420
Views
2
CrossRef citations to date
0
Altmetric
Review Article

Functionalization of soft materials for cardiac repair and regeneration

, , , , &
Pages 451-468 | Received 29 Mar 2018, Accepted 22 Dec 2018, Published online: 01 Apr 2019

References

  • Gyongyosi M, Wojakowski W, Lemarchand P. 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.
  • 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.
  • Emmert MY, Hitchcock RW, Hoerstrup SP. Cell therapy, 3D culture systems and tissue engineering for cardiac regeneration. Adv Drug Deliv Rev. 2014;69–70:254–269.
  • 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;5:173ra25.
  • Ventrix I. A phase I, open-label study of the effects of percutaneous administration of an extracellular matrix hydrogel, VentriGel, following myocardial infarction. ClinicalTrialsgov Identifier: NCT02305602. 2014.
  • WHO. Global atlas on cardiovascular disease prevention and control. Geneva, Switzerland: World Health Organization. 2011.
  • WHO. Cardiovascular disease (CVDs)–fact sheet. Geneva, Switzerland: World Health Organization. 2017.
  • Yellon DM, Hausenloy DJ. Myocardial reperfusion injury. N Engl J Med. 2007;357:1121–1135.
  • Kuraitis D, Ruel M, Suuronen EJ. Mesenchymal stem cells for cardiovascular regeneration. Cardiovasc Drugs Ther. 2011;25:349–362.
  • Dobaczewski M, Gonzalez-Quesada C, Frangogiannis NG. The extracellular matrix as a modulator of the inflammatory and reparative response following myocardial infarction. J Mol Cell Cardiol. 2010;48:504–511.
  • Grilo GA, Shaver PR, de Castro Brás LE. Mechanisms of cardioprotection via modulation of the immune response. Curr Opin Pharmacol. 2017;33:6–11.
  • Liu SQ, Tefft BJ, Zhang D. Cardioprotective mechanisms activated in response to myocardial ischemia. Mol Cell Biomech. 2011;8:319–338.
  • Gnecchi M, Zhang Z, Ni A, et al. Paracrine mechanisms in adult stem cell signaling and therapy. Circ Res. 2008;103:1204–1219.
  • Suuronen EJ, Kuraitis D, Ruel M. Improving cell engraftment with tissue engineering. Semin Thorac Cardiovasc Surg. 2008;20:110–114.
  • 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.
  • 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.
  • van Berlo JH, Kanisicak O, Maillet M, et al. c-kit + cells minimally contribute cardiomyocytes to the heart. Nature. 2014;509:337–341.
  • Liu Q, Yang R, Huang X, et al. Genetic lineage tracing identifies in situ Kit-expressing cardiomyocytes. Cell Res. 2016;26:119–130.
  • Keith MC, Bolli R. "String theory" of c-kit(pos) cardiac cells: a new paradigm regarding the nature of these cells that may reconcile apparently discrepant results. Circ Res. 2015;116:1216–1230.
  • Amini H, Rezaie J, Vosoughi A, et al. Cardiac progenitor cells application in cardiovascular disease. J Cardiovasc Thorac Res. 2017;9:127–132.
  • van den Borne SW, Diez J, Blankesteijn WM, et al. Myocardial remodeling after infarction: the role of myofibroblasts. Nat Rev Cardiol. 2010;7:30.
  • van Amerongen MJ, Bou-Gharios G, Popa E, et al. Bone marrow-derived myofibroblasts contribute functionally to scar formation after myocardial infarction. J Pathol. 2008;214:377–386.
  • Frangogiannis NG. The extracellular matrix in myocardial injury, repair, and remodeling. J Clin Invest. 2017;127:1600–1612.
  • Apstein CS, Lorell BH. The physiological basis of left ventricular diastolic dysfunction. J Cardiac Surgery. 1988;3:475–485.
  • Beltrami AP, Urbanek K, Kajstura J, et al. Evidence that human cardiac myocytes divide after myocardial infarction. N Engl J Med. 2001;344:1750–1757.
  • Kajstura J, Gurusamy N, Ogorek B, et al. Myocyte turnover in the aging human heart. Circ Res. 2010;107:1374–1386.
  • Kajstura J, Urbanek K, Perl S, et al. Cardiomyogenesis in the adult human heart. Circ Res. 2010;107:305–315.
  • Lázár E, Sadek HA, Bergmann O. Cardiomyocyte renewal in the human heart: insights from the fall-out. Eur Heart J. 2017;38:2333–2342.
  • Ko HC, Milthorpe BK, McFarland CD. Engineering thick tissues - the vascularisation problem. Eur Cell Mater. 2007;14:1–18.
  • Grounds MD. Complexity of extracellular matrix and skeletal muscle regeneration. In: Schiaffino S, Patridge T, editors. Skeletal muscle repair and regeneration. Springer; 2008;269–301.
  • 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.
  • Kuraitis D, Suuronen EJ, Sellke FW, et al. The future of regenerating the myocardium. Curr Opin Cardiol. 2010;25:575–582.
  • Ruel M, Song J, Sellke FW. Protein-, gene-, and cell-based therapeutic angiogenesis for the treatment of myocardial ischemia. Mol Cell Biochem. 2004;264:119–131.
  • Patra C, Boccaccini AR, Engel FB. Vascularization for cardiac tissue engineering: the extracellular matrix. Thromb Haemost. 2015;113:532–547.
  • Freedman SB, Isner JM. Therapeutic angiogenesis for coronary artery disease. Ann Intern Med. 2002;136:54–71.
  • 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;33:428–443.
  • Bayomy AF, Bauer M, Qiu Y, et al. Regeneration in heart disease – is ECM the key? Life Sci. 2012;91:823–827.
  • Ruvinov E, Harel-Adar T, Cohen S. Bioengineering the infarcted heart by applying bio-inspired materials. J Cardiovasc Transl Res. 2011;4:559–574.
  • 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.
  • Frangogiannis NG. The immune system and cardiac repair. Pharmacol Res. 2008;58:88–111.
  • Zeyda M, Farmer D, Todoric J, et al. Human adipose tissue macrophages are of an anti-inflammatory phenotype but capable of excessive pro-inflammatory mediator production. Int J Obes. 2007;31:1420–1428.
  • Mantovani A, Sica A, Sozzani S, et al. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol. 2004;25:677–686.
  • Stanimirovic DB, Wong J, Shapiro A, et al. Increase in surface expression of ICAM-1, VCAM-1 and E-selectin in human cerebromicrovascular endothelial cells subjected to ischemia-like insults. Acta Neurochir Suppl. 1997;70:12–16.
  • Zheng Z, Yenari MA. Post-ischemic inflammation: molecular mechanisms and therapeutic implications. Neurol Res. 2004;26:884–892.
  • Entman ML, Michael L, Rossen RD, et al. Inflammation in the course of early myocardial ischemia. FASEB J. 1991;5:2529–2537.
  • Abbott JD, Huang Y, Liu D, et al. Stromal cell-derived factor-1alpha plays a critical role in stem cell recruitment to the heart after myocardial infarction but is not sufficient to induce homing in the absence of injury. Circulation. 2004;110:3300–3305.
  • Vandervelde S, van Luyn MJ, Tio RA, et al. Signaling factors in stem cell-mediated repair of infarcted myocardium. J Mol Cell Cardiol. 2005;39:363–376.
  • Petit I, Jin D, Rafii S. The SDF-1-CXCR4 signaling pathway: a molecular hub modulating neo-angiogenesis. Trends Immunol. 2007;28:299–307.
  • Detillieux KA, Sheikh F, Kardami E, et al. Biological activities of fibroblast growth factor-2 in the adult myocardium. Cardiovasc Res. 2003;57:8–19.
  • Cleutjens JP, Kandala JC, Guarda E, et al. Regulation of collagen degradation in the rat myocardium after infarction. J Mol Cell Cardiol. 1995;27:1281–1292.
  • Sutton MG, Sharpe N. Left ventricular remodeling after myocardial infarction: pathophysiology and therapy. Circulation. 2000;101:2981–2988.
  • Weber KT, Sun Y, Tyagi SC, et al. Collagen network of the myocardium: function, structural remodeling and regulatory mechanisms. J Mol Cell Cardiol. 1994;26:279–292.
  • Frangogiannis NG. Targeting the inflammatory response in healing myocardial infarcts. Curr Med Chem. 2006;13:1877–1893.
  • Engler AJ, Carag-Krieger C, Johnson CP, et al. Embryonic cardiomyocytes beat best on a matrix with heart-like elasticity: scar-like rigidity inhibits beating. J Cell Sci. 2008;121:3794–3802.
  • Mirsky I, Parmley WW. Assessment of passive elastic stiffness for isolated heart muscle and the intact heart. Circ Res. 1973;33:233–243.
  • Purcell BP, Lobb D, Charati MB, et al. Injectable and bioresponsive hydrogels for on-demand matrix metalloproteinase inhibition. Nature Mater. 2014;13:653–661.
  • Eckhouse SR, Purcell BP, McGarvey JR, et al. Local hydrogel release of recombinant TIMP-3 attenuates adverse left ventricular remodeling after experimental myocardial infarction. Sci Transl Med. 2014;6:223ra21.
  • Fan Z, Fu M, Xu Z, et al. Sustained release of a peptide-based matrix metalloproteinase-2 inhibitor to attenuate adverse cardiac remodeling and improve cardiac function following myocardial infarction. Biomacromolecules. 2017;18:2820–2829.
  • Barlow SC, Doviak H, Jacobs J, et al. Intracoronary delivery of recombinant TIMP-3 after myocardial infarction: effects on myocardial remodeling and function. Am J Physiol Heart Circ Physiol. 2017;313:H690–H699.
  • Berry MF, Engler AJ, Woo YJ, et al. Mesenchymal stem cell injection after myocardial infarction improves myocardial compliance. Am J Physiol Heart Circ Physiol. 2006;290:H2196–H2203.
  • Engler AJ, Sen S, Sweeney HL, et al. Matrix elasticity directs stem cell lineage specification. Cell. 2006;126:677–689.
  • Plotkin M, Vaibavi SR, Rufaihah AJ, et al. The effect of matrix stiffness of injectable hydrogels on the preservation of cardiac function after a heart attack. Biomaterials. 2014;35:1429–1438.
  • Ifkovits JL, Tous E, Minakawa M, et al. Injectable hydrogel properties influence infarct expansion and extent of postinfarction left ventricular remodeling in an ovine model. Proc Natl Acad Sci USA. 2010;107:11507–11512.
  • Rodell CB, Lee ME, Wang H, et al. Injectable shear-thinning hydrogels for minimally invasive delivery to infarcted myocardium to limit left ventricular remodeling. Circ Cardiovasc Interv. 2016;9:e004058.
  • Pinney JR, Du KT, Ayala P, et al. Discrete microstructural cues for the attenuation of fibrosis following myocardial infarction. Biomaterials. 2014;35:8820–8828.
  • 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.
  • Bastings MM, Koudstaal S, Kieltyka RE, et al. A fast pH-switchable and self-healing supramolecular hydrogel carrier for guided, local catheter injection in the infarcted myocardium. Adv Healthc Mater. 2014;3:70–78.
  • Kim K, Wagner WR. Non-invasive and non-destructive characterization of tissue engineered constructs using ultrasound imaging technologies: a review. Ann Biomed Eng. 2016;44:621–635.
  • Ahmadi A, Thorn SL, Alarcon EI, et al. PET imaging of a collagen matrix reveals its effective injection and targeted retention in a mouse model of myocardial infarction. Biomaterials. 2015;49:18–26.
  • Xu Y, Guan J. Biomaterial property-controlled stem cell fates for cardiac regeneration. Bioact Mater. 2016;1:18–28.
  • Zhu Y, Matsumura Y, Wagner WR. Ventricular wall biomaterial injection therapy after myocardial infarction: Advances in material design, mechanistic insight and early clinical experiences. Biomaterials. 2017;129:37–53.
  • Moorthi A, Tyan YC, Chung TW. Surface-modified polymers for cardiac tissue engineering. Biomater Sci. 2017;5:1976–1987.
  • Hubbell JA. Biomaterials in tissue engineering. Biotechnology (NY). 1995;13:565–576.
  • Seliktar D. Designing cell-compatible hydrogels for biomedical applications. Science. 2012;336:1124–1128.
  • Hoffman AS. Hydrogels for biomedical applications. Adv Drug Deliv Rev. 2002;54:3–12.
  • Yu T, Wang W, Nassiri S, et al. Temporal and spatial distribution of macrophage phenotype markers in the foreign body response to glutaraldehyde-crosslinked gelatin hydrogels. J Biomater Sci Polym Ed. 2016;27:721–742.
  • Dalgliesh AJ, Parvizi M, Lopera-Higuita M, et al. Graft-specific immune tolerance is determined by residual antigenicity of xenogeneic extracellular matrix scaffolds. Acta Biomater. 2018;79:253–264.
  • Young JL, Tuler J, Braden R, et al. In vivo response to dynamic hyaluronic acid hydrogels. Acta Biomater. 2013;9:7151–7157.
  • Adams DO. The granulomatous inflammatory response. a review. Am J Pathol. 1976;84:164–192.
  • Morais JM, Papadimitrakopoulos F, Burgess DJ. Biomaterials/tissue interactions: possible solutions to overcome foreign body response. AAPS J. 2010;12:188–196.
  • Weinberger F, Mannhardt I, Eschenhagen T. Engineering cardiac muscle tissue: a maturating field of research. Circ Res. 2017;120:1487–1500.
  • Morris AH, Stamer DK, Kyriakides TR. The host response to naturally-derived extracellular matrix biomaterials. Semin Immunol. 2017;29:72–91.
  • Londono R, Badylak SF. Biologic scaffolds for regenerative medicine: mechanisms of in vivo remodeling. Ann Biomed Eng. 2015;43:577–592.
  • Badylak SF, Gilbert TW. Immune response to biologic scaffold materials. Semin Immunol. 2008;20:109–116.
  • Brown BN, Valentin JE, Stewart-Akers AM, et al. Macrophage phenotype and remodeling outcomes in response to biologic scaffolds with and without a cellular component. Biomaterials. 2009;30:1482–1491.
  • Fishman JM, Lowdell MW, Urbani L, et al. Immunomodulatory effect of a decellularized skeletal muscle scaffold in a discordant xenotransplantation model. Proc Natl Acad Sci USA. 2013;110:14360–14365.
  • Wolf MT, Dearth CL, Ranallo CA, et al. Macrophage polarization in response to ECM coated polypropylene mesh. Biomaterials. 2014;35:6838–6849.
  • D'Amore A, Yoshizumi T, Luketich SK, et al. Bi-layered polyurethane – Extracellular matrix cardiac patch improves ischemic ventricular wall remodeling in a rat model. Biomaterials. 2016;107:1–14.
  • Hashizume R, Hong Y, Takanari K, et al. The effect of polymer degradation time on functional outcomes of temporary elastic patch support in ischemic cardiomyopathy. Biomaterials. 2013;34:7353–7363.
  • Wang Z, Ying Z, Bosy-Westphal A, et al. Specific metabolic rates of major organs and tissues across adulthood: evaluation by mechanistic model of resting energy expenditure. Am J Clin Nutr. 2010;92:1369–1377.
  • Shin H, Jo S, Mikos AG. Biomimetic materials for tissue engineering. Biomaterials. 2003;24:4353–4364.
  • Agrawal CM, Ray RB. Biodegradable polymeric scaffolds for musculoskeletal tissue engineering. J Biomed Mater Res. 2001;55:141–150.
  • Hernandez MJ, Christman KL. Designing acellular injectable biomaterial therapeutics for treating myocardial infarction and peripheral artery disease. JACC Basic Transl Sci. 2017;2:212–226.
  • Lindsey ML, Iyer RP, Zamilpa R, et al. A novel collagen matricryptin reduces left ventricular dilation post-myocardial infarction by promoting scar formation and angiogenesis. J Am Coll Cardiol. 2015;66:1364–1374.
  • Das D, Noh I. Overviews of biomimetic medical materials. Adv Exp Med Biol. 2018;1064:3–24.
  • Rasouli R, Barhoum A, Uludag H. A review of nanostructured surfaces and materials for dental implants: surface coating, patterning and functionalization for improved performance. Biomater Sci. 2018;6:1312–1338.
  • Tallawi M, Rosellini E, Barbani N, et al. Strategies for the chemical and biological functionalization of scaffolds for cardiac tissue engineering: a review. J R Soc Interface. 2015;12:20150254.
  • Sun H, Lu S, Jiang XX, et al. Carbon nanotubes enhance intercalated disc assembly in cardiac myocytes via the beta1-integrin-mediated signaling pathway. Biomaterials. 2015;55:84–95.
  • Ahmadi A, McNeill B, Vulesevic B, et al. The role of integrin alpha2 in cell and matrix therapy that improves perfusion, viability and function of infarcted myocardium. Biomaterials. 2014;35:4749–4758.
  • Shi C, Li Q, Zhao Y, et al. Stem-cell-capturing collagen scaffold promotes cardiac tissue regeneration. Biomaterials. 2011;32:2508–2515.
  • 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 hind limb ischemia model. FASEB J. 2009;23:1447–1458.
  • 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;29:1198–1207.
  • Lin Q, Ding X, Qiu F, et al. In situ endothelialization of intravascular stents coated with an anti-CD34 antibody functionalized heparin-collagen multilayer. Biomaterials. 2010;31:4017–4025.
  • Saik JE, Gould DJ, Keswani AH, et al. Biomimetic hydrogels with immobilized ephrinA1 for therapeutic angiogenesis. Biomacromolecules. 2011;12:2715–2722.
  • Moon JJ, Lee SH, West JL. Synthetic biomimetic hydrogels incorporated with ephrin-A1 for therapeutic angiogenesis. Biomacromolecules. 2007;8:42–49.
  • Nam HY, McGinn A, Kim PH, et al. Primary cardiomyocyte-targeted bioreducible polymer for efficient gene delivery to the myocardium. Biomaterials. 2010;31:8081–8087.
  • Keene AM, Balasubramanian R, Lloyd J, et al. Multivalent dendrimeric and monomeric adenosine agonists attenuate cell death in HL-1 mouse cardiomyocytes expressing the A(3) receptor. Biochem Pharmacol. 2010;80:188–196.
  • Chang MY, Yang YJ, Chang CH, et al. Functionalized nanoparticles provide early cardioprotection after acute myocardial infarction. J Control Release. 2013;170:287–294.
  • 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.
  • Purcell BP, Elser JA, Mu A, et al. Synergistic effects of SDF-1alpha chemokine and hyaluronic acid release from degradable hydrogels on directing bone marrow derived cell homing to the myocardium. Biomaterials. 2012;33:7849–7857.
  • Rajabi S, Jalili-Firoozinezhad S, Ashtiani MK, et al. Effect of chemical immobilization of SDF-1alpha into muscle-derived scaffolds on angiogenesis and muscle progenitor recruitment. J Tissue Eng Regen Med. 2018;12:e438–e450.
  • Simon-Yarza T, Tamayo E, Benavides C, et al. Functional benefits of PLGA particulates carrying VEGF and CoQ10 in an animal of myocardial ischemia. Int J Pharm. 2013;454:784–790.
  • Wang Y, Liu XC, Zhao J, et al. Degradable PLGA scaffolds with basic fibroblast growth factor: experimental studies in myocardial revascularization. Tex Heart Inst J. 2009;36:89–97.
  • Pascual-Gil S, Simon-Yarza T, Garbayo E, et al. Cytokine-loaded PLGA and PEG-PLGA microparticles showed similar heart regeneration in a rat myocardial infarction model. Int J Pharm. 2017;523:531–533.
  • Spadaccio C, Nappi F, De Marco F, et al. Implantation of a poly-L-lactide GCSF-functionalized scaffold in a model of chronic myocardial infarction. J Cardiovasc Trans Res. 2017;10:47–65.
  • Mewhort HE, Turnbull JD, Meijndert HC, et al. Epicardial infarct repair with basic fibroblast growth factor-enhanced CorMatrix-ECM biomaterial attenuates postischemic cardiac remodeling. J Thorac Cardiovasc Surg. 2014;147:1650–1659.
  • Sonnenberg SB, Rane AA, Liu CJ, et al. Delivery of an engineered HGF fragment in an extracellular matrix-derived hydrogel prevents negative LV remodeling post-myocardial infarction. Biomaterials. 2015;45:56–63.
  • Lee J, Cha MJ, Lim KS, et al. Injectable microsphere/hydrogel hybrid system containing heat shock protein as therapy in a murine myocardial infarction model. J Drug Target. 2013;21:822–829.
  • Rodness J, Mihic A, Miyagi Y, et al. VEGF-loaded microsphere patch for local protein delivery to the ischemic heart. Acta Biomater. 2016;45:169–181.
  • Zhu H, Jiang X, Li X, et al. Intramyocardial delivery of VEGF165 via a novel biodegradable hydrogel induces angiogenesis and improves cardiac function after rat myocardial infarction. Heart Vessels. 2016;31:963–975.
  • Steele AN, Cai L, Truong VN, et al. A novel protein-engineered hepatocyte growth factor analog released via a shear-thinning injectable hydrogel enhances post-infarction ventricular function. Biotechnol Bioeng. 2017;114:2379–2389.
  • Hong J, Ku SH, Lee MS, et al. Cardiac RNAi therapy using RAGE siRNA/deoxycholic acid-modified polyethylenimine complexes for myocardial infarction. Biomaterials. 2014;35:7562–7573.
  • Paul A, Hasan A, Kindi HA, et al. Injectable graphene oxide/hydrogel-based angiogenic gene delivery system for vasculogenesis and cardiac repair. ACS Nano. 2014;8:8050–8062.
  • Kim D, Ku SH, Kim H, et al. Simultaneous regulation of apoptotic gene silencing and angiogenic gene expression for myocardial infarction therapy: single-carrier delivery of SHP-1 siRNA and VEGF-expressing pDNA. J Control Release. 2016;243:182–194.
  • Wang LL, Liu Y, Chung JJ, et al. Local and sustained miRNA delivery from an injectable hydrogel promotes cardiomyocyte proliferation and functional regeneration after ischemic injury. Nat Biomed Eng. 2017;1:983–992.
  • Monaghan MG, Holeiter M, Brauchle E, et al. Exogenous miR-29B delivery through a hyaluronan-based injectable system yields functional maintenance of the infarcted myocardium. Tissue Eng Part A. 2018;24:57–67.
  • Projahn D, Simsekyilmaz S, Singh S, et al. Controlled intramyocardial release of engineered chemokines by biodegradable hydrogels as a treatment approach of myocardial infarction. J Cell Mol Med. 2014;18:790–800.
  • Ruvinov E, Leor J, Cohen S. The promotion of myocardial repair by the sequential delivery of IGF-1 and HGF from an injectable alginate biomaterial in a model of acute myocardial infarction. Biomaterials. 2011;32:565–578.
  • 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.
  • Cittadini A, Monti MG, Petrillo V, et al. Complementary therapeutic effects of dual delivery of insulin-like growth factor-1 and vascular endothelial growth factor by gelatin microspheres in experimental heart failure. Eur J Heart Fail. 2011;13:1264–1274.
  • Banquet S, Gomez E, Nicol L, et al. Arteriogenic therapy by intramyocardial sustained delivery of a novel growth factor combination prevents chronic heart failure. Circulation. 2011;124:1059–1069.
  • Zieris A, Chwalek K, Prokoph S, et al. Dual independent delivery of pro-angiogenic growth factors from starPEG-heparin hydrogels. J Control Release. 2011;156:28–36.
  • Zieris A, Prokoph S, Levental KR, et al. FGF-2 and VEGF functionalization of starPEG-heparin hydrogels to modulate biomolecular and physical cues of angiogenesis. Biomaterials. 2010;31:7985–7994.
  • Lakshmanan R, Kumaraswamy P, Krishnan UM, et al. Engineering a growth factor embedded nanofiber matrix niche to promote vascularization for functional cardiac regeneration. Biomaterials. 2016;97:176–195.
  • Quijada P, Salunga HT, Hariharan N, et al. Cardiac stem cell hybrids enhance myocardial repair. Circ Res. 2015;117:695–706.
  • Rufaihah AJ, Johari NA, Vaibavi SR, et al. Dual delivery of VEGF and ANG-1 in ischemic hearts using an injectable hydrogel. Acta Biomater. 2017;48:58–67.
  • Awada HK, Johnson NR, Wang Y. Sequential delivery of angiogenic growth factors improves revascularization and heart function after myocardial infarction. J Control Release. 2015;207:7–17.
  • 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.
  • Vu TD, Pal SN, Ti LK, et al. An autologous platelet-rich plasma hydrogel compound restores left ventricular structure, function and ameliorates adverse remodeling in a minimally invasive large animal myocardial restoration model: a translational approach: Vu and Pal "Myocardial repair: PRP, hydrogel and supplements". Biomaterials. 2015;45:27–35.
  • Zhang J, Ding L, Zhao Y, et al. Collagen-targeting vascular endothelial growth factor improves cardiac performance after myocardial infarction. Circulation. 2009;119:1776–1784.
  • Seif-Naraghi SB, Horn D, Schup-Magoffin PJ, et al. Injectable extracellular matrix derived hydrogel provides a platform for enhanced retention and delivery of a heparin-binding growth factor. Acta Biomater. 2012;8:3695–3703.
  • Schesny MK, Monaghan M, Bindermann AH, et al. Preserved bioactivity and tunable release of a SDF1-GPVI bi-specific protein using photo-crosslinked PEGda hydrogels. Biomaterials. 2014;35:7180–7187.
  • Lutolf MP, Gilbert PM, Blau HM. Designing materials to direct stem-cell fate. Nature. 2009;462:433–441.
  • Ruoslahti E, Pierschbacher MD. New perspectives in cell adhesion: RGD and integrins. Science. 1987;238:491–497.
  • Schussler O, Coirault C, Louis-Tisserand M, et al. Use of arginine-glycine-aspartic acid adhesion peptides coupled with a new collagen scaffold to engineer a myocardium-like tissue graft. Nat Rev Cardiol. 2009;6:240–249.
  • Shachar M, Tsur-Gang O, Dvir T, et al. The effect of immobilized RGD peptide in alginate scaffolds on cardiac tissue engineering. Acta Biomater. 2011;7:152–162.
  • Yu J, Gu Y, Du KT, et al. The effect of injected RGD modified alginate on angiogenesis and left ventricular function in a chronic rat infarct model. Biomaterials. 2009;30:751–756.
  • Sondermeijer H, Witkowski P, Seki T, et al. RGDfK-peptide modified alginate scaffold for cell transplantation and cardiac neovascularization. Tissue Eng Part A. 2018;24:740–751.
  • Boateng SY, Lateef SS, Mosley W, et al. RGD and YIGSR synthetic peptides facilitate cellular adhesion identical to that of laminin and fibronectin but alter the physiology of neonatal cardiac myocytes. Am J Physiol Cell Physiol. 2005;288:C30–C38.
  • Rask F, Dallabrida SM, Ismail NS, et al. Photocrosslinkable chitosan modified with angiopoietin-1 peptide, QHREDGS, promotes survival of neonatal rat heart cells. J Biomed Mater Res. 2010;95:105–117.
  • Miklas JW, Dallabrida SM, Reis LA, et al. QHREDGS enhances tube formation, metabolism and survival of endothelial cells in collagen-chitosan hydrogels. PLoS One. 2013;8:e72956.
  • Reis LA, Chiu LL, Wu J, et al. Hydrogels with integrin-binding angiopoietin-1-derived peptide, QHREDGS, for treatment of acute myocardial infarction. Circ Heart Fail. 2015;8:333–341.
  • Andukuri A, Sohn YD, 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.
  • Zachman AL, Crowder SW, Ortiz O, et al. Pro-angiogenic and anti-inflammatory regulation by functional peptides loaded in polymeric implants for soft tissue regeneration. Tissue Eng Part A. 2013;19:437–447.
  • Chiu LL, Reis LA, Momen A, et al. Controlled release of thymosin beta4 from injected collagen-chitosan hydrogels promotes angiogenesis and prevents tissue loss after myocardial infarction. Regen Med. 2012;7:523–533.
  • Shu Y, Hao T, Yao F, et al. RoY peptide-modified chitosan-based hydrogel to improve angiogenesis and cardiac repair under hypoxia. ACS Appl Mater Interfaces. 2015;7:6505–6517.
  • Deng C, Li F, Griffith M, et al. Application of chitosan-based biomaterials for blood vessel regeneration. Macromol Symp. 2010;297:138–146.
  • Li Y, Rodrigues J, Tomas H. Injectable and biodegradable hydrogels: gelation, biodegradation and biomedical applications. Chem Soc Rev. 2012;41:2193–2221.
  • Henning RJ, Khan A, Jimenez E. Chitosan hydrogels significantly limit left ventricular infarction and remodeling and preserve myocardial contractility. J Surg Res. 2016;201:490–497.
  • 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.
  • Chi NH, Yang MC, Chung TW, et al. Cardiac repair using chitosan-hyaluronan/silk fibroin patches in a rat heart model with myocardial infarction. Carbohydr Polym. 2013;92:591–597.
  • Francis MP, Breathwaite E, Bulysheva AA, et al. Human placenta hydrogel reduces scarring in a rat model of cardiac ischemia and enhances cardiomyocyte and stem cell cultures. Acta Biomater. 2017;52:92–104.
  • Lakshmanan R, Krishnan UM, Sethuraman S. Polymeric scaffold aided stem cell therapeutics for cardiac muscle repair and regeneration. Macromol Biosci. 2013;13:1119–1134.
  • Rane AA, Christman KL. Biomaterials for the treatment of myocardial infarction: a 5-year update. J Am Coll Cardiol. 2011;58:2615–2629.
  • Segers VF, Lee RT. Biomaterials to enhance stem cell function in the heart. Circ Res. 2011;109:910–922.
  • Discher DE, Mooney DJ, Zandstra PW. Growth factors, matrices, and forces combine and control stem cells. Science. 2009;324:1673–1677.
  • Shapira-Schweitzer K, Seliktar D. Matrix stiffness affects spontaneous contraction of cardiomyocytes cultured within a PEGylated fibrinogen biomaterial. Acta Biomater. 2007;3:33–41.
  • Young JL, Engler AJ. Hydrogels with time-dependent material properties enhance cardiomyocyte differentiation in vitro. Biomaterials. 2011;32:1002–1009.
  • Boothe SD, Myers JD, Pok S, et al. The effect of substrate stiffness on cardiomyocyte action potentials. Cell Biochem Biophys. 2016;74:527–535.
  • Chopra A, Lin V, McCollough A, et al. Reprogramming cardiomyocyte mechanosensing by crosstalk between integrins and hyaluronic acid receptors. J Biomech. 2012;45:824–831.
  • Zhang J, Wilson GF, Soerens AG, et al. Functional cardiomyocytes derived from human induced pluripotent stem cells. Circ Res. 2009;104:e30–e41.
  • Kehat I, Kenyagin-Karsenti D, Snir M, et al. Human embryonic stem cells can differentiate into myocytes with structural and functional properties of cardiomyocytes. J Clin Invest. 2001;108:407–414.
  • Moretti A, Bellin M, Welling A, et al. Patient-specific induced pluripotent stem-cell models for long-QT syndrome. N Engl J Med. 2010;363:1397–1409.
  • Nunes SS, Miklas JW, Liu J, et al. Biowire: a platform for maturation of human pluripotent stem cell-derived cardiomyocytes. Nat Methods. 2013;10:781–787.
  • Tandon N, Cannizzaro C, Chao PH, et al. Electrical stimulation systems for cardiac tissue engineering. Nat Protoc. 2009;4:155–173.
  • Schaaf S, Shibamiya A, Mewe M, et al. Human engineered heart tissue as a versatile tool in basic research and preclinical toxicology. PLoS One. 2011;6:e26397.
  • Chan YC, Ting S, Lee YK, et al. Electrical stimulation promotes maturation of cardiomyocytes derived from human embryonic stem cells. J Cardiovasc Trans Res. 2013;6:989–999.
  • Ma R, Liang J, Huang W, et al. Electrical stimulation enhances cardiac differentiation of human induced pluripotent stem cells for myocardial infarction therapy. Antioxid Redox Signal. 2017;28:371–384.
  • Hsiao CW, Bai MY, Chang Y, et al. Electrical coupling of isolated cardiomyocyte clusters grown on aligned conductive nanofibrous meshes for their synchronized beating. Biomaterials. 2013;34:1063–1072.
  • Dvir T, Timko BP, Brigham MD, et al. Nanowired three-dimensional cardiac patches. Nat Nanotechnol. 2011;6:720–725.
  • Mihic A, Cui Z, Wu J, et al. A conductive polymer hydrogel supports cell electrical signaling and improves cardiac function after implantation into myocardial infarct. Circulation. 2015;132:772–784.
  • Bao R, Tan B, Liang S, et al. A pi-pi conjugation-containing soft and conductive injectable polymer hydrogel highly efficiently rebuilds cardiac function after myocardial infarction. Biomaterials. 2017;122:63–71.
  • Menasche P, Vanneaux V, Hagege A, et al. Transplantation of human embryonic stem cell-derived cardiovascular progenitors for severe ischemic left ventricular dysfunction. J Am Coll Cardiol. 2018;71:429–438.
  • 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.
  • Frey N, Linke A, Suselbeck T, et al. Intracoronary delivery of injectable bioabsorbable scaffold (IK-5001) to treat left ventricular remodeling after ST-elevation myocardial infarction: a first-in-man study. Circ Cardiovasc Interv. 2014;7:806–812.
  • Liu CJ, Jones DS, 2nd, Tsai PC, et al. An engineered dimeric fragment of hepatocyte growth factor is a potent c-MET agonist. FEBS Lett. 2014;588:4831–4837.
  • Faulkner A. Law's performativities: shaping the emergence of regenerative medicine through European Union legislation. Soc Stud Sci. 2012;42:753–774.
  • Tobita M, Konomi K, Torashima Y, et al. Japan's challenges of translational regenerative medicine: Act on the safety of regenerative medicine. Regen Ther. 2016;4:78–81.
  • Witten CM, McFarland RD, Simek SL. Concise review: the U.S. Food and Drug Administration and regenerative medicine. Stem Cells Transl Med. 2015;4:1495–1499.
  • Perea-Gil I, Prat-Vidal C, Bayes-Genis A. In vivo experience with natural scaffolds for myocardial infarction: the times they are a-changin'. Stem Cell Res Ther. 2015;6:248.
  • Madonna R, Van Laake LW, Davidson SM, et al. Position paper of the European Society of Cardiology working group cellular biology of the heart: cell-based therapies for myocardial repair and regeneration in ischemic heart disease and heart failure. Eur Heart J. 2016;37:1789–1798.
  • Ruvinov E, Cohen S. Alginate biomaterial for the treatment of myocardial infarction: progress, translational strategies, and clinical outlook: from ocean algae to patient bedside. Adv Drug Deliv Rev. 2016;96:54–76.
  • 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.
  • Liu Z, Wang H, Wang Y, et al. The influence of chitosan hydrogel on stem cell engraftment, survival and homing in the ischemic myocardial microenvironment. Biomaterials. 2012;33:3093–3106.
  • Zhang G, Nakamura Y, Wang X, et al. Controlled release of stromal cell-derived factor-1 alpha in situ increases c-kit + cell homing to the infarcted heart. Tissue Eng. 2007;13:2063–2071.
  • Wang H, Zhang X, Li Y, et al. Improved myocardial performance in infarcted rat heart by co-injection of basic fibroblast growth factor with temperature-responsive chitosan hydrogel. J Heart Lung Transplant. 2010;29:881–887.
  • Ruvinov E, Leor J, Cohen S. The effects of controlled HGF delivery from an affinity-binding alginate biomaterial on angiogenesis and blood perfusion in a hindlimb ischemia model. Biomaterials. 2010;31:4573–4582.
  • Miyagi Y, Chiu LL, Cimini M, et al. Biodegradable collagen patch with covalently immobilized VEGF for myocardial repair. Biomaterials. 2011;32:1280–1290.
  • Formiga FR, Pelacho B, Garbayo E, et al. Sustained release of VEGF through PLGA microparticles improves vasculogenesis and tissue remodeling in an acute myocardial ischemia-reperfusion model. J Control Release. 2010;147:30–37.
  • Hao X, Silva EA, Mansson BA, et al. Angiogenic effects of sequential release of VEGF-A165 and PDGF-BB with alginate hydrogels after myocardial infarction. Cardiovasc Res. 2007;75:178–185.
  • Miyagi Y, Zeng F, Huang XP, et al. Surgical ventricular restoration with a cell- and cytokine-seeded biodegradable scaffold. Biomaterials. 2010;31:7684–7694.

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.