{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,6]],"date-time":"2026-10-06T12:23:24Z","timestamp":1791289404356,"version":"4.3.0"},"reference-count":48,"publisher":"The Company of Biologists","issue":"11","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2001,6,1]]},"abstract":"<jats:p>The cerebral cortex is composed of a large variety of different neuron types. All cortical neurons, except some interneurons, are born in two proliferative zones, the cortical ventricular (VZ) and subventricular (SVZ) zones. The relative contribution of both proliferative zones to the generation of the diversity of the cortical neurons is not well understood. To further dissect the underlying mechanism, molecular markers specific for the SVZ are required. Towards this end we performed a subtraction of cDNA libraries, generated from E15.5 and E18.5 mouse cerebral cortex. A novel cDNA, Svet1, was cloned which was specifically expressed in the proliferating cells of the SVZ but not the VZ. The VZ is marked by the expression of the Otx1 gene. Later in development, Svet1 and Otx1 were expressed in subsets of cells of upper (II-IV) and deep (V-VI) layers, respectively. In the reeler cortex, where the layers are inverted, Svet1 and Otx1 label precursors of the upper and deeper layers, respectively, in their new location. Interestingly, in the Pax6\/small eye mutant, Svet1 activity was abolished in the SVZ and in the upper part of the cortical plate while the Otx1 expression domain remained unchanged. Therefore, using Svet1 and Otx1 as cell-type-specific molecular markers for the upper and deep cortical layers we conclude that the Sey mutation affects predominantly the differentiation of the SVZ cells that fail to migrate into the cortical plate. The abnormality of the SVZ coincides with the absence of upper layer cells in the cortex. Taken together our data suggest that while the specification of deep cortical layers occurs in the ventricular zone, the SVZ is important for the proper specification of upper layers.<\/jats:p>","DOI":"10.1242\/dev.128.11.1983","type":"journal-article","created":{"date-parts":[[2021,4,26]],"date-time":"2021-04-26T05:51:07Z","timestamp":1619416267000},"page":"1983-1993","source":"Crossref","is-referenced-by-count":274,"title":["Cortical upper layer neurons derive from the subventricular zone as indicated by<i>Svet1<\/i>gene expression"],"prefix":"10.1242","volume":"128","author":[{"given":"Victor","family":"Tarabykin","sequence":"first","affiliation":[{"name":"Department of Molecular Cell Biology, Max-Planck Institute for Biophysical Chemistry, 37077 Go\u0308ttingen, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anastassia","family":"Stoykova","sequence":"additional","affiliation":[{"name":"Department of Molecular Cell Biology, Max-Planck Institute for Biophysical Chemistry, 37077 Go\u0308ttingen, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Natalia","family":"Usman","sequence":"additional","affiliation":[{"name":"Department of Molecular Cell Biology, Max-Planck Institute for Biophysical Chemistry, 37077 Go\u0308ttingen, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Peter","family":"Gruss","sequence":"additional","affiliation":[{"name":"Department of Molecular Cell Biology, Max-Planck Institute for Biophysical Chemistry, 37077 Go\u0308ttingen, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"237","reference":[{"key":"2021042604571880000_ACAMPORA-ETAL-1996","doi-asserted-by":"crossref","unstructured":"Acampora, D., Mazan, S., Avantaggiato, V., Barone, P., Tuorto, F., Lallemand, Y., Brulet, P. and Simeone, A. (1996). Epilepsy and brain abnormalities in mice lacking the Otx1 gene. Nat. Genet.14, 218-222.","DOI":"10.1038\/ng1096-218"},{"key":"2021042604571880000_ANDERSON-ETAL-1997","doi-asserted-by":"crossref","unstructured":"Anderson, S. A., Qiu, M., Bulfone, A., Eisenstat, D. D., Meneses, J., Pedersen, R. and Rubenstein, J. L. (1997). Mutations of the homeobox genes Dlx-1 and Dlx-2 disrupt the striatal subventricular zone and differentiation of late born striatal neurons. Neuron19,27-37.","DOI":"10.1016\/S0896-6273(00)80345-1"},{"key":"2021042604571880000_ANGEVINE-AND-SIDMAN-1961","doi-asserted-by":"crossref","unstructured":"Angevine J. B. and Sidman R. L. (1961). Autoradiographic study of cell migration during histogenesis og crebral cortex in the mouse. Nature192, 766-768","DOI":"10.1038\/192766b0"},{"key":"2021042604571880000_BAYER-AND-ALTMAN-1991","unstructured":"Bayer, S. A. and Altman, J. (1991). Neocortical Development. New York, Raven Press."},{"key":"2021042604571880000_BETARBET-ETAL-1996","doi-asserted-by":"crossref","unstructured":"Betarbet, R., Zigova, T., Bakay, R. A. and Luskin, M. B. (1996). Dopaminergic and GABAergic interneurons of the olfactory bulb are derived from the neonatal subventricular zone. Int. J. Dev. Neurosci.14,921-930.","DOI":"10.1016\/S0736-5748(96)00066-4"},{"key":"2021042604571880000_BISHOP-ETAL-2000","doi-asserted-by":"crossref","unstructured":"Bishop, K. M., Goudreau, G. and O\u2019Leary, D. D. (2000). Regulation of area identity in the mammalian neocortex by Emx2 and Pax6. Science288, 344-349.","DOI":"10.1126\/science.288.5464.344"},{"key":"2021042604571880000_BRUNJES-ETAL-1998","doi-asserted-by":"crossref","unstructured":"Brunjes, P. C., Fisher, M. and Grainger, R. (1998). The small-eye mutation results in abnormalities in the lateral cortical migratory stream. Brain Res. Dev. Brain Res.110, 121-125.","DOI":"10.1016\/S0165-3806(98)00089-3"},{"key":"2021042604571880000_THE-BOULDER-COMMITTEE-1970","unstructured":"The Boulder Committee (1970). Embryonic vertebrate central nervous system: revised terminology. Anat Rec166, 257-61."},{"key":"2021042604571880000_BROCKDORFF-ETAL-1992","doi-asserted-by":"crossref","unstructured":"Brockdorff, N., Ashworth, A., Kay, G. F., McCabe, V. M., Norris, D. P., Cooper, P. J., Swift, S. and Rastan, S. ( 1992). The product of the mouse Xist gene is a 15 kb inactive X-specific transcript containing no conserved ORF and located in the nucleus. Cell71, 515-526.","DOI":"10.1016\/0092-8674(92)90519-I"},{"key":"2021042604571880000_BROWN-ETAL-1992","doi-asserted-by":"crossref","unstructured":"Brown, C. J., Hendrich, B. D., Rupert, J. L., Lafreniere, R. G., Xing, Y., Lawrence, J. and Willard. H. F. ( 1992). The human XIST gene: analysis of a 17 kb inactive X-specific RNA that contains conserved repeats and is highly localized within the nucleus. Cell71, 527-542.","DOI":"10.1016\/0092-8674(92)90520-M"},{"key":"2021042604571880000_CARIC-ETAL-1997","doi-asserted-by":"crossref","unstructured":"Caric, D., Gooday, D., Hill, R. E., McConnell, S. K. and Price, D. J. (1997). Determination of the migratory capacity of embryonic cortical cells lacking the transcription factor Pax-6. Development124,5087-5096.","DOI":"10.1242\/dev.124.24.5087"},{"key":"2021042604571880000_DARCANGELO-ETAL-1996","doi-asserted-by":"crossref","unstructured":"D\u2019Arcangelo, G., Miao, G. G., and Curran, T. (1996). Detection of the reelin breakpoint in reeler mice. Brain Res. Mol. Brain Res.39,234-6.","DOI":"10.1016\/0169-328X(96)00046-0"},{"key":"2021042604571880000_FRANTZ-AND-MCCONNELL-1996","doi-asserted-by":"crossref","unstructured":"Frantz, G. D. and McConnell, S. K. (1996). Restriction of late cerebral cortical progenitors to an upper-layer fate. Neuron17, 55-61.","DOI":"10.1016\/S0896-6273(00)80280-9"},{"key":"2021042604571880000_FRANTZ-ETAL-1994","doi-asserted-by":"crossref","unstructured":"Frantz, G. D., Weimann, J. M., Levin, M. E., and McConnell, S. K. (1994). Otx1 and Otx2 define layers and regions in developing cerebral cortex and cerebellum. J. Neurosci.14,5725-5740.","DOI":"10.1523\/JNEUROSCI.14-10-05725.1994"},{"key":"2021042604571880000_GOETZ-ETAL-1998","unstructured":"Goetz, M., A. Stoykova, and P. Gruss. 1998. Pax6 controls radial glia differentiation in the cerebral cortex. Neuron21, 1031-1044."},{"key":"2021042604571880000_GURSKAYA-ETAL-1996","doi-asserted-by":"crossref","unstructured":"Gurskaya, N. G., Diatchenko, L., Chenchik, A., Siebert, P. D., Khaspekov, G. L., Lukyanov, K. A., Vagner, L. L., Ermolaeva, O. D., Lukyanov, S. A. and Sverdlov, E. D. (1996). Equalizing cDNA subtraction based on selective suppression of polymerase chain reaction: cloning of Jurkat cell transcripts induced by phytohemaglutinin and phorbol 12-myristate 13-acetate. Anal. Biochem.240,90-97.","DOI":"10.1006\/abio.1996.0334"},{"key":"2021042604571880000_HAYDAR-ETAL-2000","doi-asserted-by":"crossref","unstructured":"Haydar, T. F., Wang, F., Schwartz, M. L. and Rakic, P. (2000) Differential modulation of proliferation in the neocortical ventricular and subventricular zone. J. Neurosci.20, 5764-5774","DOI":"10.1523\/JNEUROSCI.20-15-05764.2000"},{"key":"2021042604571880000_HILL-ETAL-1991","unstructured":"Hill, R. E., Favor, J., Hogan, B. L., Ton, C. C., Saunders, G. F., Hanson, I. M., Prosser, J., Jordan, T., Hastie, N. D. and van Heyningen. V. ( 1991). Mouse small eye results from mutations in a paired-like homeobox-containing gene [published erratum appears in Nature 1992 Feb 20;355(6362):750]. Nature354, 522-525."},{"key":"2021042604571880000_HOGAN-ETAL-1988","doi-asserted-by":"crossref","unstructured":"Hogan, B L., Hirst, E.M. Horsburgh, G. and Hetherington, C.M. ( 1988). Small eye (Sey): a mouse model for the genetic analysis of craniofacial abnormalities. Development103, 115-119.","DOI":"10.1242\/dev.103.Supplement.115"},{"key":"2021042604571880000_LOIS-ETAL-1993","doi-asserted-by":"crossref","unstructured":"Lois, C. and Alvarez-Buylla, A. (1993). Proliferating subventricular zone cells in the adult mammalian forebrain can differentiate into neurons and glia. Proc. Natl. Acad. Sci. USA90,2074-2077.","DOI":"10.1073\/pnas.90.5.2074"},{"key":"2021042604571880000_LUKIANOV-ETAL-1994","unstructured":"Luk\u2019ianov, S. A., Gurskaia, N. G., Luk\u2019ianov, K. A., Tarabykin, V. S., and Sverdlov, E. D. (1994). Highly-effective subtractive hybridization of cDNA (letter). Bioorg. Khim.20,701-704."},{"key":"2021042604571880000_MARIN-PADILLA-1978","unstructured":"Marin-Padilla, M. (1978) Dual origin of the mammalian neocortex and evolution of the cortical plate. Anat. Embryol. (Berl) 152, 109-126."},{"key":"2021042604571880000_MCCONNELL-AND-KAZNOWSKI-1991","doi-asserted-by":"crossref","unstructured":"McConnell, S. K. and Kaznowski, C. E. (1991). Cell cycle dependence of laminar determination in developing neocortex. Science254, 282-285.","DOI":"10.1126\/science.1925583"},{"key":"2021042604571880000_OSUMI-ETAL-1997","doi-asserted-by":"crossref","unstructured":"Osumi, N., Hirota, A. Ohuchi, H. Nakafuku, M. Iimura, T. Kuratani, S. Fujiwara, M. Noji, S. and Eto, K. ( 1997). Pax-6 is involved in the specification of hindbrain motor neuron subtype. Development124, 2961-2972.","DOI":"10.1242\/dev.124.15.2961"},{"key":"2021042604571880000_PELLEGRINI-ETAL-1996","doi-asserted-by":"crossref","unstructured":"Pellegrini, M., Mansouri, A., Simeone, A., Boncinelli, E. and Gruss, P. (1996). Dentate gyrus formation requires Emx2. Development122,3893-3898.","DOI":"10.1242\/dev.122.12.3893"},{"key":"2021042604571880000_PRIVAT-1975","doi-asserted-by":"crossref","unstructured":"Privat, A. (1975). Postnatal gliogenesis in the mammalian brain. Int. Rev. Cytol.40,281-323.","DOI":"10.1016\/S0074-7696(08)60955-9"},{"key":"2021042604571880000_RAKIC-1972","doi-asserted-by":"crossref","unstructured":"Rakic, P. (1972). Mode of cell migration to the superficial layers of fetal monkey neocortex. J. Comp. Neurol.145,61-83.","DOI":"10.1002\/cne.901450105"},{"key":"2021042604571880000_RAKIC-1988","doi-asserted-by":"crossref","unstructured":"Rakic, P. (1988). Specification of cerebral cortical areas. Science241, 170-176.","DOI":"10.1126\/science.3291116"},{"key":"2021042604571880000_RAKIC-AND-CAVINESS-1995","doi-asserted-by":"crossref","unstructured":"Rakic, P. and Caviness, V. S., Jr. (1995). Cortical development: view from neurological mutants two decades later. Neuron14,1101-1104.","DOI":"10.1016\/0896-6273(95)90258-9"},{"key":"2021042604571880000_SAUER-AND-WALKER-1959","doi-asserted-by":"crossref","unstructured":"Sauer, M. E. and Walker, B, E, (1959). Radioautographic study of interkinetic nuclear migration in the neural tube. Proc. Sci. Exp. Biol.101, 557-560.","DOI":"10.3181\/00379727-101-25014"},{"key":"2021042604571880000_SCHAEREN-WIEMERS-ETAL-1993","doi-asserted-by":"crossref","unstructured":"Schaeren-Wiemers, N. and Gerfin-Moser, A. (1993). A single protocol to detect transcripts of various types and expression levels in neural tissue and cultured cells: in situ hybridization using digoxigenin-labelled cRNA probes. Histochemistry100, 431-440.","DOI":"10.1007\/BF00267823"},{"key":"2021042604571880000_SCHMAHL-ETAL-1993","doi-asserted-by":"crossref","unstructured":"Schmahl, W., Knoedlseder, M., Favor, J. and Davidson, D. (1993). Defects of neuronal migration and the pathogenesis of cortical malformations are associated with Small eye (Sey) in the mouse, a point mutation at the Pax-6-locus. Acta Neuropathol.86, 126-135.","DOI":"10.1007\/BF00334879"},{"key":"2021042604571880000_SIMEONE-ETAL-1993","doi-asserted-by":"crossref","unstructured":"Simeone, A., Acampora, D., Mallamaci, A., Stornaiuolo, A., D\u2019Apice, M. R., Nigro, V., and Boncinelli, E. (1993). A vertebrate gene related to orthodenticle contains a homeodomain of the bicoid class and demarcates anterior neuroectoderm in the gastrulating mouse embryo. EMBO J.12, 2735-2747.","DOI":"10.1002\/j.1460-2075.1993.tb05935.x"},{"key":"2021042604571880000_SMART-AND-MCSHERRY-1982","unstructured":"Smart, I. H. and McSherry, G. M. (1982). Growth patterns in the lateral wall of the mouse telencephalon. II. Histological changes during and subsequent to the period of isocortical neuron production. J. Anat.134,415-442."},{"key":"2021042604571880000_SMART-AND-SMART-1982","unstructured":"Smart, I. H. and Smart, M. (1982). Growth patterns in the lateral wall of the mouse telencephalon: I. Autoradiographic studies of the histogenesis of the isocortex and adjacent areas. J. Anat.134,273-298."},{"key":"2021042604571880000_STOYKOVA-ETAL-1996","doi-asserted-by":"crossref","unstructured":"Stoykova, A., Fritsch, R., Walther, C. and Gruss, P. (1996). Forebrain patterning defects in small eye mutant mice. Development122, 3453-3465.","DOI":"10.1242\/dev.122.11.3453"},{"key":"2021042604571880000_STOYKOVA-AND-GRUSS-1994","doi-asserted-by":"crossref","unstructured":"Stoykova, A. and Gruss, P. (1994). Roles of Pax-genes in developing and adult brain as suggested by expression patterns. J. Neurosci.14, 1395-1412.","DOI":"10.1523\/JNEUROSCI.14-03-01395.1994"},{"key":"2021042604571880000_STOYKOVA-ETAL-1997","doi-asserted-by":"crossref","unstructured":"Stoykova, A., Gotz, M., Gruss, P. and Price, J. ( 1997). Pax6-dependent regulation of adhesive patterning, R-cadherin expression and boundary formation in developing forebrain. Development124, 3765-3777.","DOI":"10.1242\/dev.124.19.3765"},{"key":"2021042604571880000_STOYKOVA-ETAL-2000","doi-asserted-by":"crossref","unstructured":"Stoykova, A., Treichel, D., Hallonet, M. and Gruss. P. ( 2000). Pax6 modulates the dorsoventral patterning of the mammalian telencephalon. J. Neurosci. 20, 8042-8050.","DOI":"10.1523\/JNEUROSCI.20-21-08042.2000"},{"key":"2021042604571880000_TAKAHASHI-ETAL-1994","doi-asserted-by":"crossref","unstructured":"Takahashi, T., Nowakowski, R. S., and Caviness, V. S., Jr. (1994). Mode of cell proliferation in the developing mouse neocortex. Proc. Natl. Acad. Sci. USA91,375-379.","DOI":"10.1073\/pnas.91.1.375"},{"key":"2021042604571880000_TAKAHASHI-ETAL-1995","doi-asserted-by":"crossref","unstructured":"Takahashi, T., Nowakowski, R. S., and Caviness, V. S., Jr. (1995). The cell cycle of the pseudostratified ventricular epithelium of the embryonic murine cerebral wall. J. Neurosci.15,6046-6057.","DOI":"10.1523\/JNEUROSCI.15-09-06046.1995"},{"key":"2021042604571880000_TARABYKIN-ETAL-1995","doi-asserted-by":"crossref","unstructured":"Tarabykin, V. S., Lukyanov, K. A., Potapov, V. K. and Lukyanov, S. A. (1995). Detection of planarian Antennapedia-like homeobox genes expressed during regeneration. Gene158,197-202.","DOI":"10.1016\/0378-1119(95)00006-R"},{"key":"2021042604571880000_TORESSON-ETAL-2000","doi-asserted-by":"crossref","unstructured":"Toresson, H., Potter, S. S. and Campbell, K. ( 2000). Genetic control of dorsal-ventral identity in the telencephalon: opposing roles for Pax6 and Gsh2. Development127, 4361-4371.","DOI":"10.1242\/dev.127.20.4361"},{"key":"2021042604571880000_WARREN-AND-PRICE-1997","doi-asserted-by":"crossref","unstructured":"Warren, N. and Price. D. J. ( 1997). Roles of Pax-6 in murine diencephalic development. Development124, 1573-1582.","DOI":"10.1242\/dev.124.8.1573"},{"key":"2021042604571880000_WARREN-ETAL-1999","doi-asserted-by":"crossref","unstructured":"Warren, N., Caric, D., Pratt, T., Clausen, J.A., Asavaritikrai, P., Mason, J. O., Hill R. E. and Price, D. J. ( 1999). The transcription factor, Pax6, is required for cell proliferation and differentiation in the developing cerebral cortex. Cereb. Cortex9, 627-635.","DOI":"10.1093\/cercor\/9.6.627"},{"key":"2021042604571880000_WEIMANN-ETAL-1999","doi-asserted-by":"crossref","unstructured":"Weimann, J. M., Zhang, Y. A., Levin, M. E., Devine, W. P., Brulet, P. and McConnell, S. K. ( 1999). Cortical neurons require Otx1 for the refinement of exuberant axonal projections to subcortical targets. Neuron24, 819-831.","DOI":"10.1016\/S0896-6273(00)81030-2"},{"key":"2021042604571880000_YUN-ETAL-2001","doi-asserted-by":"crossref","unstructured":"Yun, K., Potter, S. and Rubenstein., J. L. ( 2001). Gsh2 and Pax6 play complementary roles in dorsoventral patterning of the mammalian telencephalon. Development128, 193-205.","DOI":"10.1242\/dev.128.2.193"},{"key":"2021042604571880000_ZIGOVA-ETAL-1996","doi-asserted-by":"crossref","unstructured":"Zigova, T., Betarbet, R., Soteres, B. J., Brock, S., Bakay, R. A., and Luskin, M. B. (1996). A comparison of the patterns of migration and the destinations of homotopically transplanted neonatal subventricular zone cells and heterotopically transplanted telencephalic ventricular zone cells. Dev. Biol.173, 459-474.","DOI":"10.1006\/dbio.1996.0040"}],"container-title":["Development"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/journals.biologists.com\/dev\/article-pdf\/128\/11\/1983\/1136763\/1983.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"http:\/\/journals.biologists.com\/dev\/article-pdf\/128\/11\/1983\/1136763\/1983.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,12,25]],"date-time":"2022-12-25T12:02:45Z","timestamp":1671969765000},"score":1,"resource":{"primary":{"URL":"https:\/\/journals.biologists.com\/dev\/article\/128\/11\/1983\/41294\/Cortical-upper-layer-neurons-derive-from-the"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2001,6,1]]},"references-count":48,"journal-issue":{"issue":"11","published-print":{"date-parts":[[2001,6,1]]}},"URL":"https:\/\/doi.org\/10.1242\/dev.128.11.1983","relation":{},"ISSN":["1477-9129","0950-1991"],"issn-type":[{"value":"1477-9129","type":"electronic"},{"value":"0950-1991","type":"print"}],"subject":[],"published":{"date-parts":[[2001,6,1]]}}}