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eLife Volume 9 ,2020-04-06
Conservation and divergence of related neuronal lineages in the Drosophila central brain
Developmental Biology
Ying-Jou Lee 1 Ching-Po Yang 1 Rosa L Miyares 1 Yu-Fen Huang 1 Yisheng He 1 Qingzhong Ren 1 Hui-Min Chen 1 Takashi Kawase 1 Masayoshi Ito 1 Hideo Otsuna 1 Ken Sugino 1 Yoshi Aso 1 Kei Ito 1 Tzumin Lee 1
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DOI:10.7554/eLife.53518
Received 2019-11-12, accepted for publication 2020-04-06, Published 2020-04-06
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摘要

Wiring a complex brain requires many neurons with intricate cell specificity, generated by a limited number of neural stem cells. Drosophila central brain lineages are a predetermined series of neurons, born in a specific order. To understand how lineage identity translates to neuron morphology, we mapped 18 Drosophila central brain lineages. While we found large aggregate differences between lineages, we also discovered shared patterns of morphological diversification. Lineage identity plus Notch-mediated sister fate govern primary neuron trajectories, whereas temporal fate diversifies terminal elaborations. Further, morphological neuron types may arise repeatedly, interspersed with other types. Despite the complexity, related lineages produce similar neuron types in comparable temporal patterns. Different stem cells even yield two identical series of dopaminergic neuron types, but with unrelated sister neurons. Together, these phenomena suggest that straightforward rules drive incredible neuronal complexity, and that large changes in morphology can result from relatively simple fating mechanisms.

关键词

D. melanogaster;twin-spot MARCM;central complex;mushroom body;vnd;temporal fate;hemilineage

授权许可

© 2020, Lee et al
http://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

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Ying-Jou Lee,Ching-Po Yang,Rosa L Miyares,Yu-Fen Huang,Yisheng He,Qingzhong Ren,Hui-Min Chen,Takashi Kawase,Masayoshi Ito,Hideo Otsuna,Ken Sugino,Yoshi Aso,Kei Ito,Tzumin Lee. Conservation and divergence of related neuronal lineages in the Drosophila central brain. eLife ,Vol.9(2020)

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参考文献
[1] D Shepherd, V Sahota, R Court, DW Williams. et al.(2019). Developmental organization of central neurons in the adult ventral nervous system. Journal of Comparative Neurology.527:2573-2598. DOI: 10.7554/eLife.04577.
[2] C-P Yang, TJ Samuels, Y Huang, L Yang. et al.(2017). Imp and Syp RNA-binding proteins govern decommissioning of neural stem cells. Development.144:3454-3464. DOI: 10.7554/eLife.04577.
[3] R Urbach, GM Technau. (2003). Molecular markers for identified neuroblasts in the developing brain of. Development.130:3621-3637. DOI: 10.7554/eLife.04577.
[4] Z Liu, CP Yang, K Sugino, CC Fu. et al.(2015). Opposing intrinsic temporal gradients guide neural stem cell production of varied neuronal fates. Science.350:317-320. DOI: 10.7554/eLife.04577.
[5] H-H Yu, C-H Chen, L Shi, Y Huang. et al.(2009). Twin-spot MARCM to reveal the developmental origin and identity of neurons. Nature Neuroscience.12:947-953. DOI: 10.7554/eLife.04577.
[6] R Urbach, GM Technau. (2008). Dorsoventral patterning of the brain: a comparative approach. Advances in Experimental Medicine and Biology.628:42-56. DOI: 10.7554/eLife.04577.
[7] JW Truman, M Bate. (1988). Spatial and temporal patterns of neurogenesis in the central nervous system of. Developmental Biology.125:145-157. DOI: 10.7554/eLife.04577.
[8] K Rein, M Zöckler, MT Mader, C Grübel. et al.(2002). The standard brain. Current Biology.12:227-231. DOI: 10.7554/eLife.04577.
[9] GS Jefferis, EC Marin, RF Stocker, L Luo. et al.(2001). Target neuron prespecification in the olfactory map of. Nature.414:204-208. DOI: 10.7554/eLife.04577.
[10] S Lin, CF Kao, HH Yu, Y Huang. et al.(2012). Lineage analysis of lateral antennal lobe neurons reveals notch-dependent binary temporal fate decisions. PLOS Biology.10. DOI: 10.7554/eLife.04577.
[11] HH Yu, CF Kao, Y He, P Ding. et al.(2010). A complete developmental sequence of aneuronal lineage as revealed by twin-spot MARCM. PLOS Biology.8. DOI: 10.7554/eLife.04577.
[12] CQ Doe. (2017). Temporal Patterning in the CNS. Annual Review of Cell and Developmental Biology.33:219-240. DOI: 10.7554/eLife.04577.
[13] J Thurmond, JL Goodman, VB Strelets, H Attrill. et al.(2019). FlyBase 2.0: the next generation. Nucleic Acids Research.47:D759-D765. DOI: 10.7554/eLife.04577.
[14] YS Rong, KG Golic. (2000). Gene targeting by homologous recombination in. Science.288:2013-2018. DOI: 10.7554/eLife.04577.
[15] T Erclik, X Li, M Courgeon, C Bertet. et al.(2017). Integration of temporal and spatial patterning generates neural diversity. Nature.541:365-370. DOI: 10.7554/eLife.04577.
[16] T Lee, A Lee, L Luo. (1999). Development of themushroom bodies: sequential generation of three distinct types of neurons from a neuroblast. Development.126:4065-4076. DOI: 10.7554/eLife.04577.
[17] J Schindelin, I Arganda-Carreras, E Frise, V Kaynig. et al.(2012). Fiji: an open-source platform for biological-image analysis. Nature Methods.9:676-682. DOI: 10.7554/eLife.04577.
[18] A Murata, S-I Hayashi. (2016). Notch-Mediated cell adhesion. Biology.5. DOI: 10.7554/eLife.04577.
[19] S Sen, D Cao, R Choudhary, S Biagini. et al.(2014). Genetic transformation of structural and functional circuitry rewires the brain. eLife.3. DOI: 10.7554/eLife.04577.
[20] T Lee, L Luo. (1999). Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron.22:451-461. DOI: 10.7554/eLife.04577.
[21] LY Liu, X Long, CP Yang, RL Miyares. et al.(2019). Mamo Decodes hierarchical temporal gradients into terminal neuronal fate. eLife.8. DOI: 10.7554/eLife.04577.
[22] C Maurange, L Cheng, AP Gould. (2008). Temporal transcription factors and their targets schedule the end of neural proliferation in. Cell.133:891-902. DOI: 10.7554/eLife.04577.
[23] RL Miyares, T Lee. (2019). Temporal control of central nervous system development. Current Opinion in Neurobiology.56:24-32. DOI: 10.7554/eLife.04577.
[24] R Lichtneckert, H Reichert. (2008). Anteroposterior regionalization of the brain: genetic and comparative aspects. Advances in Experimental Medicine and Biology.628:32-41. DOI: 10.7554/eLife.04577.
[25] Z Zheng, JS Lauritzen, E Perlman, CG Robinson. et al.(2018). A complete electron microscopy volume of the brain of adult. Cell.174:730-743. DOI: 10.7554/eLife.04577.
[26] Y Wan, H Otsuna, CB Chien, C Hansen. et al.(2009). An interactive visualization tool for multi-channel confocal microscopy data in neurobiology research. IEEE Transactions on Visualization and Computer Graphics.15:1489-1496. DOI: 10.7554/eLife.04577.
[27] H Li, F Horns, B Wu, Q Xie. et al.(2017). Classifying olfactory projection neuron subtypes by Single-Cell RNA sequencing. Cell.171:1206-1220. DOI: 10.7554/eLife.04577.
[28] KJ Venken, JH Simpson, HJ Bellen. (2011). Genetic manipulation of genes and cells in the nervous system of the fruit fly. Neuron.72:202-230. DOI: 10.7554/eLife.04577.
[29] S Zhu, S Lin, CF Kao, T Awasaki. et al.(2006). Gradients of the chinmo BTB-zinc finger protein govern neuronal temporal identity. Cell.127:409-422. DOI: 10.7554/eLife.04577.
[30] ZJ Huang. (2014). Toward a genetic dissection of cortical circuits in the mouse. Neuron.83:1284-1302. DOI: 10.7554/eLife.04577.
[31] Y Wan, H Otsuna, CB Chien, C Hansen. et al.(2012). Interactive extraction of neural structures with User-Guided morphological diffusion. :1-8. DOI: 10.7554/eLife.04577.
[32] M Costa, JD Manton, AD Ostrovsky, S Prohaska. et al.(2016). NBLAST: rapid, sensitive comparison of neuronal structure and construction of neuron family databases. Neuron.91:293-311. DOI: 10.7554/eLife.04577.
[33] HM Chen, Y Huang, BD Pfeiffer, X Yao. et al.(2015). An enhanced gene targeting toolkit for : golic+. Genetics.199:683-694. DOI: 10.7554/eLife.04577.
[34] L Biffar, A Stollewerk. (2014). Conservation and evolutionary modifications of neuroblast expression patterns in insects. Developmental Biology.388:103-116. DOI: 10.7554/eLife.04577.
[35] SY Takemura, Y Aso, T Hige, A Wong. et al.(2017). A connectome of a learning and memory center in the adult brain. eLife.6. DOI: 10.7554/eLife.04577.
[36] T Rohlfing, CR Maurer. (2003). Nonrigid image registration in shared-memory multiprocessor environments with application to brains, breasts, and bees. IEEE Transactions on Information Technology in Biomedicine.7:16-25. DOI: 10.7554/eLife.04577.
[37] K Ito, K Shinomiya, M Ito, JD Armstrong. et al.(2014). A systematic nomenclature for the insect brain. Neuron.81:755-765. DOI: 10.7554/eLife.04577.
[38] T Awasaki, C-F Kao, Y-J Lee, C-P Yang. et al.(2014). Making lineage–restricted drivers via patterned recombination in neuroblasts. Nature Neuroscience.17:631-637. DOI: 10.7554/eLife.04577.
[39] FF Vasconcelos, DS Castro. (2014). Transcriptional control of vertebrate neurogenesis by the proneural factor Ascl1. Frontiers in Cellular Neuroscience.8. DOI: 10.7554/eLife.04577.
[40] EP Spana, CQ Doe. (1996). Numb antagonizes notch signaling to specify sibling neuron cell fates. Neuron.17:21-26. DOI: 10.7554/eLife.04577.
[41] Q Ren, T Awasaki, YC Wang, YF Huang. et al.(2018). Lineage-guided Notch-dependent gliogenesis by multi-potent progenitors. Development.145. DOI: 10.7554/eLife.04577.
[42] M Ito, N Masuda, K Shinomiya, K Endo. et al.(2013). Systematic analysis of neural projections reveals clonal composition of the brain. Current Biology.23:644-655. DOI: 10.7554/eLife.04577.
[43] HH Yu, T Awasaki, MD Schroeder, F Long. et al.(2013). Clonal development and organization of the Central Brain. Current Biology : CB.23:633-643. DOI: 10.7554/eLife.04577.
[44] JW Truman, W Moats, J Altman, EC Marin. et al.(2010). Role of notch signaling in establishing the hemilineages of secondary neurons in. Development.137:53-61. DOI: 10.7554/eLife.04577.
[45] AP Jarman, M Brand, LY Jan, YN Jan. et al.(1993). The regulation and function of the helix-loop-helix gene, asense, inneural precursors. Development.119:19-29. DOI: 10.7554/eLife.04577.
[46] Y Aso, D Hattori, Y Yu, RM Johnston. et al.(2014). The neuronal architecture of the mushroom body provides a logic for associative learning. eLife.3. DOI: 10.7554/eLife.04577.
[47] S Lin, SL Lai, HH Yu, T Chihara. et al.(2010). Lineage-specific effects of notch/Numb signaling in post-embryonic development of the brain. Development.137:43-51. DOI: 10.7554/eLife.04577.
[48] Q Ren, CP Yang, Z Liu, K Sugino. et al.(2017). Stem Cell-Intrinsic, Seven-up-Triggered temporal factor gradients diversify intermediate neural progenitors. Current Biology.27:1303-1313. DOI: 10.7554/eLife.04577.