Axonal netrin-Gs transneuronally determine lamina-specific subdendritic segments
Open accessAbstract
Axons from a distinct group of neurons make contact with dendritic trees of target neurons in clearly segregated and laminated patterns, thereby forming functional units for processing multiple inputs of information in the vertebrate central nervous system. Whether and how dendrites acquire lamina-specific properties corresponding to each pathway is not known. We show here that vertebrate-specific membrane-anchored members of the UNC-6/netrin family, netrin-G1 and -G2, organize the lamina/pathway-specific differentiation of dendrites. Netrin-G1 and -G2 distribute on axons of different pathways and specifically interact with receptors NGL-1 and -2, respectively. In the hippocampus, parietal cortex, and piriform cortex, NGL-1 is concentrated in the dendritic segments corresponding to the lamina-specific termination of netrin-G1-positive axons, and NGL-2 is concentrated in distinct dendritic segments corresponding to the termination of netrin-G2-positive axons. In netrin-G1- and -G2-deficient mice, in which axonal path-finding is normal, the segmental distribution of NGL-1 and -2 is selectively disrupted, and the individual receptors are diffused along the dendrites. These findings indicate that transneuronal interactions of netrin-Gs and their specific receptors provide a molecular basis for the axonal innervation-dependent mechanism of postsynaptic membrane organization, and provide insight into the formation of the laminar structure within the dendrites.
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?
LII EC axons form excitatory synapses on granule cells in the molecular layer of dentate gyrus, then project onto the distal dendrites of CA3 neurons, and finally terminate in a U-shaped area near the distal dendrites of CA2.
“LII EC axons form excitatory synapses on granule cells in the molecular layer of dentate gyrus (DG), then project onto the distal dendrites of CA3 neurons, and finally terminate in a U shaped-area near the distal dendrites of CA2 (Niimi et al., 2007; Nishimura-Akiyoshi et al., 2007; Tamamaki and Nojyo, 1995).”
From Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop (2010) · cites this paper as Nishimura-Akiyoshi et al., 2007
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
Paxinos, G. (1985) · Cited by 3,715 · see citing works
PDZ domain proteins of synapses
Kim, E., & Sheng, M. (2004) · Nature reviews. Neuroscience · doi:10.1038/nrn1517 · Cited by 1,565 · see citing works
The netrins define a family of axon outgrowth-promoting proteins homologous to C. elegans UNC-6
Serafini, T. A., Kennedy, T. E., Gaiko, M. J., Mirzayan, C., Jessell, T. M., & Tessier‐Lavigne, M. (1994) · Cell · doi:10.1016/0092-8674(94)90420-0 · Cited by 1,369 · see citing works
HPRT-deficient (Lesch–Nyhan) mouse embryos derived from germline colonization by cultured cells
Hooper, M., Hardy, K., Handyside, A. H., Hunter, S., & Monk, M. (1987) · Nature · doi:10.1038/326292a0 · Cited by 1,218 · see citing works
Neurexins Induce Differentiation of GABA and Glutamate Postsynaptic Specializations via Neuroligins
Graf, E. R., Zhang, X., Jin, S., Linhoff, M. W., & Craig, A. M. (2004) · Cell · doi:10.1016/j.cell.2004.11.035 · Cited by 989 · see citing works
EphB Receptors Interact with NMDA Receptors and Regulate Excitatory Synapse Formation
Dalva, M. B., Takasu, M. A., Lin, M. Z., Shamah, S. M., Hu, L. S., Gale, N. W., & Greenberg, M. E. (2000) · Cell · doi:10.1016/s0092-8674(00)00197-5 · Cited by 716 · see citing works
Control of Excitatory and Inhibitory Synapse Formation by Neuroligins
Chih, B., Engelman, H. S., & Scheiffele, P. (2005) · Science · doi:10.1126/science.1107470 · Cited by 707 · see citing works
Laminar organization of thalamic projections to the rat neocortex.
Herkenham, M. (1980) · Science · doi:10.1126/science.7352263 · Cited by 579 · see citing works
Distinct roles of nerve and muscle in postsynaptic differentiation of the neuromuscular synapse
Lin, W., Burgess, R. W., Dominguez, B., Pfaff, S. L., Sanes, J. R., & Lee, K. (2001) · Nature · doi:10.1038/35074025 · Cited by 534 · see citing works
Organization of the entorhinal—hippocampal system: A review of current anatomical data
Witter, M. P. (1993) · Hippocampus · doi:10.1002/hipo.1993.4500030707 · Cited by 534 · see citing works
UNC-6, a laminin-related protein, guides cell and pioneer axon migrations in C. elegans
Ishii, N., Wadsworth, W. G., Stern, B. D., et al. (1992) · Neuron · doi:10.1016/0896-6273(92)90240-e · Cited by 511 · see citing works
Polarized and compartment-dependent distribution of HCN1 in pyramidal cell dendrites
Lőrincz, A., Notomi, T., Tamás, G., Shigemoto, R., & Nusser, Z. (2002) · Nature Neuroscience · doi:10.1038/nn962 · Cited by 442 · see citing works
Ango, F., Cristo, G. D., Higashiyama, H., Bennett, V., Wu, P., & Huang, Z. J. (2004) · Cell · doi:10.1016/j.cell.2004.10.004 · Cited by 371 · see citing works
Witter, M. P., & Amaral, D. G. (2004) · Elsevier eBooks · doi:10.1016/b978-012547638-6/50022-5 · Cited by 344 · see citing works
Mburu, P., Mustapha, M., Varela, A., Weil, D., El-Amraoui, A., Holme, R. H., Rump, A., Hardisty, R., Blanchard, S., Coimbra, R. S., et al. (2003) · Nature Genetics · doi:10.1038/ng1208 · Cited by 343 · see citing works
Postsynaptic assembly induced by neurexin-neuroligin interaction and neurotransmitter
Nam, C. I., & Chen, L. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0502038102 · Cited by 322 · see citing works
Assembly of the postsynaptic membrane at the neuromuscular junction: paradigm lost
Kummer, T. T., Misgeld, T., & Sanes, J. R. (2005) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2005.12.003 · Cited by 291 · see citing works
NGL family PSD-95–interacting adhesion molecules regulate excitatory synapse formation
Kim, S.-H., Burette, A., Chung, H. S., Kwon, S., Woo, J., Lee, H. W., Kim, K., Kim, H., Weinberg, R. J., & Kim, E. (2006) · Nature Neuroscience · doi:10.1038/nn1763 · Cited by 272 · see citing works
Binder, M. D., Hirokawa, N., & Windhorst, U. (2008) · Springer eBooks · doi:10.1007/978-3-540-29678-2_3942 · Cited by 245 · see citing works
Delprat, B., Michel, V., Goodyear, R. J., et al. (2004) · Human Molecular Genetics · doi:10.1093/hmg/ddi036 · Cited by 193 · see citing works
Nicholson, D. A., Trana, R. E., Katz, Y., Kath, W. L., Spruston, N., & Geinisman, Y. (2006) · Neuron · doi:10.1016/j.neuron.2006.03.022 · Cited by 188 · see citing works
The netrin-G1 ligand NGL-1 promotes the outgrowth of thalamocortical axons
Lin, J. C., Ho, W.-H., Gurney, A. L., & Rosenthal, A. (2003) · Nature Neuroscience · doi:10.1038/nn1148 · Cited by 182 · see citing works
Nakashiba, T., Ikeda, T., Nishimura, S., et al. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-17-06540.2000 · Cited by 166 · see citing works
Self-citationFormation of lamina-specific synaptic connections
Sanes, J. R., & Yamagata, M. (1999) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(99)80010-5 · Cited by 157 · see citing works
Complementary expression and neurite outgrowth activity of netrin-G subfamily members
Nakashiba, T., Nishimura, S., Ikeda, T., et al. (2002) · Mechanisms of Development · doi:10.1016/s0925-4773(01)00600-1 · Cited by 145 · see citing works
Self-citationMAGUKs in synapse assembly and function: an emerging view
Montgomery, J. M., Zamorano, P. L., & Garner, C. C. (2004) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-003-3364-5 · Cited by 128 · see citing works
Otmakhova, N. A., Otmakhov, N., & Lisman, J. E. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-04-01199.2002 · Cited by 123 · see citing works
Aoki-Suzuki, M., Yamada, K., Meerabux, J., Iwayama‐Shigeno, Y., Ohba, H., Iwamoto, K., Takao, H., Toyota, T., Suto, Y., Nakatani, N., et al. (2005) · Biological Psychiatry · doi:10.1016/j.biopsych.2004.11.022 · Cited by 105 · see citing works
Self-citationNew molecules for hippocampal development
Skutella, T., & Nitsch, R. (2001) · Trends in Neurosciences · doi:10.1016/s0166-2236(00)01717-3 · Cited by 104 · see citing works
Disruption of Netrin G1 by a balanced chromosome translocation in a girl with Rett syndrome
Borg, I., Freude, K., Kübart, S., Hoffmann, K., Menzel, C., Laccone, F., Firth, H., Ferguson-Smith, M. A., Tommerup, N., Ropers, H.-H., et al. (2005) · European Journal of Human Genetics · doi:10.1038/sj.ejhg.5201429 · Cited by 95 · see citing works
Laminets: Laminin- and Netrin-Related Genes Expressed in Distinct Neuronal Subsets
Yin, Y., Miner, J. H., & Sanes, J. R. (2002) · Molecular and Cellular Neuroscience · doi:10.1006/mcne.2001.1089 · Cited by 84 · see citing works
Livesey, F. J. (1999) · Cellular and Molecular Life Sciences · doi:10.1007/s000180050006 · Cited by 76 · see citing works
Schwob, J. E., & Price, J. L. (1984) · The Journal of Comparative Neurology · doi:10.1002/cne.902230205 · Cited by 71 · see citing works
Arrigoni, E., & Greene, R. W. (2004) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0705744 · Cited by 65 · see citing works
Inaki, K., Nishimura, S., Nakashiba, T., Itohara, S., & Yoshihara, Y. (2004) · The Journal of Comparative Neurology · doi:10.1002/cne.20270 · Cited by 62 · see citing works
Self-citationStrong expression of NETRIN-G2 in the monkey claustrum
Miyashita, T., Nishimura-Akiyoshi, S., Itohara, S., et al. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.08.025 · Cited by 31 · see citing works
Self-citationPostnatal expression of Cdkl2 in mouse brain revealed by LacZ inserted into the Cdkl2 locus
Sassa, T., Gomi, H., & Itohara, S. (2004) · Cell and Tissue Research · doi:10.1007/s00441-003-0828-8 · Cited by 22 · see citing works
Self-citation
Flagged first, then by citations
Research works printed but not linked: 1
- [2]Witter MP. Hippocampus. 1993;3:33–44. [PubMed] [Google Scholar]
Cited by
Sorted by citations
Sporadic autism exomes reveal a highly interconnected protein network of de novo mutations
O’Roak, B. J., Vives, L., Girirajan, S., Karakoc, E., Krumm, N., Coe, B. P., Levy, R., Ko, A., Lee, C., Smith, J. D., et al. (2012) · Nature · doi:10.1038/nature10989 · Cited by 2,165 · see citing works
Cell type–specific genetic and optogenetic tools reveal hippocampal CA2 circuits
Kohara, K., Pignatelli, M., Rivest, A. J., Jung, H.-Y., Kitamura, T., Suh, J., Frank, D., Kajikawa, K., Mise, N., Obata, Y., et al. (2014) · Nature Neuroscience · doi:10.1038/nn.3614 · Cited by 528 · see citing works
Transgenic inhibition of synaptic transmission reveals role of CA3 output in hippocampal learning
Nakashiba, T., Young, J. Z., McHugh, T. J., Buhl, D. L., & Tonegawa, S. (2008) · Science · doi:10.1126/science.1151120 · Cited by 492 · see citing works
Self-citationStrong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop
Chevaleyre, V., & Siegelbaum, S. A. (2010) · Neuron · doi:10.1016/j.neuron.2010.04.013 · Cited by 324 · see citing works
Protein tyrosine phosphatases PTPδ, PTPσ, and LAR: presynaptic hubs for synapse organization
Takahashi, H., & Craig, A. M. (2013) · Trends in Neurosciences · doi:10.1016/j.tins.2013.06.002 · Cited by 257 · see citing works
Eastwood, S. L., & Harrison, P. J. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2009.12.004 · Cited by 122 · see citing works
Kaulich, E., Waselenchuk, Q., Fürst, N., Desch, K., Mosbacher, J., Ciirdaeva, E., Juengling, M., Tushev, G., Langer, J., & Schuman, E. M. (2024) · doi:10.1101/2024.08.05.606570 · Cited by 22 · see citing works
Monoclonal antibodies discriminating netrin-G1 and netrin-G2 neuronal pathways
Niimi, K., Nishimura-Akiyoshi, S., Nakashiba, T., & Itohara, S. (2007) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2007.09.026 · Cited by 16 · see citing works
Self-citation
- Authors
- Nishimura-Akiyoshi, S., Niimi, K., Nakashiba, T., & Itohara, S.
- Affiliations
- RIKEN Center for Brain Science (JP)
- Massachusetts Institute of Technology (US)
- RIKEN (JP)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2007-09-11
- Volume
- 104
- Issue
- 37
- Pages
- 14801-14806
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC1964543
- OpenAlex
- W2090587506
- Cited by
- 132
- References
- 37
- Citations by year
- 2026: 4 · 2025: 7 · 2024: 7 · 2023: 4 · 2022: 3 · 2021: 6 · 2020: 3 · 2019: 6 · 2018: 8 · 2017: 4 · 2016: 11 · 2015: 9 · 2014: 9 · 2013: 13 · 2012: 12
- FWCI
- 2.39
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- RIKEN
- RIKEN Brain Science Institute
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Axon Guidance and Neuronal Signaling
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- axon guidance, hippocampus, piriform cortex, parietal cortex
- MeSH terms
- Netrins, Animals, Axons, Cell Line, Cerebral Cortex, Dendrites, Homozygote, Humans, Immunohistochemistry, Kidney, Mice, Mutant Strains, Models, Biological, Nerve Tissue Proteins, Protein Binding, In Situ Hybridization, Mice
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
