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Cutting off ciliary protein import: intraflagellar transport after dendritic femtosecond-laser ablation

Primary cilia, organelles protruding from the surface of eukaryotic cells, act as cellular antennae to detect and transmit signals from the extracellular environment. They are built and maintained by continuous cycles of intraflagellar transport (IFT), where ciliary proteins are transported between...

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Autores principales: Mijalkovic, Jona, Girard, Jules, van Krugten, Jaap, van Loo, Jasmijn, Zhang, Zhiqing, Loseva, Elizaveta, Oswald, Felix, Peterman, Erwin J. G.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The American Society for Cell Biology 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7183794/
https://www.ncbi.nlm.nih.gov/pubmed/31940255
http://dx.doi.org/10.1091/mbc.E18-06-0399
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author Mijalkovic, Jona
Girard, Jules
van Krugten, Jaap
van Loo, Jasmijn
Zhang, Zhiqing
Loseva, Elizaveta
Oswald, Felix
Peterman, Erwin J. G.
author_facet Mijalkovic, Jona
Girard, Jules
van Krugten, Jaap
van Loo, Jasmijn
Zhang, Zhiqing
Loseva, Elizaveta
Oswald, Felix
Peterman, Erwin J. G.
author_sort Mijalkovic, Jona
collection PubMed
description Primary cilia, organelles protruding from the surface of eukaryotic cells, act as cellular antennae to detect and transmit signals from the extracellular environment. They are built and maintained by continuous cycles of intraflagellar transport (IFT), where ciliary proteins are transported between the ciliary base and tip. These proteins originate from the cell body because cilia lack protein synthesis machinery. How input from the cell body affects IFT and ciliary function is not well understood. Here, we use femtosecond-laser ablation to perturb the dendritic input of proteins to chemosensory cilia in living Caenorhabditis elegans. Using fluorescence microscopy, we visualize and quantify the real-time response of ciliary proteins to dendritic ablation. We find that the response occurs in three distinct stages. First, IFT dynein is activated within seconds, redistributing IFT components toward the ciliary base; second, the ciliary axoneme shortens and motors slow down; and third, motors leave the cilium. Depletion of ATP by adding azide also results in IFT slowdown and IFT components leaving the cilium, but not in activation of retrograde IFT. These results indicate that laser ablation triggers a specific mechanism important for IFT regulation that allows the cilium to rapidly adapt to changes in the outside environment.
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spelling pubmed-71837942020-06-06 Cutting off ciliary protein import: intraflagellar transport after dendritic femtosecond-laser ablation Mijalkovic, Jona Girard, Jules van Krugten, Jaap van Loo, Jasmijn Zhang, Zhiqing Loseva, Elizaveta Oswald, Felix Peterman, Erwin J. G. Mol Biol Cell Brief Reports Primary cilia, organelles protruding from the surface of eukaryotic cells, act as cellular antennae to detect and transmit signals from the extracellular environment. They are built and maintained by continuous cycles of intraflagellar transport (IFT), where ciliary proteins are transported between the ciliary base and tip. These proteins originate from the cell body because cilia lack protein synthesis machinery. How input from the cell body affects IFT and ciliary function is not well understood. Here, we use femtosecond-laser ablation to perturb the dendritic input of proteins to chemosensory cilia in living Caenorhabditis elegans. Using fluorescence microscopy, we visualize and quantify the real-time response of ciliary proteins to dendritic ablation. We find that the response occurs in three distinct stages. First, IFT dynein is activated within seconds, redistributing IFT components toward the ciliary base; second, the ciliary axoneme shortens and motors slow down; and third, motors leave the cilium. Depletion of ATP by adding azide also results in IFT slowdown and IFT components leaving the cilium, but not in activation of retrograde IFT. These results indicate that laser ablation triggers a specific mechanism important for IFT regulation that allows the cilium to rapidly adapt to changes in the outside environment. The American Society for Cell Biology 2020-03-01 /pmc/articles/PMC7183794/ /pubmed/31940255 http://dx.doi.org/10.1091/mbc.E18-06-0399 Text en © 2020 Mijalkovic et al. “ASCB®,” “The American Society for Cell Biology®,” and “Molecular Biology of the Cell®” are registered trademarks of The American Society for Cell Biology. http://creativecommons.org/licenses/by-nc-sa/3.0 This article is distributed by The American Society for Cell Biology under license from the author(s). Two months after publication it is available to the public under an Attribution–Noncommercial–Share Alike 3.0 Unported Creative Commons License.
spellingShingle Brief Reports
Mijalkovic, Jona
Girard, Jules
van Krugten, Jaap
van Loo, Jasmijn
Zhang, Zhiqing
Loseva, Elizaveta
Oswald, Felix
Peterman, Erwin J. G.
Cutting off ciliary protein import: intraflagellar transport after dendritic femtosecond-laser ablation
title Cutting off ciliary protein import: intraflagellar transport after dendritic femtosecond-laser ablation
title_full Cutting off ciliary protein import: intraflagellar transport after dendritic femtosecond-laser ablation
title_fullStr Cutting off ciliary protein import: intraflagellar transport after dendritic femtosecond-laser ablation
title_full_unstemmed Cutting off ciliary protein import: intraflagellar transport after dendritic femtosecond-laser ablation
title_short Cutting off ciliary protein import: intraflagellar transport after dendritic femtosecond-laser ablation
title_sort cutting off ciliary protein import: intraflagellar transport after dendritic femtosecond-laser ablation
topic Brief Reports
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7183794/
https://www.ncbi.nlm.nih.gov/pubmed/31940255
http://dx.doi.org/10.1091/mbc.E18-06-0399
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