RETRACTED: Hierarchical Organization of Guidance Receptors: Silencing of Netrin Attraction by Slit Through a Robo/DCC Receptor Complex
Open accessAbstract
Axonal growth cones that cross the nervous system midline change their responsiveness to midline guidance cues: They become repelled by the repellent Slit and simultaneously lose responsiveness to the attractant netrin. These mutually reinforcing changes help to expel growth cones from the midline by making a once-attractive environment appear repulsive. Here, we provide evidence that these two changes are causally linked: In the growth cones of embryonic Xenopus spinal axons, activation of the Slit receptor Roundabout (Robo) silences the attractive effect of netrin-1, but not its growth-stimulatory effect, through direct binding of the cytoplasmic domain of Robo to that of the netrin receptor DCC. Biologically, this hierarchical silencing mechanism helps to prevent a tug-of-war between attractive and repulsive signals in the growth cone that might cause confusion. Molecularly, silencing is enabled by a modular and interlocking design of the cytoplasmic domains of these potentially antagonistic receptors that predetermines the outcome of their simultaneous activation.
Integrity signals
Registry
Cites
Statistics
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?
ROBO silences the attractive effect that Netrin 1 has on DCC, allowing SLIT2 to bind to this ligand and enabling axon pathfinding in the developing brain.
“ROBO silences the attractive effect that Netrin 1 has on DCC, allowing SLIT2 to bind to this ligand and enabling axon pathfinding in the developing brain [106, 107].”
From Self-domestication in Homo sapiens: Insights from comparative genomics (2017) · cites this paper as [106]
Cites
2 retracted
Hong, K., Hinck, L., Nishiyama, M., Poo, M.-M., Tessier‐Lavigne, M., & Stein, E. (1999) · Cell · doi:10.1016/s0092-8674(00)80804-1 · Cited by 684 · see citing works
Self-citationRetractedStein, E., Zou, Y., Poo, M., & Tessier‐Lavigne, M. (2001) · Science · doi:10.1126/science.1059391 · Cited by 242 · see citing works
Self-citationRetractedThe Molecular Biology of Axon Guidance
Tessier‐Lavigne, M., & Goodman, C. S. (1996) · Science · doi:10.1126/science.274.5290.1123 · Cited by 3,295 · see citing works
Self-citationBrose, K., Bland, K. S., Wang, K. H., Arnott, D., Henzel, W., Goodman, C., Tessier-Lavigne, M., & Kidd, T. (1999) · Cell · doi:10.1016/s0092-8674(00)80590-5 · Cited by 1,276 · see citing works
Self-citationDeleted in Colorectal Cancer (DCC) Encodes a Netrin Receptor
Keino‐Masu, K., Masu, M., Hinck, L., Leonardo, E. D., Chan, S. S.-Y., Culotti, J. G., & Tessier‐Lavigne, M. (1996) · Cell · doi:10.1016/s0092-8674(00)81336-7 · Cited by 1,013 · see citing works
Self-citationSlit Is the Midline Repellent for the Robo Receptor in Drosophila
Kidd, T., Bland, K. S., & Goodman, C. S. (1999) · Cell · doi:10.1016/s0092-8674(00)80589-9 · Cited by 953 · see citing works
cAMP-induced switching in turning direction of nerve growth cones
Song, H., Ming, G., & Poo, M.-M. (1997) · Nature · doi:10.1038/40864 · Cited by 620 · see citing works
Turning of nerve growth cones induced by neurotransmitters
Zheng, J. Q., Felder, M., Connor, J. A., & Poo, M.-M. (1994) · Nature · doi:10.1038/368140a0 · Cited by 580 · see citing works
cAMP-Dependent Growth Cone Guidance by Netrin-1
Ming, G., Song, H., Berninger, B., Holt, C. E., Tessier‐Lavigne, M., & Poo, M.-M. (1997) · Neuron · doi:10.1016/s0896-6273(00)80414-6 · Cited by 560 · see citing works
Self-citationChan, S., Zheng, H., Su, M., Wilk, R., Killeen, M. T., Hedgecock, E. M., & Culotti, J. G. (1996) · Cell · doi:10.1016/s0092-8674(00)81337-9 · Cited by 503 · see citing works
Wang, K. H., Brose, K., Arnott, D. P., Kidd, T., Goodman, C. S., Henzel, W. J., & Tessier‐Lavigne, M. (1999) · Cell · doi:10.1016/s0092-8674(00)80588-7 · Cited by 471 · see citing works
Self-citationLi, H.-S., Chen, J., Wu, W., Fagaly, T., Zhou, L., Yuan, W., Dupuis, S., Jiang, Z., Nash, W. E., Gick, C., et al. (1999) · Cell · doi:10.1016/s0092-8674(00)80591-7 · Cited by 460 · see citing works
Kolodziej, P. A., Timpe, L. C., Mitchell, K. J., Fried, S. R., Goodman, C. S., Jan, L. Y., & Jan, Y. N. (1996) · Cell · doi:10.1016/s0092-8674(00)81338-0 · Cited by 460 · see citing works
Bashaw, G. J., Kidd, T., Murray, D., Pawson, T. J., & Goodman, C. S. (2000) · Cell · doi:10.1016/s0092-8674(00)80883-1 · Cited by 438 · see citing works
Stein, E., Lane, A. A., Cerretti, D. P., Schoecklmann, H. O., Schroff, A. D., Etten, R. L. V., & Daniel, T. O. (1998) · Genes & Development · doi:10.1101/gad.12.5.667 · Cited by 424 · see citing works
Self-citationSlit proteins: key regulators of axon guidance, axonal branching, and cell migration.
Brose, K., & Tessier-Lavigne, M. (2000) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(99)00066-5 · Cited by 381 · see citing works
Self-citationSqueezing Axons Out of the Gray Matter
Zou, Y., Stoeckli, E. T., Chen, H., & Tessier‐Lavigne, M. (2000) · Cell · doi:10.1016/s0092-8674(00)00041-6 · Cited by 365 · see citing works
Self-citationShort-Range and Long-Range Guidance by Slit and Its Robo Receptors
Simpson, J. H., Bland, K. S., Fetter, R. D., & Goodman, C. S. (2000) · Cell · doi:10.1016/s0092-8674(00)00206-3 · Cited by 304 · see citing works
SAM as a protein interaction domain involved in developmental regulation
Schultz, J., Peer Bork, B., Ponting, C. P., & Hofmann, K. (1997) · Protein Science · doi:10.1002/pro.5560060128 · Cited by 300 · see citing works
Yuan, W., Zhou, L., Chen, J., Wu, J. Y., Rao, Y., & Ornitz, D. M. (1999) · Developmental Biology · doi:10.1006/dbio.1999.9371 · Cited by 299 · see citing works
Turning of Retinal Growth Cones in a Netrin-1 Gradient Mediated by the Netrin Receptor DCC
de la Torre, J. R., Höpker, V. H., Ming, G., Poo, M.-M., Tessier‐Lavigne, M., Hemmati‐Brivanlou, A., & Holt, C. E. (1997) · Neuron · doi:10.1016/s0896-6273(00)80413-4 · Cited by 287 · see citing works
Self-citationSlit2-Mediated Chemorepulsion and Collapse of Developing Forebrain Axons
Nguyen-Ba-Charvet, K. T., Brose, K., Marillat, V., Kidd, T., Goodman, C. S., Tessier‐Lavigne, M., Sotelo, C., & Chédotal, A. (1999) · Neuron · doi:10.1016/s0896-6273(00)80702-3 · Cited by 282 · see citing works
Self-citationSelecting a Longitudinal Pathway
Rajagopalan, S., Vivancos, V., Nicolas, É., et al. (2000) · Cell · doi:10.1016/s0092-8674(00)00207-5 · Cited by 280 · see citing works
Ming, G., Song, H., Berninger, B., Inagaki, N., Tessier‐Lavigne, M., & Poo, M. (1999) · Neuron · doi:10.1016/s0896-6273(00)80760-6 · Cited by 279 · see citing works
Self-citationErskine, L., Williams, S. E., Brose, K., Kidd, T., Rachel, R. A., Goodman, C. S., Tessier‐Lavigne, M., & Mason, C. A. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-13-04975.2000 · Cited by 265 · see citing works
Self-citationChimeric Axon Guidance Receptors
Bashaw, G. J., & Goodman, C. S. (1999) · Cell · doi:10.1016/s0092-8674(00)80803-x · Cited by 189 · see citing works
Change in Chemoattractant Responsiveness of Developing Axons at an Intermediate Target
Shirasaki, R., Katsumata, R., & Murakami, F. (1998) · Science · doi:10.1126/science.279.5347.105 · Cited by 187 · see citing works
Ringstedt, T., Braisted, J. E., Brose, K., Kidd, T., Goodman, C. S., Tessier‐Lavigne, M., & O'Leary, D. D. M. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-13-04983.2000 · Cited by 147 · see citing works
Self-citationFailure of kynurenic acid to inhibit amino acid release from the ischemic rat cerebral cortex
Phillis, J. W., Song, D., Guyot, L. L., et al. (1999) · Neuroscience Letters · doi:10.1016/s0304-3940(99)00612-6 · Cited by 8 · see citing works
Tabti, N., & Poo, M. (1994) · Neuroscience Letters · doi:10.1016/0304-3940(94)90141-4 · Cited by 7 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Biomolecular gradients in cell culture systems
Keenan, T. M., & Folch, A. (2008) · Lab Chip · doi:10.1039/b711887b · Cited by 596 · see citing works
Extracellular Matrix: Functions in the Nervous System
Barros, C. S., Franco, S. J., & Muller, U. (2011) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a005108 · Cited by 506 · see citing works
Osteoclast-secreted SLIT3 coordinates bone resorption and formation
Kim, B.-J., Lee, Y.-S., Lee, S.-Y., Baek, W.-Y., Choi, Y. J., Moon, S. A., Lee, S. H., Kim, J.-E., Chang, E.-J., Kim, E.-Y., et al. (2018) · Journal of Clinical Investigation · doi:10.1172/jci91086 · Cited by 174 · see citing works
Self-domestication in Homo sapiens: Insights from comparative genomics
Theofanopoulou, C., Gastaldon, S., O’Rourke, T., Samuels, B. D., Messner, A., Martins, P. T., Delogu, F., Alamri, S., & Boeckx, C. (2017) · PLOS ONE · doi:10.1371/journal.pone.0185306 · Cited by 174 · see citing works
Torres-Berrío, A., Lopez, J. P., Bagot, R. C., Nouel, D., Dal Bo, G., Cuesta, S., Zhu, L., Manitt, C., Eng, C., Cooper, H. M., et al. (2017) · Biological Psychiatry · doi:10.1016/j.biopsych.2016.08.017 · Cited by 153 · see citing works
The SLIT–ROBO pathway: a regulator of cell function with implications for the reproductive system
Dickinson, R. E., & Duncan, W. C. (2010) · Reproduction · doi:10.1530/rep-10-0017 · Cited by 123 · see citing works
Assembly and function of spinal circuits for motor control
Catela, C., Shin, M. M., & Dasen, J. S. (2015) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-100814-125155 · Cited by 77 · see citing works
Lei, H., Yan, Z., Sun, X., Zhang, Y., Wang, J., Ma, C., Xu, Q., Wang, R., Jarvis, E. D., & Sun, Z. (2017) · Brain and Language · doi:10.1016/j.bandl.2017.06.007 · Cited by 18 · see citing works
Zhou, Y., Tao, L., & Zhu, Y. (2023) · Brain Sciences · doi:10.3390/brainsci13071070 · Cited by 7 · see citing works
- Authors
- Stein, E., & Tessier-Lavigne, M.
- Affiliations
- Howard Hughes Medical Institute (US)
- Department of Anatomy and Department of Biochemistry and Biophysics, Howard Hughes Medical Institute, University of California, San Francisco, CA 94143, USA.
- Venue
- Science
- Published
- 2001-03-09
- Volume
- 291
- Issue
- 5510
- Pages
- 1928-1938
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- OpenAlex
- W1964817578
- Cited by
- 601
- References
- 30
- Citations by year
- 2025: 1 · 2024: 1 · 2023: 7 · 2022: 9 · 2021: 7 · 2020: 9 · 2019: 12 · 2018: 14 · 2017: 16 · 2016: 16 · 2015: 16 · 2014: 26 · 2013: 25 · 2012: 31
- FWCI
- 20.57
- Type
- journal article
- Language
- en
- Status
- Retracted
- Open access
- hybrid
- doi.org
- Licence
- cc-by
- Locations
- Science (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Axon Guidance and Neuronal Signaling
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- axon guidance, netrin-1, slits, Roundabout receptors, DCC receptor, growth cones, midline crossing, receptor complex, cytoplasmic domain
- MeSH terms
- Netrin Receptors, Netrin-1, Roundabout Proteins, Slit Homolog 2 Protein, Animals, Axons, Cell Movement, Cells, Cultured, Cytoplasm, Embryo, Nonmammalian, Ligands, Mutation, Nerve Growth Factors, Nerve Tissue Proteins, Precipitin Tests, Receptors, Cell Surface, Receptors, Immunologic, Recombinant Fusion Proteins, Transfection, Xenopus, Signal Transduction, Cell Adhesion Molecules, Hepatocyte Growth Factor, Protein Structure, Tertiary, Growth Cones, Tumor Suppressor Proteins, Intercellular Signaling Peptides and Proteins
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