Ultrastructure of human cumulus oophorus: a transmission electron microscopic study on oviductal oocytes and fertilized eggs.

Abstract

The aim of the present study was to assess the heterogeneity of cumulus cells that occurs in human cumuli associated with oviductal oocytes and fertilized eggs. Transmission electron microscopy was used to study the cumulus masses surrounding both unfertilized oocytes and fertilized eggs (a pronuclear and a 4-cell stage) recovered at different intervals after ovulation. The specimens were obtained by flushing the oviducts of normal cycling women who underwent surgical sterilization. The cumuli were expanded due to large and irregular intercellular spaces; small linear gap junctions were seen at cell contacts, whereas annular gap junctions were found only in the cytoplasm of some cells. Both types of junction were less abundant in fertilized specimens. Cells surrounding fertilized eggs projected numerous long, thin microvilli into the intercellular spaces. As a rule, the inner layer of the cumulus mass (corona cells) was composed of cells whose surface was relatively smooth. Cumulus cells showed oval nuclei with one or more nucleoli. The cytoplasm of most cells possessed abundant organelles typical of steroidosynthesis: (i) mitochondria with tubular or villiform cristae; (ii) a well-developed smooth endoplasmic reticulum; and (iii) electron dense lipid droplets often surrounded by a few concentric membranes of smooth endoplasmic reticulum and/or in close contact with microtubules and microfilaments. Microperoxisome-like structures were also present. After fertilization, an enhancement of the steroidosynthetic characteristics occurred in the outer layers of the cumulus mass, but not in the corona cells, which still appeared capable of protidosynthesis. Together, these morphological features support the hypothesis that the cumulus of oviductal oocytes and particularly of fertilized eggs, luteinizes like parietal granulosa cells, generating a steroid hormonal micro-environment in the oviduct which may affect fertilization and zygote segmentation. Cumulus cells showing spermiophagic activity, as well as activated macrophages, leukocytes and red blood cells, were also found in the cumulus mass. The macrophages may play a local role both by phagocytic activity and by modulating the steroid secretion of the neighbouring cumulus cells which occurs in the ovarian follicle and corpus luteum. In conclusion, the cumulus mass surrounding tubal oocytes and fertilized eggs appears to be a heterogeneous and dynamic system, in which the micro-environment for fertilization and early embryo development is provided by diverse cell populations in addition to the oviductal cells.