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Optimal doses of EGF and GDNF act as biological response modifiers to improve porcine oocyte maturation and quality

Published online by Cambridge University Press:  11 July 2017

Mehdi Vafaye Valleh ,
Nahid Karimi Zandi ,
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
Nahid Karimi Zandi
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 93 58237550. Fax: + 98 54 31232101. E-mail: [email protected] or [email protected]
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Summary

It is well documented that both epidermal growth factor (EGF) and glial cell line-derived neurotrophic factor (GDNF) are critical for porcine oocyte maturation, however, little information is known about their mechanism of action in vitro. To gain insight into the mechanisms of action of the optimum doses of EGF and GDNF on porcine oocyte maturation, porcine cumulus–oocyte complexes (COCs) were matured in defined porcine oocyte medium supplemented with EGF, GDNF or a combination of both at varying concentrations (0–100 ng/ml) for 44 h. Nuclear and cytoplasmic maturation were determined in terms of nuclear stage after DNA staining with Hoechst and cortical granule distribution after lectin labeling, respectively. Mature oocytes were subsequently collected for gene expression analysis or subjected to in vitro fertilization and cultured for 7 days. The results showed that EGF and/or GDNF, when administered in a certain dose (50 ng/μl) to the maturation medium, not only effectively improved the synchronization of nuclear and cytoplasmic maturation processes within the oocyte, but enhanced expression of their corresponding receptors in mature oocytes (P < 0.05). Moreover, supplementation with an optimal combination of EGF + GDNF resulted in elevation of TFAM transcripts as well as a decrease of caspase-3 transcripts compared with the other studied groups (P < 0.05). Collectively, our results indicate that treatment of porcine oocytes with specific-dose combinations of EGF and GDNF stimulates oocyte quality and competence by transcriptional modulation of genes involved in oocyte survival and competence.

Keywords

Cortical granulesEGFGDNFOocyte maturationPorcine
Type
Research Article
Information
Zygote , Volume 25 , Issue 4 , August 2017 , pp. 423 - 433
Copyright
Copyright © Cambridge University Press 2017 

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References

Abeydeera, L.R. (2002). In vitro production of embryos in swine. Theriogenology 57, 256–73.CrossRefGoogle ScholarPubMed
Barbieri, E., Di Fiore, P.P. & Sigismund, S. (2016). Endocytic control of signaling at the plasma membrane. Curr. Opin. Cell Biol. 39, 21–7.CrossRefGoogle ScholarPubMed
Boku, S., Nakagawa, S., Takamura, N., Kato, A., Takebayashi, M., Hisaoka-Nakashima, K., Omiya, Y., Inoue, T. & Kusumi, I. (2013). GDNF facilitates differentiation of the adult dentate gyrus-derived neural precursor cells into astrocytes via STAT3. Biochem. Biophys. Res. Commun. 434, 779–84.CrossRefGoogle ScholarPubMed
Cao, X., Zhu, H., Ali-Osman, F. & Lo, H.W. (2011). EGFR and EGFRvIII undergo stress- and EGFR kinase inhibitor-induced mitochondrial translocalization: a potential mechanism of EGFR-driven antagonism of apoptosis. Mol. Cancer 10, 26.CrossRefGoogle ScholarPubMed
Chappel, S. (2013). The role of mitochondria from mature oocyte to viable blastocyst. Obstet. Gynecol. Int. 2013, 183024.CrossRefGoogle ScholarPubMed
Chen, H., Wang, W., Mo, Y., Ma, Y., Ouyang, N., Li, R., Mai, M., He, Y., Bodombossou-Djobo, M.M. & Yang, D. (2011a). Women with high telomerase activity in luteinised granulosa cells have a higher pregnancy rate during in vitro fertilisation treatment. J. Assist. Reprod. Genet. 28, 797–807.CrossRefGoogle ScholarPubMed
Chen, J., Melton, C., Suh, N., Oh, J.S., Horner, K., Xie, F., Sette, C., Blelloch, R. & Conti, M. (2011b). 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.CrossRefGoogle ScholarPubMed
Chen, J., Torcia, S., Xie, F., Lin, C.J., Cakmak, H., Franciosi, F., Horner, K., Onodera, C., Song, J.S., Cedars, M.I., Ramalho-Santos, M. & Conti, M. (2013). Somatic cells regulate maternal mRNA translation and developmental competence of mouse oocytes. Nature Cell Biol. 15, 1415–23.CrossRefGoogle ScholarPubMed
Cosme-Blanco, W., Shen, M.F., Lazar, A.J., Pathak, S., Lozano, G., Multani, A.S. & Chang, S. (2007). Telomere dysfunction suppresses spontaneous tumorigenesis in vivo by initiating p53-dependent cellular senescence. EMBO Rep. 8, 497–503.CrossRefGoogle ScholarPubMed
Czabotar, P.E., Lessene, G., Strasser, A. & Adams, J.M. (2014). Control of apoptosis by the BCL-2 protein family: implications for physiology and therapy. Nat. Rev. Mol. Cell. Biol. 15, 49–63.CrossRefGoogle ScholarPubMed
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. [Nihon chikusan Gakkaiho], 82, 374–82.Google ScholarPubMed
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
Esseghir, S., Todd, S.K., Hunt, T., Poulsom, R., Plaza-Menacho, I., Reis-Filho, J.S. & Isacke, C.M. (2007). A role for glial cell derived neurotrophic factor induced expression by inflammatory cytokines and RET/GFR alpha 1 receptor up-regulation in breast cancer. Cancer Res. 67, 11732–41.CrossRefGoogle ScholarPubMed
Fragouli, E. & Wells, D. (2015). Mitochondrial DNA assessment to determine oocyte and embryo viability. Semin. Reprod. Med. 33, 401–9.Google ScholarPubMed
Fujihara, M., Comizzoli, P., Keefer, C.L., Wildt, D.E. & Songsasen, N. (2014). Epidermal growth factor (EGF). sustains in vitro primordial follicle viability by enhancing stromal cell proliferation via MAPK and PI3K pathways in the prepubertal, but not adult, cat ovary. Biol. Reprod. 90, 86.CrossRefGoogle Scholar
Funahashi, H. (2003). Polyspermic penetration in porcine IVM-IVF systems. Reprod. Fertil. Dev. 15, 167–77.CrossRefGoogle ScholarPubMed
Ge, H., Tollner, T.L., Hu, Z., Dai, M., Li, X., Guan, H., Shan, D., Zhang, X., Lv, J., Huang, C. & Dong, Q. (2012). The importance of mitochondrial metabolic activity and mitochondrial DNA replication during oocyte maturation in vitro on oocyte quality and subsequent embryo developmental competence. Mol. Reprod. Dev. 79, 392–401.CrossRefGoogle ScholarPubMed
Henson, E.S. & Gibson, S.B. (2006). Surviving cell death through epidermal growth factor (EGF) signal transduction pathways: implications for cancer therapy. Cell. Signal. 18, 2089–97.CrossRefGoogle ScholarPubMed
Hsu, C.J., Holmes, S.D. & Hammond, J.M. (1987). Ovarian epidermal growth factor-like activity. Concentrations in porcine follicular fluid during follicular enlargement. Biochem. Biophys. Res. Commun. 147, 242–7.CrossRefGoogle ScholarPubMed
Iqbal, K., Kues, WA., 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.CrossRefGoogle ScholarPubMed
Jin, Y. X., Lee, J.Y., Choi, S.H., Kim, T., Cui, X.S. & Kim, N.H. (2007). Heat shock induces apoptosis related gene expression and apoptosis in porcine parthenotes developing in vitro . Anim. Reprod. Sci. 100, 118–27.CrossRefGoogle ScholarPubMed
Jones, G.M., Cram, D.S., Song, B., Magli, M.C., Gianaroli, L., Lacham-Kaplan, O., Findlay, J.K., Jenkin, G. & Trounson, A.O. (2008). Gene expression profiling of human oocytes following in vivo or in vitro maturation. Hum. Reprod. 23, 1138–44.CrossRefGoogle ScholarPubMed
Kalmbach, K.H., Fontes Antunes, D.M., Dracxler, R.C., Knier, T.W., Seth-Smith, M.L., Wang, F., Liu, L. & Keefe, D.L. (2013). Telomeres and human reproduction. Fertil. Steril. 99, 23–9.CrossRefGoogle ScholarPubMed
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
Keefe, D., Kumar, M. & Kalmbach, K. (2015). Oocyte competency is the key to embryo potential. Fertil. Steril. 103, 317–22.CrossRefGoogle ScholarPubMed
Keefe, D.L. & Liu, L. (2009). Telomeres and reproductive aging. Reprod. Fertil. Dev. 21, 10–4.CrossRefGoogle ScholarPubMed
Krall, J.A., Beyer, E.M. & MacBeath, G. (2011). High- and low-affinity epidermal growth factor receptor–ligand interactions activate distinct signaling pathways. PLoS One 6, e15945.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Lakhani, S.A., Masud, A., Kuida, K., Porter, G.A. Jr., Booth, C.J., Mehal, W.Z., Inayat, I. & Flavell, R.A. (2006). Caspases 3 and 7: key mediators of mitochondrial events of apoptosis. Science 311, 847–51.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Li, Y., Zhang, Z., He, C., Zhu, K., Xu, Z., Ma, T., Tao, J. & Liu, G. (2015). Melatonin protects porcine oocyte in vitro maturation from heat stress. J. Pineal Res. 59, 365–75.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Liu, J., Linher, K. & Li, J. (2009). Porcine DAZL messenger RNA: its expression and regulation during oocyte maturation. Mol. Cell. Endocrinol. 311, 101–8.CrossRefGoogle ScholarPubMed
Lo, H.W. & Hung, M.C. (2006). Nuclear EGFR signalling network in cancers: linking EGFR pathway to cell cycle progression, nitric oxide pathway and patient survival. Br. J. Cancer 94, 184–8.CrossRefGoogle ScholarPubMed
Maida, Y., Kyo, S., Kanaya, T., Wang, Z., Yatabe, N., Tanaka, M., Nakamura, M., Ohmichi, M., Gotoh, N., Murakami, S. & Inoue, M. (2002). Direct activation of telomerase by EGF through Ets-mediated transactivation of TERT via MAP kinase signaling pathway. Oncogene 21, 4071–9.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.CrossRefGoogle ScholarPubMed
Mayer, M.P. & Bukau, B. (2005). Hsp70 chaperones: cellular functions and molecular mechanism. Cellular and molecular life sciences: CMLS 62, 670–84.CrossRefGoogle Scholar
Meka, D.P., Muller-Rischart, A.K., Nidadavolu, P., Mohammadi, B., Motori, E., Ponna, S.K., Aboutalebi, H., Bassal, M., Annamneedi, A., Finckh, B., Miesbauer, M., Rotermund, N., Lohr, C., Tatzelt, J., Winklhofer, K.F. & Kramer, E.R. (2015). Parkin cooperates with GDNF/RET signaling to prevent dopaminergic neuron degeneration. J. Clin. Invest. 125, 1873–85.CrossRefGoogle ScholarPubMed
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
Mulligan, L.M. (2014). RET revisited: expanding the oncogenic portfolio. Nat. Rev. Cancer 14, 173–86.CrossRefGoogle ScholarPubMed
Myers, S.M. & Mulligan, L.M. (2004). The RET receptor is linked to stress response pathways. Cancer Res. 64, 4453–63.CrossRefGoogle ScholarPubMed
Ni, H., Sheng, X., Cui, X., Gu, M., Liu, Y., Qi, X., Xing, S. & Guo, Y. (2015). Epidermal growth factor-mediated mitogen-activated protein kinase3/1 pathway is conducive to in vitro maturation of sheep oocytes. PLoS One 10, e0120418.CrossRefGoogle ScholarPubMed
Ozturk, S., Sozen, B. & Demir, N. (2014). Telomere length and telomerase activity during oocyte maturation and early embryo development in mammalian species. Mol. Hum. Reprod. 20, 15–30.CrossRefGoogle ScholarPubMed
Prochazka, R., Srsen, V., Nagyova, E., Miyano, T. & Flechon, J.E. (2000). Developmental regulation of effect of epidermal growth factor on porcine oocyte-cumulus cell complexes: nuclear maturation, expansion, and F-actin remodeling. Mol. Reprod. Dev. 56, 63–73.3.0.CO;2-D>CrossRefGoogle ScholarPubMed
Richardson, D.S., Lai, A.Z. & Mulligan, L.M. (2006). RET ligand-induced internalization and its consequences for downstream signaling. Oncogene 25, 3206–11.CrossRefGoogle ScholarPubMed
Ritter, L.J., Sugimura, S. & Gilchrist, R.B. (2015). Oocyte induction of EGF responsiveness in somatic cells is associated with the acquisition of porcine oocyte developmental competence. Endocrinology 156, 2299–312.CrossRefGoogle ScholarPubMed
Sakaguchi, M., Dominko, T., Yamauchi, N., Leibfried-Rutledge, M.L., Nagai, T. & First, N.L. (2002). Possible mechanism for acceleration of meiotic progression of bovine follicular oocytes by growth factors in vitro . Reproduction 123, 135–42.CrossRefGoogle ScholarPubMed
Salakou, S., Kardamakis, D., Tsamandas, A.C., Zolota, V., Apostolakis, E., Tzelepi, V., Papathanasopoulos, P., Bonikos, D.S., Papapetropoulos, T., Petsas, T. & Dougenis, D. (2007). Increased Bax/Bcl-2 ratio up-regulates caspase-3 and increases apoptosis in the thymus of patients with myasthenia gravis. In Vivo 21, 123–32.Google ScholarPubMed
Sariola, H. & Saarma, M. (2003). Novel functions and signalling pathways for GDNF. J. Cell Sci. 116, 3855–62.CrossRefGoogle ScholarPubMed
Schmittgen, T.D. & Livak, K.J. (2008). Analysing real-time PCR data by the comparative CT method. Nat. Protoc. 3, 1101–8.CrossRefGoogle Scholar
Scott, R.P., Eketjall, S., Aineskog, H. & Ibanez, C.F. (2005). Distinct turnover of alternatively spliced isoforms of the RET kinase receptor mediated by differential recruitment of the Cbl ubiquitin ligase. J. Biol. Chem. 280, 13442–9.CrossRefGoogle ScholarPubMed
Sigismund, S., Algisi, V., Nappo, G., Conte, A., Pascolutti, R., Cuomo, A., Bonaldi, T., Argenzio, E., Verhoef, L.G., Maspero, E., Bianchi, F., Capuani, F., Ciliberto, A., Polo, S. & Di Fiore, P.P. (2013). Threshold-controlled ubiquitination of the EGFR directs receptor fate. EMBO J. 32, 2140–57.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Sirard, M.A. (2012). Factors affecting oocyte and embryo transcriptomes. Reprod. Domest. Anim. [Zuchthygiene] 47 (Suppl 4), 148–55.CrossRefGoogle ScholarPubMed
Sirard, M.A., Richard, F., Blondin, P. & Robert, C. (2006). Contribution of the oocyte to embryo quality. Theriogenology 65, 126–36.CrossRefGoogle ScholarPubMed
Spikings, E.C., Alderson, J. & St John, J.C. (2007). Regulated mitochondrial DNA replication during oocyte maturation is essential for successful porcine embryonic development. Biol. Reprod. 76, 327–35.CrossRefGoogle ScholarPubMed
Stojkovic, M., Machado, S.A., Stojkovic, P., Zakhartchenko, V., Hutzler, P., Goncalves, P.B. & Wolf, E. (2001). Mitochondrial distribution and adenosine triphosphate content of bovine oocytes before and after in vitro maturation: correlation with morphological criteria and developmental capacity after in vitro fertilization and culture. Biol. Reprod. 64, 904–9.CrossRefGoogle ScholarPubMed
Sugimura, S., Ritter, L.J., Rose, R.D., Thompson, J.G., Smitz, J., Mottershead, D.G. & Gilchrist, R.B. (2015). Promotion of EGF receptor signaling improves the quality of low developmental competence oocytes. Dev. Biol. 403, 139–49.CrossRefGoogle ScholarPubMed
Sun, J.-w., Zhu, H.-j., Chao, L., LI, M.-z. & Hua, J.-l. (2013). GDNF up-regulates c-Myc transcription via the PI3K/Akt pathway to promote dairy goat male germline stem cells (mGSC) proliferation. J. Integ. Agric. 12, 1054–65.CrossRefGoogle Scholar
Sun, Q.Y., Lai, L. X., Park, K.W., Kuhholzer, B., Prather, R.S. & Schatten, H. (2001). Dynamic events are differently mediated by microfilaments, microtubules, and mitogen-activated protein kinase during porcine oocyte maturation and fertilization in vitro . Biol. Reprod. 64, 879–89.CrossRefGoogle ScholarPubMed
Sun, Q.Y. & Nagai, T. (2003). Molecular mechanisms underlying pig oocyte maturation and fertilization. J. Reprod. Dev. 49, 347–59.CrossRefGoogle ScholarPubMed
Tiwari, M., Prasad, S., Tripathi, A., Pandey, A.N., Ali, I., Singh, A.K., Shrivastav, T.G. & Chaube, S.K. (2015). Apoptosis in mammalian oocytes: a review. Apoptosis 20, 1019–25.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Toms, D.D. (2014). Involvement of GDNF and microRNA-378 in the regulation of porcine follicle maturation (Doctoral dissertation).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.CrossRefGoogle ScholarPubMed
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
Valleh, M.V., Rasmussen, M.A. & Hyttel, P. (2016). Combination effects of epidermal growth factor and glial cell line-derived neurotrophic factor on the in vitro developmental potential of porcine oocytes. Zygote 24, 465–76.CrossRefGoogle ScholarPubMed
Wang, W.H., Sun, Q.Y., Hosoe, M., Shioya, Y. & Day, B.N. (1997). Quantified analysis of cortical granule distribution and exocytosis of porcine oocytes during meiotic maturation and activation. Biol. Reprod. 56, 1376–82.CrossRefGoogle ScholarPubMed
Wang, X. (2013). Structural studies of GDNF family ligands with their receptors-Insights into ligand recognition and activation of receptor tyrosine kinase RET. Biochim. Biophys. Acta 1834, 2205–12.CrossRefGoogle ScholarPubMed
Wang, X., McCullough, K.D., Franke, T.F. & Holbrook, N.J. (2000). Epidermal growth factor receptor-dependent Akt activation by oxidative stress enhances cell survival. J. Biol. Chem. 275, 14624–31.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.CrossRefGoogle ScholarPubMed
Zhao, P., Qiao, J., Huang, S., Zhang, Y., Liu, S., Yan, L.Y., Hsueh, A.J. & Duan, E.K. (2011). Gonadotrophin-induced paracrine regulation of human oocyte maturation by BDNF and GDNF secreted by granulosa cells. Hum. Reprod. 26, 695–702.CrossRefGoogle ScholarPubMed