Circadian regulation of vertebrate cone photoreceptor function

Abstract

Eukaryotes generally display a circadian rhythm as an adaption to the reoccurring day/night cycle. This is particularly true for visual physiology that is directly affected by changing light conditions. Here we investigate the influence of the circadian rhythm on the expression and function of visual transduction cascade regulators in diurnal zebrafish and nocturnal mice. We focused on regulators of shut-off kinetics such as recoverins, arrestins, opsin kinases, and GTPase-accelerating protein that have direct effects on temporal vision. Transcript as well as protein levels of most analyzed genes show a robust circadian rhythm dependent regulation, which correlates with changes in photoresponse kinetics. Electroretinography demonstrates that photoresponse recovery in zebrafish is delayed in the evening and accelerated in the morning. This physiological rhythmicity is mirrored in visual behaviors, such as optokinetic and optomotor responses. Functional rhythmicity persists in continuous darkness, it is reversed by an inverted light cycle and disrupted by constant light. This is in line with our finding that orthologous gene transcripts from diurnal zebrafish and nocturnal mice are often expressed in an anti-phasic daily rhythm.

Data availability

All data generated and analysed during this study are included in the manuscript and supporting files. The dataset has been uploaded to dryad at http://dx.doi.org/10.5061/dryad.0cfxpnw26

The following data sets were generated

Article and author information

Author details

  1. Jingjing Zang

    Department of Molecular Life Sciences, University of Zurich, Zurich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  2. Matthias Gesemann

    Molecular Life Sciences and Neuroscience Center Zurich, University of Zurich, Zurich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7635-1235
  3. Jennifer Keim

    Institute of Molecular Life Sciences, University of Zurich, Zurich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  4. Marijana Samardzija

    Lab for Retinal Cell Biology, Department of Ophthalmology, University of Zurich, Schlieren, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  5. Christian Grimm

    Institute of Molecular Life Sciences, University of Zurich, Zurich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9318-4352
  6. Stephan CF Neuhauss

    Institute of Molecular Life Sciences, University of Zurich, Zurich, Switzerland
    For correspondence
    stephan.neuhauss@mls.uzh.ch
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9615-480X

Funding

Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (310030_200376)

  • Marijana Samardzija

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

Ethics

Animal experimentation: All animal experiments were carried out in the line with the ARVO Statement for the Use of Animals in Ophthalmic and Vision Research and were approved by the Veterinary Authorities of Kanton Zurich, Switzerland (TV4206)

Reviewing Editor

  1. Kristin Tessmar-Raible, University of Vienna, Austria

Publication history

  1. Received: March 30, 2021
  2. Preprint posted: May 7, 2021 (view preprint)
  3. Accepted: September 20, 2021
  4. Accepted Manuscript published: September 22, 2021 (version 1)
  5. Version of Record published: October 6, 2021 (version 2)

Copyright

© 2021, Zang 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.

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  1. Jingjing Zang
  2. Matthias Gesemann
  3. Jennifer Keim
  4. Marijana Samardzija
  5. Christian Grimm
  6. Stephan CF Neuhauss
(2021)
Circadian regulation of vertebrate cone photoreceptor function
eLife 10:e68903.
https://doi.org/10.7554/eLife.68903
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