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Effects of different oocyte retrieval and in vitro maturation systems on bovine embryo development and quality

Published online by Cambridge University Press:  15 January 2014

Sandra Milena Bernal ,
Julia Heinzmann ,
Doris Herrmann ,
Bernd Timmermann ,
Ulrich Baulain ,
Rudolf Großfeld ,
Mike Diederich ,
Andrea Lucas-Hahn  and
Heiner Niemann
Sandra Milena Bernal
Affiliation:
Institute of Farm Animal Genetics, Biotechnology, Friedrich-Loeffler-Institut (FLI), Mariensee, Neustadt, Germany. Facultad de Ciencias Agropecuarias, Universidad de Ciencias Aplicadas y Ambientales, Calle 222 No. 55–37, Bogotá, Colombia. Adaptation Physiology Group, Wageningen University, De Elst 1 (Building 122) 6708 WD Wageningen, The Netherlands.
Julia Heinzmann
Affiliation:
Institute of Farm Animal Genetics, Biotechnology, Friedrich-Loeffler-Institut (FLI), Mariensee, Neustadt, Germany.
Doris Herrmann
Affiliation:
Institute of Farm Animal Genetics, Biotechnology, Friedrich-Loeffler-Institut (FLI), Mariensee, Neustadt, Germany.
Bernd Timmermann
Affiliation:
Max Planck Institute for Molecular Genetics, Ihnestraße 63–73, 14195, Berlin, Germany.
Ulrich Baulain
Affiliation:
Institute of Farm Animal Genetics, Biotechnology, Friedrich-Loeffler-Institut (FLI), Mariensee, Neustadt, Germany.
Rudolf Großfeld
Affiliation:
Minitube GmbH Hauptstrasse 41, Tiefenbach, Germany.
Mike Diederich
Affiliation:
Weser-Ems-Union eG, Aussenstelle Rodenkirchen, Bullenmutterstation, Mittenfelder Weg 11, 26935 Rodenkirchen, Germany.
Andrea Lucas-Hahn
Affiliation:
Institute of Farm Animal Genetics, Biotechnology, Friedrich-Loeffler-Institut (FLI), Mariensee, Neustadt, Germany.
Heiner Niemann*
Affiliation:
Institute of Farm Animal Genetics, Biotechnology, Friedrich-Loeffler-Institut (FLI), Mariensee, Höltystraße 10, Mariensee, 31535 Neustadt, Germany. Institute of Farm Animal Genetics, Biotechnology, Friedrich-Loeffler-Institut (FLI), Mariensee, Neustadt, Germany.
*
All correspondence to: Heiner Niemann. Institute of Farm Animal Genetics, Biotechnology, Friedrich-Loeffler-Institut (FLI), Mariensee, Höltystraße 10, Mariensee, 31535 Neustadt, Germany. Tel: +49 5034871136. Fax: +49 5034871143. e-mail: heiner.niemann@fli.bund.de
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Summary

Cyclic adenosine monophosphate (cAMP) modulators have been used to avoid spontaneous oocyte maturation and concomitantly improve oocyte developmental competence. The current work evaluated the effects of the addition of cAMP modulators forskolin, 3-isobutyl-1-methylxanthine (IBMX) and cilostamide during in vitro maturation on the quality and yields of blastocysts. The following experimental groups were evaluated: (i) slicing or (ii) aspiration and maturation in tissue culture medium (TCM)199 for 24 h (TCM24slicing and TCM24aspiration, respectively), (iii) aspiration and maturation in the presence of cAMP modulators for 30 h (cAMP30aspiration) and in vivo-produced blastocysts. In vitro-matured oocytes were fertilized and presumptive zygotes were cultured in vitro to assess embryo development. Cleavage, blastocyst formation, blastocyst cell number, mRNA abundance of selected genes and global methylation profiles were evaluated. Blastocyst rate/zygotes for the TCM24aspiration protocol was improved (32.2 ± 2.1%) compared with TCM24slicing and cAMP30aspiration (23.4 ± 1.2% and 23.3 ± 2.0%, respectively, P<0.05). No statistical differences were found for blastocyst cell numbers. The mRNA expression for the EGR1 gene was down-regulated eight-fold in blastocysts that had been produced in vitro compared with their in vivo counterparts. Gene expression profiles for IGF2R, SLC2A8, COX2, DNMT3B and PCK2 did not differ among experimental groups. Bovine testis satellite I and Bos taurus alpha satellite methylation profiles from cAMP30aspiration protocol-derived blastocysts were similar to patterns that were observed in their in vivo equivalents (P > 0.05), while those from the other groups were significantly elevated. It is concluded that retrieval, collection systems and addition of cAMP modulators can affect oocyte developmental competence, which is reflected not only in blastocyst rates but also in global DNA methylation and gene expression patterns.

Keywords

cAMP modulatorsIn vitro maturationOocyte competencePreimplantation embryo
Type
Research Article
Information
Zygote , Volume 23 , Issue 3 , June 2015 , pp. 367 - 377
Copyright
Copyright © Cambridge University Press 2014 

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References

Albuz, F.K., Sasseville, M., Lane, M., Armstrong, D.T., Thompson, J.G. & Gilchrist, R.B. (2010). Simulated physiological oocyte maturation (SPOM): a novel in vitro maturation system that substantially improves embryo yield and pregnancy outcomes. Hum. Reprod. 25, 2999–3011.CrossRefGoogle ScholarPubMed
Bilodeau-Goeseels, S. (2011). Cows are not mice: the role of cyclic AMP, phosphodiesterases, and adenosine monophosphate-activated protein kinase in the maintenance of meiotic arrest in bovine oocytes. Mol. Reprod. Dev. 78, 734–43.CrossRefGoogle Scholar
Bock, C., Reither, S., Mikeska, T., Paulsen, M., Walter, J. & Lengauer, T. (2005). BiQ Analyzer: visualization and quality control for DNA methylation data from bisulfite sequencing. Bioinformatics 21, 4067–8.CrossRefGoogle ScholarPubMed
Bungartz, L. & Niemann, H. (1994). Assessment of the presence of a dominant follicle and selection of dairy cows suitable for superovulation by a single ultrasound examination. J. Reprod. Fertil. 101, 583–91.CrossRefGoogle ScholarPubMed
Cheng, J.F., Raid, L. & Hardison, R.C. (1986). Isolation and nucleotide sequence of the rabbit globin gene cluster ψξ-α1-ψα. Absence of a pair of α-globin genes evolving in concert. J. Biol. Chem. 261, 84–938.CrossRefGoogle ScholarPubMed
Diederich, M., Hansmann, T., Heinzmann, J., Barg-Kues, B., Herrmann, D., Aldag, P., Baulain, U., Reinhard, R., Kues, W., Weissgerber, C., Haaf, T. & Niemann, H. (2012). DNA methylation and mRNA expression profiles in bovine oocytes derived from prepubertal and adult donors. Reproduction 144, 319–30.CrossRefGoogle ScholarPubMed
Downs, S.M., Schroeder, A.C. & Eppig, J.J. (1986). Developmental capacity of mouse oocytes following maintenance of meiotic arrest in vitro . Gamete Res. 15, 305–16.CrossRefGoogle Scholar
Eckert, J. & Niemann, H. (1995). In vitro maturation, fertilization and culture to blastocysts of bovine oocytes in protein-free media. Theriogenology 43, 1211–25.CrossRefGoogle ScholarPubMed
El-Sayed, A., Hoelker, M., Rings, F., Salilew, D., Jennen, D., Tholen, E., Sirard, M. A., Schellander, K. & Tesfaye, D. (2006). Large-scale transcriptional analysis of bovine embryo biopsies in relation to pregnancy success after transfer to recipients. Physiol. Genomics 28, 84–96.CrossRefGoogle ScholarPubMed
Farin, P.W., Piedrahita, J.A. & Farin, C.E. (2006). Errors in development of fetuses and placentas from in vitro-produced bovine embryos. Theriogenology 65, 178–91.CrossRefGoogle ScholarPubMed
Farin, C.E., Alexander, J.E. & Farin, P.W. (2010). Expression of messenger RNAs for insulin-like growth factors and their receptors in bovine fetuses at early gestation from embryos produced in vivo or in vitro . Theriogenology 74, 1288–95.CrossRefGoogle ScholarPubMed
Goodhand, K.L., Watt, R.G., Staines, M.E., Hutchinson, J.S.M. & Broadbent, P.J. (1999). In vivo oocyte recovery and in vitro embryo production from bovine donors aspirated at different frequencies or following FSH treatment. Theriogenology 51, 951–61.CrossRefGoogle ScholarPubMed
Hashimoto, S., Minami, N., Takakura, R. & Imai, H. (2002). Bovine immature oocytes acquire developmental competence during meiotic arrest in vitro . Biol. Reprod. 66, 1696–701.CrossRefGoogle ScholarPubMed
Heinzmann, J., Hansmann, T., Herrmann, D., Wrenzycki, C., Zechner, U., Haaf, T. & Niemann, H. (2011). Epigenetic profile of developmentally important genes in bovine oocytes. Mol. Reprod. Dev. 78, 188–201.CrossRefGoogle ScholarPubMed
Holker, M., Petersen, B., Hassel, P., Kues, W.A., Lemme, E., Lucas-Hahn, A. & Niemann, H. (2005). Duration of in vitro maturation of recipient oocytes affects blastocyst development of cloned porcine embryos. Cloning Stem Cells 7, 35–44.CrossRefGoogle ScholarPubMed
Horii, T., Suetake, I., Yanagisawa, E., Morita, S., Kimura, M., Nagao, Y., Imai, H., Tajima, S. & Hatada, I. (2011). The Dnmt3b splice variant is specifically expressed in in vitro-manipulated blastocysts and their derivative ES cells. J. Reprod. Develop. 57, 579–85.CrossRefGoogle ScholarPubMed
Kang, Y.K., Koo, D.B., Park, J.S., Choi, Y.H., Chung, A.S., Lee, K.K. & Han, Y.M. (2001). Aberrant methylation of donor genome in cloned bovine embryos. Nat. Genet. 28, 173–7.CrossRefGoogle ScholarPubMed
Kang, Y.K., Lee, H.J., Shim, J.J., Yeo, S., Kim, S.H., Koo, D.B., Lee, K.K., Beyhan, Z., First, N.L. & Han, Y.M. (2005). Varied patterns of DNA methylation change between different satellite regions in bovine preimplantation development. Mol. Reprod. Dev. 71, 29–35.CrossRefGoogle ScholarPubMed
Katari, S., Turan, N., Bibikova, M., Erinle, O., Chalian, R., Foster, M., Gaughan, J.P., Coutifaris, C. & Sapienza, C. (2009). DNA methylation and gene expression differences in children conceived in vitro or in vivo. Hum. Mol. Genet. 18, 3769–78.CrossRefGoogle ScholarPubMed
Looney, C.R., Lindsey, B.R., Gonseth, C.L. & Johnson, D.L. (1994). Commercial aspects of oocyte retrieval and in-vitro fertilization (IVF) for embryo production in problem cows. Theriogenology 41, 67–72.CrossRefGoogle Scholar
Mehlmann, L.M. (2005). Stops and starts in mammalian oocytes: recent advances in understanding the regulation of meiotic arrest and oocyte maturation. Reproduction 130, 791–9.CrossRefGoogle ScholarPubMed
Moore, K., Kramer, J.M., Rodriguez-Sallaberry, C.J., Yelich, J.V. & Drost, M. (2007). Insulin-like growth factor (IGF) family genes are aberrantly expressed in bovine conceptuses produced in vitro or by nuclear transfer. Theriogenology 68, 717–27.CrossRefGoogle ScholarPubMed
Mori, M., Otoi, T. & Suzuki, T. (2002). Correlation between the cell number and diameter in bovine embryos produced in vitro . Reprod. Domest. Anim. 37, 181–4.CrossRefGoogle ScholarPubMed
Niemann, H., Carnwath, J. W., Herrmann, D., Wieczorek, G., Lemme, E., Lucas-Hahn, A. & Olek, S. (2010). DNA methylation patterns reflect epigenetic reprogramming in bovine embryos. Cell Reprogram. 12, 33–42.CrossRefGoogle ScholarPubMed
Pakrasi, P.L. & Jain, A.K. (2008). Cyclooxygenase-2-derived endogenous prostacyclin reduces apoptosis and enhances embryo viability in mouse. Prostaglandins Leukot. Essent. Fatty Acids 79, 27–33.CrossRefGoogle Scholar
Paoloni-Giacobino, A. (2007). Epigenetics in reproductive medicine. Pediatr. Res. 61, 51R–7R.CrossRefGoogle ScholarPubMed
Parrish, J.J., Susko-Parrish, J.L., Leibfried-Rutledge, M.L., Critser, E.S., Eyestone, W.H. & First, N.L. (1986). Bovine in vitro fertilization with frozen–thawed semen. Theriogenology 25, 591–600.CrossRefGoogle ScholarPubMed
Parrish, J.J., Susko-Parrish, J., Winer, M.A. & First, N.L. (1988). Capacitation of bovine sperm by heparin. Biol. Reprod. 38, 1171–1180.CrossRefGoogle ScholarPubMed
Pincus, G. & Enzmann, E. V. (1935). The comparative behavior of mammalian eggs in vivo and in vitro: I. the activation of ovarian eggs. J. Exp. Med. 62, 665–75.CrossRefGoogle ScholarPubMed
Pinto, A.B., Carayannopoulos, M.O., Hoehn, A., Dowd, L. & Moley, K.H. (2002). Glucose transporter 8 expression and translocation are critical for murine blastocyst survival. Biol. Reprod. 66, 1729–33.CrossRefGoogle ScholarPubMed
Robert, C., Gagne, D., Bousquet, D., Barnes, F.L. & Sirard, M.A. (2001). Differential display and suppressive subtractive hybridization used to identify granulosa cell messenger RNA associated with bovine oocyte developmental competence. Biol. Reprod. 64, 1812–20.CrossRefGoogle ScholarPubMed
Sawai, K., Takahashi, M., Fujii, T., Moriyasu, S., Hirayama, H., Minamihashi, A., Hashizume, T. & Onoe, S. (2011). DNA methylation status of bovine blastocyst embryos obtained from various procedures. J. Reprod. Dev. 57, 236–41.CrossRefGoogle ScholarPubMed
Smith, W.L., DeWitt, D.L. & Garavito, R.M. (2000). Cyclooxygenases: structural, cellular, and molecular biology. Ann. Rev. Biochem. 69, 145–82.CrossRefGoogle ScholarPubMed
Stroud, B. (2012). IETS 2012 Statistics and Data Retrieval Committee Report. The year 2012 worldwide statistics of embryo transfer in domestic farm animals. IETS Newsletter 30, 16–26.Google Scholar
Suteevun-Phermthai, T., Curchoe, C.L., Evans, A.C., Boland, E., Rizos, D., Fair, T., Duffy, P., Sung, L.Y., Du, F., Chaubal, S., Xu, J., Wechayant, T., Yang, X., Lonergan, P., Parnpai, R. & Tian, X.C. (2009). Allelic switching of the imprinted IGF2R gene in cloned bovine fetuses and calves. Anim. Reprod. Sci. 116, 19–27.CrossRefGoogle ScholarPubMed
Thouas, G.A., Korfiatis, N.A., French, A.J., Jones, G.M. & Trounson, A.O. (2001). Simplified technique for differential staining of inner cell mass and trophectoderm cells of mouse and bovine blastocysts. Reprod. Biomed. Online 3, 25–9.CrossRefGoogle ScholarPubMed
Tripathi, A., Kumar, K.V. & Chaube, S.K. (2010). Meiotic cell cycle arrest in mammalian oocytes. J. Cell Physiol. 223, 592–600.CrossRefGoogle ScholarPubMed
Tsafriri, A. & Pomerantz, S.H. (1986). Oocyte maturation inhibitor. Clin. Endocrinol. Metab 15, 157–70.CrossRefGoogle ScholarPubMed
Ushijima, H., Akiyama, K. & Tajima, T. (2008). Transition of cell numbers in bovine preimplantation embryos: in vivo collected and in vitro produced embryos. J. Reprod. Dev. 54, 239–43.CrossRefGoogle ScholarPubMed
Velazquez, M.A., Hadeler, K.G., Herrmann, D., Kues, W.A., Remy, B., Beckers, J.F. & Niemann, H. (2012). In vivo oocyte IGF-1 priming increases inner cell mass proliferation of in vitro-formed bovine blastocysts. Theriogenology 78, 517–27.CrossRefGoogle ScholarPubMed
Wilkins-Haug, L. (2009). Epigenetics and assisted reproduction. Curr. Opin. Obstet. Gynecol. 21, 201–6.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Wrenzycki, C., Herrmann, D., Lucas-Hahn, A., Gebert, C., Korsawe, K., Lemme, E., Carnwath, J.W. & Niemann, H. (2005a). Epigenetic reprogramming throughout preimplantation development and consequences for assisted reproductive technologies. Birth Defects Res. C Embryo. Today 75, 1–9.CrossRefGoogle ScholarPubMed
Wrenzycki, C., Herrmann, D., Lucas-Hahn, A., Korsawe, K., Lemme, E. & Niemann, H. (2005b). Messenger RNA expression patterns in bovine embryos derived from in vitro procedures and their implications for development. Reprod. Fertil. Dev. 17, 23–35.CrossRefGoogle ScholarPubMed
Wrenzycki, C., Herrmann, D. & Niemann, H. (2007). Messenger RNA in oocytes and embryos in relation to embryo viability. Theriogenology 68 Suppl 1, S77–83.CrossRefGoogle ScholarPubMed
Yamanaka, K., Kaneda, M., Inaba, Y., Saito, K., Kubota, K., Sakatani, M., Sugimura, S., Imai, K., Watanabe, S. & Takahashi, M. (2011). DNA methylation analysis on satellite I region in blastocysts obtained from somatic cell cloned cattle. Anim. Sci. J. 82, 523–30.CrossRefGoogle ScholarPubMed
Zhang, M., Su, Y.Q., Sugiura, K., Xia, G. & Eppig, J.J. (2010). Granulosa cell ligand NPPC and its receptor NPR2 maintain meiotic arrest in mouse oocytes. Science 330, 366–9.CrossRefGoogle ScholarPubMed