BIG-2 Mediates Olfactory Axon Convergence to Target Glomeruli
Open accessAbstract
Olfactory sensory neurons expressing a given odorant receptor converge axons onto a few topographically fixed glomeruli in the olfactory bulb, leading to establishment of the odor map. Here, we report that BIG-2/contactin-4, an axonal glycoprotein belonging to the immunoglobulin superfamily, is expressed in a subpopulation of mouse olfactory sensory neurons. A mosaic pattern of glomerular arrangement is observed with strongly BIG-2-positive, weakly positive, and negative axon terminals in the olfactory bulb, which is overlapping but not identical with those of Kirrel2 and ephrin-A5. There is a close correlation between the BIG-2 expression level and the odorant receptor choice in individual sensory neurons. In BIG-2-deficient mice, olfactory sensory neurons expressing a given odorant receptor frequently innervate multiple glomeruli at ectopic locations. These results suggest that BIG-2 is one of the axon guidance molecules crucial for the formation and maintenance of functional odor map in the olfactory bulb.
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?
CLCN3, SNAP91, and TSNARE1 are direct synaptic components, and CNTN4 and FURIN play roles in neurodevelopment.
“CLCN3, SNAP91, and TSNARE1 are direct synaptic components, and CNTN4 and FURIN play roles in neurodevelopment.”
From Gene expression elucidates functional impact of polygenic risk for schizophrenia (2016) · cites this paper as [29]
Cites
Combinatorial Receptor Codes for Odors
Malnic, B., Hirono, J., Sato, T., & Buck, L. B. (1999) · Cell · doi:10.1016/s0092-8674(00)80581-4 · Cited by 2,302 · see citing works
Visualizing an Olfactory Sensory Map
Mombaerts, P., Wang, F., Dulac, C. G., Chao, S. K., Nemes, A., Mendelsohn, M. M., Edmondson, J., & Axel, R. (1996) · Cell · doi:10.1016/s0092-8674(00)81387-2 · Cited by 1,992 · see citing works
pEF-BOS, a powerful mammalian expression vector
Mizushima, S., & Nagata, S. (1990) · Nucleic Acids Research · doi:10.1093/nar/18.17.5322 · Cited by 1,632 · see citing works
Topographic organization of sensory projections to the olfactory bulb
Vassar, R. J., Chao, S. K., Sitcheran, R., ̃ez, J. M. N., Vosshall, L. B., & Axel, R. (1994) · Cell · doi:10.1016/0092-8674(94)90029-9 · Cited by 1,281 · see citing works
Ressler, K. J., Sullivan, S. L., & Buck, L. B. (1994) · Cell · doi:10.1016/0092-8674(94)90015-9 · Cited by 1,202 · see citing works
Allelic inactivation regulates olfactory receptor gene expression
Chess, A. J., Simon, I., Cedar, H., & Axel, R. (1994) · Cell · doi:10.1016/s0092-8674(94)90562-2 · Cited by 1,066 · see citing works
The Olfactory Bulb: Coding and Processing of Odor Molecule Information
Mori, K., Nagao, H., & Yoshihara, Y. (1999) · Science · doi:10.1126/science.286.5440.711 · Cited by 937 · see citing works
Self-citationManess, P. F., & Schachner, M. (2006) · Nature Neuroscience · doi:10.1038/nn1827 · Cited by 850 · see citing works
Negative Feedback Regulation Ensures the One Receptor-One Olfactory Neuron Rule in Mouse
Serizawa, S., Miyamichi, K., Nakatani, H., Suzuki, M., Saito, M., Yoshihara, Y., & Sakano, H. (2003) · Science · doi:10.1126/science.1089122 · Cited by 540 · see citing works
Self-citationBoyle, M. E., Berglund, E., Murai, K., Weber, L., Peles, E., & Ranscht, B. (2001) · Neuron · doi:10.1016/s0896-6273(01)00296-3 · Cited by 539 · see citing works
The molecular receptive range of an odorant receptor
Araneda, R. C., Kini, A. D., & Firestein, S. (2000) · Nature Neuroscience · doi:10.1038/81774 · Cited by 525 · see citing works
Brunet, L. J., Gold, G. H., & Ngai, J. (1996) · Neuron · doi:10.1016/s0896-6273(00)80200-7 · Cited by 510 · see citing works
Maps of Odorant Molecular Features in the Mammalian Olfactory Bulb
Mori, K., Takahashi, Y. K., Igarashi, K. M., & Yamaguchi, M. (2006) · Physiological Reviews · doi:10.1152/physrev.00021.2005 · Cited by 397 · see citing works
Immunohistochemical localization of candidates for vesicular glutamate transporters in the rat brain
Kaneko, T., Fujiyama, F., & Hioki, H. (2002) · The Journal of Comparative Neurology · doi:10.1002/cne.10129 · Cited by 395 · see citing works
A Neuronal Identity Code for the Odorant Receptor-Specific and Activity-Dependent Axon Sorting
Serizawa, S., Miyamichi, K., Takeuchi, H., Yamagishi, Y., Suzuki, M., & Sakano, H. (2006) · Cell · doi:10.1016/j.cell.2006.10.031 · Cited by 349 · see citing works
Cheng, H.-J., & Flanagan, J. G. (1994) · Cell · doi:10.1016/0092-8674(94)90408-1 · Cited by 335 · see citing works
Odorant Receptor–Derived cAMP Signals Direct Axonal Targeting
Imai, T., Suzuki, M., & Sakano, H. (2006) · Science · doi:10.1126/science.1131794 · Cited by 323 · see citing works
Yoshihara, Y., Kawasaki, M., Tamada, A., Fujita, H., Hayashi, H., Kagamiyama, H., & Mori, K. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-15-05830.1997 · Cited by 299 · see citing works
Self-citationGene Switching and the Stability of Odorant Receptor Gene Choice
Shykind, B., Rohani, S., O'Donnell, S., Nemes, A., Mendelsohn, M. M., Sun, Y., Axel, R., & Barnea, G. (2004) · Cell · doi:10.1016/j.cell.2004.05.015 · Cited by 273 · see citing works
Mutually exclusive expression of odorant receptor transgenes
Serizawa, S., Ishii, T., Nakatani, H., Tsuboi, A., Nagawa, F., Asano, M., Sudo, K., Sakagami, J., Sakano, H., Ijiri, T., et al. (2000) · Nature Neuroscience · doi:10.1038/76641 · Cited by 264 · see citing works
A feedback mechanism regulates monoallelic odorant receptor expression
Lewcock, J. W., & Reed, R. R. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0307986100 · Cited by 250 · see citing works
Traka, M., Goutebroze, L., Denisenko, N., Bessa, M. J., Nifli, A., Havaki, S., Iwakura, Y., Fukamauchi, F., Watanabe, K., Soliven, B. C., et al. (2003) · The Journal of Cell Biology · doi:10.1083/jcb.200305078 · Cited by 249 · see citing works
Zheng, C., Feinstein, P. G., Bozza, T. C., Rodríguez, I., & Mombaerts, P. (2000) · Neuron · doi:10.1016/s0896-6273(00)81140-x · Cited by 233 · see citing works
Ataxia and abnormal cerebellar microorganization in mice with ablated contactin gene expression.
Berglund, E., Murai, K., Fredette, B., Sekerkovâ, G., Marturano, B., Weber, L., Mugnaini, E., & Ranscht, B. (1999) · Neuron · doi:10.1016/s0896-6273(00)81126-5 · Cited by 216 · see citing works
Local Permutations in the Glomerular Array of the Mouse Olfactory Bulb
Strotmann, J. M., Conzelmann, S., Beck, A., Feinstein, P. G., Breer, H., & Mombaerts, P. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-18-06927.2000 · Cited by 210 · see citing works
Semaphorin 3A Is Required for Guidance of Olfactory Axons in Mice
Schwarting, G. A., Kostek, C. A., Ahmad, N., Dibble, C. C., Pays, L., & Püschel, A. W. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-20-07691.2000 · Cited by 205 · see citing works
Axonal Ephrin-As and Odorant Receptors
Cutforth, T., Moring, L., Mendelsohn, M. M., Nemes, A., Shah, N. M., Kim, M. M., Frisén, J., & Axel, R. (2003) · Cell · doi:10.1016/s0092-8674(03)00568-3 · Cited by 196 · see citing works
Zhao, H., & Reed, R. R. (2001) · Cell · doi:10.1016/s0092-8674(01)00262-8 · Cited by 194 · see citing works
Fernandez, T. V., Morgan, T. M., Davis, N., Klin, A. J., Morris, A., Farhi, A., Lifton, R. P., & State, M. W. (2004) · The American Journal of Human Genetics · doi:10.1086/421474 · Cited by 191 · see citing works
Odorant Receptors on Axon Termini in the Brain
Barnea, G., O'Donnell, S., Mancia, F., Sun, X., Nemes, A., Mendelsohn, M. M., & Axel, R. (2004) · Science · doi:10.1126/science.1096146 · Cited by 181 · see citing works
Aberrant Sensory Innervation of the Olfactory Bulb in Neuropilin-2 Mutant Mice
Walz, A., Rodríguez, I., & Mombaerts, P. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-10-04025.2002 · Cited by 173 · see citing works
Oka, Y., Katada, S., Omura, M., Suwa, M., Yoshihara, Y., & Touhara, K. (2006) · Neuron · doi:10.1016/j.neuron.2006.10.019 · Cited by 173 · see citing works
Self-citationNadi, N. S., Head, R. J., Grillo, M., et al. (1981) · Brain Research · doi:10.1016/0006-8993(81)90241-9 · Cited by 169 · see citing works
Yoshihara, Y., Kawasaki, M., Tamada, A., Nagata, S., Kagamiyama, H., & Mori, K. (1995) · Journal of Neurobiology · doi:10.1002/neu.480280106 · Cited by 154 · see citing works
Self-citationMcBride, K. (2003) · Chemical Senses · doi:10.1093/chemse/bjg053 · Cited by 144 · see citing works
F3/contactin, a neuronal cell adhesion molecule implicated in axogenesis and myelination
Falk, J., Bonnon, C., Girault, J., & Faivre-Sarrailh, C. (2002) · Biology of the Cell · doi:10.1016/s0248-4900(02)00006-0 · Cited by 139 · see citing works
Olfactory Receptor Proteins in Axonal Processes of Chemosensory Neurons
Strotmann, J. M., Lévai, O., Fleischer, J., et al. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.2588-04.2004 · Cited by 138 · see citing works
Distorted Odor Maps in the Olfactory Bulb of Semaphorin 3A-Deficient Mice
Taniguchi, M., Nagao, H., Takahashi, Y. K., Yamaguchi, M., Mitsui, S., Yagi, T., Mori, K., & Shimizu, T. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-04-01390.2003 · Cited by 113 · see citing works
Flanagan, J. G., Cheng, H.-J., Feldheim, D. A., Hattori, M., Lü, Q., & Vanderhaeghen, P. (2000) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(00)27264-9 · Cited by 113 · see citing works
Arxhomeobox gene is essential for development of mouse olfactory system
Yoshihara, S., Omichi, K., Yanazawa, M., Kitamura, K., & Yoshihara, Y. (2005) · Development · doi:10.1242/dev.01619 · Cited by 108 · see citing works
Self-citationVariability of position of the P2 glomerulus within a map of the mouse olfactory bulb
Schaefer, M. L., Finger, T. E., & Restrepo, D. (2001) · The Journal of Comparative Neurology · doi:10.1002/cne.1072 · Cited by 107 · see citing works
Miyasaka, N., Knaut, H., & Yoshihara, Y. (2007) · Development · doi:10.1242/dev.001958 · Cited by 102 · see citing works
Self-citationMurai, K., Misner, D., & Ranscht, B. (2002) · Current Biology · doi:10.1016/s0960-9822(02)00680-2 · Cited by 98 · see citing works
Two mirror-image sensory maps with domain organization in the mouse main olfactory bulb
Nagao, H., Yoshihara, Y., Mitsui, S., et al. (2000) · Neuroreport · doi:10.1097/00001756-200009110-00039 · Cited by 89 · see citing works
Self-citationRobo2 is required for establishment of a precise glomerular map in the zebrafish olfactory system
Miyasaka, N., Sato, Y., Yeo, S.-Y., et al. (2005) · Development · doi:10.1242/dev.01698 · Cited by 83 · see citing works
Transgenic expression of Cre recombinase in mitral/tufted cells of the olfactory bulb
Nagai, Y., Sano, H., & Yokoi, M. (2005) · genesis · doi:10.1002/gene.20146 · Cited by 82 · see citing works
Stone, D. M., Wessel, T. C., JOH, T. H., & Baker, H. A. (1990) · Molecular Brain Research · doi:10.1016/0169-328x(90)90042-c · Cited by 76 · see citing works
Takeda, Y., Akasaka, K., Lee, S., Kobayashi, S., Kawano, H., Murayama, S., Takahashi, N., Hashimoto, K., Kano, M., Asano, M., et al. (2003) · Journal of Neurobiology · doi:10.1002/neu.10222 · Cited by 71 · see citing works
Faivre‐Sarrailh, C., & Rougon, G. (1997) · Molecular and Cellular Neuroscience · doi:10.1006/mcne.1997.0609 · Cited by 63 · see citing works
Denaxa, M., Kyriakopoulou, K., Theodorakis, Κ., Trichas, G., Vidaki, M., Takeda, Y., Watanabe, K., & Karagogeos, D. (2005) · Developmental Biology · doi:10.1016/j.ydbio.2005.09.021 · Cited by 58 · see citing works
Yoshihara, Y., Oka, S., Watanabe, Y., et al. (1991) · The Journal of Cell Biology · doi:10.1083/jcb.115.3.731 · Cited by 56 · see citing works
Self-citationNakajima, D., Nakayama, M., Kikuno, R. F., Hirosawa, M., Nagase, T., & Ohara, O. (2001) · Molecular Brain Research · doi:10.1016/s0169-328x(01)00218-2 · Cited by 52 · see citing works
Experience-Dependent Modifications in MAP2 Phosphorylation in Rat Olfactory Bulb
Philpot, B. D., Lim, J. H., Halpain, S., et al. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-24-09596.1997 · Cited by 47 · see citing works
Aberrant responses to acoustic stimuli in mice deficient for neural recognition molecule NB‐2
Li, H., Takeda, Y., Niki, H., Ogawa, J., Kobayashi, S., Kai, N., Akasaka, K., Asano, M., Sudo, K., Iwakura, Y., et al. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02514.x · Cited by 45 · see citing works
The contactin 4 gene locus at 3p26 is a candidate gene of SCA16
Miura, S., Shibata, H., Furuya, H., et al. (2006) · Neurology · doi:10.1212/01.wnl.0000238510.84932.82 · Cited by 39 · see citing works
Zeng, L., Zhang, C., Xu, J., Ye, X., Wu, Q. Y., Dai, J., Ji, C., Gu, S., Xie, Y., & Mao, Y. (2002) · Journal of Human Genetics · doi:10.1007/s100380200073 · Cited by 30 · see citing works
Cloning and characterization of the human neural cell adhesion molecule, CNTN4 (alias BIG-2)
Hansford, L. M., Smith, S. A., Haber, M., et al. (2003) · Cytogenetic and Genome Research · doi:10.1159/000073412 · Cited by 28 · see citing works
Defining a Role and Mechanism for Igcam Function in Vertebrate Axon Guidance
Rutishauser, U. S. (2000) · The Journal of Cell Biology · doi:10.1083/jcb.149.4.757 · Cited by 19 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Gene expression elucidates functional impact of polygenic risk for schizophrenia
Fromer, M., Roussos, P., Sieberts, S. K., Johnson, J. S., Kavanagh, D. H., Perumal, T. M., Ruderfer, D. M., Oh, E. C., Topol, A., Shah, H. R., et al. (2016) · Nature Neuroscience · doi:10.1038/nn.4399 · Cited by 1,091 · see citing works
Contactins: Emerging key roles in the development and function of the nervous system
Shimoda, Y., & Watanabe, K. (2009) · Cell Adhesion & Migration · doi:10.4161/cam.3.1.7764 · Cited by 149 · see citing works
Bouyain, S., & Watkins, D. J. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0911235107 · Cited by 119 · see citing works
- Authors
- Kaneko-Goto, T., Yoshihara, S.-I., Miyazaki, H., & Yoshihara, Y.
- Affiliations
- RIKEN Center for Brain Science (JP)
- Corresponding author
- Yoshihara, Yoshihiro
- ORCID
- Yoshihara, Yoshihiro
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2008-03
- Volume
- 57
- Issue
- 6
- Pages
- 834-846
- ISSN
- 0896-6273 (ISSN-L)
- OpenAlex
- W2050495774
- Cited by
- 142
- References
- 58
- Citations by year
- 2026: 2 · 2024: 6 · 2023: 4 · 2022: 3 · 2021: 8 · 2020: 3 · 2019: 6 · 2018: 11 · 2017: 8 · 2016: 9 · 2015: 7 · 2014: 4 · 2013: 11 · 2012: 14
- FWCI
- 6.63
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 2000 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Ministry of Education, Culture, Sports, Science and Technology
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Axon Guidance and Neuronal Signaling
- Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- olfactory sensory neurons, axon guidance, olfactory glomeruli, olfactory receptors, odor maps, olfactory bulb, immunoglobulin superfamily, ephrin-A5
- MeSH terms
- Animals, Animals, Newborn, Axons, Gene Expression Regulation, Membrane Proteins, Mice, Transgenic, Nerve Net, Olfactory Bulb, Olfactory Nerve, Cell Adhesion Molecules, Neuronal, Gene Expression, Mutagenesis, Olfactory Receptor Neurons, Ephrin-A5, Mice, Olfactory Marker Protein, Contactins, Olfactory Nerve Injuries
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
