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Annual Review of Biomedical Engineering

Volume 19, 2017

Epigenetic Regulation: A New Frontier for Biomedical Engineers

Abstract

Gene expression in mammalian cells depends on the epigenetic status of the chromatin, including DNA methylation, histone modifications, promoter–enhancer interactions, and noncoding RNA–mediated regulation. The coordinated actions of these multifaceted regulations determine cell development, cell cycle regulation, cell state and fate, and the ultimate responses in health and disease. Therefore, studies of epigenetic modulations are critical for our understanding of gene regulation mechanisms at the molecular, cellular, tissue, and organ levels. The aim of this review is to provide biomedical engineers with an overview of the principles of epigenetics, methods of study, recent findings in epigenetic regulation in health and disease, and computational and sequencing tools for epigenetics analysis, with an emphasis on the cardiovascular system. This review concludes with the perspectives of the application of bioengineering to advance epigenetics and the utilization of epigenetics to translate bioengineering research into clinical medicine.

Keyword(s): chromatin remodeling, DNA methylation, gene regulation, histone modification, long noncoding RNA, systems biology
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2017-06-21
2024-04-18
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Literature Cited

  1. Watson JD, Crick FH. 1.  1953. Molecular structure of nucleic acids: a structure for deoxyribose nucleic acid. Nature 171:737–38 [Google Scholar]
  2. Crick F. 2.  1970. Central dogma of molecular biology. Nature 227:561–63 [Google Scholar]
  3. Ehrlich M, Gama-Sosa MA, Huang LH, Midgett RM, Kuo KC. 3.  et al. 1982. Amount and distribution of 5-methylcytosine in human DNA from different types of tissues of cells. Nucleic Acids Res 10:2709–21 [Google Scholar]
  4. Wu H, Zhang Y. 4.  2014. Reversing DNA methylation: mechanisms, genomics, and biological functions. Cell 156:45–68 [Google Scholar]
  5. Holliday R, Pugh JE. 5.  1975. DNA modification mechanisms and gene activity during development. Science 187:226–32 [Google Scholar]
  6. Riggs AD. 6.  1975. X inactivation, differentiation, and DNA methylation. Cytogenet. Cell Genet. 14:9–25 [Google Scholar]
  7. Lin JC, Jeong S, Liang G, Takai D, Fatemi M. 7.  et al. 2007. Role of nucleosomal occupancy in the epigenetic silencing of the MLH1 CpG island. Cancer Cell 12:432–44 [Google Scholar]
  8. Wade PA, Wolffe AP. 8.  2001. ReCoGnizing methylated DNA. Nat. Struct. Biol. 8:575–77 [Google Scholar]
  9. Wolf SF, Jolly DJ, Lunnen KD, Friedmann T, Migeon BR. 9.  1984. Methylation of the hypoxanthine phosphoribosyltransferase locus on the human X chromosome: implications for X-chromosome inactivation. PNAS 81:2806–10 [Google Scholar]
  10. Aran D, Sabato S, Hellman A. 10.  2013. DNA methylation of distal regulatory sites characterizes dysregulation of cancer genes. Genome Biol 14:R21 [Google Scholar]
  11. Holmgren C, Kanduri C, Dell G, Ward A, Mukhopadhya R. 11.  et al. 2001. CpG methylation regulates the Igf2/H19 insulator. Curr. Biol. 11:1128–30 [Google Scholar]
  12. Fatemi M, Hermann A, Pradhan S, Jeltsch A. 12.  2001. The activity of the murine DNA methyltransferase Dnmt1 is controlled by interaction of the catalytic domain with the N-terminal part of the enzyme leading to an allosteric activation of the enzyme after binding to methylated DNA. J. Mol. Biol. 309:1189–99 [Google Scholar]
  13. Hermann A, Goyal R, Jeltsch A. 13.  2004. The Dnmt1 DNA-(cytosine-C5)-methyltransferase methylates DNA processively with high preference for hemimethylated target sites. J. Biol. Chem. 279:48350–59 [Google Scholar]
  14. Okano M, Bell DW, Haber DA, Li E. 14.  1999. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99:247–57 [Google Scholar]
  15. Fatemi M, Hermann A, Gowher H, Jeltsch A. 15.  2002. Dnmt3a and Dnmt1 functionally cooperate during de novo methylation of DNA. Eur. J. Biochem. 269:4981–84 [Google Scholar]
  16. Christman JK. 16.  2002. 5-Azacytidine and 5-aza-2′-deoxycytidine as inhibitors of DNA methylation: mechanistic studies and their implications for cancer therapy. Oncogene 21:5483–95 [Google Scholar]
  17. Garcia-Manero G, Kantarjian HM, Sanchez-Gonzalez B, Yang H, Rosner G. 17.  et al. 2006. Phase 1/2 study of the combination of 5-aza-2′-deoxycytidine with valproic acid in patients with leukemia. Blood 108:3271–9 [Google Scholar]
  18. Momparler RL, Rivard GE, Gyger M. 18.  1985. Clinical trial on 5-aza-2′-deoxycytidine in patients with acute leukemia. Pharmacol. Ther. 30:277–86 [Google Scholar]
  19. Ito S, Shen L, Dai Q, Wu SC, Collins LB. 19.  et al. 2011. Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine. Science 333:1300–3 [Google Scholar]
  20. Karimi M, Johansson S, Stach D, Corcoran M, Grander D. 20.  et al. 2006. LUMA (LUminometric Methylation Assay)—a high throughput method to the analysis of genomic DNA methylation. Exp. Cell Res. 312:1989–95 [Google Scholar]
  21. Yang AS, Estecio MR, Doshi K, Kondo Y, Tajara EH, Issa JP. 21.  2004. A simple method for estimating global DNA methylation using bisulfite PCR of repetitive DNA elements. Nucleic Acids Res 32:e38 [Google Scholar]
  22. Frommer M, McDonald LE, Millar DS, Collis CM, Watt F. 22.  et al. 1992. A genomic sequencing protocol that yields a positive display of 5-methylcytosine residues in individual DNA strands. PNAS 89:1827–31 [Google Scholar]
  23. Mizugaki M, Itoh K, Yamaguchi T, Ishiwata S, Hishinuma T. 23.  et al. 1996. Preparation of a monoclonal antibody specific for 5-methyl-2′-deoxycytidine and its application for the detection of DNA methylation levels in human peripheral blood cells. Biol. Pharm. Bull. 19:1537–40 [Google Scholar]
  24. Herman JG, Graff JR, Myohanen S, Nelkin BD, Baylin SB. 24.  1996. Methylation-specific PCR: a novel PCR assay for methylation status of CpG islands. PNAS 93:9821–26 [Google Scholar]
  25. Uhlmann K, Brinckmann A, Toliat MR, Ritter H, Nurnberg P. 25.  2002. Evaluation of a potential epigenetic biomarker by quantitative methyl–single nucleotide polymorphism analysis. Electrophoresis 23:4072–79 [Google Scholar]
  26. Colella S, Shen L, Baggerly KA, Issa JP, Krahe R. 26.  2003. Sensitive and quantitative universal Pyrosequencing™ methylation analysis of CpG sites. BioTechniques 35:146–50 [Google Scholar]
  27. Ehrich M, Nelson MR, Stanssens P, Zabeau M, Liloglou T. 27.  et al. 2005. Quantitative high-throughput analysis of DNA methylation patterns by base-specific cleavage and mass spectrometry. PNAS 102:15785–90 [Google Scholar]
  28. Weber M, Davies JJ, Wittig D, Oakeley EJ, Haase M. 28.  et al. 2005. Chromosome-wide and promoter-specific analyses identify sites of differential DNA methylation in normal and transformed human cells. Nat. Genet. 37:853–62 [Google Scholar]
  29. Meissner A, Gnirke A, Bell GW, Ramsahoye B, Lander ES, Jaenisch R. 29.  2005. Reduced representation bisulfite sequencing for comparative high-resolution DNA methylation analysis. Nucleic Acids Res 33:5868–77 [Google Scholar]
  30. Harris RA, Wang T, Coarfa C, Nagarajan RP, Hong C. 30.  et al. 2010. Comparison of sequencing-based methods to profile DNA methylation and identification of monoallelic epigenetic modifications. Nat. Biotechnol. 28:1097–105 [Google Scholar]
  31. Laird PW. 31.  2010. Principles and challenges of genomewide DNA methylation analysis. Nat. Rev. Genet. 11:191–203 [Google Scholar]
  32. Ordovas JM, Smith CE. 32.  2010. Epigenetics and cardiovascular disease. Nat. Rev. Cardiol. 7:510–19 [Google Scholar]
  33. Breton CV, Byun HM, Wenten M, Pan F, Yang A, Gilliland FD. 33.  2009. Prenatal tobacco smoke exposure affects global and gene-specific DNA methylation. Am. J. Respir. Crit. Care Med. 180:462–67 [Google Scholar]
  34. Smolarek I, Wyszko E, Barciszewska AM, Nowak S, Gawronska I. 34.  et al. 2010. Global DNA methylation changes in blood of patients with essential hypertension. Med. Sci. Monit 16CR149–55 [Google Scholar]
  35. Castro R, Rivera I, Struys EA, Jansen EE, Ravasco P. 35.  et al. 2003. Increased homocysteine and S-adenosylhomocysteine concentrations and DNA hypomethylation in vascular disease. Clin. Chem. 49:1292–96 [Google Scholar]
  36. Chatzizisis YS, Coskun AU, Jonas M, Edelman ER, Feldman CL, Stone PH. 36.  2007. Role of endothelial shear stress in the natural history of coronary atherosclerosis and vascular remodeling: molecular, cellular, and vascular behavior. J. Am. Coll. Cardiol. 49:2379–93 [Google Scholar]
  37. Chiu JJ, Chien S. 37.  2011. Effects of disturbed flow on vascular endothelium: pathophysiological basis and clinical perspectives. Physiol. Rev. 91:327–87 [Google Scholar]
  38. Dunn J, Qiu H, Kim S, Jjingo D, Hoffman R. 38.  et al. 2014. Flow-dependent epigenetic DNA methylation regulates endothelial gene expression and atherosclerosis. J. Clin. Investig. 124:3187–99 [Google Scholar]
  39. Jiang YZ, Jimenez JM, Ou K, McCormick ME, Zhang LD, Davies PF. 39.  2014. Hemodynamic disturbed flow induces differential DNA methylation of endothelial Krüppel-like factor 4 promoter in vitro and in vivo. Circ. Res. 115:32–43 [Google Scholar]
  40. Zhou J, Li YS, Wang KC, Chien S. 40.  2014. Epigenetic mechanism in regulation of endothelial function by disturbed flow: induction of DNA hypermethylation by DNMT1. Cell. Mol. Bioeng. 7:218–24 [Google Scholar]
  41. Jiang YZ, Manduchi E, Stoeckert CJ Jr., Davies PF. 41.  2015. Arterial endothelial methylome: differential DNA methylation in athero-susceptible disturbed flow regions in vivo. BMC Genom 16:506 [Google Scholar]
  42. Zhou G, Hamik A, Nayak L, Tian H, Shi H. 42.  et al. 2012. Endothelial Krüppel-like factor 4 protects against atherothrombosis in mice. J. Clin. Investig. 122:4727–31 [Google Scholar]
  43. Rivera CM, Ren B. 43.  2013. Mapping human epigenomes. Cell 155:39–55 [Google Scholar]
  44. Bannister AJ, Kouzarides T. 44.  2011. Regulation of chromatin by histone modifications. Cell Res 21:381–95 [Google Scholar]
  45. Workman JL, Kingston RE. 45.  1998. Alteration of nucleosome structure as a mechanism of transcriptional regulation. Annu. Rev. Biochem. 67:545–79 [Google Scholar]
  46. Pasini D, Hansen KH, Christensen J, Agger K, Cloos PA, Helin K. 46.  2008. Coordinated regulation of transcriptional repression by the RBP2 H3K4 demethylase and polycomb-repressive complex 2. Genes Dev 22:1345–55 [Google Scholar]
  47. Pflum MK, Tong JK, Lane WS, Schreiber SL. 47.  2001. Histone deacetylase 1 phosphorylation promotes enzymatic activity and complex formation. J. Biol. Chem. 276:47733–41 [Google Scholar]
  48. Yang SH, Sharrocks AD. 48.  2004. SUMO promotes HDAC-mediated transcriptional repression. Mol. Cell 13:611–17 [Google Scholar]
  49. 49. ENCODE Proj. Consort 2004. The ENCODE (ENCyclopedia Of DNA Elements) Project. Science 306:636–40 [Google Scholar]
  50. Tian Z, Tolic N, Zhao R, Moore RJ, Hengel SM. 50.  et al. 2012. Enhanced top-down characterization of histone post-translational modifications. Genome Biol 13:R86 [Google Scholar]
  51. Tan S, Davey CA. 51.  2011. Nucleosome structural studies. Curr. Opin. Struct. Biol. 21:128–36 [Google Scholar]
  52. Brown JD, Lin CY, Duan Q, Griffin G, Federation AJ. 52.  et al. 2014. NF-κB directs dynamic super enhancer formation in inflammation and atherogenesis. Mol. Cell 56:219–31 [Google Scholar]
  53. Geisberg JV, Struhl K. 53.  2004. Quantitative sequential chromatin immunoprecipitation, a method for analyzing co-occupancy of proteins at genomic regions in vivo. Nucleic Acids Res 32:e151 [Google Scholar]
  54. Rhee HS, Pugh BF. 54.  2011. Comprehensive genome-wide protein–DNA interactions detected at single-nucleotide resolution. Cell 147:1408–19 [Google Scholar]
  55. Brinkman AB, Gu H, Bartels SJ, Zhang Y, Matarese F. 55.  et al. 2012. Sequential ChIP-bisulfite sequencing enables direct genome-scale investigation of chromatin and DNA methylation cross-talk. Genome Res 22:1128–38 [Google Scholar]
  56. Statham AL, Robinson MD, Song JZ, Coolen MW, Stirzaker C, Clark SJ. 56.  2012. Bisulfite sequencing of chromatin immunoprecipitated DNA (BisChIP-seq) directly informs methylation status of histone-modified DNA. Genome Res 22:1120–27 [Google Scholar]
  57. Kee HJ, Sohn IS, Nam KI, Park JE, Qian YR. 57.  et al. 2006. Inhibition of histone deacetylation blocks cardiac hypertrophy induced by angiotensin II infusion and aortic banding. Circulation 113:51–59 [Google Scholar]
  58. Kook H, Lepore JJ, Gitler AD, Lu MM, Yung WW-M. 58.  et al. 2003. Cardiac hypertrophy and histone deacetylase–dependent transcriptional repression mediated by the atypical homeodomain protein Hop. J. Clin. Investig. 112:863–71 [Google Scholar]
  59. Zhang QJ, Chen HZ, Wang L, Liu DP, Hill JA, Liu ZP. 59.  2011. The histone trimethyllysine demethylase JMJD2A promotes cardiac hypertrophy in response to hypertrophic stimuli in mice. J. Clin. Investig. 121:2447–56 [Google Scholar]
  60. Kaneda R, Takada S, Yamashita Y, Choi YL, Nonaka-Sarukawa M. 60.  et al. 2009. Genome-wide histone methylation profile for heart failure. Genes Cells 14:69–77 [Google Scholar]
  61. Villeneuve LM, Reddy MA, Lanting LL, Wang M, Meng L, Natarajan R. 61.  2008. Epigenetic histone H3 lysine 9 methylation in metabolic memory and inflammatory phenotype of vascular smooth muscle cells in diabetes. PNAS 105:9047–52 [Google Scholar]
  62. Miao F, Chen Z, Genuth S, Paterson A, Zhang L. 62.  et al. 2014. Evaluating the role of epigenetic histone modifications in the metabolic memory of type 1 diabetes. Diabetes 63:1748–62 [Google Scholar]
  63. Fish JE, Matouk CC, Rachlis A, Lin S, Tai SC. 63.  et al. 2005. The expression of endothelial nitric-oxide synthase is controlled by a cell-specific histone code. J. Biol. Chem. 280:24824–38 [Google Scholar]
  64. Lee DY, Lee CI, Lin TE, Lim SH, Zhou J. 64.  et al. 2012. Role of histone deacetylases in transcription factor regulation and cell cycle modulation in endothelial cells in response to disturbed flow. PNAS 109:1967–72 [Google Scholar]
  65. Abend A, Kehat I. 65.  2015. Histone deacetylases as therapeutic targets—from cancer to cardiac disease. Pharmacol. Ther. 147:55–62 [Google Scholar]
  66. Lu X, Wang L, Yu C, Yu D, Yu G. 66.  2015. Histone acetylation modifiers in the pathogenesis of Alzheimer's disease. Front. Cell. Neurosci. 9:226 [Google Scholar]
  67. Luger K, Dechassa ML, Tremethick DJ. 67.  2012. New insights into nucleosome and chromatin structure: an ordered state or a disordered affair?. Nat. Rev. Mol. Cell Biol. 13:436–47 [Google Scholar]
  68. Saha A, Wittmeyer J, Cairns BR. 68.  2006. Chromatin remodelling: the industrial revolution of DNA around histones. Nat. Rev. Mol. Cell Biol. 7:437–47 [Google Scholar]
  69. Trifonov EN. 69.  2011. Cracking the chromatin code: precise rule of nucleosome positioning. Phys. Life Rev. 8:39–50 [Google Scholar]
  70. Pugh BF. 70.  2010. A preoccupied position on nucleosomes. Nat. Struct. Mol. Biol. 17:923 [Google Scholar]
  71. Struhl K, Segal E. 71.  2013. Determinants of nucleosome positioning. Nat. Struct. Mol. Biol. 20:267–73 [Google Scholar]
  72. Zhang Z, Wippo CJ, Wal M, Ward E, Korber P, Pugh BF. 72.  2011. A packing mechanism for nucleosome organization reconstituted across a eukaryotic genome. Science 332:977–80 [Google Scholar]
  73. Vincent JA, Kwong TJ, Tsukiyama T. 73.  2008. ATP-dependent chromatin remodeling shapes the DNA replication landscape. Nat. Struct. Mol. Biol. 15:477–84 [Google Scholar]
  74. Bazett-Jones DP, Cote J, Landel CC, Peterson CL, Workman JL. 74.  1999. The SWI/SNF complex creates loop domains in DNA and polynucleosome arrays and can disrupt DNA–histone contacts within these domains. Mol. Cell. Biol. 19:1470–78 [Google Scholar]
  75. Bell AC, West AG, Felsenfeld G. 75.  1999. The protein CTCF is required for the enhancer blocking activity of vertebrate insulators. Cell 98:387–96 [Google Scholar]
  76. Cavalli G, Misteli T. 76.  2013. Functional implications of genome topology. Nat. Struct. Mol. Biol. 20:290–99 [Google Scholar]
  77. Kagey MH, Newman JJ, Bilodeau S, Zhan Y, Orlando DA. 77.  et al. 2010. Mediator and cohesin connect gene expression and chromatin architecture. Nature 467:430–35 [Google Scholar]
  78. Wendt KS, Yoshida K, Itoh T, Bando M, Koch B. 78.  et al. 2008. Cohesin mediates transcriptional insulation by CCCTC-binding factor. Nature 451:796–801 [Google Scholar]
  79. Li G, Levitus M, Bustamante C, Widom J. 79.  2005. Rapid spontaneous accessibility of nucleosomal DNA. Nat. Struct. Mol. Biol. 12:46–53 [Google Scholar]
  80. Miyagi A, Ando T, Lyubchenko YL. 80.  2011. Dynamics of nucleosomes assessed with time-lapse high-speed atomic force microscopy. Biochemistry 50:7901–8 [Google Scholar]
  81. Song F, Chen P, Sun D, Wang M, Dong L. 81.  et al. 2014. Cryo-EM study of the chromatin fiber reveals a double helix twisted by tetranucleosomal units. Science 344:376–80 [Google Scholar]
  82. Barski A, Cuddapah S, Cui K, Roh TY, Schones DE. 82.  et al. 2007. High-resolution profiling of histone methylations in the human genome. Cell 129:823–37 [Google Scholar]
  83. Hesselberth JR, Chen X, Zhang Z, Sabo PJ, Sandstrom R. 83.  et al. 2009. Global mapping of protein–DNA interactions in vivo by digital genomic footprinting. Nat. Methods 6:283–89 [Google Scholar]
  84. Buenrostro JD, Giresi PG, Zaba LC, Chang HY, Greenleaf WJ. 84.  2013. Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position. Nat. Methods 10:1213–18 [Google Scholar]
  85. Giresi PG, Kim J, McDaniell RM, Iyer VR, Lieb JD. 85.  2007. FAIRE (formaldehyde-assisted isolation of regulatory elements) isolates active regulatory elements from human chromatin. Genome Res 17:877–85 [Google Scholar]
  86. Meyer CA, Liu XS. 86.  2014. Identifying and mitigating bias in next-generation sequencing methods for chromatin biology. Nat. Rev. Genet. 15:709–21 [Google Scholar]
  87. Dekker J, Rippe K, Dekker M, Kleckner N. 87.  2002. Capturing chromosome conformation. Science 295:1306–11 [Google Scholar]
  88. van de Werken HJ, Landan G, Holwerda SJ, Hoichman M, Klous P. 88.  et al. 2012. Robust 4C-seq data analysis to screen for regulatory DNA interactions. Nat. Methods 9:969–72 [Google Scholar]
  89. Dostie J, Richmond TA, Arnaout RA, Selzer RR, Lee WL. 89.  et al. 2006. Chromosome Conformation Capture Carbon Copy (5C): a massively parallel solution for mapping interactions between genomic elements. Genome Res 16:1299–309 [Google Scholar]
  90. Fullwood MJ, Liu MH, Pan YF, Liu J, Xu H. 90.  et al. 2009. An oestrogen-receptor-α-bound human chromatin interactome. Nature 462:58–64 [Google Scholar]
  91. Lieberman-Aiden E, van Berkum NL, Williams L, Imakaev M, Ragoczy T. 91.  et al. 2009. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326:289–93 [Google Scholar]
  92. Jäger R, Migliorini G, Henrion M, Kandaswamy R, Speedy HE. 92.  et al. 2015. Capture Hi-C identifies the chromatin interactome of colorectal cancer risk loci. Nat. Commun. 6:6178 [Google Scholar]
  93. Griffin CT, Brennan J, Magnuson T. 93.  2008. The chromatin-remodeling enzyme BRG1 plays an essential role in primitive erythropoiesis and vascular development. Development 135:493–500 [Google Scholar]
  94. Stankunas K, Hang CT, Tsun ZY, Chen H, Lee NV. 94.  et al. 2008. Endocardial Brg1 represses ADAMTS1 to maintain the microenvironment for myocardial morphogenesis. Dev. Cell 14:298–311 [Google Scholar]
  95. Harismendy O, Notani D, Song X, Rahim NG, Tanasa B. 95.  et al. 2011. 9p21 DNA variants associated with coronary artery disease impair interferon-γ signalling response. Nature 470:264–68 [Google Scholar]
  96. Djebali S, Davis CA, Merkel A, Dobin A, Lassmann T. 96.  et al. 2012. Landscape of transcription in human cells. Nature 489:101–8 [Google Scholar]
  97. Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC. 97.  1998. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. . Nature 391:806–11 [Google Scholar]
  98. Hamilton AJ, Baulcombe DC. 98.  1999. A species of small antisense RNA in posttranscriptional gene silencing in plants. Science 286:950–52 [Google Scholar]
  99. Lee RC, Feinbaum RL, Ambros V. 99.  1993. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75:843–54 [Google Scholar]
  100. De Santa F, Barozzi I, Mietton F, Ghisletti S, Polletti S. 100.  et al. 2010. A large fraction of extragenic RNA pol II transcription sites overlap enhancers. PLOS Biol 8:e1000384 [Google Scholar]
  101. Carthew RW, Sontheimer EJ. 101.  2009. Origins and mechanisms of miRNAs and siRNAs. Cell 136:642–55 [Google Scholar]
  102. Iwasaki YW, Siomi MC, Siomi H. 102.  2015. PIWI-interacting RNA: its biogenesis and functions. Annu. Rev. Biochem. 84:405–33 [Google Scholar]
  103. Sun W, Li YSJ, Huang HD, Shyy JJ-Y, Chien S. 103.  2010. microRNA: a master regulator of cellular processes for bioengineering systems. Annu. Rev. Biomed. Eng 121–27 [Google Scholar]
  104. Uchida S, Dimmeler S. 104.  2015. Long noncoding RNAs in cardiovascular diseases. Circ. Res. 116:737–50 [Google Scholar]
  105. Wang KC, Chang HY. 105.  2011. Molecular mechanisms of long noncoding RNAs. Mol. Cell 43:904–14 [Google Scholar]
  106. Volders PJ, Verheggen K, Menschaert G, Vandepoele K, Martens L. 106.  et al. 2015. An update on LNCipedia: a database for annotated human lncRNA sequences. Nucleic Acids Res 43:D174–80 [Google Scholar]
  107. Amaral PP, Clark MB, Gascoigne DK, Dinger ME, Mattick JS. 107.  2011. lncRNAdb: A reference database for long noncoding RNAs. Nucleic Acids Res 39:D146–51 [Google Scholar]
  108. Quek XC, Thomson DW, Maag JL, Bartonicek N, Signal B. 108.  et al. 2015. lncRNAdb v2.0: expanding the reference database for functional long noncoding RNAs. Nucleic Acids Res 43:D168–73 [Google Scholar]
  109. Kim TK, Hemberg M, Gray JM, Costa AM, Bear DM. 109.  et al. 2010. Widespread transcription at neuronal activity–regulated enhancers. Nature 465:182–87 [Google Scholar]
  110. Trimarchi T, Bilal E, Ntziachristos P, Fabbri G, Dalla-Favera R. 110.  et al. 2014. Genome-wide mapping and characterization of Notch-regulated long noncoding RNAs in acute leukemia. Cell 158:593–606 [Google Scholar]
  111. Ferguson-Smith AC, Sasaki H, Cattanach BM, Surani MA. 111.  1993. Parental-origin-specific epigenetic modification of the mouse H19 gene. Nature 362:751–55 [Google Scholar]
  112. Zhang Y, Tycko B. 112.  1992. Monoallelic expression of the human H19 gene. Nat. Genet. 1:40–44 [Google Scholar]
  113. Bell AC, Felsenfeld G. 113.  2000. Methylation of a CTCF-dependent boundary controls imprinted expression of the Igf2 gene. Nature 405:482–85 [Google Scholar]
  114. Moulton T, Crenshaw T, Hao Y, Moosikasuwan J, Lin N. 114.  et al. 1994. Epigenetic lesions at the H19 locus in Wilms’ tumour patients. Nat. Genet. 7:440–47 [Google Scholar]
  115. Steenman MJ, Rainier S, Dobry CJ, Grundy P, Horon IL, Feinberg AP. 115.  1994. Loss of imprinting of IGF2 is linked to reduced expression and abnormal methylation of H19 in Wilms’ tumour. Nat. Genet 7:433–39 [Google Scholar]
  116. Brown CJ, Lafreniere RG, Powers VE, Sebastio G, Ballabio A. 116.  et al. 1991. Localization of the X inactivation centre on the human X chromosome in Xq13. Nature 349:82–84 [Google Scholar]
  117. Herzing LB, Romer JT, Horn JM, Ashworth A. 117.  1997. Xist has properties of the X-chromosome inactivation centre. Nature 386:272–75 [Google Scholar]
  118. Lee JT. 118.  2012. Epigenetic regulation by long noncoding RNAs. Science 338:1435–39 [Google Scholar]
  119. Yap KL, Li S, Muñoz-Cabello AM, Raguz S, Zeng L. 119.  et al. 2010. Molecular interplay of the noncoding RNA ANRIL and methylated histone H3 lysine 27 by polycomb CBX7 in transcriptional silencing of INK4a. Mol. Cell 38:662–74 [Google Scholar]
  120. Guo JU, Agarwal V, Guo H, Bartel DP. 120.  2014. Expanded identification and characterization of mammalian circular RNAs. Genome Biol 15:409 [Google Scholar]
  121. Hansen TB, Jensen TI, Clausen BH, Bramsen JB, Finsen B. 121.  et al. 2013. Natural RNA circles function as efficient microRNA sponges. Nature 495:384–88 [Google Scholar]
  122. Memczak S, Jens M, Elefsinioti A, Torti F, Krueger J. 122.  et al. 2013. Circular RNAs are a large class of animal RNAs with regulatory potency. Nature 495:333–38 [Google Scholar]
  123. Guttman M, Donaghey J, Carey BW, Garber M, Grenier JK. 123.  et al. 2011. lincRNAs act in the circuitry controlling pluripotency and differentiation. Nature 477:295–300 [Google Scholar]
  124. Ule J, Jensen KB, Ruggiu M, Mele A, Ule A, Darnell RB. 124.  2003. CLIP identifies Nova-regulated RNA networks in the brain. Science 302:1212–15 [Google Scholar]
  125. Huarte M, Guttman M, Feldser D, Garber M, Koziol MJ. 125.  et al. 2010. A large intergenic noncoding RNA induced by p53 mediates global gene repression in the p53 response. Cell 142:409–19 [Google Scholar]
  126. Chu C, Qu K, Zhong FL, Artandi SE, Chang HY. 126.  2011. Genomic maps of long noncoding RNA occupancy reveal principles of RNA–chromatin interactions. Mol. Cell 44:667–78 [Google Scholar]
  127. Li W, Notani D, Ma Q, Tanasa B, Nunez E. 127.  et al. 2013. Functional roles of enhancer RNAs for oestrogen-dependent transcriptional activation. Nature 498:516–20 [Google Scholar]
  128. Quinn JJ, Ilik IA, Qu K, Georgiev P, Chu C. 128.  et al. 2014. Revealing long noncoding RNA architecture and functions using domain-specific chromatin isolation by RNA purification. Nat. Biotechnol. 32:933–40 [Google Scholar]
  129. Holdt LM, Beutner F, Scholz M, Gielen S, Gäbel G. 129.  et al. 2010. ANRIL expression is associated with atherosclerosis risk at chromosome 9p21. Arterioscler. Thromb. Vasc. Biol. 30:620–27 [Google Scholar]
  130. Congrains A, Kamide K, Oguro R, Yasuda O, Miyata K. 130.  et al. 2012. Genetic variants at the 9p21 locus contribute to atherosclerosis through modulation of ANRIL and CDKN2A/B. . Atherosclerosis 220:449–55 [Google Scholar]
  131. Tsai PC, Liao YC, Lin TH, Hsi E, Yang YH, Juo SH. 131.  2012. Additive effect of ANRIL and BRAP polymorphisms on ankle-brachial index in a Taiwanese population. Circ. J. 76:446–52 [Google Scholar]
  132. Holdt LM, Hoffmann S, Sass K, Langenberger D, Scholz M. 132.  et al. 2013. Alu elements in ANRIL non-coding RNA at chromosome 9p21 modulate atherogenic cell functions through trans-regulation of gene networks. PLOS Genet. 9:e1003588 [Google Scholar]
  133. Wu G, Cai J, Han Y, Chen J, Huang ZP. 133.  et al. 2014. LincRNA–p21 regulates neointima formation, vascular smooth muscle cell proliferation, apoptosis, and atherosclerosis by enhancing p53 activity. Circulation 130:1452–65 [Google Scholar]
  134. Li K, Blum Y, Verma A, Liu Z, Pramanik K. 134.  et al. 2010. A noncoding antisense RNA in tie-1 locus regulates tie-1 function in vivo. Blood 115:133–39 [Google Scholar]
  135. Klattenhoff CA, Scheuermann JC, Surface LE, Bradley RK, Fields PA. 135.  et al. 2013. Braveheart, a long noncoding RNA required for cardiovascular lineage commitment. Cell 152:570–83 [Google Scholar]
  136. Kumarswamy R, Bauters C, Volkmann I, Maury F, Fetisch J. 136.  et al. 2014. Circulating long noncoding RNA, LIPCAR, predicts survival in patients with heart failure. Circ. Res. 114:1569–75 [Google Scholar]
  137. Yang KC, Yamada KA, Patel AY, Topkara VK, George I. 137.  et al. 2014. Deep RNA sequencing reveals dynamic regulation of myocardial noncoding RNAs in failing human heart and remodeling with mechanical circulatory support. Circulation 129:1009–21 [Google Scholar]
  138. Park PJ. 138.  2009. ChIP-seq: advantages and challenges of a maturing technology. Nat. Rev. Genet. 10:669–80 [Google Scholar]
  139. Yong WS, Hsu FM, Chen PY. 139.  2016. Profiling genome-wide DNA methylation. Epigenet. Chromatin 9:26 [Google Scholar]
  140. Gilchrist M, Thorsson V, Li B, Rust AG, Korb M. 140.  et al. 2006. Systems biology approaches identify ATF3 as a negative regulator of Toll-like receptor 4. Nature 441:173–78 [Google Scholar]
  141. Garmire LX, Garmire DG, Huang W, Yao J, Glass CK, Subramaniam S. 141.  2011. A global clustering algorithm to identify long intergenic non-coding RNA—with applications in mouse macrophages. PLOS ONE 6:e24051 [Google Scholar]
  142. Das A, Morley M, Moravec CS, Tang WH, Hakonarson H. 142.  et al. 2015. Bayesian integration of genetics and epigenetics detects causal regulatory SNPs underlying expression variability. Nat. Commun. 6:8555 [Google Scholar]
  143. Skogsberg J, Lundström J, Kovacs A, Nilsson R, Noori P. 143.  et al. 2008. Transcriptional profiling uncovers a network of cholesterol-responsive atherosclerosis target genes. PLOS Genet 4:e1000036 [Google Scholar]
  144. Stelzer Y, Shivalila CS, Soldner F, Markoulaki S, Jaenisch R. 144.  2015. Tracing dynamic changes of DNA methylation at single-cell resolution. Cell 163:218–29 [Google Scholar]
  145. Sasaki K, Ito T, Nishino N, Khochbin S, Yoshida M. 145.  2009. Real-time imaging of histone H4 hyperacetylation in living cells. PNAS 106:16257–62 [Google Scholar]
  146. Linhoff MW, Garg SK, Mandel G. 146.  2015. A high-resolution imaging approach to investigate chromatin architecture in complex tissues. Cell 163:246–55 [Google Scholar]
  147. Sander JD, Joung JK. 147.  2014. CRISPR–Cas systems for editing, regulating and targeting genomes. Nat. Biotechnol. 32:347–55 [Google Scholar]
  148. Falkenberg KJ, Johnstone RW. 148.  2014. Histone deacetylases and their inhibitors in cancer, neurological diseases and immune disorders. Nat. Rev. Drug Discov. 13:673–91 [Google Scholar]
  149. Brien GL, Valerio DG, Armstrong SA. 149.  2016. Exploiting the epigenome to control cancer-promoting gene-expression programs. Cancer Cell 29:464–76 [Google Scholar]
  150. Wilczewska AZ, Niemirowicz K, Markiewicz KH, Car H. 150.  2012. Nanoparticles as drug delivery systems. Pharmacol. Rep. 64:1020–37 [Google Scholar]
  151. Hu CM, Fang RH, Wang KC, Luk BT, Thamphiwatana S. 151.  et al. 2015. Nanoparticle biointerfacing by human platelet membrane cloaking. Nature 526:118–21 [Google Scholar]
/content/journals/10.1146/annurev-bioeng-071516-044720
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Epigenetic Regulation: A New Frontier for Biomedical Engineers
Annual Review of Biomedical Engineering 19, 195 (2017); https://doi.org/10.1146/annurev-bioeng-071516-044720
/content/journals/10.1146/annurev-bioeng-071516-044720
/content/journals/10.1146/annurev-bioeng-071516-044720
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