72
Xenopus
recently been linked to Wnt signaling by Xenopus experiments, such as RAPGEF5 ( Griffn et al., 2018) and AGMO
(Duncan et al., 2019). These examples clearly demonstrate
the enormous potential for Xenopus to model human disease
related to the Wnt signaling network.
ACKNOWLEDGMENTS
The authors would like to thank their lab members (past and
present) and colleagues of the Xenopus and Wnt signaling
research felds from around the world for many stimulating
discussions and scientif c encouragement.
REFERENCES
Afouda, B.A., Hoppler, S., 2011. Different requirements for GATA
factors in cardiogenesis are mediated by non-canonical Wnt
signaling. Dev Dyn 240, 649–662.
Afouda, B.A., Martin, J., Liu, F., Ciau-Uitz, A., Patient, R., Hoppler,
S., 2008. GATA transcription factors integrate Wnt signalling
during heart development. Development 135, 3185–3190.
Afouda, B.A., Nakamura, Y., Shaw, S., Charney, R.M., Paraiso,
K.D., Blitz, I.L., Cho, K.W.Y., Hoppler, S., 2020. Foxh1/nodal
def nes context-specifc direct maternal Wnt/beta-catenin target gene regulation in early development. iScience 23, 101314.
Azzolin, L., Panciera, T., Soligo, S., Enzo, E., Bicciato, S., Dupont,
S., Bresolin, S., Frasson, C., Basso, G., Guzzardo, V., Fassina,
A., Cordenonsi, M., Piccolo, S., 2014. YAP/TAZ incorporation in the beta-catenin destruction complex orchestrates the
Wnt response. Cell 158, 157–170.
Baker, N.E., 1987. Molecular cloning of sequences from wingless,
a segment polarity gene in Drosophila: The spatial distribution of a transcript in embryos. EMBO J 6, 1765–1773.
Behrens, J., von Kries, J.P., Kuhl, M., Bruhn, L., Wedlich, D.,
Grosschedl, R., Birchmeier, W., 1996. Functional interaction
of beta-catenin with the transcription factor LEF-1. Nature
382, 638–642.
Bilic, J., Huang, Y.L., Davidson, G., Zimmermann, T., Cruciat,
C.M., Bienz, M., Niehrs, C., 2007. Wnt induces LRP6 signalosomes and promotes dishevelled-dependent LRP6 phosphorylation. Science 316, 1619–1622.
Bovolenta, B., Gorny, A.-K., Esteve, P., Steinbeisser, H., 2014.
Secreted Wnt inhibitors or modulators. In: Hoppler, S.,
Moon, R.T. (Eds.), Wnt Signaling in Development and
Disease: Molecular Mechanisms and Biological Functions.
John Wiley & Sons, Ltd, Hoboken, NJ, pp. 179–193.
Brannon, M., Gomperts, M., Sumoy, L., Moon, R.T., Kimelman,
D., 1997. A beta-catenin/XTcf-3 complex binds to the
siamois promoter to regulate dorsal axis specif cation in
Xenopus. Genes Dev 11, 2359–2370.
Buitrago-Delgado, E., Nordin, K., Rao, A., Geary, L., LaBonne, C.,
2015. Neurodevelopment: Shared regulatory programs suggest retention of blastula-stage potential in neural crest cells.
Science 348, 1332–1335.
Butler, M.T., Wallingford, J.B., 2018. Spatial and temporal analysis
of PCP protein dynamics during neural tube closure. Elife 7.
Chang, L.S., Kim, M., Glinka, A., Reinhard, C., Niehrs, C., 2020.
The tumor suppressor PTPRK promotes ZNRF3 internalization and is required for Wnt inhibition in the Spemann organizer. Elife 9.
Chen, M., Amado, N., Tan, J., Reis, A., Ge, M., Abreu, J.G., He, X.,
2020. TMEM79/MATTRIN defnes a pathway for Frizzled
regulation and is required for Xenopus embryogenesis. Elife 9.
Chen, T., Wallace, H., Ahmed, Y., Lee, E., 2014. Wnt signal transduction in the cytoplasm: An introduction to the destruction
complex. In: Hoppler, S., Moon, R.T. (Eds.), Wnt Signaling
in Development and Disease: Molecular Mechanisms and
Biological Functions. John Wiley & Sons, Ltd, Hoboken,
NJ, pp. 33–49.
Choudhry, P., Trede, N.S., 2013. DiGeorge syndrome gene tbx1
functions through wnt11r to regulate heart looping and differentiation. PLoS One 8, e58145.
Cizelsky, W., Tata, A., Kuhl, M., Kuhl, S.J., 2014. The Wnt/JNK
signaling target gene alcam is required for embryonic kidney
development. Development 141, 2064–2074.
Collu, G.M., Hidalgo-Sastre, A., Acar, A., Bayston, L., Gildea,
C., Leverentz, M.K., Mills, C.G., Owens, T.W., Meurette,
O., Dorey, K., Brennan, K., 2012. Dishevelled limits Notch
signalling through inhibition of CSL. Development 139,
4405–4415.
Davidson, G., Wu, W., Shen, J., Bilic, J., Fenger, U., Stannek, P.,
Glinka, A., Niehrs, C., 2005. Casein kinase 1 gamma couples
Wnt receptor activation to cytoplasmic signal transduction.
Nature 438, 867–872.
De Calisto, J., Araya, C., Marchant, L., Riaz, C.F., Mayor, R., 2005.
Essential role of non-canonical Wnt signalling in neural crest
migration. Development 132, 2587–2597.
Dejmek, J., Safholm, A., Kamp Nielsen, C., Andersson, T.,
Leandersson, K., 2006. Wnt-5a/Ca2+-induced NFAT activity
is counteracted by Wnt-5a/Yes-Cdc42-casein kinase 1alpha
signaling in human mammary epithelial cells. Mol Cell Biol
26, 6024–6036.
Devotta, A., Hong, C.S., Saint-Jeannet, J.P., 2018. Dkk2 promotes
neural crest specifcation by activating Wnt/beta-catenin signaling in a GSK3beta independent manner. Elife 7.
Ding, Y., Colozza, G., Sosa, E.A., Moriyama, Y., Rundle, S.,
Salwinski, L., De Robertis, E.M., 2018. Bighead is a Wnt
antagonist secreted by the Xenopus Spemann organizer that
promotes Lrp6 endocytosis. Proc Natl Acad Sci U S A 115,
E9135–E9144.
Dissanayake, S.K., Wade, M., Johnson, C.E., O’Connell, M.P.,
Leotlela, P.D., French, A.D., Shah, K.V., Hewitt, K.J.,
Rosenthal, D.T., Indig, F.E., Jiang, Y., Nickoloff, B.J., Taub,
D.D., Trent, J.M., Moon, R.T., Bittner, M., Weeraratna,
A.T., 2007. The Wnt5A/protein kinase C pathway mediates
motility in melanoma cells via the inhibition of metastasis
suppressors and initiation of an epithelial to mesenchymal
transition. J Biol Chem 282, 17259–17271.
Djiane, A., Riou, J., Umbhauer, M., Boucaut, J., Shi, D., 2000. Role
of frizzled 7 in the regulation of convergent extension movements during gastrulation in Xenopus laevis. Development
127, 3091–3100.
Domingos, P.M., Itasaki, N., Jones, C.M., Mercurio, S., Sargent,
M.G., Smith, J.C., Krumlauf, R., 2001. The Wnt/beta-catenin
pathway posteriorizes neural tissue in Xenopus by an indirect
mechanism requiring FGF signalling. Dev Biol 239, 148–160.
Du, S.J., Purcell, S.M., Christian, J.L., McGrew, L.L., Moon, R.T.,
1995. Identifcation of distinct classes and functional domains
of Wnts through expression of wild-type and chimeric proteins in Xenopus embryos. Mol Cell Biol 15, 2625–2634.
Duncan, A.R., Gonzalez, D.P., Del Viso, F., Robson, A., Khokha,
M.K., Griffn, J.N., 2019. Alkylglycerol monooxygenase, a
heterotaxy candidate gene, regulates left-right patterning via
Wnt signaling. Dev Biol 456, 1–7.
Esmaeili, M., Blythe, S.A., Tobias, J.W., Zhang, K., Yang, J., Klein,
P.S., 2020. Chromatin accessibility and histone acetylation in
Xenopus
recently been linked to Wnt signaling by Xenopus experiments, such as RAPGEF5 ( Griffn et al., 2018) and AGMO
(Duncan et al., 2019). These examples clearly demonstrate
the enormous potential for Xenopus to model human disease
related to the Wnt signaling network.
ACKNOWLEDGMENTS
The authors would like to thank their lab members (past and
present) and colleagues of the Xenopus and Wnt signaling
research felds from around the world for many stimulating
discussions and scientif c encouragement.
REFERENCES
Afouda, B.A., Hoppler, S., 2011. Different requirements for GATA
factors in cardiogenesis are mediated by non-canonical Wnt
signaling. Dev Dyn 240, 649–662.
Afouda, B.A., Martin, J., Liu, F., Ciau-Uitz, A., Patient, R., Hoppler,
S., 2008. GATA transcription factors integrate Wnt signalling
during heart development. Development 135, 3185–3190.
Afouda, B.A., Nakamura, Y., Shaw, S., Charney, R.M., Paraiso,
K.D., Blitz, I.L., Cho, K.W.Y., Hoppler, S., 2020. Foxh1/nodal
def nes context-specifc direct maternal Wnt/beta-catenin target gene regulation in early development. iScience 23, 101314.
Azzolin, L., Panciera, T., Soligo, S., Enzo, E., Bicciato, S., Dupont,
S., Bresolin, S., Frasson, C., Basso, G., Guzzardo, V., Fassina,
A., Cordenonsi, M., Piccolo, S., 2014. YAP/TAZ incorporation in the beta-catenin destruction complex orchestrates the
Wnt response. Cell 158, 157–170.
Baker, N.E., 1987. Molecular cloning of sequences from wingless,
a segment polarity gene in Drosophila: The spatial distribution of a transcript in embryos. EMBO J 6, 1765–1773.
Behrens, J., von Kries, J.P., Kuhl, M., Bruhn, L., Wedlich, D.,
Grosschedl, R., Birchmeier, W., 1996. Functional interaction
of beta-catenin with the transcription factor LEF-1. Nature
382, 638–642.
Bilic, J., Huang, Y.L., Davidson, G., Zimmermann, T., Cruciat,
C.M., Bienz, M., Niehrs, C., 2007. Wnt induces LRP6 signalosomes and promotes dishevelled-dependent LRP6 phosphorylation. Science 316, 1619–1622.
Bovolenta, B., Gorny, A.-K., Esteve, P., Steinbeisser, H., 2014.
Secreted Wnt inhibitors or modulators. In: Hoppler, S.,
Moon, R.T. (Eds.), Wnt Signaling in Development and
Disease: Molecular Mechanisms and Biological Functions.
John Wiley & Sons, Ltd, Hoboken, NJ, pp. 179–193.
Brannon, M., Gomperts, M., Sumoy, L., Moon, R.T., Kimelman,
D., 1997. A beta-catenin/XTcf-3 complex binds to the
siamois promoter to regulate dorsal axis specif cation in
Xenopus. Genes Dev 11, 2359–2370.
Buitrago-Delgado, E., Nordin, K., Rao, A., Geary, L., LaBonne, C.,
2015. Neurodevelopment: Shared regulatory programs suggest retention of blastula-stage potential in neural crest cells.
Science 348, 1332–1335.
Butler, M.T., Wallingford, J.B., 2018. Spatial and temporal analysis
of PCP protein dynamics during neural tube closure. Elife 7.
Chang, L.S., Kim, M., Glinka, A., Reinhard, C., Niehrs, C., 2020.
The tumor suppressor PTPRK promotes ZNRF3 internalization and is required for Wnt inhibition in the Spemann organizer. Elife 9.
Chen, M., Amado, N., Tan, J., Reis, A., Ge, M., Abreu, J.G., He, X.,
2020. TMEM79/MATTRIN defnes a pathway for Frizzled
regulation and is required for Xenopus embryogenesis. Elife 9.
Chen, T., Wallace, H., Ahmed, Y., Lee, E., 2014. Wnt signal transduction in the cytoplasm: An introduction to the destruction
complex. In: Hoppler, S., Moon, R.T. (Eds.), Wnt Signaling
in Development and Disease: Molecular Mechanisms and
Biological Functions. John Wiley & Sons, Ltd, Hoboken,
NJ, pp. 33–49.
Choudhry, P., Trede, N.S., 2013. DiGeorge syndrome gene tbx1
functions through wnt11r to regulate heart looping and differentiation. PLoS One 8, e58145.
Cizelsky, W., Tata, A., Kuhl, M., Kuhl, S.J., 2014. The Wnt/JNK
signaling target gene alcam is required for embryonic kidney
development. Development 141, 2064–2074.
Collu, G.M., Hidalgo-Sastre, A., Acar, A., Bayston, L., Gildea,
C., Leverentz, M.K., Mills, C.G., Owens, T.W., Meurette,
O., Dorey, K., Brennan, K., 2012. Dishevelled limits Notch
signalling through inhibition of CSL. Development 139,
4405–4415.
Davidson, G., Wu, W., Shen, J., Bilic, J., Fenger, U., Stannek, P.,
Glinka, A., Niehrs, C., 2005. Casein kinase 1 gamma couples
Wnt receptor activation to cytoplasmic signal transduction.
Nature 438, 867–872.
De Calisto, J., Araya, C., Marchant, L., Riaz, C.F., Mayor, R., 2005.
Essential role of non-canonical Wnt signalling in neural crest
migration. Development 132, 2587–2597.
Dejmek, J., Safholm, A., Kamp Nielsen, C., Andersson, T.,
Leandersson, K., 2006. Wnt-5a/Ca2+-induced NFAT activity
is counteracted by Wnt-5a/Yes-Cdc42-casein kinase 1alpha
signaling in human mammary epithelial cells. Mol Cell Biol
26, 6024–6036.
Devotta, A., Hong, C.S., Saint-Jeannet, J.P., 2018. Dkk2 promotes
neural crest specifcation by activating Wnt/beta-catenin signaling in a GSK3beta independent manner. Elife 7.
Ding, Y., Colozza, G., Sosa, E.A., Moriyama, Y., Rundle, S.,
Salwinski, L., De Robertis, E.M., 2018. Bighead is a Wnt
antagonist secreted by the Xenopus Spemann organizer that
promotes Lrp6 endocytosis. Proc Natl Acad Sci U S A 115,
E9135–E9144.
Dissanayake, S.K., Wade, M., Johnson, C.E., O’Connell, M.P.,
Leotlela, P.D., French, A.D., Shah, K.V., Hewitt, K.J.,
Rosenthal, D.T., Indig, F.E., Jiang, Y., Nickoloff, B.J., Taub,
D.D., Trent, J.M., Moon, R.T., Bittner, M., Weeraratna,
A.T., 2007. The Wnt5A/protein kinase C pathway mediates
motility in melanoma cells via the inhibition of metastasis
suppressors and initiation of an epithelial to mesenchymal
transition. J Biol Chem 282, 17259–17271.
Djiane, A., Riou, J., Umbhauer, M., Boucaut, J., Shi, D., 2000. Role
of frizzled 7 in the regulation of convergent extension movements during gastrulation in Xenopus laevis. Development
127, 3091–3100.
Domingos, P.M., Itasaki, N., Jones, C.M., Mercurio, S., Sargent,
M.G., Smith, J.C., Krumlauf, R., 2001. The Wnt/beta-catenin
pathway posteriorizes neural tissue in Xenopus by an indirect
mechanism requiring FGF signalling. Dev Biol 239, 148–160.
Du, S.J., Purcell, S.M., Christian, J.L., McGrew, L.L., Moon, R.T.,
1995. Identifcation of distinct classes and functional domains
of Wnts through expression of wild-type and chimeric proteins in Xenopus embryos. Mol Cell Biol 15, 2625–2634.
Duncan, A.R., Gonzalez, D.P., Del Viso, F., Robson, A., Khokha,
M.K., Griffn, J.N., 2019. Alkylglycerol monooxygenase, a
heterotaxy candidate gene, regulates left-right patterning via
Wnt signaling. Dev Biol 456, 1–7.
Esmaeili, M., Blythe, S.A., Tobias, J.W., Zhang, K., Yang, J., Klein,
P.S., 2020. Chromatin accessibility and histone acetylation in