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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Available from: Elisabetta Bucciarelli, Oct 01, 2015
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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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    • "However midbodies characterize only very late stages of cytokinesis. A fruitful approach, that allowed to identify several molecular players, consists of the genetic dissection of this process in suitable model organisms such as Drosophila melanogaster.18 "
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    ABSTRACT: Cytokinesis separates the cytoplasm and the duplicated genome into two daughter cells at the end of cell division. This process must be finely regulated to maintain ploidy and prevent tumor formation. Drosophila male meiosis provides an excellent cell system for investigating cytokinesis. Mutants affecting this process can be easily identified and spermatocytes are large cells particularly suitable for cytological analysis of cytokinetic structures. Over the past decade, the powerful tools of Drosophila genetics and the unique characteristics of this cell system have led researchers to identify molecular players of the cell cleavage machinery and to address important open questions. Although spermatocyte cytokinesis is incomplete, resulting in formation of stable intercellular bridges, the molecular mechanisms are largely conserved in somatic cells. Thus, studies of Drosophila male meiosis will shed new light on the complex cell circuits regulating furrow ingression and substantially further our knowledge of cancer and other human diseases.
    07/2012; 2(3):185-196. DOI:10.4161/spmg.21711
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    • "To examine anillin function in vivo, we focused on meiotic cytokinesis in Drosophila spermatocytes and on later stages during differentiation of mature sperm. Spermatocytes provide an excellent system for studying animal cell cytokinesis because they are large, their mechanism of cytokinesis is conserved with other animal cells, and they are amenable to manipulation using powerful molecular genetic techniques (Fuller, 1993; Giansanti et al., 2001). Germ cell cytokinesis is incomplete, and developing male germ cells remain connected by stable intercellular bridges called ring canals. "
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    ABSTRACT: The scaffolding protein anillin is required for completion of cytokinesis. Anillin binds filamentous (F) actin, nonmuscle myosin II, and septins and in cell culture models has been shown to restrict actomyosin contractility to the cleavage furrow. Whether anillin also serves this function during the incomplete cytokinesis that occurs in developing germ cells has remained unclear. Here, we show that anillin is required for cytokinesis in dividing Drosophila melanogaster spermatocytes and that anillin, septins, and myosin II stably associate with the cleavage furrow in wild-type cells. Anillin is necessary for recruitment of septins to the cleavage furrow and for maintenance of F-actin and myosin II at the equator in late stages of cytokinesis. Remarkably, expression of DE-cadherin suppresses the cytokinesis defect of anillin-depleted spermatocytes. DE-cadherin recruits beta-catenin (armadillo) and alpha-catenin to the cleavage furrow and stabilizes F-actin at the equator. Similarly, E-cadherin expression suppresses the cytokinesis defect caused by anillin knockdown in mouse L-fibroblast cells. Our results show that the anillin-septin and cadherin-catenin complexes can serve as alternative cassettes to promote tight physical coupling of F-actin and myosin II to the cleavage furrow and successful completion of cytokinesis.
    Molecular biology of the cell 03/2010; 21(9):1482-93. DOI:10.1091/mbc.E09-08-0714 · 4.47 Impact Factor
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