N6-methyladenine: The other methylated base of DNA

BioEssays

Volumn 28, Issue 3, 2006, Pages 309-315

  Ratel, David ^a   Ravanat, Jean Luc ^b   Berger, François ^a   Wion, Didier ^a  

^a HÔPITAL MICHALLON   (France)

^b UNIV GRENOBLE ALPES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

6 N METHYLADENINE; BACTERIAL DNA; DNA ADENINE METHYLTRANSFERASE; PLANT DNA;

DNA METHYLATION; DNA REPAIR; DNA REPLICATION; DNA TRANSPOSITION; EUKARYOTIC CELL; GENE EXPRESSION; PROKARYOTE; REVIEW; VIRULENCE;

ADENINE; ANIMALS; DNA; DNA METHYLATION; EUKARYOTIC CELLS; PHYLOGENY;

BACTERIA (MICROORGANISMS); EUKARYOTA; MAMMALIA; PROKARYOTA; PROTISTA;

EID: 33645389087     PISSN: 02659247     EISSN: None     Source Type: Journal    
DOI: 10.1002/bies.20342     Document Type: Review

References (91)

1. Doskocil J, Sormo'Va Z. 1965. The Occurrence of 5-Methylcytosine in Bacterial Deoxyribonucleic Acids. Biochim Biophys Acta 95:513-515.
2. Dunn DB, Smith JD. 1958. The occurrence of 6-methylaminopurine in deoxyribonucleic acids. Biochem J 68:627-636.
3. Ehrlich M, Gama-Sosa MA, Carreira LH, Ljungdahl LG, Kuo KC, et al. 1985. DNA methylation in thermophilic bacteria: N4-methylcytosine, 5-methylcytosine, and N6-methyladenine. Nucleic Acids Res 13:1399-1412.
4. Reisenauer A, Shapiro L. 2002. DNA methylation affects the cell cycle transcription of the CtrA global regulator in Caulobacter. Embo J 21:4969-4977.
5. Robertson GT, Reisenauer A, Wright R, Jensen RB, Jensen A, et al. 2000. The Brucella abortus CcrM DNA methyltransferase is essential for viability, and its overexpression attenuates intracellular replication in murine macrophages. J Bacteriol 182:3482-3489.
6. Stephens C, Reisenauer A, Wright R, Shapiro L, 1996. A cell cycle-regulated bacterial DNA methyltransferase is essential for viability. Proc Natl Acad Sci USA 93:1210-1214.
7. Wright R, Stephens C, Shapiro L. 1997. The CcrM DNA methyltransferase is widespread in the alpha subdivision of proteobacteria, and its essential functions are conserved in Rhizobium meliloti and Caulobacter crescentus. J Bacteriol 179:5869-5877.
8. Kahng LS, Shapiro L. 2001. The CcrM DNA methyltransferase of Agrobacterium tumefaciens is essential, and its activity is cell cycle regulated. J Bacteriol 183:3065-3075.
9. Julio SM, Heithoff DM, Provenzano D, Klose KE, Sinsheimer RL, 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 69:7610-7615.
10. 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 532:367-372.
11. Kay PH, Pereira E, Marlow SA, Turbett G, Mitchell CA, et al. 1994. Evidence for adenine methylation within the mouse myogenic gene Myo-D1. Gene 151:89-95.
12. 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 18:372-377.
13. Pintor-Toro JA. 1987. Adenine methylation in zein genes. Biochem Biophys Res Commun 147:1082-1087.
14. Cummings DJ, Tait A, Goddard JM. 1974. Methylated bases in DNA from Paramecium aurelia. Biochim Biophys Acta 374:1-11.
15. Bertani G, Weigle JJ. 1953. Host controlled variation in bacterial viruses. J Bacteriol 65:113-121.
16. Luria SE, Human ML. 1952. A nonhereditary, host-induced variation of bacterial viruses. J Bacteriol 64:557-569.
17. Schlagman SL, Hattman S. 1983. Molecular cloning of a functional dam gene coding for phage T4 DNA adenine methylase. Gene 22:139-156.
18. Magrini V, Salmi D, Thomas D, Herbert SK, Hartzell PL, et al. 1997. Temperate Myxococcus xanthus phage Mx8 encodes a DNA adenine methylase. Mox. J Bacteriol 179:4254-4263.
19. Baranyi U, Klein R, Lubitz W, Kruger DH, Witte A. 2000. The archaeal halophilic virus-encoded Dam-like methyltransferase M. phiCh1-I methylates adenine residues and complements dam mutants in the low salt environment of Escherichia coli. Mol Microbiol 35:1168-1179.
20. Arnold HP, Ziese U, Zillig W. 2000. SNDV, a novel virus of the extremely thermophilic and acidophilic archaeon Sulfolobus. Virology 272:409-416.
21. Naito T, Kusano K, Kobayashi I. 1995. Selfish behavior of restriction-modification systems. Science 267:897-899.
22. LodwicK D, Ross HN, Harris JE, Almond JW, Grant WD. 1986. dam methylation in the archaebacteria. J Gen Microbiol 132:3055-3059.
23. Barbeyron T, Kean K, Forterre P. 1984. DNA adenine methylation of GATC sequences appeared recently in the Escherichia coli lineage. J Bacteriol 160:586-590.
24. Reisenauer A, Kahng LS, McCollum S, Shapiro L. 1999. Bacterial DNA methylation: a cell cycle regulator? J Bacteriol 181:5135-5139.
25. Lu M, Campbell JL, Boye E, Kleckner N. 1994. SeqA: a negative modulator of replication initiation in E. coli. Cell 77:413-426.
26. Laengle-Rouault F, Maenhaut-Michel G, Radman M. 1986. GATC sequence and mismatch repair in Escherichia coli. Embo J 5:2009-2013.
27. Barras F, Marinus MG. 1989. The great GATC: DNA methylation in E. coli. Trends Genet 5:139-143.
28. Lobner-Olesen A, Skovgaard O, Marinus MG. 2005. Dam methylation: coordinating cellular processes. Curr Opin Microbiol 8:154-160.
29. Casadesus J, D'Ari R. 2002. Memory in bacteria and phage. Bioessays 24:512-518.
30. Roberts D, Hoopes BC, McClure WR, Kleckner N. 1985. IS10 transposition is regulated by DNA adenine methylation. Cell 43:117-130.
31. Zweiger G, Marczynski G, Shapiro L. 1994. A Caulobacter DNA methyltransferase that functions only in the predivisional cell. J Mol Biol 235:472-485.
32. Oshima T, Wada C, Kawagoe Y, Ara T, Maeda M, et al. 2002. Genome-wide analysis of deoxyadenosine methyltransferase-mediated control of gene expression in Escherichia coli. Mol Microbiol 45:673-695.
33. Laub MT, Chen SL, Shapiro L, McAdams HH. 2002. Genes directly controlled by CtrA, a master regulator of the Caulobacter cell cycle. Proc Natl Acad Sci USA 99:4632-4637.
34. Boye E, Lobner-Olesen A. 1990. The role of dam methyltransferase in the control of DNA replication in E. coli. Cell 62:981-989.
35. Braaten BA, Nou X, Kaltenbach LS, Low DA. 1994. Methylation patterns in pap regulatory DNA control pyelonephritis-associated pili phase variation in E. coli. Cell 76:577-588.
36. Heithoff DM, Sinsheimer RL, Low DA, Mahan MJ. 1999. An essential role for DNA adenine methylation in bacterial virulence. Science 284:967-970.
37. Garcia-Del Portillo F, Pucciarelli MG, Casadesus J. 1999. DNA adenine methylase mutants of Salmonella typhimurium show defects in protein secretion, cell invasion, and M cell cytotoxicity. Proc Natl Acad Sci USA 96:11578-11583.
38. Low DA, Weyand NJ, Mahan MJ. 2001. Roles of DNA adenine methylation in regulating bacterial gene expression and virulence. Infect Immun 69:7197-7204.
39. Mashhoon N, Carroll M, Pruss C, Eberhard J, Ishikawa S, et al. 2004. Functional characterization of Escherichia coli DNA adenine methyltransferase, a novel target for antibiotics. J Biol Chem 279:52075-52081.
40. Wahnon DC, Shier VK, Benkovic SJ. 2001. Mechanism-based inhibition of an essential bacterial adenine DNA methyltransferase: rationally designed antibiotics. J Am Chem Soc 123:976-977.
41. Hattman S, Kenny C, Berger L, Pratt K. 1978. Comparative study of DNA methylation in three unicellular eucaryotes. J Bacteriol 135:1156-1157.
42. Hattman S. 2005. DNA-[adenine] methylation in lower eukaryotes. Biochemistry (Mosc) 70:550-558.
43. Rae PM, Spear BB. 1978. Macronuclear DNA of the hypotrichous ciliate Oxytricha fallax. Proc Natl Acad Sci USA 75:4992-4996.
44. Pratt K, Hattman S. 1981. Deoxyribonucleic acid methylation and chromatin organization in Tetrahymena thermophila. Mol Cell Biol 1:600-608.
45. Capowski EE, Wells JM, Harrison GS, Karrer KM. 1989. Molecular analysis of N6-methyladenine patterns in Tetrahymena thermophila nuclear DNA. Mol Cell Biol 9:2598-2605.
46. Harrison GS, Findly RC, Karrer KM. 1986. Site-specific methylation of adenine in the nuclear genome of a eucaryote, Tetrahymena thermophila. Mol Cell Biol 6:2364-2370.
47. Gutierrez JC, Callejas S, Borniquel S, Martin-Gonzalez A. 2000. DNA methylation in ciliates: implications in differentiation processes. Int Microbiol 3:139-146.
48. Gorovsky MA, Hattman S, Pleger GL. 1973. (6 N)methyl adenine in the nuclear DNA of a eucaryote, Tetrahymena pyriformis. J Cell Biol 56:697-701.
49. Zhang Y, Nelson M, Nietfeldt JW, Burbank DE, Van Etten JL. 1992. Characterization of Chlorella virus PBCV-1 CviAII restriction and modification system. Nucleic Acids Res 20:5351-5356.
50. Que Q, Zhang Y, Nelson M, Ropp S, Burbank DE, et al. 1997. Chlorella virus SC-1A encodes at least five functional and one nonfunctional DNA methyltransferases. Gene 190:237-244.
51. Karrer KM, VanNuland TA. 2002. Methylation of adenine in the nuclear DNA of Tetrahymena is internucleosomal and independent of histone H1. Nucleic Acids Res 30:1364-1370.
52. Zhu CM, Henney HR Jr. 1990. DNA methylation pattern during the encystment of Physarum flavicomum. Biochem Cell Biol 68:944-948.
53. Nakayama S, Endoh H. 2003. Preferential cleavage of Paramecium DNA mediated by the C. elegans Tc1 transposase in vitro. Genes Genet Syst 78:391-398.
54. Gunthert U, Schweiger M, Stupp M, Doerfler W. 1976. DNA methylation in adenovirus, adenovirus-transformed cells, and host cells. Proc Natl Acad Sci USA 73:3923-3927.
55. Lawley PD, Crathorn AR, Shah SA, Smith BA. 1972. Biomethylation of deoxyribonucleic acid in cultured human tumour cells (HeLa). Methylated bases other than 5-methylcytosine not detected. Biochem J 128:133-138.
56. Vanyushin BF, Tkacheva SG, Belozersky AN. 1970. Rare bases in animal DNA. Nature 225:948-949.
57. Poole A, Penny D, Sjoberg BM. 2001. Confounded cytosine! Tinkering and the evolution of DNA. Nat Rev Mol Cell Biol 2:147-151.
58. Bestor TH. 2000. The DNA methyltransferases of mammals. Hum Mol Genet 9:2395-2402.
59. Yoder JA, Walsh CP, Bestor TH. 1997. Cytosine methylation and the ecology of intragenomic parasites. Trends Genet 13:335-340.
60. Ngernprasirtsiri J, Akazawa T. 1990. Modulation of DNA methylation and gene expression in cultured sycamore cells treated by hypomethylating base analog. Eur J Biochem 194:513-520.
61. Vanyushin BF, Alexandrushkina NI, Kirnos MD. 1988. N6-methyladenine in mitochondrial DNA of higher plants. FEBS Lett 233:397-399.
62. Dhar MS, Pethe W, Gupta VS, Ranjekar PK. 1990. Predominance and tissue specificity of adenine methylation in rice. Theor Appl Genet 80:402-408.
63. Adams RL, McKay EL, Craig LM, Burdon RH. 1979. Methylation of mosquito DNA. Biochim Biophys Acta 563:72-81.
64. Fedoreyeva LI, Vanyushin BF. 2002. N(6)-Adenine DNA-methyltransferase in wheat seedlings. FEBS Lett 514:305-308.
65. Tronche F, Rollier A, Bach I, Weiss MC, Yaniv M. 1989. The rat albumin promoter: cooperation with upstream elements is required when binding of APF/HNF1 to the proximal element is partially impaired by mutation or bacterial methylation. Mol Cell Biol 9:4759-4766.
66. Knebel D, Doerfler W. 1986. N6-methyldeoxyadenosine residues at specific sites decrease the activity of the E1A promoter of adenovirus type 12 DNA. J Mol Biol 189:371-375.
67. Truss M, Bartsch J, Chalepakis G, Beato M. 1992. Artificial steroid hormone response element generated by dam-methylation. Nucleic Acids Res 20:1483-1486.
68. Allamane S, Jourdes P, Ratel D, Vicat JM, Dupre I, et al. 2000. Bacterial DNA methylation and gene transfer efficiency. Biochem Biophys Res Commun 276:1261-1264.
69. Berger F, Canova C, Benabid AL, Wion D. 1999. Are sequences of plasmid DNA used in gene therapy erroneous? Nat Biotechnol 17:517.
70. Graham MW, Larkin PJ. 1995. Adenine methylation at dam sites increases transient gene expression in plant cells. Transgenic Res 4:324-331.
71. Sugimoto K, Takeda S, Hirochika H. 2003. Transcriptional activation mediated by binding of a plant GATA-type zinc finger protein AGP1 to the AG-motif (AGATCCAA) of the wound-inducible Myb gene NtMyb2. Plant J 36:550-564.
72. Rogers JC, Rogers SW. 1995. Comparison of the effects of N6-methyldeoxyadenosine and N5-methyldeoxycytosine on transcription from nuclear gene promoters in barley. Plant J 7:221-233.
73. Ratel D, Boisseau S, Davidson SM, Ballester B, Mathieu J, et al. 2001. The bacterial nucleoside N(6)-methyldeoxyadenosine induces the differentiation of mammalian tumor cells. Biochem Biophys Res Commun 285:800-805.
74. Charles MP, Ravanat JL, Adamski D, D'Orazi G, Cadet J, et al. 2004. N(6)-Methyldeoxyadenosine, a nucleoside commonly found in prokaryotes, induces C2C12 myogenic differentiation. Biochem Biophys Res Commun 314:476-482.
75. Gowher H, Leismann O, Jeltsch A. 2000. DNA of Drosophila melanogaster contains 5-methylcytosine. Embo J 19:6918-6923.
76. Tweedie S, Ng HH, Barlow AL, Turner BM, Hendrich B, et al. 1999. Vestiges of a DNA methylation system in Drosophila melanogaster? Nat Genet 23:389-390.
77. Wienhues U, Doerfler W. 1985. Lack of evidence for methylation of parental and newly synthesized adenovirus type 2 DNA in productive infections. J Virol 56:320-324.
78. Pollack Y, Kogan N, Golenser J. 1991. Plasmodium falciparum: evidence for a DNA methylation pattern. Exp Parasitol 72:339-344.
79. Cairns J. 1975. Mutation selection and the natural history of cancer. Nature 255:197-200.
80. Merok JR, Lansita JA, Tunstead JR, Sherley JL. 2002. Cosegregation of chromosomes containing immortal DNA strands in cells that cycle with asymmetric stem cell kinetics. Cancer Res 62:6791-6795.
81. Potten CS, Owen G, Booth D. 2002. Intestinal stem cells protect their genome by selective segregation of template DNA strands. J Cell Sci 115:2381-2388.
82. Frelon S, Douki T, Ravanat JL, Pouget JP, Tornabene C, et al. 2000. High-performance liquid chromatography-tandem mass spectrometry measurement of radiation-induced base damage to isolated and cellular DNA. Chem Res Toxicol 13:1002-1010.
83. Guetens G, De Boeck G, Highley M, van Oosterom AT, de Bruijn EA. 2002. Oxidative DNA damage: biological significance and methods of analysis. Crit Rev Clin Lab Sci 39:331-457.
84. Jeltsch A, Christ F, Fatemi M, Roth M. 1999. On the substrate specificity of DNA methyltransferases. adenine-N6 DNA methyltransferases also modify cytosine residues at position N4. J Biol Chem 274:19538-19544.
85. Shorning BY, Vanyushin BF. 2001. Putative DNA-(amino)methyltransferases in eucaryotes. Biochemistry (Mosc) 66:753-762.
86. Antonarakis SE. 1998. 10 years of Genomics, chromosome 21, and Down syndrome. Genomics 51:1-16.
87. Malone T, Blumenthal RM, Cheng X. 1995. Structure-guided analysis reveals nine sequence motifs conserved among DNA amino-methyltransferases, and suggests a catalytic mechanism for these enzymes. J Mol Biol 253:618-632.
88. Schofield MJ, Hsieh P. 2003. DNA mismatch repair: molecular mechanisms and biological function. Annu Rev Microbiol 57:579-608.
89. Degnen ST, Morris NR. 1973. Deoxyribonucleic acid methylation and development in Caulobacter bacteroides. J Bacteriol 116:48-53.
90. Srivastava R, Gopinathan KP, Ramakrishnan T. 1981. Deoxyribonucleic acid methylation in mycobaoteria. J Bacteriol 148:716-719.
91. Razin A, Razin S. 1980. Methylated bases in mycoplasmal DNA. Nucleic Acids Res 8:1383-1390.