A light- and electron-microscope study of the nucleolus during growth of the oocyte in the prepubertal mouse.

Abstract

ABSTRACT The ordered changes which occur in the structural organization of the nucleolus during growth of the mouse oocyte have been studied by both light and electron microscopy. All observations have been made on those oocytes whose growth is initiated on the day of birth and completed by postnatal day 14 in prepubertal animals of the ICR albino mouse strain. During that period the oocyte nucleolus undergoes an approximate 90-fold increase in volume. During the unilaminar follicle stage (from birth to postnatal day 4), the growing nucleolus exhibits an overall reticulated-type of structure consisting of: (1) a moderately electron-dense fibrillogranular component occupying most parts of the nucleolar framework; (2) an electron-transparent nucleoplasm-like component filling the numerous interstices of the nucleolar framework; (3) an electron-dense fibrillar component located in the peripheral portion of a number of small islands widely and uniformly scattered within the nucleolar framework, and (4) a slightly less-dense fibrillar component situated in the central portion of these same islands and referred to as fibrillar centres. Increase in nucleolar volume during that stage is brought about mainly through an increase in the overall dimensions of the fibrillogranular framework, accompanied by a parallel increase in the number and, to a certain extent, the size of its electron-transparent interstices. During the bilaminar follicle stage (postnatal day 5 through 8), the following structural and organizational changes take place more or less concomitantly within the still enlarging nucleolar mass: (1) the fibrillogranular framework becomes predominantly fibrillar in texture as a result of what appears to be an unravelling or unfolding of its constituent granules of ribosomal dimensions; (2) the nucleolar interstices decrease rapidly both in number and size because of the accumulation within their interior of a material the texture and density of which match that present in the nucleolar framework itself; and (3) a number of rounded electron-transparent spaces, the nucleolar vacuoles, make their appearance in the regions formerly occupied by some of the fibrillar islands and adjacent interstices. Increase in nucleolar volume during that stage is largely due to the appearance and subsequent enlargement of the nucleolar vacuoles in question. During the plurilaminar follicle stage (postnatal day 9 through 14), the following sequential events take place within the nucleolar mass: (1) a moderately electron-dense fibrillogranular material accumulates within the nucleolar vacuoles; (2) this fibrillogranular material, which eventually fills all vacuolar spaces, undergoes degranulation and a concomitant increase in density, eventually matching that of the rest of the nucleolar mass; (3) ail remnants of the lightly stained nucleolar interstices disappear from view; and (4) the fully grown rounded nucleolus finally appears as a dense, compact mass, exclusively fibrillar in texture, and exhibiting no internal structural organization. An attempt is made to interpret these changes in the light of current knowledge concerning the architectural and functional organization of the mammalian nucleolus in general. The observations are consistent with the view that the nucleolus, during growth of the primary oocyte, is the site of massive synthesis and storage of nucleolar material.