Potential role of epigenetic mechanisms in regulation of trophoblast differentiation, migration, and invasion in the human placenta

References

• Cross JC, Werb Z, Fisher SJ. Implantation and the placenta: key pieces of the development puzzle. Science 1994; 266:1508-18; PMID:7985020; http://dx.doi.org/10.1126/science.7985020
   PubMed Web of Science ®Google Scholar
• Hamilton WJ, Boyd JD. Development of the human placenta in the first three months of gestation. J Anat 1960; 94:297-328; PMID:14399291
   PubMed Web of Science ®Google Scholar
• Zhou Y, Fisher SJ, Janatpour M, Genbacev O, Dejana E, Wheelock M, Damsky CH. Human cytotrophoblasts adopt a vascular phenotype as they differentiate. A strategy for successful endovascular invasion? J Clin Invest 1997; 99:2139-51; PMID:9151786; http://dx.doi.org/10.1172/JCI119387
   PubMed Web of Science ®Google Scholar
• Redman CW, Sargent IL. Latest advances in understanding preeclampsia. Science 2005; 308:1592-4; PMID:15947178; http://dx.doi.org/10.1126/science.1111726
   PubMed Web of Science ®Google Scholar
• Ball E, Bulmer JN, Ayis S, Lyall F, Robson SC. Late sporadic miscarriage is associated with abnormalities in spiral artery transformation and trophoblast invasion. J Pathol 2006; 208:535-42; PMID:16402350; http://dx.doi.org/10.1002/path.1927
   PubMed Web of Science ®Google Scholar
• McMaster-Fay RA. Failure of physiologic transformation of the spiral arteries of the uteroplacental circulation in patients with preterm labor and intact membranes. Am J Obstet Gynecol 2004; 191:1837-8; author reply 8-9; PMID:15547578; http://dx.doi.org/10.1016/j.ajog.2004.05.091
   PubMed Web of Science ®Google Scholar
• Khong TY. The pathology of placenta accreta, a worldwide epidemic. J Clin Pathol 2008; 61:1243-6; PMID:18641410; http://dx.doi.org/10.1136/jcp.2008.055202
   PubMed Web of Science ®Google Scholar
• Tseng JJ, Chou MM. Differential expression of growth-, angiogenesis- and invasion-related factors in the development of placenta accreta. Taiwan J Obstet Gynecol 2006; 45:100-6; PMID:17197348; http://dx.doi.org/10.1016/S1028-4559(09)60205-9
   PubMedGoogle Scholar
• Baczyk D, Drewlo S, Proctor L, Dunk C, Lye S, Kingdom J. Glial cell missing-1 transcription factor is required for the differentiation of the human trophoblast. Cell Death Differ 2009; 16:719-27; PMID:19219068; http://dx.doi.org/10.1038/cdd.2009.1
   PubMed Web of Science ®Google Scholar
• Loregger T, Pollheimer J, Knofler M. Regulatory transcription factors controlling function and differentiation of human trophoblast–a review. Placenta 2003; 24 Suppl A:S104-10; PMID:12842421; http://dx.doi.org/10.1053/plac.2002.0929
   PubMedGoogle Scholar
• Knofler M, Pollheimer J. IFPA Award in Placentology lecture: molecular regulation of human trophoblast invasion. Placenta 2012; 33 Suppl:S55-62; PMID:22019198; http://dx.doi.org/10.1016/j.placenta.2011.09.019
   PubMedGoogle Scholar
• Damsky CH, Fitzgerald ML, Fisher SJ. Distribution patterns of extracellular matrix components and adhesion receptors are intricately modulated during first trimester cytotrophoblast differentiation along the invasive pathway, in vivo. J Clin Invest 1992; 89:210-22; PMID:1370295; http://dx.doi.org/10.1172/JCI115565
   PubMed Web of Science ®Google Scholar
• Norwitz ER. Defective implantation and placentation: laying the blueprint for pregnancy complications. Reprod Biomed Online 2006; 13:591-9; PMID:17007686; http://dx.doi.org/10.1016/S1472-6483(10)60649-9
   PubMed Web of Science ®Google Scholar
• Bird A. Perceptions of epigenetics. Nature 2007; 447:396-8; PMID:17522671; http://dx.doi.org/10.1038/nature05913
   PubMed Web of Science ®Google Scholar
• Haluskova J. Epigenetic studies in human diseases. Folia biologica 2010; 56:83-96; PMID:20653993
   PubMed Web of Science ®Google Scholar
• Szyf M. Epigenetics, DNA methylation, and chromatin modifying drugs. Annu Rev Pharmacol Toxicol 2009; 49:243-63; PMID:18851683; http://dx.doi.org/10.1146/annurev-pharmtox-061008-103102
   PubMed Web of Science ®Google Scholar
• Kouzarides T. Chromatin modifications and their function. Cell 2007; 128:693-705; PMID:17320507; http://dx.doi.org/10.1016/j.cell.2007.02.005
   PubMed Web of Science ®Google Scholar
• Szymanski M, Barciszewski J. Beyond the proteome: non-coding regulatory RNAs. Genome Biol 2002; 3:reviews0005; PMID:12049667
   PubMed Web of Science ®Google Scholar
• Duggirala A, Delogu F, Angelini TG, Smith T, Caputo M, Rajakaruna C, Emanueli C. Non coding RNAs in aortic aneurysmal disease. Front Genet 2015; 6:125; PMID:25883602; http://dx.doi.org/10.3389/fgene.2015.00125
   PubMed Web of Science ®Google Scholar
• Ma Y, Ma W, Huang L, Feng D, Cai B. Long non-coding RNAs, a new important regulator of cardiovascular physiology and pathology. Int J Cardiol 2015; 188:105-10; PMID:25917923; http://dx.doi.org/10.1016/j.ijcard.2015.04.021
   PubMed Web of Science ®Google Scholar
• Morlando M, Ballarino M, Fatica A. Long Non-Coding RNAs: New Players in Hematopoiesis and Leukemia. Front Med (Lausanne) 2015; 2:23; PMID:25927065
   PubMed Web of Science ®Google Scholar
• Hemberger M. Epigenetic landscape required for placental development. Cell Mol Life Sci 2007; 64:2422-36; PMID:17585370; http://dx.doi.org/10.1007/s00018-007-7113-z
   PubMed Web of Science ®Google Scholar
• Dupont C, Armant DR, Brenner CA. Epigenetics: definition, mechanisms and clinical perspective. Semin Reprod Med 2009; 27:351-7; PMID:19711245; http://dx.doi.org/10.1055/s-0029-1237423
   PubMed Web of Science ®Google Scholar
• Berger SL. Histone modifications in transcriptional regulation. Curr Opin Genet Dev 2002; 12:142-8; PMID:11893486; http://dx.doi.org/10.1016/S0959-437X(02)00279-4
   PubMed Web of Science ®Google Scholar
• Narlikar GJ, Fan HY, Kingston RE. Cooperation between complexes that regulate chromatin structure and transcription. Cell 2002; 108:475-87; PMID:11909519; http://dx.doi.org/10.1016/S0092-8674(02)00654-2
   PubMed Web of Science ®Google Scholar
• Gan Q, Yoshida T, McDonald OG, Owens GK. Concise Review: Epigenetic Mechanisms Contribute to Pluripotency and Cell Lineage Determination of Embryonic Stem Cells. Stem Cells 2007; 25:2-9; PMID:17023513; http://dx.doi.org/10.1634/stemcells.2006-0383
   PubMed Web of Science ®Google Scholar
• Grunstein M. Histone acetylation in chromatin structure and transcription. Nature 1997; 389:349-52; PMID:9311776; http://dx.doi.org/10.1038/38664
   PubMed Web of Science ®Google Scholar
• Kurdistani SK, Grunstein M. Histone acetylation and deacetylation in yeast. Nat Rev Mol Cell Biol 2003; 4:276-84; PMID:12671650; http://dx.doi.org/10.1038/nrm1075
   PubMed Web of Science ®Google Scholar
• Shogren-Knaak M, Ishii H, Sun JM, Pazin MJ, Davie JR, Peterson CL. Histone H4-K16 acetylation controls chromatin structure and protein interactions. Science 2006; 311:844-7; PMID:16469925; http://dx.doi.org/10.1126/science.1124000
   PubMed Web of Science ®Google Scholar
• Maltepe E, Krampitz GW, Okazaki KM, Red-Horse K, Mak W, Simon MC, Fisher SJ. Hypoxia-inducible factor-dependent histone deacetylase activity determines stem cell fate in the placenta. Development 2005; 132:3393-403; PMID:15987772; http://dx.doi.org/10.1242/dev.01923
   PubMed Web of Science ®Google Scholar
• Kozak KR, Abbott B, Hankinson O. ARNT-deficient mice and placental differentiation. Dev Biol 1997; 191:297-305; PMID:9398442; http://dx.doi.org/10.1006/dbio.1997.8758
   PubMed Web of Science ®Google Scholar
• Adelman DM, Gertsenstein M, Nagy A, Simon MC, Maltepe E. Placental cell fates are regulated in vivo by HIF-mediated hypoxia responses. Genes Dev 2000; 14:3191-203; PMID:11124810; http://dx.doi.org/10.1101/gad.853700
   PubMed Web of Science ®Google Scholar
• Abell AN, Jordan NV, Huang W, Prat A, Midland AA, Johnson NL, Granger DA, Mieczkowski PA, Perou CM, Gomez SM, et al. MAP3K4/CBP-regulated H2B acetylation controls epithelial-mesenchymal transition in trophoblast stem cells. Cell Stem Cell 2011; 8:525-37; PMID:21549327; http://dx.doi.org/10.1016/j.stem.2011.03.008
   PubMed Web of Science ®Google Scholar
• Dokras A, Gardner LM, Kirschmann DA, Seftor EA, Hendrix MJ. The tumour suppressor gene maspin is differentially regulated in cytotrophoblasts during human placental development. Placenta 2002; 23:274-80; PMID:11969337; http://dx.doi.org/10.1053/plac.2001.0784
   PubMed Web of Science ®Google Scholar
• Dokras A, Coffin J, Field L, Frakes A, Lee H, Madan A, Nelson T, Ryu GY, Yoon JG, Madan A. Epigenetic regulation of maspin expression in the human placenta. Mol Hum Reprod 2006; 12:611-7; PMID:16936308; http://dx.doi.org/10.1093/molehr/gal074
   PubMed Web of Science ®Google Scholar
• Camolotto SA, Racca AC, Ridano ME, Genti-Raimondi S, Panzetta-Dutari GM. PSG gene expression is up-regulated by lysine acetylation involving histone and nonhistone proteins. PLoS One 2013; 8:e55992; PMID:23418492; http://dx.doi.org/10.1371/journal.pone.0055992
   PubMed Web of Science ®Google Scholar
• Murray K. THE OCCURRENCE OF EPSILON-N-METHYL LYSINE IN HISTONES. Biochemistry 1964; 3:10-5; PMID:14114491; http://dx.doi.org/10.1021/bi00889a003
   PubMed Web of Science ®Google Scholar
• Strahl BD, Ohba R, Cook RG, Allis CD. Methylation of histone H3 at lysine 4 is highly conserved and correlates with transcriptionally active nuclei in Tetrahymena. Proc Natl Acad Sci U S A 1999; 96:14967-72; PMID:10611321; http://dx.doi.org/10.1073/pnas.96.26.14967
   PubMed Web of Science ®Google Scholar
• Shilatifard A. Chromatin modifications by methylation and ubiquitination: implications in the regulation of gene expression. Annu Rev Biochem 2006; 75:243-69; PMID:16756492; http://dx.doi.org/10.1146/annurev.biochem.75.103004.142422
   PubMed Web of Science ®Google Scholar
• Fogarty NM, Burton GJ, Ferguson-Smith AC. Different epigenetic states define syncytiotrophoblast and cytotrophoblast nuclei in the trophoblast of the human placenta. Placenta 2015; 36(8):796-802; PMID:26008948
   PubMed Web of Science ®Google Scholar
• Ellery PM, Cindrova-Davies T, Jauniaux E, Ferguson-Smith AC, Burton GJ. Evidence for transcriptional activity in the syncytiotrophoblast of the human placenta. Placenta 2009; 30:329-34; PMID:19215981; http://dx.doi.org/10.1016/j.placenta.2009.01.002
   PubMed Web of Science ®Google Scholar
• Tachibana M, Sugimoto K, Nozaki M, Ueda J, Ohta T, Ohki M, Fukuda M, Takeda N, Niida H, Kato H, et al. G9a histone methyltransferase plays a dominant role in euchromatic histone H3 lysine 9 methylation and is essential for early embryogenesis. Genes Dev 2002; 16:1779-91; PMID:12130538; http://dx.doi.org/10.1101/gad.989402
   PubMed Web of Science ®Google Scholar
• Wang J, Mager J, Schnedier E, Magnuson T. The mouse PcG gene eed is required for Hox gene repression and extraembryonic development. Mamm Genome 2002; 13:493-503; PMID:12370779; http://dx.doi.org/10.1007/s00335-002-2182-7
   PubMed Web of Science ®Google Scholar
• Pawlak MR, Scherer CA, Chen J, Roshon MJ, Ruley HE. Arginine N-methyltransferase 1 is required for early postimplantation mouse development, but cells deficient in the enzyme are viable. Mol Cell Biol 2000; 20:4859-69; PMID:10848611; http://dx.doi.org/10.1128/MCB.20.13.4859-4869.2000
   PubMed Web of Science ®Google Scholar
• Hassa PO, Hottiger MO. The diverse biological roles of mammalian PARPS, a small but powerful family of poly-ADP-ribose polymerases. Front Biosci 2008; 13:3046-82; PMID:17981777; http://dx.doi.org/10.2741/2909
   PubMed Web of Science ®Google Scholar
• Messner S, Altmeyer M, Zhao H, Pozivil A, Roschitzki B, Gehrig P, Rutishauser D, Huang D, Caflisch A, Hottiger MO. PARP1 ADP-ribosylates lysine residues of the core histone tails. Nucleic Acids Res 2010; 38:6350-62; PMID:20525793; http://dx.doi.org/10.1093/nar/gkq463
   PubMed Web of Science ®Google Scholar
• Messner S, Hottiger MO. Histone ADP-ribosylation in DNA repair, replication and transcription. Trends Cell Biol 2011; 21:534-42; PMID:21741840; http://dx.doi.org/10.1016/j.tcb.2011.06.001
   PubMed Web of Science ®Google Scholar
• Hemberger M, Nozaki T, Winterhager E, Yamamoto H, Nakagama H, Kamada N, Suzuki H, Ohta T, Ohki M, Masutani M, et al. Parp1-deficiency induces differentiation of ES cells into trophoblast derivatives. Dev Biol 2003; 257:371-81; PMID:12729565; http://dx.doi.org/10.1016/S0012-1606(03)00097-6
   PubMed Web of Science ®Google Scholar
• Nozaki T, Masutani M, Watanabe M, Ochiya T, Hasegawa F, Nakagama H, Suzuki H, Sugimura T. Syncytiotrophoblastic giant cells in teratocarcinoma-like tumors derived from Parp-disrupted mouse embryonic stem cells. Proc Natl Acad Sci U S A 1999; 96:13345-50; PMID:10557323; http://dx.doi.org/10.1073/pnas.96.23.13345
   PubMed Web of Science ®Google Scholar
• Nozaki T, Fujimori H, Wang J, Suzuki H, Imai H, Watanabe M, Ohura K, Masutani M. Parp-1 deficiency in ES cells promotes invasive and metastatic lesions accompanying induction of trophoblast giant cells during tumorigenesis in uterine environment. Pathol Int 2013; 63:408-14; PMID:23957916; http://dx.doi.org/10.1111/pin.12086
   PubMed Web of Science ®Google Scholar
• Hotchkiss RD. The quantitative separation of purines, pyrimidines, and nucleosides by paper chromatography. J Biol Chem 1948; 175:315-32; PMID:18873306
   PubMed Web of Science ®Google Scholar
• Gellersen B, Kempf R. Human prolactin gene expression: positive correlation between site-specific methylation and gene activity in a set of human lymphoid cell lines. Mol Endocrinol 1990; 4:1874-86; PMID:1707126; http://dx.doi.org/10.1210/mend-4-12-1874
   PubMed Web of Science ®Google Scholar
• Niesen MI, Osborne AR, Yang H, Rastogi S, Chellappan S, Cheng JQ, Boss JM, Blanck G. Activation of a methylated promoter mediated by a sequence-specific DNA-binding protein, RFX. J Biol Chem 2005; 280:38914-22; PMID:16166088; http://dx.doi.org/10.1074/jbc.M504633200
   PubMed Web of Science ®Google Scholar
• van Dijk M, Drewlo S, Oudejans CB. Differential methylation of STOX1 in human placenta. Epigenetics 2010; 5:736-42; PMID:20716964; http://dx.doi.org/10.4161/epi.5.8.13084
   PubMed Web of Science ®Google Scholar
• Watt F, Molloy PL. Cytosine methylation prevents binding to DNA of a HeLa cell transcription factor required for optimal expression of the adenovirus major late promoter. Genes Dev 1988; 2:1136-43; PMID:3192075; http://dx.doi.org/10.1101/gad.2.9.1136
   PubMed Web of Science ®Google Scholar
• Ng HH, Bird A. DNA methylation and chromatin modification. Curr Opin Genet Dev 1999; 9:158-63; PMID:10322130; http://dx.doi.org/10.1016/S0959-437X(99)80024-0
   PubMed Web of Science ®Google Scholar
• Boyes J, Bird A. DNA methylation inhibits transcription indirectly via a methyl-CpG binding protein. Cell 1991; 64:1123-34; PMID:2004419; http://dx.doi.org/10.1016/0092-8674(91)90267-3
   PubMed Web of Science ®Google Scholar
• Ito S, Shen L, Dai Q, Wu SC, Collins LB, Swenberg JA, He C, Zhang Y. Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine. Science 2011; 333:1300-3; PMID:21778364; http://dx.doi.org/10.1126/science.1210597
   PubMed Web of Science ®Google Scholar
• Hsieh CL. In vivo activity of murine de novo methyltransferases, Dnmt3a and Dnmt3b. Mol Cell Biol 1999; 19:8211-8; PMID:10567546
   PubMed Web of Science ®Google Scholar
• Okano M, Bell DW, Haber DA, Li E. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 1999; 99:247-57; PMID:10555141; http://dx.doi.org/10.1016/S0092-8674(00)81656-6
   PubMed Web of Science ®Google Scholar
• Takeshima H, Suetake I, Shimahara H, Ura K, Tate S, Tajima S. Distinct DNA methylation activity of Dnmt3a and Dnmt3b towards naked and nucleosomal DNA. J Biochem 2006; 139:503-15; PMID:16567415; http://dx.doi.org/10.1093/jb/mvj044
   PubMed Web of Science ®Google Scholar
• Nakanishi MO, Hayakawa K, Nakabayashi K, Hata K, Shiota K, Tanaka S. Trophoblast-specific DNA methylation occurs after the segregation of the trophectoderm and inner cell mass in the mouse periimplantation embryo. Epigenetics 2012; 7:173-82; PMID:22395467; http://dx.doi.org/10.4161/epi.7.2.18962
   PubMed Web of Science ®Google Scholar
• Hemberger M. Genetic-epigenetic intersection in trophoblast differentiation: implications for extraembryonic tissue function. Epigenetics 2010; 5:24-9; PMID:20083894; http://dx.doi.org/10.4161/epi.5.1.10589
   PubMed Web of Science ®Google Scholar
• Liao J, Karnik R, Gu H, Ziller MJ, Clement K, Tsankov AM, Akopian V, Gifford CA, Donaghey J, Galonska C, et al. Targeted disruption of DNMT1, DNMT3A and DNMT3B in human embryonic stem cells. Nat Genet 2015; 47:469-78; PMID:25822089; http://dx.doi.org/10.1038/ng.3258
   PubMed Web of Science ®Google Scholar
• Koh KP, Yabuuchi A, Rao S, Huang Y, Cunniff K, Nardone J, Laiho A, Tahiliani M, Sommer CA, Mostoslavsky G, et al. Tet1 and Tet2 regulate 5-hydroxymethylcytosine production and cell lineage specification in mouse embryonic stem cells. Cell Stem Cell 2011; 8:200-13; PMID:21295276; http://dx.doi.org/10.1016/j.stem.2011.01.008
   PubMed Web of Science ®Google Scholar
• Sakaue M, Ohta H, Kumaki Y, Oda M, Sakaide Y, Matsuoka C, Yamagiwa A, Niwa H, Wakayama T, Okano M. DNA methylation is dispensable for the growth and survival of the extraembryonic lineages. Curr Biol 2010; 20:1452-7; PMID:20637626; http://dx.doi.org/10.1016/j.cub.2010.06.050
   PubMed Web of Science ®Google Scholar
• Vicovac L, Aplin JD. Epithelial-mesenchymal transition during trophoblast differentiation. Acta Anat (Basel) 1996; 156:202-16; PMID:9124037; http://dx.doi.org/10.1159/000147847
   PubMedGoogle Scholar
• Carver EA, Jiang R, Lan Y, Oram KF, Gridley T. The mouse snail gene encodes a key regulator of the epithelial-mesenchymal transition. Mol Cell Biol 2001; 21:8184-8; PMID:11689706; http://dx.doi.org/10.1128/MCB.21.23.8184-8188.2001
   PubMed Web of Science ®Google Scholar
• Blechschmidt K, Mylonas I, Mayr D, Schiessl B, Schulze S, Becker KF, Jeschke U. Expression of E-cadherin and its repressor snail in placental tissue of normal, preeclamptic and HELLP pregnancies. Virchows Arch 2007; 450:195-202; PMID:17149611; http://dx.doi.org/10.1007/s00428-006-0343-x
   PubMed Web of Science ®Google Scholar
• Chen Y, Wang K, Qian CN, Leach R. DNA methylation is associated with transcription of Snail and Slug genes. Biochem Biophys Res Commun 2013; 430:1083-90; PMID:23261445; http://dx.doi.org/10.1016/j.bbrc.2012.12.034
   PubMed Web of Science ®Google Scholar
• Blond JL, Lavillette D, Cheynet V, Bouton O, Oriol G, Chapel-Fernandes S, Mandrand B, Mallet F, Cosset FL. An envelope glycoprotein of the human endogenous retrovirus HERV-W is expressed in the human placenta and fuses cells expressing the type D mammalian retrovirus receptor. J Virol 2000; 74:3321-9; PMID:10708449; http://dx.doi.org/10.1128/JVI.74.7.3321-3329.2000
   PubMed Web of Science ®Google Scholar
• Ruebner M, Strissel PL, Ekici AB, Stiegler E, Dammer U, Goecke TW, Faschingbauer F, Fahlbusch FB, Beckmann MW, Strick R. Reduced syncytin-1 expression levels in placental syndromes correlates with epigenetic hypermethylation of the ERVW-1 promoter region. PLoS One 2013; 8:e56145; PMID:23457515; http://dx.doi.org/10.1371/journal.pone.0056145
   PubMed Web of Science ®Google Scholar
• Zhuang XW, Li J, Brost BC, Xia XY, Chen HB, Wang CX, Jiang SW. Decreased expression and altered methylation of syncytin-1 gene in human placentas associated with preeclampsia. Curr Pharm Des 2014; 20:1796-802; PMID:23888950; http://dx.doi.org/10.2174/13816128113199990541
   PubMed Web of Science ®Google Scholar
• Hu Y, Blair JD, Yuen RK, Robinson WP, von Dadelszen P. Genome-wide DNA methylation identifies trophoblast invasion-related genes: Claudin-4 and Fucosyltransferase IV control mobility via altering matrix metalloproteinase activity. Mol Hum Reprod 2015; 21:452-65; PMID:25697377; http://dx.doi.org/10.1093/molehr/gav007
   PubMed Web of Science ®Google Scholar
• Rachmilewitz J, Gileadi O, Eldar-Geva T, Schneider T, de-Groot N, Hochberg A. Transcription of the H19 gene in differentiating cytotrophoblasts from human placenta. Mol Reprod Dev 1992; 32:196-202; PMID:1497869; http://dx.doi.org/10.1002/mrd.1080320303
   PubMed Web of Science ®Google Scholar
• Lu LS, Hou Z, Li L, Yang YH, Wang XH, Zhang BL, Ren M, Zhao D, Miao Z, Yu L, et al. Methylation pattern of H19 exon 1 is closely related to preeclampsia and trophoblast abnormalities. Int J Mol Med 2014; 34:765-71; PMID:24969494
   PubMed Web of Science ®Google Scholar
• Guo L, Choufani S, Ferreira J, Smith A, Chitayat D, Shuman C, Uxa R, Keating S, Kingdom J, Weksberg R. Altered gene expression and methylation of the human chromosome 11 imprinted region in small for gestational age (SGA) placentae. Dev Biol 2008; 320:79-91; PMID:18550048; http://dx.doi.org/10.1016/j.ydbio.2008.04.025
   PubMed Web of Science ®Google Scholar
• Bourque DK, Avila L, Penaherrera M, von Dadelszen P, Robinson WP. Decreased placental methylation at the H19/IGF2 imprinting control region is associated with normotensive intrauterine growth restriction but not preeclampsia. Placenta 2010; 31:197-202; PMID:20060582; http://dx.doi.org/10.1016/j.placenta.2009.12.003
   PubMed Web of Science ®Google Scholar
• van Dijk M, van Bezu J, van Abel D, Dunk C, Blankenstein MA, Oudejans CB, Lye SJ. The STOX1 genotype associated with pre-eclampsia leads to a reduction of trophoblast invasion by α-T-catenin upregulation. Hum Mol Genet 2010; 19:2658-67; PMID:20400461; http://dx.doi.org/10.1093/hmg/ddq152
   PubMed Web of Science ®Google Scholar
• Wang H, Cheng H, Shao Q, Dong Z, Xie Q, Zhao L, Wang Q, Kong B, Qu X. Leptin-promoted human extravillous trophoblast invasion is MMP14 dependent and requires the cross talk between Notch1 and PI3K/Akt signaling. Biol Reprod 2014; 90:78; PMID:24571988; http://dx.doi.org/10.1095/biolreprod.113.114876
   PubMed Web of Science ®Google Scholar
• Schrey S, Kingdom J, Baczyk D, Fitzgerald B, Keating S, Ryan G, Drewlo S. Leptin is differentially expressed and epigenetically regulated across monochorionic twin placenta with discordant fetal growth. Mol Hum Reprod 2013; 19(11):764-72; PMID:23832168
   PubMed Web of Science ®Google Scholar
• Tahiliani M, Koh KP, Shen Y, Pastor WA, Bandukwala H, Brudno Y, Agarwal S, Iyer LM, Liu DR, Aravind L, et al. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 2009; 324:930-5; PMID:19372391; http://dx.doi.org/10.1126/science.1170116
   PubMed Web of Science ®Google Scholar
• Ficz G, Branco MR, Seisenberger S, Santos F, Krueger F, Hore TA, Marques CJ, Andrews S, Reik W. Dynamic regulation of 5-hydroxymethylcytosine in mouse ES cells and during differentiation. Nature 2011; 473:398-402; PMID:21460836; http://dx.doi.org/10.1038/nature10008
   PubMed Web of Science ®Google Scholar
• Chen Y, Wang K, Leach R. Five-Aza-dC treatment induces mesenchymal-to-epithelial transition in 1st trimester trophoblast cell line HTR8/SVneo. Biochem Biophys Res Commun 2013; 432:116-22; PMID:23376068; http://dx.doi.org/10.1016/j.bbrc.2013.01.075
   PubMed Web of Science ®Google Scholar
• Lytle JR, Yario TA, Steitz JA. Target mRNAs are repressed as efficiently by microRNA-binding sites in the 5′ UTR as in the 3′ UTR. Proc Natl Acad Sci U S A 2007; 104:9667-72; PMID:17535905; http://dx.doi.org/10.1073/pnas.0703820104
   PubMed Web of Science ®Google Scholar
• Landthaler M, Yalcin A, Tuschl T. The human DiGeorge syndrome critical region gene 8 and Its D. melanogaster homolog are required for miRNA biogenesis. Curr Biol 2004; 14:2162-7; PMID:15589161; http://dx.doi.org/10.1016/j.cub.2004.11.001
   PubMed Web of Science ®Google Scholar
• Fabian MR, Sonenberg N, Filipowicz W. Regulation of mRNA translation and stability by microRNAs. Annu Rev Biochem 2010; 79:351-79; PMID:20533884; http://dx.doi.org/10.1146/annurev-biochem-060308-103103
   PubMed Web of Science ®Google Scholar
• Choudhury M, Friedman JE. Epigenetics and microRNAs in preeclampsia. Clin Exp Hypertens 2012; 34:334-41; PMID:22468840; http://dx.doi.org/10.3109/10641963.2011.649931
   PubMed Web of Science ®Google Scholar
• Gu Y, Sun J, Groome LJ, Wang Y. Differential miRNA expression profiles between the first and third trimester human placentas. Am J Physiol Endocrinol Metabol 2013; 304:E836-43; PMID:23443922; http://dx.doi.org/10.1152/ajpendo.00660.2012
   PubMed Web of Science ®Google Scholar
• Morales-Prieto DM, Ospina-Prieto S, Chaiwangyen W, Schoenleben M, Markert UR. Pregnancy-associated miRNA-clusters. J Reprod Immunol 2013; 97:51-61; PMID:23432872; http://dx.doi.org/10.1016/j.jri.2012.11.001
   PubMed Web of Science ®Google Scholar
• Donker RB, Mouillet JF, Chu T, Hubel CA, Stolz DB, Morelli AE, Sadovsky Y. The expression profile of C19MC microRNAs in primary human trophoblast cells and exosomes. Mol Hum Reprod 2012; 18:417-24; PMID:22383544; http://dx.doi.org/10.1093/molehr/gas013
   PubMed Web of Science ®Google Scholar
• Xie L, Mouillet JF, Chu T, Parks WT, Sadovsky E, Knofler M, Sadovsky Y. C19MC microRNAs regulate the migration of human trophoblasts. Endocrinology 2014; 155:4975-85; PMID:25211593; http://dx.doi.org/10.1210/en.2014-1501
   PubMed Web of Science ®Google Scholar
• Mouillet JF, Donker RB, Mishima T, Cronqvist T, Chu T, Sadovsky Y. The unique expression and function of miR-424 in human placental trophoblasts. Biol Reprod 2013; 89:25; PMID:23803556; http://dx.doi.org/10.1095/biolreprod.113.110049
   PubMed Web of Science ®Google Scholar
• Luo L, Ye G, Nadeem L, Fu G, Yang BB, Honarparvar E, Dunk C, Lye S, Peng C. MicroRNA-378a-5p promotes trophoblast cell survival, migration and invasion by targeting Nodal. J Cell Sci 2012; 125:3124-32; PMID:22454525; http://dx.doi.org/10.1242/jcs.096412
   PubMed Web of Science ®Google Scholar
• Jones RL, Stoikos C, Findlay JK, Salamonsen LA. TGF-β superfamily expression and actions in the endometrium and placenta. Reproduction 2006; 132:217-32; PMID:16885531; http://dx.doi.org/10.1530/rep.1.01076
   PubMed Web of Science ®Google Scholar
• Nadeem U, Ye G, Salem M, Peng C. MicroRNA-378a-5p targets cyclin G2 to inhibit fusion and differentiation in BeWo cells. Biol Reprod 2014; 91:76; PMID:25122062; http://dx.doi.org/10.1095/biolreprod.114.119065
   PubMed Web of Science ®Google Scholar
• Fu G, Ye G, Nadeem L, Ji L, Manchanda T, Wang Y, Zhao Y, Qiao J, Wang YL, Lye S, et al. MicroRNA-376c impairs transforming growth factor-β and nodal signaling to promote trophoblast cell proliferation and invasion. Hypertension 2013; 61:864-72; PMID:23424236; http://dx.doi.org/10.1161/HYPERTENSIONAHA.111.203489
   PubMed Web of Science ®Google Scholar
• Bai Y, Yang W, Yang HX, Liao Q, Ye G, Fu G, Ji L, Xu P, Wang H, Li YX, et al. Downregulated miR-195 detected in preeclamptic placenta affects trophoblast cell invasion via modulating ActRIIA expression. PloS One 2012; 7:e38875; PMID:22723898; http://dx.doi.org/10.1371/journal.pone.0038875
   PubMed Web of Science ®Google Scholar
• Yu Y, Wang L, Liu T, Guan H. MicroRNA-204 suppresses trophoblast-like cell invasion by targeting matrix metalloproteinase-9. Biochem Biophys Res Commun 2015; 463(3):285-91.
   PubMed Web of Science ®Google Scholar
• Tamaru S, Mizuno Y, Tochigi H, Kajihara T, Okazaki Y, Okagaki R, Kamei Y, Ishihara O, Itakura A. MicroRNA-135b suppresses extravillous trophoblast-derived HTR-8/SVneo cell invasion by directly down regulating CXCL12 under low oxygen conditions. Biochem Biophys Res Commun 2015; 461:421-6; PMID:25896762; http://dx.doi.org/10.1016/j.bbrc.2015.04.055
   PubMed Web of Science ®Google Scholar
• Xie L, Mouillet JF, Chu T, Parks WT, Sadovsky E, Knofler M, Sadovsky Y. C19MC microRNAs Regulate the Migration of Human Trophoblasts. Endocrinology 2014; 155(12):4975-85: en20141501.
   PubMed Web of Science ®Google Scholar
• Wang Y, Zhang Y, Wang H, Wang J, Zhang Y, Wang Y, Pan Z, Luo S. Aberrantly up-regulated miR-20a in pre-eclampsic placenta compromised the proliferative and invasive behaviors of trophoblast cells by targeting forkhead box protein A1. Int J Biol Sci 2014; 10:973-82; PMID:25210495; http://dx.doi.org/10.7150/ijbs.9088
   PubMed Web of Science ®Google Scholar
• Luo R, Shao X, Xu P, Liu Y, Wang Y, Zhao Y, Liu M, Ji L, Li YX, Chang C, et al. MicroRNA-210 contributes to preeclampsia by downregulating potassium channel modulatory factor 1. Hypertension 2014; 64:839-45; PMID:24980667; http://dx.doi.org/10.1161/HYPERTENSIONAHA.114.03530
   PubMed Web of Science ®Google Scholar
• Li P, Guo W, Du L, Zhao J, Wang Y, Liu L, Hu Y, Hou Y. microRNA-29b contributes to pre-eclampsia through its effects on apoptosis, invasion and angiogenesis of trophoblast cells. Clin Sci 2013; 124:27-40; PMID:22716646; http://dx.doi.org/10.1042/CS20120121
   PubMed Web of Science ®Google Scholar
• Li Q, Pan Z, Wang X, Gao Z, Ren C, Yang W. miR-125b-1-3p inhibits trophoblast cell invasion by targeting sphingosine-1-phosphate receptor 1 in preeclampsia. Biochem Biophys Res Commun 2014; 453:57-63; PMID:25251470; http://dx.doi.org/10.1016/j.bbrc.2014.09.059
   PubMed Web of Science ®Google Scholar
• Li X, Li C, Dong X, Gou W. MicroRNA-155 inhibits migration of trophoblast cells and contributes to the pathogenesis of severe preeclampsia by regulating endothelial nitric oxide synthase. Mol Med Rep 2014; 10:550-4; PMID:24806148
   PubMed Web of Science ®Google Scholar
• Khong TY, De Wolf F, Robertson WB, Brosens I. Inadequate maternal vascular response to placentation in pregnancies complicated by pre-eclampsia and by small-for-gestational age infants. Br J Obstet Gynaecol 1986; 93:1049-59; PMID:3790464; http://dx.doi.org/10.1111/j.1471-0528.1986.tb07830.x
   PubMedGoogle Scholar
• Allaire AD, Ballenger KA, Wells SR, McMahon MJ, Lessey BA. Placental apoptosis in preeclampsia. Obstet Gynecol 2000; 96:271-6; PMID:10908776; http://dx.doi.org/10.1016/S0029-7844(00)00895-4
   PubMed Web of Science ®Google Scholar
• Xu P, Zhao Y, Liu M, Wang Y, Wang H, Li YX, Zhu X, Yao Y, Wang H, Qiao J, et al. Variations of microRNAs in human placentas and plasma from preeclamptic pregnancy. Hypertension 2014; 63:1276-84; PMID:24664294; http://dx.doi.org/10.1161/HYPERTENSIONAHA.113.02647
   PubMed Web of Science ®Google Scholar
• Dai Y, Qiu Z, Diao Z, Shen L, Xue P, Sun H, Hu Y. MicroRNA-155 inhibits proliferation and migration of human extravillous trophoblast derived HTR-8/SVneo cells via down-regulating cyclin D1. Placenta 2012; 33:824-9; PMID:22858023; http://dx.doi.org/10.1016/j.placenta.2012.07.012
   PubMed Web of Science ®Google Scholar
• Zou Y, Jiang Z, Yu X, Sun M, Zhang Y, Zuo Q, Zhou J, Yang N, Han P, Ge Z, et al. Upregulation of long noncoding RNA SPRY4-IT1 modulates proliferation, migration, apoptosis, and network formation in trophoblast cells HTR-8SV/neo. PLoS One 2013; 8:e79598; PMID:24223182; http://dx.doi.org/10.1371/journal.pone.0079598
   PubMed Web of Science ®Google Scholar
• van Dijk M, Oudejans CB. STOX1: Key player in trophoblast dysfunction underlying early onset preeclampsia with growth retardation. J Pregnancy 2011; 2011:521826; PMID:21490791; http://dx.doi.org/10.1155/2011/521826
   PubMedGoogle Scholar
• Higashijima A, Miura K, Mishima H, Kinoshita A, Jo O, Abe S, Hasegawa Y, Miura S, Yamasaki K, Yoshida A, et al. Characterization of placenta-specific microRNAs in fetal growth restriction pregnancy. Prenat Diagn 2013; 33:214-22; PMID:23354729; http://dx.doi.org/10.1002/pd.4045
   PubMed Web of Science ®Google Scholar