57
Views
188
CrossRef citations to date
0
Altmetric
Cell Growth and Development

Bone Morphogenetic Proteins Induce Cardiomyocyte Differentiation through the Mitogen-Activated Protein Kinase Kinase Kinase TAK1 and Cardiac Transcription Factors Csx/Nkx-2.5 and GATA-4

, , , , , , , , , , , & show all
Pages 7096-7105 | Received 22 Jan 1999, Accepted 20 Jul 1999, Published online: 28 Mar 2023

REFERENCES

  • Andrée, B., D. Duprez, B. Vorbusch, H. Arnold, and J. Brand 1998. BMP-2 induces ectopic expression of cardiac lineage markers and interferes with somite formation in chicken embryos. Mech. Dev. 70:119–131.
  • Arceri, R. J., A. A. J. King, M. C. Simon, S. H. Orkin, and J. Wilson 1993. Mouse GATA-4: a retinoic acid-inducible GATA-binding transcription factor expressed in endodermally derived tissues and heart. Mol. Cell. Biol. 13:2235–2246.
  • Bader, D., T. Masaki, and J. Fischman 1982. Immunochemical analysis of myosin heavy chain during avian myogenesis in vivo and in vitro. J. Cell Biol. 95:763–770.
  • Bodmer, R., L. Y. Jan, and J. Jan 1990. A new homeobox-containing gene, msh-2, is transiently expressed early during mesoderm formation in Drosophila. Development 110:661–669.
  • Bodmer, R. 1993. The gene tinman is required for specification of the heart and visceral muscles in Drosophila. Development 118:719–729.
  • Bour, B. A., M. A. O’Brien, W. L. Lockwood, E. S. Goldstein, R. Bodmer, P. H. Taghert, S. M. Abmayr, and J. Nguyen 1995. Drosophila MEF2, a transcription factor that is essential for myogenesis. Genes Dev. 9:730–741.
  • Cleaver, O. B., K. D. Patterson, and J. Krieg 1996. Overexpression of the tinman-related genes XNkx-2.5 and XNkx-2.3 in Xenopus embryos results in myocardial hyperplasia. Development 122:3549–3556.
  • Edwards, M. K. S., J. F. Harris, and J. McBurney 1983. Induced muscle differentiation in an embryonal carcinoma cell line. Mol. Cell. Biol. 3:2280–2286.
  • Evans, T. 1997. Regulation of cardiac gene expression by GATA-4/5/6. Trends Cardiovasc. Med. 7:75–83.
  • Frasch, M. 1995. Induction of visceral and cardiac mesoderm by ectodermal Dpp in the early Drosophila embryo. Nature 374:464–467.
  • Fu, Y., and J. Izumo 1995. Cardiac myogenesis: overexpression of XCsx2 or XMEF2A in whole Xenopus embryos induces the precocious expression of the XMHCα gene. Roux’s Arch. Dev. Biol. 205:198–202.
  • Gajewski, K., Y. Kim, Y. M. Lee, E. N. Olson, and J. Schulz 1997. D-mef2 is a target for Tinman activation during Drosophila heart development. EMBO J. 16:515–522.
  • Gonzalez-Sanchez, A., and J. Bader 1990. In vitro analysis of cardiac progenitor cell differentiation. Dev. Biol. 139:197–209.
  • Graff, J. M., R. S. Thies, J. J. Song, A. J. Celeste, and J. Melton 1994. Studies with a Xenopus BMP receptor suggest that ventral mesoderm-inducing signals override dorsal signals in vivo. Cell 79:169–179.
  • Grépin, C., L. Dagnino, L. Robitaille, L. Haberstroh, T. Antakly, and J. Nemer 1994. A hormone-encoding gene identifies a pathway for cardiac but not skeletal muscle gene transcription. Mol. Cell. Biol. 14:3115–3129.
  • Grépin, C., G. Nemer, and J. Nemer 1997. Enhanced cardiogenesis in embryonic stem cells overexpressing the GATA-4 transcription factor. Development 124:2387–2395.
  • Habara-Ohkubo, A. 1996. Differentiation of beating cardiac muscle cells from a derivative of P19 embryonal carcinoma cells. Cell Struct. Funct. 21:101–110.
  • Han, Y., J. E. Dennis, L. Cohen-Gould, D. M. Bader, and J. Fischman 1992. Expression of sarcomeric myosin in the presumptive myocardium of chicken embryos occurs within six hours of myocyte commitment. Dev. Dyn. 193:257–265.
  • Hawley, S. H., K. Wunnenberg-Stapleton, C. Hashimoto, M. N. Laurent, T. Watabe, B. W. Blunberg, and J. Cho 1995. Disruption of BMP signals in embryonic Xenopus ectoderm leads to direct neural induction. Genes Dev. 9:2923–2935.
  • Heldin, C., K. Miyazono, and J. ten Dijke 1997. TGF-β signalling from cell membrane to nucleus through SMAD proteins. Nature 390:465–471.
  • Holtzer, H., T. Schultheiss, C. Dilullo, J. Choi, M. Costa, M. Lu, and J. Holtzer 1990. Autonomous expression of the differentiation programs of cells in the cardiac and skeletal myogenic lineages. Ann. N. Y. Acad. Sci. 599:158–169.
  • Ip, H. S., D. B. Wilson, M. Heikinheimo, Z. Tang, C. N. Ting, M. C. Simon, L. M. Leiden, and J. Parmasek 1994. The GATA-4 transcription factor transactivates the cardiac-specific troponin C promoter-enhancer in nonmuscle cells. Mol. Cell. Biol. 14:7517–7526.
  • Jacobson, A. G., and J. Sater 1988. Features of embryonic induction. Development 104:341–359.
  • Johansson, B. M., and J. Wiles 1995. Evidence for involvement of activin A and bone morphogenetic protein 4 in mammalian mesoderm and hematopoietic development. Mol. Cell. Biol. 15:141–151.
  • Komuro, I., and J. Izumo 1993. Csx: a murine homeobox-containing gene specifically expressed in the developing heart. Proc. Natl. Acad. Sci. USA 90:8145–8149.
  • Kuo, C. T., E. E. Morrisey, R. Anandappa, K. Sigrist, M. M. Lu, M. S. Parmasek, C. Soudais, and J. Leiden 1997. GATA4 transcription factor is required for ventral morphogenesis and heart tube formation. Genes Dev. 11:1048–1056.
  • Lee, Y., T. Shiroi, H. Kasahara, S. M. Jobe, R. J. Wiese, B. E. Markham, and J. Izumo 1998. The cardiac tissue-restricted homeobox protein Csx/Nkx2.5 physically associates with the zinc finger protein GATA4 and cooperatively activates atrial natriuretic factor gene expression. Mol. Cell. Biol. 18:3120–3129.
  • Lee, Y. M., T. Park, R. A. Schulz, and J. Kim 1997. Twist-mediated activation of the NK-4 homeobox gene in the visceral mesoderm of Drosophila requires two distinct clusters of E-box regulatory elements. J. Biol. Chem. 272:17531–17541.
  • Lilly, B., B. Zhao, G. Ranganayakulu, B. M. Paterson, R. A. Schulz, and J. Olson 1995. Requirement of MADS domain transcription factor D-MEF2 for muscle formation in Drosophila. Science 267:688–693.
  • Lin, Q., J. Schwarz, C. Bucana, and J. Olson 1997. Control of mouse cardiac morphogenesis and myogenesis by transcription factor MEF2C. Science 276:1404–1407.
  • Lints, T. J., L. M. Parsons, L. Hartley, I. Lyons, and J. Harvey 1993. Nkx-2.5: a novel murine homeobox gene expressed in early heart progenitor cells and their myogenic descendants. Development 119:419–431.
  • Lyons, I., L. M. Parsons, L. Hartley, R. Li, J. E. Andrews, L. Robb, and J. Harvey 1995. Myogenic and morphogenetic defects in the heart tubes of murine embryos lacking the homeo box gene Nkx2-5. Genes Dev. 9:1654–1666.
  • Maeno, M., R. C. Ong, A. Suzuki, N. Ueno, and J. Kung 1994. A truncated bone morphogenetic protein 4 receptor alters the fate of ventral mesoderm to dorsal mesoderm: roles of animal pole tissue in the development of ventral mesoderm. Proc. Natl. Acad. Sci. USA 91:10260–10264.
  • Martin, G. R. 1980. Teratocarcinomas and mammalian embryogenesis. Science 209:768–776.
  • McBurney, M. W., E. M. V. Jones-Villeneuve, M. K. S. Edwards, and J. Anderson 1982. Control of muscle and neuronal differentiation in a cultured embryonal carcinoma cell line. Nature 299:165–167.
  • McMahon, J. A., S. Takada, L. B. Zimmerman, C. M. Fan, R. M. Harland, and J. McMahon 1998. Noggin-mediated antagonism of BMP signaling is required for growth and patterning of the neural tube and somite. Genes Dev. 12:1438–1452.
  • Minden, A., A. Lin, M. McMahon, C. Lange-Carter, B. Dérijard, R. J. Davis, G. L. Johnson, and J. Karin 1994. Differential activation of ERK and JNK mitogen-activated protein kinases by Raf-1 and MEKK. Science 266:1719–1723.
  • Molkentin, J., Q. Lin, S. A. Duncan, and J. Olson 1997. Requirement of the transcription factor GATA-4 for heart tube formation and ventral morphogenesis. Genes Dev. 11:1061–1072.
  • Molkentin, J. D., D. V. Kalvakolanu, and J. Markham 1994. Transcription factor GATA-4 regulates cardiac muscle-specific expression of the α-myosin heavy chain gene. Mol. Cell. Biol. 14:4947–4957.
  • Monzen, K., and I. Komuro. Unpublished data.
  • Moriguchi, T., N. Kuroyanagi, K. Yamaguchi, Y. Gotoh, K. Irie, T. Kano, K. Shirakabe, Y. Muro, H. Shibuya, K. Matsumoto, E. Nishida, and J. Hagiwara 1996. A novel kinase cascade mediated by mitogen-activated protein kinase kinase 6 and MKK3. J. Biol. Chem. 271:13675–13679.
  • Nakaoka, T., K. Gonda, T. Ogita, Y. Otawara-Hamamoto, F. Okabe, Y. Kira, K. Harii, K. Miyazono, Y. Takuwa, and J. Fujita 1997. Inhibition of rat vascular smooth muscle proliferation in vitro and in vivo by bone morphogenetic protein-2. J. Clin. Investig. 100:2824–2832.
  • Nascone, N., and J. Mercola 1995. An inductive role for the endoderm in Xenopus cardiogenesis. Development 121:515–523.
  • Olson, E. N., and J. Srivastava 1996. Molecular pathway controlling heart development. Science 272:671–676.
  • Ranganayakulu, G., B. Zhao, A. Dokidis, J. D. Molkentin, E. N. Olson, and J. Schulz 1995. A series of mutations in the D-MEF2 transcription factor reveal multiple functions in larval and adult myogenesis in Drosophila. Dev. Biol. 171:169–181.
  • Reshef, R., M. Maroto, and J. Lassar 1998. Regulation of dorsal somitic cell fates: BMPs and noggin control the timing and pattern of myogenic regulator expression. Genes Dev. 12:290–303.
  • Rosenquist, G. C., and J. Dehaan 1966. Migration of precardiac cells in the chick embryo: a radioautographic study. Carnegie Inst. Wash. Contrib. Embryol. 38:111–121.
  • Sater, A. K., and J. Jacobson 1990. The restriction of the heart morphogenetic field in Xenopus laevis. Dev. Biol. 140:328–336.
  • Schultheiss, T. M., S. Xydas, and J. Lassar 1995. Induction of avian cardiac myogenesis by anterior endoderm. Development 121:4203–4214.
  • Schultheiss, T. M., J. B. E. Burch, and J. Lassar 1997. A role for bone morphogenetic proteins in the induction of cardiac myogenesis. Genes Dev. 11:451–462.
  • Sepulveda, J. L., N. Belaguli, V. Nigam, C. Chen, M. Nemar, and J. Schwartz 1998. GATA-4 and Nkx-2.5 coactivate Nkx-2 DNA binding targets: role for regulating early cardiac gene expression. Mol. Cell. Biol. 18:3405–3415.
  • Serbedzija, G. N., J. N. Chen, and J. Fishman 1998. Regulation in the heart field of zebrafish. Development 125:1095–1101.
  • Shibuya, H., H. Iwata, N. Masuyama, Y. Gotoh, K. Yamaguchi, K. Irie, K. Matsumoto, E. Nishida, and J. Ueno 1998. Role of TAK1 and TAB1 in BMP signaling in early Xenopus development. EMBO J. 17:1019–1028.
  • Shiojima, I., I. Komuro, T. Mizuno, R. Aikawa, H. Akazawa, T. Oka, T. Yamazaki, and J. Yazaki 1996. Molecular cloning and characterization of human cardiac homeobox gene CSX1. Circ. Res. 79:920–929.
  • Shiojima, I., I. Komuro, T. Oka, Y. Hiroi, T. Mizuno, E. Takimoto, K. Monzen, R. Aikawa, H. Akazawa, T. Yamazaki, S. Kudoh, and J. Yazaki 1999. Context-dependent transcriptional cooperation mediated by cardiac transcription factors Csx/Nkx-2.5 and GATA-4. J. Biol. Chem. 274:8231–8239.
  • Simon, M. C. 1995. Gotta have GATA. Nat. Genet. 11:9–11.
  • Skerjanc, I. S., H. Petropoulos, A. G. Ridgeway, and J. Wilton 1998. Myocyte enhancer factor 2C and Nkx2-5 up-regulate each other’s expression and initiate cardiomyogenesis in P19 cells. J. Biol. Chem. 273:34904–34910.
  • Smith, W. C., and J. Harland 1992. Expression cloning of noggin, a new dorsalizing factor localized to the Spemann organizer in Xenopus embryos. Cell 70:829–840.
  • Steinbeisser, H., A. Fainsod, C. Niehrs, Y. Sasai, and J. Robertis 1995. The role of gsc and BMP-4 in dorsal-ventral patterning of the marginal zone in Xenopus: a loss-of-function study using antisense RNA. EMBO J. 14:5230–5243.
  • Sugi, Y., and J. Lough 1995. Activin-A and FGF-2 mimic the inductive effects of anterior endoderm on terminal cardiac myogenesis in vitro. Dev. Biol. 168:567–574.
  • Suzuki, A., R. S. Thies, N. Yamaji, J. J. Song, J. M. Wozney, K. Murakami, and J. Ueno 1994. A truncated bone morphogenetic protein receptor affects dorsal-ventral patterning in the early Xenopus embryo. Proc. Natl. Acad. Sci. USA 91:10255–10259.
  • Takano, H., I. Komuro, T. Oka, I. Shiojima, Y. Hiroi, T. Mizuno, and J. Yazaki 1998. The Rho family G proteins play a critical role in muscle differentiation. Mol. Cell. Biol. 18:1580–1589.
  • Takimoto, E., and I. Komuro. Unpublished data.
  • Winnier, G., M. Blessing, P. A. Labosky, and J. Hogan 1995. Bone morphogenetic protein-4 is required for mesoderm formation and patterning in the mouse. Genes Dev. 9:2105–2116.
  • Xu, X., Z. Yin, J. B. Hudson, E. L. Ferguson, and J. Frasch 1998. Smad proteins act in combination with synergistic and antagonistic regulators to target Dpp responses to the Drosophila mesoderm. Genes Dev. 12:2354–2370.
  • Yamaguchi, K., K. Shirakabe, H. Shibuya, K. Irie, I. Oishi, N. Ueno, T. Taniguchi, E. Nishida, and J. Matsumoto 1995. Identification of a member of the MAPKKK family as a potential mediator of TGF-β signal transduction. Science 270:2008–2011.
  • Zhang, H., and J. Bradley 1996. Mice deficient for BMP2 are nonviable and have defects in amnion/chorion and cardiac development. Development 122:2977–2986.
  • Zimmerman, L. B., J. D. Jesus-Escobar, and J. Harland 1996. The Spemann organizer signal noggin binds and inactivates bone morphogenetic protein-4. Cell 86:599–606.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.