{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,25]],"date-time":"2026-09-25T06:31:59Z","timestamp":1790317919296,"version":"4.1.0"},"reference-count":56,"publisher":"The Company of Biologists","issue":"22","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2007,11,15]]},"abstract":"<jats:p>The olfactory system of the mouse includes several subsystems that project axons from the olfactory epithelium to the olfactory bulb. Among these is a subset of neurons that do not express the canonical pathway of olfactory signal transduction, but express guanylate cyclase-D (GC-D). These GC-D-positive (GC-D+) neurons are not known to express odorant receptors. Axons of GC-D+ neurons project to the necklace glomeruli, which reside between the main and accessory olfactory bulbs. To label the subset of necklace glomeruli that receive axonal input from GC-D+ neurons, we generated two strains of mice with targeted mutations in the GC-D gene (Gucy2d). These mice co-express GC-D with an axonal marker, tau-\u03b2-galactosidase or tauGFP, by virtue of a bicistronic strategy that leaves the coding region of the Gucy2d gene intact. With these strains, the patterns of axonal projections of GC-D+ neurons to necklace glomeruli can be visualized in whole mounts. We show that deficiency of one of the neuropilin 2 ligands of the class III semaphorin family, Sema3f, but not Sema3b, phenocopies the loss of neuropilin 2 (Nrp2) for axonal wiring of GC-D+ neurons. Some glomeruli homogeneously innervated by axons of GC-D+ neurons form ectopically within the glomerular layer, across wide areas of the main olfactory bulb. Similarly, axonal wiring of some vomeronasal sensory neurons is perturbed by a deficiency of Nrp2 or Sema3f, but not Sema3b or Sema3c. Our findings provide genetic evidence for a Nrp2-Sema3f interaction as a determinant of the wiring of axons of GC-D+ neurons into the unusual configuration of necklace glomeruli.<\/jats:p>","DOI":"10.1242\/dev.008722","type":"journal-article","created":{"date-parts":[[2007,10,18]],"date-time":"2007-10-18T01:04:17Z","timestamp":1192669457000},"page":"4063-4072","source":"Crossref","is-referenced-by-count":62,"title":["Axonal wiring of guanylate cyclase-D-expressing olfactory neurons is dependent on neuropilin 2 and semaphorin 3F"],"prefix":"10.1242","volume":"134","author":[{"given":"Andreas","family":"Walz","sequence":"first","affiliation":[{"name":"The Rockefeller University, 1230 York Avenue, New York, NY 10021,USA."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Paul","family":"Feinstein","sequence":"additional","affiliation":[{"name":"The Rockefeller University, 1230 York Avenue, New York, NY 10021,USA."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mona","family":"Khan","sequence":"additional","affiliation":[{"name":"The Rockefeller University, 1230 York Avenue, New York, NY 10021,USA."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Peter","family":"Mombaerts","sequence":"additional","affiliation":[{"name":"The Rockefeller University, 1230 York Avenue, New York, NY 10021,USA."}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"237","reference":[{"key":"2021042621072332400_REF1","doi-asserted-by":"crossref","unstructured":"Axel, R. (2005). Scents and sensibility: a molecular logic of olfactory perception. Angew. Chem. Int. Ed. Engl.38,6110-6127.","DOI":"10.1002\/anie.200501726"},{"key":"2021042621072332400_REF2","doi-asserted-by":"crossref","unstructured":"Belluscio, L., Koentges, G., Axel, R. and Dulac, C.(1999). A map of pheromone receptor activation in the mammalian brain. Cell97,209-220.","DOI":"10.1016\/S0092-8674(00)80731-X"},{"key":"2021042621072332400_REF3","doi-asserted-by":"crossref","unstructured":"Bozza, T., Feinstein, P., Zheng, C. and Mombaerts, P.(2002). Odorant receptor expression defines functional units in the mouse olfactory system. J. Neurosci.22,3033-3043.","DOI":"10.1523\/JNEUROSCI.22-08-03033.2002"},{"key":"2021042621072332400_REF4","doi-asserted-by":"crossref","unstructured":"Buck, L. B. (2005). Unraveling the sense of smell. Angew. Chem. Int. Ed. Engl.38,6128-6140.","DOI":"10.1002\/anie.200501120"},{"key":"2021042621072332400_REF5","doi-asserted-by":"crossref","unstructured":"Cai, H. and Reed, R. R. (1999). Cloning and characterization of neuropilin-1-interacting protein: a PSD-95\/Dlg\/ZO-1 domain-containing protein that interacts with the cytoplasmic domain of neuropilin-1. J. Neurosci.19,6519-6527.","DOI":"10.1523\/JNEUROSCI.19-15-06519.1999"},{"key":"2021042621072332400_REF6","doi-asserted-by":"crossref","unstructured":"Castellani, V., Chedotal, A., Schachner, M., Faivre-Sarrailh, C. and Rougon, G. (2000). Analysis of the L1-deficient mouse phenotype reveals cross-talk between Sema3A and L1 signaling pathways in axonal guidance. Neuron27,237-249.","DOI":"10.1016\/S0896-6273(00)00033-7"},{"key":"2021042621072332400_REF7","doi-asserted-by":"crossref","unstructured":"Chen, H., Chedotal, A., He, Z., Goodman, C. S. and Tessier-Lavigne, M. (1997). Neuropilin-2, a novel member of the neuropilin family, is a high affinity receptor for the semaphorins Sema E and Sema IV but not Sema III. Neuron19,547-559.","DOI":"10.1016\/S0896-6273(00)80371-2"},{"key":"2021042621072332400_REF8","doi-asserted-by":"crossref","unstructured":"Cloutier, J. F., Giger, R. J., Koentges, G., Dulac, C.,Kolodkin, A. L. and Ginty, D. D. (2002). Neuropilin-2 mediates axonal fasciculation, zonal segregation, but not axonal convergence,of primary accessory olfactory neurons. Neuron33,877-892.","DOI":"10.1016\/S0896-6273(02)00635-9"},{"key":"2021042621072332400_REF9","doi-asserted-by":"crossref","unstructured":"Cloutier, J. F., Sahay, A., Chang, E. C., Tessier-Lavigne, M.,Dulac, C., Kolodkin, A. L. and Ginty, D. D. (2004). Differential requirements for semaphorin 3F and Slit-1 in axonal targeting,fasciculation, and segregation of olfactory sensory neuron projections. J. Neurosci.24,9087-9096.","DOI":"10.1523\/JNEUROSCI.2786-04.2004"},{"key":"2021042621072332400_REF10","doi-asserted-by":"crossref","unstructured":"Fan, J. and Raper, J. A. (1995). Localized collapsing cues can steer growth cones without inducing their full collapse. Neuron14,263-274.","DOI":"10.1016\/0896-6273(95)90284-8"},{"key":"2021042621072332400_REF11","doi-asserted-by":"crossref","unstructured":"Feiner, L., Webber, A. L., Brown, C. B., Lu, M. M., Jia, L.,Feinstein, P., Mombaerts, P., Epstein, J. A. and Raper, J. A.(2001). Targeted disruption of semaphorin 3C leads to persistent truncus arteriosus and aortic arch interruption. Development128,3061-3070.","DOI":"10.1242\/dev.128.16.3061"},{"key":"2021042621072332400_REF12","doi-asserted-by":"crossref","unstructured":"Feinstein, P. and Mombaerts, P. (2004). A contextual model for axonal sorting into glomeruli in the mouse olfactory system. Cell117,817-831.","DOI":"10.1016\/j.cell.2004.05.011"},{"key":"2021042621072332400_REF13","doi-asserted-by":"crossref","unstructured":"Fleischer, J., Schwarzenbacher, K., Besser, S., Hass, N. and Breer, H. (2006). Olfactory receptors and signaling elements in the Grueneberg ganglion. J. Neurochem.98,543-554.","DOI":"10.1111\/j.1471-4159.2006.03894.x"},{"key":"2021042621072332400_REF14","doi-asserted-by":"crossref","unstructured":"Fu\u0308lle, H. J., Vassar, R., Foster, D. C., Yang, R. B., Axel,R. and Garbers, D. L. (1995). A receptor guanylate cyclase expressed specifically in olfactory sensory neurons. Proc. Natl. Acad. Sci. USA92,3571-3575.","DOI":"10.1073\/pnas.92.8.3571"},{"key":"2021042621072332400_REF15","doi-asserted-by":"crossref","unstructured":"Fuss, S. H., Omura, M. and Mombaerts, P.(2005). The Grueneberg ganglion of the mouse projects axons to glomeruli in the olfactory bulb. Eur. J. Neurosci.22,2649-2654.","DOI":"10.1111\/j.1460-9568.2005.04468.x"},{"key":"2021042621072332400_","doi-asserted-by":"crossref","unstructured":"Gonthier, B., Nasarre, C., Roth, L., Perraut, M., Thomasset, N.,Roussel, G., Aunis, D. and Bagnard, D. (2007). Functional interaction between matrix metalloproteinase-3 and semaphorin-3C during cortical axonal growth and guidance. Cereb. Cortex17,1712-1721.","DOI":"10.1093\/cercor\/bhl082"},{"key":"2021042621072332400_REF17","doi-asserted-by":"crossref","unstructured":"Greer, C. A., Stewart, W. B., Teicher, M. H. and Shepherd, G. M. (1982). Functional development of the olfactory bulb and a unique glomerular complex in the neonatal rat. J. Neurosci.2,1744-1759.","DOI":"10.1523\/JNEUROSCI.02-12-01744.1982"},{"key":"2021042621072332400_REF18","doi-asserted-by":"crossref","unstructured":"Grosmaitre, X., Santarelli, L. C., Tan, J., Luo, M. and Ma,M. (2007). Dual functions of mammalian olfactory sensory neurons as odor detectors and mechanical sensors. Nat. Neurosci.10,348-354.","DOI":"10.1038\/nn1856"},{"key":"2021042621072332400_REF19","unstructured":"Grueneberg, H. (1973). A ganglion probably belonging to the N. terminalis system in the nasal mucosa of the mouse. Z. Anat. Entwicklungsgesch.140, 39-52."},{"key":"2021042621072332400_REF20","doi-asserted-by":"crossref","unstructured":"Hu, J., Zhong, C., Ding, C., Chi, Q., Walz, A., Mombaerts, P.,Matsunami, H. and Luo, M. (2007). Detection of near-atmospheric concentrations of CO2 by an olfactory subsystem in the mouse. Science317,953-957.","DOI":"10.1126\/science.1144233"},{"key":"2021042621072332400_REF21","doi-asserted-by":"crossref","unstructured":"Juilfs, D. M., Fu\u0308lle, H. J., Zhao, A. Z., Houslay, M. D.,Garbers, D. L. and Beavo, J. A. (1997). A subset of olfactory neurons that selectively express cGMP-stimulated phosphodiesterase (PDE2) and guanylate cyclase-D define a unique olfactory signal transduction pathway. Proc. Natl. Acad. Sci. USA94,3388-3395.","DOI":"10.1073\/pnas.94.7.3388"},{"key":"2021042621072332400_REF22","doi-asserted-by":"crossref","unstructured":"Julien, F., Bechara, A., Fiore, R., Nawabi, H., Zhou, H.,Hoyo-Becerra, C., Bozon, M., Rougon, G., Grumet, M., Pu\u0308schel, A. W. et al. (2005). Dual functional activity of semaphorin 3B is required for positioning the anterior commissure. Neuron48,63-75.","DOI":"10.1016\/j.neuron.2005.08.033"},{"key":"2021042621072332400_REF23","doi-asserted-by":"crossref","unstructured":"Kolodkin, A. L., Levengood, D. V., Rowe, E. G., Tai, Y. T.,Giger, R. J. and Ginty, D. D. (1997). Neuropilin is a semaphorin III receptor. Cell90,753-762.","DOI":"10.1016\/S0092-8674(00)80535-8"},{"key":"2021042621072332400_REF24","doi-asserted-by":"crossref","unstructured":"Koos, D. S. and Fraser, S. E. (2005). The Grueneberg ganglion projects to the olfactory bulb. Neuroreport16,1929-1932.","DOI":"10.1097\/01.wnr.0000186597.72081.10"},{"key":"2021042621072332400_REF25","doi-asserted-by":"crossref","unstructured":"Kuhn, M. (2003). Structure, regulation, and function of mammalian membrane guanylate cyclase receptors, with a focus on guanylate cyclase-A. Circ. Res.93,700-709.","DOI":"10.1161\/01.RES.0000094745.28948.4D"},{"key":"2021042621072332400_REF26","doi-asserted-by":"crossref","unstructured":"Le Jeune, H. and Jourdan, F. (1991). Postnatal development of cholinergic markers in the rat olfactory bulb: a histochemical and immunocytochemical study. J. Comp. Neurol.314,383-395.","DOI":"10.1002\/cne.903140212"},{"key":"2021042621072332400_REF27","doi-asserted-by":"crossref","unstructured":"Le Jeune, H. and Jourdan, F. (1993). Cholinergic innervation of olfactory glomeruli in the rat: an ultrastructural immunocytochemical study. J. Comp. Neurol.336,279-292.","DOI":"10.1002\/cne.903360209"},{"key":"2021042621072332400_REF28","doi-asserted-by":"crossref","unstructured":"Liberles, S. D. and Buck, L. B. (2006). A second class of chemosensory receptors in the olfactory epithelium. Nature442,645-650.","DOI":"10.1038\/nature05066"},{"key":"2021042621072332400_REF29","doi-asserted-by":"crossref","unstructured":"Ma, M., Grosmaitre, X., Iwema, C. L., Baker, H., Greer, C. A. and Shepherd, G. M. (2003). Olfactory signal transduction in the mouse septal organ. J. Neurosci.23,317-324.","DOI":"10.1523\/JNEUROSCI.23-01-00317.2003"},{"key":"2021042621072332400_REF30","doi-asserted-by":"crossref","unstructured":"Meyer, M. R., Angele, A., Kremmer, E., Kaupp, U. B. and Muller,F. (2000). A cGMP-signaling pathway in a subset of olfactory sensory neurons. Proc. Natl. Acad. Sci. USA97,10595-10600.","DOI":"10.1073\/pnas.97.19.10595"},{"key":"2021042621072332400_REF31","doi-asserted-by":"crossref","unstructured":"Miyazaki, N., Furuyama, T., Sakai, T., Fujioka, S., Mori, T.,Ohoka, Y., Takeda, N., Kubo, T. and Inagaki, S. (1999). Developmental localization of semaphorin H messenger RNA acting as a collapsing factor on sensory axons in the mouse brain. Neuroscience93,401-408.","DOI":"10.1016\/S0306-4522(99)00134-7"},{"key":"2021042621072332400_REF32","doi-asserted-by":"crossref","unstructured":"Mombaerts, P. (2004). Genes and ligands for odorant, vomeronasal and taste receptors. Nat. Rev. Neurosci.5,263-278.","DOI":"10.1038\/nrn1365"},{"key":"2021042621072332400_REF33","doi-asserted-by":"crossref","unstructured":"Mombaerts, P. (2006). Axonal wiring in the mouse olfactory system. Annu. Rev. Cell Dev. Biol.22,713-737.","DOI":"10.1146\/annurev.cellbio.21.012804.093915"},{"key":"2021042621072332400_REF34","doi-asserted-by":"crossref","unstructured":"Mombaerts, P., Wang, F., Dulac, C., Chao, S. K., Nemes, A.,Mendelsohn, M., Edmondson, J. and Axel, R. (1996). Visualizing an olfactory sensory map. Cell87,675-686.","DOI":"10.1016\/S0092-8674(00)81387-2"},{"key":"2021042621072332400_REF35","doi-asserted-by":"crossref","unstructured":"Moon, C., Jaberi, P., Otto-Bruc, A., Baehr, W., Palczewski, K. and Ronnett, G. V. (1998). Calcium-sensitive particulate guanylate cyclase as a modulator of cAMP in olfactory receptor neurons. J. Neurosci.18,3195-3205.","DOI":"10.1523\/JNEUROSCI.18-09-03195.1998"},{"key":"2021042621072332400_REF36","doi-asserted-by":"crossref","unstructured":"Moreno-Flores, M. T., Martin-Aparicio, E., Martin-Bermejo, M. J., Agudo, M., McMahon, S., Avila, J., Diaz-Nido, J. and Wandosell, F.(2003). Semaphorin 3C preserves survival and induces neuritogenesis of cerebellar granule neurons in culture. J. Neurochem.87,879-890.","DOI":"10.1046\/j.1471-4159.2003.02051.x"},{"key":"2021042621072332400_REF37","doi-asserted-by":"crossref","unstructured":"Ring, G., Mezza, R. C. and Schwob, J. E.(1997). Immunohistochemical identification of discrete subsets of rat olfactory neurons and the glomeruli that they innervate. J. Comp. Neurol.388,415-434.","DOI":"10.1002\/(SICI)1096-9861(19971124)388:3<415::AID-CNE5>3.0.CO;2-3"},{"key":"2021042621072332400_REF38","doi-asserted-by":"crossref","unstructured":"Risser, J. M. and Slotnick, B. M. (1987). Suckling behavior in rat pups with lesions which destroy the modified glomerular complex. Brain Res. Bull.19,275-281.","DOI":"10.1016\/0361-9230(87)90093-1"},{"key":"2021042621072332400_REF39","unstructured":"Rodolfo-Masera, T. (1943). Su l'esistenza di un particolare organo olfacttivo nel setto nasale della cavia e di altri roditori. Arch. Ital. Anat. Embryol.48,157-212."},{"key":"2021042621072332400_REF40","doi-asserted-by":"crossref","unstructured":"Rodriguez, I., Feinstein, P. and Mombaerts, P.(1999). Variable patterns of axonal projections of sensory neurons in the mouse vomeronasal system. Cell97,199-208.","DOI":"10.1016\/S0092-8674(00)80730-8"},{"key":"2021042621072332400_REF41","doi-asserted-by":"crossref","unstructured":"Roppolo, D., Ribaud, V., Jungo, V. P., Luscher, C. and Rodriguez, I. (2006). Projection of the Grueneberg ganglion to the mouse olfactory bulb. Eur. J. Neurosci.23,2887-2894.","DOI":"10.1111\/j.1460-9568.2006.04818.x"},{"key":"2021042621072332400_REF42","doi-asserted-by":"crossref","unstructured":"Sahay, A., Molliver, M. E., Ginty, D. D. and Kolodkin, A. L.(2003). Semaphorin 3F is critical for development of limbic system circuitry and is required in neurons for selective CNS axon guidance events. J. Neurosci.23,6671-6680.","DOI":"10.1523\/JNEUROSCI.23-17-06671.2003"},{"key":"2021042621072332400_REF43","doi-asserted-by":"crossref","unstructured":"Shinoda, K., Shiotani, Y. and Osawa, Y. (1989).\u201cNecklace olfactory glomeruli\u201d form unique components of the rat primary olfactory system. J. Comp. Neurol.284,362-373.","DOI":"10.1002\/cne.902840304"},{"key":"2021042621072332400_REF44","doi-asserted-by":"crossref","unstructured":"Shinoda, K., Ohtsuki, T., Nagano, M. and Okumura, T.(1993). A possible functional necklace formed by placental antigen X-P2-immunoreactive and intensely acetylcholinesterase-reactive(PAX\/IAE) glomerular complexes in the rat olfactory bulb. Brain Res.618,160-166.","DOI":"10.1016\/0006-8993(93)90440-X"},{"key":"2021042621072332400_REF45","doi-asserted-by":"crossref","unstructured":"Steup, A., Ninnemann, O., Savaskan, N. E., Nitsch, R.,Pu\u0308schel, A. W. and Skutella, T. (1999). Semaphorin D acts as a repulsive factor for entorhinal and hippocampal neurons. Eur. J. Neurosci.11,729-734.","DOI":"10.1046\/j.1460-9568.1999.00517.x"},{"key":"2021042621072332400_REF46","doi-asserted-by":"crossref","unstructured":"Takahashi, T., Nakamura, F., Jin, Z., Kalb, R. G. and Strittmatter, S. M. (1998). Semaphorins A and E act as antagonists of neuropilin-1 and agonists of neuropilin-2 receptors. Nat. Neurosci.1,487-493.","DOI":"10.1038\/2203"},{"key":"2021042621072332400_REF47","unstructured":"Tamagnone, L., Artigiani, S., Chen, H., He, Z., Ming, G. I.,Song, H., Chedotal, A., Winberg, M. L., Goodman, C. S., Poo, M. et al.(2001). Plexins are a large family of receptors for transmembrane, secreted, and GPI-anchored semaphorins in vertebrates. Cell99,71-80."},{"key":"2021042621072332400_REF48","doi-asserted-by":"crossref","unstructured":"Terman, J. R., Mao, T., Pasterkamp, R. J., Yu, H. H. and Kolodkin, A. L. (2002). MICALs, a family of conserved flavoprotein oxidoreductases, function in plexin-mediated axonal repulsion. Cell109,887-900.","DOI":"10.1016\/S0092-8674(02)00794-8"},{"key":"2021042621072332400_REF49","doi-asserted-by":"crossref","unstructured":"Tian, H. and Ma, M. (2004). Molecular organization of the olfactory septal organ. J. Neurosci.24,8383-8390.","DOI":"10.1523\/JNEUROSCI.2222-04.2004"},{"key":"2021042621072332400_REF50","doi-asserted-by":"crossref","unstructured":"Walz, A., Rodriguez, I. and Mombaerts, P.(2002). Aberrant sensory innervation of the olfactory bulb in neuropilin-2 mutant mice. J. Neurosci.22,4025-4035.","DOI":"10.1523\/JNEUROSCI.22-10-04025.2002"},{"key":"2021042621072332400_REF51","doi-asserted-by":"crossref","unstructured":"Walz, A., Omura, M. and Mombaerts, P. (2006). Development and topography of the lateral olfactory tract in the mouse:imaging by genetically encoded and injected fluorescent markers. J. Neurobiol.66,835-846.","DOI":"10.1002\/neu.20266"},{"key":"2021042621072332400_REF52","doi-asserted-by":"crossref","unstructured":"Weruaga, E., Brinon, J. G., Porteros, A., Arevalo, R., Aijon, J. and Alonso, J. R. (2001). A sexually dimorphic group of atypical glomeruli in the mouse olfactory bulb. Chem. Senses26,7-15.","DOI":"10.1093\/chemse\/26.1.7"},{"key":"2021042621072332400_REF53","doi-asserted-by":"crossref","unstructured":"Yang, R. B., Fu\u0308lle, H. J. and Garbers, D. L.(1996). Chromosomal localization and genomic organization of genes encoding guanylate cyclase receptors expressed in olfactory sensory neurons and retina. Genomics31,367-372.","DOI":"10.1006\/geno.1996.0060"},{"key":"2021042621072332400_REF54","doi-asserted-by":"crossref","unstructured":"Yaron, A., Huang, P. H., Cheng, H. J. and Tessier-Lavigne,M. (2005). Differential requirement for Plexin-A3 and -A4 in mediating responses of sensory and sympathetic neurons to distinct class 3 Semaphorins. Neuron45,513-523.","DOI":"10.1016\/j.neuron.2005.01.013"},{"key":"2021042621072332400_REF55","doi-asserted-by":"crossref","unstructured":"Zhang, X., Zhang, Z. and Firestein, S. (2007). Comparative genomics of odorant and pheromone receptor genes in rodents. Genomics89,441-450.","DOI":"10.1016\/j.ygeno.2007.01.002"},{"key":"2021042621072332400_REF56","doi-asserted-by":"crossref","unstructured":"Zheng, L. M., Ravel, N. and Jourdan, F. (1987). Topography of centrifugal acetylcholinesterase-positive fibres in the olfactory bulb of the rat: evidence for original projections in atypical glomeruli. Neuroscience23,1083-1093.","DOI":"10.1016\/0306-4522(87)90183-7"}],"container-title":["Development"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/journals.biologists.com\/dev\/article-pdf\/134\/22\/4063\/1528285\/4063.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"http:\/\/journals.biologists.com\/dev\/article-pdf\/134\/22\/4063\/1528285\/4063.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,2,18]],"date-time":"2024-02-18T14:34:59Z","timestamp":1708266899000},"score":1,"resource":{"primary":{"URL":"https:\/\/journals.biologists.com\/dev\/article\/134\/22\/4063\/64624\/Axonal-wiring-of-guanylate-cyclase-D-expressing"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2007,11,15]]},"references-count":56,"journal-issue":{"issue":"22","published-print":{"date-parts":[[2007,11,15]]}},"URL":"https:\/\/doi.org\/10.1242\/dev.008722","relation":{},"ISSN":["1477-9129","0950-1991"],"issn-type":[{"value":"1477-9129","type":"electronic"},{"value":"0950-1991","type":"print"}],"subject":[],"published":{"date-parts":[[2007,11,15]]}}}