Amassive suspensionculturesystemwithmetabolic purification for human pluripotent stem cell-derived cardiomyocytes

Stem Cells Translational Medicine

Volumn 3, Issue 12, 2014, Pages 1473-1483

  Hemmi, Natsuko ^a   Tohyama, Shugo ^a,b   Nakajima, Kazuaki ^a   Kanazawa, Hideaki ^a   Suzuki, Tomoyuki ^c   Hattori, Fumiyuki ^a   Seki, Tomohisa ^a   Kishino, Yoshikazu ^a   Hirano, Akinori ^a   Okada, Marina ^a   Tabei, Ryota ^a   Ohno, Rei ^a   Fujita, Chihana ^a   Haruna, Tomoko ^a   Yuasa, Shinsuke ^a   Sano, Motoaki ^a   Fujita, Jun ^a   Fukuda, Keiichi ^a  

^a KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b JAPAN SOCIETY FOR THE PROMOTION OF SCIENCE   (Japan)

^c NAGOYA UNIVERSITY   (Japan)

Author keywords

Cardiac; Cell culture; Cellular therapy; Differentiation; Embryonic stem cells; Induced pluripotent stem cells; Stem cell transplantation

Indexed keywords

ALPHA ACTININ; CALCIUM; LIPOCORTIN 5; MYOSIN LIGHT CHAIN; OCTAMER TRANSCRIPTION FACTOR 4; ORGANIC CATION TRANSPORTER 3; PROPIDIUM IODIDE; TRA 1 60 ANTIBODY; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NKX2.5; TROPONIN T; UNCLASSIFIED DRUG; DIFFERENTIATION ANTIGEN;

ACTION POTENTIAL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELL METABOLISM; CELL SEPARATION; COLONY FORMATION; CONFOCAL LASER MICROSCOPY; CULTURE MEDIUM; ELECTROPHYSIOLOGY; EMBRYOID BODY; EMBRYONIC STEM CELL; FLUORESCENCE ACTIVATED CELL SORTING; HEART MUSCLE CELL; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; IMMUNOFLUORESCENCE; MALE; MASSIVE SUSPENSION CULTURE SYSTEM; MOUSE; NONHUMAN; PLURIPOTENT STEM CELL; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WHOLE CELL PATCH CLAMP; ANIMAL; CULTURE TECHNIQUE; CYTOLOGY; METABOLISM; NONOBESE DIABETIC MOUSE; PROCEDURES; SCID MOUSE;

ANIMALS; ANTIGENS, DIFFERENTIATION; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL SEPARATION; HUMANS; MICE; MICE, INBRED NOD; MICE, SCID; MYOCYTES, CARDIAC; PLURIPOTENT STEM CELLS;

EID: 84913525381     PISSN: 21576564     EISSN: 21576580     Source Type: Journal    
DOI: 10.5966/sctm.2014-0072     Document Type: Article

References (37)

1. Writing Committee Members, Yancy CW, Jessup M et al. 2013 ACCF/AHA guideline for the management of heart failure: A report of the American College of Cardiology Foundation/American Heart Association Task Force on practice guidelines. Circulation 2013;128:e240–e327.
2. Stehlik J, Edwards LB, Kucheryavaya AY et al. The Registry of the International Society for Heart and Lung Transplantation: 29th Official adult heart transplantreport—2012. JHeart Lung Transplant 2012;31:1052–1064.
3. Thomson JA, Itskovitz-Eldor J, Shapiro SS et al. Embryonicstem cell lines derived from human blastocysts. Science 1998;282:1145–1147.
4. Takahashi K, Tanabe K, Ohnuki M et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007; 131:861–872.
5. 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.
6. Gruen L, Grabel L. Concise review: Scientific and ethical roadblocks to human embryonic stem cell therapy. Stem Cells 2006;24:2162–2169.
7. Kattman SJ, Witty AD, Gagliardi M et al. Stage-specific optimization of activin/nodal and BMP signaling promotes cardiac differentiation of mouse and human pluripotent stem cell lines. Cell Stem Cell 2011;8:228–240.
8. Shafa M, Day B, Yamashita A et al. Derivation of iPSCs in stirred suspension bioreactors. Nat Methods 2012;9:465–466.
9. Olmer R, Lange A, Selzer S et al. Suspension culture of human pluripotent stem cells in controlled, stirred bioreactors. Tissue Eng Part C Methods 2012;18:772–784.
10. Jing D, Parikh A, Tzanakakis ES. Cardiac cell generation from encapsulated embryonic stem cellsinstatic and scalable culture systems. Cell Transplant 2010;19:1397–1412.
11. Niebruegge S, Nehring A, Bär H et al. Car-diomyocyte production in mass suspension culture: Embryonic stem cells as a source for great amounts of functional cardiomyocytes. Tissue Eng Part A 2008;14:1591–1601.
12. Shafa M, Krawetz R, Zhang Y et al. Impact of stirred suspension bioreactor culture on the differentiation of murine embryonic stem cells into cardiomyocytes. BMC Cell Biol 2011;12:53.
13. Niebruegge S, Bauwens CL, Peerani R et al. Generation of human embryonic stem cell-derived mesoderm and cardiac cells using size-specified aggregates in an oxygen-controlled bioreactor. Biotechnol Bioeng 2009;102:493–507.
14. Yirme G, Amit M, Laevsky I et al. Establishing a dynamic process for the formation, propagation, and differentiation of human embryoid bodies. Stem Cells Dev 2008;17: 1227–1241.
15. Gerecht-Nir S, Cohen S, Itskovitz-Eldor J. Bioreactor cultivation enhances the efficiency of human embryoid body (hEB) formation and differentiation. Biotechnol Bioeng 2004;86: 493–502.
16. Schroeder M, Niebruegge S, Werner A et al. Differentiation and lineage selection of mouse embryonic stem cells in a stirred bench scale bioreactor with automated process control. Biotechnol Bioeng 2005;92:920–933.
17. Miura K, Okada Y, Aoi T et al. Variation in thesafetyofinducedpluripotentstem cell lines. Nat Biotechnol 2009;27:743–745.
18. Hattori F, Chen H, Yamashita H et al. Non-genetic method for purifying stem cell-derived cardiomyocytes. Nat Methods 2010;7:61–66.
19. Dubois NC, Craft AM, Sharma P et al. SIRPA is a specific cell-surface marker for isolating cardi-omyocytes derived from human pluripotent stem cells. Nat Biotechnol 2011;29:1011–1018.
20. Anderson D, Self T, Mellor IR et al. Trans-genic enrichment of cardiomyocytes from human embryonic stem cells. Mol Ther 2007;15: 2027–2036.
21. Elliott DA, Braam SR, Koutsis K et al. NKX2-5(eGFP/w) hESCs for isolation of human cardiac progenitors and cardiomyocytes. Nat Methods 2011;8:1037–1040.
22. Tohyama S, Hattori F, Sano M et al. Distinct metabolic flow enables large-scale purification of mouse and human pluripotent stem cell-derived cardiomyocytes. Cell Stem Cell 2013;12:127–137.
23. Yuasa S, Itabashi Y, Koshimizu U et al. Transient inhibition of BMP signaling by Noggin induces cardiomyocyte differentiation of mouse embryonic stem cells. Nat Biotechnol 2005;23:607–611.
24. Tanaka T, Tohyama S, Murata M et al. In vitro pharmacologic testing using human induced pluripotent stem cell-derived cardio-myocytes. Biochem Biophys Res Commun 2009;385:497–502.
25. Zwi L, Caspi O, Arbel G et al. Cardiomyocyte differentiation of human induced pluripotent stem cells. Circulation 2009;120:1513–1523.
26. Takahashi T, Lord B, Schulze PC et al. Ascorbic acid enhances differentiation of embryonic stem cells into cardiac myocytes. Circulation 2003;107:1912–1916.
27. Willems E, Spiering S, Davidovics H et al. Small-molecule inhibitors of the Wnt pathway potently promote cardiomyocytes from human embryonic stem cell-derived mesoderm. Circ Res 2011;109:360–364.
28. Vermes I, Haanen C, Steffens-Nakken H et al. Anovel assay for apoptosis: Flow cytomet-ric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labelled annexin V. J Immunol Methods 1995; 184:39–51.
29. Chen VC, Couture SM, Ye J et al. Scalable GMP compliant suspension culture system for human ES cells. Stem Cell Res (Amst) 2012;8: 388–402.
30. Osafune K, Caron L, Borowiak M et al. Marked differences in differentiation propensity among human embryonic stem cell lines. Nat Biotechnol 2008;26:313–315.
31. Holtzinger A, Rosenfeld GE, Evans T. Gata4 directs development of cardiac-inducing endoderm from ES cells. Dev Biol 2010; 337:63–73.
32. Mummery CL, Zhang J, Ng ES et al. Differ-entiationof human embryonic stem cells and induced pluripotent stem cells tocardiomyocytes: A methods overview. Circ Res 2012;111:344–358.
33. Matsuura K, Wada M, Shimizu T et al. Creation of human cardiac cell sheets using plu-ripotent stem cells. Biochem Biophys Res Com-mun 2012;425:321–327.
34. Shiba Y, Fernandes S, Zhu WZ et al. Human ES-cell-derived cardiomyocytes electrically couple and suppress arrhythmias in injured hearts. Nature 2012;489:322–325.
35. Chong JJ, Yang X, Don CW et al. Human embryonic-stem-cell-derived cardiomyocytes regenerate non-human primate hearts. Nature 2014;510:273–277.
36. Thompson SA, Burridge PW, Lipke EA et al. Engraftment of human embryonic stem cell derived cardiomyocytes improves conduction in an arrhythmogenic in vitro model. J Mol Cell Cardiol 2012;53:15–23.
37. Thompson SA, Copeland CR, Reich DH et al. Mechanical coupling between myofibro-blasts and cardiomyocytes slows electric conduction in fibrotic cell monolayers. Circulation 2011;123:2083–2093.