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REVIEW |
1 Department of Biotechnology, Institute of Farm Animal Genetics, Friedrich-Loeffler-Institute (FLI), Höltystrasse 10, 31535 Neustadt-Mariensee, Germany2 Escuela Superior de Ciencias Agropecuarias, Universidad Autónoma de Campeche, Calle 53 s/n, C.P. 24350 Escárcega, Campeche, México3 Departamento de Genética y Reproducción Animal, Decanato de Ciencias Veterinarias, Universidad Centroccidental ‘Lisandro Alvarado’ (UCLA), Apartado 400, Barquisimeto 3001, Venezuela4 Division of Animal Sciences, School of Biosciences, University of Nottingham, Sutton Bonington Campus, Loughborough, Leicestershire LE12 5RD, UK
Correspondence should be addressed to M A Velazquez; Email: lestaurus_18{at}hotmail.com H Niemann; Email: heiner.niemann{at}fli.bund.de
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Abstract |
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Introduction |
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The effects of IGF1 on ovarian follicular growth and preimplantation embryo development of non-superovulated domestic ruminants have been the subject of a number of reviews (Kaye et al. 1992, Simmen et al. 1993, Spicer & Echternkamp 1995, Wathes et al. 1998, 2003, Watson et al. 1999, Lucy 2000, Kaiser et al. 2001, Khamsi et al. 2001a, Gong 2002, Mihm & Austin 2002, Zulu et al. 2002, Mazerbourg et al. 2003, Sinclair et al. 2003, Webb et al. 2003, Beg & Ginther 2006, Webb & Campbell 2007). Growing evidence has demonstrated the importance of IGF1 for the success of superovulatory treatments (Herrler et al. 1994, O'Callaghan et al. 2000, Cushman et al. 2001, Velazquez et al. 2005). For instance, oocyte quality and embryo viability have been associated with IGF1 concentrations in domestic ruminants undergoing superovulation (O'Callaghan et al. 2000, Velazquez et al. 2005). Moreover, treatments capable of increasing IGF1 concentrations in ovarian follicular fluid of superstimulated donors were related to increased numbers of viable embryos in vivo (Herrler et al. 1994, Cushman et al. 2001).
In this review, we emphasize the link between both local and peripheral IGF1 concentrations and bovine embryo production in vivo by superovulation, and propose new directions for future research, including the possible use of superovulated cattle as an alternative model to investigate reproductive disorders in humans associated with IGF1 concentrations outside the physiological range.
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The IGF superfamily |
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IGF1 is one of two ligands of the IGF family (Hwa et al. 1999, Spicer 2004) and is a small peptide consisting of 70 amino acids with a molecular mass of 7649 kDa (Laron 2001). The established components of the IGF system also include two receptors, six high-affinity IGF-binding proteins (IGFBPs) and IGFBP proteases (Giudice 1995, Hwa et al. 1999, Spicer 2004). Furthermore, another group of low-affinity binding proteins, known as IGFBP-related proteins (IGFBP-rPs), belongs to the IGF family. However, no final nomenclature has been agreed for these proteins, as several research groups have identified the same protein and each group has used a different nomenclature (Hwa et al. 1999, Rosenfeld et al. 2001). Potential receptors for IGFBP(s) and IGFBP-rP(s) have also been reported to be part of the IGF family (Hwa et al. 1999; Table 1). Due to similarities in structure and sharing intracellular signalling cascades with other members of the IGF system, insulin, its receptor and a hybrid insulin/IGF receptor are also considered to be part of the IGF superfamily (Jones & Clemmons 1995, Monget & Martin 1997, McCusker 1998, Poretsky et al. 1999, Butler & Le Roith 2001, Juul 2003).
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Brief overview on the role of IGF1 in non-superovulated cattle |
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The biological significance of IGF1 in ovarian physiology was further demonstrated in an autotransplanted ovarian sheep model in which the ovary is relocated to a site under the skin of the neck. Direct infusion of an IGF1 analogue for 12 h (80–90 µg/h) into the ovarian artery of the conscious animal significantly enhanced the secretion of oestradiol (Scaramuzzi et al. 1999). Spicer et al. (2000) infused IGF1 concentrations closer to the physiological range with osmotic minipumps at a rate of 150 ng/ml per hour for 7 days directly into the ovary. This treatment increased the concentrations of oestradiol and IGF1 in the follicular fluid of small follicles (2–5 mm). Surprisingly, the follicle diameter was increased by IGF1 infusion only in the largest follicle, even though follicular fluid IGF1 concentrations were not altered. This discrepancy was attributed to an increased clearance of IGF1 in large follicles due to lower levels of IGFBPs when compared with small follicles (Spicer et al. 2000). IGFBPs play a pivotal role in the control of IGF1 bioavailability. IGFBPs inhibit the effects of IGF1 possibly by sequestering extracellular IGF1 and thereby limiting access to cell surface receptors. IGFBPs also potentiate IGF1 actions by prolonging its half-life (via protection against degradation), acting as a reservoir to sustain controlled delivery to target cells and facilitating transport from the peripheral circulation to target tissues (Clemmons 1998, Baxter 2000, Firth & Baxter 2002). As evidenced in several studies, high levels of IGFBP2, 4 and 5 were found in bovine follicular fluid from atretic subordinate follicles compared with dominant healthy follicles (Table 2). These three IGFBPs correlate negatively with follicular diameter during antral follicle development (Austin et al. 2001). IGFBP3 is the major circulatory carrier of IGF1 and is predominantly present in dominant follicles (Gradela et al. 1998, Nicholas et al. 2002). The complexity of the IGF system is further illustrated by specific IGFBP proteases described in several species including cattle (Spicer et al. 2004), which enhance the amount of free IGF1 within a follicle despite synthesis of IGFBPs (Mihm & Austin 2002).
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Effects of IGF1 in bovine preimplantation embryo development
The effects of IGF1 on early bovine embryos are mediated by its own receptor (Matsui et al. 1997). Several studies have found IGF1 mRNA in the bovine uterus (Geisert et al. 1991, Robinson et al. 2000, Meikle et al. 2001, Pershing et al. 2002), but not in the oviducts (Viuff et al. 1995, Xia et al. 1996, Pershing et al. 2002). However, other studies have reported that bovine oviductal cells produce IGF1 (Schmidt et al. 1994, Makarevich & Sirotkin 1997, Winger et al. 1997, Pushpakumara et al. 2002). Hence, during the preimplantation period, endocrine and/or paracrine IGF1 may act directly on the embryo or indirectly via modulation of the oviductal and uterine secretions (Wathes et al. 1998, 2003, Velazquez et al. 2008a).
Direct effects of IGF1 on in vivo embryo viability in non-superovulated cattle have not yet been demonstrated. A positive effect of IGF1 on embryogenesis has been proposed by the studies in which improved bovine embryo production in vitro was found after IGF1 supplementation in the concentrations ranging from 10 to 200 ng/ml (Herrler et al. 1992, Matsui et al. 1997, Palma et al. 1997, Prelle et al. 2001, Byrne et al. 2002a, Makarevich & Markkula 2002, Moreira et al. 2002a, Sirisathien & Brackett 2003, Sirisathien et al. 2003, Lima et al. 2006, Stefanello et al. 2006, Velazquez et al. 2008b). The beneficial effects of IGF1 were visible as decreased apoptosis and increased total cell number in preimplantation embryos (Byrne et al. 2002b, Makarevich & Markkula 2002). In bovine preimplantation embryos IGF1 stimulates cell proliferation through the mitogen-activated protein kinase signalling cascade, while the anti-apoptotic actions are mediated via the phosphatidylinositol 3-kinase (P13K)/AKT1 (also known as protein kinase B) pathway (Jousan & Hansen 2007, Jousan et al. 2008). IGF1 blocked the induction of apoptosis in bovine embryos exposed to heat shock in vitro, suggesting a protective role against embryonic stressors (Jousan & Hansen 2004, 2007, Jousan et al. 2008). Similarly, IGF1 improved embryo development, cell proliferation and embryo diameter in rabbit embryos exposed to uv radiation (Herrler et al. 1998). In mouse embryos, the detrimental effects of oxidative stress induced by hydrogen peroxide could be alleviated by the addition of IGF1 to the culture medium (Kurzawa et al. 2002, 2004). Rodent embryos were protected against specific apoptosis inducing factors such as tumour necrosis factor-
, camptothecin or actinomycin D by supplementation of the culture media with IGF1 (Byrne et al. 2002b, Fabian et al. 2004, Glabowski et al. 2005). Pregnancy rates were increased after transfer of in vitro-produced cattle embryos treated with IGF1, showing a substantial improvement of the embryonic developmental capacity (Block et al. 2003, Block 2007, Block & Hansen 2007). However, IGF1 cannot overcome the negative effects following cryopreservation (Willemsen et al. 1995, Hernandez-Fonseca et al. 2002). It should also be noted that some authors did not find the beneficial effects of IGF1 treatment during in vitro production of bovine embryos (Flood et al. 1993, Lee & Fukui 1995, Quetglas et al. 2001, Hernandez-Fonseca et al. 2002, Block et al. 2008). Differences in culture media, protein supplementation and the concentrations of IGF1 utilised might explain these contrasting results.
Recent data indicate that IGF1 affects the physiology of the bovine embryo by altering the relative abundance of developmentally important mRNA transcripts, including desmocollin II, Na/K-ATPase, BAX, IGF1 receptor, IGFBP3 and heat shock protein 70. Furthermore, these gene expression changes may occur without detectable changes in cell number, apoptosis and the ratio between inner cell mass and trophectoderm cells (Block et al. 2008).
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Effects of IGF1 in bovine superovulatory treatments |
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During superovulation, IGF1 changes in plasma are also mediated primarily through oestradiol (Kuehner et al. 1993). Oestradiol stimulates IGF1 secretion in the liver (Richards et al. 1991), via an increase in the number of GH receptors (Enright et al. 1994). Changes in IGF1 concentrations might depend on the magnitude of the increment in oestradiol, which in turn will depend on the superovulatory response, i.e. the number of gonadotrophin-active follicles responding to the superstimulatory treatment. Indeed, a higher number of corpora lutea was observed when peripheral IGF1 concentrations were affected by superovulation (Kuehner et al. 1993) compared with unchanged IGF1 concentrations (Herrler et al. 1994, Cushman et al. 2001).
Paracrine IGF1 production
Studies on IGF1 production in bovine oviducts and uterus during superovulation have not been reported. Analysis of gene expression and determination of concentrations in oviductal and uterine fluids would be critical for understanding embryo–hormonal milieu interactions. This information will be valuable for the development of improved culture conditions during in vitro embryo production, especially for humans undergoing superovulation during in vitro fertilization–embryo transfer (IVF-ET) cycles, where the same individual acts as donor and recipient.
Effect of IGF1 during superovulation on follicular development and oocyte quality
The variability within and between animals in both the number of follicles that are stimulated and the number that ovulate is the limiting factor for the success of ET programmes (Adams 1994, Kanitz et al. 2002, Mapletoft et al. 2002, 2006). The number of gonadotrophin-responsive follicles present in both ovaries at the start of a superovulatory treatment is important to achieve a satisfactory superstimulatory response (González-Bulnes et al. 2003). In superstimulated animals the preovulatory LH surge occurs earlier, which is associated with a lack of time for the follicles to acquire adequate maturation and thus to ovulate (D'Occhio et al. 1999). This indicates that oocytes with a proper maturational period during superovulation could yield more viable embryos. IGF1 accelerates the meiotic progress of bovine oocytes in small (
3 mm) follicles (Sakaguchi et al. 2000, 2002) and more viable embryos can be obtained in sheep (Veiga-Lopez et al. 2005) and cattle (Ireland et al. 2007) when a greater population of follicles around 3 mm in size is present at the time of stimulation. Accordingly, increments in blood IGF1 concentrations induced by bST treatment have been associated with increased numbers of follicles between 2 and 5 mm in diameter (Gong et al. 1991, 1993a, 1997, De la Sota et al. 1993). This treatment was also effective in increasing the superovulatory response in cattle (Gong et al. 1993b, 1996, Herrler et al. 1994). Statistically significant increases in ovulation rate in terms of numbers of corpora lutea and embryo viability due to bST treatment have been found in some, but not all studies (Table 3). Variability between experiments could be related to several factors including the dose of bST, method of ovarian examination, type and dose of gonadotrophin, and both number and body condition of animals used in such studies. The effect of bST has been suggested to be mediated through GH, IGF1 and insulin acting either separately or in synergy (Gong et al. 1993b).
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It has been hypothesized that elevated intraovarian IGF1 levels are associated with enhanced follicular growth, but that these could be detrimental to oocyte maturation in growing follicles (Armstrong et al. 2003). Indeed, higher levels of follicular IGF1 in superovulated ruminants have been associated with abnormal oocyte morphology (O'Callaghan et al. 2000). Likewise, in vitro treatment with high IGF1 concentrations did increase follicular size (Walters et al. 2006), but higher IGF1 exposure induced smaller oocytes in treated follicles (McCaffery et al. 2000). Development to the morula and blastocyst stages is positively associated with oocyte diameter (Arlotto et al. 1996). Failure of the oocyte to reach a proper size coincides with the inability to undergo meiotic maturation and increased frequency of polyspermic fertilization (Fair et al. 1995, Otoi et al. 1997). The potentially deleterious action of high IGF1 levels on oocyte competence has been demonstrated in women, where low concentrations of IGF1 in the follicular fluid of patients undergoing superovulation were correlated with successful early embryo development (Wang et al. 2006). Albeit speculative, this inverse relationship between oocyte competence and high intrafollicular IGF1 concentrations might be related to the fact that when more ovulations occur during superovulation less viable embryos are produced (Driancourt 2001, Ireland et al. 2007). In this regard, it is worthy to mention that higher levels of intrafollicular IGF1 were observed after the use of FSH when compared with human menopausal gonadotrophin (hMG; Fried et al. 1998, Hammadeh et al. 2000), indicating that the intrafollicular concentrations of IGF1 can be affected by the type of hormone used for superstimulation. Bovine superovulation has been induced with FSH extracted from either porcine, ovine or equine pituitaries (Staigmiller et al. 1992, Kanuya et al. 1997), eCG (Gonzalez et al. 1994), hMG (Lauria et al. 1982), recombinant bovine FSH (Wilson et al. 1993) or recombinant human FSH (Takagi et al. 2001). Notwithstanding, the effect of different gonadotrophin preparations upon intrafollicular IGF1 concentrations has not yet been studied in cattle.
The other ligand of the IGF system, IGF2, is also increased in the follicular fluid by superovulation, and has been associated with decreased oocyte quality (O'Callaghan et al. 2000). In superstimulated women, high follicular concentrations of IGF2 were positively related to oocyte maturation and early embryo development (Wang et al. 2006). By contrast, the intrafollicular microenvironment of IGF2 was not associated with clinical outcome in the patients subjected to IVF-ET cycles (Choi et al. 2006). However, studies on the role of IGF2 during bovine superovulation are lacking.
Oocyte maturation has been positively associated with follicular fluid levels of IGF1 in women undergoing ovarian superstimulation (Nardo et al. 2001). IGF1 levels in follicular fluid compatible with bovine oocyte competence are modulated to a great extent by IGFBPs (Nicholas et al. 2005). It has been observed that the amount of IGFBP2, 4 and 5 in the follicular fluid of follicles >8 mm from cows superstimulated with eCG was less compared with that of medium-sized follicles, and that IGFBP3 was present in all follicles (van de Leemput et al. 1997). FSH-stimulated cows had less IGFBP2 and relatively constant levels of IGFBP3 in large oestrogen-active follicles (
17 mm or greater) compared with large oestrogen-inactive (12–14 mm), medium (5–7 mm) and small follicles (4 mm; Echternkamp et al. 1994). Superovulated ewes had lower concentrations of IGFBP2, 4 and 5 than non-superovulated controls in follicular fluid from follicles 
3 mm (O'Callaghan et al. 2000). In a model of follicular co-dominance induction, treatment with 2–6 mg recombinant bovine FSH for 36–48 h decreased the amounts of IGFBP2, 4 and 5, and increased levels of IGFBP3 and IGFBP proteases 4 and 5 in the follicular fluid of co-dominant follicles (9–12 mm) compared with subordinate follicles (7–9 mm; Rivera & Fortune 2001, 2003). Although these findings partially suggest that the action of the IGFBP system during superovulation operates in a manner similar to non-superovulated conditions, more work is required to further elucidate the role of IGFBPs in follicular development during bovine superovulatory treatments.
Effects of IGF1 during superovulation on preimplantation embryo development
The main objective of a superstimulatory treatment is to obtain the maximum number of viable embryos with a high probability of producing pregnancies. Although the best indicator of the success of an ET programme is the number of live calves born per donor over a given period of time (Armstrong 1993), the number of viable embryos produced per donor is frequently used as an indicator of MOET success (Peixoto et al. 2002). Embryo viability in the MOET programmes is not only affected by the ovulation rate but also depends critically on whether normal fertilization occurs (Armstrong 1993) and the oviductal and uterine milieu in which the embryo develops prior to embryo recovery (Barnes 2000).
The IGF1 receptor mediates the effects of IGF1 during the preimplantation period (Matsui et al. 1997). Day 7 bovine embryos collected from superovulated animals express the IGF1 receptor (Bertolini et al. 2002, Moore et al. 2007). Receptors for IGF1 are also observed in embryos produced either partially (Lazzari et al. 2002, Lonergan et al. 2003) or totally by standard in vitro procedures (Watson et al. 1992, Yoshida et al. 1998, Yaseen et al. 2001, Lazzari et al. 2002, Moore et al. 2007) or by somatic cell nuclear transfer (Sawai et al. 2005, 2007, Moore et al. 2007). In vitro procedures can alter the relative abundance of IGF1 receptor transcripts in bovine embryos (Bertolini et al. 2002, Lazzari et al. 2002, Sawai et al. 2005, 2007, Warzych et al. 2007). Preimplantation embryos collected from superovulated cows have shown either high (Bertolini et al. 2002), low (Lazzari et al. 2002, Sawai et al. 2007) or similar (Moore et al. 2007) transcript abundance when compared with in vitro-produced embryos. It is unknown whether or not differences exist between embryos derived from single spontaneous ovulations and stimulated multiple ovulations, with regard to the expression of the IGF1 receptor.
Convincing evidence has demonstrated that IGF1 can affect positively embryos from superovulated cattle. Improvements in embryo production have been achieved by treating superovulated donors with bST (Gong et al. 1993b, 1996, Herrler et al. 1994, Cushman et al. 2001, Moreira et al. 2002b, Neves et al. 2005), which was associated with increments in IGF1 concentrations in follicular fluid and peripheral plasma (Herrler et al. 1994, Cushman et al. 2001). Since bST also exerts direct effects on several reproductive events, including embryogenesis (Kaiser et al. 2001, Sirotkin 2005), a complementary effect of bST and IGF1 cannot be ruled out. Support for a beneficial action of IGF1 on embryonic development during superovulation can be derived from the positive correlation found between the plasma concentrations of IGFI and the number of viable embryos produced by superovulated mature cows (Velazquez et al. 2005). Insulin is closely linked with IGF1 during superovulation as shown by the greater diameter of large follicles and increased levels of IGF1 in the follicular fluid induced with exogenous application of insulin during the period of gonadotrophin treatment (Simpson et al. 1994). Both hormones were found to be closely related with body condition score (BCS) and embryo production in superovulated cows (Velazquez et al. 2005; Table 4).
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Experiments in rodents found that locally enhanced IGF1 production in the uterus during a superovulatory treatment can be detrimental to early embryo development. This increase in IGF1 production is thought to be due to the hyperoestrogenaemia caused by superovulation, as uterine IGF1 production is primarily regulated by oestrogens (Murphy et al. 1987, Simmen et al. 1990, Sahlin et al. 1994, van Lier et al. 2006, Suzuki et al. 2007). Katagiri et al. (1996) reported a decrease in both the rate of blastocyst formation and blastocyst cell number, and an increased proportion of degenerated blastocysts after culturing eight-cell embryos with uterine luminal fluids isolated from rat uteri infused with IGF1, thus mimicking IGF1 concentrations caused during superovulation. The same results were obtained with uterine luminal fluid from superovulated animals, and even more interesting, a reversed trend was observed in both models (superovulation and IGF1 infusion) when the uterine fluids were treated with anti-IGF1 antibody (Katagiri et al. 1996). The same rat model was applied in a study in which an altered uterine electrolyte environment, especially cations, was suggested to be partially responsible for the detrimental effects of IGF1 on embryonic development after superovulatory treatment (Katagiri et al. 1997a). Recent studies have reported that exposure of mice embryos at the two- or four-cell stage to high IGF1 concentrations (950 ng/ml) triggered apoptosis in blastocysts via downregulation of the IGF1 receptor (Chi et al. 2000), which in turn increased embryo resorption rates (Pinto et al. 2002, Eng et al. 2007). It has been suggested that this high IGF1 induced apoptosis in embryos associated with reduced IGF1 receptor signalling requires activation of the TP53 pathway (Moley et al. 2005). However, extrapolation of the results from rodents to cattle needs to be done with caution. The downregulation of the IGF1 receptor found in bovine embryos treated with IGF1 concentrations considered beneficial for embryogenesis (100 ng/ml; Prelle et al. 2001) highlights the importance of species-specific differences on the detrimental effects of IGF1 upon embryonic development.
Partial evidence for an adverse effect of IGF1 in vivo was found in superovulated maiden heifers in which a negative correlation between embryonic viability and plasma concentrations of IGF1 was observed (Velazquez et al. 2005). The concentrations of IGF1 in blood are higher in heifers than in cows (Wathes et al. 2001, Velazquez et al. 2004). Therefore, both high endogenous concentrations and the superovulatory gonadotrophins might elevate IGF1 concentrations in both oviduct and uterus to a level that is suboptimal for embryonic development (Figs 1 and 2). The potential deleterious effects of high concentrations of IGF1 on embryo viability are also partially supported by studies in non-superovulated cows in which a decrease in pregnancy rates was attributed to the hyperstimulation of IGF1 production induced by bST treatment (Bilby et al. 2004).
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Modulation of the IGF system to improve results of superovulation in cattle |
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The use of exogenous IGF1 to enhance in vivo embryo production in superovulated cows has not yet been tested. This approach could be useful to improve embryo yields in animals with reduced superovulatory response. Reliable methods for the prediction of embryo production in donor animals would be helpful in improving the outcome in the MOET programmes. Total plasma IGF1 concentrations have been found to be of limited value for the prediction of the number of viable embryos (Velazquez et al. 2005). Measuring the concentrations of circulating IGF1 and IGFBPs in combination could improve the prediction of the number of viable embryos. This is supported by the fact that mouse embryos cultured in medium supplemented with dephosphorylated IGFBP1 in the form of an IGF1/IGFBP1 complex showed a higher increase in the rate of blastocyst formation compared with supplementation with IGF1 alone (Lin et al. 2003). The ratio of IGF1 and IGFBP1 in serum and follicular fluid has been suggested to reflect oocyte quality, which in turn influences embryo viability (Fried et al. 2003).
Stimulatory gonadotrophin treatments can also affect gamete transport in the oviductal–uterine tract and the fertilization process (Greve & Callesen 2001). IGF1 has been found in bovine seminal plasma and its receptor was present in ejaculated bovine sperm, indicating that it might play an important role during fertilization (Henricks et al. 1998, Hoeflich et al. 1999). In vitro studies have shown that treatment with IGF1 increased important characteristics of bovine spermatozoa, including the percentage of motile sperm and straight-line velocity (Henricks et al. 1998, Lackey et al. 1998). Significant fluctuations in the oviductal IGF1 concentrations have been found in superovulated ruminants (Kakar et al. 2005). However, the effects of different IGF1 concentrations in oviducts during superovulatory treatments on sperm viability and fertilization success have not yet been studied.
Although IGF1 ligand expression in the preimplantation stage has been proposed as a potential marker for embryo quality in humans and mice (Liu et al. 1997, Kowalik et al. 1999), the autocrine role of IGF1 in bovine embryogenesis has not been fully elucidated. Some studies have reported expression of the IGF1 ligand in bovine embryos during the preimplantation period (Schultz et al. 1992, Yoshida et al. 1998, Lonergan et al. 2000), while others did not find the molecule (Yaseen et al. 2001, Bertolini et al. 2002, Moore et al. 2007, Warzych et al. 2007). Nevertheless, it would be useful to determine whether oestradiol concentrations, associated with the superovulatory response, do induce expression of the IGF1 ligand in embryos, as has been observed in some types of brain cells (Shingo & Kito 2003).
It has been speculated that the high rates of embryonic mortality observed in dairy cows with severe negative energy balance could be due to impaired embryo development caused by increased signalling of IGF2 in the oviduct (Fenwick et al. 2008). Since IGF2 is produced in oviducts and uterus and both the ligand and the receptor are expressed from the zygote to the blastocyst stage (Yaseen et al. 2001), the interaction between IGF2 and preimplantation embryo development in superovulated cattle warrant future research.
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The superovulated bovine female as an alternative model to investigate reproductive endocrinological disorders associated with IGF1 in humans |
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 TopAbstractIntroductionThe IGF superfamilyBrief overview on the...Effects of IGF1 in...Modulation of the IGF... The superovulated bovine female... ConclusionsDeclaration of interestAcknowledgementsReferences |
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As discussed above, high IGF1 concentrations associated with high superovulatory response may exert detrimental effects on oocyte and early embryo development in stimulated cattle. This raises the interesting possibility of producing high superovulatory profiles in domestic cattle, aiming at mimicking a polycystic-like ovarian milieu. This could be useful to develop strategies to enhance oocyte competence in order to improve the outcome of IVF-ET cycles in women with PCOS. Alternatively, this bovine model could be used to test the efficacy and/or to determine the method of action of drugs used for the treatment of PCOS, both in vivo and in vitro. Support for this hypothesis comes from in vitro studies recently carried out to investigate the effect of metformin on bovine ovarian steroidogenesis in response to IGF1 and FSH (Tosca et al. 2007). This drug is used for fertility treatment in women with PCOS (Palomba et al. 2008). Moreover, the use of artificial insemination in this bovine PCOS model could also be a valuable approach to study the fertilization success and preimplantation embryo development in vivo, with the goal of designing therapies to increase the chance of pregnancy in PCOS women.
Patients with PCOS that are stimulated in assisted reproduction cycles have an increased risk of developing the ovarian hyperstimulation syndrome (OHSS; Mikkelsen 2005, Tummon et al. 2005). Treatments leading to reduced IGF1 levels in blood of PCOS patients are associated with a decrease in ovarian stromal blood flow, which in turn is related to a lower likelihood of developing the OHSS (Amin et al. 2003). OHSS could also be investigated in the superovulated bovine model. For instance, after inducing a PCOS-like status by superovulation, animals developing multiple ovarian cysts (Todoroki et al. 2004) could be retreated with gonadotrophins in an attempt to mimic the conditions observed in humans. Another condition possibly associated with IGF1 is the low ovarian response after stimulation with gonadotrophins. Women with a poor response to ovarian stimulation have shown either similar (Hammadeh et al. 2003) or reduced levels of IGF1 in the follicular fluid (Bahceci et al. 2007) compared with good responders. Superovulated cattle could prove to be a superior approach to unravelling the underlying cause of this condition, as shown recently by Ireland et al. (2007). The feasibility of inducing these two contrasting superovulatory responses observed in women (OHSS and low ovarian response) is further supported by the fact that similar superovulatory profiles have been found in cattle, ranging from low to high responders (De Roover et al. 2005, Durocher et al. 2006).
Human polycystic ovaries have been shown to have a significantly reduced proportion of primordial follicles and an increased proportion of primary follicles compared with normal ovaries (Webber et al. 2003). It has been proposed that abnormal preantral folliculogenesis observed in polycystic ovaries is at least partially due to an excessive androgen exposure during the prenatal period (Forsdike et al. 2007). In primates, this androgen-induced ovarian follicular growth is thought to be mediated by an enhanced local IGF1 effect (Vendola et al. 1999). The accelerated progression of primordial follicles into the primary stages of development found in a prenatally androgenized sheep model is strikingly similar to the situation observed in women with PCOS (Forsdike et al. 2007). This model could be easily applied to cattle as both species have similar reproductive patterns (Campbell et al. 2003) and androgenization of cows is a well-established procedure in the cattle industry (Nix et al. 1998). Moreover, prenatally androgenized heifers used in a model to increase beef production showed higher body fat accumulation, higher serum IGF1 concentrations and a tendency for increased insulin levels compared with controls (Aldrich et al. 1995, 1996, Reiling et al. 1997). These features are largely similar to some characteristics of PCOS such as obesity and altered components of the IGF system (Chang 2007, Cocksedge 2008, Franks et al. 2008). Refinement of the bovine prenatal PCOS-like model will primarily relate androgen doses and timing of application during pregnancy. The assessment of the developmental competence of oocytes, both in vivo and in vitro, from adult superovulated cattle exposed to high androgens during foetal development may be relevant to the study of in utero programming of PCOS aetiology. The preantral stage last approximately 3 months in cattle (Webb & Campbell 2007), and the environment to which preantral oocytes are exposed during this period could potentially affect future oocyte competence. This has been shown by Adamiak et al. (2005) in a non-superovulated cattle model, in which nutritional-induced hyperinsulinaemia, similar to the high insulin concentrations present in PCOS, during three consecutive oestrous cycles induced a detrimental effect on oocyte developmental competence in vitro. It would be interesting to analyse the IGF system in the reproductive tract using this hyperinsulinaemic model, in conjunction with superovulation, to further explore embryo–maternal interactions under PCOS-like conditions.
Creation of a ‘universal’ PCOS animal model is unlikely, as the induction of all pathological conditions observed in PCOS women is not possible (Szukiewicz & Uilenbroek 1998, Singh 2005). Common clinical features of PCOS include polycystic ovaries, anovulation, hyperinsulinaemia, hyperandrogenism and hypersecretion of LH (Chang 2007, Cocksedge 2008, Franks et al. 2008). Still, the ultimate diagnostic criterion for PCOS is controversial and several phenotypes have been proposed. For instance, a patient with anovulation and polycystic ovaries but with no clinical or biochemical evidence of androgen excess can be diagnosed as having PCOS (Norman et al. 2007). Development of a suitable animal model critically depends on the PCOS-related disorder to be investigated (Szukiewicz & Uilenbroek 1998). Although the model for prenatal exposure of androgens is hypothetical in cattle, some clinical conditions present in PCOS have been observed in cows, including polycystic ovaries, anovulation (Todoroki & Kaneko 2006) and hyperinsulinaemia (Adamiak et al. 2005).
Since the increase in uterine IGF1 concentrations following superovulation is related to hyperoestrogenaemia (Katagiri et al. 1997b), and high uterine maternal levels of oestrogen and IGF1 are linked to endometrial cancer (Schernhammer 2002, Moyano & Rotwein 2004), models to study uterine cancer development could also be created in superovulated cattle. This might be accomplished by the combined use of oestrogen implants and gonadotrophin stimulation, which could be applied as a chronic intermittent treatment monitored over the years. The suitability of this model, with regard to long-term monitoring and induction of neoplastic tumours, is supported partially by the current use of domestic cattle for the study of reproductive aging in women (Malhi et al. 2005, 2006) and the documentation of tumours in the bovine reproductive tract (García-Iglesias et al. 1991, 1995, Pérez-Martínez et al. 2001).
Cattle models are especially relevant as procedures that are rarely applied in women can be carried out more frequently in cattle, including intrafollicular drug treatments (Oropeza et al. 2004, 2006), interfollicular oocyte transfer (Bergfelt et al. 1998), intrafallopian transfer of gametes (Wetscher et al. 2005) and oviductal recovery and transfer of early embryos (Besenfelder & Brem 1998, Besenfelder et al. 2001). Valuable data could also be obtained with this experimental approach, especially when using in vivo collection and monitoring techniques presently used in women and already validated in cattle, such as cytology (Kasimanickam et al. 2004) and biopsy (Katagiri & Takahashi 2004) of endometrial tissue and reproductive ultrasound techniques (Rajamahendran et al. 1994, Ribadu & Nakao 1999, Miyamoto et al. 2006, Oropeza et al. 2006). Moreover, several variables such as nutrition, age, health and parity can be precisely controlled in cattle populations.
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Conclusions |
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Declaration of interest |
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Funding |
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Acknowledgements |
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Received August 21, 2008
First decision October 8, 2008
Accepted November 21, 2008
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