1932

Abstract

A small pool of neural progenitors generates the vast diversity of cell types in the CNS. Spatial patterning specifies progenitor identity, followed by temporal patterning within progenitor lineages to expand neural diversity. Recent work has shown that in , all neural progenitors (neuroblasts) sequentially express temporal transcription factors (TTFs) that generate molecular and cellular diversity. Embryonic neuroblasts use a lineage-intrinsic cascade of five TTFs that switch nearly every neuroblast cell division; larval optic lobe neuroblasts also use a rapid cascade of five TTFs, but the factors are completely different. In contrast, larval central brain neuroblasts undergo a major molecular transition midway through larval life, and this transition is regulated by a lineage-extrinsic cue (ecdysone hormone signaling). Overall, every neuroblast lineage uses a TTF cascade to generate diversity, illustrating the widespread importance of temporal patterning.

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2017-10-06
2024-04-16
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Literature Cited

  1. Allan DW, Thor S. 2015. Transcriptional selectors, masters, and combinatorial codes: regulatory principles of neural subtype specification. Wiley Interdiscip. Rev. Dev. Biol. 4:505–28 [Google Scholar]
  2. Almeida MS, Bray SJ. 2005. Regulation of post-embryonic neuroblasts by Drosophila Grainyhead. Mech. Dev. 122:1282–93 [Google Scholar]
  3. Alsio JM, Tarchini B, Cayouette M, Livesey FJ. 2013. Ikaros promotes early-born neuronal fates in the cerebral cortex. PNAS 110:E716–25 [Google Scholar]
  4. Apitz H, Salecker I. 2016. Retinal determination genes coordinate neuroepithelial specification and neurogenesis modes in the Drosophila optic lobe. Development 143:2431–42 [Google Scholar]
  5. Awasaki T, Kao CF, Lee YJ, Yang CP, Huang Y. et al. 2014. Making Drosophila lineage-restricted drivers via patterned recombination in neuroblasts. Nat. Neurosci. 17:631–37 [Google Scholar]
  6. Baek M, Enriquez J, Mann RS. 2013. Dual role for Hox genes and Hox co-factors in conferring leg motoneuron survival and identity in Drosophila. Development 140:2027–38 [Google Scholar]
  7. Baek M, Mann RS. 2009. Lineage and birth date specify motor neuron targeting and dendritic architecture in adult Drosophila. J. Neurosci. 29:6904–16 [Google Scholar]
  8. Baumgardt M, Karlsson D, Salmani BY, Bivik C, MacDonald RB. et al. 2014. Global programmed switch in neural daughter cell proliferation mode triggered by a temporal gene cascade. Dev. Cell 30:192–208 [Google Scholar]
  9. Baumgardt M, Karlsson D, Terriente J, Diaz-Benjumea FJ, Thor S. 2009. Neuronal subtype specification within a lineage by opposing temporal feed-forward loops. Cell 139:969–82 [Google Scholar]
  10. Bayraktar OA, Doe CQ. 2013. Combinatorial temporal patterning in progenitors expands neural diversity. Nature 498:445–55 [Google Scholar]
  11. 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 [Google Scholar]
  12. Benito-Sipos J, Estacio-Gomez A, Moris-Sanz M, Baumgardt M, Thor S, Diaz-Benjumea FJ. 2010. A genetic cascade involving klumpfuss, nab and castor specifies the abdominal leucokinergic neurons in the Drosophila CNS. Development 137:3327–36 [Google Scholar]
  13. Benito-Sipos J, Ulvklo C, Gabilondo H, Baumgardt M, Angel A. et al. 2011. Seven up acts as a temporal factor during two different stages of neuroblast 5–6 development. Development 138:5311–20 [Google Scholar]
  14. Berger C, Urban J, Technau GM. 2001. Stage-specific inductive signals in the Drosophila neuroectoderm control the temporal sequence of neuroblast specification. Development 128:3243–51 [Google Scholar]
  15. Bertet C, Li X, Erclik T, Cavey M, Wells B, Desplan C. 2014. Temporal patterning of neuroblasts controls Notch-mediated cell survival through regulation of Hid or Reaper. Cell 158:1173–86 [Google Scholar]
  16. Boglev Y, Wilanowski T, Caddy J, Parekh V, Auden A. et al. 2011. The unique and cooperative roles of the Grainy head-like transcription factors in epidermal development reflect unexpected target gene specificity. Dev. Biol. 349:512–22 [Google Scholar]
  17. Boone JQ, Doe CQ. 2008. Identification of Drosophila type II neuroblast lineages containing transit amplifying ganglion mother cells. Dev. Neurobiol. 68:1185–95 [Google Scholar]
  18. Bossing T, Udolph G, Doe CQ, Technau GM. 1996. The embryonic central nervous system lineages of Drosophila melanogaster. I. Neuroblast lineages derived from the ventral half of the neuroectoderm. Dev. Biol. 179:41–64 [Google Scholar]
  19. 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 14:535–46 [Google Scholar]
  20. Boyan GS, Reichert H. 2011. Mechanisms for complexity in the brain: generating the insect central complex. Trends Neurosci 34:247–57 [Google Scholar]
  21. Brierley DJ, Rathore K, VijayRaghavan K, Williams DW. 2012. Developmental origins and architecture of Drosophila leg motoneurons. J. Comp. Neurol. 520:1629–49 [Google Scholar]
  22. Broadus J, Skeath JB, Spana EP, Bossing T, Technau G, Doe CQ. 1995. New neuroblast markers and the origin of the aCC/pCC neurons in the Drosophila central nervous system. Mech. Dev. 53:393–402 [Google Scholar]
  23. Brody T, Odenwald WF. 2000. Programmed transformations in neuroblast gene expression during Drosophila CNS lineage development. Dev. Biol. 226:34–44 [Google Scholar]
  24. Cenci C, Gould AP. 2005. Drosophila Grainyhead specifies late programmes of neural proliferation by regulating the mitotic activity and Hox-dependent apoptosis of neuroblasts. Development 132:3835–45 [Google Scholar]
  25. Chawla G, Sokol NS. 2012. Hormonal activation of let-7-C microRNAs via EcR is required for adult Drosophila melanogaster morphology and function. Development 139:1788–97 [Google Scholar]
  26. Chu-LaGraff Q, Doe CQ. 1993. Neuroblast specification and formation regulated by wingless in the Drosophila CNS. Science 261:1594–97 [Google Scholar]
  27. Cleary MD, Doe CQ. 2006. Regulation of neuroblast competence: Multiple temporal identity factors specify distinct neuronal fates within a single early competence window. Genes Dev 20:429–34 [Google Scholar]
  28. Clements M, Duncan D, Milbrandt J. 2003. Drosophila NAB (dNAB) is an orphan transcriptional co-repressor required for correct CNS and eye development. Dev. Dyn. 226:67–81 [Google Scholar]
  29. Cui X, Doe CQ. 1992. ming is expressed in neuroblast sublineages and regulates gene expression in the Drosophila central nervous system. Development 116:943–52 [Google Scholar]
  30. Egger B, Boone JQ, Stevens NR, Brand AH, Doe CQ. 2007. Regulation of spindle orientation and neural stem cell fate in the Drosophila optic lobe. Neural Dev 2:1 [Google Scholar]
  31. Elliott J, Jolicoeur C, Ramamurthy V, Cayouette M. 2008. Ikaros confers early temporal competence to mouse retinal progenitor cells. Neuron 60:26–39 [Google Scholar]
  32. 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 86:955–70 [Google Scholar]
  33. Erclik T, Li X, Courgeon M, Bertet C, Chen Z. et al. 2017. Integration of temporal and spatial patterning generates neural diversity. Nature 541:365–70 [Google Scholar]
  34. Eroglu E, Burkard TR, Jiang Y, Saini N, Homem CC. et al. 2014. SWI/SNF complex prevents lineage reversion and induces temporal patterning in neural stem cells. Cell 156:1259–73 [Google Scholar]
  35. Farnsworth DR, Bayraktar OA, Doe CQ. 2015. Aging neural progenitors lose competence to respond to mitogenic Notch signaling. Curr. Biol. 25:3058–68 [Google Scholar]
  36. Gabilondo H, Losada-Perez M, del Saz D, Molina I, Leon Y. et al. 2011. A targeted genetic screen identifies crucial players in the specification of the Drosophila abdominal Capaergic neurons. Mech. Dev. 128:208–21 [Google Scholar]
  37. Greig LC, Woodworth MB, Galazo MJ, Padmanabhan H, Macklis JD. 2013. Molecular logic of neocortical projection neuron specification, development and diversity. Nat. Rev. Neurosci. 14:755–69 [Google Scholar]
  38. Grosskortenhaus R, Pearson BJ, Marusich A, Doe CQ. 2005. Regulation of temporal identity transitions in Drosophila neuroblasts. Dev. Cell 8:193–202 [Google Scholar]
  39. Grosskortenhaus R, Robinson KJ, Doe CQ. 2006. Pdm and Castor specify late-born motor neuron identity in the NB7-1 lineage. Genes Dev 20:2618–27 [Google Scholar]
  40. Hanesch U, Fischbach KF, Heisenberg M. 1989. Neuronal architecture of the central complex in Drosophila melanogaster. Cell Tissue Res. 257:343–66 [Google Scholar]
  41. Hartenstein V, Younossi-Hartenstein A, Lekven A. 1994. Delamination and division in the Drosophila neurectoderm: spatiotemporal pattern, cytoskeletal dynamics, and common control by neurogenic and segment polarity genes. Dev. Biol. 165:480–99 [Google Scholar]
  42. Herrero P, Estacio-Gomez A, Moris-Sanz M, Alvarez-Rivero J, Diaz-Benjumea FJ. 2014. Origin and specification of the brain leucokinergic neurons of Drosophila: similarities to and differences from abdominal leucokinergic neurons. Dev. Dyn. 243:402–14 [Google Scholar]
  43. Hirono K, Kohwi M, Clark MQ, Heckscher EA, Doe CQ. 2017. Hb expression in post-mitotic neurons is dispensible for maintaining neuronal identity, morphology, or behavior. Neural Dev 12:1 [Google Scholar]
  44. Hirono K, Margolis JS, Posakony JW, Doe CQ. 2012. Identification of hunchback cis-regulatory DNA conferring temporal expression in neuroblasts and neurons. Gene Expr. Patterns 12:11–17 [Google Scholar]
  45. 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 106:511–21 [Google Scholar]
  46. Ito K, Awano W, Suzuki K, Hiromi Y, Yamamoto D. 1997. The Drosophila mushroom body is a quadruple structure of clonal units each of which contains a virtually identical set of neurones and glial cells. Development 124:761–71 [Google Scholar]
  47. Ito M, Masuda N, Shinomiya K, Endo K, Ito K. 2013. Systematic analysis of neural projections reveals clonal composition of the Drosophila brain. Curr. Biol. 23:644–55 [Google Scholar]
  48. Izergina N, Balmer J, Bello B, Reichert H. 2009. Postembryonic development of transit amplifying neuroblast lineages in the Drosophila brain. Neural Dev 4:44 [Google Scholar]
  49. Jefferis GS, Marin EC, Stocker RF, Luo L. 2001. Target neuron prespecification in the olfactory map of Drosophila. Nature 414:204–8 [Google Scholar]
  50. Jenett A, Rubin GM, Ngo TT, Shepherd D, Murphy C. et al. 2012. A GAL4-driver line resource for Drosophila neurobiology. Cell Rep 2:991–1001 [Google Scholar]
  51. Kahsai L, Winther AM. 2011. Chemical neuroanatomy of the Drosophila central complex: distribution of multiple neuropeptides in relation to neurotransmitters. J. Comp. Neurol. 519:290–315 [Google Scholar]
  52. Kambadur R, Koizumi K, Stivers C, Nagle J, Poole SJ, Odenwald WF. 1998. Regulation of POU genes by castor and hunchback establishes layered compartments in the Drosophila CNS. Genes Dev. 12:246–60 [Google Scholar]
  53. Kanai MI, Okabe M, Hiromi Y. 2005. seven-up controls switching of transcription factors that specify temporal identities of Drosophila neuroblasts. Dev. Cell 8:203–13 [Google Scholar]
  54. 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 73:677–84 [Google Scholar]
  55. Karlsson D, Baumgardt M, Thor S. 2010. Segment-specific neuronal subtype specification by the integration of anteroposterior and temporal cues. PLOS Biol 8:e1000368 [Google Scholar]
  56. Knoblich JA. 2008. Mechanisms of asymmetric stem cell division. Cell 132:583–97 [Google Scholar]
  57. Kohwi M, Doe CQ. 2013. Temporal fate specification and neural progenitor competence during development. Nat. Rev. Neurosci. 14:823–38 [Google Scholar]
  58. Kohwi M, Lupton JR, Lai SL, Miller MR, Doe CQ. 2013. Developmentally regulated subnuclear genome reorganization restricts neural progenitor competence in Drosophila. Cell 152:97–108 [Google Scholar]
  59. Koniszewski ND, Kollmann M, Bigham M, Farnworth M, He B. et al. 2016. The insect central complex as model for heterochronic brain development: background, concepts, and tools. Dev. Genes Evol. 226:209–19 [Google Scholar]
  60. Kucherenko MM, Shcherbata HR. 2013. Steroids as external temporal codes act via microRNAs and cooperate with cytokines in differential neurogenesis. Fly 7:173–83 [Google Scholar]
  61. Kuzin A, Kundu M, Ross J, Koizumi K, Brody T, Odenwald WF. 2012. The cis-regulatory dynamics of the Drosophila CNS determinant castor are controlled by multiple sub-pattern enhancers. Gene Expr. Patterns 12:261–72 [Google Scholar]
  62. Lacin H, Truman JW. 2016. Lineage mapping identifies molecular and architectural similarities between the larval and adult Drosophila central nervous system. eLife 5:e13399 [Google Scholar]
  63. Lai SL, Doe CQ. 2014. Transient nuclear Prospero induces neural progenitor quiescence. eLife 3:e03363 [Google Scholar]
  64. Lee T, Luo L. 1999. Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22:451–61 [Google Scholar]
  65. Li X, Erclik T, Bertet C, Chen Z, Voutev R. et al. 2013. Temporal patterning of Drosophila medulla neuroblasts controls neural fates. Nature 498:456–62 [Google Scholar]
  66. Liu Z, Yang CP, Sugino K, Fu CC, Liu LY. et al. 2015. Opposing intrinsic temporal gradients guide neural stem cell production of varied neuronal fates. Science 350:317–20 [Google Scholar]
  67. Maisak MS, Haag J, Ammer G, Serbe E, Meier M. et al. 2013. A directional tuning map of Drosophila elementary motion detectors. Nature 500:212–16 [Google Scholar]
  68. Mattar P, Ericson J, Blackshaw S, Cayouette M. 2015. A conserved regulatory logic controls temporal identity in mouse neural progenitors. Neuron 85:497–504 [Google Scholar]
  69. 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 [Google Scholar]
  70. Meier M, Serbe E, Maisak MS, Haag J, Dickson BJ, Borst A. 2014. Neural circuit components of the Drosophila OFF motion vision pathway. Curr. Biol. 24:385–92 [Google Scholar]
  71. Meinertzhagen IA, Hanson TE. 1993. The Development of the Optic Lobe Cold Spring Harbor, NY: Cold Spring Harb. Lab. Press
  72. 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 133:429–37 [Google Scholar]
  73. Moris-Sanz M, Estacio-Gomez A, Alvarez-Rivero J, Diaz-Benjumea FJ. 2014. Specification of neuronal subtypes by different levels of Hunchback. Development 141:4366–74 [Google Scholar]
  74. 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. Nat. Neurosci. 11:1014–23 [Google Scholar]
  75. Narbonne-Reveau K, Lanet E, Dillard C, Foppolo S, Chen CH. et al. 2016. Neural stem cell–encoded temporal patterning delineates an early window of malignant susceptibility in Drosophila. eLife 5:e13463 [Google Scholar]
  76. 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 129:1027–36 [Google Scholar]
  77. Pearson BJ, Doe CQ. 2003. Regulation of neuroblast competence in Drosophila. Nature 425:624–28 [Google Scholar]
  78. Pearson BJ, Doe CQ. 2004. Specification of temporal identity in the developing nervous system. Annu. Rev. Cell Dev. Biol. 20:619–47 [Google Scholar]
  79. Pfeiffer K, Homberg U. 2014. Organization and functional roles of the central complex in the insect brain. Annu. Rev. Entomol. 59:165–84 [Google Scholar]
  80. Prokop A, Technau GM. 1994. Early tagma-specific commitment of Drosophila CNS progenitor NB1-1. Development 120:2567–78 [Google Scholar]
  81. Ren Q, Yang CP, Liu Z, Sugino K, Mok K. et al. 2017. Stem cell–intrinsic, Seven-up-triggered temporal factor gradients diversify intermediate neural progenitors. Curr. Biol. 27:1303–13 [Google Scholar]
  82. Riebli N, Viktorin G, Reichert H. 2013. Early-born neurons in type II neuroblast lineages establish a larval primordium and integrate into adult circuitry during central complex development in Drosophila. Neural Dev. 8:6 [Google Scholar]
  83. Rogulja-Ortmann A, Technau GM. 2008. Multiple roles for Hox genes in segment-specific shaping of CNS lineages. Fly 2:316–19 [Google Scholar]
  84. Ross J, Kuzin A, Brody T, Odenwald WF. 2015. cis-regulatory analysis of the Drosophila pdm locus reveals a diversity of neural enhancers. BMC Genom. 16:700 [Google Scholar]
  85. Schmid A, Chiba A, Doe CQ. 1999. Clonal analysis of Drosophila embryonic neuroblasts: neural cell types, axon projections and muscle targets. Development 126:4653–89 [Google Scholar]
  86. Schmidt H, Rickert C, Bossing T, Vef O, Urban J, Technau GM. 1997. The embryonic central nervous system lineages of Drosophila melanogaster. II. Neuroblast lineages derived from the dorsal part of the neuroectoderm. Dev. Biol. 189:186–204 [Google Scholar]
  87. Sempere LF, Dubrovsky EB, Dubrovskaya VA, Berger EM, Ambros V. 2002. The expression of the let-7 small regulatory RNA is controlled by ecdysone during metamorphosis in Drosophila melanogaster. Dev. Biol. 244:170–79 [Google Scholar]
  88. Sempere LF, Sokol NS, Dubrovsky EB, Berger EM, Ambros V. 2003. Temporal regulation of microRNA expression in Drosophila melanogaster mediated by hormonal signals and Broad-Complex gene activity. Dev. Biol. 259:9–18 [Google Scholar]
  89. Sen S, Cao D, Choudhary R, Biagini S, Wang JW. et al. 2014. Genetic transformation of structural and functional circuitry rewires the Drosophila brain. eLife 3:e04407 [Google Scholar]
  90. Senga K, Mostov KE, Mitaka T, Miyajima A, Tanimizu N. 2012. Grainyhead-like 2 regulates epithelial morphogenesis by establishing functional tight junctions through the organization of a molecular network among claudin3, claudin4, and Rab25. Mol. Biol. Cell 23:2845–55 [Google Scholar]
  91. Serbe E, Meier M, Leonhardt A, Borst A. 2016. Comprehensive characterization of the major presynaptic elements to the Drosophila OFF motion detector. Neuron 89:829–41 [Google Scholar]
  92. Skeath JB, Zhang Y, Holmgren R, Carroll SB, Doe CQ. 1995. Specification of neuroblast identity in the Drosophila embryonic central nervous system by gooseberry-distal. Nature 376:427–30 [Google Scholar]
  93. Stratmann J, Gabilondo H, Benito-Sipos J, Thor S. 2016. Neuronal cell fate diversification controlled by sub-temporal action of Kruppel. eLife 5:e19311 [Google Scholar]
  94. Strauss R. 2002. The central complex and the genetic dissection of locomotor behaviour. Curr. Opin. Neurobiol. 12:633–38 [Google Scholar]
  95. Suzuki T, Kaido M, Takayama R, Sato M. 2013. A temporal mechanism that produces neuronal diversity in the Drosophila visual center. Dev. Biol. 380:12–24 [Google Scholar]
  96. Syed MH, Mark BJ, Doe CQ. 2017. Steroid hormone induction of temporal gene expression in Drosophila brain neuroblasts generates neuronal and glial diversity. eLife 6:e26287 [Google Scholar]
  97. Thummel CS. 2001. Molecular mechanisms of developmental timing in C. elegans and Drosophila. Dev. Cell 1:453–65 [Google Scholar]
  98. Touma JJ, Weckerle FF, Cleary MD. 2012. Drosophila Polycomb complexes restrict neuroblast competence to generate motoneurons. Development 139:657–66 [Google Scholar]
  99. Tran KD, Doe CQ. 2008. Pdm and Castor close successive temporal identity windows in the NB3-1 lineage. Development 135:3491–99 [Google Scholar]
  100. Truman JW, Bate M. 1988. Spatial and temporal patterns of neurogenesis in the central nervous system of Drosophila melanogaster. Dev. Biol. 125:145–57 [Google Scholar]
  101. 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 135:3859–69 [Google Scholar]
  102. Urbach R, Technau GM. 2003. Early steps in building the insect brain: neuroblast formation and segmental patterning in the developing brain of different insect species. Arthropod Struct. Dev. 32:103–23 [Google Scholar]
  103. Urban J, Mettler U. 2006. Connecting temporal identity to mitosis: the regulation of Hunchback in Drosophila neuroblast lineages. Cell Cycle 5:950–52 [Google Scholar]
  104. Viktorin G, Riebli N, Popkova A, Giangrande A, Reichert H. 2011. Multipotent neural stem cells generate glial cells of the central complex through transit amplifying intermediate progenitors in Drosophila brain development. Dev. Biol. 356:553–65 [Google Scholar]
  105. Viktorin G, Riebli N, Reichert H. 2013. A multipotent transit-amplifying neuroblast lineage in the central brain gives rise to optic lobe glial cells in Drosophila. Dev. Biol. 379:182–94 [Google Scholar]
  106. Wang YC, Yang JS, Johnston R, Ren Q, Lee YJ. et al. 2014. Drosophila intermediate neural progenitors produce lineage-dependent related series of diverse neurons. Development 141:253–58 [Google Scholar]
  107. Wolff T, Iyer NA, Rubin GM. 2015. Neuroarchitecture and neuroanatomy of the Drosophila central complex: a GAL4-based dissection of protocerebral bridge neurons and circuits. J. Comp. Neurol. 523:997–1037 [Google Scholar]
  108. Wu YC, Chen CH, Mercer A, Sokol NS. 2012. let-7-Complex microRNAs regulate the temporal identity of Drosophila mushroom body neurons via chinmo. Dev. Cell 23:202–9 [Google Scholar]
  109. Yamanaka N, Rewitz KF, O'Connor MB. 2013. Ecdysone control of developmental transitions: lessons from Drosophila research. Annu. Rev. Entomol. 58:497–516 [Google Scholar]
  110. Yang JS, Awasaki T, Yu HH, He Y, Ding P. et al. 2013. Diverse neuronal lineages make stereotyped contributions to the Drosophila locomotor control center, the central complex. J. Comp. Neurol. 521:2645–62 [Google Scholar]
  111. Yasugi T, Umetsu D, Murakami S, Sato M, Tabata T. 2008. Drosophila optic lobe neuroblasts triggered by a wave of proneural gene expression that is negatively regulated by JAK/STAT. Development 135:1471–80 [Google Scholar]
  112. Young JM, Armstrong JD. 2010. Structure of the adult central complex in Drosophila: organization of distinct neuronal subsets. J. Comp. Neurol. 518:1500–24 [Google Scholar]
  113. Yu HH, Awasaki T, Schroeder MD, Long F, Yang JS. et al. 2013. Clonal development and organization of the adult Drosophila central brain. Curr. Biol. 23:633–43 [Google Scholar]
  114. 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 Biol 8:e1000461 [Google Scholar]
  115. Zhang Y, Ungar A, Fresquez C, Holmgren R. 1994. Ectopic expression of either the Drosophila gooseberry-distal or proximal gene causes alterations of cell fate in the epidermis and central nervous system. Development 120:1151–61 [Google Scholar]
  116. 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 Dev. 4:39 [Google Scholar]
  117. 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 127:409–22 [Google Scholar]
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