Skip to main content
Top
Published in: Experimental Brain Research 2/2012

Open Access 01-01-2012 | Mini-Review

Cytoarchitecture of mouse and human subventricular zone in developing cerebral neocortex

Authors: Hidenori Tabata, Satoshi Yoshinaga, Kazunori Nakajima

Published in: Experimental Brain Research | Issue 2/2012

Login to get access

Abstract

During cerebral neocortical development, excitatory neurons are generated from radial glial cells in the ventricular zone (VZ) or from secondary progenitor cells in the subventricular zone (SVZ); these neurons then migrate toward the pial surface. We have observed that post-mitotic neurons generated directly in the VZ accumulated just above the VZ with a multipolar morphology, while secondary progenitor cells having a long ascending process left the VZ faster than the post-mitotic neurons. Recent observations of human developing neocortex have revealed the existence of radial glia-like progenitors (oRG cells) in the SVZ. This type of progenitor was first thought to be human specific; however, similar cells have also been found in mouse neocortex, and the morphology of these cells resembled that of some of the secondary progenitor cells that we had previously observed, suggesting the existence of a common architecture for the developing neocortex among mammals. In this review, we discuss the nature of the SVZ and its similarities and differences between humans and mice.
Literature
go back to reference Arnold SJ, Huang GJ, Cheung AF, Era T, Nishikawa S, Bikoff EK, Molnar Z, Robertson EJ, Groszer M (2008) The T-box transcription factor Eomes/Tbr2 regulates neurogenesis in the cortical subventricular zone. Genes Dev 22:2479–2484PubMedCrossRef Arnold SJ, Huang GJ, Cheung AF, Era T, Nishikawa S, Bikoff EK, Molnar Z, Robertson EJ, Groszer M (2008) The T-box transcription factor Eomes/Tbr2 regulates neurogenesis in the cortical subventricular zone. Genes Dev 22:2479–2484PubMedCrossRef
go back to reference Boulder-Committee (1970) Embryonic vertebrate central nervous system: revised terminology. Anat Rec 166:257–261CrossRef Boulder-Committee (1970) Embryonic vertebrate central nervous system: revised terminology. Anat Rec 166:257–261CrossRef
go back to reference Bultje RS, Castaneda-Castellanos DR, Jan LY, Jan YN, Kriegstein AR, Shi SH (2009) Mammalian Par3 regulates progenitor cell asymmetric division via notch signaling in the developing neocortex. Neuron 63:189–202PubMedCrossRef Bultje RS, Castaneda-Castellanos DR, Jan LY, Jan YN, Kriegstein AR, Shi SH (2009) Mammalian Par3 regulates progenitor cell asymmetric division via notch signaling in the developing neocortex. Neuron 63:189–202PubMedCrossRef
go back to reference Costa MR, Wen G, Lepier A, Schroeder T, Gotz M (2008) Par-complex proteins promote proliferative progenitor divisions in the developing mouse cerebral cortex. Development 135:11–22PubMedCrossRef Costa MR, Wen G, Lepier A, Schroeder T, Gotz M (2008) Par-complex proteins promote proliferative progenitor divisions in the developing mouse cerebral cortex. Development 135:11–22PubMedCrossRef
go back to reference Cubelos B, Sebastian-Serrano A, Kim S, Redondo JM, Walsh C, Nieto M (2008) Cux-1 and Cux-2 control the development of Reelin expressing cortical interneurons. Dev Neurobiol 68:917–925PubMedCrossRef Cubelos B, Sebastian-Serrano A, Kim S, Redondo JM, Walsh C, Nieto M (2008) Cux-1 and Cux-2 control the development of Reelin expressing cortical interneurons. Dev Neurobiol 68:917–925PubMedCrossRef
go back to reference Englund C, Fink A, Lau C, Pham D, Daza RA, Bulfone A, Kowalczyk T, Hevner RF (2005) Pax6, Tbr2, and Tbr1 are expressed sequentially by radial glia, intermediate progenitor cells, and postmitotic neurons in developing neocortex. J Neurosci 25:247–251PubMedCrossRef Englund C, Fink A, Lau C, Pham D, Daza RA, Bulfone A, Kowalczyk T, Hevner RF (2005) Pax6, Tbr2, and Tbr1 are expressed sequentially by radial glia, intermediate progenitor cells, and postmitotic neurons in developing neocortex. J Neurosci 25:247–251PubMedCrossRef
go back to reference Fietz SA, Kelava I, Vogt J, Wilsch-Brauninger M, Stenzel D, Fish JL, Corbeil D, Riehn A, Distler W, Nitsch R, Huttner WB (2010) OSVZ progenitors of human and ferret neocortex are epithelial-like and expand by integrin signaling. Nat Neurosci 13:690–699PubMedCrossRef Fietz SA, Kelava I, Vogt J, Wilsch-Brauninger M, Stenzel D, Fish JL, Corbeil D, Riehn A, Distler W, Nitsch R, Huttner WB (2010) OSVZ progenitors of human and ferret neocortex are epithelial-like and expand by integrin signaling. Nat Neurosci 13:690–699PubMedCrossRef
go back to reference Hansen DV, Lui JH, Parker PR, Kriegstein AR (2010) Neurogenic radial glia in the outer subventricular zone of human neocortex. Nature 464:554–561PubMedCrossRef Hansen DV, Lui JH, Parker PR, Kriegstein AR (2010) Neurogenic radial glia in the outer subventricular zone of human neocortex. Nature 464:554–561PubMedCrossRef
go back to reference Haubensak W, Attardo A, Denk W, Huttner WB (2004) Neurons arise in the basal neuroepithelium of the early mammalian telencephalon: a major site of neurogenesis. Proc Natl Acad Sci USA 101:3196–3201PubMedCrossRef Haubensak W, Attardo A, Denk W, Huttner WB (2004) Neurons arise in the basal neuroepithelium of the early mammalian telencephalon: a major site of neurogenesis. Proc Natl Acad Sci USA 101:3196–3201PubMedCrossRef
go back to reference Kamei Y, Inagaki N, Nishizawa M, Tsutsumi O, Taketani Y, Inagaki M (1998) Visualization of mitotic radial glial lineage cells in the developing rat brain by Cdc2 kinase-phosphorylated vimentin. Glia 23:191–199PubMedCrossRef Kamei Y, Inagaki N, Nishizawa M, Tsutsumi O, Taketani Y, Inagaki M (1998) Visualization of mitotic radial glial lineage cells in the developing rat brain by Cdc2 kinase-phosphorylated vimentin. Glia 23:191–199PubMedCrossRef
go back to reference Konno D, Shioi G, Shitamukai A, Mori A, Kiyonari H, Miyata T, Matsuzaki F (2008) Neuroepithelial progenitors undergo LGN-dependent planar divisions to maintain self-renewability during mammalian neurogenesis. Nat Cell Biol 10:93–101PubMedCrossRef Konno D, Shioi G, Shitamukai A, Mori A, Kiyonari H, Miyata T, Matsuzaki F (2008) Neuroepithelial progenitors undergo LGN-dependent planar divisions to maintain self-renewability during mammalian neurogenesis. Nat Cell Biol 10:93–101PubMedCrossRef
go back to reference Kosodo Y, Roper K, Haubensak W, Marzesco AM, Corbeil D, Huttner WB (2004) Asymmetric distribution of the apical plasma membrane during neurogenic divisions of mammalian neuroepithelial cells. EMBO J 23:2314–2324PubMedCrossRef Kosodo Y, Roper K, Haubensak W, Marzesco AM, Corbeil D, Huttner WB (2004) Asymmetric distribution of the apical plasma membrane during neurogenic divisions of mammalian neuroepithelial cells. EMBO J 23:2314–2324PubMedCrossRef
go back to reference Kowalczyk T, Pontious A, Englund C, Daza RA, Bedogni F, Hodge R, Attardo A, Bell C, Huttner WB, Hevner RF (2009) Intermediate neuronal progenitors (basal progenitors) produce pyramidal-projection neurons for all layers of cerebral cortex. Cereb Cortex 19:2439–2450PubMedCrossRef Kowalczyk T, Pontious A, Englund C, Daza RA, Bedogni F, Hodge R, Attardo A, Bell C, Huttner WB, Hevner RF (2009) Intermediate neuronal progenitors (basal progenitors) produce pyramidal-projection neurons for all layers of cerebral cortex. Cereb Cortex 19:2439–2450PubMedCrossRef
go back to reference Land PW, Monaghan AP (2003) Expression of the transcription factor, tailless, is required for formation of superficial cortical layers. Cereb Cortex 13:921–931PubMedCrossRef Land PW, Monaghan AP (2003) Expression of the transcription factor, tailless, is required for formation of superficial cortical layers. Cereb Cortex 13:921–931PubMedCrossRef
go back to reference Lukaszewicz A, Savatier P, Cortay V, Giroud P, Huissoud C, Berland M, Kennedy H, Dehay C (2005) G1 phase regulation, area-specific cell cycle control, and cytoarchitectonics in the primate cortex. Neuron 47:353–364PubMedCrossRef Lukaszewicz A, Savatier P, Cortay V, Giroud P, Huissoud C, Berland M, Kennedy H, Dehay C (2005) G1 phase regulation, area-specific cell cycle control, and cytoarchitectonics in the primate cortex. Neuron 47:353–364PubMedCrossRef
go back to reference Miyata T, Kawaguchi A, Okano H, Ogawa M (2001) Asymmetric inheritance of radial glial fibers by cortical neurons. Neuron 31:727–741PubMedCrossRef Miyata T, Kawaguchi A, Okano H, Ogawa M (2001) Asymmetric inheritance of radial glial fibers by cortical neurons. Neuron 31:727–741PubMedCrossRef
go back to reference Miyata T, Kawaguchi A, Saito K, Kawano M, Muto T, Ogawa M (2004) Asymmetric production of surface-dividing and non-surface-dividing cortical progenitor cells. Development 131:3133–3145PubMedCrossRef Miyata T, Kawaguchi A, Saito K, Kawano M, Muto T, Ogawa M (2004) Asymmetric production of surface-dividing and non-surface-dividing cortical progenitor cells. Development 131:3133–3145PubMedCrossRef
go back to reference Nadarajah B, Brunstrom JE, Grutzendler J, Wong RO, Pearlman AL (2001) Two modes of radial migration in early development of the cerebral cortex. Nat Neurosci 4:143–150PubMedCrossRef Nadarajah B, Brunstrom JE, Grutzendler J, Wong RO, Pearlman AL (2001) Two modes of radial migration in early development of the cerebral cortex. Nat Neurosci 4:143–150PubMedCrossRef
go back to reference Nieto M, Monuki ES, Tang H, Imitola J, Haubst N, Khoury SJ, Cunningham J, Gotz M, Walsh CA (2004) Expression of Cux-1 and Cux-2 in the subventricular zone and upper layers II-IV of the cerebral cortex. J Comp Neurol 479:168–180PubMedCrossRef Nieto M, Monuki ES, Tang H, Imitola J, Haubst N, Khoury SJ, Cunningham J, Gotz M, Walsh CA (2004) Expression of Cux-1 and Cux-2 in the subventricular zone and upper layers II-IV of the cerebral cortex. J Comp Neurol 479:168–180PubMedCrossRef
go back to reference Noctor SC, Flint AC, Weissman TA, Dammerman RS, Kriegstein AR (2001) Neurons derived from radial glial cells establish radial units in neocortex. Nature 409:714–720PubMedCrossRef Noctor SC, Flint AC, Weissman TA, Dammerman RS, Kriegstein AR (2001) Neurons derived from radial glial cells establish radial units in neocortex. Nature 409:714–720PubMedCrossRef
go back to reference Noctor SC, Martinez-Cerdeno V, Ivic L, Kriegstein AR (2004) Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat Neurosci 7:136–144PubMedCrossRef Noctor SC, Martinez-Cerdeno V, Ivic L, Kriegstein AR (2004) Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat Neurosci 7:136–144PubMedCrossRef
go back to reference Noctor SC, Martinez-Cerdeno V, Kriegstein AR (2008) Distinct behaviors of neural stem and progenitor cells underlie cortical neurogenesis. J Comp Neurol 508:28–44PubMedCrossRef Noctor SC, Martinez-Cerdeno V, Kriegstein AR (2008) Distinct behaviors of neural stem and progenitor cells underlie cortical neurogenesis. J Comp Neurol 508:28–44PubMedCrossRef
go back to reference Rakic P (1972) Mode of cell migration to the superficial layers of fetal monkey neocortex. J Comp Neurol 145:61–83PubMedCrossRef Rakic P (1972) Mode of cell migration to the superficial layers of fetal monkey neocortex. J Comp Neurol 145:61–83PubMedCrossRef
go back to reference Sasaki S, Tabata H, Tachikawa K, Nakajima K (2008) The cortical subventricular zone-specific molecule Svet1 is part of the nuclear RNA coded by the putative Netrin receptor gene Unc5d and is expressed in multipolar migrating cells. Mol Cell Neurosci 38:474–483PubMedCrossRef Sasaki S, Tabata H, Tachikawa K, Nakajima K (2008) The cortical subventricular zone-specific molecule Svet1 is part of the nuclear RNA coded by the putative Netrin receptor gene Unc5d and is expressed in multipolar migrating cells. Mol Cell Neurosci 38:474–483PubMedCrossRef
go back to reference Sessa A, Mao CA, Hadjantonakis AK, Klein WH, Broccoli V (2008) Tbr2 directs conversion of radial glia into basal precursors and guides neuronal amplification by indirect neurogenesis in the developing neocortex. Neuron 60:56–69PubMedCrossRef Sessa A, Mao CA, Hadjantonakis AK, Klein WH, Broccoli V (2008) Tbr2 directs conversion of radial glia into basal precursors and guides neuronal amplification by indirect neurogenesis in the developing neocortex. Neuron 60:56–69PubMedCrossRef
go back to reference Shimojo H, Ohtsuka T, Kageyama R (2008) Oscillations in notch signaling regulate maintenance of neural progenitors. Neuron 58:52–64PubMedCrossRef Shimojo H, Ohtsuka T, Kageyama R (2008) Oscillations in notch signaling regulate maintenance of neural progenitors. Neuron 58:52–64PubMedCrossRef
go back to reference Shitamukai A, Konno D, Matsuzaki F (2011) Oblique radial glial divisions in the developing mouse neocortex induce self-renewing progenitors outside the germinal zone that resemble primate outer subventricular zone progenitors. J Neurosci 31:3683–3695PubMedCrossRef Shitamukai A, Konno D, Matsuzaki F (2011) Oblique radial glial divisions in the developing mouse neocortex induce self-renewing progenitors outside the germinal zone that resemble primate outer subventricular zone progenitors. J Neurosci 31:3683–3695PubMedCrossRef
go back to reference Smart IH, Dehay C, Giroud P, Berland M, Kennedy H (2002) Unique morphological features of the proliferative zones and postmitotic compartments of the neural epithelium giving rise to striate and extrastriate cortex in the monkey. Cereb Cortex 12:37–53PubMedCrossRef Smart IH, Dehay C, Giroud P, Berland M, Kennedy H (2002) Unique morphological features of the proliferative zones and postmitotic compartments of the neural epithelium giving rise to striate and extrastriate cortex in the monkey. Cereb Cortex 12:37–53PubMedCrossRef
go back to reference Sugitani Y, Nakai S, Minowa O, Nishi M, Jishage K, Kawano H, Mori K, Ogawa M, Noda T (2002) Brn-1 and Brn-2 share crucial roles in the production and positioning of mouse neocortical neurons. Genes Dev 16:1760–1765PubMedCrossRef Sugitani Y, Nakai S, Minowa O, Nishi M, Jishage K, Kawano H, Mori K, Ogawa M, Noda T (2002) Brn-1 and Brn-2 share crucial roles in the production and positioning of mouse neocortical neurons. Genes Dev 16:1760–1765PubMedCrossRef
go back to reference Tabata H, Nakajima K (2001) Efficient in utero gene transfer system to the developing mouse brain using electroporation: visualization of neuronal migration in the developing cortex. Neuroscience 103:865–872PubMedCrossRef Tabata H, Nakajima K (2001) Efficient in utero gene transfer system to the developing mouse brain using electroporation: visualization of neuronal migration in the developing cortex. Neuroscience 103:865–872PubMedCrossRef
go back to reference Tabata H, Kanatani S, Nakajima K (2009) Differences of migratory behavior between direct progeny of apical progenitors and basal progenitors in the developing cerebral cortex. Cereb Cortex 19:2092–2105PubMedCrossRef Tabata H, Kanatani S, Nakajima K (2009) Differences of migratory behavior between direct progeny of apical progenitors and basal progenitors in the developing cerebral cortex. Cereb Cortex 19:2092–2105PubMedCrossRef
go back to reference Takahashi T, Nowakowski RS, Caviness VS Jr (1996) The leaving or Q fraction of the murine cerebral proliferative epithelium: a general model of neocortical neuronogenesis. J Neurosci 16:6183–6196PubMed Takahashi T, Nowakowski RS, Caviness VS Jr (1996) The leaving or Q fraction of the murine cerebral proliferative epithelium: a general model of neocortical neuronogenesis. J Neurosci 16:6183–6196PubMed
go back to reference Tarabykin V, Stoykova A, Usman N, Gruss P (2001) Cortical upper layer neurons derive from the subventricular zone as indicated by Svet1 gene expression. Development 128:1983–1993PubMed Tarabykin V, Stoykova A, Usman N, Gruss P (2001) Cortical upper layer neurons derive from the subventricular zone as indicated by Svet1 gene expression. Development 128:1983–1993PubMed
go back to reference Wang X, Tsai JW, Lamonica B, Kriegstein AR (2011) A new subtype of progenitor cell in the mouse embryonic neocortex. Nat Neurosci 14:555–561PubMedCrossRef Wang X, Tsai JW, Lamonica B, Kriegstein AR (2011) A new subtype of progenitor cell in the mouse embryonic neocortex. Nat Neurosci 14:555–561PubMedCrossRef
go back to reference Wu SX, Goebbels S, Nakamura K, Kometani K, Minato N, Kaneko T, Nave KA, Tamamaki N (2005) Pyramidal neurons of upper cortical layers generated by NEX-positive progenitor cells in the subventricular zone. Proc Natl Acad Sci USA 102:17172–17177PubMedCrossRef Wu SX, Goebbels S, Nakamura K, Kometani K, Minato N, Kaneko T, Nave KA, Tamamaki N (2005) Pyramidal neurons of upper cortical layers generated by NEX-positive progenitor cells in the subventricular zone. Proc Natl Acad Sci USA 102:17172–17177PubMedCrossRef
go back to reference Yu F, Kuo CT, Jan YN (2006) Drosophila neuroblast asymmetric cell division: recent advances and implications for stem cell biology. Neuron 51:13–20PubMedCrossRef Yu F, Kuo CT, Jan YN (2006) Drosophila neuroblast asymmetric cell division: recent advances and implications for stem cell biology. Neuron 51:13–20PubMedCrossRef
go back to reference Zappone MV, Galli R, Catena R, Meani N, De Biasi S, Mattei E, Tiveron C, Vescovi AL, Lovell-Badge R, Ottolenghi S, Nicolis SK (2000) Sox2 regulatory sequences direct expression of a (beta)-geo transgene to telencephalic neural stem cells and precursors of the mouse embryo, revealing regionalization of gene expression in CNS stem cells. Development 127:2367–2382PubMed Zappone MV, Galli R, Catena R, Meani N, De Biasi S, Mattei E, Tiveron C, Vescovi AL, Lovell-Badge R, Ottolenghi S, Nicolis SK (2000) Sox2 regulatory sequences direct expression of a (beta)-geo transgene to telencephalic neural stem cells and precursors of the mouse embryo, revealing regionalization of gene expression in CNS stem cells. Development 127:2367–2382PubMed
go back to reference Zimmer C, Tiveron MC, Bodmer R, Cremer H (2004) Dynamics of Cux2 expression suggests that an early pool of SVZ precursors is fated to become upper cortical layer neurons. Cereb Cortex 14:1408–1420PubMedCrossRef Zimmer C, Tiveron MC, Bodmer R, Cremer H (2004) Dynamics of Cux2 expression suggests that an early pool of SVZ precursors is fated to become upper cortical layer neurons. Cereb Cortex 14:1408–1420PubMedCrossRef
Metadata
Title
Cytoarchitecture of mouse and human subventricular zone in developing cerebral neocortex
Authors
Hidenori Tabata
Satoshi Yoshinaga
Kazunori Nakajima
Publication date
01-01-2012
Publisher
Springer-Verlag
Published in
Experimental Brain Research / Issue 2/2012
Print ISSN: 0014-4819
Electronic ISSN: 1432-1106
DOI
https://doi.org/10.1007/s00221-011-2933-3

Other articles of this Issue 2/2012

Experimental Brain Research 2/2012 Go to the issue