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Ovarian Follicle Reserve: Emerging Concepts and Applications Anim. Reprod., v.10, n.3, p.180-186, Jul./Sept. 2013 Ovarian follicle reserve: emerging concepts and applications K.C. Silva-Santos, L.S.R. Marinho, G.M.G. Santos, F.Z. Machado, S.M. Gonzalez, L.A. Lisboa, M.M. Seneda1 Laboratório de Reprodução Animal, Centro de Ciências Agrárias, Universidade Estadual de Londrina, Londrina, PR, Brazil. Abstract migrate from the yolk sac to the primordial gonads. Initially by mitosis, these germ cells are multiplied and This paper presents new concepts in the study of many groups of oogonia are established, interacting folliculogenesis and describes some of the current one to each other by cytoplasmic communications. applications to reproductive biotechnology. The After that, oogonia are surrounded by somatic cells, importance of better understanding this issue is addressed forming the cortical cords, which are precursors of both for basic and applied research. After a brief review primordial follicles. The oogonias differentiate into of the basic conceptions of the origin, formation, and oocytes, which will form primordial follicles when growth of follicles according to established concepts, associated with pregranulosa cells. Oocytes initiate some controversial points, as the postnatal production of meiotic division and arrest at the prophase of meiosis I, the follicles and the role of multioocyte follicles, are in diplotene stage. This interruption lasts until follicle discussed. The importance of the ovarian follicular recruitment, either in puberty or final period of the reserve is considered for fertility and reproductive reproductive life (Soto-Suazo and Zorn, 2005; van den parameters, as well as some questions about the presence Hurk and Zhao, 2005). of multioocyte follicles in adult ovaries. Finally, some future prospects are proposed. Antral follicles, number of oocytes, and embryo production Keywords: follicular population, folliculogenesis, multioocyte follicle, neo-folliculogenesis, preantral follicle. The impact of the size of the ovarian follicle reserve on applied aspects of reproduction, such as Introduction fertility and pregnancy rates has challenged the The interest in both applied and basic issues conventional concept of the ovary as a fairly static relating to folliculogenesis has increased significantly in organ. There is high variability among individual the recent years. Many points may clarify this increased animals in the numbers of preantral and antral interest. In commercial aspects, the industry of embryo follicles and oocytes in the ovaries of bovine females, production, most notably in vitro embryo production, has and it seems that the breed and or subspecies may dramatically increased worldwide. Other biotechnologies, have a strong influence on that, especially when such as timed artificial insemination, cloning and comparing Bos taurus vs. Bos indicus (Burns et al., transgenic animals have been widely used, due to their 2005; Ireland et al., 2007; Santos et al., 2012). benefits on animal breeding or human health. However, However, there is repeatability in antral follicle count many aspects in follicular physiology remain unknown, (AFC) within individuals regardless of age, breed, particularly the role of the ovarian follicle reserve and stage of lactation or season (Burns et al., 2005). This fertility in cattle. Regarding basic research, some new repeatability was also observed on Bos indicus-taurus theories have been presented on the follicular pool, females (Santos et al., 2012). providing interesting debates about follicle origin and the Extreme variation among donors in embryo mechanisms involved in their recruitment and growth. production by in vitro and in vivo methods remains one The purpose of this article is to summarize recent studies of the problems in bovine embryo production. It is focusing on how the follicle reserve is related to the interesting to note that some donors present better improvement of reproductive efficiency results following MOET or IVF, independently of the Basic concepts of folliculogenesis number of follicles and oocytes (Pontes et al., 2009). However, the most common situation is a higher In female mammals, folliculogenesis starts production of embryos from those donors with higher during fetal life (Fig. 1). First, primordial germ cells number of follicles (Table 1). _________________________________________ 1Corresponding author: [email protected] Received: May 1, 2013 Accepted: July, 24, 2013 Silva-Santos et al. Ovarian follicle reserve. Figure 1. A model of folliculogenesis in ruminants. Adapted from Scaramuzzi et al. (2011). Table 1. Variation in embryo production among 6 Nelore cows (I-VI), comparing in vitro (OPU/IVF) versus in vivo (MOET) procedures. Donors (I-VI) I II III IV V VI Total no. OPU IVF cycles 5 5 4 4 5 5 Mean no. oocytes/collection 36.6 25.6 49 29.7 22.8 16 Mean no. viable oocytes/collection 32.2 23.4 45.2 26 19.6 14.4 Mean no. embryos/OPU IVF 15.6 10.4 24.1 10.3 6.8 3.8 Mean no. pregnancies/OPU IVF 4.8 2.8 9.25 4.3 2.2 1 Total no. MOET cycles 2 3 2 2 2 3 Mean no. embryos/collection 10 4.3 6.5 2 12.5 5.3 Mean no. pregnancies/collection 5.5 2 1 1.5 6.5 1.3 From Pontes et al. (2009). In large scale commercial embryo production ovaries, trying to identify those animals with higher programs, individual animal variation in the number of numbers of antral follicles. It is important to emphasize follicles is very important (Table 2). The ordinary that this selection, based on number of follicles, must be method of donor selection in this case consists in done after the evaluation of the genetic merit of the performing a pre-evaluation by ultrasound of the donors. Anim. Reprod., v.10, n.3, p.180-186, Jul./Sept. 2013 181 Silva-Santos et al. Ovarian follicle reserve. Table 2. Mean (± SD) for reproductive performance following OPU/IVP procedures (n = 656) performed in Nelore donors (n = 317), sorted according to oocyte collection (G1 = highest production and G4 = lowest production). Values given are per donor animal. Group No. cattle No. viable No. viable No. pregnancies No. pregnancies oocytes embryos on day 30 on day 60 G1 n = 78 47.06 ± 1.6a 15.06 ± 0.86a 5.62 ± 0.54a 5.52 ± 0.81ª G2 n = 80 24.95 ± 0.33b 9.17 ± 0.63b 3.63 ± 0.36b 3.32 ± 0.33b G3 n = 79 15.57 ± 0.26c 6.00 ± 0.39c 2.10 ± 0.21c 1.92 ± 0.20b G4 n = 80 6.31 ± 0.38d 2.42 ± 0.25d 0.92 ± 0.13d 0.85 ± 0.13c Total n = 137 23.35 ± 0.72 8.13 ± 0.30 3.03 ± 0.15 2.91 ± 0.013 a,b,c,dWithin a column, means without a common superscript differed (P < 0.05). From Pontes et al. (2011). Fertility and number of antral follicles and delayed fetal ovarian development (Borwick et al., 1997; da Silva et al., 2002). In recent years, low AFC in dairy cattle has The health management of cattle on dairy been associated with some characteristics of low farms influences long-term reproductive performance of fertility, such as smaller ovaries, lower numbers of the herd. Mammary gland infection is the major factor follicles and oocytes in the ovaries (Ireland et al., 2008), affecting somatic cell count (SCC) in milk. Studies lower odds of being pregnant in the end of the breeding suggest that offspring of cows with chronically high season (Mossa et al., 2012), reduced responsiveness to SCC during gestation have reduced anti-Müllerian superovulation (Singh et al., 2004; Ireland et al., 2007), hormone (AMH) concentrations. Lower AMH lower circulating concentrations of progesterone and concentrations are indicative of a diminished size of the anti-Mullerian hormone (AMH; Ireland et al., 2008; ovarian reserve and potential reduction in reproductive Jimenez-Krassel et al., 2009), reduced endometrial efficiency (Ireland et al., 2010; Evans et al., 2012). thickness from day 0 to day 6 of the estrous cycle (Jimenez-Krassel et al., 2009), and higher amounts of Population of antral follicles versus ovarian reserve cumulus cell markers for diminished oocyte quality (Ireland et al., 2009). It is known that Bos indicus cattle have 3-4 times Nutritional influences affect folliculogenesis at more antral follicles and number of oocytes than Bos multiple levels (Scaramuzzi et al., 2011). Increased taurus cattle (Pontes et al., 2009, 2011). To test if the energy supply is known to exert a stimulating effect at ovarian reserve could account for this difference, we an ovarian level (Letelier et al., 2008). Despite the fact counted preantral follicles in ovaries obtained at that some dietary components like IGF-I or leptin are abattoirs from fetuses, heifers and cows (Nelore and great stimulators of follicular growth (Muñoz-Gutiérrez Aberdeen Angus). There was no clear answer to explain et al., 2005; Mihm and Evans, 2008), it is unlikely that why Bos indicus donors have more antral follicles and there is a single metabolic mediator of nutritional produce more oocytes than B. taurus females. Despite influences on folliculogenesis. the high variation between groups and among females In cattle suffering food restriction in the first within the same group, there were no differences trimester of pregnancy, the number of antral follicles of between the number of preantral follicles in the ovaries the fetus can be reduced up to 60%, although the weight of fetuses, heifers or cows of Nelore versus Bos taurus of the calf at birth was not altered (Mossa et al., 2013). females (Fig. 2). These results suggest that total follicle Furthermore, in sheep variations in maternal diet can reserve is not the reason for the difference in oocyte not only limit the growth of the fetus, but also inhibit yield (Silva-Santos et al., 2011). We are currently the expression of genes related to the release of pituitary investigating the rate of follicular atresia in Nelore cows gonadotropins.
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