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The effect of temporary meiotic attenuation on the in vitro maturation outcome of bovine oocytes

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Abstract

The aim of this study was to investigate the effect of delaying maturation by extended culture of immature bovine oocytes in prematuration medium (PMC) containing single maturation inhibitor on their meiotic resumption and embryonic development. Bovine immature oocytes were cultured in M199 containing 10 μM of either inhibitor (roscovitine, cilostamide, or forskolin) for either 72 or 120 h followed by up to 48 h in maturation media supplemented with 7.5 IU follicle-stimulating hormone (FSH)/luteinizing hormone (LH). Two control groups were used. In untreated control, immature oocytes were cultured in the same medium as the experimental group without any inhibitors. In the FSH/LH control group, oocytes were cultured directly in the maturation medium supplemented with FSH/LH up to 48 h. In vitro matured oocytes were then inseminated with frozen–thawed bull sperm. Fertilization, defined as two-cell division 48 h post-insemination, and blastocyst formation were recorded. Total maturation rate for the 72-h group was 73%, 70%, 66%, and 69% for roscovitine, forskolin, cilostamide, and FSH/LH control, respectively, with no significant difference indicating that inhibitors have no negative effect on the oocyte maturation rate. The total fertilization rate for the 72-h group revealed that cilostamide (47%) and roscovitine (35%) were significantly higher than FSH/LH control (20%). The total blastocyst formation rates per inseminated oocytes revealed that among treatment groups, roscovitine (20%) had significantly higher rate than forskolin (9%). Overall, 72-h exposure period had better outcomes than 120 h in all the treated groups. In conclusion, prematuration culture of the bovine oocytes in the presence of maturation inhibitor for 72-h period at 10 μM concentration is sufficient in improving the bovine oocyte developmental competence.

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References

  • Aktas H, Wheeler MB, First NL, Leibfried-Rutledge ML (1995a) Maintenance of meiotic arrest by increasing [cAMP]i may have physiological relevance in bovine oocytes. J Reprod Fertil 105(2):237–245

    Article  CAS  PubMed  Google Scholar 

  • Aktas H, Wheeler MB, Rosenkrans CF Jr, First NL, Leibfried-Rutledge ML (1995b) Maintenance of bovine oocytes in prophase of meiosis I by high [cAMP]i. J Reprod Fertil 105(2):227–235

    Article  CAS  PubMed  Google Scholar 

  • Albuz FK, Sasseville M, Lane M, Armstrong DT, Thompson JG, Gilchrist RB (2010) Simulated physiological oocyte maturation (SPOM): a novel in vitro maturation system that substantially improves embryo yield and pregnancy outcomes. Hum Reprod 25(12):2999–3011

    Article  CAS  PubMed  Google Scholar 

  • Avery B, Hay-Schmidt A, Hyttel P, Greve T (1998) Embryo development, oocyte morphology, and kinetics of meiotic maturation in bovine oocytes exposed to 6-dimethylaminopurine prior to in vitro maturation. Mol Reprod Dev 50(3):334–344

    Article  CAS  PubMed  Google Scholar 

  • Bilodeau S, Fortier MA, Sirard MA (1993) Effect of adenylate cyclase stimulation on meiotic resumption and cyclic AMP content of zona-free and cumulus-enclosed bovine oocytes in vitro. J Reprod Fertil 97(1):5–11

    Article  CAS  PubMed  Google Scholar 

  • Brunet S, Maro B (2005) Cytoskeleton and cell cycle control during meiotic maturation of the mouse oocyte: integrating time and space. Reproduction 130(6):801–811

    Article  CAS  PubMed  Google Scholar 

  • Cekleniak NA, Combelles CM, Ganz DA, Fung J, Albertini DF, Racowsky C (2001) A novel system for in vitro maturation of human oocytes. Fertil Steril 75(6):1185–1193

    Article  CAS  PubMed  Google Scholar 

  • Choi YH, Love LB, Varner DD, Hinrichs K (2006) Blastocyst development in equine oocytes with low meiotic competence after suppression of meiosis with roscovitine prior to in vitro maturation. Zygote 14(1):1–8

    Article  CAS  PubMed  Google Scholar 

  • Colleoni S, Luciano AM, Gandolfi F (2004) Cumulus-oocyte communications in the horse: role of the breeding season and of the maturation medium. Reprod Domest Anim 39(2):70–75

    Article  CAS  PubMed  Google Scholar 

  • Combelles CM, Cekleniak NA, Racowsky C, Albertini DF (2002) Assessment of nuclear and cytoplasmic maturation in in-vitro matured human oocytes. Hum Reprod 17(4):1006–1016

    Article  CAS  PubMed  Google Scholar 

  • Coy P, Romar R, Payton RR, McCann L, Saxton AM, Edwards JL (2005a) Maintenance of meiotic arrest in bovine oocytes using the S-enantiomer of roscovitine: effects on maturation, fertilization and subsequent embryo development in vitro. Reproduction 129(1):19–26

    Article  CAS  PubMed  Google Scholar 

  • Coy P, Romar R, Ruiz S (2005b) Birth of piglets after transferring of in vitro-produced embryos pre-matured with R-roscovitine. Reproduction 129(6):747–755

    Article  CAS  PubMed  Google Scholar 

  • Donnay I, Faerge I, Grondahl C (2004) Effect of prematuration, meiosis activating sterol and enriched maturation medium on the nuclear maturation and competence to development of calf oocytes. Theriogenology 62(6):1093–1107

    Article  CAS  PubMed  Google Scholar 

  • Edwards RG (1965a) Maturation in vitro of mouse, sheep, cow, pig, rhesus monkey and human ovarian oocytes. Nature 208(5008):349–351

    Article  CAS  PubMed  Google Scholar 

  • Edwards RG (1965b) Maturation in vitro of human ovarian oocytes. Lancet 2(7419):926–929

    Article  CAS  PubMed  Google Scholar 

  • Fan HY, Sun QY (2004) Involvement of mitogen-activated protein kinase cascade during oocyte maturation and fertilization in mammals. Biol Reprod 70(3):535–547

    Article  CAS  PubMed  Google Scholar 

  • Hashimoto S, Minami N, Takakura R, Imai H (2002) Bovine immature oocytes acquire developmental competence during meiotic arrest in vitro. Biol Reprod 66(6):1696–1701

    Article  CAS  PubMed  Google Scholar 

  • Jensen JT, Schwinof KM, Zelinski-Wooten MB, Conti M, DePaolo LV, Stouffer RL (2002) Phosphodiesterase 3 inhibitors selectively block the spontaneous resumption of meiosis by macaque oocytes in vitro. Hum Reprod 17(8):2079–2084

    Article  CAS  PubMed  Google Scholar 

  • Jurema MW, Nogueira D (2006) In vitro maturation of human oocytes for assisted reproduction. Fertil Steril 86(5):1277–1291

    Article  PubMed  Google Scholar 

  • Kaedei Y, Fujiwara A, Tanhira F (2010) Effect of roscovitine pretreatment on the meiotic maturation of bovine oocytes and their subsequant development after somatic cell nuclear transfer. Anim Vet Adv 9(22):2848–2853

    Article  CAS  Google Scholar 

  • Kim JS, Cho YS, Song BS (2008) Exogenous dibutyryl cAMP affects meiotic maturation via protein kinase A activation; it stimulates further embryonic development including blastocyst quality in pigs. Theriogenology 69(3):290–301

    Article  CAS  PubMed  Google Scholar 

  • Kuyt JR, Kruip TA, de Jong-Brink M (1988) Cytochemical localization of adenylate cyclase in bovine cumulus-oocyte complexes. Exp Cell Res 174(1):139–145

    Article  CAS  PubMed  Google Scholar 

  • Laforest MF, Pouliot E, Gueguen L, Richard FJ (2005) Fundamental significance of specific phosphodiesterases in the control of spontaneous meiotic resumption in porcine oocytes. Mol Reprod Dev 70(3):361–372

    Article  CAS  PubMed  Google Scholar 

  • 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(2):355–365

    Article  CAS  PubMed  Google Scholar 

  • Mario AM, Marc-André S (2002) Effect of type 3 and type 4 phosphodiesterase inhibitors on the maintenance of bovine oocytes in meiotic arrest. Biol Reprod 66:180–184

    Article  Google Scholar 

  • Mayes MA, Sirard MA (2002) Effect of type 3 and type 4 phosphodiesterase inhibitors on the maintenance of bovine oocytes in meiotic arrest. Biol Reprod 66(1):180–184

    Article  CAS  PubMed  Google Scholar 

  • Mayes MA, Laforest MF, Guillemette C, Gilchrist RB, Richard FJ (2007) Adenosine 5′-monophosphate kinase-activated protein kinase (PRKA) activators delay meiotic resumption in porcine oocytes. Biol Reprod 76(4):589–597

    Article  CAS  PubMed  Google Scholar 

  • Mehlmann LM (2005) Stops and starts in mammalian oocytes: recent advances in understanding the regulation of meiotic arrest and oocyte maturation. Reproduction 130(6):791–799

    Article  CAS  PubMed  Google Scholar 

  • Mermillod P, Tomanek M, Marchal R, Meijer L (2000) High developmental competence of cattle oocytes maintained at the germinal vesicle stage for 24 hours in culture by specific inhibition of MPF kinase activity. Mol Reprod Dev 55(1):89–95

    Article  CAS  PubMed  Google Scholar 

  • Miller MA, Technau U, Smith KM, Steele RE (2000) Oocyte development in Hydra involves selection from competent precursor cells. Dev Biol 224(2):326–338

    Article  CAS  PubMed  Google Scholar 

  • Nogueira D, Cortvrindt R, De Matos DG, Vanhoutte L, Smitz J (2003a) Effect of phosphodiesterase type 3 inhibitor on developmental competence of immature mouse oocytes in vitro. Biol Reprod 69(6):2045–2052

    Article  CAS  PubMed  Google Scholar 

  • Nogueira D, Albano C, Adriaenssens T (2003b) Human oocytes reversibly arrested in prophase I by phosphodiesterase type 3 inhibitor in vitro. Biol Reprod 69(3):1042–1052

    Article  CAS  PubMed  Google Scholar 

  • Nogueira D, Ron-El R, Friedler S (2006) Meiotic arrest in vitro by phosphodiesterase 3-inhibitor enhances maturation capacity of human oocytes and allows subsequent embryonic development. Biol Reprod 74(1):177–184

    Article  CAS  PubMed  Google Scholar 

  • Oussaid B, Lonergan P, Khatir H (2000) Effect of GnRH antagonist-induced prolonged follicular phase on follicular atresia and oocyte developmental competence in vitro in superovulated heifers. J Reprod Fertil 118(1):137–144

    Article  CAS  PubMed  Google Scholar 

  • Richard FJ, Sirard MA (1996) Effects of follicular cells on oocyte maturation. I: effects of follicular hemisections on bovine oocyte maturation in vitro. Biol Reprod 54(1):16–21

    Article  CAS  PubMed  Google Scholar 

  • Rose-Hellekant TA, Bavister BD (1996) Roles of protein kinase A and C in spontaneous maturation and in forskolin or 3-isobutyl-1-methylxanthine maintained meiotic arrest of bovine oocytes. Mol Reprod Dev 44(2):241–249

    Article  CAS  PubMed  Google Scholar 

  • Schramm RD, Paprocki AM, VandeVoort CA (2003) Causes of developmental failure of in-vitro matured rhesus monkey oocytes: impairments in embryonic genome activation. Hum Reprod 18(4):826–833

    Article  CAS  PubMed  Google Scholar 

  • Shu YM, Zeng HT, Ren Z (2008) Effects of cilostamide and forskolin on the meiotic resumption and embryonic development of immature human oocytes. Hum Reprod 23(3):504–513

    Article  CAS  PubMed  Google Scholar 

  • Sugiura K, Naito K, Endo T, Tojo H (2006) Study of germinal vesicle requirement for the normal kinetics of maturation/M-phase-promoting factor activity during porcine oocyte maturation. Biol Reprod 74(3):593–600

    Article  CAS  PubMed  Google Scholar 

  • Teissier MP, Chable H, Paulhac S, Aubard Y (2000) Comparison of follicle steroidogenesis from normal and polycystic ovaries in women undergoing IVF: relationship between steroid concentrations, follicle size, oocyte quality and fecundability. Hum Reprod 15(12):2471–2477

    Article  CAS  PubMed  Google Scholar 

  • Thomas RE, Armstrong DT, Gilchrist RB (2004a) Bovine cumulus cell-oocyte gap junctional communication during in vitro maturation in response to manipulation of cell-specific cyclic adenosine 3′,5′-monophosophate levels. Biol Reprod 70(3):548–556

    Article  CAS  PubMed  Google Scholar 

  • Thomas RE, Thompson JG, Armstrong DT, Gilchrist RB (2004b) Effect of specific phosphodiesterase isoenzyme inhibitors during in vitro maturation of bovine oocytes on meiotic and developmental capacity. Biol Reprod 71(4):1142–1149

    Article  CAS  PubMed  Google Scholar 

  • Trounson A, Anderiesz C, Jones G (2001) Maturation of human oocytes in vitro and their developmental competence. Reproduction 121(1):51–75

    Article  CAS  PubMed  Google Scholar 

  • Tsafriri A, Chun SY, Zhang R, Hsueh AJ, Conti M (1996) Oocyte maturation involves compartmentalization and opposing changes of cAMP levels in follicular somatic and germ cells: studies using selective phosphodiesterase inhibitors. Dev Biol 178(2):393–402

    Article  CAS  PubMed  Google Scholar 

  • Zhang DX, Park WJ, Sun SC (2011) Regulation of maternal gene expression by MEK/MAPK and MPF signaling in porcine oocytes during in vitro meiotic maturation. J Reprod Dev 57(1):49–56

    Article  CAS  PubMed  Google Scholar 

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Authors’ contributions

Tarek Farghaly, MD participated in study design, execution, analysis, manuscript drafting, and critical discussion. Prof. Essam-Aldein M. Khalifa, MD participated in the study design and manuscript drafting. Prof. Sayed M. Mostafa, MD participated in the study design and manuscript drafting. Mostafa Hussien, MD participated in the study design and manuscript drafting. Mohamed A. Bedaiwy, MD participated in the study design and manuscript drafting. Ali Ahmady, PhD, HCLD participated in study design, analysis, manuscript drafting, and critical discussion.

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Authors and Affiliations

  1. University Hospitals Fertility Center, 1000 Auburn Dr, Beachwood, OH, 44122, USA

    A. Ahmady

  2. Obstetrics and Gynecology Department, Assiut University, Assiut University Street, Assiut, 71515, Egypt

    T. Farghaly, E. Khalifa, S. Mostafa & M. Hussein

  3. Department of Obstetrics and Gynaecologyology, University of British Columbia, Vancouver, BC, Canada

    M. Bedaiwy

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  1. T. Farghaly
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  2. E. Khalifa
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  3. S. Mostafa
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  4. M. Hussein
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Correspondence to A. Ahmady.

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Editor: T. Okamoto

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Farghaly, T., Khalifa, E., Mostafa, S. et al. The effect of temporary meiotic attenuation on the in vitro maturation outcome of bovine oocytes. In Vitro Cell.Dev.Biol.-Animal 51, 662–671 (2015). https://doi.org/10.1007/s11626-015-9878-y

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  • DOI: https://doi.org/10.1007/s11626-015-9878-y

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