Small molecule-mediated directed differentiation of human embryonic stem cells toward ventricular cardiomyocytes

Stem Cells Translational Medicine

Volumn 3, Issue 1, 2014, Pages 18-31

  Karakikes, Ioannis ^a   Senyei, Grant D ^a   Hansen, Jens ^a   Kong, Chi Wing ^b   Azeloglu, Evren U ^a   Stillitano, Francesca ^a   Lieu, Deborah K ^b   Wang, Jiaxian ^b   Ren, Lihuan ^b   Hulot, Jean Sebastien ^a   Iyengar, Ravi ^a   Li, Ronald A ^a,b   Hajjar, Roger J ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

Cardiac; Differentiation; Embryonic stem cells; Pluripotent stem cells

Indexed keywords

DICKKOPF 1 PROTEIN; IWR-1; RECEPTOR BLOCKING AGENT; TNNT2; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ACTION POTENTIAL; ARTICLE; CALCIUM CELL LEVEL; CELL DIFFERENTIATION; CHEMICAL MODIFICATION; CONTROLLED STUDY; ELECTROPHYSIOLOGY; EMBRYONIC STEM CELL; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; GENE REGULATORY NETWORK; HEART BEAT; HEART MUSCLE CELL; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; MICROELECTRODE; PATCH CLAMP TECHNIQUE; VENTRICULAR CARDIOMYOCYTE; WNT SIGNALING PATHWAY;

CARDIAC; DIFFERENTIATION; EMBRYONIC STEM CELLS; PLURIPOTENT STEM CELLS;

ACTION POTENTIALS; ACTIVINS; ANTINEOPLASTIC AGENTS; BONE MORPHOGENETIC PROTEIN 4; CALCIUM; CELL DIFFERENTIATION; CELL LINE; CULTURE MEDIA; EMBRYONIC STEM CELLS; HEART VENTRICLES; HUMANS; IMIDES; INDUCED PLURIPOTENT STEM CELLS; MYOCYTES, CARDIAC; QUINOLINES; TRANSCRIPTOME; WNT SIGNALING PATHWAY;

EID: 84892752194     PISSN: 21576564     EISSN: 21576580     Source Type: Journal    
DOI: 10.5966/sctm.2013-0110     Document Type: Article

References (47)

1. Evans SM, Yelon D, Conlon FL et al. Myocardial lineage development. Circ Res 2010; 107:1428-1444.
2. Olson EN. Gene regulatory networks in the evolution and development of the heart. Science 2006;313:1922-1927.
3. Noseda M, Peterkin T, Simões FC et al. Cardiopoietic factors: Extracellular signals for cardiac lineage commitment. Circ Res 2011;108: 129-152.
4. 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.
5. LaflammeMA, Chen KY, NaumovaAV 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.
6. Yang L, Soonpaa MH, Adler ED et al. Human cardiovascular progenitor cells develop from a KDR+ embryonic-stem-cell-derived population. Nature 2008;453:524-528.
7. He JQ, MaY, Lee Y et al. Human embryonic stem cells develop into multiple types of cardiac myocytes: Action potential characterization. Circ Res 2003;93:32-39.
8. Mummery C, Ward-van Oostwaard D, Doevendans P et al. Differentiation of human embryonic stem cells to cardiomyocytes: Role of coculture with visceral endoderm-like cells. Circulation 2003;107:2733-2740.
9. Xu C, Police S, RaoNet al. Characterization and enrichment of cardiomyocytes derived from human embryonic stem cells. Circ Res 2002;91:501-508.
10. Burridge PW, Thompson S, Millrod MA et al. A universal system for highly efficient cardiac differentiation of human induced pluripotent stem cells that eliminates interline variability. PLoS One 2011;6:e18293.
11. Anderson D, Self T, Mellor IR et al. Transgenic enrichment of cardiomyocytes from human embryonic stem cells. Mol Ther 2007;15: 2027-2036.
12. Kita-Matsuo H, Barcova M, Prigozhina N et al. Lentiviral vectors and protocols for creation of stable hESC lines for fluorescent tracking and drug resistance selection of cardiomyocytes. PLoS One 2009;4:e5046.
13. Huber I, Itzhaki I, Caspi O et al. Identification and selection of cardiomyocytes during human embryonic stem cell differentiation. FASEB J 2007;21:2551-2563.
14. Ao A, Hao J, Hong CC. Regenerative chemical biology: Current challenges and future potential. Chem Biol 2011;18:413-424.
15. Wu X, Ding S, Ding Q et al. Small molecules that induce cardiomyogenesis in embryonic stem cells. J Am Chem Soc 2004;126: 1590-1591.
16. Takahashi T, Lord B, Schulze PC et al. Ascorbic acid enhances differentiation of embryonic stem cells into cardiac myocytes. Circulation 2003;107:1912-1916.
17. Sadek H, Hannack B, Choe E et al. Cardiogenic small molecules that enhance myocardial repair by stem cells. Proc Natl Acad Sci USA 2008;105:6063-6068.
18. Diamandis P, Wildenhain J, Clarke ID et al. Chemical genetics reveals a complex functional ground state of neural stem cells. Nat Chem Biol 2007;3:268-273.
19. Borowiak M, Maehr R, Chen S et al. Small molecules efficiently direct endodermal differentiation of mouse and human embryonic stem cells. Cell Stem Cell 2009;4:348-358.
20. Galende E, Karakikes I, Edelmann L et al. Amniotic fluid cells are more efficiently reprogrammed to pluripotency than adult cells. Cell Reprogram 2010;12:117-125.
21. Ludwig TE, Bergendahl V, Levenstein ME et al. Feeder-independent culture of human embryonic stemcells. NatMethods 2006;3:637-646.
22. Moore JC, Fu J, Chan YC et al. Distinct cardiogenic preferences of two human embryonic stem cell (hESC) lines are imprinted in their proteomes in the pluripotent state. Biochem Biophys Res Commun 2008;372:553-558.
23. Weinberg S, Lipke EA, Tung L. In vitro electrophysiological mapping of stem cells. Methods Mol Biol 2010;660:215-237.
24. de Hoon MJ, Imoto S, Nolan J et al. Open source clustering software. Bioinformatics 2004; 20:1453-1454.
25. Chen EY, Xu H, Gordonov S et al. Expression2Kinases: mRNA profiling linked to multiple upstream regulatory layers. Bioinformatics 2012; 28:105-111.
26. ChenG, HouZ, GulbransonDRetal. Actinmyosin contractility is responsible for the reduced viability of dissociated human embryonic stem cells. Cell Stem Cell 2010;7:240-248.
27. Ohgushi M, Matsumura M, Eiraku M et al. Molecular pathway and cell state responsible for dissociation-induced apoptosis in human pluripotent stem cells. Cell Stem Cell 2010;7:225-239.
28. Keller GM. In vitro differentiation of embryonic stem cells. Curr Opin Cell Biol 1995;7: 862-869.
29. Jaenisch R, Young R. Stem cells, the molecular circuitry of pluripotency and nuclear reprogramming. Cell 2008;132:567-582.
30. Kispert A, Herrmann BG, Leptin M et al. Homologs of the mouse Brachyury gene are involved in the specification of posterior terminal structures in Drosophila, Tribolium, and Locusta. Genes Dev 1994;8:2137-2150.
31. Ng ES, Azzola L, Sourris K et al. The primitive streak gene Mixl1 is required for efficient haematopoiesis and BMP4-induced ventral mesoderm patterning in differentiating ES cells. Development 2005;132:873-884.
32. Saga Y, Kitajima S, Miyagawa-Tomita S. Mesp1 expression is the earliest sign of cardiovascular development. Trends Cardiovasc Med 2000;10:345-352.
33. Bondue A, Lapouge G, Paulissen C et al. Mesp1acts as a master regulator of multipotent cardiovascular progenitor specification. Cell Stem Cell 2008;3:69-84.
34. BuckinghamM, Meilhac S, Zaffran S. Building the mammalian heart from two sources of myocardial cells. Nat Rev Genet 2005;6:826-835.
35. Moretti A, Caron L, Nakano A et al. Multipotent embryonic isl1+ progenitor cells lead to cardiac, smooth muscle, and endothelial cell diversification. Cell 2006;127:1151-1165.
36. Chen B, Dodge ME, Tang W et al. Small molecule-mediated disruption of Wnt-dependent signaling in tissue regeneration and cancer. Nat Chem Biol 2009;5:100-107.
37. O'Brien TX, Lee KJ, Chien KR. Positional specification of ventricular myosin light chain 2 expression in the primitive murine heart tube. Proc Natl Acad Sci USA 1993;90:5157-5161.
38. Bruneau BG, Bao ZZ, TanakaMet al. Cardiac expression of the ventricle-specific homeobox gene Irx4 is modulated by Nkx2-5 and dHand. Dev Biol 2000;217:266-277.
39. Bao ZZ, Bruneau BG, Seidman JG et al. Regulation ofchamber-specific gene expression in the developing heart by Irx4. Science 1999; 283:1161-1164.
40. Glinka A, WuW, DeliusHet al. Dickkopf-1 is amemberof anewfamily of secreted proteins and functions in head induction. Nature 1998; 391:357-362.
41. GlukhovaMA, FridMG, KotelianskyVE. Developmental changes in expression of contractile and cytoskeletal proteins in human aortic smooth muscle. J Biol Chem 1990;265:13042-13046.
42. Bers DM. Cardiac excitation-contraction coupling. Nature 2002;415:198-205.
43. Feldman DS, Carnes CA, Abraham WT et al. Mechanisms of disease: Beta-adrenergic receptors-alterations in signal transduction and pharmacogenomics in heart failure. Nat Clin Pract Cardiovasc Med 2005;2:475-483.
44. Ueno S, Weidinger G, Osugi T et al. Biphasic role for Wnt/beta-catenin signaling in cardiac specification in zebrafish and embryonic stem cells. Proc Natl Acad Sci USA 2007;104: 9685-9690.
45. Naito AT, Shiojima I, Akazawa H et al. Developmental stage-specific biphasic roles of Wnt/beta-catenin signaling in cardiomyogenesis and hematopoiesis. Proc Natl Acad Sci USA 2006;103:19812-19817.
46. Gessert S, Kühl M. The multiple phases and faces of wnt signaling during cardiac differentiation and development. Circ Res 2010; 107:186-199.
47. Ni TT, Rellinger EJ, Mukherjee A et al. Discovering small molecules that promote cardiomyocyte generation by modulating Wnt signaling. Chem Biol 2011;18:1658-1668.