Snail coordinately regulates downstream pathways to control multiple aspects of mammalian neural precursor development

Journal of Neuroscience

Volumn 34, Issue 15, 2014, Pages 5164-5175

  Zander, Mark A ^a   Burns, Sarah E ^a   Yang, Guang ^a   Kaplan, David R ^a,b   Miller, Freda D ^a,b,c  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b Institute of Medical Science Hospital for Sick Children ^*  (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

Cdc25; Cortical development; Neural stem cell; P53; Radial glial precursor; Self renewal

Indexed keywords

CASPASE 2; EOMESODERMIN; NEDD8 PROTEIN; PROTEIN P53; TRANSCRIPTION FACTOR PAX6; TRANSCRIPTION FACTOR SNAIL; UBIQUITIN PROTEIN LIGASE NEDD4;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DOWNSTREAM PROCESSING; EMBRYO; FEMALE; FLOW CYTOMETRY; GENE OVEREXPRESSION; GENETIC TRANSFECTION; HISTOLOGY; IMMUNOCYTOCHEMISTRY; MOUSE; NERVE GROWTH; NONHUMAN; PRIORITY JOURNAL; RADIOIMMUNOPRECIPITATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

CDC25; CORTICAL DEVELOPMENT; NEURAL STEM CELL; P53; RADIAL GLIAL PRECURSOR; SELF-RENEWAL;

ANIMALS; CDC25 PHOSPHATASES; CELL PROLIFERATION; CEREBRAL CORTEX; EPENDYMOGLIAL CELLS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEK293 CELLS; HUMANS; MICE; NEURAL STEM CELLS; NEUROGENESIS; NEURONS; TRANSCRIPTION FACTORS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84899475878     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0370-14.2014     Document Type: Article

References (35)

1. Acloque H, Adams MS, Fishwick K, Bronner-Fraser M, Nieto MA (2009) Epithelial-mesenchymal transitions: the importance of changing cell state in development and disease. J Clin Invest 119:1438-1449. CrossRef Medline
2. Akhtar RS, Geng Y, Klocke BJ, Latham CB, Villunger A, Michalak EM, Strasser A, Carroll SL, Roth KA (2006) BH3-only proapoptotic Bcl-2 family members Noxa and Puma mediate neural precursor cell death. J Neurosci 26:7257-7264. CrossRef Medline
3. Ashraf SI, Ip YT (2001) The Snail protein family regulates neuroblast expression of inscuteable and string, genes involved in asymmetry and cell division in Drosophila. Development 128:4757-4767. Medline
4. Barnabé-Heider F, Wasylnka JA, Fernandes KJ, Porsche C, Sendtner M, Kaplan DR, Miller FD (2005) Evidence that embryonic neurons regulate the onset of cortical gliogenesis via cardiotrophin-1. Neuron 48:253-265. CrossRef Medline
5. Bartkowska K, Paquin A, Gauthier AS, Kaplan DR, Miller FD (2007) Trk signaling regulates neural precursor cell proliferation and differentiation during cortical development. Development 134:4369-4380. CrossRef Medline
6. Batlle E, Sancho E, Francí C, Domínguez D, Monfar M, Baulida J, García De Herreros A (2000) The transcription factor snail is a repressor of E-cadherin gene expression in epithelial tumour cells. Nat Cell Biol 2:84-89. CrossRef Medline
7. Biernaskie J, Paris M, Morozova O, Fagan BM, Marra M, Pevny L, Miller FD (2009) SKPs derive from hair follicle precursors and exhibit properties of adult dermal stem cells. Cell Stem Cell 5:610-623. CrossRef Medline
8. Boutros R, Lobjois V, Ducommun B (2007) CDC25 phosphatases in cancer cells: key players? Good targets? Nat Rev Cancer 7:495-507. CrossRef Medline
9. Brummelkamp TR, Bernards R, Agami R (2002) A system for stable expression of short interfering RNAs in mammalian cells. Science 296:550-553. CrossRef Medline
10. Cai Y, Chia W, Yang X (2001) A family of snail-related zinc finger proteins regulates two distinct and parallel mechanisms that mediate Drosophila neuroblast asymmetric divisions. EMBO J 20:1704-1714. CrossRef Medline
11. Cancino GI, Yiu AP, Fatt MP, Dugani CB, Flores ER, Frankland PW, Josselyn SA, Miller FD, Kaplan DR (2013) p63 regulates adult neural precursor and newly born neuron survival to control hippocampal-dependent behavior. J Neurosci 33:12569-12585. CrossRef Medline
12. De Craene B, van Roy F, Berx G (2005) Unraveling signalling cascades for the Snail family of transcription factors. Cell Signal 17:535-547. CrossRef Medline
13. Dehay C, Kennedy H (2007) Cell-cycle control and cortical development. Nat Rev Neurosci 8:438-450. CrossRef Medline
14. Dugani CB, Paquin A, Fujitani M, Kaplan DR, Miller FD (2009) p63 antagonizes p53 to promote the survival of embryonic neural precursor cells. J Neurosci 29:6710-6721. CrossRef Medline
15. Ellis P, Fagan BM, Magness ST, Hutton S, Taranova O, Hayashi S, McMahon A, Rao M, Pevny L (2004) SOX2, a persistent marker for multipotential neural stem cells derived from embryonic stem cells, the embryo or the adult. Dev Neurosci 26:148-165. CrossRef Medline
16. Gallagher D, Norman AA, Woodard CL, Yang G, Gauthier-Fisher A, Fujitani M, Vessey JP, Cancino GI, Sachewsky N, Woltjen K, Fatt MP, Morshead CM, Kaplan DR, Miller FD (2013) Transient maternal IL-6 mediates long-lasting changes in neural stem cell pools by deregulating an endogenous self-renewal pathway. Cell Stem Cell 13:564-576. CrossRef Medline
17. Gauthier AS, Furstoss O, Araki T, Chan R, Neel BG, Kaplan DR, Miller FD (2007) Control of CNS cell fate decisions by SHP-2 and its dysregulation in Noonan syndrome. Neuron 54:245-262. CrossRef Medline
18. Gauthier-Fisher A, Lin DC, Greeve M, Kaplan DR, Rottapel R, Miller FD (2009) Lfc and Tctex-1 regulate the genesis of neurons from cortical precursor cells. Nat Neurosci 12:735-744. CrossRef Medline
19. Hatzold J, Conradt B (2008) Control of apoptosis by asymmetric cell division. PLoS Biol 6:e84. CrossRef Medline
20. Hutton SR, Pevny LH (2011) SOX2 expression levels distinguish between neural progenitor populations of the developing dorsal telencephalon. Dev Biol 352:40-47. CrossRef Medline
21. Itoh Y, Moriyama Y, Hasegawa T, Endo TA, Toyoda T, Gotoh Y (2013) Scratch regulates neuronal migration onset via an epithelialmesenchymal transition-like mechanism. Nat Neurosci 16:416-425. CrossRef Medline
22. Kusek G, Campbell M, Doyle F, Tenenbaum SA, Kiebler M, Temple S (2012) Asymmetric segregation of the double-stranded RNA binding protein Staufen2 during mammalian neural stem cell divisions promotes lineage progression. Cell Stem Cell 11:505-516. CrossRef Medline
23. Lai SL, Miller MR, Robinson KJ, Doe CQ (2012) The snail family member Worniu is continuously required in neuroblasts to prevent Elav-induced premature differentiation. Dev Cell 23:849-857. CrossRef Medline
24. Lange C, Huttner WB, Calegari F (2009) Cdk4/cyclinD1 overexpression in neural stem cells shortens G1, delays neurogenesis, and promotes the generation and expansion of basal progenitors. Cell Stem Cell 5:320-331. CrossRef Medline
25. Nieto MA (2002) The snail superfamily of zinc-finger transcription factors. Nat Rev Mol Cell Biol 3:155-166. CrossRef Medline
26. Peco E, Escude T, Agius E, Sabado V, Medevielle F, Ducommun B, Pituello F (2012) The CDC25B phosphatase shortens the G2 phase of neural progenitors and promotes efficient neuron production. Development 139: 1095-1104. CrossRef Medline
27. Postiglione MP, Jüschke C, Xie Y, Haas GA, Charalambous C, Knoblich JA (2011) Mouse inscuteable induces apical-basal spindle orientation to facilitate intermediate progenitor generation in the developing neocortex. Neuron 72:269-284. CrossRef Medline
28. Salomoni P, Calegari F (2010) Cell cycle control of mammalian neural stem cells: putting a speed limit on G1. Trends Cell Biol 20:233-243. CrossRef Medline
29. Schwamborn JC, Berezikov E, Knoblich JA (2009) The TRIM-NHL protein TRIM32 activates microRNAs and prevents self-renewal in mouse neural progenitors. Cell 136:913-925. CrossRef Medline
30. Southall TD, Brand AH (2009) Neural stem cell transcriptional networks highlight genes essential for nervous system development. EMBO J 28: 3799-3807. CrossRef Medline
31. Thellmann M, Hatzold J, Conradt B (2003) The Snail-like CES-1 protein of C. elegans can block the expression of theBH3-only cell-death activator gene egl-1 by antagonizing the function of bHLH proteins. Development 130:4057-4071. CrossRef Medline
32. Tsui D, Vessey JP, Tomita H, Kaplan DR, Miller FD (2013) FoxP2 regulates neurogenesis during embryonic cortical development. J Neurosci 33: 244-258. CrossRef Medline
33. Vessey JP, Amadei G, Burns SE, Kiebler MA, Kaplan DR, Miller FD (2012) An asymmetrically localized Staufen2-dependent RNA complex regulates maintenance of mammalian neural stem cells. Cell Stem Cell 11:517-528. CrossRef Medline
34. Woltjen K, Michael IP, Mohseni P, Desai R, Mileikovsky M, Hämäläinen R, Cowling R, Wang W, Liu P, Gertsenstein M, Kaji K, Sung HK, Nagy A (2009) piggyBac transposition reprograms fibroblasts to induced pluripotent stem cells. Nature 458:766-770. CrossRef Medline
35. Zhou BP, Deng J, Xia W, Xu J, Li YM, Gunduz M, Hung MC (2004) Dual regulation of Snail by GSK-3[beta]-mediated phosphorylation in control of epithelial-mesenchymal transition. Nat Cell Biol 6:931-940. CrossRef Medline