Dynamics of Bovine Sperm Interaction with Epithelium Differ Between Oviductal Isthmus and Ampulla

Abstract

In mammals, many sperm that reach the oviduct are held in a reservoir by binding to epithelium. To leave the reservoir, sperm detach from the epithelium; however, they may bind and detach again as they ascend into the ampulla toward oocytes. In order to elucidate the nature of binding interactions along the oviduct, we compared the effects of bursts of strong fluid flow (as would be caused by oviductal contractions), heparin, and hyperactivation on detachment of bovine sperm bound in vitro to epithelium on intact folds of isthmic and ampullar mucosa. Intact folds of oviductal mucosa were used to represent the strong attachments of epithelial cells to each other and to underlying connective tissue that exist in vivo. Effects of heparin on binding were tested because heparin binds to the Binder of SPerm (BSP) proteins that attach sperm to oviductal epithelium. Sperm bound by their heads to beating cilia on both isthmic and ampullar epithelia and could not be detached by strong bursts of fluid flow. Addition of heparin immediately detached sperm from isthmic epithelium but not ampullar epithelium. Addition of 4-aminopyridine immediately stimulated hyperactivation of sperm but did not detach them from isthmic or ampullar epithelium unless added with heparin. These observations indicate that the nature of binding of sperm to ampullar epithelium differs from that of binding to isthmic epithelium; specifically, sperm bound to isthmic epithelium can be detached by heparin alone, while sperm bound to ampullar epithelium requires both heparin and hyperactivation to detach from the epithelium.

Toll‐like receptor 2 mediates the immune response of the bovine oviductal ampulla to sperm binding

“…Our results showed that both heparin-pretreated and nonpretreated sperm rapidly attached to the epithelium of the preovulatory ampulla explants, as similarly observed in explants containing only ampullary epithelium (i.e., epithelium lacking underlying connective tissue of the lamina propria; Lefebvre & Suarez, 1996) and in confluent monolayers of the ampullary epithelium (Gualtieri & Talevi, 2000). In our current and previous experiments using explants (Ardon et al, 2016;Lefebvre & Suarez, 1996), it was clear that sperm bind primarily to the beating cilia of the explants and remain bound, despite rapid beating of both the cilia and the sperm flagella.…”

TRPV4 is the temperature-sensitive ion channel of human sperm

“…During maturation in the female reproductive tract, human sperm are exposed to elevated temperature, especially before and during ovulation, which is correlated with an increase in basal body temperature by 1°C. As spermatozoa are able to survive in the female reproductive tract for several days by binding to the ciliated epithelia of the fallopian tubes, they must eventually undergo hyperactivation to detach ( Ardon et al, 2016 ). Accordingly, CatSper-deficient spermatozoa that cannot hyperactivate are not able to ascend the fallopian tubes ( Ho et al, 2009 ).…”

Steroid hormones regulate sperm–oviduct interactions in the bovine

“…However, our results support a direct action of P4 on spermatozoa or simultaneously on both sperm and oviduct epithelial cell surface to trigger sperm release. It is likely that hyperactivation plays an important role in the release of spermatozoa from the oviduct epithelium in mammals (Demott & Suarez 1992, Chang & Suarez 2012, Ardon et al 2016. Spermatozoa with hyperactivated motility were observed while they detached from bovine mucosal folds of oviduct epithelium in vitro (Ardon et al 2016) and from the epithelium in entire oviducts retrieved from mouse females just after mating (Demott & Suarez 1992, Chang & Suarez 2012.…”

“…It is likely that hyperactivation plays an important role in the release of spermatozoa from the oviduct epithelium in mammals (Demott & Suarez 1992, Chang & Suarez 2012, Ardon et al 2016. Spermatozoa with hyperactivated motility were observed while they detached from bovine mucosal folds of oviduct epithelium in vitro (Ardon et al 2016) and from the epithelium in entire oviducts retrieved from mouse females just after mating (Demott & Suarez 1992, Chang & Suarez 2012. Hyperactivated spermatozoa display asymmetrical, high-amplitude flagellar movements (Yanagimachi 1970) that are not only important for sperm release but also essential for the penetration of the cumulus oophorus and the zona pellucida surrounding the oocyte (Hung & Suarez 2010).…”