Paraspermatogenesis inCeratostoma foliatum (Neogastropoda): confirmation of programmed nuclear death

Abstract

Sperm dimorphism, where ejaculates contain both fertile "eusperm" and sterile "parasperm", has been implicated in sperm competition in animals. Most parasperm lack an acrosome, eliminate the nucleus and develop a complex cytoplasm, swollen with secretory vesicles. This study of parasperm in the foliate whelk Ceratostoma foliatum, focuses on characterizing the process of nuclear breakdown and the nature of cytoplasmic secretions. Testis squash preparations were treated with a Promega apoptosis detection [terminal deoxynucleotidyl transferase (TdT)-mediated dUTP nick-end labeling-TUNEL] assay (Cedar Lane) to detect nuclear apoptosis; acridine orange was used to localize lysosomes. Parasperm were isolated on Percoll gradients and their proteins characterized by running electrophoresis of lysed, purified fractions on polyacrylamide gels. Results show that the process of nuclear breakdown follows the hallmarks of apoptosis in ultrastructure, which is confirmed by the presence of 3'-OH overhangs of DNA fragments. This research implicates snail parasperm as models for elucidating the nuclear events of apoptosis.

The complexity of apoptotic cell death in mollusks: An update

“…Apoptosis has also been described in hemocytes [119,127], which is not surprising given that the hemocytes are the immune cells in bivalves and apoptosis has been described as a host defense mechanism against parasites, viral and bacterial pathogens [57,127]. Apoptosis enables the adequate clearance of damaged, senescent and infected cells without inflammation [8,120,123]. Motta et al [86] analyzed the localization and possible function of the caspase-3 gene in various molluscan tissues.…”

“…Essentially, there is no inflammatory reaction associated with the process of apoptosis or with the removal of apoptotic cells because apoptotic cells do not release their cellular constituents into the surrounding interstitial tissue, and the apoptotic bodies are rapidly engulfed by surrounding cells without the production of antiinflammatory cytokines [59,113]. All these characteristic morphological hallmarks of apoptosis have been well described in a variety of mollusks, mainly in bivalves [120,123,1,109] but also in gastropods [8,80,111] and cephalopods [55,56].…”

Colchicine-induced degeneration of the micronucleus during conjugation in Tetrahymena

“…Nuclear elimination in living cells also occurs in vertebrates during lens cell differentiation ( Wride and Sanders, 1998 ; Wride, 2000 ; Bassnett, 2009 ), parasperm nuclear loss in the sea snail, Ceratostoma foliatum ( Buckland-Nicks and Tompkins, 2005 ), and skeletal muscle atrophy ( Allen et al, 1997 ) (although recently that observation has been challenged ( Bruusgaard et al, 2012 )). Also, Gandarillas et al have observed TUNEL labeled nuclei in keratinocytes of viable cells ( Gandarillas et al, 1999 ), suggesting that nuclear elimination occurs in living cells in skin under certain conditions.…”

Riders on the sperm: sperm dimorphism and spermatozeugmata in nematodes from the genus Steinernema (Rhabditida: Steinernematidae)

“…No nucleus or nuclear material was observed in the giant cell. The non-fertilising aberrant spermatozoa which lose their nuclei, or have nuclei represented only by remnants, are well known, for example, in molluscs (giant paraspermatozoa) and insects (apyrene spermatozoa) (Friedlander, 1997;Buckland-Nicks, 1998;Kawamura et al, 2003;Buckland-Nicks & Tompkins, 2005).…”