Roles of the reproductive tract in modifications of the sperm membrane surface

Abstract

Successful fertilization requires viable and functional spermatozoa to recognize and fuse with the oocyte. In most mammalian species, mature spermatozoa are not capable of fertilizing the oocytes immediately after ejaculation. However, unlike somatic cells, spermatozoa, after leaving the testis, are transcriptionally and translationally silent; therefore, upon completion of spermiogenesis, spermatozoa carry only a minimal amount of essential proteins on their membranes as well as within their restricted volume of cytoplasm. To develop into a fully functional and competent sperm that is capable of successful fertilization, modifications of the sperm membrane surface during its transit in the reproductive tracts is critical. These post-spermatogenesis modifications advance the maturation of epididymal spermatozoa. In addition, components secreted into the lumen of the reproductive tracts that are later added onto the sperm membrane surface also regulate (inhibit or activate) the functions of the spermatozoa. This acquisition of additional proteins from the reproductive tracts may compensate for the inactivity of morphologically mature spermatozoa. In this review, we discuss the contributions of the male and female genital tracts to modifications of the sperm membrane surface at different stages of fertilization.

Fig. 1.

Hypothetical model regarding membrane-shedding process from the COCs. Membrane shedding (either via exosomes or by trogocytosis) from the COCs serves as a material exchange mechanism between the COCs and the spermatozoa and is a continuous but CD9-independent process. (1) The shed materials can be either CD9-positive membrane vesicles (in red, likely can only be derived from the oolemma) or CD9-negative membrane vesicles (in blue, can be derived from parts of the COCs other than the oolemma). (2) When the spermatozoa come in contact with these membrane vesicles, the sperm membrane surface may undergo further remodeling that will favor the subsequent acrosome reaction or interactions of the sperm with the cumulus cells and the intercellular matrix. (3) Processes from step 2 serve to create a path for the binding of other spermatozoa with and for their recognition of the ZP, which this might be independent of whether the sperm cell captures shed materials from the COCs in step 2. (4) Fusion between the sperm cell and the oolemma is regulated by the presence of oolemma-derived CD9. Only when the sperm cell captures CD9-positive vesicles/membrane fragments shed from the oolemma into the perivitelline (PVS) space, can it further undergo fusion with the oocyte, and this 2^nd capture of materials in the PVS might be independent of whether (4a) or not (4b) the sperm cell captured CD9-negative material before its entry into the PVS.