Oocyte and Embryo Quality: Effect of Origin, Culture Conditions and Gene Expression Patterns
P Lonergan
Department of Animal Science and Production, Conway Institute of Biomolecular and Biomedical Research, University College Dublin, Lyons Research Farm, Newcastle, County Dublin, Ireland
Search for more papers by this authorD Rizos
Department of Animal Science and Production, Conway Institute of Biomolecular and Biomedical Research, University College Dublin, Lyons Research Farm, Newcastle, County Dublin, Ireland
Search for more papers by this authorA Gutierrez-Adan
Dpto. de Reproducción Animal y Conservación de Recursos Zoogenéticos, INIA, Ctra de la Coruña Km 5.9, Madrid 28040, Spain
Search for more papers by this authorT Fair
Department of Animal Science and Production, Conway Institute of Biomolecular and Biomedical Research, University College Dublin, Lyons Research Farm, Newcastle, County Dublin, Ireland
Search for more papers by this authorMP Boland
Department of Animal Science and Production, Conway Institute of Biomolecular and Biomedical Research, University College Dublin, Lyons Research Farm, Newcastle, County Dublin, Ireland
Search for more papers by this authorP Lonergan
Department of Animal Science and Production, Conway Institute of Biomolecular and Biomedical Research, University College Dublin, Lyons Research Farm, Newcastle, County Dublin, Ireland
Search for more papers by this authorD Rizos
Department of Animal Science and Production, Conway Institute of Biomolecular and Biomedical Research, University College Dublin, Lyons Research Farm, Newcastle, County Dublin, Ireland
Search for more papers by this authorA Gutierrez-Adan
Dpto. de Reproducción Animal y Conservación de Recursos Zoogenéticos, INIA, Ctra de la Coruña Km 5.9, Madrid 28040, Spain
Search for more papers by this authorT Fair
Department of Animal Science and Production, Conway Institute of Biomolecular and Biomedical Research, University College Dublin, Lyons Research Farm, Newcastle, County Dublin, Ireland
Search for more papers by this authorMP Boland
Department of Animal Science and Production, Conway Institute of Biomolecular and Biomedical Research, University College Dublin, Lyons Research Farm, Newcastle, County Dublin, Ireland
Search for more papers by this authorContents
In general, the majority of immature bovine oocytes fail to develop to the blastocyst stage following maturation, fertilization and culture in vitro. The evidence suggests that while culture conditions during in vitro embryo production can impact on the developmental potential of the early embryo, the intrinsic quality of the oocyte is the key factor determining the proportion of oocytes developing to the blastocyst stage. In addition, evidence suggests that the period of post-fertilization embryo culture is the most critical in determining blastocyst quality. This paper reviews the current literature, with emphasis on the bovine model, demonstrating evidence for an effect of oocyte origin and/or in vitro maturation conditions on the developmental capacity and gene expression patterns in the oocyte. Furthermore, the well-documented effects of post-fertilization culture environment on embryo gene expression and quality are highlighted.
References
- Abd El Razek IM, Charpigny G, Kodja S, Marquant-Le Guienne B, Mermillod P, Guyader-Joly C, Humblot P, 2000: Differences in lipid composition between in vivo- and in vitro-produced bovine embryos. Theriogenology 53, 346 (abstract).
- Bavister BD, Boatman DE, Leibfried ML, Loose M, Vernon MW, 1983: Fertilization and cleavage of rhesus monkey oocytes in vitro. Biol Reprod 28, 983–999.
- Bertolini M, Mason JB, Beam SW, Carneiro GF, Sween ML, Kominek DJ, Moyer AL, Famula TR, Sainz RD, Anderson GB, 2002: Morphology and morphometry of in vivo- and in vitro-produced bovine concepti from early pregnancy to term and association with high birth weights. Theriogenology 58, 973–994.
- Besenfelder U, Havlicek V, Mosslacher G, Brem G, 2001: Collection of tubal stage bovine embryos by means of endoscopy: a technique report. Theriogenology 55, 837–845.
- Besenfelder U, Brem G, 1998: Tubal transfer of bovine embryos: a simple endoscopic method reducing long-term exposure of in vitro produced embryos. Theriogenology 50, 739–745.
- Blondin P, Coenan K, Guilbault LA, Sirard MA, 1997a: In vitro production of bovine embryos: developmental competence is acquired before maturation. Theriogenology 47, 1061–1075.
- Blondin P, Guibault L, Sirard MA, 1997b: The time interval between FSH-P administration and slaughter can influence the developmental competence of beef heifer oocytes. Theriogenology 48, 803–813.
- Blondin P, Bousquet D, Twagiramungu H, Barnes F, Sirard MA, 2002: Manipulation of follicular development to produce developmentally competent bovine oocytes. Biol Reprod 66, 38–43.
- Boni R, Tosti E, Roviello S, Dale B, 1999: Intracellular communication in in vivo- and in vitro-produced bovine embryos. Biol Reprod 61, 1050–1055.
- Bordignon V, Morin N, Durocher J, Bousquet D, Smith LC, 1997: GnRH improves the recovery rate and the in vitro developmental competence of oocytes obtained by transvaginal follicular aspiration from superstimulated heifers. Theriogenology 48, 291–298.
- Brevini-Gandolfi T, Lonergan P, Cillo F, Favetta LA, Fair T, Gandolfi F, 2002: Evolution of mRNA polyadenylation between oocyte maturation and first embryonic cleavage in cattle and its relation with developmental competence. Mol Reprod Dev 63, 510–517.
- Comizzoli P, Marquant-Le Guienne B, Heyman Y, Renard JP, 2000: Onset of the first S-phase is determined by a paternal effect during the G1-phase in bovine zygotes. Biol Reprod 62, 1677–1684.
- Crosier AE, Farin PW, Dykstra MJ, Alexander JE, Farin CE, 2000: Ultrastructural morphometry of bovine compact morulae produced in vivo or in vitro. Biol Reprod 62, 1459–1465.
- Crosier AE, Farin PW, Dykstra MJ, Alexander JE, Farin CE, 2001: Ultrastructural Morphometry of Bovine Blastocysts produced in vivo or in vitro. Biol Reprod 64, 1375–1385.
- Crosier AE, Farin CE, Rodriguez KF, Blondin P, Alexander JE, Farin PW, 2002: Development of skeletal muscle and expression of candidate genes in bovine fetuses from embryos produced in vivo or in vitro. Biol Reprod 67, 401–408.
- Dalbies-Tran R, Mermillod P, 2003: Use of heterologous complementary DNA screening to analyze bovine oocyte transcriptome and its evolution during in vitro maturation. Biol Reprod 68, 252–261.
- De Sousa PA, Caveney A, Westhusin ME, Watson AJ, 1998a: Temporal patterns of embryonic gene expression and their dependence on oogenetic factors. Theriogenology 49, 115–128.
-
De Sousa PA,
Westhusin ME,
Watson AJ, 1998b: Analysis of variation in relative mRNA abundance for specific gene transcripts in single bovine oocytes and early embryos.
Mol Reprod Dev
49, 119–130.
10.1002/(SICI)1098-2795(199802)49:2<119::AID-MRD3>3.0.CO;2-SCAS PubMed Web of Science® Google Scholar
- Dieleman SJ, Hendriksen PJ, Viuff D, Thomsen PD, Hyttel P, Knijn HM, Wrenzycki C, Kruip TA, Niemann H, Gadella BM, Bevers MM, Vos PL, 2002: Effects of in vivo prematuration and in vivo final maturation on developmental capacity and quality of pre-implantation embryos. Theriogenology 57, 5–20.
-
Dinnyes 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.
10.1002/(SICI)1098-2795(199907)53:3<318::AID-MRD7>3.0.CO;2-OCAS PubMed Web of Science® Google Scholar
- Doherty AS, Mann MRW, Tremblay KD, Bartolomei MS, Schultz RM, 2000: Differential effects of culture on imprinted H19 expression in the preimplantation mouse embryo. Biol Reprod 62, 1526–1535.
-
Duby RT,
Hill JL,
O'Callaghan D,
Overstrom EW,
Boland MP, 1997: Changes induced in the bovine zona pellucida by ovine and bovine oviducts.
Theriogenology
47, 332 (abstract).
10.1016/S0093-691X(97)82459-4Google Scholar
- Eckert J, Niemann H, 1998: mRNA expression of leukaemia inhibitory factor (Lif) and its receptor subunits glycoprotein 130 and Lif-receptor-beta in bovine embryos derived in vitro or in vivo. Molecular Human Reproduction 4, 957–965.
- Eid LN, Parrish JJ, 1995: Duration of G2-phase and onset of M-phase during the first cell cycle of the bovine embryo is dependent on bull in vivo fertility. Theriogenology 205, (abstract).
- Enright BP, Lonergan P, Dinnyes A, Fair T, Ward FA, Yang X, Boland MP, 2000: Culture of in vitro produced bovine zygotes in vitro vs in vivo: implications for early embryo development and quality. Theriogenology 54, 659–673.
- Fair T, Hyttel P, Greve T, 1995: Bovine oocyte diameter in relation to maturational competence and transcriptional activity. Mol Reprod Dev 42, 437–442.
- Fair T, Lonergan P, Dinnyes A, Cottell D, Hyttel P, Ward FA, Boland MP, 2001: Ultrastructure of bovine blastocysts following cryopreservation: effect of method of embryo production on blastocyst quality. Mol Reprod Dev 58, 186–195.
- Fair T, Murphy M, Martin F, Boland M, Lonergan P, 2002: Identification of differentially expressed genes in early and late cleaving bovine embryos using suppressive subtractive hybridization. Theriogenology 57, 636 (abstract).
- Fenwick J, Platteau P, Murdoch AP, Herbert M, 2002: Time from insemination to first cleavage predicts developmental competence of human preimplantation embryos in vitro. Hum Reprod 17, 407–412.
- Galli C, Lazzari G, 1996: Practical aspects of IVM/IVF in cattle. Anim Reprod Sci 42, 371–379.
- Gandolfi TA, Gandolfi F, 2001: The maternal legacy to the embryo: cytoplasmic components and their effects on early development. Theriogenology 55, 1255–1276.
- Goto T, Jones GM, Lolatgis N, Pera MF, Trounson A, 2002: Identification and characterisation of known and novel transcripts expressed during the final stages of human oocyte maturation. Mol Reprod Dev 62, 13–28.
- Greve T, Xu KP, Callesen H, Hyttel P, 1987: In vivo development of in vitro fertilized bovine oocytes matured in vivo versus in vitro. J IVF Embryo Transfer 4, 281–285.
- Grisart B, Massip A, Dessy F, 1994: Cinematographic analysis of bovne embryo development in serum-free oviduct-conditioned medium. J Reprod Fertil 101, 257–264.
- Hasler JF, Henderson WB, Hurtgen 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.
- Hendriksen PJM, Vos PLAM, Steenweg WNM, Bevers MM, Dieleman SJ, 2000: Bovine follicular development and its effect on the in vitro competence of oocytes. Theriogenology 53, 11–20.
- Holm P, Walker SK, Seamark RF, 1996: Embryo viability, duration of gestation and birth weight in sheep after transfer of in vitro matured and in vitro fertilized zygotes cultured in vitro or in vivo. J Reprod Fertil 107, 175–181.
- Holm P, Shukri NN, Vajta G, Booth P, Bendixen C, Callesen H, 1998: Developmental kinetics of the first cell cycles of bovine in vitro produced embryos in relation to their in vitro viability and sex. Theriogenology 50, 1285–1299.
- Holm P, Booth PJ, Callesen H, 2002: 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 123, 553–565.
- Holm P, Callesen H, 1998: In vivo versus in vitro produced bovine ova: similarities and differences relevant for practical application. 14th Meeting of the European Embryo Transfer Society, Venice.
- Hunter RHF, Lawson RAS, Rowson LEA, 1972: Maturation, transplantation and fertilization of ovarian oocytes in cattle. J Reprod Fertil 30, 325–328.
- Hyttel P, Callesen H, Greve T, 1986a: Ultrastructural features of preovulatory oocyte maturation in superovulated cattle. J Reprod Fertil 76, 645–656.
- Hyttel P, Xu KP, Smith S, Greve T, 1986b: Ultrastructure of in vitro oocyte maturation in cattle. J Reprod Fertil 78, 615–625.
- Hyttel P, Greve T, Callesen H, 1989: Ultrastructural aspects of oocyte maturation and fertilization in cattle. J Reprod Fert, Suppl. 38, 35–47.
- Hyttel P, Fair T, Callesen H, Greve T, 1997: Oocyte growth, capacitation and final maturation in cattle. Theriogenology 47, 23–32.
- Khurana NK, Niemann H, 2000: Energy metabolism in preimplantation bovine embryos derived in vitro or in vivo. Biol Reprod 62, 847–856.
- Knijn HM, Wrenzycki C, Hendriksen PJ, Vos PL, Herrmann D, Van Der Weijden GC, Niemann H, Dieleman SJ, 2002: Effects of oocyte maturation regimen on the relative abundance of gene transcripts in bovine blastocysts derived in vitro or in vivo. Reproduction 124, 365–75.
- Kruip TAM, den Daas JHG, 1997: In vitro produced and cloned embryos effects on pregnancy, parturition and offspring. Theriogenology 47, 43–52.
- Kubelka M, Motlik J, Schultz RM, Pavlok A, 2000: Butyrolactone I reversibly inhibits meiotic maturation of bovine oocytes without influencing chromosome condensation activity. Biol Reprod 62, 292–301.
- Kuran M, McEvoy TG, Young LE, Broadbent PJ, Robinson JJ, Sinclair KD, 2000: Ovine fetal development following different periods of in vitro culture. Theriogenology 53, 275 (abstract).
- Langendonckt AV, 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.
- Lazzari G, Wrenzycki C, Herrmann D, Duchi R, Kruip T, Niemann H, Galli C, 2002: Cellular and molecular deviations in bovine in vitro-produced embryos are related to the large offspring syndrome. Biol Reprod 67, 767–775.
- Lee K-F, Chow JFC, Xu J-S, Chan STH, Ip S-M, Yeung WSB, 2001: A comparative study of gene expression in murine embryos developed in vivo, cultured in vitro, and cocultured with human oviductal cells using messenger ribonucleic acid differential display. Biol Reprod 64, 910–917.
- van de Leemput EE, Vos PLAM, Zeinstra EC, Bevers MM, der Weijden GC, Dieleman SJ, 1999: Improved in vitro embryo development using in vivo matured oocytes from heifers superiovulated with a controlled preovulatory LH surge. Theriogenology 52, 335–349.
- Leibfried-Rutledge ML, Critser ES, Eyestone WH, Northey DL, First NL, 1987: Development potential of bovine oocytes matured in vitro or in vivo. Biol Reprod 36, 376–383.
- Lequarre A-S, Feugang J-M, Malhomme O, Donnay I, Massip A, Dessy F, Van Langendonckt A, 2001: Expression of Cu/Zn and Mn superoxide dismutases during bovine embryo development: influence of in vitro culture. Mol Reprod Dev 58, 45–53.
- Lockwood GM, Muttukrishna S, Ledger WL, 1998: Inhibins and activins in human ovulation, conception and pregnancy. Hum Reprod Update 4, 284–295.
- Lonergan P, Monaghan P, Rizos D, Boland MP, Gordon I, 1994: Effect of follicle size on bovine oocyte quality and developmental competence following maturation, fertilization, and culture in vitro. Mol Reprod Dev 37, 48–53.
- Lonergan P, Khatir H, Carolan C, Mermillod P, 1997: Bovine blastocyst production in vitro after inhibition of oocyte meiotic resumption for 24 h. J Reprod Fertil 109, 355–365.
- 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 and pregnancy rates following transfer of bovine preimplantation embryos. J Reprod Fertil 117, 159–167.
- Lonergan P, Dinnyes A, Fair T, Yang X, Boland M, 2000a: Bovine oocyte and embryo development following meiotic inhibition with butyrolactone I. Mol Reprod Dev 57, 204–209.
- Lonergan P, Gutierrez-Adan A, Pintado B, Fair T, Ward F, De La Fuente JD, Boland M, 2000b: Relationship between time of first cleavage and the expression of IGF-I growth factor, its receptor, and two housekeeping genes in bovine two- cell embryos and blastocysts produced in vitro. Mol Reprod Dev 57, 146–152.
- Lonergan P, Rizos D, Kingston M, Boland MP, 2002: Temporal sensitivity of bovine embryos to culture environment. 18th Annual Meeting of the European Embryo Transfer Association, Rolduc.
- Lonergan P, Gutierrez-Adan A, Rizos D, Pintado B, De La Fuente J, Wade M, Boland MP, 2003: Relative messenger RNA abundance in bovine oocytes collected at the LH surge and matured in vitro or their counterparts matured in vivo. Theriogenology 59, 493 (abstract).
-
McCaffrey C,
McEvoy TG,
Diskin MG,
Gwazdauskas FC,
Kane MT,
Sreenan JM, 1991: Successful co-culture of 1-4 cell cattle ova to the morula or blastocyst stage.
J Reprod Fertil
91, 119–124.
10.1530/jrf.0.0920119Google Scholar
- McEvoy TG, Sinclair KD, Broadbent PJ, Goodhand KL, Robinson JJ, 1998: Post-natal growth and development of simmental calves derived from in vivo or in vitro embryos. Reprod Fertil Dev 10, 459–464.
- McEvoy TG, Sinclair KD, Young LE, Wilmut I, Robinson JJ, 2000: Large offspring syndrome and other consequences of ruminant embryo culture in vitro: relevance to blastocyst culture in human ART. Hum Fertil 3, 238–246.
- McEvoy TG, Robinson JJ, Sinclair KD, 2001: Developmental consequences of embryo and cell manipulation in mice and farm animals. Reproduction 122, 507–518.
- McKiernan SH, Bavister BD, 1994: Timing of development is a critical parameter for predicting successful embryogenesis. Hum Reprod 9, 2123–2129.
- Marquant-Le Guienne B, Gerard M, Solari A, Thibault C, 1989: In vitro culture of bovine egg fertilized either in vivo or in vitro. Reprod Nutr Dev 29, 559–568.
- Memli E, First NL, 2000: Zygotic and embryonic gene expression in cow: a review of timing and mechanisms of early gene expression as compared with other species. Zygote 8, 87–96.
- Minami N, Sasaki K, Aizawa A, Miyamoto M, Imai H, 2001: Analysis of gene expression in mouse 2-cell embryos using fluorescein differential display: comparison of culture environments. Biol Reprod 64, 30–35.
- Myers MW, Zhang L, Stroud BK, Godke RA, 1992: Development of in vitro-matured bovine oocytes fertilized either in vitro or in vivo. Proceedings of the 12th Congress on Animal Reproduction, The Hague.
-
Negrin Pereira N,
McEvoy TG,
Staines ME,
King ME,
Broadbent PJ,
Mackie K,
Ranilla M,
Robinson JJ, 1997: Effect of exposure to two different culture systems on the development and metabolism of in vivo derived sheep zygotes.
Theriogenology
47, 377 (abstract).
10.1016/S0093-691X(97)82504-6Google Scholar
- Newcomb R, Christie WB, Rowson LEA, 1978: Birth of calves after in vivo fertilisation of oocytes removed from follicles and matured in vitro. Vet Rec 102, 461–462.
- Pavlok A, Lucas-Hahn A, Niemann H, 1992: Fertilization and developmental competence of bovine oocytes derived from different categories of antral follicles. Mol Reprod Dev 31, 63–67.
- Pincus G, Enzmann EV, 1935: The comparative behaviour of mammalian eggs in vivo and in vitro. J Exp Med 62, 665–675.
- Pinyopummintr T, Bavister BD, 1994: Development of bovine embryos in a cell-free culture medium: effects of type of serum, timing of its inclusion and heat inactivation. Theriogenology 41, 1241–1249.
- Pocar P, Brevini TA, Perazzoli F, Cillo F, Modina S, Gandolfi F, 2001: Cellular and molecular mechanisms mediating the effects of polychlorinated biphenyls on oocyte developmental competence in cattle. Mol Reprod Dev 60, 535–541.
- Pollard JW, Leibo SP, 1994: Chilling sensitivity of mammalian embryos. Theriogenology 41, 101–106.
- Rief S, Sinowatz F, Stojkovic M, Einspanier R, Wolf E, Prelle K, 2002: Effects of a novel co-culture system on development, metabolism and gene expression of bovine embryos produced in vitro. Reproduction 124, 543–56.
- Rizos D, Lonergan P, Ward F, Boland M (2001). Effect of modification of synthetic oviduct fluid (SOF) composition on yield and quality of bovine blastocysts. 17th Scientific Meeting of the European Embryo Transfer Association, Lyon.
- Rizos D, Fair T, Papadopoulos S, Boland M, Lonergan P, 2002a: Developmental, qualitative and ultrastructural differences between ovine and bovine embryos produced in vivo or in vitro. Mol Reprod Dev 62, 320–327.
- Rizos D, Lonergan P, Boland MP, Arroyo-Garcia R, Pintado B, La Fuente J, Gutierrez-Adan de A, 2002b: Analysis of differential mRNA expression between bovine blastocysts produced in different culture systems: Implications for blastocyst quality. Biol Reprod 66, 589–595.
- Rizos D, Lonergan P, Ward F, Duffy P, Boland MP, 2002c: Consequences of bovine oocyte maturation, fertilization or early embryo development in vitro versus in vivo: implications for blastocyst yield and blastocyst quality. Mol Reprod Dev 61, 234–248.
- Rizos D, Gutierrez-Adan A, Perez-Garnalo S, De La Fuente J, Boland MP, Lonergan P , 2003: Bovine embryo culture in the presence or absence of serum: Implications for blastocyst development, cryotolerance, and messenger RNA expression. Biol Reprod 68, 236–243.
- Robert C, Barnes FL, Hue I, Sirard M-A, 2000: Subtractive hybridization used to identify mRNA associated with the maturation of bovine oocytes. Mol Reprod Dev 57, 167–175.
- Robert C, Gagne D, Bousquet D, Barnes FL, Sirard MA, 2001: Differential display and suppressive subtractive hybridization used to identify granulosa cell messenger RNA associated with bovine oocyte developmental competence. Biol Reprod 64, 1812–1820.
- Robert C, Hue I, McGraw S, Gagne D, Sirard MA, 2002: Quantification of cyclin B1 and p34(cdc2) in bovine cumulus-oocyte complexes and expression mapping of genes involved in the cell cycle by complementary DNA macroarrays. Biol Reprod 67, 1456–1464.
- Sakkas D, Shoukir Y, Chardonnens D, Bianchi PG, Campana A, 1998: Early cleavage of human embryos to the two-cell stage after intracytoplasmic sperm injection as an indicator of embryo viability. Hum Reprod 13, 182–187.
- Shoukir Y, Chardonnens D, Campana A, Bischof P, Sakkas D, 1998: The rate of development and time of transfer play different roles in influencing the viability of human blastocysts. Hum Reprod 13, 676–681.
- Sinclair KD, McEvoy TG, Maxfield EK, Maltin CA, Young LE, Wilmut I, Broadbent PJ, Robinson JJ, 1999: Aberrant fetal growth and development after in vitro culture of sheep zygotes. J Reprod Fertil 116, 177–186.
- Sinclair KD, Young LE, Wilmut I, McEvoy TG, 2000: In-utero overgrowth in ruminants following embryo culture: lessons from mice and a warning to men. Hum Reprod 15(Suppl. 5), 68–86.
- Sirard MA, 2001: Resumption of meiosis: mechanism involved in meiotic progression and its relation with developmental competence. Theriogenology 55, 1241–1254.
- Slimane W, Heyman Y, Renard J-P, 2000: Assessing chromosomal abnormalities by FISH analysis in 2-cell bovine embryos derived from in vitro and in vivo fertilization. Theriogenology 53, 432 (abstract).
- Sreenan J, 1970: In vitro maturation and attempted fertilization of cattle follicular oocytes. J Agric Sci Camb 75, 393–396.
- Thompson JG, 2000: In vitro culture and embryo metabolism of cattle and sheep embryos – a decade of achievement. Anim Reprod Sci 60–61, 263–275.
- Totey SM, Daliri M, Rao KBCA, Pawshe CH, Taneja M, Chillar RS, 1996: Differential cleavage and developmental rates and their correlation with cell numbers and sex ratios in buffalo embryos generated in vitro. Theriogenology 45, 521–533.
- Trounson AO, Willadsen SM, Rowson LEA, 1977: Fertilization and development capability of bovine follicular oocytes matured in vitro and in vivo and transferred to the oviducts of rabbits and cows. J Reprod Fertil 51, 321–327.
- Van Soom A, Vlaenderen IV, Mahmoudzadeh AR, Deluyker H, de Kruif A, 1992: Compaction rate of in vitro fertilized bovine embryos related to the interval from insemination to first cleavage. Theriogenology 38, 905–919.
- Viuff D, Rickords L, Offenberg H, Hyttel P, Avery B, Greve T, Olsaker I, Williams JL, Callesen H, Thomsen PD, 1999: A high proportion of bovine blastocysts produced in vitro are mixoploid. Biol Reprod 60, 1273–1278.
- Viuff D, Greve T, Avery B, Hyttel P, Brockhoff PB, Thomsen PD, 2000: Chromosome aberrations in in vitro-produced bovine embryos at Days 2-5 post-insemination. Biol Reprod 63, 1143–1148.
- Viuff D, Hendriksen PJM, Vos PLAM, Dieleman SJ, Bibby BM, Greve T, Hyttel P, Thomsen PD, 2001: Chromosomal abnormalities and developmental kinetics in in vivo-developed cattle embryos at days 2-5 after ovulation. Biol Reprod 65, 204–208.
- van Wagtendonk-de Leeuw AM, Mullaart E, De Roos APW, Merton JS, Den Daas JHG, Kemp B, Ruígh L, 2000: Effects of different reproduction techniques: AI, MOET or IVP, on health and welfare of bovine offspring. Theriogenology 53, 575–597.
- Walker SK, Hartwich KM, Robinson JS, 2000: Long-term effects on offspring of exposure of oocytes and embryos to chemical and physical agents. Hum Reprod Update 6, 564–577.
- Ward FA, Rizos D, Corridan D, Quinn K, Boland MP, Lonergan P, 2001: Paternal influence on the time of the first embryonic cleavage post insemination and the implications for subsequent bovine embryo development in vitro and fertility in vivo. Mol Reprod Dev 60, 47–55.
- Warner CM, McElhinny AS, Wu L, Cieluch C, Ke X, Cao W, Tang C, Exley GE, 1998: Role of the Ped gene and apoptosis genes in control of preimplantation development. J Assist Reprod Genet 15, 331–337.
- Watson AJ, 1992: The cell biology of blastocyst development. Mol Reprod Dev 33, 492–504.
- Watson AJ, Sousa PD, Caveney A, Bancroft LC, Natale D, Urquhart J, Westhusin ME, 2000: Impact of bovine oocyte maturation media on oocyte transcript levels, blastocyst development, cell number, and apoptosis. Biol Reprod 62, 355–364.
- Wrenzycki C, Herrmann D, Carnwath JW, Niemann H, 1999: Alterations in the relative abundance of gene transcripts in preimplantation bovine embryos cultured in medium supplemented with either serum or PVA. Mol Reprod Dev 53, 8–18.
- Wrenzycki C, Herrmann D, Korsawe K, Hadeler K-G, Niemann H, 2000: Relative abundance of specific mRNAs in bovine embryos produced in vivo or in vitro employing two different culture systems. Theriogenology 53, 415 (abstract).
- Wrenzycki C, Herrmann D, Keskintepe L, Martins A, Jr, Sirisathien S, Brackett B, Niemann H, 2001: Effects of culture system and protein supplementation on mRNA expression in pre-implantation bovine embryos. Hum Reprod 16, 893–901.
- Wrenzycki C, De Sousa P, Overstrom EW, Duby RT, Herrman D, Watson AJ, Niemann H, O'Callaghan D, Boland MP, 2000: Effects of superovulated heifer diet type and quantity on relative mRNA abundances and pyruvate metabolism in recovered embryos. J Reprod Fertil 118, 69–78.
- Young LE, Sinclair KD, Wilmut I, 1998: Large offspring syndrome in cattle and sheep. Rev Reprod 3, 155–163.
- Zeng F, Schultz RM, 2003: Gene expression in mouse oocytes and preimplantation embryos: use of suppressive subtractive hybridization to identify oocyte- and embryo-specific genes. Biol Reprod 68, 31–39.
Citing Literature
Recommended
Details
Publication History
- 29 July 2003
- 29 July 2003
- Submitted: 12.02.2003
Article Metrics
Scite metrics
See how this article has been cited at scite.ai
scite shows how a scientific paper has been cited by providing the context of the citation, a classification describing whether it supports, mentions, or contrasts the cited claim, and a label indicating in which section the citation was made.
Explore this article's citation statements on scite.ai
Share QR Code
Generating QR code
https://onlinelibrary.wiley.com/doi/10.1046/j.1439-0531.2003.00437.x
QR code copied to clipboard!
Something went wrong while generating your QR code. Please try again in a moment. If the issue persists, refresh the page or contact support.
Export citation
Unable to load citation data. Please try again in a moment.
How to cite
Elkins, L. J., & Spiegelman, M. (2021). pyUserCalc: A revised Jupyter notebook calculator for uranium-series disequilibria in basalts. Earth and Space Science, 8, e2020EA001619. https://doi.org/10.1029/2020EA001619
Download Citation
If you have the appropriate software installed, you can download article citation data to the citation manager of your choice. Simply select your manager software from the list below and click on download.
This feature enables you to download the bibliographic information (also called citation data, header data, or metadata) for the articles on our site.
Citation manager file format
Use the dropdown list to choose how to format the bibliographic data you're harvesting. Several citation manager formats are available, including EndNote and BibTex. You can then copy the formatted citation (as displayed) or download it as file, to your device. If the RefWorks format is chosen, the 'Download' button will be replaced with an option to directly export to RefWorks