Drosophila Male Meiosis as a Model System for the Study of Cytokinesis in Animal Cells

Istituto Pasteur-Fondazione Cenci Bolognetti, Universita' Roma La Sapienza, Italy.
Cell Structure and Function (Impact Factor: 1.68). 01/2002; 26(6):609-17. DOI: 10.1247/csf.26.609
Source: PubMed


Drosophila male meiosis offers unique opportunities for mutational dissection of cytokinesis. This system allows easy and unambiguos identification of mutants defective in cytokinesis through the examination of spermatid morphology. Moreover, cytokinesis defects and protein immunostaining can be analyzed with exquisite cytological resolution because of the large size of meiotic spindles. In the past few years several mutations have been isolated that disrupt meiotic cytokinesis in Drosophila males. These mutations specify genes required for the assembly, proper constriction or disassembly of the contractile ring. Molecular characterization of these genes has identified essential components of the cytokinetic machinery, highlighting the role of the central spindle during cytokinesis. This structure appears to be both necessary and sufficient for signaling cytokinesis. In addition, many data indicate that the central spindle microtubules cooperatively interact with elements of the actomyosin contractile ring, so that impairment of either of these structures prevents the formation of the other.

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    • "The hypothesis that there exist potential sites assurr ing such interactions between microtubules and actin filaments has been suggested repeatedly (Goode et al., 2000; MimoriiKiyosue, Tsukita, 2003; Minestrini et al., 2003; Tamura and Draviam, 2012). The idea that there is harmonized regulation of all elements of the syncytium is supported by the fact that connections between cytoskeleton and centrosomes and kinetoo chores and periplasmic actin filaments are sites of location for signaling molecules that regulate synchroo nous transitions from one stage of the nuclear cycle to another (Carmena et al., 1998; Giansanti et al., 2001; Minestrini et al., 2003).The results of our analysis of first meiotic division in oocytes of D. melanogaster females bearing different combinations of sbr alleles point to the involvement of SBR (Dm NXF1) in the formation of the cytoskeleton (Golubkova et al., 2009). This data is consistent with the fact that sbr mutations lead to chromosome instability (Nikitina et al., 2003). "
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    ABSTRACT: The syncytial development is a feature of early embryogenesis and spermatogenesis in Drosophila melanogaster. All elements of syncytium are interconnected by single cytoskeletal network that enables equal conditions and provides synchronic development. The cytoskeleton is essential for the formation and functioning of the mitotic spindle, cytoskeletal elements are the main structural component of cilia and flagella. Intra- and intercellular transport, morphogenesis processes depend from cytoskeleton on both within a single cell, and at the level of the whole organism. The sbr (small bristles) gene of D. melanogaster belongs to the NXF (nuclear export factor) evolutionarily conservative proteins family. Gene Dm nxf1 (sbr), as well as its orthologs in other organisms, controls the export of poly(A)-containing RNA from the nucleus to the cytoplasm, and the corresponding proteins are usually localized in the nucleus or in the nuclear envelope. For SBR protein we have shown the localization not only in the nucleus, but in the cytoplasm marking of characteristic cytoplasmic structures. A breach of the cytoskeleton in the sbr (Dm nxf1) mutant in D. melanogaster shown by us and cytoplasmic localization of the protein SBR allow us to link the specific functions of this protein with the dynamics of the cytoskeleton.
    Cell and Tissue Biology 07/2015; 9(4):271-283. DOI:10.1134/S1990519X15040057
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    • "During spermatogenesis , the 16-cell cluster will enlarge and differentiate before undergoing two successive rounds of meiosis by incomplete cytokinesis, giving rise to a total number of 64 interconnected haploid spermatids (Fig. 1A) (Fuller, 1993; Hime et al., 1996). The two meiotic male germ cell divisions provide an excellent model for cytological, molecular and functional analysis of cytokinesis in vivo (Giansanti et al., 2001; Gonzalez and Glover, 1993). Studies in this system have greatly contributed to the understanding of mitotic spindle regulation, plasma membrane composition, contractile ring formation and membrane trafficking during cytokinesis (Adams et al., 1998; Brill et al., 2000; Cenci et al., 1994; Dyer et al., 2007; Giansanti et al., 2004; Goldbach et al., 2010). "
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    ABSTRACT: During male and female gametogenesis in species ranging from insects to mammals, germ cell cyst formation by incomplete cytokinesis involves the stabilization of cleavage furrows and the formation of stable intercellular bridges called ring canals. Accurate regulation of incomplete cytokinesis is required for both female and male fertility in Drosophila melanogaster. Nevertheless, the molecular mechanisms controlling complete versus incomplete cytokinesis are largely unknown. Here, we show that the scaffold protein Cindr is a novel component of both mitotic and meiotic ring canals during Drosophila spermatogenesis. Strikingly, unlike other male germline ring canal components, including Anillin and Pavarotti, Cindr and contractile ring F-actin dissociate from mitotic ring canals and translocate to the fusome upon completion of the mitotic germ cell divisions. We provide evidence that the loss of Cindr from mitotic ring canals is coordinated by signals that mediate the transition from germ cell mitosis to differentiation. Interestingly, Cindr loss from ring canals coincides with completion of the mitotic germ cell divisions in both Drosophila females and males, thus marking a common step of gametogenesis. We also show that Cindr co-localizes with Anillin at mitotic and meiotic ring canals and is recruited to the contractile ring by Anillin during male germ cell meiotic cytokinesis. Taken together, our analyses reveal a key step of incomplete cytokinesis at the endpoint of the mitotic germ cell divisions in D. melanogaster.
    Developmental Biology 03/2013; 377(1). DOI:10.1016/j.ydbio.2013.02.021 · 3.55 Impact Factor
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    • "n 876 Giansanti and Fuller CYTOSKELETON intervening interphase [Fuller, 1993; Giansanti et al., 2001] "
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    ABSTRACT: Cytokinesis separates the genomic material and organelles of a dividing cell equitably into two physically distinct daughter cells at the end of cell division. This highly choreographed process involves coordinated reorganization and regulated action of the actin and microtubule cytoskeletal systems, an assortment of motor proteins, and membrane trafficking components. Due to their large size, the ease with which exquisite cytological analysis may be performed on them, and the availability of numerous mutants and other genetic tools, Drosophila spermatocytes have provided an excellent system for exploring the mechanistic basis for the temporally programmed and precise spatially localized events of cytokinesis. Mutants defective in male meiotic cytokinesis can be easily identified in forward genetic screens by the production of multinucleate spermatids. In addition, the weak spindle assembly checkpoint in spermatocytes, which causes only a small delay of anaphase onset in the presence of unattached chromosomes, allows investigation of whether gene products required for spindle assembly and chromosome segregation are also involved in cytokinesis. Perhaps due to the large size of spermatocytes and the requirement for two rapid-fire rounds of division without intervening S or growth phases during meiosis, male meiotic mutants have also revealed much about molecular mechanisms underlying new membrane addition during cytokinesis. Finally, cell type-specific differences in the events that set up and complete cytokinesis are emerging from comparison of spermatocytes with cells undergoing mitosis either elsewhere in the organism or in tissue culture. © 2012 Wiley Periodicals, Inc.
    Cytoskeleton 11/2012; 69(11). DOI:10.1002/cm.21063 · 3.12 Impact Factor
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