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Vol. 30, No. 1-3, 2008
Issue release date: December 2007
Dev Neurosci 2008;30:24–32
(DOI:10.1159/000109848)

Role of Intermediate Progenitor Cells in Cerebral Cortex Development

Pontious A. · Kowalczyk T. · Englund C. · Hevner R.F.
Department of Pathology, University of Washington, Seattle, Wash., USA

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Abstract

Intermediate progenitor cells (IPCs) are a type of neurogenic transient amplifying cells in the developing cerebral cortex. IPCs divide symmetrically at basal (abventricular) positions in the neuroepithelium to produce pairs of new neurons or, in amplifying divisions, pairs of new IPCs. In contrast, radial unit progenitors (neuroepithelial cells and radial glia) divide at the apical (ventricular) surface and produce only single neurons or single IPCs by asymmetric division, or self-amplify by symmetric division. Histologically, IPCs are most prominent during the middle and late stages of neurogenesis, when they accumulate in the subventricular zone, a progenitor compartment linked to the genesis of upper neocortical layers (II–IV). Nevertheless, IPCs are present throughout cortical neurogenesis and produce neurons for all layers. In mice, changes in the abundance of IPCs caused by mutations of Pax6, Ngn2, Id4 and other genes are associated with parallel changes in cortical thickness but not surface area. In gyrencephalic brains, IPCs may play broader roles in determining not only laminar thickness, but also cortical surface area and gyral patterns. We propose that regulation of IPC genesis and amplification across developmental stages and regional subdivisions modulates laminar neurogenesis and contributes to the cytoarchitectonic differentiation of cortical areas.



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References

  1. Haubensak W, Attardo A, Denk W, Huttner WB: Neurons arise in the basal neuroepithelium of the early mammalian telencephalon: a major site of neurogenesis. Proc Natl Acad Sci USA 2004;101:3196–3201.
  2. Miyata T, Kawaguchi A, Saito K, Kawano M, Muto T, Ogawa M: Asymmetric production of surface-dividing and non-surface-dividing cortical progenitor cells. Development 2004;131:3133–3145.
  3. Noctor SC, Martínez-Cerdeño V, Ivic L, Kriegstein AR: Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat Neurosci 2004;7:136–144.
  4. Takahashi T, Nowakowski RS, Caviness VS Jr: Early ontogeny of the secondary proliferative population of the embryonic murine cerebral wall. J Neurosci 1995;15:6058–6068.
  5. Heins N, Malatesta P, Cecconi F, Nakafuku M, Tucker KL, Hack MA, Chapouton P, Barde Y-A, Götz M: Glial cells generate neurons: the role of the transcription factor Pax6. Nat Neurosci 2002;5:308–315.
  6. Götz M, Huttner WB: The cell biology of neurogenesis. Nat Rev Mol Cell Biol 2005;6:777–788.
  7. Huttner WB, Kosodo Y: Symmetric versus asymmetric cell division during neurogenesis in the developing vertebrate nervous system. Curr Opin Cell Biol 2005;17:648–657.
  8. Götz M, Barde Y-A: Radial glial cells: defined and major intermediates between embryonic stem cells and CNS neurons. Neuron 2005;46:369–372.
  9. Gal JS, Morozov YM, Ayoub AE, Chatterjee M, Rakic P, Haydar TF: Molecular and morphological heterogeneity of neural precursors in the mouse neocortical proliferative zones. J Neurosci 2006;26:1045–1056.
  10. Englund C, Fink A, Lau C, Pham D, Daza RAM, Bulfone A, Kowalczyk T, Hevner RF: Pax6, Tbr2, and Tbr1 are expressed sequentially by radial glia, intermediate progenitor cells, and postmitotic neurons in developing neocortex. J Neurosci 2005;25:247–251.
  11. Wu SX, Goebbels S, Nakamura K, Nakamura K, Kometani K, Minato N, Kaneko T, Nave K-A, Tamamaki N: Pyramidal neurons of upper cortical layers generated by NEX-positive progenitor cells in the subventricular zone. Proc Natl Acad Sci USA 2005;102:17172–17177.
  12. Kornack DR, Rakic P: Radial and horizontal deployment of clonally related cells in the primate neocortex: relationship to distinct mitotic lineages. Neuron 1995;15:311–321.
  13. Noctor SC, Flint AC, Weissman TA, Dammerman RS, Kriegstein AR: Neurons derived from radial glial cells establish radial units in neocortex. Nature 2001;409:714–720.
  14. Miyata T, Kawaguchi A, Okano H, Ogawa M: Asymmetric inheritance of radial glial fibers by cortical neurons. Neuron 2001;31:727–741.
  15. Malatesta P, Hack MA, Hartfuss E, Kettenmann H, Klinkert W, Kirchhoff F, Götz M: Neuronal or glial progeny: regional differences in radial glia fate. Neuron 2003;37:751–764.
  16. Anthony TE, Klein C, Fishell G, Heintz N: Radial glia serve as neuronal progenitors in all regions of the central nervous system. Neuron 2004;41:881–890.
  17. Hevner RF: From radial glia to pyramidal-projection neuron: transcription factor cascades in cerebral cortex development. Mol Neurobiol 2006;33:33–50.
  18. Tarabykin V, Stoykova A, Usman N, Gruss P: Cortical upper layer neurons derive from the subventricular zone as indicated by Svet1 gene expression. Development 2001;128:1983–1993.
  19. Zimmer C, Tiveron M-C, Bodmer R, Cremer H: Dynamics of Cux2 expression suggest that an early pool of SVZ precursors is fated to become upper cortical layer neurons. Cereb Cortex 2004;14:1408–1420.
  20. Lukaszewicz A, Savatier P, Cortay V, Giroud P, Huissoud C, Berland M, Kennedy H, Dehay C: G1 phase regulation, area-specific cell cycle control, and cytoarchitectonics in the primate cortex. Neuron 2005;47:353–364.
  21. Lukaszewicz A, Cortay V, Giroud P, Berland M, Smart I, Kennedy H, Dehay C: The concerted modulation of proliferation and migration contributes to the specification of the cytoarchitecture and dimensions of cortical areas. Cereb Cortex 2006;16:i26–i34.
  22. Kriegstein A, Noctor S, Martínez-Cerdeño V: Patterns of neural stem and progenitor cell division may underlie evolutionary cortical expansion. Nat Rev Neurosci 2006;7:883–890.
  23. Rakic P: Specification of cerebral cortical areas. Science 1988;241:170–176.
  24. Shen Q, Wang Y, Dimos JT, Fasano CA, Phoenix TN, Lemischka IR, Ivanova NB, Stifani S, Morrisey EE, Temple S: The timing of cortical neurogenesis is encoded within lineages of individual progenitor cells. Nat Neurosci 2006;9:743–751.
  25. Martínez-Cerdeño V, Noctor SC, Kriegstein AR: The role of intermediate progenitor cells in the evolutionary expansion of the cerebral cortex. Cereb Cortex 2006;16:i152–i161.
  26. Molnár Z, Métin C, Stoykova A, Tarabykin V, Price DJ, Francis F, Meyer G, Dehay C, Kennedy H: Comparative aspects of cerebral cortical development. Eur J Neurosci 2006;23:921–934.
  27. Nieto M, Monuki ES, Tang H, Imitola J, Haubst N, Khoury SJ, Cunningham J, Gotz M, Walsh CA: Expression of Cux-1 and Cux-2 in the subventricular zone and upper layers II–IV of the cerebral cortex. J Comp Neurol 2004;479:168–180.
  28. Britanova O, Akopov S, Lukyanov S, Gruss P, Tarabykin V: Novel transcription factor Satb2 interacts with matrix attachment region DNA elements in a tissue-specific manner and demonstrates cell-type-dependent expression in the developing mouse CNS. Eur J Neurosci 2005;21:658–668.
  29. Takahashi T, Goto T, Miyama S, Nowakowski RS, Caviness VS Jr: Sequence of neuron origin and neocortical laminar fate: relation to cell cycle of origin in the developing murine cerebral wall. J Neurosci 1999;19:10357–10371.
  30. Schuurmans C, Armant O, Nieto M, Stenman JM, Britz O, Klenin N, Brown C, Langevin L-M, Seibt J, Tang H, Cunningham JM, Dyck R, Walsh C, Campbell K, Polleux F, Guillemot F: Sequential phases of cortical specification involve neurogenin-dependent and -independent pathways. EMBO J 2004;23:2892–2902.
  31. Quinn JC, Molinek M, Martynoga BS, Zaki PA, Faedo A, Bulfone A, Hevner RF, West JD, Price DJ: Pax6 controls cerebral cortical cell number by regulating exit from the cell cycle and specifies cortical cell identity by a cell autonomous mechanism. Dev Biol 2007;302:50–65.
  32. Holm PC, Mader MT, Haubst N, Wizenmann A, Sigvardsson M, Götz M: Loss- and gain-of-function analyses reveal targets of Pax6 in the developing mouse telencephalon. Mol Cell Neurosci 2007;34:99–119.
  33. Viti J, Gulacsi A, Lillien L: Wnt regulation of progenitor maturation in the cortex depends on Shh or fibroblast growth factor 2. J Neurosci 2003;23:5919–5927.
  34. Molyneaux BJ, Arlotta P, Hirata T, Hibi M, Macklis JD: Fezl is required for the birth and specification of corticospinal motor neurons. Neuron 2005;47:817–831.
  35. Chen B, Schaevitz LR, McConnell SK: Fezl regulates the differentiation and axon targeting of layer 5 subcortical projection neurons in cerebral cortex. Proc Natl Acad Sci USA 2005;102:17184–17189.
  36. Chen J-G, Rasin M-R, Kwan KY, Sestan N: Zfp312 is required for subcortical axonal projections and dendritic morphology of deep-layer pyramidal neurons of the cerebral cortex. Proc Natl Acad Sci USA 2005;102:17792–17797.
  37. Smart IHM: Proliferative characteristics of the ependymal layer during the early development of the mouse neocortex: a pilot study based on recording the number, location and plane of cleavage of mitotic figures. J Anat 1973;116:67–91.
  38. Takahashi T, Nowakowski RS, Caviness VS Jr: The cell cycle of the pseudostratified ventricular epithelium of the embryonic murine cerebral wall. J Neurosci 1995;15:6046–6057.
  39. Smart IHM, Dehay C, Giroud P, Berland M, Kennedy H: 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 2002;12:37–53.
  40. Cheung AFP, Pollen AA, Tavare A, DeProto J, Molnár Z: Comparative aspects of cortical neurogenesis in vertebrates. J Anat, in press.
  41. Land PW, Monaghan AP: Expression of the transcription factor, tailless, is required for formation of superficial cortical layers. Cereb Cortex 2003;13:921–931.
  42. Roy K, Kuznicki K, Wu Q, Sun Z, Bock D, Schutz G, Vranich N, Monaghan AP: The Tlx gene regulates the timing of neurogenesis in the cortex. J Neurosci 2004;24:8333–8345.
  43. Yun K, Mantani A, Garel S, Rubenstein J, Israel MA: Id4 regulates neural progenitor proliferation and differentiation in vivo. Development 2004;131:5441–5448.
  44. Bedford L, Walker R, Kondo T, van Crüchten I, King ER, Sablitzky F: Id4 is required for the correct timing of neural differentiation. Dev Biol 2005;280:386–395.
  45. Cappello S, Attardo A, Wu X, Iwasato T, Itohara S, Wilsch-Bräuninger M, Eilken HM, Rieger MA, Schroeder TT, Huttner WB, Brakebusch C, Götz M: The Rho-GTPase cdc42 regulates neural progenitor fate at the apical surface. Nat Neurosci 2006;9:1099–1107.
  46. Chen L, Liao G, Yang L, Campbell K, Nakafuku M, Kuan C-Y, Zheng Y: Cdc42 deficiency causes Sonic hedgehog-independent holoprosencephaly. Proc Natl Acad Sci USA 2006;103:16520–16525.
  47. Zhou C-J, Borello U, Rubenstein JLR, Pleasure SJ: Neuronal production and precursor proliferation defects in the neocortex of mice with loss of function in the canonical Wnt signaling pathway. Neuroscience 2006;142:1119–1131.
  48. Goto T, Mitsuhashi T, Takahashi T: Altered patterns of neuron production in the p27Kip1 knockout mouse. Dev Neurosci 2004;26:208–217.
  49. Glaser T, Jepeal L, Edwards JG, Young SR, Favor J, Maas RL: PAX6 gene dosage effect in a family with congenital cataracts, aniridia, anophthalmia and central nervous system defects. Nat Genet 1994;7:463–471.
  50. Baala L, Briault S, Etchevers HC, Laumonnier F, Natiq A, Amiel J, Boddaert N, Picard C, Sbiti A, Asermouh A, Attié-Bitach T, Encha-Razavi F, Munnich A, Sefiani A, Lyonnet S: Homozygous silencing of T-box transcription factor EOMES leads to microcephaly with polymicrogyria and corpus callosum agenesis. Nat Genet 2007, E-pub ahead of print.
  51. Chenn A, Walsh CA: Regulation of cerebral cortical size by control of cell cycle exit in neural precursors. Science 2002;297:365–369.
  52. Kuida K, Haydar TF, Kuan C-Y, Gu Y, Taya C, Karasuyama H, Su MS-S, Rakic P, Flavell RA: Reduced apoptosis and cytochrome c-mediated caspase activation in mice lacking caspase 9. Cell 1998;94:325–337.
  53. Hevner RF: The cerebral cortex malformation in thanatophoric dysplasia: neuropathology and pathogenesis. Acta Neuropathol 2005;110:208–221.

    External Resources

  54. Inglis-Broadgate SL, Thomson RE, Pellicano F, Tartaglia MA, Pontikis CC, Cooper JD, Iwata T: FGFR3 regulates brain size by controlling progenitor cell proliferation and apoptosis during embryonic development. Dev Biol 2005;279:73–85.
  55. Dehay C, Horsburgh G, Berland M, Killackey H, Kennedy H: Maturation and connectivity of the visual cortex in monkey is altered by prenatal removal of retinal input. Nature 1989;337:265–267.
  56. Dehay C, Giroud P, Berland M, Killackey H, Kennedy H: Contribution of thalamic input to the specification of cytoarchitectonic cortical fields in the primate: effects of bilateral enucleation in the fetal monkey on the boundaries, dimensions, and gyrification of striate and extrastriate cortex. J Comp Neurol 1996;367:70–89.
  57. Dehay C, Giroud P, Berland M, Smart I, Kennedy H: Modulation of the cell cycle contributes to the parcellation of the primate visual cortex. Nature 1993;366:464–466.
  58. Polleux F, Dehay C, Kennedy H: The timetable of laminar neurogenesis contributes to the specification of cortical areas in mouse isocortex. J Comp Neurol 1997;385:95–116.
  59. Polleux F, Dehay C, Kennedy H: Neurogenesis and commitment of corticospinal neurons in reeler. J Neurosci 1998;18:9910–9923.
  60. Zecevic N, Chen Y, Filipovic R: Contributions of cortical subventricular zone to the development of the human cerebral cortex. J Comp Neurol 2005;491:109–122.
  61. Letinic K, Zoncu R, Rakic P: Origin of GABAergic neurons in the human neocortex. Nature 2002;417:645–649.
  62. Van Essen DC: A tension-based theory of morphogenesis and compact wiring in the central nervous system. Nature 1997;385:313–318.
  63. Hilgetag CC, Barbas H: Developmental mechanics of the primate cerebral cortex. Anat Embryol 2005;210:411–417.
  64. Hilgetag CC, Barbas H: Role of mechanical factors in the morphology of the primate cerebral cortex. PLoS Comput Biol 2006;2:146–159.
  65. Rockel AJ, Hiorns RW, Powell TPS: The basic uniformity in structure of the neocortex. Brain 1980;103:221–244.
  66. DeFelipe J, Alonso-Nanclares L, Arellano JI: Microstructure of the neocortex: comparative aspects. J Neurocytol 2002;31:299–316.
  67. O’Leary DDM, Nakagawa Y: Patterning centers, regulatory genes and extrinsic mechanisms controlling arealization of the neocortex. Curr Opin Neurobiol 2002;12:14–25.
  68. Grove EA, Fukuchi-Shimogori T: Generating the cerebral cortical area map. Annu Rev Neurosci 2003;26:355–380.
  69. Muzio L, Soria JM, Pannese M, Piccolo S, Mallamaci A: A mutually stimulating loop involving Emx2 and canonical Wnt signaling specifically promotes expansion of occipital cortex and hippocampus. Cereb Cortex 2005;15:2021–2028.
  70. Lillien L, Gulacsi A: Environmental signals elicit multiple responses in dorsal telencephalic progenitors by threshold-dependent mechanisms. Cereb Cortex 2006;16:i74–i81.
  71. Guillemot F: Cellular and molecular control of neurogenesis in the mammalian telencephalon. Curr Opin Cell Biol 2005;17:639–647.
  72. Dehay C, Savatier P, Cortay V, Kennedy H: Cell-cycle kinetics of neocortical precursors are influenced by embryonic thalamic axons. J Neurosci 2001;21:201–214.


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