Molecules and Cells

Korean Society for Molecular and Cellular Biology (한국분자세포생물학회)
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PV.1 Suppresses the Expression of FoxD5b during Neural Induction in Xenopus Embryos

  • Yoon, Jaeho (Department of Biochemistry, Institute of Cell Differentiation and Aging, College of Medicine, Hallym University) ;
  • Kim, Jung-Ho (Department of Biochemistry, Institute of Cell Differentiation and Aging, College of Medicine, Hallym University) ;
  • Kim, Sung Chan (Department of Biochemistry, Institute of Cell Differentiation and Aging, College of Medicine, Hallym University) ;
  • Park, Jae-Bong (Department of Biochemistry, Institute of Cell Differentiation and Aging, College of Medicine, Hallym University) ;
  • Lee, Jae-Yong (Department of Biochemistry, Institute of Cell Differentiation and Aging, College of Medicine, Hallym University) ;
  • Kim, Jaebong (Department of Biochemistry, Institute of Cell Differentiation and Aging, College of Medicine, Hallym University)
  • Received : 2013.10.17
  • Accepted : 2013.12.18
  • Published : 2014.03.31
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Abstract

Suppression of bone morphogenetic protein (BMP) signaling induces neural induction in the ectoderm of developing embryos. BMP signaling inhibits neural induction via the expression of various neural suppressors. Previous research has demonstrated that the ectopic expression of dominant negative BMP receptors (DNBR) reduces the expression of target genes down-stream of BMP and leads to neural induction. Additionally, gain-of-function experiments have shown that BMP downstream target genes such as MSX1, GATA1b and Vent are involved in the suppression of neural induction. For example, the Vent1/2 genes are involved in the suppression of Geminin and Sox3 expression in the neural ectodermal region of embryos. In this paper, we investigated whether PV.1, a BMP downstream target gene, negatively regulates the expression of FoxD5b, which plays a role in maintaining a neural progenitor population. A promoter assay and a cyclohexamide experiment demonstrated that PV.1 negatively regulates FoxD5b expression.

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References

  1. Ault, K.T., Dirksen, M.L., and Jamrich, M. (1996). A novel homeobox gene PV.1 mediates induction of ventral mesoderm in Xenopus embryos. Proc. Natl. Acad. Sci. USA 93, 6415-6420. https://doi.org/10.1073/pnas.93.13.6415
  2. Ault, K.T., Xu, R.H., Kung, H.F., and Jamrich, M. (1997). The homeobox gene PV.1 mediates specification of the prospective neural ectoderm in Xenopus embryos. Dev. Biol. 192, 162-171. https://doi.org/10.1006/dbio.1997.8737
  3. Chung, H.G., and Chung, H.M. (1999). Neuregulin induces the expression of mesodermal genes in the ectoderm of Xenopus laevis. Mol. Cells 9, 497-503.
  4. Dale, L., and Jones, C.M. (1999). BMP signalling in early Xenopus development. Bioessays 21, 751-760. https://doi.org/10.1002/(SICI)1521-1878(199909)21:9<751::AID-BIES6>3.0.CO;2-I
  5. Dale, L., and Wardle, F.C. (1999). A gradient of BMP activity specifies dorsal-ventral fates in early Xenopus embryos. Semin. Cell Dev. Biol. 10, 319-326. https://doi.org/10.1006/scdb.1999.0308
  6. Dosch, R., Gawantka, V., Delius, H., Blumenstock, C., and Niehrs, C. (1997). Bmp-4 acts as a morphogen in dorsoventral mesoderm patterning in Xenopus. Development (Cambridge, England) 124, 2325-2334.
  7. Fetka, I., Doederlein, G., and Bouwmeester, T. (2000). Neuroectodermal specification and regionalization of the Spemann organizer in Xenopus. Mech. Dev. 93, 49-58. https://doi.org/10.1016/S0925-4773(00)00265-3
  8. Friedle, H., and Knochel, W. (2002). Cooperative interaction of Xvent-2 and GATA-2 in the activation of the ventral homeobox gene Xvent-1B. J. Biol. Chem. 277, 23872-23881. https://doi.org/10.1074/jbc.M201831200
  9. Gawantka, V., Delius, H., Hirschfeld, K., Blumenstock, C., and Niehrs, C. (1995). Antagonizing the Spemann organizer: role of the homeobox gene Xvent-1. EMBO J. 14, 6268-6279.
  10. Glinka, A., Wu, W., Onichtchouk, D., Blumenstock, C., and Niehrs, C. (1997). Head induction by simultaneous repression of Bmp and Wnt signalling in Xenopus. Nature 389, 517-519. https://doi.org/10.1038/39092
  11. Hawley, S.H., Wunnenberg-Stapleton, K., Hashimoto, C., Laurent, M.N., Watabe, T., Blumberg, B.W., and Cho, K.W. (1995). Disruption of BMP signals in embryonic Xenopus ectoderm leads to direct neural induction. Genes Dev. 9, 2923-2935. https://doi.org/10.1101/gad.9.23.2923
  12. Hwang, Y.S., Seo, J.J., Cha, S.W., Lee, H.S., Lee, S.Y., Roh, D.H., Kung Hf, H.F., Kim, J., and Ja Park, M. (2002). Antimorphic PV.1 causes secondary axis by inducing ectopic organizer. Biochem. Biophys. Res. Commun. 292, 1081-1086. https://doi.org/10.1006/bbrc.2002.6740
  13. Hwang, Y.S., Lee, H.S., Roh, D.H., Cha, S., Lee, S.Y., Seo, J.J., Kim, J., and Park, M.J. (2003). Active repression of organizer genes by C-terminal domain of PV.1. Biochem. Biophys. Res. Commun. 308, 79-86. https://doi.org/10.1016/S0006-291X(03)01321-4
  14. Jackson, B.C., Carpenter, C., Nebert, D.W., and Vasiliou, V. (2010). Update of human and mouse forkhead box (FOX) gene families. Hum. Genomics 4, 345-352.
  15. Katoh, M., and Katoh, M. (2004). Human FOX gene family (Review). Int. J. Oncol. 25, 1495-1500.
  16. Katoh, M., Igarashi, M., Fukuda, H., Nakagama, H., and Katoh, M. (2012). Cancer genetics and genomics of human FOX family genes. Cancer Lett. 328, 198-206.
  17. Kuroda, H., Fuentealba, L., Ikeda, A., Reversade, B., and De Robertis, E.M. (2005). Default neural induction: neuralization of dissociated Xenopus cells is mediated by Ras/MAPK activation. Genes Dev. 19, 1022-1027. https://doi.org/10.1101/gad.1306605
  18. Lee, H.C., Tseng, W.A., Lo, F.Y., Liu, T.M., and Tsai, H.J. (2009). FoxD5 mediates anterior-posterior polarity through upstream modulator Fgf signaling during zebrafish somitogenesis. Dev. Biol. 336, 232-245. https://doi.org/10.1016/j.ydbio.2009.10.001
  19. Lee, H.S., Lee, S.Y., Lee, H., Hwang, Y.S., Cha, S.W., Park, S., Lee, J.Y., Park, J.B., Kim, S., Park, M.J., et al. (2011). Direct response elements of BMP within the PV.1A promoter are essential for its transcriptional regulation during early Xenopus development. PLoS One 6, e22621. https://doi.org/10.1371/journal.pone.0022621
  20. Moore, K.B., Mood, K., Daar, I.O., and Moody, S.A. (2004). Morphogenetic movements underlying eye field formation require interactions between the FGF and ephrinB1 signaling pathways. Dev. Cell 6, 55-67. https://doi.org/10.1016/S1534-5807(03)00395-2
  21. Nieuwkoop, P.D., and Faber, J. (1967). Normal table of Xenopus laevis, Vol. 2nd ed. (Northe Holland, Amsterdam).
  22. Pohl, B.S., and Knochel, W. (2005). Of Fox and Frogs: Fox (fork head/winged helix) transcription factors in Xenopus development. Gene 344, 21-32. https://doi.org/10.1016/j.gene.2004.09.037
  23. Rogers, C.D., Archer, T.C., Cunningham, D.D., Grammer, T.C., and Casey, E.M. (2008). Sox3 expression is maintained by FGF signaling and restricted to the neural plate by Vent proteins in the Xenopus embryo. Dev. Biol. 313, 307-319. https://doi.org/10.1016/j.ydbio.2007.10.023
  24. Rogers, C.D., Moody, S.A., and Casey, E.S. (2009). Neural induction and factors that stabilize a neural fate. Birth Defects Res. C Embryo Today 87, 249-262. https://doi.org/10.1002/bdrc.20157
  25. Shibata, K., Ishimura, A., and Maeno, M. (1998). GATA-1 inhibits the formation of notochord and neural tissue in Xenopus embryo. Biochem. Biophys. Res. Commun. 252, 241-248. https://doi.org/10.1006/bbrc.1998.9490
  26. Smith, J.C., and Slack, J.M. (1983). Dorsalization and neural induction: properties of the organizer in Xenopus laevis. J. Embryol. Exp. Morphol. 78, 299-317.
  27. Sullivan, S.A., Akers, L., and Moody, S.A. (2001). foxD5a, a Xenopus winged helix gene, maintains an immature neural ectoderm via transcriptional repression that is dependent on the Cterminal domain. Dev. Biol. 232, 439-457. https://doi.org/10.1006/dbio.2001.0191
  28. Suzuki, A., Ueno, N., and Hemmati-Brivanlou, A. (1997). Xenopus msx1 mediates epidermal induction and neural inhibition by BMP4. Development (Cambridge, England) 124, 3037-3044.
  29. Taylor, J.J., Wang, T., and Kroll, K.L. (2006). Tcf- and Vent-binding sites regulate neural-specific geminin expression in the gastrula embryo. Dev. Biol. 289, 494-506. https://doi.org/10.1016/j.ydbio.2005.10.047
  30. Wacker, S.A., McNulty, C.L., and Durston, A.J. (2004). The initiation of Hox gene expression in Xenopus laevis is controlled by Brachyury and BMP-4. Dev. Biol. 266, 123-137. https://doi.org/10.1016/j.ydbio.2003.10.011
  31. Wilson, P.A., and Hemmati-Brivanlou, A. (1995). Induction of epidermis and inhibition of neural fate by Bmp-4. Nature 376, 331-333. https://doi.org/10.1038/376331a0
  32. Xu, R.H., Kim, J., Taira, M., Zhan, S., Sredni, D., and Kung, H.F. (1995). A dominant negative bone morphogenetic protein 4 receptor causes neuralization in Xenopus ectoderm. Biochem. Biophys. Res. Commun. 212, 212-219. https://doi.org/10.1006/bbrc.1995.1958
  33. Yan, B., Neilson, K.M., and Moody, S.A. (2009a). foxD5 plays a critical upstream role in regulating neural ectodermal fate and the onset of neural differentiation. Dev. Biol. 329, 80-95. https://doi.org/10.1016/j.ydbio.2009.02.019
  34. Yan, B., Neilson, K.M., and Moody, S.A. (2009b). Notch signaling downstream of foxD5 promotes neural ectodermal transcription factors that inhibit neural differentiation. Dev. Dyn. 238, 1358-1365. https://doi.org/10.1002/dvdy.21885
  35. Yu, J.K., Holland, N.D., and Holland, L.Z. (2002). An amphioxus winged helix/forkhead gene, AmphiFoxD: insights into vertebrate neural crest evolution. Dev. Dyn. 225, 289-297. https://doi.org/10.1002/dvdy.10173

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