Abstract
Ovarian follicular granulosa cells surround and nurture oocytes, and produce sex steroid hormones. It is believed that during development the ovarian surface epithelial cells penetrate into the ovary and develop into granulosa cells when associating with oogonia to form follicles. Using bovine fetal ovaries (n = 80) we identified a novel cell type, termed GREL for Gonadal Ridge Epithelial-Like. Using 26 markers for GREL and other cells and extracellular matrix we conducted immunohistochemistry and electron microscopy and chronologically tracked all somatic cell types during development. Before 70 days of gestation the gonadal ridge/ovarian primordium is formed by proliferation of GREL cells at the surface epithelium of the mesonephros. Primordial germ cells (PGCs) migrate into the ovarian primordium. After 70 days, stroma from the underlying mesonephros begins to penetrate the primordium, partitioning the developing ovary into irregularly-shaped ovigerous cords composed of GREL cells and PGCs/oogonia. Importantly we identified that the cords are always separated from the stroma by a basal lamina. Around 130 days of gestation the stroma expands laterally below the outermost layers of GREL cells forming a sub-epithelial basal lamina and establishing an epithelial-stromal interface. It is at this stage that a mature surface epithelium develops from the GREL cells on the surface of the ovary primordium. Expansion of the stroma continues to partition the ovigerous cords into smaller groups of cells eventually forming follicles containing an oogonium/oocyte surrounded by GREL cells, which become granulosa cells, all enclosed by a basal lamina. Thus in contrast to the prevailing theory, the ovarian surface epithelial cells do not penetrate into the ovary to form the granulosa cells of follicles, instead ovarian surface epithelial cells and granulosa cells have a common precursor, the GREL cell.
Highlights
Knowing how the fetal ovary develops is important for human medical conditions such as premature ovarian failure and polycystic ovary syndrome (PCOS)
Some of the genes expressed in Gonadal Ridge Epithelial-Like (GREL) cells, such as plakophilin, desmoplakin, StAR and cytokeratin 19, have been identified before as expressed in the adult human ovarian surface epithelium [18,19,20]
Other ovarian surface epithelium markers, such as adipophilin, fibulin 2, merocin or mucin 1 [18], were not expressed in the GREL cells and, these cells did not require culture conditions that are needed for culture of ovarian surface epithelium, suggesting that these GREL cells were not ovarian surface epithelial cells, but correspond to the GREL cells
Summary
Knowing how the fetal ovary develops is important for human medical conditions such as premature ovarian failure and polycystic ovary syndrome (PCOS). It is known that the primordial germ cells (PGCs) arise from the yolk sac and migrate under the control of stem cell factor through the primitive gut into dorsal mesentery and laterally to the gonadal ridges. These ridges develop on the abdominal side of the mesonephros that operates as a functional kidney in the mammalian fetus until the metanephros assumes this role. Knowledge of the origins and lineages of somatic cells and of the events of regionalization of the ovary into the tunica albuginea, cortex and medulla are not universally agreed upon
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