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Chapter 4 - Embryo Metabolism and What Does the Embryo Need?

Published online by Cambridge University Press:  15 April 2021

By
Paula Vergaro  and
Roger G. Sturmey
Edited by
Kersti Lundin  and
Aisling Ahlström
Kersti Lundin
Affiliation:
Sahlgrenska University Hospital, Gothenburg
Aisling Ahlström
Affiliation:
Livio Fertility Center, Gothenburg
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Summary

The embryo is a dynamic structure that can be affected by the interaction with the surrounding environment. During its journey through the female reproductive tract from fertilization to implantation, the embryo undergoes numerous biochemical and physiological changes which are essential for a successful reproductive outcome. During successive cleavage rounds, the embryo increases in cell number, switches from maternal to embryonic genome control (embryonic genome activation; EGA) and forms cell–cell junctions. This coincides with the cells flattening and compacting at the morula stage (Coticchio et al., 2019). At the final stage of the preimplantation period, the blastomeres differentiate to form the trophectoderm and the inner cell mass cell lineages. The blastocyst undergoes remarkable events in preparation for implantation and establishment of pregnancy, including initiation of overall growth, significant rise in transcriptional activity, increased protein synthesis, and active Na+/K+ ATPase activity in the trophectoderm leading to the formation of the blastocoel cavity (reviewed by Smith & Sturmey, 2013). The blastocyst also improves homeostatic regulatory mechanisms, including defense against oxidative damage (Lane & Gardner, 2000). These changes are energy dependent, and therefore underpinned by specific metabolic pathways. Disruptions in energy production during the preimplantation period are related to embryonic developmental impairment and reduced fetal viability post-transfer (Gardner, ; Lane & Gardner, 2005b). For these reasons, metabolism is considered a key determinant of embryo competence and viability.

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Manual of Embryo Culture in Human Assisted Reproduction , pp. 30 - 41
Publisher: Cambridge University Press
Print publication year: 2021

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References

Aguilar, J, Reyley, M. The uterine tubal fluid: secretion, composition and biological effects. Anim Reprod. 2005;2:91–105.Google Scholar
Balaban, RS, Nemoto, S, Finkel, T. Mitochondria, oxidants, and aging. Cell. 2005;120:483–495.Google Scholar
Barker, DJ. The origins of the developmental origins theory. J Intern Med. 2007;261:412–417.Google Scholar
Batt, PA, Gardner, DK, Cameron, AW. Oxygen concentration and protein source affect the development of preimplantation goat embryos in vitro. Reprod Fertil Dev. 1991;3:601–607.Google Scholar
Bauer, BK, Isom, SC, Spate, LD, et al. Transcriptional profiling by deep sequencing identifies differences in mRNA transcript abundance in in vivo-derived versus in vitro-cultured porcine blastocyst stage embryos. Biol Reprod. 2010;83:791–798.Google Scholar
Baumann, CG, Morris, DG, Sreenan, JM, Leese, HJ. The quiet embryo hypothesis: molecular characteristics favoring viability. Mol Reprod Dev. 2007;74:1345–1353.CrossRefGoogle ScholarPubMed
Bontekoe, S, Mantikou, E, van Wely, M, Seshadri, S, Repping, S, Mastenbroek, S. Low oxygen concentrations for embryo culture in assisted reproductive technologies. Cochrane Database Syst Rev. 2012; (7), CD008950.Google Scholar
Bradley, J, Pope, I, Masia, F, et al. Quantitative imaging of lipids in live mouse oocytes and early embryos using CARS microscopy. Development. 2016;143:2238–2247.Google Scholar
Brison, DR, Houghton, FD, Falconer, D, et al. Identification of viable embryos in IVF by non-invasive measurement of amino acid turnover. Hum Reprod. 2004;19:2319–2324.Google Scholar
Brison, DR, Sturmey, RG, Leese, HJ. Metabolic heterogeneity during preimplantation development: the missing link? Hum Reprod Update. 2014;20:632–640.Google Scholar
Cagnone, G, Sirar, A. The embryonic stress response to in vitro culture: insight from genomic analysis. Reproduction. 2016;152:R247–R261.Google Scholar
Capalbo, A, Hoffmann, ER, Cimadomo, D, Ubaldi, FM, Rienzi, L. Human female meiosis revised: new insights into the mechanisms of chromosome segregation and aneuploidies from advanced genomics and time-lapse imaging. Hum Reprod Update. 2017;23:706–722.CrossRefGoogle ScholarPubMed
Castillo, CM, Horne, G, Fitzgerald, CT, et al. The impact of IVF on birthweight from 1991 to 2015: a cross-sectional study. Hum Reprod. 2019;34:920–931.Google Scholar
Catt, JW, Henman, M. Toxic effects of oxygen on human embryo development. Hum Reprod. 2000;15 (Suppl 2):199–206.Google Scholar
Chen, PR, Redel, BK, Spate, LD, Ji, T, Salazar, SR, Prather, RS. Glutamine supplementation enhances development of in vitro-produced porcine embryos and increases leucine consumption from the medium. Biol Reprod. 2018;99:938–948.CrossRefGoogle ScholarPubMed
Cheong, Y, Boomsma, C, Heijnen, C, Macklon, N. Uterine secretomics: a window on the maternal-embryo interface. Fertil Steril. 2013;99:1093–1099.Google Scholar
Coticchio, G, Lagalla, C, Sturmey, R, Pennetta, F, Borini, A. The enigmatic morula: mechanisms of development, cell fate determination, self-correction and implications for ART. Hum Reprod Update. 2019;25:422–438.Google Scholar
Coull, G, Speake, B, Staines, M, Broadbent, P, McEvoy, T. Lipid and fatty acid composition of zona-intact sheep oocytes. Theriogenology. 1998;49:179.Google Scholar
Crosby, IM, Gandolfi, F, Moor, RM. Control of protein synthesis during early cleavage of sheep embryos. J Reprod Fertil. 1988;82:769–775.Google Scholar
Dagilgan, S, Dundar-Yenilmez, E, Tuli, A, Urunsak, IF, Erdogan, S. Evaluation of intracellular pH regulation and alkalosis defense mechanisms in preimplantation embryos. Theriogenology. 2015;83:1075–1084.Google Scholar
Dawson, KM, Baltz, JM. Organic osmolytes and embryos: substrates of the Gly and beta transport systems protect mouse zygotes against the effects of raised osmolarity. Biol Reprod. 1997;56:1550–1558.Google Scholar
De Geyter, C, Calhaz-Jorge, C, Kupka, MS, et al. ART in Europe, 2014: results generated from European registries by ESHRE: The European IVF-monitoring Consortium (EIM) for the European Society of Human Reproduction and Embryology (ESHRE). Hum Reprod. 2018;33:1586–1601.CrossRefGoogle ScholarPubMed
De Munck, N, Janssens, R, Segers, I, Tournaye, H, Van de Velde, H, Verheyen, G. Influence of ultra-low oxygen (2%) tension on in-vitro human embryo development. Hum Reprod. 2019;34:228–234.Google Scholar
Devreker, F, Winston, RM, Hardy, K. Glutamine improves human preimplantation development in vitro. Fertil Steril. 1998;69;293–299.Google Scholar
Eckert, JJ, Houghton, FD, Hawkhead, JA, et al. Human embryos developing in vitro are susceptible to impaired epithelial junction biogenesis correlating with abnormal metabolic activity. Hum Reprod. 2007;22:2214–2224.Google Scholar
Eckert, JJ, Porter, R, Watkins, AJ, et al. Metabolic induction and early responses of mouse blastocyst developmental programming following maternal low protein diet affecting life-long health. PLoS One. 2012;7:e52791.Google Scholar
Edwards, LJ, Williams, DA, Gardner, DK. Intracellular pH of the mouse preimplantation embryo: amino acids act as buffers of intracellular pH. Hum Reprod. 1998a;13:3441–3448.CrossRefGoogle ScholarPubMed
Edwards, LJ, Williams, DA, Gardner, DK. Intracellular pH of the preimplantation mouse embryo: effects of extracellular pH and weak acids. Mol Reprod Dev. 1998b;50:434–442.3.0.CO;2-J>CrossRefGoogle ScholarPubMed
Epstein, CJ, Smith, SA. Amino acid uptake and protein synthesis in preimplanatation mouse embryos. Dev Biol. 1973;33:171–184.Google Scholar
Fall, CH, Sachdev, HS, Osmond, C, et al. Association between maternal age at childbirth and child and adult outcomes in the offspring: a prospective study in five low-income and middle-income countries (COHORTS collaboration). Lancet Glob Health. 2015;3:e366–377.Google Scholar
Favetta, LA, St John, EJ, King, WA, Betts, DH. High levels of p66shc and intracellular ROS in permanently arrested early embryos. Free Radic Biol Med. 2007;42:1201–1210.Google Scholar
Ferguson, EM, Leese, HJ. Triglyceride content of bovine oocytes and early embryos. J Reprod Fertil. 1999;116:373–378.Google Scholar
Fernandez-Gonzalez, R, Moreira, P, Bilbao, A, et al. Long-term effect of in vitro culture of mouse embryos with serum on mRNA expression of imprinting genes, development, and behavior. Proc Natl Acad Sci U S A. 2004;101:5880–5885.Google Scholar
Fischer, B, Bavister, BD. Oxygen tension in the oviduct and uterus of rhesus monkeys, hamsters and rabbits. J Reprod Fertil. 1993;99:673–679.CrossRefGoogle ScholarPubMed
Gad, A, Hoelker, M, Besenfelder, U, et al. Molecular mechanisms and pathways involved in bovine embryonic genome activation and their regulation by alternative in vivo and in vitro culture conditions. Biol Reprod. 2012;87:100.Google Scholar
Gardner, DK. Changes in requirements and utilization of nutrients during mammalian preimplantation embryo development and their significance in embryo culture. Theriogenology. 1998;49; 83–102.Google Scholar
Gardner, DK. Metabolism of the viable embryo. In: Gardner, DK, Sakkas, D, Seli, E, Wells, D, ed. Emerging Technologies for the Assessment and Diagnosis of Gametes and Embryos. New York: Springer; 2013:211–223.Google Scholar
Gardner, DK. Lactate production by the mammalian blastocyst: manipulating the microenvironment for uterine implantation and invasion? Bioessays. 2015;37:364–371.CrossRefGoogle ScholarPubMed
Gardner, DK, Hamilton, R, McCallie, B, Schoolcraft, WB, Katz-Jaffe, MG. Human and mouse embryonic development, metabolism and gene expression are altered by an ammonium gradient in vitro. Reproduction. 2013;146:49–61.Google Scholar
Gardner, DK, Lane, M, Calderon, I, Leeton, J. Environment of the preimplantation human embryo in vivo: metabolite analysis of oviduct and uterine fluids and metabolism of cumulus cells. Fertil Steril. 1996;65:349–353.Google Scholar
Gardner, DK, Leese, HJ. Concentrations of nutrients in mouse oviduct fluid and their effects on embryo development and metabolism in vitro. J Reprod Fertil. 1990;88:361–368.Google Scholar
Gardner, DK, Wale, P, Collins, R, Lane, M. Glucose consumption of single post-compaction human embryos is predictive of embryo sex and live birth outcome. Hum Reprod. 2011;26:1981–1986.Google Scholar
Gonzalez, IM, Martin, PM, Burdsal, C, et al. Leucine and arginine regulate trophoblast motility through mTOR-dependent and independent pathways in the preimplantation mouse embryo. Dev Biol. 2012;361:286–300.Google Scholar
Goto, K, Kumasako, Y, Koike, M, et al. Prediction of the in vitro developmental competence of early-cleavage-stage human embryos with time-lapse imaging and oxygen consumption rate measurement. Reprod Med Biol. 2018;17:289–296.Google Scholar
Guerif, F, McKeegan, P, Leese, HJ, Sturmey, RG. A simple approach for COnsumption and RElease (CORE) analysis of metabolic activity in single mammalian embryos. PLoS One. 2013;8: e67834.Google Scholar
Guerin, P, El Mouatassim, S, Menezo, Y. Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings. Hum Reprod Update. 2001;7:175–189.Google Scholar
Haggarty, P, Wood, M, Ferguson, E, et al. Fatty acid metabolism in human preimplantation embryos. Hum Reprod. 2006;21:766–773.Google Scholar
Hamdi, M, Lopera-Vasquez, R, Maillo, V, et al. Bovine oviductal and uterine fluid support in vitro embryo development. Reprod Fertil Dev. 2018;30:935–945.Google Scholar
Hancock, JT, Desikan, R, Neill, SJ. Role of reactive oxygen species in cell signalling pathways. Biochem Soc Trans. 2001;29:345–350.CrossRefGoogle ScholarPubMed
Harper, J, Magli, MC, Lundin, K, Barratt, CL, Brison, D. When and how should new technology be introduced into the IVF laboratory? Hum Reprod. 2012;27:303–313.CrossRefGoogle ScholarPubMed
Houghton, FD, Hawkhead, JA, Humpherson, PG, et al. Non-invasive amino acid turnover predicts human embryo developmental capacity. Hum Reprod. 2002;17:999–1005.Google Scholar
Houghton, FD, Humpherson, PG, Hawkhead, JA, Hall, CJ, Leese, HJ. Na+, K+, ATPase activity in the human and bovine preimplantation embryo. Dev Bio. 2003;263:360–366.Google Scholar
Houghton, FD, Thompson, JG, Kennedy, CJ, Leese, HJ. Oxygen consumption and energy metabolism of the early mouse embryo. Mol Reprod Dev. 1996;44:476–485.Google Scholar
Humpherson, PG, Leese, HJ, Sturmey, RG. Amino acid metabolism of the porcine blastocyst. Theriogenology. 2005;64:1852–1866.Google Scholar
Kaser, DJ, Bogale, B, Sarda, V, Farland, LV, Williams, PL, Racowsky, C. Randomized controlled trial of low (5%) versus ultralow (2%) oxygen for extended culture using bipronucleate and tripronucleate human preimplantation embryos. Fertil Steril. 2018;109:1030–1037 e2.Google Scholar
Kenny, LC, Lavender, T, McNamee, R, O’Neill, SM, Mills, T, Khashan, AS. Advanced maternal age and adverse pregnancy outcome: evidence from a large contemporary cohort. PLoS One. 2013;8:e56583.Google Scholar
Kermack, AJ, Finn-Sell, S, Cheong, YC, et al. Amino acid composition of human uterine fluid: association with age, lifestyle and gynaecological pathology. Hum Reprod. 2015; 30:917–924.Google Scholar
Kleijkers, SH, van Montfoort, AP, Bekers, O, et al. Ammonium accumulation in commercially available embryo culture media and protein supplements during storage at 2–8 degrees C and during incubation at 37 degrees C. Hum Reprod. 2016; 31:1192–1199.Google Scholar
Koustas, G, Sjoblom, C. Epigenetic consequences of pH stress in mouse embryos. Hum Reprod. 2011:26(suppl_1):i78.Google Scholar
Kovacic, B, Sajko, MC, Vlaisavljevic, V. A prospective, randomized trial on the effect of atmospheric versus reduced oxygen concentration on the outcome of intracytoplasmic sperm injection cycles. Fertil Steri. 2010;94:511–519.CrossRefGoogle ScholarPubMed
Kovacic, B, Vlaisavljevic, V. Influence of atmospheric versus reduced oxygen concentration on development of human blastocysts in vitro: a prospective study on sibling oocytes. Reprod Biomed Online. 2008;17:229–236.Google Scholar
Lane, M, Gardner, DK. Selection of viable mouse blastocysts prior to transfer using a metabolic criterion. Hum Reprod. 1996;11:1975–1978.Google Scholar
Lane, M, Gardner, DK. Amino acids and vitamins prevent culture-induced metabolic perturbations and associated loss of viability of mouse blastocysts. Hum Reprod. 1998;13:991–997.Google Scholar
Lane, M, Gardner, DK. Regulation of ionic homeostasis by mammalian embryos. Semin Reprod Med. 2000;18:195–204.Google Scholar
Lane, M, Gardner, DK. Ammonium induces aberrant blastocyst differentiation, metabolism, pH regulation, gene expression and subsequently alters fetal development in the mouse. Biol Reprod. 2003;69:1109–1117.Google Scholar
Lane, M, Gardner, DK. Mitochondrial malate-aspartate shuttle regulates mouse embryo nutrient consumption. J Biol Chem. 2005a;280:18361–18367.CrossRefGoogle ScholarPubMed
Lane, M, Gardner, DK. Understanding cellular disruptions during early embryo development that perturb viability and fetal development. Reprod Fertil Dev. 2005b;17: 371–378.Google Scholar
Leese, HJ. The formation and function of oviduct fluid. J Reprod Fertil. 1988;82:843–856.Google Scholar
Leese, HJ. Metabolic control during preimplantation mammalian development. Hum Reprod Update. 1995;1:63–72.Google Scholar
Leese, HJ. Quiet please, do not disturb: a hypothesis of embryo metabolism and viability. Bioessays. 2002;24:845–849.Google Scholar
Leese, HJ. Metabolism of the preimplantation embryo: 40 years on. Reproduction. 2012;143:417–427.Google Scholar
Leese, HJ, Barton, AM. Pyruvate and glucose uptake by mouse ova and preimplantation embryos. J Reprod Fertil. 1984;72:9–13.Google Scholar
Leese, HJ, Barton, AM. Production of pyruvate by isolated mouse cumulus cells. J Exp Zool. 1985;234:231–236.Google Scholar
Leese, HJ, Baumann, CG, Brison, DR, McEvoy, TG, Sturmey, RG. Metabolism of the viable mammalian embryo: quietness revisited. Mol Hum Reprod. 2008a;14:667–672.Google Scholar
Leese, HJ, Conaghan, J, Martin, KL, Hardy, K. Early human embryo metabolism. Bioessays. 1993;15:259–264.Google Scholar
Leese, HJ, Donnay, I, Thompson, JG. Human assisted conception: a cautionary tale. Lessons from domestic animals. Hum Reprod. 1998;13(Suppl 4):184–202.Google Scholar
Leese, HJ, Guerif, F, Allgar, V, Brison, DR, Lundin, K, Sturmey, RG. Biological optimization, the Goldilocks principle, and how much is lagom in the preimplantation embryo. Mol Reprod Dev. 2016;83:748–754.Google Scholar
Leese, HJ, Hugentobler, SA, Gray, SM, et al. Female reproductive tract fluids: composition, mechanism of formation and potential role in the developmental origins of health and disease. Reprod Fertil Dev. 2008b:20:1–8.Google Scholar
Leese, HJ, Sathyapalan, T, Allgar, V, Brison, DR, Sturmey, R. Going to extremes: the Goldilocks/Lagom principle and data distribution. BMJ Open. 2019;9:e027767.CrossRefGoogle ScholarPubMed
Leese, HJ, Sturmey, RG, Baumann, CG, McEvoy, TG. Embryo viability and metabolism: obeying the quiet rules. Hum Reprod. 2007;22:3047–3050.Google Scholar
Leroy, JL, Genicot, G, Donnay, I, Van Soom, A. Evaluation of the lipid content in bovine oocytes and embryos with nile red: a practical approach. Reprod Domest Anim. 2005;40:76–87.Google Scholar
Lewis, N, Sturmey, RG. Embryo metabolism: what does it really mean? Anim. Reprod. 12;2015:521–528.Google Scholar
Marei, WFA, Van den Bosch, L, Pintelon, I, Mohey-Elsaeed, O, Bols, PEJ, Leroy, J. Mitochondria-targeted therapy rescues development and quality of embryos derived from oocytes matured under oxidative stress conditions: a bovine in vitro model. Hum Reprod. 2019;34:1984–1998.Google Scholar
Matorras, R, Ruiz, JI, Mendoza, R, Ruiz, N, Sanjurjo, P, Rodriguez-Escudero, FJ. Fatty acid composition of fertilization-failed human oocytes. Hum Reprod. 1998;13:2227–2230.Google Scholar
McEvoy, TG, Coull, GD, Broadbent, PJ, Hutchinson, JS, Speake, BK. Fatty acid composition of lipids in immature cattle, pig and sheep oocytes with intact zona pellucida. J Reprod Fertil. 2000;118:163–170.Google Scholar
McPherson, NO, Zander-Fox, D, Lane, M. Stimulation of mitochondrial embryo metabolism by dichloroacetic acid in an aged mouse model improves embryo development and viability. Fertil Steril. 2014;101:1458–1466.Google Scholar
Merton, JS, de Roos, AP, Mullaart, E, et al. Factors affecting oocyte quality and quantity in commercial application of embryo technologies in the cattle breeding industry. Theriogenology. 2003;59:651–674.CrossRefGoogle ScholarPubMed
Mitchell, M, Cashman, KS, Gardner, DK, Thompson, JG, Lane, M. Disruption of mitochondrial malate-aspartate shuttle activity in mouse blastocysts impairs viability and fetal growth. Biol Reprod. 2009;80:295–301.Google Scholar
Morin, SJ, Kaser, DJ, Juneau, CR, et al. The LO2 trial, phase 1: a paired randomized controlled trial (RCT) comparing blastulation rate in ultra-low (2%) vs. low (5%) oxygen in extended culture. Fertil Steril 2017;108(3 suppl):e58–59.Google Scholar
Nagaraj, R, Sharpley, MS, Chi, F, et al. Nuclear localization of mitochondrial TCA cycle enzymes as a critical step in mammalian zygotic genome activation. Cell. 2017;168:210–223 e11.Google Scholar
Ng, KYB, Mingels, R, Morgan, H, Macklon, N, Cheong, Y. In vivo oxygen, temperature and pH dynamics in the female reproductive tract and their importance in human conception: a systematic review. Hum Reprod Update. 2018;24:15–34.Google Scholar
Orsi, NM, Leese, HJ. Amino acid metabolism of preimplantation bovine embryos cultured with bovine serum albumin or polyvinyl alcohol. Theriogenology, 2004a;61:561–572.Google Scholar
Orsi, NM, Leese, HJ. Ammonium exposure and pyruvate affect the amino acid metabolism of bovine blastocysts in vitro. Reproduction. 2004b;127:131–140.Google Scholar
Phillips, KP, Leveille, MC, Claman, P, Baltz, JM. Intracellular pH regulation in human preimplantation embryos. Hum Reprod. 2000;15:896–904.Google Scholar
Picton, HM, Elder, K, Houghton, FD, et al. Association between amino acid turnover and chromosome aneuploidy during human preimplantation embryo development in vitro. Mol Hum Reprod. 2010;16:557–569.Google Scholar
Redel, BK, Brown, AN, Spate, LD, Whitworth, KM, Green, JA, Prather, RS. Glycolysis in preimplantation development is partially controlled by the Warburg effect. Mol Reprod Dev. 2012;79:262–271.Google Scholar
Reid, MA, Dai, Z, Locasale, JW. The impact of cellular metabolism on chromatin dynamics and epigenetics. Nat Cell Biol. 2017;19:1298–1306.Google Scholar
Rezk, Y, Huff, C, Rizk, B. Effect of glutamine on preimplantation mouse embryo development in vitro. Am J Obstet Gynecol. 2004;190:1450–1454.Google Scholar
Salilew-Wondim, D, Saeed-Zidane, M, Hoelker, M, et al. Genome-wide DNA methylation patterns of bovine blastocysts derived from in vivo embryos subjected to in vitro culture before, during or after embryonic genome activation. BMC Genomics. 2018;19:424.Google Scholar
Shi, Y, Ma, J, Xue, Y, Wang, J, Yu, B, Wang, T. The assessment of combined karyotype analysis and chromosomal microarray in pregnant women of advanced maternal age: a multicenter study. Ann Transl Med. 2019;7:318.Google Scholar
Smith, DG, Sturmey, RG. Parallels between embryo and cancer cell metabolism. Biochem Soc Trans. 2013;41:664–669.Google Scholar
Steeves, TE, Gardner, DK. Temporal and differential effects of amino acids on bovine embryo development in culture. Biol Reprod. 1999;61:731–740.Google Scholar
Stokes, PJ, Hawkhead, JA, Fawthrop, RK, et al. Metabolism of human embryos following cryopreservation: implications for the safety and selection of embryos for transfer in clinical IVF. Hum Reprod. 2007;22:829–835.Google Scholar
Sturmey, RG, Bermejo-Alvarez, P, Gutierrez-Adan, A, Rizos, D, Leese, HJ, Lonergan, P. Amino acid metabolism of bovine blastocysts: a biomarker of sex and viability. Mol Reprod Dev. 2010;77:285–296.Google Scholar
Sturmey, RG, Brison, DR, Leese, HJ. Symposium: innovative techniques in human embryo viability assessment. Assessing embryo viability by measurement of amino acid turnover. Reprod Biomed Online. 2008;17:486–496.Google Scholar
Sturmey, RG, Hawkhead, JA, Barker, EA, Leese, HJ. DNA damage and metabolic activity in the preimplantation embryo. Hum Reprod. 2009;24:81–91.Google Scholar
Sturmey, RG, Leese, HJ. Energy metabolism in pig oocytes and early embryos. Reproduction. 2003;126:197–204.Google Scholar
Sturmey, RG, O’Toole, PJ, Leese, HJ. Fluorescence resonance energy transfer analysis of mitochondrial:lipid association in the porcine oocyte. Reproduction. 2006;132:829–837.Google Scholar
Sudano, MJ, Paschoal, DM, Rascado Tda, S, et al. Lipid content and apoptosis of in vitro-produced bovine embryos as determinants of susceptibility to vitrification. Theriogenology. 2011;75:1211–1220.Google Scholar
Summers, MC, Biggers, JD. Chemically defined media and the culture of mammalian preimplantation embryos: historical perspective and current issues. Hum Reprod Update. 2003;9:557–582.Google Scholar
Sunde, A, Brison, D, Dumoulin, J, et al. Time to take human embryo culture seriously. Hum Reprod. 2016;31:2174–2182.CrossRefGoogle ScholarPubMed
Suzuki, C, Yoshioka, K, Sakatani, M, Takahashi, M. Glutamine and hypotaurine improves intracellular oxidative status and in vitro development of porcine preimplantation embryos. Zygote. 2007;15:317–324.Google Scholar
Swain, JE. Optimizing the culture environment in the IVF laboratory: impact of pH and buffer capacity on gamete and embryo quality. Reprod Biomed Online. 2010;21:6–16.Google Scholar
Swain, JE. Is there an optimal pH for culture media used in clinical IVF? Hum Reprod Update. 2012;18:333–339.Google Scholar
Tatsumi, T, Takayama, K, Ishii, S et al. Forced lipophagy reveals that lipid droplets are required for early embryonic development in mouse. Development. 2018;145:dev161893.Google Scholar
Thompson, JG. Comparison between in vivo-derived and in vitro-produced pre-elongation embryos from domestic ruminants. Reprod Fertil Dev. 1997;9:341–354.Google Scholar
Thompson, JG, Kind, KL, Roberts, CT, Robertson, SA, Robinson, JS. Epigenetic risks related to assisted reproductive technologies: short- and long-term consequences for the health of children conceived through assisted reproduction technology: more reason for caution? Hum Reprod. 2002;17:2783–2786.Google Scholar
Thompson, JG, Partridge, RJ, Houghton, FD, Cox, CI, Leese, HJ. Oxygen uptake and carbohydrate metabolism by in vitro derived bovine embryos. J Reprod Fertil. 1996;106:299–306.Google Scholar
Thompson, JG, Simpson, AC, Pugh, PA, Donnelly, PE, Tervit, HR. Effect of oxygen concentration on in-vitro development of preimplantation sheep and cattle embryos. J Reprod Fertil. 1990;89:573–578.CrossRefGoogle ScholarPubMed
Truong, T, Gardner, DK. Antioxidants improve IVF outcome and subsequent embryo development in the mouse. Hum Reprod. 2017;32:2404–2413.Google Scholar
Truong, TT, Soh, YM, Gardner, DK. Antioxidants improve mouse preimplantation embryo development and viability. Hum Reprod. 2016;31:1445–1454.CrossRefGoogle ScholarPubMed
Van Winkle, LJ, Tesch, JK, Shah, A, Campione, L. System B0,+ amino acid transport regulates the penetration stage of blastocyst implantation with possible long-term developmental consequences through adulthood. Hum Reprod Update. 2006;12:145–157.CrossRefGoogle ScholarPubMed
Velazquez, MA, Sheth, B, Smith, SJ, Eckert, JJ, Osmond, C Fleming, TP. Insulin and branched-chain amino acid depletion during mouse preimplantation embryo culture programmes body weight gain and raised blood pressure during early postnatal life. Biochim Biophys Acta Mol Basis Dis. 2018;1864;590–600.Google Scholar
Velazquez, MA, Smith, CG, Smyth, NR, Osmond, C, Fleming, TP. Advanced maternal age causes adverse programming of mouse blastocysts leading to altered growth and impaired cardiometabolic health in post-natal life. Hum Reprod. 2016;31:1970–1980.Google Scholar
Wale, PL, Gardner, DK. Time-lapse analysis of mouse embryo development in oxygen gradients. Reprod Biomed Online. 2010;21:402–410.Google Scholar
Wale, PL, Gardner, DK. Oxygen affects the ability of mouse blastocysts to regulate ammonium. Biol Reprod. 2013;89:75.Google Scholar
Wale, PL, Gardner, DK. The effects of chemical and physical factors on mammalian embryo culture and their importance for the practice of assisted human reproduction. Hum Reprod Update. 2016;22:2–22.Google Scholar
Walther, TC, Farese, RV Jr. Lipid droplets and cellular lipid metabolism. Annu Rev Biochem. 2012;81:687–714.Google Scholar
Warburg, O. On the origin of cancer cells. Science. 1956;123:309–314.Google Scholar
Zaninovic, N, Goldschlag, J, Yin, H,Ye, Z, Clarke, R, Rosenwaks, Z. Impact of oxygen concentration on embryo development, embryo morphology and morphokinetics. Fertil Steril. 2013;100:S240.Google Scholar

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