Nemo-like kinase (NLK) acts downstream of Notch/Delta signalling to downregulate TCF during mesoderm induction in the sea urchin embryo
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Studies in Caenorhabditis elegans and vertebrates have established that the MAP kinase-related protein NLK counteracts Wnt signalling by downregulating the transcription factor TCF. Here, we present evidence that during early development of the sea urchin embryo, NLK is expressed in the mesodermal precursors in response to Notch signalling and directs their fate by downregulating TCF. The expression pattern of nlk is strikingly similar to that of Delta and the two genes regulate the expression of each other. nlk overexpression, like ectopic activation of Notch signalling, provoked massive formation of mesoderm and associated epithelial mesenchymal transition. NLK function was found to be redundant with that of the MAP kinase ERK during mesoderm formation and to require the activity of the activating kinase TAK1. In addition, the sea urchin NLK, like its vertebrate counterpart, antagonizes the activity of the transcription factor TCF. Finally, activating the expression of a TCF-VP16 construct at blastula stages strongly inhibits endoderm and mesoderm formation, indicating that while TCF activity is required early for launching the endomesoderm gene regulatory network, it has to be downregulated at blastula stage in the mesodermal lineage. Taken together, our results indicate that the evolutionarily conserved TAK/NLK regulatory pathway has been recruited downstream of the Notch/Delta pathway in the sea urchin to switch off TCF-β-catenin signalling in the mesodermal territory, allowing precursors of this germ layer to segregate from the endomesoderm.
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NLK was initially shown to be involved in various developmental processes, such as promotion of mesoderm specification in sea urchins, mesoderm patterning, patterning of midbrain and forebrain in zebrafish, and oocyte maturation in Xenopus Laevis and in mouse testes.
“NLK was initially shown to be involved in various developmental processes, such as the promotion of mesoderm specification in sea urchins [32], mesoderm patterning, patterning of midbrain and forebrain in zebrafish [33], as well as oocyte maturation in Xenopus Laevis [34] and in mouse testes [35].”
From Nemo-Like Kinase in Development and Diseases: Insights from Mouse Studies (2020) · cites this paper as [32]
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Self-citationEdgar, A., Byrne, M., McClay, D. R., & Wray, G. A. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/712216 · Cited by 3 · see citing works
Dorsal-ventral axis formation in sea urchin embryos
Su, Y. (2022) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2021.10.007 · Cited by 2 · see citing works
Arató, K. (2010) · Repositori digital de la UPF (Universitat Pompeu Fabra)
Dong, T., Kokubu, H., Driessen, T. M., Tejwani, L., & Lim, J. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/358010
- Authors
- Röttinger, E., Croce, J., Lhomond, G., Besnardeau, L., Gache, C., & Lepage, T.
- Affiliations
- UMR 7009 CNRS, Université de Pierre et Marie Curie (Paris 6),Observatoire Oceanologique, 06230 Villefranche-sur-Mer, France.
- Centre National de la Recherche Scientifique (FR)
- Corresponding author
- Lepage, Thierry
- Venue
- Development
- Publisher
- The Company of Biologists
- Published
- 2006-11-01
- Volume
- 133
- Issue
- 21
- Pages
- 4341-4353
- ISSN
- 0950-1991 (ISSN-L)
- 1477-9129
- OpenAlex
- W2065963386
- Cited by
- 54
- References
- 49
- Citations by year
- 2023: 1 · 2022: 1 · 2021: 2 · 2020: 3 · 2019: 2 · 2018: 5 · 2017: 3 · 2016: 2 · 2015: 4 · 2014: 5 · 2013: 2 · 2012: 6
- FWCI
- 1.08
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Development (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- Funders
- Association pour la Recherche sur le Cancer
- Agence Nationale de la Recherche
- Centre National de la Recherche Scientifique
- 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
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
- Keywords
- Nemo-like kinase, TCF transcription factors, mesoderm induction, sea urchin embryo, germ layer specification, TAK1, ERK MAP kinase, Wnt/β-catenin signaling, epithelial-mesenchymal transition, blastula, gene regulatory network evolution
- MeSH terms
- MAP Kinase Kinase Kinase 7, Amino Acid Sequence, Animals, Embryonic Induction, Lithium, Membrane Proteins, Mesoderm, Molecular Sequence Data, Phenotype, Signal Transduction, Gene Expression Regulation, Enzymologic, Sequence Alignment, In Situ Hybridization, Gene Expression Regulation, Developmental, Mitogen-Activated Protein Kinases, MAP Kinase Kinase Kinases, Paracentrotus, Intracellular Signaling Peptides and Proteins, beta Catenin, TCF Transcription Factors, Receptors, Notch
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