Xenopus Dishevelled signaling regulates both neural and mesodermal convergent extension: parallel forces elongating the body axis
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During amphibian development, non-canonical Wnt signals regulate the polarity of intercalating dorsal mesoderm cells during convergent extension. Cells of the overlying posterior neural ectoderm engage in similar morphogenetic cell movements. Important differences have been discerned in the cell behaviors associated with neural and mesodermal cell intercalation, raising the possibility that different mechanisms may control intercalations in these two tissues. In this report, targeted expression of mutants of Xenopus Dishevelled (Xdsh) to neural or mesodermal tissues elicited different defects that were consistent with inhibition of either neural or mesodermal convergent extension. Expression of mutant Xdsh also inhibited elongation of neural tissues in vitro in Keller sandwich explants and in vivo in neural plate grafts. Targeted expression of other Wnt signaling antagonists also inhibited neural convergent extension in whole embryos. In situ hybridization indicated that these defects were not due to changes in cell fate. Examination of embryonic phenotypes after inhibition of convergent extension in different tissues reveals a primary role for mesodermal convergent extension in axial elongation, and a role for neural convergent extension as an equalizing force to produce a straight axis. This study demonstrates that non-canonical Wnt signaling is a common mechanism controlling convergent extension in two very different tissues in the Xenopus embryo and may reflect a general conservation of control mechanisms in vertebrate convergent extension.
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In cells undergoing convergent extension, Dsh is localized at the plasma membrane and accumulates in lamellipodia.
“In cells undergoing convergent extension, Dsh is localized at the plasma membrane and accumulates in lamellipodia.86”
From Wnt signal transduction pathways (2008) · cites this paper as [86]
Cites
Normal Table of Xenopus Laevis (Daudin)
Nieuwkoop, P. D., & Faber, J. (1958) · Copeia · doi:10.2307/1439568 · Cited by 4,542 · see citing works
Early development of Xenopus laevis : a laboratory manual
Sive, H. L., Grainger, R. M., & Harland, R. M. (2000) · Medical Entomology and Zoology · Cited by 1,222 · see citing works
Self-citationSilberblick/Wnt11 mediates convergent extension movements during zebrafish gastrulation
Heisenberg, C.-P., Tada, M., Rauch, G.-J., Saúde, L., Concha, M. L., Geisler, R., Stemple, D. L., Smith, J. C., & Wilson, S. W. (2000) · Nature · doi:10.1038/35011068 · Cited by 1,013 · see citing works
Dishevelled controls cell polarity during Xenopus gastrulation
Wallingford, J. B., Rowning, B. A., Vogeli, K. M., Rothbächer, U., Fraser, S. E., & Harland, R. M. (2000) · Nature · doi:10.1038/35011077 · Cited by 751 · see citing works
Self-citationTada, M., & Smith, J. C. (2000) · Development · doi:10.1242/dev.127.10.2227 · Cited by 675 · see citing works
Vital dye mapping of the gastrula and neurula of Xenopus laevis
Keller, R. E. (1976) · Developmental Biology · doi:10.1016/0012-1606(76)90127-5 · Cited by 576 · see citing works
Mechanisms of convergence and extension by cell intercalation
Keller, R. E., Davidson, L. A., Edlund, A., Elul, T., Ezin, M., Shook, D. R., & Skoglund, P. (2000) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2000.0626 · Cited by 521 · see citing works
Irvine, K. D., & Wieschaus, E. F. (1994) · Development · doi:10.1242/dev.120.4.827 · Cited by 506 · see citing works
Injected Wnt RNA induces a complete body axis in Xenopus embryos
Sokol, S. Y., Christian, J. L., Moon, R. T., & Melton, D. A. (1991) · Cell · doi:10.1016/0092-8674(91)90069-b · Cited by 501 · see citing works
Vital dye mapping of the gastrula and neurula of Xenopus laevis
Keller, R. E. (1975) · Developmental Biology · doi:10.1016/0012-1606(75)90331-0 · Cited by 438 · see citing works
Analysis of Dishevelled signalling pathways during Xenopus development
Sokol, S. Y. (1996) · Current Biology · doi:10.1016/s0960-9822(96)00750-6 · Cited by 406 · see citing works
Torres, M. A., Yang-Snyder, J., Purcell, S. M., DeMarais, A. A., McGrew, L. L., & Moon, R. T. (1996) · The Journal of Cell Biology · doi:10.1083/jcb.133.5.1123 · Cited by 405 · see citing works
Keller, R. E., & Danilchik, M. (1988) · Development · doi:10.1242/dev.103.1.193 · Cited by 378 · see citing works
Cell motility driving mediolateral intercalation in explants of Xenopus laevis
Shih, J., & Keller, R. E. (1992) · Development · doi:10.1242/dev.116.4.901 · Cited by 356 · see citing works
Wnt signaling in Xenopus embryos inhibits Bmp4 expression and activates neural developmentPreprint
Baker, J. C., Beddington, R. S. P., & Harland, R. M. (1999) · Genes & Development · doi:10.1101/gad.13.23.3149 · Cited by 337 · see citing works
Self-citationMoon, R. T., Campbell, R. M., Christian, J. L., McGrew, L. L., Shih, J., & Fraser, S. E. (1993) · Development · doi:10.1242/dev.119.1.97 · Cited by 330 · see citing works
Altaba, A. R. I., & Jessell, T. M. (1992) · Development · doi:10.1242/dev.116.1.81 · Cited by 329 · see citing works
Djiane, A., Riou, J.-F., Umbhauer, M., Boucaut, J.-C., & Shi, D.-L. (2000) · Development · doi:10.1242/dev.127.14.3091 · Cited by 316 · see citing works
Rothbächer, U., Laurent, M. N., Deardorff, M. A., Klein, P. S., Cho, K. W. Y., & Fraser, S. E. (2000) · The EMBO Journal · doi:10.1093/emboj/19.5.1010 · Cited by 299 · see citing works
Jacobson, A. G., & Gordon, R. (1976) · Journal of Experimental Zoology · doi:10.1002/jez.1401970205 · Cited by 295 · see citing works
Mouse models for neural tube closure defects
Juriloff, D. M. (2000) · Human Molecular Genetics · doi:10.1093/hmg/9.6.993 · Cited by 283 · see citing works
Dishevelled: at the crossroads of divergent intracellular signaling pathways
Boutros, M., & Mlodzik, M. (1999) · Mechanisms of Development · doi:10.1016/s0925-4773(99)00046-5 · Cited by 275 · see citing works
Miller, J. R., Rowning, B. A., Larabell, C. A., Yang-Snyder, J., Bates, R. L., & Moon, R. T. (1999) · The Journal of Cell Biology · doi:10.1083/jcb.146.2.427 · Cited by 254 · see citing works
Davidson, L. A., & Keller, R. E. (1999) · Development · doi:10.1242/dev.126.20.4547 · Cited by 251 · see citing works
The cellular basis of the convergence and extension of the Xenopus neural plate
Keller, R. E., Shih, J., & Sater, A. K. (1992) · Developmental Dynamics · doi:10.1002/aja.1001930302 · Cited by 251 · see citing works
Sharpe, C. R., Fritz, A., Robertis, E. M. D., & Gurdon, J. B. (1987) · Cell · doi:10.1016/0092-8674(87)90333-3 · Cited by 250 · see citing works
Neurulation: coming to closure
Smith, J. L. (1997) · Trends in Neurosciences · doi:10.1016/s0166-2236(97)01121-1 · Cited by 246 · see citing works
Harland, R. M. (2000) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(00)00096-4 · Cited by 234 · see citing works
Self-citationWnt and FGF pathways cooperatively pattern anteroposterior neural ectoderm in Xenopus
McGrew, L. L., Hoppler, S., & Moon, R. T. (1997) · Mechanisms of Development · doi:10.1016/s0925-4773(97)00160-3 · Cited by 225 · see citing works
McGrew, L. L., Lai, C.-J., & Moon, R. T. (1995) · Developmental Biology · doi:10.1006/dbio.1995.0027 · Cited by 223 · see citing works
Patterns of cell motility in the organizer and dorsal mesoderm of Xenopus laevis
Shih, J., & Keller, R. E. (1992) · Development · doi:10.1242/dev.116.4.915 · Cited by 214 · see citing works
Bradley, L., Snape, A. M., Bhatt, S., & Wilkinson, D. G. (1993) · Mechanisms of Development · doi:10.1016/0925-4773(93)90089-g · Cited by 212 · see citing works
Chapter 5 Early Embryonic Development of Xenopus laevis
Keller, R. E. (1991) · Methods in cell biology · doi:10.1016/s0091-679x(08)60273-3 · Cited by 203 · see citing works
Sokol, S. Y., Klingensmith, J., Perrimon, N., & Itoh, K. (1995) · Development · doi:10.1242/dev.121.6.1637 · Cited by 189 · see citing works
Medina, A., Reintsch, W., & Steinbeißer, H. (2000) · Mechanisms of Development · doi:10.1016/s0925-4773(00)00240-9 · Cited by 174 · see citing works
Cell autonomous regulation of multiple Dishevelled-dependent pathways by mammalian Nkd
Yan, D. M., Wallingford, J. B., Sun, T., Nelson, A. M., Sakanaka, C., Reinhard, C., Harland, R. M., Fantl, W. J., & Williams, L. T. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.071041898 · Cited by 167 · see citing works
Self-citationFrizzled-8 is expressed in the Spemann organizer and plays a role in early morphogenesis
Deardorff, M. A., Tan, C. L., Conrad, L. J., & Klein, P. S. (1998) · Development · doi:10.1242/dev.125.14.2687 · Cited by 160 · see citing works
Calcium signaling during convergent extension in Xenopus
Wallingford, J. B., Ewald, A. J., Harland, R. M., & Fraser, S. E. (2001) · Current Biology · doi:10.1016/s0960-9822(01)00201-9 · Cited by 156 · see citing works
Self-citationImaging of multicellular large-scale rhythmic calcium waves during zebrafish gastrulation
Gilland, E., Miller, A. L., Karplus, E., Baker, R., & Webb, S. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.1.157 · Cited by 143 · see citing works
Segregation of fate during cleavage of frog (Xenopus laevis) blastomeres
Moody, S. A., & Kline, M. J. (1990) · Anatomy and Embryology · doi:10.1007/bf02433495 · Cited by 136 · see citing works
Planar induction of convergence and extension of the neural plate by the organizer of Xenopus
Keller, R. E., Shih, J., Sater, A. K., et al. (1992) · Developmental Dynamics · doi:10.1002/aja.1001930303 · Cited by 126 · see citing works
Analysis of morphogenetic movements in the neural plate of the newt Taricha torosa
Burnside, M. B., & Jacobson, A. G. (1968) · Developmental Biology · doi:10.1016/0012-1606(68)90025-0 · Cited by 119 · see citing works
Wallingford, J. B., Vogeli, K. M., & Harland, R. M. (2001) · The International Journal of Developmental Biology · doi:10.1387/ijdb.11291850 · Cited by 116 · see citing works
Self-citationCellular Mechanism Underlying Neural Convergent Extension inXenopus laevisEmbryos
Elul, T., Koehl, M. A. R., & Keller, R. E. (1997) · Developmental Biology · doi:10.1006/dbio.1997.8711 · Cited by 115 · see citing works
Imaging patterns of calcium transients during neural induction in Xenopus laevis embryos
Leclerc, C., Webb, S., Daguzan, C., Moreau, M., & Miller, A. L. (2000) · Journal of Cell Science · doi:10.1242/jcs.113.19.3519 · Cited by 111 · see citing works
Elul, T., & Keller, R. E. (2000) · Developmental Biology · doi:10.1006/dbio.2000.9746 · Cited by 109 · see citing works
ventral ectoderm of Xenopus forms neural tissue, including hindbrain, in response to activin
Bolce, M. E., Hemmati‐Brivanlou, A., Kushner, P. D., et al. (1992) · Development · doi:10.1242/dev.115.3.681 · Cited by 105 · see citing works
Keller, R. E., Shih, J., & Domingo, C. R. (1992) · Development · doi:10.1242/dev.116.supplement.81 · Cited by 96 · see citing works
Ribisi, S., Mariani, F. V., Aamar, E., Lamb, T. M., Frank, D., & Harland, R. M. (2000) · Developmental Biology · doi:10.1006/dbio.2000.9889 · Cited by 94 · see citing works
Self-citationBrook, F. A., Shum, A. S. W., van Straaten, H. W. M., et al. (1991) · Development · doi:10.1242/dev.113.2.671 · Cited by 89 · see citing works
XBF-2 is a transcriptional repressor that converts ectoderm into neural tissue
Mariani, F. V., & Harland, R. M. (1998) · Development · doi:10.1242/dev.125.24.5019 · Cited by 89 · see citing works
Self-citationvan Straaten, H. W. M., Hekking, J. W. M., Consten, C., et al. (1993) · Development · doi:10.1242/dev.117.3.1163 · Cited by 67 · see citing works
4 The Cellular Basis of Sea Urchin Gastrulation
Hardin, J. D. (1996) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/s0070-2153(08)60339-7 · Cited by 56 · see citing works
The Neural Plate Specifies Somite Size in the Xenopus laevis Gastrula
Mariani, F. V., Choi, G. B., & Harland, R. M. (2001) · Developmental Cell · doi:10.1016/s1534-5807(01)00018-1 · Cited by 28 · see citing works
Self-citationFurther evidence that formation of the neural tube requires elongation of the nervous system
Jacobson, A. G. (1984) · Journal of Experimental Zoology · doi:10.1002/jez.1402300105 · Cited by 28 · see citing works
Larkin, K., & Danilchik, M. V. (1999) · Developmental Biology · doi:10.1006/dbio.1999.9495 · Cited by 23 · see citing works
Normal Neurulation in Amphibians
Jacobson, A. G. (2007) · Novartis Foundation symposium · doi:10.1002/9780470514559.ch2 · Cited by 15 · see citing works
Drawbridge, J., & Steinberg, M. S. (2000) · Developmental Biology · doi:10.1006/dbio.2000.9712 · Cited by 13 · see citing works
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Wallingford, J. B., Fraser, S. E., & Harland, R. M. (2002) · Developmental Cell · doi:10.1016/s1534-5807(02)00197-1 · Cited by 613 · see citing works
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Wallingford, J. B., & Habas, R. (2005) · Development · doi:10.1242/dev.02068 · Cited by 509 · see citing works
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- Authors
- Wallingford, J. B., & Harland, R. M.
- Affiliations
- University of California, Berkeley (US)
- Venue
- Development
- Publisher
- The Company of Biologists
- Published
- 2001-07-01
- Volume
- 128
- Issue
- 13
- Pages
- 2581-2592
- ISSN
- 0950-1991 (ISSN-L)
- 1477-9129
- OpenAlex
- W2134485689
- Cited by
- 217
- References
- 58
- Citations by year
- 2026: 3 · 2025: 7 · 2024: 1 · 2023: 3 · 2022: 4 · 2021: 6 · 2020: 6 · 2019: 6 · 2018: 1 · 2017: 10 · 2016: 7 · 2015: 7 · 2014: 10 · 2013: 12 · 2012: 9
- FWCI
- 5.94
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by
- Locations
- Development (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Wnt/β-catenin signaling in development and cancer
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular Mechanics and Interactions
- Keywords
- convergent extension, non-canonical Wnt signaling, Dishevelled, Xenopus embryo, body axis elongation, Wnt signaling antagonist, cell intercalation, amphibian embryonic development
- MeSH terms
- Wnt-5a Protein, Dishevelled Proteins, Animals, Cell Differentiation, DNA-Binding Proteins, Female, Humans, Mesoderm, Nerve Tissue Proteins, Neural Crest, Phenotype, Phosphoproteins, Proteins, Receptors, Cell Surface, Xenopus laevis, Signal Transduction, Body Patterning, Xenopus Proteins, Adaptor Proteins, Signal Transducing, Wnt Proteins
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