The caspase-dependent apoptosis gradient in the testis of the blue shark, Prionace glauca

Abstract

The severe degenerative phenomena that characterises spermatogenesis in mating blue sharks involves spatially separated germ cell and Sertoli cell apoptosis. Unlike that observed in multilayered type B spermatogonial and spermatocyte cysts caspase-3-dependent apoptosis of single and multinucleate type B spermatogonia in one to three spermatogonial layered cysts resulted in their complete fragmentation, delayed phagocytic removal and displacement of the apoptotic bodies towards the perilumenar Sertoli nuclei. Changes were observed in the immunostaining patterns of proliferating cell nuclear antigen (PCNA), including subtle changes in cytoplasmic and overall intense immunostaining, labelled single and multinucleate cell (MNC) apoptotic spermatogonial masses in premeiotic cysts in different stages of the protracted death process. Initial massive MNC formation at the mitosis-meiosis transition eventually left its imprint in the spermatogenic sequence in the form of vacuolated areas in the affected and subsequent stages. Some of the latter attempted further developmental advance but eventually degenerated. The observed higher PCNA index of spermatogonia in vacuolated testes compared to testes with the MNC type of degeneration indicated that the former testicular morphology represented, in essence, the recovery phase from the pronounced MNC death earlier. Events culminating in the eventual apoptotic demise of the Sertoli cells themselves included the abortion of further development (presumably due to a suboptimal Sertoli:germ cell ratio) of those germ cells left over from the wave of MNC death that swept the cysts. Eventually the Sertoli-cell-only cysts became apoptotic as they were engulfed by the infiltrating lymphomyeloid cells from the epigonal organ associated with the mature pole of the testis.

Apoptotic and nonapoptotic function of caspase 7 in spermatogenesis

“…Although several caspases have been found to be involved in the apoptosis of germ cells,1617 the relationship between caspase 7 and germ cells apoptosis has never been reported. Then, we constructed the models of spermatogenic dysfunction by busulfan.…”

“…Recent studies report that caspase signal pathways are relative to the apoptosis of germ cells 1617. However, whether the function of caspase 7 is involved in spermatogenesis remains unknown.…”

Multiple Sources for Sertoli Cells and Two Sertoli Phenotypes in the Adult Elasmobranch Testis: Insight from Two Species Belonging to Different Orders

“…An earlier analysis of the life–death balance in germ cell cohorts during spermatogenesis found that the large mature, rather than the small immature spermatogonial cysts of summer breeding P. glauca displayed a protracted two‐stage form of caspase 3‐dependent cell death, all of which allowed the distinction between two types of testicular conditions in these wild‐caught specimens (McClusky, ). The latter study distinguished histologically between testes that showed extensive multinucleate cell death (MNC) in preferentially mature spermatogonial cysts, and those with vacuolated areas in the spermatogonial layers of the same cyst stages.…”

“…Quantitative analyses of the apoptosis gradient in the expansive premeiotic (PrM) regions of Squalus (McClusky, ) and P. glauca (McClusky, , ) noted the low incidence of multinucleate cell (MNC) corpses among immature PrM cysts and their preponderance among mature PrM cysts. In both elasmobranchs, some developing PrM cysts that display a scattering of MNC death corpses may yet recover from the earlier graded onset of cell death since such cysts simultaneously display mitotic and apoptotic activity in different parts of the cysts as well as between neighboring spermatogonia (McClusky, , ).…”

“…Quantitative analyses of the apoptosis gradient in the expansive premeiotic (PrM) regions of Squalus (McClusky, ) and P. glauca (McClusky, , ) noted the low incidence of multinucleate cell (MNC) corpses among immature PrM cysts and their preponderance among mature PrM cysts. In both elasmobranchs, some developing PrM cysts that display a scattering of MNC death corpses may yet recover from the earlier graded onset of cell death since such cysts simultaneously display mitotic and apoptotic activity in different parts of the cysts as well as between neighboring spermatogonia (McClusky, , ). It is plausible that the statistically and highly significant quantitative correlation revealed here between the proportion of newly assembled cysts with the small dark Sertoli cells and the degenerate testicular condition may well relate to a putative role of small atypical Sertoli cells in limiting the spread of MNC death to a confined area in cysts engaged in the nonpatterned ➔ patterned transition simultaneously as they promote compensatory spermatogonial mitosis (Fig.…”