Transient nuclear Prospero induces neural progenitor quiescence

eLife

Volumn 3, Issue October2014, 2014, Pages 1-12

  Lai, Sen Lin ^a   Doe, Chris Q ^a  

^a UNIVERSITY OF OREGON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROSPERO PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; DROSOPHILA PROTEIN; NERVE PROTEIN; NUCLEAR PROTEIN; PROS PROTEIN, DROSOPHILA;

ARTICLE; CELL DIFFERENTIATION; CELL FUNCTION; CELL PROLIFERATION; CELL QUIESCENCE; CONTROLLED STUDY; DROSOPHILA; EMBRYO; NEURAL STEM CELL; NEUROBLAST; NONHUMAN; PROTEIN EXPRESSION; SCORING SYSTEM; ANIMAL; BRAIN; CELL LINEAGE; CELL NUCLEUS; CYTOLOGY; DROSOPHILA MELANOGASTER; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LARVA; METABOLISM; TEMPERATURE;

PROSPERO;

ANIMALS; BRAIN; CELL DIFFERENTIATION; CELL LINEAGE; CELL NUCLEUS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; LARVA; NERVE TISSUE PROTEINS; NEURAL STEM CELLS; NUCLEAR PROTEINS; TEMPERATURE; TRANSCRIPTION FACTORS;

EID: 84931864114     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.03363     Document Type: Article

References (54)

1. Ashraf SI, Ganguly A, Roote J, Ip YT. 2004. Worniu, a Snail family zinc-finger protein, is required for brain development in Drosophila. Developmental Dynamics 231:379-386. doi: 10.1002/dvdy.20130.
2. Bayraktar OA, Boone JQ, Drummond ML, Doe CQ. 2010. Drosophila type II neuroblast lineages keep Prospero levels low to generate large clones that contribute to the adult brain central complex. Neural Development 5:26. doi: 10.1186/1749-8104-5-26.
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. doi: 10.1242/dev.02429.
4. 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. doi: 10.1016/j.cell.2006.01.038.
5. Bi X, Jones T, Abbasi F, Lee H, Stultz B, Hursh DA, Mortin MA. 2005. Drosophila caliban, a nuclear export mediator, can function as a tumor suppressor in human lung cancer cells. Oncogene 24:8229-8239. doi: 10.1038/sj.onc.1208962.
6. 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.
7. Britton JS, Edgar BA. 1998. Environmental control of the cell cycle in Drosophila: nutrition activates mitotic and endoreplicative cells by distinct mechanisms. Development 125:2149-2158.
8. Broadus J, Doe CQ. 1997. Extrinsic cues, intrinsic cues and microfilaments regulate asymmetric protein localization in Drosophila neuroblasts. Current Biology 7:827-835. doi: 10.1016/S0960-9822(06)00370-8.
9. Broadus J, Fuerstenberg S, Doe CQ. 1998. Staufen-dependent localization of prospero mRNA contributes to neuroblast daughter-cell fate. Nature 391:792-795. doi: 10.1038/35861.
10. Cabernard C, Doe CQ. 2009. Apical/basal spindle orientation is required for neuroblast homeostasis and neuronal differentiation in Drosophila. Developmental Cell 17:134-141. doi: 10.1016/j.devcel.2009.06.009.
11. Caldwell MC, Datta S. 1998. Expression of cyclin E or DP/E2F rescues the G1 arrest of trol mutant neuroblasts in the Drosophila larval central nervous system. Mechanisms of Development 79:121-130. doi: 10.1016/S0925-4773(98)00178-6.
12. Carney TD, Struck AJ, Doe CQ. 2013. midlife crisis encodes a conserved zinc-finger protein required to maintain neuronal differentiation in Drosophila. Development 140:4155-4164. doi: 10.1242/dev.093781.
13. Chai PC, Liu Z, Chia W, Cai Y. 2013. Hedgehog signaling acts with the temporal cascade to promote neuroblast cell cycle exit. PLOS Biology 11:e1001494. doi: 10.1371/journal.pbio.1001494.
14. Chell JM, Brand AH. 2010. Nutrition-responsive glia control exit of neural stem cells from quiescence. Cell 143:1161-1173. doi: 10.1016/j.cell.2010.12.007.
15. Chen X, Patel TP, Simirskii VI, Duncan MK. 2008a. PCNA interacts with Prox1 and represses its transcriptional activity. Molecular Vision 14:2076-2086.
16. Chen X, Taube JR, Simirskii VI, Patel TP, Duncan MK. 2008b. Dual roles for Prox1 in the regulation of the chicken betaB1-crystallin promoter. Investigative Ophthalmology & Visual Science 49:1542-1552. doi: 10.1167/iovs.07-1300.
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. Developmental Cell 11:775-789. doi: 10.1016/j.devcel.2006.09.015.
18. Cooper MT, Tyler DM, Furriols M, Chalkiadaki A, Delidakis C, Bray S. 2000. Spatially restricted factors cooperate with notch in the regulation of Enhancer of split genes. Developmental Biology 221:390-403. doi: 10.1006/dbio.2000.9691.
19. Datta S. 1995. Control of proliferation activation in quiescent neuroblasts of the Drosophila central nervous system. Development 121:1173-1182.
20. Doe CQ. 2008. Neural stem cells: balancing self-renewal with differentiation. Development 135:1575-1587. doi: 10.1242/dev.014977.
21. Doe CQ, Fuerstenberg S, Peng CY. 1998. Neural stem cells: from fly to vertebrates. Journal of Neurobiology 36:111-127. doi: 10.1002/(SICI)1097-4695(199808)36:23.0.CO;2-4.
22. Dyer MA. 2003. Regulation of proliferation, cell fate specification and differentiation by the homeodomain proteins Prox1, Six3, and Chx10 in the developing retina. Cell Cycle 2:350-357. doi: 10.4161/cc.2.4.429.
23. Ebens AJ, Garren H, Cheyette BN, Zipursky SL. 1993. The Drosophila anachronism locus: a glycoprotein secreted by glia inhibits neuroblast proliferation. Cell 74:15-27. doi: 10.1016/0092-8674(93)90291-W.
24. Egger B, Chell JM, Brand AH. 2008. Insights into neural stem cell biology from flies. Philosophical Transactions of the Royal Society of London Series B, Biological Sciences 363:39-56. doi: 10.1098/rstb.2006.2011.
25. Foskolou IP, Stellas D, Rozani I, Lavigne MD, Politis PK. 2013. Prox1 suppresses the proliferation of neuroblastoma cells via a dual action in p27-Kip1 and Cdc25A. Oncogene 32:947-960. doi: 10.1038/onc.2012.129.
26. Freeman MR, Doe CQ. 2001. Asymmetric Prospero localization is required to generate mixed neuronal/glial lineages in the Drosophila CNS. Development 128:4103-4112.
27. Griffiths RL, Hidalgo A. 2004. Prospero maintains the mitotic potential of glial precursors enabling them to respond to neurons. The EMBO Journal 23:2440-2450. doi: 10.1038/sj.emboj.7600258.
28. Higashijima S, Shishido E, Matsuzaki M, Saigo K. 1996. eagle, a member of the steroid receptor gene superfamily, is expressed in a subset of neuroblasts and regulates the fate of their putative progeny in the Drosophila CNS. Development 122:527-536.
29. Hirata J, Nakagoshi H, Nabeshima Y, Matsuzaki F. 1995. Asymmetric segregation of the homeodomain protein Prospero during Drosophila development. Nature 377:627-630. doi: 10.1038/377627a0.
30. Homem CC, Knoblich JA. 2012. Drosophila neuroblasts: a model for stem cell biology. Development 139:4297-4310. doi: 10.1242/dev.080515.
31. Ikeshima-Kataoka H, Skeath JB, Nabeshima Y, Doe CQ, Matsuzaki F. 1997. Miranda directs Prospero to a daughter cell during Drosophila asymmetric divisions. Nature 390:625-629. doi: 10.1038/37641.
32. Ito K, Hotta Y. 1992. Proliferation pattern of postembryonic neuroblasts in the brain of Drosophila melanogaster. Developmental Biology 149:134-148. doi: 10.1016/0012-1606(92)90270-Q.
33. Karcavich R, Doe CQ. 2005. Drosophila neuroblast 7-3 cell lineage: a model system for studying programmed cell death, Notch/Numb signaling, and sequential specification of ganglion mother cell identity. Journal of Comparative Neurology 481:240-251. doi: 10.1002/cne.20371.
34. 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. Developmental Cell 23:849-857. doi: 10.1016/j.devcel.2012.09.007.
35. 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. Developmental Cell 10:441-449. doi: 10.1016/j.devcel.2006.01.017.
36. Li L, Vaessin H. 2000. Pan-neural Prospero terminates cell proliferation during Drosophila neurogenesis. Genes & Development 14:147-151.
37. Maurange C, Gould AP. 2005. Brainy but not too brainy: starting and stopping neuroblast divisions in Drosophila. Trends in Neuroscience 28:30-36. doi: 10.1016/j.tins.2004.10.009.
38. Maurange C, Cheng L, Gould AP. 2008. Temporal transcription factors and their targets schedule the end of neural proliferation in Drosophila. Cell 133:891-902. doi: 10.1016/j.cell.2008.03.034.
39. McGuire SE, Le PT, Osborn AJ, Matsumoto K, Davis RL. 2003. Spatiotemporal rescue of memory dysfunction in Drosophila. Science 302:1765-1768. doi: 10.1126/science.1089035.
40. Robinow S, White K. 1988. The locus elav of Drosophila melanogaster is expressed in neurons at all developmental stages. Developmental Biology 126:294-303. doi: 10.1016/0012-1606(88)90139-X.
41. Schuldt AJ, Adams JH, Davidson CM, Micklem DR, Haseloff J, St Johnston D, Brand AH. 1998. Miranda mediates asymmetric protein and RNA localization in the developing nervous system. Genes & Development 12:1847-1857. doi: 10.1101/gad.12.12.1847.
42. Shen CP, Knoblich JA, Chan YM, Jiang MM, Jan LY, Jan YN. 1998. Miranda as a multidomain adapter linking apically localized inscuteable and basally localized Staufen and Prospero during asymmetric cell division in Drosophila. Genes & Development 12:1837-1846. doi: 10.1101/gad.12.12.1837.
43. Sousa-Nunes R, Cheng LY, Gould AP. 2010. Regulating neural proliferation in the Drosophila CNS. Current Opinion in Neurobiology 20:50-57. doi: 10.1016/j.conb.2009.12.005.
44. Sousa-Nunes R, Yee LL, Gould AP. 2011. Fat cells reactivate quiescent neuroblasts via TOR and glial insulin relays in Drosophila. Nature 471:508-512. doi: 10.1038/nature09867.
45. Spana EP, Doe CQ. 1995. The prospero transcription factor is asymmetrically localized to the cell cortex during neuroblast mitosis in Drosophila. Development 121:3187-3195.
46. Takahashi M, Yoshimoto T, Shimoda M, Kono T, Koizumi M, Yazumi S, Shimada Y, Doi R, Chiba T, Kubo H. 2006. Loss of function of the candidate tumor suppressor prox1 by RNA mutation in human cancer cells. Neoplasia 8:1003-1010. doi: 10.1593/neo.06595.
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 Biology 8:R145. doi: 10.1186/gb-2007-8-7-r145.
48. Truman JW, Bate M. 1988. Spatial and temporal patterns of neurogenesis in the central nervous system of Drosophila melanogaster. Developmental Biology 125:145-157. doi: 10.1016/0012-1606(88)90067-X.
49. Tsuji T, Hasegawa E, Isshiki T. 2008. Neuroblast entry into quiescence is regulated intrinsically by the combined action of spatial Hox proteins and temporal identity factors. Development 135:3859-3869. doi: 10.1242/dev.025189.
50. Ulvklo C, MacDonald R, Bivik C, Baumgardt M, Karlsson D, Thor S. 2012. Control of neuronal cell fate and number by integration of distinct daughter cell proliferation modes with temporal progression. Development 139:678-689. doi: 10.1242/dev.074500.
51. Wech I, Bray S, Delidakis C, Preiss A. 1999. Distinct expression patterns of different enhancer of split bHLH genes during embryogenesis of Drosophila melanogaster. Development Genes and Evolution 209:370-375. doi: 10.1007/s004270050266.
52. Weng R, Cohen SM. 2012. Drosophila miR-124 regulates neuroblast proliferation through its target anachronism. Development 139:1427-1434. doi: 10.1242/dev.075143.
53. Xiong WC, Okano H, Patel NH, Blendy JA, Montell C. 1994. repo encodes a glial-specific homeo domain protein required in the Drosophila nervous system. Genes & Development 8:981-994. doi: 10.1101/gad.8.8.981.
54. Zhu CC, Boone JQ, Jensen PA, Hanna S, Podemski L, Locke J, Doe CQ, O'Connor MB. 2008. Drosophila Activin-and the Activin-like product Dawdle function redundantly to regulate proliferation in the larval brain. Development 135:513-521. doi: 10.1242/dev.010876.