Sperm capacitation in humans is transient and correlates with chemotactic responsiveness to follicular factors.

Abstract

In humans, only a small fraction (2-12%) of a sperm population can respond by chemoattraction to follicular factors. This recent finding led to the hypothesis that chemotaxis provides a mechanism for selective recruitment of functionally mature spermatozoa (i.e., of capacitated spermatozoa, which possess the potential to undergo the acrosome reaction and fertilize the egg). This study aimed to examine this possibility. Capacitated spermatozoa were identified by their ability to undergo the acrosome reaction upon stimulation with phorbol 12-myristate 13-acetate. Under capacitating conditions, only a small portion (2-14%) of the spermatozoa were found to be capacitated. The spermatozoa were then separated according to their chemotactic activity, which resulted in a subpopulation enriched with chemotactically responsive spermatozoa and a subpopulation depleted of such spermatozoa. The level of capacitated spermatozoa in the former was -13-fold higher than that in the latter. The capacitated state was temporary (50 min < life span < 240 min), and it was synchronous with the chemotactic activity. A continuous process of replacement of capacitated/chemotactic spermatozoa within a sperm population was observed.Spermatozoa that had stopped being capacitated did not become capacitated again, which indicates that the capacitated state is acquired only once in a sperm's lifetime. A total sperm population depleted of capacitated spermatozoa stopped being chemotactic. When capacitated spermatozoa reappeared, chemotactic activity was restored. These observations suggest that spermatozoa acquire their chemotactic responsiveness as part of the capacitation process and lose this responsiveness when the capacitated state is terminated. We suggest that the role of sperm chemotaxis in sperm-egg interaction in vivo may indeed be selective recruitment of capacitated spermatozoa for fertilizing the egg.Human spermatozoa are attracted to follicular factors in vitro, and the attraction is correlated with egg fertilizability (1). The attraction results from chemotaxis and is accompanied by speed enhancement (ref. 2; for reviews, see refs. 3 and 4). Unlike the case of species with external fertilization in which most, if not all, of the sperm population is chemotactically responsive (for reviews, see refs. 5 and 6), in humans only a small fraction of the sperm population (2-12%) is chemotactically responsive at any given time (7). The identity of the responsive spermatozoa in humans changes with time by turnover: chemotactic spermatozoa lose their activity while others acquire it (7). This raised the possibility that spermatozoa are selectively chemotactic only at a certain physiological stage. The capacitated stage-i.e., the stage at which spermatozoa possess the potential to undergo the acrosome reaction (a release of proteolytic enzymes enabling sperm penetration through the egg coat) and to fertilize the egg (for recent reviews, see refs. 8-13)-seemed a reasonable possibility (3, 7). This study investigates this possibility an...

Glycodelin-S in Human Seminal Plasma Reduces Cholesterol Efflux andInhibits Capacitation ofSpermatozoa

“…After capacitation, the spermatozoa are capable of undergoing acrosome reaction upon stimulation by the zona pellucida (ZP) 1 proteins (2) and progesterone (3), thereby releasing acrosomal enzymes for penetration through the ZP. Capacitated human spermatozoa remain responsive to ZP-induced acrosome reaction in vitro for 50 -240 min only (4). Thus a tight control in the timing of capacitation is important to ensure the occurrence of appropriate sequence of events in the fertilization process.…”

Human sperm pattern of movement during chemotactic re-orientation towards a progesterone source

“…24,25 Conversely, in internal-fertilizing species, such as humans, only ,10% of cells are capable of a chemotactic response while swimming towards the source of an attractant (positive gradient), whereas there is no evidence of a visible change in the pattern of movement. [2][3][4]6,16,26 In fact, in our system, the cells that chemotactically swam from W1 (containing spermatozoa) to W2 (containing progesterone) could not be distinguished from the nonchemotactic cells according to the patterns of movement. These features of mammalian sperm chemotaxis make it technically difficult to identify an individual chemotactic cell.…”

“…1 Only those spermatozoa that are already capacitated (,10% of the cells) are chemotactic at any given time. [2][3][4] Follicular fluid, oviductal fluid and the conditioned medium of the egg-cumulus complex are biological sources of chemoattractants. [3][4][5][6][7][8][9][10][11] Follicular fluid that has been obtained from one species may attract spermatozoa of other species, suggesting that chemotaxis may not be a species-specific phenomenon.…”

Le chimiotactisme du spermatozoïde est régulé par la fixation de la progestérone sur le canal calcique CATSPER

“…Les preuves de la présence d'un chimioattractant dans le liquide folliculaire chez les mammifères seront apportées en 1990, mais l'identité de ce dernier restait inconnue [11]. Les chimioattractants sont produits par les cellules du cumulus qui entourent l'ovocyte ou par l'ovocyte lui-même [12] mais ne se limitent pas à la progestérone décrite ici. De plus, seuls les spermatozoïdes pour lesquels la capacitation a eu lieu sont sensibles aux chimioattractants [13].…”