Browse > Article
http://dx.doi.org/10.14348/molcells.2016.0006

xCyp26c Induced by Inhibition of BMP Signaling Is Involved in Anterior-Posterior Neural Patterning of Xenopus laevis  

Yu, Saet-Byeol (Department of Biochemistry, Institute of Cell Differentiation and Aging, College of Medicine, Hallym University)
Umair, Zobia (Department of Biochemistry, Institute of Cell Differentiation and Aging, College of Medicine, Hallym University)
Kumar, Shiv (Department of Biochemistry, Institute of Cell Differentiation and Aging, College of Medicine, Hallym University)
Lee, Unjoo (Department of Electrical Engineering, Hallym University)
Lee, Seung-Hwan (Department of Biochemistry, Institute of Cell Differentiation and Aging, College of Medicine, Hallym University)
Kim, Jong-Il (Department of Biochemistry and Molecular Biology, Seoul National University College of Medicine)
Kim, SungChan (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)
Abstract
Vertebrate neurogenesis requires inhibition of endogenous bone morphogenetic protein (BMP) signals in the ectoderm. Blocking of BMPs in animal cap explants causes the formation of anterior neural tissues as a default fate. To identify genes involved in the anterior neural specification, we analyzed gene expression profiles using a Xenopus Affymetrix Gene Chip after BMP-4 inhibition in animal cap explants. We found that the xCyp26c gene, encoding a retinoic acid (RA) degradation enzyme, was upregulated following inhibition of BMP signaling in early neuroectodermal cells. Whole-mount in situ hybridization analysis showed that xCyp26c expression started in the anterior region during the early neurula stage. Overexpression of xCyp26c weakly induced neural genes in animal cap explants. xCyp26c abolished the expression of all trans-/cis-RA-induced posterior genes, but not basic FGF-induced posterior genes. Depletion of xCyp26c by morpholino-oligonucleotides suppressed the normal formation of the axis and head, indicating that xCyp26c plays a critical role in the specification of anterior neural tissue in whole embryos. In animal cap explants, however, xCyp26c morpholinos did not alter anterior-to-posterior neural tissue formation. Together, these results suggest that xCyp26c plays a specific role in anterior-posterior (A-P) neural patterning of Xenopus embryos.
Keywords
A-P neural formation; BMP-4; xCyp26c; Xenopus laevis;
Citations & Related Records
Times Cited By KSCI : 2  (Citation Analysis)
연도 인용수 순위
1 Graff, J.M., Thies, R.S., Song, J.J., Celeste, A.J. and Melton, D.A. (1994). Studies with a Xenopus BMP receptor suggest that ventral mesoderm-inducing signals override dorsal signals in vivo. Cell 79, 169-179.   DOI
2 Harland, R.M. (1991). In situ hybridization: an improved wholemount method for Xenopus embryos. Methods Cell Biol. 36, 685.   DOI
3 Harland, R. and Gerhart, J. (1997). Formation and function of Spemann's organizer. Annu. Rev. Cell Dev .Biol. 13, 611-667.   DOI
4 Hemmati-Brivanlou, A. and Melton, D.A. (1994). Inhibition of activin receptor signaling promotes neuralization in Xenopus. Cell 77, 273-281.   DOI
5 Hemmati-Brivanlou, A. and Thomsen, G.H. (1995). Ventral mesodermal patterning in Xenopus embryos: expression patterns and activities of BMP-2 and BMP-4. Dev. Genet. 17, 78-89.   DOI
6 Hollemann, T., Chen, Y., Grunz, H. and Pieler, T. (1998). Regionalized metabolic activity establishes boundaries of retinoic acid signalling. EMBO J. 17, 7361-7372.   DOI
7 Hwang, Y.-S., Seo, J.-J., Cha, S.-W., Lee, H.-S., Lee, S.-Y., Roh, D.-H., Kung, H.-f., Kim, J., and Park, M.J. (2002). Antimorphic PV. 1 causes secondary axis by inducing ectopic organizer. Biochem. Biophys. Res. Commun. 292, 1081-1086.   DOI
8 Hwang, Y.-S., Lee, H.-S., Roh, D.-H., Cha, S.-W., 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.   DOI
9 Jones, C.M., and Smith, J. (1998). Establishment of a BMP-4 morphogen gradient by long-range inhibition. Dev. Biol. 194, 12-17.   DOI
10 Jones, C.M., Lyons, K.M., Lapan, P., Wright, C., and Hogan, B. (1992). DVR-4 (bone morphogenetic protein-4). as a posteriorventralizing factor in Xenopus mesoderm induction. Development 115, 639-647.
11 Kessler, D.S., and Melton, D.A. (1994). Vertebrate embryonic induction: mesodermal and neural patterning. Science 266, 596-604.   DOI
12 Knecht, A.K., and Harland, R.M. (1997). Mechanisms of dorsalventral patterning in noggin-induced neural tissue. Development 124, 2477-2488.
13 Kolm, P.J., Apekin, V., and Sive, H. (1997). Xenopus hindbrain patterning requires retinoid signaling. Dev. Biol. 192, 1-16.   DOI
14 Kudoh, T., Wilson, S.W., and Dawid, I.B. (2002). Distinct roles for Fgf, Wnt and retinoic acid in posteriorizing the neural ectoderm. Development 129, 4335-4346.
15 Kuhl, M. (2003). Wnt Signaling in Development.
16 Lee, H.-S., Lee, S.-Y., Lee, H., Hwang, Y.-S., Cha, S.-W., Park, S., Lee, J.-Y., Park, J.-B., Kim, S., and Park, M.J. (2011a). Direct response elements of BMP within the PV. 1A promoter are essential for its transcriptional regulation during early Xenopus development. PLoS One 6, e22621.   DOI
17 Lee, S.-Y., Yoon, J., Lee, H.-S., Hwang, Y.-S., Cha, S.-W., Jeong, C.-H., Kim, J.-I., Park, J.-B., Lee, J.-Y., and Kim, S. (2011b). The function of heterodimeric AP-1 comprised of c-Jun and c-Fos in activin mediated Spemann organizer gene expression. PLoS One 6, e21796.   DOI
18 MacLean, G., Abu-Abed, S., Dollé, P., Tahayato, A., Chambon, P., and Petkovich, M. (2001). Cloning of a novel retinoic-acid metabolizing cytochrome P450, Cyp26B1, and comparative expression analysis with Cyp26A1 during early murine development. Mech. Dev. 107, 195-201.   DOI
19 Nebert, D.W., and Russell, D.W. (2002). Clinical importance of the cytochromes P450. The Lancet 360, 1155-1162.   DOI
20 Mason, I. (1996). Neural induction: Do fibroblast growth factors strike a cord? Curr. Biol. 6, 672-675.   DOI
21 Nieuwkoop, P. (1952). Activation and organization of the central nervous system in amphibians. Part III. Synthesis of a new working hypothesis. J. Exp. Zool. 120, 83-108.   DOI
22 Nieuwkoop, P.D., and Faber, J. (1956). Normal table of Xenopus laevis (Daudin).. A systematical and chronological survey of the development from the fertilized egg till the end of metamorphosis. (Amsterdam: North-Holland Publishing Company. Guilders).
23 Ray, W.J., Bain, G., Yao, M., and Gottlieb, D.I. (1997). Cyp26, a novel mammalian cytochrome P450, is induced by retinoic acid and defines a new family. J. Biol. Chem. 272, 18702-18708.   DOI
24 Ruiz i Altaba, A., and Jessell, T.M (1991). Retinoic acid modifies the pattern of cell differentiation in the central nervous system of neurula stage Xenopus embryos. Development 112, 945-958.
25 Sakai, Y., Meno, C., Fujii, H., Nishino, J., Shiratori, H., Saijoh, Y., Rossant, J., and Hamada, H. (2001). The retinoic acidinactivating enzyme Cyp26 is essential for establishing an uneven distribution of retinoic acid along the anterio-posterior axis within the mouse embryo. Genes Dev. 15, 213-225.   DOI
26 Schmidt, J., Francois, V., Bier, E., and Kimelman, D. (1995). Drosophila short gastrulation induces an ectopic axis in Xenopus: evidence for conserved mechanisms of dorsal-ventral patterning. Development 121, 4319-4328.
27 Sirbu, I.O., Gresh, L., Barra, J., and Duester, G. (2005). Shifting boundaries of retinoic acid activity control hindbrain segmental gene expression. Development 132, 2611-2622.   DOI
28 Suzuki, A., Thies, R.S., Yamaji, N., Song, J.J., Wozney, J.M., Murakami, K., and Ueno, N. (1994). A truncated bone morphogenetic protein receptor affects dorsal-ventral patterning in the early Xenopus embryo. Proc. Natl. Acad. Sci. USA 91, 10255-10259.   DOI
29 Smith, J., and Slack, J. (1983). Dorsalization and neural induction: properties of the organizer in Xenopus laevis. J. Embryol. Exp. Morphol. 78, 299-317.
30 Summerton, J., and Weller, D. (1997). Morpholino antisense oligomers: design, preparation, and properties. Antisense Nucleic Acid Drug Dev. 7, 187-195.   DOI
31 Tahayato, A., Dollé, P., and Petkovich, M. (2003). Cyp26C1 encodes a novel retinoic acid-metabolizing enzyme expressed in the hindbrain, inner ear, first branchial arch and tooth buds during murine development. Gene Expr. Patterns 3, 449-454.   DOI
32 Tanibe, M., Michiue, T., Yukita, A., Danno, H., Ikuzawa, M., Ishiura, S., and Asashima, M. (2008). Retinoic acid metabolizing factor xCyp26c is specifically expressed in neuroectoderm and regulates anterior neural patterning in Xenopus laevis. Int. J. Dev. Biol. 52, 893-901.   DOI
33 Wawersik, S., Evola, C., and Whitman, M. (2005). Conditional BMP inhibition in Xenopus reveals stage-specific roles for BMPs in neural and neural crest induction. Dev. Biol. 277, 425-442.   DOI
34 White, J.A., Guo, Y.-D., Baetz, K., Beckett-Jones, B., Bonasoro, J., Hsu, K.E., Dilworth, F.J., Jones, G., and Petkovich, M. (1996). Identification of the retinoic acid-inducible all-trans-retinoic acid 4- hydroxylase. J. Biol. Chem. 271, 29922-29927.   DOI
35 Xu, R.-H., Kim, J., Taira, M., Zhan, S., Sredni, D., and Kung, H. (1995). A dominant negative bone morphogenetic protein 4 receptor causes neuralization in Xenopus ectoderm. Biochem. Biophys. Res. Commun. 212, 212-219.   DOI
36 Yoon, J., Kim, J.-H., Lee, S.-Y., Kim, S., Park, J.-B., Lee, J.-Y., and Kim, J. (2014b). PV. 1 induced by FGF-Xbra functions as a repressor of neurogenesis in Xenopus embryos. BMB Rep. 47, 673.   DOI
37 Xu, R.H., Kim, J., Taira, M., Sredni, D., and Kung, H. (1997). Studies on the role of fibroblast growth factor signaling in neurogenesis using conjugated/aged animal caps and dorsal ectoderm-grafted embryos. J. Neurosci. 17, 6892-6898.   DOI
38 Xu, R.-H., Ault, K.T., Kim, J., Park, M.-J., Hwang, Y.-S., Peng, Y., Sredni, D., and Kung, H.-f. (1999). Opposite effects of FGF and BMP-4 on embryonic blood formation: roles of PV. 1 and GATA-2. Dev. Biol. 208, 352-361.   DOI
39 Yoon, J., Kim, J.H., Kim, S.C., Park, J.B., Lee, J.Y., and Kim, J. (2014a). PV. 1 suppresses the expression of FoxD5b during neural induction in Xenopus embryos. Mol. Cells 37, 220-225.   DOI
40 Abu-Abed, S., Dollé, P., Metzger, D., Beckett, B., Chambon, P. and Petkovich, M. (2001). The retinoic acid-metabolizing enzyme, Cyp26A1, is essential for normal hindbrain patterning, vertebral identity, and development of posterior structures. Genes Dev. 15, 226-240.   DOI
41 Doniach, T. (1995). Basic FGF as an inducer of anteroposterior neural pattern. Cell 83, 1067-1070.   DOI
42 Blumberg, B., Bolado, J., Moreno, T.A., Kintner, C., Evans, R.M. and Papalopulu, N. (1997). An essential role for retinoid signaling in anteroposterior neural patterning. Development 124, 373-379.
43 Dale, L., Howes, G., Price, B. and Smith, J. (1992). Bone morphogenetic protein 4: a ventralizing factor in early Xenopus development. Development 115, 573-585.
44 de Roos, K., Sonneveld, E., Compaan, B., ten Berge, D., Durston, A.J. and van der Saag, P.T. (1999). Expression of retinoic acid 4- hydroxylase (Cyp26). during mouse and Xenopus laevis embryogenesis. Mech. Dev. 82, 205-211.   DOI
45 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 124, 2325-2334.
46 Fujii, H., Sato, T., Kaneko, S., Gotoh, O., Fujii‐Kuriyama, Y., Osawa, K., Kato, S. and Hamada, H. (1997). Metabolic inactivation of retinoic acid by a novel P450 differentially expressed in developing mouse embryos. EMBO J. 16, 4163-4173.   DOI
47 Gamse, J. and Sive, H. (2000). Vertebrate anteroposterior patterning: the Xenopus neurectoderm as a paradigm. BioEssays 22, 976-986.   DOI
48 Gavalas, A. and Krumlauf, R. (2000). Retinoid signalling and hindbrain patterning. Curr. Opin. Genet. Dev. 10, 380-386.   DOI
49 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.   DOI