DOI: 10.1242/dev.122.10.2987. Maternal β-catenin establishes a ‘dorsal signal’ in early <i>Xenopus</i> embryos

Maternal β-catenin establishes a ‘dorsal signal’ in early Xenopus embryos

10.1242/dev.122.10.2987

Crossref journal-article

The Company of Biologists

Development (237)

Abstract

ABSTRACT In previous work, we demonstrated that maternally encoded β-catenin, the vertebrate homolog of armadillo, is required for formation of dorsal axial structures in early Xenopus embryos (Heasman, J., Crawford, A., Goldstone, K., Garner-Hamrick, P., Gumbiner, B., Kintner, C., Yoshida-Noro, C. and Wylie, C. (1994). Cell 79, 791-803). Here we investigated, firstly, the role(s) of β-catenin in spatial terms, in different regions of the embryo, by injecting β-catenin mRNA into individual blastomeres of β-catenin-depleted embryos at the 32 cell stage. The results indicate that β-catenin can rescue the dorsal axial structures in a non-cell-autonomous way and without changing the fates of the injected cells. This suggests that cells overexpressing β-catenin send a ‘dorsal signal’ to other cells. This was confirmed by showing that β-catenin overexpressing animal caps did not cause wild-type caps to form mesoderm, but did cause isolated β-catenin-deficient marginal zones to form dorsal mesoderm. Furthermore β-catenin-deficient vegetal masses treated with overexpressing caps regained their ability to act as Nieuwkoop Centers. Secondly, we studied the temporal activity of β-catenin. We showed that zygotic transcription of β-catenin starts after the midblastula transition (MBT), but does not rescue dorsal axial structures. We further demonstrated that the vegetal mass does not release a dorsal signal until after the onset of transcription, at the midblastula stage, suggesting that maternal β-catenin protein is required at or before this time. Thirdly we investigated where, in relationship to other gene products known to be active in axis formation,β-catenin is placed. We find that BVg1, bFGF, tBR (the truncated form of BMP2/4R), siamois and noggin activities are all downstream of β-catenin, as shown by the fact that injection of their mRNAs rescues the effect of depleting maternally encoded β-catenin. Interference with the action of glycogen synthase kinase (GSK), a vertebrate homolog of the Drosophila gene product, zeste white 3 kinase, does not rescue the effect, suggesting that it is upstream.

Bibliography

Wylie, C., Kofron, M., Payne, C., Anderson, R., Hosobuchi, M., Joseph, E., & Heasman, J. (1996). Maternal Î²-catenin establishes a âdorsal signalâ in early Xenopus embryos. Development, 122(10), 2987â2996.

Authors 7

C. Wylie (first)
M. Kofron (additional)
C. Payne (additional)
R. Anderson (additional)
M. Hosobuchi (additional)
E. Joseph (additional)
J. Heasman (additional)

References 44 Referenced 162

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{'key': '2025021323362688600_DEVELOP_122_10_2987C31', 'first-page': '299', 'article-title': 'Dorsalization and neural induction: Properties of the organizer in Xenopus laevis', 'volume': '78', 'author': 'Smith', 'year': '1983', 'journal-title': 'J. Embryol. exp. Morph'} / J. Embryol. exp. Morph / Dorsalization and neural induction: Properties of the organizer in Xenopus laevis by Smith (1983)
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Dates

Type	When
Created	4 years, 4 months ago (April 25, 2021, 10:31 p.m.)
Deposited	6 months, 3 weeks ago (Feb. 13, 2025, 6:36 p.m.)
Indexed	3 months ago (June 2, 2025, 11:49 a.m.)
Issued	28 years, 11 months ago (Oct. 1, 1996)
Published	28 years, 11 months ago (Oct. 1, 1996)
Published Online	28 years, 11 months ago (Oct. 1, 1996)
Published Print	28 years, 11 months ago (Oct. 1, 1996)

Funders 0

None

BibTeX

@article{Wylie_1996, title={Maternal β-catenin establishes a ‘dorsal signal’ in early Xenopus embryos}, volume={122}, ISSN={1477-9129}, url={http://dx.doi.org/10.1242/dev.122.10.2987}, DOI={10.1242/dev.122.10.2987}, number={10}, journal={Development}, publisher={The Company of Biologists}, author={Wylie, C. and Kofron, M. and Payne, C. and Anderson, R. and Hosobuchi, M. and Joseph, E. and Heasman, J.}, year={1996}, month=oct, pages={2987–2996} }

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  "abstract": "<jats:title>ABSTRACT</jats:title>\n               <jats:p>In previous work, we demonstrated that maternally encoded \u03b2-catenin, the vertebrate homolog of armadillo, is required for formation of dorsal axial structures in early Xenopus embryos (Heasman, J., Crawford, A., Goldstone, K., Garner-Hamrick, P., Gumbiner, B., Kintner, C., Yoshida-Noro, C. and Wylie, C. (1994). Cell 79, 791-803). Here we investigated, firstly, the role(s) of \u03b2-catenin in spatial terms, in different regions of the embryo, by injecting \u03b2-catenin mRNA into individual blastomeres of \u03b2-catenin-depleted embryos at the 32 cell stage. The results indicate that \u03b2-catenin can rescue the dorsal axial structures in a non-cell-autonomous way and without changing the fates of the injected cells. This suggests that cells overexpressing \u03b2-catenin send a \u2018dorsal signal\u2019 to other cells. This was confirmed by showing that \u03b2-catenin overexpressing animal caps did not cause wild-type caps to form mesoderm, but did cause isolated \u03b2-catenin-deficient marginal zones to form dorsal mesoderm. Furthermore \u03b2-catenin-deficient vegetal masses treated with overexpressing caps regained their ability to act as Nieuwkoop Centers.</jats:p>\n               <jats:p>Secondly, we studied the temporal activity of \u03b2-catenin. We showed that zygotic transcription of \u03b2-catenin starts after the midblastula transition (MBT), but does not rescue dorsal axial structures. We further demonstrated that the vegetal mass does not release a dorsal signal until after the onset of transcription, at the midblastula stage, suggesting that maternal \u03b2-catenin protein is required at or before this time. Thirdly we investigated where, in relationship to other gene products known to be active in axis formation,\u03b2-catenin is placed. We find that BVg1, bFGF, tBR (the truncated form of BMP2/4R), siamois and noggin activities are all downstream of \u03b2-catenin, as shown by the fact that injection of their mRNAs rescues the effect of depleting maternally encoded \u03b2-catenin. Interference with the action of glycogen synthase kinase (GSK), a vertebrate homolog of the Drosophila gene product, zeste white 3 kinase, does not rescue the effect, suggesting that it is upstream.</jats:p>",
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