Sensing of the non-essential amino acid tyrosine governs the response to protein restriction in Drosophila

Kosakamoto, Hina; Okamoto, Naoki; Aikawa, Hide; Suematsu, Makoto; Niwa, Ryusuke; Miura, Masayuki; Obata, Fumiaki

doi:10.1038/s42255-022-00608-7

Cited by 20 publications

(18 citation statements)

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“…Metabolite are measured by LC-MS/MS as reported previously [ 18 , 49 ]. Briefly, approximately 100 mg of fly diet at/near the surface was picked up by a plastic straw and homogenized in 150 μL of 80% methanol containing 10 μM of internal standards (methionine sulfone and 2-morpholinoethanesulfonic acid), and deproteinized by mixing with 75 μL of acetonitrile.…”

Section: Methodsmentioning

confidence: 99%

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Recognition of commensal bacterial peptidoglycans defines Drosophila gut homeostasis and lifespan

et al. 2023

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Commensal microbes in animals have a profound impact on tissue homeostasis, stress resistance, and ageing. We previously showed in Drosophila melanogaster that Acetobacter persici is a member of the gut microbiota that promotes ageing and shortens fly lifespan. However, the molecular mechanism by which this specific bacterial species changes lifespan and physiology remains unclear. The difficulty in studying longevity using gnotobiotic flies is the high risk of contamination during ageing. To overcome this technical challenge, we used a bacteria-conditioned diet enriched with bacterial products and cell wall components. Here, we demonstrate that an A. persici-conditioned diet shortens lifespan and increases intestinal stem cell (ISC) proliferation. Feeding adult flies a diet conditioned with A. persici, but not with Lactiplantibacillus plantarum, can decrease lifespan but increase resistance to paraquat or oral infection of Pseudomonas entomophila, indicating that the bacterium alters the trade-off between lifespan and host defence. A transcriptomic analysis using fly intestine revealed that A. persici preferably induces antimicrobial peptides (AMPs), while L. plantarum upregulates amidase peptidoglycan recognition proteins (PGRPs). The specific induction of these Imd target genes by peptidoglycans from two bacterial species is due to the stimulation of the receptor PGRP-LC in the anterior midgut for AMPs or PGRP-LE from the posterior midgut for amidase PGRPs. Heat-killed A. persici also shortens lifespan and increases ISC proliferation via PGRP-LC, but it is not sufficient to alter the stress resistance. Our study emphasizes the significance of peptidoglycan specificity in determining the gut bacterial impact on healthspan. It also unveils the postbiotic effect of specific gut bacterial species, which turns flies into a "live fast, die young" lifestyle.

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Section: Methodsmentioning

confidence: 99%

“…For transcriptomic analysis, 3’ RNA-seq analysis was performed as previously described [ 49 ]. Briefly, the guts of w Dah flies were dissected.…”

Section: Methodsmentioning

confidence: 99%

Recognition of commensal bacterial peptidoglycans defines Drosophila gut homeostasis and lifespan

et al. 2023

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“…Flies were transferred to a modified version of holidic medium (Kosakamoto et al, 2022) supplemented with 3.82 mM d 8 -Met (Cambridge Isotope Laboratories: DLM-6797-0.1) instead of Met, for up to 48 h prior to dissection unless otherwise stated. Third instar larvae or one-week-old adult Drosophila were placed in Frontiers in Chemistry frontiersin.org phosphate buffered saline (PBS) (4 °C) dissected using forceps (Dumont, Inox, #5) under a dissecting microscope.…”

Section: Sample Preparation For Srs Imaging Of Drosophila Tissuementioning

confidence: 99%

Imaging the uptake of deuterated methionine in Drosophila with stimulated Raman scattering

Spratt

Mizuguchi²,

Akaboshi³

et al. 2023

Front. Chem.

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Introduction: Visualizing small individual biomolecules at subcellular resolution in live cells and tissues can provide valuable insights into metabolic activity in heterogeneous cells, but is challenging.Methods: Here, we used stimulated Raman scattering (SRS) microscopy to image deuterated methionine (d-Met) incorporated into Drosophila tissues in vivo.Results: Our results demonstrate that SRS can detect a range of previously uncharacterized cell-to-cell differences in d-Met distribution within a tissue at the subcellular level.Discussion: These results demonstrate the potential of SRS microscopy for metabolic imaging of less abundant but important amino acids such as methionine in tissue.

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“…Tyrosine is a nonessential amino acid critical for catecholamine and melanin synthesis in addition to protein synthesis. Previously, we revealed that tyrosine (Tyr) plays a crucial role in sensing dietary protein sufficiency (Kosakamoto et al, 2022). The scarcity of Tyr is perceived through activating transcription factor 4 (ATF4) in the fat body, which alters protein synthesis, mTORC1 signalling, and feeding behaviour.…”

Section: Introductionmentioning

confidence: 99%

Epidermal tyrosine catabolism is critical for metabolic homeostasis and survival against high-protein diets inDrosophila

Kosakamoto

Miura

Obata

2023

Preprint

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The insect epidermis that forms the exoskeleton and determines the body size of an organism has the potential to respond and adapt to the changing nutritional environment. However, the extent to which the tissue contributes to adaptation to varying dietary protein availability, as well as its role as a metabolic regulator, remains incompletely understood. Here, we show that the Drosophila epidermis promptly reacts to dietary protein intake, promoting tyrosine (Tyr) catabolism. Among the enzymes involved in Tyr degradation, 4-hydroxyphenylpyruvate dioxygenase (Hpd) is particularly induced under high-protein regimens. We found that AMP-activated protein kinase (AMPK) pathway and forkhead box O subfamily (FoxO) induce Hpd expression. Impaired Hpd function in the epidermis leads to aberrant increases in internal Tyr levels and its metabolites, disrupting larval development under high-protein diets. Taken together, our findings uncover the critical role of epidermal metabolism in adapting to imbalanced protein environments and hence in promoting animal survival.

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Sensing of the non-essential amino acid tyrosine governs the response to protein restriction in Drosophila

Cited by 20 publications

References 73 publications

Recognition of commensal bacterial peptidoglycans defines Drosophila gut homeostasis and lifespan

Recognition of commensal bacterial peptidoglycans defines Drosophila gut homeostasis and lifespan

Imaging the uptake of deuterated methionine in Drosophila with stimulated Raman scattering

Epidermal tyrosine catabolism is critical for metabolic homeostasis and survival against high-protein diets inDrosophila

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