Drosophila Fezf coordinates laminar-specific connectivity through cell-intrinsic and cell-extrinsic mechanisms

Peng, Jing; Santiago, Ivan J.; Ahn, Curie; Gür, Burak; Tsui, C. Kimberly; Su, Zhixiao; Xu, Chengpei; Karakhanyan, Aziz; Silies, Marion; Pecot, Matthew Y.

doi:10.7554/elife.33962

Cited by 42 publications

(54 citation statements)

References 48 publications

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“…In contrast, when T4/T5 axons failed to form distinct layers in the lobula plate, the dendrites of their postsynaptic partners also failed to form layers, suggesting that T4/T5 neurons play an instructive role in lobula plate patterning. The finding that SoxN and Sox102F function in T4/T5 neurons is non-autonomously required for the layer specificity of lobula plate tangential cells supports a recently proposed model describing layer formation as a stepwise process relying on transcription factors that restrict neurons to specific layers in a cell-intrinsic manner, and recruit other circuit components in a cell-extrinsic manner (Peng et al, 2018).…”

Section: Discussionsupporting

confidence: 70%

Transcriptional control of morphological properties of direction-selective T4/T5 neurons inDrosophila

et al. 2019

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In the Drosophila visual system, T4/T5 neurons represent the first stage of computation of the direction of visual motion. T4 and T5 neurons exist in four subtypes, each responding to motion in one of the four cardinal directions and projecting axons into one of the four lobula plate layers. However, all T4/T5 neurons share properties essential for sensing motion. How T4/T5 neurons acquire their properties during development is poorly understood. We reveal that the transcription factors SoxN and Sox102F control the acquisition of properties common to all T4/T5 neuron subtypes, i.e. the layer specificity of dendrites and axons. Accordingly, adult flies are motion blind after disruption of SoxN or Sox102F in maturing T4/T5 neurons. We further find that the transcription factors Ato and Dac are redundantly required in T4/T5 neuron progenitors for SoxN and Sox102F expression in T4/T5 neurons, linking the transcriptional programmes specifying progenitor identity to those regulating the acquisition of morphological properties in neurons. Our work will help to link structure, function and development in a neuronal type performing a computation that is conserved across vertebrate and invertebrate visual systems.

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Section: Discussionsupporting

confidence: 70%

Transcriptional control of morphological properties of direction-selective T4/T5 neurons inDrosophila

et al. 2019

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“…Next, we sought to determine whether Dpr-DIP interactions are necessary for selective synapse formation between L2 and L4 neurons. To address this, we used synaptic tagging with recombination (Chen et al, 2014;Peng et al, 2018) to label L2-L4 synapses selectively. Using STaR the active zone protein Bruchpilot (Brp) (Wagh et al, 2006) can be tagged in a cell type-specific manner depending on the expression of Flp recombinase (Golic and Lindquist, 1989), while being expressed from its native promoter within a bacterial artificial chromosome (BAC).…”

Section: Dip Function Is Necessary To Prevent the Formation Of Ectopimentioning

confidence: 99%

“…The following fly stocks were used: (Tuthill et al, 2013)] (gift from the Janelia Research Campus), 79C23S-GS- FRT-stop-FRT-smFPV5-2A-LexAVP16 (Peng et al, 2018), LexAopmyr::tdTomato (III) (gift from S.L. Zipursky), UAS-Flp (II) (BDSC 4540), 31C06AD (II) 34G07DBD (III) [L4 split-GAL4 (Tuthill et al, 2013)] (gift from the Janelia Research Campus), 27G05-FLPG5.PEST (attp5) (gift from the Janelia research campus) (Peng et al, 2018), GMR-GAL4 (III) (BDSD 8121),…”

Section: Fly Strainsmentioning

confidence: 99%

Control of synaptic specificity by limiting promiscuous synapse formation

Theisen

Rumbaut

et al. 2018

Preprint

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The ability of neurons to distinguish appropriate from inappropriate synaptic partners in their local environment is fundamental to the proper assembly and function of neural circuits. How synaptic partner selection is regulated is a longstanding question in Neurobiology. A prevailing hypothesis is that appropriate partners express complementary molecules that match them together and promote synaptogenesis. Dpr and DIP IgSF proteins bind heterophilically and are expressed in a complementary manner between synaptic partners in the Drosophila visual system. Here, we show that in the lamina, DIP mis-expression is sufficient to promote synapse formation with Dpr-expressing neurons, and that DIP proteins are not necessary for synaptogenesis but rather function to prevent ectopic synapse formation. These findings indicate that Dpr-DIP interactions regulate synaptic specificity by biasing synapse formation towards specific cell-types. We propose that synaptogenesis occurs independent of synaptic partner choice, and that precise synaptic connectivity is established by limiting promiscuous synapse formation.

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“… The D. melanogaster visual system and lamina neuron layer specificity. Schematics illustrating the various morphologies and layer-specific innervation patterns found throughout the fruit fly optic lobe, as well as a synopsis of the findings from Peng et al ( 12 ). ( A ) Visual information is received by the retina and relayed to four downstream neuropil known as the lamina, medulla, lobula, and lobula plate (lobula and lobula plate are not shown in the diagram).…”

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confidence: 99%

Drosophila Fezf functions as a transcriptional repressor to direct layer-specific synaptic connectivity in the fly visual system

Santiago

Zhang

Saras

et al. 2021

Proc. Natl. Acad. Sci. U.S.A.

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The layered compartmentalization of synaptic connections, a common feature of nervous systems, underlies proper connectivity between neurons and enables parallel processing of neural information. However, the stepwise development of layered neuronal connections is not well understood. The medulla neuropil of the Drosophila visual system, which comprises 10 discrete layers (M1 to M10), where neural computations underlying distinct visual features are processed, serves as a model system for understanding layered synaptic connectivity. The first step in establishing layer-specific connectivity in the outer medulla (M1 to M6) is the innervation by lamina (L) neurons of one of two broad, primordial domains that will subsequently expand and transform into discrete layers. We previously found that the transcription factor dFezf cell-autonomously directs L3 lamina neurons to their proper primordial broad domain before they form synapses within the developing M3 layer. Here, we show that dFezf controls L3 broad domain selection through temporally precise transcriptional repression of the transcription factor slp1 (sloppy paired 1). In wild-type L3 neurons, slp1 is transiently expressed at a low level during broad domain selection. When dFezf is deleted, slp1 expression is up-regulated, and ablation of slp1 fully rescues the defect of broad domain selection in dFezf-null L3 neurons. Although the early, transient expression of slp1 is expendable for broad domain selection, it is surprisingly necessary for the subsequent L3 innervation of the M3 layer. DFezf thus functions as a transcriptional repressor to coordinate the temporal dynamics of a transcriptional cascade that orchestrates sequential steps of layer-specific synapse formation.

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Drosophila Fezf coordinates laminar-specific connectivity through cell-intrinsic and cell-extrinsic mechanisms

Cited by 42 publications

References 48 publications

Transcriptional control of morphological properties of direction-selective T4/T5 neurons inDrosophila

Transcriptional control of morphological properties of direction-selective T4/T5 neurons inDrosophila

Control of synaptic specificity by limiting promiscuous synapse formation

Drosophila Fezf functions as a transcriptional repressor to direct layer-specific synaptic connectivity in the fly visual system

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