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

Abstract

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...

The Microtubule Cytoskeleton during the Early Drosophila Spermiogenesis

“…One feature that is unique to meiosis II in Drosophila and insect spermatogenesis is the presence of a single centriole in each centrosome [ 26 , 27 ]. Therefore, at the end of meiosis, each spermatid inherits a centriole and an associated cilium-like region (CLR) ( Figure 3 A″) that is the precursor of the sperm axoneme [ 1 ].…”

“…Unlike mammalian cells, in which stable MTs are only associated with ciliary axonemes, the anti-acetylated tubulin antibody recognized some cytoplasmic MTs in Drosophila testis in addition to the axoneme MTs ( Figure 3A,B). One feature that is unique to meiosis II in Drosophila and insect spermatogenesis is the presence of a single centriole in each centrosome [26,27]. Therefore, at the end of meiosis, each spermatid inherits a centriole and an associated cilium-like region (CLR) ( Figure 3A") that is the precursor of the sperm axoneme [1].…”

A role for primary cilia in coral calcification?

“…fruit flies), procentriole formation (daughter centriole initiation) starts already at telophase, and centrosomes are duplicated almost throughout the entire cell cycle. In these organisms, the primary cilium exists only in a small number of cell types, and in specific cell lineages, the two centrioles are able to promote formation of an axoneme (Lattao et al 2017 ; Riparbelli et al 2020 ). In anthozoans, the biology of centrioles and centrosomes along the cell cycle is not well documented; this is especially true for the calicoblast cells.…”

The Centrosome: Conclusions and Perspectives

“…Often, the exceptions to rules allow us to better understand the rules themselves. One such exception in centrosomal biology is the centriole structure observed in some Hexapoda groups [ 26 ]. An interesting remark by Riparbelli and co-authors suggests that this group of organisms, which are the most numerous in the animal world and live in different habitats, represent a kind of living laboratory.…”

“…The discovery of groups of Hexapoda with centrioles of an unusual structure that deviates from the generally accepted nine-arm symmetry raises the question of the roles of the cartwheel and the Sas6 protein in the assembly of centrioles, as described in the case of model organisms. To the results of this work on the diversity of centriole shapes [ 26 ], we can add another type of deviation, which we observed in wasps: centrioles without microtubules [ 27 ]. At the same time, these forms retained a ninth-order symmetry and contained nine prongs, which, together, formed a cogwheel structure.…”