The DOI matches its Crossref record; 38 of the 38 references it cites were found in a registry or an index.
Phosphorylation by the β-Catenin/MAPK Complex Promotes 14-3-3-Mediated Nuclear Export of TCF/POP-1 in Signal-Responsive Cells in C. elegans
Open accessAbstract
In C. elegans embryos, a Wnt/MAPK signaling pathway downregulates the TCF/LEF transcription factor POP-1, resulting in a lower nuclear level in signal-responsive cells compared to their sisters. Although the beta-catenin WRM-1 is required for POP-1 downregulation, a direct interaction between these two proteins does not seem to be required, as the beta-catenin-interacting domain of POP-1 is dispensable for both POP-1 downregulation and function in early embryos. We show here that WRM-1 downregulates POP-1 by promoting its phosphorylation by the MAP kinase LIT-1 and subsequent nuclear export via a 14-3-3 protein, PAR-5. In signal-responsive cells, we also detect a concurrent upregulation of nuclear LIT-1 that is dependent on Wnt/MAPK signaling. Our results suggest a model whereby Wnt/MAPK signaling downregulates POP-1 levels in responsive cells, in part by increasing nuclear LIT-1 levels, thereby increasing POP-1 phosphorylation and PAR-5-mediated nuclear export.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
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?
In the citing paper
“In C. elegans, the phosphorylation sites in POP-1 by LIT-1 were identified and these sites did not correspond to the target sites in LEF1 by NLK.16)”
From Mammalian Nemo-like kinase enhances .BETA.-catenin-TCF transcription activity in human osteosarcoma and neuroblastoma cells (2007) · cites this paper as [16]
Citations
Cites
Polakis, P. (2000) · Genes & Development · doi:10.1101/gad.14.15.1837 · Cited by 3,183
CRM1 Is an Export Receptor for Leucine-Rich Nuclear Export Signals
Fornerod, M. W. J., Ohno, M., Yoshida, M., & Mattaj, I. W. (1997) · Cell · doi:10.1016/s0092-8674(00)80371-2 · Cited by 2,086
Specific interference by ingested dsRNA
Timmons, L., & Fire, A. Z. (1998) · Nature · doi:10.1038/27579 · Cited by 1,938
14-3-3 Proteins: Structure, Function, and Regulation
Fu, H., Subramanian, R. R., & Masters, S. C. (2000) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev.pharmtox.40.1.617 · Cited by 1,596
CRM1 is responsible for intracellular transport mediated by the nuclear export signal
Fukuda, M., Asano, S., Nakamura, T., Adachi, M., Yoshida, M., Yanagida, M., & Nishida, E. (1997) · Nature · doi:10.1038/36894 · Cited by 1,213
Exportin 1 (Crm1p) Is an Essential Nuclear Export Factor
Stade, K., Ford, C. S., Guthrie, C., & Weis, K. (1997) · Cell · doi:10.1016/s0092-8674(00)80370-0 · Cited by 1,145
Creation of Low-Copy Integrated Transgenic Lines in Caenorhabditis elegans
Praitis, V., Casey, E., Collar, D. C., & Austin, J. (2001) · Genetics · doi:10.1093/genetics/157.3.1217 · Cited by 817
Drosophila Tcf and Groucho interact to repress Wingless signalling activity
Cavallo, R. A., Cox, R. T., Moline, M. M., Roose, J., Polevoy, G. A., Clevers, H., Peifer, M., & Bejsovec, A. (1998) · Nature · doi:10.1038/26982 · Cited by 730
Evidence for a Role of CRM1 in Signal-Mediated Nuclear Protein Export
Ossareh‐Nazari, B., Bachelerie, F., & Dargemont, C. (1997) · Science · doi:10.1126/science.278.5335.141 · Cited by 713
Wnt Signaling and an APC-Related Gene Specify Endoderm in Early C. elegans Embryos
Rocheleau, C. E., Downs, W. D., Lin, R., Wittmann, C., Bei, Y., Cha, Y.-H., Ali, M., Priess, J. R., & Mello, C. C. (1997) · Cell · doi:10.1016/s0092-8674(00)80531-0 · Cited by 660
Self-citation
Cited by
Sorted by citations
Items 101–143 of 143
Systematic Discovery of New Recognition Peptides Mediating Protein Interaction
Neduva, N., Linding, R., Angrand, I., Stark, A., Masi, F. D., Gibson, T. J., Lewis, J., Serrano, L. G., & Russell, R. B. (2005) · Cited by 14
Sugioka, K., & Sawa, H. (2010) · Genes to Cells · doi:10.1111/j.1365-2443.2010.01388.x · Cited by 13
Wnt/β‐catenin‐mediated transcriptional regulation
Parker, D. S., Blauwkamp, T. A., & Cadigan, K. M. (2007) · Advances in developmental biology · doi:10.1016/s1574-3349(06)17001-5 · Cited by 14
Neuronal specification in C. elegans : combining lineage inheritance with intercellular signaling
Barrière, A., & Bertrand, V. (2020) · Journal of Neurogenetics · doi:10.1080/01677063.2020.1781850 · Cited by 12
Mila, D., Calderón, A. G. T., Baldwin, A. T., Moore, K. M., Watson, M. J., Phillips, B. T., & Putzke, A. P. (2015) · Genetics · doi:10.1534/genetics.115.181412 · Cited by 10
β-Catenin–related protein WRM-1 is a multifunctional regulatory subunit of the LIT-1 MAPK complex
Yang, X., Karhadkar, T. R., Medina, J., Robertson, S. M., & Lin, R. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1416339112 · Cited by 8
Self-citationDing, S. S., & Woollard, A. C. S. (2017) · Scientific Reports · doi:10.1038/s41598-017-01675-7 · Cited by 9
Althoff, M. J., Flick, K. F., & Trzepacz, C. (2014) · Development Genes and Evolution · doi:10.1007/s00427-014-0470-3 · Cited by 8
Nikolaou, S., & Gasser, R. B. (2006) · Parasitology · doi:10.1017/s0031182006001727 · Cited by 8
Pati, A., Jin, Y., Klage, K., Helm, R. F., Heath, L. S., & Ramakrishnan, N. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkm804 · Cited by 7
YASUDA, J., & ICHIKAWA, H. (2007) · Proceedings of the Japan Academy, Series B · doi:10.2183/pjab.83.16 · Cited by 6
Functional analyses of vertebrate TCF proteins in C. elegans embryos
Robertson, S. M., Lo, M., Odom, R. S., Yang, X., Medina, J., Huang, S., & Lin, R. (2011) · Developmental Biology · doi:10.1016/j.ydbio.2011.04.012 · Cited by 6
Self-citationOur evolving view of Wnt signaling in C. elegans
Robertson, S. M., & Lin, R. (2012) · Worm · doi:10.4161/worm.19156 · Cited by 6
Self-citationAnalysis of Wnt Signaling During Caenorhabditis elegans Postembryonic Development
Hoffelen, S. J. V., & Herman, M. A. (2008) · Methods in molecular biology · doi:10.1007/978-1-60327-469-2_8 · Cited by 6
Ferrando-Marco, M., & Barkoulas, M. (2025) · Development · doi:10.1242/dev.204546 · Cited by 2
MEL-47, a novel protein required for early cell divisions in the nematode Caenorhabditis elegans
Minasaki, R., & Streit, A. (2006) · Molecular Genetics and Genomics · doi:10.1007/s00438-006-0191-z · Cited by 5
Rumley, J. D., Preston, E. A., Cook, D., Peng, F., Zacharias, A. L., Wu, L., Jileaeva, I., & Murray, J. I. (2022) · Developmental Biology · doi:10.1016/j.ydbio.2022.05.019 · Cited by 4
Korswagen, H. C. (2007) · Advances in developmental biology · doi:10.1016/s1574-3349(06)17003-9 · Cited by 4
Function of the Ryk intracellular domain in C. elegans vulval development
Poh, W. C., Yanqing, S., & Inoue, T. (2014) · Developmental Dynamics · doi:10.1002/dvdy.24159 · Cited by 3
RNT‐1 regulation in C. elegans
Ji, Y. J., Singaravelu, G., & Ahnn, J. (2005) · Journal of Cellular Biochemistry · doi:10.1002/jcb.20423 · Cited by 3
PAR-5is a PARty hub in the germline
Aristizábal-Corrales, D., Schwartz, S., & Cerón, J. (2013) · Worm · doi:10.4161/worm.21834 · Cited by 3
Inductive asymmetric cell division
Ishidate, T., Kim, S. Y., Mello, C. C., & Shirayama, M. (2013) · Worm · doi:10.4161/worm.26276 · Cited by 3
Cell Polarity and Asymmetric Cell Division by the Wnt Morphogen
Baldwin, A. T., & Phillips, B. T. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-802438-6.00003-6 · Cited by 3
Reciprocal signaling by Wnt and Notch specifies a muscle precursor in the C. elegans embryo
Robertson, S. M., Medina, J., Oldenbroek, M., & Lin, R. (2017) · Development · doi:10.1242/dev.145391 · Cited by 2
Self-citationFerrando-Marco, M., Berger, S., & Barkoulas, M. (2026) · Genetics · doi:10.1093/genetics/iyag147 · Cited by 1
Wolf, A. K.-L., Adams-Phillips, L. C., Adams, A. N. D., Erives, A. J., & Phillips, B. T. (2021) · Cells and Development · doi:10.1016/j.cdev.2025.204013 · Cited by 1
Mikl, M., & Cowan, C. R. (2015) · Springer eBooks · doi:10.1007/978-3-319-14466-5_1 · Cited by 1
Characterizing the role of C. elegans dsh-2 in asymmetric cell division and embryonic development
Lee, S. C.-H. (2005) · Summit (Simon Fraser University) · Cited by 1
CHARACTERIZATION OF HAM-1 IN THE ASYMMETRIC DIVISION OF C. ELEGANS NEUROBLASTS
Leung, A. (2007) · Summit (Simon Fraser University)
A NOVEL NON-CANONICAL WNT PATHWAY REGULATES THE ASYMMETRIC B CELL DIVISION IN CAENORHABDITIS ELEGANS
Wu, M. (2005) · K-State Research Exchange (Kansas State University)
Maduro, M., Kasmir, J. J., Zhu, J., & Rothman, J. H. (2005)
Wnt/β-catenin Pathway Functions by Inactivation of Tcf7l1 Protein
Wu, C.-S. P. (2014) · Figshare
Maduro, M., Hill, R. J., Heid, P. J., Newman-Smith, E. D., Zhu, J., Priess, J. R., & Rothman, J. H. (2005)
Kormish, J. D. (2004) · Libraries and Cultural Resources (University of Calgary) · doi:10.11575/prism/11628
14-3-3 sigma interacts with liver X receptor beta
Jackson, E. A. (2010) · Louisiana State University · doi:10.31390/gradschool_theses.4251
Ferrando-Marco, M., & Barkoulas, M. (2024) · bioRxiv · doi:10.1101/2024.07.01.601538
SYS-1/beta-catenin inheritance and regulation by Wnt signaling during asymmetric cell division
Michel, M. F. V., & Phillips, B. T. (2025) · Molecular Biology of the Cell · doi:10.1091/mbc.e24-10-0441
Kim, J. H., & Greenwald, I. (2025) · G3 Genes Genomes Genetics · doi:10.1093/g3journal/jkaf288
Investigation of PHR Signaling in C. elegans
Tulgren, E. D. (2013) · University of Minnesota Digital Conservancy (University of Minnesota)
Ferrando-Marco, M., Berger, S., & Barkoulas, M. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.03.04.709659
Role of Wnt signaling in the polarization of neuronal precursors in the C. elegans embryo
Kaur, S. (2018) · theses.fr (ABES) · doi:10.70675/2f0f57b8z5525z48a8z9c69z90d6e94c149b
Metadata
- Authors
- Lo, M.-C., Gay, F., Odom, R., Shi, Y., & Lin, R.
- Affiliations
- The University of Texas Southwestern Medical Center (US)
- Harvard University (US)
- Corresponding author
- Lin, Rueyling
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2004-04
- Volume
- 117
- Issue
- 1
- Pages
- 95-106
- ISSN
- 0092-8674 (ISSN-L)
- OpenAlex
- W2157756800
- Cited by
- 138
- References
- 38
- Citations by year
- 2026: 1 · 2025: 3 · 2023: 1 · 2022: 2 · 2021: 2 · 2020: 3 · 2019: 1 · 2018: 4 · 2017: 5 · 2016: 2 · 2015: 6 · 2014: 10 · 2013: 9 · 2012: 9
- FWCI
- 4.94
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (HD37933)
- March of Dimes Foundation (GM58012, FY01-265)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Wnt/β-catenin signaling in development and cancer
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › 14-3-3 protein interactions
- Keywords
- β-catenin, POP-1, TCF/LEF transcription factors, 14-3-3 proteins, protein phosphorylation, nuclear export, Caenorhabditis elegans embryo, transcriptional downregulation
- MeSH terms
- Animals, Cell Differentiation, Cell Nucleus, Cytoskeletal Proteins, DNA-Binding Proteins, Embryo, Nonmammalian, High Mobility Group Proteins, Membrane Proteins, Phosphorylation, Tyrosine 3-Monooxygenase, Trans-Activators, Down-Regulation, Caenorhabditis elegans, Protein Serine-Threonine Kinases, Protein Structure, Tertiary, MAP Kinase Signaling System, Active Transport, Cell Nucleus, Caenorhabditis elegans Proteins, Macromolecular Substances, 14-3-3 Proteins, beta Catenin
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