{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,25]],"date-time":"2026-09-25T23:29:34Z","timestamp":1790378974177,"version":"4.1.0"},"reference-count":77,"publisher":"Oxford University Press (OUP)","issue":"5","license":[{"start":{"date-parts":[[2020,4,25]],"date-time":"2020-04-25T00:00:00Z","timestamp":1587772800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/journals\/pages\/open_access\/funder_policies\/chorus\/standard_publication_model"}],"funder":[{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["RO1DC016222"],"award-info":[{"award-number":["RO1DC016222"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["U19NS112953"],"award-info":[{"award-number":["U19NS112953"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Simons Collaboration on the Global Brain"},{"DOI":"10.13039\/100000065","name":"National Institute of Neurological Disorders and Stroke","doi-asserted-by":"publisher","award":["NS072030"],"award-info":[{"award-number":["NS072030"]}],"id":[{"id":"10.13039\/100000065","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2020,5,29]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Both canonical olfactory sensory neurons (OSNs) and sensory neurons belonging to the guanylate cyclase D (GCD) \u201cnecklace\u201d subsystem are housed in the main olfactory epithelium, which is continuously bombarded by toxins, pathogens, and debris from the outside world. Canonical OSNs address this challenge, in part, by undergoing renewal through neurogenesis; however, it is not clear whether GCD OSNs also continuously regenerate and, if so, whether newborn GCD precursors follow a similar developmental trajectory to that taken by canonical OSNs. Here, we demonstrate that GCD OSNs are born throughout adulthood and can persist in the epithelium for several months. Phosphodiesterase 2A is upregulated early in the differentiation process, followed by the sequential downregulation of \u03b2-tubulin and the upregulation of CART protein. The GCD and MS4A receptors that confer sensory responses upon GCD neurons are initially expressed midway through this process but become most highly expressed once CART levels are maximal late in GCD OSN development. GCD OSN maturation is accompanied by a horizontal migration of neurons toward the central, curved portions of the cul-de-sac regions where necklace cells are concentrated. These findings demonstrate that\u2014like their canonical counterparts\u2014GCD OSNs undergo continuous renewal and define a GCD-specific developmental trajectory linking neurogenesis, maturation, and migration.<\/jats:p>","DOI":"10.1093\/chemse\/bjaa027","type":"journal-article","created":{"date-parts":[[2020,4,22]],"date-time":"2020-04-22T19:10:45Z","timestamp":1587582645000},"page":"333-346","source":"Crossref","is-referenced-by-count":8,"title":["Renewal and Differentiation of GCD Necklace Olfactory Sensory Neurons"],"prefix":"10.1093","volume":"45","author":[{"given":"Maria Lissitsyna","family":"Bloom","sequence":"first","affiliation":[{"name":"Department of Neurobiology, Harvard Medical School, Boston, MA, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lucille B","family":"Johnston","sequence":"first","affiliation":[{"name":"Department of Neurobiology, Harvard Medical School, Boston, MA, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8068-3862","authenticated-orcid":false,"given":"Sandeep Robert","family":"Datta","sequence":"first","affiliation":[{"name":"Department of Neurobiology, Harvard Medical School, Boston, MA, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2020,4,25]]},"reference":[{"issue":"11","key":"2020062701340334300_CIT0001","doi-asserted-by":"crossref","first-page":"1683","DOI":"10.1289\/EHP136","article-title":"Effects of ambient air pollution exposure on olfaction: a review","volume":"124","author":"Ajmani","year":"2016","journal-title":"Environ Health Perspect"},{"issue":"5","key":"2020062701340334300_CIT0002","doi-asserted-by":"crossref","first-page":"391","DOI":"10.1093\/chemse\/bjt015","article-title":"The receptor guanylyl cyclase type D (GC-D) ligand uroguanylin promotes the acquisition of food preferences in mice","volume":"38","author":"Arakawa","year":"2013","journal-title":"Chem Senses"},{"issue":"4","key":"2020062701340334300_CIT0003","doi-asserted-by":"crossref","first-page":"154","DOI":"10.1038\/scientificamerican1095-154","article-title":"The molecular logic of smell","volume":"273","author":"Axel","year":"1995","journal-title":"Sci Am"},{"issue":"2","key":"2020062701340334300_CIT0004","doi-asserted-by":"crossref","first-page":"246","DOI":"10.1002\/cne.902850207","article-title":"Biochemical and immunocytochemical characterization of olfactory marker protein in the rodent central nervous system","volume":"285","author":"Baker","year":"1989","journal-title":"J Comp Neurol"},{"issue":"4","key":"2020062701340334300_CIT0005","doi-asserted-by":"crossref","first-page":"495","DOI":"10.1002\/mrd.20265","article-title":"Mammalian sperm phosphodiesterases and their involvement in receptor-mediated cell signaling important for capacitation","volume":"71","author":"Baxendale","year":"2005","journal-title":"Mol Reprod Dev"},{"key":"2020062701340334300_CIT0006","doi-asserted-by":"crossref","first-page":"182","DOI":"10.3389\/fnins.2014.00182","article-title":"A lifetime of neurogenesis in the olfactory system","volume":"8","author":"Brann","year":"2014","journal-title":"Front Neurosci"},{"issue":"1","key":"2020062701340334300_CIT0007","doi-asserted-by":"crossref","first-page":"90","DOI":"10.1513\/pats.201006-038RN","article-title":"Microbiology of sinusitis","volume":"8","author":"Brook","year":"2011","journal-title":"Proc Am Thorac Soc"},{"issue":"4","key":"2020062701340334300_CIT0008","doi-asserted-by":"crossref","first-page":"457","DOI":"10.1002\/cne.11031","article-title":"Multipotency of purified, transplanted globose basal cells in olfactory epithelium","volume":"469","author":"Chen","year":"2004","journal-title":"J Comp Neurol"},{"issue":"5","key":"2020062701340334300_CIT0009","doi-asserted-by":"crossref","first-page":"814","DOI":"10.1523\/JNEUROSCI.3594-17.2018","article-title":"Spatial determination of neuronal diversification in the olfactory epithelium","volume":"39","author":"Coleman","year":"2019","journal-title":"J Neurosci"},{"issue":"2","key":"2020062701340334300_CIT0010","doi-asserted-by":"crossref","first-page":"303","DOI":"10.1016\/S0012-1606(02)00095-7","article-title":"The roles of Pax6 in the cornea, retina, and olfactory epithelium of the developing mouse embryo","volume":"255","author":"Collinson","year":"2003","journal-title":"Dev Biol"},{"issue":"3","key":"2020062701340334300_CIT0011","doi-asserted-by":"crossref","first-page":"204","DOI":"10.1002\/jemt.10150","article-title":"Apoptosis in the mature and developing olfactory neuroepithelium","volume":"58","author":"Cowan","year":"2002","journal-title":"Microsc Res Tech"},{"key":"2020062701340334300_CIT0012","doi-asserted-by":"crossref","first-page":"961","DOI":"10.1002\/dneu.20838","article-title":"Neurogenesis in subclasses of vomeronasal sensory neurons in adult mice","volume":"70","author":"de la Rosa-Prieto","year":"2010","journal-title":"Dev Neurobiol"},{"issue":"3","key":"2020062701340334300_CIT0013","doi-asserted-by":"crossref","first-page":"443","DOI":"10.1083\/jcb.201008163","article-title":"The cell biology of smell","volume":"191","author":"DeMaria","year":"2010","journal-title":"J Cell Biol"},{"issue":"2","key":"2020062701340334300_CIT0014","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1016\/S0304-3940(00)00935-6","article-title":"Cocaine- and amphetamine-regulated transcript-immunoreactivity in the rat sympatho-adrenal axis","volume":"283","author":"Dun","year":"2000","journal-title":"Neurosci Lett"},{"issue":"6","key":"2020062701340334300_CIT0015","doi-asserted-by":"crossref","first-page":"817","DOI":"10.1016\/j.stem.2017.04.003","article-title":"Deconstructing olfactory stem cell trajectories at single-cell resolution","volume":"20","author":"Fletcher","year":"2017","journal-title":"Cell Stem Cell"},{"issue":"8","key":"2020062701340334300_CIT0016","doi-asserted-by":"crossref","first-page":"3571","DOI":"10.1073\/pnas.92.8.3571","article-title":"A receptor guanylyl cyclase expressed specifically in olfactory sensory neurons","volume":"92","author":"F\u00fclle","year":"1995","journal-title":"Proc Natl Acad Sci USA"},{"issue":"10","key":"2020062701340334300_CIT0017","doi-asserted-by":"crossref","first-page":"2649","DOI":"10.1111\/j.1460-9568.2005.04468.x","article-title":"The Grueneberg ganglion of the mouse projects axons to glomeruli in the olfactory bulb","volume":"22","author":"Fuss","year":"2005","journal-title":"Eur J Neurosci"},{"issue":"3","key":"2020062701340334300_CIT0018","doi-asserted-by":"crossref","first-page":"881","DOI":"10.1016\/j.neuroscience.2010.08.006","article-title":"Integration of CO2 and odorant signals in the mouse olfactory bulb","volume":"170","author":"Gao","year":"2010","journal-title":"Neuroscience"},{"issue":"1","key":"2020062701340334300_CIT0019","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/BF01206454","article-title":"Neurogenesis and neuron regeneration in the olfactory system of mammals. I. Morphological aspects of differentiation and structural organization of the olfactory sensory neurons","volume":"8","author":"Graziadei","year":"1979","journal-title":"J Neurocytol"},{"issue":"7","key":"2020062701340334300_CIT0020","doi-asserted-by":"crossref","first-page":"1734","DOI":"10.1016\/j.cell.2016.05.001","article-title":"A family of non-GPCR chemosensors defines an alternative logic for mammalian olfaction","volume":"165","author":"Greer","year":"2016","journal-title":"Cell"},{"issue":"Pt 1","key":"2020062701340334300_CIT0021","first-page":"83","article-title":"Comparative morphometry of the nasal cavity in rats and mice","volume":"135","author":"Gross","year":"1982","journal-title":"J Anat"},{"issue":"21","key":"2020062701340334300_CIT0022","doi-asserted-by":"crossref","first-page":"4395","DOI":"10.1002\/cne.22463","article-title":"Expression of pax6 and sox2 in adult olfactory epithelium","volume":"518","author":"Guo","year":"2010","journal-title":"J Comp Neurol"},{"issue":"3","key":"2020062701340334300_CIT0023","doi-asserted-by":"crossref","first-page":"245","DOI":"10.1016\/S0301-0082(03)00103-5","article-title":"Structure and function of the vomeronasal system: an update","volume":"70","author":"Halpern","year":"2003","journal-title":"Prog Neurobiol"},{"key":"2020062701340334300_CIT0024","doi-asserted-by":"crossref","first-page":"115","DOI":"10.1186\/1471-2202-9-115","article-title":"Is TrpM5 a reliable marker for chemosensory cells? Multiple types of microvillous cells in the main olfactory epithelium of mice","volume":"9","author":"Hansen","year":"2008","journal-title":"BMC Neurosci"},{"issue":"2","key":"2020062701340334300_CIT0025","doi-asserted-by":"crossref","first-page":"375","DOI":"10.1002\/ar.1092100213","article-title":"An autoradiographic study of the mouse olfactory epithelium: evidence for long-lived receptors","volume":"210","author":"Hinds","year":"1984","journal-title":"Anat Rec"},{"issue":"5840","key":"2020062701340334300_CIT0026","doi-asserted-by":"crossref","first-page":"953","DOI":"10.1126\/science.1144233","article-title":"Detection of near-atmospheric concentrations of CO2 by an olfactory subsystem in the mouse","volume":"317","author":"Hu","year":"2007","journal-title":"Science"},{"key":"2020062701340334300_CIT0027","doi-asserted-by":"crossref","DOI":"10.1101\/346502","article-title":"Unique molecular markers for GC-D-expressing olfactory sensory neurons and chemosensory neurons of the Grueneberg ganglion","author":"Huang","year":"2018"},{"key":"2020062701340334300_CIT0028","doi-asserted-by":"crossref","first-page":"475","DOI":"10.3389\/fimmu.2016.00475","article-title":"Environmental toxicants-induced immune responses in the olfactory mucosa","volume":"7","author":"Imamura","year":"2016","journal-title":"Front Immunol"},{"key":"2020062701340334300_CIT0029","doi-asserted-by":"crossref","DOI":"10.1038\/s41580-020-0214-3","article-title":"The tubulin code and its role in controlling microtubule properties and functions","author":"Janke","year":"2020","journal-title":"Nat Rev Mol Cell Biol"},{"issue":"33","key":"2020062701340334300_CIT0030","doi-asserted-by":"crossref","first-page":"13410","DOI":"10.1073\/pnas.1206724109","article-title":"Neurons expressing trace amine-associated receptors project to discrete glomeruli and constitute an olfactory subsystem","volume":"109","author":"Johnson","year":"2012","journal-title":"Proc Natl Acad Sci USA"},{"issue":"7","key":"2020062701340334300_CIT0031","doi-asserted-by":"crossref","first-page":"3388","DOI":"10.1073\/pnas.94.7.3388","article-title":"A subset of olfactory neurons that selectively express cGMP-stimulated phosphodiesterase (PDE2) and guanylyl cyclase-D define a unique olfactory signal transduction pathway","volume":"94","author":"Juilfs","year":"1997","journal-title":"Proc Natl Acad Sci USA"},{"issue":"11","key":"2020062701340334300_CIT0032","doi-asserted-by":"crossref","first-page":"1962","DOI":"10.1002\/cne.22316","article-title":"Age-related changes in cell dynamics of the postnatal mouse olfactory neuroepithelium: cell proliferation, neuronal differentiation, and cell death","volume":"518","author":"Kondo","year":"2010","journal-title":"J Comp Neurol"},{"issue":"3","key":"2020062701340334300_CIT0033","doi-asserted-by":"crossref","first-page":"489","DOI":"10.1007\/s00441-008-0739-9","article-title":"Distribution and severity of spontaneous lesions in the neuroepithelium and Bowman\u2019s glands in mouse olfactory mucosa: age-related progression","volume":"335","author":"Kondo","year":"2009","journal-title":"Cell Tissue Res"},{"issue":"4","key":"2020062701340334300_CIT0034","doi-asserted-by":"crossref","first-page":"1282","DOI":"10.1016\/j.stemcr.2018.02.010","article-title":"Retinal ganglion cell diversity and subtype specification from human pluripotent stem cells","volume":"10","author":"Langer","year":"2018","journal-title":"Stem Cell Rep"},{"issue":"2","key":"2020062701340334300_CIT0035","doi-asserted-by":"crossref","first-page":"209","DOI":"10.1016\/0165-3806(94)00139-1","article-title":"Age and differentiation-related differences in neuron-specific tubulin immunostaining of olfactory sensory neurons","volume":"83","author":"Lee","year":"1994","journal-title":"Brain Res Dev Brain Res"},{"issue":"36","key":"2020062701340334300_CIT0036","doi-asserted-by":"crossref","first-page":"14507","DOI":"10.1073\/pnas.0704965104","article-title":"Contribution of the receptor guanylyl cyclase GC-D to chemosensory function in the olfactory epithelium","volume":"104","author":"Leinders-Zufall","year":"2007","journal-title":"Proc Natl Acad Sci USA"},{"key":"2020062701340334300_CIT0037","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.conb.2015.01.001","article-title":"Trace amine-associated receptors: ligands, neural circuits, and behaviors","volume":"34","author":"Liberles","year":"2015","journal-title":"Curr Opin Neurobiol"},{"issue":"14","key":"2020062701340334300_CIT0038","doi-asserted-by":"crossref","first-page":"3703","DOI":"10.1523\/JNEUROSCI.0188-04.2004","article-title":"Odors detected by mice deficient in cyclic nucleotide-gated channel subunit A2 stimulate the main olfactory system","volume":"24","author":"Lin","year":"2004","journal-title":"J Neurosci"},{"issue":"1","key":"2020062701340334300_CIT0039","doi-asserted-by":"crossref","first-page":"36","DOI":"10.1002\/cne.22096","article-title":"Grueneberg ganglion olfactory subsystem employs a cGMP signaling pathway","volume":"516","author":"Liu","year":"2009","journal-title":"J Comp Neurol"},{"issue":"3","key":"2020062701340334300_CIT0040","doi-asserted-by":"crossref","first-page":"229","DOI":"10.1080\/01677060802340228","article-title":"The necklace olfactory system in mammals","volume":"22","author":"Luo","year":"2008","journal-title":"J Neurogenet"},{"issue":"2","key":"2020062701340334300_CIT0041","doi-asserted-by":"crossref","first-page":"325","DOI":"10.1016\/j.cell.2013.06.039","article-title":"An epigenetic trap stabilizes singular olfactory receptor expression","volume":"154","author":"Lyons","year":"2013","journal-title":"Cell"},{"key":"2020062701340334300_CIT0042","doi-asserted-by":"crossref","first-page":"1133","DOI":"10.1002\/9781118971758.ch52","article-title":"The septal organ, grueneberg ganglion, and terminal nerve","volume-title":"Handbook of olfaction and gestation","author":"Ma","year":"2015"},{"issue":"5","key":"2020062701340334300_CIT0043","doi-asserted-by":"crossref","first-page":"2042","DOI":"10.1111\/j.1471-4159.2008.05548.x","article-title":"Native cone photoreceptor cyclic nucleotide-gated channel is a heterotetrameric complex comprising both CNGA3 and CNGB3: a study using the cone-dominant retina of Nrl-\/- mice","volume":"106","author":"Matveev","year":"2008","journal-title":"J Neurochem"},{"issue":"1","key":"2020062701340334300_CIT0044","doi-asserted-by":"crossref","first-page":"26","DOI":"10.1002\/neu.480270104","article-title":"Dividing neuron precursors express neuron-specific tubulin","volume":"27","author":"Memberg","year":"1995","journal-title":"J Neurobiol"},{"issue":"9","key":"2020062701340334300_CIT0045","doi-asserted-by":"crossref","first-page":"5399","DOI":"10.1523\/JNEUROSCI.14-09-05399.1994","article-title":"Expression of neuron-specific tubulin defines a novel population in the proliferative layers of the developing telencephalon","volume":"14","author":"Menezes","year":"1994","journal-title":"J Neurosci"},{"issue":"19","key":"2020062701340334300_CIT0046","doi-asserted-by":"crossref","first-page":"10595","DOI":"10.1073\/pnas.97.19.10595","article-title":"A cGMP-signaling pathway in a subset of olfactory sensory neurons","volume":"97","author":"Meyer","year":"2000","journal-title":"Proc Natl Acad Sci USA"},{"issue":"1","key":"2020062701340334300_CIT0047","doi-asserted-by":"crossref","first-page":"245","DOI":"10.1016\/0006-8993(82)90846-0","article-title":"Experimental studies on the olfactory marker protein. II. Appearance of the olfactory marker protein during differentiation of the olfactory sensory neurons of mouse: an immunohistochemical and autoradiographic study","volume":"239","author":"Miragall","year":"1982","journal-title":"Brain Res"},{"issue":"9","key":"2020062701340334300_CIT0048","doi-asserted-by":"crossref","first-page":"667","DOI":"10.1093\/chemse\/bjy061","article-title":"Signal detection and coding in the accessory olfactory system","volume":"43","author":"Mohrhardt","year":"2018","journal-title":"Chem Senses"},{"issue":"7246","key":"2020062701340334300_CIT0049","doi-asserted-by":"crossref","first-page":"521","DOI":"10.1038\/459521a","article-title":"Olfaction: noses within noses","volume":"459","author":"Munger","year":"2009","journal-title":"Nature"},{"issue":"16","key":"2020062701340334300_CIT0050","doi-asserted-by":"crossref","first-page":"1438","DOI":"10.1016\/j.cub.2010.06.021","article-title":"An olfactory subsystem that detects carbon disulfide and mediates food-related social learning","volume":"20","author":"Munger","year":"2010","journal-title":"Curr Biol"},{"issue":"14","key":"2020062701340334300_CIT0051","doi-asserted-by":"crossref","first-page":"2713","DOI":"10.1002\/cne.24051","article-title":"Expression of homeobox genes in the mouse olfactory epithelium","volume":"524","author":"Parrilla","year":"2016","journal-title":"J Comp Neurol"},{"issue":"3","key":"2020062701340334300_CIT0052","doi-asserted-by":"crossref","first-page":"415","DOI":"10.1002\/(SICI)1096-9861(19971124)388:3<415::AID-CNE5>3.0.CO;2-3","article-title":"Immunohistochemical identification of discrete subsets of rat olfactory neurons and the glomeruli that they innervate","volume":"388","author":"Ring","year":"1997","journal-title":"J Comp Neurol"},{"issue":"18","key":"2020062701340334300_CIT0053","doi-asserted-by":"crossref","first-page":"5821","DOI":"10.1073\/pnas.1417955112","article-title":"Odorant receptors regulate the final glomerular coalescence of olfactory sensory neuron axons","volume":"112","author":"Rodriguez-Gil","year":"2015","journal-title":"Proc Natl Acad Sci USA"},{"issue":"11","key":"2020062701340334300_CIT0054","doi-asserted-by":"crossref","first-page":"2887","DOI":"10.1111\/j.1460-9568.2006.04818.x","article-title":"Projection of the Gr\u00fcneberg ganglion to the mouse olfactory bulb","volume":"23","author":"Roppolo","year":"2006","journal-title":"Eur J Neurosci"},{"issue":"1","key":"2020062701340334300_CIT0055","doi-asserted-by":"crossref","first-page":"191","DOI":"10.1016\/S0306-4522(97)00344-8","article-title":"Expression of neuron-specific beta-III tubulin during olfactory neurogenesis in the embryonic and adult rat","volume":"83","author":"Roskams","year":"1998","journal-title":"Neuroscience"},{"issue":"1","key":"2020062701340334300_CIT0056","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1007\/s10863-018-9774-8","article-title":"Low survival rate of young adult-born olfactory sensory neurons in the undamaged mouse olfactory epithelium","volume":"51","author":"Savya","year":"2019","journal-title":"J Bioenerg Biomembr"},{"issue":"7","key":"2020062701340334300_CIT0057","doi-asserted-by":"crossref","first-page":"676","DOI":"10.1038\/nmeth.2019","article-title":"Fiji: an open-source platform for biological-image analysis","volume":"9","author":"Schindelin","year":"2012","journal-title":"Nat Methods"},{"issue":"4","key":"2020062701340334300_CIT0058","doi-asserted-by":"crossref","first-page":"1034","DOI":"10.1002\/cne.24105","article-title":"Stem and progenitor cells of the mammalian olfactory epithelium: taking poietic license","volume":"525","author":"Schwob","year":"2017","journal-title":"J Comp Neurol"},{"issue":"6","key":"2020062701340334300_CIT0059","doi-asserted-by":"crossref","first-page":"1159","DOI":"10.1016\/j.otc.2004.06.007","article-title":"Postviral olfactory loss","volume":"37","author":"Seiden","year":"2004","journal-title":"Otolaryngol Clin North Am"},{"issue":"3","key":"2020062701340334300_CIT0060","doi-asserted-by":"crossref","first-page":"362","DOI":"10.1002\/cne.902840304","article-title":"\u201cNecklace olfactory glomeruli\u201d form unique components of the rat primary olfactory system","volume":"284","author":"Shinoda","year":"1989","journal-title":"J Comp Neurol"},{"key":"2020062701340334300_CIT0061","doi-asserted-by":"crossref","first-page":"e13722","DOI":"10.7554\/eLife.13722","article-title":"The cell proliferation antigen Ki-67 organises heterochromatin","volume":"5","author":"Sobecki","year":"2016","journal-title":"Elife"},{"issue":"11","key":"2020062701340334300_CIT0062","doi-asserted-by":"crossref","first-page":"8306","DOI":"10.1007\/s12035-018-0987-y","article-title":"Transcriptional and epigenetic control of mammalian olfactory epithelium development","volume":"55","author":"Sokpor","year":"2018","journal-title":"Mol Neurobiol"},{"key":"2020062701340334300_CIT0063","doi-asserted-by":"crossref","first-page":"108","DOI":"10.1016\/j.peptides.2014.01.004","article-title":"CART in the brain of vertebrates: circuits, functions and evolution","volume":"54","author":"Subhedar","year":"2014","journal-title":"Peptides"},{"issue":"4","key":"2020062701340334300_CIT0064","doi-asserted-by":"crossref","first-page":"779","DOI":"10.1016\/0896-6273(95)90170-1","article-title":"Target-independent pattern specification in the olfactory epithelium","volume":"15","author":"Sullivan","year":"1995","journal-title":"Neuron"},{"issue":"11","key":"2020062701340334300_CIT0065","doi-asserted-by":"crossref","first-page":"2154","DOI":"10.1002\/cne.22611","article-title":"Age-related changes of the regeneration mode in the mouse peripheral olfactory system following olfactotoxic drug methimazole-induced damage","volume":"519","author":"Suzukawa","year":"2011","journal-title":"J Comp Neurol"},{"issue":"1","key":"2020062701340334300_CIT0066","doi-asserted-by":"crossref","first-page":"107","DOI":"10.1016\/0165-3806(93)90052-C","article-title":"Basal cells in the mouse olfactory epithelium during development: immunohistochemical and electron-microscopic studies","volume":"73","author":"Suzuki","year":"1993","journal-title":"Brain Res Dev Brain Res"},{"key":"2020062701340334300_CIT0067","doi-asserted-by":"crossref","first-page":"363","DOI":"10.1146\/annurev-neuro-071013-013941","article-title":"Coding and transformations in the olfactory system","volume":"37","author":"Uchida","year":"2014","journal-title":"Annu Rev Neurosci"},{"issue":"8","key":"2020062701340334300_CIT0068","doi-asserted-by":"crossref","first-page":"1383","DOI":"10.1097\/00005537-200408000-00012","article-title":"Pathology of the olfactory epithelium: smoking and ethanol exposure","volume":"114","author":"Vent","year":"2004","journal-title":"Laryngoscope"},{"issue":"2","key":"2020062701340334300_CIT0069","doi-asserted-by":"crossref","first-page":"683","DOI":"10.1523\/JNEUROSCI.09-02-00683.1989","article-title":"The expression of the growth associated protein B50\/GAP43 in the olfactory system of neonatal and adult rats","volume":"9","author":"Verhaagen","year":"1989","journal-title":"J Neurosci"},{"issue":"22","key":"2020062701340334300_CIT0070","doi-asserted-by":"crossref","first-page":"4063","DOI":"10.1242\/dev.008722","article-title":"Axonal wiring of guanylate cyclase-D-expressing olfactory neurons is dependent on neuropilin 2 and semaphorin 3F","volume":"134","author":"Walz","year":"2007","journal-title":"Development"},{"issue":"1","key":"2020062701340334300_CIT0071","doi-asserted-by":"crossref","first-page":"22","DOI":"10.1016\/j.jmoldx.2011.08.002","article-title":"RNAscope: a novel in situ RNA analysis platform for formalin-fixed, paraffin-embedded tissues","volume":"14","author":"Wang","year":"2012","journal-title":"J Mol Diagn"},{"issue":"3\u20135","key":"2020062701340334300_CIT0072","doi-asserted-by":"crossref","first-page":"217","DOI":"10.1007\/s11068-005-8355-z","article-title":"Olfactory epithelia differentially express neuronal markers","volume":"34","author":"Weiler","year":"2005","journal-title":"J Neurocytol"},{"issue":"10","key":"2020062701340334300_CIT0073","doi-asserted-by":"crossref","first-page":"3610","DOI":"10.1523\/JNEUROSCI.17-10-03610.1997","article-title":"Proliferation in the rat olfactory epithelium: age-dependent changes","volume":"17","author":"Weiler","year":"1997","journal-title":"J Neurosci"},{"key":"2020062701340334300_CIT0074","doi-asserted-by":"crossref","first-page":"230","DOI":"10.1111\/j.1749-6632.1998.tb10572.x","article-title":"Proliferation decrease in the olfactory epithelium during postnatal development","volume":"855","author":"Weiler","year":"1998","journal-title":"Ann NY Acad Sci"},{"issue":"4","key":"2020062701340334300_CIT0075","doi-asserted-by":"crossref","first-page":"315","DOI":"10.1002\/(SICI)1098-1136(199804)22:4<315::AID-GLIA1>3.0.CO;2-2","article-title":"Supporting cell proliferation in the olfactory epithelium decreases postnatally","volume":"22","author":"Weiler","year":"1998","journal-title":"Glia"},{"issue":"7","key":"2020062701340334300_CIT0076","doi-asserted-by":"crossref","first-page":"581","DOI":"10.1093\/chemse\/bjg047","article-title":"The septal organ of the rat during postnatal development","volume":"28","author":"Weiler","year":"2003","journal-title":"Chem Senses"},{"issue":"5","key":"2020062701340334300_CIT0077","doi-asserted-by":"crossref","first-page":"564","DOI":"10.1016\/j.devcel.2018.07.010","article-title":"FGF20-expressing, wnt-responsive olfactory epithelial progenitors regulate underlying turbinate growth to optimize surface area","volume":"46","author":"Yang","year":"2018","journal-title":"Dev Cell"}],"container-title":["Chemical Senses"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/academic.oup.com\/chemse\/advance-article-pdf\/doi\/10.1093\/chemse\/bjaa027\/33302842\/bjaa027.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"http:\/\/academic.oup.com\/chemse\/article-pdf\/45\/5\/333\/33435431\/bjaa027.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"http:\/\/academic.oup.com\/chemse\/article-pdf\/45\/5\/333\/33435431\/bjaa027.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,8,4]],"date-time":"2024-08-04T13:16:24Z","timestamp":1722777384000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/chemse\/article\/45\/5\/333\/5825298"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,4,25]]},"references-count":77,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2020,4,25]]},"published-print":{"date-parts":[[2020,5,29]]}},"URL":"https:\/\/doi.org\/10.1093\/chemse\/bjaa027","relation":{},"ISSN":["0379-864X","1464-3553"],"issn-type":[{"value":"0379-864X","type":"print"},{"value":"1464-3553","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2020,6]]},"published":{"date-parts":[[2020,4,25]]}}}