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http://dx.doi.org/10.14348/molcells.2021.0055

Goosecoid Controls Neuroectoderm Specification via Dual Circuits of Direct Repression and Indirect Stimulation in Xenopus Embryos  

Umair, Zobia (Department of Biochemistry, Institute of Cell Differentiation and Aging, College of Medicine, Hallym University)
Kumar, Vijay (Department of Biochemistry, Institute of Cell Differentiation and Aging, College of Medicine, Hallym University)
Goutam, Ravi Shankar (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)
Kim, Jaebong (Department of Biochemistry, Institute of Cell Differentiation and Aging, College of Medicine, Hallym University)
Publication Information
Molecules and Cells / v.44, no.10, 2021 , pp. 723-735 More about this Journal
Abstract
Spemann organizer is a center of dorsal mesoderm and itself retains the mesoderm character, but it has a stimulatory role for neighboring ectoderm cells in becoming neuroectoderm in gastrula embryos. Goosecoid (Gsc) overexpression in ventral region promotes secondary axis formation including neural tissues, but the role of gsc in neural specification could be indirect. We examined the neural inhibitory and stimulatory roles of gsc in the same cell and neighboring cells contexts. In the animal cap explant system, Gsc overexpression inhibited expression of neural specific genes including foxd4l1.1, zic3, ncam, and neurod. Genome-wide chromatin immunoprecipitation sequencing (ChIP-seq) and promoter analysis of early neural genes of foxd4l1.1 and zic3 were performed to show that the neural inhibitory mode of gsc was direct. Site-directed mutagenesis and serially deleted construct studies of foxd4l1.1 promoter revealed that Gsc directly binds within the foxd4l1.1 promoter to repress its expression. Conjugation assay of animal cap explants was also performed to demonstrate an indirect neural stimulatory role for gsc. The genes for secretory molecules, Chordin and Noggin, were up-regulated in gsc injected cells with the neural fate only achieved in gsc uninjected neighboring cells. These experiments suggested that gsc regulates neuroectoderm formation negatively when expressed in the same cell and positively in neighboring cells via soluble factors. One is a direct suppressive circuit of neural genes in gsc expressing mesoderm cells and the other is an indirect stimulatory circuit for neurogenesis in neighboring ectoderm cells via secreted BMP antagonizers.
Keywords
chordin; dorsal organizer; Gsc; Gsc response element; neuroectoderm; Noggin; transcriptional regulation; Xenopus;
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1 Seiliez, I., Thisse, B., and Thisse, C. (2006). FoxA3 and goosecoid promote anterior neural fate through inhibition of Wnt8a activity before the onset of gastrulation. Dev. Biol. 290, 152-163.   DOI
2 Sherman, J.H., Karpinski, B.A., Fralish, M.S., Cappuzzo, J.M., Dhindsa, D.S., Thal, A.G., Moody, S.A., LaMantia, A.S., and Maynard, T.M. (2017). Foxd4 is essential for establishing neural cell fate and for neuronal differentiation. Genesis 55, e23031.   DOI
3 Smith, S.T. and Jaynes, J.B. (1996). A conserved region of engrailed, shared among all en-, gsc-, Nk1-, Nk2- and msh-class homeoproteins, mediates active transcriptional repression in vivo. Development 122, 3141-3150.   DOI
4 Spemann, H. (1967). Embryonic Development and Induction (New York: Hafner Publishing Company).
5 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 C-terminal domain. Dev. Biol. 232, 439-457.   DOI
6 Fetka, I., Doederlein, G., and Bouwmeester, T. (2000). Neuroectodermal specification and regionalization of the Spemann organizer in Xenopus. Mech. Dev. 93, 49-58.   DOI
7 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.   DOI
8 Katoh, M. and Katoh, M. (2004). Human FOX gene family (Review). Int. J. Oncol. 25, 1495-1500.
9 Kumar, V., Umair, Z., Kumar, S., Lee, U., and Kim, J. (2021). Smad2 and Smad3 differentially modulate chordin transcription via direct binding on the distal elements in gastrula Xenopus embryos. Biochem. Biophys. Res. Commun. 559, 168-175.   DOI
10 Lee, S.Y., Lee, H.S., Moon, J.S., Kim, J.I., Park, J.B., Lee, J.Y., Park, M.J., and Kim, J. (2004). Transcriptional regulation of Zic3 by heterodimeric AP-1(c-Jun/c-Fos) during Xenopus development. Exp. Mol. Med. 36, 468-475.   DOI
11 Roskoski, R., Jr. (2020). Properties of FDA-approved small molecule protein kinase inhibitors: a 2020 update. Pharmacol. Res. 152, 104609.   DOI
12 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.   DOI
13 Niehrs, C., Steinbeisser, H., and De Robertis, E.M. (1994). Mesodermal patterning by a gradient of the vertebrate homeobox gene goosecoid. Science 263, 817-820.   DOI
14 Oelgeschlager, M., Kuroda, H., Reversade, B., and De Robertis, E.M. (2003). Chordin is required for the Spemann organizer transplantation phenomenon in Xenopus embryos. Dev. Cell 4, 219-230.   DOI
15 Shim, S., Bae, N., Park, S.Y., Kim, W.S., and Han, J.K. (2005). Isolation of Xenopus FGF-8b and comparison with FGF-8a. Mol. Cells 19, 310-317.
16 Borchers, A. and Pieler, T. (2010). Programming pluripotent precursor cells derived from Xenopus embryos to generate specific tissues and organs. Genes (Basel) 1, 413-426.   DOI
17 Umair, Z., Kumar, S., Kim, D.H., Rafiq, K., Kumar, V., Kim, S., Park, J.B., Lee, J.Y., Lee, U., and Kim, J. (2018). Ventx1.1 as a direct repressor of early neural gene zic3 in Xenopus laevis. Mol. Cells 41, 1061-1071.
18 Umair, Z., Kumar, S., Rafiq, K., Kumar, V., Reman, Z.U., Lee, S.H., Kim, S., Lee, J.Y., Lee, U., and Kim, J. (2020). Dusp1 modulates activin/smad2 mediated germ layer specification via FGF signal inhibition in Xenopus embryos. Anim. Cells Syst. (Seoul) 24, 359-370.   DOI
19 Beddington, R.S. and Robertson, E.J. (1999). Axis development and early asymmetry in mammals. Cell 96, 195-209.   DOI
20 Blythe, S.A., Reid, C.D., Kessler, D.S., and Klein, P.S. (2009). Chromatin immunoprecipitation in early Xenopus laevis embryos. Dev. Dyn. 238, 1422-1432.   DOI
21 Cho, K.W., Blumberg, B., Steinbeisser, H., and De Robertis, E.M. (1991). Molecular nature of Spemann's organizer: the role of the Xenopus homeobox gene goosecoid. Cell 67, 1111-1120.   DOI
22 De Robertis, E.M., Blum, M., Niehrs, C., and Steinbeisser, H. (1992). Goosecoid and the organizer. Dev. Suppl. 167-171.
23 Dixon Fox, M. and Bruce, A.E. (2009). Short- and long-range functions of Goosecoid in zebrafish axis formation are independent of Chordin, Noggin 1 and Follistatin-like 1b. Development 136, 1675-1685.   DOI
24 Artinger, M., Blitz, I., Inoue, K., Tran, U., and Cho, K.W. (1997). Interaction of goosecoid and brachyury in Xenopus mesoderm patterning. Mech. Dev. 65, 187-196.   DOI
25 Zhang, Y., Liu, T., Meyer, C.A., Eeckhoute, J., Johnson, D.S., Bernstein, B.E., Nusbaum, C., Myers, R.M., Brown, M., Li, W., et al. (2008). Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9, R137.   DOI
26 Yasuo, H. and Lemaire, P. (2001). Role of Goosecoid, Xnot and Wnt antagonists in the maintenance of the notochord genetic programme in Xenopus gastrulae. Development 128, 3783-3793.   DOI
27 Yoon, J., Kim, J.H., Lee, O.J., Lee, S.Y., Lee, S.H., Park, J.B., Lee, J.Y., Kim, S.C., and Kim, J. (2013). AP-1(c-Jun/FosB) mediates xFoxD5b expression in Xenopus early developmental neurogenesis. Int. J. Dev. Biol. 57, 865-872.   DOI
28 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.   DOI
29 Yao, J. and Kessler, D.S. (2001). Goosecoid promotes head organizer activity by direct repression of Xwnt8 in Spemann's organizer. Development 128, 2975-2987.   DOI
30 Harland, R. and Gerhart, J. (1997). Formation and function of Spemann's organizer. Annu. Rev. Cell Dev. Biol. 13, 611-667.   DOI
31 Kumar, S., Umair, Z., Kumar, V., Lee, U., Choi, S.C., and Kim, J. (2019). Ventx1.1 competes with a transcriptional activator Xcad2 to regulate negatively its own expression. BMB Rep. 52, 403-408.   DOI
32 Niehrs, C., Keller, R., Cho, K.W., and De Robertis, E.M. (1993). The homeobox gene goosecoid controls cell migration in Xenopus embryos. Cell 72, 491-503.   DOI
33 Mailhos, C., Andre, S., Mollereau, B., Goriely, A., Hemmati-Brivanlou, A., and Desplan, C. (1998). Drosophila Goosecoid requires a conserved heptapeptide for repression of paired-class homeoprotein activators. Development 125, 937-947.   DOI
34 Rivera-Perez, J.A., Mallo, M., Gendron-Maguire, M., Gridley, T., and Behringer, R.R. (1995). Goosecoid is not an essential component of the mouse gastrula organizer but is required for craniofacial and rib development. Development 121, 3005-3012.   DOI
35 Sasai, Y., Lu, B., Steinbeisser, H., Geissert, D., Gont, L.K., and De Robertis, E.M. (1994). Xenopus chordin: a novel dorsalizing factor activated by organizer-specific homeobox genes. Cell 79, 779-790.   DOI
36 Thisse, C., Thisse, B., Halpern, M.E., and Postlethwait, J.H. (1994). Goosecoid expression in neurectoderm and mesendoderm is disrupted in zebrafish cyclops gastrulas. Dev. Biol. 164, 420-429.   DOI
37 Christian, J.L. and Moon, R.T. (1993). Interactions between Xwnt-8 and Spemann organizer signaling pathways generate dorsoventral pattern in the embryonic mesoderm of Xenopus. Genes Dev. 7, 13-28.   DOI
38 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.   DOI
39 Lee, H.K., Lee, H.S., and Moody, S.A. (2014). Neural transcription factors: from embryos to neural stem cells. Mol. Cells 37, 705-712.   DOI
40 Lemaire, P. and Kodjabachian, L. (1996). The vertebrate organizer: structure and molecules. Trends Genet. 12, 525-531.   DOI
41 Neilson, K.M., Klein, S.L., Mhaske, P., Mood, K., Daar, I.O., and Moody, S.A. (2012). Specific domains of FoxD4/5 activate and repress neural transcription factor genes to control the progression of immature neural ectoderm to differentiating neural plate. Dev. Biol. 365, 363-375.   DOI
42 Nieto, M.A. (1999). Reorganizing the organizer 75 years on. Cell 98, 417-425.   DOI
43 Nieuwkoop, P.D. and Nigtevecht, G.V. (1954). Neural activation and transformation in explants of competent ectoderm under the influence of fragments of anterior notochord in urodeles. Development 2, 175-193.   DOI
44 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.   DOI
45 De Robertis, E.M. and Kuroda, H. (2004). Dorsal-ventral patterning and neural induction in Xenopus embryos. Annu. Rev. Cell Dev. Biol. 20, 285-308.   DOI
46 Ryu, H., Lee, H., Lee, J., Noh, H., Shin, M., Kumar, V., Hong, S., Kim, J., and Park, S. (2021). The molecular dynamics of subdistal appendages in multi-ciliated cells. Nat. Commun. 12, 612.   DOI
47 Sander, V., Reversade, B., and De Robertis, E.M. (2007). The opposing homeobox genes Goosecoid and Vent1/2 self-regulate Xenopus patterning. EMBO J. 26, 2955-2965.   DOI
48 Danilov, V., Blum, M., Schweickert, A., Campione, M., and Steinbeisser, H. (1998). Negative autoregulation of the organizer-specific homeobox gene goosecoid. J. Biol. Chem. 273, 627-635.   DOI
49 Latinkic, B.V., Umbhauer, M., Neal, K.A., Lerchner, W., Smith, J.C., and Cunliffe, V. (1997). The Xenopus Brachyury promoter is activated by FGF and low concentrations of activin and suppressed by high concentrations of activin and by paired-type homeodomain proteins. Genes Dev. 11, 3265-3276.   DOI
50 Steinbeisser, H., Fainsod, A., Niehrs, C., Sasai, Y., and De Robertis, E.M. (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.   DOI
51 Harland, R. (2000). Neural induction. Curr. Opin. Genet. Dev. 10, 357-362.   DOI
52 De Robertis, E.M., Larrain, J., Oelgeschlager, M., and Wessely, O. (2000). The establishment of Spemann's organizer and patterning of the vertebrate embryo. Nat. Rev. Genet. 1, 171-181.   DOI
53 Fainsod, A., Steinbeisser, H., and De Robertis, E.M. (1994). On the function of BMP-4 in patterning the marginal zone of the Xenopus embryo. EMBO J. 13, 5015-5025.   DOI
54 Ferreiro, B., Artinger, M., Cho, K., and Niehrs, C. (1998). Antimorphic goosecoids. Development 125, 1347-1359.   DOI
55 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.   DOI
56 Katoh, M., Igarashi, M., Fukuda, H., Nakagama, H., and Katoh, M. (2013). Cancer genetics and genomics of human FOX family genes. Cancer Lett. 328, 198-206.   DOI
57 Kumar, S., Umair, Z., Kumar, V., Kumar, S., Lee, U., and Kim, J. (2020). Foxd4l1.1 negatively regulates transcription of neural repressor ventx1.1 during neuroectoderm formation in Xenopus embryos. Sci. Rep. 10, 16780.   DOI
58 Kuroda, H., Wessely, O., and De Robertis, E.M. (2004). Neural induction in Xenopus: requirement for ectodermal and endomesodermal signals via Chordin, Noggin, beta-Catenin, and Cerberus. PLoS Biol. 2, E92.   DOI
59 Latinkic, B.V. and Smith, J.C. (1999). Goosecoid and mix.1 repress Brachyury expression and are required for head formation in Xenopus. Development 126, 1769-1779.   DOI
60 Yan, B., Neilson, K.M., and Moody, S.A. (2009). foxD5 plays a critical upstream role in regulating neural ectodermal fate and the onset of neural differentiation. Dev. Biol. 329, 80-95.   DOI
61 Yoon, J., Kim, J.H., Kim, S.C., Park, J.B., Lee, J.Y., and Kim, J. (2014). PV.1 suppresses the expression of FoxD5b during neural induction in Xenopus embryos. Mol. Cells 37, 220-225.   DOI
62 Yu, S.B., Umair, Z., Kumar, S., Lee, U., Lee, S.H., Kim, J.I., Kim, S., Park, J.B., Lee, J.Y., and Kim, J. (2016). xCyp26c induced by inhibition of BMP signaling is involved in anterior-posterior neural patterning of Xenopus laevis. Mol. Cells 39, 352-357.   DOI
63 Ulmer, B., Tingler, M., Kurz, S., Maerker, M., Andre, P., Monch, D., Campione, M., Deissler, K., Lewandoski, M., Thumberger, T., et al. (2017). A novel role of the organizer gene Goosecoid as an inhibitor of Wnt/PCP-mediated convergent extension in Xenopus and mouse. Sci. Rep. 7, 43010.   DOI