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Biology Strony.Indd Vol. 6, No. 2 ORIGINAL RESEARCH Oogenesis in pig ovaries during the prenatal period: ultrastructure and morphometry Zofia Bielańska-Osuchowska1 Department of Histology and Embryology, Warsaw Agricultural University, Warsaw, Poland Received: 9 May 2006; accepted: 22 June 2006 SUMMARY Oogenesis in fetal pig ovaries comprises the successive changes from the primordial germ cells to the dictyotene oocytes in primordial ovarian follicles. In this study the observations were carried out with an electron microscope and stereological analysis was performed. At the ultrastructural level there are no differences between the primordial germ cells and oogonia, but oogonia are connected with the intercellular bridges. The onset of the dictyotene phase was accompanied by the changes in the cytoplasm of oocytes. Near the nucleus, the yolk nucleus is formed containing numerous Golgi bodies, endoplasmic reticulum (ER), mitochondria and granules. ER proliferates in contact with the external leaflet of the nuclear envelope forming the narrow ER cisterns. Between the nuclear envelope and ER cisterns, the vesicles with grey content are visible. The proliferating ER forms numerous concentric cisterns around the nucleus. Next, the most external cisterns fragment, detach, and then form the cup-like structures. These structures separate the distinct areas of cytoplasm-compartments, which contain mitochondria, ribosomes and lipid droplets. The cells of cortical sex cords of the ovary, which encloses 1Address for correspondence: Department of Histology and Embryology, Warsaw Agricultural University, ul. Nowoursynowska 159, 02-776 Warszawa, Poland Copyright © 2006 by the Society for Biology of Reproduction 162 Oogenesis in pig fetal ovaries the oocyte, form the follicles. The volume of oocytes in forming follicle increases due to the increase in the number of the cell inclusions: lipid droplets, vacuoles and yolk globules. In the oocytes of primordial ovarian follicles, the compartments are transformed into the yolk globules, which are encountered by a sheath of ER cisterns and the grey vesicles; they contain the mitochondria, lipid droplets and light vacuoles. The role of the compartments and yolk globules as metabolic units is discussed in comparison with similar structures of the mature eggs of pigs and other mammal species. Reproductive Biology 2006 6:161–193. Key words: oogenesis, yolk globule, ultrastructure, fetus, pig INTRODUCTION In pigs, similarly to primates and cattle, oogenesis begins very early in the prenatal period and is asynchronous. In the fetal ovary the mitotic prophase oogonia coexist with meiotic oocytes and with the primordial follicles. Although histology and histochemistry of the developing pig ovary in the prenatal period were previously described [6, 9], changes during this period were observed using primarily a light microscope. The few reports studying the ultrastructure of germ cells during oogenesis in this species are limited to the description of 1/ the ultrastructure of primordial germ cells and young oogonia in the ovary from 24, 26 and 27th day of development [38-40], and 2/ sex determinants in pig oogonia and oocytes during the prenatal period [7]. Other reports are concerned with maturing and tubal oocytes [10, 18, 34-36]. There is also some data on the ultrastructure of developing oocytes of other mammalian species. In the middle of the 20th century the main interest was in the ultrastructure of mature oocytes and eggs, and then the maturation of oocytes was extensively studied as the basis for a more frequent application of fertilization and early embryo development in vitro [11, 14, 21-23, 29]. The aim of the present research was to investigate the ultrastructural changes in ovarian germ cells from genital ridge stage to the end of the perinatal development. The study focused mainly on alternations in ooplasm during the primordial follicles formation. Bielańska-Osuchowska 163 MATERIALS AND METHODS The observations were carried out on ovaries obtained from 45 pig fetuses aged 24 to 113 days post coitum (dpc) and their characteristic are presented in Table 1. The study was performed in accordance with the principles and Table 1. Characteristics of fetuses used in the experiment Number of fetuses Number of fetuses Stage visible for the dpc used for morphology used for stereology first time 24 3 3 primordial germ cells 26 2 27 1 28 1 31 2 2 33 3 2 oogonia connected with 39 3* 3* intracellular bridges 40 1* 45 1 oocytes in meiotic 47 7 [3*] 5 prophase 49 1 541 1 1 oocytes I; forming 56 2 ovarian follicles I 60 1* 1* 64 2 66 2 73 5 74 1 77 3 1 83 4 3 oocytes II 90 1 1 95 1 1 100 3 2 101 1 1 oocytes III, primordial 106 1 1 ovarian follicles 112 1 113 3 2 Total 57 29 *fetuses obtained from sows of unknown bread 164 Oogenesis in pig fetal ovaries procedures of the Animal Ethic Committee. Eight fetuses were obtained from sows of unknown breed slaughtered at the municipal slaughterhouse in Warsaw. The approximate age of these fetuses was determined on the basis of their cromp-rump length [30]. Thirty-seven fetuses of the exactly determined dpc were obtained from Large White sows bred at the local farm. Immediately after slaughter, a hysterectomy was performed and the fetuses were removed. Small blocks of dissected ovaries were fixed with 2.5% glutaraldehyde in 0.1 M phosphate buffer at pH 7.4, postfixed in 1.5% osmic acid in the same buffer and embedded in Epon 812. The time between the sow slaughtering and the fixation of the tissue was not longer than 20 minutes. Semithin and ultrathin sections were cut on the LKB ultramicrotome. Semithin sections were stained with Azure I and methylene blue. Ultrathin sections were contrasted with uranyl acetate and lead acetate. Observations were carried out in the electron microscope JEOL JAM 100C (Tokyo, Japan). The mean diameter of the profile of cells and their nuclei was measured on the electronograms at the final magnification of ×2500. Assuming that oogonia and oocytes were nearly spherical, the volume of the cell and the nucleus were calculated using the mean diameter of the area of profile. On the electronograms at the final magnification of ×5330, the procedure of the differential point counting [55] was performed and the volumetric density (Vv) of organelles was calculated. Differences between two successive means in each examined parameter were analyzed by t-test. RESULTS 1. Morphology The ovaries of embryos from 24 dpc were in the phase of genital ridge, in which the ameboidal gonocytes were located between the mesenchymatic cells (fig.1). The sex of genital ridge was confirmed by the presence of PAS- positive granules in some mesenchymatic cells, characteristic for early sex cords cells of the pig ovary [4]. During the morphological differentiation of Bielańska-Osuchowska 165 Figure 1. Primordial germ cell (PGC) in the genital ridge; embryo 24 dpc; B: blastema cell; magnification ×3900 the ovary starting from 24 dpc until approximately 40 dpc, the gonocytes were present exclusively in the oogonia phase. In older ovaries, oogonia were grouped in so-called egg nest (Eiballen, clusters, cysts; [31, 32]). Until the end of the prenatal development, oogonia were present in smaller numbers in the external part of the ovarian cortex. The first formation of ovarian follicles was observed in the deepest part of the cortex, next to the medulla (56 dpc). The sex cord cells transformed into follicular cells. In the oldest fetuses (106, 112, 113 dpc), the primordial follicles, in which a single oocyte was completely surrounded by a layer of flattened follicular cells, formed a layer close to the medullar part of the ovary [8]. Ultrastructure of oogonia Oogonia differing from sex cord cells were significantly bigger and rounded (fig. 2, 17A) and many of them were polarized in the shape of a pear. The narrow part was filled with hyaloplasm in which only free polyribosomes and mitochondria were scattered. In the distended part short profilesofendoplasmic reticulum (ER), free polyribosomes and mitochondria were distributed quite regularly near the nucleus. The free polyribosomes were observed in all examined phases of oogenesis. Close to the nucleus, apart from centrioles, single 166 Oogenesis in pig fetal ovaries Figure 2. Two oogonia connected with the intercellular bridge (arrow); ovary 47 dpc; magnification ×3900 Figure 2a. Intercellular bridge (arrow), a fragment of fig. 2; N; nucleus, M: mitochondrion; magnification ×15000 dictyosomes were observed. Mitochondria were spherical with narrow, nearly tubular cristae, often associated with dense granular bodies [7]. The nucleus was spherical with abundant nucleoplasm, short segments of heterochromatin and dense marginal chromatin. One or two spongy nucleoli were composed of fibrillar and granular parts. On many sections two wide segments of dense heterochromatin adjacent to the nucleolus were seen (fig. 5), which coincide with nucleolus associated chromatin, visible on histological slides [6]. The Bielańska-Osuchowska 167 neighbouring oogonia or oogonia and sex cord cells were connected with macula adherens. Mitotic divisions of oogonia were visible especially during the early period of the ovary development. Oogonia connected with intercellular bridges were observed from 39 dpc (figs. 2, 2a, 17A). On some single sections two bridges opened into Figure 3. Oblique section of an intercellular bridge between two oogonia, the rib- like structures on the surface (arrow); ovary 83 dpc; magnification ×30000 Figure 4. Nucleus (N) of an oocyte in meiotic prophase with synaptenemal complexes (arrow) between the homologue chromosomes; ovary 83 dpc; magnification ×15000 168 Oogenesis in pig fetal ovaries Figure 5. Fragment of an oocyte; Figure 6. Oocyte with the yolk nucleus nucleus (N) connected with two (YN) in the young follicle; ovary 90 dpc; segments of heterochromatin; ova- N: nucleus, L: lipid droplets; magnification ry 100 dpc; magnification ×3900 ×3900 one oogonium. The bridges were cylindrical canals surrounded by a thick cell membrane, which was continuous with the oogonial cell membranes.
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