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Vertebrate reproductive science and technology
REVIEW

History of oocyte and embryo metabolism

Henry J. Leese
+ Author Affiliations
- Author Affiliations

Metabolic Research Unit, Centre for Cardiovascular and Metabolic Research, Hull York Medical School, University of Hull, Hull HU6 7RX, UK. Email: henry.leese@hyms.ac.uk

Reproduction, Fertility and Development 27(4) 567-571 https://doi.org/10.1071/RD14278
Submitted: 30 July 2014  Accepted: 10 January 2015   Published: 20 February 2015

Abstract

The basic pattern of metabolism in mammalian oocytes and early embryos was established in the 1960s and 1970s, largely in terms of the consumption of oxygen and the utilisation of nutrients present in culture media at the time, mainly glucose, pyruvate and lactate. The potential importance of endogenous fuels was also recognised but was largely ignored, only to be rediscovered quite recently. The 1980s and 1990s saw the arrival of a ‘new generation’ of culture media, characterised metabolically by the addition of amino acids, an initiative driven strongly by the need to improve embryo culture and selection methods in assisted reproductive technologies. This trend has continued alongside some basic metabolic studies and the general recognition of the importance of metabolism in all aspects of biology. A framework for future studies on oocyte and early embryo metabolism has been provided by: (1) the developmental origins of health and disease concept and recognition of the relationship between development, epigenetics and metabolism; (2) the need to understand cell signalling within, and between the cells of, the early embryo; and (3) the importance of identifying the mechanisms underlying dialogue between the oocyte and early embryo and the female reproductive tract.

Additional keywords: assisted reproductive technologies, culture media, energy sources, mammalian.


References

Barbehenn, E. K., Wales, R. G., and Lowry, O. H. (1978). Measurement of metabolites in single preimplantation embryos; a new means to study metabolic control in early embryos. J. Embryol. Exp. Morphol. 43, 29–46.
| 1:CAS:528:DyaE1cXhtlarur0%3D&md5=b84072e2f2cf296fadcff50d771fda09CAS | 580293PubMed |

Barker, D. J., Winter, P. D., Osmond, C., Margetts, B., and Simmonds, S. J. (1989). Weight in infancy and death from ischaemic heart disease. Lancet 334, 577–580.
Weight in infancy and death from ischaemic heart disease.Crossref | GoogleScholarGoogle Scholar |

Brinster, R. L. (1973). Nutrition and metabolism of the ovum, zygote and blastocyst. In ‘Handbook of Physiology’. (Eds R. O. Greep and E. D. Astwood.) pp. 165–185. (American Physiological Society: Washington, DC.)

Brison, D. R., Houghton, F. D., Falconer, D., Roberts, S. A., Hawkhead, J., Humpherson, P. G., Lieberman, B. A., and Leese, H. J. (2004). Identification of viable embryos in IVF by non-invasive measurement of amino acid turnover. Hum. Reprod. 19, 2319–2324.
Identification of viable embryos in IVF by non-invasive measurement of amino acid turnover.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXns1OmsrY%3D&md5=3ff2d5fd93abbd46cff68c534c3e2688CAS | 15298971PubMed |

Chason, R. J., Csokmay, J., Segars, J. H., DeCherney, A. H., and Armant, D. R. (2011). Environmental and epigenetic effects upon preimplantation embryo metabolism and development. Trends Endocrinol. Metab. 22, 412–420.
Environmental and epigenetic effects upon preimplantation embryo metabolism and development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1eit7rL&md5=215c6dc57164cdb306069002b5ce3dd9CAS | 21741268PubMed |

DeBerardinis, R. J., and Thompson, C. B. (2012). Cellular metabolism and disease: what do metabolic outliers teach us? Cell 148, 1132–1144.
Cellular metabolism and disease: what do metabolic outliers teach us?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xkt1Ggt7w%3D&md5=3988bb293fde3515b928bd145f08a7caCAS | 22424225PubMed |

Devreker, F., Hardy, K., Van den Bergh, M., Vannin, A. S., Emiliani, S., and Englert, Y. (2001). Amino acids promote human blastocyst development in vitro. Hum. Reprod. 16, 749–756.
Amino acids promote human blastocyst development in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjsFSisrg%3D&md5=11bbe71027ee22f33e66ad3e312f3474CAS | 11278228PubMed |

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 |

Eckert, J. J., and Fleming, T. P. (2008). Tight junction biogenesis during early development. Biochim. Biophys. Acta 1778, 717–728.
Tight junction biogenesis during early development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjtVSqt7c%3D&md5=74e35db34ff59fe17a4eb7bcdd66f3c9CAS | 18339299PubMed |

Eckert, J. J., Porter, R., Watkins, A. J., Burt, E., Brooks, S., Leese, H. J., Humpherson, P. G., Cameron, I. T., and Fleming, T. P. (2012). Metabolic induction and early responses of mouse blastocyst developmental programming following maternal low protein diet affecting life-long health. PLoS ONE 7, e52791.
Metabolic induction and early responses of mouse blastocyst developmental programming following maternal low protein diet affecting life-long health.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXnsVKmtg%3D%3D&md5=646873f5cb17b61f90fc321f8cf61fbdCAS | 23300778PubMed |

Elder, K., and Cohen, J. (2007). ‘Human Preimplantation Embryo Selection.’ (Informa Healthcare: London.)

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=f2578182c56ab88a367fbfe61db95607CAS | 16804881PubMed |

Forde, N., Simintiras, C. A., Sturmey, R., Mamo, S., Kelly, A. K., Spencer, T. E., Bazer, F. W., and Lonergan, P. (2014). Amino acids in the uterine luminal fluid reflects the temporal changes in transporter expression in the endometrium and conceptus during early pregnancy in cattle. PLoS ONE 9, e100010.
Amino acids in the uterine luminal fluid reflects the temporal changes in transporter expression in the endometrium and conceptus during early pregnancy in cattle.Crossref | GoogleScholarGoogle Scholar | 24960174PubMed |

Fritz, R., Jain, C., and Armant, D. R. (2014). Cell signaling in trophoblast–uterine communication. Int. J. Dev. Biol. 58, 261–271.
Cell signaling in trophoblast–uterine communication.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhslSrsL3K&md5=2ceea5b01cb67897c6dc340ea277af1dCAS | 25023692PubMed |

Gardner, D. K., Lane, M., Spitzer, A., and Batt, P. A. (1994). Enhanced rates of cleavage and development of sheep zygotes cultured to the blastocyst stage in vitro in the absence of serum and somatic cells: amino acids, vitamins and culturing embryos in groups stimulate development. Biol. Reprod. 50, 390–400.
Enhanced rates of cleavage and development of sheep zygotes cultured to the blastocyst stage in vitro in the absence of serum and somatic cells: amino acids, vitamins and culturing embryos in groups stimulate development.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2c7ptFWisA%3D%3D&md5=43f76c2437603172743d672e15b6abdaCAS | 8142556PubMed |

Gardner, D. K., Wale, P. L., Collins, R., and Lane, M. (2011). Glucose consumption of single post-compaction human embryos is predictive of embryo sex and live birth outcome. Hum. Reprod. 26, 1981–1986.
Glucose consumption of single post-compaction human embryos is predictive of embryo sex and live birth outcome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXptFCnsbw%3D&md5=a296d48ffa89da35a0f6ef4f0e9c752aCAS | 21572086PubMed |

Harper, J., Magli, M. C., Lundin, K., Barratt, C. L. R., and Brison, D. (2012). When and how should new technology be introduced into the IVF laboratory? Hum. Reprod. 27, 303–313.
When and how should new technology be introduced into the IVF laboratory?Crossref | GoogleScholarGoogle Scholar | 22166806PubMed |

Hemmings, K. E., Leese, H. J., and Picton, H. M. (2012). Amino acid turnover by bovine oocytes provides an index of oocyte developmental competence in vitro. Biol. Reprod. 86, 165.
Amino acid turnover by bovine oocytes provides an index of oocyte developmental competence in vitro.Crossref | GoogleScholarGoogle Scholar | 22378762PubMed |

Houghton, F. D., Hawkhead, J. A., Humpherson, P. G., Hogg, J. E., Balen, A. H., Rutherford, A. J., and Leese, H. J. (2002). Non-invasive amino acid turnover predicts human embryo developmental capacity. Hum. Reprod. 17, 999–1005.
Non-invasive amino acid turnover predicts human embryo developmental capacity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xjs12isLg%3D&md5=adfd3bb337f670f6d799e1d8fe73da21CAS | 11925397PubMed |

Ikeda, S., Koyama, H., Sugimoto, M., and Kume, S. (2012). Roles of one-carbon metabolism in preimplantation period: effects on short-term development and long-term programming. J. Reprod. Dev. 58, 38–43.
Roles of one-carbon metabolism in preimplantation period: effects on short-term development and long-term programming.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XlvVOntr8%3D&md5=8796fb5b0d195ad69c4b50222fcfd55aCAS | 22450283PubMed |

Jansen, S., Cashman, K., Thompson, J. G., Pantaleon, M., and Kaye, P. L. (2009). Glucose deprivation, oxidative stress and peroxisome proliferator-activated receptor-alpha (PPARα) cause peroxisome proliferation in preimplantation mouse embryos. Reproduction 138, 493–505.
Glucose deprivation, oxidative stress and peroxisome proliferator-activated receptor-alpha (PPARα) cause peroxisome proliferation in preimplantation mouse embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFOgtrvK&md5=e9a0b52a0d88fd9f1cf789f852b406b8CAS | 19531609PubMed |

Johnson, M. H. (2002). Only the best conceptus will do! But what does best mean? In: ‘Assessment of Mammalian Embryo Quality’. (Eds A. Van Soom and M. Boerjan). pp. xiii–xxvii. (Kluwer Academic Publishers: Dortrecht.)

Juetten, J., and Bavister, B. D. (1983). The effects of amino acids, cumulus cells, and bovine serum albumin on in vitro fertilization and first cleavage of hamster eggs. J. Exp. Zool. 227, 487–490.
The effects of amino acids, cumulus cells, and bovine serum albumin on in vitro fertilization and first cleavage of hamster eggs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXmtFSgtbY%3D&md5=3f2447fd96a202857248f9b7903c8273CAS | 6685753PubMed |

Kane, M. T. (1987). Minimal nutrient requirements for culture of one-cell rabbit embryos. Biol. Reprod. 37, 775–778.
Minimal nutrient requirements for culture of one-cell rabbit embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXjsVCisw%3D%3D&md5=ee0f6cd8e31debc75c676d3863eacbceCAS | 3689846PubMed |

Leese, H. J. (2012). Metabolism of the preimplantation embryo: 40 years on. Reproduction 143, 417–427.
Metabolism of the preimplantation embryo: 40 years on.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XntV2ns7k%3D&md5=f555309438a1c10cea0035b1d323ea61CAS | 22408180PubMed |

Leese, H. J., and Whittall, H. (2001). Regulation of the transition from research to clinical practice in human assisted conception. Hum. Fertil. (Camb.) 4, 172–176.
Regulation of the transition from research to clinical practice in human assisted conception.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MrksVKkug%3D%3D&md5=56b40e80bfb2ca638a3bbde5ac35ace3CAS | 11591276PubMed |

Martin, P. M., and Sutherland, A. E. (2001). Exogenous amino acids regulate trophectoderm differentiation in the mouse blastocyst through an mTOR-dependent pathway. Dev. Biol. 240, 182–193.
Exogenous amino acids regulate trophectoderm differentiation in the mouse blastocyst through an mTOR-dependent pathway.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXptFegt7s%3D&md5=1da7c1b643887577cc52595f9c73d4b1CAS | 11784055PubMed |

Menezo, Y., Khatchadourian, C., Gharib, A., Hamidi, J., Greenland, T., and Sarda, N. (1989). Regulation of S-adenosyl methionine synthesis in the mouse embryo. Life Sci. 44, 1601–1609.
Regulation of S-adenosyl methionine synthesis in the mouse embryo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXksFClu7g%3D&md5=ac6511201f0ccc142bb375c5bffb7e26CAS | 2733543PubMed |

Metallo, C. M., and Vander Heiden, M. G. (2010). Metabolism strikes back: metabolic flux regulates cell signalling. Genes Dev. 24, 2717–2722.
Metabolism strikes back: metabolic flux regulates cell signalling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXltVGn&md5=37a9bdf3ce114081ba199efed502fadfCAS | 21159812PubMed |

O’Neill, C. (2008). The potential roles for embryotrophic ligands in preimplantation embryo development. Hum. Reprod. Update 14, 275–288.
The potential roles for embryotrophic ligands in preimplantation embryo development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXkvFOqtbw%3D&md5=e525251ddaaac37eb7bb54cb28b9db3cCAS | 18281694PubMed |

Pearsall, J. (Ed.) (1999). ‘The Concise Oxford Dictionary. 10th edn.’ (Oxford University Press: Oxford)

Rieger, D., Loskutoff, N. M., and Betteridge, K. J. (1992). Developmentally related changes in the metabolism of glucose and glutamine by cattle embryos produced and co-cultured in vitro. J. Reprod. Fertil. 95, 585–595.
Developmentally related changes in the metabolism of glucose and glutamine by cattle embryos produced and co-cultured in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XlsVOrt7g%3D&md5=ede4728c386ea85ddaa71a89299aac30CAS | 1518013PubMed |

Robertson, S. A., Chin, P. Y., Glynn, D. J., and Thompson, J. G. (2011). Peri-conceptual cytokines: setting the trajectory for embryo implantation, pregnancy and beyond. Am. J. Reprod. Immunol. 66, 2–10.
Peri-conceptual cytokines: setting the trajectory for embryo implantation, pregnancy and beyond.Crossref | GoogleScholarGoogle Scholar | 21726333PubMed |

Steegers-Theunissen, R. P., Twigt, J., Pestinger, V., and Sinclair, K. D. (2013). The periconceptional period, reproduction and long-term health of offspring: the importance of one-carbon metabolism. Hum. Reprod. Update 19, 640–655.
The periconceptional period, reproduction and long-term health of offspring: the importance of one-carbon metabolism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhs1GqurnM&md5=2ad85c89624602a89ddf97ff4a456cd3CAS | 23959022PubMed |

Sturmey, R. G., and Leese, H. J. (2003). Energy metabolism in pig oocytes and early embryos. Reproduction 126, 197–204.
Energy metabolism in pig oocytes and early embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXntFyjtr4%3D&md5=64ce8e53c53d9e7b3d87d6e095fa23a0CAS | 12887276PubMed |

Sturmey, R. G., O’Toole, P. J., and Leese, H. J. (2006). Fluorescence resonance energy transfer analysis of mitochondrial:lipid association in the porcine oocyte. Reproduction 132, 829–837.
Fluorescence resonance energy transfer analysis of mitochondrial:lipid association in the porcine oocyte.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmsF2isw%3D%3D&md5=41804fc5d2cbb5f9dfe8f86c072f1501CAS | 17127743PubMed |

Sturmey, R. G., Reiss, 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 | 19660080PubMed |

Sturmey, R. G., Bermejo-Alvarez, P., Gutierrez-Adan, A., Rizos, D., Leese, H. J., and Lonergan, P. (2010). Amino acid metabolism of bovine blastocysts: a biomarker of sex and viability. Mol. Reprod. Dev. 77, 285–296.
Amino acid metabolism of bovine blastocysts: a biomarker of sex and viability.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXotFSmuw%3D%3D&md5=e95dd21b2c1d7b3b02318a8323bd5bd9CAS | 20058302PubMed |

Warburg, O. (1926). ‘Über den Stoffwechsel der Tumoren.’ (Springer Verlag: Berlin.)

Xie, Y., Awonuga, A., Liu, J., Rings, E., Puscheck, E. E., and Rappolee, D. A. (2013). Stress induces AMP-dependent loss of potency factors Id2 and Cdx2 in early embryos and stem cells. Stem Cells Dev. 22, 1564–1575.
Stress induces AMP-dependent loss of potency factors Id2 and Cdx2 in early embryos and stem cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXnsVWhtrw%3D&md5=40239c201cdcf4b850207487a8e8cdbdCAS | 23316940PubMed |