119
Notch Signaling in Early Embryogenesis
Hein, K., Mittler, G., Cizelsky, W., Kühl, M., Ferrante, F., Liefke, R.,
Berger, I.M., Just, S., Sträng, J.E., Kestler, H.A., Oswald, F.,
Borggrefe, T., 2015. Site-specifc methylation of Notch1 controls the amplitude and duration of the Notch1 response. Sci.
Signal. 8, ra30. https://doi.org/10.1126/scisignal.2005892
Heitzler, P., 2010. Biodiversity and noncanonical Notch signaling.
Curr. Top. Dev. Biol. 92, 457–481. https://doi.org/10.1016/
S0070-2153(10)92014-0
Hindley, C., Ali, F., McDowell, G., Cheng, K., Jones, A., Guillemot,
F., Philpott, A., 2012. Post-translational modif cation of
Ngn2 differentially affects transcription of distinct targets
to regulate the balance between progenitor maintenance and
differentiation. Development 139, 1718–1723. https://doi.
org/10.1242/dev.077552
Hitachi, K., Danno, H., Tazumi, S., Aihara, Y., Uchiyama, H.,
Okabayashi, K., Kondow, A., Asashima, M., 2009. The
Xenopus Bowline/Ripply family proteins negatively regulate the transcriptional activity of T-box transcription factors. Int. J. Dev. Biol. 53, 631–639. https://doi.org/10.1387/
ijdb.082823kh
Hitachi, K., Kondow,A., Danno, H., Inui, M., Uchiyama, H., Asashima,
M., 2008. Tbx6, Thylacine1, and E47 synergistically activate
bowline expression in Xenopus somitogenesis. Dev. Biol. 313,
816–828. https://doi.org/10.1016/J.YDBIO.2007.10.015
Hong, C.-S., Saint-Jeannet, J.-P., 2018. The b-HLH transcription
factor Hes3 participates in neural plate border formation by
interfering with Wnt/β-catenin signaling. Dev. Biol. 442,
162–172. https://doi.org/10.1016/j.ydbio.2018.07.011
Howell, M., Inman, G.J., Hill, C.S., 2002. A novel Xenopus Smadinteracting forkhead transcription factor (XFast-3) cooperates with XFast-1 in regulating gastrulation movements.
Development 129, 2823–2834.
Huang, C., Chan, J. A., Schuurmans, C., 2014. Proneural bHLH genes
in development and disease. Curr. Top. Dev. Biol. 110, 75–127.
https://doi.org/10.1016/B978-0-12-405943-6.00002-6
Hubaud, A., Pourquié, O., 2014. Signalling dynamics in vertebrate
segmentation. Nat. Rev. Mol. Cell Biol. 15, 709–721. https://
doi.org/10.1038/nrm3891
Hufton, A.L., Vinayagam, A., Suhai, S., Baker, J.C., 2006. Genomic
analysis of Xenopus organizer function. BMC Dev. Biol. 6,
27. https://doi.org/10.1186/1471-213X-6-27
Imayoshi, I., Kageyama, R., 2014. Oscillatory control of bHLH
factors in neural progenitors. Trends Neurosci 37, 531–538.
https://doi.org/10.1016/j.tins.2014.07.006
Ito, M., Katada, T., Miyatani, S., Kinoshita, T., 2007a. XSu(H)2 is
an essential factor for gene expression and morphogenesis of
the Xenopus gastrula embryo. Int. J. Dev. Biol. 51, 27–36.
https://doi.org/10.1387/ijdb.062211mi
Ito, M., Nishitani, E., Kinoshita, T., 2007b. Xenopus suppressor
of Hairless 2 is involved in the cell fate decision during gastrulation through the transcriptional regulation of Xoct25/91.
Biochem. Biophys. Res. Commun. 353, 644–649. https://doi.
org/10.1016/j.bbrc.2006.12.087
Janesick, A., Tang, W., Nguyen, T.T.L., Blumberg, B., 2017. RARβ2
is required for vertebrate somitogenesis. Development 144,
1997–2008. https://doi.org/10.1242/dev.144345
Jen, W.C., Gawantka, V., Pollet, N., Niehrs, C., Kintner, C., 1999.
Periodic repression of Notch pathway genes governs the segmentation of Xenopus embryos. Genes Dev. 13, 1486–1499.
https://doi.org/10.1101/gad.13.11.1486
Jen, W.C., Wettstein, D., Turner, D., Chitnis, A., Kintner, C., 1997.
The Notch ligand, X-Delta-2, mediates segmentation of the
paraxial mesoderm in Xenopus embryos. Development 124,
1169–1178.
Jorissen, E., De Strooper, B., 2010. Gamma-secretase and the intramembrane proteolysis of Notch. Curr. Top. Dev. Biol. 92,
201–230. https://doi.org/10.1016/S0070-2153(10)92006-1
Kageyama, R., Ohtsuka, T., Kobayashi, T., 2007. The Hes gene family: Repressors and oscillators that orchestrate embryogenesis. Development 134, 1243–1251. https://doi.org/10.1242/
dev.000786
Kao, H.Y., Ordentlich, P., Koyano-Nakagawa, N., Tang, Z., Downes,
M., Kintner, C.R., Evans, R.M., Kadesch, T., 1998. A histone
deacetylase corepressor complex regulates the Notch signal
transduction pathway. Genes Dev. 12, 2269–2277. https://
doi.org/10.1101/gad.12.15.2269
Karimi, K., Fortriede, J.D., Lotay, V.S., Burns, K.A., Wang,
D.Z., Fisher, M.E., Pells, T.J., James-Zorn, C., Wang, Y.,
Ponferrada, V.G., Chu, S., Chaturvedi, P., Zorn, A.M., Vize,
P.D., 2018. Xenbase: A genomic, epigenomic and transcriptomic model organism database. Nucleic Acids Res 46,
D861–D868. https://doi.org/10.1093/nar/gkx936
Katada, T., Kinoshita, T., 2003. XMam1, the Xenopus homologue of mastermind, is essential to primary neurogenesis
in Xenopus laevis embryos. Int. J. Dev. Biol. 47, 397–404.
https://doi.org/10.1387/IJDB.14584777
Keller, R., Danilchik, M., 1988. Regional expression, pattern and
timing of convergence and extension during gastrulation of
Xenopus laevis. Development 103, 193–209.
Kenyon, K.L., Moody, S.A., Jamrich, M., 1999. A novel fork head
gene mediates early steps during Xenopus lens formation.
Development 126, 5107–5116.
Kiecker, C., Niehrs, C., 2001. The role of prechordal mesendoderm
in neural patterning. Curr. Opin. Neurobiol. 11, 27–33.
Kim, S.H., Jen, W.C., De Robertis, E.M., Kintner, C., 2000. The
protocadherin PAPC establishes segmental boundaries during somitogenesis in xenopus embryos. Curr. Biol. 10, 821–
830.
Kinoshita, T., Haruta, Y., Sakamoto, C., Imaoka, S., 2011.
Antagonistic role of XESR1 and XESR5 in mesoderm formation in Xenopus laevis. Int. J. Dev. Biol. 55, 25–31. https://
doi.org/10.1387/ijdb.092990tk
Kirby, M.L., Lawson, A., Stadt, H.A., Kumiski, D.H., Wallis, K.T.,
McCraney, E., Waldo, K.L., Li, Y.-X., Schoenwolf, G.C.,
2003. Hensen’s node gives rise to the ventral midline of the
foregut: Implications for organizing head and heart development. Dev. Biol. 253, 175–188. https://doi.org/10.1016/
S0012-1606(02)00024-6
Kirmizitas, A., Meiklejohn, S., Ciau-Uitz, A., Stephenson, R.,
Patient, R., 2017. Dissecting BMP signaling input into the
gene regulatory networks driving specifcation of the blood
stem cell lineage. Proc. Natl. Acad. Sci. U. S. A. 114, 5814–
5821. https://doi.org/10.1073/pnas.1610615114
Kiyota, T., Jono, H., Kuriyama, S., Hasegawa, K., Miyatani, S.,
Kinoshita, T., 2001. X-Serrate-1 is involved in primary neurogenesis in Xenopus laevis in a complementary manner
with X-Delta-1. Dev. Genes Evol. 211, 367–376. https://doi.
org/10.1007/s004270100165
Kiyota, T., Kinoshita, T., 2004. The intracellular domain of
X-Serrate-1 is cleaved and suppresses primary neurogenesis
in Xenopus laevis. Mech. Dev. 121, 573–585. https://doi.
org/10.1016/j.mod.2004.03.034
Kjolby, R.A.S., Harland, R.M., 2017. Genome-wide identif cation
of Wnt/β-catenin transcriptional targets during Xenopus gastrulation. Dev. Biol. 426, 165–175. https://doi.org/10.1016/j.
ydbio.2016.03.021
Kondow, A., Hitachi, K., Ikegame, T., Asashima, M., 2006. Bowline,
a novel protein localized to the presomitic mesoderm,
Notch Signaling in Early Embryogenesis
Hein, K., Mittler, G., Cizelsky, W., Kühl, M., Ferrante, F., Liefke, R.,
Berger, I.M., Just, S., Sträng, J.E., Kestler, H.A., Oswald, F.,
Borggrefe, T., 2015. Site-specifc methylation of Notch1 controls the amplitude and duration of the Notch1 response. Sci.
Signal. 8, ra30. https://doi.org/10.1126/scisignal.2005892
Heitzler, P., 2010. Biodiversity and noncanonical Notch signaling.
Curr. Top. Dev. Biol. 92, 457–481. https://doi.org/10.1016/
S0070-2153(10)92014-0
Hindley, C., Ali, F., McDowell, G., Cheng, K., Jones, A., Guillemot,
F., Philpott, A., 2012. Post-translational modif cation of
Ngn2 differentially affects transcription of distinct targets
to regulate the balance between progenitor maintenance and
differentiation. Development 139, 1718–1723. https://doi.
org/10.1242/dev.077552
Hitachi, K., Danno, H., Tazumi, S., Aihara, Y., Uchiyama, H.,
Okabayashi, K., Kondow, A., Asashima, M., 2009. The
Xenopus Bowline/Ripply family proteins negatively regulate the transcriptional activity of T-box transcription factors. Int. J. Dev. Biol. 53, 631–639. https://doi.org/10.1387/
ijdb.082823kh
Hitachi, K., Kondow,A., Danno, H., Inui, M., Uchiyama, H., Asashima,
M., 2008. Tbx6, Thylacine1, and E47 synergistically activate
bowline expression in Xenopus somitogenesis. Dev. Biol. 313,
816–828. https://doi.org/10.1016/J.YDBIO.2007.10.015
Hong, C.-S., Saint-Jeannet, J.-P., 2018. The b-HLH transcription
factor Hes3 participates in neural plate border formation by
interfering with Wnt/β-catenin signaling. Dev. Biol. 442,
162–172. https://doi.org/10.1016/j.ydbio.2018.07.011
Howell, M., Inman, G.J., Hill, C.S., 2002. A novel Xenopus Smadinteracting forkhead transcription factor (XFast-3) cooperates with XFast-1 in regulating gastrulation movements.
Development 129, 2823–2834.
Huang, C., Chan, J. A., Schuurmans, C., 2014. Proneural bHLH genes
in development and disease. Curr. Top. Dev. Biol. 110, 75–127.
https://doi.org/10.1016/B978-0-12-405943-6.00002-6
Hubaud, A., Pourquié, O., 2014. Signalling dynamics in vertebrate
segmentation. Nat. Rev. Mol. Cell Biol. 15, 709–721. https://
doi.org/10.1038/nrm3891
Hufton, A.L., Vinayagam, A., Suhai, S., Baker, J.C., 2006. Genomic
analysis of Xenopus organizer function. BMC Dev. Biol. 6,
27. https://doi.org/10.1186/1471-213X-6-27
Imayoshi, I., Kageyama, R., 2014. Oscillatory control of bHLH
factors in neural progenitors. Trends Neurosci 37, 531–538.
https://doi.org/10.1016/j.tins.2014.07.006
Ito, M., Katada, T., Miyatani, S., Kinoshita, T., 2007a. XSu(H)2 is
an essential factor for gene expression and morphogenesis of
the Xenopus gastrula embryo. Int. J. Dev. Biol. 51, 27–36.
https://doi.org/10.1387/ijdb.062211mi
Ito, M., Nishitani, E., Kinoshita, T., 2007b. Xenopus suppressor
of Hairless 2 is involved in the cell fate decision during gastrulation through the transcriptional regulation of Xoct25/91.
Biochem. Biophys. Res. Commun. 353, 644–649. https://doi.
org/10.1016/j.bbrc.2006.12.087
Janesick, A., Tang, W., Nguyen, T.T.L., Blumberg, B., 2017. RARβ2
is required for vertebrate somitogenesis. Development 144,
1997–2008. https://doi.org/10.1242/dev.144345
Jen, W.C., Gawantka, V., Pollet, N., Niehrs, C., Kintner, C., 1999.
Periodic repression of Notch pathway genes governs the segmentation of Xenopus embryos. Genes Dev. 13, 1486–1499.
https://doi.org/10.1101/gad.13.11.1486
Jen, W.C., Wettstein, D., Turner, D., Chitnis, A., Kintner, C., 1997.
The Notch ligand, X-Delta-2, mediates segmentation of the
paraxial mesoderm in Xenopus embryos. Development 124,
1169–1178.
Jorissen, E., De Strooper, B., 2010. Gamma-secretase and the intramembrane proteolysis of Notch. Curr. Top. Dev. Biol. 92,
201–230. https://doi.org/10.1016/S0070-2153(10)92006-1
Kageyama, R., Ohtsuka, T., Kobayashi, T., 2007. The Hes gene family: Repressors and oscillators that orchestrate embryogenesis. Development 134, 1243–1251. https://doi.org/10.1242/
dev.000786
Kao, H.Y., Ordentlich, P., Koyano-Nakagawa, N., Tang, Z., Downes,
M., Kintner, C.R., Evans, R.M., Kadesch, T., 1998. A histone
deacetylase corepressor complex regulates the Notch signal
transduction pathway. Genes Dev. 12, 2269–2277. https://
doi.org/10.1101/gad.12.15.2269
Karimi, K., Fortriede, J.D., Lotay, V.S., Burns, K.A., Wang,
D.Z., Fisher, M.E., Pells, T.J., James-Zorn, C., Wang, Y.,
Ponferrada, V.G., Chu, S., Chaturvedi, P., Zorn, A.M., Vize,
P.D., 2018. Xenbase: A genomic, epigenomic and transcriptomic model organism database. Nucleic Acids Res 46,
D861–D868. https://doi.org/10.1093/nar/gkx936
Katada, T., Kinoshita, T., 2003. XMam1, the Xenopus homologue of mastermind, is essential to primary neurogenesis
in Xenopus laevis embryos. Int. J. Dev. Biol. 47, 397–404.
https://doi.org/10.1387/IJDB.14584777
Keller, R., Danilchik, M., 1988. Regional expression, pattern and
timing of convergence and extension during gastrulation of
Xenopus laevis. Development 103, 193–209.
Kenyon, K.L., Moody, S.A., Jamrich, M., 1999. A novel fork head
gene mediates early steps during Xenopus lens formation.
Development 126, 5107–5116.
Kiecker, C., Niehrs, C., 2001. The role of prechordal mesendoderm
in neural patterning. Curr. Opin. Neurobiol. 11, 27–33.
Kim, S.H., Jen, W.C., De Robertis, E.M., Kintner, C., 2000. The
protocadherin PAPC establishes segmental boundaries during somitogenesis in xenopus embryos. Curr. Biol. 10, 821–
830.
Kinoshita, T., Haruta, Y., Sakamoto, C., Imaoka, S., 2011.
Antagonistic role of XESR1 and XESR5 in mesoderm formation in Xenopus laevis. Int. J. Dev. Biol. 55, 25–31. https://
doi.org/10.1387/ijdb.092990tk
Kirby, M.L., Lawson, A., Stadt, H.A., Kumiski, D.H., Wallis, K.T.,
McCraney, E., Waldo, K.L., Li, Y.-X., Schoenwolf, G.C.,
2003. Hensen’s node gives rise to the ventral midline of the
foregut: Implications for organizing head and heart development. Dev. Biol. 253, 175–188. https://doi.org/10.1016/
S0012-1606(02)00024-6
Kirmizitas, A., Meiklejohn, S., Ciau-Uitz, A., Stephenson, R.,
Patient, R., 2017. Dissecting BMP signaling input into the
gene regulatory networks driving specifcation of the blood
stem cell lineage. Proc. Natl. Acad. Sci. U. S. A. 114, 5814–
5821. https://doi.org/10.1073/pnas.1610615114
Kiyota, T., Jono, H., Kuriyama, S., Hasegawa, K., Miyatani, S.,
Kinoshita, T., 2001. X-Serrate-1 is involved in primary neurogenesis in Xenopus laevis in a complementary manner
with X-Delta-1. Dev. Genes Evol. 211, 367–376. https://doi.
org/10.1007/s004270100165
Kiyota, T., Kinoshita, T., 2004. The intracellular domain of
X-Serrate-1 is cleaved and suppresses primary neurogenesis
in Xenopus laevis. Mech. Dev. 121, 573–585. https://doi.
org/10.1016/j.mod.2004.03.034
Kjolby, R.A.S., Harland, R.M., 2017. Genome-wide identif cation
of Wnt/β-catenin transcriptional targets during Xenopus gastrulation. Dev. Biol. 426, 165–175. https://doi.org/10.1016/j.
ydbio.2016.03.021
Kondow, A., Hitachi, K., Ikegame, T., Asashima, M., 2006. Bowline,
a novel protein localized to the presomitic mesoderm,