Oocyte maturation. A.Trounson 1 ' 3, C.Anderiesz 1, G.MJones 1, A.Kausche 1, N.Lolatgis 2 and C.Wood 2

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1 A.Trounson 1 ' 3, C.Anderiesz 1, G.MJones 1, A.Kausche 1, N.Lolatgis 2 and C.Wood 2 Centre for Early Human Development, Institute of Reproduction and Development, Monash University, Monash Medical Centre, 246 Clayton Road, Clayton, Victoria, Australia 3168, and 2 Monash IVF Pty Ltd, Epworth Hospital, 89 Bridge Road, Richmond, Victoria, Australia To whom correspondence should be addressed Primary oocytes recovered from small and growing follicles of 2*3 mm in the ovaries of untreated women, can be matured in vitro, will fertilize and develop in vitro, and when transferred to the patient, develop to term. However, the implantation rate of cleaved embryos has been disappointingly low and when embryos are allowed to develop beyond the 4-cell in vitro, retardation of development and blockage is frequently observed, with relatively few embryos developing to blastocysts. We have devised new culture systems for human embryos to enable high rates of development of in-vivo matured oocytes to blastocysts within 5-6 days of culture, and high implantation rates of these blastocysts when they are transferred to the patients' uterus. These culture systems are now being used for in-vitro matured oocytes. In order to determine whether embryo developmental competence could be improved, a number of factors were examined. Treatment of patients with pure follicle stimulating hormone (FSH) early in the follicular phase, or treatment with oestrogen prior to oocyte recovery, had no apparent effect on any parameters of oocyte developmental competence. There was no indication that a medium made specifically for human oocyte maturation improved oocyte developmental competence. Nuclear and cytoplasmic changes in oocytes matured in vitro appear to be similar to that in vivo, although some lack of synchronization in completing maturation is evident. It is possible that follicles of <10 mm diameter in the human contain developmentally-incompetent oocytes. However, the development to term and birth of normal babies from germinal vesicle stage oocytes recovered from small follicles and matured in vitro, suggests that further research will identify the factors necessary to improve embryo developmental competence. The application of immature oocyte collection (IOC) and in vitro maturation (IVM) as an alternative to ovulation stimulation with high doses of gonadotrophins for in-vitro fertilization (IVF), remains a priority for research in human medicine. Key words: gonadotrophins/in-vitro maturation/ivf/oocyte/ovulation stimulation 52 European Society for Human Reproduction and Embryology Human Reproduction Volume 13 Supplement

2 Introduction The recovery of immature oocytes from women who have not been given large doses of follicle stimulating hormone (FSH) or other ovulation stimulating drugs, remains a research priority for the development of alternative treatment modalities in human in-vitro fertilization (IVF). It would be preferable to expose oocytes to maturational doses of gonadotrophins in vitro, rather than in vivo, now that a reasonable recovery rate of oocytes can be achieved by transvaginal ultrasound guided follicle aspiration, in small growing follicles (5=3 mm diameter) (Trounson etal, 1994). The present situation is that immature oocytes can be recovered efficiently from small follicles by transvaginal follicular aspiration, the oocytes show nuclear maturation changes, consistent with ultrastructural and cytogenetic observations of oocytes matured in vivo, and fertilize and begin cleavage as expected for in vivo matured oocytes recovered from IVF patients in whom ovulation was stimulated (Trounson et al, 1994, 1996; Barnes et al, 1996; Jones and Trounson, 1998). However, there is a major problem of embryo developmental competence in oocytes matured in vitro, despite the birth of normal children using this technique (Trounson et al, 1994; Barnes et al, 1995). The present review examines progress on human oocyte maturation and explores the possible reasons for the reduced developmental competence of in-vitro matured human oocytes. Nuclear maturation of human oocytes in the germinal vesicle stage oocytes Oocytes aspirated from small and growing follicles of women in the early follicular phase of the menstrual cycle, or from anovulatory women with polycystic ovarian syndrome (PCOS), will show nuclear maturation in culture in a variety of media and conditions. Using Eagle's modified minimum essential medium (EMEM) with Earle's salts and glutamine (Flow Laboratories, Irvine, Scotland, UK) and 10% fetal calf serum, IU/ml human menopausal gonadotrophin (HMG, Pergonal ; Serono, Frenchs Forest, NSW, Australia), 0.5 IU human chorionic gonadotrophin (HCG, Profasi ; Serono) and 1 (ig oestradiol/ ml (Sigma, St Louis, MO, USA), ~60% of oocytes had extruded a polar body and were at the metaphase II (Mil) stage of meiosis after h of culture. This increased to ~80% of oocytes by h of culture. However, there was considerable asynchrony of maturation because at 24 h (23-25 h) ~20% of oocytes were already at MIL These data are shown in Figure 1. The proportion of oocytes maturing to Mil was not affected by the classification of atresia but was significantly reduced in PCOS patients (Barnes et al, 1996; Trounson et al, 1996). The lack of influence of atresia on oocyte maturational competence is similar to that reported for the sheep (Moor and Trounson, 1977). 53

3 A.Trounson et al. PERCENTAGE OF OOCYTES GV MI Mil 100 r 80 n=31 n=47 n=63 n= TIME (Hours) Figure 1. Maturation of human oocytes in vitro after h to h culture in Eagle's modified minimum essential medium (EMEM) and gonadotrophins. Oocytes were classified as immature germinal vesicle (GV) stage, maturing metaphase I (MI) or mature metaphase II (Mil) with an extruded polar body (reproduced with permission from Trounson et al, 1994). Oocyte maturation media A range of oocyte maturation media and additives have been tried to improve the speed and synchrony of completing maturation, and the developmental competence of the mature oocytes. The addition of human granulosa cells from preovulatory follicles containing mature oocytes, to maturation medium EMEM, did not alter the maturation or developmental competence of the cocultured oocytes (Trounson et al, 1994). High success rates are routinely obtained for maturation and development to blastocysts (35-44% of cultured oocytes) in the cow using tissue culture medium (TCM) 199 (Sigma), supplemented with 10% fetal calf serum (or human serum), IU recombinant human FSH/ml (Gonal F ; Serono), 0.5 IU HCG/ml (Profasi; Serono), 0.29 mm pyruvate and antibiotics. This medium was therefore used for the maturation of human oocytes. However, the results were similar to that obtained with EMEM (Barnes et al, 1996), despite the occasional success in development to term (Barnes et al, 1995). Maturation of human oocytes could also be achieved in a commercial medium used to grow human amniocytes, that contains no gonadotrophins at all (Chang's medium; Irvine Scientific). Almost the same proportion of oocytes matured to Mil after 48 h culture in Chang's medium as those in the more conventional TCM 199 maturation medium (62% for Chang's medium compared with 65% 54

4 HOURS AFTER INSEMINATION Figure 2. Embryo developmental rate (EDR) of cleaving embryos after maturation in vitro. Each embryo is shown as a dot point and those within circles resulted in development to term. The regression line has been taken from Cummins et al. (1986) and represents an EDR of 100. for TCM gonadotrophins) (Trounson et al, 1996). These data suggest that gonadotrophins are not driving oocyte maturation in vitro, which is not the situation in vivo. Developmental competence of oocytes after maturation in vitro Fertilization rates can be significantly increased from ~30% for insemination in vitro to ~50% using intracytoplasmic sperm injection (ICSI) (Trounson et al, 1996). However, the improvement in the development of oocytes with two pronuclei was only significant in PCOS patients and not in naturally cycling non-pcos patients (Trounson et al, 1996). Hence, ICSI can only really be justified for in-vitro matured oocytes in couples where the male partner has low quality semen or where the female partner has PCOS. By day 2 after insemination, the cleavage and development of embryos was significantly retarded in PCOS patients but not non-pcos naturally cycling patients (Barnes et al, 1996). If the embryo development rate (EDR) (Cummins et al, 1986) for embryos derived from in-vitro matured oocytes is examined over the first 48 h of culture (Figure 2), some embryos block or become retarded in development (on the right-hand side of the regression line), while others remain close to that expected for superovulated in-vivo matured oocytes. Pregnancies derive from embryos close to the regression line (Figure 2). However, 55

5 A.Trounson et al i 80 - EDR day 2 day 3 day 4 Day after insemination of culture in. vitro Figure 3. Embryo developmental rate (EDR) of embryos derived from oocytes matured in vitro. An EDR of 100 is expected for each day of culture. Embryos were grown in human tubal fluid medium containing 10% patient's serum. 70 n 50 % Of 40 - mature oocytes Pronulear oocytes 4-cell (day 2) 8-cell (day 3) Morulae (day 4) Blastocyst (day 5) Figure 4. Proportion of in-vitro matured oocytes that fertilized and developed to cleavage stage embryos, morulae and blastocysts in vitro. Oocytes were matured in TCM gonadotrophins or Chang's medium for 48 h, fertilized by intracytoplasmic sperm injection (ICSI) and cultured in Earle's medium with 10% patient's serum (Trounson et al, 1996). as time in culture in vitro progresses, the EDR progressively drops away from 100 (expected cleavage rate) and the embryos progressively become more retarded in development (Figure 3). As a consequence, development to the 8- cell stage and beyond is characterized by blockage at succeeding cleavage stages (Figure 4) with few embryos growing to blastocysts (Barnes et al, 1995) and implantation rates of transferred embryos being very low (<1%). Examination of factors influencing the developmental competence oocytes Detailed examination of cytoplasmic maturation has revealed no apparent defect in the activation of maturation (or M-phase) promoting factor (MPF) as determined 56

6 by histone kinase activity and phosphorylation and dephosphorylation of the regulatory subunit, cyclin B, and catalytic subunit, p34 cdc2 respectively (Collas, 1996). These phosphorylation events, and protein synthesis, are required for oocyte maturation. Expression of the c-mos proto-oncogene product, mos, which is a component of cytostatic factor (CSF), is also required to stabilise MPF during Mil arrest. Since oocytes matured in vitro undergo the meiotic nuclear changes and remain arrested at Mil, it is perhaps not surprising that these molecular changes are detected in human oocytes matured in vitro. MPF activity can be manipulated experimentally but does not apparently alter oocyte developmental competence (C.Anderiesz and A.Trounson, unpublished data). A number of treatments have been explored to determine whether an increase in embryo developmental competence can be obtained for oocytes matured in vitro. Administration of pure FSH to accelerate follicle growth A brief treatment of patients on day 2 of their menstrual cycle with 150 IU recombinant FSH (Gonal F; Serono) and treatment of patients with 150 IU recombinant FSH/day for 3 days from days 2-4 of their menstrual cycle, was compared to no treatment with FSH. The observations are summarized in Figure 5. Oocytes were aspirated from the follicles of naturally-cycling non-pco women and ovulatory PCO women on days 8-10 of their menstrual cycles. Oocytes were matured in TCM 199 medium with gonadotrophins and 10% patients serum, as previously described. There was no significant difference in the number of oocytes recovered, the rate of maturation and rate of fertilization between the treatments. Consequently, there were no significant differences in the developmental capacity of embryos or the proportion of patients transferred embryos; as a result, this treatment was discontinued. Treatment of patients with oestrogen It was claimed that the pretreatment of patients with oestrogen was important for improvement of embryo developmental competence and uterine receptivity for transferred embryos (Russell et al., 1996). Oral oestradiol valerate tablets were taken at dose rates of 2 mg/day on days 7 and 8 of the menstrual cycle, 4 mg/day on days 9 and 10, 8 mg/day on days 11 and 12 and 2 mg/day thereafter. Oocytes were recovered on days of the menstrual cycle and matured in TCM 199 with gonadotrophins and 10% patient serum as previously described. There was no evidence that oestrogen treatment improved any measure of oocyte developmental competence (Figure 6). Revised oocyte maturation medium A new oocyte maturation medium (HOM medium) was devised that involved reducing lactate levels, increased glucose and salt levels, added cysteine, cysteamine (for glutathione production), amino acids and vitamins together with 57

7 A.Trounson et al. I S «10- o o i 5 D2 150 IU D ll»day Figure 5. Effects of treatment of natural cycle ( ) and ovulatory polycystic ovary (PCO; H patients receiving recombinant follicle stimulating hormone (FSH; 150 IU/day) during the early follicular phase (day 2 or days 2-4) on oocyte recovery and the rate of maturation and fertilization in vitro. 80 -I 60 - % PCO Maturation Nat PCO Fertilization Nat PCO Nat Patients transferred embryos Figure 6. Effects of oestrogen treatment (+) of natural cycle (Nat) and polycystic ovary (PCO) patients compared with no oestrogen treatment (-) on the rate of maturation, fertilization and proportion of patients transferred embryos (day 3 of culture). 58

8 Ch Horn PCO Maturation Ch Horn Nat Ch Horn PCO Fertilization Ch Horn Nat Figure 7. Comparison of maturation and fertilization of oocytes matured in Chang's medium and HOM medium for natural cycle (Nat) and polycystic ovary (PCO) patients. Oocytes were matured in Chang's medium (Ch) or HOM medium (see text for details) for 48 h and the matured oocytes inseminated in vitro. recombinant FSH, HCG and epidermal growth factor (EGF). When compared with Chang's medium, there was no obvious benefits for the use of the revised medium for culture of oocytes for 48 h (Figure 7). Improved culture media and systems for growing blastocysts The need to improve the culture conditions for growth of human embryos to the blastocyst stage was considered necessary to properly evaluate the developmental capacity of embryos derived from in-vitro matured oocytes. While some embryos were capable of development to blastocysts, and to term, in conventional IVF culture medium (Barnes et al, 1995), the overall performance of these culture conditions was considered less than optimal. A detailed description of the development of more appropriate culture methods and conditions is given by Jones et al. (1998). Using a combination of HTF medium (IVF50; Scandinavian IVF Sciences, Gothenberg, Sweden) for culture of embryos in groups for days 1-3 after insemination and Gardner's G2 medium (Barnes et al, 1995) for culture of embryos in groups for days 3-7 (medium changed every 48 h), high pregnancy rates (47% per transfer) and implantation rates (23% per transferred embryo) were achieved with superovulated oocytes matured in vivo (Jones et al., 1998). Provided that one.or two blastocysts or more are produced in this culture system, pregnancy rates are 5=40%, whereas pregnancy did not occur at all if no blastocysts were produced (embryos transferred as morulae or less developed embryos) (Figure 8). These methods are now in routine use for superovulated patients where the oocytes are matured in vivo. We are exploring the use of blastocyst transfers in natural cycle IVF and re-examining the development of embryos derived from oocytes matured in vitro. 59

9 A.Trounson et al (10) o Pregnancy Rate (20) (8) (8) 0 i (4) 0 i i No. of Blastocysts Produced 11 + Figure 8. The relationship between the number of blastocysts produced by superovulated and in-vivo matured in-vitro fertilization (IVF) patients and the pregnancy rate obtained for the transfer of 1-3 embryos on day 6 of culture after insemination. The embryos grown under conditions described in the text. Number of patients transferred embryos are shown in brackets for each group. The relationship of follicle size to oocyte developmental competence Oocytes from small growing follicles of ^2 mm in cattle also have reduced developmental competence, with a low rate of cleavage and development to blastocysts (Trounson et al, 1996). However, these small follicles are at the limit of visibility by transvaginal ultrasound in the human, and are unlikely to represent a large proportion of the immature oocytes recovered. Dubey et al. (1995) noted a decline in fertilization rates of oocytes from superovulated follicles of decreasing size (74% of oocytes from mm; 70% of oocytes from mm; 58% of oocytes of mm). It is possible that the human oocyte, unlike the cow, is not developmentally competent as an embryo until a minimum follicular size is obtained. From the data of Dubey et al. (1995), this would appear to be <10 mm. Studies underway in our own laboratory indicate that normal rates of development to blastocysts can be obtained from natural cycle patients with follicle sizes in the range of mm diameter, when given HCG to induce maturation in vivo. Discussion The primary defect in oocytes matured in vitro is a reduced developmental competence, particularly cleavage and development beyond the 4-cell stage. This is different to observations in other species, in particular the cow. In this species 30-45% of cultured oocytes obtained from ovaries without reference to the follicular or luteal phase, or indeed pregnancy, develop to blastocysts in culture, and 50% develop to term when transferred to recipients (Trounson et al, 1996). Pregnancies and births have been obtained in the human from oocytes recovered from ovariectomy specimens (Cha et al, 1991). Pregnancies have also been reported for PCOS patients following aspiration of follicles and their maturation 60

10 in vitro in systems similar to those described in this paper (oocytes matured for 48 h in TCM 199 with 10% fetal calf serum) (Cha et al, 1996). Given the normal births also reported by Trounson et al (1994), Barnes et al. (1995) and Russell et al. (1996) from in-vitro matured oocytes, it is likely that further research will result in improvements in embryo developmental competence that will make this technique an attractive alternative to stimulating ovulation in patients using large doses of FSH. Dramatic improvements already made to the culture of human embryos to the blastocyst stage (Jones et al, 1998), may enable improvements to development of embryos formed from oocytes matured in vitro, but it is also likely that maturation conditions used in vitro are not mimicking those achieved in vivo. The persistent retardation of cleavage and blockage observed during culture are suggestive of defects in cell cycle regulators, yet to date no specific abnormality has been identified in the molecular components of the cell cycle. Examination of oocyte ultrastructure and chromosomal structure and changes during maturation have not revealed any obvious abnormalities. Presently we are examining the pattern of proteins produced during oocyte maturation using two-dimensional gel electrophoresis and proteome analysis, to identify any specific deletions which may explain the present observations of loss of embryo developmental competence. Acknowledgements The studies were supported by a research grant from IntegraMed Inc, Purchase, New York, USA. References Barnes, F.L., Crombie, A., Gardner, D.K. et al. (1995) Blastocyst development and birth after in vitro maturation of human primary oocytes, intracytoplasmic sperm injection and assisted hatching. Hum. Reprod., 10, Barnes, F.L., Kausche, A., Tiglias, J. et al. (1996) Production of embryos from in vryro-matured primary human oocytes. Fertil. Steril, 65, Cha, K.Y., Koo, J.J., Ko, J.J. et al. (1991) Pregnancy after in vitro fertilization of human follicular oocytes collected from non-stimulated cycles, their culture in vitro and their transfer in a donor oocyte program. Fertil. Steril, 55, Cha, K.Y., Chung, H.M., Han, S.Y. et al. (1996) Successful in vitro maturation, fertilization and pregnancy by using immature follicular oocytes collected from unstimulated polycystic ovarian syndrome patients. [Abstr ] In Proceedings of the American Society of Reproductive Medicine, Boston, Nov. 2-6, 1996, p. S23. Collas, P. (1996) Molecular aspects of oocyte maturation. Singapore J. Obstet. Gynaecol., 27, Cummins, J.M., Breen, T.M., Harrison, K.L. et al. (1986) A formula for scoring human embryo growth in in vitro fertilization: its value in predicting pregnancy and in comparison with visual estimates of embryo quality. J. In Vitro Fertil. Embryo Transfer, 3, Dubey, A.K., Wang, H.A., Duffy, P. et al. (1995) The correlation between follicular measurements, oocyte morphology, and fertilization rates in an in vitro fertilization program. Fertil. Steril., 64, Jones, G. and Trounson, A. (1997) In vitro maturation of primary oocytes recovered from polycystic ovaries. In Human Oocytes From Physiology to IVF. Monduzzi Editore, Bologna, Italy, in press. 61

11 A.Trounson et al. Jones, G.M., Trounson, A.O., Gardner, D.K. et al. (1998) Evolution of a culture protocol for successful blastocyst development and pregnancy. Hum. Reprod., 13, Moor, R.M., Trounson, A.O. (1977) Hormonal and follicular factors affecting maturation of sheep oocytes in vitro and their subsequent developmental capacity. J. Reprod. FertiL, 49, Russell, J.B., Knezevich, K.M., Fabian, K. et al. (1996) In vitro oocyte maturation: clinical applicability. [Abstr ] In Proceedings of the American Society of Reproductive Medicine, Boston, Nov. 2-6, 1996, p. S22. Trounson, A., Wood, C, Kausche, A. (1994) In vitro maturation and the fertilization and developmental competence of oocytes recovered from untreated polycystic ovarian patients. FertiL SteriL, 62, Trounson, A.O., Bongso, A., Szell, A. et al. (1996) Maturation of human and bovine primary oocytes in vitro for fertilization and embryo production. Singapore J. Obstet. Gynaecol, 27,

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