Steroid hormone induction of temporal gene expression in drosophila brain neuroblasts generates neuronal and glial diversity

eLife

Volumn 6, Issue , 2017, Pages

  Syed, Mubarak Hussain ^a   Mark, Brandon ^a   Doe, Chris Q ^a  

^a UNIVERSITY OF OREGON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ECDYSONE; STEROID HORMONE; TRANSCRIPTION FACTOR;

ADULT; ARTICLE; CARCINOGENESIS; CELL CYCLE PROGRESSION; CELL DIFFERENTIATION; CELL PROLIFERATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DROSOPHILA; EMBRYO DEVELOPMENT; GENE EXPRESSION; GENETIC VARIABILITY; IMAGE ANALYSIS; IMMUNOHISTOCHEMISTRY; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NEUROBLAST; NONHUMAN; NUCLEAR REPROGRAMMING; RNA ISOLATION; RNA SEQUENCE; ANIMAL; BRAIN; CYTOLOGY; DRUG EFFECTS; EMBRYOLOGY; GENE EXPRESSION REGULATION; METABOLISM; PHYSIOLOGY;

ANIMALS; BRAIN; CELL DIFFERENTIATION; DROSOPHILA; ECDYSONE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; NEURAL STEM CELLS;

EID: 85018305000     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.26287     Document Type: Article

References (77)

1. Awasaki T, Lee T. 2011. Orphan nuclear receptors control neuronal remodeling during fly metamorphosis. Nature Neuroscience 14:6–7. doi: 10.1038/nn0111-6, PMID: 21187848
2. Baehrecke EH. 1996. Ecdysone signaling cascade and regulation of Drosophila metamorphosis. Archives of Insect Biochemistry and Physiology 33:231–244. doi: 10.1002/(SICI)1520-6327(1996)33:3/4<231::AIDARCH5>3.0.CO;2-V, PMID: 8913033
3. 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. doi: 10.1016/j.neuron.2005.08.037, PMID: 16242406
4. Baumgardt M, Karlsson D, Terriente J, Díaz-Benjumea FJ, Thor S. 2009. Neuronal subtype specification within a lineage by opposing temporal feed-forward loops. Cell 139:969–982. doi: 10.1016/j.cell.2009.10.032, PMID: 1 9945380
5. Bayraktar OA, Doe CQ. 2013. Combinatorial temporal patterning in progenitors expands neural diversity. Nature 498:449–455. doi: 10.1038/nature12266, PMID: 23783519
6. Bello BC, Izergina N, Caussinus E, Reichert H. 2008. Amplification of neural stem cell proliferation by intermediate progenitor cells in Drosophila brain development. Neural Development 3:5. doi: 10.1186/17498104-3-5, PMID: 18284664
7. Benito-Sipos J, Ulvklo C, Gabilondo H, Baumgardt M, Angel A, Torroja L, Thor S. 2011. Seven up acts as a temporal factor during two different stages of neuroblast 5-6 development. Development 138:5311–5320. doi: 10.1242/dev.070946, PMID: 22071101
8. Bertet C, Li X, Erclik T, Cavey M, Wells B, Desplan C. 2014. Temporal patterning of neuroblasts controls Notchmediated cell survival through regulation of hid or reaper. Cell 158:1173–1186. doi: 10.1016/j.cell.2014.07.045, PMID: 25171415
9. Boone JQ, Doe CQ. 2008. Identification of Drosophila type II neuroblast lineages containing transit amplifying ganglion mother cells. Developmental Neurobiology 68:1185–1195. doi: 10.1002/dneu.20648, PMID: 18548484
10. Boulanger A, Clouet-Redt C, Farge M, Flandre A, Guignard T, Fernando C, Juge F, Dura JM. 2011. ftz-f1 and Hr39 opposing roles on EcR expression during Drosophila mushroom body neuron remodeling. Nature Neuroscience 14:37–44. doi: 10.1038/nn.2700, PMID: 21131955
11. 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. Developmental Cell 14:535–546. doi: 10. 1016/j.devcel.2008.03.004, PMID: 18342578
12. Brown HL, Cherbas L, Cherbas P, Truman JW. 2006. Use of time-lapse imaging and dominant negative receptors to dissect the steroid receptor control of neuronal remodeling in Drosophila. Development 133:275–285. doi: 10.1242/dev.02191, PMID: 16354717
13. Caussinus E, Hirth F. 2007. Asymmetric stem cell division in development and cancer. In: Progress in Molecular and Subcellular Biology Vol.45. p. 205–225. doi: 10.1007/978-3-540-69161-7_9
14. 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, PMID: 23468593
15. Cui X, Doe CQ. 1992. Ming is expressed in neuroblast sublineages and regulates gene expression in the Drosophila central nervous system. Development 116:943–952. PMID: 1339340
16. Doe CQ. 2008. Neural stem cells: balancing self-renewal with differentiation. Development 135:1575–1587. doi: 10.1242/dev.014977, PMID: 18356248
17. Enriquez J, Venkatasubramanian L, Baek M, Peterson M, Aghayeva U, Mann RS. 2015. Specification of individual adult motor neuron morphologies by combinatorial transcription factor codes. Neuron 86:955–970. doi: 10. 1016/j.neuron.2015.04.011, PMID: 25959734
18. Faunes F, Larraín J. 2016. Conservation in the involvement of heterochronic genes and hormones during developmental transitions. Developmental Biology 416:3–17. doi: 10.1016/j.ydbio.2016.06.013, PMID: 27297 887
19. Garen A, Kauvar L, Lepesant JA. 1977. Roles of ecdysone in Drosophila development. PNAS 74:5099–5103. doi: 10.1073/pnas.74.11.5099, PMID: 16592466
20. Gay L, Miller MR, Ventura PB, Devasthali V, Vue Z, Thompson HL, Temple S, Zong H, Cleary MD, Stankunas K, Doe CQ. 2013. Mouse TU tagging: a chemical/genetic intersectional method for purifying cell type-specific nascent RNA. Genes & Development 27:98–115. doi: 10.1101/gad.205278.112, PMID: 23307870
21. Gay L, Karfilis KV, Miller MR, Doe CQ, Stankunas K. 2014. Applying thiouracil tagging to mouse transcriptome analysis. Nature Protocols 9:410–420. doi: 10.1038/nprot.2014.023, PMID: 24457332
22. Gissendanner CR, Crossgrove K, Kraus KA, Maina CV, Sluder AE. 2004. Expression and function of conserved nuclear receptor genes in Caenorhabditis elegans. Developmental Biology 266:399–416. doi: 10.1016/j.ydbio. 2003.10.014, PMID: 14738886
23. Grosskortenhaus R, Pearson BJ, Marusich A, Doe CQ. 2005. Regulation of temporal identity transitions in Drosophila neuroblasts. Developmental Cell 8:193–202. doi: 10.1016/j.devcel.2004.11.019, PMID: 15691761
24. Grosskortenhaus R, Robinson KJ, Doe CQ. 2006. Pdm and Castor specify late-born motor neuron identity in the NB7-1 lineage. Genes & Development 20:2618–2627. doi: 10.1101/gad.1445306, PMID: 16980589
25. Gunnar E, Bivik C, Starkenberg A, Thor S. 2016. Sequoia controls the type I>0 daughter proliferation switch in the developing Drosophila nervous system. Development 143:3774–3784. doi: 10.1242/dev.139998, PMID: 27578794
26. Hasegawa E, Kitada Y, Kaido M, Takayama R, Awasaki T, Tabata T, Sato M. 2011. Concentric zones, cell migration and neuronal circuits in the Drosophila visual center. Development 138:983–993. doi: 10.1242/dev. 058370, PMID: 21303851
27. Homem CC, Reichardt I, Berger C, Lendl T, Knoblich JA. 2013. Long-term live cell imaging and automated 4D analysis of Drosophila neuroblast lineages. PLoS One 8:e79588. doi: 10.1371/journal.pone.0079588, PMID: 24260257
28. Homem CC, Steinmann V, Burkard TR, Jais A, Esterbauer H, Knoblich JA. 2014. Ecdysone and mediator change energy metabolism to terminate proliferation in Drosophila neural stem cells. Cell 158:874–888. doi: 10.1016/j. cell.2014.06.024, PMID: 25126791
29. Homem CC, Repic M, Knoblich JA. 2015. Proliferation control in neural stem and progenitor cells. Nature Reviews Neuroscience 16:647–659. doi: 10.1038/nrn4021, PMID: 26420377
30. Isshiki T, Pearson B, Holbrook S, Doe CQ. 2001. Drosophila neuroblasts sequentially express transcription factors which specify the temporal identity of their neuronal progeny. Cell 106:511–521. doi: 10.1016/S0092-8674(01) 00465-2, PMID: 11525736
31. Ito K, Awasaki T. 2008. Clonal unit architecture of the adult fly brain. Advances in Experimental Medicine and Biology 628:137–158. doi: 10.1007/978-0-387-78261-4_9, PMID: 18683643
32. Ito M, Masuda N, Shinomiya K, Endo K, Ito K. 2013. Systematic analysis of neural projections reveals clonal composition of the Drosophila brain. Current Biology 23:644–655. doi: 10.1016/j.cub.2013.03.015, PMID: 23541729
33. Jiang Y, Reichert H. 2014. Drosophila neural stem cells in brain development and tumor formation. Journal of Neurogenetics 28:181–189. doi: 10.3109/01677063.2014.898639, PMID: 24766377
34. Kanai MI, Okabe M, Hiromi Y. 2005. Seven-up Controls switching of transcription factors that specify temporal identities of Drosophila neuroblasts. Developmental Cell 8:203–213. doi: 10.1016/j.devcel.2004.12.014, PMID: 15691762
35. Kao CF, Yu HH, He Y, Kao JC, Lee T. 2012. Hierarchical deployment of factors regulating temporal fate in a diverse neuronal lineage of the Drosophila central brain. Neuron 73:677–684. doi: 10.1016/j.neuron.2011.12. 018, PMID: 22365543
36. King-Jones K, Thummel CS. 2005. Developmental biology. less steroids make bigger flies. Science 310:630–631. doi: 10.1126/science.1120410, PMID: 16254176
37. Kiss I, Bencze G, Fekete E, Fodor A, Gausz J, Maróy P, Szabad J, Szidonya J. 1976. Isolation and characterization of X-linked lethal mutants affecting differentiation of the imaginal discs in Drosophila melanogaster. Theoretical and Applied Genetics 48:217–226. doi: 10.1007/BF00281284, PMID: 24413794
38. Kohwi M, Doe CQ. 2013. Temporal fate specification and neural progenitor competence during development. Nature Reviews Neuroscience 14:823–838. doi: 10.1038/nrn3618, PMID: 24400340
39. Kozlova T, Thummel CS. 2000. Steroid regulation of postembryonic development and reproduction in Drosophila. Trends in Endocrinology & Metabolism 11:276–280. doi: 10.1016/S1043-2760(00)00282-4, PMID: 10920384
40. Kucherenko MM, Shcherbata HR. 2013. Steroids as external temporal codes act via microRNAs and cooperate with cytokines in differential neurogenesis. Fly 7:173–183. doi: 10.4161/fly.25241, PMID: 23839338
41. Lai SL, Awasaki T, Ito K, Lee T. 2008. Clonal analysis of Drosophila antennal lobe neurons: diverse neuronal architectures in the lateral neuroblast lineage. Development 135:2883–2893. doi: 10.1242/dev.024380, PMID: 1 8653555
42. Lam G, Hall BL, Bender M, Thummel CS. 1999. DHR3 is required for the prepupal-pupal transition and differentiation of adult structures during Drosophila metamorphosis. Developmental Biology 212:204–216. doi: 10.1006/dbio.1999.9343, PMID: 10419696
43. Lee T, Marticke S, Sung C, Robinow S, Luo L. 2000. Cell-autonomous requirement of the USP/EcR-B ecdysone receptor for mushroom body neuronal remodeling in Drosophila. Neuron 28:807–818. doi: 10.1016/S08966273(00)00155-0, PMID: 11163268
44. Lee CY, Andersen RO, Cabernard C, Manning L, Tran KD, Lanskey MJ, Bashirullah A, Doe CQ. 2006. Drosophila Aurora-A kinase inhibits neuroblast self-renewal by regulating aPKC/Numb cortical polarity and spindle orientation. Genes & Development 20:3464–3474. doi: 10.1101/gad.1489406, PMID: 17182871
45. Li X, Erclik T, Bertet C, Chen Z, Voutev R, Venkatesh S, Morante J, Celik A, Desplan C. 2013. Temporal patterning of Drosophila medulla neuroblasts controls neural fates. Nature 498:456–462. doi: 10.1038/nature12319, PMID: 23783517
46. Liu Z, Yang CP, Sugino K, Fu CC, Liu LY, Yao X, Lee LP, Lee T. 2015. Opposing intrinsic temporal gradients guide neural stem cell production of varied neuronal fates. Science 350:317–320. doi: 10.1126/science.aad1886, PMID: 26472907
47. Love MI, Huber W, Anders S. 2014. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology 15:550. doi: 10.1186/s13059-014-0550-8, PMID: 25516281
48. Mattar P, Ericson J, Blackshaw S, Cayouette M. 2015. A conserved regulatory logic controls temporal identity in mouse neural progenitors. Neuron 85:497–504. doi: 10.1016/j.neuron.2014.12.052, PMID: 25654255
49. Maurange C, Gould AP. 2005. Brainy but not too brainy: starting and stopping neuroblast divisions in Drosophila. Trends in Neurosciences 28:30–36. doi: 10.1016/j.tins.2004.10.009, PMID: 15626494
50. 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, PMID: 18510932
51. Mettler U, Vogler G, Urban J. 2006. Timing of identity: spatiotemporal regulation of hunchback in neuroblast lineages of Drosophila by seven-up and prospero. Development 133:429–437. doi: 10.1242/dev.02229, PMID: 16396905
52. Miller MR, Robinson KJ, Cleary MD, Doe CQ. 2009. TU-tagging: cell type-specific RNA isolation from intact complex tissues. Nature Methods 6:439–441. doi: 10.1038/nmeth.1329, PMID: 19430475
53. Mlodzik M, Hiromi Y, Weber U, Goodman CS, Rubin GM. 1990. The Drosophila seven-up gene, a member of the steroid receptor gene superfamily, controls photoreceptor cell fates. Cell 60:211–224. doi: 10.1016/0092-8674 (90)90737-Y, PMID: 2105166
54. Moris-Sanz M, Estacio-Gómez A, Alvarez-Rivero J, Díaz-Benjumea FJ. 2014. Specification of neuronal subtypes by different levels of hunchback. Development 141:4366–4374. doi: 10.1242/dev.113381, PMID: 25344076
55. Naka H, Nakamura S, Shimazaki T, Okano H. 2008. Requirement for COUP-TFI and II in the temporal specification of neural stem cells in CNS development. Nature Neuroscience 11:1014–1023. doi: 10.1038/nn. 2168, PMID: 19160499
56. Narbonne-Reveau K, Lanet E, Dillard C, Foppolo S, Chen CH, Parrinello H, Rialle S, Sokol NS, Maurange C. 2016. Neural stem cell-encoded temporal patterning delineates an early window of malignant susceptibility in Drosophila. eLife 5: e13463. doi: 10.7554/eLife.13463, PMID: 27296804
57. Novotny T, Eiselt R, Urban J. 2002. Hunchback is required for the specification of the early sublineage of neuroblast 7-3 in the Drosophila central nervous system. Development 129:1027–1036. PMID: 11861485
58. Pearson BJ, Doe CQ. 2003. Regulation of neuroblast competence in Drosophila. Nature 425:624–628. doi: 10. 1038/nature01910, PMID: 14534589
59. Powsner L. 1935. The effects of temperature on the durations of the developmental stages of Drosophila melanogaster. Physiological Zoology 8:474–520. doi: 10.1086/physzool.8.4.30151263
60. Rossi AM, Fernandes VM, Desplan C. 2017. Timing temporal transitions during brain development. Current Opinion in Neurobiology 42:84–92. doi: 10.1016/j.conb.2016.11.010, PMID: 27984764
61. Schubiger M, Wade AA, Carney GE, Truman JW, Bender M. 1998. Drosophila EcR-B ecdysone receptor isoforms are required for larval molting and for neuron remodeling during metamorphosis. Development 125:2053– 2062. PMID: 9570770
62. Skeath JB, Thor S. 2003. Genetic control of Drosophila nerve cord development. Current Opinion in Neurobiology 13:8–15. doi: 10.1016/S0959-4388(03)00007-2, PMID: 12593977
63. Stratmann J, Gabilondo H, Benito-Sipos J, Thor S. 2016. Neuronal cell fate diversification controlled by subtemporal action of kruppel. eLife 5:e19311. doi: 10.7554/eLife.19311, PMID: 27740908
64. Suzuki T, Kaido M, Takayama R, Sato M. 2013. A temporal mechanism that produces neuronal diversity in the Drosophila visual center. Developmental Biology 380:12–24. doi: 10.1016/j.ydbio.2013.05.002, PMID: 23665475
65. Thummel CS. 2001. Molecular mechanisms of developmental timing in C. elegans and Drosophila. Developmental Cell 1:453–465. doi: 10.1016/S1534-5807(01)00060-0, PMID: 11703937
66. Tran KD, Doe CQ. 2008. Pdm and Castor close successive temporal identity windows in the NB3-1 lineage. Development 135:3491–3499. doi: 10.1242/dev.024349, PMID: 18832394
67. 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, PMID: 3119399
68. Wang YC, Yang JS, Johnston R, Ren Q, Lee YJ, Luan H, Brody T, Odenwald WF, Lee T. 2014. Drosophila intermediate neural progenitors produce lineage-dependent related series of diverse neurons. Development 141:253–258. doi: 10.1242/dev.103069, PMID: 24306106
69. Wu TD, Nacu S. 2010. Fast and SNP-tolerant detection of complex variants and splicing in short reads. Bioinformatics 26:873–881. doi: 10.1093/bioinformatics/btq057, PMID: 20147302
70. Yamanaka N, Rewitz KF, O’Connor MB. 2013. Ecdysone control of developmental transitions: lessons from Drosophila research. Annual Review of Entomology 58:497–516. doi: 10.1146/annurev-ento-120811-153608, PMID: 23072462
71. Yu HH, Lee T. 2007. Neuronal temporal identity in post-embryonic Drosophila brain. Trends in Neurosciences 30: 520–526. doi: 10.1016/j.tins.2007.07.003, PMID: 17825435
72. Yu HH, Kao CF, He Y, Ding P, Kao JC, Lee T. 2010. A complete developmental sequence of a Drosophila neuronal lineage as revealed by twin-spot MARCM. PLoS Biology 8:e1000461. doi: 10.1371/journal.pbio. 1000461, PMID: 20808769
73. Yu HH, Awasaki T, Schroeder MD, Long F, Yang JS, He Y, Ding P, Kao JC, Wu GY, Peng H, Myers G, Lee T. 2013. Clonal development and organization of the adult Drosophila central brain. Current Biology 23:633–643. doi: 10.1016/j.cub.2013.02.057, PMID: 23541733
74. Yu F, Schuldiner O. 2014. Axon and dendrite pruning in Drosophila. Current Opinion in Neurobiology 27:192– 198. doi: 10.1016/j.conb.2014.04.005, PMID: 24793180
75. Zelhof AC, Yao TP, Chen JD, Evans RM, McKeown M. 1995. Seven-up inhibits ultraspiracle-based signaling pathways in vitro and in vivo. Molecular and Cellular Biology 15:6736–6745. doi: 10.1128/MCB.15.12.6736, PMID: 8524239
76. Zhou B, Williams DW, Altman J, Riddiford LM, Truman JW. 2009. Temporal patterns of broad isoform expression during the development of neuronal lineages in Drosophila. Neural Development 4:39. doi: 10.1186/17498104-4-39, PMID: 19883497
77. Zhu S, Lin S, Kao CF, Awasaki T, Chiang AS, Lee T. 2006. Gradients of the Drosophila Chinmo BTB-zinc finger protein govern neuronal temporal identity. Cell 127:409–422. doi: 10.1016/j.cell.2006.08.045, PMID: 17055440