Nutrigenomic regulation of sensory plasticity

Diet profoundly influences brain physiology, but how metabolic information is transmuted into neural activity and behavior changes remains elusive. Here, we show that the metabolic enzyme O-GlcNAc Transferase (OGT) moonlights on the chromatin of the D. melanogaster gustatory neurons to instruct chan...

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Main Authors: Hayeon Sung, Anoumid Vaziri, Daniel Wilinski, Riley KR Woerner, Lydia Freddolino, Monica Dus
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2023-03-01
Series:eLife
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Online Access:https://elifesciences.org/articles/83979
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author Hayeon Sung
Anoumid Vaziri
Daniel Wilinski
Riley KR Woerner
Lydia Freddolino
Monica Dus
author_facet Hayeon Sung
Anoumid Vaziri
Daniel Wilinski
Riley KR Woerner
Lydia Freddolino
Monica Dus
author_sort Hayeon Sung
collection DOAJ
description Diet profoundly influences brain physiology, but how metabolic information is transmuted into neural activity and behavior changes remains elusive. Here, we show that the metabolic enzyme O-GlcNAc Transferase (OGT) moonlights on the chromatin of the D. melanogaster gustatory neurons to instruct changes in chromatin accessibility and transcription that underlie sensory adaptations to a high-sugar diet. OGT works synergistically with the Mitogen Activated Kinase/Extracellular signal Regulated Kinase (MAPK/ERK) rolled and its effector stripe (also known as EGR2 or Krox20) to integrate activity information. OGT also cooperates with the epigenetic silencer Polycomb Repressive Complex 2.1 (PRC2.1) to decrease chromatin accessibility and repress transcription in the high-sugar diet. This integration of nutritional and activity information changes the taste neurons’ responses to sugar and the flies’ ability to sense sweetness. Our findings reveal how nutrigenomic signaling generates neural activity and behavior in response to dietary changes in the sensory neurons.
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spelling doaj-art-76b83b9ae22541ebb6a83c7482031a662025-01-24T14:07:07ZengeLife Sciences Publications LtdeLife2050-084X2023-03-011210.7554/eLife.83979Nutrigenomic regulation of sensory plasticityHayeon Sung0https://orcid.org/0000-0002-9015-8877Anoumid Vaziri1Daniel Wilinski2Riley KR Woerner3https://orcid.org/0009-0000-0702-138XLydia Freddolino4https://orcid.org/0000-0002-5821-4226Monica Dus5https://orcid.org/0000-0003-1465-9028Department of Molecular, Cellular and Developmental Biology, College of Literature, Science, and the Arts, The University of Michigan, Ann Arbor, United StatesDepartment of Molecular, Cellular and Developmental Biology, College of Literature, Science, and the Arts, The University of Michigan, Ann Arbor, United States; The Molecular, Cellular and Developmental Biology Graduate Program, The University of Michigan, Ann Arbor, United StatesDepartment of Molecular, Cellular and Developmental Biology, College of Literature, Science, and the Arts, The University of Michigan, Ann Arbor, United StatesDepartment of Molecular, Cellular and Developmental Biology, College of Literature, Science, and the Arts, The University of Michigan, Ann Arbor, United StatesDepartment of Biological Chemistry, The University of Michigan Medical School, Ann Arbor, United States; Department of Computational Medicine and Bioinformatics, The University of Michigan Medical School, Ann Arbor, United StatesDepartment of Molecular, Cellular and Developmental Biology, College of Literature, Science, and the Arts, The University of Michigan, Ann Arbor, United States; The Molecular, Cellular and Developmental Biology Graduate Program, The University of Michigan, Ann Arbor, United States; The Michigan Neuroscience Institute, Ann Arbor, United StatesDiet profoundly influences brain physiology, but how metabolic information is transmuted into neural activity and behavior changes remains elusive. Here, we show that the metabolic enzyme O-GlcNAc Transferase (OGT) moonlights on the chromatin of the D. melanogaster gustatory neurons to instruct changes in chromatin accessibility and transcription that underlie sensory adaptations to a high-sugar diet. OGT works synergistically with the Mitogen Activated Kinase/Extracellular signal Regulated Kinase (MAPK/ERK) rolled and its effector stripe (also known as EGR2 or Krox20) to integrate activity information. OGT also cooperates with the epigenetic silencer Polycomb Repressive Complex 2.1 (PRC2.1) to decrease chromatin accessibility and repress transcription in the high-sugar diet. This integration of nutritional and activity information changes the taste neurons’ responses to sugar and the flies’ ability to sense sweetness. Our findings reveal how nutrigenomic signaling generates neural activity and behavior in response to dietary changes in the sensory neurons.https://elifesciences.org/articles/83979sensory neurosciencegene regulationnutrition
spellingShingle Hayeon Sung
Anoumid Vaziri
Daniel Wilinski
Riley KR Woerner
Lydia Freddolino
Monica Dus
Nutrigenomic regulation of sensory plasticity
eLife
sensory neuroscience
gene regulation
nutrition
title Nutrigenomic regulation of sensory plasticity
title_full Nutrigenomic regulation of sensory plasticity
title_fullStr Nutrigenomic regulation of sensory plasticity
title_full_unstemmed Nutrigenomic regulation of sensory plasticity
title_short Nutrigenomic regulation of sensory plasticity
title_sort nutrigenomic regulation of sensory plasticity
topic sensory neuroscience
gene regulation
nutrition
url https://elifesciences.org/articles/83979
work_keys_str_mv AT hayeonsung nutrigenomicregulationofsensoryplasticity
AT anoumidvaziri nutrigenomicregulationofsensoryplasticity
AT danielwilinski nutrigenomicregulationofsensoryplasticity
AT rileykrwoerner nutrigenomicregulationofsensoryplasticity
AT lydiafreddolino nutrigenomicregulationofsensoryplasticity
AT monicadus nutrigenomicregulationofsensoryplasticity