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Control of Growth and Development of Preantral Follicle: Insights from in Vitro Culture

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Control of Growth and Development of Preantral Follicle: Insights from in Vitro Culture DOI: 10.21451/1984-3143-AR2018-0019 Proceedings of the 10th International Ruminant Reproduction Symposium (IRRS 2018); Foz do Iguaçu, PR, Brazil, September 16th to 20th, 2018. Control of growth and development of preantral follicle: insights from in vitro culture José Ricardo de Figueiredo1,*, Laritza Ferreira de Lima1, José Roberto Viana Silva2, Regiane Rodrigues Santos3 1Laboratory of Manipulation of Oocytes and Preantral Follicles, Faculty of Veterinary, State University of Ceara, Fortaleza CE, Brazil. 2Biotecnology Nucleus of Sobral (NUBIS), Federal University of Ceara, Sobral, CE, Brazil. 3Schothorst Feed Research, Lelystad, The Netherlands. Abstract interaction among endocrine, paracrine and autocrine factors, which in turn affects the steroidogenesis, The regulation of folliculogenesis involves a angiogenesis, basement membrane turnover, oocyte complex interaction among endocrine, paracrine and growth and maturation as well as follicular atresia autocrine factors. The mechanisms involved in the (reviewed by Atwood and Meethala, 2016). It is well initiation of the growth of the primordial follicle, i.e., known that mammalian ovaries contain from thousands follicular activation and the further growth of primary to millions of follicles, whereby about 90% of them are follicles up to the pre-ovulatory stage, are not well represented by preantral follicles (PFs). The understood at this time. The present review focuses on mechanisms involved in the initiation of growth of the the regulation and development of early stage primordial follicles, i.e., follicular activation and the (primordial, primary, and secondary) folliculogenesis further growth of primary follicles up to the pre- highlighting the mechanisms of primordial follicle ovulatory stage, are not well understood at this time. It activation, growth of primary and secondary follicles is important to emphasize that despite the large number and finally transition from secondary to tertiary of follicles in the ovary, the vast majority follicles. We also discuss the importance of in vitro (approximately 99.9%) of them become atretic during follicle culture for the understanding of folliculogenesis their growth and development stages (reviewed by during the preantral phase. Studies suggest that Figueiredo et al., 2011). follicular development from primordial to early antral The in vitro follicle culture (IVFC) technology stages is primarily controlled by intra-ovarian ligands represents a valuable tool to preserve the fertility in but it can also be influenced by many extra-ovarian individuals subjected to cancer treatment as well as sub- factors. The control of early folliculogenesis is, or infertility treatment, to create gamete banks from therefore, extremely complex because several ligands endangered species and breeds, to complement other act through distinct signaling pathways that form reproductive technologies (e.g., in vitro embryo sophisticated information networks responding to production), and to be used as models for studies in multiple, often opposing, stimuli. The balance among reproductive toxicology (reviewed by Figueiredo et al., different stimuli determines follicular survival or death 2011). Furthermore, IVFC provides insights on the as well as quiescence or activation (growth). The control of growth and development of preantral and distribution of the ligands and their corresponding antral follicles (Cadenas et al., 2017). The present receptors varies among follicular compartments and review focuses on the regulation and development of species, and significant changes in gene expression early stage (primordial, primary, and secondary) of pattern among follicular categories have been reported. folliculogenesis highlighting the mechanisms of Knowing that follicular requirements during early primordial follicle activation, growth of primary and folliculogenesis can be stage-specific and species- secondary follicles and, finally, transition from specific, in vitro culture studies offer an alternative to secondary to tertiary follicles. We also discuss the evaluate single and combined factors during a specific importance of IVFC for the understanding of period of follicular development. Herewith we folliculogenesis during the preantral phase. summarize the main findings obtained in vitro together with the mechanisms regulating folliculogenesis. Basic aspects of follicle structure and populations Keywords: folliculogenesis, in vitro development, The ovarian follicle is the functional unit of the ovary, preantral follicle. ovary composed of an oocyte surrounded by companion somatic cells (granulosa and theca cells). To facilitate Introduction the understanding of this review the following follicular classification was adopted: quiescent or dormant Folliculogenesis is the physiological process of follicles represented by the primordial follicles (one formation, activation, growth and maturation of ovarian layer of flattened granulosa cells around the oocyte) and follicles. It describes the progression of some small growing follicles (intermediate: one layer of flattened primordial follicles into large preovulatory follicles. The and cuboidal granulosa cells; primary: one layer of regulation of folliculogenesis involves a complex cuboidal granulosa cells, and secondary: two or more _________________________________________ *Corresponding author: [email protected] Received: February 1, 2018 Copyright © The Author(s). Published by CBRA. Accepted: June 1, 2018 This is an Open Access article under the Creative Commons Attribution License (CC BY 4.0 license) Figueiredo et al. Regulation of preantral follicle development. layers of cuboidal granulosa cells around the oocyte; development of PFs is primarily controlled by Silva et al., 2004). However, some authors named intraovarian (autocrine/paracrine regulation) ligands dormant follicles the ones containing either one layer of (e.g., growth factors, cytokines, and gonadal steroids) flattened granulosa cells or with flattened and/or even though it can be influenced by many extraovarian cuboidal (Jimenez et al., 2016). All preantral follicle ligands (endocrine regulation) from different tissues categories contain an immature oocyte at the germinal including the endocrine glands (reviewed by Atwood vesicle stage. and Meethala, 2016; Fig. 1-2). The control of folliculogenesis is, therefore, extremely complex Regulation of folliculogenesis during the preantral because the aforementioned ligands act through distinct follicle phase signaling pathways. These cell-signaling pathways do not act in isolation, but interact in various ways forming Folliculogenesis is a highly regulated sophisticated information networks that respond to developmental sequence resulting in the growth and multiple, often opposing, stimuli. This connection may differentiation of the oocyte and associated somatic involve components that are common between cells. Capacity of the oocyte to resume meiosis, pathways, as well as positive and negative feedback complete maturation (oocyte maturational competence), loops (Hunter, 2000). The main pathways currently undergo successful fertilization, support normal embryo studied are adenylate cyclase, MAPK / Erk, PI3K / Akt, and fetal development and produce healthy offspring phospholipase C, JAKS / STATS, SMADS and nuclear (oocyte developmental competence) is gradually receptors. The ligands that regulate folliculogenesis act acquired as the oocyte develops as the follicles pass by binding to different types of receptors that activate through the primordial to the preovulatory stages one or more of these pathways leading to responses (reviewed by Figueiredo et al., 2011). The production of related to activation, survival, proliferation and a good quality oocyte (developmental competence) follicular maturation (reviewed by Atwood and depends on a fine crosstalk between the oocyte and its Meethala, 2016). The following sections describe the surrounding follicular cells that begins during the proposed mechanisms involved in the regulation of preantral follicle phase of folliculogenesis. The follicle growth from primordial to antral stage. Figure 1. Control of the development of preantral follicle. Follicular development from primordial to early antral stages is primarily controlled by intra-ovarian ligands, but it can also be influenced by many extra-ovarian factors. This process is complex and involves autocrine (blue arrows), paracrine (green arrows) and endocrine (pink arrows) regulations. Anim. Reprod., v.15, (Suppl.1), p.648-659. 2018 649 Figueiredo et al. Regulation of preantral follicle development. Figure 2- Distribution of some key growth factors and hormones within primordial and developing follicular compartments (oocyte, granulosa and theca cells) in ruminants. Ligands (bold black letter) and receptors (bold white letter). KL – Kit ligand; E2 - 17b-estradiol; FGFb – basic fibroblast growth factor; VEGF – vascular endothelial growth factor; GDF-9 – Growth differentiation factor-9; LIF – leukemia inhibitory factor; GH – growth hormone; EGF – Epidermal growth factor; AMH – Antimullerian hormone; BMP15 – Bone morphogenetic protein 15; BMP6 - Bone morphogenetic protein 6; BMP2 - Bone morphogenetic protein 2; BMP4 - Bone morphogenetic protein 4; IGF1 and IGF2 – Insulin growth factors 1 and 2; TGFβ- tumor growth factor beta; BMPs - Bone morphogenetic proteins superfamily; FSH – Follicle stimulating hormone; LH – Luteinizing hormone. Activation of primordial follicle pathway, leading to an
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