Cargando…

Mechanisms of HsSAS-6 assembly promoting centriole formation in human cells

SAS-6 proteins are thought to impart the ninefold symmetry of centrioles, but the mechanisms by which their assembly occurs within cells remain elusive. In this paper, we provide evidence that the N-terminal, coiled-coil, and C-terminal domains of HsSAS-6 are each required for procentriole formation...

Descripción completa

Detalles Bibliográficos
Autores principales: Keller, Debora, Orpinell, Meritxell, Olivier, Nicolas, Wachsmuth, Malte, Mahen, Robert, Wyss, Romain, Hachet, Virginie, Ellenberg, Jan, Manley, Suliana, Gönczy, Pierre
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Rockefeller University Press 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3941056/
https://www.ncbi.nlm.nih.gov/pubmed/24590172
http://dx.doi.org/10.1083/jcb.201307049
_version_ 1782305861749702656
author Keller, Debora
Orpinell, Meritxell
Olivier, Nicolas
Wachsmuth, Malte
Mahen, Robert
Wyss, Romain
Hachet, Virginie
Ellenberg, Jan
Manley, Suliana
Gönczy, Pierre
author_facet Keller, Debora
Orpinell, Meritxell
Olivier, Nicolas
Wachsmuth, Malte
Mahen, Robert
Wyss, Romain
Hachet, Virginie
Ellenberg, Jan
Manley, Suliana
Gönczy, Pierre
author_sort Keller, Debora
collection PubMed
description SAS-6 proteins are thought to impart the ninefold symmetry of centrioles, but the mechanisms by which their assembly occurs within cells remain elusive. In this paper, we provide evidence that the N-terminal, coiled-coil, and C-terminal domains of HsSAS-6 are each required for procentriole formation in human cells. Moreover, the coiled coil is necessary and sufficient to mediate HsSAS-6 centrosomal targeting. High-resolution imaging reveals that GFP-tagged HsSAS-6 variants localize in a torus around the base of the parental centriole before S phase, perhaps indicative of an initial loading platform. Moreover, fluorescence recovery after photobleaching analysis demonstrates that HsSAS-6 is immobilized progressively at centrosomes during cell cycle progression. Using fluorescence correlation spectroscopy and three-dimensional stochastic optical reconstruction microscopy, we uncover that HsSAS-6 is present in the cytoplasm primarily as a homodimer and that its oligomerization into a ninefold symmetrical ring occurs at centrioles. Together, our findings lead us to propose a mechanism whereby HsSAS-6 homodimers are targeted to centrosomes where the local environment and high concentration of HsSAS-6 promote oligomerization, thus initiating procentriole formation.
format Online
Article
Text
id pubmed-3941056
institution National Center for Biotechnology Information
language English
publishDate 2014
publisher The Rockefeller University Press
record_format MEDLINE/PubMed
spelling pubmed-39410562014-09-03 Mechanisms of HsSAS-6 assembly promoting centriole formation in human cells Keller, Debora Orpinell, Meritxell Olivier, Nicolas Wachsmuth, Malte Mahen, Robert Wyss, Romain Hachet, Virginie Ellenberg, Jan Manley, Suliana Gönczy, Pierre J Cell Biol Research Articles SAS-6 proteins are thought to impart the ninefold symmetry of centrioles, but the mechanisms by which their assembly occurs within cells remain elusive. In this paper, we provide evidence that the N-terminal, coiled-coil, and C-terminal domains of HsSAS-6 are each required for procentriole formation in human cells. Moreover, the coiled coil is necessary and sufficient to mediate HsSAS-6 centrosomal targeting. High-resolution imaging reveals that GFP-tagged HsSAS-6 variants localize in a torus around the base of the parental centriole before S phase, perhaps indicative of an initial loading platform. Moreover, fluorescence recovery after photobleaching analysis demonstrates that HsSAS-6 is immobilized progressively at centrosomes during cell cycle progression. Using fluorescence correlation spectroscopy and three-dimensional stochastic optical reconstruction microscopy, we uncover that HsSAS-6 is present in the cytoplasm primarily as a homodimer and that its oligomerization into a ninefold symmetrical ring occurs at centrioles. Together, our findings lead us to propose a mechanism whereby HsSAS-6 homodimers are targeted to centrosomes where the local environment and high concentration of HsSAS-6 promote oligomerization, thus initiating procentriole formation. The Rockefeller University Press 2014-03-03 /pmc/articles/PMC3941056/ /pubmed/24590172 http://dx.doi.org/10.1083/jcb.201307049 Text en © 2014 Keller et al. This article is distributed under the terms of an Attribution–Noncommercial–Share Alike–No Mirror Sites license for the first six months after the publication date (see http://www.rupress.org/terms). After six months it is available under a Creative Commons License (Attribution–Noncommercial–Share Alike 3.0 Unported license, as described at http://creativecommons.org/licenses/by-nc-sa/3.0/).
spellingShingle Research Articles
Keller, Debora
Orpinell, Meritxell
Olivier, Nicolas
Wachsmuth, Malte
Mahen, Robert
Wyss, Romain
Hachet, Virginie
Ellenberg, Jan
Manley, Suliana
Gönczy, Pierre
Mechanisms of HsSAS-6 assembly promoting centriole formation in human cells
title Mechanisms of HsSAS-6 assembly promoting centriole formation in human cells
title_full Mechanisms of HsSAS-6 assembly promoting centriole formation in human cells
title_fullStr Mechanisms of HsSAS-6 assembly promoting centriole formation in human cells
title_full_unstemmed Mechanisms of HsSAS-6 assembly promoting centriole formation in human cells
title_short Mechanisms of HsSAS-6 assembly promoting centriole formation in human cells
title_sort mechanisms of hssas-6 assembly promoting centriole formation in human cells
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3941056/
https://www.ncbi.nlm.nih.gov/pubmed/24590172
http://dx.doi.org/10.1083/jcb.201307049
work_keys_str_mv AT kellerdebora mechanismsofhssas6assemblypromotingcentrioleformationinhumancells
AT orpinellmeritxell mechanismsofhssas6assemblypromotingcentrioleformationinhumancells
AT oliviernicolas mechanismsofhssas6assemblypromotingcentrioleformationinhumancells
AT wachsmuthmalte mechanismsofhssas6assemblypromotingcentrioleformationinhumancells
AT mahenrobert mechanismsofhssas6assemblypromotingcentrioleformationinhumancells
AT wyssromain mechanismsofhssas6assemblypromotingcentrioleformationinhumancells
AT hachetvirginie mechanismsofhssas6assemblypromotingcentrioleformationinhumancells
AT ellenbergjan mechanismsofhssas6assemblypromotingcentrioleformationinhumancells
AT manleysuliana mechanismsofhssas6assemblypromotingcentrioleformationinhumancells
AT gonczypierre mechanismsofhssas6assemblypromotingcentrioleformationinhumancells