Temporally differential protein expression of glycolytic and glycogenic enzymes during in vitro preimplantation bovine embryo development
Manuel García-Herreros A B C , Constantine A. Simintiras B and Patrick Lonergan BA National Institute for Agricultural and Veterinary Research (INIAV, I.P.), Quinta da Fonte Boa 2005-048, Santarém, Portugal.
B School of Agriculture and Food Science, University College Dublin, Belfield, Dublin 4, Dublin D04 N2E5, Ireland.
C Corresponding author. Email: herrerosgm@gmail.com
Reproduction, Fertility and Development 30(9) 1245-1252 https://doi.org/10.1071/RD17429
Submitted: 17 October 2017 Accepted: 1 March 2018 Published: 23 March 2018
Abstract
Proteomic analyses are useful for understanding the metabolic pathways governing embryo development. This study investigated the presence of enzymes involved in glycolysis and glycogenesis in in vitro-produced bovine embryos at five developmental stages leading up to blastocyst formation. The enzymes examined were: (1) glycolytic: hexokinase-I (HK-I), phosphofructokinase-1 (PFK-1), pyruvate kinase mutase 1/2 (PKM-1/2), glyceraldehyde-3-phosphate dehydrogenase (GAPDH) and (2) glycogenic: glycogen synthase kinase-3 isoforms α/ β (GSK-3α/β). Glucose transporter-1 (GLUT-1) was also analysed. The developmental stages examined were: (1) 2–4-cell, (2) 5–8-cell, (3) 16-cell, (4) morula and (5) expanded blastocyst. The enzymes HK-I, PFK-1, PKM-1/2, GAPDH and GLUT-1 were differentially expressed throughout all stages (P < 0.05). GSK-3α and β were also differentially expressed from the 2–4-cell to the expanded blastocyst stage (P < 0.05) and GLUT-1 was identified throughout. The general trend was that the abundance of PFK1, GAPDH and PKM-1/2 decreased whereas HK-I, phospho-GSK3α (P-GSK3α) and P-GSK3β levels increased as the embryo advanced. In contrast, GLUT-1 expression peaked at the 16-cell stage. These data combined suggest that in vitro bovine embryo metabolism switches from being glycolytic-centric to glycogenic-centric around the 16-cell stage, the developmental window also characterised by embryonic genome activation.
Additional keywords: cattle, developmental stages, early embryos, metabolic pathways, signal transduction.
References
Bermejo-Álvarez, P., Lonergan, P., Rizos, D., and Gutiérrez-Adan, A. (2010). Low oxygen tension during IVM improves bovine oocyte competence and enhances anaerobic glycolysis. Reprod. Biomed. Online 20, 341–349.| Low oxygen tension during IVM improves bovine oocyte competence and enhances anaerobic glycolysis.Crossref | GoogleScholarGoogle Scholar |
Blomberg, L., Hashizume, K., and Viebahn, C. (2008). Blastocyst elongation, trophoblastic differentiation, and embryonic pattern formation. Reproduction 135, 181–195.
| Blastocyst elongation, trophoblastic differentiation, and embryonic pattern formation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXit1yrtL8%3D&md5=0249923464e9c7796fa2d5033faaaa43CAS |
Brison, D. R., and Leese, H. J. (1991). Energy metabolism in late preimplantation rat embryos. J. Reprod. Fertil. 93, 245–251.
| Energy metabolism in late preimplantation rat embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXmt12isL4%3D&md5=a516eee644768761282fc24b78bc579cCAS |
Cagnone, G. L., and Sirard, M. A. (2013). Transcriptomic signature to oxidative stress exposure at the time of embryonic genome activation in bovine blastocysts. Mol. Reprod. Dev. 80, 297–314.
| Transcriptomic signature to oxidative stress exposure at the time of embryonic genome activation in bovine blastocysts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXltlOhsLw%3D&md5=1daa3cf3eac27e296ad56c016466ccc3CAS |
Cagnone, G. L., Dufort, I., Vigneault, C., and Sirard, M. A. (2012). Differential gene expression profile in bovine blastocysts resulting from hyperglycemia exposure during early cleavage stages. Biol. Reprod. 86, 50.
| Differential gene expression profile in bovine blastocysts resulting from hyperglycemia exposure during early cleavage stages.Crossref | GoogleScholarGoogle Scholar |
Chappel, S. (2013). The role of mitochondria from mature oocyte to viable blastocyst. Obstet. Gynecol. Int. 2013, 183024.
| The role of mitochondria from mature oocyte to viable blastocyst.Crossref | GoogleScholarGoogle Scholar |
Collado-Fernandez, E., Picton, H. M., and Dumollard, R. (2012). Metabolism throughout follicle and oocyte development in mammals. Int. J. Dev. Biol. 56, 799–808.
| Metabolism throughout follicle and oocyte development in mammals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXmvVyqsL8%3D&md5=168ed0d9f0f3251935447f56246101e8CAS |
De Bie, J., Marei, W. F., Maillo, V., Jordaens, L., Gutierrez-Adan, A., Bols, P. E., and Leroy, J. L. (2017). Differential effects of high and low glucose concentrations during lipolysis-like conditions on bovine in vitro oocyte quality, metabolism and subsequent embryo development. Reprod. Fertil. Dev. 29, 2284–2300.
| Differential effects of high and low glucose concentrations during lipolysis-like conditions on bovine in vitro oocyte quality, metabolism and subsequent embryo development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2sXhsFylsrjM&md5=7742b46b75f886ef995cd229f6200394CAS |
Diskin, M. G., and Morris, D. G. (2008). Embryonic and early foetal losses in cattle and other ruminants. Reprod. Domest. Anim. 43, 260–267.
| Embryonic and early foetal losses in cattle and other ruminants.Crossref | GoogleScholarGoogle Scholar |
Diskin, M. G., Parr, M. H., and Morris, D. G. (2012). Embryo death in cattle: an update. Reprod. Fertil. Dev. 24, 244–251.
| Embryo death in cattle: an update.Crossref | GoogleScholarGoogle Scholar |
Garcia-Herreros, M., Aparicio, I. M., Rath, D., Fair, T., and Lonergan, P. (2012). Differential glycolytic and glycogenogenic transduction pathways in male and female bovine embryos produced in vitro. Reprod. Fertil. Dev. 24, 344–352.
| Differential glycolytic and glycogenogenic transduction pathways in male and female bovine embryos produced in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht1OitLY%3D&md5=b3d04988ede5b5a0ed342d94eb2c2b6aCAS |
Gardner, D. K., Lane, M., and Batt, P. (1993). Uptake and metabolism of pyruvate and glucose by individual sheep preattachment embryos developed in vivo. Mol. Reprod. Dev. 36, 313–319.
| Uptake and metabolism of pyruvate and glucose by individual sheep preattachment embryos developed in vivo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXitFentLo%3D&md5=2e0535e286b85b4bd36c96decd9801a7CAS |
Harris, D., Huang, B., and Oback, B. (2013). Inhibition of MAP2K and GSK3 signaling promotes bovine blastocyst development and epiblast-associated expression of pluripotency factors. Biol. Reprod. 88, 74.
| Inhibition of MAP2K and GSK3 signaling promotes bovine blastocyst development and epiblast-associated expression of pluripotency factors.Crossref | GoogleScholarGoogle Scholar |
Harvey, A. J., Navarrete Santos, A., Kirstein, M., Kind, K. L., Fischer, B., and Thompson, J. G. (2007). Differential expression of oxygen-regulated genes in bovine blastocysts. Mol. Reprod. Dev. 74, 290–299.
| Differential expression of oxygen-regulated genes in bovine blastocysts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjtlCltbk%3D&md5=3636566c42b08e9407d5cc7fbd930ae2CAS |
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=0ce78714046e1344c7ebc67217c55bdeCAS |
Jensen-Smith, H. C., Hallworth, R., and Nichols, M. G. (2012). Gentamicin rapidly inhibits mitochondrial metabolism in high-frequency cochlear outer hair cells. PLoS One 7, e38471.
| Gentamicin rapidly inhibits mitochondrial metabolism in high-frequency cochlear outer hair cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XovFSqtr4%3D&md5=ec1955ad7cb68e0524af8b83444eaba8CAS |
Kimura, K., Iwata, H., and Thompson, J. G. (2008). The effect of glucosamine concentration on the development and sex ratio of bovine embryos. Anim. Reprod. Sci. 103, 228–238.
| The effect of glucosamine concentration on the development and sex ratio of bovine embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsVSmtLfL&md5=2c1caf1f5226ff87f5549eae6b7b21bfCAS |
Krisher, R. L., Lane, M., and Bavister, B. D. (1999). Developmental competence and metabolism of bovine embryos cultured in semi-defined and defined culture media. Biol. Reprod. 60, 1345–1352.
| Developmental competence and metabolism of bovine embryos cultured in semi-defined and defined culture media.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjsVejtr4%3D&md5=3b25820bf59eb9dc6e847aa804f750f0CAS |
Laskowski, D., Båge, R., Humblot, P., Andersson, G., Sirard, M. A., and Sjunnesson, Y. (2017). Insulin during in vitro oocyte maturation has an impact on development, mitochondria, and cytoskeleton in bovine Day 8 blastocysts. Theriogenology 101, 15–25.
| Insulin during in vitro oocyte maturation has an impact on development, mitochondria, and cytoskeleton in bovine Day 8 blastocysts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2sXhtFGnurjO&md5=73237e44605e1ffafa961647a68844b1CAS |
Leese, H. J. (1995). Metabolic control during preimplantation mammalian development Hum. Reprod. Update 1, 63–72.
| Metabolic control during preimplantation mammalian developmentCrossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2s3jsFSmuw%3D%3D&md5=308fc5b7938181d053ebc190cecc705fCAS |
Leese, H. J. (2015). History of oocyte and embryo metabolism. Reprod. Fertil. Dev. 27, 567–571.
| History of oocyte and embryo metabolism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXntVWnurg%3D&md5=caaf18a5881b97042432ba45f86704a0CAS |
Lequarre, A. S., Grisart, B., Moreau, B., Schuurbiers, N., Massip, A., and Dessy, F. (1997). Glucose metabolism during bovine preimplantation development: analysis of gene expression in single oocytes and embryos. Mol. Reprod. Dev. 48, 216–226.
| Glucose metabolism during bovine preimplantation development: analysis of gene expression in single oocytes and embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXlvFKms7s%3D&md5=48f1de5e00744f64c207f5fbcf5ed5dcCAS |
Leroy, J. L., Valckx, S. D., Jordaens, L., De Bie, J., Desmet, K. L., Van Hoeck, V., Britt, J. H., Marei, W. F., and Bols, P. E. (2015). Nutrition and maternal metabolic health in relation to oocyte and embryo quality: critical views on what we learned from the dairy cow model. Reprod. Fertil. Dev. 27, 693–703.
| Nutrition and maternal metabolic health in relation to oocyte and embryo quality: critical views on what we learned from the dairy cow model.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXntVWntbc%3D&md5=03d3cbc427c1a426c71a1d061d5c2611CAS |
Lonergan, P., Fair, T., Forde, N., and Rizos, D. (2016). Embryo development in dairy cattle. Theriogenology 86, 270–277.
| Embryo development in dairy cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XnsVWgurk%3D&md5=fce87f53561130a817e5fc0320d8bdffCAS |
Lucy, M. C., Butler, S. T., and Garverick, H. A. (2014). Endocrine and metabolic mechanisms linking postpartum glucose with early embryonic and foetal development in dairy cows. Animal 8, 82–90.
| Endocrine and metabolic mechanisms linking postpartum glucose with early embryonic and foetal development in dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXotF2qtrY%3D&md5=d0e1cd952231494d93fe2fd0047634c0CAS |
Miyazawa, H., Yamaguchi, Y., Sugiura, Y., Honda, K., Kondo, K., Matsuda, F., Yamamoto, T., Suematsu, M., and Miura, M. (2017). Rewiring of embryonic glucose metabolism via suppression of PFK-1 and aldolase during mouse chorioallantoic branching. Development 144, 63–73.
| Rewiring of embryonic glucose metabolism via suppression of PFK-1 and aldolase during mouse chorioallantoic branching.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2sXhtF2hu7nJ&md5=1fd08bcd0c99d0047c55a98f58cc3b5aCAS |
Niemann, H., and Wrenzycki, C. (2000). Alterations of expression of developmentally important genes in preimplantation bovine embryos by in vitro culture conditions: implications for subsequent development. Theriogenology 53, 21–34.
| Alterations of expression of developmentally important genes in preimplantation bovine embryos by in vitro culture conditions: implications for subsequent development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXkvVyqug%3D%3D&md5=b2fa5b25ae2c398000fc3baa3f2b73faCAS |
Rieger, D., McGowan, L. T., Cox, S. F., Pugh, P. A., and Thompson, J. G. (2002). Effect of 2,4-dinitrophenol on the energy metabolism of cattle embryos produced by in vitro fertilization and culture. Reprod. Fertil. Dev. 14, 339–343.
| Effect of 2,4-dinitrophenol on the energy metabolism of cattle embryos produced by in vitro fertilization and culture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XovFKnt7w%3D&md5=406012640fb9213321a50d363fca0af5CAS |
Rizos, D., Maillo, V., Sánchez-Calabuig, M. J., and Lonergan, P. (2017). The consequences of maternal–embryonic cross talk during the periconception period on subsequent embryonic development. Adv. Exp. Med. Biol. 1014, 69–86.
| The consequences of maternal–embryonic cross talk during the periconception period on subsequent embryonic development.Crossref | GoogleScholarGoogle Scholar |
Sandra, O., Charpigny, G., Galio, L., and Hue, I. (2017). Preattachment embryos of domestic animals: insights into development and paracrine secretions. Annu. Rev. Anim. Biosci. 5, 205–228.
| Preattachment embryos of domestic animals: insights into development and paracrine secretions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XitVyis7zJ&md5=5a52c61bd84af74b78d73950cfa647efCAS |
Sartori, R., Bastos, M. R., and Wiltbank, M. C. (2010). Factors affecting fertilisation and early embryo quality in single- and superovulated dairy cattle. Reprod. Fertil. Dev. 22, 151–158.
| Factors affecting fertilisation and early embryo quality in single- and superovulated dairy cattle.Crossref | GoogleScholarGoogle Scholar |
Schultz, G. A., Hogan, A., Watson, A. J., Smith, R. M., and Heyner, S. (1992). Insulin, insulin-like growth factors and glucose transporters: temporal patterns of gene expression in early murine and bovine embryos. Reprod. Fertil. Dev. 4, 361–371.
| Insulin, insulin-like growth factors and glucose transporters: temporal patterns of gene expression in early murine and bovine embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXlt1yhsA%3D%3D&md5=48ae1cb0f155c22e1be4a8cec1adc7d6CAS |
Sinclair, K. D., Rooke, J. A., and McEvoy, T. G. (2003). Regulation of nutrient uptake and metabolism in pre-elongation ruminant embryos. Reprod. Suppl. 61, 371–385.
| 1:CAS:528:DC%2BD3sXptFKhtrs%3D&md5=dcbd93602081acd24e679b0e5e7c7caaCAS |
Sirard, M. A., Dufort, I., Coenen, K., Tremblay, K., Massicotte, L., and Robert, C. (2003). The use of genomics and proteomics to understand oocyte and early embryo functions in farm animals. Reprod. Suppl. 61, 117–129.
| 1:CAS:528:DC%2BD3sXptFKhsLk%3D&md5=b373c88d2345f7f2016fb5fae2dd4f54CAS |
Smith, L. C., Thundathil, J., and Filion, F. (2005). Role of the mitochondrial genome in preimplantation development and assisted reproductive technologies. Reprod. Fertil. Dev. 17, 15–22.
| Role of the mitochondrial genome in preimplantation development and assisted reproductive technologies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVKrurnE&md5=63910b0477deb55f25b6c0d368aef9aaCAS |
Thatcher, W., Santos, J. E., and Staples, C. R. (2011). Dietary manipulations to improve embryonic survival in cattle. Theriogenology 76, 1619–1631.
| Dietary manipulations to improve embryonic survival in cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsVanur3N&md5=205297d2fc085135ef883b3e1f4f4227CAS |
Thompson, J. G. (2000). In vitro culture and embryo metabolism of cattle and sheep embryos – a decade of achievement. Anim. Reprod. Sci. 60–61, 263–275.
| In vitro culture and embryo metabolism of cattle and sheep embryos – a decade of achievement.Crossref | GoogleScholarGoogle Scholar |
Thompson, J. G., Partridge, R. J., Houghton, F. D., Cox, C. I., and Leese, H. J. (1996). Oxygen uptake and carbohydrate metabolism by in vitro-derived bovine embryos. J. Reprod. Fertil. 106, 299–306.
| Oxygen uptake and carbohydrate metabolism by in vitro-derived bovine embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XitFKntrc%3D&md5=9035f52d82055c617fd096b648cf24afCAS |
Velazquez, M. A. (2015). Impact of maternal malnutrition during the periconceptional period on mammalian preimplantation embryo development. Domest. Anim. Endocrinol. 51, 27–45.
| Impact of maternal malnutrition during the periconceptional period on mammalian preimplantation embryo development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXitVSiu77O&md5=27b8e0f08c3f82aa5ffff835aaadcfdfCAS |
Wathes, D. C. (2012). Mechanisms linking metabolic status and disease with reproductive outcome in the dairy cow. Reprod. Domest. Anim. 47, 304–312.
| Mechanisms linking metabolic status and disease with reproductive outcome in the dairy cow.Crossref | GoogleScholarGoogle Scholar |
Wrenzycki, C., Herrmann, D., Carnwath, J. W., and Niemann, H. (1998). Expression of RNA from developmentally important genes in preimplantation bovine embryos produced in TCM supplemented with BSA. J. Reprod. Fertil. 112, 387–398.
| Expression of RNA from developmentally important genes in preimplantation bovine embryos produced in TCM supplemented with BSA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXktVentbg%3D&md5=914bb8716cb63fcd791e3de52e30aeb9CAS |