International Journal of Cardiology
Volume 127, Issue 1 , Pages 78-87 , 23 June 2008

Effect of bone morphogenetic protein-4 on cardiac differentiation from mouse embryonic stem cells in serum-free and low-serum media

  • Masoumeh Fakhr Taha

      Affiliations

    • Department of Anatomy, School of Medical Sciences, Tarbiat Modares University, Tehran, Iran
  • ,
  • Mojtaba Rezazadeh Valojerdi

      Affiliations

    • Department of Anatomy, School of Medical Sciences, Tarbiat Modares University, Tehran, Iran
    • Department of Embryology, Royan Institute, Tehran, Iran
    • Corresponding Author InformationCorresponding author. Department of Anatomy, School of Medical Sciences, Tarbiat Modares University, P.O. Box: 14115-111, Tehran, Iran.

Received 14 November 2006 ,Revised 10 April 2007 ,Accepted 12 April 2007.

References 

  1. Hogan BL. Bone morphogenetic proteins in development. Curr Opin Genet Dev. 1996;6:432–438
  2. Zaffran S, Frasch M. Early signals in cardiac development. Circ Res. 2002;91:457–469
  3. Andrée B, Duprez D, Vorbusch B, Arnold HH, Brand T. BMP-2 induces ectopic expression of cardiac lineage markers and interferes with somite formation in chicken embryos. Mech Dev. 1998;70:119–131
  4. Schultheiss TM, Burch JB, Lassar AB. A role for bone morphogenetic proteins in the induction of cardiac myogenesis. Genes Dev. 1997;11:451–462
  5. Nakajima Y, Yamagishi T, Ando K, Nakamura H. Significance of bone morphogenetic protein-4 function in the initial myofibrillogenesis of chick cardiogenesis. Dev Biol. 2002;245:291–303
  6. Reiter J, Verkade H, Stainier D. Bmp2b and Oep promote early myocardial differentiation through their regulation of gata5. Dev Biol. 2001;234:330–338
  7. Walters MJ, Wayman GA, Christian JL. Bone morphogenetic protein function is required for terminal differentiation of the heart but not for early expression of cardiac marker genes. Mech Dev. 2001;100:263–273
  8. Yamada M, Revelli JP, Eichele G, Barron M, Schwartz RJ. Expression of chick Tbx-2, Tbx-3, and Tbx-5 genes during early heart development: evidence for BMP2 induction of Tbx2. Dev Biol. 2000;228:95–105
  9. Sparrow DB, Kotecha S, Towers N, Mohun TJ. Xenopus eHAND: a marker for the developing cardiovascular system of the embryo that is regulated by bone morphogenetic proteins. Mech Dev. 1998;71:151–163
  10. Schlange T, Andree B, Arnold HH, Brand T. BMP2 is required for early heart development during a distinct time period. Mech Dev. 2000;91:259–270
  11. Shi Y, Katsev S, Cai C, Evans S. BMP signaling is required for heart formation in vertebrates. Dev Biol. 2000;224:226–237
  12. Behfar A, Zingman LV, Hodgson DM, et al. Stem cell differentiation requires a paracrine pathway in the heart. FASEB J. 2002;16:1558–1566
  13. Yuasa S, Itabashi Y, Koshimizu U, et al. Transient inhibition of BMP signaling by Noggin induces cardiomyocyte differentiation of mouse embryonic stem cells. Natl Biotechnol. 2005;23:607–611
  14. Taha MF, Valojerdi MR, Mowla SJ. Effect of bone morphogenetic protein-4 (BMP-4) on cardiomyocyte differentiation from mouse embryonic stem cell. Int J Cardiol. 2007;120:92–101
  15. Sachinidis A, Fleischmann BK, Kolossov E, Wartenberg M, Sauer H, Hescheler J. Cardiac specific differentiation of mouse embryonic stem cells. Cardiovasc Res. 2003;58:278–291
  16. Baharvand H, Ashtiani SK, Valojerdi MR, Shahverdi A, Taee A, Sabour D. Establishment and in vitro differentiation of a new embryonic stem cell line from human blastocyst. Differentiation. 2004;72:224–229
  17. Baharvand H, Matthaei KI. The ultrastructure of mouse embryonic stem cells. Reprod Biomed Online. 2003;7:330–335
  18. Maltsev VA, Wobus AM, Rohwedel J, Bader M, Hescheler J. Cardiomyocytes differentiated in vitro from embryonic stem cells developmentally cardiac specific genes and ionic currents. Circ Res. 1994;75:233–244
  19. Hatami L, Valojerdi MR, Mowla SJ. Effects of oxytocin on cardiomyocyte differentiation from mouse embryonic stem cells. Int J Cardiol. 2007;117:80–89
  20. Nikpoor P, Mowla SJ, Movahedin M, Ziaee SA, Tiraihi T. CatSper gene expression in postnatal development of mouse testis and in subfertile men with deficient sperm motility. Hum Reprod. 2004;19:124–128
  21. Baharvand H, Azarnia M, Parivar K, Ashtiani SK. The effect of extracellular matrix on embryonic stem cell-derived cardiomyocytes. J Mol Cell Cardiol. 2005;38:495–503
  22. Wobus AM, Guan K, Yang H–T, Boheler KR. Embryonic stem cells as a model to study cardiac, skeletal muscle, and vascular smooth muscle cell differentiation. In:  Turksen K editors. Embryonic stem cells: methods and protocols. Totowa, NJ: Humana Press Inc; 2001;p. 134
  23. Heng BC, Haider HKh, Sim EK, Cao T, Ng SC. Strategies for directing the differentiation of stem cells into the cardiomyogenic lineage in vitro. Cardiovasc Res. 2004;62:34–42
  24. Goldsborough MD, Tilkins ML, Price PJ, et al. Serum-free culture of murine embryonic stem (ES) cells. Focus®. 1998;20:8–12
  25. Barron M, Gao M, Lough J. Requirement for BMP and FGF signaling during cardiogenic induction in non-precardiac mesoderm is specific, transient, and cooperative. Dev Dyn. 2000;218:383–393
  26. Mohun T, Sparrow D. Early steps in vertebrate cardiogenesis. Curr Opin Genet Dev. 1997;7:628–633
  27. Ladd AN, Yatskievyeh TA, Antin PB. Regulation of avian cardiac myogenesis by activin/TGFbeta and bone morphogenetic proteins. Dev Biol. 1998;204:407–419
  28. Lough J, Barron M, Brogley M, Sugi Y, Bolender DL, Zhu X. Combined BMP-2 and FGF-4, but neither factor alone, induces cardiogenesis in non-precardiac embryonic mesoderm. Dev Biol. 1996;178:198–202
  29. Metzger JM, Lin WI, Johnston RA, Westfall MV, Samuelson LC. Myosin heavy chain expression in contracting myocytes isolated during embryonic stem cell cardiogenesis. Circ Res. 1995;76:710–719
  30. Taha MF, Valojerdi MR, Mowla SJ. Effect of bone morphogenetic protein-4 (BMP-4) on adipocyte differentiation from mouse embryonic stem cells. Anat Histol Embryol. 2006;35:271–278
  31. Yang HT, Tweedie D, Wang S, et al. The ryanodine receptor modulates the spontaneous beating rate of cardiomyocytes during development. Proc Natl Acad Sci U S A. 2002;99:9225–9230
  32. Manasek FJ. Histogenesis of the embryonic myocardium. Am J Cardiol. 1970;25:149–168
  33. Chacko KJ. Observations on the ultrastructure of developing myocardium of rat embryos. J Morphol. 1976;150:681–709
  34. 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
  35. Lompre AM, Mercadier JJ, Wisnewsky C, et al. Species- and age-dependent changes in the relative amounts of cardiac myosin isoenzymes in mammals. Dev Biol. 1981;84:286–290
  36. Lyons GE, Schiaffino S, Sassoon D, Barton P, Buckingham M. Developmental regulation of myosin gene expression in mouse cardiac muscle. J Cell Biol. 1990;111:2427–2436
  37. Ng WA, Grupp IL, Subramaniam A, Robbins J. Cardiac myosin heavy chain mRNA expression and myocardial function in the mouse heart. Circ Res. 1991;68:1742–1750
  38. Sanchez A, Jones WK, Gulick J, Doetschman T, Robbins J. Myosin heavy chain gene expression in mouse embryoid bodies. An in vitro developmental study. J Biol Chem. 1991;266:22419–22426
  39. Robbins J, Gulick J, Sanchez A, Howles P, Doetschman T. Mouse embryonic stem cells express the cardiac myosin heavy chain genes during development in vitro. J Biol Chem. 1990;265:11905–11909
  40. Fassler R, Rohwedel J, Maltsev V, et al. Differentiation and integrity of cardiac muscle cells are impaired in the absence of β1 integrin. J Cell Sci. 1996;109:2989–2999
  41. Christoffels VM, Habets PE, Franco D, et al. Chamber formation and morphogenesis in the developing mammalian heart. Dev Biol. 2000;223:266–278
  42. Franco D, Campione M, Kelly R, et al. Multiple transcriptional domains, with distinct left and right components, in the atrial chambers of the developing heart. Circ Res. 2000;87:984–991
  43. Zeller R, Bloch KD, Williams BS, Arceci RJ, Seidman CE. Localized expression of the atrial natriuretic factor gene during cardiac embryogenesis. Gene Dev. 1987;1:693–698
  44. Doevendans PA, Kubalak SW, An RH, Becker DK, Chien KR, Kass RS. Differentiation of cardiomyocytes in floating embryoid bodies is comparable to fetal cardiomyocytes. J Mol Cell Cardiol. 2000;32:839–851
  45. Miller-Hance WC, LaCorbiere M, Fuller SJ, et al. In vitro chamber specification during embryonic stem cell cardiogenesis. Expression of the ventricular myosin light chain-2 gene is independent of hearttube formation. J Biol Chem. 1993;268:25244–25252
  46. Muller M, Fleischmann BK, Selbert S, et al. Selection of ventricular-like cardiomyocytes from ES cells in vitro. FASEB J. 2000;14:2540–2548
  47. 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

PII: S0167-5273(07)01031-5

doi: 10.1016/j.ijcard.2007.04.173

International Journal of Cardiology
Volume 127, Issue 1 , Pages 78-87 , 23 June 2008