Novel Expression of Gonadotropin Subunit Genes in Oocytes of the Gilthead Seabream (Sparus aurata)

Abstract

It is widely believed that FSH and LH, which are known to play key roles in controlling the production of functional oocytes in vertebrates, are synthesized and secreted exclusively by the anterior pituitary. Here we present evidence for the novel expression of FSH␤, LH␤, and the common glycoprotein-␣ (Cg␣) in the gilthead seabream ovary. Using in situ hybridization and immunocytochemistry, FSH␤ was detected in primary-growth and secondary-growth-I oocytes, LH␤ was found in secondary-growth oocytes, and Cg␣ was observed in both primary and secondary-growth oocytes. Northern blot analyses demonstrated that Fsh␤ transcript is 0.6 kb in both pituitary and ovary, whereas the ovarian Lh␤ transcript (1.1 kb), unexpectedly, is longer than the known pituitary Lh␤ transcript (0.6 kb). Sequence analyses revealed that ovarian T HE HYPOTHALAMIC-PITUITARY-GONADAL (HPG)axis is a fundamental component of the endocrine control of gametogenesis in which FSH and LH are integral endocrine messengers. In response to hypothalamic GnRH, pituitary FSH and LH are secreted into the circulation. Via the blood, they reach the gonad and bind to their respective G protein-coupled receptors, FSH receptor and LH receptor, on the ovarian follicle cells to coordinate the complex process of oocyte development. From studies of genetically derived reproductive defects in humans and mouse models, we have learned about the essential roles of FSH and LH in female reproduction (1-5). FSH acts on the granulosa cells to stimulate the activity of the aromatase system, which catalyzes the conversion of androgens into estrogens as well as to enhance the expression of LH receptor; LH plays a key role in thecal cell differentiation and promotes androgen production by these cells (6). In the late stages of follicular development, the action of LH on granulosa cells leads to the termination of their differentiation, induces oocyte meiotic maturation, and triggers follicular rupture (7,8).Oocyte development in teleosts can be divided into two major processes, follicular growth and final oocyte maturation (FOM). Follicular growth consists of two phases, the primary-growth (PG) phase and the secondary-growth (SG) phase. In the SG phase, oocytes undergo rapid growth associated with the uptake and accumulation of lipid and vitellogenin, i.e. vitellogenesis. Upon completion of the SG phase, the fully grown follicle is ready to undergo FOM, a series of developmental events preparing the oocyte for ovulation and fertilization. Pituitary gonadotropins are hormones of primary importance that trigger these two major processes. The actions of pituitary gonadotropins, however, are not direct but rather are mediated by the follicular steroids, estrogens for oocyte growth, and maturation-inducing hormone (MIH) for oocyte maturation (9).It has long been recognized that oocyte development is supported by the ovarian follicle cells, which not only mediate the FSH and LH signals from the endocrine system but also regulate the progression of oocyte development through autocrine ...

Extragonadal LH/hCG action—Not yet time to rewrite textbooks

“…LHβ, FSHβ and common-α subunit expression at mRNA and protein level has been found in gonads, suggesting a paracrine pituitary independent component of gonadotropin action (Markkula et al, 1995;Zhang et al, 1995b;Zhang et al, 1995a;Markkula et al, 1996;Wong and Zohar, 2004). However, as with the receptors, the evidence for a physiologically significant role of the extrapituitary sources of gonadotropins is missing.…”

Involvement of GnRH and Gonadotropin Genes in Oocyte Development of Blue Gourami Females (<i>Trichogaster trichopterus</i>)

“…However, the mRNA level in both the brain and the ovary was higher in FOM compared to VIT [3] [20]. Wong and Zohar (2004) [8] suggest that a GnRH-gonadotropin axis is present in the gilthead seabream ovary, and that FSH and LH, the well-characterized pituitary hormones, may play prominent Figure 1. The expression of GnRH1 (left) and GnRH3 (right) genes in oocytes at various stages of oogenesis: previtellogenesis (PV), vitellogenesis (vit) and final oocyte maturation (FOM).…”

“…It was proposed that gonadotropin-releasing hormone (GnRH) plays an autocrine/paracrine regulatory role in mammalian and fish ovaries [8]. In the current study, the ovary mRNA levels of the expression of GnRH1, GnRH3, follicle-stimulating hormone (βFSH) and luteinizing hormone (βLH) female gene in oocytes at various stages of oogenesis-previtellogenesis (PV), vitellogenesis (VIT) and final oocyte maturation (FOM)-were described in blue gourami (Trichogaster trichopterus sp.…”

“…Three GnRH genes exist in teleost fish that are comprised of three systems: 1) the midbrain (MB)-GnRH system that produces the highly conserved GnRH2, also known as the chicken II GnRH form [4]- [6]; 2) the preoptic (POA)-GnRH system that produces a species-specific GnRH form, GnRH1, which serves as a hypophysiotropic regulator; and 3) the terminal nerve ganglia (TNg)-GnRH system, which produces GnRH3 (also known as salmon GnRH) [5] [6]. It is accepted in many teleost fish orders that the three GnRH genes [3] [5] exist and transcript in the hypothalamus, FSH and LH in the pituitary gland [7], however not much information has been published on autocrine and paracrine secretion of GnRH, FSH and LH from the gonads [8] [9]. GnRH plays an autocrine/paracrine regulatory role in mammalian and fish ovaries.…”

“…There is evidence of ovarian GnRH playing an autocrine/paracrine regulatory role in controlling ovarian function in vertebrates (fish and mammals). Wong and Zohar [8] suggest that a GnRH gonadotropin axis is present in the gilthead seabream ovary and that FSH and LH, the well-characterized pituitary hormones, may play prominent novel roles in teleost intraovarian communication between oocytes and ovarian follicle cells.…”