Internal amino acid state modulates yeast taste neurons to support protein homeostasis in Drosophila

  1. Kathrin Steck
  2. Samuel J Walker
  3. Pavel M Itskov
  4. Celia Baltazar
  5. José-Maria Moreira
  6. Carlos Ribeiro  Is a corresponding author
  1. Champalimaud Centre for the Unknown, Portugal

Abstract

To optimize fitness, animals must dynamically match food choices to their current needs. For drosophilids, yeast fulfils most dietary protein and micronutrient requirements. While several yeast metabolites activate known gustatory receptor neurons (GRNs) in Drosophila melanogaster, the chemosensory channels mediating yeast feeding remain unknown. Here we identify a class of proboscis GRNs required for yeast intake. Within this class, taste peg GRNs are specifically required to sustain yeast feeding. Sensillar GRNs, however, mediate feeding initiation. Furthermore, the response of yeast GRNs, but not sweet GRNs, is enhanced following deprivation from amino acids, providing a potential basis for protein-specific appetite. Although nutritional and reproductive states synergistically increase yeast appetite, reproductive state acts independently of nutritional state, modulating processing downstream of GRNs. Together, these results suggest that different internal states act at distinct levels of a dedicated gustatory circuit to elicit nutrient-specific appetites towards a complex, ecologically relevant protein source.

Article and author information

Author details

  1. Kathrin Steck

    Champalimaud Research, Champalimaud Centre for the Unknown, Lisbon, Portugal
    Competing interests
    No competing interests declared.
  2. Samuel J Walker

    Champalimaud Research, Champalimaud Centre for the Unknown, Lisbon, Portugal
    Competing interests
    No competing interests declared.
  3. Pavel M Itskov

    Champalimaud Research, Champalimaud Centre for the Unknown, Lisbon, Portugal
    Competing interests
    Pavel M Itskov, PMI has a commercial interest in the flyPAD open-source technology.
  4. Celia Baltazar

    Champalimaud Research, Champalimaud Centre for the Unknown, Lisbon, Portugal
    Competing interests
    No competing interests declared.
  5. José-Maria Moreira

    Champalimaud Research, Champalimaud Centre for the Unknown, Lisbon, Portugal
    Competing interests
    No competing interests declared.
  6. Carlos Ribeiro

    Champalimaud Research, Champalimaud Centre for the Unknown, Lisbon, Portugal
    For correspondence
    carlos.ribeiro@neuro.fchampalimaud.org
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9542-7335

Funding

Fundação para a Ciência e a Tecnologia (PTDC/BIA-BCM/118684/2010)

  • Carlos Ribeiro

Fundação para a Ciência e a Tecnologia (SFRH/BPD/79325/2011)

  • Pavel M Itskov

Human Frontier Science Program (RGP0022/2012)

  • Carlos Ribeiro

Fundação Bial (283/14)

  • Carlos Ribeiro

Fundação Bial (279/16)

  • Carlos Ribeiro

European Commission (FLiACT ITN)

  • Carlos Ribeiro

Champalimaud Foundation

  • Carlos Ribeiro

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Mani Ramaswami, Trinity College Dublin, Ireland

Publication history

  1. Received: August 30, 2017
  2. Accepted: January 19, 2018
  3. Accepted Manuscript published: February 2, 2018 (version 1)
  4. Version of Record published: February 14, 2018 (version 2)

Copyright

© 2018, Steck et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 5,954
    Page views
  • 892
    Downloads
  • 56
    Citations

Article citation count generated by polling the highest count across the following sources: Scopus, Crossref, PubMed Central.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Kathrin Steck
  2. Samuel J Walker
  3. Pavel M Itskov
  4. Celia Baltazar
  5. José-Maria Moreira
  6. Carlos Ribeiro
(2018)
Internal amino acid state modulates yeast taste neurons to support protein homeostasis in Drosophila
eLife 7:e31625.
https://doi.org/10.7554/eLife.31625
  1. Further reading

Further reading

    1. Developmental Biology
    2. Neuroscience
    Tanya L Brown, Emma C Horton ... Jeffrey P Rasmussen
    Research Article Updated

    Touch system function requires precise interactions between specialized skin cells and somatosensory axons, as exemplified by the vertebrate mechanosensory Merkel cell-neurite complex. Development and patterning of Merkel cells and associated neurites during skin organogenesis remain poorly understood, partly due to the in utero development of mammalian embryos. Here, we discover Merkel cells in the zebrafish epidermis and identify Atonal homolog 1a (Atoh1a) as a marker of zebrafish Merkel cells. We show that zebrafish Merkel cells derive from basal keratinocytes, express neurosecretory and mechanosensory machinery, extend actin-rich microvilli, and complex with somatosensory axons, all hallmarks of mammalian Merkel cells. Merkel cells populate all major adult skin compartments, with region-specific densities and distribution patterns. In vivo photoconversion reveals that Merkel cells undergo steady loss and replenishment during skin homeostasis. Merkel cells develop concomitant with dermal appendages along the trunk and loss of Ectodysplasin signaling, which prevents dermal appendage formation, reduces Merkel cell density by affecting cell differentiation. By contrast, altering dermal appendage morphology changes the distribution, but not density, of Merkel cells. Overall, our studies provide insights into touch system maturation during skin organogenesis and establish zebrafish as an experimentally accessible in vivo model for the study of Merkel cell biology.

    1. Chromosomes and Gene Expression
    2. Neuroscience
    Tooba Abbassi-Daloii, Salma el Abdellaoui ... Vered Raz
    Tools and Resources

    Skeletal muscles support the stability and mobility of the skeleton but differ in biomechanical properties and physiological functions. The intrinsic factors that regulate muscle-specific characteristics are poorly understood. To study these, we constructed a large atlas of RNA-seq profiles from six leg muscles and two locations from one muscle, using biopsies from 20 healthy young males. We identified differential expression patterns and cellular composition across the seven tissues using three bioinformatics approaches confirmed by large-scale newly developed quantitative immune-histology procedures. With all three procedures, the muscle samples clustered into three groups congruent with their anatomical location. Concomitant with genes marking oxidative metabolism, genes marking fast- or slow-twitch myofibers differed between the three groups. The groups of muscles with higher expression of slow-twitch genes were enriched in endothelial cells and showed higher capillary content. In addition, expression profiles of Homeobox (HOX) transcription factors differed between the three groups and were confirmed by spatial RNA hybridization. We created an open-source graphical interface to explore and visualize the leg muscle atlas (https://tabbassidaloii.shinyapps.io/muscleAtlasShinyApp/). Our study reveals the molecular specialization of human leg muscles, and provides a novel resource to study muscle-specific molecular features, which could be linked with (patho)physiological processes.