Combinations of DIPs and Dprs control organization of olfactory receptor neuron terminals in Drosophila

Abstract

In Drosophila, 50 classes of olfactory receptor neurons (ORNs) connect to 50 class-specific and uniquely positioned glomeruli in the antennal lobe. Despite the identification of cell surface receptors regulating axon guidance, how ORN axons sort to form 50 stereotypical glomeruli remains unclear. Here we show that the heterophilic cell adhesion proteins, DIPs and Dprs, are expressed in ORNs during glomerular formation. Many ORN classes express a unique combination of DIPs/dprs, with neurons of the same class expressing interacting partners, suggesting a role in class-specific self-adhesion between ORN axons. Analysis of DIP/Dpr expression revealed that ORNs that target neighboring glomeruli have different combinations, and ORNs with very similar DIP/Dpr combinations can project to distant glomeruli in the antennal lobe. DIP/Dpr profiles are dynamic during development and correlate with sensilla type lineage for some ORN classes. Perturbations of DIP/dpr gene function result in local projection defects of ORN axons and glomerular positioning, without altering correct matching of ORNs with their target neurons. Our results suggest that context-dependent differential adhesion through DIP/Dpr combinations regulate self-adhesion and sort ORN axons into uniquely positioned glomeruli.

Chromatin-based reprogramming of a courtship regulator by concurrent pheromone perception and hormone signaling

“…Given the requirement for both group housing and JH signaling in stabilizing active chromatin marks around fru P1, we predicted that the disruption of JH receptor function in the first 2 to 3 days after eclosion could have different effects on fru M expression. Previous studies have shown that performing GAL4-driven RNAi knockdown experiments at different temperatures can modify RNAi effects, where lower temperatures weaken and, at times, completely rescue knockdown phenotypes (25,26). Given that fru GAL4 -mediated met and gce RNAi knockdown phenotypes are highly penetrant at 28°C, we probed fru M expression in experiments where we restricted the knockdown to specific days by performing temperature shifts.…”

A combinatorial code of transcription factors specifies subtypes of visual motion-sensing neurons in Drosophila

“…Drosophila (Keleman et al, 2002;Furrer et al, 2007;Zarin et al, 2014;Ward et al, 2015;Tadros et al, 2016;Li et al, 2017;Barish et al, 2018;Xu et al, 2018). We hypothesise that those cell-membrane proteins with stable subtype-specific expression patterns during, at least, the first phase of dendrite growth are the most likely candidates to regulate the development of the four dendrite orientations in a combinatorial way.…”

Neurogenetic and genomic approaches reveal roles for Dpr/DIP cell adhesion molecules inDrosophilareproductive behavior

“…CC-BY 4.0 International license available under a (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made The copyright holder for this preprint this version posted October 4, 2020. ; https://doi.org/10.1101/2020.10.02.323477 doi: bioRxiv preprint interactome partner pairs mediating these critical functions (CARRILLO et al 2015;TAN et al 2015;BARISH et al 2018;XU et al 2018;ASHLEY et al 2019;COURGEON AND DESPLAN 2019;MENON et al 2019;VENKATASUBRAMANIAN et al 2019;XU et al 2019). Our screen to identify morphological or synaptic changes in fru P1 ∩ DIP-α and DIP-δ neurons, using dpr/DIP RNAi or overexpression transgenes identified only one perturbation with an impact; reduction of DIP-ε by RNAi on the fru P1 ∩ DIP-α pattern, with both cell autonomous and non-autonomous roles.…”

“…Additionally, some Dprs interact dimerically with Dprs through either heterophilic or homophilic interactions, and some of the DIPs interact dimerically through homophilic interactions (OZKAN et al 2013;CARRILLO et al 2015;COSMANESCU et al 2018)(summarized in Supplemental Table 1). Functional analyses of the Dprs and DIPs have revealed roles in synaptic connectivity and specificity of neuronal targeting in the Drosophila neuromuscular junction, visual system and olfactory system (CARRILLO et al 2015;TAN et al 2015;BARISH et al 2018;XU et al 2018;ASHLEY et al 2019;COURGEON AND DESPLAN 2019;MENON et al 2019;VENKATASUBRAMANIAN et al 2019;XU et al 2019). Cell adhesion molecules have already been shown to be important for sculpting dimorphism in fru P1 neurons, with studies of the IgSF member encoded by roundabout (robo) shown to be a direct target of Fru M and responsible for dimorphic projections and morphology (MELLERT et al 2010;ITO et al 2016).…”