Wnt3a-induced mesoderm formation and cardiomyogenesis in human embryonic stem cells

Stem Cells

Volumn 27, Issue 8, 2009, Pages 1869-1878

  Tran, Thanh H ^a   Wang, Xiurong ^a   Browne, Carol ^a   Zhang, Yunyu ^a   Schinke, Martina ^a   Izumo, Seigo ^b   Burcin, Mark ^a  

^a NOVARTIS INSTITUTES FOR BIOMEDICAL RESEARCH   (United States)

^b GILEAD SCIENCES   (United States)

Author keywords

Cardiomyogenesis; Cell pharmacology; Directed differentiation; Human embryonic stem cells; Mesendoderm; Preclinical safety; Wnt3A

Indexed keywords

WNT3A PROTEIN;

ARTICLE; CELL DIFFERENTIATION; CELL REGENERATION; CELL RENEWAL; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; GENE EXPRESSION; HEART DEVELOPMENT; HEART MUSCLE CELL; HUMAN; HUMAN CELL; MESODERM;

ANIMALS; CELL COMMUNICATION; CELL DIFFERENTIATION; EMBRYONIC STEM CELLS; HUMANS; INSULIN; MESODERM; MICE; MYOCYTES, CARDIAC; RECOMBINANT PROTEINS; TISSUE ENGINEERING; WNT PROTEINS;

EID: 69249121687     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.95     Document Type: Article

References (44)

1. Thomson JA, Itskovitz-Eldor J, Shapiro SS et al. Embryonic stem cell lines derived from human blastocysts. Science 1998;282:1145-1147.
2. Oh SK, Kim HS, Ahn HJ et al. Derivation and characterization of new human embryonic stem cell lines: SNUhES1, SNUhES2, and SNUhES3 Stem Cells 2005;23:211-219.
3. Burridge PW, Anderson D, Priddle H 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 2007;25:929-938.
4. Graichen R, Xu X, Braam SR et al. Enhanced cardiomyogenesis of human embryonic stem cells by a small molecular inhibitor of p38 MAPK. Differentiation 2008;76:357-370.
5. Pal R, Khanna A. Similar pattern in cardiac differentiation of human embryonic stem cell lines, BG01V And ReliCellhES1, under low serum concentration supplemented with bone morphogenetic protein-2. Differentiation 2007;75:112-122.
6. Passier R, Oostwaard DW, Snapper J et al. Increased cardiomyocyte differentiation from human embryonic stem cells in serum-free cultures. Stem Cells 2005;23:772-780.
7. Yoon BS, Yoo SJ, Lee JE et al. Enhanced differentiation of human embryonic stem cells into cardiomyocytes by combining hanging drop culture and 5-azacytidine treatment. Differentiation 2006;74:149-159.
8. Laflamme MA, Chen KY, Naumova AV 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.
9. Haegel H, Larue L, Ohsugi M et al. Lack of β-catenin affects mouse development at gastrulation. Development 1995;121:3529-3537.
10. Kelly OG, Pinson KI, Skarnes WC. The Wnt co-receptors Lrp5 and Lrp6 are essential for gastrulation in mice. Development 2004;131:2803-2815.
11. Kemler R, Hierholzer A, Kanzler B et al. Stabilization of beta-catenin in the mouse zygote leads to premature epithelial-mesenchymal transition in the epiblast. Development 2004;131:5817-5824.
12. Mohamed OA, Clarke HJ, Dufort D. Beta-catenin signaling marks the prospective site of primitive streak formation in the mouse embryo. Dev Dyn 2004;231:416-424.
13. Rivera-Pérez JA, Magnuson T. Primitive streak formation in mice is preceded by localized activation of Brachyury and Wnt3. Dev Biol 2005;288:363-371.
14. Lindsley RC, Gill JG, Kyba M et al. Canonical Wnt signaling is required for development of embryonic stem cell-derived mesoderm. Development 2006;133:3787-3796.
15. Sumi T, Tsuneyoshi N, Nakatsuji N et al. Defining early lineage specification of human embryonic stem cells by the orchestrated balance of canonical Wnt/beta-catenin, activin/nodal and BMP signaling. Development 2008;135:2969-2979.
16. Cheon SS, Cheah AY, Turley S et al. β-catenin stabilization dysregulates mesenchymal cell proliferation, motility, and invasiveness and causes aggressive fibromatosis and hyperplastic cutaneous wounds. Proc Natl Acad Sci U S A 2002;99:6973-6978.
17. 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 U S A 2006;103:19812-19817.
18. 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 U S A 2007;104:9685-9690.
19. Davidson KC, Jamshidi P, Daly R et al. Wnt3a regulates survival, expansion, and maintenance of neural progenitors derived from human embryonic stem cells. Mol Cell Neurosci 2007;36:408-415.
20. Dravid G, Ye Z, Hammond H et al. Defining the role of Wnt/beta-catenin signaling in the survival, proliferation, and self-renewal of human embryonic stem cells. Stem Cells 2005;23:1489-1501.
21. Bakre MM, Hoi A, Mong JC et al. Generation of multipotential mesendodermal progenitors from mouse embryonic stem cells via sustained Wnt pathway activation. J Biol Chem 2007;282:31703-31712.
22. Xu C, He JQ, Kamp TJ et al. Human embryonic stem cell-derived cardiomyocytes can be maintained in defined medium without serum. Stem Cells Dev 2006;15:931-941.
23. Reimers M, Carey VJ. Bioconductor: An open source framework for bioinformatics and computational biology. Methods Enzymol 2006;411:119-134.
24. Hubbell E, Liu WM, Mei R. Guide to Probe Logarithmic Intensity Error (PLIER) Estimation. Available at http://www.affymetrix.com/support/technical/ technotes/plier-technote.pdf, accessed March 19, 2009.
25. Dai M, Wang P, Boyd AD et al. Evolving gene/transcript definitions significantly alter the interpretation of GeneChip data. Nucleic Acids Res 2005;33:e175.
26. Smyth GK. Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 2004;3:Article3.
27. Benjamini Y, Hochberg Y. Controlling the false discovery rate - a practical and powerful approach to multiple testing. J R Stat Soc Series B Methodol 1995;57:289-300.
28. Liu Y, Asakura M, Inoue H et al. Sox17 is essential for the specification of cardiac mesoderm in embryonic stem cells. Proc Natl Acad Sci U S A 2007;104:3859-3864.
29. Zaret KS. Hepatocyte differentiation: from the endoderm and beyond. Curr Opin Genet Dev 2001;11:568-574.
30. Liao G, Tao Q, Kofron M et al. Jun NH2-terminal kinase (JNK) prevents nuclear beta-catenin accumulation and regulates axis formation in Xenopus embryos. Proc Natl Acad Sci U S A 2006;103:16313-16318.
31. Markiewicz E, Tilgner K, Barker N et al. The inner nuclear membrane protein emerin regulates beta-catenin activity by restricting its accumulation in the nucleus. EMBO J 2006;25:3275-3285.
32. Hogan BLM. Bone morphogenetic proteins: Multifunctional regulators of vertebrate development. Genes Dev 1996;10:1580-1594.
33. Lin SY, Chen CL, Wu YL et al. Ratio of Wnt3a to BMP4 doses is critical to their synergistic effects on proliferation of differentiating mouse embryonic stem cells. Cell Prolif 2008;41:492-505.
34. Montesano R. Bone morphogenetic protein-4 abrogates lumen formation by mammary epithelial cells and promotes invasive growth. Biochem Biophys Res Commun 2007;353:817-822.
35. Freund C, Ward-van Oostwaard D, Monshouwer-Kloots J et al. Insulin redirects differentiation from cardiogenic mesoderm and endoderm to neuroectoderm in differentiating human embryonic stem cells. Stem Cells 2008;26:724-733.
36. Goh G, Self T, Barbadillo Muñoz MD et al. Molecular and phenotypic analyses of human embryonic stem cell-derived cardiomyocytes: Opportunities and challenges for clinical translation. Thromb Haemost 2005;94:728-737.
37. He JQ, Ma Y, Lee Y et al. Human embryonic stem cells develop into multiple types of cardiac myocytes: Action potential characterization. Circ Res 2003;93:32-39.
38. 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.
39. Reppel M, Boettinger C, Hescheler J. Beta-adrenergic and muscarinic modulation of human embryonic stem cell-derived cardiomyocytes. Cell Physiol Biochem 2004;14:187-196.
40. Sartiani L, Bettiol E, Stillitano F et al. Developmental changes in cardiomyocytes differentiated from human embryonic stem cells: A molecular and electrophysiological approach. Stem Cells 2007;25:1136-1144.
41. Xu C, Police S, Rao N et al. Characterization and enrichment of cardiomyocytes derived from human embryonic stem cells. Circ Res 2002;91:501-508.
42. 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.
43. Yu J, Vodyanik MA, Smuga-Otto K et al. Induced pluripotent stem cell lines derived from human somatic cells. Science 2007;318:1917-1920.
44. Mauritz C, Schwanke K, Reppel M et al. Generation of functional murine cardiac myocytes from induced pluripotent stem cells. Circulation 2008;118:507-517.