New insights into human pre-implantation metabolism in vivo and in vitro

Journal of Assisted Reproduction and Genetics

Volumn 30, Issue 3, 2013, Pages 293-303

  Ménézo, Yves ^a,b   Lichtblau, Isabelle ^c   Elder, Kay ^d  

^a Laboratoire Clément   (France)

^b London Fertility Associates   (United Kingdom)

^c Clinique de la Muette   (France)

^d Bourn Hall Clinic ^*  (United Kingdom)

Author keywords

Culture medium; Human embryo; Imprinting; Metabolism; Oxidative stress

Indexed keywords

ASCORBIC ACID; ELECTROLYTE; ESSENTIAL AMINO ACID; GROWTH FACTOR; NONESSENTIAL AMINO ACID; PURINE; PYRIMIDINE; SERUM ALBUMIN; SULFUR AMINO ACID; TRIACYLGLYCEROL;

AMINO ACID COMPOSITION; CPG ISLAND; DNA REPAIR; FERTILIZATION; HUMAN; IN VITRO STUDY; IN VIVO STUDY; LEARNING; LIPID METABOLISM; LIPID SOLUBILITY; MACROMOLECULE; METABOLITE; METHYLATION; NONHUMAN; PHYSICAL CHEMISTRY; PRECURSOR; PREIMPLANTATION EMBRYO; PRIORITY JOURNAL; REVIEW; RNA SYNTHESIS; UREA CYCLE;

AMINO ACIDS; EMBRYONIC DEVELOPMENT; FERTILIZATION IN VITRO; GENOMIC IMPRINTING; HUMANS; LIPID METABOLISM; METABOLISM; OXIDATIVE STRESS; VITAMINS;

ANIMALIA;

EID: 84876285926     PISSN: 10580468     EISSN: 15737330     Source Type: Journal    
DOI: 10.1007/s10815-013-9953-9     Document Type: Review

References (92)

1. Whitten WK. Culture of tubal mouse ova. Nature. 1956;177:96.
2. Brinster RL. Studies on the development of mouse embryos in vitro I the effect of osmolarity and hydrogen ion concentration. J Exp Zool. 1965;158:49-57.
3. Brinster RL. Studies on the development of mouse embryos in vitro II. The effect of energy sources. J Exp Zool. 1965;158:59-68.
4. Brinster RL. Studies on the development of mouse embryos in vitro III the effect of fixed nitrogen source. J Exp Zool. 1965;158:69-77.
5. Brinster RL. In vitro culture of mammalian embryos. J Anim Sci. 1968;27 Suppl 1:1-14.
6. Whittingham DG. Culture of mouse ova. J Reprod Fertil Suppl. 1971;14:7-21.
7. Tervit HR, Whittingham D, Rowson LEA. Successful culture in vitro of sheep and cattle ova. J Reprod Fertil. 1972;20:493-7.
8. Ménézo Y. Milieu synthétique pour la survie et la maturation des gamètes et pour la culture de l'œuf fécondé. CR Acad Sci D Paris. 1976;282:1967-70.
9. Ao A, Erickson RP, Winston RM, Handyside AH. Transcription of paternal Y-linked genes in the human zygote as early as the pronucleate stage. Zygote. 1994;2:281-7.
10. Lopes S, Jurisicova A, Casper RF. Gamete-specific DNA fragmentation in unfertilized human oocytes after intracytoplasmic sperm injection. Hum Reprod. 1998;13:703-8.
11. Ménézo Y, Dale B, Cohen M. DNA damage and repair in human oocytes and embryos: a review. Zygote. 2010;18:357-65.
12. Betteridge KJ, Rieger D. Embryo transfer and related techniques in domestic animals, and their implications for human medicine. Hum Reprod. 1993;8:147-67.
13. Ho Y, Doherty AS, Schultz RM. Mouse preimplantation embryo embryo development in vitro: effect of sodium concentration in culture media on RNA synthesis and accumulation and gene expression. Mol Reprod Dev. 1994;38:131-41.
14. Jung T. Protein synthesis and degradation in non-cultured and in vitro cultured rabbit blastocysts. J Reprod Fertil. 1989;86:507-12.
15. Wrenzycki C, Herrmann D, Carnwath JW, Niemann H. Alterations in the relative abundance of gene transcripts in preimplantation bovine embryos cultured in medium supplemented with either serum or PVA. Mol Reprod Dev. 1999;53:8-18.
16. Hiura H, Okae H, Miyauchi N, Sato F, Sato A, Van De Pette M, et al. Characterization of DNA methylation errors in patients with imprinting disorders conceived by assisted reproduction technologies. Hum Reprod. 2012;27:2541-8.
17. Naglee DL, Maurer RR, Foote RH. Effect of osmolarity on in vitro development of rabbit embryos in a chemically defined medium. Exp Cell Res. 1969;58:331-3.
18. Ménézo YJ, Hérubel F. Mouse and bovine models for human IVF. Reprod Biomed Online. 2002;4:170-5.
19. Liu Z, Foote RH. Sodium chloride, osmolytes, and osmolarity effects on blastocyst formation in bovine embryos produced by in vitro fertilization (IVF) and cultured in simple serum-free media. J Assist Reprod Genet. 1996;13:562-8.
20. Kane MT. Bicarbonate requirements for culture of one-cell rabbit ova to blastocysts. Biol Reprod. 1975;12:552-5.
21. Gomes Sobrinho DB, Oliveira JB, Petersen CG, Mauri AL, Silva LF, Massaro FC, et al. IVF/ICSI outcomes after culture of human embryos at low oxygen tension: a meta-analysis. Reprod Biol Endocrinol. 2011;9:143-54.
22. Guérin P, El Mouatassim S, Ménézo Y. Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings. Hum Reprod Update. 2001;7:175-89.
23. Martín-Romero FJ, Miguel-Lasobras EM, Domínguez-Arroyo JA, González-Carrera E, Alvarez IS. Contribution of culture media to oxidative stress and its effect on human oocytes. Reprod Biomed Online. 2008;17:652-6.
24. Wales RG, Brinster RL. The uptake of hexoses by mouse pre-implantation embryos in vitro. J Reprod Fertil. 1968;15:415-22.
25. Schini, Bavister BD. Two-cell block to development of cultured hamster embryos is caused by phosphate and glucose. Biol Reprod. 1988;39:1183-92.
26. Chatot CL, Ziomek CA, Bavister BD, Lewis JL, Torres I. An improved culture medium supports development of random-bred 1-cell mouse embryos in vitro. J Reprod Fertil. 1989;86:679-88.
27. Biggers JD, McGinnis LK. Evidence that glucose is not always an inhibitor of mouse preimplantation development in vitro. Hum Reprod. 2001;16:153-63.
28. Pampfer S. Apoptosis in rodent peri-implantation embryos: differential susceptibility of inner cell mass and trophectoderm cell lineages - a review. Placenta. 2000;21(suppltA):S3-10.
29. Jimenez A, Madrid-Bury N, Fernandez R, Pérez-Garnelo S, Moreira P, Pintado B, et al. Hyperglycemia-induced apoptosis affects sex ratio of bovine and murine preimplantation embryos. Mol Reprod Dev. 2003;65:180-7.
30. Cassuto G, Chavrier M, Menezo Y. Culture conditions and not prolonged culture time are responsible for monozygotic twinning in human in vitro fertilization. Fertil Steril. 2003;80:462-3.
31. Ménézo Y, Khatchadourian C. Implication of glucose 6 phosphate isomerase (EC 5.3.1.9) activity in blocking segmentation of the mouse ovum at the 2 cell stage in vitro. CR Acad Sci. 1990;310:297-301.
32. Ludwig TE, Lane M, Bavister BD. Differential effect of hexoses on hamster embryo development in culture. Biol Reprod. 2001;64:1366-74.
33. Downs SM, Mosey JL, Klinger J. Fatty acid oxidation and meiotic resumption in mouse oocytes. Mol Reprod. Dev. 2009; 76:844-53.
34. Dunning KR, Akison LK, Russell DL, Norman RJ, Robker RL. Increased beta-oxidation and improved oocyte developmental competence in response to L-carnitine during ovarian in vitro follicle development in mice. Biol Reprod. 2011;85:548-55.
35. Dunning KR, Cashman K, Russell DL, Thompson JG, Norman RJ, Robker RL. Beta-oxidation is essential for mouse oocyte developmental competence and early embryo development. Biol Reprod. 2010;83:909-18.
36. Waterman RA, Wall RJ. Lipid interactions with in vitro development of mammalian zygotes. Gamete Res. 1988;21:243-54.
37. Hillman N, Flynn TJ. The metabolism of exogenous fatty acids by preimplantation mouse embryos developing in vitro. J Embryol Exp Morphol. 1980;56:157-68.
38. Ferguson EM, Leese HJ. A potential role for triglyceride as an energy source during bovine oocyte maturation and early embryo development. Mol Reprod Dev. 2006;73:1195-201.
39. Homa ST, Racowsky C, McGaughey RW. Lipid analysis of immature pig oocytes. J Reprod Fertil. 1986;77:425-34.
40. Flynn TJ, Hillman N. Lipid synthesis from [U14C]glucose in pre-implantation mouse embryos in culture. Biol Reprod. 1978;19:922-6.
41. Ménézo Y, Renard JP, Delobel B, Pageaux JF. Kinetic study of fatty acid composition of day 7 to day 14 cow embryos. Biol Reprod. 1982;26:787-90.
42. Montjean D, Entezami F, Lichtblau I, Belloc S, Gurgan T, Menezo Y. Carnitine content in the follicular fluid and expression of the enzymes involved in beta oxidation in oocytes and cumulus cells. J Assist Reprod Genet. 2012;29:1221-5.
43. Abdelrazik A, El-Damen H, Badrawi R, Sharma A. Agarwal Introduction of a single step medium from fertilization through blastocyst stage by supplementation of the culture media with L-Carnitine. ASRM meeting, Washington DC; 2007. p. 312.
44. Casslén BG. Free amino acids in human uterine fluid. Possible role of high taurine concentration. J Reprod Med. 1987;32:181-4.
45. 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;56:1550-8.
46. Baltz JM. Media composition: salts and osmolality. Methods Mol Biol. 2012;912:61-80.
47. Khatchadourian C, Guillaud J, Menezo Y. Interactions in glycine and methionine uptake, conversion and incorporation into proteins in the preimplantation mouse embryo. Zygote. 1994;2:301-6.
48. Summers MC, Biggers JD. Chemically defined media and the culture of mammalian preimplantation embryos: historical perspective and current issues. Hum Reprod Update. 2003;9:557-82.
49. Guyader-Joly C, Khatchadourian C, Ménézo Y. Comparative glucose and fructose incorporation and conversion by in vitro produced bovine embryos. Zygote. 1996;4:85-91.
50. Brison DR, Houghton FD, Falconer D, Roberts SA, Hawkhead J, Humpherson PG, et al. Identification of viable embryos in IVF by non-invasive measurement of amino acid turnover. Hum Reprod. 2004;19:2319-24.
51. Ménézo Y, Testart J, Perone D. Serum is not necessary in human in vitro fertilization, early embryo culture, and transfer. Fertil Steril. 1984;42:750-5.
52. Tay JI, Rutherford AJ, Killick SR, Maguiness SD, Partridge RJ, Leese HJ. Human tubal fluid: production, nutrient composition and response to adrenergic agents. Hum Reprod. 1997;12:2451-6.
53. De Groot N, Hochberg A. Gene imprinting during placental and embryonic development. Mol Reprod Dev. 1993;36:390-406.
54. Goshen R, Ben Rafael Z, Gonik B, Lustig O, Tannos V, de-Groot N, et al. The role of genomic imprinting in implantation. Fertil Steril. 1994;2:903-10.
55. Khosla S, Dean W, Reik W. Culture of pre-implantation embryos and its long-term effects on gene expression and phenotype. Hum Reprod Updat. 2001;7:419-27.
56. Ménézo Y, Khatchadourian C, Gharrib A, Hamidi J, Sarda N. Regulation of sadenosyl methionine synthesis in the mouse embryo. Life Sci. 1989;44:1601-9.
57. Benkhalifa M, Montjean D, Cohen-Bacrie P, Ménézo Y. Imprinting: RNA expression for ho mocysteine recycling in the human oocyte. Fertil Steril. 2010;93:1585-90.
58. Niemitz EL, Feinberg AP. Epigenetics and assisted reproductive technology: a call for investigation. Am J Hum Genet. 2004;74:599-609.
59. Wolff GL, Kodell RL, Moore SR, Cooney CE. Maternal epigenetics and methyl supplements affect agouti gene expression in Avy/mice. FASEB J. 1998;12:949-57.
60. Xin Z, Tachibana M, Guggiari, et al. Role of histone methyltransferase G9a in CpG methylation of the Prader-Willi syndrome imprinting centre. J Biol Chem. 2003;278:14996-5000.
61. Hoffman M. Hypothesis: hyperhomocysteinemia is an indicator of oxidant stress. Med Hypotheses. 2011;77:1088-93.
62. Ménézo Y, Mares P, Cohen M, Brack M, Viville S, Elder K. Autism, imprinting and epigenetic disorders: a metabolic syndrome linked to anomalies in homocysteine recycling starting in early life J Assist Reprod Genet. 2011;28:1143-5.
63. Lu S, Hoestje SM, Choo E, Epner DE. Induction of caspase dependant and independant apoptosis in response to methionine restriction. Int J Oncol. 2003;22:415-20.
64. Guérin P, Ménézo Y. Hypotaurine and taurine in gamete and embryo environments: de novo synthesis via the cysteine sulfinic acid pathway in oviduct cells. Zygote. 1995;3:333-43.
65. Dumoulin JC, van Wissen LC, Menheere PP, Michiels AH, Geraedts JP, Evers JL. Taurine acts as an osmolyte in human and mouse oocytes and embryos. Biol Reprod. 1997;56:739-44.
66. Gardner DK, Lane M. Amino acids and ammonium regulate mouse embryo development in culture. Biol Reprod. 1993;48:377-85.
67. Elhassan YM, Wu G, Leanez AC, et al. Amino acid concentrations in fluids from the bovine oviduct and uterus and in KSOM-based culture media. Theriogenology. 2001;55:1907-18.
68. Katari S, Turan N, Bibikova M, Erinle O, Chalian R, Foster M, et al. DNA methylation and gene expression differences in children conceived in vitro or in vivo. Hum Mol Genet. 2009;18:3769-78.
69. Pike IL, Murdoch RN, Wales RG. The incorporation of carbon dioxide into the major classes of RNA during culture of the preimplantation mouse embryo. J Reprod Fertil. 1975;45:211-2.
70. Badouard C, Ménézo Y, Panteix G, Ravanat JL, Douki T, Cadet J, et al. Determination of new types of DNA lesions in human sperm. Zygote. 2008;16:9-13.
71. Zenzes MT, Puy LA, Bielecki R. Immunodetection of benzo[a]pyrene adducts in ovarian cells of women exposed to cigarette smoke. Mol Hum Reprod. 1998;4:159-65.
72. Wachsman JT. DNA methylation and the association between genetic and epigenetic changes: relation to carcinogenesis. Mutat Res. 1997;375:1-8.
73. Ménézo YJR, Russo G, Tosti E, El Mouatassim S, Benkhalifa M. Expression profile of genes coding for DNA repair in human oocytes using pangenomic microarrays, with a special focus on ROS linked decays. J Assist Reprod Genet. 2007;24:513-20.
74. Epstein CJ. Gene expression and macromolecular synthesis during pre-implantation embryonic development. Biol Reprod. 1975;12:82-105.
75. Olson SE, Seidel Jr GE. Culture of in vitro-produced bovine embryos with vitamin E improves development in vitro and after transfer to recipients. Biol Reprod. 2000;62:248-52.
76. Giustarini D, Dalle-Donne I, Colombo R, Milzani A, Rossi R. Is ascorbate able to reduce disulfide bridges? A cautionary note. Nitric Oxide. 2008;19:252-8.
77. Bavister BD, Leibfried ML, Lieberman G. Development of preimplantation embryos of the golden hamster in a defined culture medium. Biol Reprod. 1983;28:235-47.
78. Tsai FC, Gardner DK. Nicotinamide, a component of complex culture media, inhibits mouse embryo development in vitro and reduces subsequent developmental potential after transfer. Fertil Steril. 1994;61:376-82.
79. O'Neill C. Endogenous folic acid is essential for normal development of preimplantation embryos. Hum Reprod. 1998;13:1312-6.
80. Ménézo Y, Entezami F, Lichtblau I, Belloc S, Cohen M, Dale B. Oxidative stress and fertility: incorrect assumptions and ineffective solutions? Zygote. 2012;12:1-11.
81. Caro CM, Trounson A. Successful fertilization, embryo development, and pregnancy in human in vitro fertilization (IVF) using a chemically defined culture medium containing no protein. J In Vitro Fert Embryo Transf. 1986;3:215-7.
82. Menezo Y, Khatchadourian C. Peptides bound to albumin. Life Sci. 1986;39:1751-3.
83. Croteau S, Menezo Y. Growth factors: from oocyte maturation to blastocyst. Contracept Fertil Sex. 1994;22:648-55.
84. Richter KS. The importance of growth factors for preimplantation embryo development and in-vitro culture. Curr Opin Obstet Gynecol. 2008;20:292-304.
85. Ménézo YJ, Servy E, Veiga A, Hazout A, Elder K. Culture systems: embryo co-culture. Methods Mol Biol. 2012;912:231-47.
86. Paria BC, Dey SK. Preimplantation embryo development in vitro: cooperative interactions among embryos and the role of growth factors. Proc Natl Acad Sci USA. 1990;87:4756-60.
87. Gopichandran N, Leese HJ. The effect of paracrine/autocrine interactions on the in vitro culture of bovine preimplantation embryos. Reprod. 2006;131:269-67.
88. O'Neill C. Evidence for the requirement of autocrine growth factors for development of mouse - preimplantation embryos in vitro. Biol Reprod. 1997;56:229-37.
89. Desai NN, Goldfarb JM. Growth factor/cytokine secretion by a permanent human endometrial cell line with embryotrophic properties. J Assist Reprod Genet. 1996;13:546-50.
90. Desai NN, Goldfarb J. Co-cultured human embryos may be subjected to widely different microenvironments: pattern of growth factor/cytokine release by Vero cells during the co-culture interval. Hum Reprod. 1998;13:1600-5.
91. Patrizio P, Sakkas D. From oocyte to baby: a clinical evaluation of the biological efficiency of in vitro fertilization. Fertil Steril. 2009;91:1061-6.
92. Menezo Y, Guerin P. Preimplantation embryo metabolism and embryo interaction with the in vitro environment. In: Elder K, Cohen J, editors. Human preimplantation Embryo evaluation and selection. London: Taylor-Francis; 2007. p. 191-200.