Glycolytic pathway activity: effect on IVM and oxidative metabolism of bovine oocytes
Cynthia Gutnisky A C , Sergio Morado A , Gabriel C. Dalvit A , Jeremy G. Thompson B and Pablo D. Cetica A
+ Author Affiliations
- Author Affiliations
A Institute of Research and Technology on Animal Reproduction, School of Veterinary Sciences, University of Buenos Aires, Chorroarín 280, Buenos Aires C1427CWO, Argentina.
B Research Centre for Reproductive Health, The Robinson Institute, School of Paediatrics and Reproductive Health, The University of Adelaide, 2nd Floor, Medical School South, Adelaide, SA 5005, Australia.
C Corresponding author. Email: cgutnisky@fvet.uba.ar
Reproduction, Fertility and Development 25(7) 1026-1035 https://doi.org/10.1071/RD12193
Submitted: 19 June 2012 Accepted: 20 September 2012 Published: 26 October 2012
Abstract
The aim of the present study was to determine the effect of altering glycolytic pathway activity during bovine IVM on the meiotic maturation rate, oxidative activity, mitochondrial activity and the mitochondrial distribution within oocytes. Glycolytic activity was manipulated using two inhibitors (ATP, NaF) and a stimulator (AMP) of key enzymes of the pathway. Inhibition of glucose uptake, lactate production and meiotic maturation rates was observed when media were supplemented with ATP or NaF. The addition of AMP to the maturation medium had no effect on glucose uptake, lactate production or meiotic maturation. In the absence of gonadotrophin supplementation, AMP stimulated both glucose uptake and lactate production. However, AMP also decreased cytoplasmic maturation, as determined by early cleavage. During IVM, oocyte oxidative and mitochondrial activity was observed to increase at 15 and 22 h maturation. Inhibiting glycolysis with ATP or NaF led to a reduced oxidative and mitochondrial pattern compared with the respective control groups. Stimulation of the pathway with AMP increased oxidative and mitochondrial activity. A progressive mitochondrial migration to the central area was observed during maturation; oocytes treated with ATP, NaF or AMP showed limited migration. The present study reveals the effects of altering glycolytic pathway activity in cumulus–oocyte complexes, revealing the link between glycolysis of the cumulus–oocyte complex and the oxidative and mitochondrial activity of the oocyte.
Additional keywords : cumulus–oocyte complex, glycolysis, maturation, mitotracker green, redox sensor red.
References
Arzondo, M., Caballero, J., Marin Briggiler, C., Dalvit, G., Cetica, P., and Vazquez-Levin, M. (2012). Glass wool filtration of bull cryopreserved semen: a rapid, effective method to obtain a high percentage of functional spermatozoa. Theriogenology 78, 201–209.| Glass wool filtration of bull cryopreserved semen: a rapid, effective method to obtain a high percentage of functional spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC38rosVCqtA%3D%3D&md5=27b8a30bb432336820a99ad2b5bda809CAS | 22537998PubMed |
Barham, D., and Trinder, P. (1972). An improved colour reagent for the determination of glucose by the oxidase system. Analyst 97, 142–145.
| An improved colour reagent for the determination of glucose by the oxidase system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE38XhtlOks7Y%3D&md5=b3b09cacdcc4290925fb9f86b5896681CAS | 5037807PubMed |
Bilodeau-Goeseels, S., Sasseville, M., Guillemette, C., and Richard, F. (2007). Effects of adenosine monophosphate-activated kinase activators on bovine oocyte nuclear maturation in vitro. Mol. Reprod. Dev. 74, 1021–1034.
| Effects of adenosine monophosphate-activated kinase activators on bovine oocyte nuclear maturation in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXntVOhurY%3D&md5=c764b55a468e522d83d3e818b5ace7e6CAS | 17290417PubMed |
Brackett, B., and Zuelke, K. (1993). Analysis of factors involved in the in vitro production of bovine embryos. Theriogenology 39, 43–64.
| Analysis of factors involved in the in vitro production of bovine embryos.Crossref | GoogleScholarGoogle Scholar |
Cetica, P., Pintos, L., Dalvit, G., and Beconi, M. (1999). Effect of lactate dehydrogenase activity and isoenzyme localization in bovine oocytes and utilization of oxidative substrates on in vitro maturation. Theriogenology 51, 541–550.
| Effect of lactate dehydrogenase activity and isoenzyme localization in bovine oocytes and utilization of oxidative substrates on in vitro maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXisFent7k%3D&md5=94c3cc3bba9e72d474e600fbf295aca3CAS | 10729040PubMed |
Cetica, P., Pintos, L., Dalvit, G., and Beconi, M. (2002). Activity of key enzymes involved in glucose and triglyceride catabolism during bovine oocyte maturation in vitro. Reproduction 124, 675–681.
| Activity of key enzymes involved in glucose and triglyceride catabolism during bovine oocyte maturation in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXht1KksA%3D%3D&md5=6b95b807c0908810b258257554508a83CAS | 12417006PubMed |
Cetica, P., Pintos, L., Dalvit, G., and Beconi, M. (2003). Involvement of enzymes of amino acid metabolism and tricarboxylic acid cycle in bovine oocyte maturation in vitro. Reproduction 126, 753–763.
| Involvement of enzymes of amino acid metabolism and tricarboxylic acid cycle in bovine oocyte maturation in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmvFWktg%3D%3D&md5=b03d00e67d1409546a6dff2c1f8a2f84CAS | 14748694PubMed |
Chen, C., and Gee, K. (2000). Redox-dependent trafficking of 2,3,4,5,6- of pentafluorodihydrotetramethylrosamine, a novel fluorogenic indicator of cellular oxidative activity. Free Radic. Biol. Med. 28, 1266–1278.
| Redox-dependent trafficking of 2,3,4,5,6- of pentafluorodihydrotetramethylrosamine, a novel fluorogenic indicator of cellular oxidative activity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXkslSitrw%3D&md5=c0f6e039b7c74844eeb8f1496b497739CAS | 10889457PubMed |
Clarenburg, R. (1992). Carbohydrate metabolism. In ‘Physiological Chemistry of Domestic Animals’. (Ed. R. Reinhardt.) pp. 239–291. (Mosby Year Book: St Louis.)
Downs, S., and Mastropolo, A. (1994). The participation of energy substrates in the control of meiotic maturation in murine oocytes. Dev. Biol. 162, 154–168.
| The participation of energy substrates in the control of meiotic maturation in murine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXhvVyitLs%3D&md5=9b2c901f69561a8113c811e81b6c4bbdCAS | 8125183PubMed |
Downs, S., and Utecht, A. (1999). Metabolism of radiolabeled glucose by mouse oocytes and oocyte–cumulus cell complexes. Biol. Reprod. 60, 1446–1452.
| Metabolism of radiolabeled glucose by mouse oocytes and oocyte–cumulus cell complexes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjsVeisLs%3D&md5=40a29e21043de48843a9804dc3dc55b9CAS | 10330104PubMed |
Dumollard, R., Ward, Z., Carroll, J., and Duchen, M. (2007). Regulation of redox metabolism in the mouse oocyte and embryo. Development 134, 455–465.
| Regulation of redox metabolism in the mouse oocyte and embryo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjtlWgs7g%3D&md5=4b4cbbbebd98cde4bb2ccf7c6c324186CAS | 17185319PubMed |
Ferreira, E., Vireque, A., Adona, P., Meirelles, F., Ferriani, R., and Navarro, P. (2009). Cytoplasmic maturation of bovine oocytes: structural and biochemical modification and acquisition of developmental competence. Theriogenology 71, 836–848.
| Cytoplasmic maturation of bovine oocytes: structural and biochemical modification and acquisition of developmental competence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXitVSgs7k%3D&md5=35488856dc001df692a7f4a39bdf2316CAS | 19121865PubMed |
Fleming, W., and Saacke, R. (1972). Fine structure of the bovine oocytes and early embryos. J. Reprod. Fertil. 29, 203–213.
| Fine structure of the bovine oocytes and early embryos.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE387nslKjtg%3D%3D&md5=1b3d3c75cfe7ce18713fd05a3d223c05CAS | 4112454PubMed |
Gordon, I. (Ed.) (1994). Oocyte recovery and maturation. In ‘Laboratory Production of Cattle Embryos’. pp. 31: 142. (Cab International: Wallingford.)
Gutnisky, C., Dalvit, G., Pintos, L., Thompson, J., Beconi, M., and Cetica, P. (2007). Influence of hyaluronic acid synthesis and cumulus mucification on bovine oocyte in vitro maturation, fertilisation and embryo development. Reprod. Fertil. Dev. 19, 488–497.
| Influence of hyaluronic acid synthesis and cumulus mucification on bovine oocyte in vitro maturation, fertilisation and embryo development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjtFKnsLg%3D&md5=e812165019d4f2fe29f038fd67f3ca99CAS | 17394798PubMed |
Harvey, A., Kind, K., and Thompson, J. (2002). Redox regulation of embryo development. Reproduction 123, 479–486.
| Redox regulation of embryo development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XivFGhtLk%3D&md5=9fd096bc97f1acf8effd2811c5de9304CAS | 11914110PubMed |
Herrick, J., Brad, A., and Krisher, R. (2006). Chemical manipulation of glucose metabolism in porcine oocytes: effects on nuclear and cytoplasmatic maturation in vitro. Reproduction 131, 289–298.
| Chemical manipulation of glucose metabolism in porcine oocytes: effects on nuclear and cytoplasmatic maturation in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XisFalsLs%3D&md5=bba7ac496aa8aa1b04909bc37a9456cfCAS | 16452722PubMed |
Hyttel, P., Xu, K., Smith, S., and Greve, T. (1986). Ultrastructure of in vitro oocyte maturation in cattle. J. Reprod. Fertil. 78, 615–625.
| Ultrastructure of in vitro oocyte maturation in cattle.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2s7ht1equg%3D%3D&md5=75cee80d377e77c6eb8817a243d6ab0cCAS | 3806520PubMed |
Khurana, N., and Niemann, H. (2000). Effect of oocyte quality, oxygen tension, embryo density, cumulus cells and energy substrates on cleavage and morula/blastocyst formation of bovine embryos. Theriogenology 54, 741–756.
| Effect of oocyte quality, oxygen tension, embryo density, cumulus cells and energy substrates on cleavage and morula/blastocyst formation of bovine embryos.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3M%2FovVGrtA%3D%3D&md5=9437dfe3bb3430944ec13158291ffef1CAS | 11101035PubMed |
Kruip, T., Cran, D., Beneden, T., and Dieleman, S. (1983). Structural changes in bovine oocytes during final maturation in vivo. Gamete Res. 8, 29–47.
| Structural changes in bovine oocytes during final maturation in vivo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXlvVyisLc%3D&md5=94dab6499b671f1097e563b4aca70eb3CAS |
Lim, J., Lee, B., Lee, E., Chung, H., Ko, J., Park, S., Cha, K., and Hwang, W. (1999). In vitro maturation and in vitro fertilization of bovine oocytes cultured in a chemically defined, protein-free medium: effects of carbohydrates and amino acids. Reprod. Fertil. Dev. 11, 127–132.
| In vitro maturation and in vitro fertilization of bovine oocytes cultured in a chemically defined, protein-free medium: effects of carbohydrates and amino acids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXitVKqtr4%3D&md5=3866de99fb6a1670e6d189e59faf2f1aCAS | 10735557PubMed |
Mayes, P., and Bender, D. (2004). Glucólisis y la oxidación del piruvato. In ‘Harper. Bioquímica Ilustrada’. 16th edn. (Ed. R. K. Murray.) pp. 153–161. (Editorial El Manual Moderno: México DF.)
Morado, S., Cetica, P., Beconi, M., and Dalvit, G. (2009). Reactive oxygen species in bovine oocyte maturation in vitro. Reprod. Fertil. Dev. 21, 608–614.
| Reactive oxygen species in bovine oocyte maturation in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXksF2rtbk%3D&md5=3c9fb24489b1b10730efbe3b3cd2fd60CAS | 19383267PubMed |
Nelson, D., and Cox, M. (2005). Glycolysis, gluconeogenesis and the pentose phosphate pathway. In ‘Lehninger. Principles of Biochemistry’. 4th edn. (Eds K. Ahr and M. Ryan.) pp. 522–534. (W. H. Freeman and Co.: New York.)
Nishi, Y., Takeshita, T., Sato, K., and Araki, T. (2003). Change of the mithocondrial distribution in mouse ooplasm during in vitro maturation. J. Nippon Med. Sch. 70, 408–415.
| Change of the mithocondrial distribution in mouse ooplasm during in vitro maturation.Crossref | GoogleScholarGoogle Scholar | 14578941PubMed |
Preis, K., Seidel, G., and Gardner, D. (2005). Metabolic markers of developmental competence for in vitro-matured oocytes. Reproduction 130, 475–483.
| Metabolic markers of developmental competence for in vitro-matured oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFent7rI&md5=c4220751321568a1167cf9587788c023CAS | 16183865PubMed |
Roberts, R., Stark, J., Iatropoulou, A., Becker, D., Franks, S., and Hardy, K. (2004). Energy substrate metabolism of mouse cumulus–oocyte complexes: response to follicle-stimulating hormone is mediated by the phosphatidylinositol 3-kinase pathway and is associated with oocyte maturation. Biol. Reprod. 71, 199–209.
| Energy substrate metabolism of mouse cumulus–oocyte complexes: response to follicle-stimulating hormone is mediated by the phosphatidylinositol 3-kinase pathway and is associated with oocyte maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXltFKkurs%3D&md5=1e8d9fa575d73c7ff874d2e47fbcee61CAS | 15028625PubMed |
Rose-Hellekant, T., Libersky-Williamson, E., and Bavister, B. (1998). Energy substrates and amino acids provided during in vitro maturation of bovine oocytes after acquisition of developmental competence. Zygote 6, 285–294.
| Energy substrates and amino acids provided during in vitro maturation of bovine oocytes after acquisition of developmental competence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhtVyqu7o%3D&md5=e2ae3e415fb9ea964adca71e276747bfCAS | 9921638PubMed |
Schirmer, T., and Evans, P. (1990). Structural basis of the allosteric behaviour of phosphofructokinase. Nature 343, 140–145.
| Structural basis of the allosteric behaviour of phosphofructokinase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXpsVarsA%3D%3D&md5=ccdf1a2e0f51c433b1a92bac51cf53a3CAS | 2136935PubMed |
Stojkovic, M., Machado, S., Stojkovic, P., Zakhartchenko, V., Hutzler, P., Gonçalves, P., and Wolfi, E. (2001). Mitochondrial distribution and adenosine triphosphate content of bovine oocytes before and after in vitro maturation: correlation with morphological criteria and developmental capacity after in vitro fertilization and culture. Biol. Reprod. 64, 904–909.
| Mitochondrial distribution and adenosine triphosphate content of bovine oocytes before and after in vitro maturation: correlation with morphological criteria and developmental capacity after in vitro fertilization and culture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhsVKjtrk%3D&md5=6d2ac9c4e7dc9eb10db34f96f2204365CAS | 11207207PubMed |
Sun, Q., Wu, G., Lai, L., Park, K., Cabot, R., Cheong, H., Day, B., Prather, R., and Schatten, H. (2001). Translocation of active mitochondria during pig oocyte maturation, fertilization and early embryo development in vitro. Reproduction 122, 155–163.
| Translocation of active mitochondria during pig oocyte maturation, fertilization and early embryo development in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlsVGis7g%3D&md5=a2a51f2c512c3da8ce3ec6690bc4b53aCAS | 11425340PubMed |
Sutton, M., Cetica, P., Beconi, M., Kind, K., Gilchrist, R., and Thompson, J. (2003). Influence of oocyte-secreted factors and culture duration on the metabolic activity of bovine cumulus cell complexes. Reproduction 126, 27–34.
| Influence of oocyte-secreted factors and culture duration on the metabolic activity of bovine cumulus cell complexes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXlvFCntbY%3D&md5=a8397aebe8ab5442ed68bf7113bdb310CAS | 12814344PubMed |
Sutton-McDowall, M., Gilchrist, R., and Thompson, J. (2005). Effect of hexoses and gonadotrophin supplementation on bovine oocyte nuclear maturation during in vitro maturation in a synthetic fluid medium. Reprod. Fertil. Dev. 17, 407–415.
| Effect of hexoses and gonadotrophin supplementation on bovine oocyte nuclear maturation during in vitro maturation in a synthetic fluid medium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjtFOktbs%3D&md5=495f8e3267cf80bd95d9d644857e276dCAS | 15899152PubMed |
Sutton-McDowall, M., Gilchrist, R., and Thompson, J. (2010). The pivotal role of glucose metabolism in determining oocyte developmental competence. Reproduction 139, 685–695.
| The pivotal role of glucose metabolism in determining oocyte developmental competence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXltFajtr0%3D&md5=e999bd2e5438715c307566da1c288f51CAS | 20089664PubMed |
Takahashi, Y., and First, N. (1992). In vitro development of bovine one-cell embryos: influence of glucose, lactate, pyruvate, amino acid and vitamins. Theriogenology 37, 963–978.
| In vitro development of bovine one-cell embryos: influence of glucose, lactate, pyruvate, amino acid and vitamins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXpvVOmtg%3D%3D&md5=1dd465b2ef07457f200658945ccfbb01CAS | 16727096PubMed |
Tarkowski, A. K. (1966). An air-drying method for chromosome preparations from mouse eggs. Cytogenetics 5, 394–400.
| An air-drying method for chromosome preparations from mouse eggs.Crossref | GoogleScholarGoogle Scholar |
Trinder, P. (1969). Determination of glucose in blood using glucose oxidase with an alternative oxygen acceptor. Ann. Clin. Biochem. 6, 24–27.
| 1:CAS:528:DyaE3MXotl2itA%3D%3D&md5=42d6b14600b78f6feb39e58d15fee870CAS |
Wakefield, S., Lane, M., Schulz, S., Hebart, M., Thompson, J., and Mitchell, M. (2007). Maternal supply of omega-3 polyunsaturated fatty acids alter mechanisms involved in oocyte and early embryo development in the mouse. Am. J. Physiol. Endocrinol. Metab. 294, E425–E434.
| Maternal supply of omega-3 polyunsaturated fatty acids alter mechanisms involved in oocyte and early embryo development in the mouse.Crossref | GoogleScholarGoogle Scholar | 18073322PubMed |
Yu, Y., Dumollard, R., Rossbach, A., Lai, A., and Swann, K. (2010). Redistribution of mitochondria leads to burst of ATP production during spontaneous mouse oocyte maturation. J. Cell. Physiol. 1, 672–680.
Zuelke, K., and Brackett, B. (1992). Effects of luteinizing hormone on glucose metabolism in cumulus-enclosed bovine oocytes matured in vitro. Endocrinology 131, 2690–2696.
| Effects of luteinizing hormone on glucose metabolism in cumulus-enclosed bovine oocytes matured in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXlt1OltA%3D%3D&md5=148ddfd2d8706e51c6c61886f32fbbc5CAS | 1446610PubMed |
