Rod nuclear architecture determines contrast transmission of the retina and behavioral sensitivity in mice
- Max Planck Institute of Molecular Cell Biology and Genetics, Germany
- Technische Universität Dresden, Germany
- Ludwig Maximilians Universität, Germany
Abstract
Rod photoreceptors of nocturnal mammals display a striking inversion of nuclear architecture, which has been proposed as an evolutionary adaptation to dark environments. However, the nature of visual benefits and the underlying mechanisms remains unclear. It is widely assumed that improvements in nocturnal vision would depend on maximization of photon capture at the expense of image detail. Here we show that retinal optical quality improves 2-fold during terminal development, and that this enhancement is caused by nuclear inversion. We further demonstrate that improved retinal contrast transmission, rather than photon-budget or resolution, enhances scotopic contrast sensitivity by 18-27%, and improves motion detection capabilities up to 10-fold in dim environments. Our findings therefore add functional significance to a prominent exception of nuclear organization and establish retinal contrast transmission as a decisive determinant of mammalian visual perception.
Data availability
Data and specifications of simulations supporting the findings of this study are available via https://owncloud.mpi-cbg.de/index.php/s/SaCJjsMCfyOAaTb . The biobeam software is available publicly from: https://maweigert.github.io/biobeam
Article and author information
Author details
Funding
Max-Planck-Gesellschaft
- Kaushikaram Subramanian
- Martin Weigert
- Heike Petzold
- Alfonso Garcia-Ulloa
- Eugene W Myers
- Moritz Kreysing
Technische Universität Dresden
- Oliver Borsch
- Marius Ader
Deutsche Forschungsgemeinschaft (AD375/6-1)
- Oliver Borsch
- Marius Ader
Bundesministerium für Bildung und Forschung (031L0044)
- Kaushikaram Subramanian
- Eugene W Myers
- Moritz Kreysing
Deutsche Forschungsgemeinschaft (SO1054/3)
- Irina Solovei
Deutsche Forschungsgemeinschaft (FZT111)
- Oliver Borsch
- Marius Ader
Deutsche Forschungsgemeinschaft (EXC68)
- Oliver Borsch
- Marius Ader
Deutsche Forschungsgemeinschaft (SFB1064)
- Irina Solovei
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 studies were performed in accordance with European and German animal welfare legislation (Tierschutzgesetz), the ARVO Statement for the Use of Animals in Ophthalmic and Vision Research, and the NIH Guide for the care and use of laboratory work in strict pathogen-free conditions in the animal facilities of the Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany and the Center for Regenerative Therapies Dresden, Germany. Protocols were approved by the Institutional Animal Welfare Officer (Tierschutzbeauftragter) and the ethics committee of the TU Dresden. Necessary licenses 24-9168.24-9/2012-1, DD24.1-5131/451/8 and TVV 16/2018 (DD24-5131/354/19) were obtained from the regional Ethical Commission for Animal Experimentation of Dresden, Germany (Tierversuchskommission, Landesdirektion Sachsen)"
Copyright
© 2019, Subramanian 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.
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)
Rod nuclear architecture determines contrast transmission of the retina and behavioral sensitivity in mice
eLife 8:e49542.
https://doi.org/10.7554/eLife.49542
Further reading
-
- Cell Biology
- Neuroscience
The gut-brain axis mediates bidirectional signaling between the intestine and the nervous system and is critical for organism-wide homeostasis. Here, we report the identification of a peptidergic endocrine circuit in which bidirectional signaling between neurons and the intestine potentiates the activation of the antioxidant response in Caenorhabditis elegans in the intestine. We identify an FMRF-amide-like peptide, FLP-2, whose release from the intestine is necessary and sufficient to activate the intestinal oxidative stress response by promoting the release of the antioxidant FLP-1 neuropeptide from neurons. FLP-2 secretion from the intestine is positively regulated by endogenous hydrogen peroxide (H2O2) produced in the mitochondrial matrix by sod-3/superoxide dismutase, and is negatively regulated by prdx-2/peroxiredoxin, which depletes H2O2 in both the mitochondria and cytosol. H2O2 promotes FLP-2 secretion through the DAG and calcium-dependent protein kinase C family member pkc-2 and by the SNAP25 family member aex-4 in the intestine. Together, our data demonstrate a role for intestinal H2O2 in promoting inter-tissue antioxidant signaling through regulated neuropeptide-like protein exocytosis in a gut-brain axis to activate the oxidative stress response.
-
- Cell Biology
- Microbiology and Infectious Disease
The coordination of cell cycle progression and flagellar synthesis is a complex process in motile bacteria. In γ-proteobacteria, the localization of the flagellum to the cell pole is mediated by the SRP-type GTPase FlhF. However, the mechanism of action of FlhF, and its relationship with the cell pole landmark protein HubP remain unclear. In this study, we discovered a novel protein called FipA that is required for normal FlhF activity and function in polar flagellar synthesis. We demonstrated that membrane-localized FipA interacts with FlhF and is required for normal flagellar synthesis in Vibrio parahaemolyticus, Pseudomonas putida, and Shewanella putrefaciens, and it does so independently of the polar localization mediated by HubP. FipA exhibits a dynamic localization pattern and is present at the designated pole before flagellar synthesis begins, suggesting its role in licensing flagellar formation. This discovery provides insight into a new pathway for regulating flagellum synthesis and coordinating cellular organization in bacteria that rely on polar flagellation and FlhF-dependent localization.
