Egg-sperm interactions in humans: ultrastructural aspects.

Abstract

A large cumulus mass usually covers the human ovulated oocyte, and voluminous clusters of cumulus cells are still seen after fertilization around the egg. Cumulus cells surround oocytes and fertilized eggs also during in vitro fertilization (IVF) procedures. This study describes, by transmission and scanning electron microscopy, the morphology and the microtopography of the cells forming the human cumulus mass surrounding IVF samples (insemined but not fertilized oocytes and fertilized eggs). Particularly emphasized is their morphodynamic role in sperm-egg interactions. A comparison with the behavior in vivo of cumulus-enclosed oocyte/fertilized eggs has been also performed. All patients have given their informed consent to participate in this protocol. An inner layer (corona radiata cells) and an outer layer (proper cumulus cells) can be microtopographically recognized in the cumulus mass. Numerous cumulus-corona cells, particularly after fertilization, showed ultrastructural characteristics typical for steroid synthetic cells, thus undergoing a sort of "luteinization" parallel to that occurring in the sister granulosa cells of the postovulatory follicle. This steroid synthetic activity, particularly enhanced in vitro but present also in vivo, may be finalized to the release of small amount of steroids (estrogens and progesterone) in the oocyte/fertilized egg milieu. Various proteins, secreted by other cell subpopulations--as revealed in other studies by our research group--, may even enrich this milieu. Lymphocytes and macrophages were often found in the cumulus mass. They may modulate the steroid secretion of the neighboring cumulus cells by production of cytokines, mimicking what occurs in the ovarian follicle and, later, in the corpus luteum. Spermatozoa, both normal (acrosome-intact or--reacted) and abnormal, were frequently seen in the cumulus mass, free in the intercellular spaces or close to the cumulus cells, that can induce sperm capacitation and acrosome reaction. Leukocytes and cumuluscorona cells appeared both capable of actively phagocytizing supernumerary and/or abnormal sperms. Such spermiophagic response is present in a lesser extent around oocytes and eggs fertilized in vivo. In vitro, instead, cumulus spermiophagy leads to the elimination of a large part of the excess spermatozoa that have reached the oocyte, thus restoring in an extracorporeal medium the spermiophagic activity physiologically exerted by leukocytes and epithelial cells in the female and male genital tracts. In conclusion, the cumulus mass surrounding oocytes and fertilized eggs appears as a highly dynamic system, in which various subpopulations of cells cooperate in order to provide a suitable and healthy microenvironment for fertilization and early embryo development.