High oxygen tension increases global methylation in bovine 4-cell embryos and blastocysts but does not affect general retrotransposon expression
Wenwen Li A , Karen Goossens A , Mario Van Poucke A , Katrien Forier B C , Kevin Braeckmans B C , Ann Van Soom D and Luc J. Peelman A E
+ Author Affiliations
- Author Affiliations
A Department of Nutrition, Genetics and Ethology, Faculty of Veterinary Medicine, Ghent University, Heidestraat 19, 9820 Merelbeke, Belgium.
B Laboratory of General Biochemistry and Physical Pharmacy,Ghent University, Harelbekestraat 72, 9000 Ghent, Belgium.
C Center for Nano- and Biophotonics, Harelbekestraat 72, 9000 Ghent, Belgium.
D Department of Reproduction, Obstetrics and Herd Health, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820 Merelbeke, Belgium.
E Corresponding author. Email: luc.peelman@ugent.be
Reproduction, Fertility and Development 28(7) 948-959 https://doi.org/10.1071/RD14133
Submitted: 18 April 2014 Accepted: 1 November 2014 Published: 17 December 2014
Abstract
Retrotransposons are transposable elements that insert extra copies of themselves throughout the genome via an RNA intermediate using a ‘copy and paste’ mechanism. They account for more than 44% of the bovine genome and have been reported to be functional, especially during preimplantation embryo development. In the present study, we tested whether high oxygen tension (20% O2) influences global DNA methylation analysed by immunofluorescence staining of developing bovine embryos and whether this has an effect on the expression of some selected retrotransposon families. High oxygen tension significantly increased global DNA methylation in 4-cell embryos and blastocysts. A significant expression difference was observed for ERV1-1-I_BT in female blastocysts, but no significant changes were observed for the other retrotransposon families tested. Therefore, the study indicates that global DNA methylation is not necessarily correlated with retrotransposon expression in bovine preimplantation embryos.
Additional keywords: bovine preimplantation embryo, DNA methylation, oxidative stress, reference genes.
References
Abràmoff, M. D., Magalhães, P. J., and Ram, S. J. (2004). Image processing with ImageJ. Biophotonics Intern. 11, 36–42.Adelson, D. L., Raison, J. M., and Edgar, R. C. (2009). Characterization and distribution of retrotransposons and simple sequence repeats in the bovine genome. Proc. Natl Acad. Sci. USA 106, 12 855–12 860.
| Characterization and distribution of retrotransposons and simple sequence repeats in the bovine genome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVKlt7%2FK&md5=bf177e9516b62fdb327536f04fd92c96CAS |
Arányi, T., Váradi, A., Simon, I., and Tusnády, G. E. (2006). The BiSearch web server. BMC Bioinformatics 7, 431–437.
| The BiSearch web server.Crossref | GoogleScholarGoogle Scholar | 17022803PubMed |
Asada, K., Kotake, Y., Asada, R., Saunders, D., Broyles, R. H., Towner, R. A., Fukui, H., and Floyd, R. A. (2006). LINE-1 hypomethylation in a choline-deficiency-induced liver cancer in rats: dependence on feeding period. BioMed Research International 2006, 17 142.
Beaujean, N., Taylor, J., Gardner, J., Wilmut, I., Meehan, R., and Young, L. (2004). Effect of limited DNA methylation reprogramming in the normal sheep embryo on somatic cell nuclear transfer. Biol. Reprod. 71, 185–193.
| Effect of limited DNA methylation reprogramming in the normal sheep embryo on somatic cell nuclear transfer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXltFKkur0%3D&md5=ec72e997dd88a71fa6379c5b61d5fc2cCAS | 14998909PubMed |
Beraldi, R., Pittoggi, C., Sciamanna, I., Mattei, E., and Spadafora, C. (2006). Expression of LINE-1 retroposons is essential for murine preimplantation development. Mol. Reprod. Dev. 73, 279–287.
| Expression of LINE-1 retroposons is essential for murine preimplantation development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhsVKht7w%3D&md5=b1d5171bcd31db799d02742f8e704b83CAS | 16365895PubMed |
Bermejo-Alvarez, P., Rizos, D., Rath, D., Lonergan, P., and Gutierrez-Adan, A. (2008). Epigenetic differences between male and female bovine blastocysts produced in vitro. Physiol. Genomics 32, 264–272.
| Epigenetic differences between male and female bovine blastocysts produced in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmt1Wjurw%3D&md5=7f386446185a445513119a7d1b33e471CAS | 17986520PubMed |
Bermejo-Álvarez, P., Lonergan, P., Rath, D., Gutiérrez-Adan, A., and Rizos, D. (2010a). Developmental kinetics and gene expression in male and female bovine embryos produced in vitro with sex-sorted spermatozoa. Reprod. Fertil. Dev. 22, 426–436.
| Developmental kinetics and gene expression in male and female bovine embryos produced in vitro with sex-sorted spermatozoa.Crossref | GoogleScholarGoogle Scholar | 20047728PubMed |
Bermejo-Alvarez, P., Rizos, D., Rath, D., Lonergan, P., and Gutierrez-Adan, A. (2010b). Sex determines the expression level of one third of the actively expressed genes in bovine blastocysts. Proc. Natl Acad. Sci. USA 107, 3394–3399.
| Sex determines the expression level of one third of the actively expressed genes in bovine blastocysts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjtFymtbo%3D&md5=da68184c3a41f146c24ecc4dd6f79b34CAS | 20133684PubMed |
Bestor, T., and Bourc’his, D. (2004). Transposon silencing and imprint establishment in mammalian germ cells. In ‘Cold Spring Harbor Symposia on Quantitative Biology’. (Eds B. Stillman and D. Stewart.) pp. 381–388. (Cold Spring Harbor Laboratory Press: Exeter, DEV, UK.)
Biniszkiewicz, D., Gribnau, J., Ramsahoye, B., Gaudet, F., Eggan, K., Humpherys, D., Mastrangelo, M. A., Jun, Z., Walter, J., and Jaenisch, R. (2002). Dnmt1 overexpression causes genomic hypermethylation, loss of imprinting, and embryonic lethality. Mol. Cell. Biol. 22, 2124–2135.
| Dnmt1 overexpression causes genomic hypermethylation, loss of imprinting, and embryonic lethality.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xit1Kitr4%3D&md5=fb9aca8723c36da53bfc27028cb39252CAS | 11884600PubMed |
Bourc’his, D., Le Bourhis, D., Patin, D., Niveleau, A., Comizzoli, P., Renard, J. P., and Viegas-Pequignot, E. (2001). Delayed and incomplete reprogramming of chromosome methylation patterns in bovine cloned embryos. Curr. Biol. 11, 1542–1546.
| Delayed and incomplete reprogramming of chromosome methylation patterns in bovine cloned embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnsF2ms7o%3D&md5=a1da80f40ec970d81b6981323deb38e2CAS | 11591324PubMed |
Burroughs, C. A., Williamson, G. L., Golding, M. C., and Long, C. R. (2013). Oxidative stress induced changes in epigenetic modifying gene mRNA in pre-implantation in vitro bovine embryos. Reprod. Fertil. Dev. 25, 149.
| Oxidative stress induced changes in epigenetic modifying gene mRNA in pre-implantation in vitro bovine embryos.Crossref | GoogleScholarGoogle Scholar |
Bustin, S. A., Benes, V., Garson, J. A., Hellemans, J., Huggett, J., Kubista, M., Mueller, R., Nolan, T., Pfaffl, M. W., and Shipley, G. L. (2009). The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin. Chem. 55, 611–622.
| The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXktVWqs7g%3D&md5=78315fac3e32033dbd8014eacd0b3e3eCAS | 19246619PubMed |
Corpet, F. (1988). Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res. 16, 10 881–10 890.
| Multiple sequence alignment with hierarchical clustering.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXjsVOqtA%3D%3D&md5=73db3f95f6c10761f19aca7a8c8bd4b1CAS |
De La Fuente, R., Hahnel, A., Basrur, P. K., and King, W. A. (1999). X inactive-specific transcript (Xist) expression and X chromosome inactivation in the preattachment bovine embryo. Biol. Reprod. 60, 769–775.
| X inactive-specific transcript (Xist) expression and X chromosome inactivation in the preattachment bovine embryo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhsFekur8%3D&md5=3599849954620358f6343568e6967bcaCAS | 10026129PubMed |
Dean, W., Santos, F., Stojkovic, M., Zakhartchenko, V., Walter, J., Wolf, E., and Reik, W. (2001). Conservation of methylation reprogramming in mammalian development: aberrant reprogramming in cloned embryos. Proc. Natl Acad. Sci. USA 98, 13 734–13 738.
| Conservation of methylation reprogramming in mammalian development: aberrant reprogramming in cloned embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXovVyntrs%3D&md5=e73da2e3bdcb4689b20df1fbac5b40b5CAS |
Deshmukh, R. S., Østrup, O., Østrup, E., Vejlsted, M., Niemann, H., Lucas-Hahn, A., Petersen, B., Li, J., Callesen, H., and Hyttel, P. (2011). DNA methylation in porcine preimplantation embryos developed in vivo and produced by in vitro fertilization, parthenogenetic activation and somatic cell nuclear transfer. Epigenetics 6, 177–187.
| DNA methylation in porcine preimplantation embryos developed in vivo and produced by in vitro fertilization, parthenogenetic activation and somatic cell nuclear transfer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjs12ksLY%3D&md5=591615abb4092ec0f1627d508d4fabb7CAS | 20935454PubMed |
Dewannieux, M., Esnault, C., and Heidmann, T. (2003). LINE-mediated retrotransposition of marked Alu sequences. Nat. Genet. 35, 41–48.
| LINE-mediated retrotransposition of marked Alu sequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmslemu70%3D&md5=00ee8ddd9f66b216a127d45af425b482CAS | 12897783PubMed |
Dobbs, K. B., Rodriguez, M., Sudano, M. J., Ortega, M. S., and Hansen, P. J. (2013). Dynamics of DNA methylation during early development of the preimplantation bovine embryo. PLoS ONE 8, e66230.
| Dynamics of DNA methylation during early development of the preimplantation bovine embryo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtVemsLvJ&md5=c810d4d11d2a75d0346a585534d33d2bCAS | 23799080PubMed |
Ehrlich, M. (2002). DNA methylation in cancer: too much, but also too little. Oncogene 21, 5400–5413.
| DNA methylation in cancer: too much, but also too little.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XlslSqtL8%3D&md5=ec06ce2556cfb6953386358f315aaf80CAS | 12154403PubMed |
Epstein, C. J., Smith, S., Travis, B., and Tucker, G. (1978). Both X chromosomes function before visible X-chromosome inactivation in female mouse embryos. Nature 274, 500–503.
| Both X chromosomes function before visible X-chromosome inactivation in female mouse embryos.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE1c3itlKisA%3D%3D&md5=26ba798c5c6a121737f8f125602be583CAS | 672979PubMed |
Fulka, H., Mrazek, M., Tepla, O., and Fulka, J. (2004). DNA methylation pattern in human zygotes and developing embryos. Reproduction 128, 703–708.
| DNA methylation pattern in human zygotes and developing embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFSlug%3D%3D&md5=a99d1baf063b18aa342876923378eb5bCAS | 15579587PubMed |
Garcia-Etxebarria, K., and Jugo, B. M. (2010). Genome-wide detection and characterization of endogenous retroviruses in Bos taurus. J. Virol. 84, 10 852–10 862.
| Genome-wide detection and characterization of endogenous retroviruses in Bos taurus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlaku7rJ&md5=0a1ce34d9728faa7dc265071a35232aaCAS |
Goossens, K., Van Poucke, M., Van Soom, A., Vandesompele, J., Van Zeveren, A., and Peelman, L. J. (2005). Selection of reference genes for quantitative real-time PCR in bovine preimplantation embryos. BMC Dev. Biol. 5, 27.
| Selection of reference genes for quantitative real-time PCR in bovine preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 16324220PubMed |
Gu, T.-P., Guo, F., Yang, H., Wu, H.-P., Xu, G.-F., Liu, W., Xie, Z.-G., Shi, L., He, X., and Jin, S.-g. (2011). The role of Tet3 DNA dioxygenase in epigenetic reprogramming by oocytes. Nature 477, 606–610.
| The role of Tet3 DNA dioxygenase in epigenetic reprogramming by oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFersL7M&md5=2478c1cc5a5c00b8d36c3d1ff935f2a3CAS | 21892189PubMed |
Gutiérrez-Adán, A., Behboodi, E., Andersen, G., Medrano, J., and Murray, J. (1996). Relationship between stage of development and sex of bovine IVM-IVF embryos cultured in vitro versus in the sheep oviduct. Theriogenology 46, 515–525.
| Relationship between stage of development and sex of bovine IVM-IVF embryos cultured in vitro versus in the sheep oviduct.Crossref | GoogleScholarGoogle Scholar | 16727919PubMed |
Gutiérrez-Adán, A., Granados, J., Pintado, B., and De La Fuente, J. (2001). Influence of glucose on the sex ratio of bovine IVM/IVF embryos cultured in vitro. Reprod. Fertil. Dev. 13, 361–365.
| Influence of glucose on the sex ratio of bovine IVM/IVF embryos cultured in vitro.Crossref | GoogleScholarGoogle Scholar | 11833931PubMed |
Haaf, T. (2006). Methylation dynamics in the early mammalian embryo: implications of genome reprogramming defects for development. In ‘DNA Methylation: Development, Genetic Disease and Cancer’. (Eds W. Doerfler and P. Böhm.) pp. 13–22. (Springer: Berlin.)
Hamilton, C. K., Combe, A., Caudle, J., Ashkar, F. A., Macaulay, A. D., Blondin, P., and King, W. A. (2012). A novel approach to sexing bovine blastocysts using male-specific gene expression. Theriogenology 77, 1587–1596.
| A novel approach to sexing bovine blastocysts using male-specific gene expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XltVKmt70%3D&md5=f59cc6080ab4343387c1415a0eba2377CAS | 22341705PubMed |
Harris, R. A., Wang, T., Coarfa, C., Nagarajan, R. P., Hong, C., Downey, S. L., Johnson, B. E., Fouse, S. D., Delaney, A., Zhao, Y., Olshen, A., Ballinger, T., Zhou, X., Forsberg, K. J., Gu, J., Echipare, L., O’Geen, H., Lister, R., Pelizzola, M., Xi, Y., Epstein, C. B., Bernstein, B. E., Hawkins, R. D., Ren, B., Chung, W.-Y., Gu, H., Bock, C., Gnirke, A., Zhang, M. Q., Haussler, D., Ecker, J. R., Li, W., Farnham, P. J., Waterland, R. A., Meissner, A., Marra, M. A., Hirst, M., Milosavljevic, A., and Costello, J. F. (2010). Comparison of sequencing-based methods to profile DNA methylation and identification of monoallelic epigenetic modifications. Nat. Biotechnol. 28, 1097–1105.
| Comparison of sequencing-based methods to profile DNA methylation and identification of monoallelic epigenetic modifications.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtFOht7bN&md5=eabe77a2c20fdabefd51fb0eaa676ddcCAS | 20852635PubMed |
Hata, K., and Sakaki, Y. (1997). Identification of critical CpG sites for repression of L1 transcription by DNA methylation. Gene 189, 227–234.
| Identification of critical CpG sites for repression of L1 transcription by DNA methylation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjtlGmtrw%3D&md5=abcadbd175903d45b3a07a7410225443CAS | 9168132PubMed |
Hellemans, J., Mortier, G., De Paepe, A., Speleman, F., and Vandesompele, J. (2007). qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol. 8, R19.
| qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data.Crossref | GoogleScholarGoogle Scholar | 17291332PubMed |
Horie, K., Saito, E. S., Keng, V. W., Ikeda, R., Ishihara, H., and Takeda, J. (2007). Retrotransposons influence the mouse transcriptome: implication for the divergence of genetic traits. Genetics 176, 815–827.
| Retrotransposons influence the mouse transcriptome: implication for the divergence of genetic traits.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXovVOrurk%3D&md5=ae51ce1e1fcd4860b6b822a334bf3b1bCAS | 17435252PubMed |
Hou, J., Liu, L., Lei, T., Cui, X., An, X., and Chen, Y. (2007). Genomic DNA methylation patterns in bovine preimplantation embryos derived from in vitro fertilization. Sci. China C Life Sci. 50, 56–61.
| Genomic DNA methylation patterns in bovine preimplantation embryos derived from in vitro fertilization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXkt1agtbs%3D&md5=b1d0a0119e6252ff6032e6a4b80f689eCAS | 17393083PubMed |
Howard, G., Eiges, R., Gaudet, F., Jaenisch, R., and Eden, A. (2008). Activation and transposition of endogenous retroviral elements in hypomethylation induced tumors in mice. Oncogene 27, 404–408.
| Activation and transposition of endogenous retroviral elements in hypomethylation induced tumors in mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXksVKmtg%3D%3D&md5=a2187ac3084ec0bd6478274b0ecbb3e1CAS | 17621273PubMed |
Hsieh, C. L. (2005). The de novo methylation activity of Dnmt3a is distinctly different than that of Dnmt1. BMC Biochem. 6, 6.
| The de novo methylation activity of Dnmt3a is distinctly different than that of Dnmt1.Crossref | GoogleScholarGoogle Scholar | 15799776PubMed |
Inoue, A., Matoba, S., and Zhang, Y. (2012). Transcriptional activation of transposable elements in mouse zygotes is independent of Tet3-mediated 5-methylcytosine oxidation. Cell Res. 22, 1640–1649.
| Transcriptional activation of transposable elements in mouse zygotes is independent of Tet3-mediated 5-methylcytosine oxidation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhslKrsb3E&md5=1387a3085710c12ae08469bf9c15fa32CAS | 23184059PubMed |
Jurka, J., Kapitonov, V. V., Pavlicek, A., Klonowski, P., Kohany, O., and Walichiewicz, J. (2005). Repbase Update, a database of eukaryotic repetitive elements. Cytogenet. Genome Res. 110, 462–467.
| Repbase Update, a database of eukaryotic repetitive elements.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2Mvislertw%3D%3D&md5=71a65d754f8026002ac5ecc625bcaf8fCAS | 16093699PubMed |
Kigami, D., Minami, N., Takayama, H., and Imai, H. (2003). MuERV-L is one of the earliest transcribed genes in mouse one-cell embryos. Biol. Reprod. 68, 651–654.
| MuERV-L is one of the earliest transcribed genes in mouse one-cell embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXntVCgsw%3D%3D&md5=5cd8e53be930a942e162b2000663da6aCAS | 12533431PubMed |
Kobayashi, H., Sakurai, T., Imai, M., Takahashi, N., Fukuda, A., Yayoi, O., and Kono, T. (2012). Contribution of intragenic DNA methylation in mouse gametic DNA methylomes to establish oocyte-specific heritable marks. PLoS Genet. 8, e1002440.
| Contribution of intragenic DNA methylation in mouse gametic DNA methylomes to establish oocyte-specific heritable marks.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVyitrg%3D&md5=a8a7a8c616fe6b3327b9feaa6f540222CAS | 22242016PubMed |
Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R., Thompson, J. D., Gibson, T. J., and Higgins, D. G. (2007). Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947–2948.
| Clustal W and Clustal X version 2.0.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlaqsL%2FM&md5=dca8f3edf29cd80c1dfcf85b861dc8a2CAS | 17846036PubMed |
Li, Y., and O’Neill, C. (2012). Persistence of cytosine methylation of DNA following fertilisation in the mouse. PLoS ONE 7, e30687.
| Persistence of cytosine methylation of DNA following fertilisation in the mouse.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xitlaqsb8%3D&md5=86e625c4ffb854e8dd144b981bb46242CAS | 22292019PubMed |
Li, N., Ye, M., Li, Y., Yan, Z., Butcher, L. M., Sun, J., Han, X., Chen, Q., Zhang, X., and Wang, J. (2010). Whole genome DNA methylation analysis based on high throughput sequencing technology. Methods 52, 203–212.
| Whole genome DNA methylation analysis based on high throughput sequencing technology.Crossref | GoogleScholarGoogle Scholar | 20430099PubMed |
McClintock, B. (1984). The significance of responses of the genome to challenge. Science 226, 792–801.
| The significance of responses of the genome to challenge.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2M7gvV2juw%3D%3D&md5=fee0829ea718689ddb43afd0ede5ea1eCAS | 15739260PubMed |
Moissiard, G., Cokus, S. J., Cary, J., Feng, S., Billi, A. C., Stroud, H., Husmann, D., Zhan, Y., Lajoie, B. R., and McCord, R. P. (2012). MORC family ATPases required for heterochromatin condensation and gene silencing. Science 336, 1448–1451.
| MORC family ATPases required for heterochromatin condensation and gene silencing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XotlCjsrg%3D&md5=d1d0a0bbae53fdac445debd8e2c7ddb6CAS | 22555433PubMed |
Morales, J. F., Snow, E. T., and Murnane, J. P. (2003). Environmental factors affecting transcription of the human L1 retrotransposon. II. Stressors. Mutagenesis 18, 151–158.
| Environmental factors affecting transcription of the human L1 retrotransposon. II. Stressors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXit12ltbc%3D&md5=595133c4a43e6cdc11ed951c9043844cCAS | 12621071PubMed |
Nakanishi, M. O., Hayakawa, K., Nakabayashi, K., Hata, K., Shiota, K., and Tanaka, S. (2012). Trophoblast-specific DNA methylation occurs after the segregation of the trophectoderm and inner cell mass in the mouse periimplantation embryo. Epigenetics 7, 173–182.
| Trophoblast-specific DNA methylation occurs after the segregation of the trophectoderm and inner cell mass in the mouse periimplantation embryo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XnsVKjtbo%3D&md5=d1bf55f9073d2045d6f12edff76a915eCAS | 22395467PubMed |
Okano, M., Xie, S., and Li, E. (1998). Cloning and characterization of a family of novel mammalian DNA (cytosine-5) methyltransferases. Nature genetics 19, 219–220.
| Cloning and characterization of a family of novel mammalian DNA (cytosine-5) methyltransferases.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXls1Sns7w%3D&md5=3b38ebd96c91d6203c38f31cd6c607a6CAS | 9662389PubMed |
Okano, M., Bell, D. W., Haber, D. A., and Li, E. (1999). DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99, 247–257.
| DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXnt1Gqsrc%3D&md5=fdaea9eda23862054886b06f0941ab45CAS | 10555141PubMed |
Ostertag, E. M., DeBerardinis, R. J., Goodier, J. L., Zhang, Y., Yang, N., Gerton, G. L., and Kazazian, H. H. (2002). A mouse model of human L1 retrotransposition. Nat. Genet. 32, 655–660.
| A mouse model of human L1 retrotransposition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XptVShtbY%3D&md5=0047116290475dc47c3bbf2fe1fa81f4CAS | 12415270PubMed |
Peaston, A. E., Evsikov, A. V., Graber, J. H., de Vries, W. N., Holbrook, A. E., Solter, D., and Knowles, B. B. (2004). Retrotransposons regulate host genes in mouse oocytes and preimplantation embryos. Dev. Cell 7, 597–606.
| Retrotransposons regulate host genes in mouse oocytes and preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXptlGjur4%3D&md5=45668691b386a9556101a5866dfa10b5CAS | 15469847PubMed |
Perillo, B., Ombra, M. N., Bertoni, A., Cuozzo, C., Sacchetti, S., Sasso, A., Chiariotti, L., Malorni, A., Abbondanza, C., and Avvedimento, E. V. (2008). DNA oxidation as triggered by H3K9me2 demethylation drives estrogen-induced gene expression. Science 319, 202–206.
| DNA oxidation as triggered by H3K9me2 demethylation drives estrogen-induced gene expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXis1amug%3D%3D&md5=72ad4876779e8b02e49557df3d2dfb93CAS | 18187655PubMed |
Raiz, J., Damert, A., Chira, S., Held, U., Klawitter, S., Hamdorf, M., Löwer, J., Strätling, W. H., Löwer, R., and Schumann, G. G. (2012). The non-autonomous retrotransposon SVA is trans-mobilized by the human LINE-1 protein machinery. Nucleic Acids Res. 40, 1666–1683.
| The non-autonomous retrotransposon SVA is trans-mobilized by the human LINE-1 protein machinery.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XjtlGksLs%3D&md5=8c5fe18db09b5297ac9546caf6e2dc4dCAS | 22053090PubMed |
Reik, W., Dean, W., and Walter, J. (2001). Epigenetic reprogramming in mammalian development. Science 293, 1089–1093.
| Epigenetic reprogramming in mammalian development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmtVWltL8%3D&md5=515f471e9704a69bd6eb622cea4426eeCAS | 11498579PubMed |
Rizos, D., Gutierrez-Adan, A., Perez-Garnelo, S., De La Fuente, J., Boland, M., and Lonergan, P. (2003). Bovine embryo culture in the presence or absence of serum: implications for blastocyst development, cryotolerance, and messenger RNA expression. Biol. Reprod. 68, 236–243.
| Bovine embryo culture in the presence or absence of serum: implications for blastocyst development, cryotolerance, and messenger RNA expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjtFWj&md5=36cd06bb3cfffc9b313839eb36bc0c50CAS | 12493719PubMed |
Rozen, S., and Skaletsky, H. (1999). Primer3 on the WWW for general users and for biologist programmers. In ‘Bioinformatics methods and protocols’. (Eds S. Misener and S. A. Krawetz.) pp. 365–86. (Springer: New Jersey.)
Santos, F., and Dean, W. (2006). Using immunofluorescence to observe methylation changes in mammalian preimplantation embryos. In ‘Nuclear Reprogramming’. (Eds S. Pells.) pp. 129–38. (Springer: New Jersey.)
Santos, F., Zakhartchenko, V., Stojkovic, M., Peters, A., Jenuwein, T., Wolf, E., Reik, W., and Dean, W. (2003). Epigenetic marking correlates with developmental potential in cloned bovine preimplantation embryos. Curr. Biol. 13, 1116–1121.
| Epigenetic marking correlates with developmental potential in cloned bovine preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXlt1entrY%3D&md5=60a0ec5f68ec715c9ade6ae3fb2d58a1CAS | 12842010PubMed |
Schulz, W. A. (2006). L1 retrotransposons in human cancers. BioMed Research International 2006, 83 672.
Shi, W., Dirim, F., Wolf, E., Zakhartchenko, V., and Haaf, T. (2004). Methylation reprogramming and chromosomal aneuploidy in in vivo fertilized and cloned rabbit preimplantation embryos. Biol. Reprod. 71, 340–347.
| Methylation reprogramming and chromosomal aneuploidy in in vivo fertilized and cloned rabbit preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXltFKrsr4%3D&md5=3952a747e7f4d87b6b66678f33da4807CAS | 15028628PubMed |
Shi, X., Seluanov, A., and Gorbunova, V. (2007). Cell divisions are required for L1 retrotransposition. Mol. Cell. Biol. 27, 1264–1270.
| Cell divisions are required for L1 retrotransposition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXit1amsr8%3D&md5=df064e0d5f9e12a7072fb40afd0bc26cCAS | 17145770PubMed |
Smith, Z. D., Chan, M. M., Mikkelsen, T. S., Gu, H., Gnirke, A., Regev, A., and Meissner, A. (2012). A unique regulatory phase of DNA methylation in the early mammalian embryo. Nature 484, 339–344.
| A unique regulatory phase of DNA methylation in the early mammalian embryo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xks1yrsbw%3D&md5=de248ce4dfeac66796f9c788a937d7f7CAS | 22456710PubMed |
Spadafora, C. (2004). Endogenous reverse transcriptase: a mediator of cell proliferation and differentiation. Cytogenet. Genome Res. 105, 346–350.
| Endogenous reverse transcriptase: a mediator of cell proliferation and differentiation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlsV2js7g%3D&md5=efdafba2d3afb37eedd5dd9e395bcbd0CAS | 15237222PubMed |
Sperber, G. O., Airola, T., Jern, P., and Blomberg, J. (2007). Automated recognition of retroviral sequences in genomic data: RetroTector©. Nucleic Acids Res. 35, 4964–4976.
| Automated recognition of retroviral sequences in genomic data: RetroTector©.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpvFWgsbg%3D&md5=2d43b9798aa284629dafed39da3c86d8CAS | 17636050PubMed |
Tam, O. H., Aravin, A. A., Stein, P., Girard, A., Murchison, E. P., Cheloufi, S., Hodges, E., Anger, M., Sachidanandam, R., and Schultz, R. M. (2008). Pseudogene-derived small interfering RNAs regulate gene expression in mouse oocytes. Nature 453, 534–538.
| Pseudogene-derived small interfering RNAs regulate gene expression in mouse oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmt1OrtLg%3D&md5=99af547c10bef9017c16680b6c21abfbCAS | 18404147PubMed |
Van Soom, A., Yuan, Y. Q., Peelman, L. J., de Matos, D. G., Dewulf, J., Laevens, H., and de Kruif, A. (2002). Prevalence of apoptosis and inner cell allocation in bovine embryos cultured under different oxygen tensions with or without cysteine addition. Theriogenology 57, 1453–1465.
| Prevalence of apoptosis and inner cell allocation in bovine embryos cultured under different oxygen tensions with or without cysteine addition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XkvVCntL4%3D&md5=19343b2377cc0b62ef66f836c711ff4eCAS | 12054204PubMed |
Vanden Berghe, W. (2012). Epigenetic impact of dietary polyphenols in cancer chemoprevention: lifelong remodeling of our epigenomes. Pharmacol. Res. 65, 565–576.
| Epigenetic impact of dietary polyphenols in cancer chemoprevention: lifelong remodeling of our epigenomes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XmtlSltrs%3D&md5=f9ba1037ad8cde00cbc3785726519910CAS | 22465217PubMed |
Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A., and Speleman, F. (2002). Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biology 3, research0034–research0034.11.
| Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes.Crossref | GoogleScholarGoogle Scholar | 12184808PubMed |
Watanabe, T., Totoki, Y., Toyoda, A., Kaneda, M., Kuramochi-Miyagawa, S., Obata, Y., Chiba, H., Kohara, Y., Kono, T., and Nakano, T. (2008). Endogenous siRNAs from naturally formed dsRNAs regulate transcripts in mouse oocytes. Nature 453, 539–543.
| Endogenous siRNAs from naturally formed dsRNAs regulate transcripts in mouse oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmt1OrtLk%3D&md5=74756cf2616f8b1bbc2cecc1b97aafdeCAS | 18404146PubMed |
Wheeler, D. L., Chappey, C., Lash, A. E., Leipe, D. D., Madden, T. L., Schuler, G. D., Tatusova, T. A., and Rapp, B. A. (2000). Database resources of the National Center for Biotechnology Information. Nucleic Acids Res. 28, 10–14.
| Database resources of the National Center for Biotechnology Information.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhvVGqurg%3D&md5=9c66720c87903679286b87ff418f3d62CAS | 10592169PubMed |
Wydooghe, E., Heras, S., Dewulf, J., Piepers, S., Van Den Abbeel, E., De Sutter, P., Vandaele, L., and Van Soom, A. (2014). Replacing serum in culture medium with albumin and insulin, transferrin and selenium is the key to successful bovine embryo development in individual culture. Reprod. Fertil. Dev. 26, 717–724.
| Replacing serum in culture medium with albumin and insulin, transferrin and selenium is the key to successful bovine embryo development in individual culture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtVentb3E&md5=ac2181e639ad18ac9c287705f93109e5CAS | 23711172PubMed |
Yang, N., and Kazazian, H. H. (2006). L1 retrotransposition is suppressed by endogenously encoded small interfering RNAs in human cultured cells. Nat. Struct. Mol. Biol. 13, 763–771.
| L1 retrotransposition is suppressed by endogenously encoded small interfering RNAs in human cultured cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XptFWiur0%3D&md5=b92fc2de653c756483113dd1613f1a24CAS | 16936727PubMed |
Yoder, J. A., Walsh, C. P., and Bestor, T. H. (1997). Cytosine methylation and the ecology of intragenomic parasites. Trends Genet. 13, 335–340.
| Cytosine methylation and the ecology of intragenomic parasites.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXlt1Ggu78%3D&md5=33b8d5810d1ac1460affb50b3c786c85CAS | 9260521PubMed |
Yuan, Y. Q., Van Soom, A., Coopman, F. O. J., Mintiens, K., Boerjan, M. L., Van Zeveren, A., de Kruif, A., and Peelman, L. J. (2003). Influence of oxygen tension on apoptosis and hatching in bovine embryos cultured in vitro. Theriogenology 59, 1585–1596.
| Influence of oxygen tension on apoptosis and hatching in bovine embryos cultured in vitro.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3s%2FltFSrsA%3D%3D&md5=5b4510152a75c8cb463a511b67ebabe1CAS | 12559463PubMed |
Zuker, M. (2003). Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 31, 3406–3415.
| Mfold web server for nucleic acid folding and hybridization prediction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXltVWisr8%3D&md5=0c12a546725f6c8ed64e575bfbd108b2CAS | 12824337PubMed |
