Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-29T02:05:16.396Z Has data issue: false hasContentIssue false

Modulation of phosphatidylinositol 3-kinase activity during in vitro oocyte maturation increases the production of bovine blastocysts

Published online by Cambridge University Press:  03 August 2020

Janaína Leite Pereira
Affiliation:
Laboratório de Reprodução e Melhoramento Genético Animal, Centro de Ciências e Tecnologias Agropecuárias, Universidade Estadual do Norte Fluminense Darcy Ribeiro, Avenida Alberto Lamego, 2000, CEP: 28013-602. Campos dos Goytacazes, Rio de Janeiro, Brazil
Alinne Glória Curcio
Affiliation:
Laboratório de Reprodução e Melhoramento Genético Animal, Centro de Ciências e Tecnologias Agropecuárias, Universidade Estadual do Norte Fluminense Darcy Ribeiro, Avenida Alberto Lamego, 2000, CEP: 28013-602. Campos dos Goytacazes, Rio de Janeiro, Brazil
Laura Mathias Barroso
Affiliation:
Laboratório de Reprodução e Melhoramento Genético Animal, Centro de Ciências e Tecnologias Agropecuárias, Universidade Estadual do Norte Fluminense Darcy Ribeiro, Avenida Alberto Lamego, 2000, CEP: 28013-602. Campos dos Goytacazes, Rio de Janeiro, Brazil
Edgar Mauricio Mogollón-Waltero
Affiliation:
Laboratório de Reprodução e Melhoramento Genético Animal, Centro de Ciências e Tecnologias Agropecuárias, Universidade Estadual do Norte Fluminense Darcy Ribeiro, Avenida Alberto Lamego, 2000, CEP: 28013-602. Campos dos Goytacazes, Rio de Janeiro, Brazil
Helga Fernandes Gomes
Affiliation:
Laboratório de Reprodução e Melhoramento Genético Animal, Centro de Ciências e Tecnologias Agropecuárias, Universidade Estadual do Norte Fluminense Darcy Ribeiro, Avenida Alberto Lamego, 2000, CEP: 28013-602. Campos dos Goytacazes, Rio de Janeiro, Brazil
Roger Cardoso Maia
Affiliation:
Laboratório de Reprodução e Melhoramento Genético Animal, Centro de Ciências e Tecnologias Agropecuárias, Universidade Estadual do Norte Fluminense Darcy Ribeiro, Avenida Alberto Lamego, 2000, CEP: 28013-602. Campos dos Goytacazes, Rio de Janeiro, Brazil
Kelen Salaroli Viana
Affiliation:
Laboratório de Reprodução e Melhoramento Genético Animal, Centro de Ciências e Tecnologias Agropecuárias, Universidade Estadual do Norte Fluminense Darcy Ribeiro, Avenida Alberto Lamego, 2000, CEP: 28013-602. Campos dos Goytacazes, Rio de Janeiro, Brazil
Maria Clara Caldas Bussiere
Affiliation:
Laboratório de Reprodução e Melhoramento Genético Animal, Centro de Ciências e Tecnologias Agropecuárias, Universidade Estadual do Norte Fluminense Darcy Ribeiro, Avenida Alberto Lamego, 2000, CEP: 28013-602. Campos dos Goytacazes, Rio de Janeiro, Brazil
Diego Fernando Dubeibe Marin
Affiliation:
Laboratório de Reprodução e Melhoramento Genético Animal, Centro de Ciências e Tecnologias Agropecuárias, Universidade Estadual do Norte Fluminense Darcy Ribeiro, Avenida Alberto Lamego, 2000, CEP: 28013-602. Campos dos Goytacazes, Rio de Janeiro, Brazil
Angelo José Burla Dias*
Affiliation:
Laboratório de Reprodução e Melhoramento Genético Animal, Centro de Ciências e Tecnologias Agropecuárias, Universidade Estadual do Norte Fluminense Darcy Ribeiro, Avenida Alberto Lamego, 2000, CEP: 28013-602. Campos dos Goytacazes, Rio de Janeiro, Brazil
*
Author for correspondence: Angelo José Burla Dias. Avenida Alberto Lamego, 2000. CEP: 28013-602. Campos dos Goytacazes, Rio de Janeiro, Brazil. Tel: +55 22 27397285. E-mail: [email protected]

Summary

This study aimed to evaluate the effect of regulating phosphatidylinositol 3-kinase (PI3K) activity on the kinetics of oocyte nuclear maturation and the blastocyst rate. To evaluate oocyte viability, nuclear maturation rate and in vitro embryo production, cumulus–oocyte complexes (COCs) were maintained for 0, 10 min, 6 h or 22 h in TCM 199 medium supplemented with 20 nM wortmannin, an inhibitor of PI3K. After each period, COCs were transferred to the same medium without wortmannin and kept under the same conditions until completion of 22 h of in vitro maturation (IVM). To evaluate the effect of time on progression of nuclear maturation, COCs cultivated with 20 nM wortmannin was maintained for 22, 28 or 34 h of IVM. To determine the effect of wortmannin on the activity of maturation-promoting factor (MPF), COCs were kept under IVM conditions in the presence of the inhibitor for 0, 1, 3, 6, or 8 h. Exposure of COCs to wortmannin decreased (P < 0.05) the percentage of oocytes that reached metaphase II (MII) up to 22 h, MPF activity and reduced PI3K activity by 30%. However, after 28 and 34 h, 70% of oocytes reached the MII stage in the presence of inhibitor Moreover, COCs matured in the presence of wortmannin showed an increase (P < 0.05) in the blastocyst rate. These findings suggested that the regulation of the PI3K activity during IVM of bovine COCs interfered with the meiotic progression due to control of MPF activity, positively affecting the blastocyst rate.

Type
Research Article
Copyright
© Cambridge University Press 2020

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

Albuz, FK, Sasseville, M, Lane, M, Armstrong, DT, Thompson, JG and Gilchrist, RB (2010). Simulated physiological oocyte maturation (SPOM): a novel in vitro maturation system that substantially improves embryo yield and pregnancy out comes. Hum Reprod 25, 29993011.CrossRefGoogle Scholar
Anas, MKI, Shimada, M and Terada, T (1997). Possible role for phosphatidylinositol 3-kinase in regulation meiotic maturation of bovine oocytes in vitro. Theriogenology 50, 347–56.CrossRefGoogle Scholar
Anas, MKI, Shojo, A, Shimada, M and Terada, T (2000). Effects of wortmannin on the kinetics of GVBD and the activities of the maturation promoting factor and mitogen-activated protein kinase during bovine oocyte maturation in vitro. Theriogenology 53, 1797–806.CrossRefGoogle ScholarPubMed
Bilodeau-Goessels, S (2011). Cows are not mice: the role of cyclic amp, phosphodiesterases, and adenosine monophosphate-activated protein kinase in the maintenance of meiotic arrest in bovine oocytes. Mol Reprod Dev 78, 734–43.CrossRefGoogle Scholar
Bilodeau-Goeseels, S (2012). Bovine oocyte meiotic inhibition before in vitro maturation and its value to in vitro embryo production. Does it improve developmental competence? Reprod Domest Anim 47, 687–93.CrossRefGoogle ScholarPubMed
Bozzo, SRetamal, C (1991). Geles unidimensionales. Unnuevo método densitometrico para computadores personales. Arch Biol Med Exp 24, 181.Google Scholar
Brunet, S and Maro, B (2005). Cytoskeleton and cell cycle control during meiotic maturation of the mouse oocyte: integrating time and space. Reproduction 130, 801–11.CrossRefGoogle ScholarPubMed
Carnero, A and Lacal, JC (1998). Wortmannin, an inhibitor of phosphatidyl-inositol 3-kinase, induces oocyte maturation through a MPF-MAPK-dependent pathway. FEBS Lett 422, 155–9.CrossRefGoogle ScholarPubMed
Carvalheira, JBC, Zecchin, HG and Saad, MJA (2002). Vias de Sinalização da Insulina. Arq Bras Endocrinol Metabol 46, 419–25.CrossRefGoogle Scholar
Chaves, RN, Duarte, ABG, Matos, MHT and Figueiredo, JR (2010). Systems in vitro development of immature oocytes of mammalians. Rev Bras Reprod Anim 34, 3749.Google Scholar
Conti, M, Andersen, CB, Richard, F, Mehats, C, Chuns, Y, Horner, K, Jin, C and Tsafriri, A (2002). Role of cyclic nucleotide signaling in oocyte maturation. Mol Cell Endocrinol 187, 153–9.CrossRefGoogle ScholarPubMed
Conti, M, Hsieh, M, Zamah, AM and Oh, JS (2012). Novel signaling mechanisms in the ovary during oocyte maturation and ovulation. Mol Cell Endocrinol 356, 6573.CrossRefGoogle ScholarPubMed
Das, D, Khan, PP and Maitra, S (2013). Participation of PI3-Kinase/Akt signaling in insulin stimulation of p34cdc2 activation in zebrafish oocyte: phosphodiesterase 3 as a potential downstream target. Mol Cell Endocrinol 374, 4655.CrossRefGoogle ScholarPubMed
De Loss, F, Van Vliet, C, Van Maurik, P and Kruip, TA (1989). Morphology of immature bovine oocytes. Mol Reprod Dev 24, 197204.Google Scholar
Dekel, N (2005). Cellular, biochemical and molecular mechanisms regulating oocyte maturation. Mol Cell Endocrinol 234, 1925.CrossRefGoogle ScholarPubMed
Falasca, M (2010). PI3K/Akt signalling pathway specific inhibitors: a novel strategy to sensitize cancer cells to anti-cancer drugs. Curr Pharm Design 16, 1410–6.CrossRefGoogle ScholarPubMed
Ferreira, EM, Vireque, AA, Adona, PR, Meirelles, FV, Ferriani, RA and Navarro, PAAS (2009). Cytoplasmic maturation of bovine oocytes: structural and biochemical modifications and acquisition of developmental competence. Theriogenology 71, 836–48.CrossRefGoogle ScholarPubMed
Gomes, HF (2010). Influência da via de sinalização por insulina na maturação e desenvolvimento embrionário inicial em bovinos (Doctoral dissertation), Universidade Estadual do Norte Fluminense Darcy Ribeiro (UENF), Rio de Janeiro, Brazil.Google Scholar
Han, S, Vaccari, S, Nedachi, T, Andersen, C, Kovacina, K, Roth, R and Conti, M (2006). Protein kinase B/Akt phosphorylation of PDE3A and its role in mammalian oocyte maturation. EMBO J 25, 5716–25.CrossRefGoogle ScholarPubMed
Heald, R and Mckeon, F (1990). Mutations of phosphorylation sites in lamin A that prevent nuclear lamina disassembly in mitosis. Cell 61, 579–89.CrossRefGoogle Scholar
Katz-Jaffe, MG, Mccallie, BR, Preis, KA, Filipovits, J and Gardner, DK (2009). Transcriptome analysis of in vivo and in vitro matured bovine MII oocytes. Theriogenology 71, 939946.CrossRefGoogle ScholarPubMed
Liu, Y, Jiang, N, Wu, J and Rosenblum, JS (2007). Polo-like kinases inhibited by wortmannin. J Biol Chem 282, 25052511.CrossRefGoogle ScholarPubMed
Lonergan, P, Khatir, H, Carolan, C and Mermillod, P (1997). Bovine blastocyst production in vitro after inhibition of oocyte meiotic resumption for 24 h. J Reprod Fertil 109, 355365.CrossRefGoogle ScholarPubMed
Lonergan, P, Fair, T, Khatir, H, Cesaroni, G and Mermillod, P (1998). Effect of protein synthesis inhibition before or during in vitro maturation on subsequent development of bovine oocytes. Theriogenology 50, 417431.CrossRefGoogle ScholarPubMed
Lonergan, P, Faerge, I, Hyttel, PM, Boland, M and Fair, T (2003). Ultrastructural modifications in bovine oocytes maintained in meiotic arrest in vitro using roscovitine or butyrolactone. Mol Reprod Dev 64, 369378.CrossRefGoogle ScholarPubMed
Luciano, AM, Pocar, P, Milanesi, E, Modina, S, Rieger, D, Lauria, A and Gandolfi, F (1999). Effect of different levels of intracellular cAMP on the in vitro maturation of cattle oocytes and their subsequent development following in vitro fertilization. Mol Reprod Dev 54, 8691.3.0.CO;2-C>CrossRefGoogle ScholarPubMed
Manning, BD and Toker, A (2017). AKT/PKB Signaling: navigating the network. Cell 169, 381405.CrossRefGoogle ScholarPubMed
Mehlmann, LM (2005). Stopsand starts in mammalian oocytes: recent advances in understanding the regulation of meiotic arrest and oocyte maturation. Reproduction 130, 791–9.CrossRefGoogle ScholarPubMed
Mermillod, P, Tomanek, M, Marchal, R and Meijer, L (2000). High developmental competence of cattle oocytes maintained at the germinal vesicle stage for 24 hours in culture by specific inhibition of MPF kinase activity. Mol Reprod Dev 55, 8995.3.0.CO;2-M>CrossRefGoogle ScholarPubMed
Mogollón-Waltero, EM (2013). Inibição da fosfatidilinositol3quinase (PI3K) na maturação in vitro de oócitos bovinos (Doctoral dissertation), Universidade Estadual do Norte Fluminense Darcy Ribeiro (UENF), Rio de Janeiro, Brazil.Google Scholar
Mogollón-Waltero, EM, Dias, AJB, Gomes, HF, Dubeibe, DF, Maia, RC and Viana, KS (2015). Effect of wortmannin in vitro maturation of bovine oocytes. Reprod Fertil Dev 27, 175.CrossRefGoogle Scholar
Murray, AW and Kirschner, MW (1989). Cyclin synthesis drives the early embryonic cell cycle. Nature 6222, 275–80.CrossRefGoogle Scholar
Nogueira, D, Cortvrindt, R, De Matos, DG, Vanhoutte, L and Smitz, J (2003). Effect of phosphodiesterase type 3 inhibitor on developmental competence of immature mouse oocytes in vitro. Biol Reprod 69, 2045–52.CrossRefGoogle ScholarPubMed
Richard, FJ (2007). Regulation of meiotic maturation. J Anim Sci 85, E46.CrossRefGoogle ScholarPubMed
Rizos, D, Ward, F, Duffy, P, Boland, M and Lonergan, P (2002). Consequences of bovine oocyte maturation, fertilization or early embryo development in vitro versus in vivo: implications for blastocyst yield and blastocyst quality. Mol Reprod Dev 61, 234–68.CrossRefGoogle ScholarPubMed
Salhab, M, Dhorne-Pollet, S, Auclair, S and Guyader-Joly, C (2013). In vitro maturation of oocytes alters gene expression and signaling pathways in bovine cumulus cells. Mol Reprod Dev 80, 116–82.CrossRefGoogle ScholarPubMed
SAS®, Statistical Analysis System (2009). SAS/STAT User´s Guide. Version 9.2. Cary, NC: SAS Institute Incorporation.Google Scholar
Schmitt, A and Nebreda, AR (2002). Signalling pathways in oocyte meiotic maturation. J Cell Sci 115, 2457–9.Google ScholarPubMed
Sirard, MA, Florman, HM, Leibfried-Rutledge, ML, Barnes, FL, Sims, ML and First, NL (1989). Timing of nuclear progression and protein synthesis necessary for meiotic maturation of bovine oocytes. Biol Reprod 40, 1257–63.CrossRefGoogle ScholarPubMed
Sirard, MA, Dufort, I, Coenen, K, Massicote, L and Robert, C (2003). The use of genomics and proteomics to understand oocyte and early embryo functions in farm animals. Reproduction 61, 117229.Google ScholarPubMed
Thompson, PE, Manganiello, V and Degerman, E (2007). Re-discovering PDE3 inhibitors-new opportunities for a long neglected target. Curr Topics Med Chem 7, 421–36.CrossRefGoogle ScholarPubMed
Ward, GE and Kirschner, MW (1990). Identification of cell cycle-regulated phosphorylation sites on nuclear lamin C. Cell 4, 561–77.CrossRefGoogle Scholar
Yu, JSL and Cu, W (2016). Proliferation, survival and metabolism: the role of PI3K/AKT/ mTOR signalling in pluripotency and cell fate determination. Development 143, 3050–60.CrossRefGoogle ScholarPubMed