Hostname: page-component-78c5997874-t5tsf Total loading time: 0 Render date: 2024-11-10T14:48:02.424Z Has data issue: false hasContentIssue false

Maternal effect gene expression in porcine metaphase II oocytes and embryos in vitro: effect of epidermal growth factor, interleukin-1β and leukemia inhibitory factor

Published online by Cambridge University Press:  23 December 2016

Marta Wasielak*
Affiliation:
Department of Gamete and Embryo Biology, Institute of Animal Reproduction and Food Research of the Polish Academy of Sciences, Tuwima 10, 10–747 Olsztyn, Poland. Department of Gamete and Embryo Biology, Institute of Animal Reproduction and Food Research of the Polish Academy of Sciences, Tuwima 10, 10–748 Olsztyn, Poland.
Teresa Więsak
Affiliation:
Department of Gamete and Embryo Biology, Institute of Animal Reproduction and Food Research of the Polish Academy of Sciences, Tuwima 10, 10–748 Olsztyn, Poland.
Iwona Bogacka
Affiliation:
Department of Animal Physiology, University of Warmia and Mazury, Oczapowskiego 1A, 10–719 Olsztyn, Poland.
Beenu Moza Jalali
Affiliation:
Department of Gamete and Embryo Biology, Institute of Animal Reproduction and Food Research of the Polish Academy of Sciences, Tuwima 10, 10–748 Olsztyn, Poland.
Marek Bogacki
Affiliation:
Department of Gamete and Embryo Biology, Institute of Animal Reproduction and Food Research of the Polish Academy of Sciences, Tuwima 10, 10–748 Olsztyn, Poland.
*
All correspondence to: M. Wasielak. Department of Gamete and Embryo Biology, Institute of Animal Reproduction and Food Research of the Polish Academy of Sciences, Tuwima 10, 10–747 Olsztyn, Poland. Tel: +48 89 539 3114. Fax: +48 89 539 3155. E-mail: m.wasielak@pan.olsztyn.pl

Summary

Maternal effect genes (MEG) play a crucial role in early embryogenesis. In vitro culture conditions may affect MEG expression in porcine oocytes and embryos. We investigated whether in vitro culture medium supplementation with epidermal growth factor (EGF), IL-1β or LIF (leukemia inhibitory factor) affects the mRNA level of ZAR-1 (zygote arrest 1), NPM2 (nucleoplasmin 2) and DPPA3 (developmental associated protein 3) in porcine MII oocytes and embryos. Cumulus–oocyte complexes (COCs) were matured in NCSU-37 medium (control) or in NCSU-37 with EGF 10 ng/ml, IL-1β 10 ng/ml or LIF 50 ng/ml. After maturation for 44–46 h, MII oocytes were preserved for the analysis of MEG mRNA levels (experiment 1). In experiment 2, COCs were fertilized, and the presumptive zygotes were cultured in the same groups. Then, 2-, 4-, 8-cell embryos, morulae and blastocysts were collected for the analysis of MEG mRNA levels. LIF addition to the maturation medium increased MII oocyte numbers (P < 0.05), while EGF and IL-1β did not affect oocyte maturation. Medium supplementation with EGF resulted in lower DPPA3 mRNA levels in MII oocytes and in 2- and 4-cell embryos versus control embryos (P < 0.05). LIF treatment increased DPPA3 mRNA levels in morulae and blastocysts (P < 0.05). Culture with EGF and IL-1β decreased ZAR-1 and NPM2 mRNA levels in 2-cell embryos (P < 0.05). The inclusion of EGF or IL-1β in the porcine in vitro production system influences ZAR-1, NPM2 and DPPA3 mRNA in MII oocytes and embryos but not beyond the 4-cell stage. LIF stimulates oocyte maturation and affects DPPA3 mRNA in porcine morulae and blastocysts in vitro.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2016 

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

Abeydeera, L.R., Wang, W.-H., Cantley, T.C., Rieke, A., Prather, R.S. & Day, B.N. (1998). Presence of epidermal growth factor during in vitro maturation of pig oocytes and embryo culture can modulate blastocyst development after in vitro fertilization. Mol. Reprod. Dev. 51, 395401.Google Scholar
Bogacki, M., Wasielak, M., Kitewska, A., Bogacka, I. & Jalali, B.M. (2014). The effect of hormonal estrus induction on maternal effect and apoptosis-related genes expression in porcine cumulus–oocyte complexes. Reprod. Biol. Endocrinol. 12, 32.Google Scholar
Bowles, J., Teasdale, R.P., James, K. & Koopman, P. (2003). Dppa3 is a marker of pluripotency and has a human homologue that is expressed in germ cell tumours. Cytogenet. Genome Res. 101, 261–5.Google Scholar
Burns, K.H., Viveiros, M.M., Ren, Y., Wang, P., DeMayo, F.J., Frail, D.E., Eppig, J.J. & Matzuk, M.M. (2003). Roles of NPM2 in chromatin and nucleolar organization in oocytes and embryos. Science 300, 633–6.Google Scholar
Choi, Y.B., Kim, S.J., Park, E.J., Song, K.Y., Moon, J.H. & Lee, B.C. (2014). Effect of leukemia inhibitory factor (LIF) on maturation of porcine oocytes in vitro maturation and development of parthenogenetic embryos. Reprod. Fertil. Dev. 26, 159.Google Scholar
Dang-Nguyen, T.Q., Haraguchi, S., Kikuchi, K., Somfai, T., Bodó, S. & Nagai, T. (2014). Leukemia inhibitory factor promotes porcine oocyte maturation and is accompanied by activation of signal transducer and activator of transcription 3. Mol. Reprod. Dev. 8, 230–9.Google Scholar
Marques, M.G, Nicacio, A.C, de Oliveira, V.P., Nascimento, A.B., Caetano, H.V., Mendes, C.M., Mello, M.R., Milazzotto, M.P., Assumpção, M.E. & Visintin, J.A. (2007). In vitro maturation of pig oocytes with different media, hormone and meiosis inhibitors. Anim. Reprod. Sci. 97, 375–81.CrossRefGoogle ScholarPubMed
Heikinheimo, O. & Gibbons, W.E. (1998). The molecular mechanisms of oocyte maturation and early embryonic development are unveiling new insights into reproductive medicine. Mol. Hum. Reprod. 4, 745–56.Google Scholar
Jeung, S.-H., Jeon, Y.-B., Biswas, D., Choi, K.-Ch., Jeung, E.-B. & Hyun, S.-H. (2012). Effect of EGF and AREG treatment during porcine in vitro maturation on in vitro developmental potential of preimplantation embryos. J. Anim. Vet. Adv. 11, 1100–5.Google Scholar
Jiwakanon, J., Berg, M., Persson, E., Fossum, C. & Dalin, A.-M. (2010). Cytokine expression in the gilt oviduct: effects of seminal plasma, spermatozoa and extender after insemination. Anim. Reprod. Sci. 119, 244–57.Google Scholar
Jiwakanon, J., Persson, E., Berg, M. & Dalin, A.-M. (2011). Influence of seminal plasma, spermatozoa and semen extender on cytokine expression in the porcine endometrium after insemination. Anim. Reprod. Sci. 123, 210–20.Google Scholar
Jung, S.K., Kim, H.J., Kim, C.L., Lee, J.H., You, J.Y., Lee, E.S., Lim, J.M., Yun, S.J., Song, J.Y. & Cha, S.H. (2014). Enhancing effects of serum-rich and cytokine-supplemented culture conditions on developing blastocysts and deriving porcine parthenogenetic embryonic stem cells. J. Vet. Sci. 15, 519–28.Google Scholar
Kikuchi, K., Onishi, A., Kashiwazaki, N., Iwamoto, M., Noguchi, J., Kaneko, H., Akita, T. & Nagai, T. (2002). Successful piglet production after transfer of blastocysts produced by a modified in vitro system. Biol. Reprod. 66, 1033–41.CrossRefGoogle ScholarPubMed
Kohata, C., Izquierdo-Rico, M.J., Romar, R. & Funahashi, H. (2013). Development competence and relative transcript abundance of oocytes derived from small and medium follicles of prepubertal gilts. Theriogenology 80, 970–8.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. (2005). Effect of epidermal growth factor in preimplantation development of porcine cloned embryos. Mol. Reprod. Dev. 71, 4551.Google Scholar
Lingenfelter, B.M., Tripurani, S.K., Tejomurtula, J., Smith, G.W. & Yao, J. (2011). Molecular cloning and expression of bovine nucleoplasmin 2 (NPM2): a maternal effect gene regulated by miR-181a. Reprod. Biol. Endocrinol. 9, 40.Google Scholar
Litter, R.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.Google Scholar
Mo, X., Wu, G., Yuan, D., Jia, B., Liu, C., Zhu, S. & Hou, Y. (2014). Leukemia inhibitory factor enhances bovine oocyte maturation and early embryo development. Mol. Reprod. Dev. 81, 608–18.Google Scholar
Nakamura, T., Arai, Y., Umehara, H., Masuhara, M., Kimura, T., Taniguchi, H., Sekimoto, T., Ikawa, M., Yoneda, Y., Okabe, M., Tanaka, S., Shiota, K. & Nakano, T. (2007). PGC7/Stella protects against DNA demethylation in early embryogenesis. Nat. Cell Biol. 9, 6471.Google Scholar
Nakatani, T., Yamagata, K., Kimura, T., Oda, M., Nakashima, H., Hori, M., Sekita, Y., Arakawa, T., Nakamura, T. & Nakano, T. (2015). Stella preserves maternal chromosome integrity by inhibiting 5hmC-induced γH2AX accumulation. EMBO Rep. 16, 582–9.Google Scholar
Neira, J.A., Tainturier, D., Peña, M.A. & Martal, J. (2010). Effect of the association of IGF-I, IGF-II, bFGF, TGF-β1, GM-CSF, and LIF on the development of bovine embryos produced in vitro. Theriogenology 73, 595604.Google Scholar
Paciolla, M., Boni, R., Fusco, F., Pescatore, A., Poeta, L., Ursini, M.V., Lioi, M.B. & Miano, M.G. (2011). Nuclear factor-kappa-B-inhibitor alpha (NFKBIA) is a developmental marker of NF-κB/p65 activation during in vitro oocyte maturation and early embryogenesis. Hum. Reprod. 26, 1191–201.Google Scholar
Passos, J.R.S., Costa, J.J.N., da Cunha, E.V., Silva, A.W.B., Ribeiro, R.P., de Souz, G.B., Barroso, P.A.A., Dau, A.M.P., Saraiva, M.V.A., Gonçalves, P.B.D., van den Hurk, R. & Silva, J.R.V. (2015). Protein and messenger RNA expression of interleukin 1 system members in bovine ovarian follicles and effects of interleukin 1β on primordial follicle activation and survival in vitro . Domest. Anim. Endocrinol. 54, 4859.Google Scholar
Richani, D., Wang, X., Zeng, H.T., Smitz, J., Thompson, J.G. & Gilchrist, R.B. (2014). Pre-maturation with cAMP modulators in conjunction with EGF-like peptides during in vitro maturation enhances mouse oocyte developmental competence. Mol. Reprod. Dev. 81, 422–35.CrossRefGoogle ScholarPubMed
Rodriguez, A., Allegrucci, C. & Alberio, R. (2012). Modulation of pluripotency in the porcine embryo and iPS cells. PLoS ONE 7, e49079.Google Scholar
Romar, R., De Santis, T., Papillier, P., Perreau, C., Thelie, A., Dell'Aquila, M.E., Mermillod, P. & Dalbie, R. (2011). Expression of maternal transcripts during bovine oocyte in vitro maturation is affected by donor age. Reprod. Domest. Anim. 46, 2330.Google Scholar
Ropka-Molik, K., Oczkowicz, M., Mucha, A., Piórkowska, K. & Piestrzyńska-Kajtoch, A. (2012). Variability of mRNA abundance of leukemia inhibitory factor gene (LIF) in porcine ovary, oviduct and uterus tissues. Mol. Biol. Rep. 39, 7965–72.Google Scholar
Samudio-Ruiz, S.L. & Hudson, L.G. (2012). Increased DNA methyltransferase activity and DNA methylation following epidermal growth factor stimulation in ovarian cancer cells. Epigenetics 7, 216–24.Google Scholar
Scaltiri, M. & Baselaga, J. (2006). The epidermal growth factor receptor pathway: a model for targeted therapy. Clin. Cancer Res. 12, 18.Google Scholar
Takakura, K., Taii, S., Fukuoka, M., Yasuda, K., Tagaya, Y., Yodoi, J. & Mori, T. (1989). Interleukin-2 receptor/p55(Tac)-inducing activity in porcine follicular fluids. Endocrinology 125, 618–23.Google Scholar
Uzbekova, S., Roy-Sabau, M., Dalbiès-Tran, R., Perreau, C., Papillier, P., Mompart, F., Thelie, A., Pennetier, S., Cognie, J., Cadoret, V., Royere, D., Monget, P. & Mermillod, P. (2006). Zygote arrest 1 gene in the pig, cattle and human: evidence of different transcripts variants in male and female germ cells. Reprod. Biol. Endocrinol. 4, 12.Google Scholar
Valleh, M.V., Rasmussen, M.A. & Hyttel, P. (2015). Combination effects of epidermal growth factor and glial cell line-derived neurotrophic factor on the in vitro developmental potential of porcine oocytes. Zygote 9, 112.Google Scholar
Wu, G., Jia, B., Mo, X., Liu, C., Fu, X., Zhu, S. & Hou, Y. (2013). Nuclear maturation and embryo development of porcine oocytes vitrified by cryotop: effect of different stages of in vitro maturation. Cryobiology 67, 95101.Google Scholar
Wu, X., Viveiros, M.M, Eppig, J.J., Bai, Y., Fitzpatrick, S.L. & Matzuk, M.M. (2003). Zygote arrest 1 (Zar1) is a novel maternal-effect gene critical for the oocyte-to-embryo transition. Nat. Genet. 33, 187–91.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, 299304.Google Scholar
Yasuda, K., Fukuoka, M., Taii, S., Takakura, K. & Mori, T. (1990). Inhibitory effects of interleukin-1 on follicle-stimulating hormone induction of aromatase activity, progesterone secretion, and functional luteinizing hormone receptors in cultures of porcine granulosa cells. Biol. Reprod. 43, 905–12.Google Scholar
Zhang, W., Chen, Q., Yang, Y., Liu, W., Zhang, M., Xia, G. & Wang, C. (2014). Epidermal growth factor-network signaling mediates luteinizing hormone regulation of BNP and CNP and their receptor NPR2 during porcine oocyte meiotic resumption. Mol. Reprod. Dev. 81, 1030–41.Google Scholar
Zhao, S. & Fernald, R.D. (2005). Comprehensive algorithm for quantitative real-time polymerase chain reaction. J. Comput. Biol. 12, 1045–62.Google Scholar