Centriolar remodeling underlies basal body maturation during ciliogenesis in Caenorhabditis elegans

The primary cilium is nucleated by the mother centriole-derived basal body (BB) via as yet poorly characterized mechanisms. BBs have been reported to degenerate following ciliogenesis in the C. elegans embryo, although neither BB architecture nor early ciliogenesis steps have been described in this...

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Main Authors: Inna V Nechipurenko, Cristina Berciu, Piali Sengupta, Daniela Nicastro
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2017-04-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/25686
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author Inna V Nechipurenko
Cristina Berciu
Piali Sengupta
Daniela Nicastro
author_facet Inna V Nechipurenko
Cristina Berciu
Piali Sengupta
Daniela Nicastro
author_sort Inna V Nechipurenko
collection DOAJ
description The primary cilium is nucleated by the mother centriole-derived basal body (BB) via as yet poorly characterized mechanisms. BBs have been reported to degenerate following ciliogenesis in the C. elegans embryo, although neither BB architecture nor early ciliogenesis steps have been described in this organism. In a previous study (Doroquez et al., 2014), we described the three-dimensional morphologies of sensory neuron cilia in adult C. elegans hermaphrodites at high resolution. Here, we use serial section electron microscopy and tomography of staged C. elegans embryos to demonstrate that BBs remodel to support ciliogenesis in a subset of sensory neurons. We show that centriolar singlet microtubules are converted into BB doublets which subsequently grow asynchronously to template the ciliary axoneme, visualize degeneration of the centriole core, and define the developmental stage at which the transition zone is established. Our work provides a framework for future investigations into the mechanisms underlying BB remodeling.
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spelling doaj.art-5dd61b6efa3245f88d2d0eab763ed90f2022-12-22T04:32:17ZengeLife Sciences Publications LtdeLife2050-084X2017-04-01610.7554/eLife.25686Centriolar remodeling underlies basal body maturation during ciliogenesis in Caenorhabditis elegansInna V Nechipurenko0https://orcid.org/0000-0003-0249-6620Cristina Berciu1Piali Sengupta2https://orcid.org/0000-0001-7468-0035Daniela Nicastro3https://orcid.org/0000-0002-0122-7173Department of Biology and National Center for Behavioral Genomics, Brandeis University, Waltham, United StatesDepartment of Biology and Rosenstiel Basic Medical Sciences Research Center, Brandeis University, Waltham, United StatesDepartment of Biology and National Center for Behavioral Genomics, Brandeis University, Waltham, United StatesDepartment of Biology and Rosenstiel Basic Medical Sciences Research Center, Brandeis University, Waltham, United States; Departments of Cell Biology and Biophysics, University of Texas Southwestern Medical Center, Dallas, United StatesThe primary cilium is nucleated by the mother centriole-derived basal body (BB) via as yet poorly characterized mechanisms. BBs have been reported to degenerate following ciliogenesis in the C. elegans embryo, although neither BB architecture nor early ciliogenesis steps have been described in this organism. In a previous study (Doroquez et al., 2014), we described the three-dimensional morphologies of sensory neuron cilia in adult C. elegans hermaphrodites at high resolution. Here, we use serial section electron microscopy and tomography of staged C. elegans embryos to demonstrate that BBs remodel to support ciliogenesis in a subset of sensory neurons. We show that centriolar singlet microtubules are converted into BB doublets which subsequently grow asynchronously to template the ciliary axoneme, visualize degeneration of the centriole core, and define the developmental stage at which the transition zone is established. Our work provides a framework for future investigations into the mechanisms underlying BB remodeling.https://elifesciences.org/articles/25686ciliabasal bodieselectron microscopy
spellingShingle Inna V Nechipurenko
Cristina Berciu
Piali Sengupta
Daniela Nicastro
Centriolar remodeling underlies basal body maturation during ciliogenesis in Caenorhabditis elegans
eLife
cilia
basal bodies
electron microscopy
title Centriolar remodeling underlies basal body maturation during ciliogenesis in Caenorhabditis elegans
title_full Centriolar remodeling underlies basal body maturation during ciliogenesis in Caenorhabditis elegans
title_fullStr Centriolar remodeling underlies basal body maturation during ciliogenesis in Caenorhabditis elegans
title_full_unstemmed Centriolar remodeling underlies basal body maturation during ciliogenesis in Caenorhabditis elegans
title_short Centriolar remodeling underlies basal body maturation during ciliogenesis in Caenorhabditis elegans
title_sort centriolar remodeling underlies basal body maturation during ciliogenesis in caenorhabditis elegans
topic cilia
basal bodies
electron microscopy
url https://elifesciences.org/articles/25686
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AT cristinaberciu centriolarremodelingunderliesbasalbodymaturationduringciliogenesisincaenorhabditiselegans
AT pialisengupta centriolarremodelingunderliesbasalbodymaturationduringciliogenesisincaenorhabditiselegans
AT danielanicastro centriolarremodelingunderliesbasalbodymaturationduringciliogenesisincaenorhabditiselegans