Building the Centriole

Department of Biochemistry and Biophysics, University of California, San Francisco, 94143, USA.
Current biology: CB (Impact Factor: 9.57). 09/2010; 20(18):R816-25. DOI: 10.1016/j.cub.2010.08.010
Source: PubMed


Centrioles are conserved microtubule-based organelles that lie at the core of the animal centrosome and play a crucial role in nucleating the formation of cilia and flagella in most eukaryotes. Centrioles have a complex ultrastructure with ninefold symmetry and a well-defined length. This structure is assembled from a host of proteins, including a variety of disease gene products. Over a century after the discovery of centrioles, the mechanisms underlying the assembly of these fascinating organelles, in particular the establishment of ninefold symmetry and the control of centriole length, are now starting to be uncovered.

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Available from: Juliette Azimzadeh, Apr 15, 2014
    • "It is beyond the scope of this chapter to introduce even a subset of the bona fide components of centrioles or centrosomes , let alone discuss their discovery, potential functions, and hierarchy of assembly. Several excellent reviews exist, which detail the identity, function , and mode of discovery for many centriole proteins (Bornens, 2002; Nigg, 2007; Strnad and Gönczy, 2008; Bettencourt-Dias and Glover, 2007; Azimzadeh and Marshall, 2010; Nigg and Stearns, 2011; Brito et al., 2012; Gönczy, 2012; Avidor-Reiss and Gopalakrishnan, 2013). "
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    ABSTRACT: The assembly of a bipolar spindle lies at the heart of mitotic chromosome segregation. In animal somatic cells, the process of spindle assembly involves multiple complex interactions between various cellular compartments, including an emerging antiparallel microtubule network, microtubule-associated motor proteins and spindle assembly factors, the cell's cortex, and the chromosomes themselves. The result is a dynamic structure capable of aligning pairs of sister chromatids, sensing chromosome misalignment, and generating force to segregate the replicated genome into two daughters. Because the centrosome lies at the center of the array of microtubule minus-ends, and the essential one-to-two duplication of the centrosome prior to mitosis is linked to cell cycle progression, this organelle has long been implicated as a device to generate spindle bipolarity. However, this classic model for spindle assembly is challenged by observations and experimental manipulations demonstrating that acentrosomal cells can and do form bipolar spindles, both mitotic and meiotic. Indeed, recent comprehensive proteomic analysis of centrosome-dependent versus independent mitotic spindle assembly mechanisms reveals a large, common set of genes required for both processes, with very few genes needed to differentiate between the two. While these studies cast doubt on an absolute role for the centrosome in establishing spindle polarity, it is clear that having too few or too many centrosomes results in abnormal chromosome segregation and aneuploidy. Here we review the case both for and against the role of the centrioles and centrosomes in ensuring proper assembly of a bipolar spindle, an essential element in the maintenance of genomic stability.
    International review of cell and molecular biology 11/2014; 313:179-217. DOI:10.1016/B978-0-12-800177-6.00006-2 · 3.42 Impact Factor
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    • "For the establishment of the ninefold symmetrical centriole structure, the length of the cartwheel spoke is as important as the assembly of the ninefold symmetrical hub [53,54]. Experiments using Chlamydomonas bld10 mutants expressing truncated Bld10p revealed that Bld10p constitutes the distal part of the spoke and contributes to the formation of spokes of the proper length (figure 5b) [26]. "
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    ABSTRACT: The cartwheel is a subcentriolar structure consisting of a central hub and nine radially arranged spokes, located at the proximal end of the centriole. It appears at the initial stage of the centriole assembly process as the first ninefold symmetrical structure. The cartwheel was first described more than 50 years ago, but it is only recently that its pivotal role in establishing the ninefold symmetry of the centriole was demonstrated. Significant progress has since been made in understanding its fine structure and assembly mechanism. Most importantly, the central part of the cartwheel, from which the ninefold symmetry originates, is shown to form by self-association of nine dimers of the protein SAS-6. This finding, together with emerging data on other components of the cartwheel, has opened new avenues in centrosome biology.
    Philosophical Transactions of The Royal Society B Biological Sciences 09/2014; 369(1650). DOI:10.1098/rstb.2013.0458 · 7.06 Impact Factor
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    • "The cilium is the cell's ''antenna'': a specialized membrane domain enriched in specific receptors that detect extracellular signals. Primary cilia are involved in a variety of functions from cell fate determination during embryogenesis, to tissue maintenance and homeostasis (Goetz and Anderson, 2010; Hildebrandt et al., 2011; Berbari et al., 2009; Bettencourt-Dias et al., 2011; Nigg and Raff, 2009; Azimzadeh and Marshall, 2010). Defects in cilia assembly, structure or function lead to disorders of heterogeneous severity collectively referred to as ciliopathies. "
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    ABSTRACT: The primary cilium is an essential organelle required for animal development and adult homeostasis that is found on most animal cells. The primary cilium contains a microtubule-based axoneme cytoskeleton that typically grows from the mother centriole in G0/G1 phase of the cell cycle as a membrane-bound compartment that protrudes from the cell surface. A unique system of bidirectional transport, intraflagellar transport (IFT), maintains the structure and function of cilia. While the axoneme is dynamic, growing and shrinking at its tip, at the same time it is very stable to the effects of microtubule-targeting drugs. The primary cilia found on Drosophila spermatocytes diverge from the general rules of primary cilium biology in several respects. Among these unique attributes, spermatocyte cilia assemble from all four centrioles in an IFT-independent manner in G2 phase, and persist continuously through two cell divisions. Here, we show that Drosophila spermatocyte primary cilia are extremely sensitive to microtubule-targeting drugs, unlike their mammalian counterparts. Spermatocyte cilia and their axonemes fail to assemble or be maintained upon nocodazole treatment, while centriole replication appears unperturbed. On the other hand, paclitaxel (Taxol), a microtubule-stabilizing drug, disrupted transition zone assembly and anchoring to the plasma membrane while causing spermatocyte primary cilia to grow extensively long during the assembly/elongation phase, but did not overtly affect the centrioles. However, once assembled to their mature length, spermatocyte cilia appeared unaffected by Taxol. The effects of these drugs on axoneme dynamics further demonstrate that spermatocyte primary cilia are endowed with unique assembly properties.
    Biology Open 11/2013; 2(11):1137-47. DOI:10.1242/bio.20135355 · 2.42 Impact Factor
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