117
Notch Signaling in Early Embryogenesis
involved in proliferation, apoptosis, cell-fate choice, signaling pathways, metabolism, and cytoskeletal regulators
(Bray and Bernard, 2010; Meier-Stiegen et al., 2010). The
discovery of new targets and modulators in Xenopus will be
essential to building Notch-regulated GRNs that control different developmental processes. microRNAs regulate Notch
signaling during multiciliogenesis in the epidermis (Marcet
et al., 2011), and RITA (RBPJ-interacting and tubulinassociated protein) negatively modulates Notch signaling
through nuclear export of RBPJ during primary neurogenesis (Wacker et al., 2011). It will be exciting to extend the
study of such modulations to the different contexts in which
Notch signaling operates.
REFERENCES
Acosta, H., López, S.L., Revinski, D.R., Carrasco, A.E., 2011. Notch
destabilises maternal beta-catenin and restricts dorsal-anterior
development in Xenopus. Development 138, 2567–2579.
https://doi.org/10.1242/dev.061143
Aguirre, C.E., Murgan, S., Carrasco, A.E., López, S.L., 2013. An
intact brachyury function is necessary to prevent spurious
axial development in Xenopus laevis. PLoS One 8, e54777.
https://doi.org/10.1371/journal.pone.0054777
Ali, F.R., Cheng, K., Kirwan, P., Metcalfe, S., Livesey, F.J., Barker,
R.A., Philpott, A., 2014. The phosphorylation status of Ascl1
is a key determinant of neuronal differentiation and maturation in vivo and in vitro. Development 141, 2216–2224.
https://doi.org/10.1242/dev.106377
Anderson, C., Stern, C.D., 2016. Organizers in development.
Curr. Top. Dev. Biol. 117, 435–454. https://doi.org/10.1016/
BS.CTDB.2015.11.023
Andreazzoli, M., Gestri, G., Cremisi, F., Casarosa, S., Dawid, I.B.,
Barsacchi, G., 2003. Xrx1 controls proliferation and neurogenesis in Xenopus anterior neural plate. Development 130,
5143–5154. https://doi.org/10.1242/dev.00665
Artavanis-Tsakonas, S., Grimwade, B.G., Harrison, R.G.,
Markopoulou, K., Muskavitch, M.A.T., Schlesinger-Bryant,
R., Wharton, K., Yedvobnick, B., 1983. The Notch locus of
Drosophila melanogaster: A molecular analysis. Dev. Genet.
4, 233–254. https://doi.org/10.1002/dvg.1020040403
Artinger, M., Blitz, I., Inoue, K., Tran, U., Cho, K.W., 1997.
Interaction of goosecoid and brachyury in Xenopus mesoderm patterning. Mech. Dev. 65, 187–196.
Beck, C., Slack, J.M., 1998. Analysis of the developing Xenopus
tail bud reveals separate phases of gene expression during
determination and outgrowth. Mech. Dev. 72, 41–52. https://
doi.org/10.1016/S0925-4773(98)00015-X
Bellefroid, E.J., Bourguignon, C., Hollemann, T., Ma, Q., Anderson,
D.J., Kintner, C., Pieler, T., 1996. X-MyT1, a Xenopus
C2HC-type zinc fnger protein with a regulatory function in
neuronal differentiation. Cell 87, 1191–1202.
Bertrand, N., Castro, D.S., Guillemot, F., 2002. Proneural genes
and the specifcation of neural cell types. Nat. Rev. Neurosci.
3, 517–530. https://doi.org/10.1038/nrn874
Blewitt, R., 2009. Enhancer of split-related-2 mRNA shows
cyclic expression during somitogenesis in Xenopus laevis. Biosci. Horizons 2, 22–31. https://doi.org/10.1093/
biohorizons/hzp006
Bonev, B., Pisco, A., Papalopulu, N., 2011. microRNA-9 reveals
regional diversity of neural progenitors along the anteriorposterior axis. Dev. Cell 20, 19–32. https://doi.org/10.1016/j.
devcel.2010.11.018
Bouwmeester, T., Kim, S., Sasai, Y., Lu, B., De Robertis, E.M.,
1996. Cerberus is a head-inducing secreted factor expressed
in the anterior endoderm of Spemann’s organizer. Nature
382, 595–601. https://doi.org/10.1038/382595a0
Bowes, J.B., Snyder, K.A., Segerdell, E., Jarabek, C.J., Azam, K.,
Zorn, A.M., Vize, P.D., 2010. Xenbase: Gene expression and
improved integration. Nucleic Acids Res 38, D607–D612.
https://doi.org/10.1093/nar/gkp953
Bray, S.J., 2016. Notch signalling in context. Nat. Rev. Mol. Cell
Biol. 17, 722–735. https://doi.org/10.1038/nrm.2016.94
Bray, S.J., Bernard, F., 2010. Notch targets and their regulation.
Curr. Top. Dev. Biol. 92, 253–275. https://doi.org/10.1016/
S0070-2153(10)92008-5
Brewster, R., Lee, J., Ruiz i Altaba, A., 1998. Gli/Zic factors pattern
the neural plate by defning domains of cell differentiation.
Nature 393, 579–583. https://doi.org/10.1038/31242
Bridges, C.B., Morgan, T.H., 1916. Sex-Linked Inheritance in
Drosophila. Carnegie Institution of Washington, Washington.
https://doi.org/10.5962/bhl.title.22854
Brugmann, S.A., Pandur, P.D., Kenyon, K.L., Pignoni, F., Moody,
S.A., 2004. Six1 promotes a placodal fate within the lateral
neurogenic ectoderm by functioning as both a transcriptional activator and repressor. Development 131, 5871–5881.
https://doi.org/10.1242/dev.01516
Campos-Ortega, J.A., 1985. Genetics of early neurogenesis in
Drosophila melanogaster. Trends Neurosci 8, 245–250.
https://doi.org/10.1016/0166-2236(85)90097-9
Castro Colabianchi, A.M., Revinski, D.R., Encinas, P.I., Baez,
M.V., Monti, R.J., Rodríguez Abinal, M., Kodjabachian, L.,
Franchini, L.F., López, S.L., 2018. Notch1 is asymmetrically distributed from the beginning of embryogenesis and
controls the ventral center. Development 145, dev159368.
https://doi.org/10.1242/dev.159368
Chalmers, A.D., Welchman, D., Papalopulu, N., 2002. Intrinsic
differences between the superfcial and deep layers of the
Xenopus ectoderm control primary neuronal differentiation.
Dev. Cell 2, 171–182.
Chan, T., Satow, R., Kitagawa, H., Kato, S., Asashima, M., 2006.
Ledgerline, a novel Xenopus laevis gene, regulates differentiation of presomitic mesoderm during somitogenesis. Zoolog.
Sci. 23, 689–697. https://doi.org/10.2108/zsj.23.689
Chen, J.-A., Voigt, J., Gilchrist, M., Papalopulu, N., Amaya, E.,
2005. Identifcation of novel genes affecting mesoderm formation and morphogenesis through an enhanced large scale
functional screen in Xenopus. Mech. Dev. 122, 307–331.
https://doi.org/10.1016/J.MOD.2004.11.008
Chitnis, A., Henrique, D., Lewis, J., Ish-Horowicz, D., Kintner, C.,
1995. Primary neurogenesis in Xenopus embryos regulated
by a homologue of the Drosophila neurogenic gene Delta.
Nature 375, 761–766. https://doi.org/10.1038/375761a0
Chitnis, A., Kintner, C., 1996. Sensitivity of proneural genes to
lateral inhibition affects the pattern of primary neurons in
Xenopus embryos. Development 122, 2295–2301.
Ciau-Uitz, A., Pinheiro, P., Gupta, R., Enver, T., Patient, R., 2010.
Tel1/ETV6 specifes blood stem cells through the agency
of VEGF signaling. Dev. Cell 18, 569–578. https://doi.
org/10.1016/j.devcel.2010.02.009
Cibois, M., Gautier-Courteille, C., Kodjabachian, L., Paillard,
L., 2013. A gene regulation network controlled by Celf1
protein-rbpj mRNA interaction in Xenopus somite segmentation. Biol. Open 2, 1078–1083. https://doi.org/10.1242/
bio.20135629
Cibois, M., Gautier-Courteille, C., Vallée, A., Paillard, L., 2010.
A strategy to analyze the phenotypic consequences of
inhibiting the association of an RNA-binding protein with
Notch Signaling in Early Embryogenesis
involved in proliferation, apoptosis, cell-fate choice, signaling pathways, metabolism, and cytoskeletal regulators
(Bray and Bernard, 2010; Meier-Stiegen et al., 2010). The
discovery of new targets and modulators in Xenopus will be
essential to building Notch-regulated GRNs that control different developmental processes. microRNAs regulate Notch
signaling during multiciliogenesis in the epidermis (Marcet
et al., 2011), and RITA (RBPJ-interacting and tubulinassociated protein) negatively modulates Notch signaling
through nuclear export of RBPJ during primary neurogenesis (Wacker et al., 2011). It will be exciting to extend the
study of such modulations to the different contexts in which
Notch signaling operates.
REFERENCES
Acosta, H., López, S.L., Revinski, D.R., Carrasco, A.E., 2011. Notch
destabilises maternal beta-catenin and restricts dorsal-anterior
development in Xenopus. Development 138, 2567–2579.
https://doi.org/10.1242/dev.061143
Aguirre, C.E., Murgan, S., Carrasco, A.E., López, S.L., 2013. An
intact brachyury function is necessary to prevent spurious
axial development in Xenopus laevis. PLoS One 8, e54777.
https://doi.org/10.1371/journal.pone.0054777
Ali, F.R., Cheng, K., Kirwan, P., Metcalfe, S., Livesey, F.J., Barker,
R.A., Philpott, A., 2014. The phosphorylation status of Ascl1
is a key determinant of neuronal differentiation and maturation in vivo and in vitro. Development 141, 2216–2224.
https://doi.org/10.1242/dev.106377
Anderson, C., Stern, C.D., 2016. Organizers in development.
Curr. Top. Dev. Biol. 117, 435–454. https://doi.org/10.1016/
BS.CTDB.2015.11.023
Andreazzoli, M., Gestri, G., Cremisi, F., Casarosa, S., Dawid, I.B.,
Barsacchi, G., 2003. Xrx1 controls proliferation and neurogenesis in Xenopus anterior neural plate. Development 130,
5143–5154. https://doi.org/10.1242/dev.00665
Artavanis-Tsakonas, S., Grimwade, B.G., Harrison, R.G.,
Markopoulou, K., Muskavitch, M.A.T., Schlesinger-Bryant,
R., Wharton, K., Yedvobnick, B., 1983. The Notch locus of
Drosophila melanogaster: A molecular analysis. Dev. Genet.
4, 233–254. https://doi.org/10.1002/dvg.1020040403
Artinger, M., Blitz, I., Inoue, K., Tran, U., Cho, K.W., 1997.
Interaction of goosecoid and brachyury in Xenopus mesoderm patterning. Mech. Dev. 65, 187–196.
Beck, C., Slack, J.M., 1998. Analysis of the developing Xenopus
tail bud reveals separate phases of gene expression during
determination and outgrowth. Mech. Dev. 72, 41–52. https://
doi.org/10.1016/S0925-4773(98)00015-X
Bellefroid, E.J., Bourguignon, C., Hollemann, T., Ma, Q., Anderson,
D.J., Kintner, C., Pieler, T., 1996. X-MyT1, a Xenopus
C2HC-type zinc fnger protein with a regulatory function in
neuronal differentiation. Cell 87, 1191–1202.
Bertrand, N., Castro, D.S., Guillemot, F., 2002. Proneural genes
and the specifcation of neural cell types. Nat. Rev. Neurosci.
3, 517–530. https://doi.org/10.1038/nrn874
Blewitt, R., 2009. Enhancer of split-related-2 mRNA shows
cyclic expression during somitogenesis in Xenopus laevis. Biosci. Horizons 2, 22–31. https://doi.org/10.1093/
biohorizons/hzp006
Bonev, B., Pisco, A., Papalopulu, N., 2011. microRNA-9 reveals
regional diversity of neural progenitors along the anteriorposterior axis. Dev. Cell 20, 19–32. https://doi.org/10.1016/j.
devcel.2010.11.018
Bouwmeester, T., Kim, S., Sasai, Y., Lu, B., De Robertis, E.M.,
1996. Cerberus is a head-inducing secreted factor expressed
in the anterior endoderm of Spemann’s organizer. Nature
382, 595–601. https://doi.org/10.1038/382595a0
Bowes, J.B., Snyder, K.A., Segerdell, E., Jarabek, C.J., Azam, K.,
Zorn, A.M., Vize, P.D., 2010. Xenbase: Gene expression and
improved integration. Nucleic Acids Res 38, D607–D612.
https://doi.org/10.1093/nar/gkp953
Bray, S.J., 2016. Notch signalling in context. Nat. Rev. Mol. Cell
Biol. 17, 722–735. https://doi.org/10.1038/nrm.2016.94
Bray, S.J., Bernard, F., 2010. Notch targets and their regulation.
Curr. Top. Dev. Biol. 92, 253–275. https://doi.org/10.1016/
S0070-2153(10)92008-5
Brewster, R., Lee, J., Ruiz i Altaba, A., 1998. Gli/Zic factors pattern
the neural plate by defning domains of cell differentiation.
Nature 393, 579–583. https://doi.org/10.1038/31242
Bridges, C.B., Morgan, T.H., 1916. Sex-Linked Inheritance in
Drosophila. Carnegie Institution of Washington, Washington.
https://doi.org/10.5962/bhl.title.22854
Brugmann, S.A., Pandur, P.D., Kenyon, K.L., Pignoni, F., Moody,
S.A., 2004. Six1 promotes a placodal fate within the lateral
neurogenic ectoderm by functioning as both a transcriptional activator and repressor. Development 131, 5871–5881.
https://doi.org/10.1242/dev.01516
Campos-Ortega, J.A., 1985. Genetics of early neurogenesis in
Drosophila melanogaster. Trends Neurosci 8, 245–250.
https://doi.org/10.1016/0166-2236(85)90097-9
Castro Colabianchi, A.M., Revinski, D.R., Encinas, P.I., Baez,
M.V., Monti, R.J., Rodríguez Abinal, M., Kodjabachian, L.,
Franchini, L.F., López, S.L., 2018. Notch1 is asymmetrically distributed from the beginning of embryogenesis and
controls the ventral center. Development 145, dev159368.
https://doi.org/10.1242/dev.159368
Chalmers, A.D., Welchman, D., Papalopulu, N., 2002. Intrinsic
differences between the superfcial and deep layers of the
Xenopus ectoderm control primary neuronal differentiation.
Dev. Cell 2, 171–182.
Chan, T., Satow, R., Kitagawa, H., Kato, S., Asashima, M., 2006.
Ledgerline, a novel Xenopus laevis gene, regulates differentiation of presomitic mesoderm during somitogenesis. Zoolog.
Sci. 23, 689–697. https://doi.org/10.2108/zsj.23.689
Chen, J.-A., Voigt, J., Gilchrist, M., Papalopulu, N., Amaya, E.,
2005. Identifcation of novel genes affecting mesoderm formation and morphogenesis through an enhanced large scale
functional screen in Xenopus. Mech. Dev. 122, 307–331.
https://doi.org/10.1016/J.MOD.2004.11.008
Chitnis, A., Henrique, D., Lewis, J., Ish-Horowicz, D., Kintner, C.,
1995. Primary neurogenesis in Xenopus embryos regulated
by a homologue of the Drosophila neurogenic gene Delta.
Nature 375, 761–766. https://doi.org/10.1038/375761a0
Chitnis, A., Kintner, C., 1996. Sensitivity of proneural genes to
lateral inhibition affects the pattern of primary neurons in
Xenopus embryos. Development 122, 2295–2301.
Ciau-Uitz, A., Pinheiro, P., Gupta, R., Enver, T., Patient, R., 2010.
Tel1/ETV6 specifes blood stem cells through the agency
of VEGF signaling. Dev. Cell 18, 569–578. https://doi.
org/10.1016/j.devcel.2010.02.009
Cibois, M., Gautier-Courteille, C., Kodjabachian, L., Paillard,
L., 2013. A gene regulation network controlled by Celf1
protein-rbpj mRNA interaction in Xenopus somite segmentation. Biol. Open 2, 1078–1083. https://doi.org/10.1242/
bio.20135629
Cibois, M., Gautier-Courteille, C., Vallée, A., Paillard, L., 2010.
A strategy to analyze the phenotypic consequences of
inhibiting the association of an RNA-binding protein with