Adult Drosophila sensory neurons specify dendritic territories independently of dendritic contacts through the Wnt5–Drl signaling pathway

Abstract

Sensory neurons with common functions are often nonrandomly arranged and form dendritic territories in stereotypic spatial patterns throughout the nervous system, yet molecular mechanisms of how neurons specify dendritic territories remain largely unknown. In Drosophila larvae, dendrites of class IV sensory (C4da) neurons completely but nonredundantly cover the whole epidermis, and the boundaries of these tiled dendritic fields are specified through repulsive interactions between homotypic dendrites. Here we report that, unlike the larval C4da neurons, adult C4da neurons rely on both dendritic repulsive interactions and external positional cues to delimit the boundaries of their dendritic fields. We identify Wnt5 derived from sternites, the ventral-most part of the adult abdominal epidermis, as the critical determinant for the ventral boundaries. Further genetic data indicate that Wnt5 promotes dendrite termination on the periphery of sternites through the Ryk receptor family kinase Derailed (Drl) and the Rho GTPase guanine nucleotide exchange factor Trio in C4da neurons. Our findings thus uncover the dendritic contact-independent mechanism that is required for dendritic boundary specification and suggest that combinatory actions of the dendritic contact-dependent and -independent mechanisms may ensure appropriate dendritic territories of a given neuron.

JNK signaling coordinates with ecdysone signaling to promote dendrite pruning ofDrosophilasensory neurons

“…7C). The expression pattern of drl-GAL4 in larval c4da neurons is consistent with its expression in adult c4da neurons (Yasunaga et al, 2015). Therefore, Drl is endogenously expressed in c4da neurons throughout development and could potentially mediate Wnt5 signaling.…”

“…Studies in various model systems have shown that Wnt5 can bind to different receptors, including Frizzled, Ror2, CD146 and RYK, to activate JNK (Kumawat and Gosens, 2016;Fradkin et al, 2010;Nishita et al, 2010). A recent article reported that, in adult c4da neurons, Wnt5 acts through Drl and Drl2 to restrict the growth of dendrites within specific dendritic territories (Yasunaga et al, 2015). We show in this study that there are consistent dendritepruning defects in different drl or drl-2 mutant alleles, suggesting that Drl and Drl-2 may also be involved in dendrite pruning in c4da neurons.…”

“…In Drosophila, Wnt5 binds to the RYK (related-to-tyrosine-kinase) receptor Derailed (Drl) to regulate axon guidance and salivary gland development (Yoshikawa et al, 2003;Harris and Beckendorf, 2007). A recent study also demonstrated that both Drl and a closely related RYK receptor, Derailed-2 (Drl-2), have a partially redundant function in c4da neurons to mediate Wnt5 signaling to specify the dendritic territory of adult c4da neurons (Yasunaga et al, 2015). To investigate whether Wnt5 similarly functions through Drl and/or Drl-2 to regulate dendrite pruning of c4da neurons, we first examined whether Drl was expressed in larval c4da neurons.…”

Long-Term Memory inDrosophilaIs Influenced by Histone Deacetylase HDAC4 Interacting with SUMO-Conjugating Enzyme Ubc9

“…STRING analysis of the 26 genes identified in our screen revealed potential mechanistic links between HDAC4 and genes encoding proteins with nuclear functions (Smr, Gcn5, Sin3A, and CrebB), proteins involved in SUMOylation (Nup358 and Ubc9), and proteins that interact with the cytoskeleton or influence cytoskeletal growth (Moesin, Ankyrin, Ankyrin 2, Netrin-B, trio, Sra-1, derailed, and Prosap) (Figure 3). In neurons, the latter group of genes also regulates axon and/or dendritic growth (Harris et al 1996;Bonkowsky et al 1999;Schenck et al 2003;Lee et al 2007;Briancon-Marjollet et al 2008;Iyer et al 2012;Siegenthaler et al 2015;Yasunaga et al 2015).…”

Wnt signalling in the development of axon, dendrites and synapses

“…In zebrafish, tiling of left and right trigeminal ganglionic axons along the dorsal midline of the head depends on mutual repulsion between axons, and ablation of unilateral trigeminal ganglion results in the invasion of contralateral trigeminal ganglionic axons [ 77 ]. In adult Drosophila , the v'ada sensory neurons from the left and right sides of the body tile their sensory territories along the ventral midline with the nonoverlapping distribution of their dendrites [ 78 ] ( figure 3 c ). Interestingly, dendritic tiling of v'ada neurons does not depend on inter-neuronal repulsion; rather, repulsive Wnt5 signals from the ventral-most epidermal tissues keep dendrites away from the ventral midline [ 78 ] ( figure 3 c ).…”