Ephrin-A/EphA specific co-adaptation as a novel mechanism in topographic axon guidance

Genetic hardwiring during brain development provides computational architectures for innate neuronal processing. Thus, the paradigmatic chick retinotectal projection, due to its neighborhood preserving, topographic organization, establishes millions of parallel channels for incremental visual field...

Full description

Bibliographic Details
Main Authors: Felix Fiederling, Markus Weschenfelder, Martin Fritz, Anne von Philipsborn, Martin Bastmeyer, Franco Weth
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2017-07-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/25533
_version_ 1811181051788132352
author Felix Fiederling
Markus Weschenfelder
Martin Fritz
Anne von Philipsborn
Martin Bastmeyer
Franco Weth
author_facet Felix Fiederling
Markus Weschenfelder
Martin Fritz
Anne von Philipsborn
Martin Bastmeyer
Franco Weth
author_sort Felix Fiederling
collection DOAJ
description Genetic hardwiring during brain development provides computational architectures for innate neuronal processing. Thus, the paradigmatic chick retinotectal projection, due to its neighborhood preserving, topographic organization, establishes millions of parallel channels for incremental visual field analysis. Retinal axons receive targeting information from quantitative guidance cue gradients. Surprisingly, novel adaptation assays demonstrate that retinal growth cones robustly adapt towards ephrin-A/EphA forward and reverse signals, which provide the major mapping cues. Computational modeling suggests that topographic accuracy and adaptability, though seemingly incompatible, could be reconciled by a novel mechanism of coupled adaptation of signaling channels. Experimentally, we find such ‘co-adaptation’ in retinal growth cones specifically for ephrin-A/EphA signaling. Co-adaptation involves trafficking of unliganded sensors between the surface membrane and recycling endosomes, and is presumably triggered by changes in the lipid composition of membrane microdomains. We propose that co-adaptative desensitization eventually relies on guidance sensor translocation into cis-signaling endosomes to outbalance repulsive trans-signaling.
first_indexed 2024-04-11T09:13:09Z
format Article
id doaj.art-c70bfe9613d14cc6b3024c98c8830fb3
institution Directory Open Access Journal
issn 2050-084X
language English
last_indexed 2024-04-11T09:13:09Z
publishDate 2017-07-01
publisher eLife Sciences Publications Ltd
record_format Article
series eLife
spelling doaj.art-c70bfe9613d14cc6b3024c98c8830fb32022-12-22T04:32:26ZengeLife Sciences Publications LtdeLife2050-084X2017-07-01610.7554/eLife.25533Ephrin-A/EphA specific co-adaptation as a novel mechanism in topographic axon guidanceFelix Fiederling0https://orcid.org/0000-0001-7837-5556Markus Weschenfelder1Martin Fritz2Anne von Philipsborn3https://orcid.org/0000-0002-7921-8744Martin Bastmeyer4Franco Weth5https://orcid.org/0000-0002-6819-7028Department of Cell and Neurobiology, Karlsruhe Institute of Technology, Zoological Institute, Karlruhe, GermanyDepartment of Cell and Neurobiology, Karlsruhe Institute of Technology, Zoological Institute, Karlruhe, GermanyDepartment of Cell and Neurobiology, Karlsruhe Institute of Technology, Zoological Institute, Karlruhe, GermanyDepartment of Cell and Neurobiology, Karlsruhe Institute of Technology, Zoological Institute, Karlruhe, GermanyDepartment of Cell and Neurobiology, Karlsruhe Institute of Technology, Zoological Institute, Karlruhe, GermanyDepartment of Cell and Neurobiology, Karlsruhe Institute of Technology, Zoological Institute, Karlruhe, GermanyGenetic hardwiring during brain development provides computational architectures for innate neuronal processing. Thus, the paradigmatic chick retinotectal projection, due to its neighborhood preserving, topographic organization, establishes millions of parallel channels for incremental visual field analysis. Retinal axons receive targeting information from quantitative guidance cue gradients. Surprisingly, novel adaptation assays demonstrate that retinal growth cones robustly adapt towards ephrin-A/EphA forward and reverse signals, which provide the major mapping cues. Computational modeling suggests that topographic accuracy and adaptability, though seemingly incompatible, could be reconciled by a novel mechanism of coupled adaptation of signaling channels. Experimentally, we find such ‘co-adaptation’ in retinal growth cones specifically for ephrin-A/EphA signaling. Co-adaptation involves trafficking of unliganded sensors between the surface membrane and recycling endosomes, and is presumably triggered by changes in the lipid composition of membrane microdomains. We propose that co-adaptative desensitization eventually relies on guidance sensor translocation into cis-signaling endosomes to outbalance repulsive trans-signaling.https://elifesciences.org/articles/25533Axon guidancegrowth coneretinotectalephrinEphtopographic map
spellingShingle Felix Fiederling
Markus Weschenfelder
Martin Fritz
Anne von Philipsborn
Martin Bastmeyer
Franco Weth
Ephrin-A/EphA specific co-adaptation as a novel mechanism in topographic axon guidance
eLife
Axon guidance
growth cone
retinotectal
ephrin
Eph
topographic map
title Ephrin-A/EphA specific co-adaptation as a novel mechanism in topographic axon guidance
title_full Ephrin-A/EphA specific co-adaptation as a novel mechanism in topographic axon guidance
title_fullStr Ephrin-A/EphA specific co-adaptation as a novel mechanism in topographic axon guidance
title_full_unstemmed Ephrin-A/EphA specific co-adaptation as a novel mechanism in topographic axon guidance
title_short Ephrin-A/EphA specific co-adaptation as a novel mechanism in topographic axon guidance
title_sort ephrin a epha specific co adaptation as a novel mechanism in topographic axon guidance
topic Axon guidance
growth cone
retinotectal
ephrin
Eph
topographic map
url https://elifesciences.org/articles/25533
work_keys_str_mv AT felixfiederling ephrinaephaspecificcoadaptationasanovelmechanismintopographicaxonguidance
AT markusweschenfelder ephrinaephaspecificcoadaptationasanovelmechanismintopographicaxonguidance
AT martinfritz ephrinaephaspecificcoadaptationasanovelmechanismintopographicaxonguidance
AT annevonphilipsborn ephrinaephaspecificcoadaptationasanovelmechanismintopographicaxonguidance
AT martinbastmeyer ephrinaephaspecificcoadaptationasanovelmechanismintopographicaxonguidance
AT francoweth ephrinaephaspecificcoadaptationasanovelmechanismintopographicaxonguidance