Separating from the pack: Molecular mechanisms of<i>Drosophila</i>spermatid individualization

Steinhauer, Josefa

doi:10.1080/21565562.2015.1041345

Cited by 58 publications

(53 citation statements)

References 100 publications

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“…We then stained testes with fluorescently labelled phalloidin to reveal the actin-based individualization complexes (IC) (figure 2 c ). Individualization occurs with the progression of these structures from nuclei toward the distal tip of flagella [33–36]. In wild-type testes, groups of spermatid nuclei remained tightly clustered during and after the passage of the IC (upper panels in figures 2 c , d ).…”

Section: Resultsmentioning

confidence: 99%

TheDrosophilachromosomal protein Mst77F is processed to generate an essential component of mature sperm chromatin

Kimura¹,

Loppin²

2016

Open Biol.

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In most animals, the bulk of sperm DNA is packaged with sperm nuclear basic proteins (SNBPs), a diverse group of highly basic chromosomal proteins notably comprising mammalian protamines. The replacement of histones with SNBPs during spermiogenesis allows sperm DNA to reach an extreme level of compaction, but little is known about how SNBPs actually function in vivo. Mst77F is a Drosophila SNBP with unique DNA condensation properties in vitro, but its role during spermiogenesis remains unclear. Here, we show that Mst77F is required for the compaction of sperm DNA and the production of mature sperm, through its cooperation with protamine-like proteins Mst35Ba/b. We demonstrate that Mst77F is incorporated in spermatid chromatin as a precursor protein, which is subsequently processed through the proteolysis of its N-terminus. The cleavage of Mst77F is very similar to the processing of protamine P2 during human spermiogenesis and notably leaves the cysteine residues in the mature protein intact, suggesting that they participate in the formation of disulfide cross-links. Despite the rapid evolution of SNBPs, sperm chromatin condensation thus involves remarkably convergent mechanisms in distantly related animals.

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Section: Resultsmentioning

confidence: 99%

TheDrosophilachromosomal protein Mst77F is processed to generate an essential component of mature sperm chromatin

Kimura¹,

Loppin²

2016

Open Biol.

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“…After individualization, each individualized sperm lacks most cytoplasm, no longer shares ring canals with its sisters, and is invested in its own plasma membrane. Adapted from Steinhauer (2015). (C) Drawing of a testis showing the position of basally forming ICs in contact with nuclei (blue), as well as mature, apically moving ICs (red; arrowheads) and normal WBs (arrow).…”

Section: Spermatid Individualization Is Abnormal In Cmb Mutantsmentioning

confidence: 99%

Combover interacts with the axonemal component Rsp3 and is required for sperm individualization

et al. 2019

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Gamete formation is key to survival of higher organisms. In male animals, spermatogenesis gives rise to interconnected spermatids that differentiate and individualize into mature sperm, each tightly enclosed by a plasma membrane. In Drosophila melanogaster, individualization of sister spermatids requires the formation of specialized actin cones that synchronously move along the sperm tails, removing inter-spermatid bridges and most of the cytoplasm. Here, we show that Combover (Cmb), originally identified as an effector of planar cell polarity (PCP) under control of Rho kinase, is essential for sperm individualization. cmb mutants are male sterile, with actin cones that fail to move in a synchronized manner along the flagella, despite being correctly formed and polarized initially. These defects are germline autonomous, independent of PCP genes, and can be rescued by wild-type Cmb, but not by a version of Cmb in which known Rho kinase phosphorylation sites are mutated. Furthermore, Cmb binds to the axonemal component Radial spoke protein 3, knockdown of which causes similar individualization defects, suggesting that Cmb coordinates the individualization machinery with the microtubular axonemes.

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“…This shedding event involves two steps: (1) the differential partitioning of cellular components into a cellular wastebag known as a residual body (RB), and (2) the subsequent separation of this RB from the sperm (Steinhauer, 2015). In Drosophila and vertebrates, RB formation requires both actin and microtubules (Steinhauer, 2015;O'Donnell et al, 2001) and occurs as the final step of a post-meiotic cell differentiation process (spermiogenesis) that takes days to weeks and requires extensive cytoskeletal remodeling (Fabian and Brill, 2012;Clermont, 1972;Fig. 1A).…”

Section: Introductionmentioning

confidence: 99%

Cytoskeletal variations in an asymmetric cell division support diversity in nematode sperm size and sex ratios

et al. 2017

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Asymmetric partitioning is an essential component of many developmental processes. As spermatogenesis concludes, sperm are streamlined by discarding unnecessary cellular components into cellular wastebags called residual bodies (RBs). During nematode spermatogenesis, this asymmetric partitioning event occurs shortly after anaphase II, and both microtubules and actin partition into a central RB. Here, we use fluorescence and transmission electron microscopy to elucidate and compare the intermediate steps of RB formation in , sp. SB347 (recently named ) and related nematodes. In all cases, intact microtubules reorganize and move from centrosomal to non-centrosomal sites at the RB-sperm boundary whereas actin reorganizes through cortical ring expansion and clearance from the poles. However, in species with tiny spermatocytes, these cytoskeletal changes are restricted to one pole. Consequently, partitioning yields one functional sperm with the X-bearing chromosome complement and an RB with the other chromosome set. Unipolar partitioning may not require an unpaired X, as it also occurs in XX spermatocytes. Instead, constraints related to spermatocyte downsizing may have contributed to the evolution of a sperm cell equivalent to female polar bodies.

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Separating from the pack: Molecular mechanisms ofDrosophilaspermatid individualization

Cited by 58 publications

References 100 publications

TheDrosophilachromosomal protein Mst77F is processed to generate an essential component of mature sperm chromatin

TheDrosophilachromosomal protein Mst77F is processed to generate an essential component of mature sperm chromatin

Combover interacts with the axonemal component Rsp3 and is required for sperm individualization

Cytoskeletal variations in an asymmetric cell division support diversity in nematode sperm size and sex ratios

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