Abstract
The explosion of stem cell research in the past several years has made its presence known in the field of cardiology and has been recently tasked with solving one of the largest health problems to afflict humanity: cardiovascular disease (CVD). Although stem cell therapy has shown glimmers of promise, significant problems remain that need to be addressed if these therapies are to ever find true success. One way to achieve this success is to take engineering principles and apply them to fabricate engineered cardiac tissues, composed of the aforementioned therapeutic stem cells and biomaterials to bolster the tissue’s reparative capacity. In this review, the authors examine advancements in cardiac cell therapy and biomaterial research and discuss how their combination has been used to create tissue-engineered patches capable of restoring function to the damaged or failing myocardium.
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Abbreviations
- BMMNCs:
-
bone marrow-derived mononuclear cells
- CDC:
-
cardiosphere-derived cell
- CM:
-
cardiomyocyte
- CSC:
-
cardiac stem cell
- CTE:
-
cardiac tissue engineering
- CVD:
-
cardiovascular disease
- EC:
-
endothelial cell
- ECM:
-
extracellular matrix
- EHT:
-
engineered heart tissue
- ESC:
-
embryonic stem cell
- HF:
-
heart failure
- HSF1:
-
heat shock factor 1
- iPSC:
-
induced pluripotent stem cell
- Isl-1:
-
Islet-1
- LV:
-
left ventricle
- MI:
-
myocardial infarction
- miRNA:
-
micro-RNA
- MSC:
-
mesenchymal stem cells
- PCL:
-
polycaprolactone
- PGS:
-
poly(glycerol serbate)
- PLGA:
-
poly(lactic-co-glycolic) acid
- PLLA:
-
poly-(L-lactic) acid
- Sca1:
-
stem cell antigen-1
- SIS:
-
small intestinal submucosa
- SkMBs:
-
skeletal myoblasts
- SMC:
-
smooth muscle cell
References
Abraham MR, Henrikson CA, Tung L (2005) Antiarrhythmic engineering of skeletal myoblasts for cardiac transplantation. Circ Res 97:159–167. https://doi.org/10.1161/01.RES.0000174794.22491.a0
Agarwal U, Smith AW, French KM, Boopathy AV, George A, Trac D, Brown ME, Shen M, Jiang R, Fernandez JD, Kogon BE, Kanter KR, Alsoufi B, Wagner MB, Platt MO, Davis ME (2016) Age-dependent effect of pediatric cardiac progenitor cells after juvenile heart failure: age-dependent pediatric CPC therapy. Stem Cells Transl Med 5:883–892. https://doi.org/10.5966/sctm.2015-0241
Agarwal U, George A, Bhutani S, Ghosh-Choudhary S, Maxwell JT, Brown ME, Mehta Y, Platt MO, Liang Y, Sahoo S, Davis ME (2017) Experimental, systems, and computational approaches to understanding the MicroRNA-mediated reparative potential of cardiac progenitor cell–derived exosomes from pediatric PatientsNovelty and significance. Circ Res 120:701–712. https://doi.org/10.1161/CIRCRESAHA.116.309935
Anker SD, Coats AJS, Cristian G, Dragomir D, Pusineri E, Piredda M, Bettari L, Dowling R, Volterrani M, Kirwan B-A, Filippatos G, Mas J-L, Danchin N, Solomon SD, Lee RJ, Ahmann F, Hinson A, Sabbah HN, Mann DL (2015) A prospective comparison of alginate-hydrogel with standard medical therapy to determine impact on functional capacity and clinical outcomes in patients with advanced heart failure (AUGMENT-HF trial). Eur Heart J 36:2297–2309. https://doi.org/10.1093/eurheartj/ehv259
Antanavičiūtė I, Ereminienė E, Vysockas V, Račkauskas M, Skipskis V, Rysevaitė K, Treinys R, Benetis R, Jurevičius J, Skeberdis VA (2015) Exogenous connexin43-expressing autologous skeletal myoblasts ameliorate mechanical function and electrical activity of the rabbit heart after experimental infarction. Int J Exp Pathol 96:42–53. https://doi.org/10.1111/iep.12109
Assmus B, Honold J, Schächinger V, Britten MB, Fischer-Rasokat U, Lehmann R, Teupe C, Pistorius K, Martin H, Abolmaali ND, Tonn T, Dimmeler S, Zeiher AM (2006) Transcoronary transplantation of progenitor cells after myocardial infarction. N Engl J Med 355:1222–1232. https://doi.org/10.1056/NEJMoa051779
Avolio E, Meloni M, Spencer HL, Riu F, Katare R, Mangialardi G, Oikawa A, Rodriguez-Arabaolaza I, Dang Z, Mitchell K, Reni C, Alvino VV, Rowlinson J, Livi U, Cesselli D, Angelini G, Emanueli C, Beltrami AP, Madeddu P (2015) Combined Intramyocardial delivery of human Pericytes and cardiac stem cells additively improves the healing of mouse infarcted hearts through stimulation of vascular and muscular repair. Circ Res 116:e81–e94. https://doi.org/10.1161/CIRCRESAHA.115.306146
Badrossamay MR, McIlwee HA, Goss JA, Parker KK (2010) Nanofiber assembly by rotary Jet-Spinning. Nano Lett 10:2257–2261. https://doi.org/10.1021/nl101355x
Banerjee MN, Bolli R, Hare JM (2018) Clinical studies of cell therapy in cardiovascular medicine: recent developments and future directions. Circ Res 123:266–287.https://doi.org/10.1161/CIRCRESAHA.118.311217
Beauchamp P, Moritz W, Kelm JM, Ullrich ND, Agarkova I, Anson BD, Suter TM, Zuppinger C (2015) Development and characterization of a scaffold-free 3D spheroid model of induced pluripotent stem cell-derived human cardiomyocytes. Tissue Eng Part C Methods 21:852–861. https://doi.org/10.1089/ten.tec.2014.0376
Bejleri D, Streeter BW, Nachlas ALY, Brown ME, Gaetani R, Christman KL, Davis ME (2018) A bioprinted cardiac patch composed of cardiac-specific extracellular matrix and progenitor cells for heart repair. Adv Healthc Mater:1800672. https://doi.org/10.1002/adhm.201800672
Bellamy V, Vanneaux V, Bel A, Nemetalla H, Emmanuelle Boitard S, Farouz Y, Joanne P, Perier M-C, Robidel E, Mandet C, Hagège A, Bruneval P, Larghero J, Agbulut O, Menasché P (2014) Long-term functional benefits of human embryonic stem cell-derived cardiac progenitors embedded into a fibrin scaffold. J Heart Lung Transplant 34:1198–1207. https://doi.org/10.1016/j.healun.2014.10.008
Beltrami AP, Barlucchi L, Torella D, Baker M, Limana F, Chimenti S, Kasahara H, Rota M, Musso E, Urbanek K, Leri A, Kajstura J, Nadal-Ginard B, Anversa P (2003) Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell 114:763–776. https://doi.org/10.1016/S0092-8674(03)00687-1
Benjamin EJ, Virani SS, Callaway CW, Chamberlain AM, Chang AR, Cheng S, Chiuve SE, Cushman M, Delling FN, Deo R, de Ferranti SD, Ferguson JF, Fornage M, Gillespie C, Isasi CR, Jiménez MC, Jordan LC, Judd SE, Lackland D, Lichtman JH, Lisabeth L, Liu S, Longenecker CT, Lutsey PL, Mackey JS, Matchar DB, Matsushita K, Mussolino ME, Nasir K, O’Flaherty M, Palaniappan LP, Pandey A, Pandey DK, Reeves MJ, Ritchey MD, Rodriguez CJ, Roth GA, Rosamond WD, Sampson UKA, Satou GM, Shah SH, Spartano NL, Tirschwell DL, Tsao CW, Voeks JH, Willey JZ, Wilkins JT, Wu JH, Alger HM, Wong SS, Muntner P (2018) Heart disease and stroke statistics—2018 update: a report from the American Heart Association. Circulation 137:E67–E492. https://doi.org/10.1161/CIR.0000000000000558
Bergmann O, Bhardwaj RD, Bernard S, Zdunek S, Barnabé-Heider F, Walsh S, Zupicich J, Alkass K, Buchholz BA, Druid H, Jovinge S, Frisén J (2009) Evidence for cardiomyocyte renewal in humans. Science 324:98–102. https://doi.org/10.1126/science.1164680
Bergmann O, Zdunek S, Felker A, Salehpour M, Alkass K, Bernard S, Sjostrom SL, Szewczykowska M, Jackowska T, dos Remedios C, Malm T, Andrä M, Jashari R, Nyengaard JR, Possnert G, Jovinge S, Druid H, Frisén J (2015) Dynamics of cell generation and turnover in the human heart. Cell 161:1566–1575. https://doi.org/10.1016/j.cell.2015.05.026
Best C, Onwuka E, Pepper V, Sams M, Breuer J, Breuer C (2016) Cardiovascular tissue engineering: preclinical validation to bedside application. Physiology 31:7–15. https://doi.org/10.1152/physiol.00018.2015
Blumenthal B, Golsong P, Poppe A, Heilmann C, Schlensak C, Beyersdorf F, Siepe M (2010) Polyurethane scaffolds seeded with genetically engineered skeletal myoblasts: a promising tool to regenerate myocardial function. Artif Organs 34:E46–E54. https://doi.org/10.1111/j.1525-1594.2009.00937.x
Bolli R, Chugh AR, D’Amario D, Loughran JH, Stoddard MF, Ikram S, Beache GM, Wagner SG, Leri A, Hosoda T, Elmore JB, Goihberg P, Cappetta D, Solankhi NK, Fahsah I, Rokosh DG, Slaughter MS, Kajstura J, Anversa P (2011) Effect of cardiac stem cells in patients with ischemic cardiomyopathy: initial results of the SCIPIO trial. Lancet 378:1847–1857. https://doi.org/10.1016/S0140-6736(11)61590-0
Bolli R, Hare JM, March KL, Pepine CJ, Willerson JT, Perin EC, Yang PC, Henry TD, Traverse JH, Mitrani RD, Khan A, Hernandez-Schulman I, Taylor DA, Difede DL, Lima JAC, Chugh A, Loughran J, Vojvodic RW, Sayre SL, Bettencourt J, Cohen M, Moyé L, Ebert RF, Simari RD (2018) Rationale and design of the CONCERT-HF trial (combination of mesenchymal and c-kit + cardiac stem cells as regenerative therapy for heart failure). Circ Res 122:1703–1715. https://doi.org/10.1161/CIRCRESAHA.118.312978
Boopathy AV, Che PL, Somasuntharam I, Fiore VF, Cabigas EB, Ban K, Brown ME, Narui Y, Barker TH, Yoon YS, Salaita K, Garcia AJ, Davis ME (2014) The modulation of cardiac progenitor cell function by hydrogel-dependent Notch1 activation. Biomaterials 35:8103–8112. https://doi.org/10.1016/j.biomaterials.2014.05.082
Caspi O, Lesman A, Basevitch Y, Gepstein A, Arbel G, Habib IHM, Gepstein L, Levenberg S (2007) Tissue engineering of vascularized cardiac muscle from human embryonic stem cells. Circ Res 100:263–272. https://doi.org/10.1161/01.RES.0000257776.05673.ff
Chachques JC, Trainini JC, Lago N, Masoli OH, Barisani JL, Cortes-Morichetti M, Schussler O, Carpentier A (2007) Myocardial assistance by grafting a new bioartificial upgraded myocardium (MAGNUM clinical trial): one year follow-up. Cell Transplant 16:927–934. https://doi.org/10.3727/096368907783338217
Chachques JC, Trainini JC, Lago N, Cortes-Morichetti M, Schussler O, Carpentier A (2008) Myocardial assistance by grafting a new bioartificial upgraded myocardium (MAGNUM trial): clinical feasibility study. Ann Thorac Surg 85:901–908. https://doi.org/10.1016/j.athoracsur.2007.10.052
Chavakis E, Koyanagi M, Dimmeler S (2010) Enhancing the outcome of cell therapy for cardiac repair: progress from bench to bedside and back. Circulation 121:325–335. https://doi.org/10.1161/CIRCULATIONAHA.109.901405
Chen Q-Z, Bismarck A, Hansen U, Junaid S, Tran MQ, Harding SE, Ali NN, Boccaccini AR (2008) Characterisation of a soft elastomer poly(glycerol sebacate) designed to match the mechanical properties of myocardial tissue. Biomaterials 29:47–57. https://doi.org/10.1016/j.biomaterials.2007.09.010
Chen Q-Z, Ishii H, Thouas GA, Lyon AR, Wright JS, Blaker JJ, Chrzanowski W, Boccaccini AR, Ali NN, Knowles JC, Harding SE (2010) An elastomeric patch derived from poly(glycerol sebacate) for delivery of embryonic stem cells to the heart. Biomaterials 31:3885–3893. https://doi.org/10.1016/j.biomaterials.2010.01.108
Chong JJH, Yang X, Don CW, Minami E, Liu Y-W, Weyers JJ, Mahoney WM, Biber BV, Cook SM, Palpant NJ, Gantz JA, Fugate JA, Muskheli V, Gough GM, Vogel KW, Astley CA, Hotchkiss CE, Baldessari A, Pabon L, Reinecke H, Gill EA, Nelson V, Kiem H-P, Laflamme MA, Murry CE (2014) Human embryonic-stem-cell-derived cardiomyocytes regenerate non-human primate hearts. Nature 510:273–277. https://doi.org/10.1038/nature13233
Chugh AR, Beache G, Loughran JH, Mewton N, Elmore JB, Kajstura J, Pappas P, Tatooles A, Stoddard MF, Lima JAC, Slaughter MS, Anversa P, Bolli R (2012) Administration of Cardiac Stem Cells in patients with ischemic cardiomyopathy (the SCIPIO trial): surgical aspects and interim analysis of myocardial function and viability by magnetic resonance. Circulation 126:S54–S64. https://doi.org/10.1161/CIRCULATIONAHA.112.092627
Chung H-J, Kim J-T, Kim H-J, Kyung H-W, Katila P, Lee J-H, Yang T-H, Yang Y-I, Lee S-J (2015) Epicardial delivery of VEGF and cardiac stem cells guided by 3-dimensional PLLA mat enhancing cardiac regeneration and angiogenesis in acute myocardial infarction. J Control Release 205:218–230. https://doi.org/10.1016/j.jconrel.2015.02.013
Crupi A, Costa A, Tarnok A, Melzer S, Teodori L (2015) Inflammation in tissue engineering: the Janus between engraftment and rejection. Eur J Immunol 45:3222–3236. https://doi.org/10.1002/eji.201545818
Dai W, Gerczuk P, Zhang Y, Smith L, Kopyov O, Kay GL, Jyrala AJ, Kloner RA (2013) Intramyocardial injection of heart tissue-derived extracellular matrix improves Postinfarction cardiac function in rats. J Cardiovasc Pharmacol Ther 18:270–279. https://doi.org/10.1177/1074248412472257
Dimmeler S, Burchfield J, Zeiher AM (2007) Cell-based therapy of myocardial infarction. Arterioscler Thromb Vasc Biol 28:208–216. https://doi.org/10.1161/ATVBAHA.107.155317
Dominici M, Le BK, Müller I, Slaper-Cortenbach ICM, Marini FC, Krause DS, Deans RJ, Keating A, Prockop D, Horwitz EH (2006) Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8:315–317
Ellison GM, Vicinanza C, Smith AJ, Aquila I, Leone A, Waring CD, Henning BJ, Stirparo GG, Papait R, Scarfò M, Agosti V, Viglietto G, Condorelli G, Indolfi C, Ottolenghi S, Torella D, Nadal-Ginard B (2013) Adult c-kitpos cardiac stem cells are necessary and sufficient for functional cardiac regeneration and repair. Cell 154:827–842. https://doi.org/10.1016/j.cell.2013.07.039
Eschenhagen T, Fink C, Remmers U, Scholz H, Wattchow J, Weil J, Zimmermann W, Dohmen HH, Schäfer H, Bishopric N, Wakatsuki T, Elson EL (1997) Three-dimensional reconstitution of embryonic cardiomyocytes in a collagen matrix: a new heart muscle model system. FASEB J 11:683–694
Eschenhagen T, Bolli R, Braun T, Field LJ, Fleischmann BK, Frisén J, Giacca M, Hare JM, Houser S, Lee RT, Marbán E, Martin JF, Molkentin JD, Murry CE, Riley PR, Ruiz-Lozano P, Sadek HA, Sussman MA, Hill JA (2017) Cardiomyocyte regeneration: a consensus statement. Circulation 136:680–686. https://doi.org/10.1161/CIRCULATIONAHA.117.029343
Evans MJ, Kaufman MH (1981) Establishment in culture of pluripotential cells from mouse embryos. Nature 292:154–156. https://doi.org/10.1038/292154a0
Fedak P (2017) Epicardial infarct repair using CorMatrix®-ECM: clinical feasibility study. https://clinicaltrials.gov/ct2/show/NCT02887768. Accessed 27 Aug 2018
Fischer KM, Cottage CT, Wu W, Din S, Gude NA, Avitabile D, Quijada P, Collins BL, Fransioli J, Sussman MA (2009) Enhancement of myocardial regeneration through genetic engineering of cardiac progenitor cells expressing Pim-1 kinase. Circulation 120:2077–2087. https://doi.org/10.1161/CIRCULATIONAHA.109.884403
Fischer-Rasokat U, Assmus B, Seeger FH, Honold J, Leistner D, Fichtlscherer S, Schachinger V, Tonn T, Martin H, Dimmeler S, Zeiher AM (2009) A pilot trial to assess potential effects of selective intracoronary bone marrow-derived progenitor cell infusion in patients with nonischemic dilated cardiomyopathy: final 1-year results of the transplantation of progenitor cells and functional regeneration enhancement pilot trial in patients with nonischemic dilated cardiomyopathy. Circ Heart Fail 2:417–423. https://doi.org/10.1161/CIRCHEARTFAILURE.109.855023
Fleischer S, Shevach M, Feiner R, Dvir T (2014) Coiled fiber scaffolds embedded with gold nanoparticles improve the performance of engineered cardiac tissues. Nanoscale 6:9410–9414. https://doi.org/10.1039/C4NR00300D
Fleischer S, Miller J, Hurowitz H, Shapira A, Dvir T (2015) Effect of fiber diameter on the assembly of functional 3D cardiac patches. Nanotechnology 26:291002. https://doi.org/10.1088/0957-4484/26/29/291002
Földes G, Mioulane M, Wright JS, Liu AQ, Novak P, Merkely B, Gorelik J, Schneider MD, Ali NN, Harding SE (2011) Modulation of human embryonic stem cell-derived cardiomyocyte growth: a testbed for studying human cardiac hypertrophy? J Mol Cell Cardiol 50:367–376. https://doi.org/10.1016/j.yjmcc.2010.10.029
Fong AH, Romero-López M, Heylman CM, Keating M, Tran D, Sobrino A, Tran AQ, Pham HH, Fimbres C, Gershon PD, Botvinick EL, George SC, Hughes CCW (2016) Three-dimensional adult cardiac extracellular matrix promotes maturation of human induced pluripotent stem cell-derived cardiomyocytes. Tissue Eng Part A 22:1016–1025. https://doi.org/10.1089/ten.tea.2016.0027
French KM, Maxwell JT, Bhutani S, Ghosh-Choudhary S, Fierro MJ, Johnson TD, Christman KL, Taylor WR, Davis ME (2016) Fibronectin and cyclic strain improve cardiac progenitor cell regenerative potential In Vitro. Stem Cells Int 2016:1–11. https://doi.org/10.1155/2016/8364382
Frey N, Linke A, Suselbeck T, Muller-Ehmsen J, Vermeersch P, Schoors D, Rosenberg M, Bea F, Tuvia S, Leor J (2014) 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 7:806–812. https://doi.org/10.1161/CIRCINTERVENTIONS.114.001478
Gao L, Kupfer ME, Jung JP, Yang L, Zhang P, Da Sie Y, Tran Q, Ajeti V, Freeman BT, Fast VG, Campagnola PJ, Ogle BM, Zhang J (2017) Myocardial tissue engineering with cells derived from human-induced pluripotent stem cells and a native-like, high-resolution, 3-dimensionally printed scaffold. Circ Res 120:1318–1325. https://doi.org/10.1161/CIRCRESAHA.116.310277
Gao L, Gregorich ZR, Zhu W, Mattapally S, Oduk Y, Lou X, Kannappan R, Borovjagin AV, Walcott GP, Pollard AE, Fast VG, Hu X, Lloyd SG, Ge Y, Zhang J (2018) Large cardiac muscle patches engineered from human induced-pluripotent stem cell–derived cardiac cells improve recovery from myocardial infarction in swine. Circulation 137:1712–1730. https://doi.org/10.1161/CIRCULATIONAHA.117.030785
Garikipati VNS, Shoja-Taheri F, Davis ME, Kishore R (2018) Extracellular vesicles and the application of system biology and computational modeling in cardiac repair. Circ Res 123:188–204. https://doi.org/10.1161/CIRCRESAHA.117.311215
Goldstein BA, Thomas L, Zaroff JG, Nguyen J, Menza R, Khush KK (2016) Assessment of heart transplant waitlist time and pre- and post-transplant failure: a mixed methods approach. Epidimiology Camb Mass 27:469–476. https://doi.org/10.1097/EDE.0000000000000472
Golpanian S, Wolf A, Hatzistergos KE, Hare JM (2016) Rebuilding the damaged heart: mesenchymal stem cells, cell-based therapy, and engineered heart tissue. Physiol Rev 96:1127–1168. https://doi.org/10.1152/physrev.00019.2015
Gray WD, French KM, Ghosh-Choudhary S, Maxwell JT, Brown ME, Platt MO, Searles CD, Davis ME (2015) Identification of therapeutic covariant MicroRNA clusters in hypoxia-treated cardiac progenitor cell exosomes using systems biology. Circ Res 116:255–263. https://doi.org/10.1161/CIRCRESAHA.116.304360
Gude NA, Firouzi F, Broughton KM, Ilves K, Nguyen KP, Payne CR, Sacchi V, Monsanto MM, Casillas AR, Khalafalla FG, Wang BJ, Ebeid D, Alvarez R, Dembitsky WP, Bailey BA, Van Berlo JH, Sussman MA (2018) Cardiac c-kit biology revealed by inducible Transgenesis. Circ Res 123(1):57–72. https://doi.org/10.1161/CIRCRESAHA.117.311828
Gwak S-J, Bhang SH, Kim I-K, Kim S-S, Cho S-W, Jeon O, Yoo KJ, Putnam AJ, Kim B-S (2008) The effect of cyclic strain on embryonic stem cell-derived cardiomyocytes. Biomaterials 29:844–856. https://doi.org/10.1016/j.biomaterials.2007.10.050
Hare JM, Fishman JE, Gerstenblith G, Velazquez DLD, Zambrano JP, Suncion VY, Tracy M, Ghersin E, Johnston PV, Brinker JA, Breton E, Davis-Sproul J, Byrnes J, George R, Lardo A, Schulman IH, Mendizabal AM, Lowery MH, Rouy D, Altman P, Foo CWP, Ruiz P, Amador A, Silva JD, McNiece IK, Heldman AW (2012) 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 308:2369–2379. https://doi.org/10.1001/jama.2012.25321
Heldman AW, Difede DL, Fishman JE, Zambrano JP, Trachtenberg BH, Karantalis V, Mushtaq M, Williams AR, Suncion VY, McNiece IK, Ghersin E, Soto V, Lopera G, Miki R, Willens H, Hendel R, Mitrani R, Pattany P, Feigenbaum G, Oskouei B, Byrnes J, Lowery MH, Sierra J, Pujol MV, Delgado C, Gonzalez PJ, Rodriguez JE, Bagno LL, Rouy D, Altman P, Foo CWP, da Silva J, Anderson E, Schwarz R, Mendizabal A, Hare JM (2014) Transendocardial mesenchymal stem cells and mononuclear bone marrow cells for ischemic cardiomyopathy: the TAC-HFT randomized trial. JAMA 311:62–73. https://doi.org/10.1001/jama.2013.282909
Hirt MN, Hansen A, Eschenhagen T (2014) Cardiac tissue engineering: state of the art. Circ Res 114:354–367. https://doi.org/10.1161/CIRCRESAHA.114.300522
Hsieh PCH, Segers VFM, Davis ME, MacGillivray C, Gannon J, Molkentin JD, Robbins J, Lee RT (2007) Evidence from a genetic fate-mapping study that stem cells refresh adult mammalian cardiomyocytes after injury. Nat Med 13:970–974. https://doi.org/10.1038/nm1618
Ishii O, Shin M, Sueda T, Vacanti JP (2005) In vitro tissue engineering of a cardiac graft using a degradable scaffold with an extracellular matrix–like topography. J Thorac Cardiovasc Surg 130:1358–1363. https://doi.org/10.1016/j.jtcvs.2005.05.048
Jackman CP, Ganapathi AM, Asfour H, Qian Y, Allen BW, Li Y, Bursac N (2018) Engineered cardiac tissue patch maintains structural and electrical properties after epicardial implantation. Biomaterials 159:48–58. https://doi.org/10.1016/j.biomaterials.2018.01.002
Jacot JG, Kita-Matsuo H, Wei KA, Chen HSV, Omens JH, Mercola M, Mcculloch AD (2010) Cardiac myocyte force development during differentiation and maturation. Ann N Y Acad Sci 1188:121–127. https://doi.org/10.1111/j.1749-6632.2009.05091.x
Kai D, Prabhakaran MP, Jin G, Ramakrishna S (2011) Guided orientation of cardiomyocytes on electrospun aligned nanofibers for cardiac tissue engineering. J Biomed Mater Res B Appl Biomater 98B:379–386. https://doi.org/10.1002/jbm.b.31862
Kaushal S, Wehman B, Pietris N, Naughton C, Bentzen SM, Bigham G, Mishra R, Sharma S, Vricella L, Everett AD, Deatrick KB, Huang S, Mehta H, Ravekes WA, Hibino N, Difede DL, Khan A, Hare JM (2017) Study design and rationale for ELPIS: a phase I/IIb randomized pilot study of allogeneic human mesenchymal stem cell injection in patients with hypoplastic left heart syndrome. Am Heart J 192:48–56. https://doi.org/10.1016/j.ahj.2017.06.009
Kerscher P, Turnbull IC, Hodge AJ, Kim J, Seliktar D, Easley CJ, Costa KD, Lipke EA (2016) Direct hydrogel encapsulation of pluripotent stem cells enables ontomimetic differentiation and growth of engineered human heart tissues. Biomaterials 83:383–395. https://doi.org/10.1016/j.biomaterials.2015.12.011
Khan M, Xu Y, Hua S, Johnson J, Belevych A, Janssen PML, Gyorke S, Guan J, Angelos MG (2015) Evaluation of changes in morphology and function of human induced pluripotent stem cell derived cardiomyocytes (HiPSC-CMs) cultured on an aligned-nanofiber cardiac patch. PLoS One 10:e0126338. https://doi.org/10.1371/journal.pone.0126338
Kharaziha M, Nikkhah M, Shin S-R, Annabi N, Masoumi N, Gaharwar AK, Camci-Unal G, Khademhosseini A (2013) PGS:gelatin nanofibrous scaffolds with tunable mechanical and structural properties for engineering cardiac tissues. Biomaterials 34:6355–6366. https://doi.org/10.1016/j.biomaterials.2013.04.045
Kitsara M, Agbulut O, Kontziampasis D, Chen Y, Menasché P (2017) Fibers for hearts: a critical review on electrospinning for cardiac tissue engineering. Acta Biomater 48:20–40. https://doi.org/10.1016/j.actbio.2016.11.014
Kochupura PV, Azeloglu EU, Kelly DJ, Doronin SV, Badylak SF, Krukenkamp IB, Cohen IS, Gaudette GR (2005) Tissue-engineered myocardial patch derived from extracellular matrix provides regional mechanical function. Circulation 112:I144–I149. https://doi.org/10.1161/CIRCULATIONAHA.104.524355
Kofidis T, Lebl DR, Martinez EC, Hoyt G, Tanaka M, Robbins RC (2005) Novel injectable bioartificial tissue facilitates targeted, less invasive, large-scale tissue restoration on the beating heart after myocardial injury. Circulation 112:I173–I177. https://doi.org/10.1161/CIRCULATIONAHA.104.526178
Kolanowski TJ, Rozwadowska N, Malcher A, Szymczyk E, Kasprzak JD, Mietkiewski T, Kurpisz M (2014) In vitro and in vivo characteristics of connexin 43-modified human skeletal myoblasts as candidates for prospective stem cell therapy for the failing heart. Int J Cardiol 173:55–64. https://doi.org/10.1016/j.ijcard.2014.02.009
Laflamme MA, Chen KY, Naumova AV, Muskheli V, Fugate JA, Dupras SK, Reinecke H, Xu C, Hassanipour M, Police S, O’Sullivan C, Collins L, Chen Y, Minami E, Gill EA, Ueno S, Yuan C, Gold J, Murry CE (2007) Cardiomyocytes derived from human embryonic stem cells in pro-survival factors enhance function of infarcted rat hearts. Nat Biotechnol 25:1015–1024. https://doi.org/10.1038/nbt1327
Landa N, Miller L, Feinberg MS, Holbova R, Shachar M, Freeman I, Cohen S, Leor J (2008) Effect of injectable alginate implant on cardiac remodeling and function after recent and old infarcts in rat. Circulation 117:1388–1396. https://doi.org/10.1161/CIRCULATIONAHA.107.727420
Le T, Chong J (2016) Cardiac progenitor cells for heart repair. Cell Death Discov 2:16052. https://doi.org/10.1038/cddiscovery.2016.52
Li D, Xia Y (2004) Electrospinning of nanofibers: reinventing the wheel? Adv Mater 16:1151–1170. https://doi.org/10.1002/adma.200400719
Lin Y-D, Yeh M-L, Yang Y-J, Tsai D-C, Chu T-Y, Shih Y-Y, Chang M-Y, Liu Y-W, Tang ACL, Chen T-Y, Luo C-Y, Chang K-C, Chen J-H, Wu H-L, Hung T-K, Hsieh PCH (2010) Intramyocardial peptide nanofiber injection improves Postinfarction ventricular remodeling and efficacy of bone marrow cell therapy in pigs. Circulation 122:S132–S141. https://doi.org/10.1161/CIRCULATIONAHA.110.939512
Liu W, Thomopoulos S, Xia Y (2012) Electrospun nanofibers for regenerative medicine. Adv Healthc Mater 1:10–25. https://doi.org/10.1002/adhm.201100021
Liu Q, Yang R, Huang X, Zhang H, He L, Zhang L, Tian X, Nie Y, Hu S, Yan Y, Zhang L, Qiao Z, Wang Q-D, Lui KO, Zhou B (2016a) Genetic lineage tracing identifies in situ kit-expressing cardiomyocytes. Cell Res 26:119–130. https://doi.org/10.1038/cr.2015.143
Liu Y, Xu Y, Wang Z, Wen D, Zhang W, Schmull S, Li H, Chen Y, Xue S (2016b) Electrospun nanofibrous sheets of collagen/elastin/polycaprolactone improve cardiac repair after myocardial infarction. Am J Transl Res 8:1678–1694
Luo L, Tang J, Nishi K, Yan C, Dinh P-U, Cores J, Kudo T, Zhang J, Li T-S, Cheng K (2017) Fabrication of synthetic mesenchymal stem cells for the treatment of acute myocardial infarction in MiceNovelty and significance. Circ Res 120:1768–1775. https://doi.org/10.1161/CIRCRESAHA.116.310374
Lux M, Andrée B, Horvath T, Nosko A, Manikowski D, Hilfiker-Kleiner D, Haverich A, Hilfiker A (2016) In vitro maturation of large-scale cardiac patches based on a perfusable starter matrix by cyclic mechanical stimulation. Acta Biomater 30:177–187. https://doi.org/10.1016/j.actbio.2015.11.006
Makkar RR, Smith RR, Cheng K, Malliaras K, Thomson LEJ, Berman D, Czer LSC, Marbán L, Mendizabal A, Johnston PV, Russell SD, Schuleri KH, Lardo AC, Gerstenblith G, Marbán E (2012) Intracoronary cardiosphere-derived cells for heart regeneration after myocardial infarction (CADUCEUS): a prospective, randomised phase 1 trial. Lancet 379:895–904. https://doi.org/10.1016/S0140-6736(12)60195-0
Mann DL, Lee RJ, Coats AJS, Neagoe G, Dragomir D, Pusineri E, Piredda M, Bettari L, Kirwan B-A, Dowling R, Volterrani M, Solomon SD, Sabbah HN, Hinson A, Anker SD (2016) 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 18:314–325. https://doi.org/10.1002/ejhf.449
Martherus RSRM, Vanherle SJV, Timmer EDJ, Zeijlemaker VA, Broers JL, Smeets HJ, Geraedts JP, Ayoubi TAY (2010) Electrical signals affect the cardiomyocyte transcriptome independently of contraction. Physiol Genomics 42A:283–289. https://doi.org/10.1152/physiolgenomics.00182.2009
Martino H, Brofman P, Greco O, Bueno R, Bodanese L, Clausell N, Maldonado JA, Mill J, Braile D, Moraes J, Silva S, Bozza A, Santos B, Campos De Carvalho A (2015) Multicentre, randomized, double-blind trial of intracoronary autologous mononuclear bone marrow cell injection in non-ischaemic dilated cardiomyopathy (the dilated cardiomyopathy arm of the MiHeart study). Eur Heart J 36:2898–2904. https://doi.org/10.1093/eurheartj/ehv477
Mauritz C, Schwanke K, Reppel M, Neef S, Katsirntaki K, Maier LS, Nguemo F, Menke S, Haustein M, Hescheler J, Hasenfuss G, Martin U (2008) Generation of functional murine cardiac myocytes from induced pluripotent stem cells. Circulation 118:507–517. https://doi.org/10.1161/CIRCULATIONAHA.108.778795
Maxwell JT, Wagner MB, Davis ME (2016) Electrically induced calcium handling in cardiac progenitor cells. Stem Cells Int 2016:8917380. https://doi.org/10.1155/2016/8917380
Mayourian J, Savizky RM, Sobie EA, Costa KD (2016) Modeling electrophysiological coupling and fusion between human mesenchymal stem cells and cardiomyocytes. PLoS Comput Biol 12:e1005014. https://doi.org/10.1371/journal.pcbi.1005014
Mayourian J, Cashman TJ, Ceholski DK, Johnson BV, Sachs D, Kaji DA, Sahoo S, Hare JM, Hajjar RJ, Sobie EA, Costa KD (2017) Experimental and computational insight into human mesenchymal stem cell paracrine signaling and Heterocellular coupling effects on cardiac contractility and Arrhythmogenicity. Circ Res 121:411–423. https://doi.org/10.1161/CIRCRESAHA.117.310796
Mayourian J, Ceholski DK, Gorski PA, Mathiyalagan P, Murphy JF, Salazar SI, Stillitano F, Hare JM, Sahoo S, Hajjar RJ, Costa KD (2018) Exosomal microRNA-21-5p mediates mesenchymal stem cell paracrine effects on human cardiac tissue ContractilityNovelty and significance. Circ Res 122:933–944. https://doi.org/10.1161/CIRCRESAHA.118.312420
Menasché P, Hagège AA, Scorsin M, Pouzet B, Desnos M, Duboc D, Schwartz K, Vilquin J-T, Marolleau J-P (2001) Myoblast transplantation for heart failure. Lancet 357:279–280. https://doi.org/10.1016/S0140-6736(00)03617-5
Menasche P, Alfieri O, Janssens S, McKenna W, Reichenspurner H, Trinquart L, Vilquin J-T, Marolleau J-P, Seymour B, Larghero J, Lake S, Chatellier G, Solomon S, Desnos M, Hagege AA (2008) The myoblast autologous grafting in ischemic cardiomyopathy (MAGIC) trial: first randomized placebo-controlled study of myoblast transplantation. Circulation 117:1189–1200. https://doi.org/10.1161/CIRCULATIONAHA.107.734103
Mewhort HEM, Turnbull JD, Meijndert HC, Ngu JMC, Fedak PWM (2014) Epicardial infarct repair with basic fibroblast growth factor–enhanced CorMatrix-ECM biomaterial attenuates postischemic cardiac remodeling. J Thorac Cardiovasc Surg 147:1650–1659. https://doi.org/10.1016/j.jtcvs.2013.08.005
Mewhort HEM, Turnbull JD, Satriano A, Chow K, Flewitt JA, Andrei A-C, Guzzardi DG, Svystonyuk DA, White JA, Fedak PWM (2016) Epicardial infarct repair with bioinductive extracellular matrix promotes vasculogenesis and myocardial recovery. J Heart Lung Transplant 35:661–670. https://doi.org/10.1016/j.healun.2016.01.012
Mosadegh B, Xiong G, Dunham S, Min JK (2015) Current progress in 3D printing for cardiovascular tissue engineering. Biomed Mater 10:034002. https://doi.org/10.1088/1748-6041/10/3/034002
Murphy SV, Atala A (2014) 3D bioprinting of tissues and organs. Nat Biotechnol 32:773–785. https://doi.org/10.1038/nbt.2958
Naito H (2006) Optimizing engineered heart tissue for therapeutic applications as surrogate heart muscle. Circulation 114:I-72–I-78. https://doi.org/10.1161/CIRCULATIONAHA.105.001560
Nguyen PK, Rhee J-W, Wu JC (2016) Adult stem cell therapy and heart failure, 2000 to 2016: a systematic review. JAMA Cardiol 1:831–841. https://doi.org/10.1001/jamacardio.2016.2225
Okada M, Payne TR, Oshima H, Momoi N, Tobita K, Huard J (2010) Differential efficacy of gels derived from small intestinal submucosa as an injectable biomaterial for myocardial infarct repair. Biomaterials 31:7678–7683. https://doi.org/10.1016/j.biomaterials.2010.06.056
Okano H, Nakamura M, Yoshida K, Okada Y, Tsuji O, Nori S, Ikeda E, Yamanaka S, Miura K (2013) Steps toward safe cell therapy using induced pluripotent stem cells. Circ Res 112:523–533. https://doi.org/10.1161/CIRCRESAHA.111.256149
Ott HC, Matthiesen TS, Goh S-K, Black LD, Kren SM, Netoff TI, Taylor DA (2008) Perfusion-decellularized matrix: using nature’s platform to engineer a bioartificial heart. Nat Med 14:213–221. https://doi.org/10.1038/nm1684
Papalamprou A, Chang CW, Vapniarsky N, Clark A, Walker N, Griffiths LG (2016) Xenogeneic cardiac extracellular matrix scaffolds with or without seeded mesenchymal stem cells exhibit distinct in vivo immunosuppressive and regenerative properties. Acta Biomater 45:155–168. https://doi.org/10.1016/j.actbio.2016.07.032
Perin EC, Dohmann HFR, Borojevic R, Silva SA, Sousa ALS, Mesquita CT, Rossi MID, Carvalho AC, Dutra HS, Dohmann HJF, Silva GV, Belém L, Vivacqua R, Rangel FOD, Esporcatte R, Geng YJ, Vaughn WK, Assad JAR, Mesquita ET, Willerson JT (2003) Transendocardial, autologous bone marrow cell transplantation for severe, chronic ischemic heart failure. Circulation 107:2294–2302. https://doi.org/10.1161/01.CIR.0000070596.30552.8B
Perin EC, Dohmann HFR, Borojevic R, Silva SA, Sousa ALS, Silva GV, Mesquita CT, Belém L, Vaughn WK, Rangel FOD, Assad JAR, Carvalho AC, Branco RVC, Rossi MID, Dohmann HJF, Willerson JT (2004) Improved exercise capacity and ischemia 6 and 12 months after transendocardial injection of autologous bone marrow mononuclear cells for ischemic cardiomyopathy. Circulation 110:II213–II218. https://doi.org/10.1161/01.CIR.0000138398.77550.62
Perin EC, Willerson JT, Pepine CJ, Henry TD, Ellis SG, Zhao DXM, Silva GV, Lai D, Thomas JD, Kronenberg MW, Martin AD, Anderson RD, Traverse JH, Penn MS, Anwaruddin S, Hatzopoulos AK, Gee AP, Taylor DA, Cogle CR, Smith D, Westbrook L, Chen J, Handberg E, Olson RE, Geither C, Bowman S, Francescon J, Baraniuk S, Piller LB, Simpson LM, Loghin C, Aguilar D, Richman S, Zierold C, Bettencourt J, Sayre SL, Vojvodic RW, Skarlatos SI, Gordon DJ, Ebert RF, Kwak M, Moyé LA, Simari RD, Network (CCTRN) for the CCTR (2012) Effect of Transendocardial delivery of autologous bone marrow mononuclear cells on functional capacity, left ventricular function, and perfusion in chronic heart failure: the FOCUS-CCTRN trial. JAMA 307:1717–1726. https://doi.org/10.1001/jama.2012.418
Pok S, Myers JD, Madihally SV, Jacot JG (2013) A multi-layered scaffold of a chitosan and gelatin hydrogel supported by a PCL core for cardiac tissue engineering. Acta Biomater 9:5630–5642. https://doi.org/10.1016/j.actbio.2012.10.032
Porrello ER, Mahmoud AI, Simpson E, Hill JA, Richardson JA, Olson EN, Sadek HA (2011) Transient regenerative potential of the neonatal mouse heart. Science 331:1078–1080. https://doi.org/10.1126/science.1200708
Quijada P, Toko H, Fischer KM, Bailey B, Reilly P, Hunt KD, Gude NA, Avitabile D, Sussman MA (2012) Preservation of myocardial structure is enhanced by Pim-1 engineering of bone marrow cells. Circ Res 111:77–86. https://doi.org/10.1161/CIRCRESAHA.112.265207
Quijada P, Salunga HT, Hariharan N, Cubillo JD, El-Sayed FG, Moshref M, Bala KM, Emathinger JM, De La Torre A, Ormachea L, Alvarez R, Gude NA, Sussman MA (2015) Cardiac stem cell hybrids enhance myocardial RepairNovelty and significance. Circ Res 117:695–706. https://doi.org/10.1161/CIRCRESAHA.115.306838
Rajabi-Zeleti S, Jalili-Firoozinezhad S, Azarnia M, Khayyatan F, Vahdat S, Nikeghbalian S, Khademhosseini A, Baharvand H, Aghdami N (2014) The behavior of cardiac progenitor cells on macroporous pericardium-derived scaffolds. Biomaterials 35:970–982. https://doi.org/10.1016/j.biomaterials.2013.10.045
Rao SV, Zeymer U, Douglas PS, Al-Khalidi H, White JA, Liu J, Levy H, Guetta V, Gibson CM, Tanguay J-F, Vermeersch P, Roncalli J, Kasprzak JD, Henry TD, Frey N, Kracoff O, Traverse JH, Chew DP, Lopez-Sendon J, Heyrman R, Krucoff MW (2016) Bioabsorbable intracoronary matrix for prevention of ventricular remodeling after myocardial infarction. J Am Coll Cardiol 68:715–723. https://doi.org/10.1016/j.jacc.2016.05.053
Ravichandran R, Sridhar R, Venugopal JR, Sundarrajan S, Mukherjee S, Ramakrishna S (2014) Gold nanoparticle loaded hybrid nanofibers for cardiogenic differentiation of stem cells for infarcted myocardium regeneration. Macromol Biosci 14:515–525. https://doi.org/10.1002/mabi.201300407
Ravichandran R, Venugopal JR, Mukherjee S, Sundarrajan S, Ramakrishna S (2015) Elastomeric core/shell nanofibrous cardiac patch as a biomimetic support for infarcted porcine myocardium. Tissue Eng Part A 21:1288–1298. https://doi.org/10.1089/ten.tea.2014.0265
Reis LA, Chiu LLY, Feric N, Fu L, Radisic M (2016) Biomaterials in myocardial tissue engineering. J Tissue Eng Regen Med 10:11–28. https://doi.org/10.1002/term.1944
Riegler J, Tiburcy M, Ebert A, Tzatzalos E, Raaz U, Abilez OJ, Shen Q, Kooreman NG, Neofytou E, Chen VC, Wang M, Meyer T, Tsao PS, Connolly AJ, Couture LA, Gold JD, Zimmermann WH, Wu JC (2015) Human engineered heart muscles engraft and survive long term in a rodent myocardial infarction ModelNovelty and significance. Circ Res 117:720–730. https://doi.org/10.1161/CIRCRESAHA.115.306985
Robinson KA, Li J, Mathison M, Redkar A, Cui J, Chronos NAF, Matheny RG, Badylak SF (2005) Extracellular matrix scaffold for cardiac repair. Circulation 112:I135–I143. https://doi.org/10.1161/CIRCULATIONAHA.104.525436
Ronaldson-Bouchard K, Ma SP, Yeager K, Chen T, Song L, Sirabella D, Morikawa K, Teles D, Yazawa M, Vunjak-Novakovic G (2018) Advanced maturation of human cardiac tissue grown from pluripotent stem cells. Nature 556:239–243. https://doi.org/10.1038/s41586-018-0016-3
Ruan J-L, Tulloch NL, Razumova MV, Saiget M, Muskheli V, Pabon L, Reinecke H, Regnier M, Murry CE (2016) Mechanical stress conditioning and electrical stimulation promote contractility and force maturation of induced pluripotent stem cell-derived human cardiac tissue. Circulation 134:1557–1567. https://doi.org/10.1161/CIRCULATIONAHA.114.014998
Sawa Y, Yoshikawa Y, Toda K, Fukushima S, Yamazaki K, Ono M, Sakata Y, Hagiwara N, Kinugawa K, Miyagawa S (2015) Safety and efficacy of autologous skeletal myoblast sheets (TCD-51073) for the treatment of severe chronic heart failure due to ischemic heart disease. Circ J 79:991–999. https://doi.org/10.1253/circj.CJ-15-0243
Scholl FG, Boucek MM, Chan K-C, Valdes-Cruz L, Perryman R (2010) Preliminary experience with cardiac reconstruction using Decellularized porcine extracellular matrix scaffold: human applications in congenital heart disease. World J Pediatr Congenit Heart Surg 1:132–136. https://doi.org/10.1177/2150135110362092
Seif-Naraghi SB, Singelyn JM, Salvatore MA, Osborn KG, Wang JJ, Sampat U, Kwan OL, Strachan GM, Wong J, Schup-Magoffin PJ, Braden RL, Bartels K, DeQuach JA, Preul M, Kinsey AM, DeMaria AN, Dib N, Christman KL (2013) Safety and efficacy of an injectable extracellular matrix hydrogel for treating myocardial infarction. Sci Transl Med 5:173ra25. https://doi.org/10.1126/scitranslmed.3005503
Serpooshan V, Zhao M, Metzler SA, Wei K, Shah PB, Wang A, Mahmoudi M, Malkovskiy AV, Rajadas J, Butte MJ, Bernstein D, Ruiz-Lozano P (2013) The effect of bioengineered acellular collagen patch on cardiac remodeling and ventricular function post myocardial infarction. Biomaterials 34:9048–9055. https://doi.org/10.1016/j.biomaterials.2013.08.017
Seth S, Bhargava B, Narang R, Ray R, Mohanty S, Gulati G, Kumar L, Airan B, Venugopal P (2010) The ABCD (autologous bone marrow cells in dilated cardiomyopathy) trial. J Am Coll Cardiol 55:1643–1644. https://doi.org/10.1016/j.jacc.2009.11.070
Sharma S, Mishra R, Bigham GE, Wehman B, Khan MM, Xu H, Saha P, Goo YA, Datla SR, Chen L, Tulapurkar ME, Taylor BS, Yang P, Karathanasis S, Goodlett DR, Kaushal S (2017) A deep proteome analysis identifies the complete Secretome as the functional unit of human cardiac progenitor CellsNovelty and significance. Circ Res 120:816–834. https://doi.org/10.1161/CIRCRESAHA.116.309782
Shevach M, Maoz BM, Feiner R, Shapira A, Dvir T (2013) Nanoengineering gold particle composite fibers for cardiac tissue engineering. J Mater Chem B 1:5210–5217. https://doi.org/10.1039/C3TB20584C
Shiba Y, Fernandes S, Zhu W-Z, Filice D, Muskheli V, Kim J, Palpant NJ, Gantz J, Moyes KW, Reinecke H, Biber BV, Dardas T, Mignone JL, Izawa A, Hanna R, Viswanathan M, Gold JD, Kotlikoff MI, Sarvazyan N, Kay MW, Murry CE, Laflamme MA (2012) Human ES-cell-derived cardiomyocytes electrically couple and suppress arrhythmias in injured hearts. Nature 489:322–325. https://doi.org/10.1038/nature11317
Shin M, Ishii O, Sueda T, Vacanti JP (2004) Contractile cardiac grafts using a novel nanofibrous mesh. Biomaterials 25:3717–3723. https://doi.org/10.1016/j.biomaterials.2003.10.055
Siepe M, Golsong P, Poppe A, Blumenthal B, von Wattenwyl R, Heilmann C, Förster K, Schlensak C, Beyersdorf F (2010) Scaffold-based transplantation of Akt1-overexpressing skeletal myoblasts: functional regeneration is associated with angiogenesis and reduced infarction size. Tissue Eng Part A 17:205–212. https://doi.org/10.1089/ten.tea.2009.0721
Simari RD, Pepine CJ, Traverse JH, Henry TD, Bolli R, Spoon DB, Yeh E, Hare JM, Schulman IH, Anderson RD, Lambert C, Sayre SL, Taylor DA, Ebert RF, Moye LA (2014) Bone marrow mononuclear cell therapy for acute myocardial infarction: a perspective from the cardiovascular cell therapy research network. Circ Res 114:1564–1568. https://doi.org/10.1161/CIRCRESAHA.114.303720
Singelyn JM, Dequach JA, Seif-Naraghi SB, Littlefield RB, Schup-Magoffin PJ, Christman KL (2009) Naturally derived myocardial matrix as an injectable scaffold for cardiac tissue engineering. Biomaterials 30:5409–5416. https://doi.org/10.1016/j.biomaterials.2009.06.045
Singelyn JM, Sundaramurthy P, Johnson TD, Schup-Magoffin PJ, Hu DP, Faulk DM, Wang J, Mayle KM, Bartels K, Salvatore M, Kinsey AM, Demaria AN, Dib N, Christman KL (2012) Catheter-deliverable hydrogel derived from Decellularized ventricular extracellular matrix increases endogenous cardiomyocytes and preserves cardiac function post-myocardial infarction. J Am Coll Cardiol 59:751–763. https://doi.org/10.1016/j.jacc.2011.10.888
Strauer BE, Brehm M, Zeus T, Gattermann N, Hernandez A, Sorg RV, Kögler G, Wernet P (2001) Myocardial regeneration after intracoronary transplantation of human autologous stem cells following acute myocardial infarction. Dtsch Med Wochenschr 126:932–938. https://doi.org/10.1055/s-2001-16579-2
Sultana N, Zhang L, Yan J, Chen J, Cai W, Razzaque S, Jeong D, Sheng W, Bu L, Xu M, Huang G-Y, Hajjar RJ, Zhou B, Moon A, Cai C-L (2015) Resident c-kit+ cells in the heart are not cardiac stem cells. Nat Commun 6:8701. https://doi.org/10.1038/ncomms9701
Sun X, Nunes SS (2015) Overview of hydrogel-based strategies for application in cardiac tissue regeneration. Biomed Mater 10:034005. https://doi.org/10.1088/1748-6041/10/3/034005
Sürder D, Manka R, Moccetti T, Lo Cicero V, Emmert MY, Klersy C, Soncin S, Turchetto L, Radrizzani M, Zuber M, Windecker S, Moschovitis A, Bühler I, Kozerke S, Erne P, Lüscher TF, Corti R (2016) Effect of bone marrow–derived mononuclear cell treatment, early or late after acute myocardial infarction: twelve months CMR and long-term clinical results. Circ Res 119:481–490. https://doi.org/10.1161/CIRCRESAHA.116.308639
Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S (2007) Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131:861–872. https://doi.org/10.1016/j.cell.2007.11.019
Tallawi M, Dippold D, Rai R, D’Atri D, Roether JA, Schubert DW, Rosellini E, Engel FB, Boccaccini AR (2016) Novel PGS/PCL electrospun fiber mats with patterned topographical features for cardiac patch applications. Mater Sci Eng C 69:569–576. https://doi.org/10.1016/j.msec.2016.06.083
Tan MY, Zhi W, Wei RQ, Huang YC, Zhou KP, Tan B, Deng L, Luo JC, Li XQ, Xie HQ, Yang ZM (2009) Repair of infarcted myocardium using mesenchymal stem cell seeded small intestinal submucosa in rabbits. Biomaterials 30:3234–3240. https://doi.org/10.1016/j.biomaterials.2009.02.013
Tang J, Shen D, Caranasos TG, Wang Z, Vandergriff AC, Allen TA, Hensley MT, Dinh P-U, Cores J, Li T-S, Zhang J, Kan Q, Cheng K (2017) Therapeutic microparticles functionalized with biomimetic cardiac stem cell membranes and secretome. Nat Commun 8:13724. https://doi.org/10.1038/ncomms13724
Terrovitis JV, Smith RR, Marbán E (2010) Assessment and optimization of cell engraftment after transplantation into the heart. Circ Res 106:479–494. https://doi.org/10.1161/CIRCRESAHA.109.208991
Tijore A, Irvine SA, Sarig U, Mhaisalkar P, Baisane V, Venkatraman S (2018) Contact guidance for cardiac tissue engineering using 3D bioprinted gelatin patterned hydrogel. Biofabrication 10:025003. https://doi.org/10.1088/1758-5090/aaa15d
Traverse JH, Henry TD, Ellis SG, Pepine CJ, Willerson JT, Zhao DXM, Forder JR, Byrne BJ, Hatzopoulos AK, Penn MS, Perin EC, Baran KW, Chambers J, Lambert C, Raveendran G, Simon DI, Vaughan DE, Simpson LM, Gee AP, Taylor DA, Cogle CR, Thomas JD, Silva GV, Jorgenson BC, Olson RE, Bowman S, Francescon J, Geither C, Handberg E, Smith DX, Baraniuk S, Piller LB, Loghin C, Aguilar D, Richman S, Zierold C, Bettencourt J, Sayre SL, Vojvodic RW, Skarlatos SI, Gordon DJ, Ebert RF, Kwak M, Moyé LA, Simari RD, ResearchNetwork (CCTRN) for the CCT (2011) Effect of intracoronary delivery of autologous bone marrow mononuclear cells 2 to 3 weeks following acute myocardial infarction on left ventricular function: the LateTIME randomized trial. JAMA 306:2110–2119. https://doi.org/10.1001/jama.2011.1670
Traverse JH, Henry TD, Pepine CJ, Willerson JT, Zhao DXM, Ellis SG, Forder JR, Anderson RD, Hatzopoulos AK, Penn MS, Perin EC, Chambers J, Baran KW, Raveendran G, Lambert C, Lerman A, Simon DI, Vaughan DE, Lai D, Gee AP, Taylor DA, Cogle CR, Thomas JD, Olson RE, Bowman S, Francescon J, Geither C, Handberg E, Kappenman C, Westbrook L, Piller LB, Simpson LM, Baraniuk S, Loghin C, Aguilar D, Richman S, Zierold C, Spoon DB, Bettencourt J, Sayre SL, Vojvodic RW, Skarlatos SI, Gordon DJ, Ebert RF, Kwak M, Moyé LA, Simari RD, Network (CCTRN) for the CCTR (2012) Effect of the use and timing of bone marrow mononuclear cell delivery on left ventricular function after acute myocardial infarction: the TIME randomized trial. JAMA 308:2380–2389. https://doi.org/10.1001/jama.2012.28726
Treskes P, Neef K, Srinivasan SP, Halbach M, Stamm C, Cowan D, Scherner M, Madershahian N, Wittwer T, Hescheler J, Wahlers T, Choi Y-H (2015) Preconditioning of skeletal myoblast-based engineered tissue constructs enables functional coupling to myocardium in vivo. J Thorac Cardiovasc Surg 149:348–356. https://doi.org/10.1016/j.jtcvs.2014.09.034
Tulloch NL, Muskheli V, Razumova MV, Korte FS, Regnier M, Hauch KD, Pabon L, Reinecke H, Murry CE (2011) Growth of engineered human myocardium with mechanical loading and vascular coculture. Circ Res 109:47–59. https://doi.org/10.1161/CIRCRESAHA.110.237206
van Berlo JH, Kanisicak O, Maillet M, Vagnozzi RJ, Karch J, Lin S-CJ, Middleton RC, Marbán E, Molkentin JD (2014) c-kit+ cells minimally contribute cardiomyocytes to the heart. Nature 509:337–341. https://doi.org/10.1038/nature13309
van Laake LW, Passier R, Doevendans PA, Mummery CL (2008) Human embryonic stem cell–derived cardiomyocytes and cardiac repair in rodents. Circ Res 102:1008–1010. https://doi.org/10.1161/CIRCRESAHA.108.175505
Vashi AV, White JF, McLean KM, Neethling WML, Rhodes DI, Ramshaw JAM, Werkmeister JA (2015) Evaluation of an established pericardium patch for delivery of mesenchymal stem cells to cardiac tissue. J Biomed Mater Res A 103:1999–2005. https://doi.org/10.1002/jbm.a.35335
Vicinanza C, Aquila I, Scalise M, Cristiano F, Marino F, Cianflone E, Mancuso T, Marotta P, Sacco W, Lewis FC, Couch L, Shone V, Gritti G, Torella A, Smith AJ, Terracciano CM, Britti D, Veltri P, Indolfi C, Nadal-Ginard B, Ellison-Hughes GM, Torella D (2017) Adult cardiac stem cells are multipotent and robustly myogenic: c-kit expression is necessary but not sufficient for their identification. Cell Death Differ 24:2101–2116. https://doi.org/10.1038/cdd.2017.130
Vicinanza C, Aquila I, Cianflone E, Scalise M, Marino F, Mancuso T, Fumagalli F, Giovannone ED, Cristiano F, Iaccino E, Marotta P, Torella A, Latini R, Agosti V, Veltri P, Urbanek K, Isidori AM, Saur D, Indolfi C, Nadal-Ginard B, Torella D (2018) Kit cre knock-in mice fail to fate-map cardiac stem cells. Nature 555:E1–E5. https://doi.org/10.1038/nature25771
von Bahr L, Batsis I, Moll G, Hägg M, Szakos A, Sundberg B, Uzunel M, Ringden O, Blanc KL (2012) Analysis of tissues following mesenchymal stromal cell therapy in humans indicates limited long-term engraftment and no ectopic tissue formation. Stem Cells 30:1575–1578. https://doi.org/10.1002/stem.1118
Wang Q, Yang H, Bai A, Jiang W, Li X, Wang X, Mao Y, Lu C, Qian R, Guo F, Ding T, Chen H, Chen S, Zhang J, Liu C, Sun N (2016) Functional engineered human cardiac patches prepared from nature’s platform improve heart function after acute myocardial infarction. Biomaterials 105:52–65. https://doi.org/10.1016/j.biomaterials.2016.07.035
Waters R, Alam P, Pacelli S, Chakravarti AR, Ahmed RPH, Paul A (2018) Stem cell-inspired secretome-rich injectable hydrogel to repair injured cardiac tissue. Acta Biomater 69:95–106. https://doi.org/10.1016/j.actbio.2017.12.025
Wei H-J, Chen S-C, Chang Y, Hwang S-M, Lin W-W, Lai P-H, Chiang HK, Hsu L-F, Yang H-H, Sung H-W (2006) Porous acellular bovine pericardia seeded with mesenchymal stem cells as a patch to repair a myocardial defect in a syngeneic rat model. Biomaterials 27:5409–5419. https://doi.org/10.1016/j.biomaterials.2006.06.022
Wei H-J, Chen C-H, Lee W-Y, Chiu I, Hwang S-M, Lin W-W, Huang C-C, Yeh Y-C, Chang Y, Sung H-W (2008) Bioengineered cardiac patch constructed from multilayered mesenchymal stem cells for myocardial repair. Biomaterials 29:3547–3556. https://doi.org/10.1016/j.biomaterials.2008.05.009
Wickham AM, Islam MM, Mondal D, Phopase J, Sadhu V, Tamás É, Polisetti N, Richter-Dahlfors A, Liedberg B, Griffith M (2014) Polycaprolactone-thiophene-conjugated carbon nanotube meshes as scaffolds for cardiac progenitor cells. J Biomed Mater Res B Appl Biomater 102:1553–1561. https://doi.org/10.1002/jbm.b.33136
Wilhelm MJ (2015) Long-term outcome following heart transplantation: current perspective. J Thorac Dis 7:549–551. https://doi.org/10.3978/j.issn.2072-1439.2015.01.46
Wollert KC, Meyer GP, Lotz J, Ringes Lichtenberg S, Lippolt P, Breidenbach C, Fichtner S, Korte T, Hornig B, Messinger D, Arseniev L, Hertenstein B, Ganser A, Drexler H (2004) Intracoronary autologous bone-marrow cell transfer after myocardial infarction: the BOOST randomised controlled clinical trial. Lancet 364:141–148. https://doi.org/10.1016/S0140-6736(04)16626-9
Wollert KC, Meyer GP, Müller-Ehmsen J, Tschöpe C, Bonarjee V, Larsen AI, May AE, Empen K, Chorianopoulos E, Tebbe U, Waltenberger J, Mahrholdt H, Ritter B, Pirr J, Fischer D, Korf-Klingebiel M, Arseniev L, Heuft H-G, Brinchmann JE, Messinger D, Hertenstein B, Ganser A, Katus HA, Felix SB, Gawaz MP, Dickstein K, Schultheiss H-P, Ladage D, Greulich S, Bauersachs J (2017) Intracoronary autologous bone marrow cell transfer after myocardial infarction: the BOOST-2 randomised placebo-controlled clinical trial. Eur Heart J 38:2936–2943. https://doi.org/10.1093/eurheartj/ehx188
Wu KH, Mo XM, Han ZC, Zhou B (2011) Stem cell engraftment and survival in the ischemic heart. Ann Thorac Surg 92:1917–1925. https://doi.org/10.1016/j.athoracsur.2011.07.012
Xiao W, Guo S, Gao C, Dai G, Gao Y, Li M, Wang X, Hu D (2017) A randomized comparative study on the efficacy of intracoronary infusion of autologous bone marrow mononuclear cells and mesenchymal stem cells in patients with dilated cardiomyopathy. Int Heart J 58:238–244. https://doi.org/10.1536/ihj.16-328
Yanagawa B, Rao V, Yau TM, Cusimano RJ (2013) Initial experience with intraventricular repair using CorMatrix extracellular matrix. Innov Technol Tech Cardiothorac Vasc Surg 8:348–352. https://doi.org/10.1097/IMI.0000000000000014
Ye L, Zimmermann W-H, Garry DJ, Zhang J (2013) Patching the heart: cardiac repair from within and outside. Circ Res 113:922–932. https://doi.org/10.1161/CIRCRESAHA.113.300216
Ye L, Chang Y-H, Xiong Q, Zhang P, Zhang L, Somasundaram P, Lepley M, Swingen C, Su L, Wendel JS, Guo J, Jang A, Rosenbush D, Greder L, Dutton JR, Zhang J, Kamp TJ, Kaufman DS, Ge Y, Zhang J (2014) Cardiac repair in a porcine model of acute myocardial infarction with human induced pluripotent stem cell-derived cardiovascular cell populations. Cell Stem Cell 15:750–761. https://doi.org/10.1016/j.stem.2014.11.009
Yoon CH, Koyanagi M, Iekushi K, Seeger F, Urbich C, Zeiher AM, Dimmeler S (2010) Mechanism of improved cardiac function after bone marrow mononuclear cell therapy: role of cardiovascular lineage commitment. Circulation 121:2001–2011. https://doi.org/10.1161/CIRCULATIONAHA.109.909291
Yoshikawa Y, Miyagawa S, Toda K, Saito A, Sakata Y, Sawa Y (2018) Myocardial regenerative therapy using a scaffold-free skeletal-muscle-derived cell sheet in patients with dilated cardiomyopathy even under a left ventricular assist device: a safety and feasibility study. Surg Today 48:200–210. https://doi.org/10.1007/s00595-017-1571-1
Yu J, Lee A-R, Lin W-H, Lin C-W, Wu Y-K, Tsai W-B (2014) Electrospun PLGA fibers incorporated with functionalized biomolecules for cardiac tissue engineering. Tissue Eng Part A 20:1896–1907. https://doi.org/10.1089/ten.tea.2013.0008
Zhang M, Methot D, Poppa V, Fujio Y, Walsh K, Murry CE (2001) Cardiomyocyte grafting for cardiac repair: graft cell death and anti-death strategies. J Mol Cell Cardiol 33:907–921. https://doi.org/10.1006/jmcc.2001.1367
Zhang J, Zhu W, Radisic M, Vunjak-Novakovic G (2018) Can we engineer a human cardiac patch for therapy? Circ Res 123:244–265. https://doi.org/10.1161/CIRCRESAHA.118.311213
Zheng S-X, Weng Y-L, Zhou C-Q, Wen Z-Z, Huang H, Wu W, Wang J-F, Wang T (2013) Comparison of cardiac stem cells and mesenchymal stem cells transplantation on the cardiac electrophysiology in rats with myocardial infarction. Stem Cell Rev Rep 9:339–349. https://doi.org/10.1007/s12015-012-9367-6
Zimmermann W-H (2011) Embryonic and embryonic-like stem cells in heart muscle engineering. J Mol Cell Cardiol 50:320–326. https://doi.org/10.1016/j.yjmcc.2010.10.027
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Streeter, B.W., Davis, M.E. (2018). Therapeutic Cardiac Patches for Repairing the Myocardium. In: Turksen, K. (eds) Cell Biology and Translational Medicine, Volume 5. Advances in Experimental Medicine and Biology(), vol 1144. Springer, Cham. https://doi.org/10.1007/5584_2018_309
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