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Effect of butafosfan supplementation during oocyte maturation on bovine embryo development

Published online by Cambridge University Press:  15 August 2019

Lucas Teixeira Hax ,
Joao Alveiro Alvarado Rincón Open the ORCID record for Joao Alveiro Alvarado Rincón [Opens in a new window] ,
Augusto Schneider ,
Lígia Margareth Cantarelli Pegoraro ,
Letícia Franco Collares ,
Rubens Alves Pereira ,
Jorgea Pradieé ,
Francisco Augusto Burket Del Pino  and
Marcio Nunes Corrêa
Lucas Teixeira Hax
Affiliation:
Universidade Federal de Pelotas, Pelotas, RS, 96010-000, Brazil
Joao Alveiro Alvarado Rincón
Affiliation:
Universidade Federal de Pelotas, Pelotas, RS, 96010-000, Brazil
Augusto Schneider
Affiliation:
Universidade Federal de Pelotas, Pelotas, RS, 96010-000, Brazil
Lígia Margareth Cantarelli Pegoraro
Affiliation:
Empresa Brasileira de Pesquisa Agropecuária, Pelotas, RS, 96010-971, Brazil
Letícia Franco Collares
Affiliation:
Universidade Federal de Pelotas, Pelotas, RS, 96010-000, Brazil
Rubens Alves Pereira
Affiliation:
Laboratório Ibasa, Porto Alegre, RS, 90220-030, Brazil
Jorgea Pradieé
Affiliation:
Universidade Federal de Pelotas, Pelotas, RS, 96010-000, Brazil
Francisco Augusto Burket Del Pino
Affiliation:
Universidade Federal de Pelotas, Pelotas, RS, 96010-000, Brazil
Marcio Nunes Corrêa*
Affiliation:
Universidade Federal de Pelotas, Pelotas, RS, 96010-000, Brazil
*
Address for correspondence: Marcio Nunes Corrêa, Departamento de Clínicas Veterinária, Universidade Federal de Pelotas, Campus capão do Leão, CEP: 96010–000 Pelotas, RS – Brazil. Tel: +55 53 32757136. E-mail: márcio.nunescorrea@gmail.com
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Summary

Around 60–80% of oocytes maturated in vivo reached competence, while the proportion of maturation in vitro is rarely higher than 40%. In this sense, butafosfan has been used in vivo to improve metabolic condition of postpartum cows, and can represent an alternative to increase reproductive efficiency in cows. The aim of this study was to evaluate the addition of increasing doses of butafosfan during oocyte maturation in vitro on the initial embryo development in cattle. In total, 1400 cumulus–oocyte complexes (COCs) were distributed in four groups and maturated according to supplementation with increasing concentrations of butafosfan (0 mg/ml, 0.05 mg/ml, 0.1 mg/ml and 0.2 mg/ml). Then, 20 oocytes per group were collected to evaluate nuclear maturation and gene expression on cumulus cells and oocytes and the remaining oocytes were inseminated and cultured until day 7, when blastocysts were collected for gene expression analysis. A dose-dependent effect of butafosfan was observed, with decrease of cleavage rate and embryo development with higher doses. No difference between groups was observed in maturation rate and expression of genes related to oocyte quality. Our results suggest that butafosfan is prejudicial for oocytes, compromising cleavage and embryo development.

Keywords

BlastocystCattleGene expressionOocyte competencePhosphorus
Type
Research Article
Information
Zygote , Volume 27 , Issue 5 , October 2019 , pp. 321 - 328
Copyright
© Cambridge University Press 2019 

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References

Andrade, JC, Oliveira, MA, Lima, PF, Santos Filho, AS and Pina, VM (2002) Use of steroid hormone treatments prior to superovulation in Nelore donors. Anim Reprod Sci 69, 9–14.CrossRefGoogle ScholarPubMed
Ashkenazi, H, Cao, X, Motola, S, Popliker, M, Conti, M and Tsafriri, A (2005) Epidermal growth factor family members: endogenous mediators of the ovulatory response. Endocrinology 146, 77–84.CrossRefGoogle ScholarPubMed
Assou, S, Haouzi, D, Mahmoud, K, Aouacheria, A, Guillemin, Y, Pantesco, V, Reme, T, Dechaud, H, De Vos, J and Hamamah, S (2008) A non-invasive test for assessing embryo potential by gene expression profiles of human cumulus cells: a proof of concept study. Mol Hum Reprod 14, 711–9.CrossRefGoogle ScholarPubMed
Augustin, R, Pocar, P, Navarrete-Santos, A, Wrenzycki, C, Gandolfi, F, Niemann, H and Fischer, B (2001) Glucose transporter expression is developmentally regulated in in vitro derived bovine preimplantation embryos. Mol Reprod Dev 60, 370–6.CrossRefGoogle ScholarPubMed
Belloc, E, Pique, M and Mendez, R (2008) Sequential waves of polyadenylation and deadenylation define a translation circuit that drives meiotic progression. Biochem Soc Trans 36, 665–70.CrossRefGoogle ScholarPubMed
Berg, JM, Tymoczko, JL and Stryer, L (2006) Glycolysis and gluconeogenesis. In Biochemistry WH Freeman and Co., New York, pp. 433–74.Google Scholar
Boruszewska, D, Sinderewicz, E, Kowalczyk-Zieba, I, Grycmacher, K and Woclawek-Potocka, I (2015) The effect of lysophosphatidic acid during in vitro maturation of bovine cumulus–oocyte complexes: cumulus expansion, glucose metabolism and expression of genes involved in the ovulatory cascade, oocyte and blastocyst competence. Reprod Biol Endocrinol 13, 44.CrossRefGoogle ScholarPubMed
Campos, FT, Rincon, JAA, Acosta, DAV, Silveira, PAS, Pradieé, J, Correa, MN, Gasperin, BG, Pfeifer, LFM, Barros, CC, Pegoraro, LMC and Schneider, A (2017) The acute effect of intravenous lipopolysaccharide injection on serum and intrafollicular HDL components and gene expression in granulosa cells of the bovine dominant follicle. Theriogenology 89, 244–9.CrossRefGoogle ScholarPubMed
Cetica, P, Pintos, L, Dalvit, G and Beconi, M (2002) Activity of key enzymes involved in glucose and triglyceride catabolism during bovine oocyte maturation in vitro. Reproduction 124, 675–81.CrossRefGoogle ScholarPubMed
Cetica, PD, Pintos, LN, Dalvit, GC and Beconi, MT (1999) Effect of lactate dehydrogenase activity and isoenzyme localization in bovine oocytes and utilization of oxidative substrates on in vitro maturation. Theriogenology 51, 541–50.CrossRefGoogle ScholarPubMed
Colgan, DF, Murthy, KG, Prives, C and Manley, JL (1996) Cell-cycle related regulation of poly(A) polymerase by phosphorylation. Nature 384, 282–5.CrossRefGoogle ScholarPubMed
Combelles, CM, Cekleniak, NA, Racowsky, C and Albertini, DF (2002) Assessment of nuclear and cytoplasmic maturation in in-vitro matured human oocytes. Hum Reprod 17, 1006–16.CrossRefGoogle ScholarPubMed
Cunningham, JG (2002) Textbook of Veterinary Physiology, 3rd edn, WB Saunders Co, Philadelphia, USA.Google Scholar
Dumollard, R, Duchen, M and Sardet, C (2006) Calcium signals and mitochondria at fertilisation. Semin Cell Dev Biol 17, 314–23.CrossRefGoogle ScholarPubMed
El-Sayed, A, Hoelker, M, Rings, F, Salilew, D, Jennen, D, Tholen, E, Sirard, MA, Schellander, K and Tesfaye, D (2006) Large-scale transcriptional analysis of bovine embryo biopsies in relation to pregnancy success after transfer to recipients. Physiol Genomics 28, 84–96.CrossRefGoogle ScholarPubMed
Farin, CE, Rodriguez, KF, Alexander, JE, Hockney, JE, Herrick, JR and Kennedy-Stoskopf, S (2007) The role of transcription in EGF- and FSH-mediated oocyte maturation in vitro. Anim Reprod Sci 98, 97–112.CrossRefGoogle ScholarPubMed
Ferreira, EM, Vireque, AA, Adona, PR, Meirelles, FV, Ferriani, RA and Navarro, PA (2009) Cytoplasmic maturation of bovine oocytes: structural and biochemical modifications and acquisition of developmental competence. Theriogenology 71, 836–48.CrossRefGoogle ScholarPubMed
Furll, M, Deniz, A, Westphal, B, Illing, C and Constable, PD (2010) Effect of multiple intravenous injections of butaphosphan and cyanocobalamin on the metabolism of periparturient dairy cows. J Dairy Sci 93, 4155–64.CrossRefGoogle Scholar
Gavin, AC and Schorderet-Slatkine, S (1997) Ribosomal S6 kinase p90rsk and mRNA cap-binding protein eIF4E phosphorylations correlate with MAP kinase activation during meiotic reinitiation of mouse oocytes. Mol Reprod Dev 46, 383–91.3.0.CO;2-#>CrossRefGoogle ScholarPubMed
Gendelman, M, Aroyo, A, Yavin, S and Roth, Z (2010) Seasonal effects on gene expression, cleavage timing, and developmental competence of bovine preimplantation embryos. Reproduction 140, 73–82.CrossRefGoogle ScholarPubMed
Gendelman, M and Roth, Z (2012) In vivo vs. in vitro models for studying the effects of elevated temperature on the GV-stage oocyte, subsequent developmental competence and gene expression. Anim Reprod Sci 134, 125–34.CrossRefGoogle ScholarPubMed
Hao, ZD, Liu, S, Wu, Y, Wan, PC, Cui, MS, Chen, H and Zeng, SM (2009) Abnormal changes in mitochondria, lipid droplets, ATP and glutathione content, and Ca2+ release after electro-activation contribute to poor developmental competence of porcine oocyte during in vitro ageing. Reprod Fertil Dev 21, 323–32.CrossRefGoogle Scholar
Hasi Su-rong, DU, Xiao-yan, ZHU and Bei-lei, J (2004) Studies on effects of compound butaphosphan solution on endurance capability and energy metabolism in mice. Acta Vet Zoot Si 35, 4.Google Scholar
Hosoe, M, Kaneyama, K, Ushizawa, K, Hayashi, KG and Takahashi, T (2011) Quantitative analysis of bone morphogenetic protein 15 (BMP15) and growth differentiation factor 9 (GDF9) gene expression in calf and adult bovine ovaries. Reprod Biol Endocrinol 9, 33.CrossRefGoogle ScholarPubMed
Hussein, TS, Thompson, JG and Gilchrist, RB (2006) Oocyte-secreted factors enhance oocyte developmental competence. Dev Biol 296, 514–21.CrossRefGoogle ScholarPubMed
Leibfried, L and First, NL (1979) Characterization of bovine follicular oocytes and their ability to mature in vitro. J Anim Sci 48, 76–86.CrossRefGoogle ScholarPubMed
Lima, ME, Pereira, RA, Maffi, AS, Santos, JT, Martin, CEG, Del Pino, FAB, Leal, SDCBS, Brauner, CC and Correa, MN (2017) Butaphosphan and cyanocobalamin: effects on the aspiration of oocytes and in vitro embryo production in Jersey cows. Can J Anal Sci 97, 633–9.Google Scholar
Luciano, AM, Franciosi, F, Modina, SC and Lodde, V (2011) Gap junction-mediated communications regulate chromatin remodeling during bovine oocyte growth and differentiation through cAMP-dependent mechanism(s). Biol Reprod 85, 1252–9.CrossRefGoogle Scholar
Park, JY, Su, YQ, Ariga, M, Law, E, Jin, SL and Conti, M (2004) EGF-like growth factors as mediators of LH action in the ovulatory follicle. Science 303, 682–4.CrossRefGoogle ScholarPubMed
Parrish, JJ, Krogenaes, A and Susko-Parrish, JL (1995) Effect of bovine sperm separation by either swim-up or Percoll method on success of in vitro fertilization and early embryonic development. Theriogenology 44, 859–69.CrossRefGoogle ScholarPubMed
Pereira, RA, Silveira, PA, Montagner, P, Schneider, A, Schmitt, E, Rabassa, VR, Pfeifer, LF, Del Pino, FA, Pulga, ME and Correa, MN (2013) Effect of butaphosphan and cyanocobalamin on postpartum metabolism and milk production in dairy cows. Animal 7, 1143–7.CrossRefGoogle ScholarPubMed
Portela, VM, Machado, M, Buratini, J, Zamberlam, G Jr., Amorim, RL, Goncalves, P and Price, CA (2010) Expression and function of fibroblast growth factor 18 in the ovarian follicle in cattle. Biol Reprod 83, 339–46.CrossRefGoogle ScholarPubMed
Rekik, W, Dufort, I and Sirard, MA (2011) Analysis of the gene expression pattern of bovine blastocysts at three stages of development. Mol Reprod Dev 78, 226–40.CrossRefGoogle ScholarPubMed
Rincon, JAA, Madeira, EM, Campos, FT, Mion, B, Silva, JF, Absalon-Medina, VA, Butler, WR, Correa, MN, Pegoraro, L and Schneider, A (2016) Exogenous paraoxonase-1 during oocyte maturation improves bovine embryo development in vitro. Reprod Domest Anim 51, 827–30.CrossRefGoogle ScholarPubMed
Rollin, E, Berghaus, RD, Rapnicki, P, Godden, SM and Overton, MW (2010) The effect of injectable butaphosphan and cyanocobalamin on postpartum serum beta-hydroxybutyrate, calcium, and phosphorus concentrations in dairy cattle. J Dairy Sci 93, 978–87.CrossRefGoogle ScholarPubMed
Rose-Hellekant, TA, Libersky-Williamson, EA and Bavister, BD (1998) Energy substrates and amino acids provided during in vitro maturation of bovine oocytes alter acquisition of developmental competence. Zygote 6, 285–94.CrossRefGoogle ScholarPubMed
Sirard, MA and Coenen, K (2006) In vitro maturation and embryo production in cattle. Methods Mol Biol 348, 35–42.CrossRefGoogle ScholarPubMed
Stojkovic, D, Zhang, P and Crespi, VH (2001) Smallest nanotube: breaking the symmetry of sp(3) bonds in tubular geometries. Phys Rev Lett 87, 125502.CrossRefGoogle ScholarPubMed
Su, YQ, Sugiura, K, Wigglesworth, K, O’Brien, MJ, Affourtit, JP, Pangas, SA, Matzuk, MM and Eppig, JJ (2008) Oocyte regulation of metabolic cooperativity between mouse cumulus cells and oocytes: BMP15 and GDF9 control cholesterol biosynthesis in cumulus cells. Development 135, 111–21.CrossRefGoogle ScholarPubMed
Tabeleão, VC, Pereira, RA, Prietsch, RdF, Feijó, JO, Bondan, C, Mattei, P, Schmitt, E, Del Pino, FAB and Corrêa, MN (2017) Butafosfan e cianocobalamina: efeitos indiretos na recuperação da glândula mamária de vacas leiteiras após mastite clínica. Sci Anim Health 4, 238–54.CrossRefGoogle Scholar
Tanghe, S, Van Soom, A, Nauwynck, H, Coryn, M and de Kruif, A (2002) Minireview: Functions of the cumulus oophorus during oocyte maturation, ovulation, and fertilization. Mol Reprod Dev 61, 414–24.CrossRefGoogle ScholarPubMed
Thach, RE (1992) Cap recap: the involvement of eIF-4F in regulating gene expression. Cell 68, 177–80.CrossRefGoogle ScholarPubMed
van den Hurk, R and Zhao, J (2005) Formation of mammalian oocytes and their growth, differentiation and maturation within ovarian follicles. Theriogenology 63, 1717–51.CrossRefGoogle ScholarPubMed
Wang, Q and Sun, QY (2007) Evaluation of oocyte quality: morphological, cellular and molecular predictors. Reprod Fertil Dev 19, 1–12.CrossRefGoogle ScholarPubMed
Yamada, M and Isaji, Y (2011) Structural and functional changes linked to, and factors promoting, cytoplasmic maturation in mammalian oocytes. Reprod Med Biol 10, 10.CrossRefGoogle ScholarPubMed
Yang, MY and Rajamahendran, R (2002) Expression of Bcl-2 and Bax proteins in relation to quality of bovine oocytes and embryos produced in vitro. Anim Reprod Sci 70, 159–69.CrossRefGoogle ScholarPubMed
Zhang, X, Wu, XQ, Lu, S, Guo, YL and Ma, X (2006) Deficit of mitochondria-derived ATP during oxidative stress impairs mouse MII oocyte spindles. Cell Res 16, 841–50.CrossRefGoogle ScholarPubMed