Identification of genes influencing dendrite morphogenesis in developing peripheral sensory and central motor neurons

被引:26
|
作者
Ou, Yimiao [2 ,3 ,4 ]
Chwalla, Barbara [1 ]
Landgraf, Matthias [1 ]
van Meyel, Donald J. [2 ,3 ,4 ]
机构
[1] Univ Cambridge, Dept Zool, Cambridge CB2 3EJ, England
[2] McGill Univ, Ctr Res Neurosci, Montreal, PQ H3G 1A4, Canada
[3] McGill Univ, Dept Neurol & Neurosurg, Montreal, PQ H3G 1A4, Canada
[4] McGill Univ, Ctr Hlth, Res Inst, Montreal, PQ H3G 1A4, Canada
基金
英国惠康基金; 加拿大健康研究院;
关键词
D O I
10.1186/1749-8104-3-16
中图分类号
Q [生物科学];
学科分类号
07 ; 0710 ; 09 ;
摘要
Background: Developing neurons form dendritic trees with cell type-specific patterns of growth, branching and targeting. Dendrites of Drosophila peripheral sensory neurons have emerged as a premier genetic model, though the molecular mechanisms that underlie and regulate their morphogenesis remain incompletely understood. Still less is known about this process in central neurons and the extent to which central and peripheral dendrites share common organisational principles and molecular features. To address these issues, we have carried out two comparable gain-of-function screens for genes that influence dendrite morphologies in peripheral dendritic arborisation (da) neurons and central RP2 motor neurons. Results: We found 35 unique loci that influenced da neuron dendrites, including five previously shown as required for da dendrite patterning. Several phenotypes were class-specific and many resembled those of known mutants, suggesting that genes identified in this study may converge with and extend known molecular pathways for dendrite development in da neurons. The second screen used a novel technique for cell-autonomous gene misexpression in RP2 motor neurons. We found 51 unique loci affecting RP2 dendrite morphology, 84% expressed in the central nervous system. The phenotypic classes from both screens demonstrate that gene misexpression can affect specific aspects of dendritic development, such as growth, branching and targeting. We demonstrate that these processes are genetically separable. Targeting phenotypes were specific to the RP2 screen, and we propose that dendrites in the central nervous system are targeted to territories defined by Cartesian co-ordinates along the antero-posterior and the medio-lateral axes of the central neuropile. Comparisons between the screens suggest that the dendrites of peripheral da and central RP2 neurons are shaped by regulatory programs that only partially overlap. We focused on one common candidate pathway controlled by the ecdysone receptor, and found that it promotes branching and growth of developing da neuron dendrites, but a role in RP2 dendrite development during embryonic and early larval stages was not apparent. Conclusion: We identified commonalities (for example, growth and branching) and distinctions (for example, targeting and ecdysone response) in the molecular and organizational framework that underlies dendrite development of peripheral and central neurons.
引用
收藏
页数:27
相关论文
共 50 条
  • [1] Identification of genes influencing dendrite morphogenesis in developing peripheral sensory and central motor neurons
    Yimiao Ou
    Barbara Chwalla
    Matthias Landgraf
    Donald J van Meyel
    [J]. Neural Development, 3
  • [2] Dissecting the functional role of Ret in dendrite morphogenesis of sensory neurons
    Hoyer, N.
    Petersen, M.
    Morellini, F.
    Soba, P.
    [J]. JOURNAL OF NEUROGENETICS, 2012, 26 : 27 - 27
  • [3] Phospholipid Homeostasis Regulates Dendrite Morphogenesis in Drosophila Sensory Neurons
    Meltzer, Shan
    Bagley, Joshua A.
    Perez, Gerardo Lopez
    O'Brien, Caitlin E.
    DeVault, Laura
    Guo, Yanmeng
    Jan, Lily Yeh
    Jan, Yuh-Nung
    [J]. CELL REPORTS, 2017, 21 (04): : 859 - 866
  • [4] nanos and pumilio are essential for dendrite morphogenesis in Drosophila peripheral neurons
    Ye, B
    Petritsch, C
    Clark, IE
    Gavis, ER
    Jan, LY
    Jan, YN
    [J]. CURRENT BIOLOGY, 2004, 14 (04) : 314 - 321
  • [5] Deterministic and Stochastic Rules of Branching Govern Dendrite Morphogenesis of Sensory Neurons
    Palavalli, Amrutha
    Tizon-Escamilla, Nicolas
    Rupprecht, Jean-Francois
    Lecuit, Thomas
    [J]. CURRENT BIOLOGY, 2021, 31 (03) : 459 - +
  • [6] Shep interacts with posttranscriptional regulators to control dendrite morphogenesis in sensory neurons
    Olesnicky, Eugenia C.
    Antonacci, Simona
    Popitsch, Niko
    Lybecker, Meghan C.
    Titus, M. Brandon
    Valadez, Racquel
    Derkach, Paul G.
    Marean, Amber
    Miller, Katherine
    Mathai, Samuel K.
    Killian, Darrell J.
    [J]. DEVELOPMENTAL BIOLOGY, 2018, 444 (02) : 116 - 128
  • [7] A critical period for the influence of peripheral targets on the central projections of developing sensory neurons
    Mears, SC
    Frank, E
    [J]. INTERNATIONAL JOURNAL OF DEVELOPMENTAL NEUROSCIENCE, 1996, 14 (06) : 731 - 737
  • [8] The RhoGEF Trio Functions in Sculpting Class Specific Dendrite Morphogenesis in Drosophila Sensory Neurons
    Iyer, Srividya Chandramouli
    Wang, Dennis
    Iyer, Eswar Prasad R.
    Trunnell, Sarah A.
    Meduri, Ramakrishna
    Shinwari, Riaz
    Sulkowski, Mikolaj J.
    Cox, Daniel N.
    [J]. PLOS ONE, 2012, 7 (03):
  • [9] Identification of possible downstream genes required for the extension of peripheral axons in primary sensory neurons
    Aoki, Makoto
    Segawa, Hiroshi
    Naito, Mayumi
    Okamoto, Hitoshi
    [J]. BIOCHEMICAL AND BIOPHYSICAL RESEARCH COMMUNICATIONS, 2014, 445 (02) : 357 - 362
  • [10] Conserved RNA-Binding Proteins Required for Dendrite Morphogenesis in Caenorhabditis elegans Sensory Neurons
    Antonacci, Simona
    Forand, Daniel
    Wolf, Margaret
    Tyus, Courtney
    Barney, Julia
    Kellogg, Leah
    Simon, Margo A.
    Kerr, Genevieve
    Wells, Kristen L.
    Younes, Serena
    Mortimer, Nathan T.
    Olesnicky, Eugenia C.
    Killian, Darrell J.
    [J]. G3-GENES GENOMES GENETICS, 2015, 5 (04): : 639 - 653