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

Extremely low-frequency electromagnetic field exposure alters DNA methylation levels in the endometrium of pigs during the peri-implantation period

Pawel Jozef Wydorski https://orcid.org/0000-0002-3098-0199 A , Wiktoria Kozlowska https://orcid.org/0000-0002-0260-5199 A , Ewa Monika Drzewiecka https://orcid.org/0000-0002-1328-0190 A B , Agata Zmijewska https://orcid.org/0000-0002-0661-130X A and Anita Franczak https://orcid.org/0000-0003-2418-8207 A *
+ Author Affiliations
- Author Affiliations

A Department of Animal Anatomy and Physiology, Faculty of Biology and Biotechnology, University of Warmia and Mazury in Olsztyn, Oczapowskiego 1A, Olsztyn 10-719, Poland.

B Department of Reproductive Immunology and Pathology, Institute of Animal Reproduction and Food Research, Polish Academy of Sciences in Olsztyn, Tuwima 10, Olsztyn 10-748, Poland.

* Correspondence to: anitaf@uwm.edu.pl

Handling Editor: Gilles Charpigny

Reproduction, Fertility and Development 35(12) 601-613 https://doi.org/10.1071/RD22266
Published online: 4 July 2023

© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Context: Extremely low-frequency electromagnetic field (ELF-EMF) emission is increasing due to substantial technological progress. The results of previous research provided evidence that ELF-EMF may exert changes in molecular mechanisms that control female reproduction.

Aims: We hypothesised that short-term ELF-EMF treatment alters the DNA methylation level of genes in the endometrium. Hence, the research aimed to determine the methylation level of selected genes whose expression was altered in response to ELF-EMF radiation in the endometrium of pigs during the peri-implantation period (days 15–16 of pregnancy).

Methods: Porcine endometrial slices (100 ± 5 mg) were collected during the peri-implantation period and exposed to ELF-EMF at a frequency of 50 Hz for 2 h in vitro. The control endometrium was not exposed to ELF-EMF. The level of DNA methylation in the promoter regions of EGR2, HSD17B2, ID2, IL1RAP, MRAP2, NOS3, PTGER4, SERPINE1, VDR and ZFP57 was tested using qMS-PCR.

Key results: In the endometrium exposed to ELF-EMF, the level of methylation of HSD17B2, MRAP2, SERPINE1, VDR and ZFP57 was not altered; the level of methylation of EGR2, ID2 and PTGER4 increased, and the level of methylation of IL1RAP and NOS3 decreased.

Conclusions: ELF-EMF may alter the level of DNA methylation in the endometrium during the peri-implantation period.

Implications: Changes in the DNA methylation induced by ELF-EMF may affect the transcriptomic profile of the endometrium and disturb physiological processes accompanying implantation and embryo development.

Keywords: DNA methylation, endometrium, epigenetic, extremely low-frequency electromagnetic field, implantation, methyl-specific PCR, pig, reproduction.


References

Adams, KW, Kletsov, S, Lamm, RJ, Elman, JS, Mullenbrock, S, and Cooper, GM (2017). Role for Egr1 in the transcriptional program associated with neuronal differentiation of PC12 cells. PLoS ONE 12, e0170076.
Role for Egr1 in the transcriptional program associated with neuronal differentiation of PC12 cells.Crossref | GoogleScholarGoogle Scholar |

Baek, S, Quan, X, Kim, S, Lengner, C, Park, J-K, and Kim, J (2014). Electromagnetic fields mediate efficient cell reprogramming into a pluripotent state. ACS Nano 8, 10125–10138.
Electromagnetic fields mediate efficient cell reprogramming into a pluripotent state.Crossref | GoogleScholarGoogle Scholar |

Bazer, FW, and Johnson, GA (2014). Pig blastocyst–uterine interactions. Differentiation 87, 52–65.
Pig blastocyst–uterine interactions.Crossref | GoogleScholarGoogle Scholar |

Belpomme, D, Hardell, L, Belyaev, I, Burgio, E, and Carpenter, DO (2018). Thermal and non-thermal health effects of low intensity non-ionizing radiation: an international perspective. Environmental Pollution 242, 643–658.
Thermal and non-thermal health effects of low intensity non-ionizing radiation: an international perspective.Crossref | GoogleScholarGoogle Scholar |

Bernabò, N, Tettamanti, E, Russo, V, Martelli, A, Turriani, M, Mattoli, M, and Barboni, B (2010). Extremely low frequency electromagnetic field exposure affects fertilization outcome in swine animal model. Theriogenology 73, 1293–1305.
Extremely low frequency electromagnetic field exposure affects fertilization outcome in swine animal model.Crossref | GoogleScholarGoogle Scholar |

Buska, K, Kedzierska, AE, Slawek, A, and Chelmonska-Soyta, A (2017). Global decrease in the expression of signalling pathways’ genes in murine uterus during preimplantation pregnancy. Reproductive Biology 17, 89–96.
Global decrease in the expression of signalling pathways’ genes in murine uterus during preimplantation pregnancy.Crossref | GoogleScholarGoogle Scholar |

Canovas, S, and Ross, PJ (2016). Epigenetics in preimplantation mammalian development. Theriogenology 86, 69–79.
Epigenetics in preimplantation mammalian development.Crossref | GoogleScholarGoogle Scholar |

Cavalli, G, and Heard, E (2019). Advances in epigenetics link genetics to the environment and disease. Nature 571, 489–499.
Advances in epigenetics link genetics to the environment and disease.Crossref | GoogleScholarGoogle Scholar |

Cedar, H (1988). DNA methylation and gene activity. Cell 53, 3–4.
DNA methylation and gene activity.Crossref | GoogleScholarGoogle Scholar |

Cedar, H, Sabag, O, and Reizel, Y (2022). The role of DNA methylation in genome-wide gene regulation during development. Development 149, dev200118.
The role of DNA methylation in genome-wide gene regulation during development.Crossref | GoogleScholarGoogle Scholar |

Deregibus, MC, Figliolini, F, D’Antico, S, Manzini, PM, Pasquino, C, De Lena, M, Tetta, C, Brizzi, MF, and Camussi, G (2016). Charge-based precipitation of extracellular vesicles. International Journal of Molecular Medicine 38, 1359–1366.
Charge-based precipitation of extracellular vesicles.Crossref | GoogleScholarGoogle Scholar |

Drzewiecka, EM, Kozlowska, W, Zmijewska, A, Wydorski, PJ, and Franczak, A (2021a). Electromagnetic field (EMF) radiation alters estrogen release from the pig myometrium during the peri-implantation period. International Journal of Molecular Sciences 22, 2920.
Electromagnetic field (EMF) radiation alters estrogen release from the pig myometrium during the peri-implantation period.Crossref | GoogleScholarGoogle Scholar |

Drzewiecka, EM, Kozlowska, W, Paukszto, L, Zmijewska, A, Wydorski, PJ, Jastrzebski, JP, and Franczak, A (2021b). Effect of the electromagnetic field (EMF) radiation on transcriptomic profile of pig myometrium during the peri-implantation period – an in vitro study. International Journal of Molecular Sciences 22, 7322.
Effect of the electromagnetic field (EMF) radiation on transcriptomic profile of pig myometrium during the peri-implantation period – an in vitro study.Crossref | GoogleScholarGoogle Scholar |

Evans, J, Rai, A, Nguyen, HPT, Poh, QH, Elglass, K, Simpson, RJ, Salamonsen, LA, and Greening, DW (2019). Human endometrial extracellular vesicles functionally prepare human trophectoderm model for implantation: understanding bidirectional maternal-embryo communication. Proteomics 19, 1800423.
Human endometrial extracellular vesicles functionally prepare human trophectoderm model for implantation: understanding bidirectional maternal-embryo communication.Crossref | GoogleScholarGoogle Scholar |

Fazeli, A, and Holt, WV (2016). Cross talk during the periconception period. Theriogenology 86, 438–442.
Cross talk during the periconception period.Crossref | GoogleScholarGoogle Scholar |

Franczak, A (2008). Endometrial and myometrial secretion of androgens and estrone during early pregnancy and luteolysis in pigs. Reproductive Biology 8, 213–228.
Endometrial and myometrial secretion of androgens and estrone during early pregnancy and luteolysis in pigs.Crossref | GoogleScholarGoogle Scholar |

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. Journal of Physiology and Pharmacology 61, 733–742.

Franczak, A, Wojciechowicz, B, and Kotwica, G (2013). Transcriptomic analysis of the porcine endometrium during early pregnancy and the estrous cycle. Reproductive Biology 13, 229–237.
Transcriptomic analysis of the porcine endometrium during early pregnancy and the estrous cycle.Crossref | GoogleScholarGoogle Scholar |

Franczak, A, Waszkiewicz, EM, Kozlowska, W, Zmijewska, A, and Koziorowska, A (2020). Consequences of electromagnetic field (EMF) radiation during early pregnancy – androgen synthesis and release from the myometrium of pigs in vitro. Animal Reproduction Science 218, 106465.
Consequences of electromagnetic field (EMF) radiation during early pregnancy – androgen synthesis and release from the myometrium of pigs in vitro.Crossref | GoogleScholarGoogle Scholar |

Garip, A, and Akan, Z (2010). Effect of ELF-EMF on number of apoptotic cells; correlation with reactive oxygen species and HSP. Acta Biologica Hungarica 61, 158–167.
Effect of ELF-EMF on number of apoptotic cells; correlation with reactive oxygen species and HSP.Crossref | GoogleScholarGoogle Scholar |

Geisert, RD, and Yelich, JV (1997). Regulation of conceptus development and attachment in pigs. Journal of Reproduction and Fertility Supplement 52, 133–149.

Geisert, RD, Lucy, MC, Whyte, JJ, Ross, JW, and Mathew, DJ (2014). Cytokines from the pig conceptus: roles in conceptus development in pigs. Journal of Animal Science and Biotechnology 5, 51.
Cytokines from the pig conceptus: roles in conceptus development in pigs.Crossref | GoogleScholarGoogle Scholar |

Giacomini, E, Scotti, GM, Vanni, VS, Lazarevic, D, Makieva, S, Privitera, L, Signorelli, S, Cantone, L, Bollati, V, Murdica, V, Tonon, G, Papaleo, E, Candiani, M, and Viganò, P (2021). Global transcriptomic changes occur in uterine fluid-derived extracellular vesicles during the endometrial window for embryo implantation. Human Reproduction 36, 2249–2274.
Global transcriptomic changes occur in uterine fluid-derived extracellular vesicles during the endometrial window for embryo implantation.Crossref | GoogleScholarGoogle Scholar |

Groot, M, and Lee, H (2020). Sorting mechanisms for microRNAs into extracellular vesicles and their associated diseases. Cells 9, 1044–1046.
Sorting mechanisms for microRNAs into extracellular vesicles and their associated diseases.Crossref | GoogleScholarGoogle Scholar |

Guo, R, and Xing, QS (2022). Roles of Wnt signaling pathway and ROR2 receptor in embryonic development: an update review article. Epigenetics Insights 15, 25168657211064232.
Roles of Wnt signaling pathway and ROR2 receptor in embryonic development: an update review article.Crossref | GoogleScholarGoogle Scholar |

Gurung, S, Greening, DW, Rai, A, Poh, QH, Evans, J, and Salamonsen, LA (2021). The proteomes of endometrial stromal cell-derived extracellular vesicles following a decidualizing stimulus define the cells’ potential for decidualization success. Molecular Human Reproduction 27, gaab057.
The proteomes of endometrial stromal cell-derived extracellular vesicles following a decidualizing stimulus define the cells’ potential for decidualization success.Crossref | GoogleScholarGoogle Scholar |

Han, J, Seo, H, Choi, Y, Lee, C, Kim, MI, Jeon, Y, Lee, J, Hong, M, Hyun, S-H, Lee, E, and Ka, H (2018). Expression and regulation of inhibitor of DNA binding proteins ID1, ID2, ID3, and ID4 at the maternal-conceptus interface in pigs. Theriogenology 108, 46–55.
Expression and regulation of inhibitor of DNA binding proteins ID1, ID2, ID3, and ID4 at the maternal-conceptus interface in pigs.Crossref | GoogleScholarGoogle Scholar |

Hua, R, Liu, Q, Lian, W, Gao, D, Huang, C, and Lei, M (2022). Transcriptome regulation of extracellular vesicles derived from porcine uterine flushing fluids during peri-implantation on endometrial epithelial cells and embryonic trophoblast cells. Gene 822, 146337.
Transcriptome regulation of extracellular vesicles derived from porcine uterine flushing fluids during peri-implantation on endometrial epithelial cells and embryonic trophoblast cells.Crossref | GoogleScholarGoogle Scholar |

Jirtle, RL, and Skinner, MK (2007). Environmental epigenomics and disease susceptibility. Nature Reviews Genetics 8, 253–262.
Environmental epigenomics and disease susceptibility.Crossref | GoogleScholarGoogle Scholar |

Ka, H, Seo, H, Choi, Y, Yoo, I, and Han, J (2018). Endometrial response to conceptus-derived estrogen and interleukin-1β at the time of implantation in pigs. Journal of Animal Science and Biotechnology 9, 44.
Endometrial response to conceptus-derived estrogen and interleukin-1β at the time of implantation in pigs.Crossref | GoogleScholarGoogle Scholar |

Karimi, A, Ghadiri Moghaddam, F, and Valipour, M (2020). Insights in the biology of extremely low-frequency magnetic fields exposure on human health. Molecular Biology Reports 47, 5621–5633.
Insights in the biology of extremely low-frequency magnetic fields exposure on human health.Crossref | GoogleScholarGoogle Scholar |

Kennedy, TG, Keys, JL, and King, GJ (1986). Endometrial prostaglandin E2-binding sites in the pig: characterization and changes during the estrous cycle and early pregnancy. Biology of Reproduction 35, 624–632.
Endometrial prostaglandin E2-binding sites in the pig: characterization and changes during the estrous cycle and early pregnancy.Crossref | GoogleScholarGoogle Scholar |

Knight, JW, Bazer, FW, Thatcher, WW, Franke, DE, and Wallace, HD (1977). Conceptus development in intact and unilaterally hysterectomized-ovariectomized gilts: interrelations among hormonal status, placental development, fetal fluids and fetal growth. Journal of Animal Science 44, 620–637.
Conceptus development in intact and unilaterally hysterectomized-ovariectomized gilts: interrelations among hormonal status, placental development, fetal fluids and fetal growth.Crossref | GoogleScholarGoogle Scholar |

Kovacic, P, and Somanathan, R (2010). Electromagnetic fields: mechanism, cell signaling, other bioprocesses, toxicity, radicals, antioxidants and beneficial effects. Journal of Receptors and Signal Transduction 30, 214–226.
Electromagnetic fields: mechanism, cell signaling, other bioprocesses, toxicity, radicals, antioxidants and beneficial effects.Crossref | GoogleScholarGoogle Scholar |

Koziorowska, A, Waszkiewicz, EM, Romerowicz-Misielak, M, Zglejc-Waszak, K, and Franczak, A (2018). Extremely low-frequency electromagnetic field (EMF) generates alterations in the synthesis and secretion of oestradiol-17β (E2) in uterine tissues: an in vitro study. Theriogenology 110, 86–95.
Extremely low-frequency electromagnetic field (EMF) generates alterations in the synthesis and secretion of oestradiol-17β (E2) in uterine tissues: an in vitro study.Crossref | GoogleScholarGoogle Scholar |

Kozlowska, W, Drzewiecka, EM, Zmijewska, A, Koziorowska, A, and Franczak, A (2021a). Effects of electromagnetic field (EMF) radiation on androgen synthesis and release from the pig endometrium during the fetal peri-implantation period. Animal Reproduction Science 226, 106694.
Effects of electromagnetic field (EMF) radiation on androgen synthesis and release from the pig endometrium during the fetal peri-implantation period.Crossref | GoogleScholarGoogle Scholar |

Kozlowska, W, Drzewiecka, EM, Paukszto, L, Zmijewska, A, Wydorski, PJ, Jastrzebski, JP, and Franczak, A (2021b). Exposure to the electromagnetic field alters the transcriptomic profile in the porcine endometrium during the peri-implantation period. Journal of Physiology and Pharmacology 72, 857–871.
Exposure to the electromagnetic field alters the transcriptomic profile in the porcine endometrium during the peri-implantation period.Crossref | GoogleScholarGoogle Scholar |

Kozlowska, W, Drzewiecka, EM, Zmijewska, A, and Franczak, A (2022). Electromagnetic field exposure alters in vitro estrogen biosynthesis and its release by the porcine endometrium in the peri-implantation period. Reproductive Biology 22, 100642.
Electromagnetic field exposure alters in vitro estrogen biosynthesis and its release by the porcine endometrium in the peri-implantation period.Crossref | GoogleScholarGoogle Scholar |

Kwon, SG, Hwang, JH, Park, DH, Kim, TW, Kang, DG, Kang, KH, Kim, I-S, Park, HC, Na, C-S, Ha, J, and Kim, CW (2016). Identification of differentially expressed genes associated with litter size in Berkshire pig placenta. PLoS ONE 11, e0153311.
Identification of differentially expressed genes associated with litter size in Berkshire pig placenta.Crossref | GoogleScholarGoogle Scholar |

Laird, PW, and Jaenisch, R (1994). DNA methylation and cancer. Human Molecular Genetics 3, 1487–1495.
DNA methylation and cancer.Crossref | GoogleScholarGoogle Scholar |

Li, L-C, and Dahiya, R (2002). MethPrimer: designing primers for methylation PCRs. Bioinformatics 18, 1427–1431.
MethPrimer: designing primers for methylation PCRs.Crossref | GoogleScholarGoogle Scholar |

Lim, DHK, and Maher, ER (2010). DNA methylation: a form of epigenetic control of gene expression. The Obstetrician & Gynaecologist 12, 37–42.
DNA methylation: a form of epigenetic control of gene expression.Crossref | GoogleScholarGoogle Scholar |

Livak, KJ, and Schmittgen, TD (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25, 402–408.
Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method.Crossref | GoogleScholarGoogle Scholar |

Mathew, DJ, Lucy, MC, and Geisert, RD (2016). Interleukins, interferons, and establishment of pregnancy in pigs. Reproduction 151, R111–R122.
Interleukins, interferons, and establishment of pregnancy in pigs.Crossref | GoogleScholarGoogle Scholar |

McGrew, LL, Lai, C-J, and Moon, RT (1995). Rapid communication specification of the anteroposterior neural axis through synergistic interaction of the Wnt signaling cascade with noggin and follistatin. Developmental Biology 172, 337–342.
Rapid communication specification of the anteroposterior neural axis through synergistic interaction of the Wnt signaling cascade with noggin and follistatin.Crossref | GoogleScholarGoogle Scholar |

McGrew, LL, Hoppler, S, and Moon, RT (1997). Wnt and FGF pathways cooperatively pattern anteroposterior neural ectoderm in Xenopus. Mechanisms of Development 69, 105–114.
Wnt and FGF pathways cooperatively pattern anteroposterior neural ectoderm in Xenopus.Crossref | GoogleScholarGoogle Scholar |

Meyer, AE, Pfeiffer, CA, Brooks, KE, Spate, LD, Benne, JA, Cecil, R, Samuel, MS, Murphy, CN, Behura, S, McLean, MK, Ciernia, LA, Smith, MF, Whitworth, KM, Wells, KD, Spencer, TE, Prather, RS, and Geisert, RD (2019). New perspective on conceptus estrogens in maternal recognition and pregnancy establishment in the pig. Biology of Reproduction 101, 148–161.
New perspective on conceptus estrogens in maternal recognition and pregnancy establishment in the pig.Crossref | GoogleScholarGoogle Scholar |

Munro, SK, Farquhar, CM, Mitchell, MD, and Ponnampalam, AP (2010). Epigenetic regulation of endometrium during the menstrual cycle. Molecular Human Reproduction 16, 297–310.
Epigenetic regulation of endometrium during the menstrual cycle.Crossref | GoogleScholarGoogle Scholar |

Neuman, K, Nornes, HO, and Neuman, T (1995). Helix-loop-helix transcription factors regulate Id2 gene promoter activity. FEBS Letters 374, 279–283.
Helix-loop-helix transcription factors regulate Id2 gene promoter activity.Crossref | GoogleScholarGoogle Scholar |

Oestrup, O, Hall, V, Petkov, SG, Wolf, XA, Hyldig, S, and Hyttel, P (2009). From zygote to implantation: morphological and molecular dynamics during embryo development in the pig. Reproduction in Domestic Animals 44, 39–49.
From zygote to implantation: morphological and molecular dynamics during embryo development in the pig.Crossref | GoogleScholarGoogle Scholar |

Okatan, DÖ, Kaya, H, Aliyazıcıoğlu, Y, Demir, S, Çolakoğlu, S, and Odacı, E (2018). Continuous 900-megahertz electromagnetic field applied in middle and late-adolescence causes qualitative and quantitative changes in the ovarian morphology, tissue and blood biochemistry of the rat. International Journal of Radiation Biology 94, 186–198.
Continuous 900-megahertz electromagnetic field applied in middle and late-adolescence causes qualitative and quantitative changes in the ovarian morphology, tissue and blood biochemistry of the rat.Crossref | GoogleScholarGoogle Scholar |

Omer, H (2021). Radiobiological effects and medical applications of non-ionizing radiation. Saudi Journal of Biological Sciences 28, 5585–5592.
Radiobiological effects and medical applications of non-ionizing radiation.Crossref | GoogleScholarGoogle Scholar |

Panagopoulos, DJ, Johansson, O, and Carlo, GL (2015). Polarization: a key difference between man-made and natural electromagnetic fields, in regard to biological activity. Scientific Reports 5, 14914.
Polarization: a key difference between man-made and natural electromagnetic fields, in regard to biological activity.Crossref | GoogleScholarGoogle Scholar |

Patruno, A, Amerio, P, Pesce, M, Vianale, G, Di Luzio, S, Tulli, A, Franceschelli, S, Grilli, A, Muraro, R, and Reale, M (2010). Extremely low frequency electromagnetic fields modulate expression of inducible nitric oxide synthase, endothelial nitric oxide synthase and cyclooxygenase-2 in the human keratinocyte cell line HaCat: potential therapeutic effects in wound healing. British Journal of Dermatology 162, 258–266.
Extremely low frequency electromagnetic fields modulate expression of inducible nitric oxide synthase, endothelial nitric oxide synthase and cyclooxygenase-2 in the human keratinocyte cell line HaCat: potential therapeutic effects in wound healing.Crossref | GoogleScholarGoogle Scholar |

Pavani, KC, Meese, T, Pascottini, OB, Guan, XF, Lin, X, Peelman, L, Hamacher, J, Van Nieuwerburgh, F, Deforce, D, Boel, A, Heindryckx, B, Tilleman, K, Van Soom, A, Gadella, BM, Hendrix, A, and Smits, K (2022). Hatching is modulated by microRNA-378a-3p derived from extracellular vesicles secreted by blastocysts. Proceedings of the National Academy of Sciences 119, e2122708119.
Hatching is modulated by microRNA-378a-3p derived from extracellular vesicles secreted by blastocysts.Crossref | GoogleScholarGoogle Scholar |

Peng, Y, Xiang, H, Chen, C, Zheng, R, Chai, J, Peng, J, and Jiang, S (2013). MiR-224 impairs adipocyte early differentiation and regulates fatty acid metabolism. The International Journal of Biochemistry & Cell Biology 45, 1585–1593.
MiR-224 impairs adipocyte early differentiation and regulates fatty acid metabolism.Crossref | GoogleScholarGoogle Scholar |

Pesce, M, Patruno, A, Speranza, L, and Reale, M (2013). Extremely low frequency electromagnetic field and wound healing: implication of cytokines as biological mediators. European Cytokine Network 24, 1–10.
Extremely low frequency electromagnetic field and wound healing: implication of cytokines as biological mediators.Crossref | GoogleScholarGoogle Scholar |

Portha, B, Fournier, A, Ah Kioon, MD, Mezger, V, and Movassat, J (2014). Early environmental factors, alteration of epigenetic marks and metabolic disease susceptibility. Biochimie 97, 1–15.
Early environmental factors, alteration of epigenetic marks and metabolic disease susceptibility.Crossref | GoogleScholarGoogle Scholar |

Rahmani, Z, Jodeiri, M, and Soltani, A (2020). Investigation of radar cross section and electromagnetic fields around an elliptical antenna including magnetized plasma cover. Radar 8, 87–95.

Revel, A, Achache, H, Stevens, J, Smith, Y, and Reich, R (2011). MicroRNAs are associated with human embryo implantation defects. Human Reproduction 26, 2830–2840.
MicroRNAs are associated with human embryo implantation defects.Crossref | GoogleScholarGoogle Scholar |

Robertson, SA, Chin, PY, Glynn, DJ, and Thompson, JG (2011). Peri-conceptual cytokines – setting the trajectory for embryo implantation, pregnancy and beyond. American Journal of Reproductive Immunology 66, 2–10.
Peri-conceptual cytokines – setting the trajectory for embryo implantation, pregnancy and beyond.Crossref | GoogleScholarGoogle Scholar |

Ronkainen, J, Heiskala, A, Vehmeijer, FOL, Lowry, E, Caramaschi, D, Estrada Gutierrez, G, Heiss, JA, Hummel, N, Keikkala, E, Kvist, T, Kupsco, A, Melton, PE, Pesce, G, Soomro, MH, Vives-Usano, M, Baiz, N, Binder, E, Czamara, D, Guxens, M, Mustaniemi, S, London, SJ, Rauschert, S, Vääräsmäki, M, Vrijheid, M, Ziegler, A-G, Annesi-Maesano, I, Bustamante, M, Huang, R-C, Hummel, S, Just, AC, Kajantie, E, Lahti, J, Lawlor, D, Räikkönen, K, Järvelin, M-R, Felix, JF, and Sebert, S (2022). Maternal haemoglobin levels in pregnancy and child DNA methylation: a study in the pregnancy and childhood epigenetics consortium. Epigenetics 17, 19–31.
Maternal haemoglobin levels in pregnancy and child DNA methylation: a study in the pregnancy and childhood epigenetics consortium.Crossref | GoogleScholarGoogle Scholar |

Schaefke, B, Sun, W, Li, Y-S, Fang, L, and Chen, W (2018). The evolution of posttranscriptional regulation. WIREs RNA 9, e1485.
The evolution of posttranscriptional regulation.Crossref | GoogleScholarGoogle Scholar |

Schuermann, D, and Mevissen, M (2021). Manmade electromagnetic fields and oxidative stress – biological effects and consequences for health. International Journal of Molecular Sciences 22, 3772.
Manmade electromagnetic fields and oxidative stress – biological effects and consequences for health.Crossref | GoogleScholarGoogle Scholar |

Seo, H, Choi, Y, Shim, J, Choi, Y, and Ka, H (2012). Regulatory mechanism for expression of IL1B receptors in the uterine endometrium and effects of IL1B on prostaglandin synthetic enzymes during the implantation period in pigs. Biology of Reproduction 87, 1–11.
Regulatory mechanism for expression of IL1B receptors in the uterine endometrium and effects of IL1B on prostaglandin synthetic enzymes during the implantation period in pigs.Crossref | GoogleScholarGoogle Scholar |

Siegfried, Z, and Simon, I (2010). DNA methylation and gene expression. WIREs Systems Biology and Medicine 2, 362–371.
DNA methylation and gene expression.Crossref | GoogleScholarGoogle Scholar |

Simkó, M, and Mattsson, M-O (2004). Extremely low frequency electromagnetic fields as effectors of cellular responses in vitro: possible immune cell activation. Journal of Cellular Biochemistry 93, 83–92.
Extremely low frequency electromagnetic fields as effectors of cellular responses in vitro: possible immune cell activation.Crossref | GoogleScholarGoogle Scholar |

Soneja, A, Drews, M, and Malinski, T (2005). Role of nitric oxide, nitroxidative and oxidative stress in wound healing. Pharmacological Reports 57, 108–119.

Tahiliani, M, Koh, KP, Shen, Y, Pastor, WA, Bandukwala, H, Brudno, Y, Agarwal, S, Iyer, LM, Liu, DR, Aravind, L, and Rao, A (2009). Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 324, 930–935.
Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1.Crossref | GoogleScholarGoogle Scholar |

Tuo, W, Harney, JP, and Bazer, FW (1996). Developmentally regulated expression of interleukin-1β by peri-implantation conceptuses in swine. Journal of Reproductive Immunology 31, 185–198.
Developmentally regulated expression of interleukin-1β by peri-implantation conceptuses in swine.Crossref | GoogleScholarGoogle Scholar |

Waclawik, A, Jabbour, HN, Blitek, A, and Ziecik, AJ (2009). Estradiol-17β, prostaglandin E2 (PGE2), and the PGE2 receptor are involved in PGE2 positive feedback loop in the porcine endometrium. Endocrinology 150, 3823–3832.
Estradiol-17β, prostaglandin E2 (PGE2), and the PGE2 receptor are involved in PGE2 positive feedback loop in the porcine endometrium.Crossref | GoogleScholarGoogle Scholar |

Waclawik, A, Kaczmarek, MM, Blitek, A, Kaczynski, P, and Ziecik, AJ (2017). Embryo-maternal dialogue during pregnancy establishment and implantation in the pig. Molecular Reproduction and Development 84, 842–855.
Embryo-maternal dialogue during pregnancy establishment and implantation in the pig.Crossref | GoogleScholarGoogle Scholar |

Walford, G, and Loscalzo, J (2003). Nitric oxide in vascular biology. Journal of Thrombosis and Haemostasis 1, 2112–2118.
Nitric oxide in vascular biology.Crossref | GoogleScholarGoogle Scholar |

Warner, LE, Mancias, P, Butler, IJ, McDonald, CM, Keppen, L, Koob, KG, and Lupski, JR (1998). Mutations in the early growth response 2 (EGR2) gene are associated with hereditary myelinopathies. Nature Genetics 18, 382–384.
Mutations in the early growth response 2 (EGR2) gene are associated with hereditary myelinopathies.Crossref | GoogleScholarGoogle Scholar |

Wojciechowicz, B, Kołakowska, J, Zglejc-Waszak, K, Martyniak, M, Kotwica, G, and Franczak, A (2019). The whole blood transcriptome at the time of maternal recognition of pregnancy in pigs reflects certain alterations in gene expression within the endometrium and the myometrium. Theriogenology 126, 159–165.
The whole blood transcriptome at the time of maternal recognition of pregnancy in pigs reflects certain alterations in gene expression within the endometrium and the myometrium.Crossref | GoogleScholarGoogle Scholar |

Zglejc, K, Martyniak, M, Waszkiewicz, E, Kotwica, G, and Franczak, A (2018). Peri-conceptional under-nutrition alters transcriptomic profile in the endometrium during the peri-implantation period—the study in domestic pigs. Reproduction in Domestic Animals 53, 74–84.
Peri-conceptional under-nutrition alters transcriptomic profile in the endometrium during the peri-implantation period—the study in domestic pigs.Crossref | GoogleScholarGoogle Scholar |

Zglejc-Waszak, K, Waszkiewicz, EM, and Franczak, A (2019). Periconceptional undernutrition affects the levels of DNA methylation in the peri-implantation pig endometrium and in embryos. Theriogenology 123, 185–193.
Periconceptional undernutrition affects the levels of DNA methylation in the peri-implantation pig endometrium and in embryos.Crossref | GoogleScholarGoogle Scholar |

Zhang, Y, Li, W, Liu, C, Yan, J, Yuan, X, Wang, W, Wang, H, Wu, H, and Yang, Y (2019). Electromagnetic field treatment increases purinergic receptor P2X7 expression and activates its downstream Akt/GSK3β/β-catenin axis in mesenchymal stem cells under osteogenic induction. Stem Cell Research & Theraphy 10, 407.
Electromagnetic field treatment increases purinergic receptor P2X7 expression and activates its downstream Akt/GSK3β/β-catenin axis in mesenchymal stem cells under osteogenic induction.Crossref | GoogleScholarGoogle Scholar |

Ziecik, AJ, Waclawik, A, Kaczmarek, MM, Blitek, A, Jalali, BM, and Andronowska, A (2011). Mechanisms for the establishment of pregnancy in the pig. Reproduction in Domestic Animals 46, 31–41.
Mechanisms for the establishment of pregnancy in the pig.Crossref | GoogleScholarGoogle Scholar |