Human Induced Pluripotent Stem Cell-Derived Cardiomyocyte Encapsulating Bioactive Hydrogels Improve Rat Heart Function Post Myocardial Infarction

Stem Cell Reports

Volumn 9, Issue 5, 2017, Pages 1415-1422

  Chow, Andre ^a   Stuckey, Daniel J ^b,d   Kidher, Emaddin ^a   Rocco, Mark ^c   Jabbour, Richard J ^d   Mansfield, Catherine A ^d   Darzi, Ara ^a   Harding, Sian E ^d   Stevens, Molly M ^c   Athanasiou, Thanos ^a  

^a ST MARY S HOSPITAL   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

^d NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

Author keywords

erythropoietin; hydrogel; induced pluripotent stem cell derived cardiomyocytes; iPSC CMs; MRI; myocardial infarction; myocardial tissue engineering; rat

Indexed keywords

ALPHA 1A ADRENERGIC RECEPTOR; ATRIAL NATRIURETIC FACTOR; ERYTHROPOIETIN; MACROGOL; MYOSIN VI; MYOSIN VIIA; SODIUM CHLORIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARDIAC MUSCLE CELL; CARDIOVASCULAR MAGNETIC RESONANCE; CELL PROTECTION; COLLAGEN FIBER; CONTROLLED STUDY; HEART EJECTION FRACTION; HEART FAILURE; HEART FUNCTION; HEART INFARCTION; HEART LEFT VENTRICLE PRESSURE; HEART PROTECTION; HEART RATE; HEART VENTRICLE REMODELING; HYDROGEL; INDUCED PLURIPOTENT STEM CELL; ISOLATED HEART; MAJOR HISTOCOMPATIBILITY COMPLEX; MALE; NONHUMAN; OXIDATIVE STRESS; POLYMERIZATION; PRIORITY JOURNAL; RAT; ANIMAL; CELL CULTURE; CHEMISTRY; CYTOLOGY; HUMAN; INTRALESIONAL DRUG ADMINISTRATION; NUDE RAT; PROCEDURES; STEM CELL TRANSPLANTATION; TRANSPLANTATION;

ANIMALS; CELLS, CULTURED; ERYTHROPOIETIN; HUMANS; HYDROGELS; INDUCED PLURIPOTENT STEM CELLS; INJECTIONS, INTRALESIONAL; MALE; MYOCARDIAL INFARCTION; MYOCYTES, CARDIAC; POLYETHYLENE GLYCOLS; RATS; RATS, NUDE; STEM CELL TRANSPLANTATION;

EID: 85030653780     PISSN: 22136711     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.stemcr.2017.09.003     Document Type: Article

References (38)

1. Berry, M.F., Engler, A.J., Woo, Y.J., Pirolli, T.J., Bish, L.T., Jayasankar, V., Morine, K.J., Gardner, T.J., Discher, D.E., Sweeney, H.L., Mesenchymal stem cell injection after myocardial infarction improves myocardial compliance. Am. J. Physiol. Heart Circ. Physiol. 290 (2006), H2196–H2203.
2. Bolli, R., Chugh, A.R., D'Amario, D., Loughran, J.H., Stoddard, M.F., Ikram, S., Beache, G.M., Wagner, S.G., Leri, A., Hosoda, T., et al. Cardiac stem cells in patients with ischaemic cardiomyopathy (SCIPIO): initial results of a randomised phase 1 trial. Lancet 378 (2011), 1847–1857.
3. Brines, M., Cerami, A., Erythropoietin-mediated tissue protection: reducing collateral damage from the primary injury response. J. Intern. Med. 264 (2008), 405–432.
4. Carr, C.A., Stuckey, D.J., Tan, J.J., Tan, S.C., Gomes, R.S., Camelliti, P., Messina, E., Giacomello, A., Ellison, G.M., Clarke, K., Cardiosphere-derived cells improve function in the infarcted rat heart for at least 16 weeks–an MRI study. PLoS One, 6, 2011, e25669.
5. Chong, J.J., Yang, X., Don, C.W., Minami, E., Liu, Y.W., Weyers, J.J., Mahoney, W.M., Van Biber, B., Cook, S.M., Palpant, N.J., et al. Human embryonic-stem-cell-derived cardiomyocytes regenerate non-human primate hearts. Nature 510 (2014), 273–277.
6. Christman, K.L., Lee, R.J., Biomaterials for the treatment of myocardial infarction. J. Am. Coll. Cardiol. 48 (2006), 907–913.
7. Coleman, T., Brines, M., Science review: recombinant human erythropoietin in critical illness: a role beyond anemia?. Crit. Care 8 (2004), 337–341.
8. Coulombe, K.L., Bajpai, V.K., Andreadis, S.T., Murry, C.E., Heart regeneration with engineered myocardial tissue. Annu. Rev. Biomed. Eng. 16 (2014), 1–28.
9. Davis, M.E., Hsieh, P.C., Takahashi, T., Song, Q., Zhang, S., Kamm, R.D., Grodzinsky, A.J., Anversa, P., Lee, R.T., Local myocardial insulin-like growth factor 1 (IGF-1) delivery with biotinylated peptide nanofibers improves cell therapy for myocardial infarction. Proc. Natl. Acad. Sci. USA 103 (2006), 8155–8160.
10. Ellison, G.M., Vicinanza, C., Smith, A.J., Aquila, I., Leone, A., Waring, C.D., Henning, B.J., Stirparo, G.G., Papait, R., Scarfo, M., et al. Adult c-kit(pos) cardiac stem cells are necessary and sufficient for functional cardiac regeneration and repair. Cell 154 (2013), 827–842.
11. Frey, N., Linke, A., Suselbeck, T., Muller-Ehmsen, J., Vermeersch, P., Schoors, D., Rosenberg, M., Bea, F., Tuvia, S., Leor, J., 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 (2014), 806–812.
12. Gnecchi, M., He, H., Liang, O.D., Melo, L.G., Morello, F., Mu, H., Noiseux, N., Zhang, L., Pratt, R.E., Ingwall, J.S., Dzau, V.J., Paracrine action accounts for marked protection of ischemic heart by Akt-modified mesenchymal stem cells. Nat. Med. 11 (2005), 367–368.
13. Hoffman, A.S., Hydrogels for biomedical applications. Adv. Drug Deliv. Rev. 54 (2002), 3–12.
14. Jawad, H., Lyon, A.R., Harding, S.E., Ali, N.N., Boccaccini, A.R., Myocardial tissue engineering. Br. Med. Bull. 87 (2008), 31–47.
15. Kawamura, M., Miyagawa, S., Miki, K., Saito, A., Fukushima, S., Higuchi, T., Kawamura, T., Kuratani, T., Daimon, T., Shimizu, T., et al. Feasibility, safety, and therapeutic efficacy of human induced pluripotent stem cell-derived cardiomyocyte sheets in a porcine ischemic cardiomyopathy model. Circulation 126:11 Suppl 1 (2012), S29–S37.
16. Kobayashi, H., Minatoguchi, S., Yasuda, S., Bao, N., Kawamura, I., Iwasa, M., Yamaki, T., Sumi, S., Misao, Y., Ushikoshi, H., et al. Post-infarct treatment with an erythropoietin-gelatin hydrogel drug delivery system for cardiac repair. Cardiovasc. Res. 79 (2008), 611–620.
17. Kraehenbuehl, T.P., Ferreira, L.S., Hayward, A.M., Nahrendorf, M., van der Vlies, A.J., Vasile, E., Weissleder, R., Langer, R., Hubbell, J.A., Human embryonic stem cell-derived microvascular grafts for cardiac tissue preservation after myocardial infarction. Biomaterials 32 (2010), 1102–1109.
18. Laflamme, M.A., Chen, K.Y., Naumova, A.V., Muskheli, V., Fugate, J.A., Dupras, S.K., Reinecke, H., Xu, C., Hassanipour, M., Police, S., et al. Cardiomyocytes derived from human embryonic stem cells in pro-survival factors enhance function of infarcted rat hearts. Nat. Biotechnol. 25 (2007), 1015–1024.
19. Leor, J., Amsalem, Y., Cohen, S., Cells, scaffolds, and molecules for myocardial tissue engineering. Pharmacol. Ther. 105 (2005), 151–163.
20. Lin, C.C., Anseth, K.S., PEG hydrogels for the controlled release of biomolecules in regenerative medicine. Pharm. Res. 26 (2009), 631–643.
21. Makkar, R.R., Smith, R.R., Cheng, K., Malliaras, K., Thomson, L.E., Berman, D., Czer, L.S., Marban, L., Mendizabal, A., Johnston, P.V., et al. Intracoronary cardiosphere-derived cells for heart regeneration after myocardial infarction (CADUCEUS): a prospective, randomised phase 1 trial. Lancet 379 (2012), 895–904.
22. Murry, C.E., Reinecke, H., Pabon, L.M., Regeneration gaps: observations on stem cells and cardiac repair. J. Am. Coll. Cardiol. 47 (2006), 1777–1785.
23. Noseda, M., Harada, M., McSweeney, S., Leja, T., Belian, E., Stuckey, D.J., Abreu Paiva, M.S., Habib, J., Macaulay, I., de Smith, A.J., et al. PDGFRalpha demarcates the cardiogenic clonogenic Sca1+ stem/progenitor cell in adult murine myocardium. Nat. Commun., 6, 2015, 6930.
24. Orlic, D., Kajstura, J., Chimenti, S., Jakoniuk, I., Anderson, S.M., Li, B., Pickel, J., McKay, R., Nadal-Ginard, B., Bodine, D.M., et al. Bone marrow cells regenerate infarcted myocardium. Nature 410 (2001), 701–705.
25. Passier, R., van Laake, L.W., Mummery, C.L., Stem-cell-based therapy and lessons from the heart. Nature 453 (2008), 322–329.
26. Place, E.S., Evans, N.D., Stevens, M.M., Complexity in biomaterials for tissue engineering. Nat. Mater. 8 (2009), 457–470.
27. Robey, T.E., Saiget, M.K., Reinecke, H., Murry, C.E., Systems approaches to preventing transplanted cell death in cardiac repair. J. Mol. Cell. Cardiol. 45 (2008), 567–581.
28. Roger, V.L., Go, A.S., Lloyd-Jones, D.M., Benjamin, E.J., Berry, J.D., Borden, W.B., Bravata, D.M., Dai, S., Ford, E.S., Fox, C.S., et al. Heart disease and stroke statistics–2012 update: a report from the American Heart Association. Circulation 125 (2012), e2–e220.
29. Sanganalmath, S.K., Bolli, R., Cell therapy for heart failure: a comprehensive overview of experimental and clinical studies, current challenges, and future directions. Circ. Res. 113 (2013), 810–834.
30. Segers, V.F., Lee, R.T., Stem-cell therapy for cardiac disease. Nature 451 (2008), 937–942.
31. Sheikh, A.Y., Lin, S.A., Cao, F., Cao, Y., van der Bogt, K.E., Chu, P., Chang, C.P., Contag, C.H., Robbins, R.C., Wu, J.C., Molecular imaging of bone marrow mononuclear cell homing and engraftment in ischemic myocardium. Stem Cells 25 (2007), 2677–2684.
32. Speidel, A.T., Stuckey, D.J., Chow, L.W., Jackson, L.H., Noseda, M., Abreu Paiva, M., Schneider, M.D., Stevens, M.M., Multimodal hydrogel-based platform to deliver and monitor cardiac progenitor/stem cell engraftment. ACS Cent. Sci. 3 (2017), 338–348.
33. Stuckey, D.J., McSweeney, S.J., Thin, M.Z., Habib, J., Price, A.N., Fiedler, L.R., Gsell, W., Prasad, S.K., Schneider, M.D., T(1) mapping detects pharmacological retardation of diffuse cardiac fibrosis in mouse pressure-overload hypertrophy. Circ. Cardiovasc. Imaging 7 (2014), 240–249.
34. Takehara, N., Tsutsumi, Y., Tateishi, K., Ogata, T., Tanaka, H., Ueyama, T., Takahashi, T., Takamatsu, T., Fukushima, M., Komeda, M., et al. Controlled delivery of basic fibroblast growth factor promotes human cardiosphere-derived cell engraftment to enhance cardiac repair for chronic myocardial infarction. J. Am. Coll. Cardiol. 52 (2008), 1858–1865.
35. Van Tomme, S.R., Storm, G., Hennink, W.E., In situ gelling hydrogels for pharmaceutical and biomedical applications. Int. J. Pharm. 355 (2008), 1–18.
36. Wall, S.T., Walker, J.C., Healy, K.E., Ratcliffe, M.B., Guccione, J.M., Theoretical impact of the injection of material into the myocardium: a finite element model simulation. Circulation 114 (2006), 2627–2635.
37. Yamanaka, S., A fresh look at iPS cells. Cell 137 (2009), 13–17.
38. Zhang, J., Wilson, G.F., Soerens, A.G., Koonce, C.H., Yu, J., Palecek, S.P., Thomson, J.A., Kamp, T.J., Functional cardiomyocytes derived from human induced pluripotent stem cells. Circ. Res. 104 (2009), e30–41.