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Several routes of cell death to secondary necrosis in the elasmobranch testis

Journal

APOPTOSIS
Volume 27, Issue 7-8, Pages 454-464

Publisher

SPRINGER
DOI: 10.1007/s10495-022-01733-0

Keywords

Spermatogonial apoptosis; Secondary necrosis; PCNA; Phagocytosis; Sertoli cells

Funding

  1. UiT The Arctic University of Norway (incl University Hospital of North Norway)

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The process of spermatogenesis involves apoptosis and germ cell loss. Research on the testes of migrating elasmobranchs has provided insights into the apoptotic process.
The process of spermatogenesis features significant germ cell loss through apoptosis. Routine histology of the testes of well-studied animal models hardly discloses any trace of their phagocytic clearance by the supporting Sertoli cells. This review highlights lessons learnt from the cystic, diametric testes of some seasonally migrating elasmobranchs (e.g., spiny dogfish and blue sharks) that offer unconventional investigative paradigms to study these phenomena as these organs readily disclose a pronounced apoptosis gradient affecting exclusively spermatogonial clones that each are enclosed with their own Sertoli cells in spherical structures called spermatocysts. This gradient is visible at a certain time of year in the spermatogenically active shark, and peaks in mature spermatogonial cysts as clustered deaths with sporadic, and not massive secondary necrosis. Conversely, immature spermatogonial cysts in blue sharks reveal a characteristic periluminal display of single apoptotic deaths. Tracing aberrations in the immunostaining patterns of the conserved cell cycle marker, proliferating cell nuclear antigen, the gradual progression of the death process in individual or coalesced spermatogonia in contiguous cysts becomes clear. The multiple apoptotic nuclear fragmentation morphologies inform also of a protracted death process involving three different morphological routes of nuclear fragmentation (of which some are TUNEL-positive and other TUNEL-negative) and concomitant chromatin compaction that culminate in freed apoptotic bodies (i.e., secondary necrosis). It is discussed that the staggered spermatogonial deaths and accompanying intermittent secondary necrosis in mature blue shark spermatogonial cysts may well relate to the low phagocytosis capacity of cyst's Sertoli cells that are still functionally naive.

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