Functional genomics identifies neural stem cell sub-type expression profiles and genes regulating neuroblast homeostasis

Developmental Biology

Volumn 361, Issue 1, 2012, Pages 137-146

  Carney, Travis D ^a   Miller, Michael R ^a   Robinson, Kristin J ^a   Bayraktar, Omer A ^a   Osterhout, Jessica A ^a   Doe, Chris Q ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

Drosophila; Expression profiling; Neural progenitors; Neuroblast; Self renewal; Transit amplifying

Indexed keywords

ANIMAL CELL; ARTICLE; CELL AGGREGATION; CELL COUNT; CELL EXPANSION; CELL TYPE; CONTROLLED STUDY; FUNCTIONAL GENOMICS; GENE EXPRESSION PROFILING; GENE FUNCTION; GENE IDENTIFICATION; GENETIC CONSERVATION; GENETIC TRANSCRIPTION; GENOTYPE; HOMEOSTASIS; LARVA; MUTANT; NEURAL STEM CELL; NEUROBLAST; NONHUMAN; ORTHOLOGY; PREDICTION; PRIORITY JOURNAL; REGULATOR GENE; RNA INTERFERENCE; VALIDATION STUDY; WILD TYPE;

MAMMALIA;

EID: 83055184189     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2011.10.020     Document Type: Article

References (56)

1. Albertson R., Chabu C., Sheehan A., Doe C.Q. Scribble protein domain mapping reveals a multistep localization mechanism and domains necessary for establishing cortical polarity. J. Cell Sci. 2004, 117:6061-6070.
2. Almeida M.S., Bray S.J. Regulation of post-embryonic neuroblasts by Drosophila Grainyhead. Mech. Dev. 2005, 122:1282-1293.
3. Ashraf S.I., Ganguly A., Roote J., Ip Y.T. Worniu, a snail family zinc-finger protein, is required for brain development in Drosophila. Dev. Dyn. 2004, 231:379-386.
4. Atwood S.X., Prehoda K.E. aPKC phosphorylates Miranda to polarize fate determinants during neuroblast asymmetric cell division. Curr. Biol. 2009, 19:723-729.
5. Bayraktar O.A., Boone J.Q., Drummond M.L., Doe C.Q. Drosophila type II neuroblast lineages keep Prospero levels low to generate large clones that contribute to the adult brain central complex. Neural Dev. 2010, 5:26.
6. Bello B.C., Izergina N., Caussinus E., Reichert H. Amplification of neural stem cell proliferation by intermediate progenitor cells in Drosophila brain development. Neural Dev. 2008, 3:5.
7. Betschinger J., Mechtler K., Knoblich J.A. Asymmetric segregation of the tumor suppressor brat regulates self-renewal in Drosophila neural stem cells. Cell 2006, 124:1241-1253.
8. Bier E., Vaessin H., Younger-Shepherd S., Jan L.Y., Jan Y.N. deadpan, an essential pan-neural gene in Drosophila, encodes a helix-loop-helix protein similar to the hairy gene product. Genes Dev. 1992, 6:2137-2151.
9. Boone J.Q., Doe C.Q. Identification of Drosophila type II neuroblast lineages containing transit amplifying ganglion mother cells. Dev. Neurobiol. 2008, 68:1185-1195.
10. Bowman S.K., Rolland V., Betschinger J., Kinsey K.A., Emery G., Knoblich J.A. The tumor suppressors Brat and Numb regulate transit-amplifying neuroblast lineages in Drosophila. Dev. Cell 2008, 14:535-546.
11. Brand M., Jarman A.P., Jan L.Y., Jan Y.N. asense is a Drosophila neural precursor gene and is capable of initiating sense organ formation. Development 1993, 119:1-17.
12. Broadus J., Fuerstenberg S., Doe C.Q. Staufen-dependent localization of prospero mRNA contributes to neuroblast daughter-cell fate. Nature 1998, 391:792-795.
13. Caldwell M.C., Datta S. Expression of cyclin E or DP/E2F rescues the G1 arrest of trol mutant neuroblasts in the Drosophila larval central nervous system. Mech. Dev. 1998, 79:121-130.
14. Chabu C., Doe C.Q. Dap160/intersectin binds and activates aPKC to regulate cell polarity and cell cycle progression. Development 2008, 135:2739-2746.
15. Chia W., Somers W.G., Wang H. Drosophila neuroblast asymmetric divisions: cell cycle regulators, asymmetric protein localization, and tumorigenesis. J. Cell Biol. 2008, 180:267-272.
16. Choksi S.P., Southall T.D., Bossing T., Edoff K., de Wit E., Fischer B.E., van Steensel B., Micklem G., Brand A.H. Prospero acts as a binary switch between self-renewal and differentiation in Drosophila neural stem cells. Dev. Cell 2006, 11:775-789.
17. Davis R.J., Tavsanli B.C., Dittrich C., Walldorf U., Mardon G. Drosophila retinal homeobox (drx) is not required for establishment of the visual system, but is required for brain and clypeus development. Dev. Biol. 2003, 259:272-287.
18. Dietzl G., Chen D., Schnorrer F., Su K.C., Barinova Y., Fellner M., Gasser B., Kinsey K., Oppel S., Scheiblauer S., Couto A., Marra V., Keleman K., Dickson B.J. A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 2007, 448:151-156.
19. Doe C.Q. Neural stem cells: balancing self-renewal with differentiation. Development 2008, 135:1575-1587.
20. Dominguez M., Campuzano S. asense, a member of the Drosophila achaete-scute complex, is a proneural and neural differentiation gene. EMBO J. 1993, 12:2049-2060.
21. Eggert T., Hauck B., Hildebrandt N., Gehring W.J., Walldorf U. Isolation of a Drosophila homolog of the vertebrate homeobox gene Rx and its possible role in brain and eye development. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:2343-2348.
22. Eisen M.B., Spellman P.T., Brown P.O., Botstein D. Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:14863-14868.
23. Ge H., Liu Z., Church G.M., Vidal M. Correlation between transcriptome and interactome mapping data from Saccharomyces cerevisiae. Nat. Genet. 2001, 29:482-486.
24. Hirata J., Nakagoshi H., Nabeshima Y., Matsuzaki F. Asymmetric segregation of the homeodomain protein Prospero during Drosophila development. Nature 1995, 377:627-630.
25. Hosoya T., Takizawa K., Nitta K., Hotta Y. Glial cells missing: a binary switch between neuronal and glial determination in Drosophila. Cell 1995, 82:1025-1036.
26. Izergina N., Balmer J., Bello B., Reichert H. Postembryonic development of transit amplifying neuroblast lineages in the Drosophila brain. Neural Dev. 2009, 4:44.
27. Jaekel R., Klein T. The Drosophila Notch inhibitor and tumor suppressor gene lethal (2) giant discs encodes a conserved regulator of endosomal trafficking. Dev. Cell 2006, 11:655-669.
28. Jansen R., Greenbaum D., Gerstein M. Relating whole-genome expression data with protein-protein interactions. Genome Res. 2002, 12:37-46.
29. Kenyon K.L., Li D.J., Clouser C., Tran S., Pignoni F. Fly SIX-type homeodomain proteins Sine oculis and Optix partner with different cofactors during eye development. Dev. Dyn. 2005, 234:497-504.
30. Knoblich J.A. Mechanisms of asymmetric stem cell division. Cell 2008, 132:583-597.
31. Knoblich J.A., Jan L.Y., Jan Y.N. Asymmetric segregation of Numb and Prospero during cell division. Nature 1995, 377:624-627.
32. Lee C.Y., Andersen R.O., Cabernard C., Manning L., Tran K.D., Lanskey M.J., Bashirullah A., Doe C.Q. Drosophila Aurora-A kinase inhibits neuroblast self-renewal by regulating aPKC/Numb cortical polarity and spindle orientation. Genes Dev. 2006, 20:3464-3474.
33. Lee C.Y., Robinson K.J., Doe C.Q. Lgl, Pins and aPKC regulate neuroblast self-renewal versus differentiation. Nature 2006, 439:594-598.
34. Lee C.Y., Wilkinson B.D., Siegrist S.E., Wharton R.P., Doe C.Q. Brat is a Miranda cargo protein that promotes neuronal differentiation and inhibits neuroblast self-renewal. Dev. Cell 2006, 10:441-449.
35. Li L., Vaessin H. Pan-neural Prospero terminates cell proliferation during Drosophila neurogenesis. Genes Dev. 2000, 14:147-151.
36. Merkle F.T., Alvarez-Buylla A. Neural stem cells in mammalian development. Curr. Opin. Cell Biol. 2006, 18:704-709.
37. Miller M.R., Robinson K.J., Cleary M.D., Doe C.Q. TU-tagging: cell type-specific RNA isolation from intact complex tissues. Nat. Methods 2009, 6:439-441.
38. Morrison S.J., Kimble J. Asymmetric and symmetric stem-cell divisions in development and cancer. Nature 2006, 441:1068-1074.
39. Ohshiro T., Yagami T., Zhang C., Matsuzaki F. Role of cortical tumour-suppressor proteins in asymmetric division of Drosophila neuroblast. Nature 2000, 408:593-596.
40. Ouyang Y., Petritsch C., Wen H., Jan L., Jan Y.N., Lu B. Dronc caspase exerts a non-apoptotic function to restrain phospho-Numb-induced ectopic neuroblast formation in Drosophila. Development 2011, 138:2185-2196.
41. Parmentier M.L., Woods D., Greig S., Phan P.G., Radovic A., Bryant P., O'Kane C.J. Rapsynoid/partner of inscuteable controls asymmetric division of larval neuroblasts in Drosophila. J. Neurosci. 2000, 20:RC84.
42. Peng C.Y., Manning L., Albertson R., Doe C.Q. The tumour-suppressor genes lgl and dlg regulate basal protein targeting in Drosophila neuroblasts. Nature 2000, 408:596-600.
43. Robinow S., White K. The locus elav of Drosophila melanogaster is expressed in neurons at all developmental stages. Dev. Biol. 1988, 126:294-303.
44. Rolls M.M., Albertson R., Shih H.P., Lee C.Y., Doe C.Q. Drosophila aPKC regulates cell polarity and cell proliferation in neuroblasts and epithelia. J. Cell Biol. 2003, 163:1089-1098.
45. Sabherwal N., Tsutsui A., Hodge S., Wei J., Chalmers A.D., Papalopulu N. The apicobasal polarity kinase aPKC functions as a nuclear determinant and regulates cell proliferation and fate during Xenopus primary neurogenesis. Development 2009, 136:2767-2777.
46. Seimiya M., Gehring W.J. The Drosophila homeobox gene optix is capable of inducing ectopic eyes by an eyeless-independent mechanism. Development 2000, 127:1879-1886.
47. Southall T.D., Brand A.H. Neural stem cell transcriptional networks highlight genes essential for nervous system development. EMBO J. 2009, 28:3799-3807.
48. Spana E.P., Doe C.Q. The prospero transcription factor is asymmetrically localized to the cell cortex during neuroblast mitosis in Drosophila. Development 1995, 121:3187-3195.
49. Toy J., Yang J.M., Leppert G.S., Sundin O.H. The optx2 homeobox gene is expressed in early precursors of the eye and activates retina-specific genes. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:10643-10648.
50. Uv A.E., Harrison E.J., Bray S.J. Tissue-specific splicing and functions of the Drosophila transcription factor Grainyhead. Mol. Cell. Biol. 1997, 17:6727-6735.
51. van Noort V., Snel B., Huynen M.A. Predicting gene function by conserved co-expression. Trends Genet. 2003, 19:238-242.
52. Viktorin G., Riebli N., Popkova A., Giangrande A., Reichert H. Multipotent neural stem cells generate glial cells of the central complex through transit amplifying intermediate progenitors in Drosophila brain development. Dev. Biol. 2011, 356:553-565.
53. Wallace K., Liu T.H., Vaessin H. The pan-neural bHLH proteins DEADPAN and ASENSE regulate mitotic activity and cdk inhibitor dacapo expression in the Drosophila larval optic lobes. Genesis 2000, 26:77-85.
54. Wang H., Somers G.W., Bashirullah A., Heberlein U., Yu F., Chia W. Aurora-A acts as a tumor suppressor and regulates self-renewal of Drosophila neuroblasts. Genes Dev. 2006, 20:3453-3463.
55. Weng M., Golden K.L., Lee C.Y. dFezf/Earmuff maintains the restricted developmental potential of intermediate neural progenitors in Drosophila. Dev. Cell 2010, 18:126-135.
56. Xiong W.C., Okano H., Patel N.H., Blendy J.A., Montell C. Repo encodes a glial-specific homeo domain protein required in the Drosophila nervous system. Genes Dev. 1994, 8:981-994.