Spatiotemporal control of Cindr at ring canals during incomplete cytokinesis in the Drosophila male germline

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.

Src64 controls a novel actin network required for proper ring canal formation in the Drosophila male germline

“…We next examined how the septin Peanut (Field et al, 1996;Adam et al, 2000;Eikenes et al, 2013) and the Arp2/3 activator SCAR (WAVE1 in mammals) (Zallen et al, 2002), both of which are involved in actin dynamics, localize in relation to RCs in 2-CCs. Interestingly, both Peanut and SCAR accumulated around RCs in wild-type cysts, but were irregular in ∼90% of Src64 KO 2-CCs ( Fig.…”

“…RCs are required for fertility in both insects and mammals, but current knowledge of the regulation of these structures is limited (Robinson et al, 1994;Haglund et al, 2011). The scaffolding molecules Anillin and Cindr, the central spindle component Pavarotti, as well as actin and myosin have been shown to localize to RCs (Field and Alberts, 1995;Hime et al, 1996;Adams et al, 1998;Haglund et al, 2010;Eikenes et al, 2013), but little is known about the molecular mechanisms regulating incomplete cytokinesis in vivo Greenbaum et al, 2011;Haglund et al, 2011;Mathieu et al, 2013;Yamamoto et al, 2013).…”

Stay Connected: A Germ Cell Strategy

“…Ring canals in the male germline do not have Hts-RC or Kelch, critical ring canal components in the female germline. Instead, male ring canals remain associated with contractile ring components such as Anillin, Septins (Peanut, Sep1, Sep2), and Pavarotti [13, 14]. …”

Phosphoinositide signaling in sperm development

“…Other Drosophila spermatocyte cytokinesis genes encode cytoskeletal regulators or membrane-cytoskeleton crosslinking proteins [67,[94][95][96][97][98][99][100][101]. Many of these factors are predicted to interact with PIP2 at the plasma membrane.…”