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Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Oxygen consumption by bovine granulosa cells with prediction of oxygen transport in preantral follicles

Dongxing Li A , Gabe P. Redding A B and John E. Bronlund A
+ Author Affiliations
- Author Affiliations

A School of Engineering and Advanced Technology, Massey University, Private Bag 11222, Palmerston North 4414, New Zealand.

B Corresponding author. Email: g.p.redding@massey.ac.nz

Reproduction, Fertility and Development 25(8) 1158-1164 https://doi.org/10.1071/RD12283
Submitted: 30 August 2012  Accepted: 30 October 2012   Published: 28 November 2012

Abstract

The rate of oxygen consumption by granulosa cells is a key parameter in mathematical models that describe oxygen transport across ovarian follicles. This work measured the oxygen consumption rate of bovine granulosa cells in vitro to be in the range 2.1–3.3 × 10–16 mol cell–1 s–1 (0.16–0.25 mol m–3 s–1). The implications of the rates for oxygen transport in large bovine preantral follicles were examined using a mathematical model. The results indicate that oocyte oxygenation becomes increasingly constrained as preantral follicles grow, reaching hypoxic levels near the point of antrum formation. Beyond a preantral follicle radius of 134 µm, oxygen cannot reach the oocyte surface at typical values of model parameters. Since reported sizes of large bovine preantral follicles range from 58 to 145 µm in radius, this suggests that oocyte oxygenation is possible in all but the largest preantral follicles, which are on the verge of antrum formation. In preantral bovine follicles, the oxygen consumption rate of granulosa cells and fluid voidage will be the key determinants of oxygen levels across the follicle.

Additional keyword: hypoxia.


References

Braems, G., and Jensen, A. (1991). Hypoxia reduces oxygen consumption of fetal skeletal muscle cells in monolayer culture. J. Dev. Physiol. 16, 209–215.
| 1:STN:280:DyaK383ltFSkuw%3D%3D&md5=3765707ba0f9828f4f5bd8c2d5f65649CAS | 1812155PubMed |

Braw-Tal, R., and Yoseffi, S. (1997). Studies in vivo and in vitro on the initiation of follicle growth in the bovine ovary. J. Reprod. Fertil. 109, 165–171.
Studies in vivo and in vitro on the initiation of follicle growth in the bovine ovary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXhs1Gls7w%3D&md5=f85701e1b0856d7c721b0377c4c97bf1CAS | 9068428PubMed |

Calado, A. M., Rocha, E., Colaco, A., and Sousa, M. (2001). Stereologic characterization of bovine (Bos taurus) cumulus–oocyte complexes aspirated from small antral follicles during dioestrous phase. Biol. Reprod. 65, 1383–1391.
Stereologic characterization of bovine (Bos taurus) cumulus–oocyte complexes aspirated from small antral follicles during dioestrous phase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnvVersrs%3D&md5=5fde39208e4a010ab3a24d56770b1ba4CAS | 11673254PubMed |

Clark, A. R., and Stokes, Y. M. (2011). Follicle structure influences the availability of oxygen to the oocyte in antral follicles. Comput. Math. Methods Med. 2011, Article ID 287186.
Follicle structure influences the availability of oxygen to the oocyte in antral follicles.Crossref | GoogleScholarGoogle Scholar |

Ducommun, P., Ruffieux, P., Furter, M., Marison, I., and von Stockar, U. (2000). A new method for on-line measurement of the volumetric oxygen uptake rate in membrane aerated animal cell cultures. J. Biotechnol. 78, 139–147.
A new method for on-line measurement of the volumetric oxygen uptake rate in membrane aerated animal cell cultures.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhvVOrtrw%3D&md5=6638b038e20367267de160773873809fCAS | 10725537PubMed |

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=b962e7f9caf32dc872503a0dc60b91f2CAS | 16804881PubMed |

Fraser, H. M. (2006). Regulation of ovarian follicular vasculature. Reprod. Biol. Endocrin. 4, .
Regulation of ovarian follicular vasculature.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XktVCqtbk%3D&md5=8022cd7863a35fb01a6f9aff31a9bcfeCAS |

Gosden, R. G., and Byatt-Smith, J. G. (1986). Oxygen concentration gradient across the ovarian follicular epithelium: model, predictions and implications. Hum. Reprod. 1, 65–68.
| 1:STN:280:DyaL2s7ms1Kgsw%3D%3D&md5=0cfb3859899974264728b368d625c87bCAS | 3558757PubMed |

Hitchman, M. L. (1978). ‘Measurement of Dissolved Oxygen’. (Wiley: New York.)

Li, R., Norman, R. J., Armstrong, D. T., and Gilchrist, R. B. (2000). Oocyte-secreted factor(s) determine functional differences between bovine mural granulosa cells and cumulus cells. Biol. Reprod. 63, 839–845.
Oocyte-secreted factor(s) determine functional differences between bovine mural granulosa cells and cumulus cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXmtFCiu7g%3D&md5=6f2297f2e8242d9159ff9b0c17e39d90CAS | 10952929PubMed |

Lussier, J. G., Matton, P., and Dufour, J. J. (1987). Growth rates of follicles in the ovary of the cow. J. Reprod. Fertil. 81, 301–307.
Growth rates of follicles in the ovary of the cow.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1c7hvVGisg%3D%3D&md5=47733cc6c40c7396db777d5427cc03eeCAS | 3430454PubMed |

Marion, G. B., Gier, H. T., and Choudary, J. B. (1968). Micromorphology of the bovine ovarian follicular system. J. Anim. Sci. 27, 451–465.
| 1:STN:280:DyaF1c7pvVOrug%3D%3D&md5=3d1c6f8416786cb0ee6e93c7b9cceae8CAS | 5646345PubMed |

Monniaux, D., Mariana, J. C., and Gibson, W. R. (1984). Action of PMSG on follicular populations in the heifer. J. Reprod. Fertil. 70, 243–253.
Action of PMSG on follicular populations in the heifer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXotVSktg%3D%3D&md5=2a41c4a4b6a454cfefc43033f0c2856cCAS | 6694142PubMed |

Redding, G. P., Bronlund, J. E., and Hart, A. L. (2007). Mathematical modelling of oxygen transport limited follicle growth. Reproduction 133, 1095–1106.
Mathematical modelling of oxygen transport limited follicle growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpsVGnu7c%3D&md5=92aa013886794f97362647bfcc7aa53aCAS | 17636164PubMed |

Redding, G. P., Bronlund, J. E., and Hart, A. L. (2008). Theoretical investigation into the dissolved oxygen levels in follicular fluid of the developing human follicle using mathematical modelling. Reprod. Fertil. Dev. 20, 408–417.
Theoretical investigation into the dissolved oxygen levels in follicular fluid of the developing human follicle using mathematical modelling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjtVKksL0%3D&md5=0378d45fa191dfc6d955798fd6dff22fCAS | 18402761PubMed |

Riley, M. R., Muzzio, F. J., Buettner, H. M., and Reyes, S. C. (1994). Monte Carlo calculation of effective diffusivities in two- and three-dimensional heterogeneous materials of variable structure. Phys. Rev. E Stat. Phys. Plasmas Fluids Relat. Interdiscip. Topics 49, 3500–3503.
Monte Carlo calculation of effective diffusivities in two- and three-dimensional heterogeneous materials of variable structure.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXjtVyjs78%3D&md5=bfb08fdabc3646d4d5035fe4746610cbCAS | 9961622PubMed |

Riley, M. R., Muzzio, F. J., Buettner, H. M., and Reyes, S. C. (1995). Diffusion in heterogeneous media: application to immobilized cell systems. AlChE. J. 41, 691–700.
Diffusion in heterogeneous media: application to immobilized cell systems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXkt1aisro%3D&md5=c031fa371b0753c8c02e1fcc9375c353CAS |

Riley, M. R., Muzzio, F. J., Buettner, H. M., and Reyes, S. C. (1996). A simple correlation for predicting effective diffusivities in immobilized cell systems. Biotechnol. Bioeng. 49, 223–227.
A simple correlation for predicting effective diffusivities in immobilized cell systems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XislantQ%3D%3D&md5=82643869d66a64b0b6d5892f7b988aa7CAS | 18623572PubMed |

Ruffieux, P., von Stockar, U., and Marison, I. W. (1998). Measurement of volumetric (OUR) and determination-specific (qO2) oxygen uptake rates in animal cell cultures. J. Biotechnol. 63, 85–95.
Measurement of volumetric (OUR) and determination-specific (qO2) oxygen uptake rates in animal cell cultures.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXltFWqsrk%3D&md5=f8a7807687f75f509b14691fff91218dCAS | 9772750PubMed |

Sugiura, K., Pendola, F. L., and Eppig, J. J. (2005). Oocyte control of metabolic cooperativity between oocytes and companion granulosa cells: energy metabolism. Dev. Biol. 279, 20–30.
Oocyte control of metabolic cooperativity between oocytes and companion granulosa cells: energy metabolism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtlemtb4%3D&md5=6f20796c271967b6d76d4e935e4c9465CAS | 15708555PubMed |

Truskey, G. A., Yuan, F., and Katz, D. F. (2004). ‘Transport in Porous Media’. (Pearson Prentice Hall: New Jersey.)

Van Blerkom, J., Antczak, M., and Schrader, R. (1997). The developmental potential of the human oocyte is related to the dissolved oxygen content of follicular fluid: association with vascular endothelial growth factor levels and perifollicular blood flow characteristics. Hum. Reprod. 12, 1047–1055.
The developmental potential of the human oocyte is related to the dissolved oxygen content of follicular fluid: association with vascular endothelial growth factor levels and perifollicular blood flow characteristics.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2szjsl2qsQ%3D%3D&md5=fb11df80eff8ed7bd07ee56df749bfe9CAS | 9194664PubMed |

Wagner, A. E., Muir, W. W., and Grospitch, B. J. (1990). Cardiopulmonary effects of position in conscious cattle. Am. J. Vet. Res. 51, 7–10.
| 1:STN:280:DyaK3c7ksFOrsQ%3D%3D&md5=0510fcb2a974ce1eb15d4fa7adb02d0dCAS | 2301822PubMed |