Fbw7 controls neural stem cell differentiation and progenitor apoptosis via Notch and c-Jun

Nature Neuroscience

Volumn 13, Issue 11, 2010, Pages 1365-1372

  Hoeck, Joerg D ^a   Jandke, Anett ^a   Blake, Sophia M ^a   Nye, Emma ^a   Spencer Dene, Bradley ^a   Brandner, Sebastian ^b   Behrens, Axel ^a  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

F BOX PROTEIN; NOTCH1 RECEPTOR; PROTEIN C JUN; PROTEIN FBW7; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN REGION; CELL COUNT; CELL DEATH; CELL DIFFERENTIATION; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; EMBRYO; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS; BRAIN; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; EMBRYO, MAMMALIAN; F-BOX PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; INTERMEDIATE FILAMENT PROTEINS; MICE; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; PROTO-ONCOGENE PROTEINS C-JUN; RECEPTORS, NOTCH; STEM CELLS; UBIQUITIN-PROTEIN LIGASES;

EID: 78049231370     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn.2644     Document Type: Article

References (45)

1. Merkle, F.T. & Alvarez-Buylla, A. Neural stem cells in mammalian development. Curr. Opin. Cell Biol. 18, 704-709 (2006).
2. Götz, M. & Barde, Y.A. Radial glial cells defned and major intermediates between embryonic stem cells and CNS neurons. Neuron 46, 369-372 (2005).
3. Ho, M.S., Tsai, P.I. & Chien, C.T. F-box proteins: the key to protein degradation. J. Biomed. Sci. 13, 181-191 (2006).
4. Welcker, M. & Clurman, B.E. FBW7 ubiquitin ligase: a tumour suppressor at the crossroads of cell division, growth and differentiation. Nat. Rev. Cancer 8, 83-93 (2008).
5. Tan, Y., Sangfelt, O. & Spruck, C. The Fbxw7/hCdc4 tumor suppressor in human cancer. Cancer Lett. 271, 1-12 (2008).
6. Fuchs, S.Y. Tumor suppressor activities of the Fbw7 E3 ubiquitin ligase receptor. Cancer Biol. Ther. 4, 506-508 (2005).
7. Behrens, A., Sibilia, M. & Wagner, E.F. Amino-terminal phosphorylation of c-Jun regulates stress-induced apoptosis and cellular proliferation. Nat. Genet. 21, 326-329 (1999).
8. Besirli, C.G., Wagner, E.F. & Johnson, E.M. Jr. The limited role of NH2-terminal c-Jun phosphorylation in neuronal apoptosis: identifcation of the nuclear pore complex as a potential target of the JNK pathway. J. Cell Biol. 170, 401-411 (2005).
9. Raivich, G. et al. The AP-1 transcription factor c-Jun is required for effcient axonal regeneration. Neuron 43, 57-67 (2004).
10. Yoon, K.J. et al. Mind bomb 1-expressing intermediate progenitors generate notch signaling to maintain radial glial cells. Neuron 58, 519-531 (2008).
11. Mizutani, K., Yoon, K., Dang, L., Tokunaga, A. & Gaiano, N. Differential Notch signalling distinguishes neural stem cells from intermediate progenitors. Nature 449, 351-355 (2007).
12. Corbin, J.G. et al. Regulation of neural progenitor cell development in the nervous system. J. Neurochem. 106, 2272-2287 (2008).
13. Yoon, K. & Gaiano, N. Notch signaling in the mammalian central nervous system: insights from mouse mutants. Nat. Neurosci. 8, 709-715 (2005).
14. Tetzlaff, M.T. et al. Defective cardiovascular development and elevated cyclin E and Notch proteins in mice lacking the Fbw7 F-box protein. Proc. Natl. Acad. Sci. USA 101, 3338-3345 (2004).
15. Tsunematsu, R. et al. Mouse Fbw7/Sel-10/Cdc4 is required for notch degradation during vascular development. J. Biol. Chem. 279, 9417-9423 (2004).
16. Kramer, E.R. et al. Cooperation between GDNF/Ret and ephrinA/EphA4 signals for motor-axon pathway selection in the limb. Neuron 50, 35-47 (2006).
17. Hartfuss, E., Galli, R., Heins, N. & Götz, M. Characterization of CNS precursor subtypes and radial glia. Dev. Biol. 229, 15-30 (2001).
18. Reynolds, B.A. & Rietze, R.L. Neural stem cells and neurospheres-re-evaluating the relationship. Nat. Methods 2, 333-336 (2005).
19. Nateri, A.S., Riera-Sans, L., Da Costa, C. & Behrens, A. The ubiquitin ligase SCFFbw7 antagonizes apoptotic JNK signaling. Science 303, 1374-1378 (2004).
20. Bossy-Wetzel, E., Bakiri, L. & Yaniv, M. Induction of apoptosis by the transcription factor c-Jun. EMBO J. 16, 1695-1709 (1997).
21. Whitfeld, J., Neame, S.J., Paquet, L., Bernard, O. & Ham, J. Dominant-negative c-Jun promotes neuronal survival by reducing BIM expression and inhibiting mitochondrial cytochrome c release. Neuron 29, 629-643 (2001).
22. Ma, C. et al. dp5/HRK is a c-Jun target gene and required for apoptosis induced by potassium deprivation in cerebellar granule neurons. J. Biol. Chem. 282, 30901-30909 (2007).
23. Angel, P. , Hattori, K., Smeal, T. & Karin, M. The jun proto-oncogene is positively autoregulated by its product, Jun/AP1. Cell 55, 875-885 (1988).
24. Gaiano, N., Nye, J.S. & Fishell, G. Radial glial identity is promoted by Notch1 signaling in the murine forebrain. Neuron 26, 395-404 (2000).
25. Anthony, T.E., Mason, H.A., Gridley, T., Fishell, G. & Heintz, N. Brain lipid-binding protein is a direct target of Notch signaling in radial glial cells. Genes Dev. 19, 1028-1033 (2005).
26. Radtke, F. et al. Defcient T cell fate specifcation in mice with an induced inactivation of Notch1. Immunity 10, 547-558 (1999).
27. Selkoe, D. & Kopan, R. Notch and Presenilin: regulated intramembrane proteolysis links development and degeneration. Annu. Rev. Neurosci. 26, 565-597 (2003).
28. Anthony, T.E., Klein, C., Fishell, G. & Heintz, N. Radial glia serve as neuronal progenitors in all regions of the central nervous system. Neuron 41, 881-890 (2004).
29. Patten, B.A., Peyrin, J.M., Weinmaster, G. & Corfas, G. Sequential signaling through Notch1 and erbB receptors mediates radial glia differentiation. J. Neurosci. 23, 6132-6140 (2003).
30. Coffey, E.T. et al. c-Jun N-terminal protein kinase (JNK) 2/3 is specifcally activated by stress, mediating c-Jun activation, in the presence of constitutive JNK1 activity in cerebellar neurons. J. Neurosci. 22, 4335-4345 (2002).
31. Wang, X. et al. Targeted deletion of the mitogen-activated protein kinase kinase 4 gene in the nervous system causes severe brain developmental defects and premature death. Mol. Cell. Biol. 27, 7935-7946 (2007).
32. Chang, L., Jones, Y., Ellisman, M.H., Goldstein, L.S. & Karin, M. JNK1 is required for maintenance of neuronal microtubules and controls phosphorylation of microtubule-associated proteins. Dev. Cell 4, 521-533 (2003).
33. Ohtsuka, T. et al. Hes1 and Hes5 as notch effectors in mammalian neuronal differentiation. EMBO J. 18, 2196-2207 (1999).
34. de la Pompa, J.L. et al. Conservation of the Notch signalling pathway in mammalian neurogenesis. Development 124, 1139-1148 (1997).
35. Nelson, B.R., Hartman, B.H., Georgi, S.A., Lan, M.S. & Reh, T.A. Transient inactivation of Notch signaling synchronizes differentiation of neural progenitor cells. Dev. Biol. 304, 479-498 (2007).
36. Hojo, M. et al. Glial cell fate specifcation modulated by the bHLH gene Hes5 in mouse retina. Development 127, 2515-2522 (2000).
37. Thompson, B.J. et al. Control of hematopoietic stem cell quiescence by the E3 ubiquitin ligase Fbw7. J. Exp. Med. 205, 1395-1408 (2008).
38. Mao, J.H. et al. Fbxw7/Cdc4 is a p53-dependent, haploinsuffcient tumour suppressor gene. Nature 432, 775-779 (2004).
39. Welcker, M., Orian, A., Grim, J.E., Eisenman, R.N. & Clurman, B.E. A nucleolar isoform of the Fbw7 ubiquitin ligase regulates c-Myc and cell size. Curr. Biol. 14, 1852-1857 (2004).
40. Cdc4γ are required for cyclin E turnover in cell lines that do not overexpress cyclin E. Cell Cycle 7, 1075-1082 (2008).
41. van Drogen, F. et al. Ubiquitylation of cyclin E requires the sequential function of SCF complexes containing distinct hCdc4 isoforms. Mol. Cell 23, 37-48 (2006).
42. Matsuoka, S. et al. Fbxw7 acts as a critical fail-safe against premature loss of hematopoietic stem cells and development of T-ALL. Genes Dev. 22, 986-991 (2008).
43. Pollard, S.M., Conti, L., Sun, Y., Goffredo, D. & Smith, A. Adherent neural stem (NS) cells from fetal and adult forebrain. Cereb. Cortex 16 (suppl. 1): i112-i120 (2006).
44. Behrens, A. et al. Impaired intervertebral disc formation in the absence of Jun. Development 130, 103-109 (2003).
45. Nateri, A.S., Spencer-Dene, B. & Behrens, A. Interaction of phosphorylated c-Jun with TCF4 regulates intestinal cancer development. Nature 437, 281-285 (2005).