Continuing role for mouse Numb and Numbl in maintaining progenitor cells during cortical neurogenesis

Nature Neuroscience

Volumn 7, Issue 8, 2004, Pages 803-811

  Petersen, Petur H ^a   Zou, Kaiyong ^a   Krauss, Stefan ^b   Zhong, Weimin ^a  

^a YALE UNIVERSITY   (United States)

^b OSLO UNIVERSITY HOSPITAL   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN PROTEIN; PROTEIN NUMB; PROTEIN NUMBL; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL MODEL; ARTICLE; CELL CYCLE; CELL DIFFERENTIATION; CELL DIVISION; CELL FATE; CELL RENEWAL; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; FOREBRAIN; MOUSE; NEOCORTEX; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEM CELL;

ANIMALS; EMBRYO; GENE TARGETING; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; IN SITU NICK-END LABELING; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; MICE, MUTANT STRAINS; NEOCORTEX; NERVE TISSUE PROTEINS; NEURONS; STEM CELLS;

EID: 3342938070     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn1289     Document Type: Article

References (48)

1. Rakic, P. Specification of cerebral cortical areas. Science 241, 170-176 (1988).
2. McConnell, S.K. Constructing the cerebral cortex: neurogenesis and fate determination. Neuron 15, 761-768 (1995).
3. Chenn, A. & McConnell, S.K. Cleavage orientation and the asymmetric inheritance of Notch1 immunoreactivity in mammalian neurogenesis, Cell 82, 631-641 (1995).
4. 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).
5. Caviness, V.S. Jr., Takahashi, T. & Nowakowski, R.S. Numbers, time and neocortical neurogenesis: a general developmental and evolutionary model. Trends Neurosci. 18, 379-383 (1995).
6. Edlund, T. & Jessell, T.M. Progression from extrinsic to intrinsic signaling in cell fate specification: a view from the nervous system. Cell 96, 211-224 (1999).
7. Zhong, W. Diversifying neural cells through order of birth and asymmetry of division. Neuron 37, 11-14 (2003).
8. Anderson, D.A. Stem cells and pattern formation in the nervous system: the possible versus the actual. Neuron 30, 19-35 (2001).
9. Temple, S. The development of neural stem cells. Nature 414, 112-117 (2001).
10. Johe, K.K., Hazel, T.G., Muller, T., Dugich-Djordjevic, M.M. & McKay, R.D.G. Single factors direct the differentiation of stem cells from the fetal and adult central nervous system. Genes Dev. 10, 3129-3140 (1996).
11. Shah, N.M., Groves, A. & Anderson, D.J. Alternative neural crest cell fates are instructively promoted by TGFβ superfamily members. Cell 85, 331-343 (1996).
12. Hitoshi, S. et al. Notch pathway molecules are essential for the maintenance, but not the generation, of mammalian neural stem cells. Genes Dev. 16, 846-858 (2002).
13. Machon, O., van den Bout, C.J., Backman, M., Kemler, R. & Krauss, S. Role of β-Catenin in the developing cortical and hippocampal neuroepithelium. Neuroscience 122, 129-143 (2003).
14. 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).
15. Zhong, W., Feder, J.N., Jiang, M-M., Jan, L.Y. & Jan, Y.N. Asymmetric localization of a mammalian numb homolog during mouse cortical neurogenesis. Neuron 17, 43-53 (1996).
16. Zhong, W., Jiang, M-M., Weinmaster, G., Jan, L.Y. & Jan, Y.N. Differential expression of mammalian Numb, Numblike and Notch1 suggests distinct roles during mouse cortical neurogenesis. Development 124, 1887-1897 (1997).
17. Verdi, J.M. et al. Mammalian NUMB is an evolutionarily conserved signaling adapter protein that specifies cell fate. Curr. Biol. 6, 113-145 (1996).
18. Rhyu, M.S., Jan, L.Y. & Jan, Y.N. Asymmetric distribution of numb protein during division of the sensory organ precursor cell confers distinct fates to daughter cells. Cell 76, 477-491 (1994).
19. Petersen, P.H., Zou, K., Hwang, J.K., Jan, Y.N. & Zhong, W. Progenitor cell maintenance requires numb and numblike during mouse neurogenesis. Nature 419, 929-934 (2002).
20. 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).
21. Verdi, J.M. et al. Distinct human NUMB isoforms regulate differentiation vs. proliferation in the neuronal lineage. Proc. Natl. Acad. Sci. USA 96, 10472-10476 (1999).
22. Spana, E.P. & Doe, C.Q. Numb antagonizes Notch signaling to specify sibling neuron cell fates. Neuron 17, 21-26 (1996)
23. Lear, B.C., Skeath, J.B. & Patel, N.H. Neural cell fate in rac1 and cycA mutants: the roles of intrinsic and extrinsic factors in asymmetric division in the Drosophila central nervous system. Mech. Dev. 88, 207-219 (1999).
24. Wakamatsu, Y., Maynard, T.M., Jones, S.U. & Weston, J.A. NUMB localizes in the basal cortex of mitotic avian neuroepithelial cells and modulates neuronal differentiation by binding to NOTCH-1. Neuron 23, 71-81 (1999).
25. Zilian, O. et al. Multiple roles of mouse numb in tuning developmental cell fates. Curr. Biol. 11, 494-501 (2001).
26. Gu, M., Marth, J.D., Orban, P.C., Mossmann, H. & Rajewsky, K. Deletion of a DNA polymerase β gene segment in T cells using cell type-specific gene targeting. Science 265, 103-106 (1994).
27. Zhong, W. et al. Mouse numb is an essential gene involved in cortical neurogenesis. Proc. Natl. Acad. Sci. USA 97, 6844-6849 (2000).
28. Ohtsuka, T. et al. Hes1 and Hes5 as Notch effectors in mammalian neuronal differentiation. EMBO 18, 2196-2207 (1999).
29. Walther, C. & Gruss, P. Pax-6, a murine paired box gene, is expressed in the developing CNS. Development 113, 1435-1449 (1991).
30. van den Bout, C.J., Machon, O., Rosok, O., Backman, M. & Krauss, S. The mouse enhancer element D6 directs Cre recombinase activity in the neocortex and the hippocampus. Mech. Dev. 110, 179-182 (2002).
31. Machon, O. et al. Forebrain-specific promoter/enhancer D6 derived from the mouse Dach1 gene controls expression in neural stem cells. Neuroscience 112, 951-966 (2002).
32. Marin, O. & Rubenstein, J.L. Cell migration in the forebrain. Annu. Rev. Neurosci. 26, 441-483 (2003).
33. Fode, C. et al. A role for neural determination genes in specifying the dorsoventral identity of telencephalic neurons. Genes Dev. 14, 67-80 (2000).
34. Sakakibara S. et al. Mouse-Musashi-1, a neural RNA-binding protein highly enriched in the mammalian CNS stem cell. Dev. Biol. 176, 230-242 (1996).
35. Furukawa, T., Mukherjee, S., Bao, Z.Z., Morrow, E.M. & Cepko, C.L. rax, Hes1, and Notch1 promote the formation of Muller glia by postnatal retinal progenitor cells. Neuron 26, 383-394 (2000).
36. Morrison, S.J. et al. Transient Notch activation initiates an irreversible switch from neurogenesis to gliogenesis by neural crest stem cells. Cell 101, 499-510 (2000).
37. Meyers, E.N., Lewandoski, M. & Martin, G.R. An Fgf8 mutant allelic series generated by Cre- and Flp-mediated recombination. Nat. Genet. 18, 136-141 (1998).
38. Frantz, G.D., Bohner, A.P., Akers, R.M. & McConnell, S.K. Regulation of the POU domain gene SCIP during cerebral cortical development. J. Neurosci. 14, 472-485 (1994).
39. McEvilly, R.J., de Diaz, M.O., Schonemann, M.D., Hooshmand, F. & Rosenfeld, M.G. Transcriptional regulation of cortical neuron migration by POU domain factors. Science 295, 1528-1532 (2002).
40. Sugitani, Y. et al. Brn-1 and Brn-2 share crucial roles in the production and positioning of mouse neocortical neurons. Genes Dev. 16, 1760-1765 (2002).
41. 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).
42. Anderson, S.A., Eisenstat, D.D., Shi, L. & Rubenstein, J.L. Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes. Science 278, 474-476 (1997).
43. Salcini, A.E. et al. Binding specificity and in vivotargets of the EH domain, a novel protein-protein interaction module. Genes Dev. 11, 2239-2249 (1997).
44. Cayouette, M. & Raff, M. Asymmetric segregation of Numb: a mechanism for neural specification from Drosophila to mammals. Nat. Neurosci. 5, 1265-1269 (2002).
45. 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).
46. Guo, M., Jan, L.Y. & Jan, Y.N. Control of daughter cell fates during asymmetric division: interaction of Numb and Notch. Neuron 17, 27-41 (1996).
47. Cayouette, M. & Raff, M. The orientation of cell division influences cell-fate choice in the developing mammalian retina. Development 130, 2329-2339 (2003).
48. Artavanis-Tsakonas, S. Notch signaling: Cell fate control and signal integration in development. Science 284, 770-776 (1999).