Development of a scalable suspension culture for cardiac differentiation from human pluripotent stem cells

Stem Cell Research

Volumn 15, Issue 2, 2015, Pages 365-375

  Chen, Vincent C ^a   Ye, Jingjing ^a   Shukla, Praveen ^a,b   Hua, Giau ^a   Chen, Danlin ^a   Lin, Ziguang ^a   Liu, Jian chang ^a   Chai, Jing ^a   Gold, Joseph ^b   Wu, Joseph ^b   Hsu, David ^a   Couture, Larry A ^a  

^a CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cardiomyocyte differentiation; GMP; Human pluripotent stem cells; Suspension cell cultures

Indexed keywords

WNT PROTEIN; ACTININ; RNA; TROPONIN I; TROPONIN T;

ARTICLE; CELL AGGREGATION; CELL DIFFERENTIATION; CELL KINETICS; CELL SIZE; CONTROLLED STUDY; CRYOPRESERVATION; FLOW CYTOMETRY; HEART MUSCLE CELL; HUMAN; HUMAN CELL; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; SUSPENSION CELL CULTURE; CARDIAC MUSCLE CELL; CELL CULTURE TECHNIQUE; CELL LINE; CHEMISTRY; CYTOLOGY; FLUORESCENCE MICROSCOPY; GENE EXPRESSION REGULATION; ISOLATION AND PURIFICATION; METABOLISM; SEQUENCE ANALYSIS; WNT SIGNALING PATHWAY;

ACTININ; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL LINE; GENE EXPRESSION REGULATION; HUMANS; MICROSCOPY, FLUORESCENCE; MYOCYTES, CARDIAC; PLURIPOTENT STEM CELLS; RNA; SEQUENCE ANALYSIS, RNA; TROPONIN I; TROPONIN T; WNT SIGNALING PATHWAY;

EID: 84940101302     PISSN: 18735061     EISSN: 18767753     Source Type: Journal    
DOI: 10.1016/j.scr.2015.08.002     Document Type: Article

References (35)

1. Amit M., et al. Suspension culture of undifferentiated human embryonic and induced pluripotent stem cells. Stem Cell Rev. 2010, 6:248-259.
2. Ardehali R., et al. Prospective isolation of human embryonic stem cell-derived cardiovascular progenitors that integrate into human fetal heart tissue. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:3405-3410.
3. Arnold S.J., Robertson E.J. Making a commitment: cell lineage allocation and axis patterning in the early mouse embryo. Nat. Rev. Mol. Cell Biol. 2009, 10:91-103.
4. Bauwens C.L., et al. Control of human embryonic stem cell colony and aggregate size heterogeneity influences differentiation trajectories. Stem Cells 2008, 26:2300-2310.
5. Buckingham M., Meilhac S., Zaffran S. Building the mammalian heart from two sources of myocardial cells. Nat. Rev. Genet. 2005, 6:826-835.
6. 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 2012, 10:16-28.
7. Burridge P.W., et al. Chemically defined generation of human cardiomyocytes. Nat. Methods 2014, 11:855-860.
8. Chen V.C., et al. Scalable GMP compliant suspension culture system for human ES cells. Stem Cell Res. 2012, 8:388-402.
9. Chong J.J., et al. Human embryonic-stem-cell-derived cardiomyocytes regenerate non-human primate hearts. Nature 2014, 510:273-277.
10. David R., et al. MesP1 drives vertebrate cardiovascular differentiation through Dkk-1-mediated blockade of Wnt-signalling. Nat. Cell Biol. 2008, 10:338-345.
11. Drukker M., et al. Isolation of primitive endoderm, mesoderm, vascular endothelial and trophoblast progenitors from human pluripotent stem cells. Nat. Biotechnol. 2012, 30:531-542.
12. Geuss L.R., Suggs L.J. Making cardiomyocytes: how mechanical stimulation can influence differentiation of pluripotent stem cells. Biotechnol. Prog. 2013, 29:1089-1096.
13. Kalmbach A., et al. Experimental characterization of flow conditions in 2-and 20-L bioreactors with wave-induced motion. Biotechnol. Prog. 2011, 27:402-409.
14. Kattman S.J., 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.
15. Kempf H., et al. Controlling expansion and cardiomyogenic differentiation of human pluripotent stem cells in scalable suspension culture. Stem Cell Rep. 2014, 3:1132-1146.
16. Krawetz R., et al. Large-scale expansion of pluripotent human embryonic stem cells in stirred-suspension bioreactors. Tissue Eng. 2010, 16:573-582.
17. Laflamme M.A., Murry C.E. Regenerating the heart. Nat. Biotechnol. 2005, 23:845-856.
18. Leamy A.W., Shukla P., McAlexander M.A., Carr M.J., Ghatta S. Curcumin ((E, E)-1,7-bis(4-hydroxy-3-methoxyphenyl)-1,6-heptadiene-3,5-dione) activates and desensitizes the nociceptor ion channel TRPA1. Neurosci. Lett. 2011, 503:157-162.
19. Lian X., et al. Robust cardiomyocyte differentiation from human pluripotent stem cells via temporal modulation of canonical Wnt signaling. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:E1848-E1857.
20. Naito A.T., et al. Developmental stage-specific biphasic roles of Wnt/beta-catenin signaling in cardiomyogenesis and hematopoiesis. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:19812-19817.
21. Ng S.Y., Wong C.K., Tsang S.Y. Differential gene expressions in atrial and ventricular myocytes: insights into the road of applying embryonic stem cell-derived cardiomyocytes for future therapies. Am. J. Physiol. Cell Physiol. 2010, 299:C1234-C1249.
22. Niebruegge S., 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.
23. Olmer R., et al. Long term expansion of undifferentiated human iPS and ES cells in suspension culture using a defined medium. Stem Cell Res. 2010, 5:51-64.
24. Oncul A.A., Kalmbach A., Genzel Y., Reichl U., Thevenin D. Characterization of flow conditions in 2L and 20L wave bioreactors (R) using computational fluid dynamics. Biotechnol. Prog. 2010, 26:101-110.
25. Shafa M., et al. Impact of stirred suspension bioreactor culture on the differentiation of murine embryonic stem cells into cardiomyocytes. BMC Cell Biol. 2011, 12:53.
26. Shukla P., et al. Maternal nutrient restriction during pregnancy impairs an endothelium-derived hyperpolarizing factor-like pathway in sheep fetal coronary arteries. Am. J. Physiol. Heart Circ. Physiol. 2014, 307:H134-H142.
27. Singh V. Disposable bioreactor for cell culture using wave-induced agitation. Cytotechnology 1999, 30:149-158.
28. Singh H., Mok P., Balakrishnan T., Rahmat S.N., Zweigerdt R. Up-scaling single cell-inoculated suspension culture of human embryonic stem cells. Stem Cell Res. 2010, 4:165-179.
29. Steiner D., et al. Derivation, propagation and controlled differentiation of human embryonic stem cells in suspension. Nat. Biotechnol. 2010, 28:361-364.
30. Tam P.P., Loebel D.A. Gene function in mouse embryogenesis: get set for gastrulation. Nat. Rev. Genet. 2007, 8:368-381.
31. Ting S., Chen A., Reuveny S., Oh S. An intermittent rocking platform for integrated expansion and differentiation of human pluripotent stem cells to cardiomyocytes in suspended microcarrier cultures. Stem Cell Res. 2014, 13:202-213.
32. Ueno S., et al. Biphasic role for Wnt/beta-catenin signaling in cardiac specification in zebrafish and embryonic stem cells. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:9685-9690.
33. Yang L., et al. Human cardiovascular progenitor cells develop from a KDR+ embryonic-stem-cell-derived population. Nature 2008, 453:524-528.
34. Zhang J., et al. Extracellular matrix promotes highly efficient cardiac differentiation of human pluripotent stem cells: the matrix sandwich method. Circ. Res. 2012, 111:1125-1136.
35. Zhu W.Z., Van Biber B., Laflamme M.A. Methods for the derivation and use of cardiomyocytes from human pluripotent stem cells. Methods Mol. Biol. 2011, 767:419-431.