Hostname: page-component-76fb5796d-qxdb6 Total loading time: 0 Render date: 2024-04-26T10:49:34.961Z Has data issue: false hasContentIssue false
  • English
  • Français

Effect of growth factors on oocyte maturation and allocations of inner cell mass and trophectoderm cells of cloned bovine embryos

Published online by Cambridge University Press:  07 October 2015

Sezen Arat ,
Arzu Tas Caputcu ,
Mesut Cevik ,
Tolga Akkoc ,
Gaye Cetinkaya  and
Haydar Bagis
Sezen Arat*
Affiliation:
Namik Kemal University, Faculty of Agriculture, Department of Agricultural Biotechnology, Tekirdag, Turkey.
Arzu Tas Caputcu
Affiliation:
The Scientific and Technological Research Council of Turkey (TUBITAK), Marmara Research Center (MRC), Genetic Engineering and Biotechnology Institute, 41470, Gebze, Kocaeli, Turkey.
Mesut Cevik
Affiliation:
Ondokuz Mayis University, Faculty of Veterinary Medicine, Department of Reproduction and Artificial Insemination, 55200, Samsun, Turkey.
Tolga Akkoc
Affiliation:
The Scientific and Technological Research Council of Turkey (TUBITAK), Marmara Research Center (MRC), Genetic Engineering and Biotechnology Institute, 41470, Gebze, Kocaeli, Turkey.
Gaye Cetinkaya
Affiliation:
The Scientific and Technological Research Council of Turkey (TUBITAK), Marmara Research Center (MRC), Genetic Engineering and Biotechnology Institute, 41470, Gebze, Kocaeli, Turkey.
Haydar Bagis
Affiliation:
Adiyaman University, Faculty of Medicine, Department of Medical Genetics, Adiyaman, Turkey.
*
All correspondence to: Sezen Arat. Namik Kemal University, Faculty of Agriculture, Department of Agricultural Biotechnology, Tekirdag, Turkey. Tel: +90 282 250 22 90. Fax: +90 282 250 99 29. E-mail: sarat@nku.edu.tr
Get access Rights & Permissions [Opens in a new window]

Summary

This study was conducted to determine the additive effects of exogenous growth factors during in vitro oocyte maturation (IVM) and the sequential culture of nuclear transfer (NT) embryos. Oocyte maturation and culture of reconstructed embryos derived from bovine granulosa cells were performed in culture medium supplemented with either epidermal growth factor (EGF) alone or a combination of EGF with insulin-like growth factor-I (IGF-I). The maturation rates of oocytes matured in the presence of EGF or the EGF + IGF-I combination were significantly higher than those of oocytes matured in the presence of only fetal calf serum (FCS) (P < 0.05). The developing NT embryos showed no significant differences in fusion, cleavage or blastocyst rates among the culture groups (P > 0.05). IGF-I alone or in combination with EGF in sequential embryo culture medium significantly increased the ratio of inner cell mass (ICM) to total blastocyst cells (P < 0.05). Our results showed that the addition of growth factors to IVM and sequential culture media of cloned bovine embryos increased the ICM without changing the total cell number. These unknown and uncontrolled effects of growth factors can alter the allocation of ICM and trophectoderm cells (TE) in NT embryos. A decrease in TE cell numbers could be a reason for developmental abnormalities in embryos in the cloning system.

Keywords

BovineCell allocationCloningEmbryo cultureGrowth factors
Type
Research Article
Information
Zygote , Volume 24 , Issue 4 , August 2016 , pp. 554 - 562
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ahumada, C.J., Salvador, I., Cebrian-Serrano, A., Lopera, R. & Silvestre, M.A. (2013). Effect of supplementation of different growth factors in embryo culture medium with a small number of bovine embryos on in vitro embryo development and quality. Animal 7, 455–62.CrossRefGoogle ScholarPubMed
Arat, S., Rzucidlo, S.J., Gibbons, J., Miyoshi, K. & Stice, S.L. (2001). Production of transgenic bovine embryos by transfer of transfected granulosa cells into enucleated oocytes. Mol. Reprod. Dev. 60, 20–6.Google Scholar
Arat, S., Gibbons, J., Rzucidlo, S. J., Respess, D. S., Tumlin, M. & Stice, S. L. (2002). In vitro development of bovine nuclear transfer embryos from clonal lines of transgenic adult and fetal fibroblast cells of the same genotype. Biol. Reprod. 66, 1768–74.CrossRefGoogle ScholarPubMed
Arat, S., Tas, A., Bagis, H., Sagirkaya, H., Nak, Y., Nak, D., Akkoc, T. & Cetinkaya, G. (2009). Cloning of Anatolian Grey bull. Reprod. Fertil. Dev. 21, 126–7.CrossRefGoogle Scholar
Arat, S., Caputcu, A., Akkoc, T., Pabuccuoglu, S., Sagirkaya, H., Cirit, U., Nak, Y., Koban, E., Bagis, H., Demir, K., Nak, D., Senunver, A., Kilicaslan, R., Tuna, B., Cetinkaya, G., Denizci, M. & Aslan, O. (2011). Using cell banks as a tool in conservation programs of native domestic breeds: the production of the first cloned Anatolian Grey cattle. Reprod. Fertil. Dev. 23, 1012–23.CrossRefGoogle Scholar
Block, J., Wrenzycki, C., Niemann, H., Herrmann, D. & Hansen, P.J. (2008). Effects of insulin-like growth factor-1 on cellular and molecular characteristics of bovine blastocysts produced in vitro . Mol. Reprod. Dev. 75, 895–903.CrossRefGoogle ScholarPubMed
Cevik, M., Tas, A., Akkoc, T., Bagis, H. & Arat, S. (2009). A comparative study of parthenogenetic activation and in vitro fertilization of in vitro matured bovine oocytes. Turk. J. Vet. Anim. Sci. 33, 393–9.Google Scholar
Choi, Y.H., Lee, B.C., Lim, J.M., Kang, S.K. & Hwang, W.S. (2002). Optimization of culture medium for cloned bovine embryos and its influence on pregnancy and delivery outcome. Theriogenology 58, 1187–97.Google Scholar
Cibelli, J. B., Stice, S. L., Golueke, P. J., Kane, J. J., Jerry, J., Blackwell, C., Ponce de Leon, F. A. & Robl, J.M. (1998). Cloned transgenic calves from nonquiescent fetal fibroblasts. Science 280, 1256–8.Google Scholar
Cooke, S., Quinn, P., Kime, L., Ayres, C., Tyler, J.P. & Driscoll, G. L. (2002). Improvement in early human embryo development using new formulation sequential stage-specific culture media. Fertil. Steril. 78, 254–60.Google Scholar
Dadi, T.D., Li, M-W. & Lloyd, K.C.K. (2007). EGF and TGF-α supplementation enhances development of cloned mouse embryos. Cloning Stem Cells 9, 315–26.CrossRefGoogle ScholarPubMed
De la Fuente, R. & Allan King, W. (1997). Use of a chemically defined system for the direct comparison of inner cell mass and trophectoderm distribution in murine, porcine and bovine embryos. Zygote 5, 309–20.Google Scholar
Herrler, A., Lucas-Hahn, A. & Niemann, H. (1992). Effects of insulin-like growth factor-I on in vitro production of bovine embryos. Theriogenology 37, 1213–24.Google Scholar
Iwasaki, S., Yoshiba, N., Ushijima, H., Watanabe, S. & Nakahara, T. (1990). Morphology and proportion of inner cell mass of bovine blastocysts fertilized in vitro and in vivo . J. Reprod. Fertil. 90, 279–84.CrossRefGoogle ScholarPubMed
Koo, D-B., Kang, Y-K., Choi, Y-H., Park, J.S., Kim, H-N., Oh, K.B., Son, D-S., Park, H., Lee, K-K. & Han, Y-M. (2002). Aberrant allocations of inner cell mass and trophectoderm cells in bovine nuclear transfer blastocysts. Biol. Reprod. 67, 487–92.Google Scholar
Lee, G.C., Kim, H.S., Hyun, S.H., Jeon, H.Y., Nam, D.H., Jeong, Y.W., Kim, S., Kim, J.H., Kang, S.K., Lee, B.C., Hwang, W.S. (2005). Effect of epidermal growth factor in preimplantation development of porcine cloned embryos. Mol. Reprod. Dev. 71, 45–51.Google Scholar
Lonergan, P., Carolan, C., Van Langendonckt, A., Donnay, I., Khatir, H. & Mermillod, M. (1996). Role of epidermal growth factor in bovine oocyte maturation and preimplantation embryo development in vitro . Biol. Reprod. 54, 1420–9.Google Scholar
Lott, WM., Anchamparuthy, , McGilliard, V.M., Mullarky, M.L., Gwazdauskas, I.K., , FC. (2011). Influence of cysteine in conjunction with growth factors on the development of in vitro-produced bovine embryos. Reprod. Domest. Anim. 46, 585–94.CrossRefGoogle ScholarPubMed
Makarevich, A.V. & Markkula, M. (2002). Apoptosis and cell proliferation potential of bovine embryos stimulated with insulin-like growth factor I during in vitro maturation and culture. Biol. Reprod. 66, 386–92.Google Scholar
Mohan, M., Malayer, J., Geisert, R. & Morgan, G. (1999). Detection of transcripts for retinoic acid receptors., retinol-binding protein and epidermal growth factor receptor in bovine preimplantation embryos. Biol. Reprod. 60 (Supp1), 192–3.Google Scholar
Moreira, F., Paula-Lopes, F.F., Hansen, P.J., Badinga, L. & Thatcher, W.W. (2002). Effects of growth hormone and insulin-like growth factor-I on development of in vitro derived bovine embryos. Theriogenology 57, 895–907.Google Scholar
Palma, G.A., Müller, M. & Brem, G. (1997). Effect of insulin-like growth factor I (IGF-I) at high concentrations on blastocyst development of bovine embryos produced in vitro . J. Reprod. Fertil. 110, 347–53.Google Scholar
Quetglas, M.D., Coelho, L.A., Garcia, J.M., Oliveira, F.E.B. & Esper, C.R. (2001). Effect of insulin-like growth factor-I during in vitro oocyte maturation and in vitro culture of bovine embryos. Arq. Bras. Med. Vet. Zootec. 53, 1–5.Google Scholar
Rieger, D., Luciano, A. M., Modina, S., Pocar, P., Lauria, A. & Gandolfi, F. (1998). The effect of epidermal growth factor and insulin-like growth factor I on the metabolic activity, nuclear maturation and subsequent development of cattle oocytes in vitro . J. Reprod. Fertil. 112, 123–30.Google Scholar
Sakagami, N., Umeki, H., Nishino, O., Uchiyama, H., Ichikawa, K., Takeshita, K., Kaneko, E., Akiyama, K., Kobayashi, S. & Tamada, H. (2012). Normal calves produced after transfer of embryos cultured in a chemically defined medium supplemented with epidermal growth factor and insulin-like growth factor-I following ovum pick-up and in vitro fertilization in Japanese Black cows. J. Reprod. Dev. 58, 140–6.Google Scholar
SAS (2007). Statistical Software Program. SAS User Guide, Ver. 9.01, SAS Campus Drive, Cary NC 27513, USA.Google Scholar
Sharma, G.T., Dubey, PK., Nath, A. & Saikumar, G. (2013). Co-culture of buffalo (Bubalus bubalis) preantral follicles with antral follicles: a comparative study of developmental competence of oocytes derived from in vivo developed and in vitro cultured antral follicles. Zygote, 21, 286–94.CrossRefGoogle ScholarPubMed
Sirisathien, S., Hernandez-Fonseca, H.J. & Brackett, B.G. (2003). Influences of epidermal growth and insulin-like growth factor-I on bovine blastocyst development in vitro . Anim. Reprod. Sci. 77, 21–32.Google Scholar
Stefanello, J.R., Barreta, M.H., Porciuncula, P.M., Arruda, J.N., Oliveira, J.F., Oliveira, M.A. & Gonçalves, P.B. (2006). Effect of angiotensin II with follicle cells and insuline-like growth factor-I or insulin on bovine oocyte maturation and embryo development. Theriogenology 66, 2068–76.CrossRefGoogle ScholarPubMed
Stojkovic, M., Büttner, M., Zakhartchenko, V., Brem, G. & Wolf, E. (1998). A reliable procedure for differential staining of in vitro produced bovine blastocysts: comparison of tissue culture medium 199 and Menezo's B2 medium. Anim. Reprod. Sci. 50, 1–9.CrossRefGoogle ScholarPubMed
Van de Velde, A., Liu, L., Bols, P.E., Ysebaert, M.T. & Yang, X. (1999). Cell allocation and chromosomal complement of parthenogenetic and IVF bovine embryos. Mol. Reprod. Dev. 54, 57–62.Google Scholar
Van Soom, A., Boerjan, M., Ysebaert, M-T. & 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, 171–82.Google Scholar
Van Soom, A., Boerjan, M.L., Bols, P.E.J., Vanroose, G., Lein, A., Coryn, M. & Kruif, A.D. (1997). Timing of compaction and inner cell allocation in bovine embryos produced in vivo after super ovulation. Biol. Reprod. 57, 1041–9.CrossRefGoogle Scholar
Wadhwa, N., Kunj, N., Tiwari, S., Saraiya, M. & Majumdar, S.S. (2009). Optimization of embryo culture conditions for increasing efficiency of cloning in buffalo (Bubalus bubalis) and generation of transgenic embryos via cloning. Cloning Stem Cells 11, 387–95.CrossRefGoogle ScholarPubMed
Wang, Y.S., Tang, S., An, Z.X., Li, W.Z., Liu, J., Quan, F.S., Hua, S. & Zhang, Y. (2011). Effect of mSOF and G1.1/G2.2 media on the developmental competence of SCNT-derived bovine embryos. Reprod. Dom. Anim. 46, 404–9.CrossRefGoogle ScholarPubMed
Wang, L-J., Xiong, X-R., Zhang, H., Li, Y-Y., Li, Q., Wang, Y-S., Xu, W-B., Hua, S. & Zhang, Y. (2012). Defined media optimization for in vitro culture of bovine somatic cell nuclear transfer (SCNT) embryos. Theriogenology 78, 2110–9.CrossRefGoogle ScholarPubMed
Wasielak, M. & Bogacki, M. (2007). Apoptosis inhibition by insulin-like growth factor (IGF)-I during in vitro maturation of bovine oocytes. J. Reprod. Dev. 53, 419–26.CrossRefGoogle ScholarPubMed
Yoshida, Y., Miyamura, M., Hamano, S. & Yoshida, M. (1998). Expression of growth factor ligand and their receptor mRNAs in bovine ova during in vitro maturation and after fertilization in vitro . J. Vet. Med. Sci. 60, 549–54.CrossRefGoogle ScholarPubMed