Newborn

Register      Login

VOLUME 3 , ISSUE 3 ( July-September, 2024 ) > List of Articles

REVIEW ARTICLE

A Primer on Epigenetic Changes: The More We Know, the More We Find in Fetuses and Infants

Srijan Singh, Adrianna Frydrysiak-Brzozowska, Aimen E Ben Ayad, Saida S Khasanova, Jeremias Bordon, Colin Michie

Keywords : DNA methylation, Epigenetics, Genomic Imprinting, Histones, Infant, miRNA, Neonate, Newborn, RNA silencing

Citation Information : Singh S, Frydrysiak-Brzozowska A, Ayad AE, Khasanova SS, Bordon J, Michie C. A Primer on Epigenetic Changes: The More We Know, the More We Find in Fetuses and Infants. 2024; 3 (3):219-232.

DOI: 10.5005/jp-journals-11002-0104

License: CC BY-NC 4.0

Published Online: 30-09-2024

Copyright Statement:  Copyright © 2024; The Author(s).


Abstract

Epigenetics is the study of heritable traits that happen without changes to the DNA sequence. The Greek prefix epi- implies features that modify the traditional genetic mechanisms of inheritance. Increasing information underscores the importance of epigenetic changes during the fetal period and infancy. The most frequently seen epigenetic changes are mediated via DNA methylation, changes in gene expression due to non-coding RNAs, and post-translational modifications of histone proteins. DNA methylation can be confirmed using methods such as bisulfite treatment, enzyme sensitivity assays, and antibody specificity-based techniques. Histone modifications are typically detected through antibody recognition. Chromatin immunoprecipitation (ChIP) is an antibody-based technology to selectively enrich specific DNA-binding proteins along with their DNA targets. Since epigenetic alterations are often reversible, modifying epigenetic marks contributing to disease development may provide an approach to designing new therapies. Gene hypermethylation and histone hypoacetylation are attractive targets for the treatment of epigenetic diseases because these epigenetic alterations are reversible. The first 1000 days of life, from conception through infancy, comprise the most-likely time-period for environmental exposures and nutrition to exert beneficial/potentially harmful epigenetic effects. During this period, a typical metabolic reprogramming induced by extrinsic factors such as allergens, viruses, pollutants, diet, or microbiome might drive cellular metabolic dysfunctions and defective immune responses in allergic diseases. Epigenetics also plays a role in the developmental origins of adult metabolic diseases.


PDF Share
  1. Dupont C, Armant DR, Brenner CA. Epigenetics: Definition, mechanisms and clinical perspective. Semin Reprod Med 2009;27(5):351. DOI: 10.1055/S-0029-1237423.
  2. Waddington CH. The epigenotype. 1942. Int J Epidemiol 2012;41(1): 10–13. DOI: 10.1093/IJE/DYR184.
  3. Tarakhovsky A. Tools and landscapes of epigenetics. Nat Immunol 2010;11(7):565–568. DOI: 10.1038/NI0710-565.
  4. Zoghbi HY, Beaudet AL. Epigenetics and human disease. Cold Spring Harb Perspect Biol 2016;8(2):1–28. DOI: 10.1101/CSHPERSPECT.A019497.
  5. Wu CT, Morris JR. Genes, genetics, and epigenetics: A correspondence. Science 2001;293(5532):1103–1105. DOI: 10.1126/SCIENCE.293.5532.1103.
  6. Fazzari MJ, Greally JM. Epigenomics: Beyond CpG islands. Nat Rev Genet 2004;5(6):446–455. DOI: 10.1038/NRG1349.
  7. Wallace DC, Fan W. Energetics, epigenetics, mitochondrial genetics. Mitochondrion 2010;10(1):12–31. DOI: 10.1016/J.MITO.2009.09.006.
  8. Kanherkar RR, Bhatia-Dey N, Csoka AB. Epigenetics across the human lifespan. Front Cell Dev Biol 2014;2:49. DOI: 10.3389/FCELL.2014.00049.
  9. Barbara MA, Abdilla Y, Calleja-Agius J. An introduction to epigenetics. Neonatal Netw 2017;36(3):124–128. DOI: 10.1891/0730-0832.36.3.124.
  10. Bird A. Perceptions of epigenetics. Nature 2007;447(7143):396–398. DOI: 10.1038/NATURE05913.
  11. Reik W. Stability and flexibility of epigenetic gene regulation in mammalian development. Nature 2007;447(7143):425–432. DOI: 10.1038/NATURE05918.
  12. Nair J, Maheshwari A. Epigenetics in necrotizing enterocolitis. Curr Pediatr Rev 2021;17(3):172–184. DOI: 10.2174/1573396317666210421110608.
  13. Acevedo N, Alhamwe BA, Caraballo L, et al. Perinatal and early-life nutrition, epigenetics, and allergy. Nutrients 2021;13(3):1–53. DOI: 10.3390/NU13030724.
  14. Handy DE, Castro R, Loscalzo J. Epigenetic modifications: Basic mechanisms and role in cardiovascular disease. Circulation 2011;123(19):2145–2156. DOI: 10.1161/CIRCULATIONAHA.110.956839.
  15. Tost J. A translational perspective on epigenetics in allergic diseases. J Allergy Clin Immunol 2018;142(3):715–726. DOI: 10.1016/J.JACI.2018.07.009.
  16. Grazioli E, Dimauro I, Mercatelli N, et al. Physical activity in the prevention of human diseases: Role of epigenetic modifications. BMC Genomics 2017;18(8):111–123. DOI: 10.1186/S12864-017-4193-5/FIGURES/1.
  17. Felsenfeld G. A brief history of epigenetics. Cold Spring Harb Perspect Biol 2014;6(1):a018200. DOI: 10.1101/CSHPERSPECT.A018200.
  18. Bellanti JA. Epigenetic studies and pediatric research. Pediatr Res 2020;87(2):378–384. DOI: 10.1038/S41390-019-0644-9.
  19. Alhamwe BA, Miethe S, von Strandmann EP, et al. Epigenetic regulation of airway epithelium immune functions in asthma. Front Immunol 2020;11:1747. DOI: 10.3389/FIMMU.2020.01747.
  20. Alaskhar Alhamwe B, Khalaila R, Wolf J, et al. Histone modifications and their role in epigenetics of atopy and allergic diseases. Allergy Asthma Clin Immunol 2018;14(1):39. DOI: 10.1186/S13223-018-0259-4.
  21. Potaczek DP, Harb H, Michel S, et al. Epigenetics and allergy: From basic mechanisms to clinical applications. Epigenomics 2017;9(4):539–571. DOI: 10.2217/EPI-2016-0162.
  22. Brook PO, Perry MM, Adcock IM, et al. Epigenome-modifying tools in asthma. Epigenomics 2015;7(6):1017–1032. DOI: 10.2217/EPI. 15.53.
  23. Moore LD, Le T, Fan G. DNA methylation and its basic function. Neuropsychopharmacology 2013 38:1. 2012;38(1):23–38. DOI: 10.1038/npp.2012.112.
  24. De Carvalho DD, You JS, Jones PA. DNA methylation and cellular reprogramming. Trends Cell Biol 2010;20(10):609–617. DOI: 10.1016/J.TCB.2010.08.003.
  25. Cain JA, Montibus B, Oakey RJ. Intragenic CpG islands and their impact on gene regulation. Front Cell Dev Biol 2022;10:832348. DOI: 10.3389/FCELL.2022.832348.
  26. Deaton AM, Bird A. CpG islands and the regulation of transcription. Genes Dev 2011;25(10):1010. DOI: 10.1101/GAD.2037511.
  27. Core LJ, Waterfall JJ, Lis JT. Nascent RNA sequencing reveals widespread pausing and divergent initiation at human promoters. Science 2008;322(5909):1845–1848. DOI: 10.1126/SCIENCE.1162228.
  28. Golbabapour S, Majid NA, Hassandarvish P, et al. Gene silencing and polycomb group proteins: An overview of their structure, mechanisms and phylogenetics. OMICS 2013;17(6):283. DOI: 10.1089/OMI.2012.0105.
  29. Jones PA, Takai D. The role of DNA methylation in mammalian epigenetics. Science 2001;293(5532):1068–1070. DOI: 10.1126/SCIENCE.1063852.
  30. Ng HH, Zhang Y, Hendrich B, et al. MBD2 is a transcriptional repressor belonging to the MeCP1 histone deacetylase complex. Nat Genet 1999;23(1):58–61. DOI: 10.1038/12659.
  31. Nan X, Ng HH, Johnson CA, et al. Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 1998;393(6683):386–389. DOI: 10.1038/30764.
  32. Citterio E, Papait R, Nicassio F, et al. Np95 is a histone-binding protein endowed with ubiquitin ligase activity. Mol Cell Biol 2004;24(6):2526. DOI: 10.1128/MCB.24.6.2526-2535.2004.
  33. Li J, Liu C. Coding or non-coding, the converging concepts of RNAs. Front Genet 2019;10:496. DOI: 10.3389/FGENE.2019.00496.
  34. Holoch D, Moazed D. RNA-mediated epigenetic regulation of gene expression. Nat Rev Genet 2015;16(2):71–84. DOI: 10.1038/NRG3863.
  35. Kaikkonen MU, Lam MTY, Glass CK. Editor's choice: Non-coding RNAs as regulators of gene expression and epigenetics. Cardiovasc Res 2011;90(3):430. DOI: 10.1093/CVR/CVR097.
  36. Ponting CP, Oliver PL, Reik W. Evolution and functions of long non-coding RNAs. Cell 2009;136(4):629–641. DOI: 10.1016/J.CELL.2009.02.006.
  37. Li Y. Modern epigenetics methods in biological research. Methods 2021;187:104–113. DOI: 10.1016/J.YMETH.2020.06.022.
  38. Carthew RW, Sontheimer EJ. Origins and mechanisms of miRNAs and siRNAs. Cell 2009;136(4):642–655. DOI: 10.1016/J.CELL.2009.01.035.
  39. Wilson RC, Doudna JA. Molecular mechanisms of RNA interference. Annu Rev Biophys 2013;42(1):217–239. DOI: 10.1146/ANNUREV-BIOPHYS-083012-130404.
  40. Amaral PP, Mattick JS. Non-coding RNA in development. Mamm Genome 2008;19(7–8):454–492. DOI: 10.1007/S00335-008-9136-7.
  41. Krol J, Loedige I, Filipowicz W. The widespread regulation of microRNA biogenesis, function and decay. Nat Rev Genet 2010;11(9):597–610. DOI: 10.1038/NRG2843.
  42. Bernstein E, Caudy AA, Hammond SM, et al. Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 2001;409(6818):363–366. DOI: 10.1038/35053110.
  43. Lee Y, Ahn C, Han J, et al. The nuclear RNase III Drosha initiates microRNA processing. Nature 2003;425(6956):415–419. DOI: 10.1038/NATURE01957.
  44. Hutvágner G, Zamore PD. A microRNA in a multiple-turnover RNAi enzyme complex. Science 2002;297(5589):2056–2060. DOI: 10.1126/SCIENCE.1073827.
  45. Mourelatos Z, Dostie J, Paushkin S, et al. miRNPs: a novel class of ribonucleoproteins containing numerous microRNAs. Genes Dev 2002;16(6):720. DOI: 10.1101/GAD.974702.
  46. Bracken CP, Scott HS, Goodall GJ. A network-biology perspective of microRNA function and dysfunction in cancer. Nat Rev Genet 2016;17(12):719–732. DOI: 10.1038/NRG.2016.134.
  47. Grewal SIS. RNAi-dependent formation of heterochromatin and its diverse functions. Curr Opin Genet Dev 2010;20(2):134. DOI: 10.1016/J.GDE.2010.02.003.
  48. Siomi H, Siomi MC. On the road to reading the RNA-interference code. Nature 2009;457(7228):396–404. DOI: 10.1038/NATURE07754.
  49. Siomi MC, Sato K, Pezic D, et al. PIWI-interacting small RNAs: The vanguard of genome defence. Nat Rev Mol Cell Biol 2011;12(4): 246–258. DOI: 10.1038/NRM3089.
  50. Pasquinelli AE. MicroRNAs and their targets: Recognition, regulation and an emerging reciprocal relationship. Nat Rev Genet 2012;13(4):271–282. DOI: 10.1038/NRG3162.
  51. Gunawardane LS, Saito K, Nishida KM, et al. A slicer-mediated mechanism for repeat-associated siRNA 5’ end formation in Drosophila. Science 2007;315(5818):1587–1590. DOI: 10.1126/SCIENCE.1140494.
  52. Li C, Vagin VV, Lee S, et al. Collapse of germline piRNAs in the absence of Argonaute3 reveals somatic piRNAs in flies. Cell 2009;137(3): 509–521. DOI: 10.1016/J.CELL.2009.04.027.
  53. Malone CD, Brennecke J, Dus M, et al. Specialized piRNA pathways act in germline and somatic tissues of the Drosophila ovary. Cell 2009;137(3):522–535. DOI: 10.1016/J.CELL.2009.03.040.
  54. Wu Q, Ma Q, Shehadeh LA, et al. Expression of the Argonaute protein PiwiL2 and piRNAs in adult mouse mesenchymal stem cells. Biochem Biophys Res Commun 2010;396(4):915–920. DOI: 10.1016/J.BBRC.2010.05.022.
  55. Khalil AM, Guttman M, Huarte M, et al. Many human large intergenic non-coding RNAs associate with chromatin-modifying complexes and affect gene expression. Proc Natl Acad Sci USA 2009;106(28):11667–11672. DOI: 10.1073/PNAS.0904715106.
  56. Guttman M, Amit I, Garber M, et al. Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature 2009;458(7235):223–227. DOI: 10.1038/NATURE07672.
  57. Long Y, Wang X, Youmans DT, et al. How do lncRNAs regulate transcription? Sci Adv 2017;3(9):eaao2110. DOI: 10.1126/SCIADV.AAO2110.
  58. Xu X feng, Du L zhong. Epigenetics in neonatal diseases. Chin Med J (Engl) 2010;123(20):2948–2954. PMID: 21034612.
  59. Arima T, Drewell RA, Arney KL, et al. A conserved imprinting control region at the HYMAI/ZAC domain is implicated in transient neonatal diabetes mellitus. Hum Mol Genet 2001;10(14):1475–1483. DOI: 10.1093/HMG/10.14.1475.
  60. Cosgrove MS, Boeke JD, Wolberger C. Regulated nucleosome mobility and the histone code. Nat Struct Mol Biol 2004;11(11):1037–1043. DOI: 10.1038/NSMB851.
  61. Bowman GD, Poirier MG. Post-translational modifications of histones that influence nucleosome dynamics. Chem Rev 2015;115(6): 2274–2295. DOI: 10.1021/CR500350X.
  62. Mitrousis N, Tropepe V, Hermanson O. Post-translational modifications of histones in vertebrate neurogenesis. Front Neurosci 2015;9:483. DOI: 10.3389/FNINS.2015.00483.
  63. De Ruijter AJM, Van Gennip AH, Caron HN, et al. Histone deacetylases (HDACs): Characterization of the classical HDAC family. Biochem J 2003;370(Pt 3):737–749. DOI: 10.1042/BJ20021321.
  64. Turner BM. Cellular memory and the histone code. Cell 2002;111(3): 285–291. DOI: 10.1016/S0092-8674(02)01080-2.
  65. Lu Q, Qiu X, Hu N, et al. Epigenetics, disease, and therapeutic interventions. Ageing Res Rev 2006;5(4):449–467. DOI: 10.1016/J.ARR.2006.07.001.
  66. Grant PA, Berger SL. Histone acetyltransferase complexes. Semin Cell Dev Biol 1999;10(2):169–177. DOI: 10.1006/SCDB.1999.0298.
  67. Sims RJ, Nishioka K, Reinberg D. Histone lysine methylation: A signature for chromatin function. Trends Genet 2003;19(11):629–639. DOI: 10.1016/J.TIG.2003.09.007.
  68. Tamaru H, Selker EU. A histone H3 methyltransferase controls DNA methylation in Neurospora crassa. Nature 2001;414(6861):277–283. DOI: 10.1038/35104508.
  69. Henckel A, Nakabayashi K, Sanz LA, et al. Histone methylation is mechanistically linked to DNA methylation at imprinting control regions in mammals. Hum Mol Genet 2009;18(18):3375–3383. DOI: 10.1093/HMG/DDP277.
  70. Polin RA, Abman SH, Rowitch DH, et al. Fetal and Neonatal Physiology, 2-Volume Set. Published online January 1, 2017; pp: 1–1744.e3. DOI: 10.1016/B978-0-323-35214-7.00175-X.
  71. Korzus E. Rubinstein-Taybi syndrome and epigenetic alterations. Adv Exp Med Biol 2017;978:39–62. DOI: 10.1007/978-3-319-53889-1_3.
  72. Felsenfeld G, Groudine M. Controlling the double helix. Nature 2003;421(6921):448–453. DOI: 10.1038/NATURE01411.
  73. Levenson JM, Sweatt JD. Epigenetic mechanisms in memory formation. Nat Rev Neurosci 2005;6(2):108–118. DOI: 10.1038/NRN1604.
  74. Kouzarides T. Chromatin modifications and their function. Cell 2007;128(4):693–705. DOI: 10.1016/J.CELL.2007.02.005.
  75. Berger SL. Histone modifications in transcriptional regulation. Curr Opin Genet Dev 2002;12(2):142–148. DOI: 10.1016/S0959-437X(02)00279-4.
  76. Jiang C, Pugh BF. Nucleosome positioning and gene regulation: Advances through genomics. Nat Rev Genet 2009;10(3):161–172. DOI: 10.1038/NRG2522.
  77. Becker PB, Workman JL. Nucleosome remodeling and epigenetics. Cold Spring Harb Perspect Biol 2013;5(9):a017905. DOI: 10.1101/CSHPERSPECT.A017905.
  78. Workman JL, Kingston RE. Alteration of nucleosome structure as a mechanism of transcriptional regulation. Annu Rev Biochem 1998;67:545–579. DOI: 10.1146/ANNUREV.BIOCHEM.67.1.545.
  79. Hargreaves DC, Crabtree GR. ATP-dependent chromatin remodeling: Genetics, genomics and mechanisms. Cell Res 2011;21(3):396–420. DOI: 10.1038/CR.2011.32.
  80. Kingston RE, Narlikar GJ. ATP-dependent remodeling and acetylation as regulators of chromatin fluidity. Genes Dev 1999;13(18):2339–2352. DOI: 10.1101/GAD.13.18.2339.
  81. Clapier CR, Cairns BR. The biology of chromatin remodeling complexes. Annu Rev Biochem 2009;78:273–304. DOI: 10.1146/ANNUREV.BIOCHEM.77.062706.153223.
  82. Becker PB, Hörz W. ATP-dependent nucleosome remodeling. Annu Rev Biochem 2002;71:247–273. DOI: 10.1146/ANNUREV.BIOCHEM.71.110601.135400.
  83. Jansen A, Verstrepen KJ. Nucleosome positioning in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 2011;75(2):301. DOI: 10.1128/MMBR.00046-10.
  84. Djupedal I, Ekwall K. Epigenetics: Heterochromatin meets RNAi. Cell Res 2009;19(3):282–295. DOI: 10.1038/CR.2009.13.
  85. Zhang Y, Tycko B. Mono-allelic expression of the human H19 gene. Nat Genet 1992;1(1):40–44. DOI: 10.1038/NG0492-40.
  86. Giannoukakis N, Deal C, Paquette J, et al. Parental genomic imprinting of the human IGF2 gene. Nat Genet 1993;4(1):98–101. DOI: 10.1038/NG0593-98.
  87. MacDonald WA. Epigenetic mechanisms of genomic imprinting: Common themes in the regulation of imprinted regions in mammals, plants, and insects. Genet Res Int 2012;2012:1–17. DOI: 10.1155/2012/585024.
  88. Constância M, Dean W, Lopes S, et al. Deletion of a silencer element in Igf2 results in loss of imprinting independent of H19. Nat Genet 2000;26(2):203–206. DOI: 10.1038/79930.
  89. Murrell A, Heeson S, Bowden L, et al. An intragenic methylated region in the imprinted Igf2 gene augments transcription. EMBO Rep 2001;2(12):1101–1106. DOI: 10.1093/EMBO-REPORTS/KVE248.
  90. Bartolomei MS, Webber AL, Brunkow ME, et al. Epigenetic mechanisms underlying the imprinting of the mouse H19 gene. Genes Dev 1993;7(9):1663–1673. DOI: 10.1101/GAD.7.9.1663.
  91. Arney KL. H19 and Igf2--enhancing the confusion? Trends Genet 2003;19(1):17–23. DOI: 10.1016/S0168-9525(02)00004-5.
  92. Suetake I, Shinozaki F, Miyagawa J, et al. DNMT3L stimulates the DNA methylation activity of Dnmt3a and Dnmt3b through a direct interaction. J Biol Chem 2004;279(26):27816–27823. DOI: 10.1074/JBC.M400181200.
  93. Kaneda M, Okano M, Hata K, et al. Essential role for de novo DNA methyltransferase Dnmt3a in paternal and maternal imprinting. Nature 2004;429(6994):900–903. DOI: 10.1038/NATURE02633.
  94. Hirasawa R, Chiba H, Kaneda M, et al. Maternal and zygotic Dnmt1 are necessary and sufficient for the maintenance of DNA methylation imprints during preimplantation development. Genes Dev 2008;22(12):1607–1616. DOI: 10.1101/GAD.1667008.
  95. Tucker KL, Beard C, Dausman J, et al. Germline passage is required for establishment of methylation and expression patterns of imprinted but not of nonimprinted genes. Genes Dev 1996;10(8):1008–1020. DOI: 10.1101/GAD.10.8.1008.
  96. Halabian R, Valizadeh Arshad, Ahmadi A, et al. Laboratory methods to decipher epigenetic signatures: A comparative review. Cell Mol Biol Lett 2021;26(1):46. DOI: 10.1186/S11658-021-00290-9.
  97. Sulewska A, Niklinska W, Kozlowski M, et al. Detection of DNA methylation in eucaryotic cells. Folia Histochem Cytobiol 2007;45(4):315–324. PMID: 18165169.
  98. Wu H, Tao J, Sun YE. Regulation and function of mammalian DNA methylation patterns: A genomic perspective. Brief Funct Genomics 2012;11(3):240–250. DOI: 10.1093/BFGP/ELS011.
  99. Pajares MJ, Palanca-Ballester C, Urtasun R, et al. Methods for analysis of specific DNA methylation status. Methods 2021;187:3–12. DOI: 10.1016/J.YMETH.2020.06.021.
  100. Collas P. The current state of chromatin immunoprecipitation. Mol Biotechnol 2010;45(1):87–100. DOI: 10.1007/S12033-009-9239-8.
  101. Gade P, Kalvakolanu DV. Chromatin immunoprecipitation assay as a tool for analyzing transcription factor activity. Methods Mol Biol 2012;809:85–104. DOI: 10.1007/978-1-61779-376-9_6.
  102. Pillai S, Chellappan SP. ChIP on chip assays: Genome-wide analysis of transcription factor binding and histone modifications. Methods Mol Biol 2009;523:341–366. DOI: 10.1007/978-1-59745-190-1_23.
  103. Furey TS. ChIP-seq and beyond: New and improved methodologies to detect and characterize protein–DNA interactions. Nat Rev Genet 2012;13(12):840–852. DOI: 10.1038/NRG3306.
  104. Fatmi A, Chabni N, Cernada M, et al. Clinical and immunological aspects of microRNAs in neonatal sepsis. Biomed Pharmacother 2022;145:112444. DOI: 10.1016/J.BIOPHA.2021.112444.
  105. Kubota T. Epigenetics in congenital diseases and pervasive developmental disorders. Environ Health Prev Med 2008;13(1):3. DOI: 10.1007/S12199-007-0008-7.
  106. Kubota T, Das S, Christian SL, et al. Methylation-specific PCR simplifies imprinting analysis. Nat Genet 1997;16(1):15. DOI: 10.1038/NG0597-15.
  107. Nicholls RD, Saitoh S, Horsthemke B. Imprinting in Prader-Willi and Angelman syndromes. Trends Genet 1998;14(5):194–200. DOI: 10.1016/S0168-9525(98)01432-2.
  108. Simeoni U, Yzydorczyk C, Siddeek B, et al. Epigenetics and neonatal nutrition. Early Hum Dev 2014;90 Suppl 2:S23–S24. DOI: 10.1016/S0378-3782(14)50007-2.
  109. Arai Y, Ohgane J, Yagi S, et al. Epigenetic assessment of environmental chemicals detected in maternal peripheral and cord blood samples. J Reprod Dev 2011;57(4):507–517. DOI: 10.1262/JRD.11-034A.
  110. Joubert BR, Den Dekker HT, Felix JF, et al. Maternal plasma folate impacts differential DNA methylation in an epigenome-wide meta-analysis of newborns. Nat Commun 2016;7:10577. DOI: 10.1038/NCOMMS10577.
  111. Joubert BR, Felix JF, Yousefi P, et al. DNA methylation in newborns and maternal smoking in pregnancy: Genome-wide consortium meta-analysis. Am J Hum Genet 2016;98(4):680–696. DOI: 10.1016/J.AJHG.2016.02.019.
  112. Gruzieva O, Xu CJ, Breton C V, et al. Epigenome-wide meta-analysis of methylation in children related to prenatal NO2 air pollution exposure. Environ Health Perspect 2017;125(1):104–110. DOI: 10.1289/EHP36.
  113. Cardenas A, Rifas-Shiman SL, Godderis L, et al. Prenatal exposure to mercury: Associations with global DNA methylation and hydroxymethylation in cord blood and in childhood. Environ Health Perspect 2017;125(8):087022. DOI: 10.1289/EHP1467.
  114. Wang J, Luo X, Pan J, et al. (Epi)genetic variants of the sarcomere-desmosome are associated with premature utero-contraction in spontaneous preterm labor. Environ Int 2021;148:106382. DOI: 10.1016/J.ENVINT.2021.106382.
  115. Lancaster EE, Lapato DM, Jackson-Cook C, et al. Maternal biological age assessed in early pregnancy is associated with gestational age at birth. Sci Rep 2021;11(1):15440. DOI: 10.1038/S41598-021-94281-7.
  116. Cutfield WS, Hofman PL, Mitchell M, et al. Could epigenetics play a role in the developmental origins of health and disease? Pediatr Res 2007;61(5 Pt 2):68–75. DOI: 10.1203/PDR.0B013E318045764C.
  117. Mitchell MD. Unique suppression of prostaglandin H synthase-2 expression by inhibition of histone deacetylation, specifically in human amnion but not adjacent choriodecidua. Mol Biol Cell 2006;17(1):549. DOI: 10.1091/MBC.E05-08-0818.
  118. Rahnama F, Shafiei F, Gluckman PD, et al. Epigenetic regulation of human trophoblastic cell migration and invasion. Endocrinology 2006;147(11):5275–5283. DOI: 10.1210/EN.2006-0288.
  119. McCann JA, Yong QX, Frechette R, et al. The insulin-like growth factor-II receptor gene is associated with type 1 diabetes: Evidence of a maternal effect. J Clin Endocrinol Metab 2004;89(11):5700–5706. DOI: 10.1210/JC.2004-0553.
  120. Braidotti G, Baubec T, Pauler F, et al. The Air non-coding RNA: An imprinted cis-silencing transcript. Cold Spring Harb Symp Quant Biol 2004;69:55–66. DOI: 10.1101/SQB.2004.69.55.
  121. Itier JM, Tremp GL, Léonard JF, et al. Imprinted gene in postnatal growth role. Nature 1998;393(6681):125–126. DOI: 10.1038/30120.
  122. Miyoshi N, Kuroiwa Y, Kohda T, et al. Identification of the Meg1/Grb10 imprinted gene on mouse proximal chromosome 11, a candidate for the Silver-Russell syndrome gene. Proc Natl Acad Sci USA 1998;95(3):1102–1107. DOI: 10.1073/PNAS.95.3.1102.
  123. Samra H, McGrath JM, Wehbe M, et al. Epigenetics and family-centered developmental care for the preterm infant. Adv Neonatal Care 2012;12 Suppl 5:S2–S9. DOI: 10.1097/ANC.0B013E318265B4BD.
  124. Chromatin. Accessed May 19, 2024. Available from: https://www.genome.gov/genetics-glossary/Chromatin.
  125. Cooper GM. Chromosomes and Chromatin. Published online 2000. Accessed May 19, 2024. Available from: https://www.ncbi.nlm.nih.gov/books/NBK9863/.
  126. Tamaru H. Confining euchromatin/heterochromatin territory: Jumonji crosses the line. Genes Dev 2010;24(14):1465. DOI: 10.1101/GAD.1941010.
  127. Cutter AR, Hayes JJ. A brief review of nucleosome structure. FEBS Lett 2015;589(20 0 0):2914. DOI: 10.1016/J.FEBSLET.2015.05.016.
  128. Padda IS, Mahtani AU, Parmar M. Small Interfering RNA (siRNA) Therapy. StatPearls. Published online June 3, 2023. Accessed May 14, 2024. Available from: https://www.ncbi.nlm.nih.gov/books/NBK580472/.
  129. Ardekani AM, Naeini MM. The role of microRNAs in human diseases. Avicenna J Med Biotechnol 2010;2(4):161. Accessed May 14, 2024. PMCID: 3558168.
  130. Kung JTY, Colognori D, Lee JT. Long noncoding RNAs: Past, present, and future. Genetics 2013;193(3):651. DOI: 10.1534/GENETICS.112.146704.
  131. Barlow DP, Bartolomei MS. Genomic imprinting in mammals. Cold Spring Harb Perspect Biol 2014;6(2):a018382. DOI: 10.1101/CSHPERSPECT.A018382.
  132. Wiehle L, Breiling A. Chromatin immunoprecipitation. Methods Mol Biol 2016;1480:7–21. DOI: 10.1007/978-1-4939-6380-5_2.
  133. Lacagnina S. The developmental origins of health and disease (DOHaD). Am J Lifestyle Med 2020;14(1):47. DOI: 10.1177/1559827619 879694.
  134. Campagna MP, Xavier A, Lechner-Scott J, et al. Epigenome-wide association studies: Current knowledge, strategies and recommendations. Clin Epigenetics 2021;13(1):1–24. DOI: 10.1186/S13148-021-01200-8/FIGURES/12.
  135. Flanagan JM. Epigenome-wide association studies (EWAS): Past, present, and future. Methods Mol Biol 2015;1238:51–63. DOI: 10.1007/978-1-4939-1804-1_3.
PDF Share
PDF Share

© Jaypee Brothers Medical Publishers (P) LTD.