Hostname: page-component-78c5997874-m6dg7 Total loading time: 0 Render date: 2024-11-17T14:06:36.725Z Has data issue: false hasContentIssue false
  • English
  • Français

Urea changes oocyte competence and gene expression in resultant bovine embryo in vitro

Published online by Cambridge University Press:  30 April 2018

Rasoul Kowsar Open the ORCID record for Rasoul Kowsar [Opens in a new window] ,
Fatemeh Izadi ,
Nima Sadeghi ,
Ahmad Riasi ,
Faezeh Ghazvini Zadegan ,
Mehdi Hajian ,
Mohammad Hossein Nasr-Esfahani ,
Hossein Farrokhpour  and
Akio Miyamoto
Rasoul Kowsar*
Affiliation:
Department of Animal Science, College of Agriculture, Isfahan University of Technology, Isfahan, 84156-83111, Iran Graduate School of Animal and Food Hygiene, Obihiro University of Agriculture and Veterinary Medicine, Obihiro, Hokkaido 080–8555, Japan
Fatemeh Izadi
Affiliation:
Department of Animal Science, College of Agriculture, Isfahan University of Technology, Isfahan, 84156-83111, Iran
Nima Sadeghi
Affiliation:
FKA, Animal Husbandry and Agriculture Co, Isfahan, Iran
Ahmad Riasi
Affiliation:
Department of Animal Science, College of Agriculture, Isfahan University of Technology, Isfahan, 84156-83111, Iran
Faezeh Ghazvini Zadegan
Affiliation:
Department of Reproductive Biotechnology, Reproductive Biomedicine Research Center, Royan Institute for Biotechnology, ACECR, Isfahan, Iran
Mehdi Hajian
Affiliation:
Department of Reproductive Biotechnology, Reproductive Biomedicine Research Center, Royan Institute for Biotechnology, ACECR, Isfahan, Iran
Mohammad Hossein Nasr-Esfahani*
Affiliation:
Department of Reproductive Biotechnology, Reproductive Biomedicine Research Center, Royan Institute for Biotechnology, ACECR, Isfahan, Iran Department of Embryology, Reproductive Biomedicine Research Center, Royan Institute for Reproductive Biomedicine, ACECR, Tehran, Iran
Hossein Farrokhpour
Affiliation:
Department of Chemistry, Isfahan University of Technology, Isfahan, 84156-83111, Iran.
Akio Miyamoto
Affiliation:
Graduate School of Animal and Food Hygiene, Obihiro University of Agriculture and Veterinary Medicine, Obihiro, Hokkaido 080–8555, Japan
*
All correspondence to: Rasoul Kowsar. Department of Animal Science, College of Agriculture, Isfahan University of Technology, Isfahan, 84156-83111, Iran. E-mail: Rasoul_kowsarzar@yahoo.com
Mohammad Hossein Nasr-Esfahani. Department of Reproductive Biotechnology, Reproductive Biomedicine Research Center, Royan Institute for Biotechnology, ACECR, Isfahan, Iran. E-mail: mh.nasr-esfahani@royaninstitute.org
Get access Rights & Permissions [Opens in a new window]

Summary

Nutrition influences the microenvironment in the proximity of oocyte and affects early embryonic development. Elevated blood urea nitrogen, even in healthy dairy cows, is associated with reduced fertility and there is high correlation between blood urea levels and follicular fluid urea levels. Using a docking calculation (in silico), urea showed a favorable binding activity towards the ZP-N domain of ZP3, that of ZP2, and towards the predicted full-length sperm receptor ZP3. Supplementation of oocyte maturation medium with nutrition-related levels of urea (20 or 40 mg/dl as seen in healthy dairy cows fed on low or high dietary protein, respectively) dose-dependently increased: (i) the proportion of oocytes that remained uncleaved; and (ii) oocyte degeneration; and reduced cleavage, blastocyst and hatching rates. High levels of urea induced shrinkage in oocytes, visualised using scanning electron microscopy. Urea downregulated NANOG while dose-dependently upregulating OCT4, DNMT1, and BCL2 expression. Urea at 20 mg/dl induced BAX expression. Using mathematical modelling, the rate of oocyte degeneration was sensitive to urea levels; while cleavage, blastocyst and hatching rates exhibited negative sensitivity. The present data imply a novel role for urea in reducing oocyte competence and changing gene expression in the resultant embryos.

Keywords

BlastocystBovine oocyteMolecular dockingUrea
Type
Research Article
Information
Zygote , Volume 26 , Issue 3 , June 2018 , pp. 207 - 219
Copyright
Copyright © Cambridge University Press 2018 

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

Arnold, S.J. & Robertson, E.J. (2009). Making a commitment: cell lineage allocation and axis patterning in the early mouse embryo. Nat. Rev. Mol. Cell Biol. 10, 91–103.Google Scholar
Barzegar, A., Mansouri, A. & Azamat, J. (2016). Molecular dynamics simulation of non-covalent single-walled carbon nanotube functionalization with surfactant peptides. J. Mol. Graph. Model. 64, 75–84.Google Scholar
Berg, D.K., Smith, C.S., Pearton, D.J., Wells, D.N., Broadhurst, R., Donnison, M. & Pfeffer, P.L. (2011). Trophectoderm lineage determination in cattle. Dev. Cell 20, 244–55.Google Scholar
Biniszkiewicz, D., Gribnau, J., Ramsahoye, B., Gaudet, F., Eggan, K., Humpherys, D., Mastrangelo, M.A., Jun, Z., Walter, J. & Jaenisch, R. (2002). Dnmt1 overexpression causes genomic hypermethylation, loss of imprinting, and embryonic lethality. Mol. Cell. Biol. 22, 2124–35.Google Scholar
Boyer, L.A., Lee, T.I., Cole, M.F., Johnstone, S.E., Levine, S.S., Zucker, J.P., Guenther, M.G., Kumar, R.M., Murray, H.L., Jenner, R.G., Gifford, D.K., Melton, D.A., Jaenisch, R. & Young, R.A. (2005). Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 122, 947–56.Google Scholar
Butler, W., Calaman, J. & Beam, S. (1996). Plasma and milk urea nitrogen in relation to pregnancy rate in lactating dairy cattle. J. Anim. Sci. 74, 858–65.Google Scholar
Caflisch, A. & Karplus, M. (1999). Structural details of urea binding to barnase: a molecular dynamics analysis. Structure 7, 477–88.Google Scholar
Callebaut, I., Mornon, J.P. & Monget, P. (2007). Isolated ZP-N domains constitute the N-terminal extensions of zona pellucida proteins. Bioinformatics 23, 1871–74.Google Scholar
Cebrian-Serrano, A., Salvador, I., García-Roselló, E., Pericuesta, E., Pérez-Cerezales, S., Gutierrez-Adán, A., Coy, P. & Silvestre, M.A. (2013). Effect of the bovine oviductal fluid on in vitro fertilization, development and gene expression of in vitro produced bovine blastocysts. Reprod. Dom. Anim. 48, 331–8.Google Scholar
De Wit, A., Cesar, M. & Kruip, T. (2001). Effect of urea during in vitro maturation on nuclear maturation and embryo development of bovine cumulus–oocyte-complexes. J. Dairy Sci. 84, 1800–4.Google Scholar
Ferguson, J.D., Galligan, D.T., Blanchard, T. & Reeves, M. (1993). Serum urea nitrogen and conception rate: the usefulness of test information. J. Dairy Sci. 76, 3742–46.Google Scholar
Fortune, J. (1994). Ovarian follicular growth and development in mammals. Biol. Reprod. 50, 225–32.Google Scholar
Giraldo, A.M., DeCourcy, K., Ball, S.F., Hylan, D. & Ayares, D.L. (2013). Gene expression of Dnmt1 isoforms in porcine oocytes, embryos, and somatic cells. Cell. Reprogram. 15, 309–21.Google Scholar
Glinos, A., Bardi, G., Dermitzaki, K., Perez, S.A. & Talieri, M.J. (1983). Cytokinetic and cytotoxic effects of urea on Hela cells in suspension cultures. J. Natl. Cancer Inst. 71, 1211–19.Google Scholar
Gook, D.A., Edgar, D.H., Borg, J. & Martic, M. (2008). Detection of zona pellucida proteins during human Folliculogenesis. Hum. Reprod. 23, 394–402.CrossRefGoogle ScholarPubMed
Green, M.P., Harvey, A.J., Spate, L.D., Kimura, K., Thompson, J.G. & Roberts, R.M. (2016). The effects of 2, 4-dinitrophenol and d-glucose concentration on the development, sex ratio, and interferon-tau (IFNT) production of bovine blastocysts. Mol. Reprod. Dev. 83, 50–60.CrossRefGoogle ScholarPubMed
Grohmann, M., Spada, F., Schermelleh, L., Alenina, N., Bader, M., Cardoso, M.C. & Leonhardt, H. (2005). Restricted mobility of Dnmt1 in preimplantation embryos: implications for epigenetic reprogramming. BMC Dev. Biol. 5, 18.Google Scholar
Hammon, D., Holyoak, G. & Dhiman, T. (2005). Association between blood plasma urea nitrogen levels and reproductive fluid urea nitrogen and ammonia concentrations in early lactation dairy cows. Anim. Reprod. Sci. 86, 195–204.Google Scholar
Han, L., Monné, M., Okumura, H., Schwend, T, Cherry, A.L., Flot, D., Matsuda, T. & Jovine, L. (2010). Insights into egg coat assembly and egg-sperm interaction from the X-ray structure of full-length ZP3. Cell 143, 404–15.Google Scholar
Hernandez-Ledezma, J.J., Sikes, J.D., Murphy, C.N., Watson, A.J., Schultz, G.A. & Roberts, R.M. (1992). Expression of bovine trophoblast interferon in conceptuses derived by in vitro techniques. Biol. Reprod. 47, 374–80.Google Scholar
Hua, L., Zhou, R., Thirumalai, D. & Berne, B.J. (2008). Urea denaturation by stronger dispersion interactions with proteins than water implies a 2-stage unfolding. PNAS. 105, 16928–33.Google Scholar
Ibrahim, S., Salilew-Wondim, D., Rings, F., Hoelker, M., Neuhoff, C., Tholen, E., Looft, C., Schellander, K. & Tesfaye, D. (2015). Expression pattern of inflammatory response genes and their regulatory microRNAs in bovine oviductal cells in response to lipopolysaccharide: implication for early embryonic development. PLoS One 10, e0119388.Google Scholar
Jovine, L., Janssen, W.G., Litscher, E.S. & Wassarman, P.M. (2006) The PLAC1-homology region of the ZP domain is sufficient for protein polymerisation. BMC Biochem. 7, 11.Google Scholar
Józwik, M., Józwik, M., Teng, C. & Battaglia, F.C. (2006). Amino acid, ammonia and urea concentrations in human pre-ovulatory ovarian follicular fluid. Hum. Reprod. 21, 2776–82.Google Scholar
Jusman, Y., Ng, S.C. & Abu Osman, N.A. (2014). Investigation of CPD and HMDS sample preparation techniques for cervical cells in developing computer-aided screening system based on FE-SEM/EDX. Sci. World J. 2014, https://doi.org/10.1155/2014/289817.Google Scholar
Kalmar, T., Lim, C., Hayward, P., Muñoz-Descalzo, S., Nichols, J., Garcia-Ojalvo, J. & Martinez Arias, A. (2009). Regulated fluctuations in nanog expression mediate cell fate decisions in embryonic stem cells. PLoS Biol. 7, e1000149.Google Scholar
Khan, D.R., Dubé, D., Gall, L., Peynot, N., Ruffini, S., Laffont, L., Le Bourhis, D., Degrelle, S., Jouneau, A. & Duranthon, V. (2012). Expression of pluripotency master regulators during two key developmental transitions: EGA and early lineage specification in the bovine embryo. PLoS ONE 7, e34110.Google Scholar
Kim, S.J., Koo, O.J., Park, H.J., Moon, J.H., da Torre, B.R., Javaregowda, P.K., Kang, J.T., Park, S.J., Saadeldin, I.M., Choi, J.Y., Lee, B.C. & Jang, G. (2015). Oct4 overexpression facilitates proliferation of porcine fibroblasts and development of cloned embryos. Zygote 23, 704–11.Google Scholar
Kimura, K., Spate, L.D., Green, M.P. & Roberts, R.M. (2004). Effects of oxidative stress and inhibitors of the pentose phosphate pathway on sexually dimorphic production of IFN-τ by bovine blastocysts. Mol. Reprod. Dev. 68, 88–95.Google Scholar
Kowsar, R., Marey, M.A., Shimizu, T. & Miyamoto, A. (2016). Urea induces T helper 2 (Th2) type environment at transcriptional level and prostaglandin E2 secretion in bovine oviduct epithelial cells in culture. J. Dairy Sci. 99, 5844–50.Google Scholar
Koyama, K., Hasegawa, A., Inoue, M. & Isojima, S. (1991). Blocking of human sperm-zona interaction by monoclonal antibodies to a glycoprotein family (ZP4) of porcine zona pellucida. Biol. Reprod. 45, 727–35.Google Scholar
Leibfried, L. & First, N. (1979). Characterization of bovine follicular oocytes and their ability to mature in vitro. J. Anim. Sci. 48, 76–86.Google Scholar
Li, E., Beard, C. & Jaenisch, R. (1993). Role for DNA methylation in genomic imprinting. Nature 366, 362–65.Google Scholar
Madeja, Z.E., Sosnowski, J., Hryniewicz, K., Warzych, E., Pawlak, P., Rozwadowska, N., Plusa, B. & Lechniak, D. (2013). Changes in sub-cellular localisation of trophoblast and inner cell mass specific transcription factors during bovine preimplantation development. BMC Dev. Biol. 13, 32.Google Scholar
Makita, M., Ueda, M. & Miyano, T. (2016). The fertilization ability and developmental competence of bovine oocytes grown in vitro. J. Reprod. Dev. 62, 379–84.Google Scholar
Matoba, S., Bender, K., Fahey, A.G., Mamo, S., Brennan, L., Lonergan, P. & Fair, T. (2014). Predictive value of bovine follicular components as markers of oocyte developmental potential. Reprod. Fertil. Dev. 26, 337–45.Google Scholar
Messerschmidt, D.M., Knowles, B.B. & Solter, D. (2014). DNA methylation dynamics during epigenetic reprogramming in the germline and preimplantation embryos. Gene. Dev. 28, 812–28.Google Scholar
Mitsui, K., Tokuzawa, Y., Itoh, H., Segawa, K., Murakami, M., Takahashi, K., Maruyama, M., Maeda, M. & Yamanaka, S. (2003). The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell 113, 631–42.Google Scholar
Monné, M., Han, L., Schwend, T., Burendahl, S. & Jovine, L. (2008). Crystal structure of the ZP-N domain of ZP3 reveals the core fold of animal egg coats. Nature 456, 653–59.Google Scholar
Morris, G.M., Huey, R., Lindstrom, W., Sanner, M.F., Belew, R.K., Goodsell, D.S. & Olson, A.J. (2009). AutoDock4 and AutoDockTools4: Automated docking with selective receptor flexibility. J. Comput. Chem. 30, 2785–91.Google Scholar
Moulavi, F., Hosseini, S., Hajian, M., Forouzanfar, M., Abedi, P., Ostadhosseini, S., Asgari, V. & Nasr-Esfahani, M.H. (2013). Nuclear transfer technique affects mRNA abundance, developmental competence and cell fate of the reconstituted sheep oocytes. Reproduction 145, 345–55.Google Scholar
Muñoz-Descalzo, S., Rué, P., Garcia-Ojalvo, J. & Martinez Arias, A. (2012). Correlations between the levels of oct4 and nanog as a signature for naive pluripotency in mouse embryonic stem cells. Stem Cells 30, 2683–91.Google Scholar
Nagano, M., Katagiri, S. & Takahashi, Y. (2006). Relationship between bovine oocyte morphology and in vitro developmental potential. Zygote 14, 53–61.Google Scholar
Ogony, J.W., Malahias, E., Vadigepalli, R. & Anni, H. (2013). Ethanol alters the balance of Sox2, Oct4, and Nanog expression in distinct subpopulations during differentiation of embryonic stem cells. Stem Cells Dev. 22, 2196–2210.Google Scholar
Pimenta, J., Sardinha, J., Marques, C.C., Domingos, A., Baptista, M.C., Barbas, J.P., Martins, I.C., Mesquita, P., Pessa, P., Soares, R., Viegas, A., Cabrita, E., Horta, E.M., Fontes, C.A., Prates, A.M. & Pereira, M.L. (2013). Inhibition of ovine in vitro fertilization by anti-Prt antibody: hypothetical model for Prt/ZP interaction. Reprod. Biol. Endocrinol. 11, 25.Google Scholar
Revelli, A., Piane, L.D., Casano, S., Molinari, E., Massobrio, M. & Rinaudo, P. (2009). Follicular fluid content and oocyte quality: from single biochemical markers to metabolomics. Reprod. Biol. Endocrinol. 7, 40.Google Scholar
Roy, A., Kucukural, A. & Zhang, Y. (2010). I-TASSER: a unified platform for automated protein structure and function prediction. Nat. Protoc. 5, 725–38.Google Scholar
Sánchez-Alvarez, R., Gayen, S., Vadigepalli, R. & Anni, H. (2013). Ethanol diverts early neuronal differentiation trajectory of embryonic stem cells by disrupting the balance of lineage specifiers. PLoS ONE 8, e63794.Google Scholar
Santos, P., Marques, A., Antunes, G., Chaveiro, A., Andrade, M., Borba, A. & da Silva, F.M. (2009). Effects of plasma urea nitrogen levels on the bovine oocyte ability to develop after in vitro fertilization. Reprod. Dom. Anim. 44, 783–87.Google Scholar
Sinclair, K., Kuran, M., Gebbie, F., Webb, R. & McEvoy, T.G. (2000). Nitrogen metabolism and fertility in cattle: II. Development of oocytes recovered from heifers offered diets differing in their rate of nitrogen release in the rumen. J. Anim. Sci. 78, 2670–80.Google Scholar
Son, W.Y., Lee, S.Y. & Lim, J.H. (2005). Fertilization, cleavage and blastocyst development according to the maturation timing of oocytes in in vitro maturation cycles. Hum. Reprod. 20, 3204–07.Google Scholar
Theunissen, T.W., van Oosten, A.L., Castelo-Branco, G., Hall, J., Smith, A. & Silva, J.C. (2011). Nanog overcomes reprogramming barriers and induces pluripotency in minimal conditions. Curr. Biol. 21, 65–71.Google Scholar
Tosti, E. (2006). Calcium ion currents mediating oocyte maturation events. Reprod. Biol. Endocrinol. 4, 26.Google Scholar
Wagner, C.A., Huber, S.M., Wärntges, S., Zempel, G., Kaba, N.K., Fux, R., Orth, N., Busch, G.L., Waldegger, S., Lambert, I., Nilius, B., Heinle, H. & Lang, F. (2000). Effect of urea and osmotic cell shrinkage on Ca2+ entry and contraction of vascular smooth muscle cells. Pflugers Arch. 440, 295–301.Google Scholar
Wang, H., Miyazaki, J. & Smith, A.G. (2000). Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nat. Genet. 24, 372–76.Google Scholar
Wassarman, P.M. (2008). Zona pellucida glycoproteins. J. Biol. Chem. 283, 24285–89.Google Scholar
Wassarman, P.M., Chen, J., Cohen, N., Litscher, E., Liu, C., Qi, H. & Williams, Z. (1999). Structure and function of the mammalian egg zona pellucida. J. Exp. Zool. Part B: Mol. Dev. Evol. 285, 251–8.Google Scholar
Zeuthen, T. & MacAulay, N. (2012). Cotransport of water by Na+–K+–2Cl− cotransporters expressed in Xenopus oocytes: NKCC1 versus NKCC2. J. Physiol. 590, 1139–54.Google Scholar
Zhang, Y. (2007). Template-based modelling and free modelling by I-TASSER in CASP7. Proteins 69, 108–117.Google Scholar