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

Periconceptional undernutrition affects in utero methyltransferase expression and steroid hormone concentrations in uterine flushings and blood plasma during the peri-implantation period in domestic pigs

A. Franczak A C , K. Zglejc A , E. Waszkiewicz A , B. Wojciechowicz A , M. Martyniak A , W. Sobotka B , S. Okrasa A and G. Kotwica A
+ Author Affiliations
- Author Affiliations

A Department of Animal Physiology, Faculty of Biology and Biotechnology, University of Warmia and Mazury in Olsztyn, Oczapowski 1A, 10-718 Olsztyn, Poland.

B Department of Animal Nutrition and Feed Management, Faculty of Animal Bioengineering, University of Warmia and Mazury in Olsztyn, Oczapowski 5, 10-718 Olsztyn, Poland.

C Corresponding author. Email: anitaf@uwm.edu.pl

Reproduction, Fertility and Development 29(8) 1499-1508 https://doi.org/10.1071/RD16124
Submitted: 21 March 2016  Accepted: 20 June 2016   Published: 18 August 2016

Abstract

Female undernutrition during early pregnancy may affect the physiological pattern of genomic DNA methylation. We hypothesised that in utero DNA methylation may be impaired in females fed a restrictive diet in early pregnancy. In this study we evaluated whether poor maternal nutritional status, induced by applying a restricted diet during the peri-conceptional period, may influence: (1) the potential for in utero DNA methylation, expressed as changes in the mRNA expression and protein abundance of methyltransferases: DNA methyltransferase 1 (DNMT1) and DNMT3a in the endometrium and the myometrium, (2) the intrauterine microenvironment, measured as oestradiol 17β (E2) and progesterone (P4) concentrations in uterine flushings and (3) plasma concentration of E2 and P4 during the peri-implantation period. Our results indicate that maternal peri-conceptional undernutrition affects maintenance and de novo DNA methylation in the endometrium, de novo methylation in the myometrium and a results in a decrease in intrauterine E2 concentration during the peri-implantation period. The intrauterine concentration of P4 and plasma concentrations of E2 and P4 did not change. These findings suggest that undernutrition during the earliest period of pregnancy, and perhaps the pre-pregnancy period, may create changes in epigenetic mechanisms in the uterus and intrauterine milieu of E2 during the peri-implantation period.

Additional keywords: DNA methylation, endometrium, myometrium, oestradiol-17β, progesterone.


References

Altmann, S., Murani, E., Schwerin, M., Metges, C. C., Wimmers, K., and Ponsuksili, S. (2012). Maternal dietary protein restriction and excess affects offspring gene expression and methylation of non-SMC subunits of condensin I in liver and skeletal muscle. Epigenetics 7, 239–252.
Maternal dietary protein restriction and excess affects offspring gene expression and methylation of non-SMC subunits of condensin I in liver and skeletal muscle.CrossRef | 1:CAS:528:DC%2BC38XptF2lurk%3D&md5=ac9703dcc9cd2a4133bb16d81bb27766CAS | 22430800PubMed |

Altmann, S., Murani, E., Schwerin, M., Metges, C. C., Wimmers, K., and Ponsuksili, S. (2013). Dietary protein restriction and excess of pregnant German Landrace sows induce changes in hepatic gene expression and promoter methylation of key metabolic genes in the offspring. J. Nutr. Biochem. 24, 484–495.
Dietary protein restriction and excess of pregnant German Landrace sows induce changes in hepatic gene expression and promoter methylation of key metabolic genes in the offspring.CrossRef | 1:CAS:528:DC%2BC38XpsVWitL4%3D&md5=d7c53d2399767fff56040db1d66a30c5CAS | 22749136PubMed |

Ashworth, C. J., Toma, L. M., and Hunter, M. G. (2009). Nutritional effects on oocyte and embryo development in mammals: implications for reproductive efficiency and environmental sustainability. Philos. Trans. R. Soc. Lond. B Biol. Sci. 364, 3351–3361.
Nutritional effects on oocyte and embryo development in mammals: implications for reproductive efficiency and environmental sustainability.CrossRef | 19833647PubMed |

Bayol, S. A., Farrington, S. J., and Stickland, N. C. (2007). A maternal ‘junk food’ diet in pregnancy and lactation promotes an exacerbated taste for ‘junk food’ and a greater propensity for obesity in rat offspring. Br. J. Nutr. 98, 843–851.
A maternal ‘junk food’ diet in pregnancy and lactation promotes an exacerbated taste for ‘junk food’ and a greater propensity for obesity in rat offspring.CrossRef | 1:CAS:528:DC%2BD2sXhtlWhsrnJ&md5=a20092c059ef8901711a906902be73d1CAS | 17697422PubMed |

Bazer, F. W., and Spencer, T. E. (2005). Reproductive biology in the era of genomics biology. Theriogenology 64, 442–456.
Reproductive biology in the era of genomics biology.CrossRef | 1:CAS:528:DC%2BD2MXmt1artL4%3D&md5=966ecc0bb710785b57aaa330a9794b81CAS | 15946735PubMed |

Belkacemi, L., Nelson, D. M., Desai, M., and Ross, M. G. (2010). Maternal undernutrition influences placental–fetal development. Biol. Reprod. 83, 325–331.
Maternal undernutrition influences placental–fetal development.CrossRef | 1:CAS:528:DC%2BC3cXhtVyrsrrO&md5=419bcdec1a716f5974fed63563cb6949CAS | 20445129PubMed |

Bogacka, I., Przała, J., Siawrys, G., Kaminski, T., and Smolinska, N. (2006). The expression of short form of leptin receptor gene during early pregnancy in the pig examined by quantitative real time RT-PCR. J. Physiol. Pharmacol. 57, 479–489.
| 1:CAS:528:DC%2BD28XhtFKhs7%2FL&md5=0a64a80d51fa0740a42289121c0c8ce9CAS | 17033099PubMed |

Bonk, A. J., Li, R., Lai, L., Hao, Y., Liu, Z., Samuel, M., Fergason, E. A., Whitworth, K. M., Murphy, C. N., Antoniou, E., and Prather, R. S. (2008). Aberrant DNA methylation in porcine in vitro-, parthenogenetic- and somatic cell nuclear transfer-produced blastocysts. Mol. Reprod. Dev. 75, 250–264.
Aberrant DNA methylation in porcine in vitro-, parthenogenetic- and somatic cell nuclear transfer-produced blastocysts.CrossRef | 1:CAS:528:DC%2BD1cXovVCrtw%3D%3D&md5=7c0bfd02b7d59028d38fde65b587d628CAS | 17595009PubMed |

Ciereszko, R. (1999). Radioimmunoassay of steroid hormones in biological fluids. In ‘Animal Physiology. Demonstrations and Methods’. (Ed. J. Przala.) p. 157–63. (UWM Press: Olsztyn.) [In Polish]

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, 13734–13738.
Conservation of methylation reprogramming in mammalian development: aberrant reprogramming in cloned embryos.CrossRef | 1:CAS:528:DC%2BD3MXovVyntrs%3D&md5=fbd8f0e2847e93f0dcc6807df8b8b1fcCAS | 11717434PubMed |

Dean, W., Lucifero, D., and Santos, F. (2005). DNA methylation in mammalian development and disease. Birth Defects Res. C Embryo Today 75, 98–111.
DNA methylation in mammalian development and disease.CrossRef | 1:CAS:528:DC%2BD2MXnvVWhsrc%3D&md5=af88c198d78e559616618ffdb3bdcf95CAS | 16035040PubMed |

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 | 1:CAS:528:DC%2BC3MXjs12ksLY%3D&md5=59979a668c350eaaa0285f34c6162961CAS | 20935454PubMed |

de Sousa Abreu, R., Penalva, L. O., Marcotte, E. M., and Vogel, C. (2009). Global signatures of protein and mRNA expression levels. Mol. Biosyst. 5, 1512–1526.
| 20023718PubMed |

Ding, Y. B., He, J. L., Liu, X. Q., Chen, X. M., Long, C. L., and Wang, Y. X. (2012). Expression of DNA methyltransferases in the mouse uterus during early pregnancy and susceptibility to dietary folate deficiency. Reproduction 144, 91–100.
Expression of DNA methyltransferases in the mouse uterus during early pregnancy and susceptibility to dietary folate deficiency.CrossRef | 1:CAS:528:DC%2BC38XhtV2ht7vI&md5=9bd8cfade50b92b6e3e55e0e1616a832CAS | 22580371PubMed |

Fleming, T. P., Lucas, E. S., Watkins, A. J., and Eckert, J. J. (2012a). Adaptive responses of the embryo to maternal diet and consequences for post-implantation development. Reprod. Fertil. Dev. 24, 35–44.
Adaptive responses of the embryo to maternal diet and consequences for post-implantation development.CrossRef |

Fleming, T. P., Velazquez, M. A., Eckert, J. J., Lucas, E. S., and Watkins, A. J. (2012b). Nutrition of females during the peri-conceptional period and effects on foetal programming and health of offspring. Anim. Reprod. Sci. 130, 193–197.
Nutrition of females during the peri-conceptional period and effects on foetal programming and health of offspring.CrossRef | 1:STN:280:DC%2BC38zht1ekuw%3D%3D&md5=ffbe7db2630cba1c899965c0f062a60bCAS | 22341375PubMed |

Franczak, A. (2008). Endometrial and myometrial secretion of androgens and estrone during early pregnancy and luteolysis in pigs. Reprod. Biol. 8, 213–228.
Endometrial and myometrial secretion of androgens and estrone during early pregnancy and luteolysis in pigs.CrossRef | 19092984PubMed |

Franczak, A., and Kotwica, G. (2008). Secretion of estradiol-17β by porcine endometrium and myometrium during early pregnancy and luteolysis. Theriogenology 69, 283–289.
Secretion of estradiol-17β by porcine endometrium and myometrium during early pregnancy and luteolysis.CrossRef | 1:CAS:528:DC%2BD1cXlvV2itA%3D%3D&md5=b8891477a327b16a0583ca4007f04c5aCAS | 17977590PubMed |

Franczak, A., and Kotwica, G. (2010). Androgens and estradiol-17β production by porcine uterine cells: in vitro study. Theriogenology 73, 232–241.
Androgens and estradiol-17β production by porcine uterine cells: in vitro study.CrossRef | 1:CAS:528:DC%2BD1MXhsFGrsrfF&md5=5a6b319341043a20c2afb71cad042e48CAS | 19880166PubMed |

Franczak, A., Zmijewska, A., Kurowicka, B., Wojciechowicz, B., and Kotwica, G. (2010). Interleukin 1β-induced synthesis and secretion of prostaglandin E2 in the porcine uterus during various periods of pregnancy and the estrous cycle. J. Physiol. Pharmacol. 61, 733–742.
| 1:CAS:528:DC%2BC3MXitVSrtL4%3D&md5=8136e4ba88187c3770ee3a130e42c9dfCAS | 21224505PubMed |

Franczak, A., Wojciechowicz, B., and Kotwica, G. (2013a). Transcriptomic analysis of the porcine endometrium during early pregnancy and the estrous cycle. Reprod. Biol. 13, 229–237.
Transcriptomic analysis of the porcine endometrium during early pregnancy and the estrous cycle.CrossRef | 24011194PubMed |

Franczak, A., Wojciechowicz, B., and Kotwica, G. (2013b). Novel aspects of cytokine action in porcine uterus – endometrial and myometrial production of estrone (E1) in the presence of interleukin 1beta (IL1beta), interleukin 6 (IL6) and tumor necrosis factor (TNFalpha) – in vitro study. Folia Biol. (Krakow) 61, 253–261.
Novel aspects of cytokine action in porcine uterus – endometrial and myometrial production of estrone (E1) in the presence of interleukin 1beta (IL1beta), interleukin 6 (IL6) and tumor necrosis factor (TNFalpha) – in vitro study.CrossRef | 1:CAS:528:DC%2BC3sXhs1SltrzK&md5=8e767b896d419134cfeda921ccaebdffCAS | 24279177PubMed |

Franczak, A., Wojciechowicz, B., Kolakowska, J., Zglejc, K., and Kotwica, G. (2014). Transcriptomic analysis of the myometrium during peri-implantation period and luteolysis – the study on the pig model. Funct. Integr. Genomics 14, 673–682.
Transcriptomic analysis of the myometrium during peri-implantation period and luteolysis – the study on the pig model.CrossRef | 1:CAS:528:DC%2BC2cXhsFyhsbrJ&md5=bef6f5608199a7da46808879a7098cd4CAS | 25240502PubMed |

Franczak, A., Żmijewska, A., Zglejc, K., Dziekoński, M., Waszkiewicz, E., Okrasa, S., Sobotka, W., and Kotwica, G. (2015). The effect of short-lasting undernutrition of gilts during peri-conceptional period on biochemical and haematological parameters in blood plasma during peri-implantation period. J. Elementol. 21, 33–42.

Fulka, J., Fulka, H., Slavik, T., Okada, K., and Fulka, J. (2006). DNA methylation pattern in pig in vivo-produced embryos. Histochem. Cell Biol. 126, 213–217.
DNA methylation pattern in pig in vivo-produced embryos.CrossRef | 1:CAS:528:DC%2BD28XnvF2ksLw%3D&md5=85bc0d2bd744f81c7514f104a6b83d17CAS | 16435122PubMed |

Geisert, R. D., Renegar, R. H., Thatcher, W. W., Roberts, R. M., and Bazer, F. W. (1982). Establishment of pregnancy in the pig: I. Interrelationships between preimplantation development of the pig blastocyst and uterine endometrial secretions. Biol. Reprod. 27, 925–939.
Establishment of pregnancy in the pig: I. Interrelationships between preimplantation development of the pig blastocyst and uterine endometrial secretions.CrossRef | 1:CAS:528:DyaL3sXjt1Wrtw%3D%3D&md5=a486c2067e4a9e3de24494083d8bdf2bCAS | 6959653PubMed |

Heap, R. B., Flint, A. P., Hartmann, P. E., Gadsby, J. E., Staples, L. D., Ackland, N., and Hamon, M. (1981). Oestrogen production in early pregnancy. J. Endocrinol. 89, 77P–94P.
| 7241021PubMed |

Ito, J., and Kashiwazaki, N. (2012). Molecular mechanism of fertilization in the pig. Anim. Sci. J. 83, 669–682.
Molecular mechanism of fertilization in the pig.CrossRef | 1:CAS:528:DC%2BC38XhvVCit7zM&md5=d3829bbf24507c20b83201a7fa585be4CAS | 23035706PubMed |

Izawa, M., Harada, T., Taniguchi, F., Ohama, Y., Takenaka, Y., and Terakawa, N. (2008). An epigenetic disorder may cause aberrant expression of aromatase gene in endometriotic stromal cells. Fertil. Steril. 89, 1390–1396.
An epigenetic disorder may cause aberrant expression of aromatase gene in endometriotic stromal cells.CrossRef | 1:CAS:528:DC%2BD1cXht12qsLnN&md5=7d69f9a2160e8eaf2ab321a7858be80cCAS | 17662285PubMed |

Lillycrop, K. A. (2011). Effect of maternal diet on the epigenome: implications for human metabolic disease. Proc. Nutr. Soc. 70, 64–72.
Effect of maternal diet on the epigenome: implications for human metabolic disease.CrossRef | 21266093PubMed |

Lucas, E. S., Marfy-Smith, S. J., Watkins, A. J., and Fleming, T. P. (2011). Altered DNA methyltransferase expression in preimplantation mouse embryos is induced by maternal low protein diet. In ‘Periconceptional Developmental Programming; GEMINI WGIII Workshop, 2011’. (Eds Y. Heifetz, T. Fleming, P. Chavatte-Palmer.) p. 46. (Published by GEMINI COST ACTION FA0702, Israel.)

Okrasa, S., Franczak, A., Zmijewska, A., Wojciechowicz, B., Dziekoński, M., Martyniak, M., Kolakowska, J., Zglejc, K., and Kotwica, G. (2014). The uterine secretory activity and its physiological changes in the pig. Acta Biol Cracov Series Zoologica 55/56, 40–57.

Oliver, M. H., Hawkins, P., and Harding, J. E. (2005). Periconceptional undernutrition alters growth trajectory and metabolic and endocrine responses to fasting in late-gestation fetal sheep. Pediatr. Res. 57, 591–598.
Periconceptional undernutrition alters growth trajectory and metabolic and endocrine responses to fasting in late-gestation fetal sheep.CrossRef | 15695605PubMed |

Pradhan, S., Bacolla, A., Wells, R. D., and Roberts, R. J. (1999). Recombinant human DNA (cytosine-5) methyltransferase. I. Expression, purification, and comparison of de novo and maintenance methylation. J. Biol. Chem. 274, 33002–33010.
Recombinant human DNA (cytosine-5) methyltransferase. I. Expression, purification, and comparison of de novo and maintenance methylation.CrossRef | 1:CAS:528:DyaK1MXntlygurg%3D&md5=c51cf454866e4a21331b1b6148b27470CAS | 10551868PubMed |

Prunier, A., and Quesnel, H. (2000). Nutritional influences on the hormonal control of reproduction in female pigs. Livest. Prod. Sci. 63, 1–16.
Nutritional influences on the hormonal control of reproduction in female pigs.CrossRef |

Rahnama, F., Shafiei, F., Gluckman, P. D., Mitchell, M. D., and Lobie, P. E. (2006). Epigenetic regulation of human trophoblastic cell migration and invasion. Endocrinology 147, 5275–5283.
Epigenetic regulation of human trophoblastic cell migration and invasion.CrossRef | 1:CAS:528:DC%2BD28XhtFCgsLrE&md5=e16ebde14ead40d268c20a6be0aee5b6CAS | 16887905PubMed |

Reik, W. (2007). Stability and flexibility of epigenetic gene regulation in mammalian development. Nature 447, 425–432.
Stability and flexibility of epigenetic gene regulation in mammalian development.CrossRef | 1:CAS:528:DC%2BD2sXlsFOgs7w%3D&md5=e5c6e7414f488548136e2a99f078594cCAS | 17522676PubMed |

Reik, W., Dean, W., and Walter, J. (2001). Epigenetic reprogramming in mammalian development. Science 293, 1089–1093.
Epigenetic reprogramming in mammalian development.CrossRef | 1:CAS:528:DC%2BD3MXmtVWltL8%3D&md5=6009e5d8f2eaa405f3e5574d9599590dCAS | 11498579PubMed |

Roseboom, T. J., Van der Meulen, J. H., Ravelli, A. C., Osmond, C., Barker, D. J., and Bleker, O. P. (2001). Effects of prenatal exposure to the Dutch famine on adult disease in later life: an overview. Mol. Cell. Endocrinol. 185, 93–98.
Effects of prenatal exposure to the Dutch famine on adult disease in later life: an overview.CrossRef | 1:CAS:528:DC%2BD3MXovFyqtL0%3D&md5=9cd9f17044bb985990e1e165abc9d8e9CAS | 11738798PubMed |

Shiota, K. (2004). DNA methylation profiles of CpG islands for cellular differentiation and development in mammals. Cytogenet. Genome Res. 105, 325–334.
DNA methylation profiles of CpG islands for cellular differentiation and development in mammals.CrossRef | 1:CAS:528:DC%2BD2cXlsV2js7o%3D&md5=e2f7990c58de70caa7bc524e8c5a337eCAS | 15237220PubMed |

Slater-Jefferies, J. L., Lillycrop, K. A., Townsend, P. A., Torrens, C., Hoile, S. P., Hanson, M. A., and Burdge, G. C. (2011). Feeding a protein-restricted diet during pregnancy induces altered epigenetic regulation of peroxisomal proliferator-activated receptor-α in the heart of the offspring. J. Dev. Orig. Health Dis. 2, 250–255.
Feeding a protein-restricted diet during pregnancy induces altered epigenetic regulation of peroxisomal proliferator-activated receptor-α in the heart of the offspring.CrossRef | 1:CAS:528:DC%2BC3MXhtVWmsLjN&md5=639f44b06381a77ee68ac951a4eacbfbCAS | 22003431PubMed |

Staszkiewicz, J., Skowronski, M. T., Siawrys, G., Kaminski, T., Krazinski, B. E., Plonka, K. J., Wylot, B., Przala, J., and Okrasa, S. (2007). Expression of proopiomelanocortin, proenkephalin and prodynorphin genes in porcine luteal cells. Acta Vet. Hung. 55, 435–449.
Expression of proopiomelanocortin, proenkephalin and prodynorphin genes in porcine luteal cells.CrossRef | 1:CAS:528:DC%2BD1cXotlOqsw%3D%3D&md5=c7fb7e5f1858e152a954aa0b045adc36CAS | 18277703PubMed |

Szafrańska, B., Ziecik, A., and Okrasa, S. (2002). Primary antisera against selected steroids or proteins and secondary antisera against gamma-globulins – an available tool for studies of reproductive processes. Reprod. Biol. 2, 187–204.
| 14666157PubMed |

Tsuma, V. T., Einarsson, S., Madej, A., Kindhal, H., and Lundheim, N. (1996). Effect of food deprivation during early pregnancy on endocrine changes in primiparous sows. Anim. Reprod. Sci. 41, 267–278.
Effect of food deprivation during early pregnancy on endocrine changes in primiparous sows.CrossRef | 1:CAS:528:DyaK28XjtVGgur0%3D&md5=712415a3973a9380aa8d85a5bf584f0eCAS |

Turek-Plewa, J., and Jagodziński, P. P. (2005). The role of mammalian DNA methyltransferases in the regulation of gene expression. Cell. Mol. Biol. Lett. 10, 631–647.
| 1:CAS:528:DC%2BD28XhtFahsrs%3D&md5=8cd4e09ad9d758cfc18920e7ca0edd2fCAS | 16341272PubMed |

Vallet, J. L., and Christenson, R. K. (1996). The effect of estrone and estradiol treatment on endometrial total protein, uteroferrin, and retinol-binding protein secretion during midpregnancy or midpseudopregnancy in swine. J. Anim. Sci. 74, 2765–2772.
| 1:CAS:528:DyaK28XmvFSisL8%3D&md5=1fd264c924921931914c85b468c09f6dCAS | 8923192PubMed |

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 |

Watkins, A. J., Lucas, E. S., Wilkins, A., Cagampang, F. R., and Fleming, T. P. (2011). Maternal periconceptional and gestational low protein diet affects mouse offspring growth, cardiovascular and adipose phenotype at 1 year of age. PLoS One 6, e28745.
Maternal periconceptional and gestational low protein diet affects mouse offspring growth, cardiovascular and adipose phenotype at 1 year of age.CrossRef | 1:CAS:528:DC%2BC38Xis1Wktg%3D%3D&md5=85228484689fba7d8f71a581d8adc753CAS | 22194901PubMed |

Wu, Y., Halverson, G., Basir, Z., Strawn, E., Yan, P., and Guo, S. W. (2005). Aberrant methylation at HOXA10 may be responsible for its aberrant expression in the endometrium of patients with endometriosis. Am. J. Obstet. Gynecol. 193, 371–380.
Aberrant methylation at HOXA10 may be responsible for its aberrant expression in the endometrium of patients with endometriosis.CrossRef | 1:CAS:528:DC%2BD2MXns1Wms7w%3D&md5=16ecb4a1052c12528b67bba972a96a18CAS | 16098858PubMed |

Xue, Q., Lin, Z., Cheng, Y. H., Huang, C. C., Marsh, E., Yin, P., Milad, M. P., Confino, E., Reierstad, S., Innes, J., and Bulun, S. E. (2007). Promoter methylation regulates estrogen receptor 2 in human endometrium and endometriosis. Biol. Reprod. 77, 681–687.
Promoter methylation regulates estrogen receptor 2 in human endometrium and endometriosis.CrossRef | 1:CAS:528:DC%2BD2sXhtFahsb3N&md5=8fcd8b195af8eaef2223d511fc838f3eCAS | 17625110PubMed |

Yajnik, C. S., and Deshmukh, U. S. (2008). Maternal nutrition, intrauterine programming and consequential risks in the offspring. Rev. Endocr. Metab. Disord. 9, 203–211.
Maternal nutrition, intrauterine programming and consequential risks in the offspring.CrossRef | 1:CAS:528:DC%2BD1cXps1ahsL8%3D&md5=4b288ed6849aaa6f4fcf8e0f2d2ed2edCAS | 18661241PubMed |

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 |

Yin, L. J., Zhang, Y., Lv, P. P., He, W. H., Liu, A. X., Ding, G. L., Dong, M. Y., Qu, F., Xu, C. M., Zhu, X. M., and Huang, H. F. (2012). Insufficient maintenance DNA methylation is associated with abnormal embryonic development. BMC Med. 10, 26.
Insufficient maintenance DNA methylation is associated with abnormal embryonic development.CrossRef | 1:CAS:528:DC%2BC38Xos12mtbg%3D&md5=1b63d945631af6e3d42ba6e84a153599CAS | 22413869PubMed |

Zuo, X., Sheng, J., Lau, H. T., McDonald, C. M., Andrade, M., Cullen, D. E., Cullen, D. E., Bell, F. T., Iacovino, M., Kyba, M., Xu, G., and Li, X. (2012). Zinc finger protein ZFP57 requires its co-factor to recruit DNA methyltransferases and maintains DNA methylation imprint in embryonic stem cells via its transcriptional repression domain. J. Biol. Chem. 287, 2107–2118.
Zinc finger protein ZFP57 requires its co-factor to recruit DNA methyltransferases and maintains DNA methylation imprint in embryonic stem cells via its transcriptional repression domain.CrossRef | 1:CAS:528:DC%2BC38XmtlGqtw%3D%3D&md5=ae0bd222d1cbb4f722e195dd1d300760CAS | 22144682PubMed |



Rent Article (via Deepdyve) Export Citation Cited By (2)

View Altmetrics