Binucleate germ cells in Caenorhabditis elegans are removed by physiological apoptosis

Abstract

Cell death plays a major role during C. elegans oogenesis, where over half of the oogenic germ cells die in a process termed physiological apoptosis. How germ cells are selected for physiological apoptosis, or instead become oocytes, is not understood. Most oocytes produce viable embryos when apoptosis is blocked, suggesting that physiological apoptosis does not function to cull defective germ cells. Instead, cells targeted for apoptosis may function as nurse cells; the germline is syncytial, and all germ cells appear to contribute cytoplasm to developing oocytes. C. elegans has been a leading model for the genetics and molecular biology of apoptosis and phagocytosis, but comparatively few studies have examined the cell biology of apoptotic cells. We used live imaging to identify and examine pre-apoptotic germ cells in the adult gonad. After initiating apoptosis, germ cells selectively export their mitochondria into the shared pool of syncytial cytoplasm; this transport appears to use the microtubule motor kinesin. The apoptotic cells then shrink as they expel most of their remaining cytoplasm, and close off from the syncytium. Shortly thereafter the apoptotic cells restructure their microtubule and actin cytoskeletons, possibly to maintain cell integrity; the microtubules form a novel, cortical array of stabilized microtubules, and actin and cofilin organize into giant cofilin-actin rods. We discovered that some apoptotic germ cells are binucleate; the binucleate germ cells can develop into binucleate oocytes in apoptosis-defective strains, and appear capable of producing triploid offspring. Our results suggest that the nuclear layer of the germline syncytium becomes folded during mitosis and growth, and that binucleate cells arise as the layer unfolds or everts; all of the binucleate cells are subsequently removed by apoptosis. These results show that physiological apoptosis targets at least two distinct populations of germ cells, and that the apoptosis machinery efficiently recognizes cells with two nuclei.

A hydraulic instability drives the cell death decision in the nematode germline

“…1A) (5). Although the core apoptotic machinery was shown to drive the final steps of cell death, the mechanisms that select and initiate apoptosis in individual germ cells are still unclear (4,8).…”

Recent Advances in the Genetic, Anatomical, and Environmental Regulation of the C. elegans Germ Line Progenitor Zone

“…The limit on diffusion they allow from the proximal side correlates spatially with the distal extent of a GLD-1::GFP marker of differentiation, and observations and modeling propose a role in limiting the extent of Notch signaling, suggesting that diffusion barriers could help restrict cell fates within the PZ [ 9 ]. Such barriers could also act as a brake on proliferation: proliferation in excess of exit from the PZ leads to germ line folding [ 102 ], which may prevent the diffusion of pro-proliferative cues, allowing proximal PZ cells to enter meiosis. The relationship between rachis folds/diffusion barriers and Sh1-germ cell interactions have yet to be explored.…”

Niche maintenance of germline stem cells inC. elegansmales

“…Perhaps the additional DTC in males and the sex-specific characteristics of male germ cells and their regulators contribute to the slight expansion in males. Alternatively, the pattern may appear shorter in hermaphrodites due to folding in the oogenic hermaphrodite germline (RAIDERS et al 2018;SEIDEL et al 2018).…”

“…Male germ cells cycle faster ) and progress through meiotic prophase more quickly (JARAMILLO-LAMBERT et al 2007). Germ cells normally fold into the center of the arm in adult hermaphrodites, but not in males (RAIDERS et al 2018;SEIDEL et al 2018).…”