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Combination effects of epidermal growth factor and glial cell line-derived neurotrophic factor on the in vitro developmental potential of porcine oocytes

Published online by Cambridge University Press:  09 September 2015

Mehdi Vafaye Valleh ,
Mikkel Aabech Rasmussen  and
Poul Hyttel
Mehdi Vafaye Valleh*
Affiliation:
Department of Animal Science, Faculty of Agriculture, University of Zabol, P. O. Box 98615-538, Zabol, Iran.
Mikkel Aabech Rasmussen
Affiliation:
Department of Basic Animal and Veterinary Sciences, Faculty of Life Sciences, University of Copenhagen, Copenhagen, Denmark.
Poul Hyttel
Affiliation:
Department of Basic Animal and Veterinary Sciences, Faculty of Life Sciences, University of Copenhagen, Copenhagen, Denmark.
*
All correspondence to: Mehdi Vafaye Valleh. Department of Animal Science, Faculty of Agriculture, University of Zabol, P. O. Box 98615-538, Zabol, Iran. Tel: +98 9358237550. E-mail: mehdi.valleh@uoz.ac.ir, me_va84@yahoo.com
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Summary

The developmental potential of in vitro matured porcine oocytes is still lower than that of oocytes matured and fertilized in vivo. Major problems that account for the lower efficiency of in vitro production include the improper nuclear and cytoplasmic maturation of oocytes. With the aim of improving this issue, the single and combined effects of epidermal growth factor (EGF) and glial cell line-derived neurotrophic factor (GDNF) on oocyte developmental competence were investigated. Porcine cumulus–oocyte cell complexes (COCs) were matured in serum-free medium supplemented with EGF (0, 10 or 50 ng/ml) and/or GDNF (0, 10 or 50 ng/ml) for 44 h, and subsequently subjected to fertilization and cultured for 7 days in vitro. The in vitro-formed blastocysts derived from selected growth factor groups (i.e. EGF = 50 ng/ml; GDNF = 50 ng/ml; EGF = 50 ng/ml + GDNF = 50 ng/ml) were also used for mRNA expression analysis, or were subjected to Hoechst staining. The results showed that the addition of EGF and/or GDNF during oocyte maturation dose dependently enhanced oocyte developmental competence. Compared with the embryos obtained from control or single growth factor-treated oocytes, treatment with the combination of EGF and GDNF was shown to significantly improve oocyte competence in terms of blastocyst formation, blastocyst cell number and blastocyst hatching rate (P < 0.05), and also simultaneously induced the expression of BCL-xL and TERT and suppressed the expression of caspase-3 in resulting blastocysts (P < 0.05). These results suggest that both GDNF and EGF may play an important role in the regulation of porcine in vitro oocyte maturation and the combination of these growth factors could promote oocyte competency and blastocyst quality.

Keywords

Blastocyst qualityEGFGDNFIn vitro maturationPorcine
Type
Research Article
Information
Zygote , Volume 24 , Issue 3 , June 2016 , pp. 465 - 476
Copyright
Copyright © Cambridge University Press 2015 

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References

Baulida, J., Kraus, M.H., Alimandi, M., Di Fiore, P.P. & Carpenter, G. (1996). All ErbB receptors other than the epidermal growth factor receptor are endocytosis impaired. J. Biol. Chem. 271, 5251–7.CrossRefGoogle Scholar
Bodnar, A.G., Ouellette, M., Frolkis, M., Holt, S.E., Chiu, C.P., Morin, G.B., Harley, C.B., Shay, J.W., Lichtsteiner, S. & Wright, W.E. (1998). Extension of life-span by introduction of telomerase into normal human cells. Science 279, 349–52.Google Scholar
Boelhauve, M., Sinowatz, F., Wolf, E. & Paula-Lopes, F.F. (2005). Maturation of bovine oocytes in the presence of leptin improves development and reduces apoptosis of in vitro-produced blastocysts. Biol. Reprod. 73, 737–44.Google Scholar
Cauffman, G., Van de Velde, H., Liebaers, I. & Van Steirteghem, A. (2005). DAZL expression in human oocytes, preimplantation embryos and embryonic stem cells. Mol. Hum. Reprod. 11, 405–11.Google Scholar
Chen, J., Melton, C., Suh, N., Oh, J.S., Horner, K., Xie, F., Sette, C., Blelloch, R. & Conti, M. (2011). Genome-wide analysis of translation reveals a critical role for deleted in azoospermia-like (Dazl) at the oocyte-to-zygote transition. Genes Dev. 25, 755–66.Google Scholar
Clarkson, E.D., Zawada, W.M. & Freed, C.R. (1997). GDNF improves survival and reduces apoptosis in human embryonic dopaminergic neurons in vitro . Cell Tissue Res. 289, 207–10.CrossRefGoogle ScholarPubMed
Conti, M., Hsieh, M., Park, J.Y. & Su, Y.Q. (2006). Role of the epidermal growth factor network in ovarian follicles. Mol. Endocrinol. 20, 715–23.CrossRefGoogle ScholarPubMed
Coussens, M., Davy, P., Brown, L., Foster, C., Andrews, W.H., Nagata, M. & Allsopp, R. (2010). RNAi screen for telomerase reverse transcriptase transcriptional regulators identifies HIF1alpha as critical for telomerase function in murine embryonic stem cells. Proc. Natl. Acad. Sci. USA 107, 13842–7.Google Scholar
Cui, X.S. & Kim, N.H. (2003). Epidermal growth factor induces Bcl-xL gene expression and reduces apoptosis in porcine parthenotes developing in vitro . Mol. Reprod. Dev. 66, 273–8.Google Scholar
Dang-Nguyen, T.Q., Somfai, T., Haraguchi, S., Kikuchi, K., Tajima, A., Kanai, Y. & Nagai, T. (2011). In vitro production of porcine embryos: current status, future perspectives and alternative applications. Anim. Sci. J. 82, 374–82.Google Scholar
Demyda, S. & Genero, E. (2011). Developmental competence of in vivo and in vitro matured oocytes: a review. Biotech. Mol. Biol. Rev. 6, 155–165.Google Scholar
Deshmukh, R.S., Oestrup, O., Oestrup, E., Vejlsted, M., Niemann, H., Lucas-Hahn, A., Petersen, B., Li, J., Callesen, H. & Hyttel, P. (2011). DNA methylation in porcine preimplantation embryos developed in vivo and produced by in vitro fertilization, parthenogenetic activation, and somatic cell nuclear transfer. Epigenetics 6, 177–87.Google Scholar
Ding, J. & Foxcroft, G.R. (1994). Epidermal growth factor enhances oocyte maturation in pigs. Mol. Reprod. Dev. 39, 30–40.Google Scholar
Ekstrand, M.I., Falkenberg, M., Rantanen, A., Park, C.B., Gaspari, M., Hultenby, K., Rustin, P., Gustafsson, C.M. & Larsson, N.G. (2004). Mitochondrial Transcription Factor A regulates mtDNA copy number in mammals. Hum. Mol. Genet. 13, 935–44.CrossRefGoogle ScholarPubMed
Eppig, J.J. 1996. Coordination of nuclear and cytoplasmic oocyte maturation in eutherian mammals. Reprod. Fertil. Dev. 8, 485–9.Google Scholar
Esmaielzadeh, F., Hosseini, S.M., Nasiri, Z., Hajian, M., Chamani, M., Gourabi, H., Shahverdi, A.H., Vosough, A.D. & Nasr-Esfahani, M.H. (2013). Kit ligand and glial-derived neurotrophic factor as alternative supplements for activation and development of ovine preantral follicles in vitro . Mol. Reprod. Dev. 80, 35–47.Google Scholar
Exley, G.E., Tang, C., McElhinny, A.S. & Warner, C.M. (1999). Expression of caspase and BCL-2 apoptotic family members in mouse preimplantation embryos. Biol. Reprod. 61, 231–9.Google Scholar
Facucho-Oliveira, J.M. & St John, J.C. (2009). The relationship between pluripotency and mitochondrial DNA proliferation during early embryo development and embryonic stem cell differentiation. Stem Cell Rev. 5, 140–58.CrossRefGoogle ScholarPubMed
Garrels, W., Kues, W.B., Herrmann, D., Holler, S., Baulain, U. & Niemann, H. (2012). Ectopic expression of human telomerase RNA component results in increased telomerase activity and elongated telomeres in bovine blastocysts. Biol. Reprod. 87, 95.CrossRefGoogle ScholarPubMed
Green, D.R. & Kroemer, G. (2004). The pathophysiology of mitochondrial cell death. Science 305, 626–9.Google Scholar
Hardy, K. & Spanos, S. (2002). Growth factor expression and function in the human and mouse preimplantation embryo. J. Endocrinol. 172, 221–36.CrossRefGoogle ScholarPubMed
Hoffmeyer, K., Raggioli, A., Rudloff, S., Anton, R., Hierholzer, A., Del Valle, I., Hein, K., Vogt, R. & Kemler, R. (2012). Wnt/beta-catenin signaling regulates telomerase in stem cells and cancer cells. Science 336, 1549–54.CrossRefGoogle ScholarPubMed
Iqbal, K., Kues, W.A., Baulain, U., Garrels, W., Herrmann, D. & Niemann, H. (2011). Species-specific telomere length differences between blastocyst cell compartments and ectopic telomere extension in early bovine embryos by human telomerase reverse transcriptase. Biol. Reprod. 84, 723–33.Google Scholar
Jeong, Y.J., Cui, X.S., Kim, B.K., Kim, I.H., Kim, T., Chung, Y.B. & Kim, N.H. (2005). Haploidy influences Bak and Bcl-xL mRNA expression and increases incidence of apoptosis in porcine embryos. Zygote 13, 17–21.Google Scholar
Jousan, F.D., de Castro, E.P.L.A., Brad, A.M., Roth, Z. & Hansen, P.J. (2008). Relationship between group II caspase activity of bovine preimplantation embryos and capacity for hatching. J. Reprod. Dev. 54, 217–20.CrossRefGoogle ScholarPubMed
Kalmar, B. & Greensmith, L. (2009). Induction of heat shock proteins for protection against oxidative stress. Adv. Drug Deliv. Rev. 61, 310–8.Google Scholar
Kanatsu-Shinohara, M., Ogonuki, N., Inoue, K., Miki, H., Ogura, A., Toyokuni, S. & Shinohara, T. (2003). Long-term proliferation in culture and germline transmission of mouse male germline stem cells. Biol. Reprod. 69, 612–6.Google Scholar
Kanatsu-Shinohara, M., Lee, J., Inoue, K., Ogonuki, N., Miki, H., Toyokuni, S., Ikawa, M., Nakamura, T., Ogura, A. & Shinohara, T. (2008). Pluripotency of a single spermatogonial stem cell in mice. Biol. Reprod. 78, 681–7.Google Scholar
Kawamura, K., Ye, Y., Kawamura, N., Jing, L., Groenen, P., Gelpke, M.S., Rauch, R., Hsueh, A.J. & Tanaka, T. (2008). Completion of Meiosis I of preovulatory oocytes and facilitation of preimplantation embryo development by glial cell line-derived neurotrophic factor. Dev. Biol. 315, 189–202.CrossRefGoogle ScholarPubMed
Kawamura, K., Chen, Y., Shu, Y., Cheng, Y., Qiao, J., Behr, B., Pera, R.A. & Hsueh, A.J. (2012). Promotion of human early embryonic development and blastocyst outgrowth in vitro using autocrine/paracrine growth factors. PLoS One 7, e49328.CrossRefGoogle ScholarPubMed
Khalil, H., Bertrand, M.J., Vandenabeele, P. & Widmann, C. (2014). Caspase-3 and RasGAP: a stress-sensing survival/demise switch. Trends Cell. Biol. 24, 83–9.Google Scholar
Knijn, H.M., Gjorret, J.O., Vos, P.L., Hendriksen, P.J., van der Weijden, B.C., Maddox-Hyttel, P. & Dieleman, S.J. (2003). Consequences of in vivo development and subsequent culture on apoptosis, cell number, and blastocyst formation in bovine embryos. Biol. Reprod. 69, 1371–8.Google Scholar
Kuijk, E.W., du Puy, L., van Tol, H.T., Haagsman, H.P., Colenbrander, B. & Roelen, B.A. (2007). Validation of reference genes for quantitative RT-PCR studies in porcine oocytes and preimplantation embryos. BMC Dev. Biol. 7, 58.Google Scholar
Lagutina, I., Lazzari, G. & Galli, C. (2006). Effect of different pig oocyte activation protocols on embryo development in SOF and NCSU-23. Reprod. Fertil. Dev. 19, 281–282.Google Scholar
Larsson, N.G., Wang, J., Wilhelmsson, H., Oldfors, A., Rustin, P., Lewandoski, M., Barsh, G.S. & Clayton, D.A. (1998). Mitochondrial transcription factor A is necessary for mtDNA maintenance and embryogenesis in mice. Nat. Genet. 18, 231–6.Google Scholar
Lee, G.S., 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. (2005a). Effect of epidermal growth factor in preimplantation development of porcine cloned embryos. Mol. Reprod. Dev. 71, 45–51.Google Scholar
Lee, M.S., Kang, S.K., Lee, B.C. & Hwang, W.S. (2005b). The beneficial effects of insulin and metformin on in vitro developmental potential of porcine oocytes and embryos. Biol. Reprod. 73, 1264–8.Google Scholar
Leese, H.J. (2002). Quiet please, do not disturb: a hypothesis of embryo metabolism and viability. Bioessays 24, 845–9.Google Scholar
Li, M., Liang, C.G., Xiong, B., Xu, B.Z., Lin, S.L., Hou, Y., Chen, D.Y., Schatten, H. & Sun, Q.Y. (2008). PI3-kinase and mitogen-activated protein kinase in cumulus cells mediate EGF-induced meiotic resumption of porcine oocyte. Domest. Anim. Endocrinol. 34, 360–71.Google Scholar
Linher, K., Wu, D. & Li, J. (2007). Glial cell line-derived neurotrophic factor: an intraovarian factor that enhances oocyte developmental competence in vitro . Endocrinology 148, 4292–301.Google Scholar
Liu, J., Linher, K. & Li, J. (2009). Porcine DAZL messenger RNA: its expression and regulation during oocyte maturation. Mol. Cell. Endocrinol. 311, 101–8.Google Scholar
Lloyd, R.E., Romar, R., Matas, C., Gutierrez-Adan, A., Holt, W.V. & Coy, P. (2009). Effects of oviductal fluid on the development, quality, and gene expression of porcine blastocysts produced in vitro . Reproduction 137, 679–87.Google Scholar
Loo, D.T., Bradford, S., Helmrich, A. & Barnes, D.W. (1998). Bcl-2 inhibits cell death of serum-free mouse embryo cells caused by epidermal growth factor deprivation. Cell. Biol. Toxicol. 14, 375–82.CrossRefGoogle ScholarPubMed
Mao, J., Whitworth, K.M., Spate, L.D., Walters, E.M., Zhao, J. & Prather, R.S. (2012). Regulation of oocyte mitochondrial DNA copy number by follicular fluid, EGF, and neuregulin 1 during in vitro maturation affects embryo development in pigs. Theriogenology 78, 887–97.Google Scholar
Marchal, R., Feugang, J.M., Perreau, C., Venturi, E., Terqui, M. & Mermillod, P. (2001). Meiotic and developmental competence of prepubertal and adult swine oocytes. Theriogenology 56, 17–29.Google 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.Google Scholar
Metcalfe, A.D., Hunter, H.R., Bloor, D.J., Lieberman, B.A., Picton, H.M., Leese, H.J., Kimber, S.J. & Brison, D.R. (2004). Expression of 11 members of the BCL-2 family of apoptosis regulatory molecules during human preimplantation embryo development and fragmentation. Mol. Reprod. Dev. 68, 35–50.CrossRefGoogle ScholarPubMed
Park, Y.P., Choi, S.C., Cho, M.Y., Song, E.Y., Kim, J.W., Paik, S.G., Kim, Y.K., Kim, J.W. & Lee, H.G. (2006). Modulation of telomerase activity and human telomerase reverse transcriptase expression by caspases and Bcl-2 family proteins in cisplatin-induced cell death. Korean J. Lab. Med. 26, 287–93.Google ScholarPubMed
Pfaffl, M.W., Horgan, G.W. & Dempfle, L. (2002). Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 30, e36.CrossRefGoogle Scholar
Rawson, C.L., Loo, D.T., Duimstra, J.R., Hedstrom, O.R., Schmidt, E.E. & Barnes, D.W. (1991). Death of serum-free mouse embryo cells caused by epidermal growth factor deprivation. J. Cell. Biol. 113, 671–80.Google Scholar
Rho, G.J., S, B., Kim, D.S., Son, W.J., Cho, S.R., Kim, J.G., B, M.K. & Choe, S.Y. (2007). Influence of in vitro oxygen concentrations on preimplantation embryo development, gene expression and production of Hanwoo calves following embryo transfer. Mol. Reprod. Dev. 74, 486–96.Google Scholar
Richani, D., Sutton-McDowall, M.L., Frank, L.A., Gilchrist, R.B. & Thompson, J.G. (2014). Effect of epidermal growth factor-like peptides on the metabolism of in vitro- matured mouse oocytes and cumulus cells. Biol. Reprod. 90, 49.Google Scholar
Richter, K.S. (2008). The importance of growth factors for preimplantation embryo development and in-vitro culture. Curr. Opin. Obstet. Gynecol. 20, 292–304.Google Scholar
Schaetzlein, S., Lucas-Hahn, A., Lemme, E., Kues, W.A., Dorsch, M., Manns, M.P., Niemann, H. & Rudolph, K.L. (2004). Telomere length is reset during early mammalian embryogenesis. Proc. Natl. Acad. Sci. USA 101, 8034–8.Google Scholar
Singh, B., Rutledge, J.M. & Armstrong, D.T. (1995). Epidermal growth factor and its receptor gene expression and peptide localization in porcine ovarian follicles. Mol. Reprod. Dev. 40, 391–9.Google Scholar
Sun, Q.Y. & Nagai, T. (2003). Molecular mechanisms underlying pig oocyte maturation and fertilization. J. Reprod. Dev. 49, 347–59.Google Scholar
Thornberry, N.A. (1998). Caspases: key mediators of apoptosis. Chem. Biol. 5, R97–103.Google Scholar
Thornberry, N.A. & Lazebnik, Y. (1998). Caspases: enemies within. Science 281, 1312–6.CrossRefGoogle Scholar
Toms, D., Tsoi, S., Dobrinsky, J., Dyck, M.K. & Li, J. (2014). The effects of glial cell line-derived neurotrophic factor on the in vitro matured porcine oocyte transcriptome. Mol. Reprod. Dev. 81, 217–29.Google Scholar
Tsuji, T., Kiyosu, C., Akiyama, K. & Kunieda, T. (2012). CNP/NPR2 signaling maintains oocyte meiotic arrest in early antral follicles and is suppressed by EGFR-mediated signaling in preovulatory follicles. Mol. Reprod. Dev. 79, 795–802.Google Scholar
Valleh, M.V., Hyttel, P., Rasmussen, M.A. & Strøbech, L. (2014). Insulin-like growth factor 2: a modulator of anti-apoptosis related genes (HSP70, BCL2-L1) in bovine preimplantation embryos. Theriogenology 82, 942–50.CrossRefGoogle ScholarPubMed
Wang, J., Silva, J.P., Gustafsson, C.M., Rustin, P. & Larsson, N.G. (2001). Increased in vivo apoptosis in cells lacking mitochondrial DNA gene expression. Proc. Natl. Acad. Sci. USA 98, 4038–43.Google Scholar
Wang, J., Yang, J., Gu, P. & Klassen, H. (2010). Effects of glial cell line-derived neurotrophic factor on cultured murine retinal progenitor cells. Mol. Vis. 16, 2850–66.Google Scholar
Wang, Y., Kong, N., Li, N., Hao, X., Wei, K., Xiang, X., Xia, G. & Zhang, M. (2013). Epidermal growth factor receptor signaling-dependent calcium elevation in cumulus cells is required for NPR2 inhibition and meiotic resumption in mouse oocytes. Endocrinology 154, 3401–9.CrossRefGoogle ScholarPubMed
Warzych, E., Wrenzycki, C., Peippo, J. & Lechniak, D. (2007). Maturation medium supplements affect transcript level of apoptosis and cell survival related genes in bovine blastocysts produced in vitro . Mol. Reprod Dev. 74, 280–9.Google Scholar
Wei, M.C., Zong, W.X., Cheng, E.H., Lindsten, T., Panoutsakopoulou, V., Ross, A.J., Roth, K.A., MacGregor, G.R., Thompson, C.B. & Korsmeyer, S.J. (2001). Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 292, 727–30.Google Scholar
Willis, S.N., Chen, L., Dewson, G., Wei, A., Naik, E., Fletcher, J.I., Adams, J.M. & Huang, D.C. (2005). Proapoptotic Bak is sequestered by Mcl-1 and Bcl-xL, but not Bcl-2, until displaced by BH3-only proteins. Genes Dev. 19, 1294–305.Google Scholar
Yamanaka, K., Sugimura, S., Wakai, T., Kawahara, M. & Sato, E. (2009). Difference in sensitivity to culture condition between in vitro fertilized and somatic cell nuclear transfer embryos in pigs. J. Reprod. Dev. 55, 299–304.Google Scholar
Yang, C., Przyborski, S., Cooke, M.J., Zhang, X., Stewart, R., Anyfantis, G., Atkinson, S.P., Saretzki, G., Armstrong, L. & Lako, M. (2008). A key role for telomerase reverse transcriptase unit in modulating human embryonic stem cell proliferation, cell cycle dynamics, and in vitro differentiation. Stem Cells 26, 850–63.Google Scholar
Youle, R. J. & Strasser, A. (2008). The BCL-2 protein family: opposing activities that mediate cell death. Nat. Rev. Mol. Cell. Biol. 9, 47–59.Google Scholar