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Ultrastructural Study of Polyspermy During Early Embryo Development in Pigs, Observed by Scanning Electron Microscope and Transmission Electron Microscope

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Ultrastructural Study of Polyspermy During Early Embryo Development in Pigs, Observed by Scanning Electron Microscope and Transmission Electron Microscope Cell Tissue Res (2001) 303:271–275 DOI 10.1007/s004410000315 REGULAR ARTICLE Ping Xia · Zhouji Wang · Zengming Yang Jinghe Tan · Pengchun Qin Ultrastructural study of polyspermy during early embryo development in pigs, observed by scanning electron microscope and transmission electron microscope Received: 4 April 2000 / Accepted: 24 October 2000 / Published online: 10 January 2001 © Springer-Verlag 2001 Abstract Polyspermy is generally considered a patho- Keywords Morphology · Oocytes · Sperm · Fertilization · logical phenomenon in mammals. Incidence of polysper- Lysosome · Pig my in porcine eggs in vivo is extremely high (30–40%) compared with other species, and polyspermy rate in the in vitro fertilized eggs in pigs can reach 65%. It is still Introduction unknown whether polyspermy to a certain degree is a physiological condition in pigs, and whether porcine Monospermic fertilization is generally regarded as an es- eggs have any capability with which to remove the ac- sential feature of the reproductive process in mammals. cessory sperm in the cytoplasm. The objectives in the Penetration of the oocyte plasma membrane by more present study are to observe the ultrastructural changes than one spermatozoon, a condition defined as polysper- of accessory sperm during early embryonic development my, is invariably pathological and leads to failure or ab- in pigs. A total of 58 normal, early embryos at one-, two, normal development of the early embryo (Hunter 1976, three-, and four-cell and morular stages were collected 1991). The block to polyspermy occurs at either the zona from gilts and were studied by scanning electron micros- pellucida or the oocyte plasma membrane, and in some copy (SEM) and transmission electron microscopy species it may occur on both sites (Wolf 1981). In pig (TEM). The surface ultrastructure showed that sperm fu- eggs, blocks to polyspermy are located on both sites sion with the zona pellucida was a continuous process (Hunter and Nichol 1988; Hunter 1990). Incidence of during one-, two-, three-, and four-cell and morular stag- polyspermy in porcine eggs in vivo is extremely high es, as observed by the SEM. Accessory sperm were pres- (30–40%) compared with other species (Perry 1954; ent in the cytoplasm of cleaved embryos. The sperm Hanly 1961; Polge 1978). Polyspermy rate in the in vitro heads in the cytoplasm of cleaved embryos did not de- fertilized eggs in pigs can reach 65% (Wang et al. 1998). condense. TEM revealed the presence of a condensed It is still unknown whether polyspermy to a certain de- sperm head within a lysosome (or phagolysosome) in a gree is a physiological condition in pigs and whether three-cell embryo. These observations suggest that poly- porcine eggs have any mechanisms to remove the acces- spermy may be a physiological condition in pigs and that sory sperm in the cytoplasm. early embryos may develop to term if accessory sperm In the present study, normal embryos at one-, two-, do not interrupt the embryo genome. Furthermore, lyso- three-, and four-cell and morular stages collected from some activity could be another physiological mechanism pigs in vivo were processed for observation of accessory for removing accessory sperm in the cytoplasm of fertil- sperm by scanning electron microscopy (SEM) and ized eggs and cleaved embryos after fertilization in pigs. transmission electron microscopy (TEM). The objective of this study was to observe the ultrastructural changes of accessory sperm in one-, two-, three-, and four-cell embryos and morulae in pigs. P. Xia (✉) Department of Obstetrics and Gynecology, College of Medicine, University of Arizona, 1501 N. Campbell Ave., UMC, Rm 8329, Materials and methods Tucson, AZ 85724, USA e-mail: [email protected] Tel.: +1-520-6266923, Fax: +1-520-6262768 Pigs Z. Wang · Z. Yang · J. Tan · P. Qin Six normal, pubertal gilts (Harbin White, 8 months old, Department of Biotechnology, Northeast Agriculture University, 80–100 kg) were obtained from commercial herds (from autho- Harbin, People’s Republic of China rized suppliers of experimental animals to the Northeast Agricul- 272 ture University in Harbin, Heilongjiang Province, People’s Repub- ZP-free, one-cell embryo (Fig. 1). An accessory sperm lic of China). The gilts were kept under approved standard condi- head without an acrosome, partially fused with the mem- tions and were monitored for the onset of estrus cycles. The ani- mal ethics committee at the Northeast Agriculture University ap- brane of the one-cell embryo, was observed between mi- proved the experimental procedure. crovilli (Fig. 2). Sperm on the ZP of embryos at cleavage stages dem- Early porcine embryo collection onstrated a continuous process of fusion with the ZP. The embryos at the two-cell stage with intact ZP were The gilts were mated after “standing estrus”. The reproductive covered with many sperm, most of which were not em- tracts were collected after killing the pigs 24 h, 2 days, and 3 days bedded in the ZP (Fig. 3), whereas the embryos at hte after mating. The gilts were anesthetized by intravenous injection four-cell stage appeared smoother compared with those of an overdose of Mebumal into the ear vein. Cardiac arrest was achieved by intracardiac injection of saturated KCl (20 ml). After at the two-cell stage (Fig. 4). At higher magnification, it cardiac arrest had been registered by auscultation and palpation, was observed that most sperm heads were embedded the reproductive tracts were carefully dissected from the body and completely in the ZP or in the ZP with the sperm tails rapidly transferred to 0.1 M Dulbecco’s phosphate-buffer saline left out (Fig. 5). Few sperm heads without acrosomes (D-PBS). Embryos at the one-, two-, three-, and four-cell and mor- ular stages were collected by flushing the oviducts and uteri with were seen. The surfaces of morular embryos appeared 0.1 M D-PBS. smooth and all the residual sperm heads and tails were embedded in the ZP (Fig. 6). Scanning electron microscopy Embryos were individually placed on small coverslips (6×6 mm) TEM observations coated with 3% Formvar. The specimens were processed as fol- lows: (1) immersion in 1% glutaraldehyde for 20 min; (2) immer- sion in 1% tannic acid solution for 20 min; (3) immersion in 1% Many sperm heads were seen in the outer layer of ZP osmium tetroxide for 20 min; (4) dehydration in ascending con- (Fig. 7). The cortical granules were absent in the cortex centrations of ethanol (50–100%); (5) critical-point drying and cytoplasm in all the embryos observed. Accessory sperm sputter-coating with gold. The specimens were observed with an heads were present in the cytoplasm of the three-cell em- S-520 scanning electron microscope. bryo (Fig. 8). These sperm heads did not decondense. Some embryos at the one-cell stage were treated with 2.5% proteinase to remove the zona pellucida (ZP) prior to processing. Approximately 50% of blastomeres at the three- and four-cell stages contained accessory sperm heads ob- served by serial sections. TEM revealed the presence of Transmission electron microscopy a condensed sperm head within a lysosome (or phagoly- The embryos were fixed in 2% glutaraldehyde in 0.1 M D-PBS for sosome) in a three-cell embryo (Fig. 9). Organelles such 1 h at 4°C, post-fixed in 1% osmium tetroxide and then dehydrat- as mitochondria, Golgi complexes, and endoplasmic re- ed in ascending concentrations of acetone (50–100%). Subse- ticulum retained normal morphology in the embryos quently the fertilized eggs and embryos were individually embed- ded in Epon 812. Thin sections (serial thin sections for some of with polyspermy (Fig. 10). the two-, three-, and four-cell embryos) were prepared on an LKB- 5 ultramicrotome and stained with uranyl acetate and lead citrate. The sections were examined with a Hitachi-800 transmission elec- tron microscope. Results L Fig. 1 Surface ultrastructure of a one-cell porcine embryo ob- served by scanning electron microscopy. The zona pellucida (ZP) A total of 58 early embryos at one-, two-, three-, and has been partially removed by 2.5% proteinase. Uniform distribu- four-cell stages and morular stage were processed for tion of microvilli can be seen. ×1,000. Dotted bar 30 µm this study (Table 1). Fig. 2 Embryo shown in Fig. 1 at higher magnification. A sperm head (Sp) without acrosome can be seen on the surface of the mi- crovilli. ×1,200. Dotted bar 2.5 µm SEM observations Fig. 3 Surface ultrastructure of two-cell embryo with intact zona × Morphological observations by SEM revealed uniform pellucida. Many sperm cover the surface. 700. Dotted bar 43 µm distribution of numerous microvilli over the surface of a Fig. 4 Surface ultrastructure of four-cell embryo with intact zona pellucida. Most of the sperm are embedded in the zona pellucida. ×800. Dotted bar 38 µm Table 1 Total number of embryos examined at each stage Fig. 5 Embryo shown in Fig. 4 at higher magnification. Most sperm heads are embedded in the zona pellucida and sperm tails Embryo stages Total number of embryos examined are left out. A few sperm heads without an acrosome (Sp) can be seen on the surface of the zona pellucida (ZP). ×4,000. Dotted bar 1-cell 9 7.5 µm 2-cell 13 3- to 4-cell 24 Fig. 6 Surface ultrastructure of an embryo at morular stage. All of Morula 12 the sperm are embedded in the zona pellucida (ZP). Only a few sperm tails can be seen on the surface. ×600. Dotted bar 50 µm 273 Discussion the mammalian oocytes following fertilization. The inci- dence of polyspermy varies widely among species in Normal fertilization involves a combination of a single mammals. In pigs, polyspermic rate under both in vivo sperm and an oocyte.
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