Timing and dependence upon mitogen-activated protein kinase

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1 Growth Hormone & IGF Research 21 (2011) 107111 Contents lists available at ScienceDirect Growth Hormone & IGF Research j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / g h i r Timing and dependence upon mitogen-activated protein kinase signaling for pro-developmental actions of insulin-like growth factor 1 on the preimplantation bovine embryo A.Q.S. Bonilla, M. Ozawa, P.J. Hansen Department of Animal Sciences, University of Florida, Gainesville, FL 32611-0910, USA D.H. Barron Reproductive and Perinatal Biology Research Program, University of Florida, Gainesville, FL 32611-0910, USA a r t i c l e i n f o a b s t r a c t Article history: Insulin like growth factor-1 (IGF1) increases the proportion of embryos that develop to the blastocyst stage. Received 14 December 2010 The objective of the present study was to determine whether the pro-developmental actions of IGF1 are Received in revised form 5 February 2011 exerted before or after Day 4 of development (i.e., on events occurring through the period of genomic Accepted 7 March 2011 activation versus events coincident with compaction and blastocoel formation) and whether mitogen- Available online 1 April 2011 activated protein kinase (MAPK) signaling pathways mediate effects of IGF1. Treatment with IGF1 increased Keywords: the proportion becoming blastocysts at concentrations of 10, 100 and 200 ng/mL, with 100 ng/mL being more Embryo effective than 10 or 200 ng/mL. At Day 8, the percent of oocytes that became blastocysts was 30, 34, 43, and Development 36%, respectively (SEM = 2.6). As compared to controls (30.4%), IGF1 increased the percent of oocytes that MAPK were blastocysts at Day 8 when added from Days 4 to 8 (42%) or Days 0 to 8 post-insemination (40%) but there IGF1 was no signicant effect when IGF1 was added from Days 0 to 4 (37%; SEM = 2.2). Actions of IGF1 to increase blastocyst development were reduced when embryos were co-treated with the MAPK inhibitor PD98059. The percentage of oocytes becoming a blastocyst at Day 8 was 21 versus 37% for 0 and 100 ng/mL in the absence of inhibitor and 24 versus 29% in the presence of inhibitor (IGF1 inhibitor interaction, P b 0.05; pooled SEM = 1.3). In conclusion, IGF1 promotes development to the blastocyst stage by regulating MAPK-dependent events at Day 4 or later of development. 2011 Growth Hormone Research Society. Published by Elsevier Ltd. All rights reserved. 1. Introduction include vascular endothelial growth factor [3], epidermal growth factor [4], colony stimulating factor 2 [57], leukemia inhibitory factor Proper development of the embryo is dependent upon maternal [7] and interleukin-1 [8]. The mechanisms by which embryonic signals. While embryos can grow in simple dened media, the pattern development is improved by these factors are not known. Effects on of development can be disrupted. In the cow, for example, in vitro the proportion of embryos that develop to the blastocyst stage could produced embryos suffer from a variety of morphological and be caused by stimulation of cell proliferation, inhibition of apoptosis molecular abnormalities and competence of the resultant embryo to and embryo arrest, or promotion of key events such as maternal RNA survive freezing or transfer into recipients is reduced compared to degradation, embryonic genome activation, compaction and blasto- embryos produced in vivo [1,2]. An absence of maternal signals is coel formation. responsible for some of the problems inherent in embryos produced Here we evaluated how one growth factor capable of regulating in vitro because these embryos can be made more similar to embryos embryonic development, insulin-like growth factor-1 (IGF1), produced in vivo if embryos are returned to the oviduct after in vitro increases the proportion of embryos that develop to the blastocyst fertilization [2]. stage. Insulin-like growth factor-1 is mainly produced in the liver Growth factors and cytokines that can affect embryonic develop- upon stimulation by growth hormone [9] although some local ment have been identied in a variety of species. In the cow, these synthesis in the oviduct, endometrium and embryo has been reported [1014]. Signaling is transmitted through several intracellular path- ways with many of the proliferative actions of IGF1 being mediated through activation of the mitogen-activated protein kinase (MAPK) pathway [15]. Treatment with IGF1 can increase the proportion of Corresponding author at: PO Box 110910, Department of Animal Sciences, University of Florida, Gainesville, FL 32611-0910, USA. Tel.: +1 352 392 5590; fax: +1 352 392 embryos becoming blastocysts in several species including the bovine 5595. [11,16,17]. Insulin-like growth factor-1 also improves resistance of E-mail address: [email protected] (P.J. Hansen). bovine preimplantation embryos to heat shock [1820] and oxidative 1096-6374/$ see front matter 2011 Growth Hormone Research Society. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.ghir.2011.03.003

2 108 A.Q.S. Bonilla et al. / Growth Hormone & IGF Research 21 (2011) 107111 stress [21], alters expression of several genes at the blastocyst stage with mineral oil. Embryos were cultured at 38.5 C in an atmosphere [22] and improves embryo survival after transfer into heat-stressed of 5% CO2 in humidied air. recipients [6,23]. Specic objectives of the current study were to determine whether 2.3. Concentration-dependent actions of IGF1 to increase blastocyst the pro-developmental actions of IGF1 in culture of in vitro produced development embryos are exerted before or after Day 4 of development (i.e., on events occurring through the period of genomic activation versus Following fertilization, embryos were washed and cultured in events coincident with compaction and blastocoele formation) and 50 L of SOF-BE1 (control), or SOF-BE1 containing 10, 100, or 200 ng/ whether MAPK signaling pathways mediate pro-developmental mL IGF1. Concentrations were chosen so that the second concentra- effects of IGF1. tion was within the range of values for IGF1 in blood of lactating cows [26,27]. The percentage of oocytes that cleaved (2 cell) was observed at Day 3 after insemination (~72 h post-insemination) and 2. Materials and methods the percentage of embryos that became blastocyst was observed at Day 7 (168 h) and Day 8 (192 h) post-insemination. The experiment 2.1. Materials was replicated 4 times using 231 to 284 oocytes per group. Unless otherwise mentioned, reagents were purchased from 2.4. Determination of the stage of development at which IGF1 acts to Sigma-Aldrich (St. Louis, MO, USA) or Fisher Scientic (Pittsburgh, increase blastocyst development PA, USA). HEPES-Tyrodes Lactate (TL) and IVF-TL solutions were purchased from Caisson (Sugar City, ID, USA) and used to prepare This experiment tested whether IGF1 improves developmental HEPES-Tyrodes albumin lactate pyruvate (HEPES-TALP), and IVF- competence by acting from Days 0 to 4 (696 h) post-insemination TALP as previously described [24]. Oocyte collection medium (OCM) (i.e., on events occurring through the period of genomic activation at was tissue culture medium-199 (TCM-199) with Hanks salts without the 816 cell stage) or from Day 4 (96 h) to Day 8 (192 h) post- phenol red (HyClone, Logan, Utah, USA) supplemented with 2% (v/v) insemination (i.e., coincident with compaction and blastocoele bovine steer serum (Pel-Freez, Rogers, AR) containing 2 U/mL formation). Following fertilization, putative zygotes were washed heparin, 100 U/mL penicillin-G, 0.1 mg/mL streptomycin, and 1 mM and assigned to one of four treatments: control, IGF1 from Days 0 to glutamine. Oocyte maturation medium (OMM) was TCM-199 (Gibco, 8 (6192 h) post-insemination, IGF1 from Days 0 to 4 (696 h) post- Invitrogen, Grand Island, NY, USA) with Earle's salts supplemented insemination or IGF1 from Days 4 to 8 post-insemination. Embryos with 10% (v/v) bovine steer serum, 2 g/mL estradiol 17-, 20 g/mL were placed in groups of 30 in 50 L microdrops of SOF-BE1 bovine follicle stimulating hormone (Folltropin-V; Bioniche, London, containing 0 or 100 ng/mL IGF1 at Day 0 (0 h, time of insemination). ON, Canada), 22 g/mL sodium pyruvate, 50 g/mL gentamicin sulfate, The concentration of IGF1 used was based on the fact that it produced and 1 mM glutamine. Percoll was from GE Healthcare (Uppsala, optimal effects on development in the rst experiment. For all Sweden). Frozen semen from various bulls was donated by South- treatments, embryos were washed at Day 4 (96 h) and transferred to eastern Semen Services (Wellborn, FL, USA). The embryo culture fresh medium containing SOF-BE1 100 ng/mL IGF1. The percent of medium was Synthetic Oviduct Fluid-Bovine Embryo 1(SOF-BE1) oocytes that cleaved was assessed at Day 4 (96 h) post-insemination [25]. The MAPK kinase inhibitor, PD 98059, was from Sigma-Aldrich. and the percent that became blastocysts were determined at Day 7 Recombinant human IGF1, which is active in cattle [1820,22,23], was (168 h) and Day 8 (192 h) post-insemination. The experiment was purchased from Sigma-Aldrich. A vial containing 50 g of lyophilized replicated 5 times using 332 to 356 embryos per group. IGF1 was rehydrated with 200 l of water, and this stock solution was then stored at 20 C in 5 L aliquots until dilution to the requisite 2.5. Role of MAPK signaling pathway in IGF1 actions concentration with SOF-BE1 on the day of use. The design was a 2 2 factorial with main effects of IGF1 (0 or 2.2. In vitro production of embryos 100 ng/ml) and PD 98059 (0 or 100 M). Embryos were produced as described above and cultured in SOF-BE1 from Days 0 to 4 (096 h) Ovaries were obtained from a mix of beef and dairy cows (N75% post-insemination. At Day 4 (96 h), embryos were placed in groups of beef) from a commercial abattoir (Central Beef Packing Co., Center 30 in 50 L microdrops of SOF-BE1 containing 0.1% DMSO (vehicle), Hill, FL, USA), and transported in 0.9% (w/v) NaCl solution at room SOF-BE1 containing 0.1% DMSO and 100 ng/mL IGF1, SOF-BE1 temperature. Cumulusoocyte complexes (COCs) were obtained by containing 0.1% DMSO, 100 M PD 98059 (MAPK inhibitor) or SOF- slicing 2 to 8 mm follicles on the surface of ovaries. Those COCs BE1 containing 0.1% DMSO (vehicle), 100 ng/mL IGF1 and 100 M PD containing at least one layer of compact cumulus cells and even 98059. Embryo development was assessed at Day 7 and 8 (168 h and granulation were washed in OCM. COCs were matured for 2022 h in 192 h) post-insemination. The experiment was replicated 5 times groups of 10 in 50 L drops of OMM overlaid with mineral oil at using 308 to 378 oocytes per group. 38.5 C in an atmosphere of 5% (v/v) CO2 in humidied air. Matured COCs were then washed in HEPES-TALP and transferred in groups of 2.6. Statistical analysis 200 to a 35 mm petri dish containing 1700 L of IVF-TALP supple- mented with 80 L PHE (0.5 mM penicillamine, 0.25 mM hypotaurine, Data on the percent of oocytes that cleaved and became a and 25 M epinephrine in 0.9% [w/v] NaCl), and fertilized with 120 L blastocyst were analyzed by least-squares analysis of variance using Percoll-puried spermatozoa (~1 106 sperm cells). Sperm were the Proc GLM procedure of the Statistical Analysis System (SAS for prepared from a pool of frozen-thawed semen from three different Windows, Version 9.2 Cary, NC). Percent data were transformed by bulls; a different set of bulls was generally used for each replicate). arcsin-transformation before analysis. The mathematical model The day of fertilization was designated Day 0 (0 h). After 6 to 10 h in included main effects of replicate, treatment or treatments and all an atmosphere of 5% CO2 in humidied air, putative zygotes were interactions. Replicate was considered random, other main effects removed from fertilization wells, denuded of cumulus cells by were considered xed and tests of signicance were calculated after vortexing for 4 min in HEPES-TALP and hyaluronidase (10,000 U/mL determination of expected means squares. Probability values were in 600 L HEPES-TALP medium) and washed in HEPES-TALP. Embryos based on analysis of arcsin-transformed data while least-squares were then placed in groups of 30 in 50 L drops of SOF-BE1 overlaid means were from analysis of untransformed data. The following

3 A.Q.S. Bonilla et al. / Growth Hormone & IGF Research 21 (2011) 107111 109 orthogonal contrasts were used to determine differences between A a a a a individual concentrations of IGF: 0 versus others, 100 versus 10 and 80 Cleavage at Day 4 (%) 200 and 10 versus 200. For experiment on effects of time of addition of IGF1, identication of means that differed signicantly was deter- 60 mined using the pdiff procedure of SAS when the main effect of treatment was signicant. 40 3. Results 20 3.1. Concentration-dependent actions of IGF1 to increase blastocyst development 0 B c bc Blastocysts at Day 7 (%) Treatment with IGF1 beginning at 6 h post-insemination did not ab 30 affect the percentage of oocytes that cleaved by Day 3 post-insemination a (Fig. 1A) but increased the percentage of embryos that became a blastocyst at Day 7 (Pb 0.05; Fig. 1B) and 8 (P = 0.05; Fig. 1C). At Day 7, 20 there was no difference between 10, 100 and 200 ng/mL. At Day 8, the percentage of oocytes that became a blastocyst was higher (P b 0.05) for 100 ng/mL than for 10 or 200 ng/mL. 10 0 A a a a a C c bc 80 Blastocysts at Day 8 (%) 40 ab Cleavage at Day 3 (%) a 60 30 40 20 20 10 0 0 b control 0-4 4-8 0-8 B b Days of culture during which IGF1 was present Blastocysts at Day 7 (%) b 30 Fig. 2. Improvement in blastocyst development when IGF1 is added from Days 4 to 8 of a culture but not when added from Days 0 to 4. Data are least-squares means SEM and represent the percent of oocytes that cleaved (Panel A) and that became blastocysts at 20 Day 7 (Panel B) and Day 8 (Panel C) post-insemination. Embryos were either cultured without IGF1, IGF1 from Days 0 to 8 post-insemination, Days 04 post-insemination or Days 48 post-insemination. The main effect of treatment was signicant for results at Day 7 (P b 0.05) and 8 (P b 0.01) and differences between individual means (P b 0.05) are 10 indicated by different superscripts above each bar. Data are least-squares means SEM of results from 5 replicates involving 332 to 356 oocytes per group. 0 c C 3.2. Determination of the stage of development at which IGF1 acts to Blastocysts at Day 8 (%) 40 b b increase blastocyst development a 30 Treatment did not affect cleavage (Fig. 2A) but addition of IGF1 from Days 0 to 8 post-insemination increased (Pb 0.05) the percentage of oocytes that became blastocysts at Day 7 (Fig. 2B) and 8 post- 20 insemination (Fig. 2C). A similar increase in percentage of oocytes developing to the blastocyst stage was observed when embryos were 10 cultured with IGF1 from Days 4 to 8 (Pb 0.05 versus controls). There was no signicant effect of IGF1 on percent development to the blastocyst 0 stage when IGF1 was added from Days 0 to 4, although values were 0 10 100 200 intermediated between controls and embryos treated with IGF1 from IGF1 (ng/mL) Days 0 to 8 or 4 to 8 (Fig. 2B and C). Fig. 1. Concentration-dependent effects of IGF1 on the percent of oocytes that cleaved (Panel A) and that became blastocysts at Day 7 (Panel B) and Day 8 (Panel C) post- 3.3. Effect of inhibition of MAPK on actions of IGF1 to promote development insemination. Concentration of IGF1 did not affect cleavage rate (p N 0.05). IGF1 increased the percent of oocytes becoming a blastocyst at Day 7and Day 8 compared to Development at both Days 7 and 8 was affected by an inhibitor by control (p b 0.05 and p = 0.05 respectively). At Day 7 there was no difference between 10, 100 and 200 ng/mL, and at Day 8 the percent of oocytes that became a blastocyst IGF1 interaction (Fig. 3; P b 0.05). These interactions reected the fact was higher for 100 ng/mL (P b 0.05) than for 10 or 200 ng/mL. Data are least-squares that IGF1 increased development in the absence of the inhibitor but means SEM of results from 4 replicates involving 231 to 284 oocytes per group. not in the presence of PD 98059.

4 110 A.Q.S. Bonilla et al. / Growth Hormone & IGF Research 21 (2011) 107111 35 50 formation. Blastocoel formation requires actions of ATP1A1 to b increase blastocel uid and facilitate tight junction formation 30 [37,38] and IGF1 tended to increase expression of ATP1A1 in Day 7 40 b Blastocysts at Day 7 (%) Blastocysts at Day 8 (%) no inhibitor no inhibitor blastocysts [22]. 25 The effects of IGF1 before Day 4 are less clear. While there was no a signicant effect of IGF1 from Days 0 to 4 on the percentage of oocytes 30 20 ac that developed to the blastocysts stage, values were intermediate a c between untreated controls and embryos treated with IGF1 from Days 15 inhibitor inhibitor a 20 4 to 8 or 0 to 8. More research is needed to dene effects of IGF1 early a in development. Receptors for IGF1 are present as early as the two-cell 10 stage [35]. Nonetheless, IGF1 was without effect on embryo thermo- 10 tolerance at the two-cell stage [20]. Perhaps, embryonic genome 5 activation is required for IGF1 to affect embryonic function. The concentrations at which IGF1 increased competence for 0 0 development to the blastocysts stage in the present study is within 0 100 0 100 the range of those found in the blood of lactating and non-lactating [IGF1], ng/mL cows [26,27]. Surprisingly, IGF1 was more effective at increasing development at 100 ng/mL than at 200 ng/mL. The reasons for this Fig. 3. Effect of the MAPK inhibitor PD 98059 on the action of IGF1 to increase the percent of blastocysts at Day 7 and Day 8 post-insemination. Black circles represent effect are not known. Perhaps, at higher concentrations, IGF1 absence of inhibitor, and open circles represent the presence of inhibitor. Development activated receptors for other ligands that activate signaling pathways at both Day 7 and 8 was affected by inhibitor by IGF1 interactions (P b 0.05). Data are inhibitory to development. least-squares means SEM of results from 5 replicates (308 to 378 oocytes per group). Acknowledgments 4. Discussion Research was supported by National Research Initiative Compet- Results presented here indicate that the pro-developmental effects itive Grants no. 2007-35203-18073 and 2009-65203-05732 from the of IGF1 involve actions mediated by the MAPK pathway and events USDA National Institute of Food and Agriculture. The authors thank occurring during the period from Days 4 to 8 after insemination. William Rembert, for invaluable efforts in obtaining ovaries, Marshall, Moreover, IGF1 exerts its pro-developmental effects at concentrations Adam, and Alex Chernin and employees of Central Beef Packing Co. that are within the range of those found in the blood of lactating and (Center Hill, FL) for donation of ovaries; and Scott A. Randell of non-lactating cows. Southeastern Semen Services (Wellborn, FL) for donating semen. That the pro-developmental effects of IGF1 involve actions mediated by the MAPK pathway is indicated by the observation that References inhibition of this pathway with PD98059 blocked actions of IGF1 on development to the blastocyst stage. The MAPK pathway is one of the [1] D. Rizos, M. Clemente, P. Bermejo-Alvarez, J. de La Fuente, P. Lonergan, A. Gutierrez-Adan, Consequences of in vitro culture conditions on embryo main signaling pathways (the PI3K pathway being the other) through development and quality, Reprod. Domest. Anim. 43 (Suppl 4) (2008) 4450. which IGF1 alters cellular function [15]. Proliferative actions of IGF1 [2] D. Rizos, M.A. Ramirez, B. Pintado, P. Lonergan, A. Gutierrez-Adan, Culture of involve activation of the MAPK pathway [28,29]. It is possible, bovine embryos in intermediate host oviducts with emphasis on the isolated mouse oviduct, Theriogenology 73 (2010) 777785. therefore, that the main mechanism by which IGF1 increases [3] H. Luo, K. Kimura, M. Aoki, M. Hirako, Vascular endothelial growth factor (VEGF) blastocyst development is through an increase in proliferation. In promotes the early development of bovine embryo in the presence of cumulus this way, more embryos could reach a critical cell number necessary cells, J. Vet. Med. Sci. 64 (2002) 967971. [4] H. Sagirkaya, M. Misirlioglu, A. Kaya, N.L. First, J.J. Parrish, E. Memili, for differentiation into the blastocyst. Other molecules that stimulate Developmental potential of bovine oocytes cultured in different maturation and proliferation also can increase the proportion of embryos that develop culture conditions, Anim. Reprod. Sci. 101 (2007) 225240. to the blastocyst stage [3,4]. That IGF1 may increase blastocyst [5] A.A. de Moraes, P.J. Hansen, Granulocyte-macrophage colony-stimulating factor promotes development of in vitro produced bovine embryos, Biol. Reprod. 57 formation by increasing the proportion of embryos that reach a cell (1997) 10601065. number critical for blastocyst formation is supported by the nding [6] B. Loureiro, L. Bonilla, J. Block, J.M. Fear, A.Q. Bonilla, P.J. Hansen, Colony- that cell number of bovine blastocysts did not differ between control stimulating factor 2 (CSF-2) improves development and posttransfer survival of and IGF1-treated embryos [22]. bovine embryos produced in vitro, Endocrinology 150 (2009) 50465054. [7] J.A. Neira, D. Tainturier, M.A. Pena, J. Martal, Effect of the association of IGF-I, IGF- An alternative explanation for the effect of IGF1 on blastocyst II, bFGF, TGF-1, GM-CSF, and LIF on the development of bovine embryos formation, that IGF1 increases cell number by blocking apoptosis, is produced in vitro, Theriogenology 73 (2010) 595604. less likely. Although IGF1 can block induction of apoptosis in [8] F.F. Paula-Lopes, A.A. de Moraes, J.L. Edwards, J.E. Justice, P.J. Hansen, Regulation of preimplantation development of bovine embryos by interleukin-1, Biol. Reprod. preimplantation bovine embryos [19,21,30] and cause alterations in 59 (1998) 14061412. gene expression that would contribute to an anti-apoptotic state [20], [9] M.C. Lucy, Functional differences in the growth hormone and insulin-like growth the anti-apoptotic actions of IGF1 involve the PI3K pathway [19,30]. factor axis in cattle and pigs: implications for post-partum nutrition and reproduction, Reprod. Domest. Anim. 43 (Suppl 2) (2008) 3139. Moreover, in the absence of a pro-apoptotic signal, there was no effect [10] R.D. Geisert, C.Y. Lee, F.A. Simmen, M.T. Zavy, A.E. Fliss, F.W. Bazer, R.C. Simmen, of IGF1 on the proportion of blastocyst blastomeres that are apoptotic Expression of messenger RNAs encoding insulin-like growth factor-I, -II, and [22]. insulin-like growth factor binding protein-2 in bovine endometrium during the estrous cycle and early pregnancy, Biol. Reprod. 45 (1991) 975983. The fact that IGF1 was as effective at increasing embryonic [11] K. Prelle, M. Stojkovic, K. Boxhammer, J. Motlik, D. Ewald, G.J. Arnold, E. Wolf, competence to form a blastocyst when added between Days 4 and Insulin-like growth factor I (IGF-I) and long R(3)IGF-I differently affect 8 as when added between Days 0 and 8 means that actions of IGF1 to development and messenger ribonucleic acid abundance for IGF-binding proteins and type I IGF receptors in in vitro produced bovine embryos, Endocrinology 142 increase blastocyst formation involve regulation of events associated (2001) 13091316. with events after embryonic genome activation [31] and when the [12] P.G. Pushpakumara, R.S. Robinson, K.J. Demmers, G.E. Mann, K.D. Sinclair, R. embryo is undergoing compaction [31,33], DNA methylation [34], Webb, D.C. Wathes, Expression of the insulin-like growth factor (IGF) system in proliferation and blastocoel formation [32,35,36]. There is evidence the bovine oviduct at oestrus and during early pregnancy, Reproduction 123 (2002) 859868. that IGF1 increases development to the blastocyst stage, at least in [13] M.L. Rhoads, J.P. Meyer, S.J. Kolath, W.R. Lamberson, M.C. Lucy, Growth hormone part, by regulating expression of genes involved in blastocoel receptor, insulin-like growth factor (IGF)-1, and IGF-binding protein-2 expression

5 A.Q.S. Bonilla et al. / Growth Hormone & IGF Research 21 (2011) 107111 111 in the reproductive tissues of early postpartum dairy cows, J. Dairy Sci. 91 (2008) serum in dairy cows in early lactation and reproductive performance and milk 18021813. yield, J. Dairy Sci. 91 (2008) 38623868. [14] L.M. Wang, H.L. Feng, Y. Ma, M. Cang, H.J. Li, Z. Yan, P. Zhou, J.X. Wen, S. Bou, D.J. [27] M. Wu, J. Hall, R.M. Akers, H. Jiang, Effect of feeding level on serum insulin-like Liu, Expression of IGF receptors and its ligands in bovine oocytes and growth factor I (IGF-I) response to growth hormone injection, J. Endocrinol. 206 preimplantation embryos, Anim. Reprod. Sci. 114 (2009) 99108. (2010) 3745. [15] M.M. Chitnis, J.S. Yuen, A.S. Protheroe, M. Pollak, V.M. Macaulay, The type 1 [28] A. Inoue, S. Takeuchi, S. Takahashi, Insulin-like growth factor-I stimulated DNA insulin-like growth factor receptor pathway, Clin. Cancer Res. 14 (2008) replication in mouse endometrial stromal cells, J. Reprod. Dev. 51 (2005) 63646370. 305313. [16] F. Moreira, F.F. Paula-Lopes, P.J. Hansen, L. Badinga, W.W. Thatcher, Effects of [29] K. Radcliff, T.B. Tang, J. Lim, Z. Zhang, M. Abedin, L.L. Demer, Y. Tintut, Insulin-like growth hormone and insulin-like growth factor-I on development of in vitro growth factor-I regulates proliferation and osteoblastic differentiation of derived bovine embryos, Theriogenology 57 (2002) 895907. calcifying vascular cells via extracellular signal-regulated protein kinase and [17] S. Sirisathien, H.J. Hernandez-Fonseca, B.G. Brackett, Inuences of epidermal phosphatidylinositol 3-kinase pathways, Circ. Res. 96 (2005) 398400. growth factor and insulin-like growth factor-I on bovine blastocyst development [30] F.D. Jousan, L.J. Oliveira, P.J. Hansen, Short-term culture of in vitro produced in vitro, Anim. Reprod. Sci. 77 (2003) 2132. bovine preimplantation embryos with insulin-like growth factor-I prevents heat [18] F.D. Jousan, P.J. Hansen, Insulin-like growth factor-I as a survival factor for the shock-induced apoptosis through activation of the phosphatidylinositol 3-kinase/ bovine preimplantation embryo exposed to heat shock, Biol. Reprod. 71 (2004) Akt pathway, Mol. Reprod. Dev. 75 (2008) 681688. 16651670. [31] E. Memili, N.L. First, Zygotic and embryonic gene expression in cow: a review of [19] F.D. Jousan, P.J. Hansen, Insulin-like growth factor-I promotes resistance of bovine timing and mechanisms of early gene expression as compared with other species, preimplantation embryos to heat shock through actions independent of its anti- Zygote 8 (2000) 8796. apoptotic actions requiring PI3K signaling, Mol. Reprod. Dev. 74 (2007) 189196. [32] A. Van Soom, M.L. Boerjan, P.E. Bols, G. Vanroose, A. Lein, M. Coryn, A. de Kruif, [20] A.Q. Bonilla, L.J. Oliveira, M. Ozawa, E.M. Newsom, M.C. Lucy, P.J. Hansen, Timing of compaction and inner cell allocation in bovine embryos produced in Developmental changes in thermoprotective actions of insulin-like growth factor- vivo after superovulation, Biol. Reprod. 57 (1997) 10411049. 1 on the preimplantation bovine embryo, Mol. Cell. Endocrinol. 332 (2010) [33] A. Van Soom, I. Van Vlaenderen, A.R. Mahmoudzadeh, H. Deluyker, A. de Kruif, 170179. Compaction rate of in vitro fertilized bovine embryos related to the interval from [21] J.I. Moss, E. Pontes, P.J. Hansen, Insulin-like growth factor-1 protects preimplan- insemination to rst cleavage, Theriogenology 38 (1992) 905919. tation embryos from anti-developmental actions of menadione, Arch. Toxicol. 83 [34] W. Dean, F. Santos, M. Stojkovic, V. Zakhartchenko, J. Walter, E. Wolf, W. Reik, (2009) 10011007. Conservation of methylation reprogramming in mammalian development: [22] J. Block, C. Wrenzycki, H. Niemann, D. Herrmann, P.J. Hansen, Effects of insulin- aberrant reprogramming in cloned embryos, Proc. Natl. Acad. Sci. U. S. A. 98 like growth factor-1 on cellular and molecular characteristics of bovine (2001) 1373413738. blastocysts produced in vitro, Mol. Reprod. Dev. 75 (2008) 895903. [35] M. Alomar, H. Tasiaux, S. Remacle, F. George, D. Paul, I. Donnay, Kinetics of [23] J. Block, P.J. Hansen, Interaction between season and culture with insulin-like fertilization and development, and sex ratio of bovine embryos produced using growth factor-1 on survival of in vitro produced embryos following transfer to the semen of different bulls, Anim. Reprod. Sci. 107 (2008) 4861. lactating dairy cows, Theriogenology 67 (2007) 15181529. [36] P. Holm, N.N. Shukri, G. Vajta, P. Booth, C. Bendixen, H. Callesen, Developmental [24] J.J. Parrish, J.L. Susko-Parrish, M.L. Leibfried-Rutledge, E.S. Critser, W.H. Eyestone, kinetics of the rst cell cycles of bovine in vitro produced embryos in relation to N.L. First, Bovine in vitro fertilization with frozenthawed semen, Theriogenology their in vitro viability and sex, Theriogenology 50 (1998) 12851299. 25 (1986) 591600. [37] A.J. Watson, L.C. Barcroft, Regulation of blastocyst formation, Front. Biosci. 6 [25] S.D. Fields, P.J. Hansen, A.D. Ealy, Fibroblast growth factor requirements for in (2001) D708D730. vitro development of bovine embryos. Theriogenology (in press). [38] M.I. Violette, P. Madan, A.J. Watson, Na+/K+-ATPase regulates tight junction [26] U. Falkenberg, J. Haertel, K. Rotter, M. Iwersen, G. Arndt, W. Heuwieser, formation and function during mouse preimplantation development, Dev. Biol. Relationships between the concentration of insulin-like growth factor-1 in 289 (2006) 406419.

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