Tiling of R7 Axons in the Drosophila Visual System Is Mediated Both by Transduction of an Activin Signal to the Nucleus and by Mutual Repulsion

Chun Yuan Ting, Tory Herman, Shinichi Yonekura, Shuying Gao, Jian Wang, Mihaela Serpe, Michael B. O'Connor, S. Lawrence Zipursky, Chi Hon Lee

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69 Scopus citations

Abstract

The organization of neuronal wiring into layers and columns is a common feature of both vertebrate and invertebrate brains. In the Drosophila visual system, each R7 photoreceptor axon projects within a single column to a specific layer of the optic lobe. We refer to the restriction of terminals to single columns as tiling. In a genetic screen based on an R7-dependent behavior, we identified the Activin receptor Baboon and the nuclear import adaptor Importin-α3 as being required to prevent R7 axon terminals from overlapping with the terminals of R7s in neighboring columns. This tiling function requires the Baboon ligand, dActivin, the transcription factor, dSmad2, and retrograde transport from the growth cone to the R7 nucleus. We propose that dActivin is an autocrine signal that restricts R7 growth cone motility, and we demonstrate that it acts in parallel with a paracrine signal that mediates repulsion between R7 terminals.

Original languageEnglish (US)
Pages (from-to)793-806
Number of pages14
JournalNeuron
Volume56
Issue number5
DOIs
StatePublished - Dec 6 2007

Bibliographical note

Funding Information:
We thank Tzumin Lee and Claude Desplan for reagents and Zhigang He for communicating results prior to publication. We thank James Clemens, Steven Britt, Carl S. Parker, and Iris Salecker for S2 cells, Rh3 antibody, Importin-α3 antibody, and ey 3.5 -Flp flies, respectively, and Luisa Vasconcelos for in situ hybridization protocol. We thank Benjamin White, Howard Nash, Kelsey Martin, Alan Hinnebusch, and Henry Levin for carefully reading this manuscript and for helpful discussion and Margaret Dieringer for manuscript handling and editing. This work was supported by the Intramural Research Program of the NIH, National Institute of Child Health and Human Development (grant HD008748-03 to C.-H.L.), and a Burroughs-Wellcome Career Development Award (to T.H.).

Keywords

  • DEVBIO
  • MOLNEURO
  • SIGNALING

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