Epigenetic signaling and crosstalk in regulation of gene expression and disease progression

Papers of special note have been highlighted as: • of interest; •• of considerable interest

References

• 1. Verdone L, Caserta M, Di Mauro E. Role of histone acetylation in the control of gene expression. Biochem. Cell Biol. 83(3), 344–353 (2005).
  Medline CASGoogle Scholar
• 2. Patra SK, Deb M, Patra A. Molecular marks for epigenetic identification of developmental and cancer stem cells. Clin. Epigenetics 2(1), 27–53 (2011).
  Medline CASGoogle Scholar
• 3. Kar S, Parbin S, Deb M et al. Epigenetic choreography of stem cells: the DNA demethylation episode of development. Cell. Mol. Life Sci. 71(6), 1017–1032 (2014).
  Medline CASGoogle Scholar
• 4. Parbin S, Kar S, Shilpi A et al. Histone deacetylases: a saga of perturbed acetylation homeostasis in cancer. J. Histochem. Cytochem. 62(1), 11–33 (2014).
  MedlineGoogle Scholar
• 5. Loury R, Sassone-Corsi P. Histone phosphorylation: how to proceed. Methods 31(1), 40–48 (2003).
  Medline CASGoogle Scholar
• 6. Ryu HY, Hochstrasser M. Histone sumoylation and chromatin dynamics. Nucleic Acids Res. 49(11), 6043–6052 (2021).
  Medline CASGoogle Scholar
• 7. Chen JJ, Stermer D, Tanny JC. Decoding histone ubiquitylation. Front Cell Dev Biol. 10, 968398 (2022).
  MedlineGoogle Scholar
• 8. Deb M, Kar S, Sengupta D et al. Chromatin dynamics: H3K4 methylation and H3 variant replacement during development and in cancer. Cell. Mol. Life Sci. 71(18), 3439–3463 (2014).
  Medline CASGoogle Scholar
• 9. Hsieh TF, Fischer RL. Biology of chromatin dynamics. Annu. Rev. Plant Biol. 56, 327–351 (2005).
  Medline CASGoogle Scholar
• 10. Roy A, Niharika, Chakraborty S, Mishra J, Singh SP, Patra SK. Mechanistic aspects of reversible methylation modifications of arginine and lysine of nuclear histones and their roles in human colon cancer. Prog. Mol. Biol. Transl. Sci. 197, 261–302 (2023).
  MedlineGoogle Scholar
• 11. Santos-Rosa H, Schneider R, Bannister AJ et al. Active genes are tri-methylated at K4 of histone H3. Nature 419(6905), 407–411 (2002). •• One of the premier publications about H3K4 methylation status in active genes.
  Medline CASGoogle Scholar
• 12. Sasidharan Nair V, El Salhat H, Taha RZ, John A, Ali BR, Elkord E. DNA methylation and repressive H3K9 and H3K27 trimethylation in the promoter regions of PD-1, CTLA-4, TIM-3, LAG-3, TIGIT, and PD-L1 genes in human primary breast cancer. Clin. Epigenetics 10, 78 (2018).
  MedlineGoogle Scholar
• 13. Vaissière T, Sawan C, Herceg Z. Epigenetic interplay between histone modifications and DNA methylation in gene silencing. Mutat. Res. 659(1–2), 40–48 (2008).
  Medline CASGoogle Scholar
• 14. Foster BM, Stolz P, Mulholland CB et al. Critical role of the UBL domain in stimulating the E3 ubiquitin ligase activity of UHRF1 toward chromatin. Mol. Cell 72(4), 739–752.e9 (2018). • First described how RING E3 ubiquitin ligase UHRF1 controls methylation of newly replicated DNA.
  Medline CASGoogle Scholar
• 15. Rothbart SB, Krajewski K, Nady N et al. Association of UHRF1 with methylated H3K9 directs the maintenance of DNA methylation. Nat. Struct. Mol. Biol. 19(11), 1155–1160 (2012).
  Medline CASGoogle Scholar
• 16. Otani J, Nankumo T, Arita K, Inamoto S, Ariyoshi M, Shirakawa M. Structural basis for recognition of H3K4 methylation status by the DNA methyltransferase 3A ATRX-DNMT3-DNMT3L domain. EMBO Rep. 10(11), 1235–1241 (2009).
  Medline CASGoogle Scholar
• 17. Hashimoto H, Vertino PM, Cheng X. Molecular coupling of DNA methylation and histone methylation. Epigenomics 2(5), 657–669 (2010).
  CASGoogle Scholar
• 18. Morselli M, Pastor WA, Montanini B et al. In vivo targeting of de novo DNA methylation by histone modifications in yeast and mouse. Elife 4, e06205 (2015).
  MedlineGoogle Scholar
• 19. Stewart KR, Veselovska L, Kim J et al. Dynamic changes in histone modifications precede de novo DNA methylation in oocytes. Genes Dev. 29(23), 2449–2462 (2015). •• Defined how histone modifications can configure the DNA methylation pattern.
  Medline CASGoogle Scholar
• 20. Salhab A, Nordström K, Gasparoni G et al. A comprehensive analysis of 195 DNA methylomes reveals shared and cell-specific features of partially methylated domains. Genome Biol. 19(1), 150 (2018).
  MedlineGoogle Scholar
• 21. Smallwood A, Estève PO, Pradhan S, Carey M. Functional cooperation between HP1 and DNMT1 mediates gene silencing. Genes Dev. 21(10), 1169–1178 (2007).
  Medline CASGoogle Scholar
• 22. Liyanage VR, Jarmasz JS, Murugeshan N, Del Bigio MR, Rastegar M, Davie JR. DNA modifications: function and applications in normal and disease states. Biology (Basel) 3(4), 670–723 (2014).
  Medline CASGoogle Scholar
• 23. Menafra R, Stunnenberg HG. MBD2 and MBD3: elusive functions and mechanisms. Front. Genet. 5, 428 (2014).
  MedlineGoogle Scholar
• 24. Lempiäinen JK, Garcia BA. Characterizing crosstalk in epigenetic signaling to understand disease physiology. Biochem. J. 480(1), 57–85 (2023).
  Medline CASGoogle Scholar
• 25. Laugesen A, Højfeldt JW, Helin K. Molecular mechanisms directing PRC2 recruitment and H3K27 methylation. Mol. Cell 74(1), 8–18 (2019).
  Medline CASGoogle Scholar
• 26. Zhang T, Cooper S, Brockdorff N. The interplay of histone modifications – writers that read. EMBO Rep. 16(11), 1467–1481 (2015).
  Medline CASGoogle Scholar
• 27. Molina-Serrano D, Schiza V, Kirmizis A. Crosstalk among epigenetic modifications: lessons from histone arginine methylation. Biochem. Soc. Trans. 41(3), 751–759 (2013).
  Medline CASGoogle Scholar
• 28. Sugeedha J, Gautam J, Tyagi S. SET1/MLL family of proteins: functions beyond histone methylation. Epigenetics. 16(5), 469–487 (2021).
  MedlineGoogle Scholar
• 29. Wu L, Lee SY, Zhou B et al. ASH2L regulates ubiquitylation signaling to MLL: trans-regulation of H3 K4 methylation in higher eukaryotes. Mol Cell. 49(6), 1108–1120 (2013).
  Medline CASGoogle Scholar
• 30. Bian C, Xu C, Ruan J et al. Sgf29 binds histone H3K4me2/3 and is required for SAGA complex recruitment and histone H3 acetylation. EMBO J. 30(14), 2829–2842 (2011).
  Medline CASGoogle Scholar
• 31. Wu F, Li X, Looso M et al. Spurious transcription causing innate immune responses is prevented by 5-hydroxymethylcytosine. Nat Genet. 55(1), 100–111 (2023).
  Medline CASGoogle Scholar
• 32. Zhao W, Xu Y, Wang Y et al. Investigating crosstalk between H3K27 acetylation and H3K4 trimethylation in CRISPR/dCas-based epigenome editing and gene activation. Sci. Rep. 11(1), 15912 (2021). • Demonstrated that H3K27ac in the promoter region leads to H3K4me3 enrichment around transcription start sites and activates gene expression.
  Medline CASGoogle Scholar
• 33. Fischle W. Talk is cheap – cross-talk in establishment, maintenance, and readout of chromatin modifications. Genes Dev. 22(24), 3375–3382 (2008).
  Medline CASGoogle Scholar
• 34. Lee JS, Smith E, Shilatifard A. The language of histone crosstalk. Cell 42(5), 682–685 (2010). •• Histone modifications are more like a language than a code in chromatin signaling pathways.
  Google Scholar
• 35. Taubert S, Gorrini C, Frank SR et al. E2F-dependent histone acetylation and recruitment of the Tip60 acetyltransferase complex to chromatin in late G1. Mol Cell Biol. 24(10), 4546–4556 (2004).
  Medline CASGoogle Scholar
• 36. Li X. Epigenetics and cell cycle regulation in cystogenesis. Cell. Signal. 68, 109509 (2020).
  Medline CASGoogle Scholar
• 37. Ma Y, Kanakousaki K, Buttitta L. How the cell cycle impacts chromatin architecture and influences cell fate. Front. Genet. 6, 19 (2015).
  MedlineGoogle Scholar
• 38. Bou Kheir T, Lund AH. Epigenetic dynamics across the cell cycle. Essays Biochem. 48(1), 107–120 (2010).
  MedlineGoogle Scholar
• 39. Loyola A, Tagami H, Bonaldi T et al. The HP1alpha-CAF1-SetDB1-containing complex provides H3K9me1 for Suv39-mediated K9me3 in pericentric heterochromatin. EMBO Rep. 10(7), 769–775 (2009).
  Medline CASGoogle Scholar
• 40. Torrisani J, Unterberger A, Tendulkar SR, Shikimi K, Szyf M. AUF1 cell cycle variations define genomic DNA methylation by regulation of DNMT1 mRNA stability. Molecular and cellular biology 27(1), 395–410 (2007).
  Medline CASGoogle Scholar
• 41. Mancini M, Magnani E, Macchi F, Bonapace IM. The multi-functionality of UHRF1: epigenome maintenance and preservation of genome integrity. Nucleic Acids Res. 49(11), 6053–6068 (2021).
  Medline CASGoogle Scholar
• 42. Budhavarapu VN, Chavez M, Tyler JK. How is epigenetic information maintained through DNA replication? Epigenetics Chromatin 6(1), 32 (2013).
  Medline CASGoogle Scholar
• 43. Probst AV, Dunleavy E, Almouzni G. Epigenetic inheritance during the cell cycle. Nat. Rev. Mol. Cell Biol. 10(3), 192–206 (2009).
  Medline CASGoogle Scholar
• 44. Allis CD, Jenuwein T, Reinberg D. Epigenetics- Overview and concepts. Epigenetics. Allis CDJenuwein TReinberg D (Eds). Epigenetics Cold Spring Harbor Laboratory Press, 1, 23–61 (2007).
  Google Scholar
• 45. Wang J, Jia ST, Jia S. New insights into the regulation of heterochromatin. Trends Genet. 32(5), 284–294 (2016).
  MedlineGoogle Scholar
• 46. Cutter DiPiazza AR, Taneja N, Dhakshnamoorthy J, Wheeler D, Holla S, Grewal SIS. Spreading and epigenetic inheritance of heterochromatin require a critical density of histone H3 lysine 9 tri-methylation. Proc. Natl Acad. Sci. USA 118(22), e2100699118 (2021).
  MedlineGoogle Scholar
• 47. Soni DK, Biswas R. Role of non-coding RNAs in post-transcriptional regulation of lung diseases. Front. Genet. 12, 767348 (2021).
  MedlineGoogle Scholar
• 48. Kaikkonen MU, Lam MT, Glass CK. Non-coding RNAs as regulators of gene expression and epigenetics. Cardiovasc. Res. 90(3), 430–440 (2011).
  Medline CASGoogle Scholar
• 49. Butler AA, Webb WM, Lubin FD. Regulatory RNAs and control of epigenetic mechanisms: expectations for cognition and cognitive dysfunction. Epigenomics 8(1), 135–151 (2016).
  CASGoogle Scholar
• 50. Krol J, Loedige I, Filipowicz W. The widespread regulation of microRNA biogenesis, function and decay. Nat. Rev. Genet. 11(9), 597–610 (2010).
  Medline CASGoogle Scholar
• 51. Ha M, Kim VN. Regulation of microRNA biogenesis. Nat. Rev. Mol. Cell Biol. 15(8), 509–524 (2014).
  Medline CASGoogle Scholar
• 52. Sengupta D, Deb M, Kar S et al. Dissecting miRNA facilitated physiology and function in human breast cancer for therapeutic intervention. Semin. Cancer Biol. 72, 46–64 (2021). •• A landmark review which highlights recent advances in miRNA function.
  Medline CASGoogle Scholar
• 53. Saviana M, Le P, Micalo L et al. Crosstalk between miRNAs and DNA methylation in cancer. Genes 14(5), 1075 (2023).
  Medline CASGoogle Scholar
• 54. Yao Q, Chen Y, Zhou X. The roles of microRNAs in epigenetic regulation. Curr. Opin. Chem. Biol. 51, 11–17 (2019).
  Medline CASGoogle Scholar
• 55. Hillyar CR, Kanabar SS, Rallis KS, Varghese JS. Complex cross-talk between EZH2 and miRNAs confers hallmark characteristics and shapes the tumor microenvironment. Epigenomics 14(11), 699–709 (2022).
  CASGoogle Scholar
• 56. Liu X, Chen X, Yu X et al. Regulation of microRNAs by epigenetics and their interplay involved in cancer. J. Exp. Clin. Cancer Res. 32(1), 96 (2013).
  MedlineGoogle Scholar
• 57. Siomi H, Siomi MC. On the road to reading the RNA-interference code. Nature 457(7228), 396–404 (2009).
  Medline CASGoogle Scholar
• 58. Brennecke J, Aravin AA, Stark A et al. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 128(6), 1089–1103 (2007).
  Medline CASGoogle Scholar
• 59. Gunawardane LS, Saito K, Nishida KM et al. A slicer-mediated mechanism for repeat-associated siRNA 5′ end formation in Drosophila. Science 315(5818), 1587–1590 (2007).
  Medline CASGoogle Scholar
• 60. Zhang Q, Zhu Y, Cao X et al. The epigenetic regulatory mechanism of PIWI/piRNAs in human cancers. Mol Cancer. 22(1), 45 (2023).
  MedlineGoogle Scholar
• 61. Dong J, Wang X, Cao C et al. UHRF1 suppresses retrotransposons and cooperates with PRMT5 and PIWI proteins in male germ cells. Nat. Commun. 10(1), 4705 (2019).
  Medline CASGoogle Scholar
• 62. Pezic D, Manakov SA, Sachidanandam R, Aravin AA. piRNA pathway targets active LINE1 elements to establish the repressive H3K9me3 mark in germ cells. Genes Dev. 28(13), 1410–1428 (2014).
  Medline CASGoogle Scholar
• 63. Birmingham A, Anderson EM, Reynolds A et al. 3′ UTR seed matches, but not overall identity, are associated with RNAi off-targets [published correction appears in Nat. Methods 2007 Jun; 4(6): 533]. Nat. Methods 3(3), 199–204 (2006).
  Medline CASGoogle Scholar
• 64. Dueva R, Akopyan K, Pederiva C et al. Neutralization of the positive charges on histone tails by RNA promotes an open chromatin structure. Cell Chem. Biol. 26(10), 1436–1449.e5 (2019).
  Medline CASGoogle Scholar
• 65. Yap KL, Li S, Muñoz-Cabello AM et al. Molecular interplay of the noncoding RNA ANRIL and methylated histone H3 lysine 27 by polycomb CBX7 in transcriptional silencing of INK4a. Mol. Cell 38(5), 662–674 (2010).
  Medline CASGoogle Scholar
• 66. Rosa S, Duncan S, Dean C. Mutually exclusive sense–antisense transcription at FLC facilitates environmentally induced gene repression. Nat. Commun. 7, 13031 (2016).
  Medline CASGoogle Scholar
• 67. Csorba T, Questa JI, Sun Q, Dean C. Antisense COOLAIR mediates the coordinated switching of chromatin states at FLC during vernalization. Proc. Natl Acad. Sci. USA 111(45), 16160–16165 (2014).
  Medline CASGoogle Scholar
• 68. Schmitz KM, Mayer C, Postepska A, Grummt I. Interaction of noncoding RNA with the rDNA promoter mediates recruitment of DNMT3b and silencing of rRNA genes. Genes Dev. 24(20), 2264–2269 (2010).
  Medline CASGoogle Scholar
• 69. Statello L, Guo CJ, Chen LL, Huarte M. Gene regulation by long non-coding RNAs and its biological functions. Nat. Rev. Mol. Cell Biol. 22(2), 96–118 (2021).
  Medline CASGoogle Scholar
• 70. Ohzeki J, Larionov V, Earnshaw WC, Masumoto H. De novo formation and epigenetic maintenance of centromere chromatin. Curr. Opin. Cell Biol. 58, 15–25 (2019).
  Medline CASGoogle Scholar
• 71. Allshire RC, Karpen GH. Epigenetic regulation of centromeric chromatin: old dogs, new tricks? Nat. Rev. Genet. 9(12), 923–937 (2008).
  Medline CASGoogle Scholar
• 72. Nagpal H, Fierz B. The elusive structure of centro-chromatin: molecular order or dynamic heterogenetity? J. Mol. Biol. 433(6), 166676 (2021).
  Medline CASGoogle Scholar
• 73. Bergmann JH, Martins NM, Larionov V, Masumoto H, Earnshaw WC. HACking the centromere chromatin code: insights from human artificial chromosomes. Chromosome Res. 20(5), 505–519 (2012).
  Medline CASGoogle Scholar
• 74. Allshire RC, Madhani HD. Ten principles of heterochromatin formation and function. Nat. Rev. Mol. Cell Biol. 19(4), 229–244 (2018).
  Medline CASGoogle Scholar
• 75. Richards EJ, Elgin SC. Epigenetic codes for heterochromatin formation and silencing: rounding up the usual suspects. Cell 108(4), 489–500 (2002). •• Histone hypoacetylation, histone H3K9 methylation and CpG methylation are three important epigenetic bases for spreading of heterochromatin for stable epigenetic inheritance of the silent state.
  Medline CASGoogle Scholar
• 76. Saksouk N, Simboeck E, Déjardin J. Constitutive heterochromatin formation and transcription in mammals. Epigenetics Chromatin 8, 3 (2015).
  Medline CASGoogle Scholar
• 77. Achrem M, Szućko I, Kalinka A. The epigenetic regulation of centromeres and telomeres in plants and animals. Comp. Cytogenet. 14(2), 265–311 (2020).
  MedlineGoogle Scholar
• 78. Black BE, Cleveland DW. Epigenetic centromere propagation and the nature of CENP-a nucleosomes. Cell 144(4), 471–479 (2011).
  Medline CASGoogle Scholar
• 79. Westhorpe FG, Straight AF. The centromere: epigenetic control of chromosome segregation during mitosis. Cold Spring Harb. Perspect. Biol. 7(1), a015818 (2014).
  MedlineGoogle Scholar
• 80. Ohzeki J, Bergmann JH, Kouprina N et al. Breaking the HAC barrier: histone H3K9 acetyl/methyl balance regulates CENP-A assembly. EMBO J. 31(10), 2391–2402 (2012). •• Demonstrated the role of H3K9 acetyl/methyl modifications in kinetochore assembly and maintenance.
  Medline CASGoogle Scholar
• 81. Carroll CW, Straight AF. Centromere formation: from epigenetics to self-assembly. Trends Cell Biol. 16(2), 70–78 (2006).
  Medline CASGoogle Scholar
• 82. Hoffmann S, Izquierdo HM, Gamba R et al. A genetic memory initiates the epigenetic loop necessary to preserve centromere position. EMBO J. 39(20), e105505 (2020). • Genetic memory governed by CENP proteins initiates the epigenetic modification necessary for centromere formation.
  Medline CASGoogle Scholar
• 83. Dvash T, Fan G. Epigenetics of X chromosome inactivation. Handbook of Epigenetics. Academic Press, 341–351 (2011).
  Google Scholar
• 84. Galupa R, Heard E. X-chromosome inactivation: a crossroads between chromosome architecture and gene regulation. Annu. Rev. Genet. 52, 535–566 (2018).
  Medline CASGoogle Scholar
• 85. Lu Z, Carter AC, Chang HY. Mechanistic insights in X-chromosome inactivation. Philos. Trans. R. Soc. Lond. B Biol. Sci. 372(1733), 20160356 (2017).
  MedlineGoogle Scholar
• 86. Fang H, Disteche CM, Berletch JB. X inactivation and escape: epigenetic and structural features. Front Cell Dev Biol. 7, 219 (2019).
  MedlineGoogle Scholar
• 87. Żylicz JJ, Bousard A, Žumer K et al. The implication of early chromatin changes in X chromosome inactivation. Cell 176(1–2), 182–197.e23 (2019).
  Medline CASGoogle Scholar
• 88. McHugh CA, Chen CK, Chow A et al. The Xist lncRNA interacts directly with SHARP to silence transcription through HDAC3. Nature 521(7551), 232–236 (2015).
  Medline CASGoogle Scholar
• 89. Kalantry S, Mills KC, Yee D, Otte AP, Panning B, Magnuson T. The Polycomb group protein Eed protects the inactive X-chromosome from differentiation-induced reactivation. Nat. Cell Biol. 8(2), 195–202 (2006). •• PRC complexes repress the inactive X chromosome from reactivation by stably silencing gene expression.
  Medline CASGoogle Scholar
• 90. Sarma K, Levasseur P, Aristarkhov A, Lee JT. Locked nucleic acids (LNAs) reveal sequence requirements and kinetics of Xist RNA localization to the X chromosome. Proc. Natl Acad. Sci. USA 107(51), 22196–22201 (2010).
  Medline CASGoogle Scholar
• 91. Pintacuda G, Wei G, Roustan C et al. hnRNPK Recruits PCGF3/5-PRC1 to the Xist RNA B-repeat to establish Polycomb-mediated chromosomal silencing. Mol. Cell 68(5), 955–969.e10 (2017).
  Medline CASGoogle Scholar
• 92. Jeon Y, Lee JT. YY1 tethers Xist RNA to the inactive X nucleation center. Cell 146(1), 119–133 (2011).
  Medline CASGoogle Scholar
• 93. Hasegawa Y, Brockdorff N, Kawano S, Tsutui K, Tsutui K, Nakagawa S. The matrix protein hnRNP U is required for chromosomal localization of Xist RNA. Dev. Cell. 19(3), 469–476 (2010).
  Medline CASGoogle Scholar
• 94. Gdula MR, Nesterova TB, Pintacuda G et al. The non-canonical SMC protein SmcHD1 antagonises TAD formation and compartmentalisation on the inactive X chromosome. Nat. Commun. 10(1), 30 (2019).
  Medline CASGoogle Scholar
• 95. Ryan VH, Dignon GL, Zerze GH et al. Mechanistic view of hnRNPA2 low-complexity domain structure, interactions, and phase separation altered by mutation and arginine methylation. Mol. Cell 69(3), 465–479.e7 (2018).
  Medline CASGoogle Scholar
• 96. Lange UC, Verdikt R, Ait-Ammar A, Van Lint C. Epigenetic crosstalk in chronic infection with HIV-1. Semin. Immunopathol. 42(2), 187–200 (2020).
  Medline CASGoogle Scholar
• 97. Hussain T, Saha D, Purohit G et al. Transcription regulation of CDKN1A (p21/CIP1/WAF1) by TRF2 is epigenetically controlled through the REST repressor complex. Sci. Rep. 7(1), 11541 (2017).
  MedlineGoogle Scholar
• 98. Xu J, Wang Z, Lu W et al. EZH2 promotes gastric cancer cells proliferation by repressing p21 expression. Pathol. Res. Pract. 215(6), 152374 (2019).
  Medline CASGoogle Scholar
• 99. Kang N, Eccleston M, Clermont PL et al. EZH2 inhibition: a promising strategy to prevent cancer immune editing. Epigenomics 12(16), 1457–1476 (2020).
  CASGoogle Scholar
• 100. Yang CC, LaBaff A, Wei Y et al. Phosphorylation of EZH2 at T416 by CDK2 contributes to the malignancy of triple negative breast cancers. Am. J. Transl. Res. 7(6), 1009–1020 (2015).
  MedlineGoogle Scholar
• 101. Nie L, Wei Y, Zhang F et al. CDK2-mediated site-specific phosphorylation of EZH2 drives and maintains triple-negative breast cancer [published correction appears in Nat. Commun. 2020 Jan 29; 11(1): 673]. Nat. Commun. 10(1), 5114 (2019).
  Medline CASGoogle Scholar
• 102. Sengupta D, Deb M, Rath SK et al. DNA methylation and not H3K4 trimethylation dictates the expression status of miR-152 gene which inhibits migration of breast cancer cells via DNMT1/CDH1 loop. Exp. Cell Res. 346(2), 176–187 (2016). •• A landmark article which described the epigenetic command of DNA methylation for gene silencing over H3K4me3, a strong histone mark for active genes.
  Medline CASGoogle Scholar
• 103. Matsumura Y, Nakaki R, Inagaki T et al. H3K4/H3K9me3 bivalent chromatin domains targeted by lineage-specific DNA methylation pauses adipocyte differentiation. Mol. Cell 60(4), 584–596 (2015).
  Medline CASGoogle Scholar
• 104. Liu X, Wang C, Liu W et al. Distinct features of H3K4me3 and H3K27me3 chromatin domains in pre-implantation embryos. Nature 537(7621), 558–562 (2016).
  Medline CASGoogle Scholar
• 105. Prickaerts P, Adriaens ME, Beucken TVD et al. Hypoxia increases genome-wide bivalent epigenetic marking by specific gain of H3K27me3. Epigenetics Chromatin 9, 46 (2016).
  MedlineGoogle Scholar
• 106. Pradhan N, Parbin S, Kar S et al. Epigenetic silencing of genes enhanced by collective role of reactive oxygen species and MAPK signaling downstream ERK/Snail axis: ectopic application of hydrogen peroxide repress CDH1 gene by enhanced DNA methyltransferase activity in human breast cancer. Biochim. Biophys. Acta Mol. Basis Dis. 1865(6), 1651–1665 (2019).
  Medline CASGoogle Scholar
• 107. Deb M, Sengupta D, Rath SK et al. Clusterin gene is predominantly regulated by histone modifications in human colon cancer and ectopic expression of the nuclear isoform induces cell death. Biochim. Biophys. Acta 1852(8), 1630–1645 (2015).
  Medline CASGoogle Scholar
• 108. Manna S, Kirtana R, Roy A, Baral T, Patra SK. Mechanisms of Hedgehog, calcium and retinoic acid signalling pathway inhibitors: plausible modes of action along the MLL–EZH2–p53 axis in cellular growth control. Arch. Biochem. Biophys. 742, 109600 (2023).
  Medline CASGoogle Scholar
• 109. Lima-Fernandes E, Murison A, da Silva Medina T et al. Targeting bivalency de-represses Indian Hedgehog and inhibits self-renewal of colorectal cancer-initiating cells. Nat. Commun. 10(1), 1436 (2019).
  MedlineGoogle Scholar
• 110. Al-Hasani K, Mathiyalagan P, El-Osta A. Epigenetics, cardiovascular disease, and cellular reprogramming. J. Mol. Cell. Cardiol. 128, 129–133 (2019).
  Medline CASGoogle Scholar
• 111. Shi Y, Zhang H, Huang S et al. Epigenetic regulation in cardiovascular disease: mechanisms and advances in clinical trials. Signal Transduct. Target. Ther. 7(1), 200 (2022).
  Medline CASGoogle Scholar
• 112. Williams SM, Golden-Mason L, Ferguson BS et al. Class I HDACs regulate angiotensin II-dependent cardiac fibrosis via fibroblasts and circulating fibrocytes. J. Mol. Cell. Cardiol. 67, 112–125 (2014).
  Medline CASGoogle Scholar
• 113. Lan C, Chen C, Qu S et al. Inhibition of DYRK1A, via histone modification, promotes cardiomyocyte cell cycle activation and cardiac repair after myocardial infarction. EBioMedicine 82, 104139 (2022).
  Medline CASGoogle Scholar
• 114. Jiang Y, Xiang C, Zhong F et al. Histone H3K27 methyltransferase EZH2 and demethylase JMJD3 regulate hepatic stellate cells activation and liver fibrosis. Theranostics 11(1), 361–378 (2021).
  Medline CASGoogle Scholar
• 115. Daneshpajooh M, Bacos K, Bysani M et al. HDAC7 is overexpressed in human diabetic islets and impairs insulin secretion in rat islets and clonal beta cells. Diabetologia 60(1), 116–125 (2017).
  Medline CASGoogle Scholar
• 116. Zullo A, Sommese L, Nicoletti G, Donatelli F, Mancini FP, Napoli C. Epigenetics and type 1 diabetes: mechanisms and translational applications. Transl. Res. 185, 85–93 (2017).
  Medline CASGoogle Scholar
• 117. Zhang X, Liu L, Yuan X, Wei Y, Wei X. JMJD3 in the regulation of human diseases. Protein Cell 10(12), 864–882 (2019).
  Medline CASGoogle Scholar
• 118. Berson A, Nativio R, Berger SL, Bonini NM. Epigenetic regulation in neurodegenerative diseases. Trends Neurosci. 41(9), 587–598 (2018).
  Medline CASGoogle Scholar
• 119. Ghosh P, Saadat A. Neurodegeneration, and epigenetics: a review. Neurologia (Engl. Ed.) 38(6), e62–e68 (2023).
  CASGoogle Scholar
• 120. Peña CJ, Bagot RC, Labonté B, Nestler EJ. Epigenetic signaling in psychiatric disorders. J. Mol. Biol. 426(20), 3389–3412 (2014).
  Medline CASGoogle Scholar
• 121. Kwon M, Park K, Hyun K et al. H2B ubiquitylation enhances H3K4 methylation activities of human KMT2 family complexes. Nucleic Acids Res. 48(10), 5442–5456 (2020).
  Medline CASGoogle Scholar
• 122. Duan YC, Zhang SJ, Shi XJ et al. Research progress of dual inhibitors targeting crosstalk between histone epigenetic modulators for cancer therapy. Eur. J. Med. Chem. 222, 113588 (2021). • Highlights the recent advancements in dual inhibitors in epigenetic crosstalk.
  Medline CASGoogle Scholar
• 123. Garcia-Martinez L, Zhang Y, Nakata Y, Chan HL, Morey L. Epigenetic mechanisms in breast cancer therapy and resistance. Nat. Commun. 12(1), 1786 (2021).
  Medline CASGoogle Scholar
• 124. Stillman B. Histone modifications: insights into their influence on gene expression. Cell 175(1), 6–9 (2018).
  Medline CASGoogle Scholar
• 125. Lepack AE, Werner CT, Stewart AF et al. Dopaminylation of histone H3 in ventral tegmental area regulates cocaine seeking. Science 368(6487), 197–201 (2020).
  Medline CASGoogle Scholar
• 126. Farrelly LA, Thompson RE, Zhao S et al. Histone serotonylation is a permissive modification that enhances TFIID binding to H3K4me3. Nature 567(7749), 535–539 (2019).
  Medline CASGoogle Scholar
• 127. Patra SK. Emerging histone glutamine modifications mediated gene expression in cell differentiation and the VTA reward pathway. Gene 768, 145323 (2021).
  Medline CASGoogle Scholar
• 128. Patra SK, Szyf M. Epigenetic perspectives of COVID-19: virus infection to disease progression and therapeutic control. Biochim Biophys Acta Mol Basis Dis. 1868(12), 166527 (2022).
  Medline CASGoogle Scholar
• 129. Chlamydas S, Papavassiliou AG, Piperi C. Epigenetic mechanisms regulating COVID-19 infection. Epigenetics 16(3), 263–270 (2021).
  MedlineGoogle Scholar
• 130. Zhang Y, Chen Y, Li Y et al. The ORF8 protein of SARS-CoV-2 mediates immune evasion through down-regulating MHC-I. Proc. Natl Acad. Sci. USA 118(23), e2024202118 (2021).
  Medline CASGoogle Scholar
• 131. Kee J, Thudium S, Renner DM et al. SARS-CoV-2 disrupts host epigenetic regulation via histone mimicry. Nature 610(7931), 381–388 (2022).
  Medline CASGoogle Scholar
• 132. Flower TG, Buffalo CZ, Hooy RM, Allaire M, Ren X, Hurley JH. Structure of SARS-CoV-2 ORF8, a rapidly evolving immune evasion protein. Proc. Natl Acad. Sci. USA 118(2), e2021785118 (2021).
  Medline CASGoogle Scholar