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Meiotic Progression and Developmental Competence of Oocytes Collected from Juvenile and Adult Ewes S

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Meiotic Progression and Developmental Competence of Oocytes Collected from Juvenile and Adult Ewes S Meiotic progression and developmental competence of oocytes collected from juvenile and adult ewes S. Ledda, L. Bogliolo, P. Calvia, G. Leoni and S. Naitana Department of Animal Biology, University of Sassari, Italy The complete nuclear maturation and fertilization in vitro of oocytes from 30\p=n-\40-day-old juvenile lambs, and their ability to develop up to the blastocyst stage when transferred into recipient ewes after fertilization in vivo and culture was studied. Cumulus\p=n-\oocytecomplexes were recovered from juvenile ovaries and only those with several cumulus cell layers were selected and compared with oocytes from adult sheep. The rate of meiotic progression was significantly lower (P <0.001) for juvenile oocytes (8%) than for adult oocytes (58%) without gonadotrophins in the culture medium. However, a similar maturation rate was observed in oocytes of both juvenile (76%) and adult sheep (84%) in the presence of gonadotrophins. Eighteen hours after in vitro insemination, the fertilization rates for juvenile oocytes were not significantly different from those of adult oocytes (64% and 72%, respectively). Parthenogenetic activation and polyspermy were higher in juvenile than in adult oocytes (P < 0.001). The proportion of blastocysts produced was lower for juvenile (20% than for in vitro matured adult oocytes (49%) after their transfer into transitory recipients for 5.5 days (P<0.01). However, the viability of blastocysts (67%) derived from in vitro matured juvenile oocytes showed a rate of hatching similar to that obtained from adult oocytes (74%). Pregnancy rates for recipient ewes at 90 days were similar for both juvenile (57%) and adult (61%) oocytes. The results indicate that it is possible to mature and fertilize in vitro matured juvenile oocytes to produce viable embryos. Introduction to exogenous gonadotrophin until 2—4 weeks after birth (Mansour, 1959; Mauleon, 1969), when granulosa and thecal In mammals, oogénesis starts in the embryonic ovary. After cells become well developed (Kennedy et al, 1974). A further several cycles of mitotic activity primordial germ cells are advantage of using oocytes collected from juvenile animals meiotically arrested as primary oocytes. Near birth, meiosis is would be a shorter generation interval in genetic selection arrested at the dictyate stage of the first meiotic prophase and programmes (Georges and Massey, 1991). female resumes after the onset of puberty in the preovulatory follicles Oocytes obtained from ovaries of juvenile calves as the consequence of the LH surge. The cumulus—oocyte after treatment with pituitary gonadotrophins may be fertilized complex isolated from the antral follicles of most adult dom¬ and develop in vitro to the blastocyst stage at a rate that is estic and rare wildlife species can be matured, fertilized and similar to that of the adult cow (Armstrong et al, 1992; Irvine cultured in vitro, to stages competent for development to birth, et al, 1993). However, oocytes collected from untreated (Palma following transfer into synchronized recipients (see Brackett, et al, 1993) and untreated/treated (Revel et al, 1995) juvenile 1992; Loskutoff and Betteridge, 1992). The acquisition of calves result in a lower rate of development to blastocysts than meiotic competence appears to be possible not only in oocytes do those of adult cows. In juvenile goats, a lower rate of in vitro collected from adult females but also in oocytes from juvenile fertilization was observed when compared with adult animals animals which represent an alternative source of oocytes. A (Martino et al, 1995). More recently, blastocysts have been previous study showed that there are morphological changes in produced using in vitro matured (IVM) and in vitro fertilized the ovaries of juvenile Merino ewes during the first 8 weeks (IVF) oocytes from treated and untreated 60—120-day-old after birth (Kennedy et al, 1974). A significant increase in lambs (Earl et al, 1995). ovarian mass was accompanied by a marked proliferation and The aim of the present study was to examine the meiotic growth of vesicular follicles with accumulation of follicular competence of oocytes obtained from untreated juvenile fluid, although no significant differences were found in mean (30-40 day) and adult ewes under different culture conditions plasma concentrations of pituitary gonadotrophins (Tassell and their fertilization in vitro. The developmental potential of et al, 1978). Antral follicles of prepubertal ewes do not respond in vitro matured oocytes was assessed after transfer to inseminated temporary recipients and to term after transfer of Received 1 May 1996. blastocysts to definitive recipients. Downloaded from Bioscientifica.com at 09/28/2021 04:38:39PM via free access Materials and Methods motility and 5, vigorous motility. Spermatozoa that showed a motility grade of less them 4 were rejected. Semen samples were pooled and incubated at a concentration of 10 x 10 the oocytes 1 Recovery of ml Coulter Electronics Ltd, in Petri ~ (Coulter Counter, Luton) Ovaries from juvenile (30—40 days of age and body mass of dishes containing a suspension of fresh oviductal epithelial cells 6—12 kg) and from adult sheep were collected from a local and 2 ml TCM 199 + 10% FCS for 3 h at 39°C in 5% C02 in abattoir and transported in Dulbecco's phosphate-buffered air. For assessment of nuclear maturation, 15—20% of total saline (PBS; Sigma, St Louis, MO) containing 50 U penicillin oocytes were fixed for 24 h in acetic acid—ethanol solution and ml-1 and 50 µg streptomycin ml-1 (Sigma) at 20-25°C, stained with Lacmoid (1%). After capacitation, sperm motility arriving at the laboratory within 1 h. Ovaries were washed was checked and the sperm washed twice by centrifugation three times in fresh PBS with penicillin and streptomycin. (5 min at 250 g) in modified Tyrode's medium (TALP) at 35°C. the Ovaries were sliced using a microblade and contents The semen pellet was resuspended in TALP medium at a released in medium TC-199 (plus Earle's salts and bicarbonate; concentration of 1 10 spermatozoa ml" and used at this 1 and Sigma) supplemented with 25 mmol Hepes ~ (Sigma) dilution for insemination. penicillin and streptomycin, and 0.1% (w/v) polyvinyl alcohol After mechanical removal of cumulus cells surrounding the (PVA; Sigma). The cumulus-oocyte complexes (COCs) oocytes with a fine glass pipette, in vitro matured COCs were selected according to morphological criteria (intact COCs with transferred into 50 µ drops of sperm suspension covered by several dense cumulus cell layers and homogeneous cytoplasm) mineral oil and incubated for 18 h at 39°C in 5% C02 in air. were released in the medium and washed three times in the Success of fertilization was determined at 18 h after insemina¬ same medium before in vitro maturation. Oocytes obtained tion after fixation in acetoalcoholic solution for 24 h and either from juvenile or adult ovaries were selected according to staining with Lacmoid. Oocytes with only one pronucleus were their dimensions using an inverted microscope equipped with a evaluated as parthenogenetically activated. Oocytes with male calibrated eyepiece, and small oocytes ( < 135 µ ) and those and female pronuclei were considered fertilized, while those the with signs of atresia were discarded. For each ovary, that showed more than two pronuclei were evaluated as number of oocytes recovered was recorded. polyspermic. Four experiments were performed to compare the com¬ petence of juvenile ovine oocytes with those of adult ewes. Experiment 3: embryo production from oocytes matured in vitro Experiment 1: in vitro maturation after transfer to inseminated recipients The COCs obtained from juveniles were allocated to the In this the ability of juvenile and adult oocytes maturation systems. Juvenile and adult oocytes were experiment following to after their transfer to for cultured in for the first 24 h in medium TC-199 develop temporary recipients parallel fertilization and in vivo for 5.5 days was with 10% (v/v) heat-treated fetal calf serum (FCS; development supplemented ' examined. or FSH in the absence of 10 µg ml ~ and Sigma) presence After 24 h of in vitro maturation, under the conditions LH 25—30 10 mg ml ~ (Pergonal, Serono, Roma). Only described in Expt 1, oocytes were washed with fresh TCM- oocytes were put in a single Petri dish (35 mm) containing 2 ml 199 + 10% FCS and transferred to recipient ewes. culture medium which was maintained on a rotary shaker at surgically For this Sardinian ewes were low during the entire incubation The culture purpose, temporary recipient speed period. with sponges contain¬ conditions were maintained at a of 39°C in a synchronized intravaginal progestagen temperature 40 acetate and inserted for 14 All humidified with 5% in air. At the end of the ing mg fluorogestone days. atmosphere C02 were anaesthetized with 10 ~ body maturation oocytes (30%) from each culture system recipients mg kg weight period, of sodium (Farmaceutici Gellini, in saline. The were fixed for 24 h in acetic acid ethanol solution (1:3; v:v), pentothal Aprilia) abdominal cavity was opened and the genital tract exposed. stained with 1% (w/v) Lacmoid (Sigma), and examined under a Only ewes that did not have corpora lutea were used as phase-contrast microscope at x 200—400. Stages of nuclear recipients. The oviducts were ligated just above the uterotubal maturation of oocytes were evaluated as germinal vesicle (GV) and 20-30 were via the into and vesicle breakdown (GVBD), I (M I), junction oocytes injected ampulla germinal metaphase the oviduct of each in about 15-20 µ of medium and metaphase II (M II) and degenerated (Deg.). recipient 50 µ of spermatozoa (100x10 ml-1) using a Tom-Cat catheter (Sherwood, St Louis, MO) connected to a syringe. The oviducts of recipients were flushed 5.5 days later and all ova 2: sperm and in vitro Experiment capacitation fertilization and embryos were recovered from the flushing medium and This experiment was designed to evaluate the percentage of observed under an inverted microscope to assess their devel¬ in vitro fertilized oocytes obtained from juvenile and adult opmental stage.
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