Impact of pro-oxidant agents on the morula-blastocyst transition in bovine embryos.

Animals; Blastocyst/cytology/metabolism; Cattle; Cells, Cultured; Male; Morula/cytology/metabolism; Oxidants/toxicity; Oxidative Stress/drug effects; Protein Biosynthesis/drug effects

Abstract :

[en] Exposing day 5 bovine morulae to reactive oxygen species induces a delayed degeneration of some blastocysts on day 8 post-insemination (pi) but without affecting the blastocyst rates. The aim of this study was to characterize the resisting and the degenerating population of blastocysts. The kinetics of degeneration of the embryos exposed to the two pro-oxidant agents: 2,2'-azobis (2-amidinopropane) dihydrochloride (AAPH) and buthionine sulfoximine (BSO) was evaluated using time-lapse cinematography. With both agents the first signs of degeneration appeared at day 7.5 pi but the duration of the degeneration process was shorter in presence of AAPH than BSO (4.2 vs. 12.5 hr, ANOVA, P < 0.05). The resisting blastocysts derived from morulae with a larger diameter (mean diameter: 161 vs. 154 microm, ANOVA, P < 0.05) and showed an earlier cavitation (135 vs. 142 hpi, P < 0.05) than the degenerating ones. The profile of protein neosynthesis at day 7 was not affected by the treatment. The proportion of male embryos was more important in the resisting than in the degenerating population (70 vs. 55%, chi2, P < 0.05) especially when the stress was induced by AAPH. The quality of the resisting embryos, measured by the total cell number and the rate of apoptosis, did not seem to be affected when compared to control embryos. In conclusion, resistance to oxidative stress seems related to the kinetics of development and/or the sex of the embryos. Resisting embryos apparently display a quality similar to untreated embryos.

Disciplines :

Biochemistry, biophysics & molecular biology

Author, co-author :

Feugang, Jean-Magloire

Donnay, Isabelle

Mermillod, Pascal

Marchandise, Joelle

Lequarré, Anne-Sophie ; Université de Liège - ULiège > Département de productions animales > Génomique animale

Language :

English

Title :

Impact of pro-oxidant agents on the morula-blastocyst transition in bovine embryos.

Publication date :

2005

Journal title :

Molecular Reproduction and Development

ISSN :

1040-452X

eISSN :

1098-2795

Publisher :

John Wiley & Sons, Hoboken, United States - New York

Volume :

Issue :

Pages :

339-46

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 11 May 2009

Statistics

Number of views

139 (2 by ULiège)

Number of downloads

334 (1 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

OpenAlex citations

Bibliography

Avery B, Madison V, Greve T. 1991. Sex and development in bovine in vitro fertilized embryo. Theriogenology 35:953-963.
Carolan C, Lonergan P, Van Langendonckt A, Mermillod P. 1995. Factors affecting bovine embryo development in synthetic oviduct fluid following oocyte maturation and fertilization in vitro. Theriogenology 43:1115-1128.
Carvalho RV, Del campo MR, Palasz AT, Plante Y, Mapletoft RJ. 1996. Survival rate and sex ratio of bovine IVF embryos frozen at different developmental stages on day 7. Theriogenology 45:489-498.
Crozet N, Ahmed-Ali M, Dubos MP. 1995. Developmental competence of goat oocytes from follicles of different size categories following maturation, fertilization and culture in vitro. J Reprod Fertil 103: 293-298.
De La Fuente R, Hahnel A, Basrur PK, King WA. 1999. X inactive-specific transcript (Xist) expression and X chromosome inactivation in the preattachment bovine embryo. Biol Reprod 60:769-775.
De Smedt V, Crozet N, Gall L. 1994. Morphological and functional changes accompanying the acquisition of meiotic competence in ovarian goat oocyte. J Exp Zool 269:128-139.
Dinnyès A, Lonergan P, Fair T, Boland MP, Yang X. 1999. Timing of the first cleavage post-insemination affects cryosurvival of in vitro-produced bovine blastocysts. Mol Reprod Dev 53:318-324.
Donnay I, Auquier P, Kaidi S, Carolan C, Lonergan P, Mermillod P, Massip A. 1998. Vitrification of in vitro produced bovine blastocysts: Methodological studies and developmental capacity. Anim Reprod Sci 52:93-104.
Donnay I, Feugang JM, Bernard S, Marchandise J, Pampfer S, Moens A, Dessy F. 2002. Impact of adding 5.5 mM glucose to SOF medium on the development, metabolism, and quality of in vitro produced bovine embryos from the morula to the blastocyst stage. Zygote 10:189-199.
Fair T, Hyttel P, Greve T. 1995. Bovine oocyte diameter in relation to maturational competence and transcriptional activity. Mol Reprod Dev 42:437-442.
Feugang JM, Van Langendonckt A, Sayoud H, Rees JF, Pampfer S, Moens A, Dessy F, Donnay I. 2003. Effect of prooxidant agents added at the morula/blastocyst stage on bovine embryo development, cell death, and glutathione content. Zygote 11:107-118.
Filosa S, Fico A, Paglialunga F, Balestrieri M, Crooke A, Verde P, Abrescia P, Bautista JM, Martini G. 2003. Failure to increase glucose consumption through the pentose-phosphate pathway results in the death of glucose-6 phosphate gene-deleted mouse embryonic stem cells subjected to oxidative stress. Biochem J 370:935-943.
Frei RE, Schultz GA, Church RB. 1989. Qualitative and quantitative changes in protein synthesis occur at the 8-16 cell stage of embryogenesis in the cow. J Reprod Fertil 86:637-641.
Goto Y, Noda Y, Mori T, Nakano M. 1993. Increased generation of reactive oxygen species in embryo cultured in vitro. Free Rad Biol Med 15:69-75.
Grisart B, Massip A, Collette L, Dessy F. 1995. The sex ratio of bovine embryos produced in serum-free oviduct-conditioned medium is not altered. Theriogenology 43:1097-1106.
Gutiérrez-Adan A, Behboodi E, Anderson GB, Medrano JF, Murray JD. 1996. Relationship between stade of development and sex of bovine IVM-IVF embryos cultured in vitro versus in the sheep oviduct. Theriogenology 46:515-525.
Gutiérrez-Adan A, Oter M, Martinez-Madrid B, Pintado B, De La Fuente J. 2000. Differential expression of two genes located on the X chromosome between male and female in vitro produced bovine embryos at the blastocyste stage. Mol Reprod Dev 55:146-151.
Guérin P, El Mouatassim S, Ménézo Y. 2001. Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings. Human Reprod Update 7:175-189.
Halliwell B, Gutteridge JMC. 1989. The chemistry of oxygen radicals and other derived species. In: Halliwell B, Gutteridge JMC, editors. Free radical biology and medicine. 2nd edition. Oxford: Clarenton Press, pp 22-85.
Harvey AJ, Kind KL, Thompson JG. 2002. REDOX regulation of early embryo development. Reproduction 123:479-486.
Hasler JF, Henderson WB, Hurtgens PJ, Jin ZQ, McCauley AD, Mower SA, Neely B, Shuey LS, Stokes JE, Trimmer SA. 1995. Production, freezing, and transfer of bovine IVF embryos and subsequent calving results. Theriogenology 43:141-152.
Holm P, Booth P, Schmidt MH, Greve T, Callesen H. 1999. High bovine blastocyst development in a static in vitro production system using SOFaa medium supplemented with sodium citrate and myo-inositol with or without serum-proteins. Theriogenology 52:683-700.
Johnson MH, Nasr-Esfahani MH. 1994. Radical solutions and cultural problems: Could free oxygen radicals be responsible for impaired development of preimplantation mammalian embryos in vitro? BioEssays 16:31-38.
Kaidi S, Donnay I, Lambert P, Dessy F, Massip A. 2000. Osmotic behavior of in vitro produced bovine blastocysts in cryoprotectant solutions as a potential predictive test of survival. Cryobiology 41:106-115.
Khosla S, Dean W, Reik W, Freil R. 2001. Epigenetic and experimental modifications in early mammalian development: Part II-Culture of preimplantation embryos and its long-term effects on gene expression and phenotype. Human Reprod Update 7:419-427.
Kimura K, Spate LD, Green MP, Roberts RM. 2004. Effects of oxidative stress and inhibitors of the pentose phosphate pathway on sexually dimorphic production of IFN-tau by bovine blastocysts. Mol Reprod Dev 68:88-95.
King WA, Picard L, Bousquet D, Goff AK. 1992. Sex-dependent loss of bisected bovine morulae after culture and freezing. J Reprod Fertil 96:453-459.
Kölle S, Stojkovic M, Boie G, Wolf E, Sinowatz F. 2002. Growth hormone inhibits apoptosis in in vitro produced bovine embryos. Mol Reprod Dev 61:180-186.
Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
Larson M, Kimura K, Kubisch MH, Roberts MR. 2001. Sexual dimorphism among bovine embryos in their ability to make the transition to expanded blastocyst and in the expression of the signaling molecule IFN-τ. PNAS 98:9677-9682.
Leese HJ, Donnay I, Thompson JG. 1998. Human assisted conception: A cautionary tale. Lessons from domestic animals. Hum Reprod 13:184-201.
Lequarre AS, Vigneron C, Ribaucour F, Holm P, Donnay I, Dalbiès-Tran R, Callesen H, Mermillod P. 2005. Influence of antral follicle size on oocyte characteristics and embryo development in the bovine. Theriogenology 63:841-859.
Lonergan P, Khatir H, Piumi F, Rieger D, Humblot P, Boland MP. 1999. Effect of time interval from insemination to first cleavage on the developmental characteristics, sex ratio and pregnancy rate after transfer of bovine embryos. J Reprod Fertil 117:159-167.
Massip A, Mermillod P, Dinnyes A. 1995. Morphology and biochemistry of in-vitro produced bovine embryos: Implications for their cryopreservation. Hum Reprod 10:3004-3011.
Nasr-Esfahani MH, Aitken JR, Johnson MH. 1990. Hydrogen peroxide levels in mouse oocytes and early cleavage stage embryos developed in vitro or in vivo. Development 109:501-507.
Niki E. 1990. Free radical initiators as sources of water- or lipid-soluble peroxyl radicals. Methods Enzymol 186:100-108.
Peippo J, Kurkilahti M, Bredbacka P. 2001. Developmental kinetics of in vitro produced bovine embryos: The effect of sex, glucose, and exposure to time-lapse environment. Zygote 9:105-113.
Peippo JP, Farazmand A, Kurkilahti M, Markkula M, Basrur PK, King WA. 2002. Sex-chromosome linked gene expression in in-vitro produced bovine embryos. Mol Hum Reprod 8:923-929.
Perret J, Shia Y-C, Fries R, Vassart G, Georges M. 1990. A polymorphic satellite sequence maps to the pericentric region of the bovine Y chromosome. Genomics 6:482-490.
Rieger D. 1992. Relationship between energy metabolism and development of early mammalian embryos. Theriogenology 37: 75-93.
Thompson JG, Sherman A, Allen NW, McGowan LT, Tervit HR. 1998. Total protein content and protein synthesis within pre-elongation stage bovine embryos. Mol Reprod Dev 50:139-145.
Van Langendonckt A, Donnay I, Schuurbiers N, Auquier P, Carolan C, Massip A, Dessy F. 1997. Effects of supplementation with fetal calf serum on development of bovine embryos in synthetic oviduct fluid medium. J Reprod Fertil 109:87-93.
Van Soom A, Boerjan M, Ysebaert MT, de Kruif A. 1996. Cell allocation to the inner cell mass and the trophectoderm in bovine embryos cultured in two different media. Mol Reprod Dev 45:171-182.
Van Wagtendonck-de Leeuw AM, Aerts BJG, Den Daas JHG. 1998. Abnormal offspring following in vitro production of bovine pre-implantation embryos: A field study. Theriogenology 49:883-894.
Wrenzycki C, Lucas-Hahn A, Herrmann D, Lemme E, Korsawe K, Niemann H. 2002. In vitro production and nuclear transfer affect dosage compensation of the X-linked gene transcripts G6PD, PGK, and Xist in preimplantation bovine embryos. Biol Reprod 66:127-134.
Xu KP, Yadav BR, King WA, Betteridge KJ. 1992. Sex-related differences in developmental rates of bovine embryos produced and cultured in vitro. Mol Reprod Dev 31:249-252.
Yadav BR, King WA, Betteridge KJ. 1993. Relationship between the completion of first cleavage and chromosomal complement, sex, and developmental rates of bovine embryos generated in vitro. Mol Reprod Dev 36:434-439.
Yang MY, Rajamahendran R. 2002. Expression of Bcl-2 and Bax proteins in relation to quality of bovine oocytes and embryos produced in vitro. Anim Reprod Sci 70:159-169.