Sayoko Makabe

Morphodynamics of the follicular-luteal complex during early ovarian development and reproductive life.

Female reproductive activity depends upon cyclic morphofunctional changes of the ovarian tissue during the females fertile period, but the primum movens of an active gonadal rearrangement can be found from early phases of embryo development. To offer a basic account of the main steps of ovarian dynamics, we review the morphofunctional behavior of the follicular-luteal complex in an integrated study using light microscopy and transmission and scanning electron microscopy as well as through the use of numerous drawings. Particular emphasis is given to some reproductive aspects including (1) germ-somatic cell relationships and onset of folliculogenesis during early gonadal development; (2) follicular development and oocyte-follicle cell associations through adult folliculogenesis, finally leading to ovulation; (3) morphodynamics of corpus luteum formation, development, and regression, and (4) degenerative processes involving germ and somatic cells. The results reported, many of which originated in our laboratory, arise from some experiments on laboratory mammals but mostly from a large selection of human specimens. The data obtained are integrated and correlated with classic reports as well as with current views. Crucial biochemical, histophysiological, and clinical aspects are also emphasized.

Ultrastructure of the Ovary

1. Migration of germ cells, development of the ovary, and folliculogenesis.- 2. Maturation of the human oocyte.- 3. Expansion of the cumulus-oocyte complex during the preovulatory period: Possible roles in oocyte maturation, ovulation, and fertilization.- 4. Structure and function of the zona pellucida.- 5. Quantitative analysis of the membrana granulosa in developing and ovulatory follicles.- 6. Digital image analysis studies of folliculogenesis and oogenesis in mammals.- 7. Modulation of granulosa cell ultrastructure during differentiation: The role of the cytoskeleton.- 8. Ultrastructure and functional development of the theca interna.- 9. Muscular apparatus of the ovarian follicle.- 10. Ultrastructure of the ovulatory process.- 11. Ultrastructural dynamics during corpus luteum development and growth.- 12. Relaxin and other luteal secretory peptides: Cell localization and function in the ovary.- 13. Interstitial cells.- 14. Ultrastructure and immunocytochemical aspects of steroid-synthesizing and secretory cells with special reference to the mechanism of estrogen biosynthesis.- 15. Microvasculature of the ovary.- 16. Innervation of the ovary.- 17. Follicular atresia.- 18. Biopathology of ovarian mesothelium.- 19. Culture of ovarian tissues.

Natural history of the female germ cell from its origin to full maturation through prenatal ovarian development

This paper contains a number of sketches concerning the main morphological ultrastructural features of the human female germ cell during the prenatal period. The morphodynamic outline of primordial germ cells has been traced, both in their extraembryonic site of origin and during their migration towards the developing ovary. After gonadal settlement, the intraovarian differentiation of the germ cells into primary oocytes through the stage of oogonia, as well as the dramatic fall in the number of germ cells before birth, is described. The presence of morphofunctionally relevant interactions between the differentiating female gamete and the surrounding somatic microenvironment has also been evaluated and discussed.

Elimination of germ cells during differentiation of the human ovary: an electron microscopic study

Observations by scanning and transmission electron microscopy during ovarian development (from 7 wk until term of gestation) showed numerous germ cells within the superficial epithelial layer covering the ovary. In early stages of differentiation (between 7 and 11 wk), germ cells appeared to be actively migrating to the surface of the ovary by ameboid-like movements. Later, the transfer of the germ cells to the surface epithelium was also occurring passively, as a consequence of an intense proliferation of germ and somatic cells - arranged in clusters and cords - migrating towards the most superficial areas of the ovary. The present evidence suggests that a number of primordial germ cells - as well as oogonia and oocytes - which lie in the superficial epithelium can leave the ovary and ultimately rest freely upon its surface. Elimination of germ cells during differentiation of the ovary in humans was always paralleled by necrosis of oogonia and oocytes and atretic alteration of primitive follicles. The significance of these processes is discussed in relation to the reduction of the pool of oocytes at birth.

Migration of Germ Cells, Development of the Ovary, and Folliculogenesis

The ovary is a cyclically changing organ that exerts two principal secretory functions: the endocrine and the very special “exocrine” (ovulatory) function. This activity is allowed by the structural complexity of the gland, which is formed by two components, differing in origin and function: a germinal cell line and a somatic cell line. These ovarian components intermingle and begin interacting in a finely regulated manner, starting from the initial phases of the female gonad development.

Three-dimensional microanatomical dynamics of the ovary in postreproductive aged women

OBJECTIVE To evaluate the microanatomical dynamics of the ovary during postreproductive life. DESIGN Retrospective, observational research study. SETTING Institutional (university). PATIENT(S) Eleven (43- to 72-year-old) women in perimenopause, menopause, or postmenopause. INTERVENTION(S) Biopsies of ovaries obtained from patients undergoing gynecologic surgery or diagnostic procedures. MAIN OUTCOME MEASURE(S) Analysis of the 3-dimensional microanatomy of the ovary by transmission and high-resolution scanning electron microscopy. RESULT(S) The surface epithelium gets gradually flatter and is always present, even in advanced age. The surface appears smoother because of a smaller number of papillae and crypts as well as a decreased number and shortening of microvilli on surface epithelial cells. Signs of atrophy and fibrosis are evident. Primordial follicles are usually absent in postmenopause, whereas corpora atretica, hemorrhagica, and albicantia, scar tissue, and simple follicular cysts are common after menopause. Apoptotic and necrotic cells appear frequently within the surface epithelium. Major common features are a marked reduction in number and caliber of blood vessels with thickening of the vascular walls and changes in endothelial cells. CONCLUSION(S) Scanning electron microscopy studies are a useful complement to ordinary gynecologic diagnostic methods. Variations among patients of the same age range or functional status should be considered.

The ovary and ovulation: A three-dimensional ultrastructural study

The ovary is a highly complex organ that performs a dual role: it functions as an organ of reproduction and also as a gland of internal secretion. Gametogenesis has also been termed folliculogenesis (1). The ovary’s secretory activity, including the release into the circulation of nonsteroidal hormones that act locally within the ovary, was given the name hormonogenesis by Hodgen et al. (1).

Life history of the human female germ cell: Ultrastructural aspects

The haploid germ cells are produced in the adult gonad after completion of the first meiotic division, even though the diploid germ-cell line is established during the early stages of embryogenesis, when those cells are known as primordial germ cells (PGCs) (1).

STRUCTURE AND FUNCTION OF THE HUMAN OOCYTE-CUMULUS-CORONA CELL COMPLEX BEFORE AND AFTER OVULATION

SummaryThe fine structure of the human cumulus oophorus has been reviewed on the basis of scanning and transmission electron microscopic observations as well as of immunofluorescence data. Tissues sampled from preovulatory ovarian follicles and cumulus-enclosed oocytes and fertilized eggs (collected from the oviduct or obtained during in vitro fertilization procedures) have been evaluated from a microtopographic and morphodynamic point of view in order to better clarify the possible role of this population of cells. In particular, the following aspects have been studied and discussed: the presence of multiple close contacts (modulated by the interposition of the zona pellucida) between the oocyte surface and the long microvillous evaginations projecting from the inner aspect of corona cells surface (through these structures the intraovarian cumulus oophorus may control oocyte growth and metabolism up until the time of ovulation); the occurrence of different subpopulations of cells (steroid-synthetic cells, cells producing adhesive proteins, leukocytes, macrophages) in the postovulatory, extraovarian cumulus oophorus surrounding oocytes, zygotes and early developing embryos. All these elements found in the cumulus mass may positively act, through their paracrine activities, on the chemical composition of the microenvironment in which fertilization occurs.

An Ultrastructural Study of Epithelium Differentiation in the Human Fetal Fallopian Tube

The epithelial structure of the developing human fetal Fallopian tube has been studied systematically by parallel light, transmission and scanning electron microscopy. The specimens for this study were collected from spontaneous abortions at the 14th, 18th, 20th and 22nd weeks and from cases of intrauterine fetal death at the 24th and 31st weeks (hydrocephalus). The epithelium lining the wall of the female genital ducts was pseudostratified in a columnar fashion. It consisted of differentiating ciliated and microvillous cells and some degenerating elements. Microvillous cells-by far the most abundant in the early phases of tubal development-often showed a solitary cilium. Ciliated elements, though always less numerous than microvillous cells, were more densely concentrated on the developing fimbriae and at the uterotubal junction than in the ampulla. On the mucosal surface of the same regions, rounded intercellular holes delimited many crypts, from which ciliated elements sometimes sprouted. Notable aspects of cell proliferation and ciliogenesis were commonly observed and are likely to be related to circulating estrogens. These ultrastructural data indicate that the typical pattern of the adult oviduct is already sketched in fetal life. Furthermore, a strategic gathering of cilia was noted primarily at the sites of the developing oviduct, which will serve to mediate the passage of sperm and/or ova and promote fertilization in adult life.