Differential effects of high and low glucose concentrations during lipolysis-like conditions on bovine in vitro oocyte quality, metabolism and subsequent embryo development
J. De Bie A D , W. F. A. Marei A B , V. Maillo C , L. Jordaens A , A. Gutierrez-Adan C , P. E. J. Bols A and J. L. M. R. Leroy A
+ Author Affiliations
- Author Affiliations
A Gamete Research Centre, Laboratory for Veterinary Physiology and Biochemistry, Department of Veterinary Sciences, University of Antwerp, Universiteitsplein 1, 2610 Wilrijk, Belgium.
B Department of Theriogenology, Faculty of Veterinary Medicine, Cairo University, Giza square, 12211 Giza, Egypt.
C Departamento de Reproduccion Animal, Instituto nacional de Investigacion y Tecnologia Agraria y Alimentaria (INIA), Crta. De la Coruña, km 7,5 28040 Madrid, Spain.
D Corresponding author. Email: jessie.debie@uantwerpen.be
Reproduction, Fertility and Development 29(11) 2284-2300 https://doi.org/10.1071/RD16474
Submitted: 25 November 2016 Accepted: 6 March 2017 Published: 10 April 2017
Abstract
Lipolytic metabolic conditions are traditionally associated with elevated non-esterified fatty acid (NEFA) concentrations, but may also be accompanied by hyperglycaemia in obesity or by hypoglycaemia during a negative energy balance status. Elevated NEFA concentrations disrupt oocyte and embryo development and quality, but little is known about whether the effects of lipolytic conditions on oocyte developmental competence are modulated by glucose availability. To answer this, bovine cumulus–oocyte complexes (COCs) were matured under different conditions: physiological NEFA (72 µM) and normal glucose (5.5 mM), pathophysiologically high NEFA (420 µM) and normal glucose, high NEFA and high glucose (9.9 mM), high NEFA and low glucose (2.8 mM). Developmental potential, cumulus expansion and metabolism of COCs exposed to high NEFA and low glucose were affected to a greater extent compared with COCs matured under high NEFA and high glucose conditions. High NEFA and high glucose conditions caused a moderate increase in oocyte reactive oxygen species compared with their high NEFA and low glucose or control counterparts. Blastocyst metabolism and the transcriptome of metabolic and oxidative stress-related genes were not affected. However, both lipolytic conditions associated with hyper- or hypoglycaemia led to surviving embryos of reduced quality with regards to apoptosis and blastomere allocation.
Additional keywords: energy balance, fatty acid, fertility, insulin, in vitro maturation, oxidative stress.
References
Aardema, H., Vos, P. L., Lolicato, F., Roelen, B. A., Knijn, H. M., Vaandrager, A. B., Helms, J. B., and Gadella, B. M. (2011). Oleic acid prevents detrimental effects of saturated fatty acids on bovine oocyte developmental competence. Biol. Reprod. 85, 62–69.| Oleic acid prevents detrimental effects of saturated fatty acids on bovine oocyte developmental competence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXotFOls74%3D&md5=9571137421131378aaa71db56b34e36cCAS |
Abe, H., and Hoshi, H. (2003). Evaluation of bovine embryos produced in high performance serum-free media. J. Reprod. Dev. 49, 193–202.
| Evaluation of bovine embryos produced in high performance serum-free media.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmvFSqtLY%3D&md5=7d1c76b3341793de0deda73a6fe5ea31CAS |
Agarwal, A., Aponte-Mellado, A., Premkumar, B. J., Shaman, A., and Gupta, S. (2012). The effects of oxidative stress on female reproduction: a review. Reprod. Biol. Endocrinol. 10, 49.
| The effects of oxidative stress on female reproduction: a review.Crossref | GoogleScholarGoogle Scholar |
American Diabetes Association (2010). Diagnosis and classification of diabetes mellitus. Diabetes Care 33, S62–S69.
| Diagnosis and classification of diabetes mellitus.Crossref | GoogleScholarGoogle Scholar |
Augustin, R., Pocar, P., Wrenzycki, C., Niemann, H., and Fischer, B. (2003). Mitogenic and anti-apoptotic activity of insulin on bovine embryos produced in vitro. Reproduction 126, 91–99.
| Mitogenic and anti-apoptotic activity of insulin on bovine embryos produced in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXlvFCnurs%3D&md5=404d432ecbbcac73cbf4a8591c9cdfecCAS |
Barnes, D., and Sato, G. (1980). Methods for growth of cultured cells in serum-free medium. Anal. Biochem. 102, 255–270.
| Methods for growth of cultured cells in serum-free medium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXhslOrs70%3D&md5=88a44bbc8fd83f97afb6d84e3bb48944CAS |
Berg, J., Tymoczko, J., and Stryer, L. (2006). ‘Biochemistry’. (WH Freeman and Co.: New York.)
Bergman, R. N., and Ader, M. (2000). Free fatty acids and pathogenesis of Type 2 diabetes mellitus. Trends Endocrinol. Metab. 11, 351–356.
| Free fatty acids and pathogenesis of Type 2 diabetes mellitus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXotVSrsbs%3D&md5=cccf05e389881db3cf16a8d90a348fc3CAS |
Bermejo-Alvarez, P., Rizos, D., Rath, D., Lonergan, P., and Gutierrez-Adan, A. (2008). Epigenetic differences between male and female bovine blastocysts produced in vitro. Physiol. Genomics 32, 264–272.
| Epigenetic differences between male and female bovine blastocysts produced in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmt1Wjurw%3D&md5=af60d96bf152156d1913920ae1ebe746CAS |
Block, J., and Hansen, P. J. (2007). Interaction between season and culture with insulin-like growth factor-1 on survival of in vitro-produced embryos following transfer to lactating dairy cows. Theriogenology 67, 1518–1529.
| Interaction between season and culture with insulin-like growth factor-1 on survival of in vitro-produced embryos following transfer to lactating dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXkvFGgtLw%3D&md5=cc32660c67e474bb83ae6a6ea85f42b1CAS |
Bohler, H., Mokshagundam, S., and Winters, S. J. (2010). Adipose tissue and reproduction in women. Fertil. Steril. 94, 795–825.
| Adipose tissue and reproduction in women.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXpsVGhsbg%3D&md5=977c77358a2509d8c9c003d187efe633CAS |
Britt, J. H. (1992). Impacts of early postpartum metabolism on follicular development and fertility. In ‘Proceedings of the Annual Convention – American Association of Bovine Practitioners’. (Ed. E. I. Williams.) pp. 39–43. (Frontier Printers: Stillwater, OK.)
Burton, G. J., Hempstock, J., and Jauniaux, E. (2003). Oxygen, early embryonic metabolism and free radical-mediated embryopathies. Reprod. Biomed. Online 6, 84–96.
| Oxygen, early embryonic metabolism and free radical-mediated embryopathies.Crossref | GoogleScholarGoogle Scholar |
Carvalho, P. D., Souza, A. H., Amundson, M. C., Hackbart, K. S., Fuenzalida, M. J., Herlihy, M. M., Ayres, H., Dresch, A. R., Vieira, L. M., Guenther, J. N., Grummer, R. R., Fricke, P. M., Shaver, R. D., and Wiltbank, M. C. (2014). Relationships between fertility and postpartum changes in body condition and body weight in lactating dairy cows. J. Dairy Sci. 97, 3666–3683.
| Relationships between fertility and postpartum changes in body condition and body weight in lactating dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXmtFahsbo%3D&md5=1f2cb52466a3f148023b2473da65210bCAS |
Chavez, S. L., Loewke, K. E., Han, J., Moussavi, F., Colls, P., Munne, S., Behr, B., and Reijo Pera, R. A. (2012). Dynamic blastomere behaviour reflects human embryo ploidy by the four-cell stage. Nat. Commun. 3, 1251.
| Dynamic blastomere behaviour reflects human embryo ploidy by the four-cell stage.Crossref | GoogleScholarGoogle Scholar |
Choi, S. L., Kim, S. J., Lee, K. T., Kim, J., Mu, J., Birnbaum, M. J., Soo Kim, S., and Ha, J. (2001). The regulation of AMP-activated protein kinase by H(2)O(2). Biochem. Biophys. Res. Commun. 287, 92–97.
| The regulation of AMP-activated protein kinase by H(2)O(2).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXms1anu7k%3D&md5=6223bba20d3b8342a1bb0615297f0760CAS |
Colton, S. A., and Downs, S. M. (2004). Potential role for the sorbitol pathway in the meiotic dysfunction exhibited by oocytes from diabetic mice. J. Exp. Zoolog. A Comp. Exp. Biol. 301A, 439–448.
| Potential role for the sorbitol pathway in the meiotic dysfunction exhibited by oocytes from diabetic mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXks1Knsbc%3D&md5=ea200e5dd24ed899d4d8d4a3adf36b2dCAS |
Combelles, C. M., Gupta, S., and Agarwal, A. (2009). Could oxidative stress influence the in vitro maturation of oocytes? Reprod. Biomed. Online 18, 864–880.
| Could oxidative stress influence the in vitro maturation of oocytes?Crossref | GoogleScholarGoogle Scholar |
Desmet, K. L. J., Van Hoeck, V., Gagné, D., Fournier, E., Thakur, A., O’Doherty, A. M., Walsh, C. P., Sirard, M. A., Bols, P. E. J., and Leroy, J. L. M. R. (2016). Exposure of bovine oocytes and embryos to elevated non-esterified fatty acid concentrations: integration of epigenetic and transcriptomic signatures in resultant blastocysts. BMC Genomics 17, 1004.
| Exposure of bovine oocytes and embryos to elevated non-esterified fatty acid concentrations: integration of epigenetic and transcriptomic signatures in resultant blastocysts.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2sjkvVOktw%3D%3D&md5=17831142df8b63ae06288d0567655074CAS |
Diamond, M. P., Moley, K. H., Pellicer, A., Vaughn, W. K., and DeCherney, A. H. (1989). Effects of streptozotocin- and alloxan-induced diabetes mellitus on mouse follicular and early embryo development. J. Reprod. Fertil. 86, 1–10.
| Effects of streptozotocin- and alloxan-induced diabetes mellitus on mouse follicular and early embryo development.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1MzivVymsQ%3D%3D&md5=b9cac934d8ba2b1add78c43e9c37b2e2CAS |
Downs, S. M. (2015). Nutrient pathways regulating the nuclear maturation of mammalian oocytes. Reprod. Fertil. Dev. 27, 572–582.
| Nutrient pathways regulating the nuclear maturation of mammalian oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXntVWnur8%3D&md5=321f416bea1b8bfa2ac97281d41f6c66CAS |
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=5eb03769e4a4a10fb8e80c2424e92feeCAS |
Drackley, J. K., Overton, T. R., and Douglas, G. N. (2001). Adaptations of glucose and long-chain fatty acid metabolism in liver of dairy cows during the periparturient period. J. Dairy Sci. 84, E100–E112.
| Adaptations of glucose and long-chain fatty acid metabolism in liver of dairy cows during the periparturient period.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlvFalsL0%3D&md5=1f2cc79be224f67cc4fbdcbe6d742defCAS |
Dubuc, G. R., Phinney, S. D., Stern, J. S., and Havel, P. J. (1998). Changes of serum leptin and endocrine and metabolic parameters after 7 days of energy restriction in men and women. Metabolism 47, 429–434.
| Changes of serum leptin and endocrine and metabolic parameters after 7 days of energy restriction in men and women.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXitlygtbk%3D&md5=362e3f2d2764d6c5a3a9c1aae14249daCAS |
Duncan, R. E., Ahmadian, M., Jaworski, K., Sarkadi-Nagy, E., and Sul, H. S. (2007). Regulation of lipolysis in adipocytes. Annu. Rev. Nutr. 27, 79–101.
| Regulation of lipolysis in adipocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsVWisLzJ&md5=d879892716c0932e8b0338b9a530f144CAS |
Dunning, K. R., Cashman, K., Russell, D. L., Thompson, J. G., Norman, R. J., and Robker, R. L. (2010). Beta-oxidation is essential for mouse oocyte developmental competence and early embryo development. Biol. Reprod. 83, 909–918.
| Beta-oxidation is essential for mouse oocyte developmental competence and early embryo development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFahurfN&md5=548d00de5e7460a39941122d18d3ff0fCAS |
Dunning, K. R., Russell, D. L., and Robker, R. L. (2014). Lipids and oocyte developmental competence: the role of fatty acids and beta-oxidation. Reproduction 148, R15–R27.
| Lipids and oocyte developmental competence: the role of fatty acids and beta-oxidation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtFyrtrnE&md5=00089343ef289f0fe4743fd4b5d37375CAS |
Eckel, R. H. (2013) ‘Obesity: Mechanisms and Clinical Management’. (Lippincott Williams & Wilkins: Philadelphia, USA.)
Eppig, J. J., Hosoe, M., O’Brien, M. J., Pendola, F. M., Requena, A., and Watanabe, S. (2000). Conditions that affect acquisition of developmental competence by mouse oocytes in vitro: FSH, insulin, glucose and ascorbic acid. Mol. Cell. Endocrinol. 163, 109–116.
| Conditions that affect acquisition of developmental competence by mouse oocytes in vitro: FSH, insulin, glucose and ascorbic acid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlvV2ms7o%3D&md5=7863285e07fb34ea463de22e143475d5CAS |
Ferguson, E. M., and Leese, H. J. (1999). Triglyceride content of bovine oocytes and early embryos. J. Reprod. Fertil. 116, 373–378.
| Triglyceride content of bovine oocytes and early embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXkslOltbc%3D&md5=895a761c22f7c539df84fa51f83493a0CAS |
Ferguson, E. M., and Leese, H. J. (2006). A potential role for triglyceride as an energy source during bovine oocyte maturation and early embryo development. Mol. Reprod. Dev. 73, 1195–1201.
| A potential role for triglyceride as an energy source during bovine oocyte maturation and early embryo development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XnvFahtr0%3D&md5=1837e33f63b71f794fbae13aba65b6f0CAS |
Gardner, D. K. (1998). Changes in requirements and utilization of nutrients during mammalian preimplantation embryo development and their significance in embryo culture. Theriogenology 49, 83–102.
| Changes in requirements and utilization of nutrients during mammalian preimplantation embryo development and their significance in embryo culture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXnsFCrtA%3D%3D&md5=256d09b11fcb342cabc80799a88bfdefCAS |
Gardner, D. K., and Harvey, A. J. (2015). Blastocyst metabolism. Reprod. Fertil. Dev. 27, 638–654.
| Blastocyst metabolism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXntVWntbw%3D&md5=e6e9b1bebf31749873890f5608eff074CAS |
González-Recio, O., Ugarte, E., and Bach, A. (2012). Trans-generational effect of maternal lactation during pregnancy: a Holstein cow model. PLoS One 7, e51816.
| Trans-generational effect of maternal lactation during pregnancy: a Holstein cow model.Crossref | GoogleScholarGoogle Scholar |
Goud, P. T., Goud, A. P., Qian, C., Laverge, H., Van der Elst, J., De Sutter, P., and Dhont, M. (1998). In vitro maturation of human germinal vesicle stage oocytes: role of cumulus cells and epidermal growth factor in the culture medium. Hum. Reprod. 13, 1638–1644.
| In vitro maturation of human germinal vesicle stage oocytes: role of cumulus cells and epidermal growth factor in the culture medium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXkslOlurY%3D&md5=9ea8cb9823e91b87df430d9ddfc1e279CAS |
Guerif, F., McKeegan, P., Leese, H. J., and Sturmey, R. G. (2013). A simple approach for COnsumption and RElease (CORE) analysis of metabolic activity in single mammalian embryos. PLoS One 8, e67834.
| A simple approach for COnsumption and RElease (CORE) analysis of metabolic activity in single mammalian embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtleqsrvF&md5=e131bd2a02895d9943227f91d296fde2CAS |
Hardy, K. (1997). Cell death in the mammalian blastocyst. Mol. Hum. Reprod. 3, 919–925.
| Cell death in the mammalian blastocyst.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1c%2FlsFKntg%3D%3D&md5=fa02adf42426e9ad9bcfee71a1011da3CAS |
Hashimoto, S., Minami, N., Yamada, M., and Imai, H. (2000). Excessive concentration of glucose during in vitro maturation impairs the developmental competence of bovine oocytes after in vitro fertilization: relevance to intracellular reactive oxygen species and glutathione contents. Mol. Reprod. Dev. 56, 520–526.
| Excessive concentration of glucose during in vitro maturation impairs the developmental competence of bovine oocytes after in vitro fertilization: relevance to intracellular reactive oxygen species and glutathione contents.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXkslKlur8%3D&md5=2c93a943722fbaa8b9615236127dbe48CAS |
Holness, M. J., and Sugden, M. C. (2003). Regulation of pyruvate dehydrogenase complex activity by reversible phosphorylation. Biochem. Soc. Trans. 31, 1143–1151.
| Regulation of pyruvate dehydrogenase complex activity by reversible phosphorylation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXps1yqu7g%3D&md5=343d44a35972c57e914ab2d94a7a71c6CAS |
Igosheva, N., Abramov, A. Y., Poston, L., Eckert, J. J., Fleming, T. P., Duchen, M. R., and McConnell, J. (2010). Maternal diet-induced obesity alters mitochondrial activity and redox status in mouse oocytes and zygotes. PLoS One 5, e10074.
| Maternal diet-induced obesity alters mitochondrial activity and redox status in mouse oocytes and zygotes.Crossref | GoogleScholarGoogle Scholar |
Iossa, S., Mollica, M. P., Lionetti, L., Crescenzo, R., Botta, M., and Liverini, G. (2002). Skeletal muscle oxidative capacity in rats fed high-fat diet. Int. J. Obes. Relat. Metab. Disord. 26, 65–72.
| Skeletal muscle oxidative capacity in rats fed high-fat diet.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xhtleiu7Y%3D&md5=4a52047dee5e2693c1a4f044879b2c5cCAS |
Jungheim, E. S., and Moley, K. H. (2008). The impact of Type 1 and Type 2 diabetes mellitus on the oocyte and the preimplantation embryo. Semin. Reprod. Med. 26, 186–195.
| The impact of Type 1 and Type 2 diabetes mellitus on the oocyte and the preimplantation embryo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXkt1WgsrY%3D&md5=9d3d678a8124f4914629a64d1ce67cdfCAS |
Jungheim, E. S., Louden, E. D., Chi, M. M., Frolova, A. I., Riley, J. K., and Moley, K. H. (2011a). Preimplantation exposure of mouse embryos to palmitic acid results in fetal growth restriction followed by catch-up growth in the offspring. Biol. Reprod. 85, 678–683.
| Preimplantation exposure of mouse embryos to palmitic acid results in fetal growth restriction followed by catch-up growth in the offspring.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht12ht7zE&md5=ce753f51a21cf941513533c8370a4c5bCAS |
Jungheim, E. S., Macones, G. A., Odem, R. R., Patterson, B. W., Lanzendorf, S. E., Ratts, V. S., and Moley, K. H. (2011b). Associations between free fatty acids, cumulus–oocyte complex morphology and ovarian function during in vitro fertilization. Fertil. Steril. 95, 1970–1974.
| Associations between free fatty acids, cumulus–oocyte complex morphology and ovarian function during in vitro fertilization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXltFymt7s%3D&md5=519ad609bf7f7a90001c86b9c40be824CAS |
Jurisicova, A., Varmuza, S., and Casper, R. F. (1996). Programmed cell death and human embryo fragmentation. Mol. Hum. Reprod. 2, 93–98.
| Programmed cell death and human embryo fragmentation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2szotFegsA%3D%3D&md5=e6b8749b3b41e976d15dde0978410e7eCAS |
Kasper, G., Ode, A., Groothuis, A., Glaeser, J., Gaber, T., Wilson, C. J., Geissler, S., and Duda, G. N. (2010). Validation of beta-actin used as endogenous control for gene expression analysis in mechanobiology studies: amendments. Stem Cells 28, 633–634.
Kim, J. Y., Kinoshita, M., Ohnishi, M., and Fukui, Y. (2001). Lipid and fatty acid analysis of fresh and frozen–thawed immature and in vitro-matured bovine oocytes. Reproduction 122, 131–138.
| Lipid and fatty acid analysis of fresh and frozen–thawed immature and in vitro-matured bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlsVGis70%3D&md5=13bb7bf74bab482141738b873ee28d23CAS |
Krisher, R. L., and Prather, R. S. (2012). A role for the Warburg effect in preimplantation embryo development: metabolic modification to support rapid cell proliferation. Mol. Reprod. Dev. 79, 311–320.
| A role for the Warburg effect in preimplantation embryo development: metabolic modification to support rapid cell proliferation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XlsFygs7Y%3D&md5=a08c7ae5b31029fa346295ef2c4dfd48CAS |
Leary, C., Leese, H. J., and Sturmey, R. G. (2015). Human embryos from overweight and obese women display phenotypic and metabolic abnormalities. Hum. Reprod. 30, 122–132.
| Human embryos from overweight and obese women display phenotypic and metabolic abnormalities.Crossref | GoogleScholarGoogle Scholar |
Leese, H. J., and Lenton, E. A. (1990). Glucose and lactate in human follicular fluid: concentrations and interrelationships. Hum. Reprod. 5, 915–919.
| Glucose and lactate in human follicular fluid: concentrations and interrelationships.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3M7osFGmsg%3D%3D&md5=efb29052901ff987d0b4a2812da8f98aCAS |
Lehnen, H., Zechner, U., and Haaf, T. (2013). Epigenetics of gestational diabetes mellitus and offspring health: the time for action is in early stages of life. Mol. Hum. Reprod. 19, 415–422.
| Epigenetics of gestational diabetes mellitus and offspring health: the time for action is in early stages of life.Crossref | GoogleScholarGoogle Scholar |
Leroy, J. L., Vanholder, T., Delanghe, J. R., Opsomer, G., Van Soom, A., Bols, P. E., and de Kruif, A. (2004a). Metabolite and ionic composition of follicular fluid from different-sized follicles and their relationship to serum concentrations in dairy cows. Anim. Reprod. Sci. 80, 201–211.
| Metabolite and ionic composition of follicular fluid from different-sized follicles and their relationship to serum concentrations in dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXht1ygtL0%3D&md5=a803a1d9ccef431f0f50220f9b0dbea0CAS |
Leroy, J. L. M. R., Vanholder, T., Delanghe, J. R., Opsomer, G., Van Soom, A., Bols, P. E., Dewulf, J., and de Kruif, A. (2004b). Metabolic changes in follicular fluid of the dominant follicle in high-yielding dairy cows early post partum. Theriogenology 62, 1131–1143.
| Metabolic changes in follicular fluid of the dominant follicle in high-yielding dairy cows early post partum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmt1Kmsr8%3D&md5=488693da9278309bebbaa0263e39be06CAS |
Leroy, J. L., Vanholder, T., Mateusen, B., Christophe, A., Opsomer, G., de Kruif, A., Genicot, G., and Van Soom, A. (2005a). Non-esterified fatty acids in follicular fluid of dairy cows and their effect on developmental capacity of bovine oocytes in vitro. Reproduction 130, 485–495.
| Non-esterified fatty acids in follicular fluid of dairy cows and their effect on developmental capacity of bovine oocytes in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFent7rJ&md5=91880a8509879cf03ba237493485d320CAS |
Leroy, J. L. M. R., Genicot, G., Donnay, I., and Van Soom, A. (2005b). Evaluation of the lipid content in bovine oocytes and embryos with Nile red: a practical approach. Reprod. Domest. Anim. 40, 76–78.
| Evaluation of the lipid content in bovine oocytes and embryos with Nile red: a practical approach.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2M%2FivVyjsg%3D%3D&md5=016cf3b5594217f47300d2546d8a0c0bCAS |
Leroy, J. L. M. R., Vanholder, T., Opsomer, G., Van Soom, A., and de Kruif, A. (2006). The in vitro development of bovine oocytes after maturation in glucose and beta-hydroxybutyrate concentrations associated with negative energy balance in dairy cows. Reprod. Domest. Anim. 41, 119–123.
| The in vitro development of bovine oocytes after maturation in glucose and beta-hydroxybutyrate concentrations associated with negative energy balance in dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XksVygsrc%3D&md5=01cb857638c119c68168ee7a4989b288CAS |
Leroy, J. L., Vanholder, T., Van Knegsel, A. T., Garcia-Ispierto, I., and Bols, P. E. (2008a). Nutrient prioritization in dairy cows early postpartum: mismatch between metabolism and fertility? Reprod. Domest. Anim. 43, 96–103.
| Nutrient prioritization in dairy cows early postpartum: mismatch between metabolism and fertility?Crossref | GoogleScholarGoogle Scholar |
Leroy, J. L. M. R., Opsomer, G., Van Soom, A., Goovaerts, I. G., and Bols, P. E. (2008b). Reduced fertility in high-yielding dairy cows: are the oocyte and embryo in danger? Part I. The importance of negative energy balance and altered corpus luteum function to the reduction of oocyte and embryo quality in high-yielding dairy cows. Reprod. Domest. Anim. 43, 612–622.
| Reduced fertility in high-yielding dairy cows: are the oocyte and embryo in danger? Part I. The importance of negative energy balance and altered corpus luteum function to the reduction of oocyte and embryo quality in high-yielding dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1cnksVeqsg%3D%3D&md5=5207b901068c4a933459fae3e6cfdd68CAS |
Livak, K. J., and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) Method. Methods 25, 402–408.
| Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) Method.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhtFelt7s%3D&md5=27001fc4d390214adec9d2e6245c9fd6CAS |
Luciano, A. M., Modina, S., Vassena, R., Milanesi, E., Lauria, A., and Gandolfi, F. (2004). Role of intracellular cyclic adenosine 3′,5′-monophosphate concentration and oocyte–cumulus cells communications on the acquisition of the developmental competence during in vitro maturation of bovine oocyte. Biol. Reprod. 70, 465–472.
| Role of intracellular cyclic adenosine 3′,5′-monophosphate concentration and oocyte–cumulus cells communications on the acquisition of the developmental competence during in vitro maturation of bovine oocyte.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnsl2juw%3D%3D&md5=df143bd14b2b235d41dee57ebbd26da4CAS |
Marei, W. F., Ghafari, F., and Fouladi-Nashta, A. A. (2012). Role of hyaluronic acid in maturation and further early embryo development of bovine oocytes. Theriogenology 78, 670–677.
| Role of hyaluronic acid in maturation and further early embryo development of bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xmt1GqsL4%3D&md5=ef6571826bebcd29b01245c04f7daa3bCAS |
Metwally, M., Li, T. C., and Ledger, W. L. (2007). The impact of obesity on female reproductive function. Obes. Rev. 8, 515–523.
| The impact of obesity on female reproductive function.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2snisVSitw%3D%3D&md5=bd0581d31328153ee6a24d74829fdcb2CAS |
Moley, K. H., Chi, M. M., Knudson, C. M., Korsmeyer, S. J., and Mueckler, M. M. (1998). Hyperglycemia induces apoptosis in pre-implantation embryos through cell death effector pathways. Nat. Med. 4, 1421–1424.
| Hyperglycemia induces apoptosis in pre-implantation embryos through cell death effector pathways.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXnvVOhsrw%3D&md5=7c090170813313b29fc0336b9a03d4f0CAS |
Moore, S. G., Fair, T., Lonergan, P., and Butler, S. T. (2014). Genetic merit for fertility traits in Holstein cows: IV. Transition period, uterine health, and resumption of cyclicity. J. Dairy Sci. 97, 2740–2752.
| Genetic merit for fertility traits in Holstein cows: IV. Transition period, uterine health, and resumption of cyclicity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXktlWkurk%3D&md5=be81f7ff58de12d2f5f5703c010c3082CAS |
Nasr-Esfahani, M. H., Aitken, J. R., and Johnson, M. H. (1990). Hydrogen peroxide levels in mouse oocytes and early cleavage stage embryos developed in vitro or in vivo. Development 109, 501–507.
| 1:CAS:528:DyaK3cXlsV2nsbo%3D&md5=3e452df359ef8e45b6633262d3528f1eCAS |
O’Doherty, A. M., O’Gorman, A., al Naib, A., Brennan, L., Daly, E., Duffy, P., and Fair, T. (2014). Negative energy balance affects imprint stability in oocytes recovered from postpartum dairy cows. Genomics 104, 177–185.
| Negative energy balance affects imprint stability in oocytes recovered from postpartum dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXht1Kkur7L&md5=6506931d7c05b110309e5cf556e44e3aCAS |
Randle, P. J., Garland, P. B., Hales, C. N., and Newsholme, E. A. (1963). The glucose fatty-acid cycle. Its role in insulin sensitivity and the metabolic disturbances of diabetes mellitus. Lancet 281, 785–789.
| The glucose fatty-acid cycle. Its role in insulin sensitivity and the metabolic disturbances of diabetes mellitus.Crossref | GoogleScholarGoogle Scholar |
Robert, C., McGraw, S., Massicotte, L., Pravetoni, M., Gandolfi, F., and Sirard, M. A. (2002). Quantification of housekeeping transcript levels during the development of bovine preimplantation embryos. Biol. Reprod. 67, 1465–1472.
| Quantification of housekeeping transcript levels during the development of bovine preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xot1Kjs78%3D&md5=30fd6543a6af9ae0f6ed763a114decf4CAS |
Robker, R. L. (2008). Evidence that obesity alters the quality of oocytes and embryos. Pathophysiology 15, 115–121.
| Evidence that obesity alters the quality of oocytes and embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXpt1Kjurs%3D&md5=4b5c0121fe802884b78fbeda85eb10e4CAS |
Robker, R. L., Akison, L. K., Bennett, B. D., Thrupp, P. N., Chura, L. R., Russell, D. L., Lane, M., and Norman, R. J. (2009). Obese women exhibit differences in ovarian metabolites, hormones, and gene expression compared with moderate-weight women. J. Clin. Endocrinol. Metab. 94, 1533–1540.
| Obese women exhibit differences in ovarian metabolites, hormones, and gene expression compared with moderate-weight women.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlvVCqtrw%3D&md5=20826ce5cde40ed688591c2e0574aaaaCAS |
Rosen, E. D., and Spiegelman, B. M. (2006). Adipocytes as regulators of energy balance and glucose homeostasis. Nature 444, 847–853.
| Adipocytes as regulators of energy balance and glucose homeostasis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtlShtrzI&md5=911d61c141b70bcb0c7ce15bf76e0bdbCAS |
Salway, J. (1999) ‘Metabolism at a glance’. (Wiley-Blackwell: United Kingdom.)
Sinclair, K. D., and Singh, R. (2007). Modelling the developmental origins of health and disease in the early embryo. Theriogenology 67, 43–53.
| Modelling the developmental origins of health and disease in the early embryo.Crossref | GoogleScholarGoogle Scholar |
Smits, A., De Bie, J., Bols, P. E. J., Marei, W. F., and Leroy, J. L. M. R. (2016). Effect of embryo culture conditions on developmental potential of bovine oocytes matured under lipotoxic conditions. In ‘Proceedings of the 18th International Congress on Animal Reproduction, Tours, France’. (Eds F. Gandolfi, L. Brito, D. C. Sharp.) p. 279. (Elsevier: New York.)
Sturmey, R. G., and Leese, H. J. (2008). Role of glucose and fatty acid metabolism in porcine early embryo development. Reprod. Fertil. Dev. 20, 149.
| Role of glucose and fatty acid metabolism in porcine early embryo development.Crossref | GoogleScholarGoogle Scholar |
Sturmey, R. G., Reis, A., Leese, H. J., and McEvoy, T. G. (2009). Role of fatty acids in energy provision during oocyte maturation and early embryo development. Reprod. Domest. Anim. 44, 50–58.
| Role of fatty acids in energy provision during oocyte maturation and early embryo development.Crossref | GoogleScholarGoogle Scholar |
Sutton-McDowall, M. L., Gilchrist, R. B., and Thompson, J. G. (2004). Cumulus expansion and glucose utilisation by bovine cumulus–oocyte complexes during in vitro maturation: the influence of glucosamine and follicle-stimulating hormone. Reproduction 128, 313–319.
| Cumulus expansion and glucose utilisation by bovine cumulus–oocyte complexes during in vitro maturation: the influence of glucosamine and follicle-stimulating hormone.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXot1KitLk%3D&md5=bb981b99693467a2f37387ee78f826b8CAS |
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=01128e9462420c39f1187a653b345471CAS |
Valckx, S. D., De Pauw, I., De Neubourg, D., Inion, I., Berth, M., Fransen, E., Bols, P. E., and Leroy, J. L. (2012). BMI-related metabolic composition of the follicular fluid of women undergoing assisted reproductive treatment and the consequences for oocyte and embryo quality. Hum. Reprod. 27, 3531–3539.
| BMI-related metabolic composition of the follicular fluid of women undergoing assisted reproductive treatment and the consequences for oocyte and embryo quality.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhslKrsLrL&md5=f6ae888cd55bbc8979e1a212c287612fCAS |
Van Hoeck, V., Sturmey, R. G., Bermejo-Alvarez, P., Rizos, D., Gutierrez-Adan, A., Leese, H. J., Bols, P. E., and Leroy, J. L. (2011). Elevated non-esterified fatty acid concentrations during bovine oocyte maturation compromise early embryo physiology. PLoS One 6, e23183.
| Elevated non-esterified fatty acid concentrations during bovine oocyte maturation compromise early embryo physiology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFKmsLjM&md5=e9fc8e01471a033adbaebf967955952eCAS |
Van Hoeck, V., De Bie, J., Andries, S., Merckx, E., Bols, P. E. J., and Leroy, J. L. M. R. (2012). Elevated concentrations of saturated NEFA during bovine in vitro embryo culture compromise pre-implantation embryo development. In ‘Proceedings of the 28th Scientific Meeting AETE, St-Malo, France’. (Ed. U. Besenfelder.) p. 224.
Van Hoeck, V., Leroy, J. L. M. R., Arias-Alvarez, M., Rizos, D., Gutierrez-Adan, A., Schnorbusch, K., Bols, P. E. J., Leese, H. J., and Sturmey, R. G. (2013). Oocyte developmental failure in response to elevated non-esterified fatty acid concentrations: mechanistic insights. Reproduction 145, 33–44.
| Oocyte developmental failure in response to elevated non-esterified fatty acid concentrations: mechanistic insights.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhslGisb8%3D&md5=451b5a7b9c07dd9b3a281751d0ce2968CAS |
Vanholder, T., Leroy, J. L., Soom, A. V., Opsomer, G., Maes, D., Coryn, M., and de Kruif, A. (2005). Effect of non-esterified fatty acids on bovine granulosa cell steroidogenesis and proliferation in vitro. Anim. Reprod. Sci. 87, 33–44.
| Effect of non-esterified fatty acids on bovine granulosa cell steroidogenesis and proliferation in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXktVOju74%3D&md5=bb31a24ec3a3d775e2fbce41f89e1188CAS |
Wallace, M., Cottell, E., Gibney, M. J., McAuliffe, F. M., Wingfield, M., and Brennan, L. (2012). An investigation into the relationship between the metabolic profile of follicular fluid, oocyte developmental potential, and implantation outcome. Fertil. Steril. 97, 1078–1084.e8.
| An investigation into the relationship between the metabolic profile of follicular fluid, oocyte developmental potential, and implantation outcome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XmtFGhu7g%3D&md5=5da436b06b20f9fdd2955ad346a21175CAS |
Wolfe, R. R. (1998). Metabolic interactions between glucose and fatty acids in humans. Am. J. Clin. Nutr. 67, 519S–526S.
| 1:CAS:528:DyaK1cXhtlyiu7Y%3D&md5=e836d6adc1b243aca3cbc836d036286fCAS |
Wydooghe, E., Vandaele, L., Beek, J., Favoreel, H., Heindryckx, B., De Sutter, P., and Van Soom, A. (2011). Differential apoptotic staining of mammalian blastocysts based on double immunofluorescent CDX2 and active caspase-3 staining. Anal. Biochem. 416, 228–230.
| Differential apoptotic staining of mammalian blastocysts based on double immunofluorescent CDX2 and active caspase-3 staining.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXptVaku7o%3D&md5=d8023dda2022c285bcde916f2b4114daCAS |
Wyman, A., Pinto, A. B., Sheridan, R., and Moley, K. H. (2008). One-cell zygote transfer from diabetic to nondiabetic mouse results in congenital malformations and growth retardation in offspring. Endocrinology 149, 466–469.
| One-cell zygote transfer from diabetic to nondiabetic mouse results in congenital malformations and growth retardation in offspring.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1yqsLc%3D&md5=334b14893bc792819d7343432c0bb38fCAS |
Xie, H. L., Wang, Y. B., Jiao, G. Z., Kong, D. L., Li, Q., Li, H., Zheng, L. L., and Tan, J. H. (2016). Effects of glucose metabolism during in vitro maturation on cytoplasmic maturation of mouse oocytes. Sci. Rep. 6, 20764.
| Effects of glucose metabolism during in vitro maturation on cytoplasmic maturation of mouse oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XisVant7w%3D&md5=d2e4400cf6c95a6ae3a8f642df31850cCAS |
Yuan, Y. Q., Van Soom, A., Leroy, J. L., Dewulf, J., Van Zeveren, A., de Kruif, A., and Peelman, L. J. (2005). Apoptosis in cumulus cells, but not in oocytes, may influence bovine embryonic developmental competence. Theriogenology 63, 2147–2163.
| Apoptosis in cumulus cells, but not in oocytes, may influence bovine embryonic developmental competence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjtFyrtb8%3D&md5=7d5bacf4d1adb2c1df62c58016451534CAS |
