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Differential Effects of Tissue-Specific Deletion of BOSS on Feeding Behaviors and Energy Metabolism.

Kohyama-Koganeya A, Kurosawa M, Hirabayashi Y - PLoS ONE (2015)

Bottom Line: Boss mutants exhibited increased food intake but decreased stored triacylglyceride levels.Using boss-GAL4 drivers, we found that boss is expressed in select tissues that are involved in nutrient sensing and food intake, in a subset of neurons in brain and chemosensory organs, in fat body, and in endocrine cells in gut (enteroendocrine cells).These results suggest that BOSS in either neurons or peripheral nutrient-sensing tissues affects energy homeostasis in ways that relate to the sensing of nutrients and regulation of food intake.

View Article: PubMed Central - PubMed

Affiliation: Molecular Membrane Neuroscience, Brain Science Institute, RIKEN, Wako-shi, Saitama, Japan.

ABSTRACT
Food intake and energy metabolism are tightly controlled to maintain stable energy homeostasis and healthy states. Thus, animals detect their stored energy levels, and based on this, they determine appropriate food intake and meal size. Drosophila melanogaster putative G protein-coupled receptor, Bride of sevenless (BOSS) is a highly evolutionarily conserved protein that responds to extracellular glucose levels in order to regulate energy homeostasis. To address how BOSS regulates energy homeostasis, we characterized a boss mutant by assessing its food intake and stored energy levels. Boss mutants exhibited increased food intake but decreased stored triacylglyceride levels. Using boss-GAL4 drivers, we found that boss is expressed in select tissues that are involved in nutrient sensing and food intake, in a subset of neurons in brain and chemosensory organs, in fat body, and in endocrine cells in gut (enteroendocrine cells). Flies with tissue-specific boss knockdowns in these tissues had abnormal stored energy levels and abnormal food intake. These results suggest that BOSS in either neurons or peripheral nutrient-sensing tissues affects energy homeostasis in ways that relate to the sensing of nutrients and regulation of food intake.

No MeSH data available.


Related in: MedlinePlus

BOSS is expressed in nutrient-sensing tissues.Expression of boss in larval and adult flies was visualized by expression of 10xUAS-mCD8.GFP and UAS-mCherryNLS using a boss-GAL4 driver. (A-C) Expression in larval (A) and adult (B) sensory organs. (C) Adult foreleg. (D) Larval CNS. (E) Adult brain. (F) Adult thoracic ganglion. To identify the locations of boss-expressing cells, UAS-mCherryNLS (magenta) was coexpressed with 10xUAS-mCD8.GFP [9] in the brain and sensory organs. The CNS was also labeled with antibody nc82 (blue), a marker that labels synapses. Larval (G) and adult (H) midgut. The gut was counterstained with DAPI (blue) and a marker for enteroendocrine cells, prospero (magenta). Arrowheads show the prospero-positive GFP-expressing cells. See also S2 Fig. Larval (I) and adult (J) fat body. The fat body was counterstained with DAPI (blue), a cell nucleus marker. Scale bars; 500 μm in A, 30 μm in B, 200 μm in C and E, 100 μm in G, H and J, 80 μm in D, 50 μm in H.
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pone.0133083.g004: BOSS is expressed in nutrient-sensing tissues.Expression of boss in larval and adult flies was visualized by expression of 10xUAS-mCD8.GFP and UAS-mCherryNLS using a boss-GAL4 driver. (A-C) Expression in larval (A) and adult (B) sensory organs. (C) Adult foreleg. (D) Larval CNS. (E) Adult brain. (F) Adult thoracic ganglion. To identify the locations of boss-expressing cells, UAS-mCherryNLS (magenta) was coexpressed with 10xUAS-mCD8.GFP [9] in the brain and sensory organs. The CNS was also labeled with antibody nc82 (blue), a marker that labels synapses. Larval (G) and adult (H) midgut. The gut was counterstained with DAPI (blue) and a marker for enteroendocrine cells, prospero (magenta). Arrowheads show the prospero-positive GFP-expressing cells. See also S2 Fig. Larval (I) and adult (J) fat body. The fat body was counterstained with DAPI (blue), a cell nucleus marker. Scale bars; 500 μm in A, 30 μm in B, 200 μm in C and E, 100 μm in G, H and J, 80 μm in D, 50 μm in H.

Mentions: Live fluorescence imaging and immunohistochemistry showed that GFP and mCherry were expressed in tissues known to be involved in nutrient sensing and food intake (Fig 4). For example, GFP and mCherry expression were detected in chemosensory neurons of five specific chemosensory organs: the dorsal and ventral pharyngeal organ, the ventral pits of larvae, the antennae, the proboscis, and the legs of adults (Fig 4A–4C). Second, GFP and mCherry expression were detected in specific neurons of the central nervous system (CNS) (Fig 4D–4F). Third, GFP expression was detected in peripheral tissues, specifically, subsets of cells in the gut and the fat body (Fig 4G–4J). Most of these GFP-labeled cells in the midgut were co-labeled with the enteroendocrine cell marker prospero (93% in larva, and 98% in adult) (Fig 4G and 4H, S2 Fig), suggesting that boss-GAL4 expressing cells in the gut are subsets of enteroendocrine cells.


Differential Effects of Tissue-Specific Deletion of BOSS on Feeding Behaviors and Energy Metabolism.

Kohyama-Koganeya A, Kurosawa M, Hirabayashi Y - PLoS ONE (2015)

BOSS is expressed in nutrient-sensing tissues.Expression of boss in larval and adult flies was visualized by expression of 10xUAS-mCD8.GFP and UAS-mCherryNLS using a boss-GAL4 driver. (A-C) Expression in larval (A) and adult (B) sensory organs. (C) Adult foreleg. (D) Larval CNS. (E) Adult brain. (F) Adult thoracic ganglion. To identify the locations of boss-expressing cells, UAS-mCherryNLS (magenta) was coexpressed with 10xUAS-mCD8.GFP [9] in the brain and sensory organs. The CNS was also labeled with antibody nc82 (blue), a marker that labels synapses. Larval (G) and adult (H) midgut. The gut was counterstained with DAPI (blue) and a marker for enteroendocrine cells, prospero (magenta). Arrowheads show the prospero-positive GFP-expressing cells. See also S2 Fig. Larval (I) and adult (J) fat body. The fat body was counterstained with DAPI (blue), a cell nucleus marker. Scale bars; 500 μm in A, 30 μm in B, 200 μm in C and E, 100 μm in G, H and J, 80 μm in D, 50 μm in H.
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pone.0133083.g004: BOSS is expressed in nutrient-sensing tissues.Expression of boss in larval and adult flies was visualized by expression of 10xUAS-mCD8.GFP and UAS-mCherryNLS using a boss-GAL4 driver. (A-C) Expression in larval (A) and adult (B) sensory organs. (C) Adult foreleg. (D) Larval CNS. (E) Adult brain. (F) Adult thoracic ganglion. To identify the locations of boss-expressing cells, UAS-mCherryNLS (magenta) was coexpressed with 10xUAS-mCD8.GFP [9] in the brain and sensory organs. The CNS was also labeled with antibody nc82 (blue), a marker that labels synapses. Larval (G) and adult (H) midgut. The gut was counterstained with DAPI (blue) and a marker for enteroendocrine cells, prospero (magenta). Arrowheads show the prospero-positive GFP-expressing cells. See also S2 Fig. Larval (I) and adult (J) fat body. The fat body was counterstained with DAPI (blue), a cell nucleus marker. Scale bars; 500 μm in A, 30 μm in B, 200 μm in C and E, 100 μm in G, H and J, 80 μm in D, 50 μm in H.
Mentions: Live fluorescence imaging and immunohistochemistry showed that GFP and mCherry were expressed in tissues known to be involved in nutrient sensing and food intake (Fig 4). For example, GFP and mCherry expression were detected in chemosensory neurons of five specific chemosensory organs: the dorsal and ventral pharyngeal organ, the ventral pits of larvae, the antennae, the proboscis, and the legs of adults (Fig 4A–4C). Second, GFP and mCherry expression were detected in specific neurons of the central nervous system (CNS) (Fig 4D–4F). Third, GFP expression was detected in peripheral tissues, specifically, subsets of cells in the gut and the fat body (Fig 4G–4J). Most of these GFP-labeled cells in the midgut were co-labeled with the enteroendocrine cell marker prospero (93% in larva, and 98% in adult) (Fig 4G and 4H, S2 Fig), suggesting that boss-GAL4 expressing cells in the gut are subsets of enteroendocrine cells.

Bottom Line: Boss mutants exhibited increased food intake but decreased stored triacylglyceride levels.Using boss-GAL4 drivers, we found that boss is expressed in select tissues that are involved in nutrient sensing and food intake, in a subset of neurons in brain and chemosensory organs, in fat body, and in endocrine cells in gut (enteroendocrine cells).These results suggest that BOSS in either neurons or peripheral nutrient-sensing tissues affects energy homeostasis in ways that relate to the sensing of nutrients and regulation of food intake.

View Article: PubMed Central - PubMed

Affiliation: Molecular Membrane Neuroscience, Brain Science Institute, RIKEN, Wako-shi, Saitama, Japan.

ABSTRACT
Food intake and energy metabolism are tightly controlled to maintain stable energy homeostasis and healthy states. Thus, animals detect their stored energy levels, and based on this, they determine appropriate food intake and meal size. Drosophila melanogaster putative G protein-coupled receptor, Bride of sevenless (BOSS) is a highly evolutionarily conserved protein that responds to extracellular glucose levels in order to regulate energy homeostasis. To address how BOSS regulates energy homeostasis, we characterized a boss mutant by assessing its food intake and stored energy levels. Boss mutants exhibited increased food intake but decreased stored triacylglyceride levels. Using boss-GAL4 drivers, we found that boss is expressed in select tissues that are involved in nutrient sensing and food intake, in a subset of neurons in brain and chemosensory organs, in fat body, and in endocrine cells in gut (enteroendocrine cells). Flies with tissue-specific boss knockdowns in these tissues had abnormal stored energy levels and abnormal food intake. These results suggest that BOSS in either neurons or peripheral nutrient-sensing tissues affects energy homeostasis in ways that relate to the sensing of nutrients and regulation of food intake.

No MeSH data available.


Related in: MedlinePlus