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Maturational gene upregulation and mitochondrial activity enhancement in mouse in vitro matured oocytes and using granulosa cell conditioned medium

Published online by Cambridge University Press:  03 October 2018

Elnaz Zand ,
Rouhollah Fathi Open the ORCID record for Rouhollah Fathi [Opens in a new window] ,
Mitra Heydari Nasrabadi ,
Mohammad Jafari Atrabi ,
Norah Spears  and
Vahid Akbarinejad
Elnaz Zand
Affiliation:
Department of Embryology, Reproductive Biomedicine Research Center, Royan Institute for Reproductive Biomedicine, ACECR, Tehran, Iran
Rouhollah Fathi*
Affiliation:
Department of Embryology, Reproductive Biomedicine Research Center, Royan Institute for Reproductive Biomedicine, ACECR, Tehran, Iran
Mitra Heydari Nasrabadi
Affiliation:
Department of Biology, Islamic Azad University, Parand Branch, Parand, Iran
Mohammad Jafari Atrabi
Affiliation:
Department of Embryology, Reproductive Biomedicine Research Center, Royan Institute for Reproductive Biomedicine, ACECR, Tehran, Iran
Norah Spears
Affiliation:
Centre for Integrative Physiology, University of Edinburgh, Edinburgh, UK MRC Centre for Reproductive Health, University of Edinburgh, Edinburgh, UK
Vahid Akbarinejad
Affiliation:
Department of Theriogenology, Faculty of Veterinary Medicine, University of Tehran, Tehran, Iran
*
*Author for correspondence: Rouhollah Fathi. Department of Embryology, Reproductive Biomedicine Research Center, Royan Institute for Reproductive Biomedicine, ACECR, Tehran, Iran. Tel: +98 912 947 9621. E-mail: rfathi79@royaninstitute.org
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Summary

The high miscarriage rates that result following transfer of embryos derived from in vitro maturation (IVM) of oocytes necessitate improvements in the processes involved. This study aimed to improve the quality of in vitro matured oocytes using granulosa cell conditioned medium (GCCM) as the culture medium. In this work, germinal vesicle (GV)-stage oocytes from NMRI mice were collected and cultured using three types of culture medium: Base medium (BM) (control), 50% granulosa cell conditioned medium (GCCM50) and 100% GCCM (GCCM100). After IVM, the mitochondria activity potential and viability of metaphase II (MII) oocytes were evaluated by JC-1 and trypan blue staining, respectively. Maturational gene expression levels of CyclinB1, Cdk1 and Gdf9 in the control, GCCM50 and GCCM100 samples were analyzed using real-time polymerase chain reaction (PCR). The viability rate of in vitro matured oocytes was highest in the GCCM50 group. JC-1 staining showed that GCCM50 enhances mitochondrial activity more than the other groups (P < 0.05). Gene expression levels of Cdk1 and Gdf9 were higher in the group with GCCM50 treatment, than in the control and GCCM100 groups (P < 0.05), while the expression level of CyclinB1 did not differ among the groups. The results indicated that a 50% concentration of GCCM in combination with BM components enhanced MII and viability rates and mitochondria activity of mouse immature oocytes.

Keywords

Conditioned mediumGranulosa cellIn vitro maturationMitochondrial activity potentialOocyte
Type
Research Article
Information
Zygote , Volume 26 , Issue 5 , October 2018 , pp. 366 - 371
Copyright
© Cambridge University Press 2018 

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References

Bolamba, D, Russ, KD, Harper, SA, Sandler, JL Durrant, BS (2006) Effects of epidermal growth factor and hormones on granulosa expansion and nuclear maturation of dog oocytes in vitro . Theriogenology 65, 1037–1047.Google Scholar
Conti, M, Hsieh, M, Park, JY Su, YQ (2006) Role of the epidermal growth factor network in ovarian follicles. Mol Endocrinol 20, 715–723.Google Scholar
Das, K, Phipps, WR, Hensleigh, HC Tagatz, GE (1992) Epidermal growth factor in human follicular fluid stimulates mouse oocyte maturation in vitro . Fertil Steril 57, 895–901.Google Scholar
De La Fuente, R, O’Brien, MJ Eppig, JJ (1999) Epidermal growth factor enhances preimplantation developmental competence of maturing mouse oocytes. Hum Reprod 14, 3060–3068.Google Scholar
Dirnfeld, M, Goldman, S, Gonen, Y, Koifman, M, Calderon, I Abramovici, H (1997) A simplified coculture system with luteinized granulosa cells improves embryo quality and implantation rates: a controlled study. Fertil Steril 67, 120–122.Google Scholar
Gilchrist, RB Thompson, JG (2007) Oocyte maturation: emerging concepts and technologies to improve developmental potential in vitro . Theriogenology 67, 6–15.Google Scholar
Gremeau, AS, Andreadis, N, Fatum, M, Craig, J, Turner, K, McVeigh, E Child, T (2012) In vitro maturation or in vitro fertilization for women with polycystic ovaries? A case–control study of 194 treatment cycles. Fertil Steril 98, 355–360.Google Scholar
Guler, A, Poulin, N, Mermillod, P, Terqui, M Cognie, Y (2000) Effect of growth factors, EGF and IGF-I, and estradiol on in vitro maturation of sheep oocytes. Theriogenology 54, 209–218.Google Scholar
Kobayashi, K, Takagi, Y, Satoh, T, Hoshi, H Oikawa, T (1992) Development of early bovine embryos to the blastocyst stage in serum-free conditioned medium from bovine granulosa cells. In Vitro Cell Dev Biol 28A, 255–259.Google Scholar
Kuzmina, TI, Alm, H, Denisenko, V, Tuchscherer, A, Kanitz, W Torner, H (2007) Effect of recombinant bovine somatotropin (rbST) on cytoplasmic maturation of bovine oocytes and their developmental competence in vitro . J Reprod Dev 53, 309–316.Google Scholar
Lanuza, GM, Fischman, ML Baranao, JL (1998) Growth promoting activity of oocytes on granulosa cells is decreased upon meiotic maturation. Dev Biol 197, 129–139.Google Scholar
Lenie, S, Cortvrindt, R, Adriaenssens, T Smitz, J (2004) A reproducible two-step culture system for isolated primary mouse ovarian follicles as single functional units. Biol Reprod 71, 1730–1738.Google Scholar
Liang, CG, Su, YQ, Fan, HY, Schatten, H Sun, QY (2007) Mechanisms regulating oocyte meiotic resumption: roles of mitogen-activated protein kinase. Mol Endocrinol 21, 2037–2055.Google Scholar
Lonergan, P Fair, T (2016) Maturation of oocytes in vitro . Annu Rev Anim Biosci 4, 255–268.Google Scholar
Malekshah, AK, Moghaddam, AE Daraka, SM (2006) Comparison of conditioned medium and direct co-culture of human granulosa cells on mouse embryo development. Indian journal of experimental biology. J Exp Biol 44, 189–192.Google Scholar
May-Panloup, P, Chretien, MF, Malthiery, Y Reynier, P (2007) Mitochondrial DNA in the oocyte and the developing embryo. Curr Topics Dev Biol 77, 51–83.Google Scholar
Miki, H, Ogonuki, N, Inoue, K, Baba, T Ogura, A (2006) Improvement of cumulus-free oocyte maturation in vitro and its application to microinsemination with primary spermatocytes in mice. J Reprod Dev 52, 239–248.Google Scholar
Myers, MW, Broussard, JR, Menezo, Y, Prough, SG, Blackwell, J, Godke, RA Thibodeaux, JK (1994) Established cell lines and their conditioned media support bovine embryo development during in vitro culture. Hum Reprod 9, 1927–1931.Google Scholar
Nakano, H Kubo, H (2000) Study of the in vitro maturation of mouse oocytes induced by microinjection of maturation promoting factor (MPF). J Assist Reprod Genet 17, 67–73.Google Scholar
Nandi, S, Raghu, HM, Ravindranatha, BM Chauhan, MS (2002) Production of buffalo (Bubalus bubalis) embryos in vitro: premises and promises. Reprod Domest Anim 37, 65–74.Google Scholar
Park, JY, Su, YQ, Ariga, M, Law, E, Jin, SL Conti, M (2004) EGF-like growth factors as mediators of LH action in the ovulatory follicle. Science 303, 682–684.Google Scholar
Richani, D, Sutton-McDowall, ML, Frank, LA, Gilchrist, RB Thompson, JG (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
Sakaguchi, M, Dominko, T, Yamauchi, N, Leibfried-Rutledge, ML, Nagai, T First, NL (2002) Possible mechanism for acceleration of meiotic progression of bovine follicular oocytes by growth factors in vitro . Reproduction 123, 135–142.Google Scholar
Schmitt, A Nebreda, AR (2002) Inhibition of Xenopus oocyte meiotic maturation by catalytically inactive protein kinase A. Proc Natl Acad Sci USA 99, 4361–4366.Google Scholar
Shimada, M, Hernandez-Gonzalez, I, Gonzalez-Robayna, I Richards, JS (2006) Paracrine and autocrine regulation of epidermal growth factor-like factors in cumulus–oocyte complexes and granulosa cells: key roles for prostaglandin synthase 2 and progesterone receptor. Mol Endocrinol 20, 1352–1365.Google Scholar
Singhal, S, Prasad, S, Singh, B, Prasad, JK Gupta, HP (2009) Effect of including growth factors and antioxidants in maturation medium used for in vitro culture of buffalo oocytes recovered in vivo . Anim Reprod Sci 113, 44–50.Google Scholar
Sirotkin, AV, Dukesova, J, Makarevich, AV, Kubek, A Bulla, J (2000) Evidence that growth factors IGF-I, IGF-II and EGF can stimulate nuclear maturation of porcine oocytes via intracellular protein kinase A. Reprod Nutr Dev 40, 559–569.Google Scholar
Smiley, ST, Reers, M, Mottola-Hartshorn, C, Lin, M, Chen, A, Smith, TW, Steele, GD Jr Chen, LB (1991) Intracellular heterogeneity in mitochondrial membrane potentials revealed by a J-aggregate-forming lipophilic cation JC-1. Proc Natl Acad Sci USA 88, 3671–3675.Google Scholar
Smitz, JE, Thompson, JG Gilchrist, RB (2011) The promise of in vitro maturation in assisted reproduction and fertility preservation. Semin Reprod Med 29, 24–37.Google Scholar
Trounson, A, Anderiesz, C Jones, G (2001) Maturation of human oocytes in vitro and their developmental competence. Reproduction 121, 51–75.Google Scholar
Wilding, M, Dale, B, Marino, M, di Matteo, L, Alviggi, C, Pisaturo, ML, Lombardi, L De Placido, G (2001) Mitochondrial aggregation patterns and activity in human oocytes and preimplantation embryos. Hum Reprod 16, 909–917.Google Scholar