Chemically defned generation of human cardiomyocytes

Nature Methods

Volumn 11, Issue 8, 2014, Pages 855-860

  Burridge, Paul W ^a   Matsa, Elena ^a   Shukla, Praveen ^a   Lin, Ziliang C ^a   Churko, Jared M ^a   Ebert, Antje D ^a   Lan, Feng ^a   Diecke, Sebastian ^a   Huber, Bruno ^a   Mordwinkin, Nicholas M ^a   Plews, Jordan R ^a   Abilez, Oscar J ^a   Cui, Bianxiao ^a   Gold, Joseph D ^a   Wu, Joseph C ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA ACTININ; ASCORBIC ACID; BOVINE SERUM ALBUMIN; PHOSPHATE; RECOMBINANT HUMAN SERUM ALBUMIN; TROPONIN T; VITRONECTIN;

ARTICLE; CELL DIFFERENTIATION; CELL METABOLISM; CELL SPECIFICITY; CONTROLLED STUDY; CULTURE MEDIUM; FLOW CYTOMETRY; HEART MUSCLE CELL; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE MICROSCOPY; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; CYTOLOGY;

CELL DIFFERENTIATION; CULTURE MEDIA; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MYOCYTES, CARDIAC;

EID: 84905242471     PISSN: 15487091     EISSN: 15487105     Source Type: Journal    
DOI: 10.1038/nMeth.2999     Document Type: Article

References (49)

1. Matsa, E., Burridge, P.W. & Wu, J.C. Human stem cells for modeling heart disease and for drug discovery. Sci. Transl. Med. 239, 239ps6 (2014).
2. Burridge, P.W. et al. A universal system for highly effcient cardiac differentiation of human induced pluripotent stem cells that eliminates interline variability. PLoS One 6, e18293 (2011).
3. Kattman, S.J. et al. Stage-specifc optimization of activin/nodal and BMP signaling promotes cardiac differentiation of mouse and human pluripotent stem cell lines. Cell Stem Cell 8, 228-240 (2011).
4. 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).
5. Zhang, J. et al. Extracellular matrix promotes highly effcient cardiac differentiation of human pluripotent stem cells: the matrix sandwich method. Circ. Res. 111, 1125-1136 (2012).
6. Lian, X. et al. Robust cardiomyocyte differentiation from human pluripotent stem cells via temporal modulation of canonical Wnt signaling. Proc. Natl. Acad. Sci. USA 109, E1848-E1857 (2012).
7. Burridge, P.W. et al. Improved human embryonic stem cell embryoid body homogeneity and cardiomyocyte differentiation from a novel V-96 plate aggregation system highlights interline variability. Stem Cells 25, 929-938 (2007).
8. Yang, L. et al. Human cardiovascular progenitor cells develop from a KDR+ embryonic-stem-cell-derived population. Nature 453, 524-528 (2008).
9. Elliott, D.A. et al. NKX2-5(eGFP/w) hESCs for isolation of human cardiac progenitors and cardiomyocytes. Nat. Methods 8, 1037-1040 (2011).
10. Lafamme, 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. Willems, E. et al. Small molecule-mediated TGF-beta type II receptor degradation promotes cardiomyogenesis in embryonic stem cells. Cell Stem Cell 11, 242-252 (2012).
12. Titmarsh, D.M. et al. Microbioreactor arrays for full factorial screening of exogenous and paracrine factors in human embryonic stem cell differentiation. PLoS One 7, e52405 (2012).
13. Moore, G.E., Gerner, R.E. & Franklin, H.A. Culture of normal human leukocytes. J. Am. Med. Assoc. 199, 519-524 (1967).
14. Brewer, G.J. & Cotman, C.W. Survival and growth of hippocampal neurons in defned medium at low density: advantages of a sandwich culture technique or low oxygen. Brain Res. 494, 65-74 (1989).
15. Uosaki, H. et al. Effcient and scalable purifcation of cardiomyocytes from human embryonic and induced pluripotent stem cells by VCAM1 surface expression. PLoS One 6, e23657 (2011).
16. Carpenter, L. et al. Effcient differentiation of human induced pluripotent stem cells generates cardiac cells that provide protection following myocardial infarction in the rat. Stem Cells Dev. 21, 977-986 (2012).
17. Graichen, R. et al. Enhanced cardiomyogenesis of human embryonic stem cells by a small molecular inhibitor of p38 MAPK. Differentiation 76, 357-370 (2008).
18. Melkoumian, Z. et al. Synthetic peptide-acrylate surfaces for long-term self-renewal and cardiomyocyte differentiation of human embryonic stem cells. Nat. Biotechnol. 28, 606-610 (2010).
19. Nagaoka, M., Si-Tayeb, K., Akaike, T. & Duncan, S.A. Culture of human pluripotent stem cells using completely defned conditions on a recombinant E-cadherin substratum. BMC Dev. Biol. 10, 60 (2010).
20. Braam, S.R. et al. Recombinant vitronectin is a functionally defned substrate that supports human embryonic stem cell self-renewal via alphavbeta5 integrin. Stem Cells 26, 2257-2265 (2008).
21. Rodin, S. et al. Clonal culturing of human embryonic stem cells on laminin-521/E-cadherin matrix in defned and xeno-free environment. Nat. Commun. 5, 3195 (2014).
22. Rodin, S. et al. Long-term self-renewal of human pluripotent stem cells on human recombinant laminin-511. Nat. Biotechnol. 28, 611-615 (2010).
23. Miyazaki, T. et al. Laminin E8 fragments support effcient adhesion and expansion of dissociated human pluripotent stem cells. Nat. Commun. 3, 1236 (2012).
24. Domogatskaya, A., Rodin, S. & Tryggvason, K. Functional diversity of laminins. Annu. Rev. Cell Dev. Biol. 28, 523-553 (2012).
25. Tohyama, S. et al. Distinct metabolic fow enables large-scale purifcation of mouse and human pluripotent stem cell-derived cardiomyocytes. Cell Stem Cell 12, 127-137 (2013).
26. Paige, S.L. et al. Endogenous Wnt/beta-catenin signaling is required for cardiac differentiation in human embryonic stem cells. PLoS One 5, e11134 (2010).
27. Martin, A.F. Turnover of cardiac troponin subunits. Kinetic evidence for a precursor pool of troponin-I. J. Biol. Chem. 256, 964-968 (1981).
28. 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. 299, C1234-C1249 (2010).
29. Minami, I. et al. A small molecule that promotes cardiac differentiation of human pluripotent stem cells under defned, cytokine-and xeno-free conditions. Cell Reports 2, 1448-1460 (2012).
30. Chuva de Sousa Lopes, S.M. et al. Patterning the heart, a template for human cardiomyocyte development. Dev. Dyn. 235, 1994-2002 (2006).
31. Bird, S.D. et al. The human adult cardiomyocyte phenotype. Cardiovasc. Res. 58, 423-434 (2003).
32. Xie, C., Lin, Z., Hanson, L., Cui, Y. & Cui, B. Intracellular recording of action potentials by nanopillar electroporation. Nat. Nanotechnol. 7, 185-190 (2012).
33. Francis, G.L. Albumin and mammalian cell culture: implications for biotechnology applications. Cytotechnology 62, 1-16 (2010).
34. Takahashi, T. et al. Ascorbic acid enhances differentiation of embryonic stem cells into cardiac myocytes. Circulation 107, 1912-1916 (2003).
35. Cao, N. et al. Ascorbic acid enhances the cardiac differentiation of induced pluripotent stem cells through promoting the proliferation of cardiac progenitor cells. Cell Res. 22, 219-236 (2012).
36. Blaschke, K. et al. Vitamin C induces Tet-dependent DNA demethylation and a blastocyst-like state in ES cells. Nature 500, 222-226 (2013).
37. Moyes, K.W. et al. Human embryonic stem cell-derived cardiomyocytes migrate in response to gradients of fbronectin and Wnt5a. Stem Cells Dev. 22, 2315-2325 (2013).
38. Tribulova, N. et al. Enhanced connexin-43 and alpha-sarcomeric actin expression in cultured heart myocytes exposed to triiodo-L-thyronine. J. Mol. Histol. 35, 463-470 (2004).
39. Wang, B., Ouyang, J. & Xia, Z. Effects of triiodo-thyronine on angiotensin-induced cardiomyocyte hypertrophy: reversal of increased beta-myosin heavy chain gene expression. Can. J. Physiol. Pharmacol. 84, 935-941 (2006).
40. Zhang, Q. et al. Direct differentiation of atrial and ventricular myocytes from human embryonic stem cells by alternating retinoid signals. Cell Res. 21, 579-587 (2011).
41. Chen, G. et al. Chemically defned conditions for human iPSC derivation and culture. Nat. Methods 8, 424-429 (2011).
42. Yap, L.Y. et al. Defning a threshold surface density of vitronectin for the stable expansion of human embryonic stem cells. Tissue Eng. Part C Methods 17, 193-207 (2011).
43. Fusaki, N., Ban, H., Nishiyama, A., Saeki, K. & Hasegawa, M. Effcient induction of transgene-free human pluripotent stem cells using a vector based on Sendai virus, an RNA virus that does not integrate into the host genome. Proc. Jpn. Acad., Ser. B, Phys. Biol. Sci. 85, 348-362 (2009).
44. Mali, P. et al. Butyrate greatly enhances derivation of human induced pluripotent stem cells by promoting epigenetic remodeling and the expression of pluripotency-associated genes. Stem Cells 28, 713-720 (2010).
45. Okita, K. et al. A more effcient method to generate integration-free human iPS cells. Nat. Methods 8, 409-412 (2011).
46. Chou, B.K. et al. Effcient human iPS cell derivation by a non-integrating plasmid from blood cells with unique epigenetic and gene expression signatures. Cell Res. 21, 518-529 (2011).
47. Thomson, J.A. et al. Embryonic stem cell lines derived from human blastocysts. Science 282, 1145-1147 (1998).
48. Ng, E.S., Davis, R., Stanley, E.G. & Elefanty, A.G. A protocol describing the use of a recombinant protein-based, animal product-free medium (APEL) for human embryonic stem cell differentiation as spin embryoid bodies. Nat. Protoc. 3, 768-776 (2008).
49. Lin, Z.C., Xie, C., Osakada, Y., Cui, Y. & Cui, B. Iridium oxide nanotube electrodes for sensitive and prolonged intracellular measurement of action potentials. Nat. Commun. 5, 3206 (2014).