Drosophila TRPg is required in neuroendocrine cells for post-ingestive food selection

  1. Subash Dhakal
  2. Qiuting Ren
  3. Jiangqu Liu
  4. Bradley Akitake
  5. Izel Tekin
  6. Craig Montell  Is a corresponding author
  7. Youngseok Lee  Is a corresponding author
  1. Kookmin University, Republic of Korea
  2. Johns Hopkins University School of Medicine, United States
  3. University of California, Santa Barbara, United States

Abstract

The mechanism through which the brain senses the metabolic state, enabling an animal to regulate food consumption, and discriminate between nutritional and non-nutritional foods is a fundamental question. Flies choose the sweeter non-nutritive sugar, L-glucose, over the nutritive D-glucose if they are not starved. However, under starvation conditions, they switch their preference to D-glucose, and this occurs independent of peripheral taste neurons. Here, we found that eliminating the TRPγ channel impairs the ability of starved flies to choose D-glucose. This food selection depends on trpγ expression in neurosecretory cells in the brain that express Diuretic hormone 44 (DH44). Loss of trpγ increases feeding, alters the physiology of the crop, which is the fly stomach equivalent, and decreases intracellular sugars and glycogen levels. Moreover, survival of starved trpγ flies is reduced. Expression of trpγ in DH44 neurons reverses these deficits. These results highlight roles for TRPγ in coordinating feeding with the metabolic state through expression in DH44 neuroendocrine cells.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for Figures 1-7, and Figure supplements 1-7.

Article and author information

Author details

  1. Subash Dhakal

    Department of Bio and Fermentation Convergence Technology, Kookmin University, Seoul, Republic of Korea
    Competing interests
    The authors declare that no competing interests exist.
  2. Qiuting Ren

    Department of Biological Chemistry, Johns Hopkins University School of Medicine, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Jiangqu Liu

    Department of Molecular, Cellular and Developmental Biology, University of California, Santa Barbara, Santa Barbara, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Bradley Akitake

    Department of Molecular, Cellular and Developmental Biology, University of California, Santa Barbara, Santa Barbara, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Izel Tekin

    Department of Molecular, Cellular and Developmental Biology, University of California, Santa Barbara, Santa Barbara, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Craig Montell

    Department of Molecular, Cellular and Developmental Biology, University of California, Santa Barbara, Santa Barbara, United States
    For correspondence
    cmontell@ucsb.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5637-1482
  7. Youngseok Lee

    Bio and Fermentation Convergence Technology, Kookmin University, Seoul, Republic of Korea
    For correspondence
    iven1125@gmail.com
    Competing interests
    The authors declare that no competing interests exist.

Funding

National Institute on Deafness and Other Communication Disorders (DC007864)

  • Craig Montell

National Institute of Allergy and Infectious Diseases (AI65575)

  • Craig Montell

National Institute of Allergy and Infectious Diseases (AI169386)

  • Craig Montell

National Research Foundation of Korea (NRF-2018R1A2B6004202)

  • Youngseok Lee

National Research Foundation of Korea (NRF-2016R1D1A1B03931273)

  • Youngseok Lee

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

Reviewing Editor

  1. Claude Desplan, New York University, United States

Version history

  1. Received: March 7, 2020
  2. Accepted: April 12, 2022
  3. Accepted Manuscript published: April 13, 2022 (version 1)
  4. Version of Record published: May 4, 2022 (version 2)

Copyright

© 2022, Dhakal 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

  • 1,832
    Page views
  • 301
    Downloads
  • 5
    Citations

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

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. Subash Dhakal
  2. Qiuting Ren
  3. Jiangqu Liu
  4. Bradley Akitake
  5. Izel Tekin
  6. Craig Montell
  7. Youngseok Lee
(2022)
Drosophila TRPg is required in neuroendocrine cells for post-ingestive food selection
eLife 11:e56726.
https://doi.org/10.7554/eLife.56726

Share this article

https://doi.org/10.7554/eLife.56726

Further reading

    1. Neuroscience
    Songyao Zhang, Tuo Zhang ... Tianming Liu
    Research Article

    Cortical folding is an important feature of primate brains that plays a crucial role in various cognitive and behavioral processes. Extensive research has revealed both similarities and differences in folding morphology and brain function among primates including macaque and human. The folding morphology is the basis of brain function, making cross-species studies on folding morphology important for understanding brain function and species evolution. However, prior studies on cross-species folding morphology mainly focused on partial regions of the cortex instead of the entire brain. Previously, our research defined a whole-brain landmark based on folding morphology: the gyral peak. It was found to exist stably across individuals and ages in both human and macaque brains. Shared and unique gyral peaks in human and macaque are identified in this study, and their similarities and differences in spatial distribution, anatomical morphology, and functional connectivity were also dicussed.

    1. Neuroscience
    Avani Koparkar, Timothy L Warren ... Lena Veit
    Research Article

    Complex skills like speech and dance are composed of ordered sequences of simpler elements, but the neuronal basis for the syntactic ordering of actions is poorly understood. Birdsong is a learned vocal behavior composed of syntactically ordered syllables, controlled in part by the songbird premotor nucleus HVC (proper name). Here, we test whether one of HVC’s recurrent inputs, mMAN (medial magnocellular nucleus of the anterior nidopallium), contributes to sequencing in adult male Bengalese finches (Lonchura striata domestica). Bengalese finch song includes several patterns: (1) chunks, comprising stereotyped syllable sequences; (2) branch points, where a given syllable can be followed probabilistically by multiple syllables; and (3) repeat phrases, where individual syllables are repeated variable numbers of times. We found that following bilateral lesions of mMAN, acoustic structure of syllables remained largely intact, but sequencing became more variable, as evidenced by ‘breaks’ in previously stereotyped chunks, increased uncertainty at branch points, and increased variability in repeat numbers. Our results show that mMAN contributes to the variable sequencing of vocal elements in Bengalese finch song and demonstrate the influence of recurrent projections to HVC. Furthermore, they highlight the utility of species with complex syntax in investigating neuronal control of ordered sequences.