Redox Regulation of Sperm Surface Thiols Modulates Adhesion to the Fallopian Tube Epithelium1

Abstract

Sperm that adhere to the fallopian tube epithelium are of superior quality and adhesion extends their fertile life. It has been postulated that periovulatory signals, as yet undefined, promote sperm release. In the in vitro studies described here, we examined the effects of several antioxidants, reportedly present within oviductal fluid, on the modulation of sperm-oviduct adhesion in bovine species. Results showed that 1) the cell-permeant thiols (penicillamine, beta mercaptoethanol, cysteine, and dithiotreitol), as well as the nonpermeant thiol, reduced glutathione, cause adhering spermatozoa to release from the epithelium; 2) thiol action is exerted on spermatozoa; and 3) oxidized glutathione, as well as the non-thiol antioxidants (dimethylthiourea, trolox, superoxide dismutase, and catalase) have no effect. Sperm surface sulfhydryls labeled with iodoacetamide fluorescein showed that spermatozoa devoid of sulfhydryls on the head surface adhered to the fallopian epithelium in vitro, whereas thiol-induced release increased the exposure of sulfhydryls on the sperm head surface. Finally, analysis of capacitation status demonstrated that uncapacitated spermatozoa adhered to the oviduct, and that thiol-induced release of spermatozoa was accompanied by capacitation. In conclusion, thiol-reducing agents in the oviductal fluid may modulate the redox status of sperm surface proteins, leading to the release of spermatozoa selected and stored through adhesion to the fallopian tube epithelium in the bovine species.

Is there a role for endocannabinoids in sperm–oviduct interaction?

“…However, in the present study, we observed that AEA has no effects on sperm-oviduct binding and sperm release, even at a concentration of 5 mM. These data are in agreement with several evidences showing that release of spermatozoa bound to the oviductal reservoir is promoted by capacitation (Lefebvre & Suarez 1996, Gualtieri et al 2005, Talevi et al 2007, Talevi & Gualtieri 2010, whereas AEA has been shown to depress this process, at least in human and boar (Rossato et al 2005, Maccarrone et al 2005. Herein, sperm-ZP binding experiments demonstrated that AEA depresses sperm capacitation also in the bovine species.…”

“…2). Bovine spermatozoa can be released in vitro from oviductal monolayers by heparin and penicillamine, which have been previously validated as powerful inducers of sperm release (Talevi & Gualtieri 2001, Talevi et al 2007. Spermatozoa released by penicillamine had the same CB1 immunolocalization observed in the initial sperm population (compare Figs 1a and 3a).…”

“…Both release inducers act on spermatozoa and trigger capacitation-related changes (Gualtieri et al 2005, Talevi et al 2007. Although both inducers trigger capacitation, we showed that only spermatozoa capacitated by penicillamine are able to revert this process (Gualtieri et al 2009).…”

“…Heparin and penicillamine are powerful inducers of the release of bovine spermatozoa adhering to in vitrocultured oviductal epithelium, and have been suggested to represent physiological signals for release of spermatozoa sequestered in the oviduct (Talevi & Gualtieri 2001, Talevi et al 2007. Both release inducers act on spermatozoa and trigger capacitation-related changes (Gualtieri et al 2005, Talevi et al 2007.…”

Penicillamine prevents ram sperm agglutination in media that support capacitation

“…PEN, and other thiols (compounds with a sulfhydryl group), have been shown to initiate sperm release through the reduction of sperm surface disulfides to sulfhydryls (Talevi et al 2007, Gualtieri et al 2009. It is probable that PEN may prevent or revert sperm association by the reduction of disulphide bonds of a sperm protein, which are required for sperm binding, to free sulfhydryls.…”