49
Signaling Components in D-V Patterning
REFERENCES
Ambrosio, A.L., Taelman, V.F., Lee, H.X., Metzinger, C.A., Coff nier,
C. and De Robertis, E.M. 2008. Crossveinless-2 is a BMP
feedback inhibitor that binds Chordin/BMP to regulate
Xenopus embryonic patterning. Dev. Cell 15, 248–260.
Bauer, D.V., Huang, S. and Moody, S.A. 1994. The cleavage stage
origin of Spemann’s organizer: Analysis of the movements of
blastomere clones before and during gastrulation in Xenopus.
Development 120, 1179–1189.
Ben-Zvi, D., Shilo, B., Fainsod, A. and Barkai, N. 2008. Scaling
of the BMP activation gradient in Xenopus embryos. Nature
453, 1205–1211.
Bier, E. and De Robertis, E.M. 2015. BMP gradients: A paradigm
for morphogen-mediated developmental patterning. Science
348, 1443 and aaa5838.
Blum, M., De Robertis, E.M., Wallingford, J.B. and Niehrs, C.
2015. Morpholinos: Antisense and sensibility. Dev. Cell. 35,
145–149.
Bouwmeester, T., Kim, S.H., Sasai, Y., Lu, B. and 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.
Chang, C. and Harland, R.M. 2007. Neural induction requires continued suppression of both Smad1 and Smad2 signals during
gastrulation. Development 134, 3861–3872.
Cho, K.W.Y., 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.
Collavin, L. and Kirschner, M.W. 2003. The secreted Frizzled-related
protein Sizzled functions as a negative feedback regulator of
extreme ventral mesoderm. Development 130, 805–816.
Danilchik, M. and Black, S. 1988. The frst cleavage plane and the
embryonic axis are determined by separate mechanisms in
Xenopus laevis. Dev. Biol. 128, 58–64.
Demagny, H., Araki, T. and De Robertis, E.M. 2014. The tumor
suppressor Smad4/DCP4 is at the crossroads of Wnt, FGF
and TGF-β signaling. Cell Rep. 9, 688–700.
De Robertis, E.M. 2004. Goosecoid. In: Gastrulation, C. Stern,
Ed., Cold Spring Harbor Laboratory Press, New York,
pp. 581–589.
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.
De Robertis, E.M., Moriyama, Y. and Colozza, G. 2017. Generation
of animal form by the Chordin/Tolloid/BMP gradient: 100
years after D’Arcy Thompson. Dev. Growth Differ. 59,
580–592.
Ding, Y., Colozza, G., Sosa, E.A., Moriyama, Y., Rundle, S.,
Salwinski, L. and De Robertis, E.M. 2018. Bighead is a novel
Wnt antagonist secreted by the Xenopus Spemann organizer
that promotes Lrp6 endocytosis. Proc. Natl. Acad. Sci. USA
115, E9135–E9144.
Ding, Y., Colozza, G., Zhang, K., Moriyama, Y., Ploper, D.,
Sosa, E.A., Benitez, M.D.J. and De Robertis, E.M. 2017a.
Genome-wide analysis of dorsal and ventral transcriptomes
of the Xenopus laevis gastrula. Dev. Biol. 426, 176–178.
Ding, Y., Ploper, D., Sosa, E.A., Colozza, G., Moriyama, Y.,
Benitez, M.D.J., Zhang, K., Merkurjev, D. and De Robertis,
E.M. 2017b. Spemann organizer transcriptome induction by
early b-Catenin, Wnt, Nodal and Siamois signals in Xenopus
laevis. Proc. Natl. Acad. Sci. USA 114, E3081–E3090.
Dirksen, M.L. and Jamrich, M., 1992. A novel, activin-inducible,
blastopore lip-specifc gene of Xenopus laevis contains a fork
head DNA-binding domain. Genes Dev. 6, 599–608.
Fainsod, A., Deissler, K., Yelin, R., Marom, K., Epstein, M.,
Pillemer, G., Steinbeisser, H. and Blum, M. 1997. The dorsalizing and neural inducing gene follistatin is an antagonist
of BMP-4. Mech. Dev. 63, 39–50.
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.
Fuentealba, L.C., Eivers, E., Ikeda, A., Hurtado, C., Kuroda, H.,
Pera, E.M., and De Robertis, E.M. 2007. Integrating patterning signals: Wnt/GSK3 regulates the duration of the BMP/
Smad1 signal. Cell 131, 980–993.
Gawantka, V., Delius, H., Hirschfeld, K., Blumenstock, C. and
Niehrs, C. 1995. Antagonizing the Spemann organizer: The
role of the homeobox gene Xvent-1. EMBO J 14, 6268–6279.
Glinka, A., Wu, W., Delius, H., Monaghan, A.P., Blumenstock,
C. and Niehrs, C. 1998. Dickkopf-1 is a member of a new
family of secreted proteins and functions in head induction.
Nature 391, 357–362.
Gont, L.K., Steinbeisser, H., Blumberg, B. and De Robertis, E.M.
1993. Tail formation as a continuation of gastrulation: The
multiple cell populations of the Xenopus tailbud derive from
the late blastopore lip. Development 119, 991–1004.
Hamburger, V., 1988. The Heritage of Experimental Embryology:
Hans Spemann and the Organizer. Oxford University Press,
Oxford.
Hemmati-Brivanlou, A., Kelly, O.G. and Melton, D.A. 1994.
Follistatin, an antagonist of activin, is expressed in the
Spemann organizer and displays direct neuralizing activity.
Cell 77, 283–295.
Holley, S.A., Jackson, P.D., Sasai, Y., Lu, B., De Robertis, E.M.,
Hoffman, F.M. and Ferguson, E.L. 1995. A conserved system
for dorsal-ventral patterning in insects and vertebrates involving short gastrulation and chordin. Nature 376, 249–253.
Hurtado, C. and De Robertis, E.M. 2007. Neural induction in the
absence of organizer in salamanders is mediated by MAPK.
Dev. Biol. 307, 282–289.
Inomata, H., Shibata, T., Haraguchi, T. and Sasai, Y. 2013. Scaling
of dorsal-ventral patterning by embryo size-dependent
degradation of Spemann’s organizer signals. Cell 153,
1296–1311.
Karaulanov, E., Knöchel, W. and Niehrs, C. 2004. Transcriptional
regulation of BMP4 synexpression in transgenic Xenopus.
EMBO J 23, 844–856.
Khokha, M.K., Yeh, J., Grammer, T.C. and Harland, R.M., 2005.
Depletion of three BMP antagonists from Spemann’s organizer leads to a catastrophic loss of dorsal structures. Dev.
Cell 8, 401–411.
Kirsch, N., Chang, L.S., Koch, S., Glinka, A., Dolde, C., Colozza,
G., Benitez, M.D.J., De Robertis, E.M. and Niehrs, C. 2017.
Angiopoietin-like 4 is a Wnt signaling antagonist that promotes LRP6 turnover. Dev. Cell 43, 71–82.
Klein, S.L. 1987. The f rst cleavage furrow demarcates the dorsalventral axis in Xenopus embryos. Dev. Biol. 120, 299–304.
Kuroda, H., Fuentealba, L., Ikeda, A., Reversade, B. and De
Robertis, E.M. 2005. Default neural induction: Neuralization
of dissociated Xenopus cells is mediated by Ras/MAPK activation. Genes Dev. 19, 1022–1027.
Kuroda, H., Wessely, O. and De Robertis, E.M. 2004. Neural induction in Xenopus: Requirement for ectodermal and endomesoderm signals via Chordin, Noggin, β-Catenin and Cerberus.
PLoS Biology 2, 623–633.
Ladher, R., Mohun, T.J., Smith, J.C. and Snape, A.M. 1996. Xom:
A Xenopus homeobox gene that mediates the early effects of
BMP-4. Development 122, 2385–2394.
Signaling Components in D-V Patterning
REFERENCES
Ambrosio, A.L., Taelman, V.F., Lee, H.X., Metzinger, C.A., Coff nier,
C. and De Robertis, E.M. 2008. Crossveinless-2 is a BMP
feedback inhibitor that binds Chordin/BMP to regulate
Xenopus embryonic patterning. Dev. Cell 15, 248–260.
Bauer, D.V., Huang, S. and Moody, S.A. 1994. The cleavage stage
origin of Spemann’s organizer: Analysis of the movements of
blastomere clones before and during gastrulation in Xenopus.
Development 120, 1179–1189.
Ben-Zvi, D., Shilo, B., Fainsod, A. and Barkai, N. 2008. Scaling
of the BMP activation gradient in Xenopus embryos. Nature
453, 1205–1211.
Bier, E. and De Robertis, E.M. 2015. BMP gradients: A paradigm
for morphogen-mediated developmental patterning. Science
348, 1443 and aaa5838.
Blum, M., De Robertis, E.M., Wallingford, J.B. and Niehrs, C.
2015. Morpholinos: Antisense and sensibility. Dev. Cell. 35,
145–149.
Bouwmeester, T., Kim, S.H., Sasai, Y., Lu, B. and 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.
Chang, C. and Harland, R.M. 2007. Neural induction requires continued suppression of both Smad1 and Smad2 signals during
gastrulation. Development 134, 3861–3872.
Cho, K.W.Y., 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.
Collavin, L. and Kirschner, M.W. 2003. The secreted Frizzled-related
protein Sizzled functions as a negative feedback regulator of
extreme ventral mesoderm. Development 130, 805–816.
Danilchik, M. and Black, S. 1988. The frst cleavage plane and the
embryonic axis are determined by separate mechanisms in
Xenopus laevis. Dev. Biol. 128, 58–64.
Demagny, H., Araki, T. and De Robertis, E.M. 2014. The tumor
suppressor Smad4/DCP4 is at the crossroads of Wnt, FGF
and TGF-β signaling. Cell Rep. 9, 688–700.
De Robertis, E.M. 2004. Goosecoid. In: Gastrulation, C. Stern,
Ed., Cold Spring Harbor Laboratory Press, New York,
pp. 581–589.
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.
De Robertis, E.M., Moriyama, Y. and Colozza, G. 2017. Generation
of animal form by the Chordin/Tolloid/BMP gradient: 100
years after D’Arcy Thompson. Dev. Growth Differ. 59,
580–592.
Ding, Y., Colozza, G., Sosa, E.A., Moriyama, Y., Rundle, S.,
Salwinski, L. and De Robertis, E.M. 2018. Bighead is a novel
Wnt antagonist secreted by the Xenopus Spemann organizer
that promotes Lrp6 endocytosis. Proc. Natl. Acad. Sci. USA
115, E9135–E9144.
Ding, Y., Colozza, G., Zhang, K., Moriyama, Y., Ploper, D.,
Sosa, E.A., Benitez, M.D.J. and De Robertis, E.M. 2017a.
Genome-wide analysis of dorsal and ventral transcriptomes
of the Xenopus laevis gastrula. Dev. Biol. 426, 176–178.
Ding, Y., Ploper, D., Sosa, E.A., Colozza, G., Moriyama, Y.,
Benitez, M.D.J., Zhang, K., Merkurjev, D. and De Robertis,
E.M. 2017b. Spemann organizer transcriptome induction by
early b-Catenin, Wnt, Nodal and Siamois signals in Xenopus
laevis. Proc. Natl. Acad. Sci. USA 114, E3081–E3090.
Dirksen, M.L. and Jamrich, M., 1992. A novel, activin-inducible,
blastopore lip-specifc gene of Xenopus laevis contains a fork
head DNA-binding domain. Genes Dev. 6, 599–608.
Fainsod, A., Deissler, K., Yelin, R., Marom, K., Epstein, M.,
Pillemer, G., Steinbeisser, H. and Blum, M. 1997. The dorsalizing and neural inducing gene follistatin is an antagonist
of BMP-4. Mech. Dev. 63, 39–50.
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.
Fuentealba, L.C., Eivers, E., Ikeda, A., Hurtado, C., Kuroda, H.,
Pera, E.M., and De Robertis, E.M. 2007. Integrating patterning signals: Wnt/GSK3 regulates the duration of the BMP/
Smad1 signal. Cell 131, 980–993.
Gawantka, V., Delius, H., Hirschfeld, K., Blumenstock, C. and
Niehrs, C. 1995. Antagonizing the Spemann organizer: The
role of the homeobox gene Xvent-1. EMBO J 14, 6268–6279.
Glinka, A., Wu, W., Delius, H., Monaghan, A.P., Blumenstock,
C. and Niehrs, C. 1998. Dickkopf-1 is a member of a new
family of secreted proteins and functions in head induction.
Nature 391, 357–362.
Gont, L.K., Steinbeisser, H., Blumberg, B. and De Robertis, E.M.
1993. Tail formation as a continuation of gastrulation: The
multiple cell populations of the Xenopus tailbud derive from
the late blastopore lip. Development 119, 991–1004.
Hamburger, V., 1988. The Heritage of Experimental Embryology:
Hans Spemann and the Organizer. Oxford University Press,
Oxford.
Hemmati-Brivanlou, A., Kelly, O.G. and Melton, D.A. 1994.
Follistatin, an antagonist of activin, is expressed in the
Spemann organizer and displays direct neuralizing activity.
Cell 77, 283–295.
Holley, S.A., Jackson, P.D., Sasai, Y., Lu, B., De Robertis, E.M.,
Hoffman, F.M. and Ferguson, E.L. 1995. A conserved system
for dorsal-ventral patterning in insects and vertebrates involving short gastrulation and chordin. Nature 376, 249–253.
Hurtado, C. and De Robertis, E.M. 2007. Neural induction in the
absence of organizer in salamanders is mediated by MAPK.
Dev. Biol. 307, 282–289.
Inomata, H., Shibata, T., Haraguchi, T. and Sasai, Y. 2013. Scaling
of dorsal-ventral patterning by embryo size-dependent
degradation of Spemann’s organizer signals. Cell 153,
1296–1311.
Karaulanov, E., Knöchel, W. and Niehrs, C. 2004. Transcriptional
regulation of BMP4 synexpression in transgenic Xenopus.
EMBO J 23, 844–856.
Khokha, M.K., Yeh, J., Grammer, T.C. and Harland, R.M., 2005.
Depletion of three BMP antagonists from Spemann’s organizer leads to a catastrophic loss of dorsal structures. Dev.
Cell 8, 401–411.
Kirsch, N., Chang, L.S., Koch, S., Glinka, A., Dolde, C., Colozza,
G., Benitez, M.D.J., De Robertis, E.M. and Niehrs, C. 2017.
Angiopoietin-like 4 is a Wnt signaling antagonist that promotes LRP6 turnover. Dev. Cell 43, 71–82.
Klein, S.L. 1987. The f rst cleavage furrow demarcates the dorsalventral axis in Xenopus embryos. Dev. Biol. 120, 299–304.
Kuroda, H., Fuentealba, L., Ikeda, A., Reversade, B. and De
Robertis, E.M. 2005. Default neural induction: Neuralization
of dissociated Xenopus cells is mediated by Ras/MAPK activation. Genes Dev. 19, 1022–1027.
Kuroda, H., Wessely, O. and De Robertis, E.M. 2004. Neural induction in Xenopus: Requirement for ectodermal and endomesoderm signals via Chordin, Noggin, β-Catenin and Cerberus.
PLoS Biology 2, 623–633.
Ladher, R., Mohun, T.J., Smith, J.C. and Snape, A.M. 1996. Xom:
A Xenopus homeobox gene that mediates the early effects of
BMP-4. Development 122, 2385–2394.