Centriole assembly in Caenorhabditis elegans

Pelletier, Laurence; O’Toole, Eileen; Schwager, Anne; Hyman, Anthony A.; Müller‐Reichert, Thomas

doi:10.1038/nature05318

Cited by 366 publications

(568 citation statements)

References 28 publications

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“…Examination of centrioles from Drosophila sas-6 mutants has led to a model whereby centriole assembly involves incorporation of "enatosomes," modules that comprise one-ninth of the centriole's rotational architecture (Rodrigues-Martins et al, 2007). These findings have led to the hypothesis that the precursor tube that Sas-6 regulates provides ninefold assembly instruction similar to the cartwheel in Chlamydomonas (Pelletier et al, 2006;RodriguesMartins et al, 2008). These models are not exclusive and a unified model for the establishment of the elegant ninefold V. Mottier-Pavie and T. L. Megraw rotational architecture of the centriole may eventually be reconciled.…”

Section: Proper Assembly Of Centrioles and Basal Bodies Require Bld10mentioning

confidence: 99%

“…In Tetrahymena basal bodies, Sas6a was identified as a component of the cartwheel (Kilburn et al, 2007) and in Chlamydomonas, Sas-6 is a cartwheel component required to establish ninefold symmetry . In Caenorhabditis elegans there appears to be no bld10 ortholog (Dutcher, 2007), and centriole biogenesis involves assembly of a precursor tube-like structure that requires sas-6 (Pelletier et al, 2006). Examination of centrioles from Drosophila sas-6 mutants has led to a model whereby centriole assembly involves incorporation of "enatosomes," modules that comprise one-ninth of the centriole's rotational architecture (Rodrigues-Martins et al, 2007).…”

Section: Proper Assembly Of Centrioles and Basal Bodies Require Bld10mentioning

confidence: 99%

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DrosophilaBld10 Is a Centriolar Protein That Regulates Centriole, Basal Body, and Motile Cilium Assembly

Mottier-Pavie

Megraw

2009

MBoC

107

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Cilia and flagella play multiple essential roles in animal development and cell physiology. Defective cilium assembly or motility represents the etiological basis for a growing number of human diseases. Therefore, how cilia and flagella assemble and the processes that drive motility are essential for understanding these diseases. Here we show that Drosophila Bld10, the ortholog of Chlamydomonas reinhardtii Bld10p and human Cep135, is a ubiquitous centriolar protein that also localizes to the spermatid basal body. Mutants that lack Bld10 assemble centrioles and form functional centrosomes, but centrioles and spermatid basal bodies are short in length. bld10 mutant flies are viable but male sterile, producing immotile sperm whose axonemes are deficient in the central pair of microtubules. These results show that Drosophila Bld10 is required for centriole and axoneme assembly to confer cilium motility. INTRODUCTIONCentrioles lie at the core of centrosomes. They consist of a ninefold symmetrical array of nine triplet microtubules arranged in a cylinder. In most differentiated cell types, centrioles transform into basal bodies, membrane-embedded centrioles that template cilium and flagellum axoneme assembly. The requirement of cilia and flagella for many developmental and physiological processes, together with the growing list of human diseases that result from defects in basal bodies and cilia (Badano et al., 2006;Bisgrove and Yost, 2006;Bettencourt-Dias and Glover, 2007;Fliegauf et al., 2007;Marshall, 2008), drives the need to understand the basic processes involved in centriole, basal body, cilium assembly, and motility.In Drosophila several approaches have identified evolutionarily conserved centriole proteins required for centriole biogenesis including Sak, Sas4, Sas6, Ana1, Ana2, and Asterless (Bettencourt-Dias et al., 2005;Basto et al., 2006;Goshima et al., 2007;Rodrigues-Martins et al., 2007;Blachon et al., 2008). In flies, mutations in these genes abolish centrosome and cilium/flagellum assembly (except mutations in ana1 and ana2, which have not been described yet). Additional centriole/ basal body proteins including Spd-2, Drosophila pericentrin-like protein (D-PLP)/CP309, and uncoordinated (UNC) function in pericentriolar material (PCM) recruitment to centrosomes and/or the assembly of cilia and flagella Kawaguchi and Zheng, 2004;Martinez-Campos et al., 2004;Dix and Raff, 2007;Giansanti et al., 2008). Identification of the complete set of centriole components is necessary to define their individual and cooperative roles in the assembly and function of centrioles and cilia.In Chlamydomonas reinhardtii, mutations in the bld10 gene result in complete loss of flagella, giving the cells a "bald" appearance, due to a failure to assemble centrioles (Matsuura et al., 2004;Hiraki et al., 2007). Bld10p functions in the formation of the cartwheel, a ninefold symmetrical scaffold structure essential for an early step of centriole/basal body assembly . From RNA interference (RNAi) studies in cell culture, the human ort...

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Section: Proper Assembly Of Centrioles and Basal Bodies Require Bld10mentioning

confidence: 99%

Section: Proper Assembly Of Centrioles and Basal Bodies Require Bld10mentioning

confidence: 99%

DrosophilaBld10 Is a Centriolar Protein That Regulates Centriole, Basal Body, and Motile Cilium Assembly

Mottier-Pavie

Megraw

2009

MBoC

107

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“…In some cases, human homologues have been identified and shown to have similar function. For example, SAS4 was shown to be required for procentriole formation through the deposition of centriolar microtubules in C. elegans [4,5]. Centrosomal P4.1-associated protein (CPAP), a human SAS4-related protein, was found to be required for centrosome function in human cells [6,7].…”

Section: Introductionmentioning

confidence: 99%

Tankyrase 1 regulates centrosome function by controlling CPAP stability

2012

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CPAP-a gene mutated in primary microcephaly-is required for procentriole formation. Here we show that CPAP degradation and function is controlled by the poly(ADP-ribose) polymerase tankyrase 1. CPAP is PARsylated by tankyrase 1 in vitro and in vivo. Overexpression of tankyrase 1 leads to CPAP proteasomal degradation, preventing centriole duplication, whereas depletion of tankyrase 1 stabilizes CPAP in G1, generating elongated procentrioles and multipolarity. Tankyrase 1 localizes to centrosomes exclusively in G1, coinciding with CPAP degradation. Hence, tankyrase 1-mediated PARsylation regulates CPAP levels during the cell cycle to limit centriole elongation and ensure normal centrosome function.

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“…In C. elegans embryos, centriogenesis is triggered by a signal mediated by several key molecules, including ZYG-1 (O'Connell et al, 2001), which causes the targeting of SAS5 and SAS6 to a nascent centriole (Delattre et al, 2006;Pelletier et al, 2006). These molecules are required for formation and elongation of a central tube, a structural intermediate of the centriole, onto which nine sets of centriolar microtubules become organized in a SAS4-dependent manner (Pelletier et al, 2006).…”

Section: Introductionmentioning

confidence: 99%

γ-Tubulin-containing abnormal centrioles are induced by insufficient Plk4 in human HCT116 colorectal cancer cells

Kuriyama

Bettencourt-Dias

Hoffmann

et al. 2009

Journal of Cell Science

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1 essential for initiation of centriole biogenesis, is not associated with the γ-tubulin-specific abnormal centrosomes. The amount of Plk4 at each centrosome was less in cells with abnormal centrosomes than cells without γ-tubulin-specific abnormal centrosomes. In addition, the formation of abnormal structures was abolished by expression of exogenous Plk4, but not SAS6 and Cep135/Bld10p, which are downstream regulators required for the organization of nine-triplet microtubules. These results suggest that HCT116 cells fail to organize the ninefold symmetry of centrioles due to insufficient Plk4.

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Centriole assembly in Caenorhabditis elegans

Cited by 366 publications

References 28 publications

DrosophilaBld10 Is a Centriolar Protein That Regulates Centriole, Basal Body, and Motile Cilium Assembly

DrosophilaBld10 Is a Centriolar Protein That Regulates Centriole, Basal Body, and Motile Cilium Assembly

Tankyrase 1 regulates centrosome function by controlling CPAP stability

γ-Tubulin-containing abnormal centrioles are induced by insufficient Plk4 in human HCT116 colorectal cancer cells

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