Structural characterization of procentrioles in Drosophila spermatids

Gottardo, Marco; Callaini, Giuliano; Riparbelli, Maria Giovanna

doi:10.1002/cm.21260

Cited by 25 publications

(21 citation statements)

References 37 publications

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“…A similar enigma existed previously in insects until it was shown that insect sperm possesses, in addition to the known centriole, a second atypical centriolar structure 14–16 . This atypical structure has been shown to be essential for normal fertility and embryo development 15,17 .…”

Section: Introductionsupporting

confidence: 55%

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A novel atypical sperm centriole is functional during human fertilization

et al. 2018

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The inheritance of the centrosome during human fertilization remains mysterious. Here we show that the sperm centrosome contains, in addition to the known typical barrel-shaped centriole (the proximal centriole, PC), a surrounding matrix (pericentriolar material, PCM), and an atypical centriole (distal centriole, DC) composed of splayed microtubules surrounding previously undescribed rods of centriole luminal proteins. The sperm centrosome is remodeled by both reduction and enrichment of specific proteins and the formation of these rods during spermatogenesis. In vivo and in vitro investigations show that the flagellum-attached, atypical DC is capable of recruiting PCM, forming a daughter centriole, and localizing to the spindle pole during mitosis. Altogether, we show that the DC is compositionally and structurally remodeled into an atypical centriole, which functions as the zygote’s second centriole. These findings now provide novel avenues for diagnostics and therapeutic strategies for male infertility, and insights into early embryo developmental defects.

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Section: Introductionsupporting

confidence: 55%

“…However, recently a second centriole that is atypical was described in insect sperm 15,16,25,42 . Similarly, here we show that mammalian sperm also have one typical and one atypical centriole.…”

Section: Discussionmentioning

confidence: 99%

A novel atypical sperm centriole is functional during human fertilization

et al. 2018

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“…Close to the basal body of spermatids, there is a small disk of dense material, the “proximal centriole-like” or PCL (Blachon et al 2009; Gottardo et al 2015c), that may represent the origin for the second centriole in the Drosophila zygote (Blachon et al 2014; Khire et al 2016). PCL formation depends on Plk4, Sas-6, and Poc1, and the PCL contains many centriolar proteins that include Sas-6, Ana1, and Bld10p/Cep135 (Blachon et al 2009).…”

Section: When the Centriole Becomes The Basal Body: Ciliogenesismentioning

confidence: 99%

The Centrioles,Centrosomes, Basal Bodies, and Cilia ofDrosophila melanogaster

Lattao¹,

Kovács²,

Glover

2017

Genetics

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Centrioles play a key role in the development of the fly. They are needed for the correct formation of centrosomes, the organelles at the poles of the spindle that can persist as microtubule organizing centers (MTOCs) into interphase. The ability to nucleate cytoplasmic microtubules (MTs) is a property of the surrounding pericentriolar material (PCM). The centriole has a dual life, existing not only as the core of the centrosome but also as the basal body, the structure that templates the formation of cilia and flagellae. Thus the structure and functions of the centriole, the centrosome, and the basal body have an impact upon many aspects of development and physiology that can readily be modeled in Drosophila. Centrosomes are essential to give organization to the rapidly increasing numbers of nuclei in the syncytial embryo and for the spatially precise execution of cell division in numerous tissues, particularly during male meiosis. Although mitotic cell cycles can take place in the absence of centrosomes, this is an error-prone process that opens up the fly to developmental defects and the potential of tumor formation. Here, we review the structure and functions of the centriole, the centrosome, and the basal body in different tissues and cultured cells of Drosophila melanogaster, highlighting their contributions to different aspects of development and cell division.

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“…An unexpected centriole duplication is also observed in early spermatids of some insect species in which a structurally distinct procentriole is observed close to the proximal region of the basal body at the beginning of the axoneme elongation ( Figure 6B,C) [96,122,123]. The assembly of these procentrioles requires in Drosophila typical centriolar proteins, such as Ana1, Bld10/Cep135, Sak/Plk4 and Sas6 [82,124,125].…”

Section: Centriole Overduplication In Insects: Breaking the Rulesmentioning

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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Structural characterization of procentrioles in Drosophila spermatids

Cited by 25 publications

References 37 publications

A novel atypical sperm centriole is functional during human fertilization

A novel atypical sperm centriole is functional during human fertilization

The Centrioles,Centrosomes, Basal Bodies, and Cilia ofDrosophila melanogaster

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

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