Centrioles without microtubules - a new morphological type of centriole

Uzbekov, Rustem; Garanina, Anastasiia S.; Bressac, Christophe

doi:10.1242/bio.036012

Cited by 15 publications

(18 citation statements)

References 29 publications

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“…This points to the presence of a mechanism monitoring the elongation of the cartwheel during male meiosis Cells 2020, 9, 744 8 of 27 and suggests that this control could be overcome in some insect species that display very elongated cartwheels. A very strange condition has been recently reported in larval tissues of the male wasp Anisopteromalus in which cylindrical structures with nine-fold symmetry but without microtubules would be present [98]. Surprisingly, adult tissues of this species display usual centrioles with triplet microtubules and nine-fold symmetry.…”

Section: Centrioles In Hexapoda: Common and Uncommon Modelsmentioning

confidence: 72%

Centrioles and Ciliary Structures during Male Gametogenesis in Hexapoda: Discovery of New Models

Riparbelli

Persico

Dallai

et al. 2020

Cells

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Centrioles are-widely conserved barrel-shaped organelles present in most organisms. They are indirectly involved in the organization of the cytoplasmic microtubules both in interphase and during the cell division by recruiting the molecules needed for microtubule nucleation. Moreover, the centrioles are required to assemble cilia and flagella by the direct elongation of their microtubule wall. Due to the importance of the cytoplasmic microtubules in several aspects of the cell life, any defect in centriole structure can lead to cell abnormalities that in humans may result in significant diseases. Many aspects of the centriole dynamics and function have been clarified in the last years, but little attention has been paid to the exceptions in centriole structure that occasionally appeared within the animal kingdom. Here, we focused our attention on non-canonical aspects of centriole architecture within the Hexapoda. The Hexapoda is one of the major animal groups and represents a good laboratory in which to examine the evolution and the organization of the centrioles. Although these findings represent obvious exceptions to the established rules of centriole organization, they may contribute to advance our understanding of the formation and the function of these organelles.Thus, the increase of g-tubulin leads to an increase in the nucleation of both astral and spindle microtubules, which drive the assembly of a functional spindle.At the heart of the centrosome there is a pair of centrioles, two microtubule-based barrel-shaped organelles of defined length and diameter [29], that warrants the integrity and the supramolecular organization of the centrosome itself. The coiled-coil proteins, pericentrin-like protein (PLP) and Cep152/Asterless form the scaffold for the matrix proteins Cep192/Spd-2, Cep215/Cnn and g-tubulin.It was observed PLP's C termini are located close to the centriole wall [26].In addition, to be the reference point for the organization of the centrosomal material, the centrioles may also act as templates for the axoneme assembly in cilia and flagella, that are involved in signalling and motility [30]. Therefore, the proper organization and dynamics of the centrioles are mandatory to ensure healthy cell life. Structural anomalies of the centrioles are found in several human cancers [31][32][33][34][35][36] and can be the cause of a spectrum of pathologies spanning from infertility to ciliopathies [37,38].Since, the centrioles impact upon several aspects of cell development and physiology, their structure and function have been studied over the years. However, this analysis was mainly addressed to examine centrioles in a few model organisms, such as Chlamydomonas reinhardtii, Caenorhabditis elegans, Drosophila melanogaster, and some vertebrate cell lines. From these studies emerge a highly conserved organization of the centrioles. However, investigations in different animal groups revealed distinct and sometimes important differences in the architecture of the centrioles [39,40]. Therefore, the analysi...

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Section: Centrioles In Hexapoda: Common and Uncommon Modelsmentioning

confidence: 72%

Centrioles and Ciliary Structures during Male Gametogenesis in Hexapoda: Discovery of New Models

Riparbelli

Persico

Dallai

et al. 2020

Cells

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“…Each centriole consists of 9 MT triplets, and it is associated with subdistal appendages, distal appendages, striated roots, and satellites ( Figure 1 ). In some cases or certain stages of the development of organisms, the walls of the centrioles may contain MT doublets [ 14 , 15 , 16 ], MT singlets [ 17 , 18 , 19 ], or no MT at all [ 20 , 21 ], while maintaining nine-beam symmetry.…”

Section: Postulates Of Centrosomal Biologymentioning

confidence: 99%

“…Centrioles do not have MTs in haploid male larvae trophocytes and hypodermal cells of wasps Anisopteromalus calandrae [ 20 ]. However, their MT-free centrioles’ shape and size are similar to canonical centrioles with MT triplets of adult (imago) insects or late larvae of different wasps’ types ( Figure 2 ).…”

Section: Postulates Of Centrosomal Biologymentioning

confidence: 99%

“…However, their MT-free centrioles’ shape and size are similar to canonical centrioles with MT triplets of adult (imago) insects or late larvae of different wasps’ types ( Figure 2 ). The centriole’s symmetry is maintained, and they contain nine prongs of electron-dense material in their walls forming the structure of the “cogwheel” [ 20 ]. One possibility is that at this stage of development, the genes encoding the proteins responsible for the construction of MT triplets have not yet turned on.…”

Section: Postulates Of Centrosomal Biologymentioning

confidence: 99%

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Principal Postulates of Centrosomal Biology. Version 2020

Uzbekov

Avidor‐Reiss

2020

Cells

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The centrosome, which consists of two centrioles surrounded by pericentriolar material, is a unique structure that has retained its main features in organisms of various taxonomic groups from unicellular algae to mammals over one billion years of evolution. In addition to the most noticeable function of organizing the microtubule system in mitosis and interphase, the centrosome performs many other cell functions. In particular, centrioles are the basis for the formation of sensitive primary cilia and motile cilia and flagella. Another principal function of centrosomes is the concentration in one place of regulatory proteins responsible for the cell’s progression along the cell cycle. Despite the existing exceptions, the functioning of the centrosome is subject to general principles, which are discussed in this review.

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“…Therefore, a preexisting centriole can nucleate an atypical centriole as observed in insects (Blachon et al 2009, Gottardo et al 2015, Dallai et al 2017, Fishman et al 2017. Also, the atypical sperm centriole can nucleate a typical centriole in the zygote (Blachon et al 2014, Uzbekov et al 2018).…”

Section: Box 1 Centriole Duplicationmentioning

confidence: 99%

It takes two (centrioles) to tango

Avidor‐Reiss

Fishman

2019

Reproduction

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Cells that divide during embryo development require precisely two centrioles during interphase and four centrioles during mitosis. This precise number is maintained by allowing each centriole to nucleate only one centriole per cell cycle (i.e. centriole duplication). Yet, how the first cell of the embryo, the zygote, obtains two centrioles has remained a mystery in most mammals and insects. The mystery arose because the female gamete (oocyte) is thought to have no functional centrioles and the male gamete (spermatozoon) is thought to have only one functional centriole, resulting in a zygote with a single centriole. However, recent studies in fruit flies, beetles and mammals, including humans, suggest an alternative explanation: spermatozoa have a typical centriole and an atypical centriole. The sperm typical centriole has a normal structure but distinct protein composition, whereas the sperm atypical centriole is distinct in both. During fertilization, the atypical centriole is released into the zygote, nucleates a new centriole and participates in spindle pole formation. Thus, the spermatozoa’s atypical centriole acts as a second centriole in the zygote. Here, we review centriole biology in general and especially in reproduction, we describe the discovery of the spermatozoon atypical centriole, and we provide an updated model for centriole inherence during sexual reproduction. While we focus on humans and other non-rodent mammals, we also provide a broader evolutionary perspective.

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Centrioles without microtubules - a new morphological type of centriole

Cited by 15 publications

References 29 publications

Centrioles and Ciliary Structures during Male Gametogenesis in Hexapoda: Discovery of New Models

Centrioles and Ciliary Structures during Male Gametogenesis in Hexapoda: Discovery of New Models

Principal Postulates of Centrosomal Biology. Version 2020

It takes two (centrioles) to tango

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