FoxA transcription factors are essential for the development of dorsal axial structures
Open accessAbstract
In vertebrates, embryonic structures present at the dorsal midline, prechordal plate, notochord, hypochord and floor plate share a common embryonic origin. In zebrafish, they derive from a pool of progenitors located within the embryonic shield at the onset of gastrulation. The molecular mechanisms responsible for the common development of these structures remain unknown. Based on their spatial and temporal expression, transcription factors of the Forkhead box A (FoxA) family appeared to be good candidates to play such a role. In agreement with this hypothesis, we found that simultaneous knockdown of FoxA2 and FoxA3 abolish the formation of all axial derivatives, while overexpression of these transcription factors strongly enlarges dorsal mesodermal territories. We establish that, in FoxA2-FoxA3 double morphants, precursors of axial tissues are correctly induced at early gastrula stage, but their dorsal midline identity is not maintained during development and we found that progenitors of these tissues are cell-autonomously re-specified to form muscle fibers as well as cells of the ventral neural tube. Our study provides the first example of a specific loss of all dorsal midline tissues and demonstrates that members of the FoxA family have redundant functions essential to maintain the axial identity of prechordal plate, notochord, floor plate and hypochord progenitors during gastrulation.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Some known notochord regulators, such as foxa3, were not identified as they are filtered out in the first steps of data processing owing to low expression.
“However, it is important to note that some known notochord regulators, such as foxa3 (ref. 41), were not identified as they are filtered out in the first steps of data processing owing to low expression.”
From Dissecting cell identity via network inference and in silico gene perturbation (2023) · cites this paper as [41]
A perturbation cannot be simulated if a TF-binding motif is unknown or TF expression is too sparse, as in the case of foxa3 in zebrafish.
“For example, a perturbation cannot be simulated if a TF-binding motif is unknown or TF expression is too sparse, as we note in the case of foxa3 in zebrafish41.”
From Dissecting cell identity via network inference and in silico gene perturbation (2023) · cites this paper as [41]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
High-resolution in situ hybridization to whole-mount zebrafish embryos
Thisse, C., & Thisse, B. (2007) · Nature Protocols · doi:10.1038/nprot.2007.514 · Cited by 2,587 · see citing works
Self-citationCo-crystal structure of the HNF-3/fork head DNA-recognition motif resembles histone H5
Clark, K., Halay, E. D., Lai, E., & Burley, S. K. (1993) · Nature · doi:10.1038/364412a0 · Cited by 1,275 · see citing works
Opening of Compacted Chromatin by Early Developmental Transcription Factors HNF3 (FoxA) and GATA-4
Cirillo, L. A., Lin, F. R., Cuesta, I., Friedman, D., Jarník, M., & Zaret, K. S. (2002) · Molecular Cell · doi:10.1016/s1097-2765(02)00459-8 · Cited by 1,188 · see citing works
Unified nomenclature for the winged helix/forkhead transcription factorsPreprint
Kaestner, K. H., Knöchel, W., & Martínez, D. E. (2000) · Genes & Development · doi:10.1101/gad.14.2.142 · Cited by 1,162 · see citing works
Krauss, S. J. K., Concordet, J., & Ingham, P. W. (1993) · Cell · doi:10.1016/0092-8674(93)90628-4 · Cited by 1,072 · see citing works
FoxA1 Translates Epigenetic Signatures into Enhancer-Driven Lineage-Specific Transcription
Lupien, M., Eeckhoute, J., Meyer, C. A., Wang, Q., Zhang, Y., Li, W., Carroll, J. S., Liu, X. S., & Brown, M. (2008) · Cell · doi:10.1016/j.cell.2008.01.018 · Cited by 983 · see citing works
HNF-3β is essential for node and notochord formation in mouse development
Ang, S., & Rossant, J. (1994) · Cell · doi:10.1016/0092-8674(94)90522-3 · Cited by 981 · see citing works
Weinstein, D. C., Altaba, A. R. I., Chen, W. S., Hoodless, P. A., Prezioso, V. R., Jessell, T. M., & Darnell, J. E., Jr. (1994) · Cell · doi:10.1016/0092-8674(94)90523-1 · Cited by 783 · see citing works
Schulte‐Merker, S., Ho, R. K., Herrmann, B. G., & Nüsslein‐Volhard, C. (1992) · Development · doi:10.1242/dev.116.4.1021 · Cited by 644 · see citing works
no tail (ntl) is the zebrafish homologue of the mouse T (Brachyury) gene
Schulte‐Merker, S., van Eeden, F. J. M., Halpern, M. E., Kimmel, C. B., & Nüsslein‐Volhard, C. (1994) · Development · doi:10.1242/dev.120.4.1009 · Cited by 624 · see citing works
Ang, S.-L., Wierda, A., Wong, D., Stevens, K. A., Cascio, S., Rossant, J., & Zaret, K. S. (1993) · Development · doi:10.1242/dev.119.4.1301 · Cited by 618 · cited 2× · see citing works
“…chicken and frog embryos (Odenthal and Nusslein-Volhard, 1998; Kaestner et al., 2000) and shown that they are also expressed in axial mesoderm (Ang et al., 1993; Bolce et al., 1993; Dirksen and Jamrich, 1992; Knochel et al., 1992; Lef et al., 1996; Monaghan et al., 1993; Ruiz i Altaba and…”
BackgroundMonaghan, A. P., Kaestner, K. H., Grau, E., & Schütz, G. (1993) · Development · doi:10.1242/dev.119.3.567 · Cited by 497 · see citing works
A homeobox gene essential for zebrafish notochord development
Talbot, W. S., Trevarrow, B., Halpern, M. E., Melby, A. E., Farr, G., Postlethwait, J. H., Jowett, T., Kimmel, C. B., & Kimelman, D. (1995) · Nature · doi:10.1038/378150a0 · Cited by 465 · see citing works
The fork head domain: A novel DNA binding motif of eukaryotic transcription factors?
Weigel, D., & Jäckle, H. (1990) · Cell · doi:10.1016/0092-8674(90)90439-l · Cited by 463 · see citing works
Structure and function of the notochord: an essential organ for chordate development
Stemple, D. L. (2005) · Development · doi:10.1242/dev.01812 · Cited by 443 · see citing works
Thisse, B., Heyer, V., Lux, A., Alunni, V., Degrave, A., Seiliez, I., Kirchner, J., Parkhill, J.-P., & Thisse, C. (2004) · Methods in cell biology · doi:10.1016/s0091-679x(04)77027-2 · Cited by 436 · see citing works
Self-citationfork head domain genes in zebrafish
Odenthal, J., & Nüsslein‐Volhard, C. (1998) · Development Genes and Evolution · doi:10.1007/s004270050179 · Cited by 407 · see citing works
Binding of the winged‐helix transcription factor HNF3 to a linker histone site on the nucleosome
Cirillo, L. A., McPherson, C. E., Bossard, P., Stevens, K., Cherian, S., Shim, E. Y., Clark, K., Burley, S. K., & Zaret, K. S. (1998) · The EMBO Journal · doi:10.1093/emboj/17.1.244 · Cited by 381 · see citing works
Langheinrich, U., Hennen, E., Stott, G. M., & Vacun, G. (2002) · Current Biology · doi:10.1016/s0960-9822(02)01319-2 · Cited by 368 · 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
Strähle, U., Blader, P., Henrique, D., & Ingham, P. W. (1993) · Genes & Development · doi:10.1101/gad.7.7b.1436 · Cited by 279 · see citing works
Specification of cell fates at the dorsal margin of the zebrafish gastrula
Melby, A. E., Warga, R. M., & Kimmel, C. B. (1996) · Development · doi:10.1242/dev.122.7.2225 · Cited by 266 · see citing works
VEGF mediates angioblast migration during development of the dorsal aorta in Xenopus
Cleaver, O. B., & Krieg, P. A. (1998) · Development · doi:10.1242/dev.125.19.3905 · Cited by 262 · see citing works
Nodal signaling patterns the organizer
Gritsman, K., Talbot, W. S., & Schier, A. F. (2000) · Development · doi:10.1242/dev.127.5.921 · Cited by 261 · see citing works
Mutations affecting the formation of the notochord in the zebrafish, Danio rerio
Odenthal, J., Haffter, P., Vogelsang, E., Brand, M., van Eeden, F. J. M., Furutani‐Seiki, M., Granato, M., Hammerschmidt, M., Heisenberg, C., Jiang, Y., et al. (1996) · Development · doi:10.1242/dev.123.1.103 · Cited by 238 · see citing works
Catala, M., Teillet, M., Robertis, E. M. D., et al. (1996) · Development · doi:10.1242/dev.122.9.2599 · Cited by 232 · see citing works
Characterizing the zebrafish organizer: microsurgical analysis at the early-shield stage
Shih, J., & Fraser, S. E. (1996) · Development · doi:10.1242/dev.122.4.1313 · Cited by 231 · see citing works
goosecoid Expression in neurectoderm and mesendoderm is disrupted in zebrafish cyclops gastrulas
Thisse, C., Thisse, B., Halpern, M. E., & Postlethwait, J. H. (1994) · Developmental Biology · doi:10.1006/dbio.1994.1212 · Cited by 230 · see citing works
Self-citationExpression of a type II collagen gene in the zebrafish embryonic axis
Yan, Y., Hatta, K., Riggleman, B., & Postlethwait, J. H. (1995) · Developmental Dynamics · doi:10.1002/aja.1002030308 · Cited by 229 · see citing works
Dirksen, M., & Jamrich, M. (1992) · Genes & Development · doi:10.1101/gad.6.4.599 · Cited by 225 · see citing works
Kelly, C., Chin, A. J., Leatherman, J. L., Kozlowski, D. J., & Weinberg, E. S. (2000) · Development · doi:10.1242/dev.127.18.3899 · Cited by 215 · see citing works
Activin- and Nodal-related factors control antero–posterior patterning of the zebrafish embryo
Thisse, B., Wright, C. V. E., & Thisse, C. (2000) · Nature · doi:10.1038/35000200 · Cited by 211 · see citing works
Self-citationOrganization and development of the tail bud analyzed with the quail-chick chimaera system
Catala, M., Teillet, M., & Douarin, N. M. L. (1995) · Mechanisms of Development · doi:10.1016/0925-4773(95)00350-a · Cited by 203 · see citing works
Mutations affecting development of the notochord in zebrafish
Stemple, D. L., Solnica‐Krezel, L., Zwartkruis, F. J. T., Neuhauss, S. C. F., Schier, A. F., Malicki, J. J., Stainier, D. Y. R., Abdelilah, S., Rangini, Z., Mountcastle-Shah, E., et al. (1996) · Development · doi:10.1242/dev.123.1.117 · Cited by 198 · see citing works
Fekany-Lee, K., Yamanaka, Y., Leung, T., Sirotkin, H. I., Topczewski, J., Gates, M. A., Hibi, M., Renucci, A., Stemple, D. L., Radbill, A., et al. (1999) · Development · doi:10.1242/dev.126.7.1427 · Cited by 196 · see citing works
Sonic hedgehog is required for survival of both myogenic and chondrogenic somitic lineages
Teillet, M., Watanabe, Y., Jeffs, P., Duprez, D., Lapointe, F., & Douarin, N. M. L. (1998) · Development · doi:10.1242/dev.125.11.2019 · Cited by 191 · see citing works
Pani, L., Overdier, D. G., Porcella, A., Qian, X., Lai, E., & Costa, R. H. (1992) · Molecular and Cellular Biology · doi:10.1128/mcb.12.9.3723 · Cited by 188 · see citing works
Altaba, A. R. I., Prezioso, V. R., Darnell, J. E., Jr., & Jessell, T. M. (1993) · Mechanisms of Development · doi:10.1016/0925-4773(93)90060-b · Cited by 186 · see citing works
Halpern, M. E., Thisse, C., Ho, R. K., Thisse, B., Riggleman, B., Trevarrow, B., Weinberg, E. S., Postlethwait, J. H., & Kimmel, C. B. (1995) · Development · doi:10.1242/dev.121.12.4257 · Cited by 178 · see citing works
Self-citationZaret, K. S., Watts, J. A., Xu, J., Wandzioch, E., Smale, S. T., & Sekiya, T. (2008) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.2008.73.040 · Cited by 159 · see citing works
Fürthauer, M., Thisse, B., & Thisse, C. (1999) · Developmental Biology · doi:10.1006/dbio.1999.9401 · Cited by 137 · see citing works
Self-citationQian, X., & Costa, R. H. (1995) · Nucleic Acids Research · doi:10.1093/nar/23.7.1184 · Cited by 129 · see citing works
Distribution of tissue progenitors within the shield region of the zebrafish gastrula
Shih, J., & Fraser, S. E. (1995) · Development · doi:10.1242/dev.121.9.2755 · Cited by 119 · see citing works
Altaba, A. R. I., Placzek, M., Baldassare, M., Dodd, J., & Jessell, T. M. (1995) · Developmental Biology · doi:10.1006/dbio.1995.1216 · Cited by 117 · see citing works
Axis-inducing activities and cell fates of the zebrafish organizer
Saúde, L., Woolley, K., Martin, P. B., Driever, W., & Stemple, D. L. (2000) · Development · doi:10.1242/dev.127.16.3407 · Cited by 117 · see citing works
Genetic Interactions in Zebrafish Midline Development
Halpern, M. E., Hatta, K., Amacher, S. L., Talbot, W. S., Yan, Y., Thisse, B., Thisse, C., Postlethwait, J. H., & Kimmel, C. B. (1997) · Developmental Biology · doi:10.1006/dbio.1997.8605 · Cited by 114 · see citing works
Self-citationKnöchel, S., Lef, J., Clement, J. H., Klocke, B., Hille, S., Köster, M., & Knöchel, W. (1992) · Mechanisms of Development · doi:10.1016/0925-4773(92)90007-7 · Cited by 109 · see citing works
Delta-mediated specification of midline cell fates in zebrafish embryos
Appel, B., Fritz, A., Westerfield, M., Grunwald, D. J., Eisen, J. S., & Riley, B. B. (1999) · Current Biology · doi:10.1016/s0960-9822(99)80113-4 · Cited by 107 · see citing works
Charrier, J., Teillet, M., Lapointe, F., & Douarin, N. M. L. (1999) · Development · doi:10.1242/dev.126.21.4771 · Cited by 94 · see citing works
Filippi, A., Dürr, K., Ryu, S., Willaredt, M. A., Holzschuh, J., & Driever, W. (2007) · BMC Developmental Biology · doi:10.1186/1471-213x-7-135 · Cited by 87 · see citing works
Altaba, A. R. I., Cox, C. M., Jessell, T. M., & Klar, A. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.17.8268 · Cited by 87 · see citing works
Rissi, M., Wittbrodt, J., Délot, E. C., et al. (1995) · Mechanisms of Development · doi:10.1016/0925-4773(94)00320-m · Cited by 81 · see citing works
Norton, W., Mangoli, M., Lele, Z., Pogoda, H., Diamond, B., Mercurio, S., Russell, C., Teraoka, H., Stickney, H. L., Rauch, G.-J., et al. (2005) · Development · doi:10.1242/dev.01611 · Cited by 74 · see citing works
A screen for targets of the Xenopus T-box gene Xbra
Saka, Y., Tada, M., & Smith, J. C. (2000) · Mechanisms of Development · doi:10.1016/s0925-4773(00)00260-4 · Cited by 64 · see citing works
Neurulation in amniote vertebrates: a novel view deduced from the use of quail-chick chimeras
Douarin, N. M. L., Teillet, M., & Catala, M. (1998) · The International Journal of Developmental Biology · doi:10.1387/ijdb.9853821 · Cited by 58 · see citing works
Seiliez, I., Thisse, B., & Thisse, C. (2005) · Developmental Biology · doi:10.1016/j.ydbio.2005.11.021 · Cited by 57 · see citing works
Self-citationDelta-Notch signaling induces hypochord development in zebrafish
Latimer, A. J., Dong, X., Markov, Y., & Appel, B. (2002) · Development · doi:10.1242/dev.129.11.2555 · Cited by 53 · see citing works
Notch signaling regulates midline cell specification and proliferation in zebrafish
Latimer, A. J., & Appel, B. (2006) · Developmental Biology · doi:10.1016/j.ydbio.2006.05.039 · Cited by 50 · see citing works
Yaklichkin, S., Vekker, A., Stayrook, S. E., Lewis, M., & Kessler, D. S. (2007) · BMC Genomics · doi:10.1186/1471-2164-8-201 · Cited by 42 · see citing works
Bolce, M. E., Hemmati‐Brivanlou, A., & Harland, R. M. (1993) · Developmental Biology · doi:10.1006/dbio.1993.1317 · Cited by 39 · see citing works
Martynova, N. Y., Eroshkin, F. M., Алексеевна, Е. Г., et al. (2004) · Development · doi:10.1242/dev.01133 · Cited by 38 · see citing works
Inhibition of mesodermal fate by Xenopus HNF3β/FoxA2
Suri, C., Haremaki, T., & Weinstein, D. C. (2003) · Developmental Biology · doi:10.1016/j.ydbio.2003.09.017 · Cited by 26 · see citing works
A fork head related multigene family is transcribed in Xenopus laevis embryos
Lef, J., Dege, P., Scheucher, M., Forsbach-Birk, V., Clement, J. H., & Knöchel, W. (1996) · The International Journal of Developmental Biology · doi:10.1387/ijdb.8735935 · Cited by 22 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Dissecting cell identity via network inference and in silico gene perturbation
Kamimoto, K., Stringa, B., Hoffmann, C. M., Jindal, K., Solnica-Krezel, L., & Morris, S. A. (2023) · Nature · doi:10.1038/s41586-022-05688-9 · Cited by 677 · see citing works
- Authors
- Dal-Pra, S., Thisse, C., & Thisse, B.
- Affiliations
- University of Virginia (US)
- Corresponding author
- Thisse, Bernard
- Venue
- Developmental Biology
- Publisher
- Elsevier BV
- Published
- 2011-02
- Volume
- 350
- Issue
- 2
- Pages
- 484-495
- ISSN
- 0012-1606 (ISSN-L)
- OpenAlex
- W1992919344
- Cited by
- 35
- References
- 63
- Citations by year
- 2026: 2 · 2024: 2 · 2023: 6 · 2022: 6 · 2021: 3 · 2020: 4 · 2019: 1 · 2018: 2 · 2017: 1 · 2016: 2 · 2014: 2 · 2013: 3 · 2012: 1
- FWCI
- 0.52
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Developmental Biology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Institut National de la Santé et de la Recherche Médicale
- Center National de la Recherche Scientifique
- Ministère de la Recherche
- Hôpital Universitaire de Strasbourg
- Association pour la Recherche sur le Cancer
- Ligue Nationale Contre le Cancer
- University of Virginia
- 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 › Zebrafish Biomedical Research Applications
- Keywords
- FoxA transcription factor, FOXA2, FOXA3, prechordal plate, notochord, floor plate, embryonic shield, gastrulation, dorsal mesoderm, muscle fiber development, ventral neural tube, zebrafish
- MeSH terms
- Animals, Mesoderm, Zebrafish, Zebrafish Proteins, Hepatocyte Nuclear Factor 3-gamma, Forkhead Transcription Factors, Gastrulation
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review