Trends in Cardiovascular Medicine
Volume 17, Issue 3 , Pages 96-101 , April 2007

Bypassing Heterogeneity: The Road to Embryonic Stem Cell-Derived Cardiomyocyte Specification

  • Amar M. Singh
    • ,
  • Naohiro Terada

      Affiliations

    • Corresponding Author InformationAddress correspondence to: Dr. Naohiro Terada, Department of Pathology, University of Florida College of Medicine, Box 100275, Gainesville, FL 32610, USA. Tel.: (+1) 352-392-2696; fax: (+1) 352-392-6249.

References 

  1. Aouadi M, Bost F, Caron L, et al. p38 mitogen-activated protein kinase activity commits embryonic stem cells to either neurogenesis or cardiomyogenesis. Stem Cells. 2006;24:1399–1406
  2. Barandon L, Couffinhal T, Ezan J, et al. Reduction of infarct size and prevention of cardiac rupture in transgenic mice overexpressing FrzA. Circulation. 2003;108:2282–2289
  3. Behfar A, Zingman LV, Hodgson DM, et al. Stem cell differentiation requires a paracrine pathway in the heart. FASEB J. 2002;16:1558–1566
  4. Chazaud C, Yamanaka Y, Pawson T, Rossant J. Early lineage segregation between epiblast and primitive endoderm in mouse blastocysts through the Grb2-MAPK pathway. Dev Cell. 2006;10:615–624
  5. de Caestecker M. The transforming growth factor-beta superfamily of receptors. Cytokine Growth Factor Rev. 2004;15:1–11
  6. Dell'Era P, Ronca R, Coco L, et al. Fibroblast growth factor receptor-1 is essential for in vitro cardiomyocyte development. Circ Res. 2003;93:414–420
  7. E LL, Zhao YS, Guo XM, et al. Enrichment of cardiomyocytes derived from mouse embryonic stem cells. J Heart Lung Transplant. 2006;25:664–674
  8. Evans MJ, Kaufman MH. Establishment in culture of pluripotential cells from mouse embryos. Nature. 1981;292:154–156
  9. Foshay K, Rodriguez G, Hoel B, et al. JAK2/STAT3 directs cardiomyogenesis within murine embryonic stem cells in vitro. Stem Cells. 2005;23:530–543
  10. Furusawa T, Ikeda M, Inoue F, et al. Gene expression profiling of mouse embryonic stem cell subpopulations. Biol Reprod. 2006;75:555–561
  11. Gordon MD, Nusse R. Wnt signaling: multiple pathways, multiple receptors, and multiple transcription factors. J Biol Chem. 2006;281:22429–22433
  12. Hamazaki T, Kehoe SM, Nakano T, Terada N. The grb2/mek pathway represses nanog in murine embryonic stem cells. Mol Cell Biol. 2006;26:7539–7549
  13. Kanno S, Kim PK, Sallam K, et al. Nitric oxide facilitates cardiomyogenesis in mouse embryonic stem cells. Proc Natl Acad Sci U S A. 2004;101:12277–12281
  14. Kawai T, Takahashi T, Esaki M, et al. Efficient cardiomyogenic differentiation of embryonic stem cell by fibroblast growth factor 2 and bone morphogenetic protein 2. Circ J. 2004;68:691–702
  15. Kattman SJ, Huber TL, Keller GM. Multipotent flk-1+ cardiovascular progenitor cells give rise to the cardiomyocyte, endothelial, and vascular smooth muscle lineages. Dev Cell. 2006;11:723–732
  16. 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
  17. Kehat I, Khimovich L, Caspi O, et al. Electromechanical integration of cardiomyocytes derived from human embryonic stem cells. Nat Biotechnol. 2004;22:1282–1289
  18. Keller G. Embryonic stem cell differentiation: emergence of a new era in biology and medicine. Genes Dev. 2005;19:1129–1155
  19. Klinz F, Bloch W, Addicks K, Hescheler J. Inhibition of phosphatidylinositol-3-kinase blocks development of functional embryonic cardiomyocytes. Exp Cell Res. 1999;247:79–83
  20. Klug MG, Soonpaa MH, Koh GY, Field LJ. Genetically selected cardiomyocytes from differentiating embryonic stem cells form stable intracardiac grafts. J Clin Invest. 1996;98:216–224
  21. Kolossov E, Bostani T, Roell W, et al. Engraftment of engineered ES cell-derived cardiomyocytes but not BM cells restores contractile function to the infracted myocardium. J Exp Med. 2006;203:2315–2327
  22. Koyanagi M, Haendeler J, Badorff C, et al. Non-canonical Wnt signaling enhances differentiation of human circulating progenitor cells to cardiomyogenic cells. J Biol Chem. 2005;280:16838–16842
  23. LaFlamme MA, Gold J, Xu C, et al. Formation of human myocardium in the rat heart from human embryonic stem cells. Am J Pathol. 2005;167:663–671
  24. 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
  25. Lickert H, Kutsch S, Kanzler B, et al. Formation of multiple hearts in mice following deletion of beta-catenin in the embryonic endoderm. Dev Cell. 2002;3:171–181
  26. Martin GR. Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc Natl Acad Sci U S A. 1981;78:7634–7638
  27. Maye P, Zheng J, Li L, Wu D. Multiple mechanisms for Wnt11-mediated repression of the canonical Wnt signaling pathway. J Biol Chem. 2004;279:24659–24665
  28. 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
  29. Morali OG, Jouneau A, McLaughlin KJ, et al. IGF-II promotes mesoderm formation. Dev Biol. 2000;227:133–145
  30. 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
  31. Muller M, Fleischmann BK, Selbert S, et al. Selection of ventricular-like cardiomyocytes from ES cells in vitro. FASEB J. 2000;14:2540–2548
  32. Murry CE, Field LJ, Menasche P. Cell-based cardiac repair: reflections at the 10-year point. Circulation. 2005;112:3174–3183
  33. Naito AT, Shiojima I, Akazawa H, et al. Developmental stage-specific biphasic roles of Wnt/β-catenin signaling in cardiomyogenesis and hematopoiesis. Proc Natl Acad Sci U S A. 2007;103:19812–19817
  34. Nakamura T, Sano M, Songyang Z, Schneider MD. A Wnt- and beta-catenin-dependent pathway for mammalian cardiac myogenesis. Proc Natl Acad Sci U S A. 2003;100:5834–5839
  35. Nakano T, Kodama H, Honjo T. Generation of lymphohematopoietic cells from embryonic stem cells in culture. Science. 1994;265:1098–1101
  36. Nemir M, Croquelois A, Pedrazzini T, Radtke F. Induction of cardiogenesis in embryonic stem cells via downregulation of Notch1 signaling. Circ Res. 2006;98:1471–1478
  37. Schneider VA, Mercola M. Wnt antagonism initiates cardiogenesis in Xenopus laevis. Genes Dev. 2001;15:304–315
  38. Schroeder M, Niebruegge S, Werner A, et al. Differentiation and lineage selection of mouse embryonic stem cells in a stirred bench scale bioreactor with automated process control. Biotechnol Bioeng. 2005;92:920–933
  39. Schroeder T, Meier-Stiegen F, Schwanbeck R, et al. Activated Notch1 alters differentiation of embryonic stem cells into mesodermal cell lineages at multiple stages of development. Mech Dev. 2006;123:570–579
  40. Singh AM, Li FQ, Hamazaki T, et al. Chibby, an antagonist of the Wnt/beta-catenin pathway, facilitates cardiomyocyte differentiation of murine embryonic stem cells. Circulation. 2007;115:617–626
  41. Singla DK, Sun B. Transforming growth factor-beta-2 enhances differentiation of cardiac myocytes from embryonic stem cells. Biochem Biophys Res Commun. 2005;332:135–141
  42. Smith AG. Embryo-derived stem cells: of mice and men. Annu Rev Cell Dev Biol. 2001;17:435–462
  43. Stewart MH, Bosse M, Chadwick K, et al. Clonal isolation of hESCs reveals heterogeneity within the pluripotent stem cell compartment. Nat Methods. 2006;3:807–815
  44. Takahashi T, Lord B, Schulze PC, et al. Ascorbic acid enhances differentiation of embryonic stem cells into cardiac myocytes. Circulation. 2003;107:1912–1916
  45. Takemaru K, Yamaguchi S, Lee YS, et al. Chibby, a nuclear beta-catenin-associated antagonist of the Wnt/Wingless pathway. Nature. 2003;422:905–909
  46. Terami H, Hidaka K, Katsumata T, et al. Wnt 11 facilitates embryonic stem cell differentiation to Nkx2.5-positive cardiomyocytes. Biochem Biophys Res Commun. 2004;325:968–975
  47. Thomson JA, Itskovitz-Eldor J, Shapiro SS, et al. Embryonic stem cell lines derived from human blastocysts. Science. 1998;282:1145–1147
  48. Wei H, Juhasz O, Li J, et al. Embryonic stem cells and cardiomyocyte differentiation: phenotypic and molecular analyses. J Cell Mol Med. 2005;9:804–817
  49. Xu C, Liguori G, Adamson ED, Persico MG. Specific arrest of cardiogenesis in cultured embryonic stem cells lacking Cripto-1. Dev Biol. 1998;196:237–247
  50. Wobus AM, Kaomei G, Shan J, et al. Retinoic acid accelerates embryonic stem cell-derived cardiac differentiation and enhances development of ventricular cardiomyocytes. J Mol Cell Cardiol. 1997;29:1525–1539
  51. Xue T, Cho HC, Akar FG, et al. Functional integration of electrically active cardiac derivatives from genetically engineered human embryonic stem cells with quiescent recipient ventricular cardiomyocytes: insights into the development of cell-based pacemakers. Circulation. 2005;111:11–20
  52. Yamashita JK, Takano M, Hiraoka-Kanie M, et al. Prospective identification of cardiac progenitors by a novel single cell-based cardiomyocyte induction. FASEB J. 2005;19:1534–1536
  53. Yuasa S, Itabashi Y, Koshimizu U, et al. Transient inhibition of BMP signaling by Noggin induces cardiomyocyte differentiation of mouse embryonic stem cells. Nat Biotechnol. 2005;23:607–611
  54. Zandstra PW, Bauwens C, Yin T, et al. Scalable production of embryonic stem cell-derived cardiomyocytes. Tissue Eng. 2003;9:767–768

PII: S1050-1738(07)00046-1

doi: 10.1016/j.tcm.2007.02.003

Trends in Cardiovascular Medicine
Volume 17, Issue 3 , Pages 96-101 , April 2007

Article Tools

* Image Usage & Resolution