myocardial infarction. Cardiovasc Res. 2013;100:192–200. DOI:10.1093/cvr/cvt153
   PubMed Web of Science ®Google Scholar
• Chen Y-L, Tsai T-H, Wallace CG, et al. Intra-carotid arterial administration of autologous peripheral blood-derived endothelial progenitor cells improves acute ischemic stroke neurological outcomes in rats. Int J Cardiol. 2015;201:668–683. DOI:10.1016/j.ijcard.2015.03.137
   PubMed Web of Science ®Google Scholar
• Hung H-S, Yang Y-C, Lin Y-C, et al. Regulation of human endothelial progenitor cell maturation by polyurethane nanocomposites. Biomaterials. 2014;35:6810–6821. DOI:10.1016/j.biomaterials.2014.04.076
   PubMed Web of Science ®Google Scholar
• Zhang X, Yan X, Wang C, et al. The effect of autologous endothelial progenitor cell transplantation combined with extracorporeal shock-wave therapy on ischemic skin flaps in rats. Cytotherapy. 2014;16:1098–1109. DOI:10.1016/j.jcyt.2014.02.013
   PubMed Web of Science ®Google Scholar
• Chen X, Wang J, An Q, et al. Electrospun poly(l-lactic acid-co-ε-caprolactone) fibers loaded with heparin and vascular endothelial growth factor to improve blood compatibility and endothelial progenitor cell proliferation. Colloids Surf B Biointerfaces. 2015;128:106–114. DOI:10.1016/j.colsurfb.2015.02.023
   PubMed Web of Science ®Google Scholar
• González-Pecchi V, Valdés S, Pons V, et al. Apolipoprotein A-I enhances proliferation of human endothelial progenitor cells and promotes angiogenesis through the cell surface ATP synthase. Microvasc Res. 2015;98:9–15. DOI:10.1016/j.mvr.2014.11.003
   PubMed Web of Science ®Google Scholar
• Qi P, Yan W, Yang Y, et al. Immobilization of DNA aptamers via plasma polymerized allylamine film to construct an endothelial progenitor cell-capture surface. Colloids Surf B Biointerfaces. 2015;126:70–79. DOI:10.1016/j.colsurfb.2014.12.017
   PubMed Web of Science ®Google Scholar
• Li Q, Tang G, Xue S, et al. Silica-coated superparamagnetic iron oxide nanoparticles targeting of EPCs in ischemic brain injury. Biomaterials. 2013;34:4982–4992. DOI:10.1016/j.biomaterials.2013.03.030
   PubMed Web of Science ®Google Scholar
• Fadini GP, Losordo D, Dimmeler S. Critical reevaluation of endothelial progenitor cell phenotypes for therapeutic and diagnostic use. Circ Res. 2012;110:624–637. DOI:10.1161/CIRCRESAHA.111.243386
   PubMed Web of Science ®Google Scholar
• Orlic D, Kajstura J, Chimenti S, et al. Mobilized bone marrow cells repair the infarcted heart, improving function and survival. Proc Natl Acad Sci U S A. 2001;98:10344–10349. DOI:10.1073/pnas.181177898
   PubMed Web of Science ®Google Scholar
• Balsam L, Wagers A, Christensen J, et al. Haematopoietic stem cells adopt mature haematopoietic fates in ischaemic myocardium. Nature. 2004;428:668–673. DOI:10.1038/nature02460
   PubMed Web of Science ®Google Scholar
• Murry CE, Reinecke H, Pabon LM. Regeneration gaps: observations on stem cells and cardiac repair. J Am Coll Cardiol. 2006;47:1777–1785. DOI:10.1016/j.jacc.2006.02.002
   PubMed Web of Science ®Google Scholar
• Cho H-J, Lee N, Lee JY, et al. Role of host tissues for sustained humoral effects after endothelial progenitor cell transplantation into the ischemic heart. J Exp Med. 2007;204:3257–3269. DOI:10.1084/jem.20070166
   PubMed Web of Science ®Google Scholar
• Loffredo FS, Steinhauser ML, Gannon J, et al. Bone marrow-derived cell therapy stimulates endogenous cardiomyocyte progenitors and promotes cardiac repair. Cell Stem Cell. 2011;8:389–398. DOI:10.1016/j.stem.2011.02.002
   PubMed Web of Science ®Google Scholar
• Chimenti I, Smith RR, Li T-S, et al. Relative roles of direct regeneration versus paracrine effects of human cardiosphere-derived cells transplanted into infarcted mice. Circ Res. 2010;106:971–980. DOI:10.1161/CIRCRESAHA.109.210682
   PubMed Web of Science ®Google Scholar
• Cheng Y, Jiang S, Hu R, et al. Potential mechanism for endothelial progenitor cell therapy in acute myocardial infarction: activation of VEGF- PI3K/Akt-eNOS pathway. Ann Clin Lab Sci. 2013;43:395–401.
   PubMed Web of Science ®Google Scholar
• Lovell MJ, Yasin M, Lee KL, et al. Bone marrow mononuclear cells reduce myocardial reperfusion injury by activating the PI3K/Akt survival pathway. Atherosclerosis. 2010;213:67–76. DOI:10.1016/j.atherosclerosis.2010.07.045
   PubMed Web of Science ®Google Scholar
• Zhang S, Zhao L, Shen L, et al. Comparison of various niches for endothelial progenitor cell therapy on ischemic myocardial repair: coexistence of host collateralization and Akt-mediated angiogenesis produces a superior microenvironment. Arterioscler Thromb Vasc Biol. 2012;32:910–923. DOI:10.1161/ATVBAHA.111.244970
   PubMed Web of Science ®Google Scholar
• Lehtonen ST, Mäkelä J, Ohlmeier S, et al. Analysis of molecular changes after autologous cell therapy in swine myocardial infarction tissue can reveal novel targets for future therapy. J Tissue Eng Regen Med. 2014;8:97–105. DOI:10.1002/term.1502
   PubMed Web of Science ®Google Scholar
• Jansen Of Lorkeers SJ, Eding JEC, Vesterinen HM, et al. Similar effect of autologous and allogeneic cell therapy for ischemic heart disease: systematic review and meta-analysis of large animal studies. Circ Res. 2015;116:80–86. DOI:10.1161/CIRCRESAHA.116.304872
   PubMed Web of Science ®Google Scholar
• Giordano C, Kuraitis D, Beanlands RSB, et al. Cell-based vasculogenic studies in preclinical models of chronic myocardial ischaemia and hibernation. Expert Opin Biol Ther. 2013;13:411–428. DOI:10.1517/14712598.2013.748739
   PubMed Web of Science ®Google Scholar
• Hou L, Kim JJ, Woo YJ, et al. Stem cell-based therapies to promote angiogenesis in ischemic cardiovascular disease. Am J Physiol Heart Circ Physiol. 2016;310:H455–H465. DOI:10.1152/ajpheart.00726.2015
   PubMed Web of Science ®Google Scholar
• Jakob P, Landmesser U. Current status of cell-based therapy for heart failure. Curr Heart Fail Rep. 2013;10:165–176. DOI:10.1007/s11897-013-0134-z
   PubMedGoogle Scholar
• Sarto P, Balducci E, Balconi G, et al. Effects of exercise training on endothelial progenitor cells in patients with chronic heart failure. J Card Fail. 2007;13:701–708. DOI:10.1016/j.cardfail.2007.06.722
   PubMed Web of Science ®Google Scholar
• Eleuteri E, Mezzani A, Di SA, et al. Aerobic training and angiogenesis activation in patients with stable chronic heart failure: a preliminary report. Biomarkers. 2013;18:418–424. DOI:10.3109/1354750X.2013.805342
   PubMed Web of Science ®Google Scholar
• Turan RG, Brehm M, Kostering M, et al. Effects of exercise training on mobilization of BM-CPCs and migratory capacity as well as LVEF after AMI. Med Klin. 2006;101(Suppl 1):198–201.
   Google Scholar
• Vasa M, Fichtlscherer S, Adler K, et al. Increase in circulating endothelial progenitor cells by statin therapy in patients with stable coronary artery disease. Circulation. 2001;103:2885–2890.
   PubMed Web of Science ®Google Scholar
• Afzal MR, Samanta A, Shah ZI, et al. Adult bone marrow cell therapy for ischemic heart disease: evidence and insights from randomized controlled trials. Circ Res. 2015;117:558–575. DOI:10.1161/CIRCRESAHA.114.304792
   PubMed Web of Science ®Google Scholar
• Zhu K, Li J, Wang Y, et al. Intramyocardial autologous bone marrow-derived stem cells injection for ischemic heart disease ineligible for revascularization: a systematic review and meta-analysis. Arch Med Res. 2015;46:286–295. DOI:10.1016/j.arcmed.2015.06.001
   PubMed Web of Science ®Google Scholar
• Delewi R, Hirsch A, Tijssen JG, et al. Impact of intracoronary bone marrow cell therapy on left ventricular function in the setting of ST-segment elevation myocardial infarction: a collaborative meta-analysis. Eur Heart J. 2014;35:989–998. DOI:10.1093/eurheartj/eht372
   PubMed Web of Science ®Google Scholar
• Jeevanantham V, Butler M, Saad A, et al. Adult bone marrow cell therapy improves survival and induces long-term improvement in cardiac parameters: a systematic review and meta-analysis. Circulation. 2012;126:551–568. DOI:10.1161/CIRCULATIONAHA.111.086074
   PubMed Web of Science ®Google Scholar
• Gyöngyösi M, Wojakowski W, Lemarchand P, et al. Meta-analysis of cell-based CaRdiac stUdiEs (ACCRUE) in patients with acute myocardial infarction based on individual patient data. Circ Res. 2015;116:1346–1360. DOI:10.1161/CIRCRESAHA.116.304346
   PubMed Web of Science ®Google Scholar
• Fisher SA, Zhang H, Doree C, et al. Stem cell treatment for acute myocardial infarction. Cochrane Database Syst Rev. 2015;9:CD006536.
   PubMed Web of Science ®Google Scholar
• Nowbar AN, Mielewczik M, Karavassilis M, et al. Discrepancies in autologous bone marrow stem cell trials and enhancement of ejection fraction (DAMASCENE): weighted regression and meta-analysis. BMJ. 2014;348:g2688. DOI:10.1136/bmj.g2688
   PubMed Web of Science ®Google Scholar
• Pompilio G, Nigro P, Bassetti B, et al. Bone marrow cell therapy for ischemic heart disease: the never ending story. Circ Res. 2015;117:490–493. DOI:10.1161/CIRCRESAHA.115.307184
   PubMed Web of Science ®Google Scholar
• Kovacic JC, Fuster V. Cell therapy for patients with acute myocardial infarction: ACCRUEd evidence to date. Circ Res. 2015;116:1287–1290. DOI:10.1161/CIRCRESAHA.115.306323
   PubMed Web of Science ®Google Scholar
• Wollert KC. Bone marrow mononuclear cell therapy for acute myocardial infarction: we know what we want, but we just don’t know how yet. Heart. 2015;101:337–338. DOI:10.1136/heartjnl-2014-306787
   PubMed Web of Science ®Google Scholar
• Khan AR, Farid TA, Pathan A, et al. Impact of cell therapy on myocardial perfusion and cardiovascular outcomes in patients with angina refractory to medical therapy: a systematic review and meta-analysis. Circ Res. 2016;118:984–993. DOI:10.1161/CIRCRESAHA.115.308056
   PubMed Web of Science ®Google Scholar
• Ali-Hassan-Sayegh S, Mirhosseini SJ, Lotfaliani M-R, et al. Transplantation of bone marrow stem cells during cardiac surgery. Asian Cardiovasc Thorac Ann. 2014;23:363–374. DOI:10.1177/0218492314553251
   PubMedGoogle Scholar
• Liu B, Duan C, Luo C, et al. Impact of timing following acute myocardial infarction on efficacy and safety of bone marrow stem cells therapy: a network meta-analysis. Stem Cells Int. 2016;2016:1031794.
   PubMed Web of Science ®Google Scholar
• Aicher A, Brenner W, Zuhayra M, et al. Assessment of the tissue distribution of transplanted human endothelial progenitor cells by radioactive labeling. Circulation. 2003;107:2134–2139. DOI:10.1161/01.CIR.0000062649.63838.C9
   PubMed Web of Science ®Google Scholar
• Li S-H, Lai TYY, Sun Z, et al. Tracking cardiac engraftment and distribution of implanted bone marrow cells: comparing intra-aortic, intravenous, and intramyocardial delivery. J Thorac Cardiovasc Surg. 2009;137:1225–1233. DOI:10.1016/j.jtcvs.2008.11.001
   PubMed Web of Science ®Google Scholar
• Daldrup-Link HE, Rudelius M, Metz S, et al. Cell tracking with gadophrin-2: a bifunctional contrast agent for MR imaging, optical imaging, and fluorescence microscopy. Eur J Nucl Med Mol Imaging. 2004;31:1312–1321. DOI:10.1007/s00259-003-1378-8
   PubMed Web of Science ®Google Scholar
• Kang WJ, Kang HJ, Kim HS, et al. Tissue distribution of 18F-FDG-labeled peripheral hematopoietic stem cells after intracoronary administration in patients with myocardial infarction. J Nucl Med. 2006;47:1295–1301.
   PubMed Web of Science ®Google Scholar
• Karpov RS, Popov SV, Markov VA, et al. Autologous mononuclear bone marrow cells during reparative regeneratrion after acute myocardial infarction. Bull Exp Biol Med. 2005;140:640–643.
   PubMed Web of Science ®Google Scholar
• Vrtovec B, Poglajen G, Lezaic L, et al. Effects of intracoronary CD34+ stem cell transplantation in nonischemic dilated cardiomyopathy patients: 5-year follow-up. Circ Res. 2013;112:165–173. DOI:10.1161/CIRCRESAHA.112.276519
   PubMed Web of Science ®Google Scholar
• António N, Fernandes R, Soares A, et al. Reduced levels of circulating endothelial progenitor cells in acute myocardial infarction patients with diabetes or pre-diabetes: accompanying the glycemic continuum. Cardiovasc Diabetol. 2014;13:101. DOI:10.1186/1475-2840-13-80
   PubMed Web of Science ®Google Scholar
• Dimmeler S, Leri A. Aging and disease as modifiers of efficacy of cell therapy. Circ Res. 2008;102:1319–1330. DOI:10.1161/CIRCRESAHA.108.175943
   PubMed Web of Science ®Google Scholar
• Hill JM, Zalos G, Halcox JPJ, et al. Circulating endothelial progenitor cells, vascular function, and cardiovascular risk. N Engl J Med. 2003;348:593–600. DOI:10.1056/NEJMoa022287
   PubMed Web of Science ®Google Scholar
• Heeschen C, Lehmann R, Honold J, et al. Profoundly reduced neovascularization capacity of bone marrow mononuclear cells derived from patients with chronic ischemic heart disease. Circulation. 2004;109:1615–1622. DOI:10.1161/01.CIR.0000124476.32871.E3
   PubMed Web of Science ®Google Scholar
• Kim K-A, Shin Y-J, Akram M, et al. High glucose condition induces autophagy in endothelial progenitor cells contributing to angiogenic impairment. Biol Pharm Bull. 2014;37:1248–1252.
   PubMed Web of Science ®Google Scholar
• Assmus B, Leistner DM, Schächinger V, et al. Long-term clinical outcome after intracoronary application of bone marrow-derived mononuclear cells for acute myocardial infarction: migratory capacity of administered cells determines event-free survival. Eur Heart J. 2014;35:1275–1283. DOI:10.1093/eurheartj/ehu062
   PubMed Web of Science ®Google Scholar
• Lou J, Povsic TJ, Allen JD, et al. The effect of aspirin on endothelial progenitor cell biology: preliminary investigation of novel properties. Thromb Res. 2010;126:e175–e179. DOI:10.1016/j.thromres.2009.11.017
   PubMed Web of Science ®Google Scholar
• Stiles J, Amaya C, Pham R, et al. Propranolol treatment of infantile hemangioma endothelial cells: a molecular analysis. Exp Ther Med. 2012;4:594–604. DOI:10.3892/etm.2012.654
   PubMed Web of Science ®Google Scholar
• Simari R, Pepine C, Traverse J, et al. Bone marrow mononuclear cell therapy for acute myocardial infarction: a perspective from the CCTRN. Circ Res. 2014;114:1564–1568. DOI:10.1161/CIRCRESAHA.114.303720
   PubMed Web of Science ®Google Scholar
• Wollert KC, Drexler H. Cell therapy for the treatment of coronary heart disease: a critical appraisal. Nat Rev Cardiol. 2010;7:204–215. DOI:10.1038/nrcardio.2010.1
   PubMed Web of Science ®Google Scholar
• Strauer B-E, Steinhoff G. 10 years of intracoronary and intramyocardial bone marrow stem cell therapy of the heart: from the methodological origin to clinical practice. J Am Coll Cardiol. 2011;58:1095–1104. DOI:10.1016/j.jacc.2011.06.016
   PubMed Web of Science ®Google Scholar
• Cima LG, Vacanti JP, Vacanti C, et al. Tissue engineering by cell transplantation using degradable polymer substrates. J Biomech Eng. 1991;113:143–151.
   PubMed Web of Science ®Google Scholar
• Kim I-Y, Seo S-J, Moon H-S, et al. Chitosan and its derivatives for tissue engineering applications. Biotechnol Adv. 2008;26:1–21. DOI:10.1016/j.biotechadv.2007.07.009
   PubMed Web of Science ®Google Scholar
• Brown A, Barker T. Fibrin-based biomaterials: modulation of macroscopic properties through rational design at the molecular level. Acta Biomater. 2011;72:181–204.
   Google Scholar
• Okada M, Payne TR, Oshima H, et al. Differential efficacy of gels derived from small intestinal submucosa as an injectable biomaterial for myocardial infarct repair. Biomaterials. 2010;31:7678–7683. DOI:10.1016/j.biomaterials.2010.06.056
   PubMed Web of Science ®Google Scholar
• Blackburn NJR, 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. DOI:10.1016/j.biomaterials.2014.11.004
   PubMed Web of Science ®Google Scholar
• Serpooshan V, Zhao M, Metzler SA, et al. The effect of bioengineered acellular collagen patch on cardiac remodeling and ventricular function post myocardial infarction. Biomaterials. 2013;34:9048–9055. DOI:10.1016/j.biomaterials.2013.08.017
   PubMed Web of Science ®Google Scholar
• Tabuchi M, Negishi J, Yamashita A, et al. Effect of decellularized tissue powders on a rat model of acute myocardial infarction. Mater Sci Eng C. 2015;56:494–500. DOI:10.1016/j.msec.2015.07.010
   PubMed Web of Science ®Google Scholar
• Leor J, Amsalem Y, Cohen S. Cells, scaffolds, and molecules for myocardial tissue engineering. Pharmacol Ther. 2005;105:151–163. DOI:10.1016/j.pharmthera.2004.10.003
   PubMed Web of Science ®Google Scholar
• Ahmadi A, McNeill B, Vulesevic B, et al. The role of integrin α2 in cell and matrix therapy that improves perfusion, viability and function of infarcted myocardium. Biomaterials. 2014;35:4749–4758. DOI:10.1016/j.biomaterials.2014.02.028
   PubMed Web of Science ®Google Scholar
• Lalit PA, Hei DJ, Raval AN, et al. Induced pluripotent stem cells for post-myocardial infarction repair: remarkable opportunities and challenges. Circ Res. 2014;114:1328–1345. DOI:10.1161/CIRCRESAHA.114.300556
   PubMed Web of Science ®Google Scholar
• Xiang Z, Liao R, Kelly MS, et al. Collagen-GAG scaffolds grafted onto myocardial infarcts in a rat model: a delivery vehicle for mesenchymal stem cells. Tissue Eng. 2006;12:2467–2478. DOI:10.1089/ten.2006.12.2467
   PubMedGoogle Scholar
• Pozzobon M, Bollini S, Iop L, et al. Human bone marrow-derived CD133+ cells delivered to a collagen patch on cryoinjured rat heart promote angiogenesis and arteriogenesis. Cell Transplant. 2010;19:1247–1260. DOI:10.3727/096368910X505864
   PubMed Web of Science ®Google Scholar
• Chan BP, Hui TY, Yeung CW, et al. Self-assembled collagen-human mesenchymal stem cell microspheres for regenerative medicine. Biomaterials. 2007;28:4652–4666. DOI:10.1016/j.biomaterials.2007.07.041
   PubMed Web of Science ®Google Scholar
• Dai W, Hale SL, Kay GL, et al. Delivering stem cells to the heart in a collagen matrix reduces relocation of cells to other organs as assessed by nanoparticle technology. Cardiovasc Med. 2010;4:387–395.
   Google Scholar
• Liu J, Hu Q, Wang Z, et al. Autologous stem cell transplantation for myocardial repair. Am J Physiol Heart Circ Physiol. 2004;287:H501–H511. DOI:10.1152/ajpheart.00049.2004
   Web of Science ®Google Scholar
• Gaffey AC, Chen MH, Venkataraman CM, et al. Injectable shear-thinning hydrogels used to deliver endothelial progenitor cells, enhance cell engraftment, and improve ischemic myocardium. J Thorac Cardiovasc Surg. 2015;150:1268–1276. DOI:10.1016/j.jtcvs.2015.07.035
   PubMed Web of Science ®Google Scholar
• Chen C-H, Wang -S-S, Wei EI, et al. Hyaluronan enhances bone marrow cell therapy for myocardial repair after infarction. Mol Ther. 2013;21:670–679. DOI:10.1038/mt.2012.268
   PubMed Web of Science ®Google Scholar
• Chen C-H, Chang M-Y, Wang -S-S, et al. Injection of autologous bone marrow cells in hyaluronan hydrogel improves cardiac performance after infarction in pigs. Am J Physiol Heart Circ Physiol. 2014;306:H1078–H1086. DOI:10.1152/ajpheart.00481.2013
   Google Scholar
• Shevach M, Zax R, Abrahamov A, et al. Omentum ECM-based hydrogel as a platform for cardiac cell delivery. Biomed Mater. 2015;10:034106. DOI:10.1088/1748-6041/10/1/015022
   PubMedGoogle Scholar
• Ungerleider JL, Johnson TD, Rao N, et al. Fabrication and characterization of injectable hydrogels derived from decellularized skeletal and cardiac muscle. Methods. 2015;84:53–59. DOI:10.1016/j.ymeth.2015.03.024
   PubMed Web of Science ®Google Scholar
• 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;23:1447–1458. DOI:10.1096/fj.08-111054
   PubMed Web of Science ®Google Scholar
• Thitiwuthikiat P, Ii M, Saito T, et al. A vascular patch prepared from Thai silk fibroin and gelatin hydrogel incorporating simvastatin-micelles to recruit endothelial progenitor cells. Tissue Eng Part A. 2015;21:1309–1319. DOI:10.1089/ten.TEA.2014.0237
   PubMed Web of Science ®Google Scholar
• Chi N-H, Yang M-C, Chung T-W, et al. Cardiac repair achieved by bone marrow mesenchymal stem cells/silk fibroin/hyaluronic acid patches in a rat of myocardial infarction model. Biomaterials. 2012;33:5541–5551. DOI:10.1016/j.biomaterials.2012.04.030
   PubMed Web of Science ®Google Scholar
• Zhang S, Zhang F, Feng B, et al. Hematopoietic stem cell capture and directional differentiation into vascular endothelial cells for metal stent-coated chitosan/hyaluronic acid loading CD133 antibody. Tissue Eng Part A. 2015;21:1173–1183. DOI:10.1089/ten.TEA.2014.0352
   PubMed Web of Science ®Google Scholar
• Kai D, Wang Q-L, Wang H-J, et al. Stem cell-loaded nanofibrous patch promotes the regeneration of infarcted myocardium with functional improvement in rat model. Acta Biomater. 2014;10:2727–2738. DOI:10.1016/j.actbio.2014.02.030
   PubMed Web of Science ®Google Scholar
• Ravichandran R, Venugopal JR, Mukherjee S, et al. Elastomeric core/shell nanofibrous cardiac patch as a biomimetic support for infarcted porcine myocardium. Tissue Eng Part A. 2015;21:1288–1298. DOI:10.1089/ten.TEA.2014.0265
   PubMed Web of Science ®Google Scholar
• Lee YS, Lim KS, Oh J-E, et al. Development of porous PLGA/PEI1.8k biodegradable microspheres for the delivery of mesenchymal stem cells (MSCs). J Control Release. 2015;205:128–133. DOI:10.1016/j.jconrel.2015.01.004
   PubMed Web of Science ®Google Scholar
• Wall ST, Yeh -C-C, Tu RYK, et al. Biomimetic matrices for myocardial stabilization and stem cell transplantation. J Biomed Mater Res Part A. 2010;95A:1055–1066. DOI:10.1002/jbm.a.v95a:4
   Web of Science ®Google Scholar
• Xia Y, Zhu K, Lai H, et al. Enhanced infarct myocardium repair mediated by thermosensitive copolymer hydrogel-based stem cell transplantation. Exp Biol Med. 2015;240:593–600. DOI:10.1177/1535370214560957
   Web of Science ®Google Scholar
• Xu G, Wang X, Deng C, et al. Injectable biodegradable hybrid hydrogels based on thiolated collagen and oligo(acryloyl carbonate)-poly(ethylene glycol)-oligo(acryloyl carbonate) copolymer for functional cardiac regeneration. Acta Biomater. 2015;15:55–64. DOI:10.1016/j.actbio.2014.12.016
   PubMed Web of Science ®Google Scholar
• Doroudian G, Pinney J, Ayala P, et al. Sustained delivery of MGF peptide from microrods attracts stem cells and reduces apoptosis of myocytes. Biomed Microdevices. 2014;16:705–715. DOI:10.1007/s10544-014-9875-z
   PubMed Web of Science ®Google Scholar
• Lin Y-D, Yeh M-L, Yang Y-J, et al. Intramyocardial peptide nanofiber injection improves postinfarction ventricular remodeling and efficacy of bone marrow cell therapy in pigs. Circulation. 2010;122(11_suppl_1):S132–S141. DOI:10.1161/CIRCULATIONAHA.110.939512
   Google Scholar
• Tongers J, Webber MJ, Vaughan EE, et al. Enhanced potency of cell-based therapy for ischemic tissue repair using an injectable bioactive epitope presenting nanofiber support matrix. J Mol Cell Cardiol. 2014;74:231–239. DOI:10.1016/j.yjmcc.2014.05.017
   PubMed Web of Science ®Google Scholar
• Seeto WJ, Tian Y, Lipke EA. Peptide-grafted poly(ethylene glycol) hydrogels support dynamic adhesion of endothelial progenitor cells. Acta Biomater. 2013;9:8279–8289. DOI:10.1016/j.actbio.2013.05.023
   PubMed Web of Science ®Google Scholar
• Webber MJ, Tongers J, Renault M-A, et al. Reprint of: development of bioactive peptide amphiphiles for therapeutic cell delivery. Acta Biomater. 2015;23:S42–S51. DOI:10.1016/j.actbio.2015.07.018
   Google Scholar
• Felice F, Zambito Y, Belardinelli E, et al. Delivery of natural polyphenols by polymeric nanoparticles improves the resistance of endothelial progenitor cells to oxidative stress. Eur J Pharm Sci. 2013;50:393–399. DOI:10.1016/j.ejps.2013.08.008
   PubMed Web of Science ®Google Scholar
• Wang T, Wu D-Q, Jiang X-J, et al. Novel thermosensitive hydrogel injection inhibits post-infarct ventricle remodelling. Eur J Heart Fail. 2009;11:14–19. DOI:10.1093/eurjhf/hfn009
   PubMed Web of Science ®Google Scholar
• Fujimoto KL, Ma Z, Nelson DM, et al. Synthesis, characterization and therapeutic efficacy of a biodegradable, thermoresponsive hydrogel designed for application in chronic infarcted myocardium. Biomaterials. 2009;30:4357–4368. DOI:10.1016/j.biomaterials.2009.04.055
   PubMed Web of Science ®Google Scholar
• Li X-Y, Wang T, Jiang X-J, et al. Injectable hydrogel helps bone marrow-derived mononuclear cells restore infarcted myocardium. Cardiology. 2010;115:194–199. DOI:10.1159/000281840
   PubMed Web of Science ®Google Scholar
• Atluri P, Miller JS, Emery RJ, et al. Tissue-engineered, hydrogel-based endothelial progenitor cell therapy robustly revascularizes ischemic myocardium and preserves ventricular function. J Thorac Cardiovasc Surg. 2014;148:1090–1098. DOI:10.1016/j.jtcvs.2014.06.038
   PubMed Web of Science ®Google Scholar
• Roche ET, Hastings CL, Lewin SA, et al. Comparison of biomaterial delivery vehicles for improving acute retention of stem cells in the infarcted heart. Biomaterials. 2014;35:6850–6858. DOI:10.1016/j.biomaterials.2014.04.114
   PubMed Web of Science ®Google Scholar
• Ceccaldi C, Bushkalova R, Alfarano C, et al. Evaluation of polyelectrolyte complex-based scaffolds for mesenchymal stem cell therapy in cardiac ischemia treatment. Acta Biomater. 2014;10:901–911. DOI:10.1016/j.actbio.2013.10.027
   PubMed Web of Science ®Google Scholar
• Deng C, Zhang P, Vulesevic B, et al. A collagen-chitosan hydrogel for endothelial differentiation and angiogenesis. Tissue Eng Part A. 2010;16:3099–3109. DOI:10.1089/ten.tea.2009.0504
   PubMed Web of Science ®Google Scholar
• Yuan Y, Altalhi WA, Ng JJ, et al. Derivation of human peripheral blood derived endothelial progenitor cells and the role of osteopontin surface modification and eNOS transfection. Biomaterials. 2013;34:7292–7301. DOI:10.1016/j.biomaterials.2013.06.003
   PubMed Web of Science ®Google Scholar
• McNeill B, Vulesevic B, Ostojic A, et al. Collagen matrix-induced expression of integrin αVβ3 in circulating angiogenic cells can be targeted by matricellular protein CCN1 to enhance their function. FASEB J. 2015;29:1198–1207. DOI:10.1096/fj.14-261586
   PubMed Web of Science ®Google Scholar
• Chen H, Li X, Zhao Y, et al. Construction of a multifunctional coating consisting of phospholipids and endothelial progenitor cell-specific peptides on titanium substrates. Appl Surf Sci. 2015;347:169–177. DOI:10.1016/j.apsusc.2015.02.032
   Web of Science ®Google Scholar
• Prokoph S, Chavakis E, Levental KR, et al. Sustained delivery of SDF-1α from heparin-based hydrogels to attract circulating pro-angiogenic cells. Biomaterials. 2012;33:4792–4800. DOI:10.1016/j.biomaterials.2012.03.039
   PubMed Web of Science ®Google Scholar
• Kuraitis D, Zhang P, Zhang Y, et al. A stromal cell-derived factor-1 releasing matrix enhances the progenitor cell response and blood vessel growth in ischaemic skeletal muscle. Eur Cell Mater. 2011;22:109–123.
   PubMed Web of Science ®Google Scholar
• Song M, Jang H, Lee J, et al. Regeneration of chronic myocardial infarction by injectable hydrogels containing stem cell homing factor SDF-1 and angiogenic peptide Ac-SDKP. Biomaterials. 2014;35:2436–2445. DOI:10.1016/j.biomaterials.2013.12.011
   PubMed Web of Science ®Google Scholar
• Macarthur JW, Purcell BP, Shudo Y, et al. Sustained release of engineered stromal cell-derived factor 1-α from injectable hydrogels effectively recruits endothelial progenitor cells and preserves ventricular function after myocardial infarction. Circulation. 2013;128(11suppl 1):S79–S86. DOI:10.1161/CIRCULATIONAHA.112.000343
   Google Scholar
• Salimath AS, Phelps EA, Boopathy AV, et al. Dual delivery of hepatocyte and vascular endothelial growth factors via a protease-degradable hydrogel improves cardiac function in rats. PLoS One. 2012;7:e50980. DOI:10.1371/journal.pone.0050980
   PubMed Web of Science ®Google Scholar
• Rufaihah AJ, Seliktar D. Hydrogels for therapeutic cardiovascular angiogenesis. Adv Drug Deliv Rev. 2016;96:31–39. DOI:10.1016/j.addr.2015.07.003
   PubMed Web of Science ®Google Scholar
• Chen F-M, Wu L-A, Zhang M, et al. Homing of endogenous stem/progenitor cells for in situ tissue regeneration: promises, strategies, and translational perspectives. Biomaterials. 2011;32:3189–3209. DOI:10.1016/j.biomaterials.2010.12.032
   PubMed Web of Science ®Google Scholar
• Segers VFM, Lee RT. Biomaterials to enhance stem cell function in the heart. Circ Res. 2011;109:910–922. DOI:10.1161/CIRCRESAHA.111.249052
   PubMed Web of Science ®Google Scholar
• Sepantafar M, Maheronnaghsh R, Mohammadi H, et al. Stem cells and injectable hydrogels: synergistic therapeutics in myocardial repair. Biotechnol Adv. 2016;34:362–379. DOI:10.1016/j.biotechadv.2016.03.003
   PubMed Web of Science ®Google Scholar
• Wang X, Liu T, Chen Y, et al. Extracellular matrix inspired surface functionalization with heparin, fibronectin and VEGF provides an anticoagulant and endothelialization supporting microenvironment. Appl Surf Sci. 2014;320:871–882. DOI:10.1016/j.apsusc.2014.09.004
   Web of Science ®Google Scholar
• Miyagi Y, Chiu LLY, Cimini M, et al. Biodegradable collagen patch with covalently immobilized VEGF for myocardial repair. Biomaterials. 2011;32:1280–1290. DOI:10.1016/j.biomaterials.2010.10.007
   PubMed Web of Science ®Google Scholar
• Tardif K, Cloutier I, Miao Z, et al. A phosphorylcholine-modified chitosan polymer as an endothelial progenitor cell supporting matrix. Biomaterials. 2011;32:5046–5055. DOI:10.1016/j.biomaterials.2011.04.002
   PubMed Web of Science ®Google Scholar
• Kuraitis D, Hou C, Zhang Y, et al. Ex vivo generation of a highly potent population of circulating angiogenic cells using a collagen matrix. J Mol Cell Cardiol. 2011;51:187–197. DOI:10.1016/j.yjmcc.2011.04.011
   PubMed Web of Science ®Google Scholar
• Gnecchi M, Zhang Z, Ni A, et al. Paracrine mechanisms in adult stem cell signaling and therapy. Circ Res. 2008;103:1204–1219. DOI:10.1161/CIRCRESAHA.108.176826
   PubMed Web of Science ®Google Scholar
• Yang J, Ii M, Kamei N, et al. CD34+ cells represent highly functional endothelial progenitor cells in murine bone marrow. PLoS One. 2011;6:e20219. DOI:10.1371/journal.pone.0020219
   PubMed Web of Science ®Google Scholar
• Pozzoli O, Vella P, Iaffaldano G, et al. Endothelial fate and angiogenic properties of human CD34+ progenitor cells in zebrafish. Arterioscler Thromb Vasc Biol. 2011;31:1589–1597. DOI:10.1161/ATVBAHA.111.226969
   PubMed Web of Science ®Google Scholar
• Fuchs S, Motta A, Migliaresi C, et al. Outgrowth endothelial cells isolated and expanded from human peripheral blood progenitor cells as a potential source of autologous cells for endothelialization of silk fibroin biomaterials. Biomaterials. 2006;27:5399–5408. DOI:10.1016/j.biomaterials.2006.06.015
   PubMed Web of Science ®Google Scholar
• Suuronen EJ, Veinot JP, Wong S, et al. Tissue-engineered injectable collagen-based matrices for improved cell delivery and vascularization of ischemic tissue using CD133+ progenitors expanded from the peripheral blood. Circulation. 2006;114:138–145. DOI:10.1161/CIRCULATIONAHA.105.001081
   PubMed Web of Science ®Google Scholar
• Toeg HD, Tiwari-Pandey R, Seymour R, et al. Injectable small intestine submucosal extracellular matrix in an acute myocardial infarction model. Ann Thorac Surg. 2013;96:1686–1694. DOI:10.1016/j.athoracsur.2013.06.063
   PubMed Web of Science ®Google Scholar
• Lin X, Robinson M, Petrie T, et al. Small intestinal submucosa-derived extracellular matrix bioscaffold significantly enhances angiogenic factor secretion from human mesenchymal stromal cells. Stem Cell Res Ther. 2015;6:164. DOI:10.1186/s13287-015-0114-1
   PubMed Web of Science ®Google Scholar
• Mosala Nezhad Z, Poncelet A, de Kerchove L, et al. Small intestinal submucosa extracellular matrix (CorMatrix®) in cardiovascular surgery: a systematic review. Interact Cardiovasc Thorac Surg. 2016;22:839–850. DOI:10.1093/icvts/ivw020
   PubMed Web of Science ®Google Scholar
• Chang CW, Petrie T, Clark A, et al. Mesenchymal stem cell seeding of porcine small intestinal submucosal extracellular matrix for cardiovascular applications. PLoS One. 2016;11:e0153412. DOI:10.1371/journal.pone.0153412
   PubMed Web of Science ®Google Scholar
• 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;6:982–991. DOI:10.1161/CIRCIMAGING.113.000185
   PubMed Web of Science ®Google Scholar
• Zhang S, Sun A, Ma H, et al. Infarcted myocardium-like stiffness contributes to endothelial progenitor lineage commitment of bone marrow mononuclear cells. J Cell Mol Med. 2011;15:2245–2261. DOI:10.1111/j.1582-4934.2010.01217.x
   PubMed Web of Science ®Google Scholar
• Carenza E, Barceló V, Morancho A, et al. In vitro angiogenic performance and in vivo brain targeting of magnetized endothelial progenitor cells for neurorepair therapies. Nanomedicine. 2014;10:225–234. DOI:10.1016/j.nano.2013.06.005
   PubMed Web of Science ®Google Scholar
• Frederick J, Fitzpatrick R, McCormick R, et al. Stromal cell-derived factor-1α activation of tissue engineered endothelial progenitor cell matrix enhances ventricular function after myocardial infarction by inducing neovasculogenesis. Circulation. 2010;141:520–529.
   Google Scholar
• Andukuri A, Sohn Y, Anakwenze CP, et al. Enhanced human endothelial progenitor cell adhesion and differentiation by a bioinspired multifunctional nanomatrix. Tissue Eng Part C. 2013;19:375–385. DOI:10.1089/ten.tec.2012.0312
   PubMed Web of Science ®Google Scholar
• Schüssler-Lenz M, Beuneu C, Menezes-Ferreira M, et al. Cell-based therapies for cardiac repair: a meeting report on scientific observations and European regulatory viewpoints. Eur J Heart Fail. 2016;18:133–141. DOI:10.1002/ejhf.422
   PubMed Web of Science ®Google Scholar
• Farouz Y, Cossé M, Renault N, et al. Safety, regulatory, and ethical issues of human studies. In: Suuronen EJ, Ruel M, editors. Biomaterials for cardiac regeneration. New York (NY): Springer; 2015.
   Google Scholar
• Tarabah F. Good manufacturing practice (GMP) for biomaterials and medical devices in the EU and the USA. In: Amato S, Ezzell B, editors. Regulatory affairs for biomaterials and medical devices. New York (NY): Woodhead Publishing; 2015.
   Google Scholar
• Rao SV, Zeymer U, Douglas PS, et al. Bioabsorbable intracoronary matrix for prevention of ventricular remodeling after myocardial infarction. J Am Coll Cardiol. 2016;68:715–723. DOI:10.1016/j.jacc.2016.05.053
   PubMed Web of Science ®Google Scholar
• Mann DL, Lee RJ, Coats AJS, et al. One-year follow-up results from AUGMENT-HF: a multicentre randomized controlled clinical trial of the efficacy of left ventricular augmentation with Algisyl in the treatment of heart failure. Eur J Heart Fail. 2016;18:314–325. DOI:10.1002/ejhf.449
   PubMed Web of Science ®Google Scholar
• Chachques JC, Trainini JC, Lago N, et al. Myocardial assistance by grafting a new bioartificial upgraded myocardium (MAGNUM trial): clinical feasibility study. Ann Thorac Surg. 2008;85:901–908. DOI:10.1016/j.athoracsur.2007.10.052
   PubMed Web of Science ®Google Scholar
• Chachques JC, Trainini JC, Lago N, et al. Myocardial assistance by grafting a new bioartificial upgraded myocardium (MAGNUM clinical trial): one year follow-up. Cell Transplant. 2007;16:927–934. DOI:10.3727/096368907783338217
   PubMed Web of Science ®Google Scholar
• Ungerleider JL, Christman KL. Concise review: injectable biomaterials for the treatment of myocardial infarction and peripheral artery disease: translational challenges and progress. Stem Cells Transl Med. 2014;3:1090–1099. DOI:10.5966/sctm.2014-0049
   PubMed Web of Science ®Google Scholar