Differential glycolytic and glycogenogenic transduction pathways in male and female bovine embryos produced in vitro
M. Garcia-Herreros A , I. M. Aparicio A , D. Rath B , T. Fair A and P. Lonergan A CA School of Agriculture and Food Science, University College Dublin, Belfield, Dublin 4, Ireland.
B Department of Biotechnology, Institute of Animal Breeding (FAL), Mariensee, Neustadt 31535, Germany.
C Corresponding author. Email: pat.lonergan@ucd.ie
Reproduction, Fertility and Development 24(2) 344-352 https://doi.org/10.1071/RD11080
Submitted: 30 March 2011 Accepted: 9 July 2011 Published: 26 October 2011
Abstract
Previous studies have shown that developmental kinetic rates following IVF are lower in female than in male blastocysts and that this may be related to differences in glucose metabolism. In addition, an inhibition of phosphatidylinositol 3-kinase (PI3-K) inhibits glucose uptake in murine blastocysts. Therefore, the aim of this study was to identify and compare the expression of proteins involved in glucose metabolism (hexokinase-I, HK-I; phosphofructokinase-1, PFK-1; pyruvate kinase1/2, PK1/2; glyceraldehyde-3-phosphate dehydrogenase, GAPDH; glucose transporter-1, GLUT-1; and glycogen synthase kinase-3, GSK-3) in male and female bovine blastocysts to determine whether PI3-K has a role in the regulation of the expression of these proteins. Hexokinase-I, PFK-1, PK1/2, GAPDH and GLUT-1 were present in bovine embryos. Protein expression of these proteins and GSK-3 was significantly higher in male compared with female blastocysts. Inhibition of PI3-K with LY294002 significantly decreased the expression of HK-I, PFK-1, GAPDH, GSK-3 A/B and GLUT-1. Results showed that the expression of glycolytic proteins HK-I, PFK-1, GAPDH and PK1/2, and the transporters GLUT-1 and GSK-3 is regulated by PI3-K in bovine blastocysts. Moreover, the differential protein expression observed between male and female blastocysts might explain the faster developmental kinetics seen in males, as the expression of main proteins involved in glycolysis and glycogenogenesis was significantly higher in male than female bovine embryos and also could explain the sensitivity of male embryos to a high concentration of glucose, as a positive correlation between GLUT-1 expression and glucose uptake in embryos has been demonstrated.
Additional keywords: bovine blastocyst, glucose metabolism, GSK-3, in vitro fertilisation, PI3-K, sex-sorted sperm.
References
Acevedo, N., Wang, X., Dunn, R. L., and Smith, G. D. (2007). Glycogen synthase kinase-3 regulation of chromatin segregation and cytokinesis in mouse preimplantation embryos. Mol. Reprod. Dev. 74, 178–188.| Glycogen synthase kinase-3 regulation of chromatin segregation and cytokinesis in mouse preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmsV2rtA%3D%3D&md5=fbf19a2c4a2c9742ce2a7a31bee3c03fCAS | 16941690PubMed |
Aghayan, M., Rao, L. V., Smith, R. M., Jarett, L., Charron, M. J., Thorens, B., and Heyner, S. (1992). Developmental expression and cellular localization of glucose transporter molecules during mouse preimplantation development. Development 115, 305–312.
| 1:CAS:528:DyaK38Xlt1yltbk%3D&md5=4283df30609cddbe2a3e0242888409f0CAS | 1638987PubMed |
Aparicio, I. M., Bragado, M. J., Gil, M. C., Garcia-Herreros, M., Gonzalez-Fernandez, L., Tapia, J. A., and Garcia-Marin, L. J. (2007a). Porcine sperm motility is regulated by serine phosphorylation of the glycogen synthase kinase-3alpha. Reproduction 134, 435–444.
| Porcine sperm motility is regulated by serine phosphorylation of the glycogen synthase kinase-3alpha.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFKnur3I&md5=3b9fe2fc52f0a1c9058afdac6b4ada33CAS | 17709562PubMed |
Aparicio, I. M., Bragado, M. J., Gil, M. C., Garcia-Herreros, M., Gonzalez-Fernandez, L., Tapia, J. A., and Garcia-Marin, L. J. (2007b). Phosphatidylinositol 3-kinase pathway regulates sperm viability but not capacitation on boar spermatozoa. Mol. Reprod. Dev. 74, 1035–1042.
| Phosphatidylinositol 3-kinase pathway regulates sperm viability but not capacitation on boar spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXntVOhurc%3D&md5=e1951e281bb372d8c311af2ecbdd78a3CAS | 17154303PubMed |
Aparicio, I. M., Garcia-Herreros, M., Fair, T., and Lonergan, P. (2010). Identification and regulation of glycogen synthase kinase-3 during bovine embryo development. Reproduction 140, 83–92.
| Identification and regulation of glycogen synthase kinase-3 during bovine embryo development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVWls77O&md5=c42e6f89e495c557c7727976b6057c91CAS | 20427566PubMed |
Avery, B., Madison, V., and Greve, T. (1991). Sex and development in bovine in-vitro fertilized embryos. Theriogenology 35, 953–963.
| Sex and development in bovine in-vitro fertilized embryos.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD283pvFOhtA%3D%3D&md5=7437d5fe5f4ee4f465c8d99638a63ed2CAS | 16726963PubMed |
Avery, B., Jorgensen, C. B., Madison, V., and Greve, T. (1992). Morphological development and sex of bovine in vitro-fertilized embryos. Mol. Reprod. Dev. 32, 265–270.
| Morphological development and sex of bovine in vitro-fertilized embryos.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK38zmtVakug%3D%3D&md5=1d26759e8a347a0cf5852c2a9d405c5bCAS | 1497876PubMed |
Bermejo-Álvarez, P., Lonergan, P., Rath, D., Gutierrez-Adan, A., and Rizos, D. (2010). Developmental kinetics and gene expression in male and female bovine embryos produced in vitro with sex-sorted spermatozoa. Reprod. Fertil. Dev. 22, 426–436.
| Developmental kinetics and gene expression in male and female bovine embryos produced in vitro with sex-sorted spermatozoa.Crossref | GoogleScholarGoogle Scholar | 20047728PubMed |
Bertolini, M., Beam, S. W., Shim, H., Bertolini, L. R., Moyer, A. L., Famula, T. R., and Anderson, G. B. (2002). Growth, development, and gene expression by in vivo- and in vitro-produced day 7 and 16 bovine embryos. Mol. Reprod. Dev. 63, 318–328.
| Growth, development, and gene expression by in vivo- and in vitro-produced day 7 and 16 bovine embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnslSnsbs%3D&md5=72c1e28a481b588df69fa249ac20f3fdCAS | 12237947PubMed |
Frame, S., and Cohen, P. (2001). GSK3 takes centre stage more than 20 years after its discovery. Biochem. J. 359, 1–16.
| GSK3 takes centre stage more than 20 years after its discovery.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnslGnsLs%3D&md5=a8ac7c337561025d0687d222753b6e01CAS | 11563964PubMed |
Gardner, D. K., and Leese, H. J. (1987). Assessment of embryo viability prior to transfer by the noninvasive measurement of glucose uptake. J. Exp. Zool. 242, 103–105.
| Assessment of embryo viability prior to transfer by the noninvasive measurement of glucose uptake.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2s3ltlShtQ%3D%3D&md5=9cbbf3663a535d04ca79b91c560a016cCAS | 3598508PubMed |
Gopichandran, N., and Leese, H. J. (2003). Metabolic characterization of the bovine blastocyst, inner cell mass, trophectoderm and blastocoel fluid. Reproduction 126, 299–308.
| Metabolic characterization of the bovine blastocyst, inner cell mass, trophectoderm and blastocoel fluid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXnslKksbg%3D&md5=dbd5d7202a8073fd85ab63bd5165a2e5CAS | 12968937PubMed |
Gutierrez-Adan, A., Oter, M., Martinez-Madrid, B., Pintado, B., and De La Fuente, J. (2000). Differential expression of two genes located on the X chromosome between male and female in vitro-produced bovine embryos at the blastocyst stage. Mol. Reprod. Dev. 55, 146–151.
| Differential expression of two genes located on the X chromosome between male and female in vitro-produced bovine embryos at the blastocyst stage.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXkt1eitQ%3D%3D&md5=f1fe86988bd103a67f75dbad740e7022CAS | 10618653PubMed |
Holm, P., Booth, P. J., Schmidt, M. H., Greve, T., and Callesen, H. (1999). High bovine blastocyst development in a static in vitro production system using SOFaa medium supplemented with sodium citrate and myo-inositol with or without serum-proteins. Theriogenology 52, 683–700.
| High bovine blastocyst development in a static in vitro production system using SOFaa medium supplemented with sodium citrate and myo-inositol with or without serum-proteins.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c7pvVGnsw%3D%3D&md5=26633a11a012ea179b9a1f80585e2f19CAS | 10734366PubMed |
Houghton, F. D., Hawkhead, J. A., Humpherson, P. G., Hogg, J. E., Balen, A. H., Rutherford, A. J., and Leese, H. J. (2002). Non-invasive amino acid turnover predicts human embryo developmental capacity. Hum. Reprod. 17, 999–1005.
| Non-invasive amino acid turnover predicts human embryo developmental capacity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xjs12isLg%3D&md5=3ba1e2662c6daf237183fcf06cf73597CAS | 11925397PubMed |
Jimenez, A., Madrid-Bury, N., Fernandez, R., Perez-Garnelo, S., Moreira, P., Pintado, B., de la Fuente, J., and Gutierrez-Adan, A. (2003). Hyperglycemia-induced apoptosis affects sex ratio of bovine and murine preimplantation embryos. Mol. Reprod. Dev. 65, 180–187.
| Hyperglycemia-induced apoptosis affects sex ratio of bovine and murine preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjsFGht7s%3D&md5=098c67b492e1520a5df8d500ab28d7a8CAS | 12704729PubMed |
Jope, R. S., and Johnson, G. V. (2004). The glamour and gloom of glycogen synthase kinase-3. Trends Biochem. Sci. 29, 95–102.
| The glamour and gloom of glycogen synthase kinase-3.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVOrtro%3D&md5=5f4e8cadf4b1047a51d0cbfb9c3e3443CAS | 15102436PubMed |
Jousan, F. D., and Hansen, P. J. (2007). Insulin-like growth factor-I promotes resistance of bovine preimplantation embryos to heat shock through actions independent of its anti-apoptotic actions requiring PI3K signaling. Mol. Reprod. Dev. 74, 189–196.
| Insulin-like growth factor-I promotes resistance of bovine preimplantation embryos to heat shock through actions independent of its anti-apoptotic actions requiring PI3K signaling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmsV2rtQ%3D%3D&md5=4eee30d401acc05ce5c796ed3cd9ad52CAS | 16955404PubMed |
Knijn, H. M., Wrenzycki, C., Hendriksen, P. J., Vos, P. L., Herrmann, D., van der Weijden, G. C., Niemann, H., and Dieleman, S. J. (2002). Effects of oocyte maturation regimen on the relative abundance of gene transcripts in bovine blastocysts derived in vitro or in vivo. Reproduction 124, 365–375.
| Effects of oocyte maturation regimen on the relative abundance of gene transcripts in bovine blastocysts derived in vitro or in vivo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnsV2ht7o%3D&md5=f1fc53410cba3315c5af151f40d11080CAS | 12201810PubMed |
Leese, H. J., Conaghan, J., Martin, K. L., and Hardy, K. (1993). Early human embryo metabolism. Bioessays 15, 259–264.
| Early human embryo metabolism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXltFCjsLY%3D&md5=ed052b5e9bb01adc7d67d3e0a0be2da6CAS | 8517855PubMed |
Morton, K. M., Herrmann, D., Sieg, B., Struckmann, C., Maxwell, W. M. C., Rath, D., Evans, G., Lucas-Hahn, A., Niemann, H., and Wrenzycki, C. (2007). Altered mRNA expression patterns in bovine blastocysts after fertilisation in vitro using flow-cytometrically sex-sorted sperm. Mol. Reprod. Dev. 74, 931–940.
| Altered mRNA expression patterns in bovine blastocysts after fertilisation in vitro using flow-cytometrically sex-sorted sperm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXntVOhtbc%3D&md5=5cbc4f773cbb72d1008e348b677beb17CAS | 17219418PubMed |
Pantaleon, M., and Kaye, P. L. (1998). Glucose transporters in preimplantation development. Rev. Reprod. 3, 77–81.
| Glucose transporters in preimplantation development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXksVSjtL4%3D&md5=e2889b7458e5f426604d42dc0d3e4959CAS | 9685185PubMed |
Peippo, J., and Bredbacka, P. (1995). Sex-related growth rate differences in mouse preimplantation embryos in vivo and in vitro. Mol. Reprod. Dev. 40, 56–61.
| Sex-related growth rate differences in mouse preimplantation embryos in vivo and in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXivFyrsrc%3D&md5=c97cdb040daffd64f9524e09c7f45f6bCAS | 7702870PubMed |
Plas, D. R., and Thompson, C. B. (2002). Cell metabolism in the regulation of programmed cell death. Trends Endocrinol. Metab. 13, 75–78.
| Cell metabolism in the regulation of programmed cell death.Crossref | GoogleScholarGoogle Scholar | 11854022PubMed |
Ray, P. F., Conaghan, J., Winston, R. M., and Handyside, A. H. (1995). Increased number of cells and metabolic activity in male human preimplantation embryos following in vitro fertilization. J. Reprod. Fertil. 104, 165–171.
| Increased number of cells and metabolic activity in male human preimplantation embryos following in vitro fertilization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXmslaktLk%3D&md5=4c97d712ef1d2b8c11e32e43337867d7CAS | 7636798PubMed |
Renard, J. P., Philippon, A., and Menezo, Y. (1980). In-vitro uptake of glucose by bovine blastocysts. J. Reprod. Fertil. 58, 161–164.
| In-vitro uptake of glucose by bovine blastocysts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXptFKrsg%3D%3D&md5=a0878624f40d4ca94dbdf433712f41e9CAS | 7359473PubMed |
Riley, J. K., Carayannopoulos, M. O., Wyman, A. H., Chi, M., and Moley, K. H. (2006). Phosphatidylinositol 3-kinase activity is critical for glucose metabolism and embryo survival in murine blastocysts. J. Biol. Chem. 281, 6010–6019.
| Phosphatidylinositol 3-kinase activity is critical for glucose metabolism and embryo survival in murine blastocysts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhvVeju7k%3D&md5=fcd4702d1df78ccf0f8525a5aa41c3ccCAS | 16272157PubMed |
Robey, R. B., and Hay, N. (2006). Mitochondrial hexokinases, novel mediators of the antiapoptotic effects of growth factors and Akt. Oncogene 25, 4683–4696.
| Mitochondrial hexokinases, novel mediators of the antiapoptotic effects of growth factors and Akt.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xnsl2hs7g%3D&md5=9d3952b0ecfd4190ce2e1728ed641d02CAS | 16892082PubMed |
Roy, L., McDonald, C. A., Jiang, C., Maroni, D., Zeleznik, A. J., Wyatt, T. A., Hou, X., and Davis, J. S. (2009). Convergence of 3′,5′-cyclic adenosine 5′-monophosphate/protein kinase A and glycogen synthase kinase-3beta/beta-catenin signaling in corpus luteum progesterone synthesis. Endocrinology 150, 5036–5045.
| Convergence of 3′,5′-cyclic adenosine 5′-monophosphate/protein kinase A and glycogen synthase kinase-3beta/beta-catenin signaling in corpus luteum progesterone synthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsVCht7bE&md5=46c49daac2c0c7fb2b94efeda30f6f2fCAS | 19819952PubMed |
Sobis, H., Verstuyf, A., and Vandeputte, M. (1991). Histochemical differences in expression of X-linked glucose-6-phosphate dehydrogenase between ectoderm- and endoderm-derived embryonic and extra-embryonic tissues. J. Histochem. Cytochem. 39, 569–574.
| Histochemical differences in expression of X-linked glucose-6-phosphate dehydrogenase between ectoderm- and endoderm-derived embryonic and extra-embryonic tissues.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXit1Kmsbs%3D&md5=6cb5588de73d69af227fa3c5581cc881CAS | 2016509PubMed |
Telford, N. A., Watson, A. J., and Schultz, G. A. (1990). Transition from maternal to embryonic control in early mammalian development: a comparison of several species. Mol. Reprod. Dev. 26, 90–100.
| Transition from maternal to embryonic control in early mammalian development: a comparison of several species.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3c3mslOhtQ%3D%3D&md5=9fba85bb0339b45b5570cc49f8f79f96CAS | 2189447PubMed |
Tiffin, G. J., Rieger, D., Betteridge, K. J., Yadav, B. R., and King, W. A. (1991). Glucose and glutamine metabolism in pre-attachment cattle embryos in relation to sex and stage of development. J. Reprod. Fertil. 93, 125–132.
| Glucose and glutamine metabolism in pre-attachment cattle embryos in relation to sex and stage of development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXmt12is7c%3D&md5=d114a0144c5099edf96c8a24d6a08744CAS | 1920281PubMed |
Wrenzycki, C., Herrmann, D., Carnwath, J. W., and Niemann, H. (1999). Alterations in the relative abundance of gene transcripts in preimplantation bovine embryos cultured in medium supplemented with either serum or PVA. Mol. Reprod. Dev. 53, 8–18.
| Alterations in the relative abundance of gene transcripts in preimplantation bovine embryos cultured in medium supplemented with either serum or PVA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXitleju7s%3D&md5=1a411bbbee8e665fb728141b77ab215cCAS | 10230812PubMed |
Wrenzycki, C., Herrmann, D., Keskintepe, L., Martins, A., Sirisathien, S., Brackett, B., and Niemann, H. (2001). Effects of culture system and protein supplementation on mRNA expression in pre-implantation bovine embryos. Hum. Reprod. 16, 893–901.
| Effects of culture system and protein supplementation on mRNA expression in pre-implantation bovine embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXkt1Cqs74%3D&md5=8f19df08ce927b044a8f697385152bc0CAS | 11331635PubMed |
Wrenzycki, C., Herrmann, D., and Niemann, H. (2003). Timing of blastocyst expansion affects spatial messenger RNA expression patterns of genes in bovine blastocysts produced in vitro. Biol. Reprod. 68, 2073–2080.
| Timing of blastocyst expansion affects spatial messenger RNA expression patterns of genes in bovine blastocysts produced in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXks1GgsLw%3D&md5=4e298d20e0c9d24ff59f89094ff5d880CAS | 12606328PubMed |
Xu, K. P., Yadav, B. R., King, W. A., and Betteridge, K. J. (1992). Sex-related differences in developmental rates of bovine embryos produced and cultured in vitro. Mol. Reprod. Dev. 31, 249–252.
| Sex-related differences in developmental rates of bovine embryos produced and cultured in vitro.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK383jvFWnug%3D%3D&md5=155c4cb48011c09b52be667532d9a838CAS | 1571158PubMed |
Xu, X. Y., Zhang, Z., Su, W. H., Zhang, Y., Feng, C., Zhao, H. M., Zong, Z. H., Cui, C., and Yu, B. Z. (2009). Involvement of the p110α isoform of PI3K in early development of mouse embryos. Mol. Reprod. Dev. 76, 389–398.
| Involvement of the p110α isoform of PI3K in early development of mouse embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjt12hsLo%3D&md5=ee744c042c1cd2bfc416482da718f09bCAS | 18932194PubMed |