1. Neuroscience
Download icon

The role of PDF neurons in setting preferred temperature before dawn in Drosophila

  1. Xin Tang
  2. Sanne Roessingh
  3. Sean E Hayley
  4. Michelle L Chu
  5. Nobuaki K Tanaka
  6. Werner Wolfgang
  7. Seongho Song
  8. Ralf Stanewsky
  9. Fumika N Hamada  Is a corresponding author
  1. Cincinnati Children's Hospital Medical Center, United States
  2. University College London, United Kingdom
  3. Hokkaido University, Japan
  4. University of London, United Kingdom
  5. University of Cincinnati, United States
  6. Westfälische Wilhelms University, Germany
Research Article
  • Cited 21
  • Views 2,409
  • Annotations
Cite this article as: eLife 2017;6:e23206 doi: 10.7554/eLife.23206

Abstract

Animals have sophisticated homeostatic controls. While mammalian body temperature fluctuates throughout the day, small ectotherms, such as Drosophila, achieve a body temperature rhythm (BTR) through their preference of environmental temperature. Here, we demonstrate that pigment dispersing factor (PDF) neurons play an important role in setting preferred temperature before dawn. We show that small lateral ventral neurons (sLNvs), a subset of PDF neurons, activate the dorsal neurons 2 (DN2s), the main circadian clock cells that regulate temperature preference rhythm (TPR). The number of temporal contacts between sLNvs and DN2s peak before dawn. Our data suggest that the thermosensory Anterior Cells (ACs) likely contact sLNvs via serotonin signaling. Together, the ACs-sLNs-DN2s neural circuit regulates the proper setting of temperature preference before dawn. Given that sLNvs are important for sleep and that BTR and sleep have a close temporal relationship, our data highlight a possible neuronal interaction between body temperature and sleep regulation.

Article and author information

Author details

  1. Xin Tang

    Visual Systems Group, Abrahamson Pediatric Eye Institute, Division of Pediatric Ophthalmology, Cincinnati Children's Hospital Medical Center, Cincinnati, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Sanne Roessingh

    Department of Cell and Developmental Biology, University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  3. Sean E Hayley

    Visual Systems Group, Abrahamson Pediatric Eye Institute, Division of Pediatric Ophthalmology, Cincinnati Children's Hospital Medical Center, Cincinnati, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Michelle L Chu

    Visual Systems Group, Abrahamson Pediatric Eye Institute, Division of Pediatric Ophthalmology, Cincinnati Children's Hospital Medical Center, Cincinnati, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Nobuaki K Tanaka

    Creative Research Institution, Hokkaido University, Sapporo, Japan
    Competing interests
    The authors declare that no competing interests exist.
  6. Werner Wolfgang

    School of Biological and Chemical Sciences, University of London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  7. Seongho Song

    Department of Mathematical Sciences, University of Cincinnati, Cincinnati, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Ralf Stanewsky

    Institute for Neuro and Behavioral Biology, Westfälische Wilhelms University, Münster, Germany
    Competing interests
    The authors declare that no competing interests exist.
  9. Fumika N Hamada

    Visual Systems Group, Abrahamson Pediatric Eye Institute, Division of Pediatric Ophthalmology, Cincinnati Children's Hospital Medical Center, Cincinnati, United States
    For correspondence
    fumika.hamada@cchmc.org
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5365-0504

Funding

National Institutes of Health (R01 grant GM107582)

  • Fumika N Hamada

March of Dimes Foundation (Basil O'Connor Starter Scholar Research Award)

  • Fumika N Hamada

Japan Science and Technology Agency (PRESTO)

  • Fumika N Hamada

Biotechnology and Biological Sciences Research Council

  • Ralf Stanewsky

Seventh Framework Programme

  • Ralf Stanewsky

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

Reviewing Editor

  1. K VijayRaghavan, National Centre for Biological Sciences, Tata Institute of Fundamental Research, India

Publication history

  1. Received: November 12, 2016
  2. Accepted: April 23, 2017
  3. Accepted Manuscript published: May 2, 2017 (version 1)
  4. Version of Record published: May 30, 2017 (version 2)

Copyright

© 2017, Tang 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

  • 2,409
    Page views
  • 572
    Downloads
  • 21
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, Scopus, 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)

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

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

  1. Further reading

Further reading

    1. Developmental Biology
    2. Neuroscience
    Baruch Haimson et al.
    Research Article Updated

    Peripheral and intraspinal feedback is required to shape and update the output of spinal networks that execute motor behavior. We report that lumbar dI2 spinal interneurons in chicks receive synaptic input from afferents and premotor neurons. These interneurons innervate contralateral premotor networks in the lumbar and brachial spinal cord, and their ascending projections innervate the cerebellum. These findings suggest that dI2 neurons function as interneurons in local lumbar circuits, are involved in lumbo-brachial coupling, and that part of them deliver peripheral and intraspinal feedback to the cerebellum. Silencing of dI2 neurons leads to destabilized stepping in posthatching day 8 hatchlings, with occasional collapses, variable step profiles, and a wide-base walking gait, suggesting that dI2 neurons may contribute to the stabilization of the bipedal gait.

    1. Cell Biology
    2. Neuroscience
    Rene Solano Fonseca et al.
    Research Article Updated

    Concussion is associated with a myriad of deleterious immediate and long-term consequences. Yet the molecular mechanisms and genetic targets promoting the selective vulnerability of different neural subtypes to dysfunction and degeneration remain unclear. Translating experimental models of blunt force trauma in C. elegans to concussion in mice, we identify a conserved neuroprotective mechanism in which reduction of mitochondrial electron flux through complex IV suppresses trauma-induced degeneration of the highly vulnerable dopaminergic neurons. Reducing cytochrome C oxidase function elevates mitochondrial-derived reactive oxygen species, which signal through the cytosolic hypoxia inducing transcription factor, Hif1a, to promote hyperphosphorylation and inactivation of the pyruvate dehydrogenase, PDHE1α. This critical enzyme initiates the Warburg shunt, which drives energetic reallocation from mitochondrial respiration to astrocyte-mediated glycolysis in a neuroprotective manner. These studies demonstrate a conserved process in which glycolytic preconditioning suppresses Parkinson-like hypersensitivity of dopaminergic neurons to trauma-induced degeneration via redox signaling and the Warburg effect.