Ovarian innervation develops before initiation of folliculogenesis in the rat

Abstract

Sympathetic neurotransmitters have been shown to be present in the ovary of the rat during early postnatal development and to affect steroidogenesis before the ovary becomes responsive to gonadotropins, and before the first primordial follicles are formed. This study was undertaken to determine if development of the ovarian innervation is an event that antedates the initiation of folliculogenesis in the rat, Rattus norvegicus. Serial sections of postnatal ovaries revealed a negligible frequency of follicles 24 h after birth (about 1 primordial follicle per ovary). Twelve hours later there were about 500 follicles per ovary, a number that more than doubled to about 1300 during the subsequent 12 h, indicating that an explosive period of follicular differentiation occurs between the end of postnatal days 1 and 2. Electron microscopy demonstrated that before birth the ovaries are already innervated by fibers containing clear and dense-core vesicles. Immunohistochemistry performed on either fetal (day 19) or newborn (less than 15h after birth) ovaries showed the presence of catecholaminergic nerves, identified by their content of immunoreactive tyrosine hydroxylase (TH), the rate-limiting enzyme in catecholamine biosynthesis. While some of these fibers innervate blood vessels, others are associated with primordial ovarian cells, thereby suggesting their participation in non-vascular functions. Since prefollicular ovaries are insensitive to gonadotropins, the results suggest that the developing ovary becomes subjected to direct neurogenic influences before it acquires responsiveness to gonadotropins.

Developmental changes of the oestrogen receptor-alpha and -beta mRNAs in the female reproductive organ of the rat--an analysis by in situ hybridization

“…In the rat, although the ovary becomes discernible by foetal days 14-15, it is not until around postnatal day 3 that folliculogenesis commences (Malamed et al 1992). The co-expression of both ER subtypes with comparatively intense signals in the foetal ovary suggests their role in the initial stage of ovarian development.…”

The roles of glial cell line-derived neurotrophic factor, brain-derived neurotrophic factor and nerve growth factor during the final stage of folliculogenesis: a focus on oocyte maturation

“…Over the last several decades, neurotrophic factors, originally identified as affecting cells of the CNS, have also been recognized to play important roles in peripheral tissues, including the highly innervated ovary. Ovarian nerve fibres not only connect with blood vessels but also associate with follicles (Malamed et al 1992), and it has been shown that ectopic transplantation of the ovary results in rapid in-growth of nerve fibres (Lara et al 1991). Local ovarian production of neuronal growthpromoting factors, coupled with the initial insensitivity of developing embryonic ovaries to gonadotrophins, suggested that early events during folliculogenesis could, at least in part, be under neurotrophic control (Lara et al 1991, Malamed et al 1992.…”

“…Ovarian nerve fibres not only connect with blood vessels but also associate with follicles (Malamed et al 1992), and it has been shown that ectopic transplantation of the ovary results in rapid in-growth of nerve fibres (Lara et al 1991). Local ovarian production of neuronal growthpromoting factors, coupled with the initial insensitivity of developing embryonic ovaries to gonadotrophins, suggested that early events during folliculogenesis could, at least in part, be under neurotrophic control (Lara et al 1991, Malamed et al 1992. This notion was supported by the finding that neurotrophins and their receptors are expressed in the ovary before the acquisition of gonadotrophin responsiveness (Dissen et al 1995(Dissen et al , 2009.…”

Ganglionic Adrenergic Action Modulates Ovarian Steroids and Nitric Oxide in Prepubertal Rat

“…The main neural information reaches the ovaries by the hilium via the superior ovarian nerve and ovarian plexus [1,2]. Hirshfield [3] confirmed that the first follicles to start growing are those assembled near the ovarian hilium, the first region in the ovaries of the rat to be innervated during its fetoneonatal life [4]. The sympathetic innervation terminals are closely related to the steroidogenic ovarian cells [5], and peptidergic and catecholaminergic neurotransmitters, mainly norepinephrine [6][7][8], are released from the superior ovarian nerve (SON) to the ovary.…”