Combined effects of individual culture and atmospheric oxygen on preimplantation mouse embryos in vitro

Reproductive BioMedicine Online

Volumn 33, Issue 5, 2016, Pages 537-549

  Kelley, Rebecca L ^a   Gardner, David K ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

group culture; IVF; oxidative stress; paracrine factors; single culture; time lapse

Indexed keywords

OXYGEN;

ANIMAL TISSUE; ARTICLE; BLASTOCYTE; CELL KINETICS; CONTROLLED STUDY; EMBRYO; EMBRYO CULTURE; EMBRYO DEVELOPMENT; HATCHING; IN VITRO FERTILIZATION; MOUSE; NONHUMAN; OXIDATIVE STRESS; PREIMPLANTATION EMBRYO; TIME-LAPSE VIDEO MICROSCOPY; ANIMAL; BLASTOCYST; C57BL MOUSE; CHEMISTRY; CYTOLOGY; OOCYTE CLEAVAGE; PHYSIOLOGY; TIME LAPSE IMAGING; TUMOR MICROENVIRONMENT;

ANIMALS; BLASTOCYST; CELLULAR MICROENVIRONMENT; CLEAVAGE STAGE, OVUM; EMBRYO CULTURE TECHNIQUES; EMBRYONIC DEVELOPMENT; MICE; MICE, INBRED C57BL; OXYGEN; TIME-LAPSE IMAGING;

EID: 84995554275     PISSN: 14726483     EISSN: 14726491     Source Type: Journal    
DOI: 10.1016/j.rbmo.2016.08.003     Document Type: Article

References (159)

1. Almagor, M., Bejar, C., Kafka, I., Yaffe, H., Pregnancy rates after communal growth of preimplantation human embryos in vitro. Fertil. Steril 66 (1996), 394–397.
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 17 (2008), 669–675.
3. Austgulen, R., Arntzen, K.J., Vatten, L.J., Kahn, J., Sunde, A., Detection of cytokines (interleukin-1, interleukin-6, transforming growth factor-beta) and soluble tumour necrosis factor receptors in embryo culture fluids during in-vitro fertilization. Hum. Reprod 10 (1995), 171–176.
4. Aviles, M., Gutierrez-Adan, A., Coy, P., Oviductal secretions: will they be key factors for the future ARTs?. Mol. Hum. Reprod 16 (2010), 896–906.
5. Bar-Or, D., Bar-Or, R., Rael, L.T., Gardner, D.K., Slone, D.S., Craun, M.L., Heterogeneity and oxidation status of commercial human albumin preparations in clinical use. Crit. Care Med 33 (2005), 1638–1641.
6. Batt, P.A., Gardner, D.K., Cameron, A.W., Oxygen concentration and protein source affect the development of preimplantation goat embryos in vitro. Reprod. Fertil. Dev 3 (1991), 601–607.
7. Bavister, B.D., Culture of preimplantation embryos: facts and artifacts. Hum. Reprod. Update 1 (1995), 91–148.
8. Bean, C.J., Hassold, T.J., Judis, L., Hunt, P.A., Fertilization in vitro increases non-disjunction during early cleavage divisions in a mouse model system. Hum. Reprod 17 (2002), 2362–2367.
9. Binder, N.K., Mitchell, M., Gardner, D.K., Parental diet-induced obesity leads to retarded early mouse embryo development and altered carbohydrate utilisation by the blastocyst. Reprod. Fertil. Dev 24 (2012), 804–812.
10. Bolton, V.N., Cutting, R., Clarke, H., Brison, D.R., ACE consensus meeting report: culture systems. Hum. Fertil 17 (2014), 239–251.
11. 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(7), 2012 CD008950.
12. Brison, D.R., Schultz, R.M., Apoptosis during mouse blastocyst formation: evidence for a role for survival factors including transforming growth factor alpha. Biol. Reprod 56 (1997), 1088–1096.
13. Brömme, D., Wilson, S., Role of cysteine cathepsins in extracellular proteolysis. Parks, C.W., Mecham, P.R., (eds.) Extracellular Matrix Degradation, 2011, Springer-Verlag, Berlin, Heidelberg, 23–51.
14. Carolan, C., Lonergan, P., Khatir, H., Mermillod, P., In vitro production of bovine embryos using individual oocytes. Mol. Reprod. Dev 45 (1996), 145–150.
15. Catt, J.W., Henman, M., Toxic effects of oxygen on human embryo development. Hum. Reprod 15 (2000), 199–206.
16. Christianson, M.S., Zhao, Y., Shoham, G., Granot, I., Safran, A., Khafagy, A., Leong, M., Shoham, Z., Embryo catheter loading and embryo culture techniques: results of a worldwide Web-based survey. J. Assist. Reprod. Genet 31 (2014), 1029–1036.
17. Chung, Y.H., Hsiao, Y.H., Kao, W.L., Hsu, C.H., Yao, D.J., Chen, C., Microwells support high-resolution time-lapse imaging and development of preimplanted mouse embryos. Biomicrofluidics, 9, 2015, 022407.
18. Ciray, H.N., Campbell, A., Agerholm, I.E., Aguilar, J., Chamayou, S., Esbert, M., Sayed, S., Proposed guidelines on the nomenclature and annotation of dynamic human embryo monitoring by a time-lapse user group. Hum. Reprod 29 (2014), 2650–2660.
19. Conaghan, J., Chen, A.A., Willman, S.P., Ivani, K., Chenette, P.E., Boostanfar, R., Baker, V.L., Adamson, G.D., Abusief, M.E., Gvakharia, M., Loewke, K.E., Shen, S., Improving embryo selection using a computer-automated time-lapse image analysis test plus day 3 morphology: results from a prospective multicenter trial. Fertil. Steril 100 (2013), 412–419.
20. Contramaestre, A.P., Sifontes, F., Marin, R., Camejo, M.I., Secretion of stem cell factor and granulocyte-macrophage colony-stimulating factor by mouse embryos in culture: influence of group culture. Zygote 16 (2008), 297–301.
21. Coy, P., Yanagimachi, R., The common and species-specific roles of oviductal proteins in mammalian fertilization and embryo development. Bioscience 65 (2015), 973–984.
22. de Waal, E., Mak, W., Calhoun, S., Stein, P., Ord, T., Krapp, C., Coutifaris, C., Schultz, R.M., Bartolomei, M.S., In vitro culture increases the frequency of stochastic epigenetic errors at imprinted genes in placental tissues from mouse concepti produced through assisted reproductive technologies. Biol. Reprod, 90, 2014, 22.
23. Dadi, T.D., Li, M.W., Lloyd, K.C., Expression levels of EGF, TGF-alpha, and EGF-R are significantly reduced in pre-implantation cloned mouse embryos. Cloning Stem Cells 6 (2004), 267–283.
24. Dai, S.J., Xu, C.L., Wang, J., Sun, Y.P., Chian, R.C., Effect of culture medium volume and embryo density on early mouse embryonic development: tracking the development of the individual embryo. J. Assist. Reprod. Genet 29 (2012), 617–623.
25. Doherty, E.M.O., Wade, M.G., Hill, J.L., Boland, M.P., Effects of culturing bovine oocytes either singly or in groups on development to blastocysts. Theriogenology 48 (1997), 161–169.
26. Donnay, I., Van Langendonckt, A., Auquier, P., Grisart, B., Vansteenbrugge, A., Massip, A., Dessy, F., Effects of co-culture and embryo number on the in vitro development of bovine embryos. Theriogenology 47 (1997), 1549–1561.
27. Dumoulin, J.C., Meijers, C.J., Bras, M., Coonen, E., Geraedts, J.P., Evers, J.L., Effect of oxygen concentration on human in-vitro fertilization and embryo culture. Hum. Reprod 14 (1999), 465–469.
28. Dyrlund, T.F., Kirkegaard, K., Poulsen, E.T., Sanggaard, K.W., Hindkjaer, J.J., Kjems, J., Enghild, J.J., Ingerslev, H.J., Unconditioned commercial embryo culture media contain a large variety of non-declared proteins: a comprehensive proteomics analysis. Hum. Reprod 29 (2014), 2421–2430.
29. Ebner, T., Shebl, O., Moser, M., Mayer, R.B., Arzt, W., Tews, G., Group culture of human zygotes is superior to individual culture in terms of blastulation, implantation and life birth. Reprod. Biomed. Online 21 (2010), 762–768.
30. Esfandiari, N., Falcone, T., Agarwal, A., Attaran, M., Nelson, D.R., Sharma, R.K., Protein supplementation and the incidence of apoptosis and oxidative stress in mouse embryos. Obstet. Gynecol 105 (2005), 653–660.
31. Favetta, L.A., St John, E.J., King, W.A., Betts, D.H., High levels of p66shc and intracellular ROS in permanently arrested early embryos. Free Radic. Biol. Med 42 (2007), 1201–1210.
32. Ferry, L., Mermillod, P., Massip, A., Dessy, F., Bovine embryos cultured in serum-poor oviduct-conditioned medium need co-operation to reach the blastocyst stage. Theriogenology 42 (1994), 445–453.
33. Fischer, B., Bavister, B.D., Oxygen tension in the oviduct and uterus of rhesus monkeys, hamsters and rabbits. J. Reprod. Fertil 99 (1993), 673–679.
34. Fischer, B., Schumacher, A., Hegele-Hartung, C., Beier, H.M., Potential risk of light and room temperature exposure to preimplantation embryos. Fertil. Steril 50 (1988), 938–944.
35. Fischer-Brown, A., Crooks, A., Leonard, S., Monson, R., Northey, D., Rutledge, J.J., Parturition following transfer of embryos produced in two media under two oxygen concentrations. Anim. Reprod. Sci 87 (2005), 215–228.
36. Fishel, S.B., Edwards, R.G., Evans, C.J., Human chorionic gonadotropin secreted by preimplantation embryos cultured in vitro. Science 223 (1984), 816–818.
37. Fujita, T., Umeki, H., Shimura, H., Kugumiya, K., Shiga, K., Effect of group culture and embryo-culture conditioned medium on development of bovine embryos. J. Reprod. Dev 52 (2006), 137–142.
38. Gardner, D.K., Lactate production by the mammalian blastocyst: manipulating the microenvironment for uterine implantation and invasion?. Bioessays 37 (2015), 364–371.
39. Gardner, D.K., Lane, M., Alleviation of the ‘2-cell block’ and development to the blastocyst of CF1 mouse embryos: role of amino acids, EDTA and physical parameters. Hum. Reprod 11 (1996), 2703–2712.
40. Gardner, D.K., Lane, M., Culture and selection of viable blastocysts: a feasible proposition for human IVF?. Hum. Reprod. Update 3 (1997), 367–382.
41. Gardner, D.K., Lane, M., Embryo culture systems. Gardner, D.K., (eds.) In Vitro Fertilization: A Practical Approach, 2007, Informa Healthcare, New York, 221–282.
42. Gardner, D.K., Lane, M., Mammalian preimplantation embryo culture. Methods Mol. Biol 1092 (2014), 167–182.
43. Gardner, D.K., Lane, M., Spitzer, A., Batt, P.A., Enhanced rates of cleavage and development for 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 (1994), 390–400.
44. Gardner, D.K., Reed, L., Linck, D., Sheehan, C., Lane, M., Quality control in human in vitro fertilization. Semin. Reprod. Med 23 (2005), 319–324.
45. Gaspar, R.C., Arnold, D.R., Correa, C.A., da Rocha, C.V. Jr., Penteado, J.C., Del Collado, M., Vantini, R., Garcia, J.M., Lopes, F.L., Oxygen tension affects histone remodeling of in vitro-produced embryos in a bovine model. Theriogenology 83 (2015), 1408–1415.
46. Gomes Sobrinho, D.B., Oliveira, J.B., Petersen, C.G., Mauri, A.L., Silva, L.F., Massaro, F.C., Baruffi, R.L., Cavagna, M., Franco, J.G. Jr., IVF/ICSI outcomes after culture of human embryos at low oxygen tension: a meta-analysis. Reprod. Biol. Endocrinol, 9, 2011, 143.
47. Goto, Y., Noda, Y., Mori, T., Nakano, M., Increased generation of reactive oxygen species in embryos cultured in vitro. Free Radic. Biol. Med 15 (1993), 69–75.
48. Griffiths, J.R., Are cancer cells acidic?. Br. J. Cancer 64 (1991), 425–427.
49. 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 7 (2001), 175–189.
50. Hannan, N.J., Paiva, P., Meehan, K.L., Rombauts, L.J., Gardner, D.K., Salamonsen, L.A., Analysis of fertility-related soluble mediators in human uterine fluid identifies VEGF as a key regulator of embryo implantation. Endocrinology 152 (2011), 4948–4956.
51. Hardy, K., Spanos, S., Growth factor expression and function in the human and mouse preimplantation embryo. J. Endocrinol 172 (2002), 221–236.
52. Hardy, K., Handyside, A.H., Winston, R.M., The human blastocyst: cell number, death and allocation during late preimplantation development in vitro. Development 107 (1989), 597–604.
53. Harvey, A.J., Kind, K.L., Pantaleon, M., Armstrong, D.T., Thompson, J.G., Oxygen-regulated gene expression in bovine blastocysts. Biol. Reprod 71 (2004), 1108–1119.
54. Harvey, A.J., Rathjen, J., Gardner, D.K., Metaboloepigenetic Regulation of Pluripotent Stem Cells. Stem Cells Int, 2016, 2016, 1816525.
55. Harvey, M.B., Leco, K.J., Arcellana-Panlilio, M.Y., Zhang, X., Edwards, D.R., Schultz, G.A., Proteinase expression in early mouse embryos is regulated by leukaemia inhibitory factor and epidermal growth factor. Development 121 (1995), 1005–1014.
56. Hashimoto, S., Kato, N., Saeki, K., Morimoto, Y., Selection of high-potential embryos by culture in poly(dimethylsiloxane) microwells and time-lapse imaging. Fertil. Steril 97 (2012), 332–337.
57. Hemmings, R., Langlais, J., Falcone, T., Granger, L., Miron, P., Guyda, H., Human embryos produce transforming growth factors alpha activity and insulin-like growth factors II. Fertil. Steril 58 (1992), 101–104.
58. Hughes, P.M., Morbeck, D.E., Hudson, S.B., Fredrickson, J.R., Walker, D.L., Coddington, C.C., Peroxides in mineral oil used for in vitro fertilization: defining limits of standard quality control assays. J. Assist. Reprod. Genet 27 (2010), 87–92.
59. Hwang, S., Lee, E., Chung, Y., Yoon, B.K., Lee, J.H., Choi, D., Intactness of zona pellucida does not affect the secretion of a trypsin-like protease from mouse blastocyst. J. Korean Med. Sci 15 (2000), 529–532.
60. Ichikawa, S., Shibata, T., Takehara, Y., Tamada, H., Oda, K., Murao, S., Effects of proteinase inhibitors on preimplantation embryos in the rat. J. Reprod. Fertil 73 (1985), 385–390.
61. Ikeda, K., Takahashi, Y., Katagiri, S., Effect of medium change on the development of in vitro matured and fertilized bovine oocytes cultured in medium containing amino acids. J. Vet. Med. Sci 62 (2000), 121–123.
62. Isobe, T., Ikebata, Y., Do, L.T., Tanihara, F., Taniguchi, M., Otoi, T., In vitro development of OPU-derived bovine embryos cultured either individually or in groups with the silk protein sericin and the viability of frozen-thawed embryos after transfer. Anim. Sci. J. 86 (2015), 661–665.
63. Jin, X.L., O'Neill, C., Systematic analysis of the factors that adversely affect the rate of cell accumulation in mouse embryos during their culture in vitro. Reprod. Biol. Endocrinol, 12, 2014, 35.
64. Karagenc, L., Sertkaya, Z., Ciray, N., Ulug, U., Bahceci, M., Impact of oxygen concentration on embryonic development of mouse zygotes. Reprod. Biomed. Online 9 (2004), 409–417.
65. Kaser, D.J., Racowsky, C., Clinical outcomes following selection of human preimplantation embryos with time-lapse monitoring: a systematic review. Hum. Reprod. Update 20 (2014), 617–631.
66. Kato, Y., Tsunoda, Y., Effects of the culture density of mouse zygotes on the development in vitro and in vivo. Theriogenology 41 (1994), 1315–1322.
67. Kato, Y., Lambert, C.A., Colige, A.C., Mineur, P., Noel, A., Frankenne, F., Foidart, J.M., Baba, M., Hata, R., Miyazaki, K., Tsukuda, M., Acidic extracellular pH induces matrix metalloproteinase-9 expression in mouse metastatic melanoma cells through the phospholipase D-mitogen-activated protein kinase signaling. J. Biol. Chem 280 (2005), 10938–10944.
68. Katz-Jaffe, M.G., Linck, D.W., Schoolcraft, W.B., Gardner, D.K., A proteomic analysis of mammalian preimplantation embryonic development. Reproduction 130 (2005), 899–905.
69. Katz-Jaffe, M.G., Schoolcraft, W.B., Gardner, D.K., Analysis of protein expression (secretome) by human and mouse preimplantation embryos. Fertil. Steril 86 (2006), 678–685.
70. Keefer, C.L., Stice, S.L., Paprocki, A.M., Golueke, P., In vitro culture of bovine IVM-IVF embryos: co-operative interaction among embryos and the role of growth factors. Theriogenology 41 (1994), 1323–1331.
71. Khurana, N.K., Wales, R.G., Effects of oxygen concentration on the metabolism of [U-14C]glucose by mouse morulae and early blastocysts in vitro. Reprod. Fertil. Dev 1 (1989), 99–106.
72. Kind, K.L., Collett, R.A., Harvey, A.J., Thompson, J.G., Oxygen-regulated expression of GLUT-1, GLUT-3, and VEGF in the mouse blastocyst. Mol. Reprod. Dev 70 (2005), 37–44.
73. Kirkegaard, K., Hindkjaer, J.J., Ingerslev, H.J., Effect of oxygen concentration on human embryo development evaluated by time-lapse monitoring. Fertil. Steril 99 (2013), 738–744.
74. Kirkegaard, K., Campbell, A., Agerholm, I., Bentin-Ley, U., Gabrielsen, A., Kirk, J., Sayed, S., Ingerslev, H.J., Limitations of a time-lapse blastocyst prediction model: a large multicentre outcome analysis. Reprod. Biomed. Online 29 (2014), 156–158.
75. Kitagawa, Y., Suzuki, K., Yoneda, A., Watanabe, T., Effects of oxygen concentration and antioxidants on the in vitro developmental ability, production of reactive oxygen species (ROS), and DNA fragmentation in porcine embryos. Theriogenology 62 (2004), 1186–1197.
76. Kubisch, H.M., Johnson, K.M., The effects of blastomere biopsy and oxygen tension on bovine embryo development, rate of apoptosis and interferon-tau secretion. Reprod. Domest. Anim 42 (2007), 509–515.
77. Kwon, H.C., Yang, H.W., Hwang, K.J., Yoo, J.H., Kim, M.S., Lee, C.H., Ryu, H.S., Oh, K.S., Effects of low oxygen condition on the generation of reactive oxygen species and the development in mouse embryos cultured in vitro. J. Obstet. Gynaecol. Res 25 (1999), 359–366.
78. Lane, M., Gardner, D.K., Effect of incubation volume and embryo density on the development and viability of mouse embryos in vitro. Hum. Reprod 7 (1992), 558–562.
79. Lane, M., Gardner, D.K., Differential regulation of mouse embryo development and viability by amino acids. J. Reprod. Fertil 109 (1997), 153–164.
80. Lane, M., Gardner, D.K., Understanding cellular disruptions during early embryo development that perturb viability and fetal development. Reprod. Fertil. Dev 17 (2005), 371–378.
81. Lane, M., Gardner, D.K., Embryo culture medium: which is the best?. Best Pract. Res. Clin. Obstet. Gynaecol 21 (2007), 83–100.
82. Larson, M.A., Kubisch, H.M., The effects of group size on development and interferon-tau secretion by in-vitro fertilized and cultured bovine blastocysts. Hum. Reprod 14 (1999), 2075–2079.
83. Lee, E.S., Jung, Y.G., Araki, N., Fukui, Y., Effect of human or murine leukemia inhibitory factor on in vitro development of bovine morulae cultured singly or in a group. J. Mamm. Ova. Res 13 (1996), 19–23.
84. Lee, Y.S., Thouas, G.A., Gardner, D.K., Developmental kinetics of cleavage stage mouse embryos are related to their subsequent carbohydrate and amino acid utilization at the blastocyst stage. Hum. Reprod 30 (2015), 543–552.
85. Lemaire, R., Huet, G., Zerimech, F., Grard, G., Fontaine, C., Duquesnoy, B., Flipo, R.M., Selective induction of the secretion of cathepsins B and L by cytokines in synovial fibroblast-like cells. Br. J. Rheumatol 36 (1997), 735–743.
86. Li, W., Goossens, K., Van Poucke, M., Forier, K., Braeckmans, K., Van Soom, A., Peelman, L.J., High oxygen tension increases global methylation in bovine 4-cell embryos and blastocysts but does not affect general retrotransposon expression. Reprod. Fertil. Dev, 2014, 10.1071/RD14133 Epub 17 Dec 2014.
87. Lundin, K., Ahlstrom, A., Quality control and standardization of embryo morphology scoring and viability markers. Reprod. Biomed. Online 31 (2015), 459–471.
88. Mantikou, E., Jonker, M.J., Wong, K.M., van Montfoort, A.P., de Jong, M., Breit, T.M., Repping, S., Mastenbroek, S., Factors affecting the gene expression of in vitro cultured human preimplantation embryos. Hum. Reprod 31 (2016), 298–311.
89. Martinez-Hernandez, M.G., Baiza-Gutman, L.A., Castillo-Trapala, A., Armant, D.R., Regulation of proteinases during mouseperi-implantation development: urokinase-type plasminogen activator expression and cross talk with matrix metalloproteinase 9. Reproduction 141 (2011), 227–239.
90. Mastroianni, L. Jr., Jones, R., Oxygen tension within the rabbit fallopian tube. J. Reprod. Fertil 9 (1965), 99–102.
91. Meintjes, M., Chantilis, S.J., Douglas, J.D., Rodriguez, A.J., Guerami, A.R., Bookout, D.M., Barnett, B.D., Madden, J.D., A controlled randomized trial evaluating the effect of lowered incubator oxygen tension on live births in a predominantly blastocyst transfer program. Hum. Reprod 24 (2009), 300–307.
92. Meseguer, M., Herrero, J., Tejera, A., Hilligsoe, K.M., Ramsing, N.B., Remohi, J., The use of morphokinetics as a predictor of embryo implantation. Hum. Reprod 26 (2011), 2658–2671.
93. Meuter, A., Rogmann, L.M., Winterhoff, B.J., Tchkonia, T., Kirkland, J.L., Morbeck, D.E., Markers of cellular senescence are elevated in murine blastocysts cultured in vitro: molecular consequences of culture in atmospheric oxygen. J. Assist. Reprod. Genet 31 (2014), 1259–1267.
94. Moessner, J., Dodson, W.C., The quality of human embryo growth is improved when embryos are cultured in groups rather than separately. Fertil. Steril 64 (1995), 1034–1035.
95. Morbeck, D.E., Paczkowski, M., Fredrickson, J.R., Krisher, R.L., Hoff, H.S., Baumann, N.A., Moyer, T., Matern, D., Composition of protein supplements used for human embryo culture. J. Assist. Reprod. Genet 31 (2014), 1703–1711.
96. Nagao, Y., Iijima, R., Saeki, K., Interaction between embryos and culture conditions during in vitro development of bovine early embryos. Zygote 16 (2008), 127–133.
97. O'Neill, C., Autocrine mediators are required to act on the embryo by the 2-cell stage to promote normal development and survival of mouse preimplantation embryos in vitro. Biol. Reprod 58 (1998), 1303–1309.
98. O'Neill, C., The role of paf in embryo physiology. Hum. Reprod. Update 11 (2005), 215–228.
99. O'Sullivan, C.M., Rancourt, S.L., Liu, S.Y., Rancourt, D.E., A novel murine tryptase involved in blastocyst hatching and outgrowth. Reproduction 122 (2001), 61–71.
100. Paria, B.C., Dey, S.K., Preimplantation embryo development in vitro: co-operative interactions among embryos and role of growth factors. Proc. Natl. Acad. Sci. U.S.A. 87 (1990), 4756–4760.
101. Perona, R.M., Wassarman, P.M., Mouse blastocysts hatch in vitro by using a trypsin-like proteinase associated with cells of mural trophectoderm. Dev. Biol 114 (1986), 42–52.
102. Petersen, B.M., Boel, M., Montag, M., Gardner, D.K., Development of a generally applicable morphokinetic algorithm capable of predicting the implantation potential of embryos transferred on Day 3. Hum. Reprod, 2016 In press.
103. Pribenszky, C., Losonczi, E., Molnar, M., Lang, Z., Matyas, S., Rajczy, K., Molnar, K., Kovacs, P., Nagy, P., Conceicao, J., Vajta, G., Prediction of in-vitro developmental competence of early cleavage-stage mouse embryos with compact time-lapse equipment. Reprod. Biomed. Online 20 (2010), 371–379.
104. Pribenszky, C., Matyas, S., Kovacs, P., Losonczi, E., Zadori, J., Vajta, G., Pregnancy achieved by transfer of a single blastocyst selected by time-lapse monitoring. Reprod. Biomed. Online 21 (2010), 533–536.
105. Quinn, P., Harlow, G.M., The effect of oxygen on the development of preimplantation mouse embryos in vitro. J. Exp. Zool 206 (1978), 73–80.
106. Raff, M.C., Social controls on cell survival and cell death. Nature 356 (1992), 397–400.
107. Rebollar-Lazaro, I., Matson, P., The culture of human cleavage stage embryos alone or in groups: effect upon blastocyst utilization rates and implantation. Reprod. Biol 10 (2010), 227–234.
108. Rijnders, P.M., Jansen, C.A., Influence of group culture and culture volume on the formation of human blastocysts: a prospective randomized study. Hum. Reprod 14 (1999), 2333–2337.
109. Rinaudo, P.F., Giritharan, G., Talbi, S., Dobson, A.T., Schultz, R.M., Effects of oxygen tension on gene expression in preimplantation mouse embryos. Fertil. Steril 86 (2006), 1252–1265.
110. Robertson, S.A., Chin, P.Y., Schjenken, J.E., Thompson, J.G., Female tract cytokines and developmental programming in embryos. Leese, H.J., Brison, D.R., (eds.) Cell Signaling During Mammalian Early Embryo Development, 2015, Springer-Verlag, New York, 173–213.
111. Rodina, T.M., Cooke, F.N., Hansen, P.J., Ealy, A.D., Oxygen tension and medium type actions on blastocyst development and interferon-tau secretion in cattle. Anim. Reprod. Sci 111 (2009), 173–188.
112. Rubio, I., Galan, A., Larreategui, Z., Ayerdi, F., Bellver, J., Herrero, J., Meseguer, M., Clinical validation of embryo culture and selection by morphokinetic analysis: a randomized, controlled trial of the EmbryoScope. Fertil. Steril 102 (2014), 1287–1294.
113. Salahuddin, S., Ookutsu, S., Goto, K., Nakanishi, Y., Nagata, Y., Effects of embryo density and co-culture of unfertilized oocytes on embryonic development of in-vitro fertilized mouse embryos. Hum. Reprod 10 (1995), 2382–2385.
114. Salamonsen, L.A., Evans, J., Nguyen, H.P., Edgell, T.A., The microenvironment of human implantation: determinant of reproductive success. Am. J. Reprod. Immunol 75 (2016), 218–225.
115. Sawada, H., Yamazaki, K., Hoshi, M., Trypsin-like hatching protease from mouse embryos: evidence for the presence in culture medium and its enzymatic properties. J. Exp. Zool 254 (1990), 83–87.
116. Schoolcraft, W.B., Fragouli, E., Stevens, J., Munne, S., Katz-Jaffe, M.G., Wells, D., Clinical application of comprehensive chromosomal screening at the blastocyst stage. Fertil. Steril 94 (2010), 1700–1706.
117. Scott, R.T. Jr., Upham, K.M., Forman, E.J., Hong, K.H., Scott, K.L., Taylor, D., Tao, X., Treff, N.R., Blastocyst biopsy with comprehensive chromosome screening and fresh embryo transfer significantly increases in vitro fertilization implantation and delivery rates: a randomized controlled trial. Fertil. Steril 100 (2013), 697–703.
118. Seli, E., Sakkas, D., Scott, R., Kwok, S.C., Rosendahl, S.M., Burns, D.H., Noninvasive metabolomic profiling of embryo culture media using Raman and near-infrared spectroscopy correlates with reproductive potential of embryos in women undergoing in vitro fertilization. Fertil. Steril 88 (2007), 1350–1357.
119. Senatore, E.M., Xu, J., Suarez Novoa, M.V., Gong, G., Lin, T., Bella, A., Moreno, J.F., Mannino, M.E., Tian, X., Presicce, G.A., Wu, S.C., Du, F., Improved in vitro development of OPU-derived bovine (Bos taurus) embryos by group culture with agarose-embedded helper embryos. Theriogenology 74 (2010), 1643–1651.
120. Seshagiri, P.B., Vani, V., Madhulika, P., Cytokines and blastocyst hatching. Am. J. Reprod. Immunol 75 (2016), 208–217.
121. Sharkey, A.M., Dellow, K., Blayney, M., Macnamee, M., Charnock-Jones, S., Smith, S.K., Stage-specific expression of cytokine and receptor messenger ribonucleic acids in human preimplantation embryos. Biol. Reprod 53 (1995), 974–981.
122. Sharma, N., Liu, S., Tang, L., Irwin, J., Meng, G., Rancourt, D.E., Implantation Serine Proteinases heterodimerize and are critical in hatching and implantation. BMC Dev. Biol, 6, 2006, 61.
123. Somfai, T., Inaba, Y., Aikawa, Y., Ohtake, M., Kobayashi, S., Konishi, K., Imai, K., Relationship between the length of cell cycles, cleavage pattern and developmental competence in bovine embryos generated by in vitro fertilization or parthenogenesis. J. Reprod. Dev 56 (2010), 200–207.
124. Spanos, S., Becker, D.L., Winston, R.M., Hardy, K., Anti-apoptotic action of insulin-like growth factor-I during human preimplantation embryo development. Biol. Reprod 63 (2000), 1413–1420.
125. Spindler, R.E., Wildt, D.E., Quality and age of companion felid embryos modulate enhanced development by group culture. Biol. Reprod 66 (2002), 167–173.
126. Spindler, R.E., Crichton, E.G., Agca, Y., Loskutoff, N., Critser, J., Gardner, D.K., Wildt, D.E., Improved felid embryodevelopment by group culture is maintained with heterospecific companions. Theriogenology 66 (2006), 82–92.
127. Spyropoulou, I., Karamalegos, C., Bolton, V.N., A prospective randomized study comparing the outcome of in-vitro fertilization and embryo transfer following culture of human embryos individually or in groups before embryo transfer on day 2. Hum. Reprod 14 (1999), 76–79.
128. Stilley, K.S., Lane, M., Gardner, D.K., Heterologous co-culture of bovine embryos with mouse embryos stimulates blastocyst development and differentiation. Theriogenology, 59, 2003, 459.
129. Stoddart, N.R., Wild, A.E., Fleming, T.P., Stimulation of development in vitro by platelet-activating factor receptor ligands released by mouse preimplantation embryos. J. Reprod. Fertil 108 (1996), 47–53.
130. Sugimura, S., Akai, T., Hashiyada, Y., Somfai, T., Inaba, Y., Hirayama, M., Yamanouchi, T., Matsuda, H., Kobayashi, S., Aikawa, Y., Ohtake, M., Kobayashi, E., Konishi, K., Imai, K., Promising system for selecting healthy in vitro-fertilized embryos in cattle. PLoS ONE, 7, 2012, e36627.
131. Sun, B., Yu, W., Wang, F., Song, W., Jin, H., Sun, Y., Effects of group culture on the development of discarded human embryos and the construction of human embryonic stem cell lines. J. Assist. Reprod. Genet 31 (2014), 1369–1376.
132. Takahashi, M., Keicho, K., Takahashi, H., Ogawa, H., Schultz, R.M., Okano, A., Effect of oxidative stress on development and DNA damage in in-vitro cultured bovine embryos by comet assay. Theriogenology 54 (2000), 137–145.
133. Tervit, H.R., Whittingham, D.G., Rowson, L.E., Successful culture in vitro of sheep and cattle ova. J. Reprod. Fertil 30 (1972), 493–497.
134. Thompson, J.G., Simpson, A.C., Pugh, P.A., Donnelly, P.E., Tervit, H.R., Effect of oxygen concentration on in-vitro development of preimplantation sheep and cattle embryos. J. Reprod. Fertil 89 (1990), 573–578.
135. Thompson, S.M., Onwubalili, N., Brown, K., Jindal, S.K., McGovern, P.G., Blastocyst expansion score and trophectoderm morphology strongly predict successful clinical pregnancy and live birth following elective single embryo blastocyst transfer (eSET): a national study. J. Assist. Reprod. Genet 30 (2013), 1577–1581.
136. Thouas, G.A., Dominguez, F., Green, M.P., Vilella, F., Simon, C., Gardner, D.K., Soluble ligands and their receptors in human embryo development and implantation. Endocr. Rev 36 (2015), 92–130.
137. Truong, T.T., Soh, Y.M., Gardner, D.K., Antioxidants improve mouse preimplantation embryo development and viability. Hum. Reprod, 2016, 10.1093/humrep/dew098 Epub 10 May 2016.
138. Vajta, G., Korosi, T., Du, Y., Nakata, K., Ieda, S., Kuwayama, M., Nagy, Z.P., The Well-of-the-Well system: an efficient approach to improve embryo development. Reprod. Biomed. Online 17 (2008), 73–81.
139. Van Soom, A., Yuan, Y.Q., Peelman, L.J., de Matos, D.G., Dewulf, J., Laevens, H., de Kruif, A., Prevalence of apoptosis and inner cell allocation in bovine embryos cultured under different oxygen tensions with or without cysteine addition. Theriogenology 57 (2002), 1453–1465.
140. Vutyavanich, T., Saeng-Anan, U., Sirisukkasem, S., Piromlertamorn, W., Effect of embryo density and microdrop volume on the blastocyst development of mouse two-cell embryos. Fertil. Steril 95 (2011), 1435–1439.
141. Waldenstrom, U., Engstrom, A.B., Hellberg, D., Nilsson, S., Low-oxygen compared with high-oxygen atmosphere in blastocyst culture, a prospective randomized study. Fertil. Steril 91 (2009), 2461–2465.
142. Wale, P.L., Gardner, D.K., Time-lapse analysis of mouse embryo development in oxygen gradients. Reprod. Biomed. Online 21 (2010), 402–410.
143. Wale, P.L., Gardner, D.K., Oxygen regulates amino acid turnover and carbohydrate uptake during the preimplantation period of mouse embryo development. Biol. Reprod 87 (2012), 21–28.
144. Wale, P.L., Gardner, D.K., Oxygen affects the ability of mouse blastocysts to regulate ammonium. Biol. Reprod, 89, 2013, 75.
145. Wale, P.L., Gardner, D.K., The effects of chemical and physical factors on mammalian embryo culture and their importance for the practice of assisted human reproduction. Hum. Reprod. Update 22 (2016), 2–22.
146. Weinerman, R., Feng, R., Ord, T.S., Schultz, R.M., Bartolomei, M.S., Coutifaris, C., Mainigi, M., Morphokinetic evaluation of embryo development in a mouse model: functional and molecular correlates. Biol. Reprod, 2016, 10.1095/biolreprod.115.134080 Epub 24 Feb 2016.
147. Westermarck, J., Kahari, V.M., Regulation of matrix metalloproteinase expression in tumor invasion. FASEB J. 13 (1999), 781–792.
148. Whiteside, E.J., Kan, M., Jackson, M.M., Thompson, J.G., McNaughton, C., Herington, A.C., Harvey, M.B., Urokinase-type plasminogen activator (uPA) and matrix metalloproteinase-9 (MMP-9) expression and activity during early embryo development in the cow. Anat. Embryol 204 (2001), 477–483.
149. Whitten, W.K., Nutrient requirements for the culture of preimplantation embryos in vitro. Adv. Biosci 6 (1971), 129–139.
150. Wong, C.C., Loewke, K.E., Bossert, N.L., Behr, B., De Jonge, C.J., Baer, T.M., Reijo Pera, R.A., Non-invasive imaging of human embryos before embryonic genome activation predicts development to the blastocyst stage. Nat. Biotechnol 28 (2010), 1115–1121.
151. Wydooghe, E., Vandaele, L., Heras, S., De Sutter, P., Deforce, D., Peelman, L., De Schauwer, C., Van Soom, A., Autocrine embryotropins revisited: how do embryos communicate with each other in vitro when cultured in groups?. Biol. Rev. Camb. Philos. Soc, 2015, 10.1111/brv.12241 Epub 26 Nov 2015.
152. Yang, H.W., Hwang, K.J., Kwon, H.C., Kim, H.S., Choi, K.W., Oh, K.S., Detection of reactive oxygen species (ROS) and apoptosis in human fragmented embryos. Hum. Reprod 13 (1998), 998–1002.
153. Yang, Z., Liu, J., Collins, G.S., Salem, S.A., Liu, X., Lyle, S.S., Peck, A.C., Sills, E.S., Salem, R.D., Selection of single blastocysts for fresh transfer via standard morphology assessment alone and with array CGH for good prognosis IVF patients: results from a randomized pilot study. Mol. Cytogenet, 5, 2012, 24.
154. Yoon, H.J., Yoon, S.H., Son, W.Y., Im, K.S., Lim, J.H., High implantation and pregnancy rates with transfer of human hatching day 6 blastocysts. Fertil. Steril 75 (2001), 832–833.
155. Yu, S., Yehia, G., Wang, J., Stypulkowski, E., Sakamori, R., Jiang, P., Hernandez-Enriquez, B., Tran, T.S., Bonder, E.M., Guo, W., Gao, N., Global ablation of the mouse Rab11a gene impairs early embryogenesis and matrix metalloproteinase secretion. J. Biol. Chem 289 (2014), 32030–32043.
156. Yuan, Y.Q., Van Soom, A., Coopman, F.O., Mintiens, K., Boerjan, M.L., Van Zeveren, A., de Kruif, A., Peelman, L.J., Influence of oxygen tension on apoptosis and hatching in bovine embryos cultured in vitro. Theriogenology 59 (2003), 1585–1596.
157. Zhang, H., Hou, L., Li, C.M., Zhang, W.Y., The chemokine CXCL6 restricts human trophoblast cell migration and invasion by suppressing MMP-2 activity in the first trimester. Hum. Reprod 28 (2013), 2350–2362.
158. Zhang, J., Wang, X., Vikash, V., Ye, Q., Wu, D., Liu, Y., Dong, W., ROS and ROS-mediated cellular signaling. Oxid. Med. Cell. Longev, 2016, 2016, 4350965.
159. Ziebe, S., Loft, A., Povlsen, B.B., Erb, K., Agerholm, I., Aasted, M., Gabrielsen, A., Hnida, C., Zobel, D.P., Munding, B., Bendz, S.H., Robertson, S.A., A randomized clinical trial to evaluate the effect of granulocyte-macrophage colony-stimulating factor (GM-CSF) in embryo culture medium for in vitro fertilization. Fertil. Steril 99 (2013), 1600–1609.