Patterns of neural stem and progenitor cell division may underlie evolutionary cortical expansion (original) (raw)

• Lindblad-Toh, K. Genome sequencing: three's company. Nature 428, 475–476 (2004).
  Article CAS PubMed Google Scholar
• Ji, Q. et al. The earliest known eutherian mammal. Nature 416, 816–822 (2002).
  Article CAS PubMed Google Scholar
• Lois, C. & Alvarez-Buylla, A. Proliferating subventricular zone cells in the adult mammalian forebrain can differentiate into neurons and glia. Proc. Natl Acad. Sci. USA 90, 2074–2077 (1993).
  Article CAS PubMed PubMed Central Google Scholar
• Gadisseux, J. F. & Evrard, P. Glial–neuronal relationship in the developing central nervous system. A histochemical–electron microscope study of radial glial cell particulate glycogen in normal and reeler mice and the human fetus. Dev. Neurosci. 7, 12–32 (1985).
  Article CAS PubMed Google Scholar
• Bruckner, G. & Biesold, D. Histochemistry of glycogen deposition in perinatal rat brain: importance of radial glial cells. J. Neurocytol. 10, 749–757 (1981).
  Article CAS PubMed Google Scholar
• Choi, B. H. & Lapham, L. W. Radial glia in the human fetal cerebrum: a combined Golgi, immunofluorescent and electron microscopic study. Brain Res. 148, 295–311 (1978).
  Article CAS PubMed Google Scholar
• Kriegstein, A. R. & Gotz, M. Radial glia diversity: a matter of cell fate. Glia 43, 37–43 (2003).
  Article PubMed Google Scholar
• Noctor, S. C., Flint, A. C., Weissman, T. A., Dammerman, R. S. & Kriegstein, A. R. Neurons derived from radial glial cells establish radial units in neocortex. Nature 409, 714–720 (2001).
  Article CAS PubMed Google Scholar
• Misson, J. P., Edwards, M. A., Yamamoto, M. & Caviness, V. S. Jr. Mitotic cycling of radial glial cells of the fetal murine cerebral wall: a combined autoradiographic and immunohistochemical study. Brain Res. 466, 183–190 (1988).
  Article CAS PubMed Google Scholar
• Levitt, P., Cooper, M. L. & Rakic, P. Coexistence of neuronal and glial precursor cells in the cerebral ventricular zone of the fetal monkey: an ultrastructural immunoperoxidase analysis. J. Neurosci. 1, 27–39 (1981).
  Article CAS PubMed PubMed Central Google Scholar
• Schmechel, D. E. & Rakic, P. Arrested proliferation of radial glial cells during midgestation in rhesus monkey. Nature 277, 303–305 (1979).
  Article CAS PubMed Google Scholar
• Rakic, P. Neuronal migration and contact guidance in the primate telencephalon. Postgrad. Med. J. 1, 25–40 (1978).
  Google Scholar
• Miyata, T., Kawaguchi, A., Okano, H. & Ogawa, M. Asymmetric inheritance of radial glial fibers by cortical neurons. Neuron 31, 727–741 (2001).
  Article CAS PubMed Google Scholar
• Malatesta, P., Hartfuss, E. & Gotz, M. Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neuronal lineage. Development 127, 5253–5263 (2000).
  CAS PubMed Google Scholar
• Anthony, T. E. et al. Radial glia serve as neuronal progenitors in all regions of the central nervous system. Neuron 41, 881–890 (2004).
  Article CAS PubMed Google Scholar
• Tamamaki, N. et al. Radial glia is a progenitor of neocortical neurons in the developing cerebral cortex. Neurosci. Res. 41, 51–60 (2001).
  Article CAS PubMed Google Scholar
• Noctor, S. C., Martinez-Cerdeno, V., Ivic, L. & Kriegstein, A. R. Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nature Neurosci. 7, 136–144 (2004).
  Article CAS PubMed Google Scholar
• Kornack, D. R. & Rakic, P. Radial and horizontal deployment of clonally related cells in the primate neocortex: relationship to distinct mitotic lineages. Neuron 15, 311–321 (1995).
  Article CAS PubMed Google Scholar
• Rakic, P. Radial unit hypothesis of neocortical expansion. Novartis Found. Symp. 228, 30–42; discussion 42–52 (2000).
  CAS PubMed Google Scholar
• Chenn, A. & Walsh, C. A. Regulation of cerebral cortical size by control of cell cycle exit in neural precursors. Science 297, 365–369 (2002).
  Article CAS PubMed Google Scholar
• Ponting, C. & Jackson, A. P. Evolution of primary microcephaly genes and the enlargement of primate brains. Curr. Opin. Genet. Dev. 15, 241–248 (2005).
  Article CAS PubMed Google Scholar
• Gilbert, S. L., Dobyns, W. B. & Lahn, B. T. Genetic links between brain development and brain evolution. Nature Rev. Genet. 6, 581–590 (2005).
  Article CAS PubMed Google Scholar
• Woods, C. G., Bond, J. & Enard, W. Autosomal recessive primary microcephaly (MCPH): a review of clinical, molecular, and evolutionary findings. Am. J. Hum. Genet. 76, 717–728 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Bond, J. et al. ASPM is a major determinant of cerebral cortical size. Nature Genet. 32, 316–320 (2002).
  Article CAS PubMed Google Scholar
• Evans, P. D. et al. Adaptive evolution of ASPM, a major determinant of cerebral cortical size in humans. Hum. Mol. Genet. 13, 489–494 (2004).
  Article CAS PubMed Google Scholar
• Evans, P. D. et al. Microcephalin, a gene regulating brain size, continues to evolve adaptively in humans. Science 309, 1717–1720 (2005).
  Article CAS PubMed Google Scholar
• Kouprina, N. et al. Accelerated evolution of the ASPM gene controlling brain size begins prior to human brain expansion. PLoS Biol. 2, E126 (2004).
  Article PubMed PubMed Central Google Scholar
• Zhang, J. Evolution of the human ASPM gene, a major determinant of brain size. Genetics 165, 2063–2070 (2003).
  CAS PubMed PubMed Central Google Scholar
• Mekel-Bobrov, N. et al. Ongoing adaptive evolution of ASPM, a brain size determinant in Homo sapiens. Science 309, 1720–1722 (2005).
  Article CAS PubMed Google Scholar
• Ripoll, P., Pimpinelli, S., Valdivia, M. M. & Avila, J. A cell division mutant of Drosophila with a functionally abnormal spindle. Cell 41, 907–912 (1985).
  Article CAS PubMed Google Scholar
• do Carmo Avides, M. & Glover, D. M. Abnormal spindle protein, Asp, and the integrity of mitotic centrosomal microtubule organizing centers. Science 283, 1733–1735 (1999).
  Article CAS PubMed Google Scholar
• Wakefield, J. G., Bonaccorsi, S. & Gatti, M. The Drosophila protein asp is involved in microtubule organization during spindle formation and cytokinesis. J. Cell. Biol. 153, 637–648 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Ponting, C. P. A novel domain suggests a ciliary function for ASPM, a brain size determining gene. Bioinformatics 22, 1031–1035 (2006).
  Article CAS PubMed Google Scholar
• Groszer, M. et al. Negative regulation of neural stem/progenitor cell proliferation by the Pten tumor suppressor gene in vivo. Science 294, 2186–2189 (2001).
  Article CAS PubMed Google Scholar
• Groszer, M. et al. PTEN negatively regulates neural stem cell self-renewal by modulating G0–G1 cell cycle entry. Proc. Natl Acad. Sci. USA 103, 111–116 (2006).
  Article CAS PubMed Google Scholar
• Nieuwenhuys, R., ten Donkelaar, H. J. & Nicholson, C. The Central Nervous System of Vertebrates Vol. 3, 2219 (Springer, Berlin, 1998).
  Book Google Scholar
• Striedter, G. F. Principles of Brain Evolution 436 (Sinauer Associates, Sunderland, 2005).
  Google Scholar
• Rakic, P. A small step for the cell, a giant leap for mankind: a hypothesis of neocortical expansion during evolution. Trends Neurosci. 18, 383–388 (1995).
  Article CAS PubMed Google Scholar
• Rakic, P. Developmental and evolutionary adaptations of cortical radial glia. Cereb. Cortex 13, 541–549 (2003).
  Article PubMed Google Scholar
• Roth, K. A. et al. Epistatic and independent functions of caspase-3 and Bcl-XL in developmental programmed cell death. Proc. Natl Acad. Sci. USA 97, 466–471 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Smart, I. H. & McSherry, G. M. 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 (1982).
  CAS PubMed PubMed Central Google Scholar
• Megason, S. G. & McMahon, A. P. A mitogen gradient of dorsal midline Wnts organizes growth in the CNS. Development 129, 2087–2098 (2002).
  CAS PubMed Google Scholar
• Parr, B. A., Shea, M. J., Vassileva, G. & McMahon, A. P. Mouse Wnt genes exhibit discrete domains of expression in the early embryonic CNS and limb buds. Development 119, 247–261 (1993).
  CAS PubMed Google Scholar
• Tarabykin, V., Stoykova, A., Usman, N. & Gruss, P. Cortical upper layer neurons derive from the subventricular zone as indicated by Svet1 gene expression. Development 128, 1983–1993 (2001).
  CAS PubMed Google Scholar
• Zimmer, C., Tiveron, M. C., Bodmer, R. & Cremer, H. Dynamics of Cux2 expression suggests that an early pool of SVZ precursors is fated to become upper cortical layer neurons. Cereb. Cortex 14, 1408–1420 (2004).
  Article PubMed Google Scholar
• Englund, C. et al. Pax6, Tbr2, and Tbr1 are expressed sequentially by radial glia, intermediate progenitor cells, and postmitotic neurons in developing neocortex. J. Neurosci. 25, 247–251 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Anderson, S. A. et al. Mutations of the homeobox genes Dlx-1 and Dlx-2 disrupt the striatal subventricular zone and differentiation of late born striatal neurons. Neuron 19, 27–37 (1997).
  Article CAS PubMed Google Scholar
• Krubitzer, L. & Kahn, D. M. Nature versus nurture revisited: an old idea with a new twist. Prog. Neurobiol. 70, 33–52 (2003).
  Article PubMed Google Scholar
• Britanova, O. et al. A novel mode of tangential migration of cortical projection neurons. Dev. Biol. 30 Jun 2006 (doi:10.1016/j.ydbio.2006.06.040).
• Reid, C. B., Liang, I. & Walsh, C. Systematic widespread clonal organization in cerebral cortex. Neuron 15, 299–310 (1995).
  Article CAS PubMed Google Scholar
• Walsh, C. & Cepko, C. L. Widespread dispersion of neuronal clones across functional regions of the cerebral cortex. Science 255, 434–440 (1992).
  Article CAS PubMed Google Scholar
• Walsh, C. & Cepko, C. L. Clonally related cortical cells show several migration patterns. Science 241, 1342–1345 (1988).
  Article CAS PubMed Google Scholar
• Haubensak, W., Attardo, A., Denk, W. & Huttner, W. B. Neurons arise in the basal neuroepithelium of the early mammalian telencephalon: a major site of neurogenesis. Proc. Natl Acad. Sci. USA 101, 3196–3201 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Iacopetti, P. et al. Expression of the antiproliferative gene TIS21 at the onset of neurogenesis identifies single neuroepithelial cells that switch from proliferative to neuron-generating division. Proc. Natl Acad. Sci. USA 96, 4639–4644 (1999).
  Article CAS PubMed PubMed Central Google Scholar
• Martinez-Cerdeno, V., Noctor, S. C. & Kriegstein, A. R. The role of the intermediate progenitor cells in the evolutionary expansion on the cerebral cortex. Cereb. Cortex 16, 152–161 (2006).
  Article Google Scholar
• Smart, I. H., 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 12, 37–53 (2002).
  Article PubMed Google Scholar
• Zecevic, N., Chen, Y. & Filipovic, R. Contributions of cortical subventricular zone to the development of the human cerebral cortex. J. Comp. Neurol. 491, 109–122 (2005).
  Article PubMed PubMed Central Google Scholar
• Noctor, S. C., Scholnicoff, N. J. & Juliano, S. L. Histogenesis of ferret somatosensory cortex. J. Comp. Neurol. 387, 179–193 (1997).
  Article CAS PubMed Google Scholar
• Kornack, D. R. & Rakic, P. Changes in cell-cycle kinetics during the development and evolution of primate neocortex. Proc. Natl Acad. Sci. USA 95, 1242–1246 (1998).
  Article CAS PubMed PubMed Central Google Scholar
• Takahashi, T., Nowakowski, R. S. and Caviness, V. Jr. The cell cycle of the pseudostratified ventricular epithelium of the embryonic murine cerebral wall. J. Neurosci. 15, 6046–6057 (1995).
  Article CAS PubMed PubMed Central Google Scholar
• DeFelipe, J., Alonso-Nanclares, L. & Arellano, J. I. Microstructure of the neocortex: comparative aspects. J. Neurocytol. 31, 299–316 (2002).
  Article PubMed Google Scholar
• Richman, D. P., Stewart, R. M., Hutchinson, J. W. & Caviness, V. S. Jr. Mechanical model of brain convolutional development. Science 189, 18–21 (1975).
  Article CAS PubMed Google Scholar
• Bayer, S. A. & Altman, J. The Human Brain During the Second Trimester (Taylor & Francis, Boca Raton, 2005).
  Book Google Scholar
• Nery, S., Fishell, G. & Corbin, J. G. The caudal ganglionic eminence is a source of distinct cortical and subcortical cell populations. Nature Neurosci. 5, 1279–1287 (2002).
  Article CAS PubMed Google Scholar
• de Carlos, J. A., Lopez-Mascaraque, L. & Valverde, F. Dynamics of cell migration from the lateral ganglionic eminence in the rat. J. Neurosci. 16, 6146–6156 (1996).
  Article CAS PubMed PubMed Central Google Scholar
• Lavdas, A. A., Grigoriou, M., Pachnis, V. & Parnavelas, J. G. The medial ganglionic eminence gives rise to a population of early neurons in the developing cerebral cortex. J. Neurosci. 19, 7881–7888 (1999).
  Article CAS PubMed PubMed Central Google Scholar
• Anderson, S. A., Marin, O., Horn, C., Jennings, K. & Rubenstein, J. L. Distinct cortical migrations from the medial and lateral ganglionic eminences. Development 128, 353–363 (2001).
  CAS PubMed Google Scholar
• Anderson, S. A., Eisenstat, D. D., Shi, L. & Rubenstein, J. Interneuron migration from basal forebrain to neocortex: dependence on dlx genes. Science 278, 474–476 (1997).
  Article CAS PubMed Google Scholar
• Wichterle, H., Garcia-Verdugo, J. M., Herrera, D. G. & Alvarez-Buylla, A. Young neurons from medial ganglionic eminence disperse in adult and embryonic brain. Nature Neurosci. 2, 461–466 (1999).
  Article CAS PubMed Google Scholar
• Wichterle, H., Turnbull, D. H., Nery, S., Fishell, G. & Alvarez-Buylla, A. In utero fate mapping reveals distinct migratory pathways and fates of neurons born in the mammalian basal forebrain. Development 128, 3759–3771 (2001).
  CAS PubMed Google Scholar
• Sussel, L., Marin, O., Kimura, S. & Rubenstein, J. L. Loss of Nkx2.1 homeobox gene function results in a ventral to dorsal molecular respecification within the basal telencephalon: evidence for a transformation of the pallidum into the striatum. Development 126, 3359–3370 (1999).
  CAS PubMed Google Scholar
• Tamamaki, N., Fujimori, K. E. & Takauji, R. Origin and route of tangentially migrating neurons in the developing neocortical intermediate zone. J. Neurosci. 17, 8313–8323 (1997).
  Article CAS PubMed PubMed Central Google Scholar
• Halliday, A. L. & Cepko, C. L. Generation and migration of cells in the developing striatum. Neuron 9, 15–26 (1992).
  Article CAS PubMed Google Scholar
• Walsh, C. & Cepko, C. L. Clonal dispersion in proliferative layers of developing cerebral cortex. Nature 362, 632–635 (1993).
  Article CAS PubMed Google Scholar
• Reid, C. B. & Walsh, C. A. Evidence of common progenitors and patterns of dispersion in rat striatum and cerebral cortex. J. Neurosci. 22, 4002–4014 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Letinic, K., Zoncu, R. & Rakic, P. Origin of GABAergic neurons in the human neocortex. Nature 417, 645–649 (2002).
  Article CAS PubMed Google Scholar
• Brody, T. & Odenwald, W. F. Programmed transformations in neuroblast gene expression during Drosophila CNS lineage development. Dev. Biol. 226, 34–44 (2000).
  Article CAS PubMed Google Scholar
• Kambadur, R. et al. Regulation of POU genes by castor and hunchback establishes layered compartments in the Drosophila CNS. Genes. Dev. 12, 246–260 (1998).
  Article CAS PubMed PubMed Central Google Scholar
• Isshiki, T., Pearson, B., Holbrook, S. & Doe, C. Q. Drosophila neuroblasts sequentially express transcription factors which specify the temporal identity of their neuronal progeny. Cell 106, 511–521 (2001).
  Article CAS PubMed Google Scholar
• Cui, X. & Doe, C. Q. ming is expressed in neuroblast sublineages and regulates gene expression in the Drosophila central nervous system. Development 116, 943–952 (1992).
  CAS PubMed Google Scholar
• Mellerick, D. M., Kassis, J. A., Zhang, S. D. & Odenwald, W. F. castor encodes a novel zinc finger protein required for the development of a subset of CNS neurons in Drosophila. Neuron 9, 789–803 (1992).
  Article CAS PubMed Google Scholar
• Novotny, T., Eiselt, R. & Urban, J. Hunchback is required for the specification of the early sublineage of neuroblast 7–3 in the Drosophila central nervous system. Development 129, 1027–1036 (2002).
  CAS PubMed Google Scholar
• Zhong, W. Diversifying neural cells through order of birth and asymmetry of division. Neuron 37, 11–14 (2003).
  Article CAS PubMed Google Scholar
• Frantz, G. D., Weimann, J. M., Levin, M. E. & McConnell, S. K. Otx1 and Otx2 define layers and regions in developing cerebral cortex and cerebellum. J. Neurosci. 14, 5725–5740 (1994).
  Article CAS PubMed PubMed Central Google Scholar
• Molyneaux, B. J., Arlotta, P., Hirata, T., Hibi, M. & Macklis, J. D. Fezl is required for the birth and specification of corticospinal motor neurons. Neuron 47, 817–831 (2005).
  Article CAS PubMed Google Scholar
• Nieto, M. et al. Expression of Cux-1 and Cux-2 in the subventricular zone and upper layers II–IV of the cerebral cortex. J. Comp. Neurol. 479, 168–180 (2004).
  Article CAS PubMed Google Scholar
• Hanashima, C., Li, S. C., Shen, L., Lai, E. & Fishell, G. Foxg1 suppresses early cortical cell fate. Science 303, 56–59 (2004).
  Article CAS PubMed Google Scholar
• Shen, Q. et al. The timing of cortical neurogenesis is encoded within lineages of individual progenitor cells. Nature Neurosci. 9, 743–751 (2006).
  Article CAS PubMed Google Scholar
• Lavdas, A. A., Mione, M. C. & Parnavelas, J. G. Neuronal clones in the cerebral cortex show morphological and neurotransmitter heterogeneity during development. Cereb. Cortex 6, 490–497 (1996).
  Article CAS PubMed Google Scholar
• Williams, B. P., Read, J. & Price, J. The generation of neurons and oligodendrocytes from a common precursor cell. Neuron 7, 685–693 (1991).
  Article CAS PubMed Google Scholar
• Luskin, M. B., Parnavelas, J. G. & Barfield, J. A. Neurons, astrocytes, and oligodendrocytes of the rat cerebral cortex originate from separate progenitor cells: an ultrastructural analysis of clonally related cells. J. Neurosci. 13, 1730–1750 (1993).
  Article CAS PubMed PubMed Central Google Scholar
• Walsh, C. & Cepko, C. L. Cell lineage and cell migration in the developing cerebral cortex. Experientia 46, 940–947 (1990).
  Article CAS PubMed Google Scholar
• Temple, S. Division and differentiation of isolated CNS blast cells in microculture. Nature 340, 471–473 (1989).
  Article CAS PubMed Google Scholar
• Bayer, S. A. & Altman, J. Neocortical Development (Raven, New York, 1991).
  Google Scholar