N6-methyladenine functions as a potential epigenetic mark in eukaryotes

BioEssays

Volumn 37, Issue 11, 2015, Pages 1155-1162

  Sun, Qinmiao ^a   Huang, Shoujun ^a,b   Wang, Xiaona ^a   Zhu, Yuanxiang ^a   Chen, Zhenping ^a   Chen, Dahua ^a  

^a INSTITUTE OF ZOOLOGY   (China)

^b ANHUI AGRICULTURAL UNIVERSITY   (China)

Author keywords

5 methylcytosine; DNA methylation; Epigenetic control; Eukaryotes; Gene regulation; N6 methyladenine

Indexed keywords

6 N METHYLADENINE; ADENINE DERIVATIVE; DNA; N5 METHYLADENINE; UNCLASSIFIED DRUG; 5 METHYLCYTOSINE; 6-METHYLADENINE; ADENINE; GENETIC MARKER;

ARTICLE; DNA METHYLATION; DNA MODIFICATION; EPIGENETICS; EUKARYOTE; GENE CONTROL; GENE EXPRESSION; GENETIC CORRELATION; MAMMAL; NONHUMAN; ANALOGS AND DERIVATIVES; CHEMISTRY; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETIC MARKER; GENETICS; SIGNAL TRANSDUCTION;

5-METHYLCYTOSINE; ADENINE; DNA METHYLATION; EPIGENESIS, GENETIC; EUKARYOTA; GENE EXPRESSION REGULATION; GENETIC MARKERS; SIGNAL TRANSDUCTION;

EID: 84944627506     PISSN: 02659247     EISSN: 15211878     Source Type: Journal    
DOI: 10.1002/bies.201500076     Document Type: Article

References (90)

1. Drablos F, Feyzi E, Aas PA, Vaagbo CB, et al. 2004. Alkylation damage in DNA and RNA-repair mechanisms and medical significance. DNA Repair 3: 1389-407.
2. Rydberg B, Lindahl T. 1982. Nonenzymatic methylation of DNA by the intracellular methyl group donor S-adenosyl-l-methionine is a potentially mutagenic reaction. EMBO J 1: 211-6.
3. Taverna P, Sedgwick B. 1996. Generation of an endogenous DNA-methylating agent by nitrosation in Escherichia coli. J Bacteriol 178: 5105-11.
4. Hecht SS. 1999. DNA adduct formation from tobacco-specific N-nitrosamines. Mutat Res 424: 127-42.
5. Margison GP, Santibanez-Koref MF. 2002. O6-alkylguanine-DNA alkyltransferase: role in carcinogenesis and chemotherapy. BioEssays 24: 255-66.
6. Weiss RB, Issell BF. 1982. The nitrosoureas: carmustine (BCNU) and lomustine (CCNU). Cancer Treat Rev 9: 313-30.
7. Ratel D, Ravanat JL, Berger F, Wion D. 2006. N6-methyladenine: the other methylated base of DNA. BioEssays 28: 309-15.
8. Wion D, Casadesus J. 2006. N6-methyl-adenine: an epigenetic signal for DNA-protein interactions. Nat Rev Microbiol 4: 183-92.
9. Vanyushin BF, Buryanov YI, Belozersky AN. 1971. Distribution of N6-methyladenine in DNA of T2 phage and its host Escherichia coli B. Nature 230: 25-7.
10. Janulaitis A, Klimasauskas S, Petrusyte M, Butkus V. 1983. Cytosine modification in DNA by BcnI methylase yields N4-methylcytosine. FEBS Lett 161: 131-4.
11. Ehrlich M, Wilson GG, Kuo KC, Gehrke CW. 1987. N4-methylcytosine as a minor base in bacterial DNA. J Bacteriol 169: 939-43.
12. Low DA, Weyand NJ, Mahan MJ. 2001. Roles of DNA adenine methylation in regulating bacterial gene expression and virulence. Infect Immun 69: 7197-204.
13. Lobner-Olesen A, Skovgaard O, Marinus MG. 2005. Dam methylation: coordinating cellular processes. Curr Opin Microbiol 8: 154-60.
14. Hanck T, Schmidt S, Fritz HJ. 1993. Sequence-specific and mechanism-based crosslinking of Dcm DNA cytosine-C5 methyltransferase of E. coli K-12 to synthetic oligonucleotides containing 5-fluoro-2'-deoxycytidine. Nucleic Acids Res 21: 303-9.
15. Marczynski GT, Shapiro L. 2002. Control of chromosome replication in caulobacter crescentus. Annu Rev Microbiol 56: 625-56.
16. Smith ZD, Meissner A. 2013. DNA methylation: roles in mammalian development. Nat Rev Genet 14: 204-20.
17. Hackett JA, Surani MA. 2013. DNA methylation dynamics during the mammalian life cycle. Philos Trans R Soc Lond B Biol Sci 368: 20110328.
18. Baylin SB, Jones PA. 2011. A decade of exploring the cancer epigenome - biological and translational implications. Nat Rev Cancer 11: 726-34.
19. Bromberg S, Pratt K, Hattman S. 1982. Sequence specificity of DNA adenine methylase in the protozoan Tetrahymena thermophila. J Bacteriol 150: 993-6.
20. Hattman S, Kenny C, Berger L, Pratt K. 1978. Comparative study of DNA methylation in three unicellular eucaryotes. J Bacteriol 135: 1156-7.
21. Barbeyron T, Kean K, Forterre P. 1984. DNA adenine methylation of GATC sequences appeared recently in the Escherichia coli lineage. J Bacteriol 160: 586-90.
22. Ashapkin VV, Kutueva LI, Vanyushin BF. 2002. The gene for domains rearranged methyltransferase (DRM2) in Arabidopsis thaliana plants is methylated at both cytosine and adenine residues. FEBS Lett 532: 367-72.
23. Fedoreyeva LI, Vanyushin BF. 2002. N(6)-Adenine DNA-methyltransferase in wheat seedlings. FEBS Lett 514: 305-8.
24. Kay PH, Pereira E, Marlow SA, Turbett G, et al. 1994. Evidence for adenine methylation within the mouse myogenic gene Myo-D1. Gene 151: 89-95.
25. Reyes EM, Camacho-Arroyo I, Nava G, Cerbon MA. 1997. Differential methylation in steroid 5 alpha-reductase isozyme genes in epididymis, testis, and liver of the adult rat. J Androl 18: 372-7.
26. Rae PM, Spear BB. 1978. Macronuclear DNA of the hypotrichous ciliate Oxytricha fallax. Proc Natl Acad Sci USA 75: 4992-6.
27. Gorovsky MA, Hattman S, Pleger GL. 1973. (6N) methyl adenine in the nuclear DNA of a eucaryote, Tetrahymena pyriformis. J Cell Biol 56: 697-701.
28. Gunthert U, Schweiger M, Stupp M, Doerfler W. 1976. DNA methylation in adenovirus, adenovirus-transformed cells, and host cells. Proc Natl Acade Sci USA 73: 3923-7.
29. Vanyushin BF, Alexandrushkina NI, Kirnos MD. 1988. N6-methyladenine in mitochondrial-DNA of higher-plants. FEBS Lett 233: 397-9.
30. Lu M, Campbell JL, Boye E, Kleckner N. 1994. SeqA: a negative modulator of replication initiation in E. coli. Cell 77: 413-26.
31. Collier J, McAdams HH, Shapiro L. 2007. A DNA methylation ratchet governs progression through a bacterial cell cycle. Proc Natl Acad Sci USA 104: 17111-6.
32. Messer W, Noyer-Weidner M. 1988. Timing and targeting: the biological functions of Dam methylation in E. coli. Cell 54: 735-7.
33. Julio SM, Heithoff DM, Provenzano D, Klose KE, et al. 2001. DNA adenine methylase is essential for viability and plays a role in the pathogenesis of Yersinia pseudotuberculosis and Vibrio cholerae. Infect Immun 69: 7610-5.
34. Ratel D, Ravanat JL, Charles MP, Platet N, et al. 2006. Undetectable levels of N6-methyl adenine in mouse DNA: cloning and analysis of PRED28, a gene coding for a putative mammalian DNA adenine methyltransferase. FEBS Lett 580: 3179-84.
35. Zhang G, Huang H, Liu D, Cheng Y, et al. 2015. N(6)-methyladenine DNA modification in Drosophila. Cell 161: 893-906.
36. Greer EL, Blanco MA, Gu L, Sendinc E, et al. 2015. DNA methylation on N(6)-adenine in C. elegans. Cell 161: 868-78.
37. Fu Y, Luo GZ, Chen K, Deng X, et al. 2015. N(6)-methyldeoxyadenosine marks active transcription start sites in chlamydomonas. Cell 161: 879-92.
38. Guibert S, Forne T, Weber M. 2009. Dynamic regulation of DNA methylation during mammalian development. Epigenomics 1: 81-98.
39. Gopalakrishnan S, Van Emburgh BO, Robertson KD. 2008. DNA methylation in development and human disease. Mutat Res 647: 30-8.
40. Xu SY, Xiao JP, Ettwiller L, Holden M, et al. 1998. Cloning and expression of the ApaLI, NspI, NspHI, SacI, ScaI, and SapI restriction-modification systems in Escherichia coli. Mol Gen Genet 260: 226-31.
41. Bhutani N, Burns DM, Blau HM. 2011. DNA demethylation dynamics. Cell 146: 866-72.
42. Chen T, Li E. 2006. Establishment and maintenance of DNA methylation patterns in mammals. Curr Top Microbiol Immunol 301: 179-201.
43. Kohli RM, Zhang Y. 2013. TET enzymes, TDG and the dynamics of DNA demethylation. Nature 502: 472-9.
44. Bogdanovic O, Veenstra GJ. 2009. DNA methylation and methyl-CpG binding proteins: developmental requirements and function. Chromosoma 118: 549-65.
45. Jones PA, Liang G. 2009. Rethinking how DNA methylation patterns are maintained. Nat Rev Genet 10: 805-11.
46. Goll MG, Bestor TH. 2005. Eukaryotic cytosine methyltransferases. Annu Rev Biochem 74: 481-514.
47. Kriaucionis S, Heintz N. 2009. The nuclear DNA base 5-hydroxymethylcytosine is present in Purkinje neurons and the brain. Science 324: 929-30.
48. Tahiliani M, Koh KP, Shen Y, Pastor WA, et al. 2009. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner T ET1. Science 324: 930-5.
49. Zhu JK. 2009. Active DNA demethylation mediated by DNA glycosylases. Annu Rev Genet 43: 143-66.
50. Fritz EL, Papavasiliou FN. 2010. Cytidine deaminases: AIDing DNA demethylation?. Genes Dev 24: 2107-14.
51. He YF, Li BZ, Li Z, Liu P, et al. 2011. Tet-mediated formation of 5-carboxylcytosine and its excision by TDG in mammalian DNA. Science 333: 1303-7.
52. Ito S, Shen L, Dai Q, Wu SC, et al. 2011. Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine. Science 333: 1300-3.
53. Maiti A, Drohat AC. 2011. Thymine DNA glycosylase can rapidly excise 5-formylcytosine and 5-carboxylcytosine: potential implications for active demethylation of CpG sites. J Biol Chem 286: 35334-8.
54. Rai K, Huggins IJ, James SR, Karpf AR, et al. 2008. DNA demethylation in zebrafish involves the coupling of a deaminase, a glycosylase, and gadd45. Cell 135: 1201-12.
55. Cortellino S, Xu J, Sannai M, Moore R, et al. 2011. Thymine DNA glycosylase is essential for active DNA demethylation by linked deamination-base excision repair. Cell 146: 67-79.
56. Wijesinghe P, Bhagwat AS. 2012. Efficient deamination of 5-methylcytosines in DNA by human APOBEC3A, but not by AID or APOBEC3G. Nucleic Acids Res 40: 9206-17.
57. Walsh CP, Xu GL. 2006. Cytosine methylation and DNA repair. Curr Top Microbiol Immunol 301: 283-315.
58. Pfeifer GP. 2000. P53 mutational spectra and the role of methylated CpG sequences. Mutat Res 450: 155-66.
59. Pfeifer GP. 2006. Mutagenesis at methylated CpG sequences. Curr Top Microbiol Immunol 301: 259-81.
60. Lyko F, Ramsahoye BH, Jaenisch R. 2000. DNA methylation in Drosophila melanogaster. Nature 408: 538-40.
61. Raddatz G, Guzzardo PM, Olova N, Fantappie MR, et al. 2013. Dnmt2-dependent methylomes lack defined DNA methylation patterns. Proc Natl Acad Sci USA 110: 8627-31.
62. Takayama S, Dhahbi J, Roberts A, Mao G, et al. 2014. Genome methylation in D. melanogaster is found at specific short motifs and is independent of DNMT2 activity. Genome Res 24: 821-30.
63. Boffelli D, Takayama S, Martin DI. 2014. Now you see it: genome methylation makes a comeback in Drosophila. BioEssays 36: 1138-44.
64. Simpson VJ, Johnson TE, Hammen RF. 1986. Caenorhabditis elegans DNA does not contain 5-methylcytosine at any time during development or aging. Nucleic Acids Res 14: 6711-9.
65. Pratt K, Hattman S. 1981. Deoxyribonucleic-acid methylation and chromatin organization in Tetrahymena thermophila. Mol Cell Biol 1: 600-8.
66. Capowski EE, Wells JM, Harrison GS, Karrer KM. 1989. Molecular analysis of N6-methyladenine patterns in Tetrahymena thermophila nuclear DNA. Mol Cell Biol 9: 2598-605.
67. Harrison GS, Findly RC, Karrer KM. 1986. Site-specific methylation of adenine in the nuclear genome of a eucaryote, Tetrahymena thermophila. Mol Cell Biol 6: 2364-70.
68. Karrer KM, VanNuland TA. 2002. Methylation of adenine in the nuclear DNA of Tetrahymena is internucleosomal and independent of histone H1. Nucleic Acids Res 30: 1364-70.
69. Gutierrez JC, Callejas S, Borniquel S, Martin-Gonzalez A. 2000. DNA methylation in ciliates: implications in differentiation processes. Int Microbiol 3: 139-46.
70. Cummings DJ, Tait A, Goddard JM. 1974. Methylated bases in DNA from Paramecium aurelia. Biochim Biophys Acta 374: 1-1.
71. Ammermann D, Steinbruck G, Baur R, Wohlert H. 1981. Methylated bases in the DNA of the ciliate Stylonychia mytilus. Eur J Cell Biol 24: 154-6.
72. Que QD, Zhang YP, Nelson M, Ropp S, et al. 1997. Chlorella virus SC-1A encodes at least five functional and one nonfunctional DNA methyltransferases. Gene 190: 237-44.
73. Kunii M, Kanda M, Nagano H, Uyeda I, et al. 2004. Reconstruction of putative DNA virus from endogenous rice tungro bacilliform virus-like sequences in the rice genome: implications for integration and evolution. BMC Genomics 5: 80.
74. Liu RF, Koyanagi KO, Chen SL, Kishima Y. 2012. Evolutionary force of AT-rich repeats to trap genomic and episomal DNAs into the rice genome: lessons from endogenous pararetrovirus. Plant J 72: 817-28.
75. Kamat SS, Fan H, Sauder JM, Burley SK, et al. 2011. Enzymatic deamination of the epigenetic base N-6-methyladenine. J Am Chem Soc 133: 2080-3.
76. Lopez CMR, Lloyd AJ, Leonard K, Wilkinson MJ. 2012. Differential effect of three base modifications on DNA thermostability revealed by high resolution melting. Anal Chem 84: 7336-42.
77. Song QX, Ding ZD, Liu JH, Li Y, et al. 2013. Theoretical study on the binding mechanism between N6-methyladenine and natural DNA bases. J Mol Model 19: 1089-98.
78. Diekmann S. 1987. DNA methylation can enhance or induce DNA curvature. EMBO J 6: 4213-7.
79. Franchini DM, Schmitz KM, Petersen-Mahrt SK. 2012. 5-methylcytosine DNA demethylation: more than losing a methyl group. Annu Rev Genet 46: 419-41.
80. Hendrich B, Bird A. 1998. Identification and characterization of a family of mammalian methyl-CpG binding proteins. Mol Cell Biol 18: 6538-47.
81. Nan XS, Ng HH, Johnson CA, Laherty CD, et al. 1998. Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 393: 386-9.
82. Zhang Y, Ng HH, Erdjument-Bromage H, Tempst P, et al. 1999. Analysis of the NuRD subunits reveals a histone deacetylase core complex and a connection with DNA methylation. Genes Dev 13: 1924-35.
83. Ng HH, Jeppesen P, Bird A. 2000. Active repression of methylated genes by the chromosomal protein M BD1. Mol Cell Biol 20: 1394-406.
84. Lyst MJ, Ekiert R, Ebert DH, Merusi C, et al. 2013. Rett syndrome mutations abolish the interaction of MeCP2 with the NCoR/SMRT co-repressor. Nat Neurosci 16: 898-902.
85. Zoghbi HY, Amir RE, Wan M, Lee SS, et al. 2000. Rett syndrome is caused by mutations in the X-linked MECP2 gene encoding methyl-CpG-binding protein. Am J Hum Genet 66: 1723.
86. Amir RE, Van den Veyver IB, Wan M, Tran CQ, et al. 1999. Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2. Nat Genet 23: 185-8.
87. Boye E, Lobner-Olesen A, Skarstad K. 2000. Limiting DNA replication to once and only once. EMBO Rep 1: 479-83.
88. Lu M, Campbell JL, Boye E, Kleckner N. 1994. Seqa - a negative modulator of replication initiation in Escherichia coli. Cell 77: 413-26.
89. Wang X, Lu Z, Gomez A, Hon GC, et al. 2014. N6-methyladenosine-dependent regulation of messenger RNA stability. Nature 505: 117-20.
90. Wang X, Zhao BS, Roundtree IA, Lu Z, et al. 2015. N(6)-methyladenosine modulates messenger RNA translation efficiency. Cell 161: 1388-99.