Developmental kinetics of cleavage stage mouse embryos are related to their subsequent carbohydrate and amino acid utilization at the blastocyst stage

Human Reproduction

Volumn 30, Issue 3, 2015, Pages 543-552

  Lee, Y S L ^a   Thouas, G A ^a   Gardner, D K ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Metabolism; Selection; Time lapse; Viability

Indexed keywords

ALANINE; AMINO ACID; ARGININE; ASPARTIC ACID; CARBOHYDRATE; CYSTINE; GLUTAMIC ACID; GLUTAMINE; HISTIDINE; LEUCINE; METHIONINE; PROLINE; SERINE; THREONINE; TYROSINE; VALINE; CULTURE MEDIUM; GLUCOSE;

AMINO ACID METABOLISM; ARTICLE; BLASTOCYST; CARBOHYDRATE METABOLISM; CELL LINEAGE; CONTROLLED STUDY; EMBRYO; EMBRYO CULTURE; EMBRYO TRANSFER; FEMALE; FETUS DEVELOPMENT; GLUCOSE INTAKE; INNER CELL MASS; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MOUSE; NONHUMAN; OOCYTE CLEAVAGE; PREGNANCY; PREIMPLANTATION EMBRYO; ZYGOTE; ANIMAL; C57BL MOUSE; CHEMISTRY; CULTURE MEDIUM; EMBRYO DEVELOPMENT; FERTILIZATION IN VITRO; KINETICS; METABOLISM; TIME;

AMINO ACIDS; ANIMALS; BLASTOCYST; CARBOHYDRATE METABOLISM; CULTURE MEDIA; EMBRYONIC DEVELOPMENT; FERTILIZATION IN VITRO; GLUCOSE; KINETICS; MICE; MICE, INBRED C57BL; TIME FACTORS;

EID: 84928317526     PISSN: 02681161     EISSN: 14602350     Source Type: Journal    
DOI: 10.1093/humrep/deu334     Document Type: Article

References (63)

1. Adashi EY, Barri PN, Berkowitz R, Braude P, Bryan E, Carr J, Cohen J, Collins J, Devroey P, Frydman R et al. Infertility therapy-associated multiple pregnancies (births): an ongoing epidemic. Reprod Biomed Online 2003; 5:515-542.
2. Arav A, Aroyo A, Yavin S, Roth Z. Prediction of embryonic developmental competence by time-lapse observation and 'shortest-half' analysis. Reprod Biomed Online 2008;5:669-675.
3. Binder NK, Hannan NJ, Gardner DK. Paternal diet-induced obesity retards early mouse embryo development, mitochondrial activity and pregnancy health. PLoS One 2012;12:e52304.
4. Booth PJ, Watson TJ, Leese HJ. Prediction of porcine blastocyst formation using morphological, kinetic, and amino acid depletion and appearance criteria determined during the early cleavage of in vitro-produced embryos. Biol Reprod 2007;5:765-779.
5. Boughton BA, Callahan DL, Silva C, Bowne J, Nahid A, Rupasinghe T, Tull DL, Mcconville MJ, Bacic A, Roessner U. Comprehensive profiling and quantitation of amine group containing metabolites. Anal Chem 2011; 19:7523-7530.
6. Brison DR, Houghton FD, Falconer D, Roberts SA, Hawkhead J, Humpherson PG, Lieberman BA, Leese HJ. Identification of viable embryos in IVF by non-invasive measurement of amino acid turnover. Hum Reprod 2004;10:2319-2324.
7. Dawson KM, Baltz JM. Organic osmolytes and embryos: substratesofthe Gly and beta transport systems protect mouse zygotes against the effects of raised osmolarity. Biol Reprod 1997;6:1550-1558.
8. Edwards RG, Fishel SB, Cohen J, Fehilly CB, Purdy JM, Slater JM, Steptoe PC, Webster JM. Factors influencing the success of in vitro fertilization for alleviating human infertility. J In Vitro Fert Embryo Transf 1984;1:3-23.
9. Edwards LJ, Williams DA, Gardner DK. Intracellular pH of the mouse preimplantation embryo: amino acids act as buffers of intracellular pH. Hum Reprod 1998;12:3441-3448.
10. Ferraretti AP, Goossens V, Kupka M, Bhattacharya S, De Mouzon J, Castilla JA, Erb K, Korsak V, Nyboe Andersen A. Assisted reproductive technology in Europe, 2009: results generated from European registers by ESHRE. Hum Reprod 2013;9:2318-2331.
11. Gardner DK. Changes in requirements and utilization of nutrients during mammalian preimplantation embryo development and their significance in embryo culture. Theriogenology 1998;1:83-102.
12. Gardner DK. Noninvasive metabolic assessment of single cells. Methods Mol Med 2007;132:1-9.
13. Gardner DK, Leese HJ. Assessment of embryo viability prior totransfer by the noninvasive measurement of glucose uptake. J Exp Zool 1987;1:103-105.
14. 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;1:361-368.
15. Gardner DK, Lane M. Alleviationofthe '2-cell block' and developmentto the blastocyst of CF1 mouse embryos: role of amino acids, EDTA and physical parameters. Hum Reprod 1996;12:2703-2712.
16. Gardner DK, Lane M. Cultureofthe mammalian preimplantation embryo. In: Gardner DK, Lane M, Watson AJ (eds). A Laboratory Guide to the Mammalian Embryo. New York: Oxford University Press, 2004; 41-61.
17. Gardner DK, Lane M. Ex vivo early embryo development and effects on gene expression and imprinting. Reprod Fertil Dev 2005;3:361-370.
18. Gardner DK, Lane M. Mammalian preimplantation embryo culture. Methods Mol Biol 2014;1092:167-182.
19. Gardner DK, Lane M, Stevens J, Schlenker T, Schoolcraft WB. Blastocyst score affects implantation and pregnancy outcome: towards a single blastocyst transfer. Fertil Steril 2000;6:1155-1158.
20. Gardner DK, Wale PL, Collins R, Lane M. Glucose consumption of single post-compaction human embryos is predictive of embryo sex and live birth outcome. Hum Reprod 2011;8:1981-1986.
21. Gott AL, Hardy K, Winston RM, Leese HJ. Non-invasive measurement of pyruvate and glucose uptake and lactate production by single human preimplantation embryos. Hum Reprod 1990;1:104-108.
22. Grisart B, Massip A, Dessy F. Cinematographic analysis of bovine embryo development in serum-free oviduct-conditioned medium. J Reprod Fertil 1994;2:257-264.
23. Handyside AH, Hunter S. Arapid procedure for visualising the inner cell mass and trophectoderm nuclei of mouse blastocysts in situ using polynucleotide-specific fluorochromes. J Exp Zool 1984;3:429-434.
24. Hannan NJ, Paiva P, Meehan KL, Rombauts LJ, Gardner DK, Salamonsen LA. Analysis of fertility-related soluble mediators in human uterine fluid identifies VEGF as a key regulator of embryo implantation. Endocrinology 2011;12:4948-4956.
25. Harlow GM, Quinn P. Foetal and placental growth in the mouse after pre-implantation development in vitro under oxygen concentrations of 5 and 20%. Aust J Biol Sci 1979;3:363-369.
26. Herrero J, Tejera A, Albert C, Vidal C, De Los Santos MJ, Meseguer M. Atime to look back: analysis of morphokinetic characteristics of human embryo development. Fertil Steril 2013;6:1602-1609.e1-4.
27. Houghton FD, Hawkhead JA, Humpherson PG, Hogg JE, Balen AH, Rutherford AJ, Leese HJ. Non-invasive amino acid turnover predicts human embryo developmental capacity. Hum Reprod 2002;4:999-1005.
28. Katz-Jaffe MG, Schoolcraft WB, Gardner DK. Analysis of protein expression (secretome) by human and mouse preimplantation embryos. Fertil Steril 2006;3:678-685.
29. Kirkegaard K, Agerholm IE, Ingerslev HJ. Time-lapse monitoring as a tool for clinical embryo assessment. Hum Reprod 2012;5:1277-1285.
30. Kirkegaard K, Hindkjaer JJ, Ingerslev HJ. Effect of oxygen concentration on human embryo development evaluated by time-lapse monitoring. Fertil Steril 2013;3:738-744.e4.
31. Lamb VK, Leese HJ. Uptakeofamixtureofamino acidsbymouse blastocysts. J Reprod Fertil 1994;1:169-175.
32. Lane M, Gardner DK. Increase in postimplantation development of cultured mouse embryos by amino acids and induction of fetal retardation and exencephaly by ammonium ions. J Reprod Fertil 1994;2:305-312.
33. Lane M, Gardner DK. Selection of viable mouse blastocysts prior to transfer using a metabolic criterion. Hum Reprod 1996;9:1975-1978.
34. Lane M, Gardner DK. Mitochondrial malate-aspartate shuttle regulates mouse embryo nutrient consumption. JBiol Chem 2005;18:18361-18367.
35. Lawitts JA, Biggers JD. Joint effectsof sodium chloride, glutamine, and glucose in mouse preimplantation embryo culture media. Mol Reprod Dev 1992; 3:189-194.
36. Leese HJ, Barton AM. Pyruvate and glucose uptake by mouse ova and preimplantation embryos. J Reprod Fertil 1984;1:9-13.
37. Lindenbaum A. Asurveyof naturally occurring chelating ligands. Adv Exp Med Biol 1973;40:67-77.
38. 2. Biol Reprod 1995;4:786-790.
39. Lundin K, Bergh C, Hardarson T. Early embryo cleavage is a strong indicator of embryo quality in human IVF. Hum Reprod 2001;12:2652-2657.
40. Martin PM, Sutherland AE, Van Winkle LJ. Amino acid transport regulates blastocyst implantation. Biol Reprod 2003;4:1101-1108.
41. Mastenbroek S, Twisk M, Van Echten-Arends J, Sikkema-Raddatz B, Korevaar JC, Verhoeve HR, Vogel NE, Arts EG, De Vries JW, Bossuyt PM et al. In vitro fertilization with preimplantation genetic screening. N Engl J Med 2007;1:9-17.
42. Meseguer M, Herrero J, Tejera A, Hilligsoe KM, Ramsing NB, Remohi J. The use of morphokinetics as a predictorof embryo implantation. Hum Reprod 2011;10:2658-2671.
43. Meseguer M, Rubio I, Cruz M, Basile N, Marcos J, Requena A. Embryo incubation and selection in a time-lapse monitoring system improves pregnancy outcome compared with a standard incubator: a retrospective cohort study. Fertil Steril 2012;6:1481-1489.e10.
44. 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;2:295-301.
45. Montag M, Liebenthron J, Koster M. Which morphological scoring system is relevant in human embryo development? Placenta 2011;32(Suppl 3): S252-S256.
46. Nagy ZP, Jones-Colon S, Roos P, Botros L, Greco E, Dasig J, Behr B. Metabolomic assessment of oocyte viability. Reprod Biomed Online 2009; 2:219-225.
47. Pribenszky C, Losonczi E, Molnar M, Lang Z, Matyas S, Rajczy K, Molnar K, Kovacs P, Nagy P, Conceicao J et al. Prediction of in-vitro developmental competence of early cleavage-stage mouse embryos with compact time-lapse equipment. Reprod Biomed Online 2010;3:371-379.
48. Rubio I, Kuhlmann R, Agerholm I, Kirk J, Herrero J, Escriba MJ, Bellver J, Meseguer M. Limited implantation success of direct-cleaved human zygotes: a time-lapse study. Fertil Steril 2012;6:1458-1463.
49. Scott LA, Smith S. The successful use of pronuclear embryo transfers the day following oocyte retrieval. Hum Reprod 1998;4:1003-1013.
50. Seli E, Robert C, Sirard MA. OMICS in assisted reproduction: possibilities and pitfalls. Mol Hum Reprod 2010;8:513-530.
51. Shoukir Y, Campana A, Farley T, Sakkas D. Early cleavageof in-vitro fertilized human embryosto the 2-cell stage:a novel indicatorof embryo quality and viability. Hum Reprod 1997;7:1531-1536.
52. Sunderam S, Kissin DM, Crawford S, Anderson JE, Folger SG, Jamieson DJ, Barfield WD. Assisted reproductive technology surveillance-United States, 2010. MMWR Surveill Summ 2013;62:1-24.
53. 2 consumption patterns determined optimal time ranges for selecting viable human embryos. Fertil Steril 2012;4:849-857.e1-3.
54. Templeton A. Joseph Price oration. The multiple gestation epidemic: the role of the assistedreproductivetechnologies. Am J Obstet Gynecol 2004;4:894-898.
55. Van Montfoort AP, Dumoulin JC, Kester AD, Evers JL. Early cleavage is a valuable addition to existing embryo selection parameters: a study using single embryo transfers. Hum Reprod 2004;9:2103-2108.
56. Van Royen E, Mangelschots K, De Neubourg D, Valkenburg M, Van De Meerssche M, Ryckaert G, Eestermans W, Gerris J. Characterization of a top quality embryo, a step towards single-embryo transfer. Hum Reprod 1999;9:2345-2349.
57. Vickery HB, Pucher GW, Clark HE. The determination of glutamine in the presence of asparagine. Biochem J 1935;12:2710-2720.
58. Wale PL, Gardner DK. Time-lapse analysisofmouse embryo development in oxygen gradients. Reprod Biomed Online 2010;3:402-410.
59. Wale PL, Gardner DK. Oxygen regulates amino acid turnover and carbohydrate uptake during the preimplantation period of mouse embryo development. Biol Reprod 2012;1:1-8.
60. Wale PL, Gardner DK. Oxygen affects the ability of mouse blastocysts to regulate ammonium. Biol Reprod 2013;3:1-10.
61. Wong CC, Loewke KE, Bossert NL, Behr B, De Jonge CJ, Baer TM, Pera RAR. Non-invasive imaging of human embryos before embryonic genome activation predicts development to the blastocyst stage. Nat Biotechnol 2010;10:1115-1121.
62. Zander DL, Thompson JG, Lane M. Perturbations in mouse embryo development and viability caused by ammonium are more severe after exposure at the cleavage stages. Biol Reprod 2006;2:288-294.
63. Zhang JQ, Li XL, Peng Y, Guo X, Heng BC, Tong GQ. Reductioninexposure of human embryos outside the incubator enhances embryo quality and blastulation rate. Reprod Biomed Online 2010;4:510-515.