Cell cycle duration at the time of maternal zygotic transition for in vitro produced bovine embryos: effect of oxygen tension and transcription inhibition.
[en] Early embryonic cleavages are mostly regulated by maternal components then control of development progressively depends on newly synthesized zygotic products. The timing of the first cleavages is a way to assess embryo quality. The goal of this study was to evaluate the duration of the fourth cell cycle, at the time of maternal-to-zygotic transition (MZT) in in vitro-produced bovine embryos by means of cinematographic analysis. We found that 75% of the embryos displayed a long fourth cycle (43.5 +/- 5.4 h) whereas the remaining embryos had a very short fourth cell cycle (8.9 +/- 2.9 h). Both groups did not differ in cleavage rhythm up to the eight-cell stage and timing of cavitation and blastocyst expansion was identical. However, embryos with a short fourth cell cycle had a better blastocyst rate than embryos with a long cycle (59% versus 38%, P < 0.01). Total cell number, inner cell mass (ICM):total cell ratio, and hatching rate were identical for blastocysts produced from embryos with either a long or a short fourth cell cycle. In a second experiment, we showed that increasing the oxygen tension, from 5% to 20%, decreased the percentage of embryos with a short fourth cell cycle, from 25% to 11% (P < 0.01), indicating that suboptimal culture conditions can influence the length of this cycle. Finally, we investigated whether fourth cell cycle duration could be influenced by transcription inhibition. With alpha-amanitin added at 18 h postinsemination (HPI), cleavage was reduced (66% versus 79%) and, at 70 HPI, the 9- to 16-cell rate increased (50% versus 25%) concomitantly with a 5- to 8-cell rate decrease (16% versus 47%). A similar pattern was observed when the drug was added at 6 HPI or 42 HPI but not at 0 HPI. Cinematographic analysis revealed that alpha-amanitin increased the first cell cycle duration whereas the second and third cell cycles were not affected. With the drug, one third of the embryos could develop up to the 9- to 16-cell stage and they all had a short fourth cell cycle (11.2 +/- 3.7 h) with a good synchrony of cleavage between blastomeres. These results suggest that duration of the fourth cell cycle of bovine embryo, during the MZT, is under a zygotic transcriptional control that can be affected by oxidative conditions.
Disciplines :
Biochemistry, biophysics & molecular biology
Author, co-author :
Lequarré, Anne-Sophie ; Université de Liège - ULiège > Département de productions animales > Génomique animale
Marchandise, J.
Massip, A.
Donnay, Isabelle
Language :
English
Title :
Cell cycle duration at the time of maternal zygotic transition for in vitro produced bovine embryos: effect of oxygen tension and transcription inhibition.
Publication date :
2003
Journal title :
Biology of Reproduction
ISSN :
0006-3363
eISSN :
1529-7268
Publisher :
Society for the Study of Reproduction, Madison, United States - Wisconsin
Memili E, First NL. Control of gene expression at the onset of bovine embryonic development. Biol Reprod. 1999; 61:1198-1207.
Hyttel P, Viuff D, Avery B, Laurincik J, Greve T. Transcription and cell cycle-dependent development of intranuclear bodies and granules in two-cell bovine embryos. J Reprod Fertil 1996; 108:263-270.
Viuff D, Hyttel P, Avery B, Vajta G, Greve T, Callesen H, Thomsen PD. Ribosomal ribonucleic acid is transcribed at the 4-cell stage in in vitro-produced bovine embryos. Biol Reprod 1998; 59:626-631.
King WA, Niar A, Chartrain I, Betteridge KJ, Guay P. Nucleolus organizer regions and nucleoli in preattachment bovine embryos. J Reprod Fertil 1988; 82:87-95.
Kopecny V. High-resolution autoradiographic studies of comparative nucleologenesis and genome reactivation during early embryogenesis in pig, man and cattle. Rev Reprod Nutr Dev 1989; 29:589-600.
Pavlok A, Kopecny V, Lucas-Hahn A, Niemann H. Transcriptional activity and nuclear ultrastructure of 8-cell bovine embryos developed by in vitro maturation and fertilization of oocytes from different growth categories of antral follicles. Mol Reprod Dev 1993; 35:233-243.
Memili E, Dominko T, First NL. Onset of transcription in bovine oocytes and preimplantation embryos. Mol Reprod Dev 1998; 51:36-41.
Bilodeau-Goeseels S, Panich P. Effects of oocyte quality on development and transcriptional activity in early bovine embryos. Anim Reprod Sci 2002; 71:143-155.
Frei RE, Schultz GA, Church RB. Qualitative and quantitative changes in protein synthesis occur at the 8-16-cell stage of embryogenesis in the cow. J Reprod Fertil 1989; 86:637-641.
Laurincik J, Thomsen PD, Hay-Schmidt A, Avery B, Greve T, Ochs RL, Hyttel P. Nucleolar proteins and nuclear ultrastructure in preimplantation bovine embryos produced in vitro. Biol Reprod 2000; 62: 1024-1032.
Smith LC, Meirelles FV, Bustin M, Clarke HJ. Assembly of somatic histone H1 onto chromatin during bovine early embryogenesis. J Exp Zool 1995; 273:317-326.
Barnes FL, First NL. Embryonic transcription in in vitro cultured bovine embryos. Mol Reprod Dev 1991; 29:117-123.
Plante L, Plante C, Shepherd DL, King WA. Cleavage and 3H-uridine incorporation in bovine embryos of high in vitro developmental potential. Mol Reprod Dev 1994; 39:375-383.
Memili E, First NL. Developmental changes in RNA polymerase II in bovine oocytes, early embryos, and effect of alpha-amanitin on embryo development. Mol Reprod Dev 1998; 51:381-389.
Telford NA, Watson AJ, Schultz GA. Transition from maternal to embryonic control in early mammalian development: a comparison of several species. Rev Mol Reprod Dev 1990; 26:90-100.
Johnson MH, Nasr-Esfahani MH. Radical solutions and cultural problems: could free oxygen radicals be responsible for the impaired development of preimplantation mammalian embryos in vitro? Review. Bioessays 1995; 16:31-37.
Camous S, Heyman Y, Meziou W, Menezo Y. Cleavage beyond the block stage and survival after transfer of early bovine embryos cultured with trophoblastic vesicles. J Reprod Fertil 1984; 72:479-485.
Eyestone W, First NL. Characterization of developmental arrest in early bovine embryos cultured in vitro. Theriogenology 1991; 35:613-624.
Barnes FL, Eyestone W. Early cleavage and maternal zygotic transition in bovine embryos. Theriogenology 1990; 33:141-153.
Grisart B, Massip A, Dessy F. Cinematographic analysis of bovine embryo development in serum-free oviduct-conditioned medium. J Reprod Fertil 1994; 101:257-264.
Holm P, Shukri NN, Vajta G, Booth P, Bendixen C, Callesen H. Developmental kinetics of the first cell cycles of bovine in vitro produced embryos in relation to their in vitro viability and sex. Theriogenology 1998; 50:1285-1299.
Holm P, Booth PJ, Callesen H. Kinetics of early in vitro development of bovine in vivo- and in vitro-derived zygotes produced and/or cultured in chemically defined or serum-containing media. Reproduction 2002; 123:553-565.
Schoenbeck RA, Peters M, Rickords LF, Stumpf TT, Prather RS. Characterization of deoxyribonucleic acid synthesis and the transition from maternal to embryonic control in the 4-cell embryo. Biol Reprod 1992; 47:1118-1125.
Anderson JE, Matteri RL, Abeydeera LR, Day BN, Prather RS. Cyclin B1 transcript quantitation over the maternal to zygotic transition in both in vivo- and in vitro-derived 4-cell porcine embryos. Biol Reprod 1999; 61:1460-1467.
Prather RS, Day BN. Practical considerations for the in vitro production of pig embryos. Review. Theriogenology 1998; 49:23-32.
Goddard MJ, Pratt HP. Control of events during early cleavage of the mouse embryo: an analysis of the '2-cell block.' J Embryol Exp Morphol 1983; 73:111-133.
Nasr-Esfahani MM, Johnson MH. The origin of reactive oxygen species in mouse embryos cultured in vitro. Development 1991; 113:551-560.
Goto Y, Noda Y, Mori T, Nakano M. Increased generation of reactive oxygen species in embryos cultured in vitro. Free Radic Biol Med 1993; 15:69-75.
Nasr-Esfahani MH, Aitken JR, Johnson MH. Hydrogen peroxide levels in mouse oocytes and early cleavage stage embryos developed in vitro or in vivo. Development 1990; 109:501-507.
Noda Y, Matsumoto H, Umaoka Y, Tatsumi K, Kishi J, Mori T. Involvement of superoxide radicals in the mouse two-cell block. Mol Reprod Dev 1991; 28:356-360.
Guerin P, El Mouatassim S, Menezo Y. Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings. Rev Hum Reprod Update 2001; 7:175-189.
Martindale JL, Holbrook NJ. Cellular response to oxidative stress: signaling for suicide and survival. Rev J Cell Physiol 2002; 192:1-15.
Takahashi M, Keicho K, Takahashi H, Ogawa H, Schultz RM, Okano A. Effect of oxidative stress on development and DNA damage in in-vitro cultured bovine embryos by comet assay. Theriogenology 2000; 54:137-145.
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.
Takahashi Y, Hishinuma M, Matsui M, Tanaka H, Kanagawa H. Development of in vitro matured/fertilized bovine embryos in a chemically defined medium: influence of oxygen concentration in the gas atmosphere. J Vet Med Sci 1996; 58:897-902.
Lonergan P, O'Kearney-Flynn M, Boland MP. Effect of protein supplementation and presence of an antioxidant on the development of bovine zygotes in synthetic oviduct fluid medium under high or low oxygen tension. Theriogenology 1999; 51:1565-1576.
Lim JM, Reggio BC, Godke RA, Hansel W. Development of in-vitro-derived bovine embryos cultured in 5% CO2 in air or in 5% O2, 5% CO2 and 90% N2. Hum Reprod 1999; 14:458-464.
Van Soom A, Yuan YQ, Peelman LJ, de Matos DG, 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 2002; 57:1453-1465.
Yuan YQ, Van Soom A, Coopman FO, Mintiens K, Boerjan ML, Van Zeveren A, de Kruif A, Peelman LJ. Influence of oxygen tension on apoptosis and hatching in bovine embryos cultured in vitro. Theriogenology 2003; 59:1585-1596.
Holm P, Booth P, Schmidt M, Greve T, Callesen H. 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 1999; 52:683-700.
Thouas GA, Korfiatis NA, French AJ, Jones GM, Trounson AO. Simplified technique for differential staining of inner cell mass and trophectoderm cells of mouse and bovine blastocyst. Reprod Biomed Online webpaper. 2001; 3:25-29.
Hoffert KA, Anderson GB, Wildt DE, Roth TL. Transition from maternal to embryonic control of development in IVM/IVF domestic cat embryos. Mol Reprod Dev 1997; 48:208-215.
Liu Z, Foote RH. Development of bovine embryos in KSOM with added superoxide dismutase and taurine and with five and twenty percent O 2. Biol Reprod 1995; 53:786-790.
Gardner DK, Lane MW, Lane M. EDTA stimulates cleavage stage bovine embryo development in culture but inhibits blastocyst development and differentiation. Mol Reprod Dev 2000; 57:256-261.
Nakayama T, Noda Y, Umaoka Y, Narimoto K, Mori T. Development to the four cell stage of hamster embryos fertilized in vitro. Theriogenology 1993; 39:1221-1233.
Van Soom A, Ysebaert MT, de Kruif A. Relationship between timing of development, morula morphology, and cell allocation to inner cell mass and trophectoderm in in vitro-produced bovine embryos. Mol Reprod Dev 1997; 47:47-56.
Lonergan P, Khatir H, Piumi F, Rieger D, Humblot P, Boland MP. 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 1999; 117:159-167.
Koyama H, Suzuki H, Yang X, Jiang S, Foote RH. Analysis of polarity of bovine and rabbit embryos by scanning electron microscopy. Biol Reprod 1994; 50:163-170.
Van Soom A, Boerjan M, Ysebaert MT, De Kruif A. Cell allocation to the inner cell mass and the trophectoderm in bovine embryos cultured in two different media. Mol Reprod Dev 1996; 45:171-182.
Fischer-Brown A, Monson R, Parrish J, Rutledge J. Cell allocation in bovine embryos cultured in two media under two oxygen concentrations. Zygote 2002; 10:341-348.
Yoshioka K, Suzuki C, Iwamura S. Effects of activin A and follistatin on developmental kinetics of bovine embryos: cinematographic analysis in a chemically defined medium. J Reprod Fertil 2000; 118:119-125.
Zernicka-Goetz M. Activation of embryonic genes during preimplantation rat development. Mol Reprod Dev 1994; 38:30-35.
Johnson MH, Day ML. Egg timers: how is developmental time measured in early vertebrate embryo? Bioessays 2000; 22:57-63.
Newport J, Kirschner M. A major transition in early xenopus: characterisation and timing of cellular changes at the midblastula stage. Cell 1982; 30:675-686.
Audic Y, Anderson C, Bhatty R, Hartley RS. Zygotic regulation of maternal cyclin A1 and B2 mRNAs. Mol Cell Biol 2001; 21:1662-1671.
Edgar BA, Datar SA. Zygotic degradation of two maternal Cdc25 mRNAs terminates Drosophila's early cell cycle program. Genes Dev 1996; 10:1966-1977.
Anderson JE, Matteri RL, Abeydeera LR, Day BN, Prather RS. Degradation of maternal cdc25c during the maternal to zygotic transition is dependent upon embryonic transcription. Mol Reprod Dev 2001; 60:181-188.
Nilsson I, Hoffmann I. Cell cycle regulation by the Cdc25 phosphatase family. Rev Prog Cell Cycle Res 2000; 4:107-114.
Aoki F, Choi T, Mori M, Yamashita M, Nagahama Y, Kohmoto K. A deficiency in the mechanism for p34cdc2 protein kinase activation in mouse embryos arrested at 2-cell stage. Dev Biol 1992; 154:66-72.
Haraguchi S, Naito K, Azuma S, Sato E, Nagahama Y, Yamashita M, Toyoda Y. Effects of phosphate on in vitro 2-cell block of AKR/N mouse embryos based on changes in cdc2 kinase activity and phosphorylation states. Biol Reprod 1996; 55:598-603.
Rambhatla L, Latham KE. Strain-specific progression of alpha-amanitin-treated mouse embryos beyond the two-cell stage. Mol Reprod Dev 1995; 41:16-19.
Hendriksen PJ, Vos PL, Steenweg WNM, Bevers MM, Dielemans SJ. Bovine follicular development and its effect on the in vitro competence of oocytes. Theriogenology 2000; 53:11-20.
