A Proximal Centriole-Like Structure Is Present in Drosophila Spermatids and Can Serve as a Model to Study Centriole Duplication

Department of Cell Biology, Harvard Medical School, Boston, MA, USA.
Genetics (Impact Factor: 5.96). 04/2009; 182(1):133-44. DOI: 10.1534/genetics.109.101709
Source: PubMed


Most animals have two centrioles in spermatids (the distal and proximal centrioles), but insect spermatids seem to contain only one centriole (Fuller 1993), which functionally resembles the distal centriole. Using fluorescent centriolar markers, we identified a structure near the fly distal centriole that is reminiscent of a proximal centriole (i.e., proximal centriole-like, or PCL). We show that the PCL exhibits several features of daughter centrioles. First, a single PCL forms near the proximal segment of the older centriole. Second, the centriolar proteins SAS-6, Ana1, and Bld10p/Cep135 are in the PCL. Third, PCL formation depends on SAK/PLK4 and SAS-6. Using a genetic screen for PCL defect, we identified a mutation in the gene encoding the conserved centriolar protein POC1, which is part of the daughter centriole initiation site (Kilburn et al. 2007) in Tetrahymena. We conclude that the PCL resembles an early intermediate structure of a forming centriole, which may explain why no typical centriolar structure is observed under electron microscopy. We propose that, during the evolution of insects, the proximal centriole was simplified by eliminating the later steps in centriole assembly. The PCL may provide a unique model to study early steps of centriole formation.

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    • "The Cep135/Bld10p homologue in Drosophila is localized all along the centriole microtubules, not restricted to the proximal end. Importantly, Drosophila mutants that lack the Cep135/Bld10p homologue assemble cartwheels and centrioles, although the cartwheel appears to be unstable [42,45,64,65]. Instead, they have short centrioles and lack central pair microtubules in sperm flagella. "
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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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    • "We found that all of these centriolar proteins are missing from mature sperm, indicating centrosome reduction takes place in both the GC and the PCL. This indicates that the PCL, which was formed during early spermiogenesis and without microtubules (Blachon et al. 2009), loses many of the proteins that formed it during centrosome reduction. "
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    ABSTRACT: Centrosomes are composed of two centrioles surrounded by pericentriolar material (PCM). However, the sperm and the oocyte modify or lose their centrosomes. Consequently, how the zygote establishes its first centrosome, and in particular, the origin of the second zygotic centriole, is uncertain. Drosophila melanogaster spermatids contain a single centriole called the giant centriole and a proximal centriole-like (PCL) structure whose function is unknown. We found that, like the centriole, the PCL loses its protein markers at the end of spermiogenesis. After fertilization, the first two centrioles are observed via the recruitment of the zygotic PCM proteins, and are seen in asterless mutant embryos that cannot form centrioles. The zygote's centriolar proteins label only the daughter centrioles of first two centrioles. These observations demonstrate that the PCL is the origin for the second centriole in the Drosophila zygote, and that a paternal centriole precursor, without centriolar proteins, is transmitted to the egg during fertilization.
    Genetics 02/2014; 197(1). DOI:10.1534/genetics.113.160523 · 5.96 Impact Factor
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    • "Note that the extent of the signal occupied by Asl decreases in basal bodies while PACT continues to increase. This is in agreement with the characterization of Asl localization to the a proximal centriole-like structure after meiosis (Blachon et al., 2009). "
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    Biology Open 01/2014; 3(2). DOI:10.1242/bio.20146577 · 2.42 Impact Factor
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