Neural stem cell transcriptional networks highlight genes essential for nervous system development

EMBO Journal

Volumn 28, Issue 24, 2009, Pages 3799-3807

  Southall, Tony D ^a   Brand, Andrea H ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Differentiation; Multiple transcription factor binding; Neural stem cell; Self renewal; Transcriptional networks

Indexed keywords

BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ASENSE; TRANSCRIPTION FACTOR DEADPAN; TRANSCRIPTION FACTOR PROSPERO; TRANSCRIPTION FACTOR SNAIL; UNCLASSIFIED DRUG;

ARTICLE; CELL DIFFERENTIATION; CELL RENEWAL; CONTROLLED STUDY; FLY; GENE EXPRESSION PROFILING; GENE LOCUS; GENOME; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; REGULATORY SEQUENCE;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BINDING SITES; CELL DIFFERENTIATION; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE REGULATORY NETWORKS; NERVE TISSUE PROTEINS; NERVOUS SYSTEM; NEURONS; NUCLEAR PROTEINS; STEM CELLS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

GASTROPODA; PROSPERO; VERTEBRATA;

EID: 72449171924     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2009.309     Document Type: Article

References (58)

1. Arlotta P, Molyneaux BJ, Chen J, Inoue J, Kominami R, Macklis JD (2005) Neuronal subtype-specific genes that control corti-cospinal motor neuron development in vivo. Neuron 45: 207-221
2. Ashraf SI, Ip YT (2001) The Snail protein family regulates neuro-blast expression of inscuteable and string, genes involved in asymmetry and cell division in Drosophila. Development 128: 4757-4767
3. Bello B, Reichert H, Hirth F (2006) The brain tumor gene negatively regulates neural progenitor cell proliferation in the larval central brain of Drosophila. Development 133: 2639-2648
4. Bello BC, Izergina N, Caussinus E, Reichert H (2008) Amplification of neural stem cell proliferation by intermediate progenitor cells in Drosophila brain development. Neural Dev 3: 5
5. Betschinger J, Mechtler K, Knoblich JA (2006) Asymmetric segregation of the tumor suppressor brat regulates self-renewal in Drosophila neural stem cells. Cell 124: 1241-1253
6. Bianchi-Frias D, Orian A, Delrow JJ, Vazquez J, Rosales-Nieves AE, Parkhurst SM (2004) Hairy transcriptional repression targets and cofactor recruitment in Drosophila. PLoS Biol 2: E178
7. Bier E, Vaessin H, Younger-Shepherd S, Jan LY, Jan YN (1992) deadpan, an essential pan-neural gene in Drosophila, encodes a helix-loop-helix protein similar to the hairy gene product. Genes Dev 6: 2137-2151
8. Birney E, Stamatoyannopoulos JA, Dutta A, Guigo R, Gingeras TR, Margulies EH, Weng Z, Snyder M, Dermitzakis ET, Thurman RE, Kuehn MS, Taylor CM, Neph S, Koch CM, Asthana S, Malhotra A, Adzhubei I, Greenbaum JA, Andrews RM, Flicek P et al. (2007) Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 447: 799-816
9. Boone JQ, Doe CQ (2008) Identification of Drosophila type II neuroblast lineages containing transit amplifying ganglion mother cells. Dev Neurobiol 68: 1185-1195
10. Bowman SK, Rolland V, Betschinger J, Kinsey KA, Emery G, Knoblich JA (2008) The tumor suppressors Brat and Numb regulate transit-amplifying neuroblast lineages in Drosophila. Dev Cell 14: 535-546
11. Boyer LA, Lee TI, Cole MF, Johnstone SE, Levine SS, Zucker JP, Guenther MG, Kumar RM, Murray HL, Jenner RG, Gifford DK, Melton DA, Jaenisch R, Young RA. (2005) Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 122: 947-956
12. Brand M, Jarman AP, Jan LY, Jan YN (1993) asense is a Drosophila neural precursor gene and is capable of initiating sense organ formation. Development 119: 1-17
13. Brody T, Odenwald WF (2000) Programmed transformations in neuroblast gene expression during Drosophila CNS lineage development. Dev Biol 226: 34-44
14. 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
15. Castro DS, Skowronska-Krawczyk D, Armant O, Donaldson IJ, Parras C, Hunt C, Critchley JA, Nguyen L, Gossler A, Gottgens B, Matter JM, Guillemot F (2006) Proneural bHLH and Brn proteins coregulate a neurogenic program through cooperative binding to a conserved DNA motif. Dev Cell 11: 831-844
16. Chen X, Xu H, Yuan P, Fang F, Huss M, Vega VB, Wong E, Orlov YL, Zhang W, Jiang J, Loh YH, Yeo HC, Yeo ZX, Narang V, Govindarajan KR, Leong B, Shahab A, Ruan Y, Bourque G, Sung WK et al. (2008) Integration of external signaling pathways with the core transcrip-tional network in embryonic stem cells. Cell 133: 1106-1117
17. Choksi SP, Southall TD, Bossing T, Edoff K, de Wit E, Fischer BE, van Steensel B, Micklem G, Brand AH (2006) Prospero acts as a binary switch between self-renewal and differentiation in Drosophila neural stem cells. Dev Cell 11: 775-789
18. de Nooij JC, Letendre MA, Hariharan IK (1996) A cyclin-dependent kinase inhibitor, Dacapo, is necessary for timely exit from the cell cycle during Drosophila embryogenesis. Cell 87: 1237-1247
19. Doe CQ (2008) Neural stem cells: balancing self-renewal with differentiation. Development 135: 1575-1587
20. Egger B, Chell JM, Brand AH (2008) Insights into neural stem cell biology from flies. Philos Trans R Soc Lond B Biol Sci 363: 39-56
21. Elkins T, Zinn K, McAllister L, Hoffmann FM, Goodman CS (1990) Genetic analysis of a Drosophila neural cell adhesion molecule: interaction of fasciclin I and Abelson tyrosine kinase mutations. Cell 60: 565-575
22. Gonzalez F, Romani S, Cubas P, Modolell J, Campuzano S (1989) Molecular analysis of the asense gene, a member of the achaete-scute complex of Drosophila melanogaster, and its novel role in optic lobe development. EMBO J 8: 3553-3562
23. Guelen L, Pagie L, Brasset E, Meuleman W, Faza MB, Talhout W, Eussen BH, de Klein A, Wessels L, de Laat W, van Steensel B (2008) Domain organization of human chromosomes revealed by mapping of nuclear lamina interactions. Nature 453: 948-951
24. Hemavathy K, Ashraf SI, Ip YT (2000) Snail/slug family of repres-sors: slowly going into the fast lane of development and cancer. Gene 257: 1-12
25. Hoshino M, Suzuki E, Nabeshima Y, Hama C (1996) Hikaru genki protein is secreted into synaptic clefts from an early stage of synapse formation in Drosophila. Development 122: 589-597
26. Hu Y, Wang T, Stormo GD, Gordon JI (2004) RNA interference of achaete-scute homolog 1 in mouse prostate neuroendocrine cells reveals its gene targets and DNA binding sites. Proc Natl Acad Sci USA 101: 5559-5564
27. Jarman AP, Brand M, Jan LY, Jan YN (1993) The regulation and function of the helix-loop-helix gene, asense, in Drosophila neural precursors. Development 119: 19-29 (Pubitemid 23279123)
28. Jones BW, Fetter RD, Tear G, Goodman CS (1995) glial cells missing: a genetic switch that controls glial versus neuronal fate. Cell 82: 1013-1023
29. Kanai MI, Okabe M, Hiromi Y (2005) seven-up Controls switching of transcription factors that specify temporal identities of Drosophila neuroblasts. Dev Cell 8: 203-213
30. Lee CY, Wilkinson BD, Siegrist SE, Wharton RP, Doe CQ (2006) Brat is a Miranda cargo protein that promotes neuronal differentiation and inhibits neuroblast self-renewal. Dev Cell 10: 441-449
31. Liu J, Ghanim M, Xue L, Brown CD, Iossifov I, Angeletti C, Hua S, Negre N, Ludwig M, Stricker T, Al-Ahmadie HA, Tretiakova M, Camp RL, Perera-Alberto M, Rimm DL, Xu T, Rzhetsky A, White KP (2009) Analysis of Drosophila segmentation network identifies a JNK pathway factor overexpressed in kidney cancer. Science
32. Liu TH, Li L, Vaessin H (2002) Transcription of the Drosophila CKI gene dacapo is regulated by a modular array of cis-regulatory sequences. Mech Dev 112: 25-36
33. Loh YH, Wu Q, Chew JL, Vega VB, Zhang W, Chen X, Bourque G, George J, Leong B, Liu J, Wong KY, Sung KW, Lee CW, Zhao XD, Chiu KP, Lipovich L, Kuznetsov VA, Robson P, Stanton LW, Wei CL et al. (2006) The Oct4 and Nanog transcription network regulates pluripotency in mouse embryonic stem cells. Nat Genet 38: 431-440
34. Martin DM, Berriman M, Barton GJ (2004) GOtcha: a new method for prediction of protein function assessed by the annotation of seven genomes. BMC Bioinformatics 5: 178
35. Mauhin V, Lutz Y, Dennefeld C, Alberga A (1993) Definition of the DNA-binding site repertoire for the Drosophila transcription factor SNAIL. Nucleic Acids Res 21: 3951-3957
36. Moorman C, Sun LV, Wang J, de Wit E, Talhout W, Ward LD, Greil F, Lu XJ, White KP, Bussemaker HJ, van Steensel B (2006) Hotspots of transcription factor colocalization in the genome of Drosophila melanogaster. Proc Natl Acad Sci USA 103: 12027-12032
37. Parras CM, Galli R, Britz O, Soares S, Galichet C, Battiste J, Johnson JE, Nakafuku M, Vescovi A, Guillemot F (2004) Mash1 specifies neurons and oligodendrocytes in the postnatal brain. EMBO J 23: 4495-4505
38. Pickersgill H, Kalverda B, de Wit E, Talhout W, Fornerod M, van Steensel B (2006) Characterization of the Drosophila melanoga-ster genome at the nuclear lamina. Nat Genet 38: 1005-1014
39. Remm M, Storm CE, Sonnhammer EL (2001) Automatic clustering of orthologs and in-paralogs from pairwise species comparisons. J Mol Biol 314: 1041-1052
40. Shen CP, Jan LY, Jan YN (1997) Miranda is required for the asymmetric localization of Prospero during mitosis in Drosophila. Cell 90: 449-458
41. Sommer L, Shah N, Rao M, Anderson DJ (1995) The cellular function of MASH1 in autonomic neurogenesis. Neuron 15: 1245-1258
42. Song S, Cooperman J, Letting DL, Blobel GA, Choi JK (2004) Identification of cyclin D3 as a direct target of E2A using DamID. Mol Cell Biol 24: 8790-8802
43. Speicher S, Fischer A, Knoblich J, Carmena A (2008) The PDZ protein Canoe regulates the asymmetric division of Droso-phila neuroblasts and muscle progenitors. Curr Biol 18: 831-837
44. Sun LV, Chen L, Greil F, Negre N, Li TR, Cavalli G, Zhao H, Van Steensel B, White KP (2003) Protein-DNA interaction mapping using genomic tiling path microarrays in Drosophila. Proc Natl Acad Sci USA 100: 9428-9433
45. Tear G, Harris R, Sutaria S, Kilomanski K, Goodman CS, Seeger MA (1996) commissureless controls growth cone guidance across the CNS midline in Drosophila and encodes a novel membrane protein. Neuron 16: 501-514
46. Tolhuis B, de Wit E, Muijrers I, Teunissen H, Talhout W, van Steensel B, van Lohuizen M (2006) Genome-wide profiling of PRC1 and PRC2 Polycomb chromatin binding in Drosophila melanogaster. Nat Genet 38: 694-699
47. Tomancak P, Berman BP, Beaton A, Weiszmann R, Kwan E, Hartenstein V, Celniker SE, Rubin GM (2007) Global analysis of patterns of gene expression during Drosophila embryogenesis. Genome Biol 8: R145
48. Tomita K, Nakanishi S, Guillemot F, Kageyama R (1996) Mash1 promotes neuronal differentiation in the retina. Genes Cells 1: 765-774
49. Tusher VG, Tibshirani R, Chu G (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 98: 5116-5121
50. van Steensel B, Henikoff S (2000) Identification of in vivo DNA targets of chromatin proteins using tethered dam methyltransfer-ase. Nat Biotechnol 18: 424-428
51. van Steensel B, Delrow J, Henikoff S (2001) Chromatin profiling using targeted DNA adenine methyltransferase. Nat Genet 27: 304-308
52. Vogel MJ, Peric-Hupkes D, van Steensel B (2007) Detection of in vivo protein-DNA interactions using DamID in mammalian cells. Nat Protoc 2: 1467-1478
53. Wallace K, Liu TH, Vaessin H (2000) The pan-neural bHLH proteins DEADPAN and ASENSE regulate mitotic activity and cdk inhibitor dacapo expression in the Drosophila larval optic lobes. Genesis 26: 77-85
54. Winston RL, Ehley JA, Baird EE, Dervan PB, Gottesfeld JM (2000) Asymmetric DNA binding by a homodimeric bHLH protein. Biochemistry 39: 9092-9098
55. Winston RL, Millar DP, Gottesfeld JM, Kent SB (1999) Characterization of the DNA binding properties of the bHLH domain of Deadpan to single and tandem sites. Biochemistry 38: 5138-5146
56. Wodarz A (2005) Molecular control of cell polarity and asymmetric cell division in Drosophila neuroblasts. Curr Opin Cell Biol 17: 475-481
57. Yu F, Kuo CT, Jan YN (2006) Drosophila neuroblast asymmetric cell division: recent advances and implications for stem cell biology. Neuron 51: 13-20
58. Zhong W, Chia W (2008) Neurogenesis and asymmetric cell division. Curr Opin Neurobiol 18: 4-11