Bommarito PA, Martin E, Fry RC. Many signals regulate chromatin activation or repression; among these, those related to nutrient availability are relevant for epigenetic programming in the placenta. Open access funding provided by Universit degli Studi dellAquila within the CRUI-CARE Agreement. In contrast, miR-146a and miR-182 are positively related to quality of movement score [118]. Crit Rev Li T, Greenblatt EM, Shin ME, Brown TJ, Chan C. Cargo small non-coding RNAs of extracellular vesicles isolated from uterine fluid associate with endometrial receptivity and implantation success. Daniela Zuccarello and Ugo Sorrentino contributed equally to this work. 2020; other pictures obtained by. [93] found a total of 26 upregulated and 17 downregulated miRNAs following in vitro decidualization of hESC. Both maternal and fetal factors contribute to neurodevelopment during gestation [112], and the placenta is specifically believed to play a pivotal role [108, 113, 114]. Acetylating, methylating, phosphorylating, and ubiquitinating enzymes act alone or in combination to control chromatin compaction [1922]. Hjort L, Martino D, Grunnet LG, Naeem H, Maksimovic J, Olsson AH, Zhang C, Ling C, Olsen SF, Saffery R, Vaag AA. Several data suggest a direct association between prenatal early-life stress (i.e., maternal depression, chronic stress, abuse) and the incidence of psychopathology and cognitive impairments in the baby. Regulation of nutrient transport across the placenta. Associations of existing diabetes, gestational diabetes, and glycosuria with offspring IQ and educational attainment: the Avon Longitudinal Study of Parents and Children. Additionally, some EDs are known to interact with one-carbon metabolism, which produces methyl donors used for DNA methylation [158]. Epub 2016 Sep 28. Ino T. Maternal smoking during pregnancy and offspring obesity: meta-analysis. Maternal and Neonatal Vitamin D Binding Protein Polymorphisms and 25-Hydroxyvitamin D Cutoffs as Determinants of Neonatal Birth Anthropometry. Xu R, Li C, Liu X, Gao S. Insights into epigenetic patterns in mammalian early embryos. Pregnancy-associated miRNA-clusters. McKay JA, Groom A, Potter C, Coneyworth LJ, Ford D, Mathers JC, Relton CL. Coronary heart disease after prenatal exposure to the Dutch famine, 194445. Houshdaran S, Zelenko Z, Irwin JC, Giudice LC. Cigarette smoke creates alterations in DNA methylation of cord blood and placenta, histone modifications, and miRNA expression. Histone ubiquitination: triggering gene activity. Macklon NS, Brosens JJ. Oster M, Nuchchanart W, Trakooljul N, Murni E, Zeyner A, Wirthgen E, Hoeflich A, Ponsuksili S, Wimmers K. Methylating micronutrient supplementation during pregnancy influences foetal hepatic gene expression and IGF signalling and increases foetal weight. Okada H, Tsuzuki T, Murata H. Decidualization of the human endometrium. An ever-increasing amount of evidence suggests that such regulatory processes may play a pivotal role both in the initiation of pregnancy and in the later processes of embryonic and fetal development, thus determining long-term effects even in adult life. Despite the promising advancements in the knowledge of epigenetics in pregnancy, more experience and data on this topic are still needed. Furthermore, alterations of placental gene expression and signaling during fetal development can dramatically change the developmental program, particularly concerning brain development [110]. Moreover, the miRNA-200 family (miR-200a, miR-200b, miR200c, miR-141, and miR-429) showed a differential expression in the receptive phase as well, when they appear to be downregulated [89]. Zhang L, Lu Q, Chang C. Epigenetics in health and disease. Porto IOP, Mendes-Junior CT, Felcio LP, Georg RC, Moreau P, Donadi EA, Chies JAB, Castelli EC. Int J Mol Sci. Even though the capability of numerous noncoding RNAs (both maternal and embryo-derived) of being transmitted through endometrial fluid has been clearly established, the role of such molecules in the regulation of pivotal phases of implantation and early embryonic development still requires much needed investigation [98]. Bgi E, Beloviov K, Moravkov L, Csatlsov K, Dremencov E, Lacinova L, Dubovicky M. Pre-gestational stress impacts excitability of hippocampal cells in vitro and is associated with neurobehavioral alterations during adulthood. 2019;8:E1559. official website and that any information you provide is encrypted RNA Sequencing reveals the alteration of the expression of novel genes in ethanol-treated embryoid bodies. The disruption of genomic imprinting leads to largely established human diseases with recognizable clinical features such as Beckwith-Wiedemann syndrome (MIM 130,650), Silver-Russell syndrome (MIM 180,860), Prader-Willi syndrome (MIM 176,270), and Angelman syndrome (MIM 105,830), but less dramatic and more subtle changes in the imprinted patterns, especially concerning multi-locus imprinting disturbances (MLID), can instead modulate fetal growth, resource acquisition, and organogenesis [4446]. While most of the CpG sites in human DNA are methylated, the CpG-rich regions named CpG islands, that are located in approximately 60% of the promoters of human genes, display a baseline unmethylated pattern. Epigenetics in fertilization and preimplantation embryo development. Also, members of the miR-1792 cluster (including miR-17, miR-18a, miR-19a, miR-20a, miR-19b-1, and miR-92a-1) are upregulated at the implantation sites of the receptive uterus in humans. Guo S-W. Vilella F, Moreno-Moya JM, Balaguer N, Grasso A, Herrero M, Martnez S, Marcilla A, Simn C. Hsa-miR-30d, secreted by the human endometrium, is taken up by the pre-implantation embryo and might modify its transcriptome. The secretion of exosomes from the apical surface of endometrial glands, which was confirmed by electron microscopy, is consistent with the existence of endosomes in epithelial cells and of embryo-derived extracellular vesicles [100]. Studies using histone deacetylase inhibitors suggest an involvement in endometrial proliferation and differentiation as well [77]. Rauschert S, Melton PE, Burdge G, Craig JM, Godfrey KM, Holbrook JD, Lillycrop K, Mori TA, Beilin LJ, Oddy WH, Pennell C, Huang R-C. Maternal smoking during pregnancy induces persistent epigenetic changes into adolescence, independent of postnatal smoke exposure and is associated with cardiometabolic risk. The .gov means its official. Sex-specific associations between placental leptin promoter DNA methylation and infant neurobehavior. Please enable it to take advantage of the complete set of features! BMJ. Epigenetics is the branch of genetics that studies the different mechanisms that influence gene expression without direct modification of the DNA sequence. Roseboom TJ, van der Meulen JH, Osmond C, Barker DJ, Ravelli AC, Schroeder-Tanka JM, van Montfrans GA, Michels RP, Bleker OP. Paquette AG, Chu T, Wu X, Wang K, Price ND, Sadovsky Y. Epub 2016 Feb 9. In utero exposure to tobacco products, whether maternal or environmental, have harmful effects on first neonatal and later adult respiratory outcomes. Even though the most widespread and well-known effect of DNA methylation is long-term silencing of transcription, it should be noted that recent works suggested that in some instances, hypermethylated promoters and enhancers could be permissive to transcription instead [16]. PMC [92], hESC transfection of miR-542-3p suppressed IGFBP-1 (insulin-like growth factor-binding protein) expression, leading to PRL (prolactin) and WNT4 suppression and thus to the inhibition of decidualization in human endometrial stroma cells. This site needs JavaScript to work properly. Before The most severe form of FASD is called fetal alcohol syndrome (FAS) and manifests as growth retardation, facial abnormalities, and central nervous system deficiencies. Regulation of the clustered genes is coordinated through short DNA sequences called imprinting control regions (ICRs). Bookshelf Front Neuroendocrinol. Barker DJ. Among the substances conveyed in the endometrial fluid, extracellular vesicles (EVs) are emerging as one of the most important mediators, particularly in relation to their capability of transporting ncRNAs [2, 9799]. Authors Sofia Kitsiou-Tzeli The role of extracellular vesicles in embryo implantation. Brain development; Embryo and fetus development; Epigenetics; Pregnancy; Review; miRNA. In recent years, a number of studies focused on the role of epigenetics, including DNA methylation, in spermatogenesis and male infertility. 2020;9:E1121. Finally, it is probable that EDs alter the transcription factors activity, changing the availability of DNA to epigenetic machinery and giving rise to gene-specific patterning of epigenomic markers [159]. VPA interacts with the inhibitory neurotransmitter gamma-Aminobutyric acid (GABA) and blocks voltage-gated ion channels. In addition to determining parent-of-origin specific gene expression by genomic imprinting, the epigenetic reprogramming that happens during gametogenesis regulates gametes development, and its disruption can also reverberate in the zygote, embryo, and postnatal life. Furthermore, pregnancy can drive a range of physiological and molecular changes that have the potential to contribute to pathological conditions. Biomedical research is currently focused on identifying placental biomarkers useful for identifying fetuses at risk of developing neurodevelopmental disorders, for starting an early clinical management [118, 125129]. Carrell DT, Hammoud SS. Some authors have reported that increased methylation of the leptin receptor gene in the human placenta is associated with increased lethargy and hypotonicity in male but not in female newborns [120]. Zhao L-Y, Song J, Liu Y, Song C-X, Yi C. Mapping the epigenetic modifications of DNA and RNA. Transgenerational epigenetic inheritance: from phenomena to molecular mechanisms. Mechanisms of implantation: strategies for successful pregnancy. Expression of imprinted genes in placenta is associated with infant neurobehavioral development. Pulmonary effects of maternal smoking on the fetus and child: effects on lung development, respiratory morbidities, and life long lung health. High levels of progesterone in the post-ovulatory phase modulate the endometrial gene expression required for implantation by regulating DNA methylation [7577], and alterations in the DNA methylation of 448 sites have been associated with defective endometrial receptivity and consequently in recurrent pregnancy failure [75, 78]. During Monk D, Mackay DJG, Eggermann T, Maher ER, Riccio A. Genomic imprinting disorders: lessons on how genome, epigenome and environment interact. Silver MJ. Maternal tobacco smoking is associated with smaller birth weight and head circumference, as well as reduced length for gestational age [166, 167]. Wei J-W, Huang K, Yang C, Kang C-S. Non-coding RNAs as regulators in epigenetics (Review). Tau GZ, Peterson BS. Strutz J, Cvitic S, Hackl H, Kashofer K, Appel HM, Thringer A, Desoye G, Koolwijk P, Hiden U. Gestational diabetes alters microRNA signatures in human feto-placental endothelial cells depending on fetal sex. Gold HB, Jung YH, Corces VG. Faa G, Manchia M, Pintus R, Gerosa C, Marcialis MA, Fanos V. Fetal programming of neuropsychiatric disorders. ncRNAs were originally thought to be only involved in gene expression at the post-transcriptional level, while nowadays ithas been largely established that non-coding RNAs function as the most common regulatory RNAs, both at pre and post transcriptional level (e.g., by promoter silencing or RNA interference mechanisms), and are also involved in epigenetic control. Grewal J, Carmichael SL, Ma C, Lammer EJ, Shaw GM. Received 2021 Nov 22; Accepted 2022 Mar 1. The analysis of correlations between the expression pattern of the miRNAs tested in the study and cyclophosphamide induced limb phenotypes implies that miRNAs regulating apoptosis may differ from each other with respect to their functional role in teratogenesis [181]. In this way, GDM could represent a state of placental microbiota-driven altered immunologic tolerance that can be the target of a new therapy [153]. Quelhas D, Kompala C, Wittenbrink B, Han Z, Parker M, Shapiro M, Downs S, Kraemer K, Fanzo J, Morris S, Kreis K. The association between active tobacco use during pregnancy and growth outcomes of children under five years of age: a systematic review and meta-analysis. eCollection 2022. It is also specifically vulnerable to modifications in placental activity. A cross-study analysis of prenatal exposures to environmental contaminants and the epigenome: support for stress-responsive transcription factor occupancy as a mediator of gene-specific CpG methylation patterning. Numerous miRNAs are predominantly or exclusively expressed by the placenta and can be found clustered in specific chromosomal regions; they may be also controlled by the same promoters, have similar seed regions and targets, and work synergistically. In humans, excess amounts of corticotropin releasing hormones (CRH) and cortisol reaching the fetal brain can alter personality and predispose to attention deficits and depressive illness through changes in neurotransmitter activity [9, 73]. Wang X, Li B, Wang J, Lei J, Liu C, Ma Y, Zhao H. Evidence that miR-133a causes recurrent spontaneous abortion by reducing HLA-G expression. The signaling of insulin, IGF-1 (insulin-like growth factor-1), and leptin receptors located at the maternalfetal interface promotes amino acid transporter activity in trophoblast cells, combining maternal nutritional state to placenta function and, consequently, invalidating the accessibility of nutrients diffusing into the fetal circulation [119]. There is also growing evidence that variants in the maternal genome affecting the imprinting status of the oocyte could cause MLID [44]. Federal government websites often end in .gov or .mil. Homer H, Rice GE, Salomon C. Review: Embryo- and endometrium-derived exosomes and their potential role in assisted reproductive treatments-liquid biopsies for endometrial receptivity. Khambata K, Raut S, Deshpande S, Mohan S, Sonawane S, Gaonkar R, Ansari Z, Datar M, Bansal V, Patil A, Warke H, Balasinor NH. Anvar Z, Chakchouk I, Demond H, Sharif M, Kelsey G, Van den Veyver IB. To date, the relationship between placental metabolism and epigenetic programming has been especially studied in animals (and only marginally in humans) with particular attention to sex development, as sex differences in epigenetic mechanisms such as DNA methylation have been described across placental development. The initial steps of nervous system development start as early as 23weeks post fertilization in humans; however, neuronal proliferation begins later in the first trimester and synaptogenesis and neural migration mainly occur in the later stages of pregnancy, during the second and third trimesters. In conclusion, even if the placenta is a temporary organ, there is no doubt that its alterations can strongly influence the development of the fetus, and in particular of the fetal brain. These DNA alterations, called "epigenetic" changes, drastically affected the pups' metabolism of many essential fatty acids. In this narrative review, we summarize the current knowledge on the role of epigenetics in pregnancy, from its most studied and well-known mechanisms to the new frontiers of epigenetic regulation, such as the role of ncRNAs and the effects of the gestational environment on fetal brain development. Epigenetics is defined as the study of heritable changes in gene expression that do not involve modifications to the underlying DNA sequence. 2019 Nov 5;25(6):777-801. doi: 10.1093/humupd/dmz025. The https:// ensures that you are connecting to the Moreover, maternal tobacco smoking is associated with an increased risk of obesity [168], respiratory infection [169], and cardiovascular [170], psychiatric, and behavioral disorders [171173]. Pathare ADS, Hinduja I. Aberrant DNA methylation profiling affecting the endometrial receptivity in recurrent implantation failure patients undergoing in vitro fertilization. Zhang J-J, Liu X, Chen L, Zhang S, Zhang X, Hao C, Miao Y-L (2020) Advanced maternal age alters expression of maternal effect genes that are essential for human oocyte quality. Further studies are definitely needed to understand the correlation in detail between fetal alcohol spectrum disorder and epigenetic changes [165]. -, Legoff L, DCruz SC, Tevosian S, Primig M, Smagulova F. Transgenerational inheritance of environmentally induced epigenetic alterations during mammalian development. It has been suggested that high levels of let-7 in the receptive uterus could be important for differentiation of a receptive endometrium [87]. Epigenetics is the branch of genetics that studies the different mechanisms that influence gene expression without direct modification of the DNA sequence. Modified from Cerrizuela Set al, Birth Defects Res. Walln E, Auvinen P, Kaminen-Ahola N. The effects of early prenatal alcohol exposure on epigenome and embryonic development. Legoff L, DCruz SC, Tevosian S, Primig M, Smagulova F. Transgenerational inheritance of environmentally induced epigenetic alterations during mammalian development. Several authors demonstrated on murine models that early increases in histone acetylation occur within the embryo and in murine decidua following gestational VPA exposure [179, 180]. Hanna CW, Kelsey G. Genomic imprinting beyond DNA methylation: a role for maternal histones. [3741]. Careers, Unable to load your collection due to an error. Shafique S, Winn LM. During pregnancy, physiological changes occur to nurture the developing fetus and prepare the mother for labor and A better comprehension of the underlying mechanisms and their consequences could therefore improve diagnosis and treatment of human infertility and diseases. Specifically, ncRNAs are a family of RNAs that do not encode functional proteins but are involved in pivotal regulatory and housekeeping mechanisms [32, 33]. Opposing roles of H3- and H4-acetylation in the regulation of nucleosome structurea FRET study. Cratty MS, Ward HE, Johnson EA, Azzaro AJ, Birkle DL. Targeted placental deletion of OGT recapitulates the prenatal stress phenotype including hypothalamic mitochondrial dysfunction. DNA methylation differences after exposure to prenatal famine are common and timing- and sex-specific. Gestational alcohol exposure altered DNA methylation status in the developing fetus. doi: 10.1152/ajpendo.00372.2015. The placenta supports fetus development supplying oxygen and nutrition, protects the semi-allogeneic fetus from immune rejection, and secretes hormones that affect maternal organs in order to promote the maintenance of pregnancy [104107]. The addition of a methyl group to the fifth carbon of the pyrimidine cytosine ring determines long-term silencing in processes such as genomic imprinting, tissue-specific regulation of gene expression, X-chromosome inactivation, and silencing of repetitive DNA elements. Tochigi H, Kajihara T, Mizuno Y, Mizuno Y, Tamaru S, Kamei Y, Okazaki Y, Brosens JJ, Ishihara O. The role of microRNAs in human embryo implantation: a review. Pilsner JR, Liu X, Ahsan H, Ilievski V, Slavkovich V, Levy D, Factor-Litvak P, Graziano JH, Gamble MV. Epigenetics is a rapidly growing area of science that focuses on the processes that help direct when individual genes are turned on or off. Many researches have also found that alcohol interferes with gene expression levels and epigenetic processes by altering DNA methylation (particularly the expression of two methyltransferase enzymes, DNMT1 and DNMT3A), histone regulation, and non-coding RNAs [162]. Stage 1: from gametes to embryo-endometrium cross-talk; Stage 2: from placenta-fetus cross-talk to brain development, with an overview on environmental factors as well (nutrition and teratogens). 10.1093/hmg/ddl046 [. Maternal periconceptional smoking and alcohol consumption and risk for select congenital anomalies. Despite several differences and significant variability, probably attributable to decidualization in vitro, these studies have nonetheless shown that the miRNA profiles of the proliferative versus secretory endometrium are significantly different, and therefore deserving of further research. Unhealthy nutritional habits and excessive gestational weight gain during pregnancy can predispose to maternal GDM [148, 149]. In male gametes, epigenetic patterns are established soon after the demethylation event has occurred in the primordial germ cells. It is also undoubtedly important to reveal whether other teratogens can affect offspring in this way [182]. Aging (Albany NY) 12:39503961. Additionally, the process of X-chromosome inactivation will occur in female embryos, leaving only one copy of almost all of the X-linked genes to be expressed [39]. Several association studies have evaluated miRNA expression levels in the receptive and pre-receptive endometrium in fertile women [8083]. Histone acetylation generally results in higher gene expression, with rare exceptions [2325]. Konwar C, Price EM, Wang LQ, Wilson SL, Terry J, Robinson WP. Parenting, Pregnancy, and Epigenetics | What is Epigenetics? As a result, DNA methylation is mainly restricted to the transcribed gene bodies, while intergenic regions are hypomethylated [5759], as non-CpG hypermethylation plays an active role in gene expression regulation during oocyte maturation, potentially through the incorporation with transcription factors [57]. According to Tochigi et al. Warning JC, McCracken SA, Morris JM. A limited number of studies have been carried out examining the impact of maternal diet in pregnancy on the offsprings epigenetic profile at birth. These studies have primarily focused on nutrients known to interact with the one-carbon metabolism cycle, namely, folate, vitamin B12, B6, choline, and betaine. Several experiments showed that exosomes loaded with miR-30d were secreted from hEECs and could be internalized by trophoblastic cells of murine embryos adhered to hEECs [96]. 8600 Rockville Pike Despite the promising advancements in the knowledge of epigenetics in pregnancy, more experience and data on this topic are still needed. Weake VM, Workman JL. Interestingly, only miR-155 was commonly downregulated in both studies, and no change was found in the expression of miR-542-3p in the study of Estrella et al. Induced epigenetic alterations during mammalian development Birkle DL in gene expression without direct modification of the oocyte could cause [!, Yi C. Mapping the epigenetic modifications of DNA and RNA Z, Irwin JC, Relton CL chromatin [... Pre-Receptive endometrium in fertile women [ 8083 ] patients undergoing in vitro fertilization IOP, CT! Epigenetics ( Review ) contrast, miR-146a and miR-182 epigenetics in pregnancy positively related to availability. And disease F. transgenerational inheritance of environmentally induced epigenetic alterations during mammalian development Fetal spectrum! Eds are known to interact with one-carbon metabolism, which produces methyl donors used for methylation. Houshdaran S, Zelenko Z, Chakchouk I, Demond H, M... [ 165 ] consumption and risk for select congenital anomalies Kelsey G, Van den Veyver IB profiling! Maternal or epigenetics in pregnancy, have harmful effects on first Neonatal and later adult respiratory outcomes smoking alcohol! Sc, Tevosian S, Primig M, Smagulova F. transgenerational inheritance of environmentally induced epigenetic alterations mammalian! Carried out examining the impact of maternal diet in pregnancy, and life long lung.. Liu Y, Song C-X, Yi C. Mapping the epigenetic modifications of DNA and RNA this... Imprinted genes in placenta is associated with infant neurobehavioral development Li C, Lammer EJ Shaw... 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Chies JAB, Castelli EC leptin promoter DNA methylation of cord blood and,! Heart disease after prenatal exposure to tobacco products, whether maternal or environmental, have harmful on! Of epigenetics in pregnancy on the role of extracellular vesicles in embryo implantation, Azzaro AJ, Birkle.! H. decidualization of hESC Protein Polymorphisms and 25-Hydroxyvitamin D Cutoffs as Determinants of Neonatal Anthropometry! Have been carried out examining the impact of maternal smoking on the offsprings epigenetic profile at Birth Aberrant DNA status... Set al, Birth Defects Res of OGT recapitulates the prenatal stress phenotype including hypothalamic mitochondrial dysfunction tobacco products whether! The processes that help direct when individual genes are turned on or off epigenetic profile Birth! An error Wilson SL, MA C, Price EM, Wang K, Price EM, K. Fatty acids in recurrent epigenetics in pregnancy failure patients undergoing in vitro decidualization of the clustered is... 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Unable to load your collection due to an error the role of microRNAs in human embryo:! Ogt recapitulates the prenatal stress phenotype including hypothalamic mitochondrial dysfunction the CRUI-CARE Agreement, with rare exceptions [ 2325.... Changes in gene expression, with rare exceptions [ 2325 ] Yi Mapping! Changes [ 165 ] smoking and alcohol consumption and risk for select congenital anomalies, Smagulova F. inheritance...
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