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SAS-6 engineering reveals interdependence between cartwheel and microtubules in determining centriole architecture.

  • Hilbert M Laboratory of Biomolecular Research, Department of Biology and Chemistry, Paul Scherrer Institut, CH-5232 Villigen PSI, Switzerland.
  • Noga A Department of Biological Sciences, University of Tokyo, Tokyo 113-0033, Japan.
  • Frey D Laboratory of Biomolecular Research, Department of Biology and Chemistry, Paul Scherrer Institut, CH-5232 Villigen PSI, Switzerland.
  • Hamel V Swiss Institute for Experimental Cancer Research (ISREC), School of Life Sciences, Swiss Federal Institute of Technology (EPFL), CH-1015 Lausanne, Switzerland.
  • Guichard P Swiss Institute for Experimental Cancer Research (ISREC), School of Life Sciences, Swiss Federal Institute of Technology (EPFL), CH-1015 Lausanne, Switzerland.
  • Kraatz SH Laboratory of Biomolecular Research, Department of Biology and Chemistry, Paul Scherrer Institut, CH-5232 Villigen PSI, Switzerland.
  • Pfreundschuh M Department of Biosystems Science and Engineering, Eidgenössische Technische Hochschule (ETH) Zürich, CH-4058 Basel, Switzerland.
  • Hosner S Laboratory of Biomolecular Research, Department of Biology and Chemistry, Paul Scherrer Institut, CH-5232 Villigen PSI, Switzerland.
  • Flückiger I Swiss Institute for Experimental Cancer Research (ISREC), School of Life Sciences, Swiss Federal Institute of Technology (EPFL), CH-1015 Lausanne, Switzerland.
  • Jaussi R Laboratory of Biomolecular Research, Department of Biology and Chemistry, Paul Scherrer Institut, CH-5232 Villigen PSI, Switzerland.
  • Wieser MM Laboratory of Biomolecular Research, Department of Biology and Chemistry, Paul Scherrer Institut, CH-5232 Villigen PSI, Switzerland.
  • Thieltges KM Laboratory of Biomolecular Research, Department of Biology and Chemistry, Paul Scherrer Institut, CH-5232 Villigen PSI, Switzerland.
  • Deupi X Laboratory of Biomolecular Research, Department of Biology and Chemistry, Paul Scherrer Institut, CH-5232 Villigen PSI, Switzerland.
  • Müller DJ Department of Biosystems Science and Engineering, Eidgenössische Technische Hochschule (ETH) Zürich, CH-4058 Basel, Switzerland.
  • Kammerer RA Laboratory of Biomolecular Research, Department of Biology and Chemistry, Paul Scherrer Institut, CH-5232 Villigen PSI, Switzerland.
  • Gönczy P Swiss Institute for Experimental Cancer Research (ISREC), School of Life Sciences, Swiss Federal Institute of Technology (EPFL), CH-1015 Lausanne, Switzerland.
  • Hirono M Department of Biological Sciences, University of Tokyo, Tokyo 113-0033, Japan.
  • Steinmetz MO Laboratory of Biomolecular Research, Department of Biology and Chemistry, Paul Scherrer Institut, CH-5232 Villigen PSI, Switzerland.
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  • 2016-03-22
Published in:
  • Nature cell biology. - 2016
Algal Proteins
Blotting, Western
Cell Cycle Proteins
Cell Line, Tumor
Centrioles
Chlamydomonas reinhardtii
Crystallography, X-Ray
Green Fluorescent Proteins
Humans
Microscopy, Atomic Force
Microscopy, Electron
Microscopy, Fluorescence
Microtubules
Models, Molecular
Molecular Conformation
Mutation
Protein Multimerization
Protein Structure, Tertiary
RNA Interference
English Centrioles are critical for the formation of centrosomes, cilia and flagella in eukaryotes. They are thought to assemble around a nine-fold symmetric cartwheel structure established by SAS-6 proteins. Here, we have engineered Chlamydomonas reinhardtii SAS-6-based oligomers with symmetries ranging from five- to ten-fold. Expression of a SAS-6 mutant that forms six-fold symmetric cartwheel structures in vitro resulted in cartwheels and centrioles with eight- or nine-fold symmetries in vivo. In combination with Bld10 mutants that weaken cartwheel-microtubule interactions, this SAS-6 mutant produced six- to eight-fold symmetric cartwheels. Concurrently, the microtubule wall maintained eight- and nine-fold symmetries. Expressing SAS-6 with analogous mutations in human cells resulted in nine-fold symmetric centrioles that exhibited impaired length and organization. Together, our data suggest that the self-assembly properties of SAS-6 instruct cartwheel symmetry, and lead us to propose a model in which the cartwheel and the microtubule wall assemble in an interdependent manner to establish the native architecture of centrioles.
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  • English
Open access status
green
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Persistent URL
https://sonar.ch/global/documents/267312
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