Drosophila N-cadherin functions in the first stage of the two-stage layer-selection process of R7 photoreceptor afferents

Chun Yuan Ting, Shinichi Yonekura, Phoung Chung, Shu Ning Hsu, Hugh M. Robertson, Akira Chiba, Chi Hon Lee

Research output: Contribution to journalArticle

86 Citations (Scopus)

Abstract

Visual information received from the three types of photoreceptor neurons (R1-R6, R7 and R8) in the fly compound eyes converges to the external part of the medulla neuropil (M1-M6 layers) in a layer-specific fashion: R7 and R8 axons terminate at the M6 and M3 layers, respectively, whereas lamina neurons (L1-L5) relay R1-R6 to multiple medulla layers (M1-M5). Here, we show that during development, R7 and R8 neurons establish layer-specific projections in two separate stages: during the first stage, R7 and R8 axons sequentially target to the R7- and R8-temporary layers, respectively; and at the second stage, R7 and R8 growth cones progress synchronously to their destined layers. Using a set of mutations that delete different afferent subsets or alter R7 connectivity, we defined the mechanism of layer selection. We observed that R8, R7 and L1-L5 afferents target to their temporary layers independently, suggesting that afferent-target, but not afferent-afferent, interactions dictate the targeting specificity. N-cadherin is required in the first stage for R7 growth cones to reach and remain in the R7-temporary layer. The Ncad gene contains three pairs of alternatively spliced exons and encodes 12 isoforms. However, expressing a single Ncad isoform in Ncad mutant R7s is sufficient to rescue mistargeting phenotypes. Furthermore, Ncad isoforms mediate promiscuous heterophilic interactions in an in vitro cell-aggregation assay. We propose that Ncad isoforms do not form an adhesion code; rather, they provide permissive adhesion between R7 growth cones and their temporary targets.

Original languageEnglish
Pages (from-to)953-963
Number of pages11
JournalDevelopment
Volume132
Issue number5
DOIs
StatePublished - Mar 1 2005
Externally publishedYes

Fingerprint

Cadherins
Growth Cones
Drosophila
Protein Isoforms
Neurons
Axons
Cell Aggregation
Neuropil
Diptera
Exons
Phenotype
Mutation
Genes

Keywords

  • Drosophila
  • N-cadherin
  • R7

ASJC Scopus subject areas

  • Anatomy
  • Cell Biology

Cite this

Drosophila N-cadherin functions in the first stage of the two-stage layer-selection process of R7 photoreceptor afferents. / Ting, Chun Yuan; Yonekura, Shinichi; Chung, Phoung; Hsu, Shu Ning; Robertson, Hugh M.; Chiba, Akira; Lee, Chi Hon.

In: Development, Vol. 132, No. 5, 01.03.2005, p. 953-963.

Research output: Contribution to journalArticle

Ting, Chun Yuan ; Yonekura, Shinichi ; Chung, Phoung ; Hsu, Shu Ning ; Robertson, Hugh M. ; Chiba, Akira ; Lee, Chi Hon. / Drosophila N-cadherin functions in the first stage of the two-stage layer-selection process of R7 photoreceptor afferents. In: Development. 2005 ; Vol. 132, No. 5. pp. 953-963.
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