Acknowledgement
This article was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF), which is funded by the Ministry of Education, Science, and Technology of Korea (2016R1D1A1B02008770, 2018M3C7A1056285, and 2021M3H9A1097557).
References
- 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. https://doi.org/10.1016/S0925-4773(97)00073-7
- Beddington, R.S. and Robertson, E.J. (1999). Axis development and early asymmetry in mammals. Cell 96, 195-209. https://doi.org/10.1016/S0092-8674(00)80560-7
- 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. https://doi.org/10.1002/dvdy.21931
- 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. https://doi.org/10.3390/genes1030413
- 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. https://doi.org/10.1016/0092-8674(91)90288-a
- 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. https://doi.org/10.1101/gad.7.1.13
- 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. https://doi.org/10.1074/jbc.273.1.627
- De Robertis, E.M., Blum, M., Niehrs, C., and Steinbeisser, H. (1992). Goosecoid and the organizer. Dev. Suppl. 167-171.
- 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. https://doi.org/10.1146/annurev.cellbio.20.011403.154124
- 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. https://doi.org/10.1038/35042039
- 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. https://doi.org/10.1242/dev.031161
- 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. https://doi.org/10.1002/j.1460-2075.1994.tb06830.x
- Ferreiro, B., Artinger, M., Cho, K., and Niehrs, C. (1998). Antimorphic goosecoids. Development 125, 1347-1359. https://doi.org/10.1242/dev.125.8.1347
- 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
- Harland, R. (2000). Neural induction. Curr. Opin. Genet. Dev. 10, 357-362. https://doi.org/10.1016/S0959-437X(00)00096-4
- Harland, R. and Gerhart, J. (1997). Formation and function of Spemann's organizer. Annu. Rev. Cell Dev. Biol. 13, 611-667. https://doi.org/10.1146/annurev.cellbio.13.1.611
- 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
- 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. https://doi.org/10.1186/1479-7364-4-5-345
- 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. https://doi.org/10.1016/j.canlet.2012.09.017
- Katoh, M. and Katoh, M. (2004). Human FOX gene family (Review). Int. J. Oncol. 25, 1495-1500.
- 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. https://doi.org/10.1038/s41598-020-73662-4
- 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. https://doi.org/10.5483/bmbrep.2019.52.6.085
- 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. https://doi.org/10.1016/j.bbrc.2021.04.048
- 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. https://doi.org/10.1371/journal.pbio.0020092
- 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. https://doi.org/10.1242/dev.126.8.1769
- 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. https://doi.org/10.1101/gad.11.23.3265
- 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
- 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. https://doi.org/10.14348/MOLCELLS.2014.0227
- 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. https://doi.org/10.1038/emm.2004.59
- Lemaire, P. and Kodjabachian, L. (1996). The vertebrate organizer: structure and molecules. Trends Genet. 12, 525-531. https://doi.org/10.1016/S0168-9525(97)81401-1
- 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. https://doi.org/10.1242/dev.125.5.937
- 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
- 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. https://doi.org/10.1016/j.ydbio.2012.03.004
- 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. https://doi.org/10.1016/0092-8674(93)90069-3
- 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. https://doi.org/10.1126/science.7905664
- Nieto, M.A. (1999). Reorganizing the organizer 75 years on. Cell 98, 417-425. https://doi.org/10.1016/S0092-8674(00)81971-6
- 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. https://doi.org/10.1242/dev.2.3.175
- 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. https://doi.org/10.1016/S1534-5807(02)00404-5
- 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
- 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. https://doi.org/10.1242/dev.121.9.3005
- Roskoski, R., Jr. (2020). Properties of FDA-approved small molecule protein kinase inhibitors: a 2020 update. Pharmacol. Res. 152, 104609. https://doi.org/10.1016/j.phrs.2019.104609
- 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. https://doi.org/10.1038/s41467-021-20902-4
- 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. https://doi.org/10.1038/sj.emboj.7601705
- 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. https://doi.org/10.1016/0092-8674(94)90068-x
- 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. https://doi.org/10.1016/j.ydbio.2005.11.021
- 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. https://doi.org/10.1002/dvg.23031
- 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.
- 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. https://doi.org/10.1242/dev.122.10.3141
- Spemann, H. (1967). Embryonic Development and Induction (New York: Hafner Publishing Company).
- 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. https://doi.org/10.1002/j.1460-2075.1995.tb00208.x
- 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. https://doi.org/10.1006/dbio.2001.0191
- 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. https://doi.org/10.1006/dbio.1994.1212
- 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. https://doi.org/10.1038/srep43010
- 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.
- 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. https://doi.org/10.1080/19768354.2020.1847732
- 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. https://doi.org/10.1016/j.ydbio.2009.02.019
- 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. https://doi.org/10.1242/dev.128.15.2975
- 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. https://doi.org/10.1242/dev.128.19.3783
- 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. https://doi.org/10.14348/MOLCELLS.2014.2302
- 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. https://doi.org/10.1387/ijdb.130163jk
- 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
- 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. https://doi.org/10.14348/MOLCELLS.2016.0006
- 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. https://doi.org/10.1186/gb-2008-9-9-r137