Insulin inhibits cardiac mesoderm, not mesendoderm, formation during cardiac differentiation of human pluripotent stem cells and modulation of canonical wnt signaling can rescue this inhibition

Stem Cells

Volumn 31, Issue 3, 2013, Pages 447-457

  Lian, Xiaojun ^a   Zhang, Jianhua ^b   Zhu, Kexian ^a   Kamp, Timothy J ^b   Palecek, Sean P ^a  

^a University of Wisconsin Madison   (United States)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

Canonical Wnt signaling; Cardiac mesoderm; Human pluripotent stem cells; Insulin signaling; Mesendoderm

Indexed keywords

BETA CATENIN; CD31 ANTIGEN; GLYCOGEN SYNTHASE KINASE 3BETA; INSULIN; SMOOTH MUSCLE ACTIN; TRANSCRIPTION FACTOR GATA 4; TRANSCRIPTION FACTOR NKX2.5; TRANSCRIPTION FACTOR SOX1; TRANSCRIPTION FACTOR TBX5; TRANSFORMING GROWTH FACTOR BETA; WNT PROTEIN;

ARTICLE; CELL ACTIVATION; CELL DIFFERENTIATION; CELL EXPANSION; CELL FATE; CELL VIABILITY; DOWN REGULATION; ENZYME PHOSPHORYLATION; HEART DEVELOPMENT; HEART MUSCLE CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; MESODERM; PLURIPOTENT STEM CELL; PROTEIN EXPRESSION; WNT SIGNALING PATHWAY;

ANIMALS; CELL DIFFERENTIATION; HUMANS; INSULIN; MESODERM; MICE; MYOCARDIUM; MYOCYTES, CARDIAC; SIGNAL TRANSDUCTION; WNT SIGNALING PATHWAY;

EID: 84874851964     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.1289     Document Type: Article

References (53)

1. Keller G. Embryonic stem cell differentiation: Emergence of a new era in biology and medicine. Genes Dev 2005;19: 1129-1155.
2. Pera MF, Trounson AO. Human embryonic stem cells: Prospects for development. Development 2004;131: 5515-5525.
3. Meyer JS, Shearer RL, Capowski EE et al. Modeling early retinal development with human embryonic and induced pluripotent stem cells. Proc Natl Acad Sci USA 2009;106: 16698-16703.
4. Li P, Cavallero S, Gu Y et al. IGF signaling directs ventricular cardiomyocyte proliferation during embryonic heart development. Development 2011;138: 1795-1805.
5. Xin M, Kim Y, Sutherland LB et al. Regulation of insulin-like growth factor signaling by Yap governs cardiomyocyte proliferation and embryonic heart size. Sci Signal 2011;4:ra70.
6. McDevitt TC, Laflamme MA, Murry CE. Proliferation of cardiomyocytes derived from human embryonic stem cells is mediated via the IGF/PI 3-kinase/Akt signaling pathway. J Mol Cell Cardiol 2005;39: 865-873.
7. 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.
8. Wang L, Schulz TC, Sherrer ES et al. Self-renewal of human embryonic stem cells requires insulin-like growth factor-1 receptor and ERBB2 receptor signaling. Blood 2007;110: 4111-4119.
9. Naito AT, Akazawa H, Takano H et al. Phosphatidylinositol 3-kinase- Akt pathway plays a critical role in early cardiomyogenesis by regulating canonical Wnt signaling. Circ Res 2005;97: 144-151.
10. Xu XQ, Graichen R, Soo SY et al. Chemically defined medium supporting cardiomyocyte differentiation of human embryonic stem cells. Differentiation 2008;76: 958-970.
11. 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.
12. Olson EN, Schneider MD. Sizing up the heart: Development redux in disease. Genes Dev 2003;17: 1937-1956.
13. Zhu W, Shiojima I, Ito Y et al. IGFBP-4 is an inhibitor of canonical Wnt signalling required for cardiogenesis. Nature 2008;454: 345-349.
14. 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.
15. 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.
16. Azarin SM, Lian X, Larson EA et al. Modulation of Wnt/beta-catenin signaling in human embryonic stem cells using a 3-D microwell array. Biomaterials 2012;33: 2041-2049.
17. Lian X, Hsiao C, Wilson G et al. Robust cardiomyocyte differentiation from human pluripotent stem cells via temporal modulation of canonical Wnt signaling. Proc Natl Acad Sci USA 2012;109: E1848-1857.
18. 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.
19. Paige SL, Osugi T, Afanasiev OK et al. Endogenous Wnt/beta-catenin signaling is required for cardiac differentiation in human embryonic stem cells. PLoS One 2010;5:e11134.
20. Yu J, Hu K, Smuga-Otto K et al. Human induced pluripotent stem cells free of vector and transgene sequences. Science 2009;324: 797-801.
21. Yu J, Vodyanik MA, Smuga-Otto K et al. Induced pluripotent stem cell lines derived from human somatic cells. Science 2007;318: 1917-1920.
22. Thomson JA, Itskovitz-Eldor J, Shapiro SS et al. Embryonic stem cell lines derived from human blastocysts. Science 1998;282: 1145-1147.
23. 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.
24. 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.
25. Lee P, Klos M, Bollensdorff C et al. Simultaneous voltage and calcium mapping of genetically purified human induced pluripotent stem cell-derived cardiac myocyte monolayers. Circ Res 2012;110: 1556-1563.
26. Mummery CL, Zhang J, Ng ES et al. Differentiation of human embryonic stem cells and induced pluripotent stem cells to cardiomyocytes: A methods overview. Circ Res 2012;111: 344-358.
27. Bruneau BG, Logan M, Davis N et al. Chamber-specific cardiac expression of Tbx5 and heart defects in Holt-Oram syndrome. Dev Biol 1999;211: 100-108.
28. Kuo CT, Morrisey EE, Anandappa R et al. GATA4 transcription factor is required for ventral morphogenesis and heart tube formation. Gene Dev 1997;11: 1048-1060.
29. Edmondson DG, Lyons GE, Martin JF et al. Mef2 gene-expression marks the cardiac and skeletal-muscle lineages during mouse embryogenesis. Development 1994;120: 1251-1263.
30. Bu L, Jiang X, Martin-Puig S et al. Human ISL1 heart progenitors generate diverse multipotent cardiovascular cell lineages. Nature 2009; 460: 113-117.
31. Qyang Y, Martin-Puig S, Chiravuri M et al. The renewal and differentiation of Isl1+ cardiovascular progenitors are controlled by a Wnt/beta-catenin pathway. Cell Stem Cell 2007;1: 165-179.
32. 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.
33. Vallier L, Touboul T, Chng Z et al. Early cell fate decisions of human embryonic stem cells and mouse epiblast stem cells are controlled by the same signalling pathways. PLoS One 2009;4:e6082.
34. Kitajima S, Takagi A, Inoue T et al. MesP1 and MesP2 are essential for the development of cardiac mesoderm. Development 2000;127: 3215-3226.
35. Costello I, Pimeisl IM, Drager S et al. The T-box transcription factor eomesodermin acts upstream of Mesp1 to specify cardiac mesoderm during mouse gastrulation. Nat Cell Biol 2011;13: 1084-1091.
36. van den Ameele J, Tiberi L, Bondue A et al. Eomesodermin induces Mesp1 expression and cardiac differentiation from embryonic stem cells in the absence of Activin. EMBO Rep 2012;13: 355-362.
37. Choi KD, Yu J, Smuga-Otto K et al. Hematopoietic and endothelial differentiation of human induced pluripotent stem cells. Stem Cells 2009;27: 559-567.
38. Zhang J, Klos M, Wilson GF et al. Extracellular matrix promotes highly efficient cardiac differentiation of human pluripotent stem cells: The matrix sandwich method. Circ Res. 2012;111: 1125-1136.
39. Zhang J, Klos M, Wilson GF et al. Extracellular matrix promotes highly efficient cardiac differentiation of human pluripotent stem cells: The matrix sandwich method. Circ Res 2012;111: 1125-1136.
40. Cross DA, Alessi DR, Cohen P et al. Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 1995;378: 785-789.
41. Paige SL, Thomas S, Stoick-Cooper CL et al. A temporal chromatin signature in human embryonic stem cells identifies regulators of cardiac development. Cell 2012;151: 221-232.
42. Chen G, Gulbranson DR, Hou Z et al. Chemically defined conditions for human iPSC derivation and culture. Nat Methods 2011;8: 424-429.
43. Bendall SC, Stewart MH, Menendez P et al. IGF and FGF cooperatively establish the regulatory stem cell niche of pluripotent human cells in vitro. Nature 2007;448: 1015-1021.
44. McLean AB, D'Amour KA, Jones KL et al. Activin a efficiently specifies definitive endoderm from human embryonic stem cells only when phosphatidylinositol 3-kinase signaling is suppressed. Stem Cells 2007;25: 29-38.
45. Tran TH, Wang X, Browne C et al. Wnt3a-induced mesoderm formation and cardiomyogenesis in human embryonic stem cells. Stem Cells 2009;27: 1869-1878.
46. Gunduz D, Thom J, Hussain I et al. Insulin stabilizes microvascular endothelial barrier function via phosphatidylinositol 3-kinase/Aktmediated Rac1 activation. Arterioscler Thromb Vasc Biol 2010;30: 1237-1245.
47. Wu X, Tu X, Joeng KS et al. Rac1 activation controls nuclear localization of beta-catenin during canonical Wnt signaling. Cell 2008;133: 340-353.
48. Wang ZZ, Au P, Chen T et al. Endothelial cells derived from human embryonic stem cells form durable blood vessels in vivo. Nat Biotechnol 2007;25: 317-318.
49. James D, Nam HS, Seandel M et al. Expansion and maintenance of human embryonic stem cell-derived endothelial cells by TGFbeta inhibition is Id1 dependent. Nat Biotechnol 2010;28: 161-166.
50. Levenberg S, Golub JS, Amit M et al. Endothelial cells derived from human embryonic stem cells. Proc Natl Acad Sci USA 2002;99: 4391-4396.
51. Xie CQ, Zhang J, Villacorta L et al. A highly efficient method to differentiate smooth muscle cells from human embryonic stem cells. Arterioscler Thromb Vasc Biol 2007;27:e311-312.
52. Cheung C, Bernardo AS, Trotter MW et al. Generation of human vascular smooth muscle subtypes provides insight into embryological origin- dependent disease susceptibility. Nat Biotechnol 2012;30: 165-173.
53. Spence JR, Mayhew CN, Rankin SA et al. Directed differentiation of human pluripotent stem cells into intestinal tissue in vitro. Nature 2011;470: 105-109.