Residual body removal during spermatogenesis in C. elegans requires genes that mediate cell corpse clearance

Abstract

SUMMARYGeneration of spermatozoa involves segregation of most of the cytoplasm into residual bodies, which are detached from spermatids and eliminated in mammals. However, the molecular and cellular mechanism underlying the removal of residual bodies remains largely unknown. Here, we demonstrate that during C. elegans spermatogenesis residual bodies are engulfed and degraded by gonadal sheath cells, a process that uses the same set of genes underlying apoptotic cell removal. The two partially redundant engulfment pathways that clear cell corpses also mediate phagocytosis of residual bodies, possibly by recognizing the 'eat me' signal phosphatidylserine exposed on the surface. The residual body-containing phagosome undergoes a maturation process involving sequential steps including dynamic coating with PtdIns(3)P and association of RAB small GTPases. The genetic hierarchy of residual body removal in hermaphrodites is similar to that of cell corpse clearance, but male residual body removal involves a distinct hierarchy, with differential use of the engulfment genes. Efficient removal of residual bodies regulates the number of spermatids and effective transfer of spermatids during male matings. Our results indicate that a similar molecular mechanism is employed for the removal of residual bodies and apoptotic cell corpses in C. elegans.

Convergent evolution of sperm gigantism and the developmental origins of sperm size variability inCaenorhabditisnematodes

“…; Huang et al. ). The rapid meiotic divisions in C. elegans go hand in hand with a corresponding cell size reduction from primary spermatocyte to spermatid (Ward et al.…”

Infertility Caused by Inefficient Apoptotic Germ Cell Clearance inXkr8-Deficient Male Mice

“…We observed many large vacuoles in the Sertoli cells of Xkr8-null testes, consistent with this notion. In addition to apoptotic germ cells, residual bodies are engulfed by Sertoli cells in a PtdSer-dependent manner (63). Residual body-like structures were observed in Xkr8-null epididymides, suggesting that Xkr8 is also involved in the PtdSer exposure of residual bodies.…”

Faculty Opinions recommendation of Caenorhabditis elegans PIEZO channel coordinates multiple reproductive tissues to govern ovulation.

“…(G-J) Both PEZO-1::mScarlet (magenta) and GFP::PEZO-1 (green) localize to reproductive tissues, such as the plasma membranes of the germline cells (G-I), somatic gonad (G-J), spermatheca (I; in white box), and sperm (J; red arrows). PEZO-1::mScarlet (magenta) also labels the spermatids that have not yet migrated into the spermatheca (small circles, white box in panel [G]) and the residual bodies not yet engulfed by the sheath cells (bigger circles, white box in panel [G]) (Huang et al, 2012). (K-O) Figure 1 continued on next page observed ( Figure 2E, Figure 2-figure supplement 1E).…”