Pentose phosphate pathway activity: effect on in vitro maturation and oxidative status of bovine oocytes
Cynthia Gutnisky A C , Gabriel C. Dalvit A , Jeremy G. Thompson B and Pablo D. Cetica AA Area of Biochemistry, 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 26(7) 931-942 https://doi.org/10.1071/RD12397
Submitted: 13 December 2012 Accepted: 11 June 2013 Published: 17 July 2013
Abstract
The relationship between pentose phosphate pathway (PPP) activity in cumulus–oocyte complexes (COCs) and oxidative and mitochondrial activity in bovine oocytes was evaluated with the aim of analysing the impact of two inhibitors (NADPH and 6-aminonicotinamide (6-AN)) and a stimulator (NADP) of the key enzymes of the PPP on the maturation rate, oxidative and mitochondrial activity and the mitochondrial distribution in oocytes. The proportion of COCs with measurable PPP activity (assessed using brilliant cresyl blue staining), glucose uptake, lactate production and meiotic maturation rate diminished when 6-AN (0.1, 1, 5 and 10 mM for 22 h) was added to the maturation medium (P < 0.05). The addition of NADPH did not modify glucose uptake or lactate production, but reduced PPP activity in COCs and meiotic maturation rates (P < 0.05). The presence of NADP (0.0125, 0.125, 1.25 and 12.5 mM for 22 h of culture) in the maturation medium had no effect on PPP activity in COCs, glucose uptake, lactate production and meiotic maturation rate. However, in the absence of gonadotropin supplementation, NADP stimulated both glucose uptake and lactate production at 12.5 mM (the highest concentration tested; P < 0.05). NADP did not modify cleavage rate, but decreased blastocyst production (P < 0.05). During IVM, oocyte oxidative and mitochondrial activity was observed to increase at 15 and 22 h maturation, which was also related to progressive mitochondrial migration. Inhibiting the PPP with 6-AN or NADPH led to reduced oxidative and mitochondrial activity compared with the respective control groups and inhibition of mitochondrial migration (P < 0.05). Stimulation of the PPP with NADP increased oxidative and mitochondrial activity at 9 h maturation (P < 0.05) and delayed mitochondrial migration. The present study shows the significance of altering PPP activity during bovine oocyte IVM, revealing that there is a link between the activity of the PPP and the oxidative status of the oocyte.
Additional keywords: glucose metabolism, Mitotracker green, Redox Sensor red.
References
Alm, H., Torner, H., Lohrke, B., Viergutz, T., Ghoneim, I. M., and Kanitz, W. (2005). Bovine blastocyst development rate in vitro is influenced by selection of oocytes by brillant cresyl blue staining before IVM as indicator for glucose-6-phosphate dehydrogenase activity. Theriogenology 63, 2194–2205.| Bovine blastocyst development rate in vitro is influenced by selection of oocytes by brillant cresyl blue staining before IVM as indicator for glucose-6-phosphate dehydrogenase activity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjtFyrtb0%3D&md5=29d278f6d15dd802dceac74e00676bcaCAS | 15826683PubMed |
Arzondo, M. M., Caballero, J. N., Marin Briggiler, C. I., Dalvit, G., Cetica, P. D., and Vazquez-Levin, M. H. (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=3d28e104afd586c3131f0a79b58ca71eCAS | 22537998PubMed |
Barham, D., and Trinder, P. (1972). An improved colour reagent for the determiantion of glucose by the oxidase system. Analyst 97, 142–145.
| An improved colour reagent for the determiantion of glucose by the oxidase system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE38XhtlOks7Y%3D&md5=5b4e50ee4147c05694d30f2570544882CAS | 5037807PubMed |
Berg, D. K., Thompson, J. G., and Asher, G. W. (2002). Development of in vitro embryo production systems for red deer (Cervus elaphus). Part 2. The timing of in vitro nuclear oocyte maturation. Anim. Reprod. Sci. 70, 77–84.
| Development of in vitro embryo production systems for red deer (Cervus elaphus). Part 2. The timing of in vitro nuclear oocyte maturation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD387ktVyitw%3D%3D&md5=80671032fdfe5c0c160ffad921a35da6CAS | 11841908PubMed |
Bhojwani, S., Vajta, G., Callesen, H., Roschlau, K., Kuwer, A., Becker, F., Alm, H., Torner, H., Kanitz, W., and Poehland, R. (2005). Developmental competence of HMC(TM) derived bovine cloned embryos obtained from somatic cell nuclear transfer of adult fibroblasts and granulosa cells. J. Reprod. Dev. 51, 465–475.
| Developmental competence of HMC(TM) derived bovine cloned embryos obtained from somatic cell nuclear transfer of adult fibroblasts and granulosa cells.Crossref | GoogleScholarGoogle Scholar | 16141646PubMed |
Bhojwani, S., Alm, H., Torner, H., Kanitz, W., and Poehland, R. (2007). Selection of developmentally competent oocytes through brilliant cresyl blue stain enhances blastocyst development rate after bovine nuclear transfer. Theriogenology 67, 341–345.
| Selection of developmentally competent oocytes through brilliant cresyl blue stain enhances blastocyst development rate after bovine nuclear transfer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xhtlars7vE&md5=a957cb0ff43251ba8fa6b9cca03ac0ceCAS | 16999988PubMed |
Brad, A. M., Bormann, C. L., Swain, J. E., Durkin, R. E., Johnson, A. E., Clifford, A. L., and Krisher, R. L. (2003). Glutathione and adenosine triphosphate content of in vivo and in vitro matured porcine oocytes. Mol. Reprod. Dev. 64, 492–498.
| Glutathione and adenosine triphosphate content of in vivo and in vitro matured porcine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXislOqs74%3D&md5=786bf9ec14c8a497ee7bd555c043b897CAS | 12589661PubMed |
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=c9453e08293066cc264f9f81a0810d03CAS | 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=74f471be787999546296e1b51d2dc748CAS | 14748694PubMed |
Comizzoli, P., Urner, F., Sakkas, D., and Renard, J. P. (2003). Up-regulation of glucose metabolism during male pronucleus formation determines the early onset of the s phase in bovine zygotes. Biol. Reprod. 68, 1934–1940.
| Up-regulation of glucose metabolism during male pronucleus formation determines the early onset of the s phase in bovine zygotes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjt12lur4%3D&md5=742ddb5984266e26c329b87c10d8dfe2CAS | 12606355PubMed |
de Matos, D. G., and Furnus, C. C. (2000). The importance of having high glutathione (GSH) level after bovine in vitro maturation on embryo development effect of beta-mercaptoethanol, cysteine and cystine. Theriogenology 53, 761–771.
| The importance of having high glutathione (GSH) level after bovine in vitro maturation on embryo development effect of beta-mercaptoethanol, cysteine and cystine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhvVyhs7g%3D&md5=94339d178ae2bae22cffa427ebcf3417CAS | 10735042PubMed |
Dickinson, D. A., and Forman, H. J. (2002). Glutathione in defense and signalling: lessons from a small thiol. Ann. N. Y. Acad. Sci. 973, 488–504.
| Glutathione in defense and signalling: lessons from a small thiol.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xps1yiuro%3D&md5=5baad6f7169877ae37ca4c7038b617f5CAS | 12485918PubMed |
Downs, S. M., and Utecht, A. M. (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=a01480e231160bae68e79462dc7657e4CAS | 10330104PubMed |
Downs, S. M., Humpherson, P. G., and Leese, H. J. (1998). Meiotic induction in cumulus cell-enclosed mouse oocytes: involvement of the pentose phosphate pathway. Biol. Reprod. 58, 1084–1094.
| Meiotic induction in cumulus cell-enclosed mouse oocytes: involvement of the pentose phosphate pathway.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXit1KhtL0%3D&md5=a0315d23bc5703fe4df94271a7aa7635CAS | 9546744PubMed |
Dumollard, R., Ward, Z., Carroll, J., and Duchen, M. R. (2007). Rugulation of redox metabolism in the mouse oocyte and embryo. Development 134, 455–465.
| Rugulation of redox metabolism in the mouse oocyte and embryo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjtlWgs7g%3D&md5=aa6555a9d57ec034594867ef89455850CAS | 17185319PubMed |
Fleming, W. N., and Saacke, R. G. (1972). Fine structure of the bovine oocyte from the mature graafian follicle. J. Reprod. Fertil. 29, 203–213.
| Fine structure of the bovine oocyte from the mature graafian follicle.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE387nslKjtg%3D%3D&md5=d18c88ad7a227c97b6ac9615af40169cCAS | 4112454PubMed |
Funato, Y., Micchiue, T., Asashima, M., and Miki, H. (2006). The thioredoxin-related redox-regulating protein nucleoredoxin inhibits Wnt–β-catenin signalling through disheveled. Nat. Cell Biol. 8, 501–508.
| The thioredoxin-related redox-regulating protein nucleoredoxin inhibits Wnt–β-catenin signalling through disheveled.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XksVGnurc%3D&md5=2adcb329a0ae38c4f34cea2f739474bbCAS | 16604061PubMed |
Gordon, I. (1994) Oocyte recovery and maturation. In ‘Laboratory Production of Cattle Embryos’. pp. 31–142. (Cab International: Wallingford, UK.)
Gupte, S. A., Arshad, M., Viola, S., Kaminski, P. M., Ungvari, Z., Rabbani, G., Koller, A., and Wolin, M. S. (2003). Pentose phosphate pathway coordinates multiple redox-controlled relaxing mechanisms in bovine coronary arteries. Am. J. Physiol. Heart Circ. Physiol. 285, H2316–H2326.
| 1:CAS:528:DC%2BD2cXhtl2m&md5=967699e25ea063c54c0da1bd53b91cf6CAS | 12933338PubMed |
Gutnisky, C., Dalvit, G. C., Pintos, L. N., Thompson, J. G., Beconi, M. T., and Cetica, P. D. (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=8453ffeb2b8034058bd65c486ab7f29fCAS | 17394798PubMed |
Gutnisky, C., Morado, S. A., Dalvit, G. C., Thompson, J. G., and Cetica, P. D. (2012). Glycolytic pathway activity: effect on in vitro maturation and oxidative metabolism of bovine oocyte. Reprod. Fertil. Dev. , .
| Glycolytic pathway activity: effect on in vitro maturation and oxidative metabolism of bovine oocyte.Crossref | GoogleScholarGoogle Scholar | 23098776PubMed |
Harvey, A. J., Kind, K. L., and Thompson, J. G. (2002). REDOX regulation of early embryo development. Reproduction 123, 479–486.
| REDOX regulation of early embryo development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XivFGhtLk%3D&md5=44c9b7e7b26ae11dd88a72f391028cd0CAS | 11914110PubMed |
Herrick, J. R., Brad, A. M., and Krisher, R. L. (2006). Chemical manipulation of glucose metabolism in porcine oocytes: effects on nuclear and cytoplasmic maturation in vitro. Reproduction 131, 289–298.
| Chemical manipulation of glucose metabolism in porcine oocytes: effects on nuclear and cytoplasmic maturation in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XisFalsLs%3D&md5=6981341af2536fa40fff96f12e5677afCAS | 16452722PubMed |
Imai, S., Johnson, F. B., Marciniak, R. A., Mc Vey, M., Park, P. U., and Guarente, L. (2000). Sir2: an NAD-dependent histone deacetylase that connects chromatin silencing, metabolism, and aging. Cold Spring Harb. Symp. Quant. Biol. 65, 297–302.
| Sir2: an NAD-dependent histone deacetylase that connects chromatin silencing, metabolism, and aging.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlt1ejt7g%3D&md5=a58482524483d14892ccfb3f114861abCAS | 12760043PubMed |
Köhler, E., Barrach, H.-J., and Neubert, D. (1970). Inhibition of NADP dependent oxidoreductases by the 6-aminonicotinamide analogue of NADP. FEBS Lett. 6, 225–228.
| Inhibition of NADP dependent oxidoreductases by the 6-aminonicotinamide analogue of NADP.Crossref | GoogleScholarGoogle Scholar | 11947380PubMed |
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=315f2d7fa57a6dfc50eea5aff19c08f9CAS |
Lieber, C. S. (1991). Alchool, liver, and nutrition. J. Am. Coll. Nutr. 10, 602–632.
| 1:CAS:528:DyaK38XjsFOitg%3D%3D&md5=7ac1ce95da19e4b4ca724c9373162455CAS | 1770192PubMed |
Liu, H., Colavitti, R., Rovira, I. I., and Finkel, T. (2005). Redox dependent transcriptional regulation. Circ. Res. 97, 967–974.
| Redox dependent transcriptional regulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFOmtLvP&md5=d79910f27db84c63c495b29c9710e303CAS | 16284189PubMed |
Nelson, D. L., and Cox, M. M. (2005) Glycolysis, gluconeogenesis and the pentose phosphate pathway. In ‘Lehninger. Principles of Biochemistry’, 4th edn. (Eds K. Ahr and M. Ryan.) pp. 522–557. (W.H. Freeman and Co.: New York.)
Özer, N., Bilgi, C., and Ögüs, H. (2002). Dog liver glucose-6-phosphate dehydrogenase: purification and kinetic properties. Int. J. Biochem. Cell Biol. 34, 253–262.
| Dog liver glucose-6-phosphate dehydrogenase: purification and kinetic properties.Crossref | GoogleScholarGoogle Scholar | 11849992PubMed |
Pandolfi, P. P., Sonati, F., Rivi, R., Mason, P., Grosveld, F., and Luzzatto, L. (1995). Targeted disruption of the housekeeping gene encoding glucose 6-phosphate dehydrogenase (G6PD): G6PD is dispensable for pentose synthesis but essential for defense against oxidative stress. EMBO J. 14, 5209–5215.
| 1:CAS:528:DyaK2MXps1Kmsbk%3D&md5=35b32b4bb2f0a850b3a5dd4c72deb591CAS | 7489710PubMed |
Rahman, I., Marwick, J., and Kirkham, P. (2004). Redox modulation of chromatin remodeling: impact on histone acetylation and deacetylation, NF-κB and pro-inflammatory gene expression. Biochem. Pharmacol. 68, 1255–1267.
| Redox modulation of chromatin remodeling: impact on histone acetylation and deacetylation, NF-κB and pro-inflammatory gene expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmslOnsLo%3D&md5=79f74485b9789ae23e0dc195d5ee4f5cCAS | 15313424PubMed |
Rodríguez-González, E., Lopez-Bejar, M., Velilla, E., and Paramio, M. T. (2002). Selection of prepubertal goat oocytes using the brilliant cresyl blue test. Theriogenology 57, 1397–1409.
| Selection of prepubertal goat oocytes using the brilliant cresyl blue test.Crossref | GoogleScholarGoogle Scholar | 12054199PubMed |
Sato, H., Iwata, H., Hayashi, T., Kimura, K., Kuwayama, T., and Monji, Y. (2007). The effect of glucose on the progression of the nuclear maturation of pig oocytes. Anim. Reprod. Sci. 99, 299–305.
| The effect of glucose on the progression of the nuclear maturation of pig oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjslGkuro%3D&md5=7c1237a39e58b983bec3a42ce93315c2CAS | 16784824PubMed |
Stanton, R. C. (2012). Glucose 6-phosphate dehydrogenase, NADPH, and cell survival. IUBMB Life 64, 362–369.
| Glucose 6-phosphate dehydrogenase, NADPH, and cell survival.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XktFWrtL0%3D&md5=bd35e6ed70a8de317f4cf8246598d9b0CAS | 22431005PubMed |
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=0d0428403c1b604df8d5ba648fc19b4bCAS | 11207207PubMed |
Sutton, M. L., Cetica, P. D., Beconi, M. T., Kind, K. L., Gilchrist, R. B., and Thompson, J. G. (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=4e26f5ad26e618d68a1d172282aee94dCAS | 12814344PubMed |
Sutton-McDowall, M. L., Gilchrist, R. B., and Thompson, J. G. (2005). Effect of hexoses and gonadotrophin supplementation on bovine oocyte nuclear maturation during in vitro maturation in a synthetic follicle 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 follicle fluid medium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjtFOktbs%3D&md5=1820734756a4b99c44bff0f686e67149CAS | 15899152PubMed |
Sutton-McDowall, M. L., Gilchrist, R. B., and Thompson, J. G. (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=0ccf52d817b654dae440d70137d5a6b2CAS | 20089664PubMed |
Takahashi, Y., and First, N. L. (1992). In vitro development of bovine one-cell embryos: influence of glucose, lactate, pyruvate, amino acids and vitamins. Theriogenology 37, 963–978.
| In vitro development of bovine one-cell embryos: influence of glucose, lactate, pyruvate, amino acids and vitamins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXpvVOmtg%3D%3D&md5=2e75cafe1e37db9a99ff32d405842fc7CAS | 16727096PubMed |
Tarazona, A. M., Rodriguez, J. I., Restrepo, L. F., and Olivera-Angel, M. (2006). Mitochondrial activity, distribution and segregation in bovine oocytes and in embryos produced in vitro. Reprod. Domest. Anim. 41, 5–11.
| Mitochondrial activity, distribution and segregation in bovine oocytes and in embryos produced in vitro.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD28%2FjsVWnuw%3D%3D&md5=2f591aaad7236512336c257a3f66288dCAS | 16420320PubMed |
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 |
Thompson, J. G. (2006). The impact of nutrition of the cumulus oocyte complex and embryo on subsequent development in ruminants. J. Reprod. Dev. 52, 169–175.
| The impact of nutrition of the cumulus oocyte complex and embryo on subsequent development in ruminants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XksVyhsrw%3D&md5=d837c02e9b72eb5577af6e6a7999adaeCAS | 16538036PubMed |
Thompson, J. G., Bell, A. C., Pugh, P. A., and Trevit, H. R. (1993). Metabolism of pyruvate by pre-elongation sheep embryos and effect of pyruvate and lactate concentrations during culture in vitro. Reprod. Fertil. Dev. 5, 417–423.
| Metabolism of pyruvate by pre-elongation sheep embryos and effect of pyruvate and lactate concentrations during culture in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXitFenu7c%3D&md5=6f55c506e20f571ec93919d7d53e8434CAS | 8153391PubMed |
Tian, W. N., Braunstein, L. D., Pang, J., Stuhlmeier, K. M., Xi, Q. C., Tian, X., and Stanton, R. C. (1998). Importance of glucose-6-phosphate dehydrogenase activity for cell growth. J. Biol. Chem. 273, 10 609–10 617.
| Importance of glucose-6-phosphate dehydrogenase activity for cell growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXivFKnurY%3D&md5=345d808e3a1bd7643be38671e8ae67daCAS |
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=14ff9ed0fdc8c82080381aa5a42e7037CAS |
Tyson, R. L., Perron, J., and Sutherland, G. R. (2000). 6-Aminonicotinamide inhibition of the pentose phosphate pathway in rat neocortex. Neuroreport 11, 1845–1848.
| 6-Aminonicotinamide inhibition of the pentose phosphate pathway in rat neocortex.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXkslyntL4%3D&md5=bdab17a0cef0ddf48f5842645c8835b6CAS | 10884030PubMed |
Wakefield, S. L., Lane, M., Schulz, S. J., Hebart, M. L., Thompson, J. G., and Mitchell, M. (2008). 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 | 1:CAS:528:DC%2BD1cXit1ykur0%3D&md5=0f92a8e9d399562d498728f084fb714eCAS | 18073322PubMed |
Zuelke, K. A., Jones, D. P., and Perreault, S. D. (1997). Glutathione oxidation is associated with altered microtubule function and disrupted fertilization in mature hamster oocytes. Biol. Reprod. 57, 1413–1419.
| Glutathione oxidation is associated with altered microtubule function and disrupted fertilization in mature hamster oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXnvVWksb0%3D&md5=27a2da28e60fcd1ce146dc7076d1830eCAS | 9408248PubMed |