Control of Synaptic Specificity by Establishing a Relative Preference for Synaptic Partners

The ability of neurons to identify correct synaptic partners is fundamental to the proper assembly and function of neural circuits. Relative to other steps in circuit formation such as axon guidance, our knowledge of how synaptic partner selection is regulated is severely limited. Drosophila Dpr and...

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Bibliographic Details
Published in:Neuron (Cambridge, Mass.) Mass.), 2019-09, Vol.103 (5), p.865-877.e7
Main Authors: Xu, Chundi, Theisen, Emma, Maloney, Ryan, Peng, Jing, Santiago, Ivan, Yapp, Clarence, Werkhoven, Zachary, Rumbaut, Elijah, Shum, Bryan, Tarnogorska, Dorota, Borycz, Jolanta, Tan, Liming, Courgeon, Maximilien, Griffin, Tessa, Levin, Raina, Meinertzhagen, Ian A., de Bivort, Benjamin, Drugowitsch, Jan, Pecot, Matthew Y.
Format: Article
Language:English
Subjects:
Animals
Animals, Genetically Modified
Axon guidance
cell recognition molecules
Cell surface
Dpr and DIP proteins
Drosophila melanogaster
Drosophila Proteins - genetics
Drosophila Proteins - metabolism
Drosophila visual system
Gene expression
Immunoglobulins - genetics
Immunoglobulins - metabolism
Insects
Mate selection
Membrane Proteins - genetics
Membrane Proteins - metabolism
Nervous system
Neural networks
Neurons
Neurons - cytology
Neurons - metabolism
Optic Lobe, Nonmammalian - cytology
Optic Lobe, Nonmammalian - metabolism
Protein Interaction Maps
Proteins
synapse formation
Synapses - metabolism
synaptic specificity
Synaptogenesis
Visual pathways
Visual system
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Summary:The ability of neurons to identify correct synaptic partners is fundamental to the proper assembly and function of neural circuits. Relative to other steps in circuit formation such as axon guidance, our knowledge of how synaptic partner selection is regulated is severely limited. Drosophila Dpr and DIP immunoglobulin superfamily (IgSF) cell-surface proteins bind heterophilically and are expressed in a complementary manner between synaptic partners in the visual system. Here, we show that in the lamina, DIP mis-expression is sufficient to promote synapse formation with Dpr-expressing neurons and that disrupting DIP function results in ectopic synapse formation. These findings indicate that DIP proteins promote synapses to form between specific cell types and that in their absence, neurons synapse with alternative partners. We propose that neurons have the capacity to synapse with a broad range of cell types and that synaptic specificity is achieved by establishing a preference for specific partners. •DIP-β is necessary for proper synaptic connectivity in the Drosophila visual system•DIPs-β and γ are sufficient to promote synapse formation in vivo•DIP IgSF proteins are necessary for proper visual function in Drosophila Xu et al. show that in the Drosophila visual system, DIP IgSF proteins are not necessary for synaptogenesis but regulate synaptic specificity by promoting synapses to form between specific cell types.
ISSN:0896-6273
1097-4199
DOI:10.1016/j.neuron.2019.06.006