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Serotonin and dopamine modulate aging in response to food odor and availability

Author

Listed:
  • Hillary A. Miller

    (University of Michigan)

  • Shijiao Huang

    (University of Michigan)

  • Elizabeth S. Dean

    (University of Michigan)

  • Megan L. Schaller

    (University of Michigan)

  • Angela M. Tuckowski

    (University of Michigan)

  • Allyson S. Munneke

    (University of Michigan)

  • Safa Beydoun

    (University of Michigan)

  • Scott D. Pletcher

    (University of Michigan)

  • Scott F. Leiser

    (University of Michigan
    University of Michigan)

Abstract

An organism’s ability to perceive and respond to changes in its environment is crucial for its health and survival. Here we reveal how the most well-studied longevity intervention, dietary restriction, acts in-part through a cell non-autonomous signaling pathway that is inhibited by the presence of attractive smells. Using an intestinal reporter for a key gene induced by dietary restriction but suppressed by attractive smells, we identify three compounds that block food odor effects in C. elegans, thereby increasing longevity as dietary restriction mimetics. These compounds clearly implicate serotonin and dopamine in limiting lifespan in response to food odor. We further identify a chemosensory neuron that likely perceives food odor, an enteric neuron that signals through the serotonin receptor 5-HT1A/SER-4, and a dopaminergic neuron that signals through the dopamine receptor DRD2/DOP-3. Aspects of this pathway are conserved in D. melanogaster. Thus, blocking food odor signaling through antagonism of serotonin or dopamine receptors is a plausible approach to mimic the benefits of dietary restriction.

Suggested Citation

  • Hillary A. Miller & Shijiao Huang & Elizabeth S. Dean & Megan L. Schaller & Angela M. Tuckowski & Allyson S. Munneke & Safa Beydoun & Scott D. Pletcher & Scott F. Leiser, 2022. "Serotonin and dopamine modulate aging in response to food odor and availability," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-30869-5
    DOI: 10.1038/s41467-022-30869-5
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    References listed on IDEAS

    as
    1. Nicholas A. Bishop & Leonard Guarente, 2007. "Two neurons mediate diet-restriction-induced longevity in C. elegans," Nature, Nature, vol. 447(7144), pages 545-549, May.
    2. Ji Ying Sze & Martin Victor & Curtis Loer & Yang Shi & Gary Ruvkun, 2000. "Food and metabolic signalling defects in a Caenorhabditis elegans serotonin-synthesis mutant," Nature, Nature, vol. 403(6769), pages 560-564, February.
    3. Kyung Suk Lee & Shachar Iwanir & Ronen B. Kopito & Monika Scholz & John A. Calarco & David Biron & Erel Levine, 2017. "Serotonin-dependent kinetics of feeding bursts underlie a graded response to food availability in C. elegans," Nature Communications, Nature, vol. 8(1), pages 1-11, April.
    4. Michael Petrascheck & Xiaolan Ye & Linda B. Buck, 2007. "An antidepressant that extends lifespan in adult Caenorhabditis elegans," Nature, Nature, vol. 450(7169), pages 553-556, November.
    5. Paul D. Wes & Cornelia I. Bargmann, 2001. "C. elegans odour discrimination requires asymmetric diversity in olfactory neurons," Nature, Nature, vol. 410(6829), pages 698-701, April.
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