Enigmas of mammalian gamete form and function

Abstract

The gametes of man and some other Eutheria have been manipulated successfully for practical reasons, but many gaps remain in our basic understanding of the way that they function. This situation stems not least from a failure to recognize the extent to which eutherian spermatozoa and eggs, and elements related to their operation, have come to differ from those of other groups. Novel features in the male that reflect this include a radical design of the sperm head with the acrosome seeming to function primarily in egg-coat binding rather than its lysis, a multifaceted post-testicular sperm maturation and an androgen/low-temperature-regulated system of sperm storage--both tied to the epididymis, a variable male accessory sex gland complex, and descent of the testis and epididymis to a scrotum. In the female, such novelties are represented in a need for sperm capacitation, in an unusual regulation of sperm transport within the oviduct, in the cumulus oophorus and character of the zona pellucida around the small egg, and in a unique configuration of gamete fusion. The collective evidence now suggests that many of these features reflect a new fertilisation strategy or its consequences, with most being causally linked. One initial 'domino' in this regard appears to be the small yolkless state of the egg and its intolerance for polyspermy, as determinants of the unusual mode of oviductal sperm transport and possibly the existence and form of the cumulus oophorus. However, a particularly influential first 'domino' appears to be the physical character of the eutherian zona pellucida. This differs from the egg coats of other animal groups by virtue of a resilient elasticity and thickness. These qualities allow this primary and often only coat to stretch and so persist during later expansion of the blastocyst, usually until close to implantation. At the same time, the dimensions, physical character, and particularly the relative protease-insensitivity of the zona appear to have had profound effects on sperm form and function and, more indirectly, on sperm-related events in the male and the female tract. Marsupials display some similarities and also some strikingly different features, against which the enigmas of the eutherian situation can be evaluated.

Oviduct-specific glycoprotein and heparin modulate sperm–zona pellucida interaction during fertilization and contribute to the control of polyspermy

“…This proposal agrees with Bedford's suggestion that ''oviductal maturation of the ZP is necessary to acquire the insensitivity to proteinases and ability to select the entering spermatozoa'' (14). Our results reported here in pig and cow lend strong support to Bedford's hypothesis and to our proposal.…”

“…These observations prompted us to hypothesize whether the ZP in ungulates could be undergoing modifications during transit in the oviduct (before fertilization) that affect its resistance to pronase digestion and consequently its interaction with the sperm, and whether this may represent an additional mechanism to control polyspermy, different from the changes brought about by the cortical reaction. The rationale underlying this issue could support the view that spermatozoa penetrate the zona, at least in part, using physical thrust (14), and only those with the ability (or the force) to cross that protease-resistant (''hardened'') ZP would be successful at fertilizing the oocyte. However, it cannot be ruled out that oviductal modifications of the ZP could also involve the coating of ZP sperm-binding sites, representing a different mechanism to select the fertilizing spermatozoon.…”

Heterologous murine and bovine IVF using bottlenose dolphin (Tursiops truncatus) spermatozoa

“…However, they support the idea raised by Bedford [51,52] which suggests that interaction and fertilization success does not only depend on recognition between the gamete receptors, which conserved regions are unlikely to be abundant among phylogenetically distant species, such as the ones involved in the present study. Bedford [51,52] suggests that other factors, such as physical thrust or those able to reduce 505 specificity of the zona pellucida can facilitate the interaction.…”

“…Bedford [51,52] suggests that other factors, such as physical thrust or those able to reduce 505 specificity of the zona pellucida can facilitate the interaction. Among these, physical thrust seems the most obvious [51]. This factor is related to sperm motility [53].…”

Why do penetrating sperm create an oblique path in the zona pellucida?

“…The available evidence suggests that these characteristics of the egg coat have had a profound effect on the mechanism of its penetration. The novel design of the sperm head and its behaviour during fertilization imply that, after binding, zona penetration in eutherian mammals depends largely and perhaps only on the oscillating thrust of the sperm (Bedford 2004).…”