TheDrosophila Cog5Homologue Is Required for Cytokinesis, Cell Elongation, and Assembly of Specialized Golgi Architecture during Spermatogenesis

Abstract

The multisubunit conserved oligomeric Golgi (COG) complex has been shown previously to be involved in Golgi function in yeast and mammalian tissue culture cells. Despite this broad conservation, several subunits, including Cog5, were not essential for growth and showed only mild effects on secretion when mutated in yeast, raising questions about what functions these COG complex subunits play in the life of the cell. Here, we show that function of the gene four way stop (fws), which encodes the Drosophila Cog5 homologue, is necessary for dramatic changes in cellular and subcellular morphology during spermatogenesis. Loss-of-function mutations in fws caused failure of cleavage furrow ingression in dividing spermatocytes and failure of cell elongation in differentiating spermatids and disrupted the formation and/or stability of the Golgibased spermatid acroblast. Consistent with the lack of a growth defect in yeast lacking Cog5, animals lacking fws function were viable, although males were sterile. Fws protein localized to Golgi structures throughout spermatogenesis. We propose that Fws may directly or indirectly facilitate efficient vesicle traffic through the Golgi to support rapid and extensive increases in cell surface area during spermatocyte cytokinesis and polarized elongation of differentiating spermatids. Our study suggests that Drosophila spermatogenesis can be an effective sensitized genetic system to uncover in vivo functions for proteins involved in Golgi architecture and/or vesicle transport.

Mutations inCog7affect Golgi structure, meiotic cytokinesis and sperm development duringDrosophilaspermatogenesis

“…Spermatid elongation, which involves a 100-fold increase in cell surface area, may necessitate the addition of new membrane derived from Golgi vesicles and so may be especially sensitive to defects in Golgi structure and/or function (Fabian et al, 2010;Farkas et al, 2003;Fuller, 1993;Tates, 1971;Wei et al, 2008;Zhou et al, 2011). In addition, loss of Cog7 affected architecture of the developing flagellar axonemes and resulted in dissociation of the basal body from the nuclear envelope, suggesting defects in the docking to the nuclear envelope.…”

“…However, loss of Cog7 and the consequent Golgi defects did not substantially affect cytokinesis of neuroblasts. Other mutations in membrane traffic components such as fwd, fws, bru, gio and Arf6 disrupt spermatocyte cytokinesis causing little or no effects on cytokinesis of larval neuroblasts or S2 cells (Brill et al, 2000;Eggert et al, 2004;Farkas et al, 2003;Giansanti et al, 2004;Giansanti et al, 2006;Dyer et al, 2007;Robinett et al, 2009). The large size of spermatocytes and the rapid succession of two meiotic divisions might explain the particular requirement of male meiotic cytokinesis for vesicle trafficking pathways.…”

“…For example, Drosophila spermatocytes are quite large cells (more than 20 mm in diameter), that complete two meiotic divisions in less than two hours (Fuller, 1993;Giansanti et al, 2012). Spermatocyte cytokinesis proved to be sensitive to mutations affecting vesicle traffic components (Brill et al, 2000;Farkas et al, 2003;Dyer et al, 2007;Gatt and Glover, 2006;Giansanti et al, 2006;Giansanti et al, 2007;Polevoy et al, 2009;Robinett et al, 2009;Xu et al, 2002a;Zhou et al, 2011). During Drosophila spermiogenesis, round spermatids, ,12 mm in diameter, undergo drastic morphological changes in cell surface before reaching the impressive 1.8 mm in length of sperm tails (Fuller, 1993;Tates, 1971;Zhou et al, 2011).…”

“…During Drosophila spermiogenesis, round spermatids, ,12 mm in diameter, undergo drastic morphological changes in cell surface before reaching the impressive 1.8 mm in length of sperm tails (Fuller, 1993;Tates, 1971;Zhou et al, 2011). The 100-fold increase in cell length that characterises spermatid elongation is particularly dependent on membrane biosinthesis and membrane remodelling (Fabian et al, 2010;Farkas et al, 2003, Wei et al, 2008Zhou et al, 2011). Among the COG subunits, the Drosophila Cog5 homologue Four way stop (Fws) has been implicated in both male meiotic cytokinesis and spermatid elongation .…”

Cytokinesis in Animal Cells

“…Moreover, both RNA interference (RNAi)-based and classical genetic screens in Drosophila have implicated Golgi-related functions in cytokinesis (Farkas et al 2003;Echard et al 2004;Eggert et al 2004;Giansanti et al 2004;Belloni et al 2012;Kitazawa et al 2012). Genetic dissection of cytokinesis in Drosophila spermatocytes indicated the requirement of important regulatory proteins of Golgi trafficking.…”