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The RhoGEF Trio Functions in Sculpting Class Specific Dendrite Morphogenesis in Drosophila Sensory Neurons

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  • Srividya Chandramouli Iyer
  • Dennis Wang
  • Eswar Prasad R Iyer
  • Sarah A Trunnell
  • Ramakrishna Meduri
  • Riaz Shinwari
  • Mikolaj J Sulkowski
  • Daniel N Cox

Abstract

Background: As the primary sites of synaptic or sensory input in the nervous system, dendrites play an essential role in processing neuronal and sensory information. Moreover, the specification of class specific dendrite arborization is critically important in establishing neural connectivity and the formation of functional networks. Cytoskeletal modulation provides a key mechanism for establishing, as well as reorganizing, dendritic morphology among distinct neuronal subtypes. While previous studies have established differential roles for the small GTPases Rac and Rho in mediating dendrite morphogenesis, little is known regarding the direct regulators of these genes in mediating distinct dendritic architectures. Methodology/Principal Findings: Here we demonstrate that the RhoGEF Trio is required for the specification of class specific dendritic morphology in dendritic arborization (da) sensory neurons of the Drosophila peripheral nervous system (PNS). Trio is expressed in all da neuron subclasses and loss-of-function analyses indicate that Trio functions cell-autonomously in promoting dendritic branching, field coverage, and refining dendritic outgrowth in various da neuron subtypes. Moreover, overexpression studies demonstrate that Trio acts to promote higher order dendritic branching, including the formation of dendritic filopodia, through Trio GEF1-dependent interactions with Rac1, whereas Trio GEF-2-dependent interactions with Rho1 serve to restrict dendritic extension and higher order branching in da neurons. Finally, we show that de novo dendritic branching, induced by the homeodomain transcription factor Cut, requires Trio activity suggesting these molecules may act in a pathway to mediate dendrite morphogenesis. Conclusions/Significance: Collectively, our analyses implicate Trio as an important regulator of class specific da neuron dendrite morphogenesis via interactions with Rac1 and Rho1 and indicate that Trio is required as downstream effector in Cut-mediated regulation of dendrite branching and filopodia formation.

Suggested Citation

  • Srividya Chandramouli Iyer & Dennis Wang & Eswar Prasad R Iyer & Sarah A Trunnell & Ramakrishna Meduri & Riaz Shinwari & Mikolaj J Sulkowski & Daniel N Cox, 2012. "The RhoGEF Trio Functions in Sculpting Class Specific Dendrite Morphogenesis in Drosophila Sensory Neurons," PLOS ONE, Public Library of Science, vol. 7(3), pages 1-15, March.
  • Handle: RePEc:plo:pone00:0033634
    DOI: 10.1371/journal.pone.0033634
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    References listed on IDEAS

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    1. Hideji Murakoshi & Hong Wang & Ryohei Yasuda, 2011. "Local, persistent activation of Rho GTPases during plasticity of single dendritic spines," Nature, Nature, vol. 472(7341), pages 100-104, April.
    2. Mikolaj J Sulkowski & Srividya Chandramouli Iyer & Mathieu S Kurosawa & Eswar Prasad R Iyer & Daniel N Cox, 2011. "Turtle Functions Downstream of Cut in Differentially Regulating Class Specific Dendrite Morphogenesis in Drosophila," PLOS ONE, Public Library of Science, vol. 6(7), pages 1-18, July.
    3. Wun Chey Sin & Kurt Haas & Edward S. Ruthazer & Hollis T. Cline, 2002. "Dendrite growth increased by visual activity requires NMDA receptor and Rho GTPases," Nature, Nature, vol. 419(6906), pages 475-480, October.
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