The 3D architecture and molecular foundations of de novo centriole assembly via bicentrioles

Pereira, Sónia Gomes; Sousa, Ana Laura; Nabais, Catarina; Paixão, Tiago; Holmes, Alexander J.; Schorb, Martin; Goshima, Gohta; Tranfield, Erin M.; Becker, Jörg; Bettencourt-Dias, Mónica

doi:10.1016/j.cub.2021.07.063

Cited by 9 publications

(9 citation statements)

References 77 publications

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“…It will be interesting in the future to analyse in depth the 3D structure of Plasmodium BBs and their components, for example, by using these BB and mitotic spindle markers and correlative light and electron microscopy (CLEM) as described recently for the bryophyte Physcomitrium ( Pereira et al, 2021 ). In a recent study, Raspa and Brochet have used expansion microscopy to study the MTOC structures showing its bipartite architecture in Plasmodium ( Rashpa & Brochet, 2022 ), complementing our findings by live cell imaging, super resolution, and EM.…”

Section: Discussionmentioning

confidence: 99%

Plasmodium SAS4: basal body component of male cell which is dispensable for parasite transmission

et al. 2022

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The centriole/basal body (CBB) is an evolutionarily conserved organelle acting as a microtubule organising centre (MTOC) to nucleate cilia, flagella, and the centrosome. SAS4/CPAP is a conserved component associated with BB biogenesis in many model flagellated cells. Plasmodium, a divergent unicellular eukaryote and causative agent of malaria, displays an atypical, closed mitosis with an MTOC (or centriolar plaque), reminiscent of an acentriolar MTOC, embedded in the nuclear membrane. Mitosis during male gamete formation is accompanied by flagella formation. There are two MTOCs in male gametocytes: the acentriolar nuclear envelope MTOC for the mitotic spindle and an outer centriolar MTOC (the basal body) that organises flagella assembly in the cytoplasm. We show the coordinated location, association and assembly of SAS4 with the BB component, kinesin-8B, but no association with the kinetochore protein, NDC80, indicating that SAS4 is part of the BB and outer centriolar MTOC in the cytoplasm. Deletion of the SAS4 gene produced no phenotype, indicating that it is not essential for either male gamete formation or parasite transmission.

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Section: Discussionmentioning

confidence: 99%

Plasmodium SAS4: basal body component of male cell which is dispensable for parasite transmission

et al. 2022

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“…In ultrastructural analyses, abnormal BBs were observed in the Mp bld10 mutant, and electron‐dense materials were observed instead of BBs in the Pp bld10 mutant, as reported by Gomes Pereira et al . (2021). These lines of evidence suggest strongly that MpBLD10 and PpBLD10 are BB proteins that function in BB assembly.…”

Section: Discussionmentioning

confidence: 99%

“…BBs of hornworts are monomorphic, and located parallel to each other. Liverworts and mosses possess dimorphic BBs located at staggered positions; the anterior basal body (ABB) is formed at the right side and posterior basal body (PBB) is located at the left side when viewed from the anterior side of the spermatozoid (Figs 2a, 3a) with distinctive angles specific to species (Carothers & Kreitner, 1968; Renzaglia et al ., 1985; Bernhard & Renzaglia, 1995; Carothers et al ., 1997; Gomes Pereira et al ., 2021). Although thorough morphological studies have been conducted, the molecular and genetic players in streptophyte spermatogenesis, including key factors acting in the BB arrangement in bryophytes, remain to be identified.…”

Section: Introductionmentioning

confidence: 99%

Phylogenetic distribution and expression pattern analyses identified a divergent basal body assembly protein involved in land plant spermatogenesis

et al. 2022

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Land plant spermatozoids commonly possess characteristic structures such as the spline, which consists of a microtubule array, the multilayered structure (MLS) in which the uppermost layer is a continuum of the spline, and multiple flagella. However, the molecular mechanisms underpinning spermatogenesis remain to be elucidated.We successfully identified candidate genes involved in spermatogenesis, deeply divergent BLD10s, by computational analyses combining multiple methods and omics data. We then examined the functions of BLD10s in the liverwort Marchantia polymorpha and the moss Physcomitrium patens.MpBLD10 and PpBLD10 are required for normal basal body (BB) and flagella formation. Mpbld10 mutants exhibited defects in remodeling of the cytoplasm and nucleus during spermatozoid formation, and thus MpBLD10 should be involved in chromatin reorganization and elimination of the cytoplasm during spermiogenesis.We identified orthologs of MpBLD10 and PpBLD10 in diverse Streptophyta and found that MpBLD10 and PpBLD10 are orthologous to BLD10/CEP135 family proteins, which function in BB assembly. However, BLD10s evolved especially quickly in land plants and MpBLD10 might have acquired additional functions in spermatozoid formation through rapid molecular evolution.

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“…The “bicentriole” is composed of two centrioles sharing a single elongated cartwheel structure. The two centrioles subsequently separate and serve as the basal bodies forming the two flagella ( Moser and Kreitner, 1970 ; Perkins, 1970 ; Robbins, 1984 ; Gomes Pereira et al, 2021 ). Similarly, multiple centrioles form de novo through electron-dense structures termed blepharoplasts in plants such as ferns and cycads during the generation of multiciliated sperms ( Mizukami and Gall, 1966 ; Hepler, 1976 ).…”

Section: De Novo Centriole Formation Naturally Occurs In Var...mentioning

confidence: 99%

“…In the multiciliated cells of planarians, de novo centriole amplification requires the planarian homologs of Plk4, Cep152, CPAP, STIL and SAS-6, the conserved core proteins for centriole assembly ( Azimzadeh et al, 2012 ; Li et al, 2020 ). A recent study involving the bryophyte Physcomitrium patens revealed that the evolutionarily conserved centriole proteins SAS-6, Bld10 (Cep135), and POC1 are required for bicentriole-mediated de novo centriole biogenesis ( Gomes Pereira et al, 2021 ). These results suggest that a common molecular mechanism may be used for centriole formation in a wide range of species.…”

Section: De Novo Centriole Formation Naturally Occurs In Var...mentioning

confidence: 99%

Experimental and Natural Induction of de novo Centriole Formation

Takumi

Kitagawa

2022

Front. Cell Dev. Biol.

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In cycling cells, new centrioles are assembled in the vicinity of pre-existing centrioles. Although this canonical centriole duplication is a tightly regulated process in animal cells, centrioles can also form in the absence of pre-existing centrioles; this process is termed de novo centriole formation. De novo centriole formation is triggered by the removal of all pre-existing centrioles in the cell in various manners. Moreover, overexpression of polo-like kinase 4 (Plk4), a master regulatory kinase for centriole biogenesis, can induce de novo centriole formation in some cell types. Under these conditions, structurally and functionally normal centrioles can be formed de novo. While de novo centriole formation is normally suppressed in cells with intact centrioles, depletion of certain suppressor proteins leads to the ectopic formation of centriole-related protein aggregates in the cytoplasm. It has been shown that de novo centriole formation also occurs naturally in some species. For instance, during the multiciliogenesis of vertebrate epithelial cells, massive de novo centriole amplification occurs to form numerous motile cilia. In this review, we summarize the previous findings on de novo centriole formation, particularly under experimental conditions, and discuss its regulatory mechanisms.

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The 3D architecture and molecular foundations of de novo centriole assembly via bicentrioles

Cited by 9 publications

References 77 publications

Plasmodium SAS4: basal body component of male cell which is dispensable for parasite transmission

Plasmodium SAS4: basal body component of male cell which is dispensable for parasite transmission

Phylogenetic distribution and expression pattern analyses identified a divergent basal body assembly protein involved in land plant spermatogenesis

Experimental and Natural Induction of de novo Centriole Formation

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