Nutrient‐dependent increased dendritic arborization of somatosensory neurons

Abstract

Suboptimal nutrition imposes developmental constraints on infant animals, which marshal adaptive responses to eventually become mature adults. Such responses are mounted at multiple levels from systemic to cellular. At the cellular level, the underlying mechanisms of cell proliferation control have been intensively studied. However, less is known about how growth of postmitotic and morphologically complex cells, such as neurons, is controlled by nutritional status. We address this question using Class I and Class IV dendritic arborization neurons in Drosophila larvae. Class IV neurons have been shown to sense nociceptive thermal, mechanical and light stimuli, whereas Class I neurons are proprioceptors. We reared larvae on diets with different protein and carbohydrate content throughout larval stages and examined how morphologies of Class I or Class IV neurons were affected. Dendritic arbors of Class IV neurons became more complex when larvae were reared on a low-yeast diet, which contains lower amounts of amino acids and other ingredients, compared to a high-yeast diet. In contrast, such low-yeast-dependent hyperarborization was not seen in Class I neurons. The physiological and metabolic implications of the hyperarborization phenotype are discussed in relation to a recent hypothesis that Class IV neurons sense protein-deficient stress and to our characterization of how the dietary yeast contents impacted larval metabolism.

Low FoxO expression inDrosophilasomatosensory neurons protects dendrite growth under nutrient restriction

“…We asked whether nutrient stress also impacts dendritic growth of C1da and C3da neurons. Consistent with the previous report by Watanabe et al (Watanabe et al, 2017), the yeast concentration did not have obvious effects on the total dendrite length of C1da neuron ddaE (Figures 7A-7C). However, nutrient stress stimulated the dendritic growth of C3da neurons ddaA and ddaF: the total dendrite length increased by 40% and 32%, respectively; the total terminal dendrite length increased by 61% and 46%, respectively; the terminal branch numbers increased by 47% and 58%, respectively (Figures 7D-7H).…”

“…A recent study by Watanabe et al (2017) reported that C4da neurons were hyperarborized when Drosophila larvae developed on a low yeast diet that restricts the availability of lipids and amino acids, an interesting and surprising finding that agrees with our independent observation. In our experiments, we examined larvae reared in high yeast (HY, 8% yeast) and low yeast (LY, 1% yeast) media that otherwise contained only glucose as a carbon source.…”

“…Da neurons are categorized into four classes that differ in their dendrite morphology and transcription factor expression (Grueber et al, 2002; Hattori et al, 2013). Recently, class IV da (C4da) neurons, which completely cover the body surface and thus are called “space-filling” neurons (Grueber et al, 2002; Grueber et al, 2003), were found to elaborate more dendrite branches when larvae develop on a low-nutrient diet (Watanabe et al, 2017), suggesting that dendritic scaling of C4da neurons is regulated by the nutrient state. However, whether this dendritic hyperarborization is related to organ sparing and how nutrient stress promotes dendrite growth are unclear.…”

DeTerm: Software for automatic detection of neuronal dendritic branch terminals via an artificial neural network

“…Input files consisted of original image data (8‐bit and 1,024 × 1,024 pixels) of larval class IV neurons on HYD or LYD (8% and 0.8% Y diet in Watanabe et al, , respectively) and a region of interest (ROI) of each image. We used Adobe Photoshop to define the ROI by drawing a path using a pen tool and filling the path with red color.…”

“…Marker strains employed were ppk-GAL4 UAS-mCD8:GFP (Grueber et al, 2007) and Gr28b.c-GAL4 UAS-mCD8:GFP (Xiang et al, 2010). Preparing diets and rearing flies were performed as described (Watanabe et al, 2017). All of the crosses and experiments were conducted under noncrowded conditions at 25°C.…”