An investigation by mathematical modelling of whether mouse and human preimplantation embryos in static culture can satisfy their demands for oxygen by diffusion

Byatt-Smith, J. G. B.; Leese, Henry J.; Gosden, R. G.

doi:10.1093/oxfordjournals.humrep.a137258

Cited by 53 publications

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“…Warburg's (1923) model assumes that concentration is constant in a plane and varies in the direction normal to the plane. More recently, the spherically symmetric form of the steady-state diffusion equation has been employed for modelling oxygen concentrations in ovarian follicles (Gosden & Byatt-Smith 1986) and in preimplantation embryos in static culture (Byatt-Smith et al 1991).…”

Section: Discussionmentioning

confidence: 99%

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Mathematical modelling of oxygen concentration in bovine and murine cumulus–oocyte complexes

Clark¹,

Stokes²,

Lane³

et al. 2006

Reproduction

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Immature oocytes benefit from nutrient modification of the follicular environment by the surrounding cumulus mass. However, the oxygen concentration that the oocyte may be exposed to could be lower than the antral follicular concentration due to the metabolism of surrounding cumulus cells. Using metabolic data previously determined, we have developed a mathematical model of O 2 diffusion across the bovine and murine cumulus-oocyte complex. From this we have determined that across a physiological range of external pO 2 , less than 0.25% and 0.5% O 2 is removed by cumulus cells within the bovine and murine cumulus-oocyte complex respectively. Our model differs from others as it: incorporates a term that allows for nonlinear variation of the oxygen consumption rate with oxygen concentration; considers two regions (oocyte and cumulus) sharing a common boundary, both of which consume oxygen at different non linear rates. Cumulus cells therefore remove little O 2 , thus sparing this essential gas for the oocyte, which is dependent on ATP generation via oxidative phosphorylation.

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Section: Discussionmentioning

confidence: 99%

“…Gosden & Byatt-Smith 1986, Byatt-Smith et al 1991 is to solve a diffusion-equation model with the rate of oxygen consumption assumed to be constant or proportional to the oxygen concentration. This assumption allows analytical solution of the governing equations.…”

Section: Mathematical Modelmentioning

confidence: 99%

Mathematical modelling of oxygen concentration in bovine and murine cumulus–oocyte complexes

Clark¹,

Stokes²,

Lane³

et al. 2006

Reproduction

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“…More convincingly, incubation in 5% O 2 compared with 20% O 2 increases oxygen uptake and pyruvate oxidation (Hooper et al, 2001). This finding is significant as the effect of a reduction in O 2 tension from atmospheric levels to 5% within embryos has also been examined using a mathematical model (Byatt-Smith et al, 1991). Byatt-Smith et al (1991) showed that for small mammalian embryos, such as mouse embyros, O 2 from a 5% atmosphere would be able to sustain oxidative phosphorylation throughout development, albeit under hypoxic conditions.…”

Section: Manipulation Of Substrates and Metabolic Pathways During Devmentioning

confidence: 99%

“…This finding is significant as the effect of a reduction in O 2 tension from atmospheric levels to 5% within embryos has also been examined using a mathematical model (Byatt-Smith et al, 1991). Byatt-Smith et al (1991) showed that for small mammalian embryos, such as mouse embyros, O 2 from a 5% atmosphere would be able to sustain oxidative phosphorylation throughout development, albeit under hypoxic conditions. However, larger embryos, such as human or cattle embryos, would establish a significant gradient leading to anoxia in the centre of the embryo, which may explain some of the metabolic differences among embryos of different species.…”

Section: Manipulation Of Substrates and Metabolic Pathways During Devmentioning

confidence: 99%

REDOX regulation of early embryo development

Harvey

Kind²,

Thompson³

2002

Reproduction

297

144

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Early embryo development requires energy (that is, the formation of adenosine triphosphate, ATP), which is produced through two possible mechanisms: glycolysis, using glucose as a substrate, and oxidative phosphorylation, using pyruvate or oxaloacetate as a substrate. The pioneering work of Brinster, Biggers, Whitten, Whittingham and Wales from the late 1950s to the early 1970s revealed that for mouse embryo development to the blastocyst stage, pyruvate or oxaloacetate are essential for early cleavage, but that glucose is an effective substrate from the eight-cell stage (Bavister, 1995; Wales, 1975). These studies were the first to reveal that a change in metabolic state is involved in the control of early development and led many other workers to examine the concentrations of exogenous energy substrates required for optimal ex vivo embryo development (Bavister, 1995).Another key energy substrate (although usually not considered as such) is oxygen (Fig. 1). Oxygen is essential for the conversion of ADP to ATP in oxidative phosphorylation through its role as an electron acceptor in the electron transport chain. However, the use of oxygen as an energy substrate also results in the production of reactive oxygen species (ROS), particularly the superoxide anion (O 2 -• ) and the hydroxyl radical (OH • ). ROS are highly active electron acceptors, able to strip electrons from other molecules that, in turn, become free radicals. Hydrogen peroxide (H 2 O 2 ) is not a radical per se, but is a product of O 2 -• and metal ion catalysis. However, both H 2 O 2 and O 2 -• can form the extremely reactive OH • . The over-generation of intracellular ROS during culture of mammalian embryos in vitro is generally thought to be detrimental to embryo development (reviewed by Johnson and Nasr-Esfahani, 1994; Guerin et al., 2001). The consensus view is that 'over-production' of ROS is unfavourable for embryo development, coincident with perturbed metabolic activity. We believe this to be an overly simplistic view and prefer to think in terms of altered reduction-oxidation (REDOX) states, in which a prolonged oxidized state within the embryo, especially after early cleavage, is not favourable for embryo development. Other in vitro culture conditions may also shift the REDOX state unfavourably. Furthermore, there are some specific events in development that appear to be associated with a change in the REDOX state, indicating that REDOX state has a causative role. These events include sperm-mediated oocyte activation, embryonic genome activation and embryonic hatching from the zona pellucida. Intracellular reduction-oxidation statesThe intracellular REDOX state describes a complex interaction of the relative concentrations of reduced and oxidized forms of a variety of molecules, including the nicotinamide adenine nucleotides (NAD(P) + /NAD(P)H), flavins (FAD + /FADH), ubiquinones, peroxides and thiols-disulphides (for example, glutathione (GSH/GSSG)), and others (Fig. 1) REDOX state is also significantly influenced by factors that stimul...

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“…As shown in a mathematical model by ByattSmith et al [3], the culture of human embryos in a static microdrop may become marginally hypoxic, especially at lower oxygen levels (5 % O 2 ).…”

Section: Discussionmentioning

confidence: 99%

Reduced blastocyst formation in reduced culture volume

Munck¹,

Santos‐Ribeiro

Mateizel³

et al. 2015

J Assist Reprod Genet

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Purpose The aim of this prospective sibling oocyte study was to evaluate whether reduced culture volume improves blastocyst formation. Methods Twenty-three patients with extended embryo culture until day 5 were selected for the study. After injection, 345 sibling oocytes were individually cultured in either 25 or 7 μl droplets of Origio cleavage medium under oil. On day 3 of development, embryos were transferred to droplets with the corresponding volume of Origio blastocyst culture medium. Fertilization and embryo quality on day 3 and day 5/6 were evaluated. Results No statistically significant difference (p=0.326) in fertilization rate was observed (81.3 versus 83.0 %). There was no significant difference in terms of the number of excellent and good-quality embryos obtained on day 3 between both groups (p=0.655). Embryo culture in 25 μl droplets led to more embryos with a higher cell number when compared to 7 μl culture (p=0.024). On day 3, 132 and 131 embryos were considered for further culture until day 5/6. Blastulation rates were significantly higher in the 25 μl group (75.0 versus 61.6 %; p=0.017) and significantly more day 5 embryos with excellent and good quality were found in this group (54.5 versus 40.5 %; p=0.026). Finally, the utilization rates expressed per mature oocyte (41.4 versus 29.8 %; p=0.043), per fertilized oocyte (50.7 versus 36.6 %; p=0.023), and per day 3 embryo undergoing extended culture to day 5/6 (54.5 versus 39.7 %; p=0.019) were all significantly higher in the 25 μl group. Conclusion Reduced culture volume (7 μl) negatively impacts early development by reducing the cell number on day 3 and both blastocyst formation and quality.

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An investigation by mathematical modelling of whether mouse and human preimplantation embryos in static culture can satisfy their demands for oxygen by diffusion

Cited by 53 publications

References 0 publications

Mathematical modelling of oxygen concentration in bovine and murine cumulus–oocyte complexes

Mathematical modelling of oxygen concentration in bovine and murine cumulus–oocyte complexes

REDOX regulation of early embryo development

Reduced blastocyst formation in reduced culture volume

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