Sperm chemotaxis

Miller, R.L., Demonstration of sperm chemotaxis in Echinodermata Asteroidea, Holothuroidea, Ophiuroidea, J. Exp. Zool., 234, 283, 1985. 

Spehr M, Gisselmann G, Poplawski A, Riffell JA, Wetzel CH, Zimmer RK, Halt H. Identification of a testicular odorant receptor mediating human sperm chemotaxis. Science 2003 299 2054-2058. 

Sperm chemotaxis is a widespread phenomenon. It was discovered in marine species in the mid-1960s, and in the last decade it was also demonstrated in amphibians and mammals. In some of these species— marine species [35, 102], frogs [5], mice [56, 114], rabbits [52], and humans [49, 128]—the evidence for sperm chemotaxis is conclusive. In others, the evidence (if it exists) is still indirect and open to doubt (for a review, see [48]). 

Sperm chemotaxis is an example of a phenomenon in which the very same process serves different purposes in different species. In marine species, most if not all of the cells within a sperm population appear to be chemotactically responsive. The role of chemotaxis there is apparently to recruit as many sperm cells (spermatozoa) as possible to the egg. In humans, rabbits, and, perhaps, in mammals in general, the role of chemotaxis seemingly also involves sperm selection only a fraction of the sperm population, consisting of ripe spermatozoa that have the capacity to fertilize the egg, is chemotactically responsive and apparently recruited to the egg [28, 29, 52]. 

One of the characteristics of sperm chemotaxis is sperm accumulation at the optimal chemoattractant concentration. However, sperm accumulation can also be caused by speed enhancement (chemokinesis) and trapping. The latter may result from a negative effect of a stimulus on motility, from a gradient-independent change in swimming behavior at a... 

The accumulation-based assays for sperm chemotaxis can be divided into three main categories. 

In this assay, the spermatozoa in the well are suspended in a solution containing the chemoattractant. The capillary, containing either a control buffer or the chemoattractant, is immersed in the sperm suspension. When the capillary contains buffer only, the spermatozoa sense a descending gradient of the chemoattractant as they move from the well to the capillary (Figure 7). When the chemoattractant is in both the capillary and the well, they sense no gradient at all. A comparison is made between these two conditions. This assay thus measures the sperm tendency to leave the chemoattractant rather than to accumulate in it. In the case of sperm chemotaxis, sperm accumulation in the capillary is... 

Table 1. Comparison between assays for mammalian sperm chemotaxis.

Generally speaking, there is no single rule with respect to sperm chemotaxis. In some species (for example, in hydroids such as Campan-ularia or tunicate such as Ciona), the swimming direction of the spermatozoa changes abruptly towards the chemoattractant source (Figure 12A). In others (e.g., in hydromedusa, fern, or fish such as Japanese bitterlings), the approach to the chemoattractant source is... 

The occurrence of sperm chemotaxis in mammals was established in vitro only at the last decade. As a matter of fact, until then there had been resistance to the concept of mammalian sperm chemotaxis for two main reasons. First, in mammals in which fertilization is internal and very large numbers of spermatozoa are ejaculated directly into the female reproductive tract (4 0X10 in humans [185] 10 -10 in mammals in general [66]), chemotaxis was believed to be unnecessary because a sufficient number of spermatozoa would reach the egg coincidentally. Second, technical difficulties in studying mammalian sperm chemotaxis prevented the acquisition of conclusive evidence. The primary technical difficulty was a very low signal-to-noise ratio in the measurements, resulting from the fact that only a small fraction of the sperm... 

Sperm ehemotaxis ean occur only after the release of an egg ready to be fertilized (ovulation). However, all published studies were carried out with foUieular fluids containing substances secreted within the follicle prior to ovulation. For this reason it was relieving when Sun et al. [ 162] demonstrated human sperm chemotaxis to conditioned media of human cumulus-oocyte cells, i.e., media pre-incubated with mature eggs, their surrounding cumulus cells, or both. These media, therefore, contain secretions of cumulus cells and mature, ready-to-be-fertilized eggs. 

Table 3. Mammalian sperm chemotaxis to follicular fluid.

An intriguing observation was made a few years ago by Oliveira et al. [114] with mouse spermatozoa. They found that not only mouse follicular fluid, but also mouse oviductal fluid attracts spermatozoa by chemotaxis. This finding raised the possibility that sperm chemotaxis within the female genital tract occurs in steps [114]. This possibility of sequential chemotaxis awaits further evidence. 

ANP is a polypeptide hormone that is secreted in large quantities by the atrial portion of the heart and from a variety of other mammalian cell types. It exerts many of its actions via activation of particulate guanylate cyclase [16, 134]. ANP is present in human follicular fluids [163] and specific ANP receptors have been identified in human spermatozoa [144]. Sperm chemotaxis to ANP was demonstrated by sperm accumulation in capillaries with ascending [6] and descending [192] gradients and by choice assays [192] (Table 4). It is not yet known whether ANP is involved in sperm chemotaxis in vivo and whether the physiological chemoattractant for human spermatozoa is an ANP-like substance. Since chemotaxis to ANP at physiological concentrations can be observed only in the presence of a neutral endopeptidase inhibitor such... 

In conclusion, follicular fluid, bourgeonal, ANP, and RANTES are the only substances that have been demonstrated to act as chemoattractants for spermatozoa by assays that differentiate between chemotaxis and other processes causing accumulation (Table 1). ANP may not be a direct physiological chemoattractant but rather a guanylate cyclase activator. The significance of sperm chemotaxis to bourgeonal and RANTES is an open question. The identity of the chemoattractant(s) in follicular fluid has yet to be revealed. 

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