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Insulin influences developmental competence of bovine oocytes cultured in α-MEM plus follicle-simulating hormone

Published online by Cambridge University Press:  10 June 2014

Gustavo Bruno Mota ,
Ingrid Oliveira e Silva ,
Danielle Kaiser de Souza ,
Flavia Tuany ,
Michele Munk Pereira ,
Luiz Sergio de Almeida Camargo  and
Alzira Amélia Martins Rosa e Silva
Gustavo Bruno Mota
Affiliation:
Laboratory for the Study of Reproduction, Biological Institute, University of Brasília, DF, 70910–900, Brazil.
Ingrid Oliveira e Silva
Affiliation:
Laboratory for the Study of Reproduction, Biological Institute, University of Brasília, DF, 70910–900, Brazil.
Danielle Kaiser de Souza
Affiliation:
Laboratory for the Study of Reproduction, Biological Institute, University of Brasília, DF, 70910–900, Brazil. Faculty of Ceilandia, University of Brasília, DF, Brazil.
Flavia Tuany
Affiliation:
Laboratory for the Study of Reproduction, Biological Institute, University of Brasília, DF, 70910–900, Brazil.
Michele Munk Pereira
Affiliation:
Embrapa Dairy Cattle, Juiz de Fora, MG, 36038–330, Brazil.
Luiz Sergio de Almeida Camargo
Affiliation:
Embrapa Dairy Cattle, Juiz de Fora, MG, 36038–330, Brazil.
Alzira Amélia Martins Rosa e Silva*
Affiliation:
Laboratory for the Study of Reproduction, Biological Institute, University of Brasília, DF, 70910–900, Brazil.
*
All correspondence to: Alzira A. M. Rosa e Silva. Laboratory for the Study of Reproduction, Biological Institute, University of Brasília, DF, 70910–900, Brazil. Tel: +55 61 31072914. e-mail: [email protected]
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Summary

The aim of this study was to evaluate the dose–response effect of insulin, plus follicle-simulating hormone (FSH) at a fixed concentration, in a serum-free defined culture medium (DCM) on the in vitro maturation of bovine cumulus–oocyte complexes (COCs). For oocyte nuclear maturation, the expression levels of GDF9, GLUT1, PRDX1 and HSP70.1 transcripts related to oocyte and embryo developmental competence were analysed. For in vitro maturation (IVM), cumulus–oocyte complexes from slaughterhouse ovaries were distributed into four groups based on insulin concentration added to serum-free DCM, which was composed of alpha minimum essential medium (α-MEM), as basal medium: (1) DCM control: 0 ng/ml; (2) DCM1: 1 ng/ml; (3) DCM10: 10 ng/ml; and (4) DCM100: 100 ng/ml. After IVM, the nuclear status of a sample of oocytes was analysed and the other oocytes were submitted for in vitro fertilization (IVF) and in vitro culture (IVC). Different concentrations of insulin did not affect significantly the nuclear maturation and cleavage rate (72 h post-insemination) across all groups. Blastocyst rate (192 h post-insemination) did not differ in DCM control (24.3%), DCM1 (27.0%) and DCM10 (26.3%) groups, but the DCM100 (36.1%) group showed a greater blastocyst rate (P < 0.05) than the DCM control. Insulin concentrations of 1, 10, or 100 ng/ml decreased the relative levels of GDF9 and HSP70-1 transcripts in oocytes at the end of IVM (P < 0.05). The transcripts levels of PRDX1 decreased (P < 0.05) only when 10 or 100 ng/ml insulin was added to the DCM medium. No difference in levels of GLUT1 transcripts (P > 0.05) was observed at the different insulin concentrations. The results indicated that insulin added to DCM influenced levels of transcripts related to cellular stress (HSP70-1 and PRDX1) and oocyte competence (GDF9) in bovine oocytes and at higher concentrations enhanced blastocyst production.

Keywords

BovineIn vitro maturationInsulinOocytesTranscripts
Type
Research Article
Information
Zygote , Volume 23 , Issue 4 , August 2015 , pp. 563 - 572
Copyright
Copyright © Cambridge University Press 2014 

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References

Adashi, E.Y., Resnick, C.E., Hernandez, E.R., Svoboda, M.E. & Van Wyk, J.J. (1988). In vivo regulation of granulosa cell somatomedin-C/insulin-like growth factor I receptors. Endocrinology 122, 1383–9.CrossRefGoogle ScholarPubMed
Augustin, R., Pocar, P., Wrenzycki, C., Niemann, H. & Fischer, B. (2003). Mitogenic and anti-apoptotic activity of insulin on bovine embryos produced in vitro. Reproduction 126, 91–99.CrossRefGoogle ScholarPubMed
Bettegowda, A. & Smith, G.W. (2007). Mechanisms of maternal mRNA regulation: implications for mammalian early embryonic development. Front. Biosci. 12, 3713–26.CrossRefGoogle ScholarPubMed
Camargo, L., Viana, J., Ramos, A., Serapião, R., de Sa, W., Ferreira, A., Guimarães, M. & do Vale Filho, V. (2007). Developmental competence and expression of the Hsp 70.1 gene in oocytes obtained from Bos indicus and Bos taurus dairy cows in a tropical environment. Theriogenology 68, 626–32.CrossRefGoogle Scholar
Chaves, R.N., Duarte, A.B., Rodrigues, G.Q., Celestino, J.J., Silva, G.M., Lopes, C.A., Almeida, A.P., Donato, M.A., Peixoto, C.A., Moura, A.A., Lobo, C.H., Locatelli, Y., Mermillod, P., Campello, C.C. & Figueiredo, J.R. (2012). The effects of insulin and follicle-simulating hormone (FSH) during in vitro development of ovarian goat preantral follicles and the relative mRNA expression for insulin and FSH receptors and cytochrome P450 aromatase in cultured follicles. Biol. Reprod. 87, 69–79.CrossRefGoogle ScholarPubMed
Christians, E.S., Zhou, Q., Renard, J. & Benjamin, I.J. (2003). Heat shock proteins in mammalian development. Semin. Cell. Dev. Biol. 14, 283–90.CrossRefGoogle ScholarPubMed
Córdova, B., Morató, R., de Frutos, C., Bermejo-Álvarez, P., Paramio, T., Gutiérrez-Adán, A. & Mogas, T. (2011). Effect of leptin during in vitro maturation of prepubertal calf oocytes: embryonic development and relative mRNA abundances of genes involved in apoptosis and oocyte competence. Theriogenology 76, 1706–15.CrossRefGoogle ScholarPubMed
de Souza, D.K., Tuany, F., Nobre, C.S., Sousa, K.L.G. & Rosa a Silva, A.A.M. (2013). Blockage of phosphatidylinositol 3-kinase (PI3K) pathway reverts the inhibition of oocyte nuclear maturation promoted by a defined medium (MIV B). SSR 46th Annual Meeting: Reproductive Health: Nano to Global 22–26 July 2013, Abstract 424. Biol. Reprod. 89(Suppl.), 201–2.Google Scholar
Eppig, J.J. (2001). Oocyte control of ovarian follicular development and function in mammals. Reproduction 122, 829–38.CrossRefGoogle ScholarPubMed
Fair, T., Carter, F., Park, S., Evans, A. & Lonergan, P. (2007). Global gene expression analysis during bovine oocyte in vitro maturation. Theriogenology 68(Suppl. 1), S91–7.CrossRefGoogle ScholarPubMed
Ferreira, E.M., Vireque, A.A., Adona, P.R., Meirelles, F.V., Ferriani, R.A. & Navarro, P.A. (2009). Cytoplasmic maturation of bovine oocytes: structural and biochemical modifications and acquisition of developmental competence. Theriogenology 71, 836–48.CrossRefGoogle ScholarPubMed
Fouladi-Nashta, A.A. & Campbell, K.H. (2006). Dissociation of oocyte nuclear and cytoplasmic maturation by the addition of insulin in cultured bovine antral follicles. Reproduction 131, 449–60.CrossRefGoogle ScholarPubMed
Gilchrist, R. & Thompson, J. (2007). Oocyte maturation: emerging concepts and technologies to improve developmental potential in vitro. Theriogenology 67, 6–15.CrossRefGoogle ScholarPubMed
Gordon, I. (1994). Laboratory Production of Cattle Embryo. London: CAB International, Cambridge University Press.Google Scholar
Grazul-Bilska, A.T., Borowczyk, E., Bilski, J.J., Reynolds, L.P., Redmer, D.A., Caton, J.S. & Vonnahme, K.A. (2012). Overfeeding and underfeeding have detrimental effects on oocyte quality measured by in vitro fertilization and early embryonic development in sheep. Domest. Anim. Endocrinol. 43, 289–98.CrossRefGoogle ScholarPubMed
Humblot, P., Holm, P., Lonergan, P., Wrenzycki, C., Lequarré, A.S., Joly, C.G., Herrmann, D., Lopes, A., Rizos, D., Niemann, H. & Callesen, H. (2005). Effect of stage of follicular growth during superovulation on developmental competence of bovine oocytes. Theriogenology 63, 1149–66.CrossRefGoogle ScholarPubMed
Jeong, Y.W., Hossein, M.S., Bhandari, D.P., Kim, Y.W., Kim, J.H., Park, S.W., Lee, E., Park, S.M., Jeong, Y.I., Lee, J.Y., Kim, S. & Hwang, W.S. (2008). Effects of insulin–transferrin–selenium in defined and porcine follicular fluid supplemented IVM media on porcine IVF and SCNT embryo production. Anim. Reprod. Sci. 106, 13–24.CrossRefGoogle ScholarPubMed
Kiang, J.G. & Tsokos, G.C. (1998). Heat shock protein 70 kDa: molecular biology, biochemistry, and physiology. Pharmacol. Ther. 80, 183–201.CrossRefGoogle ScholarPubMed
Knight, P.G. & Glister, C. (2006). TGF-β superfamily members and ovarian follicle development. Reproduction 132, 191–206.CrossRefGoogle ScholarPubMed
Kregel, KC. (2002). Heat shock proteins: modifying factors in physiological stress responses and acquired thermotolerance. J. Appl. Physiol. 92, 2177–86.CrossRefGoogle ScholarPubMed
Lee, M.S., Kang, S.K., Lee, B.C. & Hwang, W.S. (2005). The beneficial effects of insulin and metformin on in vitro developmental potential of porcine oocytes and embryos. Biol. Reprod. 73, 1264–8.CrossRefGoogle ScholarPubMed
Lequarre, A.S., Grisart, B., Moreau, B., Schuurbies, N., Massip, A. & Dessy, F. (1997). Glucose metabolism during bovine preimplantation development: analysis of gene expression in single oocytes and embryos. Mol. Reprod. Dev. 48, 216–26.3.0.CO;2-V>CrossRefGoogle ScholarPubMed
Leyens, G., Knoops, B. & Donnay, I. (2004). Expression of peroxiredoxins in bovine oocytes and embryos produced in vitro. Mol. Reprod. Dev. 69, 243–51.CrossRefGoogle ScholarPubMed
Lonergan, P., Monaghan, P., Rizos, D., Boland, M. & Gordon, I. (1994). Effect of follicle size on bovine oocyte quality and developmental competence following maturation, fertilization, and culture in vitro. Mol. Reprod. Dev. 37, 48–53.CrossRefGoogle ScholarPubMed
Lonergan, P., Gutiérrez-Adán, A., Rizos, D., Pintado, B., de la Fuente, J. & Boland, M.P. (2003). Relative messenger RNA abundance in bovine oocytes collected in vitro or in vivo before and 20 hr after the preovulatory luteinizing hormone surge. Mol. Reprod. Dev. 66, 297–305.CrossRefGoogle ScholarPubMed
Lopes, A.S., Wrenzycki, C., Ramsing, N.B., Herrmann, D., Niemann, H., Lovendahl, P., Greve, T. & Callesen, H. (2007). Respiration rates correlate with mRNA expression of G6PD and GLUT1 genes in individual bovine in vitro-produced blastocysts. Theriogenology 68, 223–36.CrossRefGoogle ScholarPubMed
Minegishi, T., Hirakawa, T., Kishi, H., Abe, K., Abe, Y., Mizutani, T. & Miyamoto, K. (2000). A role of insulin-like growth factor I for follicle-stimulating hormone receptor expression in rat granulosa cells. Biol. Reprod. 62, 325–33.CrossRefGoogle ScholarPubMed
Mourot, M., Dufort, I., Gravel, C., Algriany, O., Dieleman, S. & Sirard, M.A. (2006). The influence of follicle size, FSH-enriched maturation medium, and early cleavage on bovine oocyte maternal mRNA levels. Mol. Reprod. Dev. 73, 1367–79.CrossRefGoogle ScholarPubMed
Neumann, C.A., Krause, D.S., Carman, C.V., Das, S., Dubey, D.P., Abraham, J.L., Bronson, R.T., Fujiwara, Y., Orkin, S.H. & Van Etten, R.A. (2003). Essential role for the peroxiredoxin Prdx1 in erythrocyte antioxidant defence and tumour suppression. Nature 424, 561–5.CrossRefGoogle ScholarPubMed
O’Brien, R.M., Streeper, R.S., Ayala, J.E., Stadelmaier, B.T. & Hornbuckle, L.A. (2001). Insulin-regulated gene expression. Biochem. Soc. Trans. 29 (Pt 4), 552–8.CrossRefGoogle ScholarPubMed
Ocaña-Quero, J.M., Pinedo-Merlin, M., Ortega- Mariscal, M. & Moreno-Millan, M. (1998). Influence of human and bovine insulin on in vitro maturation, fertilization and cleavage rates of bovine oocytes. Arch. Zootec. 47, 85–93.Google Scholar
Oliveira e Silva, I., Vasconcelos, R.B., Caetano, J.V.O., Gulart, L.V.M., Camargo, L.S.A., Báo, S.N. & Rosa e Silva, A.A. (2011). Induction of reversible meiosis arrest of bovine oocytes using a two-step procedure under defined and nondefined conditions. Theriogenology 75, 1115–24.CrossRefGoogle ScholarPubMed
Otoi, T., Yamamoto, K., Koyama, N., Tachikawa, S. & Suzuki, T. (1997). Bovine oocyte diameter in relation to developmental competence. Theriogenology 48, 769–74.CrossRefGoogle ScholarPubMed
Pereira, M.M., Machado, M.A., Costa, F.Q., Serapião, R.V., Viana, J.H.M. & Camargo, L.S.A. (2010). Effect of oxygen tension and serum during IVM on developmental competence of bovine oocytes. Reprod. Fertil. Dev. 22, 1074–82.CrossRefGoogle 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
Quirk, S.M., Harman, R.M. & Cowan, R.G. (2000). Regulation of Fas antigen (Fas, CD95)-mediated apoptosis of bovine granulosa cells by serum and growth factors. Biol. Reprod. 63, 1278–84.CrossRefGoogle ScholarPubMed
Raghu, H., Nandi, S. & Reddy, S. (2002). Effect of insulin, transferrin and selenium and epidermal growth factor on development of buffalo oocytes to the blastocyst stage in vitro in serum-free, semidefined media. Vet. Rec. 151, 260–5.CrossRefGoogle Scholar
Ramakers, C., Ruijter, J.M., Deprez, R.H. & Moorman, A.F. (2003). Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci. Lett. 339, 62–6.CrossRefGoogle ScholarPubMed
Rhee, Y.H., Choi, M., Lee, H.S., Park, C.H., Kim, S.M., Yi, S.H., Oh, S.M., Cha, H.J., Chang, M.Y. & Lee, S.H. (2013). Insulin concentration is critical in culturing human neural stem cells and neurons. Cell Death Dis. 4:e766.CrossRefGoogle ScholarPubMed
Rieger, D. & Loskutoff, N.M. (1994). Changes in the metabolism of glucose, pyruvate, glutamine and glycine during maturation of cattle oocytes in vitro. J. Reprod. Fertil. 100, 257–62.CrossRefGoogle Scholar
Rodriguez, K.F. & Farin, C.E. (2004). Gene transcription and regulation of oocyte maturation. Reprod. Fertil. Dev. 16, 55–67.CrossRefGoogle ScholarPubMed
Sagirkaya, H., Misirlioglu, M., Kaya, A., First, N., Parrish, J. & Memili, E. (2007). Developmental potential of bovine oocytes cultured in different maturation and culture conditions. Anim. Reprod. Sci. 101, 225–40.CrossRefGoogle ScholarPubMed
Shimizu, T., Murayama, C., Sudo, N., Kawashima, C., Tetsuka, M. & Miyamoto, A. (2008). Involvement of insulin and growth hormone (GH) during follicular development in the bovine ovary. Anim. Reprod. Sci. 106, 143–52.CrossRefGoogle ScholarPubMed
Sirard, M.A. & Coenen, K. (1993). The co-culture of cumulus-enclosed bovine oocytes and hemi-sections of follicles: Effects on meiotic resumption. Theriogenology 40, 933–42.CrossRefGoogle ScholarPubMed
Spicer, L.J., Chamberlain, C.S. & Maciel, S.M. (2002). Influence of gonadotropins on insulin- and insulin-like growth factor-I (IGF-I)-induced steroid production by bovine granulosa cells. Domest. Anim. Endocrinol. 22, 237–54.CrossRefGoogle ScholarPubMed
Sutton, M.L., Gilchrist, R.B. & Thompson, J.G. (2003). Effects of in vivo and in vitro environments on the metabolism of the cumulus–oocyte complex and its influence on oocyte developmental capacity. Hum. Reprod. Update 19, 35–48.CrossRefGoogle Scholar
Sutton-McDowall, M.L., Gilchrist, R.B. & Thompson, J.G. (2010). The pivotal role of glucose metabolism in determining oocyte developmental competence. Reproduction 139, 685–95.CrossRefGoogle ScholarPubMed
Thélie, A., Papillier, P., Pennetier, S., Perreau, C., Traverso, J.M., Uzbekova, S., Mermillod, P., Joly, C., Humblot, P. & Dalbiès-Tran, R. (2007). Differential regulation of abundance and deadenylation of maternal transcripts during bovine oocyte maturation in vitro and in vivo. BMC Dev. Biol. 7, 7:125.CrossRefGoogle ScholarPubMed
Van den Hurk, R. & Zhao, J. (2005). Formation of mammalian oocytes and their growth, differentiation and maturation within ovarian follicles. Theriogenology 63, 1717–51.CrossRefGoogle ScholarPubMed
Vireque, A., Camargo, L., Serapião, R., Rosa E Silva, A., Watanabe, Y., Ferreira, E., Navarro, P., Martins, W. & Ferriani, R. (2009). Preimplantation development and expression of Hsp-70 and Bax genes in bovine blastocysts derived from oocytes matured in alpha-MEM supplemented with growth factors and synthetic macromolecules. Theriogenology 71, 620–7.CrossRefGoogle ScholarPubMed
Vasconcelos, R.B., Salles, L.P., Oliveira e Silva, I., Gulart, L.V., Souza, D.K., Torres, F.A., Bocca, A.L. & Rosa e Silva, A.A. (2013). Culture of bovine ovarian follicle wall sections maintained the highly estrogenic profile under basal and chemically defined conditions. Braz. J. Med. Biol. Res. 46, 700–7.CrossRefGoogle ScholarPubMed
Wang, X., Tao, L. & Hai, C.X. (2012). Redox-regulating role of insulin: the essence of insulin effect. Mol. Cell. Endocrinol. 349, 111–27.CrossRefGoogle ScholarPubMed
Warzych, E., Peippo, J., Szydlowski, M. & Lechniak, D. (2007). Supplements to in vitro maturation media affect the production of bovine blastocysts and their apoptotic index but not the proportions of matured and apoptotic oocytes. Anim. Reprod. Sci. 97, 334–43.CrossRefGoogle Scholar
Willis, D. & Franks, S. (1995). Insulin action in human granulosa cells from normal and polycystic ovaries is mediated by the insulin receptor and not the type-I insulin-like growth factor receptor. J. Clin. Endocrinol. Metab. 80, 3788–90.CrossRefGoogle Scholar
Wrenzycki, C., Herrmann, D., Carnwath, J.W. & Niemann, H. (1999). Alterations in the relative abundance of gene transcripts in preimplantation bovine embryos cultured in medium supplemented with either serum or PVA. Mol. Reprod. Dev. 53, 8–18.3.0.CO;2-K>CrossRefGoogle ScholarPubMed