The evolution of epigenetics: From prokaryotes to humans and its biological consequences

Genetics and Epigenetics

Volumn 1, Issue 8, 2016, Pages 25-36

  Willbanks, Amber ^a   Leary, Meghan ^a   Greenshields, Molly ^a   Tyminski, Camila ^a   Heerboth, Sarah ^b   Lapinska, Karolina ^a   Haskins, Kathryn ^a   Sarkar, Sibaji ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Diseases; Epigenetics; Eukaryotes; Evolution; Mammals; Prokaryotes

Indexed keywords

EID: 85012023648     PISSN: 1179237X     EISSN: None     Source Type: Journal    
DOI: 10.4137/GeG.s31863     Document Type: Article

References (117)

1. Turner BM. Epigenetic responses to environmental change and their evolutionary implications. Philos Trans R Soc Lond B. 2009;364:1534.
2. Eid A, Zawia N. Consequences of lead exposure, and its emerging role as an epigenetic modifier in the aging brain. Neurotoxicology. 2016. doi:10.1016/j.neuro. 2016.04.006.
3. Casey SC, Vaccari M, Al-Mulla F, et al. The effect of environmental chemicals on the tumor microenvironment. Carcinogenesis. 2015;36:S160-S183.
4. Chai H, Brown RE. Field effect in cancer: an update. Ann Clin Lab Sci. 2009; 39(4):331-337.
5. Bollati V, Baccarelli A, Hou L, et al. Changes in DNA methylation patterns in subjects exposed to low-dose benzene. Cancer Res. 2007;67:876-880.
6. Choi SW, Claycombe KJ, Martinez JA, Frisco S, Schalinske KL. Nutritional epigenomics: a portal to disease prevention. Adv Nutr. 2013;4:5.
7. Bogan JA, Helmstetter CE. DNA sequestration and transcription in the oriC region of Escherichia coli. Mol Microbiol. 1997;26:889-896.
8. Campbell JL, Kleckner N. E. coli oriC and the dnaA gene promoter are sequestered from dam methyltransferase following the passage of the chromosomal replication fork. Cell. 1990;74:967-979.
9. Han JS, Kang S, Lee H, Kim HK, Hwang DS. Sequential binding of SeqA to paired hemi-ethylated GATC sequences mediates formation of higher order complexes. J Biol Chem. 2003;278:34983-34989.
10. Kang S, Lee H, Han JS, Hwang DS. Interaction of SeqA and Dam methylase on the hemimethylated origin of Escherichia coli chromosomal DNA replication. J Biol Chem. 1999;274:11463-11468.
11. Klungsoyr HK, Skarstad K. Positive supercoiling is generated in the presence of Escherichia coli SeqA protein. Mol Microbiol. 2004;54:123-131.
12. Lu M, Campbell JL, Boye E, Kleckner N. SeqA: a negative modulator of replication initiation in E. coli. Cell. 1994;77:413-426.
13. Molina F, Skarstad K. Replication fork and SeqA focus distributions in Escherichia coli suggest a replication hyperstructure dependent on nucleotide metabolism. Mol Microbiol. 2004;52:1597-1612.
14. Taghbalout A, Landoulsi A, Kern R, et al. Competition between the replication initiator DnaA and the sequestration factor SeqA for binding to the hemimethylated chromosomal origin of E. coli in vitro. Genes Cells. 2000;5:873-884.
15. Au KG, Welsh K, Modrich P. Initiation of methyl-directed mismatch repair. J Biol Chem. 1992;267:12142-12148.
16. Bakker M, Smith DW. Methylation of GATC sites is required for precise timing between rounds of DNA replication in Escherichia coli. J Bacteriol. 1989;4(10): 5738-5742.
17. Bhagwat AS, Lieb M. Cooperation and competition in mismatch repair: very short-patch repair and methyl-directed mismatch repair in Escherichia coli. Mol Microbiol. 2002;44:1421-1428.
18. Modrich P. Methyl-directed DNA mismatch correction. J Biol Chem. 1989;264: 6597-6600.
19. Schlagman SL, Hattman S, Marinus MG. Direct role of the Escherichia coli Dam DNA methyltransferase in methylation-directed mismatch repair. J Bacteriol. 1986;165:896-900.
20. Smith DW, Garland AM, Herman G, Enns RE, Baker TA, Zyskind JW. Importance of state of methylation of oriC GATC sites in initiation of DNA replication in Escherichia coli. EMBO J. 1985;4:1319-1326.
21. Arber W, Dussoix D. Host specificity of DNA produced by Escherichia coli. I. Host controlled modification of bacteriophage lambda. J Mol Biol. 1962;5: 18-36.
22. Dussoix D, Arber W. Host specific of DNA produced by Escherichia coli. II. Control over acceptance of DNA from infecting phage lambda. J Mol Biol. 1962; 5:37-49.
23. Yarmolinski MB, Sternberg N. Bacteriophage P1. Bacteriophages. 1988;1: Chapter 9: 291-292.
24. Sternberg N, Coulby J. Cleavage of the bacteriophage P1 packaging site (pac) is regulated by adenine methylation. Proc Natl Acad Sci U S A. 1990;87(20): 8070-8074.
25. Casadesus J, Low D. Epigenetic gene regulation in the bacterial world. Microbiol Mol Biol Rev. 2006;70(3):830-856.
26. Oliverio AM, Katz LA. The dynamic nature of genomes across the tree of life. Genome Biol Evol. 2014;6(3):482-488.
27. Wardleworth BN, Russell RJM, Bell SD, Taylor GL, White MF. Structure of Alba: an archaeal chromatin protein modulated by acetylation. EMBO J. 2002; 21(17):4654-4662.
28. Sandman K, Reeve JN. Structure and functional relationships of archaeal and eukaryal histones and nucleosomes. Arch Microbiol. 2000;173(3):165-169.
29. White MF, Bell SD. Holding it together: chromatin in the Archaea. Trends Gen. 2002;18(12):621-626.
30. Lurz R, Grote M, Dijk J, Reinhardt R, Dobrinski B. Electron microscopic study of DNA complexes with proteins from the Archaebacterium Sulfolobus acidocaldarius. EMBO J. 1986;5(13):3715-3721.
31. Bell SD, Botting CH, Wardleworth BN, Jackson SP, White MF. The interaction of Alba, a conserved Archaeal chromatin protein, with Sir2 and its regulation by acetylation. Science. 2002;296(5565):148-151.
32. Terns MP, Terns RM. CRISPR-based adaptive immune systems. Curr Opin Microbiol. 2011;14(3):321-327.
33. Marino-Ramirez L, Jordan IK, Landsman D. Multiple independent evolutionary solutions to core histone gene regulation. Genome Biol. 2006;7(12):R122.
34. Reeck GR, Swanson E, Teller DC. The evolution of histones. J Mol Evol. 1978;10:4.
35. Trojer P, Reinberg D. Histone lysine demethylases and their impact on epigenetics. Cell. 2006;125:2.
36. Verdin E, Ott M. 50 years of protein acetylation: from gene regulation to epigenetics, metabolism, and beyond. Nat Rev Mol Biol. 2015;16(4):258-264.
37. Soyer JL, Rouxel T, Fudal I. Chromatin-based control of effector gene expression in plant-associated fungi. Curr Opin Plant Biol. 2015;26:51-56.
38. Qian S, Wang Y, Ma H, Zhang L. Expansion and functional divergence of Jumonji c-containing histone demethylases: significance of duplications in ancestral angiosperms and vertebrates. Plant Physiol. 2015;168(4):1321-1337.
39. Luo G, Blanco MA, Greer EL, He C, Shi Y. DNA N-methyladenine: a new epigenetic mark in eukaryotes? Mol Cell Biol. 2015;16(12):705-710.
40. Hattman S, Kenny C, Berger L, Pratt K. Comparative study of DNA methylation in three unicellular eucaryotes. J Bacteriol. 1978;135(3):1156-1157.
41. Greer EL, Blanco MA, Gu L, et al. DNA methylation on N6-adenine in C. elegans. Cell. 2015;161(4):868-878.
42. Fu Y, Luo GZ, Chen K, et al. N6-methyldeoxyadenosine marks active transcription start sites in Chlamydomonas. Cell. 2015;161(4):879-892.
43. Zhang G, Huang H, Liu D, et al. N6-methyladenine DNA modification in drosophila. Cell. 2015;161:4.
44. Geyer KK, Chalmers IW, Mackintosh N, et al. Cytosine methylation is a conserved epigenetic feature found throughout the phylum Platyhelminthes. BMC Genomics. 2013;14:462.
45. Geyer KK, Rodríguez López CM, Chalmers IW, et al. Cytosine methylation regulates oviposition in the pathogenic blood fluke Schistosoma mansoni. Nat Commun. 2011;2:424.
46. Heyn H, Esteller M. An adenine code for DNA: a second life for N6-methyladenine. Cell. 2015;161(4):710-713.
47. Garza-Garcia AA, Driscoll PC, Brockes JP. Evidence for the local evolution of mechanisms underlying limb regeneration in salamanders. Integr Comp Biol. 2010; 50(4):528-535.
48. Brockes JP, Kumar A, Velloso CP. Regeneration as an evolutionary variable. J Anat. 2001;199:3-11.
49. Saxena S, Purushothaman S, Meghah V, et al. Role of annexin gene and its regulation during zebrafish caudal fin regeneration. Wound Rep Reg. 2016;24(3): 551-559.
50. Bosch TCG. Why polyps regenerate and we don't: towards a cellular and molecular framework for Hydra regeneration. Dev Biol. 2007;303(2):421-433.
51. Fujisawa T. Hydra regeneration and epitheliopeptides. Dev Dynamics. 2003; 226(2):182-189.
52. Chera S, Ghila L, Dobretz K, et al. Apoptotic cells provide an unexpected source of Wnt3 signaling to drive hydra head regeneration. Dev Cell. 2009;17(2):279-289.
53. Hobmayer B, Rentzsch F, Kuhn K, et al. WNT signalling molecules act in axis formation in the diploblastic metazoan Hydra. Nature. 2000;407(6801): 186-189.
54. Matsuzaki H, Okamura E, Takahashi T, et al. De novo DNA methylation through the 5'-segment of the H19 ICR maintains its imprint during early embryogenesis. Development. 2015;142(22):3833-3844.
55. Messerschmidt DM. A twist in zygotic reprogramming. Nat Cell Biol. 2016; 18(2):139-140.
56. Gunesdogan U, Jackle H, Herzig A. A genetic system to assess in vivo the functions of histones and histone modifications in higher eukaryotes. EMBO Rep. 2010;11(10):772-776.
57. Szyf M. Nongenetic inheritance and transgenerational epigenetics. Trends Mol Med. 2014;21(2):134-144.
58. Sanz LA, Kota SK, Feil R. Genome-wide DNA demethylation in mammals. Genome Biol. 2010;11(3):110.
59. Chi P, Allis CD, Wang GG. The histone code hypothesis. Nat Rev Cancer. 2010; 10:457-469.
60. Williams K, Christensen J, Helin K. DNA methylation: TET proteins- guardians of CpG islands? EMBO Rep. 2012;13(1):28-35.
61. Sarkar S, Horn G, Moulton K, et al. Cancer development, progression, and therapy: an epigenetic overview. Int J Mol Sci. 2013;14:10.
62. Zhao Q , Rank G, Tan YT, et al. PRMT5-mediated methylation of histone H4R3 recruits DNMT3a, coupling histone and DNA methylation in gene silencing. Nat Struct Mol Biol. 2009;16(3):304-311.
63. Dowen JM, Fan ZP, Hnisz D, et al. Control of cell identity genes occurs in insulated neighborhoods in mammalian chromosomes. Cell. 2014;159(2):374-387.
64. Wang H, Maurano MT, Qu H, et al. Widespread plasticity in CTCF occupancy linked to DNA methylation. Genome Res. 2012;22(9):1680-1688.
65. Issa J. Aging and epigenetic drift: a vicious cycle. J Clin Invest. 2014;124(1): 24-29.
66. McCauley BS, Dang W. Histone methylation and aging: lessons learned from model systems. Biochim Biophys Acta. 2014;1839(12):1454-1462.
67. Lopez-Otin C, Blasco MA, Partridge L, Serrano M, Kroemer G. The hallmarks of aging. Cell. 2013;153(6):1194-1217.
68. Vera E, Canela A, Fraga MF, Estellar M, Blasco MA. Epigenetic regulation of telomeres in human cancer. Oncogene. 2008;27(54):6817-6833.
69. Jung M, Jin S, Zhang X, et al. Longitudinal epigenetic and gene expression profiles analyzed by three-component analysis reveal down-regulation of genes involved in protein translation in human aging. Nucl Acids Res. 2015;43(15):e100.
70. Hofmann JW, Zhao X, De Cecco M, et al. Reduced expression of MYC increases longevity and enhances healthspan. Cell. 2015;160(3):477-488.
71. Dozmorov MG. Polycomb repressive complex 2 epigenomic signature defines age-associated hypermethylation and gene expression changes. Epigenetics. 2015; 10(6):484-495.
72. Ong T, Ozanne SE. Developmental programming of type 2 diabetes: early nutrition and epigenetic mechanisms. Curr Opin Clin Nutr Metabol Care. 2015; 18(4):354-360.
73. Alfredo Martinez J, Milagro FI, Claycombe KJ, Schalinske KL. Epigenetics in adipose tissue, obesity, weight loss, and diabetes. Adv Nutr. 2014;5(1):71-81.
74. Prescott SL, Allen K, Armstrong K, et al. The establishment of DOHaD working groups in Australia and New Zealand. J Dev Orig Health Dis. 2016:1-7.
75. Niculescu MD, Zeisel SH. Diet, methyl donors and DNA methylation: interactions between dietary folate, methionine, and choline. J Nutr. 2002;132(8): 2333S-2335S.
76. Remely M, Aumueller E, Merold C, et al. Effects of short chain fatty acid producing bacteria on epigenetic regulation of FFAR3 in type 2 diabetes and obesity. Gene. 2014;537(1):85-92.
77. Xiao Y, Su X, Huang W, et al. Role of S-adenosylhomocysteine in cardiovascular disease and its potential epigenetic mechanism. Int J Biochem Cell Biol. 2015;67:158-166.
78. Metes-Kosik N, Luptak I, DiBello PM, et al. Both selenium deficiency and modest selenium supplementation lead to myocardial fibrosis in mice via effects on redox-methylation balance. Mol Nutr Food Res. 2012;56(12):1812-1824.
79. Qureshi IA, Mehler MF. Understanding neurological disease mechanisms in the era of epigenetics. JAMA Neurol. 2013;70(6):703-710.
80. Huynh JL, Casaccia P. Epigenetic mechanisms in multiple sclerosis: implications for pathogenesis and treatment. Lancet Neurol. 2013;12(2):195-206.
81. Masliah E, Dumaop W, Galasko D, Desplats P. Distinctive patterns of DNA methylation associated with Parkinson disease: identification of concordant epigenetic changes in brain and peripheral blood leukocytes. Epigenetics. 2013;8(10): 1030-1038.
82. Shahbazian MD, Zoghbi HY. Rett Syndrome and MeCP2: linking epigenetics and neuronal function. Am J Hum Genet. 2002;71(6):1259-1272.
83. 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.
84. Jones PL, Veenstra GJ, Wade PA, et al. Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription. Nat Genet. 1998;19(2):187-191.
85. Steffan JS, Kazantsev A, Spasic-Boskovic O, et al. The Huntington's disease protein interacts with p53 and CREB-binding protein and represses transcription. Proc Natl Acad Sci U S A. 2000;97(12):6763-6768.
86. Kim HS, Kim EM, Kim NJ, et al. Inhibition of histone deacetylation enhances the neurotoxicity induced by the C-terminal fragments of amyloid precursor protein. J Neurosci Res. 2004;75(1):117-124.
87. Guan JS, Haggarty SJ, Giacometti E, et al. HDAC2 negatively regulates memory formation and synaptic plasticity. Nature. 2009;459(7243):55-60.
88. Kilgore M, Miller CA, Fass DM, et al. Inhibitors of class 1 histone deacetylases reverse contextual memory deficits in a mouse model of Alzheimer's Disease. Neuropsychopharmacology. 2010;35(4):870-880.
89. Aslani S, Mahmoudi M, Karami J, et al. Epigenetic alterations underlying autoimmune diseases. J Autoimmun. 2016;49(2):69-83.
90. Hewagama A, Richardson B. The genetics and epigenetics of autoimmune disease. J Autoimmun. 2009;33(1):3-11.
91. Wu H, Zhao M, Yoshimura A, Chang C, Lu Q. Critical link between epigenetics and transcription factors in the induction of autoimmunity: a comprehensive review. Clin Rev Allergy Immunol. 2016;50(3):333-344.
92. Maltby VE, Graves MC, Lea RA, et al. Genome-wide DNA methylation profiling of CD8+ T cells shows a distinct epigenetic signature to CD4+ T cells in multiple sclerosis patients. Clin Epigenetics. 2015;7:118.
93. Cohen JI. Optimal treatment for chronic active Epstein-Barr virus disease. Pediatr Transplant. 2009;13(4):393-396.
94. Birdwell CE, Queen KJ, Kilgore PC, et al. Genome-wide DNA methylation as an epigenetic consequence of Epistein-Barr virus infection of immortalized keratinocytes. J Virol. 2014;88(19):11442-11458.
95. Shirakawa K, Chavez L, Hakre S, Calvanese V, Verdin E. Reactivation of latent HIV by histone deacetylase inhibitors. Trends Microbiol. 2013;21(6):277-285.
96. Van Epps HL. Peyton Rous: father of the tumor virus. J Exp Med. 2005; 201(3):320.
97. Martin GS. The road the Src. Oncogene. 2004;23(48):7910-7917.
98. Weitzel JN, Blazer KR, MacDonald DJ, Culver JO, Offit K. Genetics, genomics, and cancer risk assessment: state of the art and future directions in the era of personalized medicine. Cancer J Clin. 2011;61(5):327-359.
99. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144(5):646-674.
100. Vogelstein B, Kinzler KW. Cancer genes and the pathways they control. Nat Med. 2004;10(8):789-799.
101. Byler S, Sarkar S. Do epigenetic drug treatments hold the key to killing cancer progenitor cells? Epigenomics. 2014;6(2):161-165.
102. Byler S, Goldgar S, Heerboth S, et al. Genetic and epigenetic aspects of breast cancer progression and therapy. Anticancer Res. 2014;34(3):1071-1077.
103. Sarkar S, Goldgar S, Byler S, Rosenthal S, Heerboth S. Demethylation and reexpression of epigenetically silenced tumor suppressor genes: Sensitization of cancer cells by combination therapy. Epigenomics. 2013;5(1):87-94.
104. Heerboth S, Housman G, Leary M, et al. EMT and tumor metastasis. Clin Transl Med. 2015;4:6.
105. Heerboth S, Lapinska K, Snyder N, Leary M, Rollinson S, Sarkar S. The use of epigenetics drugs in diseases: an overview. Gen Epigenetics. 2014;6:9-19.
106. Longacre M, Snyder NA, Housman G, et al. A comparative analysis of genetic and epigenetic events of breast and ovarian cancer related to tumorigenesis. Int J Mol Sci. 2016;17(5):E759.
107. Agrawal S, Unterberg M, Koschmieder S, et al. DNA methylation of tumor suppressor genes in clinical remission predicts the relapse risk in acute myeloid leukemia. Cancer Res. 2007;67(3):1370-1377.
108. Samorodnitsky E, Ghosh E, Mazumder S, Sarkar S. Methylation by DNMT1 is more efficient in chronic lymphocytic leukemia cells than in normal cells. J Proteomics Bioinform. 2014: doi:10.4172/jpb.S10-004.
109. Housman G, Byler S, Heerboth S, et al. Drug resistance in cancer: an overview. Cancers (Basel). 2014;6(3):1769-1792.
110. Juergens RA, Wrangle J, Vendetti FP, et al. Combination epigenetic therapy has efficacy in patients with refractory advanced non-small cell lung cancer. Cancer Discov. 2011;1(7):598-607.
111. Cacan E, Ali MW, Boyd NH, Hooks SB, Greer SF. Inhibition of HDAC1 and DNMT1 modulate RGS10 expression and decrease ovarian cancer chemoresistance. PLoS One. 2014;9(1):e87455.
112. Inaki K, Menghi F, Woo XY, et al. Systems consequences of amplicon formation in human breast cancer. Genome Res. 2014;24(10):1559-1571.
113. Ko M, An J, Pastor WA, Koralov SB, Rajewsky K, Rao A. TET proteins and 5-methylcytosine oxidation in hematological cancers. Immunol Rev. 2015;263(1): 6-21.
114. Nabel CS, Jia H, Ye Y, et al. AID/APOBEC deaminases disfavor modified cytosines implicated in DNA demethylation. Nat Chem Biol. 2012;8(9):751-758.
115. Hu J, Zhang Y, Zhao L, et al. Chromosomal loop domains direct the recombination of antigen receptor genes. Cell. 2015;163(4):947-959.
116. He Y, Meng XM, Huang C, et al. Long noncoding RNAs: novel insights into hepatocelluar carcinoma. Cancer Lett. 2014;344(1):20-27.
117. Song MA, Tiirikainen M, Kwee S, Okimoto G, Yu H, Wong LL. Elucidating the landscape of aberrant DNA methylation in hepatocellular carcinoma. PLoS One. 2013;8(2):e55761.