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Towards a molecular architecture of centriole assembly

Key Points

  • Centrioles and basal bodies (hereafter referred to as 'centrioles' for simplicity) are essential for the formation of cilia, flagella and centrosomes. Therefore, understanding the mechanisms governing centriole assembly is crucial for many fundamental biological processes.

  • Centriole ultrastructure is characterized by a ninefold symmetric arrangement of microtubules, which is imparted at the least in part by a cartwheel that also exhibits a ninefold radial symmetry.

  • Five components that were initially discovered in the nematode Caenorhabditis elegans as being essential for centriole assembly have relatives in other species that are likewise required for this process.

  • Self-assembly of spindle assembly abnormal 6 (SAS-6) proteins is crucial for the ninefold radial symmetry of the cartwheel and thus of the centriole.

  • Poorly characterized SAS-6- and cartwheel-independent mechanisms contribute to efficient centriole assembly.

  • The mechanisms that promote the addition of microtubules and regulate the length of centrioles have begun to be investigated.

Abstract

The centriole is an evolutionarily conserved macromolecular structure that is crucial for the formation of flagella, cilia and centrosomes. The ultrastructure of the centriole was first characterized decades ago with the advent of electron microscopy, revealing a striking ninefold radial arrangement of microtubules. However, it is only recently that the molecular mechanisms governing centriole assembly have begun to emerge, including the elucidation of the crucial role of spindle assembly abnormal 6 (SAS-6) proteins in imparting the ninefold symmetry. These advances have brought the field to an exciting era in which architecture meets function.

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Figure 1: Centriole and cartwheel architecture.
Figure 2: Lack of centriole assembly following depletion of SAS-6 proteins.
Figure 3: Evolutionarily conserved pathway for centriole assembly.
Figure 4: Localization of key proteins on human centrioles and procentrioles.
Figure 5: Step-wise self-assembly of SAS-6 proteins.

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Acknowledgements

The author is grateful to the members of his laboratory for fruitful discussions and to P. Guichard in particular for his encyclopedic knowledge of centrioles, as well as for his help in preparing the figures. The author thanks J. Beisson, P. Guichard, V. Hachet, M. Hirono and M. Steinmetz for useful comments on the manuscript. He apologizes to those authors whose interesting contributions could not be mentioned owing to space limitations. Work in his laboratory on different aspects of centrosome duplication is supported by grants from the Swiss Cancer League (02584-02-2010), the Sinergia programme from the Swiss National Science Foundation (CRSII3_125463) and the European Research Council (ERC AdG 233335).

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Glossary

Pericentriolar material

(PCM). A region surrounding centrioles from where most microtubules are nucleated in many cells.

Protofilaments

The building blocks for microtubules. Tubulin dimers polymerize end to end into 13 protofilaments, which associate laterally to form a single microtubule with a hollow cylindrical structure.

Chirality

The property of a structure that cannot be mapped onto its mirror image. In this case, refers to the direction in which microtubule triplets are pointing.

Biotinylated tubulin

Tubulin conjugated with biotin to mark a subset of the total tubulin pool present in the cell.

Cryo-electron tomography

Electron-microscopic method in which the sample is preserved in the native state by freezing at cryogenic temperature. This is followed by imaging of a tilt series that allows three-dimensional reconstruction of the sample.

Axoneme

A microtubule-based structure at the core of cilia and flagella. Axonemes also exhibit a ninefold symmetrical arrangement of microtubules.

Coiled-coil proteins

Proteins containing one or more coiled-coil domains in which several α-helices are coiled together, often as dimers.

Modifier genetic screens

Genetic screens that are conducted in the background of a sensitized condition (such as a temperature-sensitive mutant raised at a semi-permissive temperature) and aimed at identifying additional components that participate in a given biological process.

Rotary metal shadowing electron microscopy

Electron-microscopic method in which the surface topology of the sample is revealed by the uneven distribution of fine metal particles deposited onto it.

Super-resolution microscopy

Light microscopy approach in which a resolution that is better than the 250 nm diffraction limit of conventional optical microscopes can be used.

Autosomal recessive primary microcephaly

(MCPH). Congenital disorder in which patients have a small brain size. This disorder is thought to derive from defective asymmetric division in the ventricular zone during development of the neocortex.

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Gönczy, P. Towards a molecular architecture of centriole assembly. Nat Rev Mol Cell Biol 13, 425–435 (2012). https://doi.org/10.1038/nrm3373

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