{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,10]],"date-time":"2026-10-10T06:59:18Z","timestamp":1791615558791,"version":"4.3.4"},"reference-count":60,"publisher":"The Company of Biologists","issue":"10","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2007,5,15]]},"abstract":"<jats:p>Despite great insight into the molecular mechanisms that specify neuronal cell type in the spinal cord, cell behaviour underlying neuron production in this tissue is largely unknown. In other neuroepithelia, divisions with a perpendicular cleavage plane at the apical surface generate symmetrical cell fates, whereas a parallel cleavage plane generates asymmetric daughters, a neuron and a progenitor in a stem cell mode, and has been linked to the acquisition of neuron-generating ability. Using a novel long-term imaging assay, we have monitored single cells in chick spinal cord as they transit mitosis and daughter cells become neurons or divide again. We reveal new morphologies accompanying neuron birth and show that neurons are generated concurrently by asymmetric and terminal symmetric divisions. Strikingly,divisions that generate two progenitors or a progenitor and a neuron both exhibit a wide range of cleavage plane orientations and only divisions that produce two neurons have an exclusively perpendicular orientation. Neuron-generating progenitors are also distinguished by lengthening cell cycle times, a finding supported by cell cycle acceleration on exposure to fibroblast growth factor (FGF), an inhibitor of neuronal differentiation. This study provides a novel, dynamic view of spinal cord neurogenesis and supports a model in which cleavage plane orientation\/mitotic spindle position does not assign neuron-generating ability, but functions subsequent to this step to distinguish stem cell and terminal modes of neuron production.<\/jats:p>","DOI":"10.1242\/dev.002519","type":"journal-article","created":{"date-parts":[[2007,4,30]],"date-time":"2007-04-30T19:39:51Z","timestamp":1177961991000},"page":"1943-1954","source":"Crossref","is-referenced-by-count":108,"title":["Mitotic spindle orientation distinguishes stem cell and terminal modes of neuron production in the early spinal cord"],"prefix":"10.1242","volume":"134","author":[{"given":"Arwen C.","family":"Wilcock","sequence":"first","affiliation":[{"name":"Divisions of Cell and Developmental Biology, Wellcome Trust Biocentre, College of Life Sciences, University of Dundee, Dow Street, Dundee DD1 5EH, UK."},{"name":"Divisions of Gene Regulation and Expression, Wellcome Trust Biocentre, College of Life Sciences, University of Dundee, Dow Street, Dundee DD1 5EH, UK."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jason R.","family":"Swedlow","sequence":"additional","affiliation":[{"name":"Divisions of Gene Regulation and Expression, Wellcome Trust Biocentre, College of Life Sciences, University of Dundee, Dow Street, Dundee DD1 5EH, UK."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kate G.","family":"Storey","sequence":"additional","affiliation":[{"name":"Divisions of Cell and Developmental Biology, Wellcome Trust Biocentre, College of Life Sciences, University of Dundee, Dow Street, Dundee DD1 5EH, UK."}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"237","reference":[{"key":"2021042612172599900_REF1","doi-asserted-by":"crossref","unstructured":"Afonso, C. and Henrique, D. (2006). PAR3 acts as a molecular organizer to define the apical domain of chick neuroepithelial cells. J. Cell Sci.119,4293-4304.","DOI":"10.1242\/jcs.03170"},{"key":"2021042612172599900_REF2","doi-asserted-by":"crossref","unstructured":"Bertrand, N., Castro, D. S. and Guillemot, F.(2002). Proneural genes and the specification of neural cell types. Nat. Rev. Neurosci.3, 517-530.","DOI":"10.1038\/nrn874"},{"key":"2021042612172599900_REF3","unstructured":"Betschinger, J. and Knoblich, J. A. (2004). Dare to be different: asymmetric cell division in Drosophila, C. elegans and vertebrates. Curr. Biol.14,R674-R685."},{"key":"2021042612172599900_REF4","doi-asserted-by":"crossref","unstructured":"Cai, L., Hayes, N. L., Takahashi, T., Caviness, V. S., Jr and Nowakowski, R. S. (2002). Size distribution of retrovirally marked lineages matches prediction from population measurements of cell cycle behavior. J. Neurosci. 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Dual control of neurogenesis by PC3 through cell cycle inhibition and induction of Math1. J. Neurosci.24,3355-3369.","DOI":"10.1523\/JNEUROSCI.3860-03.2004"},{"key":"2021042612172599900_REF8","doi-asserted-by":"crossref","unstructured":"Chenn, A. and McConnell, S. K. (1995). Cleavage orientation and the asymmetric inheritance of Notch1 immunoreactivity in mammalian neurogenesis. Cell82,631-641.","DOI":"10.1016\/0092-8674(95)90035-7"},{"key":"2021042612172599900_REF9","doi-asserted-by":"crossref","unstructured":"Das, T., Payer, B., Cayouette, M. and Harris, W. A.(2003). In vivo time-lapse imaging of cell divisions during neurogenesis in the developing zebrafish retina. Neuron37,597-609.","DOI":"10.1016\/S0896-6273(03)00066-7"},{"key":"2021042612172599900_REF10","doi-asserted-by":"crossref","unstructured":"Diez del Corral, R., Breitkreuz, D. N. and Storey, K. G.(2002). Onset of neuronal differentiation is regulated by paraxial mesoderm and requires attenuation of FGF signalling. 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