Molecular mechanisms of the initiation of oocyte maturation: general and species-specific aspects

Abstract

Stimulated by maturation-inducing hormone secreted from follicle cells surrounding the oocytes, fully-grown oocytes mature and become fertilisable. During maturation, immature oocytes resume meiosis arrested at the first prophase and proceed to the first or second metaphase at which they are naturally inseminated. Paying special attention to general and species-specific aspects, we summarise the mechanisms regulating the initial phase of oocyte maturation, from the reception of hormonal signals on the oocyte surface to activation of the maturationpromoting factor in the cytoplasm, in amphibians, fishes, mammals and marine invertebrates. INTRODUCfION TO OOCYTE MATURATIONThe life of multicellular organisms begins at fertilisation, the union of germ cells (the egg and the spermatozoon). The production and maturation of germ cells and their fusion are indispensable for the maintenance of a species beyond the limited longevity of individuals. Oocytes are produced in ovaries by the entry of mitotically proliferating oogonia into meiosis. Oocytes stop their meiotic cell cycle at the first prophase, during which they grow by the accumulation of substances necessary for early embryonic development (vitellogenesis). In many species, fullygrown postvitellogenic oocytes arrested at the first meiotic prophase are immature, and they are unable to be fertilised until they mature. The oocytes that have been induced to mature resume meiosis from the first prophase and proceed to the first or second metaphase, at which time, in many invertebrates and vertebrates, they are inseminated (1). During the course of maturation, oocytes undergo drastic morphological changes associated with progression of the meiotic cell cycle, among which breakdown of the oocyte nuclear envelope (germinal vesicle breakdown, GVBD) occurring at the prophase/metaphase transition is frequently regarded as a hallmark of the progress of maturation, although it does not necessarily mean the completion of maturation (Figure 1).Oocyte maturation is induced by sequential actions of three substances (2): gonadotropic hormone (GTH; or gonad-stimulating substance in starfish, GSS), maturation-inducing hormone (MIH; or maturationinducing substance, MIS) and maturation-promoting factor (MPF) (Figure 2). Two species of GTH, a luteinizing hormone (LH) and a follicle-stimulating hormone (FSH), are secreted from the pituitary gland in vertebrates. Both LH and FSH consist of two glycoproteinous subunits, a and ~ subunits; the former is also a component of the thyroid-stimulating hormone (ISH) and the latter characterises each hormone. FSH is responsible for oocyte growth, and LH triggers oocyte maturation by stimulating follicle cells surrounding the 115 oocytes to produce MIH. MIH in vertebrates is a steroid derivative and interacts with a membrane-bound receptor on the oocyte surface, and subsequent signal transduction from the surface to the cytoplasm is probably intermediated by GfP-binding proteins (Gproteins). The MIH signal finally results in the formation and activa...

Graft site and gonadotrophin stimulation influences the number and quality of oocytes from murine ovarian tissue grafts

“…The ovary is innervated by extrinsic and intrinsic nerves that are believed to control blood flow, as well as follicle and oocyte development (Dissen et al 1995, D'Albora et al 2000, Anesetti et al 2001, Aguado 2002. Normal follicle development and the production of viable oocytes is a complicated process that involves coordination of numerous molecules including hormones, growth factors and receptors, in various signalling pathways that act in autocrine, paracrine and endocrine manners (Yamashita et al 2000, Josefsberg & Dekel 2002, Matzuk & Lamb 2002, Drummond et al 2003. Although grafted ovaries do become re-vascularized and re-innervated, the grafting process may perturb the systems that are essential for normal follicle growth and oocyte development and thus result in a reduced number of developmentally competent oocytes.…”

Identification of some unknown transcripts from SSH cDNA library of buffalo follicular oocytes

“…Maturation of mammalian oocytes presents a protracted developmental process whereby an undifferentiated female germ cell prepares itself for undertaking the process of fertilization and guides the newly formed zygote through early developmental stages until the embryo's own genome becomes eligible to undertake its own transcription (Yamashita et al, 2000;Zuccotti et al, 2011). Transcriptionally, the period of oocyte maturation displays a typical cycle of mRNA synthesis and degradation starting with a very high turnover rate, which goes silent toward the end (Tomek et al, 2002).…”

Molecular characterization of three forms of putative membrane-bound progestin receptors and their tissue-distribution in channel catfish, Ictalurus punctatus

“…Meiotic maturation of fish and amphibian oocytes is one of the most well-characterized nongenomic steroid actions mediated by membrane-bound steroid receptors at both the biochemical and cytological levels (Yamashita et al 2000). The precise mechanism for the activation and/or stabilization of the maturationpromoting factor by the maturation-inducing steroid (MIS) appears to differ among species.…”

“…For example, the MIS-receptor (MIS-R), which in fish is a membranebound progestin receptor (mPR), appears to be coupled to an inhibitory G-protein (Gi) in three fish species: rainbow trout, Atlantic croaker and spotted seatrout, (Yoshikuni & Nagahama 1994, Thomas et al 2002, Zhu et al 2003a, whereas in zebrafish and an amphibian, Xenopus, it is likely that progestins activate a stimulatory G-protein (Gallo et al 1995, Kalinowski et al 2004. However, many other processes initiated through activation of the membrane-bound MIS-R, such as a decrease in intracellular cAMP levels, have been shown to be conserved (Yamashita et al 2000).…”