The use of aggregates of purified cardiomyocytes derived from human ESCs for functional engraftment after myocardial infarction

Biomaterials

Volumn 34, Issue 16, 2013, Pages 4013-4026

  Moon, Sung Hwan ^a   Kang, Sun Woong ^b   Park, Soon Jung ^a   Bae, Daekyeong ^c   Kim, Sung Joon ^d   Lee, Hyang Ae ^d,e   Kim, Kyung Soo ^d   Hong, Ki Sung ^c   Kim, Jong Soo ^f   Do, Jeong Tae ^f   Byun, Ki Hyun ^g   Chung, Hyung Min ^a,c  

^a CHA University   (South Korea)

^b Korea University College of Medicine   (South Korea)

^c CHA Bio and Diostech Co Ltd   (South Korea)

^d Seoul National University College of Medicine   (South Korea)

^e Korea Institute of Toxicology   (South Korea)

^f Konkuk University   (South Korea)

^g Kwandong University College of Medicine   (South Korea)

Author keywords

Aggregate; Cardiomyocyte; Human embryonic stem cell; Purification; Transplantation

Indexed keywords

CARDIAC DIFFERENTIATION; CARDIOMYOCYTES; DIRECTED DIFFERENTIATIONS; FUNCTIONAL CONNECTION; HUMAN EMBRYONIC STEM CELLS; IMMUNOHISTOCHEMICAL ANALYSIS; MYOCARDIAL INFARCTION; THERAPEUTIC EFFICACY;

CELL GROWTH; CELLS; CYTOLOGY; PURIFICATION; TRANSPLANTATION (SURGICAL);

AGGREGATES;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL AGGREGATION; CELL DIFFERENTIATION; CELL FUNCTION; CELL HYPOXIA; CELL LINEAGE; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; CULTURE MEDIUM; EMBRYO; EMBRYONIC STEM CELL; ENGRAFTMENT; HEART INFARCTION; HEART LEFT VENTRICLE FUNCTION; HEART MUSCLE; HEART MUSCLE CELL; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

ANIMALS; APOPTOSIS; CELL AGGREGATION; CELL DIFFERENTIATION; CELL SEPARATION; CELL SURVIVAL; CELLS, CULTURED; COLONY-FORMING UNITS ASSAY; CULTURE MEDIA, CONDITIONED; CULTURE MEDIA, SERUM-FREE; EMBRYOID BODIES; EMBRYONIC STEM CELLS; HUMANS; MICE; MYOCARDIAL INFARCTION; MYOCYTES, CARDIAC; RATS; RECOVERY OF FUNCTION; STEM CELL TRANSPLANTATION;

RATTUS;

EID: 84874968852     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2013.02.022     Document Type: Article

References (51)

1. Rubart M., Field L.J. Cardiac regeneration: repopulating the heart. Annu Rev Physiol 2006, 68:29-49.
2. Kocher A.A., Schuster M.D., Szabolcs M.J., Takuma S., Burkhoff D., Wang J., et al. Neovascularization of ischemic myocardium by human bone-marrow-derived angioblasts prevents cardiomyocyte apoptosis, reduces remodeling and improves cardiac function. Nat Med 2001, 7:430-436.
3. Sun Y., Zhang J.Q., Zhang J., Lamparter S. Cardiac remodeling by fibrous tissue after infarction in rats. J Lab Clin Med 2000, 135:316-323.
4. Laflamme M.A., Murry C.E. Regenerating the heart. Nat Biotechnol 2005, 23:845-856.
5. Salim R., Al-Subu M., Dawod E. Efficiency of removal of cadmium from aqueous solutions by plant leaves and the effects of interaction of combinations of leaves on their removal efficiency. J Environ Manage 2008, 87:521-532.
6. Pendyala L., Goodchild T., Gadesam R.R., Chen J., Robinson K., Chronos N., et al. Cellular cardiomyoplasty and cardiac regeneration. Curr Cardiol Rev 2008, 4:72-80.
7. Murry C.E., Field L.J., Menasche P. Cell-based cardiac repair: reflections at the 10-year point. Circulation 2005, 112:3174-3183.
8. Reinecke H., Zhang M., Bartosek T., Murry C.E. Survival, integration, and differentiation of cardiomyocyte grafts: a study in normal and injured rat hearts. Circulation 1999, 100:193-202.
9. Taylor D.A., Atkins B.Z., Hungspreugs P., Jones T.R., Reedy M.C., Hutcheson K.A., et al. Regenerating functional myocardium: improved performance after skeletal myoblast transplantation. Nat Med 1998, 4:929-933.
10. Suzuki K., Murtuza B., Smolenski R.T., Sammut I.A., Suzuki N., Kaneda Y., et al. Cell transplantation for the treatment of acute myocardial infarction using vascular endothelial growth factor-expressing skeletal myoblasts. Circulation 2001, 104:I207-I212.
11. Li R.K., Jia Z.Q., Weisel R.D., Merante F., Mickle D.A. Smooth muscle cell transplantation into myocardial scar tissue improves heart function. J Mol Cell Cardiol 1999, 31:513-522.
12. He J.Q., Ma Y., Lee Y., Thomson J.A., Kamp T.J. Human embryonic stem cells develop into multiple types of cardiac myocytes: action potential characterization. Circ Res 2003, 93:32-39.
13. Kehat I., Kenyagin-Karsenti D., Snir M., Segev H., Amit M., Gepstein A., et al. Human embryonic stem cells can differentiate into myocytes with structural and functional properties of cardiomyocytes. J Clin Invest 2001, 108:407-414.
14. Zhang M., Methot D., Poppa V., Fujio Y., Walsh K., Murry C.E. Cardiomyocyte grafting for cardiac repair: graft cell death and anti-death strategies. J Mol Cell Cardiol 2001, 33:907-921.
15. Nakamura Y., Yasuda T., Weisel R.D., Li R.K. Enhanced cell transplantation: preventing apoptosis increases cell survival and ventricular function. Am J Physiol Heart Circ Physiol 2006, 291:H939-H947.
16. van Laake L.W., Passier R., den Ouden K., Schreurs C., Monshouwer-Kloots J., Ward-van Oostwaard D., et al. Improvement of mouse cardiac function by hESC-derived cardiomyocytes correlates with vascularity but not graft size. Stem Cell Res 2009, 3:106-112.
17. Shiba Y., Fernandes S., Zhu W.Z., Filice D., Muskheli V., Kim J., et al. Human ES-cell-derived cardiomyocytes electrically couple and suppress arrhythmias in injured hearts. Nature 2012, 489:322-325.
18. Laflamme M.A., Chen K.Y., Naumova A.V., Muskheli V., Fugate J.A., Dupras S.K., et al. Cardiomyocytes derived from human embryonic stem cells in pro-survival factors enhance function of infarcted rat hearts. Nat Biotechnol 2007, 25:1015-1024.
19. Huber I., Itzhaki I., Caspi O., Arbel G., Tzukerman M., Gepstein A., et al. Identification and selection of cardiomyocytes during human embryonic stem cell differentiation. FASEB J 2007, 21:2551-2563.
20. Caspi O., Huber I., Kehat I., Habib M., Arbel G., Gepstein A., et al. Transplantation of human embryonic stem cell-derived cardiomyocytes improves myocardial performance in infarcted rat hearts. J Am Coll Cardiol 2007, 50:1884-1893.
21. Hu X., Yu S.P., Fraser J.L., Lu Z., Ogle M.E., Wang J.A., et al. Transplantation of hypoxia-preconditioned mesenchymal stem cells improves infarcted heart function via enhanced survival of implanted cells and angiogenesis. J Thorac Cardiovasc Surg 2008, 135:799-808.
22. Kutschka I., Kofidis T., Chen I.Y., von Degenfeld G., Zwierzchoniewska M., Hoyt G., et al. Adenoviral human BCL-2 transgene expression attenuates early donor cell death after cardiomyoblast transplantation into ischemic rat hearts. Circulation 2006, 114:I174-I180.
23. Hudson W., Collins M.C., deFreitas D., Sun Y.S., Muller-Borer B., Kypson A.P. Beating and arrested intramyocardial injections are associated with significant mechanical loss: implications for cardiac cell transplantation. J Surg Res 2007, 142:263-267.
24. Teng C.J., Luo J., Chiu R.C., Shum-Tim D. Massive mechanical loss of microspheres with direct intramyocardial injection in the beating heart: implications for cellular cardiomyoplasty. J Thorac Cardiovasc Surg 2006, 132:628-632.
25. Kofidis T., de Bruin J.L., Yamane T., Balsam L.B., Lebl D.R., Swijnenburg R.J., et al. Insulin-like growth factor promotes engraftment, differentiation, and functional improvement after transfer of embryonic stem cells for myocardial restoration. Stem Cells 2004, 22:1239-1245.
26. Ke Q., Yang Y., Rana J.S., Chen Y., Morgan J.P., Xiao Y.F. Embryonic stem cells cultured in biodegradable scaffold repair infarcted myocardium in mice. Sheng Li Xue Bao 2005, 57:673-681.
27. Thomson J.A., Itskovitz-Eldor J., Shapiro S.S., Waknitz M.A., Swiergiel J.J., Marshall V.S., et al. Embryonic stem cell lines derived from human blastocysts. Science 1998, 282:1145-1147.
28. Lee J.E., Kang M.S., Park M.H., Shim S.H., Yoon T.K., Chung H.M., et al. Evaluation of 28 human embryonic stem cell lines for use as unrelated donors in stem cell therapy: implications of HLA and ABO genotypes. Cell Transplant 2010, 19:1383-1395.
29. Xu C., Police S., Rao N., Carpenter M.K. Characterization and enrichment of cardiomyocytes derived from human embryonic stem cells. Circ Res 2002, 91:501-508.
30. Zhang J., Wilson G.F., Soerens A.G., Koonce C.H., Yu J., Palecek S.P., et al. Functional cardiomyocytes derived from human induced pluripotent stem cells. Circ Res 2009, 104:e30-41.
31. Moon S.H., Kim J.S., Park S.J., Lee H.J., Do J.T., Chung H.M. A system for treating ischemic disease using human embryonic stem cell-derived endothelial cells without direct incorporation. Biomaterials 2011, 32:6445-6455.
32. Clausell-Tormos J., Lieber D., Baret J.C., El-Harrak A., Miller O.J., Frenz L., et al. Droplet-based microfluidic platforms for the encapsulation and screening of mammalian cells and multicellular organisms. Chem Biol 2008, 15:427-437.
33. Wold L.E., Dai W., Dow J.S., Kloner R.A. Stem cell therapy in the heart and vasculature. Methods Mol Med 2007, 139:355-365.
34. Kawamoto A., Gwon H.C., Iwaguro H., Yamaguchi J.I., Uchida S., Masuda H., et al. Therapeutic potential of ex vivo expanded endothelial progenitor cells for myocardial ischemia. Circulation 2001, 103:634-637.
35. Hartmann J., Knebel F., Eddicks S., Beling M., Grohmann A., Panda A., et al. Noninvasive monitoring of myocardial function after surgical and cytostatic therapy in a peritoneal metastasis rat model: assessment with tissue Doppler and non-Doppler 2D strain echocardiography. Cardiovasc Ultrasound 2007, 5:23.
36. Gepstein L., Ding C., Rahmutula D., Wilson E.E., Yankelson L., Caspi O., et al. In vivo assessment of the electrophysiological integration and arrhythmogenic risk of myocardial cell transplantation strategies. Stem Cells 2010, 28:2151-2161.
37. Gissel C., Doss M.X., Hippler-Altenburg R., Hescheler J., Sachinidis A. Generation and characterization of cardiomyocytes under serum-free conditions. Methods Mol Biol 2006, 330:191-219.
38. Ahuja P., Sdek P., MacLellan W.R. Cardiac myocyte cell cycle control in development, disease, and regeneration. Physiol Rev 2007, 87:521-544.
39. Anversa P., Leri A., Rota M., Hosoda T., Bearzi C., Urbanek K., et al. Concise review: stem cells, myocardial regeneration, and methodological artifacts. Stem Cells 2007, 25:589-601.
40. van Laake L.W., Passier R., Doevendans P.A., Mummery C.L. Human embryonic stem cell-derived cardiomyocytes and cardiac repair in rodents. Circ Res 2008, 102:1008-1010.
41. Yang L., Soonpaa M.H., Adler E.D., Roepke T.K., Kattman S.J., Kennedy M., et al. Human cardiovascular progenitor cells develop from a KDR+ embryonic-stem-cell-derived population. Nature 2008, 453:524-528.
42. Laflamme M.A., Gold J., Xu C., Hassanipour M., Rosler E., Police S., et al. Formation of human myocardium in the rat heart from human embryonic stem cells. Am J Pathol 2005, 167:663-671.
43. Dai W., Field L.J., Rubart M., Reuter S., Hale S.L., Zweigerdt R., et al. Survival and maturation of human embryonic stem cell-derived cardiomyocytes in rat hearts. J Mol Cell Cardiol 2007, 43:504-516.
44. van Laake L.W., van Donselaar E.G., Monshouwer-Kloots J., Schreurs C., Passier R., Humbel B.M., et al. Extracellular matrix formation after transplantation of human embryonic stem cell-derived cardiomyocytes. Cell Mol Life Sci 2010, 67:277-290.
45. Xu C., Police S., Hassanipour M., Gold J.D. Cardiac bodies: a novel culture method for enrichment of cardiomyocytes derived from human embryonic stem cells. Stem Cells Dev 2006, 15:631-639.
46. Rust W., Balakrishnan T., Zweigerdt R. Cardiomyocyte enrichment from human embryonic stem cell cultures by selection of ALCAM surface expression. Regen Med 2009, 4:225-237.
47. Passier R., Oostwaard D.W., Snapper J., Kloots J., Hassink R.J., Kuijk E., et al. Increased cardiomyocyte differentiation from human embryonic stem cells in serum-free cultures. Stem Cells 2005, 23:772-780.
48. Stevens K.R., Kreutziger K.L., Dupras S.K., Korte F.S., Regnier M., Muskheli V., et al. Physiological function and transplantation of scaffold-free and vascularized human cardiac muscle tissue. Proc Natl Acad Sci U S A 2009, 106:16568-16573.
49. Korff T., Kimmina S., Martiny-Baron G., Augustin H.G. Blood vessel maturation in a 3-dimensional spheroidal coculture model: direct contact with smooth muscle cells regulates endothelial cell quiescence and abrogates VEGF responsiveness. FASEB J 2001, 15:447-457.
50. Gaedtke L., Thoenes L., Culmsee C., Mayer B., Wagner E. Proteomic analysis reveals differences in protein expression in spheroid versus monolayer cultures of low-passage colon carcinoma cells. J Proteome Res 2007, 6:4111-4118.
51. Kehat I., Khimovich L., Caspi O., Gepstein A., Shofti R., Arbel G., et al. Electromechanical integration of cardiomyocytes derived from human embryonic stem cells. Nat Biotechnol 2004, 22:1282-1289.