Enhanced engraftment, proliferation, and therapeutic potential in heart using optimized human iPSC-derived cardiomyocytes

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Funakoshi, Shunsuke ^a,b   Miki, Kenji ^a   Takaki, Tadashi ^a   Okubo, Chikako ^a   Hatani, Takeshi ^a,b   Chonabayashi, Kazuhisa ^a   Nishikawa, Misato ^a   Takei, Ikue ^a   Oishi, Akiko ^a   Narita, Megumi ^a   Hoshijima, Masahiko ^c   Kimura, Takeshi ^b   Yamanaka, Shinya ^a,d   Yoshida, Yoshinori ^a  

^a KYOTO UNIVERSITY   (Japan)

^b KYOTO UNIVERSITY HOSPITAL   (Japan)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^d GLADSTONE INSTITUTE OF CARDIOVASCULAR DISEASE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; KI 67 ANTIGEN; MKI67 PROTEIN, MOUSE;

ANIMAL; BIOLOGICAL THERAPY; CARDIAC MUSCLE CELL; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL TRACKING; CYTOLOGY; FLUORESCENCE IMAGING; GENE EXPRESSION; GENETICS; GRAFT SURVIVAL; HUMAN; IMMUNOLOGY; INDUCED PLURIPOTENT STEM CELL; MALE; METABOLISM; MOUSE; MYOCARDIAL INFARCTION; NONOBESE DIABETIC MOUSE; PATHOLOGY; PHYSIOLOGY; PROCEDURES; TRANSPLANTATION;

ANIMALS; BIOMARKERS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL TRACKING; CELL- AND TISSUE-BASED THERAPY; GENE EXPRESSION; GRAFT SURVIVAL; HUMANS; INDUCED PLURIPOTENT STEM CELLS; KI-67 ANTIGEN; MALE; MICE; MICE, INBRED NOD; MYOCARDIAL INFARCTION; MYOCYTES, CARDIAC; OPTICAL IMAGING;

EID: 84953897607     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep19111     Document Type: Article

References (49)

1. Stehlik, J. et al. The Registry of the International Society for Heart and Lung Transplantation: Twenty-eighth Adult Heart Transplant Report-2011. The Journal of heart and lung transplantation: the official publication of the International Society for Heart Transplantation 30, 1078-1094 (2011).
2. Ptaszek, L. M., Mansour, M., Ruskin, J. N. & Chien, K. R. Towards regenerative therapy for cardiac disease. Lancet 379, 933-942 (2012).
3. Malliaras, K. et al. Intracoronary cardiosphere-derived cells after myocardial infarction: evidence of therapeutic regeneration in the final 1-year results of the CADUCEUS trial (CArdiosphere-Derived aUtologous stem CElls to reverse ventricUlar dySfunction). Journal of the American College of Cardiology 63, 110-122 (2014).
4. Schachinger, V. et al. Intracoronary bone marrow-derived progenitor cells in acute myocardial infarction. N Engl J Med 355, 1210-1221 (2006).
5. Tendera, M. et al. Intracoronary infusion of bone marrow-derived selected CD34+CXCR4+ cells and non-selected mononuclear cells in patients with acute STEMI and reduced left ventricular ejection fraction: results of randomized, multicentre Myocardial Regeneration by Intracoronary Infusion of Selected Population of Stem Cells in Acute Myocardial Infarction (REGENT) Trial. Eur Heart J 30, 1313-1321 (2009).
6. Takahashi, K. et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131, 861-872 (2007).
7. Thomson, J. A. et al. Embryonic stem cell lines derived from human blastocysts. Science 282, 1145-1147 (1998).
8. Yoshida, Y. & Yamanaka, S. Recent stem cell advances: induced pluripotent stem cells for disease modeling and stem cell-based regeneration. Circulation 122, 80-87 (2010).
9. Chong, J. J. et al. Human embryonic-stem-cell-derived cardiomyocytes regenerate non-human primate hearts. Nature 510, 273-277 (2014).
10. Laflamme, M. A. et al. Cardiomyocytes derived from human embryonic stem cells in pro-survival factors enhance function of infarcted rat hearts. Nat Biotechnol 25, 1015-1024 (2007).
11. Caspi, O. et al. Transplantation of human embryonic stem cell-derived cardiomyocytes improves myocardial performance in infarcted rat hearts. Journal of the American College of Cardiology 50, 1884-1893 (2007).
12. 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, 810-834 (2013).
13. Behfar, A., Crespo-Diaz, R., Terzic, A. & Gersh, B. J. Cell therapy for cardiac repair-lessons from clinical trials. Nat Rev Cardiol 11, 232-246 (2014).
14. Yang, L. et al. Human cardiovascular progenitor cells develop from a KDR+ embryonic-stem-cell-derived population. Nature 453, 524-528 (2008).
15. Burridge, P. W., Keller, G., Gold, J. D. & Wu, J. C. Production of de novo cardiomyocytes: human pluripotent stem cell differentiation and direct reprogramming. Cell Stem Cell 10, 16-28 (2012).
16. Ito, M. et al. NOD/SCID/gamma(c)(null) mouse: an excellent recipient mouse model for engraftment of human cells. Blood 100, 3175-3182 (2002).
17. Li, Z. et al. Differentiation, survival, and function of embryonic stem cell derived endothelial cells for ischemic heart disease. Circulation 116, I46-54 (2007).
18. van der Bogt, K. E. et al. Comparison of different adult stem cell types for treatment of myocardial ischemia. Circulation 118, S121-129 (2008).
19. Nguyen, P. K., Lan, F., Wang, Y. & Wu, J. C. Imaging: guiding the clinical translation of cardiac stem cell therapy. Circ Res 109, 962-979 (2011).
20. 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 102, 1008-1010 (2008).
21. Schmid, G. & Pfitzer, P. Mitoses and binucleated cells in perinatal human hearts. Virchows Archiv. B, Cell pathology including molecular pathology 48, 59-67 (1985).
22. Olivetti, G. et al. Aging, cardiac hypertrophy and ischemic cardiomyopathy do not affect the proportion of mononucleated and multinucleated myocytes in the human heart. J Mol Cell Cardiol 28, 1463-1477 (1996).
23. Okita, K. et al. A more efficient method to generate integration-free human iPS cells. Nat Methods 8, 409-412 (2011).
24. Okita, K. et al. An efficient nonviral method to generate integration-free human-induced pluripotent stem cells from cord blood and peripheral blood cells. Stem Cells 31, 458-466 (2013).
25. Dubois, N. C. et al. SIRPA is a specific cell-surface marker for isolating cardiomyocytes derived from human pluripotent stem cells. Nat Biotechnol 29, 1011-1018 (2011).
26. Dow, J., Simkhovich, B. Z., Kedes, L. & Kloner, R. A. Washout of transplanted cells from the heart: a potential new hurdle for cell transplantation therapy. Cardiovasc Res 67, 301-307 (2005).
27. Laflamme, M. A. et al. Formation of human myocardium in the rat heart from human embryonic stem cells. Am J Pathol 167, 663-671 (2005).
28. Porrello, E. R. et al. Transient regenerative potential of the neonatal mouse heart. Science 331, 1078-1080 (2011).
29. Poolman, R. A. & Brooks, G. Expressions and activities of cell cycle regulatory molecules during the transition from myocyte hyperplasia to hypertrophy. J Mol Cell Cardiol 30, 2121-2135 (1998).
30. Bicknell, K. A., Coxon, C. H. & Brooks, G. Can the cardiomyocyte cell cycle be reprogrammed? J Mol Cell Cardiol 42, 706-721 (2007).
31. Canseco, D. C. et al. Human ventricular unloading induces cardiomyocyte proliferation. Journal of the American College of Cardiology 65, 892-900 (2015).
32. Puente, B. N. et al. The oxygen-rich postnatal environment induces cardiomyocyte cell-cycle arrest through DNA damage response. Cell 157, 565-579 (2014).
33. Vandervelde, S. et al. Stem cell-related cardiac gene expression early after murine myocardial infarction. Cardiovasc Res 73, 783-793 (2007).
34. Vandervelde, S., van Luyn, M. J., Tio, R. A. & Harmsen, M. C. Signaling factors in stem cell-mediated repair of infarcted myocardium. J Mol Cell Cardiol 39, 363-376 (2005).
35. Stanton, L. W. et al. Altered patterns of gene expression in response to myocardial infarction. Circ Res 86, 939-945 (2000).
36. McDevitt, T. C., Laflamme, M. A. & Murry, C. E. Proliferation of cardiomyocytes derived from human embryonic stem cells is mediated via the IGF/PI 3-kinase/Akt signaling pathway. J Mol Cell Cardiol 39, 865-873 (2005).
37. Kuhn, B. et al. Periostin induces proliferation of differentiated cardiomyocytes and promotes cardiac repair. Nature medicine 13, 962-969 (2007).
38. Yang, X., Pabon, L. & Murry, C. E. Engineering adolescence: maturation of human pluripotent stem cell-derived cardiomyocytes. Circ Res 114, 511-523 (2014).
39. Kim, D. H. et al. Nanoscale cues regulate the structure and function of macroscopic cardiac tissue constructs. Proc Natl Acad Sci USA 107, 565-570 (2010).
40. van Laake, L. W. et al. Human embryonic stem cell-derived cardiomyocytes survive and mature in the mouse heart and transiently improve function after myocardial infarction. Stem Cell Res 1, 9-24 (2007).
41. Swijnenburg, R. J. et al. Immunosuppressive therapy mitigates immunological rejection of human embryonic stem cell xenografts. Proc Natl Acad Sci USA 105, 12991-12996 (2008).
42. Pearl, J. I. et al. Short-term immunosuppression promotes engraftment of embryonic and induced pluripotent stem cells. Cell Stem Cell 8, 309-317 (2011).
43. Ong, S. G. et al. Microfluidic Single-Cell Analysis of Transplanted Human Induced Pluripotent Stem Cell-Derived Cardiomyocytes After Acute Myocardial Infarction. Circulation 132, 762-771 (2015).
44. Kawamura, M. et al. Enhanced survival of transplanted human induced pluripotent stem cell-derived cardiomyocytes by the combination of cell sheets with the pedicled omental flap technique in a porcine heart. Circulation 128, S87-94 (2013).
45. Masumoto, H. et al. Pluripotent stem cell-engineered cell sheets reassembled with defined cardiovascular populations ameliorate reduction in infarct heart function through cardiomyocyte-mediated neovascularization. Stem Cells 30, 1196-1205 (2012).
46. Miki, K. et al. Efficient Detection and Purification of Cell Populations Using Synthetic MicroRNA Switches. Cell Stem Cell 16, 699-711 (2015).
47. Tanaka, A. et al. Efficient and reproducible myogenic differentiation from human iPS cells: prospects for modeling Miyoshi Myopathy in vitro. PLoS ONE 8, e61540 (2013).
48. Woltjen, K. et al. piggyBac transposition reprograms fibroblasts to induced pluripotent stem cells. Nature 458, 766-770 (2009).
49. Hayashi, T. et al. Three-dimensional electron microscopy reveals new details of membrane systems for Ca2+ signaling in the heart. J Cell Sci 122, 1005-1013 (2009).