The timing of cortical neurogenesis is encoded within lineages of individual progenitor cells

Nature Neuroscience

Volumn 9, Issue 6, 2006, Pages 743-751

  Shen, Qin ^a   Wang, Yue ^a   Dimos, John T ^b   Fasano, Christopher A ^a   Phoenix, Timothy N ^a   Lemischka, Ihor R ^b   Ivanova, Natalia B ^b   Stifani, Stefano ^c   Morrisey, Edward E ^d   Temple, Sally ^a  

^a ALBANY MEDICAL COLLEGE   (United States)

^b PRINCETON UNIVERSITY   (United States)

^c MCGILL UNIVERSITY   (Canada)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SHORT HAIRPIN RNA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FOXG1; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BRAIN CORTEX; CELL LINEAGE; COCULTURE; CONTROLLED STUDY; EMBRYO; ENVIRONMENTAL FACTOR; GESTATION PERIOD; IN VIVO STUDY; MOUSE; NERVE CELL; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NEUROBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEM CELL;

ANIMALS; CELL ADHESION MOLECULES, NEURONAL; CELL DIFFERENTIATION; CELL DIVISION; CELL LINEAGE; CELL MOVEMENT; CELL PROLIFERATION; CELLS, CULTURED; CEREBRAL CORTEX; DOWN-REGULATION; EXTRACELLULAR MATRIX PROTEINS; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MICE; MICROSCOPY, VIDEO; NERVE TISSUE PROTEINS; NEURONAL PLASTICITY; NEURONS; RNA INTERFERENCE; SERINE ENDOPEPTIDASES; STEM CELLS; TIME FACTORS;

EID: 33745726874     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn1694     Document Type: Article

References (46)

1. Bayer, S.A. & Altman, J. Neocortical Development (Raven Press, New York, 1991).
2. Sulston, J.E. & Horvitz, H.R. Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Dev. Biol. 56, 110-156 (1977).
3. Sulston, J.E., Schierenberg, E., White, J.G. & Thomson, J.N. The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev. Biol. 100, 64-119 (1983).
4. Doe, C.Q. & Technau, G.M. Identification and cell lineage of individual neural precursors in the Drosophila CNS. Trends Neurosci. 16, 510-514 (1993).
5. McConnell, S.K. & Kaznowski, C.E. Cell cycle dependence of laminar determination in developing neocortex. Science 254, 282-285 (1991).
6. Frantz, G.D. & McConnell, S.K. Restriction of late cerebral cortical progenitors to an upper-layer fate. Neuron 17, 55-61 (1996).
7. Desai, A.R. & McConnell, S.K. Progressive restriction in fate potential by neural progenitors during cerebral cortical development. Development 127, 2863-2872 (2000).
8. Qian, X. et al. Timing of CNS cell generation: a programmed sequence of neuron and glial cell production from isolated murine cortical stem cells. Neuron 28, 69-80 (2000).
9. Ware, M.L., Tavazoie, S.F., Reid, C.B. & Walsh, C.A. Coexistence of widespread clones and large radial clones in early embryonic ferret cortex. Cereb. Cortex 9, 636-645 (1999).
10. Takiguchi-Hayashi, K. et al. Generation of reelin-positive marginal zone cells from the caudomedial wall of telencephalic vesicles. J. Neurosci. 24, 2286-2295 (2004).
11. 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).
12. Bielle, F. et al. Multiple origins of Cajal-Retzius cells at the borders of the developing pallium. Nat. Neurosci. 8, 1002-1012 (2005).
13. Hanashima, C., Li, S.C., Shen, L., Lai, E. & Fishell, G. Foxg1 suppresses early cortical cell fate. Science 303, 56-59 (2004).
14. 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. Nat. Neurosci. 7, 136-144 (2004).
15. Miyata, T. et al. Asymmetric production of surface-dividing and non-surface-dividing cortical progenitor cells. Development 131, 3133-3145 (2004).
16. 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).
17. Nadarajah, B., Alifragis, P., Wong, R.O. & Parnavelas, J.G. Neuronal migration in the developing cerebral cortex: observations based on real-time imaging. Cereb. Cortex 13, 607-611 (2003).
18. Qian, X., Goderie, S.K., Shen, Q., Stern, J.H. & Temple, S. Intrinsic programs of patterned cell lineages in isolated vertebrate CNS ventricular zone cells. Development 125, 3143-3152 (1998).
19. D'Arcangelo, G. et al. Reelin is a secreted glycoprotein recognized by the CR-50 monoclonal antibody. J. Neurosci. 17, 23-31 (1997).
20. Ferland, R.J., Cherry, T.J., Preware, P.O., Morrisey, E.E. & Walsh, C.A. Characterization of Foxp2 and Foxp1 mRNA and protein in the developing and mature brain. J. Comp. Neurol. 460, 266-279 (2003).
21. Koop, K.E., MacDonald, L.M. & Lobe, C.G. Transcripts of Grg4, a murine groucho-related gene, are detected in adjacent tissues to other murine neurogenic gene homologues during embryonic development. Mech. Dev. 59, 73-87 (1996).
22. Yao, J. et al. Combinatorial expression patterns of individual TLE proteins during cell determination and differentiation suggest non-redundant functions for mammalian homologs of Drosophila Groucho. Dev. Growth Differ. 40, 133-146 (1998).
23. Hevner, R.F. et al. Beyond laminar fate: toward a molecular classification of cortical projection/pyramidal neurons. Dev. Neurosci. 25, 139-151 (2003).
24. 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).
25. Hevner, R.F., Neogi, T., Englund, C., Daza, R.A. & Fink, A. Cajal-Retzius cells in the mouse: transcription factors, neurotransmitters, and birthdays suggest a pallial origin. Brain Res. Dev. Brain Res. 141, 39-53 (2003).
26. Shen, Q., Qian, X., Capela, A. & Temple, S. Stem cells in the embryonic cerebral cortex: their role in histogenesis and patterning. J. Neurobiol. 36, 162-174 (1998).
27. Caviness, V.S., Jr., Takahashi, T. & Nowakowski, R.S. Numbers, time and neocortical neuronogenesis: a general developmental and evolutionary model. Trends Neurosci. 18, 379-383 (1995).
28. Calegari, F., Haubensak, W., Haffner, C. & Huttner, W.B. Selective lengthening of the cell cycle in the neurogenic subpopulation of neural progenitor cells during mouse brain development. J. Neurosci. 25, 6533-6538 (2005).
29. Al-Kofahi, O. et al. Automated cell lineage construction: A rapid method to analyze clonal development established with murine neural progenitor cells. Cell Cycle 5, 327-335 (2006).
30. Polleux, F., Dehay, C. & Kennedy, H. The timetable of laminar neurogenesis contributes to the specification of cortical areas in mouse isocortex. J. Comp. Neurol. 385, 95-116 (1997).
31. Luskin, M.B., Pearlman, A.L. & Sanes, J.R. Cell lineage in the cerebral cortex of the mouse studied in vivo and in vitro with a recombinant retrovirus. Neuron 1, 635-647 (1988).
32. 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).
33. Reid, C.B., Liang, I. & Walsh, C. Systematic widespread clonal organization in cerebral cortex. Neuron 15, 299-310 (1995).
34. Morrow, T., Song, M.R. & Ghosh, A. Sequential specification of neurons and glia by developmentally regulated extracellular factors. Development 128, 3585-3594 (2001).
35. Barnabe-Heider, F. et al. Evidence that embryonic neurons regulate the onset of cortical gliogenesis via cardiotrophin-1. Neuron 48, 253-265 (2005).
36. Xuan, S. et al. Winged helix transcription factor BF-1 is essential for the development of the cerebral hemispheres. Neuron 14, 1141-1152 (1995).
37. Muzio, L. & Mallamaci, A. Foxg1 confines Cajal-Retzius neuronogenesis and hippocampal morphogenesis to the dorsomedial pallium. J. Neurosci. 25, 4435-4441 (2005).
38. Isshiki, T. & Doe, C.Q. Maintaining youth in Drosophila neural progenitors. Cell Cycle 3, 296-299 (2004).
39. Grosskortenhaus, R., Pearson, B.J., Marusich, A. & Doe, C.Q. Regulation of temporal identity transitions in Drosophila neuroblasts. Dev. Cell 8, 193-202 (2005).
40. Reid, C.B., Tavazoie, S.F. & Walsh, C.A. Clonal dispersion and evidence for asymmetric cell division in ferret cortex. Development 124, 2441-2450 (1997).
41. Shen, Q., Zhong, W., Jan, Y.N. & Temple, S. Asymmetric Numb distribution is critical for asymmetric cell division of mouse cerebral cortical stem cells and neuroblasts. Development 129, 4843-4853 (2002).
42. Li, H.S. et al. Inactivation of Numb and Numblike in embryonic dorsal forebrain impairs neurogenesis and disrupts cortical morphogenesis. Neuron 40, 1105-1118 (2003).
43. Martynoga, B., Morrison, H., Price, D.J. & Mason, J.O. Foxg1 is required for specification of ventral telencephalon and region-specific regulation of dorsal telencephalic precursor proliferation and apoptosis. Dev. Biol. 283, 113-127 (2005).
44. Kruger, G.M. et al. Neural crest stem cells persist in the adult gut but undergo changes in self-renewal, neuronal subtype potential, and factor responsiveness. Neuron 35, 657-669 (2002).
45. Shen, Q. et al. Endothelial cells stimulate self-renewal and expand neurogenesis of neural stem cells. Science 304, 1338-1340 (2004).
46. Lois, C., Hong, E.J., Pease, S., Brown, E.J. & Baltimore, D. Germline transmission and tissue-specific expression of transgenes delivered by lentiviral vectors. Science 295, 868-872 (2002).