Intestine-to-neuronal signaling alters risk-taking behaviors in food-deprived Caenorhabditis elegans

Animals integrate changes in external and internal environments to generate behavior. While neural circuits detecting external cues have been mapped, less is known about how internal states like hunger are integrated into behavioral outputs. Here, we use the nematode C. elegans to examine how change...

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Bibliographic Details
Published in:PLoS genetics 2022-05, Vol.18 (5), p.e1010178-e1010178
Main Authors: Matty, Molly A, Lau, Hiu E, Haley, Jessica A, Singh, Anupama, Chakraborty, Ahana, Kono, Karina, Reddy, Kirthi C, Hansen, Malene, Chalasani, Sreekanth H
Format: Article
Language:English
Subjects:
Animal behavior
Animals
Basic Helix-Loop-Helix Transcription Factors
Biology and Life Sciences
Caenorhabditis elegans
Caenorhabditis elegans - genetics
Caenorhabditis elegans Proteins - genetics
Cellular signal transduction
Chemoreception
Cytoplasm
Dietary restrictions
Food
Food and nutrition
Forkhead protein
Forkhead Transcription Factors
Genetic aspects
Hunger
Insulin
Intestine
Intestines
Medicine and Health Sciences
Nematodes
Nervous system
Neural networks
Neurons
Nutritional status
Physiological aspects
Research and Analysis Methods
Risk-Taking
Risk-taking (Psychology)
Social Sciences
Transcription factors
Transcription Factors - genetics
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Summary:Animals integrate changes in external and internal environments to generate behavior. While neural circuits detecting external cues have been mapped, less is known about how internal states like hunger are integrated into behavioral outputs. Here, we use the nematode C. elegans to examine how changes in internal nutritional status affect chemosensory behaviors. We show that acute food deprivation leads to a reversible decline in repellent, but not attractant, sensitivity. This behavioral change requires two conserved transcription factors MML-1 (MondoA) and HLH-30 (TFEB), both of which translocate from the intestinal nuclei to the cytoplasm during food deprivation. Next, we identify the insulin-like peptide INS-31 as a candidate ligand relaying food-status signals from the intestine to other tissues. Further, we show that neurons likely use the DAF-2 insulin receptor and AGE-1/PI-3 Kinase, but not DAF-16/FOXO to integrate these intestine-released peptides. Altogether, our study shows how internal food status signals are integrated by transcription factors and intestine-neuron signaling to generate flexible behaviors via the gut-brain axis.
ISSN:1553-7404
1553-7390
1553-7404
DOI:10.1371/journal.pgen.1010178