Bovine embryo culture in vitro: new developments and post-transfer

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1 Human Reproduction Vol. 15, (Suppl. 5) pp. 59-67, 2000 Bovine embryo culture in vitro: new developments and post-transfer consequences Jeremy G.Thompson1'2 and AJim Peterson Reproductive Technologies Group, AgResearch Ruakura Research Centre, PB 3123, Hamilton, New Zealand Present address: Department of Obstetrics and Gynaecology, The University of Adelaide, The Queen Elizabeth Hospital, Woodville Rd., Woodville S.A. 5011, Australia 2 To whom correspondence should be addressed at Department of Obstetrics and Gynaecology, The University of Adelaide, The Queen Elizabeth Hospital, Woodville Rd., Woodville S.A. 5011, Australia. E-mail: [email protected] The past decade has seen a significant shift away Introduction from co-culture systems for cattle blastocyst Following the birth of Louise Brown in 1978 production. In particular, recent adoption of (Steptoe and Edwards, 1978), the clinical applica- sequential media systems has increased per- tion of mammalian embryo production in vitro formance. However, wholly defined systems, was successfully demonstrated and has grown such as the replacement of albumin with non- extensively to meet the demand that exists from biological macromolecules, fail to reproduce the infertile couples. The basic research and technical nutritive role that this molecule has during development that led to human embryo production development. Cattle blastocysts developed in had been performed using rodents. Somewhat in protein-free medium are metabolically com- contrast, the application of cattle in-vitro embryo promised. A further new concept is the use production (IVP) has been slow compared to that of metabolic inhibitors to stimulate embryo seen in the treatment of human infertility. This development in vitro. Non-toxic levels of NaN3, slow development was due to two reasons. First, 2,4-dinitrophenol or very low oxygen atmo- techniques for the collection and maturation in vitro spheres (2%) significantly increase both the of immature cattle oocytes needed to be developed yield (by -10-20%) and the quality of blasto- (e.g. Staigmiller and Moor, 1984; Sirard and cysts when these treatments are applied during Lambert, 1985). Secondly, there was no reliable in- the peri-compaction period in vitro. Neverthe- vitro culture system that supported in-vitro matured less, there are also negative consequences of and fertilized ova to the blastocyst stage. The latter cattle embryo culture, such as fetal oversize was an absolute necessity, as it had been shown and/or significant post-day 35 fetal loss. We that cattle (and sheep) embryos require to be have recently found that much of this loss is transferred to a synchronized recipient at the appro- due to failure of normal allantoic development within the conceptus. Early fetal development priate site to obtain acceptable post-transfer rates is supported by vascularization within the yolk of development (Moore and Shelton, 1964; Rowson sac, but from day 35 to day 110, loss occurs et al., 1969, 1972). Furthermore, this required a through poor nutrient supply and an inability uterine transfer to take place (either surgically or to remove nitrogenous wastes, leading to fetal non-surgically), as uterine transfer procedures are death around day 35. The cause of disrupted easier and more cost-effective compared to ovi- allantois development has not been identified as ductal transfers. yet, but may share a common 'cause-effect' The advent of co-culture technology, developed mechanism with the fetal oversize syndrome. initially in sheep (Gandolfi and Moor, 1987) and Key words: cattle/embryo culture/fetal loss then applied to cattle (Eyestone and First, 1989), overcame this problem, despite an earlier report European Society of Human Reproduction and Embryology 59

2 J.G.Thompson and A.J.Peterson that a relatively simple, semi-defined medium also tulation, led to reliable, and in some cases supported cattle and sheep embryo development improved, embryo development (Carolan et al, following IVF (Tervit et al, 1972). Nevertheless, 1995, Thompson et al, 1998a). Nevertheless, there despite the development of these techniques, the has been a continuous effort to understand early application of IVP in cattle breeding remains embryo cell biology, coupled with an understanding limited within the commercial sector. There are of the temporal relationship between the reproduct- several reasons for this, including low oocyte ive tract fluid milieu and embryo development recovery rates and poor oocyte quality from oocyte (e.g. Gardner et al, 1996). This has led to the retrieval procedures, low embryo survival to term concept that media components and physical condi- following transfer (e.g. 30-35%) and poor survival tions should be altered during development to the following storage in liquid nitrogen. Furthermore, blastocyst stage (reviewed by Thompson, 1996; for much of this decade, little progress has been Gardner and Lane, 1997). This concept has sub- achieved in improving the proportion of bovine sequently been termed 'sequential' media systems embryos developing in vitro (Thompson and (Gardner and Lane, 1997). In particular, human Duganzich, 1996), with few studies reporting IVF laboratories seeking more robust systems for results of >50% development to blastocysts from human blastocyst culture have championed the cleaved embryos. In this review, we will focus on application of sequential systems (Gardner and progress in two areas: that of in-vitro development Lane, 1997; Gardner et al, 1998), to reduce the of cattle embryos and the pathology of post- need to transfer more than one or two embryos. transfer loss of early fetuses. Both have received Indeed, several human IVF medium manufacturers considerable attention in our laboratories. now market 'sequential' medium systems. For cattle embryos, our laboratory has developed a Sequential medium development sequential medium system for fertilization and The development of more defined embryo culture culture of IVP embryos, known as 'SOF-98' systems has been one of the key achievements in (AgResearch, Hamilton, New Zealand). The per- cattle embryology over the last decade. It is now formance of this new system, based on the develop- generally accepted that although it is an efficient ment of synthetic oviduct fluid (SOF) medium system for embryo production, co-culture is diffi- (Tervit et al, 1972; Gardner et al, 1994) yields cult to improve upon, due to the different inter- improved fertilization and embryo development actions between medium components and the two rates compared to the SOFaaBSA formulation cell types in culture. Furthermore, there is the (Thompson et al, 2000). increased risk associated with transfer of viral and A further development of this concept is the use other sub-cellular pathogens between somatic cells of perfusion culture as the vehicle to introduce and the embryo (reviewed by Bavister, 1995; Leese changes in media composition (Bavister, 1995; et al, 1995, 1998; Thompson, 1997). Over the Thompson, 1996; Gardner, 1998). Although not a past decade, knowledge of the basic cell biology new technology, there has been little requirement of early embryo development and the in-vivo until now for the application of perfusion equip- environment has substantially increased. Initially ment to in-vitro embryo development. The general this led to revised formulations, such as SOFaaBSA principle of perfusion culture is that embryos are (Gardner et al 1994), or new formulations, such held in a chamber through which a medium can as CR1 (Rosenkrans and First, 1994). However, flow either continuously or intermittently. The even these formulations failed to produce consist- benefit of this is that the composition of the ent results and still require the addition of serum medium can be altered with minimal disturbance (as a growth factor 'cocktail') to achieve consistent to the embryos. With the advent of sequential and reliable results (Pinyopummintr and Bavister, medium, the benefits of a perfusion system become 1994; Carolan et al, 1995; Thompson et al, evident. However, the availability of the compon- 1998a). In particular, addition of serum following ents necessary for microperfusion culture is early cleavage, but prior to compaction and blas- extremely limited and led us to 'adapt' commer- 60

3 Bovine embryo culture in vitro cially available equipment to embryo culture, lower in blastocysts resulting from culture in PVA- although such adaptions continue to yield less than supplemented medium, compared to those in vivo optimal results (Lim et al., 1996; McGowan and or cultured in vitro in media supplemented with Thompson, 1997). This has necessitated the devel- either BSA or fetal calf serum (Figure 1; Thompson opment of specialist embryo perfusion compon- et al., 1998b). This was not attributed to a differ- entry, which has been surprisingly difficult ence in protein synthesis rates, but rather the (J.Thompson, personal observation). action of protein uptake via pinocytosis (Thompson et al., 1998b). Cattle blastocysts require albumin This suggested a nutritive role for exogenous Biological media components, such as serum albu- albumin, which we examined by measuring energy min, have been widely used in embryo culture substrate utilization. We observed that blastocyst systems. However, due to their undefined nature stage embryos cultured in PVA medium compared and variability not only in constituents, but also in to BSA medium had considerably higher uptake biological effects on cells and embryos, plus the of the key Krebs cycle substrate, pyruvate, yet a potential risk of cross-infection from contaminated reduced oxygen uptake (Eckert et al., 1998). This biological fluids, much research has been con- result would normally be difficult to explain, as ducted into embryo production using 'defined' oxygen uptake and pyruvate oxidation are usually media (Bavister, 1995) in particular, the use of non- closely correlated. However, in a separate study, proteinaceous macromolecules. Poly vinyl alcohol Lee et al. (1998a) found that oxidation of pyruvate (PVA) has been mooted as a preferred additive, was significantly lower in blastocysts derived from especially as this provides surfactant activity sim- culture in PVA medium compared to BSA medium. ilar to albumin. More recently, this list has been We believe that this demonstrates the importance extended to include glycosaminoglycans, in par- of a further role for pyruvate. Intracellular pyruvate ticular hyaluronic acid (Gardner et al., 1999), is utilized to detoxify NH3 produced by endogenous already known to stimulate cattle embryo develop- protein degradation and amino acid metabolism; ment in vitro (Furnus et al., 1998). However, the resulting alanine may then be transported from evidence from the mouse suggests that albumin the cell. Such a role has been previously reported may have intracellular roles in addition to exogen- for bovine embryos (Partridge and Leese, 1996). ous support roles (e.g. metal ion chelation) (Dungli- Kaye and colleagues at the University of son and Kaye, 1993; Dunglison et al., 1995). Queensland have demonstrated that albumin has a Although albumin is not an absolute requirement significant nutritive role to play during mouse for bovine embryo growth in vitro (Keskintepe embryo development during post-compaction et al, 1995; Eckert et al., 1998), development stages (Dunglison and Kaye, 1993; Dunglison results are generally poorer following in-vitro et al., 1995). It would appear from our data that development in PVA than for albumin-supple- cattle post-compacting embryos also show a similar mented medium (e.g. Eckert et al., 1998; Krisher requirement for protein. Whether albumin can be et al., 1999). Furthermore, few calves have been replaced by a more inert protein molecule, such derived from blastocysts produced in protein-free as casein, will require further experimentation. IVP conditions. We have investigated if the total Above all, however, despite the need for further protein content of IVP cattle blastocysts is affec- research, we believe that the move towards more ted by the presence of protein in the culture 'defined' systems, especially protein-free systems, medium. Our initial examination of total protein must be tempered by the physiological require- content in embryos revealed that during early ments of the embryo during development. cleavage, protein content decreases, followed by an increase during compaction and blastulation Metabolic regulation using inhibitors (Thompson et al., 1998b). Hence, protein degrada- Energy substrate preference during early cleavage tion exceeds protein synthesis during early cleav- of mammalian embryos developing in vitro has age. Furthermore, the total protein content was long been recognized. For example, Brinster 61

4 J.G.Thompson and A.J.Peterson 1000-| b b b b o . a -r .a E 100- Bu) tein content 10- 2 a. \ . PVA BSA PCS- D1 PCS- D5 n vivo Figure 1. Log10 plot histograms of protein content ( SEM) of day 7 blastocysts produced in vitro and incubated in medium supplemented with either: polyvinyl alcohol (PVA); bovine serum albumin (BSA); fetal calf serum (FCS-D1), BSA from day 1-5 of development and FCS for days 5-7 of development. A further group was also included (in vivo): day 7 blastocysts derived in vivo following superovulation and embryo collection. Different superscripts signify significant differences (P < 0.001). (Previously published in Molecular Reproduction and Development. J.G.Thompson et al., 1998b. Reprinted with permission from John Wiley and Sons, Inc., New York.) (1965a,b) demonstrated that glucose and lactate as embryos were cultured in vitro in oxygen levels sole energy substrates were ineffective to support ranging from 0 to 7% O2. Second, peri-compaction early cleavage in the early mouse embryo. How- embryos were cultured in non-toxic levels of the ever, cleavage in vitro will occur in the presence of oxidative phosphorylation inhibitor, sodium azide. pyruvate. Energy substrate preferences of embryos Third, embryos were incubated in the uncoupler from sheep and cattle during in-vitro culture have of oxidative phosphorylation, 2,4-dinitrophenol been well researched over the past decade (e.g. (DNP) (Thompson et al, 2000). All three experi- Javed and Wright, 1991; Rieger et al, 1992a,b; ments yielded significant improvements in embryo Gardner et al, 1993; Eckert et al, 1998). Briefly, development and quality as measured on day 7 of early cleavage is dependent on ATP generation development. Either low O2 levels (2%) or almost entirely from oxidative phosphorylation. 5-10 |imol/l NaN3 (Figure 2) or DNP were found However, as compaction proceeds, there is a shift to be stimulatory. towards a greater contribution to ATP production A similar strategy involving EDTA, but targeted via glycolysis, which coincides with the transition at the inhibition of glycolysis during early develop- from oviduct to uterus, where oxygen availability ment, has also been described (Lane and Gardner, may be a rate-limiting factor (Thompson, 1997). 1997). EDTA was found to assist the development There is also evidence that a difference exists in of 2-cell embryos from mouse strains that would both the level of ATP generated and the proportion normally suffer a culture-induced developmental generated via glycolysis between in-vivo derived ('2-cell') block (Abrumzuk et al, 1977; Mehta and IVP expanded blastocysts in cattle. In-vivo and Kiessling, 1990; Nasr-Esfahini et al, 1992). derived embryos appear to produce less ATP over- For many years it was believed that EDTA seques- all, of which a greater proportion is generated by tered the toxic effects of contaminating heavy glycolysis than IVP expanded blastocysts metal cations, perhaps by inhibiting the production (Thompson, 1997). From such observations, we of reactive oxygen species, catalysed by ions such proposed the hypothesis that facilitating the shift as Fe 2+ and Cu 2+ (e.g. Johnson and Nasr-Esfahini, in ATP production from oxidative phosphorylation 1994). Lane and Gardner (1997) demonstrated that, to glycolysis during compaction and blastulation at a cellular level, EDTA depressed glycolytic rates favours cattle embryo development in vitro. We within pre-compaction mouse embryos, a result tested this hypothesis in three ways. First, day also demonstrated for bovine embryos (Gardner 5-7 (i.e. peri-compaction/blastulation) cattle et al, 1997). These authors believe that in the 62

5 Bovine embryo culture in vitro 10 0 5 10 15 1 NaN3(umoll" ) Figure 2. Development of cleaved bovine embryos to compact morula and blastocyst stages ( ) and grade 1 and 2 compact morula and blastocyst (O) during incubation in SOFaaBSA medium supplemented with NaN3 (0, 5, 10 and 20 uM) from day 5 to day 7 of development. Different letters indicate significant differences (P < 0.05). (Previously published in Journal of Reproduction and Fertility. J.G.Thompson et al., 2000. Reprinted with permission.) mouse, at least, the mechanism of EDTA is via high variability over the incidence reported interna- the intracellular chelation of Mg 2+ , a necessary tionally (Kruip and den Daas, 1997). One reason co-factor for several glycolytic enzymes (Lane and for this is that fetal oversize can partly be attributed Gardner, 1997). The beneficial effect of EDTA to the culture conditions used (Thompson et al, is optimal only when introduced during early 1995). Perhaps of greater concern is the high development, when abnormal rates of glycolysis incidence of early fetal loss following transfer induced by the glucose concentration may com- of cattle IVP embryos also reported by many promise development (Lane and Gardner, 1997). laboratories. We have recently identified, using The use of such direct and indirect inhibitors of serial slaughter of recipients of IVP embryos metabolism to regulate embryo development opens produced in a SOF-based system, that a major cause a wide spectrum of compounds that can be used of fetal loss in the first trimester is malformation of strategically to enhance development in vitro. allantoic development (Peterson and McMillan, Perhaps more importantly, such data demonstrate 1998a,b). This malformation can range from apla- that the way in which embryonic cells produce sia through to apparently normal growth and vascu- ATP is a key regulator of embryonic development. larization but impaired haematopoesis and fetal Post-transfer embryonic loss placental development. Some 25% of IVP con- Pre-elongation culture of ruminant embryos prior ceptuses are affected during allantoic emergence to transfer can yield a number of abnormalities (days 22-34), reducing to 10% by day 70. This manifesting themselves later in development after distribution of affected conceptuses is very close transfer. The best known of these is the so-called to the pattern of embryo and fetal loss during the 'large lamb/calf syndrome, first described in sheep first trimester. In contrast, allantoic growth and by Walker et al. (1992). Other abnormalities development was normal in all control conceptuses include: high neonatal mortality (Walker et al, which resulted from artificial insemination. Growth 1992; Behboodi et al., 1995; Massip et al, 1996), and differentiation of the other extra-embryonic hydro-allantois (van Wagtendonk-de Leeuw et al., membranes, the amnion, yolk sac and trophoblast 1998) and abnormal limb and organ development appeared normal, with the vascularized yolk sac (Walker et al, 1992; Sinclair et al, 1997). How- maintaining fetal development to approximately ever, the phenomenon is not universal, there being day 35 of gestation. The trophoblast expands to 63

6 J.G.Thompson and A.J.Peterson fill both uterine horns with syncytial burrs occur- appeared normal in the yolk sac with a patent ring over the caruncles. vitelline-embryo circulation. This suggests that The phylogeny of the mammalian allantois has despite the same germ cell lineage (endoderm and been well documented (Amoroso, 1953) and allan- mesoderm), there are differing factors influencing toic development in bovine conceptuses after AI differentiation in the two membranes. Certainly (Melton et al., 1951) or natural mating (Greenstein there are marked differences in protein secretory et al., 1958) has been described. Neither reported patterns of the sheep yolk sac and allantois (Lee any malformation in development, further con- et al., 1998b) and recent information comparing firmation that this pathology is confined to the haematopoesis in avian yolk sac and allantois IVP conceptus. There has been very little recent suggests that there are specific haematopoetic pro- information on the growth of the bovine allantois grammes in each of these membranes (Caprioli since these two reports. et al., 1998). The allantois is the last extra-embryonic mem- The results suggest that something associated brane in ruminants to develop and those factors with the in-vitro conditions causes the allantoic that control its emergence from the hindgut of pathology but it is not readily apparent that either the embryo are unknown. Ruminants differ from stage of development or grade of embryo after primates and rodents in having a large fluid filled culture predicts the occurrence of this condition. lumen, whereas the lumen is vestigial in primates Removing antibiotics and phenol red from the and absent in rodents. However, it is the allantoic media has no effect on its occurrence, neither does mesoderm that contributes to the vascular com- shortening the time in culture from seven to five ponent of the placenta in all mammals (Amoroso, days. In fact, in the latter experiments the condition 1953). Surprisingly little consideration has been was exacerbated (Thompson et al., 1999). This given to the ruminant allantois as a haematopoetic suggests that a factor, or factors, is absent or organ. Indeed it has been completely overlooked reduced in the media compared to oviductal and as a possible contributor of haematopoetic stem uterine luminal fluid. Such a suggestion is sup- cells (Al Salami et al., 1985). There is extensive ported by the observation that in-vivo cultured vasculogenesis and haematopoesis in the allantoic bovine embryos (i.e. in sheep oviduct) appear not mesoderm of both sheep and cattle, and in the to suffer the post-day 35 pattern of loss associated former we have identified the early expression of with allantoic malformation (Galli and Lazzari, genes associated with endothelial differentiation 1996). Intriguingly, similar in-vitro culture condi- and P-globin synthesis (Ledgard and Peterson, tions do not seem to affect subsequent development 1998). The avian allantois acquires its endothelial in either sheep or red deer conceptuses, for their network through vasculogenesis. It produces HSC survival remains constant between pregnancy which are capable of colonizing the bone marrow detection and term (Thompson et al., 1995; of the embryo, and the endothelial cells or endothel- Peterson et al, 1997). ial cell precursors from the allantois have an Allantoic malformation leading to placental important role in the development of bone marrow insufficiency is a major cause of the fetal loss after (Caprioli et al., 1998). This suggests that a con- the transfer of the in-vitro produced bovine embryo. sequence of allantoic malformation, especially of Its cause and how it can be rectified remains to be haematopoesis, may affect subsequent bone mar- elucidated. Until it is, the application of cattle IVP row and other fetal and neonatal haematopoetic embryos will continue to produce poor calving organs. Interestingly there has been a recent report results when compared to AI and natural mating. of the death of a neonatal nuclear cloned calf from Furthermore, a link between allantois development severe anaemia, lymphoid aplasia and hypoplastic and fetal oversize has not been made to date, thymus, spleen and lymph nodes (Renard et al., although it is feasible that both phenomena are a 1999). result of the same 'cause-effect' mechanism. Fur- In contrast to the variable pathologies in allantoic ther work is required to understand fully these development, haematopoesis and vasculogenesis intriguing perturbations to in-utero development. 64

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