Hostname: page-component-8448b6f56d-42gr6 Total loading time: 0 Render date: 2024-04-24T12:30:38.739Z Has data issue: false hasContentIssue false
  • English
  • Français

Satellite DNA methylation status and expression of selected genes in Bos indicus blastocysts produced in vivo and in vitro

Published online by Cambridge University Press:  31 January 2017

R. Urrego ,
S.M. Bernal-Ulloa ,
N.A. Chavarría ,
E. Herrera-Puerta ,
A. Lucas-Hahn ,
D. Herrmann ,
S. Winkler ,
D. Pache ,
H. Niemann  and
N. Rodriguez-Osorio
R. Urrego*
Affiliation:
Grupo INCA-CES, Facultad de Medicina Veterinaria y Zootecnia, Universidad CES, Calle 10 A No. 22-04 MedellínColombia. Grupo CENTAURO, Universidad de Antioquia, Calle 70 No. 52-21 Medellín, Colombia.
S.M. Bernal-Ulloa
Affiliation:
Institute of Farm Animal Genetics, Friedrich-Loeffler-Institut (FLI), Höltystraße 10, Mariensee, 31535 Neustadt, Germany. Facultad de Ciencias Agropecuarias, Universidad de Ciencias Aplicadas y Ambientales UDCA, Calle 222 No. 55-37, Bogotá, Colombia.
N.A. Chavarría
Affiliation:
Grupo INCA-CES, Facultad de Medicina Veterinaria y Zootecnia, Universidad CES, Calle 10 A No. 22-04 Medellín, Colombia.
E. Herrera-Puerta
Affiliation:
Grupo Biología CES-EIA, Universidad CES, Calle 10 A No. 22-04 Medellín, Colombia.
A. Lucas-Hahn
Affiliation:
Institute of Farm Animal Genetics, Friedrich-Loeffler-Institut (FLI), Höltystraße 10, Mariensee, 31535 Neustadt, Germany.
D. Herrmann
Affiliation:
Institute of Farm Animal Genetics, Friedrich-Loeffler-Institut (FLI), Höltystraße 10, Mariensee, 31535 Neustadt, Germany.
S. Winkler
Affiliation:
DNA Sequencing Facility, Max Planck Institute of Molecular Cell Biology and Genetics, Pfotenhauerstraße 108, 01307 Dresden, Germany.
D. Pache
Affiliation:
DNA Sequencing Facility, Max Planck Institute of Molecular Cell Biology and Genetics, Pfotenhauerstraße 108, 01307 Dresden, Germany.
H. Niemann
Affiliation:
Institute of Farm Animal Genetics, Friedrich-Loeffler-Institut (FLI), Höltystraße 10, Mariensee, 31535 Neustadt, Germany.
N. Rodriguez-Osorio
Affiliation:
Grupo CENTAURO, Universidad de Antioquia, Calle 70 No. 52-21 Medellín, Colombia.
*
All correspondence to: R. Urrego. Grupo INCA-CES, Facultad de Medicina Veterinaria y Zootecnia, Universidad CES, Calle 10 A No. 22-04 MedellínColombia. E-mail: rodurrego@gmail.com
Get access Rights & Permissions [Opens in a new window]

Summary

Bovine embryos produced in vivo and in vitro differ with respect to molecular profiles, including epigenetic marks and gene expression profiles. This study investigated the CpG methylation status in bovine testis satellite I (BTS) and Bos taurus alpha satellite I (BTαS) DNA sequences, and concomitantly the relative abundance of transcripts, critically involved in DNA methylation (DNMT1 and DNMT3A), growth and development (IGF2R) and pluripotency (POU5F1) in Bos indicus embryos produced in vitro or in vivo. Results revealed that methylation of BTS were higher (P < 0.05) in embryos produced in vitro compared with their in vivo produced counterparts, while the methylation status of BTαS was similar in both groups. There were no significant differences in transcript abundance for DNMT3A, IGF2R and POU5F1 between blastocysts produced in vivo and in vitro. However, a significantly lower amount of DNMT1 transcripts was found in the in vitro cultured embryos (P < 0.05) compared with their in vivo derived counterparts. In conclusion, this study reported only minor changes in the expression of developmentally important genes and satellite DNA methylation related to the in vitro embryo production system.

Keywords

Bovine embryoDNA methylationDNMT1In vitro cultureSatellite DNA
Type
Research Article
Information
Zygote , Volume 25 , Issue 2 , April 2017 , pp. 131 - 140
Copyright
Copyright © Cambridge University Press 2017 

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

Baruselli, P.S., Ferreira, R.M., Sales, J.N.S., Gimenes, L.U., Sá Filho, M.F., Martins, C.M., Rodrigues, C.A. & Bó, G.A. (2011). Timed embryo transfer programs for management of donor and recipient cattle. Theriogenology 76, 1583–93.Google Scholar
Bernal, S.M., Heinzmann, J., Herrmann, D., Timmermann, B., Baulain, U., Großfeld, R., Diederich, M., Lucas-Hahn, A. & Niemann, H. (2015). Effects of different oocyte retrieval and in vitro maturation systems on bovine embryo development and quality. Zygote 23, 367–77.CrossRefGoogle Scholar
Bestor, T.H., Gundersen, G., Kolsto, A.B. & Prydz, H. (1992). CpG islands in mammalian gene promoters are inherently resistant to de novo methylation. Genet. Anal. Tech. Appl. 9, 48–53.CrossRefGoogle ScholarPubMed
Bó, G.A., Baruselli, P.S. & Martínez, M.F. (2003). Pattern and manipulation of follicular development in Bos indicus cattle. Anim. Reprod. Sci. 78, 307–26.Google Scholar
Bock, C., Reither, S., Mikeska, T., Paulsen, M., Walter, J. & Lengauer, T. (2005). BiQ Analyzer: visualization and quality control for DNA methylation data from bisulfite sequencing. Bioinformatics 21, 4067–8.CrossRefGoogle ScholarPubMed
Camargo, L.S.A., Boite, M.C., Wohlres-Viana, S., Mota, G.B., Serapiao, R.V., Sa, W.F., Viana, J.H. & Nogueira, L.A. (2011). Osmotic challenge and expression of aquaporin 3 and Na/K ATPase genes in bovine embryos produced in vitro . Cryobiology 63, 256–62.Google Scholar
Camargo, L.S.A., Freitas, C., de Sa, W.F., de Moraes Ferreira, A., Serapiao, R.V. & Viana, J.H.M. (2010). Gestation length, birth weight and offspring gender ratio of in vitro produced Gyr (Bos indicus) cattle embryos. Anim. Reprod. Sci. 120, 10–15.Google Scholar
Cirio, M. C., Ratnam, S., Ding, F., Reinhart, B., Navara, C. & Chaillet, J. R. (2008). Preimplantation expression of the somatic form of Dnmt1 suggests a role in the inheritance of genomic imprints. BMC Dev. Biol. 8, 9.Google Scholar
Diederich, M., Hansmann, T., Heinzmann, J., Barg-Kues, B., Herrmann, D., Aldag, P., Baulain, U., Reinhard, R. Kues, W., Weissgerber, C., Haaf, T. & Niemann, H. (2012). DNA methylation and mRNA expression profiles in bovine oocytes derived from prepubertal and adult donors. Reproduction 144, 319–30.Google Scholar
Dobbs, K B., Rodriguez, M., Sudano, M.J., Ortega, M.S. & Hansen, P.J. (2013). Dynamics of DNA methylation during early development of the preimplantation bovine embryo. PLoS One 8, e66230.Google Scholar
Enukashvily, N.I. & Ponomartsev, N.V. (2013). Mammalian satellite DNA: A speaking Dumb. Elsevier Inc.Google Scholar
Farin, C.E., Alexander, J.E. & Farin, P.W. (2010). Expression of messenger RNAs for insulin-like growth factors and their receptors in bovine fetuses at early gestation from embryos produced in vivo or in vitro . Theriogenology 74, 1288–95.Google Scholar
Farin, P.W., Piedrahita, J.A. & Farin, C.E. (2006). Errors in development of fetuses and placentas from in vitro produced bovine embryos. Theriogenology 65, 178–91.Google Scholar
Farmer, W. T., Farin, P. W., Piedrahita, J. a, Bischoff, S. R. & Farin, C. E. (2013). Expression of antisense of insulin-like growth factor-2 receptor RNA non-coding (AIRN) during early gestation in cattle. Anim. Reprod. Sci. 138, 64–73.Google Scholar
Golding, M.C., Williamson, G.L., Stroud, T.K., Westhusin, M.E. & Long, C.R. (2011). Examination of DNA methyltransferase expression in cloned embryos reveals an essential role for Dnmt1 in bovine development. Mol. Reprod. Dev. 78, 306–17.Google Scholar
Gómez, E., Gutiérrez-Adán, A., Díez, C., Bermejo-Alvarez, P., Muñoz, M., Rodriguez, A., Otero, J., Alvarez-Viejo, M., Martín, D., Carrocera, S. & Caamaño, JN (2009). Biological differences between in vitro produced bovine embryos and parthenotes. Reproduction 137, 285–95.Google Scholar
Gordon, I. (2003). Laboratory Production of Cattle Embryos. 2nd edition.CrossRefGoogle Scholar
Haaf, T. (2006). Methylation dynamics in the early mammalian embryo: implications of genome reprogramming defects for development. Curr. Top. Microbiol. Immunol. 310, 13–22.Google Scholar
El Hajj, N. & Haaf, T. (2013). Epigenetic disturbances in in vitro cultured gametes and embryos: implications for human assisted reproduction. Fertil. Steril. 99, 632–41.CrossRefGoogle ScholarPubMed
Herrmann, D., Dahl, J.A., Lucas-Hahn, A., Collas, P. & Niemann, H. (2013). Histone modifications and mRNA expression in the inner cell mass and trophectoderm of bovine blastocysts. Epigenetics 8, 281–9.Google Scholar
Hoffmann, K., Niemann, H., Hadeler, K.-G., Herrmann, D. & Wrenzycki, C. (2006). 247 messenger RNA expression patterns of DNA and histone methyltransferases in preimplantation development of in vivo- and in vitro produced bovine embryos. Reprod. Fertil. Dev. 18, 231.Google Scholar
Hou, J., Liu, L., Lei, T., Cui, X., An, X. & Chen, Y. (2007). Genomic DNA methylation patterns in bovine preimplantation embryos derived from in vitro fertilization. Sci. China. C. Life Sci. 50, 56–61.Google Scholar
Kang, Y.-K., Lee, H.-J., Shim, J.-J., Yeo, S., Kim, S.-H., Koo, D.-B., Lee, K.K., Beyhan, Z., First, N.L. & Han, Y.M. (2005). Varied patterns of DNA methylation change between different satellite regions in bovine preimplantation development. Mol. Reprod. Dev. 71, 29–35.Google Scholar
Khurana, N. K. & Niemann, H. (2000). Energy metabolism in preimplantation bovine embryos derived in vitro or in vivo . Biol. Reprod. 62, 847–56.Google Scholar
Kirchhof, N., Carnwath, J. W., Lemme, E., Anastassiadis, K., Schöler, H. & Niemann, H. (2000). Expression pattern of Oct-4 in preimplantation embryos of different species. Biol. Reprod. 63, 1698–705.CrossRefGoogle ScholarPubMed
Mundim, T.C.D., Ramos, A.F., Sartori, R., Dode, M.A.N., Melo, E.O., Gomes, L.F.S., Rumpf, R. & Franco, M.M. (2009). Changes in gene expression profiles of bovine embryos produced in vitro, by natural ovulation, or hormonal superstimulation. Genet. Mol. Res. 8, 1398–407.Google Scholar
Neto, A.S.C., Sanches, B.V, Binelli, M., Seneda, M.M., Perri, S.H. & Garcia, J.F. (2005). Improvement in embryo recovery using double uterine flushing. Theriogenology 63, 1249–55.Google Scholar
Niemann, H., Carnwath, J. W., Herrmann, D., Wieczorek, G., Lemme, E., Lucas-Hahn, A. & Olek, S. (2010). DNA methylation patterns reflect epigenetic reprogramming in bovine embryos. Cell. Reprogram. 12, 33–42.CrossRefGoogle ScholarPubMed
Okano, M., Bell, D. W., Haber, D. A. & Li, E. (1999). DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99, 247–57.Google Scholar
Perecin, F., Méo, S. C., Yamazaki, W., Ferreira, C.R., Merighe, G.K.F., Meirelles, F.V. & Garcia, J.M. (2009). Imprinted gene expression in in vivo- and in vitro produced bovine embryos and chorio-allantoic membranes. Genet. Mol. Res. 8, 76–85.Google Scholar
Perrin, D., Ballestar, E., Fraga, M. F., Frappart, L., Esteller, M., Guerin, J.-F. & Dante, R. (2007). Specific hypermethylation of LINE-1 elements during abnormal overgrowth and differentiation of human placenta. Oncogene 26, 2518–2524.Google Scholar
Perry, G. (2014). 2013 Statistics of embryo collection and transfer in domestic farm animals.Google Scholar
Petrussa, L., Van de Velde, H. & De Rycke, M. (2014). Dynamic regulation of DNA methyltransferases in human oocytes and preimplantation embryos after assisted reproductive technologies. Mol. Hum. Reprod. 20, 861–74.CrossRefGoogle ScholarPubMed
Pfaffl, M. W. (2002). Relative expression software tool (REST(C)) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 30, 36e–36.Google Scholar
Plohl, M., Meštrović, N. & Mravinac, B. (2012). Satellite DNA evolution. Genome Dyn. 7, 126–52.CrossRefGoogle ScholarPubMed
Pradhan, S., Bacolla, A., Wells, R.D. & Roberts, R.J. (1999). Recombinant human DNA (cytosine-5) methyltransferase. I. Expression, purification, and comparison of novo and maintenance methylation. J. Biol. Chem. 274, 33002–10.Google Scholar
Purpera, M.N., Giraldo, A.M., Ballard, C.B., Hylan, D., Godke, R.A. & Bondioli, K.R. (2009). Effects of culture medium and protein supplementation on mRNA expression of in vitro produced bovine embryos. Mol. Reprod. Dev. 76, 783–93.Google Scholar
R Development Core Team, R. (2011). R: A Language and Environment for Statistical Computing. R Found. Stat. Comput. 1, 409.Google Scholar
Ramakers, C., Ruijter, J.M., Deprez, R.H.L. & Moorman, A. F. (2003). Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci. Lett. 339, 62–6.CrossRefGoogle ScholarPubMed
Reik, W., Dean, W. & Walter, J. (2001). Epigenetic reprogramming in mammalian development. Science 293, 1089–93.Google Scholar
Rodriguez-Osorio, N., Urrego, R., Cibelli, J. B., Eilertsen, K. & Memili, E. (2012). Reprogramming mammalian somatic cells. Theriogenology 78, 1869–86.Google Scholar
Sagirkaya, H., Misirlioglu, M., Kaya, A., First, N.L., Parrish, J.J. & Memili, E. (2006). Developmental and molecular correlates of bovine preimplantation embryos. Reproduction 131, 895–904.Google Scholar
Sartori, R., Bastos, M. R., Baruselli, P.S., Gimenes, L.U., Ereno, R.L. & Barros, C.M. (2010). Physiological differences and implications to reproductive management of Bos taurus and Bos indicus cattle in a tropical environment. Soc. Reprod. Fertil. Suppl. 67, 357–75.Google Scholar
Sawai, K., Takahashi, M., Fujii, T., Moriyasu, S., Hirayama, H., Minamihashi, A., Hashizume, T. & Onoe, S. (2011). DNA methylation status of bovine blastocyst embryos obtained from various procedures. J. Reprod. Dev. 57, 236–41.Google Scholar
Smith, L.C., Therrien, J., Filion, F., Bressan, F. & Meirelles, F.V. (2015). Epigenetic consequences of artificial reproductive technologies to the bovine imprinted genes SNRPN, H19/IGF2, and IGF2R. Front. Genet. 6, 58.Google Scholar
Suzuki, J., Therrien, J., Filion, F., Lefebvre, R., Goff, A.K. & Smith, L.C. (2009). In vitro culture and somatic cell nuclear transfer affect imprinting of SNRPN gene in pre- and post-implantation stages of development in cattle. BMC Dev. Biol. 9, 9.Google Scholar
Urrego, R., Herrera-Puerta, E., Chavarria, N.A., Camargo, O., Wrenzycki, C. & Rodriguez-Osorio, N. (2015). Follicular progesterone concentrations and messenger RNA expression of MATER and OCT-4 in immature bovine oocytes as predictors of developmental competence. Theriogenology 83, 1179–87.Google Scholar
Urrego, R., Rodriguez-Osorio, N. & Niemann, H. (2014). Epigenetic disorders and altered in gene expression after use of Assisted Reproductive Technologies in domestic cattle. Epigenetics 9, 803–815.CrossRefGoogle ScholarPubMed
Vajta, G., Rienzi, L., Cobo, A. & Yovich, J. (2010). Embryo culture: can we perform better than nature? Reprod. Biomed. Online 20, 453–69.Google Scholar
Velker, B.A.M., Denomme, M.M. & Mann, M.R.W. (2012). Embryo culture and epigenetics. Methods Mol. Biol. 912, 399–421.Google Scholar
Wrenzycki, C., Herrmann, D., Lucas-Hahn, A., Korsawe, K., Lemme, E. & Niemann, H. (2005). Messenger RNA expression patterns in bovine embryos derived from in vitro procedures and their implications for development. Reprod. Fertil. Dev. 17, 23–35.Google Scholar
Wrenzycki, C., Herrmann, D. & Niemann, H. (2007). Messenger RNA in oocytes and embryos in relation to embryo viability. Theriogenology 68 Suppl 1, S77–83.Google Scholar
Wrenzycki, C., Lucas-Hahn, A., Herrmann, D., Lemme, E., Korsawe, K. & Niemann, H. (2002). In vitro production and nuclear transfer affect dosage compensation of the X-linked gene transcripts G6PD, PGK, and Xist in preimplantation bovine embryos. Biol. Reprod. 66, 127–34.Google Scholar
Young, L.E., Fernandes, K., McEvoy, T.G., Butterwith, S.C., Gutierrez, C.G., Carolan, C., Broadbent, P.J., Robinson, J.J., Wilmut, I. & Sinclair, K.D. (2001). Epigenetic change in IGF2R is associated with fetal overgrowth after sheep embryo culture. Nat. Genet. 27, 153–4.Google Scholar
Zhang, X., Wang, D., Han, Y., Duan, F., Lv, Q. & Li, Z. (2014). Altered imprinted gene expression and methylation patterns in mid-gestation aborted cloned porcine fetuses and placentas. J. Assist. Reprod. Genet. 31, 1511–17.CrossRefGoogle ScholarPubMed
Zhao, X.-M., Ren, J.-J., Du, W.-H., Hao, H.-S., Wang, D., Qin, T., Liu, Y. & Zhu, H.B. (2013). Effect of vitrification on promoter CpG island methylation patterns and expression levels of DNA methyltransferase 1o, histone acetyltransferase 1, and deacetylase 1 in metaphase II mouse oocytes. Fertil. Steril. 100, 256–61.Google Scholar