Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Imprinted and DNA methyltransferase gene expression in the endometrium during the pre- and peri-implantation period in cattle

A. M. O’Doherty A D , L. C. O’Shea A , O. Sandra B , P. Lonergan A , T. Fair A and N. Forde C
+ Author Affiliations
- Author Affiliations

A School of Agriculture and Food Science, University College Dublin, Belfield, Dublin 4, D04 V1W8, Ireland.

B Institut National de la Recherche Agronomique (INRA), UMR 1198 Biologie du Développement et Reproduction, F-78350 Jouy en Josas, France.

C Division of Reproduction and Early Development, Leeds Institute of Cardiovascular and Molecular Medicine, School of Medicine, University of Leeds, Clarendon Way, Leeds, LS2 9JT, UK.

D Corresponding author. Email: alan.odoherty@ucd.ie

Reproduction, Fertility and Development - https://doi.org/10.1071/RD16238
Submitted: 13 December 2015  Accepted: 24 August 2016   Published online: 21 September 2016

Abstract

The endometrium plays a key role in providing an optimal environment for attachment of the preimplantation embryo during the early stages of pregnancy. Investigations over the past 2 decades have demonstrated that vital epigenetic processes occur in the embryo during the preimplantation stages of development. However, few studies have investigated the potential role of imprinted genes and their associated modulators, the DNA methyltransferases (DNMTs), in the bovine endometrium during the pre- and peri-implantation period. Therefore, in the present study we examined the expression profiles of the DNMT genes (3A, 3A2 and 3B) and a panel of the most comprehensively studied imprinted genes in the endometrium of cyclic and pregnant animals. Intercaruncular (Days 5, 7, 13, 16 and 20) and caruncular (Days 16 and 20) regions were analysed for gene expression changes, with protein analysis also performed for DNMT3A, DNMT3A2 and DNMT3B on Days 16 and 20. An overall effect of day was observed for expression of several of the imprinted genes. Tissue-dependent gene expression was detected for all genes at Day 20. Differences in DNMT protein abundance were mostly observed in the intercaruncular regions of pregnant heifers at Day 16 when DNMT3A, DNMT3A2 and DNMT3B were all lower when compared with cyclic controls. At Day 20, DNMT3A2 expression was lower in the pregnant caruncular samples compared with cyclic animals. This study provides evidence that epigenetic mechanisms in the endometrium may be involved with implantation of the embryo during the early stages of pregnancy in cattle.

Additional keywords: bovine, imprinting, pregnancy.


References

Agoston, A. T., Argani, P., Yegnasubramanian, S., De Marzo, A. M., Ansari-Lari, M. A., Hicks, J. L., Davidson, N. E., and Nelson, W. G. (2005). Increased protein stability causes DNA methyltransferase 1 dysregulation in breast cancer. J. Biol. Chem. 280, 18302–18310.
Increased protein stability causes DNA methyltransferase 1 dysregulation in breast cancer.CrossRef | 1:CAS:528:DC%2BD2MXjsl2ht78%3D&md5=f1aa87839035f067d21ac21b06ed95e7CAS | 15755728PubMed | open url image1

Anckaert, E., and Fair, T. (2015). DNA methylation reprogramming during oogenesis and interference by reproductive technologies: studies in mouse and bovine models. Reprod. Fertil. Dev. 27, 739–754.
DNA methylation reprogramming during oogenesis and interference by reproductive technologies: studies in mouse and bovine models.CrossRef | 1:CAS:528:DC%2BC2MXps1Oks7w%3D&md5=b64ac1b6571ad3c025bc6f061096bb74CAS | 25976160PubMed | open url image1

Barlow, D. P., and Bartolomei, M. S. (2014). Genomic imprinting in mammals. Cold Spring Harb. Perspect. Biol. 6, a018382.
Genomic imprinting in mammals.CrossRef | 24492710PubMed | open url image1

Bauersachs, S., Ulbrich, S. E., Zakhartchenko, V., Minten, M., Reichenbach, M., Reichenbach, H. D., Blum, H., Spencer, T. E., and Wolf, E. (2009). The endometrium responds differently to cloned versus fertilized embryos. Proc. Natl. Acad. Sci. USA 106, 5681–5686.
The endometrium responds differently to cloned versus fertilized embryos.CrossRef | 1:CAS:528:DC%2BD1MXkvFGhurk%3D&md5=0371dae48afb2d5c9d4f14f7982d86d7CAS | 19307558PubMed | open url image1

Bauersachs, S., Ulbrich, S. E., Reichenbach, H. D., Reichenbach, M., Buttner, M., Meyer, H. H., Spencer, T. E., Minten, M., Sax, G., Winter, G., and Wolf, E. (2012). Comparison of the effects of early pregnancy with human interferon, alpha 2 (IFNA2), on gene expression in bovine endometrium. Biol. Reprod. 86, 46.
Comparison of the effects of early pregnancy with human interferon, alpha 2 (IFNA2), on gene expression in bovine endometrium.CrossRef | 22034527PubMed | open url image1

Bazer, F. W. (1992). Mediators of maternal recognition of pregnancy in mammals. Proc. Soc. Exp. Biol. Med. 199, 373–384.
Mediators of maternal recognition of pregnancy in mammals.CrossRef | 1:CAS:528:DyaK38XhvVyisL4%3D&md5=ced099b23dd18298c6108349915a0d6fCAS | 1549616PubMed | open url image1

Blondin, P., Farin, P. W., Crosier, A. E., Alexander, J. E., and Farin, C. E. (2000). In vitro production of embryos alters levels of insulin-like growth factor-II messenger ribonucleic acid in bovine fetuses 63 days after transfer. Biol. Reprod. 62, 384–389.
In vitro production of embryos alters levels of insulin-like growth factor-II messenger ribonucleic acid in bovine fetuses 63 days after transfer.CrossRef | 1:CAS:528:DC%2BD3cXotVOqtg%3D%3D&md5=deac4a4813a4c04321765bea5b66464fCAS | 10642577PubMed | open url image1

Bourc’his, D., and Bestor, T. H. (2004). Meiotic catastrophe and retrotransposon reactivation in male germ cells lacking DNMT3L. Nature 431, 96–99.
Meiotic catastrophe and retrotransposon reactivation in male germ cells lacking DNMT3L.CrossRef | 1:CAS:528:DC%2BD2cXntFCksrc%3D&md5=9e2af54c49916a808b7a60e932bf08fcCAS | 15318244PubMed | open url image1

Carter, F., Forde, N., Duffy, P., Wade, M., Fair, T., Crowe, M. A., Evans, A. C., Kenny, D. A., Roche, J. F., and Lonergan, P. (2008). Effect of increasing progesterone concentration from Day 3 of pregnancy on subsequent embryo survival and development in beef heifers. Reprod. Fertil. Dev. 20, 368–375.
Effect of increasing progesterone concentration from Day 3 of pregnancy on subsequent embryo survival and development in beef heifers.CrossRef | 1:CAS:528:DC%2BD1cXjtVKksLg%3D&md5=9f36e54c3ba6d9f4d0e6bb5a011eead2CAS | 18402756PubMed | open url image1

Chavatte-Palmer, P., and Guillomot, M. (2007). Comparative implantation and placentation. Gynecol. Obstet. Invest. 64, 166–174.
Comparative implantation and placentation.CrossRef | 17934314PubMed | open url image1

Coan, P. M., Burton, G. J., and Ferguson-Smith, A. C. (2005). Imprinted genes in the placenta – a review. Placenta 26, S10–S20.
Imprinted genes in the placenta – a review.CrossRef | 15837057PubMed | open url image1

Degrelle, S. A., Campion, E., Cabau, C., Piumi, F., Reinaud, P., Richard, C., Renard, J. P., and Hue, I. (2005). Molecular evidence for a critical period in mural trophoblast development in bovine blastocysts. Dev. Biol. 288, 448–460.
Molecular evidence for a critical period in mural trophoblast development in bovine blastocysts.CrossRef | 1:CAS:528:DC%2BD2MXhtlaitrjN&md5=bb04f93c61cbd04b7eabcb674f27d220CAS | 16289134PubMed | open url image1

Diskin, M. G., Murphy, J. J., and Sreenan, J. M. (2006). Embryo survival in dairy cows managed under pastoral conditions. Anim. Reprod. Sci. 96, 297–311.
Embryo survival in dairy cows managed under pastoral conditions.CrossRef | 1:STN:280:DC%2BD28nitFGgsg%3D%3D&md5=9da43b8ff83dc815755f2b99f5fe3c1aCAS | 16963203PubMed | open url image1

Dorniak, P., Bazer, F. W., and Spencer, T. E. (2011). Prostaglandins regulate conceptus elongation and mediate effects of interferon tau on the ovine uterine endometrium. Biol. Reprod. 84, 1119–1127.
Prostaglandins regulate conceptus elongation and mediate effects of interferon tau on the ovine uterine endometrium.CrossRef | 1:CAS:528:DC%2BC3MXmvFemur4%3D&md5=77561c66e096ea07162d4d8ceb8548f8CAS | 21270428PubMed | open url image1

Dorniak, P., Bazer, F. W., Wu, G., and Spencer, T. E. (2012). Conceptus-derived prostaglandins regulate endometrial function in sheep. Biol. Reprod. 87, 9.
Conceptus-derived prostaglandins regulate endometrial function in sheep.CrossRef | 22517622PubMed | open url image1

Eozenou, C., Vitorino Carvalho, A., Forde, N., Giraud-Delville, C., Gall, L., Lonergan, P., Auguste, A., Charpigny, G., Richard, C., Pannetier, M., and Sandra, O. (2012). FOXL2 is regulated during the bovine estrous cycle and its expression in the endometrium is independent of conceptus-derived interferon tau. Biol. Reprod. 87, 32.
FOXL2 is regulated during the bovine estrous cycle and its expression in the endometrium is independent of conceptus-derived interferon tau.CrossRef | 22623620PubMed | open url image1

Farin, C. E., Farmer, W. T., and Farin, P. W. (2010). Pregnancy recognition and abnormal offspring syndrome in cattle. Reprod. Fertil. Dev. 22, 75–87.
Pregnancy recognition and abnormal offspring syndrome in cattle.CrossRef | 1:CAS:528:DC%2BC3cXitlagurc%3D&md5=3430dcc8102cd43862ec219b65b8bc7aCAS | 20003848PubMed | open url image1

Ferguson-Smith, A. C., and Surani, M. A. (2001). Imprinting and the epigenetic asymmetry between parental genomes. Science 293, 1086–1089.
Imprinting and the epigenetic asymmetry between parental genomes.CrossRef | 1:CAS:528:DC%2BD3MXmtVWlt7c%3D&md5=b9a1ed1af538fb5b1b71445bb85b391bCAS | 11498578PubMed | open url image1

Forde, N., and Lonergan, P. (2012). Transcriptomic analysis of the bovine endometrium: what is required to establish uterine receptivity to implantation in cattle? J. Reprod. Dev. 58, 189–195.
Transcriptomic analysis of the bovine endometrium: what is required to establish uterine receptivity to implantation in cattle?CrossRef | 1:CAS:528:DC%2BC38XptVKju7Y%3D&md5=ca6d5d99937becc018e85524657403d7CAS | 22738902PubMed | open url image1

Forde, N., Carter, F., Spencer, T. E., Bazer, F. W., Sandra, O., Mansouri-Attia, N., Okumu, L. A., McGettigan, P. A., Mehta, J. P., McBride, R., O’Gaora, P., Roche, J. F., and Lonergan, P. (2011). Conceptus-induced changes in the endometrial transcriptome: how soon does the cow know she is pregnant? Biol. Reprod. 85, 144–156.
Conceptus-induced changes in the endometrial transcriptome: how soon does the cow know she is pregnant?CrossRef | 1:CAS:528:DC%2BC3MXotFOlsL4%3D&md5=744617d7d69d36353abdff26816cf55bCAS | 21349821PubMed | open url image1

Fowden, A. L., Sibley, C., Reik, W., and Constancia, M. (2006). Imprinted genes, placental development and fetal growth. Horm. Res. 65, 50–58.
Imprinted genes, placental development and fetal growth.CrossRef | 1:CAS:528:DC%2BD28XksV2isb0%3D&md5=4b8fb1705a14538ac935871d395e709eCAS | 16612114PubMed | open url image1

Frost, J. M., and Moore, G. E. (2010). The importance of imprinting in the human placenta. PLoS Genet. 6, e1001015.
The importance of imprinting in the human placenta.CrossRef | 20617174PubMed | open url image1

Gharib-Hamrouche, N., Chene, N., Guillomot, M., and Martal, J. (1993). Localization and characterization of EGF/TGF-alpha receptors on peri-implantation trophoblast in sheep. J. Reprod. Fertil. 98, 385–392.
Localization and characterization of EGF/TGF-alpha receptors on peri-implantation trophoblast in sheep.CrossRef | 1:CAS:528:DyaK3sXms1egurg%3D&md5=6be211ff1eb334e08061c3b2df6b42d1CAS | 8410802PubMed | open url image1

Hitchins, M. P., and Moore, G. E. (2002). Genomic imprinting in fetal growth and development. Expert Rev. Mol. Med. 4, 1–19.
Genomic imprinting in fetal growth and development.CrossRef | 14987379PubMed | open url image1

Hiura, H., Obata, Y., Komiyama, J., Shirai, M., and Kono, T. (2006). Oocyte growth-dependent progression of maternal imprinting in mice. Genes Cells 11, 353–361.
Oocyte growth-dependent progression of maternal imprinting in mice.CrossRef | 1:CAS:528:DC%2BD28Xkt1Gktr8%3D&md5=3b6a0a740308ef693ae7b9a2398b6911CAS | 16611239PubMed | open url image1

Humpherys, D., Eggan, K., Akutsu, H., Hochedlinger, K., Rideout, W. M., Biniszkiewicz, D., Yanagimachi, R., and Jaenisch, R. (2001). Epigenetic instability in ES cells and cloned mice. Science 293, 95–97.
Epigenetic instability in ES cells and cloned mice.CrossRef | 1:CAS:528:DC%2BD3MXltFCntL4%3D&md5=f6fd5d448ed7d0a35c5d024245c91612CAS | 11441181PubMed | open url image1

Jiang, Z., Dong, H., Zheng, X., Marjani, S. L., Donovan, D. M., Chen, J., and Tian, X. C. (2015). mRNA levels of imprinted genes in bovine in vivo oocytes, embryos and cross species comparisons with humans, mice and pigs. Sci. Rep. 5, 17898.
mRNA levels of imprinted genes in bovine in vivo oocytes, embryos and cross species comparisons with humans, mice and pigs.CrossRef | 1:CAS:528:DC%2BC2MXhvFyks7nF&md5=caad1b23fd8a017fe1801e1ce250a67aCAS | 26638780PubMed | open url image1

Kaneda, M., Okano, M., Hata, K., Sado, T., Tsujimoto, N., Li, E., and Sasaki, H. (2004). Essential role for de novo DNA methyltransferase DNMT3a in paternal and maternal imprinting. Nature 429, 900–903.
Essential role for de novo DNA methyltransferase DNMT3a in paternal and maternal imprinting.CrossRef | 1:CAS:528:DC%2BD2cXltVKltL8%3D&md5=ff77529507630fbbbdc2e9154d75d7e1CAS | 15215868PubMed | open url image1

Keverne, E. B. (2015). Genomic imprinting, action, and interaction of maternal and fetal genomes. Proc. Natl. Acad. Sci. USA 112, 6834–6840.
Genomic imprinting, action, and interaction of maternal and fetal genomes.CrossRef | 1:CAS:528:DC%2BC2cXhvFans7fN&md5=6a2b74348c638f4047184d45c44a3ad9CAS | 25404322PubMed | open url image1

Korucuoglu, U., Biri, A. A., Konac, E., Alp, E., Onen, I. H., Ilhan, M. N., Turkyilmaz, E., Erdem, A., Erdem, M., and Menevse, S. (2010). Expression of the imprinted IGF2 and H19 genes in the endometrium of cases with unexplained infertility. Eur. J. Obstet. Gynecol. Reprod. Biol. 149, 77–81.
Expression of the imprinted IGF2 and H19 genes in the endometrium of cases with unexplained infertility.CrossRef | 1:CAS:528:DC%2BC3cXhvFGit78%3D&md5=6c5742b10e76f328abcae057afba956cCAS | 20042264PubMed | open url image1

Li, J., and Roberts, R. M. (1994). Interferon-tau and interferon-alpha interact with the same receptors in bovine endometrium. Use of a readily iodinatable form of recombinant interferon-tau for binding studies. J. Biol. Chem. 269, 13544–13550.
| 1:CAS:528:DyaK2cXjt1WitLw%3D&md5=3dcfbb54eea69f65a8a5b85123816332CAS | 8175789PubMed | open url image1

Li, E., Bestor, T. H., and Jaenisch, R. (1992). Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 69, 915–926.
Targeted mutation of the DNA methyltransferase gene results in embryonic lethality.CrossRef | 1:CAS:528:DyaK38XksVGgsr0%3D&md5=78e220d181b54234250ed26f6520f037CAS | 1606615PubMed | open url image1

Li, E., Beard, C., and Jaenisch, R. (1993). Role for DNA methylation in genomic imprinting. Nature 366, 362–365.
Role for DNA methylation in genomic imprinting.CrossRef | 1:CAS:528:DyaK2cXlsFCm&md5=1377ad9aadbe5db960d95cca38aabd9cCAS | 8247133PubMed | open url image1

Li, J. Y., Lees-Murdock, D. J., Xu, G. L., and Walsh, C. P. (2004). Timing of establishment of paternal methylation imprints in the mouse. Genomics 84, 952–960.
Timing of establishment of paternal methylation imprints in the mouse.CrossRef | 1:CAS:528:DC%2BD2cXptlyktrs%3D&md5=050cc67703a9c1d273207715371c4acaCAS | 15533712PubMed | open url image1

Lin, R. K., Hsieh, Y. S., Lin, P., Hsu, H. S., Chen, C. Y., Tang, Y. A., Lee, C. F., and Wang, Y. C. (2010). The tobacco-specific carcinogen NNK induces DNA methyltransferase 1 accumulation and tumor suppressor gene hypermethylation in mice and lung cancer patients. J. Clin. Invest. 120, 521–532.
The tobacco-specific carcinogen NNK induces DNA methyltransferase 1 accumulation and tumor suppressor gene hypermethylation in mice and lung cancer patients.CrossRef | 1:CAS:528:DC%2BC3cXhsVOktLs%3D&md5=a15d608a92935f2a05b0de5c5a94a48aCAS | 20093774PubMed | open url image1

Lucifero, D., Mertineit, C., Clarke, H. J., Bestor, T. H., and Trasler, J. M. (2002). Methylation dynamics of imprinted genes in mouse germ cells. Genomics 79, 530–538.
Methylation dynamics of imprinted genes in mouse germ cells.CrossRef | 1:CAS:528:DC%2BD38Xis1yhu7o%3D&md5=b578c5b7d09b0792db81e4258db3b9e2CAS | 11944985PubMed | open url image1

Lucifero, D., Suzuki, J., Bordignon, V., Martel, J., Vigneault, C., Therrien, J., Filion, F., Smith, L. C., and Trasler, J. M. (2006). Bovine SNRPN methylation imprint in oocytes and Day 17 in vitro-produced and somatic cell nuclear transfer embryos. Biol. Reprod. 75, 531–538.
Bovine SNRPN methylation imprint in oocytes and Day 17 in vitro-produced and somatic cell nuclear transfer embryos.CrossRef | 1:CAS:528:DC%2BD28XhtVCgs73P&md5=5fd24c321dbc043921d6c7b25251bc61CAS | 16790688PubMed | open url image1

Mamo, S., Mehta, J. P., McGettigan, P., Fair, T., Spencer, T. E., Bazer, F. W., and Lonergan, P. (2011). RNA sequencing reveals novel gene clusters in bovine conceptuses associated with maternal recognition of pregnancy and implantation. Biol. Reprod. 85, 1143–1151.
RNA sequencing reveals novel gene clusters in bovine conceptuses associated with maternal recognition of pregnancy and implantation.CrossRef | 1:CAS:528:DC%2BC3MXhs1ShsLbO&md5=d704d967c4aed7c2a72330e5e7d3ca39CAS | 21795669PubMed | open url image1

Mann, M. R., Chung, Y. G., Nolen, L. D., Verona, R. I., Latham, K. E., and Bartolomei, M. S. (2003). Disruption of imprinted gene methylation and expression in cloned preimplantation stage mouse embryos. Biol. Reprod. 69, 902–914.
Disruption of imprinted gene methylation and expression in cloned preimplantation stage mouse embryos.CrossRef | 1:CAS:528:DC%2BD3sXmvVeitbw%3D&md5=e4c56f99906cf4de3b9b05ec627f5224CAS | 12748125PubMed | open url image1

Mansouri-Attia, N., Aubert, J., Reinaud, P., Giraud-Delville, C., Taghouti, G., Galio, L., Everts, R. E., Degrelle, S., Richard, C., Hue, I., Yang, X., Tian, X. C., Lewin, H. A., Renard, J. P., and Sandra, O. (2009a). Gene expression profiles of bovine caruncular and intercaruncular endometrium at implantation. Physiol. Genomics 39, 14–27.
Gene expression profiles of bovine caruncular and intercaruncular endometrium at implantation.CrossRef | 1:CAS:528:DC%2BC3cXhtlakt7rM&md5=678c17a879ea3aa54e62ac07fb3c6cbbCAS | 19622795PubMed | open url image1

Mansouri-Attia, N., Sandra, O., Aubert, J., Degrelle, S., Everts, R. E., Giraud-Delville, C., Heyman, Y., Galio, L., Hue, I., Yang, X., Tian, X. C., Lewin, H. A., and Renard, J. P. (2009b). Endometrium as an early sensor of in vitro embryo manipulation technologies. Proc. Natl. Acad. Sci. USA 106, 5687–5692.
Endometrium as an early sensor of in vitro embryo manipulation technologies.CrossRef | 1:CAS:528:DC%2BD1MXkvFGhurY%3D&md5=29f9b4c92a2eaa8e665f1240c1b1c669CAS | 19297625PubMed | open url image1

Moore, G. E., Ishida, M., Demetriou, C., Al-Olabi, L., Leon, L. J., Thomas, A. C., Abu-Amero, S., Frost, J. M., Stafford, J. L., Chaoqun, Y., Duncan, A. J., Baigel, R., Brimioulle, M., Iglesias-Platas, I., Apostolidou, S., Aggarwal, R., Whittaker, J. C., Syngelaki, A., Nicolaides, K. H., Regan, L., Monk, D., and Stanier, P. (2015). The role and interaction of imprinted genes in human fetal growth. Philos. Trans. R. Soc. Lond. B Biol. Sci. 370, 20140074.
The role and interaction of imprinted genes in human fetal growth.CrossRef | 1:CAS:528:DC%2BC2MXktVOhsL8%3D&md5=6926e94e0196c95822f612bb74368068CAS | 25602077PubMed | open url image1

O’Doherty, A. M., and McGettigan, P. A. (2015). Epigenetic processes in the male germline. Reprod. Fertil. Dev. 27, 725–738.
Epigenetic processes in the male germline.CrossRef | 25200708PubMed | open url image1

O’Doherty, A. M., O’Shea, L. C., and Fair, T. (2012). Bovine DNA methylation imprints are established in an oocyte size-specific manner, which are coordinated with the expression of the DNMT3 family proteins. Biol. Reprod. 86, 67.
Bovine DNA methylation imprints are established in an oocyte size-specific manner, which are coordinated with the expression of the DNMT3 family proteins.CrossRef | 22088914PubMed | open url image1

O’Doherty, A. M., O’Gorman, A., Al Naib, A., Brennan, L., Daly, E., Duffy, P., and Fair, T. (2014). Negative energy balance affects imprint stability in oocytes recovered from postpartum dairy cows. Genomics 104, 177–185.
Negative energy balance affects imprint stability in oocytes recovered from postpartum dairy cows.CrossRef | 1:CAS:528:DC%2BC2cXht1Kkur7L&md5=98ad7481a7bca85032592776ba89c3e7CAS | 25084396PubMed | open url image1

O’Doherty, A. M., Magee, D. A., O’Shea, L. C., Forde, N., Beltman, M. E., Mamo, S., and Fair, T. (2015). DNA methylation dynamics at imprinted genes during bovine pre-implantation embryo development. BMC Dev. Biol. 15, 13.
DNA methylation dynamics at imprinted genes during bovine pre-implantation embryo development.CrossRef | 25881176PubMed | open url image1

O’Hara, L., Scully, S., Maillo, V., Kelly, A. K., Duffy, P., Carter, F., Forde, N., Rizos, D., and Lonergan, P. (2012). Effect of follicular aspiration just before ovulation on corpus luteum characteristics, circulating progesterone concentrations and uterine receptivity in single-ovulating and superstimulated heifers. Reproduction 143, 673–682.
Effect of follicular aspiration just before ovulation on corpus luteum characteristics, circulating progesterone concentrations and uterine receptivity in single-ovulating and superstimulated heifers.CrossRef | 1:CAS:528:DC%2BC38XnvFKqsL8%3D&md5=aa05b7b39b0ba043246be56aef3b7fd9CAS | 22367589PubMed | open url image1

O’Hara, L., Forde, N., Carter, F., Rizos, D., Maillo, V., Ealy, A. D., Kelly, A. K., Rodriguez, P., Isaka, N., Evans, A. C., and Lonergan, P. (2014). Paradoxical effect of supplementary progesterone between Day 3 and Day 7 on corpus luteum function and conceptus development in cattle. Reprod. Fertil. Dev. 26, 328–336.
Paradoxical effect of supplementary progesterone between Day 3 and Day 7 on corpus luteum function and conceptus development in cattle.CrossRef | 1:CAS:528:DC%2BC2cXjtFCmtw%3D%3D&md5=2eee26e309777963093f19d378dea06bCAS | 23439105PubMed | open url image1

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 | 1:CAS:528:DyaK1MXnt1Gqsrc%3D&md5=062fbec0cdf783eb8494b95e283dc6caCAS | 10555141PubMed | open url image1

Ooi, S. K., O’Donnell, A. H., and Bestor, T. H. (2009). Mammalian cytosine methylation at a glance. J. Cell Sci. 122, 2787–2791.
Mammalian cytosine methylation at a glance.CrossRef | 1:CAS:528:DC%2BD1MXhtFOgsb7L&md5=ad0e8b65015f75b71fa25bfc42d76bffCAS | 19657014PubMed | open url image1

Reik, W., and Walter, J. (2001). Genomic imprinting: parental influence on the genome. Nat. Rev. Genet. 2, 21–32.
Genomic imprinting: parental influence on the genome.CrossRef | 1:CAS:528:DC%2BD3MXisVGjs70%3D&md5=35ea0c747629435348df7e98e7e62257CAS | 11253064PubMed | open url image1

Reik, W., Constancia, M., Fowden, A., Anderson, N., Dean, W., Ferguson-Smith, A., Tycko, B., and Sibley, C. (2003). Regulation of supply and demand for maternal nutrients in mammals by imprinted genes. J. Physiol. 547, 35–44.
Regulation of supply and demand for maternal nutrients in mammals by imprinted genes.CrossRef | 1:CAS:528:DC%2BD3sXivFSktro%3D&md5=0bfd4932fc6dc7e1f5a75deacc74a853CAS | 12562908PubMed | open url image1

Sandra, O., Bataillon, I., Roux, P., Martal, J., Charpigny, G., Reinaud, P., Bolifraud, P., Germain, G., and Al-Gubory, K. H. (2005). Suppressor of cytokine signalling (SOCS) genes are expressed in the endometrium and regulated by conceptus signals during early pregnancy in the ewe. J. Mol. Endocrinol. 34, 637–644.
Suppressor of cytokine signalling (SOCS) genes are expressed in the endometrium and regulated by conceptus signals during early pregnancy in the ewe.CrossRef | 1:CAS:528:DC%2BD2MXlslCisr4%3D&md5=00c5dfd6dd5be3c8e69e5ad9463ae5e7CAS | 15956335PubMed | open url image1

Spencer, T. E., Forde, N., Dorniak, P., Hansen, T. R., Romero, J. J., and Lonergan, P. (2013). Conceptus-derived prostaglandins regulate gene expression in the endometrium prior to pregnancy recognition in ruminants. Reproduction 146, 377–387.
Conceptus-derived prostaglandins regulate gene expression in the endometrium prior to pregnancy recognition in ruminants.CrossRef | 1:CAS:528:DC%2BC3sXhs1ygtr3P&md5=eed54514d961ef47412ace4913f6278bCAS | 23966582PubMed | open url image1

Starbuck, M. J., Dailey, R. A., and Inskeep, E. K. (2004). Factors affecting retention of early pregnancy in dairy cattle. Anim. Reprod. Sci. 84, 27–39.
Factors affecting retention of early pregnancy in dairy cattle.CrossRef | 15302385PubMed | open url image1

Van Soom, A., Vandaele, L., Goossens, K., Heras, S., Wydooghe, E., Rahman, M. B., Kamal, M. M., Van Eetvelde, M., Opsomer, G., and Peelman, L. (2013). Epigenetics and the periconception environment in ruminants. Proceedings of the Belgian Royal Academies of Medicine 2, 1–23. open url image1

Vincent, Z. L., Farquhar, C. M., Mitchell, M. D., and Ponnampalam, A. P. (2011). Expression and regulation of DNA methyltransferases in human endometrium. Fertil. Steril. 95, 1522–1525.e1.
Expression and regulation of DNA methyltransferases in human endometrium.CrossRef | 1:CAS:528:DC%2BC3MXjs1CktLc%3D&md5=c0558cd2d8a879d8962f21d5b37b3239CAS | 20970125PubMed | open url image1

Vitorino Carvalho, A., Reinaud, P., Forde, N., Healey, G. D., Eozenou, C., Giraud-Delville, C., Mansouri-Attia, N., Gall, L., Richard, C., Lonergan, P., Sheldon, I. M., Lea, R. G., and Sandra, O. (2014). SOCS genes expression during physiological and perturbed implantation in bovine endometrium. Reproduction 148, 545–557.
SOCS genes expression during physiological and perturbed implantation in bovine endometrium.CrossRef | open url image1

Vitorino Carvalho, A., Eozenou, C., Healey, G. D., Forde, N., Reinaud, P., Chebrout, M., Gall, L., Rodde, N., Padilla, A. L., Delville, C. G., Leveugle, M., Richard, C., Sheldon, I. M., Lonergan, P., Jolivet, G., and Sandra, O. (2016). Analysis of STAT1 expression and biological activity reveals interferon-tau-dependent STAT1-regulated SOCS genes in the bovine endometrium. Reprod. Fertil. Dev. 28, 459–474.
Analysis of STAT1 expression and biological activity reveals interferon-tau-dependent STAT1-regulated SOCS genes in the bovine endometrium.CrossRef | 1:STN:280:DC%2BC2M%2Fht1OqtA%3D%3D&md5=f914e13f16c85af3f3306ee39934b563CAS | 25116692PubMed | open url image1

Webster, K. E., O’Bryan, M. K., Fletcher, S., Crewther, P. E., Aapola, U., Craig, J., Harrison, D. K., Aung, H., Phutikanit, N., Lyle, R., Meachem, S. J., Antonarakis, S. E., de Kretser, D. M., Hedger, M. P., Peterson, P., Carroll, B. J., and Scott, H. S. (2005). Meiotic and epigenetic defects in DNMT3L-knockout mouse spermatogenesis. Proc. Natl. Acad. Sci. USA 102, 4068–4073.
Meiotic and epigenetic defects in DNMT3L-knockout mouse spermatogenesis.CrossRef | 1:CAS:528:DC%2BD2MXis12jtr8%3D&md5=4484fed47077b09660c4eb2f5559b363CAS | 15753313PubMed | open url image1

Wei, Y., Zhu, J., Huan, Y., Liu, Z., Yang, C., Zhang, X., Mu, Y., Xia, P., and Liu, Z. (2010). Aberrant expression and methylation status of putatively imprinted genes in placenta of cloned piglets. Cell. Reprogram. 12, 213–222.
Aberrant expression and methylation status of putatively imprinted genes in placenta of cloned piglets.CrossRef | 1:CAS:528:DC%2BC3cXlvVahtLg%3D&md5=216d1df539710607bf9223493bf96c99CAS | 20677935PubMed | open url image1

Wilmut, I., Beaujean, N., de Sousa, P. A., Dinnyes, A., King, T. J., Paterson, L. A., Wells, D. N., and Young, L. E. (2002). Somatic cell nuclear transfer. Nature 419, 583–587.
Somatic cell nuclear transfer.CrossRef | 1:CAS:528:DC%2BD38Xns1Ont7Y%3D&md5=ca25010a67e8d0b9a5d606ca383503b2CAS | 12374931PubMed | open url image1

Wu, Y., Strawn, E., Basir, Z., Halverson, G., and Guo, S. W. (2007). Aberrant expression of deoxyribonucleic acid methyltransferases DNMT1, DNMT3A, and DNMT3B in women with endometriosis. Fertil. Steril. 87, 24–32.
Aberrant expression of deoxyribonucleic acid methyltransferases DNMT1, DNMT3A, and DNMT3B in women with endometriosis.CrossRef | 1:CAS:528:DC%2BD2sXhvVSlsLw%3D&md5=ac79067a52641a9777c07df26a7278e3CAS | 17081533PubMed | open url image1

Yamagata, Y., Asada, H., Tamura, I., Lee, L., Maekawa, R., Taniguchi, K., Taketani, T., Matsuoka, A., Tamura, H., and Sugino, N. (2009). DNA methyltransferase expression in the human endometrium: down-regulation by progesterone and estrogen. Hum. Reprod. 24, 1126–1132.
DNA methyltransferase expression in the human endometrium: down-regulation by progesterone and estrogen.CrossRef | 1:CAS:528:DC%2BD1MXksFeju7w%3D&md5=bfb4a20ca49cdfd35d7019969ddfa57dCAS | 19202141PubMed | open url image1

Yoder, J. A., Soman, N. S., Verdine, G. L., and Bestor, T. H. (1997). DNA (cytosine-5)-methyltransferases in mouse cells and tissues. Studies with a mechanism-based probe. J. Mol. Biol. 270, 385–395.
DNA (cytosine-5)-methyltransferases in mouse cells and tissues. Studies with a mechanism-based probe.CrossRef | 1:CAS:528:DyaK2sXltFCku78%3D&md5=a6fb7d4de63937040dd6fc4ad2b1daabCAS | 9237905PubMed | open url image1

Young, L. E., Fernandes, K., McEvoy, T. G., Butterwith, S. C., Gutierrez, C. G., Carolan, C., Broadbent, P. J., Robinson, J. J., Wilmut, I., and Sinclair, K. D. (2001). Epigenetic change in IGF2R is associated with fetal overgrowth after sheep embryo culture. Nat. Genet. 27, 153–154.
Epigenetic change in IGF2R is associated with fetal overgrowth after sheep embryo culture.CrossRef | 1:CAS:528:DC%2BD3MXhtFGktL8%3D&md5=eb2f860a259dfd94c8b31fde3d21914aCAS | 11175780PubMed | open url image1



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