Distinct functions of Mst77F and protamines in nuclear shaping and chromatin condensation during Drosophila spermiogenesis

Rathke, Christina; Barckmann, Bridlin; Burkhard, Silja; Jayaramaiah-Raja, Sunil; Roote, John; Renkawitz‐Pohl, Renate

doi:10.1016/j.ejcb.2009.09.001

Cited by 89 publications

(140 citation statements)

References 45 publications

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“…This protein class includes Mst35Ba and Mst35Bb, which are the products of duplicate genes, and Mst77F (Rathke et al 2014). Consistent with the proposed role of SNBPs, males mutant for Mst35Ba and Mst35Bb or Mst77F produce spermatids or sperm with abnormal nuclear shapes (Rathke et al 2010;Tirmarche et al 2014). However, we did not detect abnormalities in sperm (n = 3050) of ddbt Z4344 /Df males, as assayed by staining with the DNA dye DAPI.…”

supporting

confidence: 86%

The Deadbeat Paternal Effect of Uncapped Sperm Telomeres on Cell Cycle Progression and Chromosome Behavior in Drosophila melanogaster

2016

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Telomere-capping complexes (TCCs) protect the ends of linear chromosomes from illegitimate repair and end-to-end fusions and are required for genome stability. The identity and assembly of TCC components have been extensively studied, but whether TCCs require active maintenance in nondividing cells remains an open question. Here we show that Drosophila melanogaster requires Deadbeat (Ddbt), a sperm nuclear basic protein (SNBP) that is recruited to the telomere by the TCC and is required for TCC maintenance during genome-wide chromatin remodeling, which transforms spermatids to mature sperm. Ddbt-deficient males produce sperm lacking TCCs. Their offspring delay the initiation of anaphase as early as cycle 1 but progress through the first two cycles. Persistence of uncapped paternal chromosomes induces arrest at or around cycle 3. This early arrest can be rescued by selective elimination of paternal chromosomes and production of gynogenetic haploid or haploid mosaics. Progression past cycle 3 can also occur if embryos have reduced levels of the maternally provided checkpoint kinase Chk2. The findings provide insights into how telomere integrity affects the regulation of the earliest embryonic cell cycles. They also suggest that other SNBPs, including those in humans, may have analogous roles and manifest as paternal effects on embryo quality.KEYWORDS telomere maintenance; telomere capping; cell cycle checkpoint; paternal effect; sperm nuclear basic protein T ELOMERES are the natural ends of linear chromosomes and have distinct properties from broken ends. Multiple proteins are enriched predominantly, if not exclusively, at telomeres and form a capping complex that protects telomeric DNA from engaging in aberrant DNA repair activities. Protein components of the telomere-capping complex (TCC) vary among organisms, in part because species differ in telomeric sequences and whether telomeres are maintained by telomerase or alternative mechanisms (Raffa et al. 2011;Mason et al. 2015). Nonetheless, the TCC's essential functions are well conserved. Failure to assemble TCCs results in telomeric DNA degradation, telomere fusions, and genomic instability.Mutations in at least 12 loci of Drosophila melanogaster lead to telomere fusions in neuroblasts. Their analysis has led to the identification of telomere-enriched and telomereexclusive proteins required for telomere elongation or TCC assembly, maintenance, or function (Cenci et al. 2005;Pimpinelli 2006). Absence of any one component results in telomere fusions but components have distinct activities (Pimpinelli 2006). For example, heterochromatin protein 1a (HP1a) binds modified histone H3-MeK9 and represses transcription of telomeric retrotransposons and telomere elongation. HP1a also binds DNA and this activity is required for its capping function. The TCC protein HOAP binds DNA and HP1a. Although HOAP is required for capping, it does not affect retrotransposon transcription or telomere elongation. A third protein, HipHop, binds both HP1a and HOAP. HOAP and HipHo...

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supporting

confidence: 86%

The Deadbeat Paternal Effect of Uncapped Sperm Telomeres on Cell Cycle Progression and Chromosome Behavior in Drosophila melanogaster

2016

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“…S8). This phenotype is similar to those of protamine mutations (Rathke et al 2010). Second, CR45542 −/− and CR44420 −/− mutant testes contained some round uncondensed nuclei (∼30% in CR45542 −/− and ∼20% in CR44420 −/− ) at the mature stage (Fig.…”

Section: Systematic Identification Of Testis-associated Lncrnas In Drsupporting

confidence: 70%

“…Next, we used HIS2AV-RFP and Protamine B-GFP to mark early spermatids and mature sperm, respectively (Rathke et al 2007(Rathke et al , 2010. The round uncondensed sperm of CR44420 −/− , tadpoleshape sperm of lncRNA:TS1 −/− , and bent sperm of CR43416 −/− were positive for Protamine B-GFP but not HIS2AV-RFP, confirming that they corresponded to the late elongate and/or mature stage (Fig.…”

Section: Systematic Identification Of Testis-associated Lncrnas In Drmentioning

confidence: 70%

“…The mutant phenotypes in late germ cell development indicate that these testis-specific lncRNAs play critical roles in the regulation of nuclear condensation and sperm individualization. During late spermatogenesis in both mammals and Drosophila, spermatids need to remodel and condense chromatin by replacing histones with protamines and also require the removal of excess cytoplasm for individualization (Rathke et al 2010). CR44455/6, CR45542, and CR44420 mutant testes exhibited scattered nuclei and round uncondensed nuclei, whereas lncRNA:TS1 and CR43484 mutant testes exhibited a crumpled nucleus phenotype similar to those of protamine mutants (Rathke et al 2010).…”

Section: Discussionmentioning

confidence: 99%

“…During late spermatogenesis in both mammals and Drosophila, spermatids need to remodel and condense chromatin by replacing histones with protamines and also require the removal of excess cytoplasm for individualization (Rathke et al 2010). CR44455/6, CR45542, and CR44420 mutant testes exhibited scattered nuclei and round uncondensed nuclei, whereas lncRNA:TS1 and CR43484 mutant testes exhibited a crumpled nucleus phenotype similar to those of protamine mutants (Rathke et al 2010). In regard to sperm individualization, the testes of 19 lncRNA KO mutants, including CR42858 −/− and CR43282 −/− , exhibited defects in coordinated actin cone movement, resulting in poorly aligned or lagging ICs.…”

Section: Discussionmentioning

confidence: 99%

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Critical roles of long noncoding RNAs in Drosophila spermatogenesis

et al. 2016

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Long noncoding RNAs (lncRNAs), a recently discovered class of cellular RNAs, play important roles in the regulation of many cellular developmental processes. Although lncRNAs have been systematically identified in various systems, most of them have not been functionally characterized in vivo in animal models. In this study, we identified 128 testis-specific Drosophila lncRNAs and knocked out 105 of them using an optimized three-component CRISPR/Cas9 system. Among the lncRNA knockouts, 33 (31%) exhibited a partial or complete loss of male fertility, accompanied by visual developmental defects in late spermatogenesis. In addition, six knockouts were fully or partially rescued by transgenes in a trans configuration, indicating that those lncRNAs primarily work in trans. Furthermore, gene expression profiles for five lncRNA mutants revealed that testis-specific lncRNAs regulate global gene expression, orchestrating late male germ cell differentiation. Compared with coding genes, the testis-specific lncRNAs evolved much faster. Moreover, lncRNAs of greater functional importance exhibited higher sequence conservation, suggesting that they are under constant evolutionary selection. Collectively, our results reveal critical functions of rapidly evolving testis-specific lncRNAs in late Drosophila spermatogenesis.

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Electron microscopic observation of the sagittal structure ofDrosophilamature sperm

Yasuno

Yamamoto

2014

Microsc. Res. Tech.

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Observation of sperm development and determination of their morphological characteristics are very important to the understanding of phylogenetic relationships and the study of sperm function during fertilization. Although ultrastructural studies of sperm development in the testes of the fruit fly Drosophila have been performed, there are few reports describing electron microscopic morphology of mature sperm, that is, those released from the testes to the seminal vesicles. Here, we present the first report of the sagittal organization of Drosophila sperm head and neck regions by scanning electron microscopy (SEM) and transmission electron microscopy (TEM). The head and tail structures of a mature sperm, for example, the acrosome, nucleus, and flagellum, were easy to distinguish by the morphological characteristics of the sperm surface by SEM. The morphological relationships between the surface and internal structures of mature sperm were confirmed by observing longitudinal sections with TEM. Our approach overcame the technical difficulties involved in sample preparation for electron microscopic observation of the Drosophila mature sperm head, and therefore, this study serves as an important foundation for future genetic dissection of sperm ultrastructure and function in male sterile mutants.

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Distinct functions of Mst77F and protamines in nuclear shaping and chromatin condensation during Drosophila spermiogenesis

Cited by 89 publications

References 45 publications

The Deadbeat Paternal Effect of Uncapped Sperm Telomeres on Cell Cycle Progression and Chromosome Behavior in Drosophila melanogaster

The Deadbeat Paternal Effect of Uncapped Sperm Telomeres on Cell Cycle Progression and Chromosome Behavior in Drosophila melanogaster

Critical roles of long noncoding RNAs in Drosophila spermatogenesis

Electron microscopic observation of the sagittal structure ofDrosophilamature sperm

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