Repair of alkylated DNA: Recent advances

DNA Repair

Volumn 6, Issue 4, 2007, Pages 429-442

  Sedgwick, Barbara ^a   Bates, Paul A ^a   Paik, Johanna ^b   Jacobs, Susan C ^a   Lindahl, Tomas ^a  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^b FLORIDA STATE UNIVERSITY   (United States)

Author keywords

1 methyladenine; 3 methyladenine; AlkB; DNA dioxygenases; DNA glycosylases

Indexed keywords

1 METHYLADENINE; 3 METHYLADENINE; CYSTEINE; DNA; DNA BASE; DNA GLYCOSYLTRANSFERASE; FORMALDEHYDE; METHYLTRANSFERASE;

ARTICLE; CRYSTAL STRUCTURE; CYTOTOXICITY; DEMETHYLATION; DNA ALKYLATION; DNA BINDING; DNA DAMAGE; DNA REPAIR; DNA STRUCTURE; EXCISION REPAIR; MUTAGENESIS; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL;

ALKYLATING AGENTS; ALKYLATION; AMINO ACID SEQUENCE; ANIMALS; CRYSTALLOGRAPHY, X-RAY; DNA; DNA METHYLATION; DNA REPAIR; DNA REPAIR ENZYMES; HUMANS; MICE; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION; S-ADENOSYLMETHIONINE;

MAMMALIA;

EID: 33847688859     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2006.10.005     Document Type: Article

References (107)

1. Beckman K.B., and Ames B.N. Oxidative decay of DNA. J. Biol. Chem. 272 (1997) 19633-19636
2. Lombard D.B., Chua K.F., Mostoslavsky R., Franco S., Gostissa M., and Alt F.W. DNA repair, genome stability, and aging. Cell 120 (2005) 497-512
3. Lindahl T. Instability and decay of the primary structure of DNA. Nature 362 (1993) 709-715
4. De Bont R., and van Larebeke N. Endogenous DNA damage in humans: a review of quantitative data. Mutagenesis 19 (2004) 169-185
5. Galperin M.Y., Moroz O.V., Wilson K.S., and Murzin A.G. House cleaning, a part of good housekeeping. Mol. Microbiol 59 (2006) 5-19
6. 6-methylguanine-DNA alkyltransferase deficient cells. Carcinogenesis 18 (1997) 1561-1567
7. Rydberg B., and Lindahl T. Nonenzymatic methylation of DNA by the intracellular methyl group donor S-adenosyl-l-methionine is a potentially mutagenic reaction. EMBO J. 1 (1982) 211-216
8. Eloranta T.O. Tissue distribution of S-adenosylmethionine and S-adenosylhomocysteine in the rat. Effect of age, sex and methionine administration on the metabolism of S-adenosylmethionine, S-adenosylhomocysteine and polyamines. Biochem. J. 166 (1977) 521-529
9. Lawley P.D., and Brookes P. Further studies on the alkylation of nucleic acids and their constituent nucleotides. Biochem. J. 89 (1963) 127-138
10. Bodell W.J., and Singer B. Influence of hydrogen bonding in DNA and polynucleotides on reaction of nitrogens and oxygens toward ethylnitrosourea. Biochemistry 18 (1979) 2860-2863
11. L. Aravind, E.V. Koonin, The alpha/beta fold uracil DNA glycosylases: a common origin with diverse fates, Genome Biol. 1 (2000) RESEARCH0007.0001-0007.0008.
12. Singer B., and Grunberger D. Molecular Biology of Mutagens and Carcinogens: Intrinsic Properties of Nucleic Acids (1983), Plenum Press, New York pp. 15-44
13. Lau A.Y., Scharer O.D., Samson L., Verdine G.L., and Ellenberger T. Crystal structure of a human alkylbase-DNA repair enzyme complexed to DNA: mechanisms for nucleotide flipping and base excision. Cell 95 (1998) 249-258
14. Banerjee A., Santos W.L., and Verdine G.L. Structure of a DNA glycosylase searching for lesions. Science 311 (2006) 1153-1157
15. Blainey P.C., van Oijen A.M., Banerjee A., Verdine G.L., and Xie X.S. A base-excision DNA-repair protein finds intrahelical lesion bases by fast sliding in contact with DNA. Proc. Natl. Acad. Sci. USA 103 (2006) 5752-5757
16. O'Brien P., and Ellenberger T. Human alkyladenine DNA glycosylase uses acid-base catalysis for selective excision of damaged purines. Biochemistry 42 (2003) 12418-12429
17. Asaeda A., Ide H., Asagoshi K., Matsuyama S., Tano K., Murakami A., Takamori Y., and Kubo K. Substrate specificity of human methylpurine DNA N-glycosylase. Biochemistry 39 (2000) 1959-1965
18. Alseth I., Rognes T., Lindback T., Solberg I., Robertsen K., Kristiansen K.I., Mainieri D., Lillehagen L., Kolsto A.B., and Bjoras M. A new protein superfamily includes two novel 3-methyladenine DNA glycosylases from Bacillus cereus, AlkC and AlkD. Mol. Microbiol. 59 (2006) 1602-1609
19. O'Brien P.J., and Ellenberger T. Dissecting the broad substrate specificity of human 3-methyladenine-DNA glycosylase. J. Biol. Chem. 279 (2004) 9750-9757
20. Berdal K.G., Johansen R.F., and Seeberg E. Release of normal bases from intact DNA by a native DNA repair enzyme. EMBO J. 17 (1998) 363-367
21. Glassner B.J., Rasmussen L.J., Najarian M.T., Posnick L.M., and Samson L.D. Generation of a strong mutator phenotype in yeast by imbalanced base excision repair. Proc. Natl. Acad. Sci. USA 95 (1998) 9997-10002
22. Watanabe S., Ichimura T., Fujita N., Tsuruzoe S., Ohki I., Shirakawa M., Kawasuji M., and Nakao M. Methylated DNA-binding domain 1 and methylpurine-DNA glycosylase link transcriptional repression and DNA repair in chromatin. Proc. Natl. Acad. Sci. USA 100 (2003) 12859-12864
23. Likhite V.S., Cass E.I., Anderson S.D., Yates J.R., and Nardulli A.M. Interaction of estrogen receptor alpha with 3-methyladenine DNA glycosylase modulates transcription and DNA repair. J. Biol. Chem. 279 (2004) 16875-16882
24. Engelward B.P., Dreslin A., Christensen J., Huszar D., Kurahara C., and Samson L. Repair-deficient-3-methyl adenine DNA glycosylase homozygous mutant mouse cells have increased sensitivity to alkylation-induced chromosome damage and cell killing. EMBO J. 15 (1996) 945-952
25. Engelward B.P., Weeda G., Wyatt M.D., Broekhof J.L.M., de Wit J., Donker I., Allan J.M., Golds B., Hoeijmakers J.H.J., and Samson L.D. Base excision repair deficient mice lacking the Aag alkyladenine DNA glycosylase. Proc. Natl. Acad. USA 94 (1997) 13087-13092
26. Elder R.H., Jansen J.G., Weeks R.J., Willington M.A., Deans B., Watson A.J., Mynett K.J., Bailey J.A., Cooper D.P., Rafferty J.A., Heeran M.C., Wijnhoven S.W.P., van Zeeland A.A., and Margison G.P. Alkylpurine-DNA-N-glycosylase knockout mice show increased susceptibility to induction of mutations by methyl methanesulfonate. Mol. Cell. Biol. 18 (1998) 5828-5837
27. Roth R.B., and Samson L. 3-methyladenine DNA glycosylase-deficient Aag null mice display unexpected bone marrow alkylation resistance. Cancer Res. 62 (2002) 656-660
28. Friedberg E., Walker G., Siede W., Wood R.D., Schultz R.A., and Ellenberger T. DNA Repair and Mutagenesis (2006), ASM Press, Washington, D.C. pp. 141-157
29. Mishina Y., Duguid E.M., and He C. Direct reversal of DNA alkylation damage. Chem. Rev. 106 (2006) 215-232
30. Liu L., and Gerson S.L. Targeted modulation of MGMT: clinical implications. Clin. Cancer Res. 12 (2006) 328-331
31. Daniels D.S., Woo T.T., Luu K.X., Noll D.M., Clarke N.D., Pegg A.E., and Tainer J.A. DNA binding and nucleotide flipping by the human DNA repair protein AGT. Nat. Struct. Mol. Biol. 11 (2004) 714-720
32. Fang Q., Kanugula S., and Pegg A.E. Function of domains of human O6-alkylguanine-DNA alkyltransferase. Biochemistry 44 (2005) 15396-15405
33. Pearson S.J., Ferguson J., Santibanez-Koref M., and Margison G.P. Inhibition of O6-methylguanine-DNA methyltransferase by an alkyltransferase-like protein from Escherichia coli. Nucl. Acids Res. 33 (2005) 3837-3844
34. Mukai T., and Sekiguchi M. Gene silencing in phenomena related to DNA repair. Oncogene 21 (2002) 9033-9042
35. Esteller M., and Herman J.G. Generating mutations but providing chemosensitivity: the role of O6-methylguanine DNA methyltransferase in human cancer. Oncogene 23 (2004) 1-8
36. Lindahl T., Sedgwick B., Sekiguchi M., and Nakabeppu Y. Regulation and expression of the adaptive response to alkylating agents. Ann. Rev. Biochem. 57 (1988) 133-157
37. Teo I., Sedgwick B., Kilpatrick M.W., McCarthy T.V., and Lindahl T. The intracellular signal for induction of resistance to alkylating agents in E.coli. Cell 45 (1986) 315-324
38. Myers L.C., Terranova M.P., Ferentz A.E., Wagner G., and Verdine G.L. Repair of DNA methylphosphotriesters through a metalloactivated cysteine nucleophile. Science 261 (1993) 1164-1167
39. He C., Hus J.C., Sun L.J., Zhou P., Norman D.P., Dotsch V., Wei H., Gross J.D., Lane W.S., Wagner G., and Verdine G.L. A methylation-dependent electrostatic switch controls DNA repair and transcriptional activation by E. coli ada. Mol. Cell 20 (2005) 117-129
40. Takinowaki H., Matsuda Y., Yoshida T., Kobayashi Y., and Ohkubo T. The solution structure of the methylated form of the N-terminal 16-kDa domain of Escherichia coli Ada protein. Protein Sci. 15 (2006) 487-497
41. Kataoka H., Yamamoto Y., and Sekiguchi M. A new gene (alkB) of Escherichia coli that controls sensitivity to methyl methane sulfonate. J. Bacteriol. 153 (1983) 1301-1307
42. Dinglay S., Trewick S.C., Lindahl T., and Sedgwick B. Defective processing of methylated single-stranded DNA by E. coli alkB mutants. Genes Dev. 14 (2000) 2097-2105
43. In: Kochetkov N.K., and Budovskii E.I. (Eds). Organic Chemistry of Nucleic Acids Part B (1972), Plenum Press, New York
44. L. Aravind, E.V. Koonin, The DNA-repair protein AlkB, EGL-9, and leprecan define new families of 2-oxoglutarate- and iron-dependent dioxygenases, Genome Biol. 2 (2001) RESEARCH0007.
45. Trewick S.C., Henshaw T.F., Hausinger R.P., Lindahl T., and Sedgwick B. Oxidative demethylation by Escherichia coli AlkB directly reverts DNA base damage. Nature 419 (2002) 174-178
46. Falnes P.O., Johansen R.F., and Seeberg E. AlkB-mediated oxidative demethylation reverses DNA damage in Escherichia coli. Nature 419 (2002) 178-181
47. Shanklin J., Achim C., Schmidt H., Fox B.G., and Munck E. Mossbauer studies of alkane w-hydroxylase: evidence for a diiron cluster in an integral-membrane enzyme. Proc. Natl. Acad. Sci. USA 94 (1997) 2981-2986
48. Austin R.N., Chang H.-K., Zylstra G.J., and Groves J.T. The non-heme diiron alkane monooxygenase of Pseudomonas oleovorans (AlkB) hydroxylates via a substrate radical intermediate. J. Am. Chem. Soc. 122 (2000) 11747-11748
49. Jordan A., and Reichard P. Ribonucleotide reductases. Annu. Rev. Biochem. 67 (1998) 71-98
50. Welford R.W.D., Schlemminger I., McNeill L.A., Hewitson K.S., and Schofield C.J. The selectivity and inhibition of AlkB. J. Biol. Chem. 278 (2003) 10157-10161
51. Koivisto P., Duncan T., Lindahl T., and Sedgwick B. Minimal methylated substrate and extended substrate range of Escherichia coli AlkB protein, a 1-methyladenine-DNA dioxygenase. J. Biol. Chem. 278 (2003) 44348-44354
52. Yu B., Edstrom W.C., Benach J., Hamuro Y., Weber P.C., Gibney B.R., and Hunt J.F. Crystal structures of catalytic complexes of the oxidative DNA/RNA repair enzyme AlkB. Nature 439 (2006) 879-884
53. Koivisto P., Robins P., Lindahl T., and Sedgwick B. Demethylation of 3- methylthymine in DNA by bacterial and human DNA dioxygenases. J. Biol. Chem. 279 (2004) 40470-40474
54. Falnes P.O. Repair of 3-methylthymine and 1-methylguanine lesions by bacterial and human AlkB proteins. Nucl. Acids Res. 32 (2004) 6260-6267
55. Delaney J.C., and Essigmann J.M. Mutagenesis, genotoxicity, and repair of 1-methyladenine, 3-alkylcytosines, 1-methylguanine, and 3-methylthymine in alkB Escherichia coli. Proc. Natl. Acad. Sci. USA 101 (2004) 14051-14056
56. Duncan T., Trewick S.C., Koivisto P., Bates P.A., Lindahl T., and Sedgwick B. Reversal of DNA alkylation damage by two human dioxygenases. Proc. Natl. Acad. Sci. USA 99 (2002) 16660-16665
57. Delaney J.C., Smeester L., Wong C., Frick L.E., Taghizadeh K., Wishnok J.S., Drennan C.L., Samson L.D., and Essigmann J.M. AlkB reverses etheno DNA lesions caused by lipid oxidation in vitro and in vivo. Nat. Struct. Mol. Biol. 12 (2005) 855-860
58. Mishina Y., Yang C.G., and He C. Direct repair of the exocyclic DNA adduct 1,N6-ethenoadenine by the DNA repair AlkB proteins. J. Am. Chem. Soc. 127 (2005) 14594-14595
59. Saparbaev M., Kleibl K., and Laval J. Escherichia coli, Saccharomyces cerevisiae, rat and human 3-methyladenine DNA glycosylases repair 1,N6-ethenoadenine when present in DNA. Nucl. Acids Res. 23 (1995) 3750-3755
60. Schofield C.J., and Ratcliffe P.J. Signalling hypoxia by HIF hydroxylases. Biochem. Biophys. Res. Commun. 338 (2005) 617-626
61. Tsukada Y., Fang J., Erdjument-Bromage H., Warren M.E., Borchers C.H., Tempst P., and Zhang Y. Histone demethylation by a family of JmjC domain-containing proteins. Nature 439 (2006) 811-816
62. Aas P.A., Otterlei M., Falnes P.O., Vagbo C.B., Skorpen F., Akbari M., Sundheim O., Bjoras M., Slupphaug G., Seeberg E., and Krokan H.E. Human and bacterial oxidative demethylases repair alkylation damage in both RNA and DNA. Nature 421 (2003) 859-863
63. Falnes P.O., Bjoras M., Aas P.A., Sundheim O., and Seeberg E. Substrate specificities of bacterial and human AlkB proteins. Nucl. Acids Res. 32 (2004) 3456-3461
64. Lee D.H., Jin S.G., Cai S., Chen Y., Pfeifer G.P., and O'Connor T.R. Repair of methylation damage in DNA and RNA by mammalian AlkB homologues. J. Biol. Chem. 280 (2005) 39448-39459
65. Sedgwick B., Robins P., and Lindahl T. Direct removal of alkylation damage from DNA by AlkB and related DNA dioxygenases. Meth. Enzymol. 408 (2006) 108-120
66. Kavli B., Sundheim O., Akbari M., Otterlei M., Nilsen H., Skorpen F., Aas P.A., Hagen L., Krokan H.E., and Slupphaug G. hUNG2 is the major repair enzyme for removal of uracil from U:A matches, U:G mismatches, and U in single-stranded DNA, with hSMUG1 as a broad specificity backup. J. Biol. Chem. 277 (2002) 39926-39936
67. Tarsounas M., Davies D., and West S.C. BRCA2-dependent and independent formation of RAD51 nuclear foci. Oncogene 22 (2003) 1115-1123
68. Ringvoll J., Nordstrand L.M., Vagbo C.B., Talstad V., Reite K., Aas P.A., Lauritzen K.H., Liabakk N.B., Bjork A., Doughty R.W., Falnes P.O., and Krokan H.E. A. Klungland, Repair deficient mice reveal mABH2 as the primary oxidative demethylase for repairing 1meA and 3meC lesions in DNA. EMBO J. 25 (2006) 2189-2198
69. Ougland R., Zhang C.M., Liiv A., Johansen R.F., Seeberg E., Hou Y.M., Remme J., and Falnes P.O. AlkB restores the biological function of mRNA and tRNA inactivated by chemical methylation. Mol. Cell 16 (2004) 107-116
70. Klungland A., Rosewell I., Hollenbach S., Larsen E., Daly G., Epe B., Seeberg E., Lindahl T., and Barnes D.E. Accumulation of premutagenic DNA lesions in mice defective in removal of oxidative base damage. Proc. Natl. Acad. Sci. USA 96 (1999) 13300-13305
71. Minowa O., Arai T., Hirano M., Monden Y., Nakai S., Fukuda M., Itoh M., Takano H., Hippou Y., Aburatani H., Masumura K., Nohmi T., Nishimura S., and Noda T. Mmh/Ogg1 gene inactivation results in accumulation of 8-hydroxyguanine in mice. Proc. Natl. Acad. Sci. USA 97 (2000) 4156-4161
72. Tsuzuki T., Sakumi K., Shiraishi A., Kawate H., Igarashi H., Iwakuma T., Tominaga Y., Zhang S., Shimizu S., Ishikawa T., et al. Targeted disruption of the DNA repair methyltransferase gene renders mice hypersensitive to alkylating agent. Carcinogenesis 17 (1996) 1215-1220
73. Paik J., Duncan T., Lindahl T., and Sedgwick B. Sensitisation of human carcinoma cells to alkylating agents by small interfering RNA suppression of 3-alkyladenine-DNA glycosylase. Cancer Res. 65 (2005) 10472-10477
74. Kawate H., Kunihiko S., Tsuzuki T., Nakatsuru Y., Ishikawa T., Takahashi S., Takano H., Noda T., and Sekiguchi M. Separation of killing and tumorigenic effects of an alkylating agent in mice defective in two of the DNA repair genes. Proc. Natl. Acad. Sci. USA 95 (1998) 5116-5120
75. Murzin A.G., Brenner S.E., Hubbard T., and Chothia C. SCOP: a structural classification of proteins database for the investigation of sequences and structures. J. Mol. Biol. 247 (1995) 536-540
76. Kurowski M.A., Bhagwat A.S., Papaj G., and Bujnicki J.M. Phylogenomic identification of five new human homologs of the DNA repair enzyme AlkB. BMC Genomics 4 (2003) 48
77. Mishina Y., Lee C.H., and He C. Interaction of human and bacterial AlkB proteins with DNA as probed through chemical cross-linking studies. Nucl. Acids Res. 32 (2004) 1548-1554
78. Sundheim O., Vagbo C.B., Bjoras M., de Sousa M.M.L., Talstad V., Aas P.A., Drablos F., Krokan H.E., Tainer J.A., and Slupphaug G. Human ABH3 structure and key residues for oxidative demethylation to reverse DNA/RNA damage. EMBO J. 25 (2006) 3389-3397
79. Yamamoto Y., Katsuki M., Sekiguchi M., and Otsuji N. Escherichia coli gene that controls sensitivity to alkylating agents. J. Bacteriol. 135 (1978) 144-152
80. Colombi D., and Gomes S.L. An alkB homologue is differentially transcribed during the Caulobacter crescentus cell cycle. J. Bacteriol. 179 (1997) 3139-3145
81. Chen B.J., Carroll P., and Samson L. The Escherichia coli AlkB protein protects human cells against alkylation-induced toxicity. J. Bacteriol. 176 (1994) 6255-6261
82. Konishi N., Nakamura M., Ishida E., Shimada K., Mitsui E., Yoshikawa R., Yamamoto H., and Tsujikawa K. High expression of a new marker PCA-1 in human prostate carcinoma. Clin. Cancer Res. 11 (2005) 5090-5097
83. Singer B., and Grunberger D. Molecular Biology of Mutagens and Carcinogens: Reactions of Directly Acting Agents with Nucleic Acids (1983), Plenum Press, New York pp. 45-96
84. Nieminuszczy J., Sikora A., Wrzesinski M., Janion C., and Grzesiuk E. AlkB dioxygenase in preventing MMS-induced mutagenesis in Escherichia coli: Effect of Pol V and AlkA proteins. DNA Repair (Amst) 5 (2005) 181-188
85. Mikhailov S.N., Rozenski J., Efimtseva E.V., Busson R., Aerschot A.V., and Herdewijn P. Chemical incorporation of 1-methyladenosine into oligonucleotides. Nucl. Acids Res. 30 (2002) 1124-1131
86. Boiteux S., and Laval J. Mutagenesis by alkylating agents: coding properties for DNA polymerase of poly(dC) template containing 3-methylcytosine. Biochimie 64 (1982) 637-641
87. Larson K., Sahm J., Shenkar R., and Strauss B. Methylation-induced blocks to in vitro DNA replication. Mutat. Res. 150 (1985) 77-84
88. 6-benzylguanine for patients with nitrosourea-resistant recurrent or progressive malignant glioma. J. Clin. Oncol. 20 (2002) 2277-2283
89. Middleton M.R., and Margison G.P. Improvement of chemotherapy efficacy by inactivation of a DNA-repair pathway. Lancet Oncol. 4 (2003) 37-44
90. Gerson S.L. MGMT: its role in cancer aetiology and cancer therapeutics. Nat. Rev. Cancer 4 (2004) 296-307
91. Falnes P.O., and Rognes T. DNA repair by bacterial AlkB proteins. Res. Microbiol. 154 (2003) 531-538
92. Drablos F., Feyzi E., Aas P.A., Vaagbo C.B., Kavli B., Bratlie M.S., Pena-Diaz J., Otterlei M., Slupphaug G., and Krokan H.E. Alkylation damage in DNA and RNA-repair mechanisms and medical significance. DNA Repair (Amst) 3 (2004) 1389-1407
93. Bratlie M.S., and Drablos F. Bioinformatic mapping of AlkB homology domains in viruses. BMC Genomics 6 1 (2005)
94. Wei Y., Carter K.C., Wang R., and Shell B.K. Molecular cloning and functional analysis of a human cDNA encoding an Escherichia coli AlkB homolog, a protein involved in DNA alkylation damage repair. Nucl. Acids Res. 24 (1996) 931-937
95. Jones P.A., and Takai D. The role of DNA methylation in mammalian epigenetics. Science 293 (2001) 1068-1070
96. Shi Y., Lan F., Matson C., Mulligan P., Whetstine J.R., Cole P.A., and Casero R.A. Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 119 (2004) 941-953
97. Yamane K., Toumazou C., Tsukada Y., Erdjument-Bromage H., Tempst P., Wong J., and Zhang Y. JHDM2A, a JmjC-containing H3K9 demethylase, facilitates transcription activation by androgen receptor. Cell 125 (2006) 483-495
98. Whetstine J.R., Nottke A., Lan F., Huarte M., Smolikov S., Chen Z., Spooner E., Li E., Zhang G., Colaiacovo M., and Shi Y. Reversal of histone lysine trimethylation by the JMJD2 family of histone demethylases. Cell 125 (2006) 467-481
99. Trewick S.C., McLaughlin P.J., and Allshire R.C. Methylation: lost in hydroxylation?. EMBO Rep. 6 (2005) 315-320
100. Sedgwick B., and Lindahl T. Recent progress on the Ada response for inducible repair of DNA alkylation damage. Oncogene 21 (2002) 8886-8894
101. Landini P., Hajec L.I., and Volkert M.R. Structure and transcriptional regulation of the Escherichia coli adaptive response gene aidB. J. Bacteriol. 176 (1994) 6583-6589
102. Rohankhedkar M.S., Mulrooney S.B., Wedemeyer W.J., and Hausinger R.P. The AidB component of the Escherichia coli adaptive response to alkylating agents is a flavin-containing, DNA-binding protein. J. Bacteriol. 188 (2006) 223-230
103. Johnston S.D., Lew J.E., and Berman J. Gbp1p, a protein with RNA recognition motifs, binds single-stranded telomeric DNA and changes its binding specificity upon dimerization. Mol. Cell. Biol. 19 (1999) 923-933
104. N. Osada, M. Hida, J. Kusuda, R. Tanuma, M. Hirata, M. Hirai, K. Terao, Y. Suzuki, S. Sugano, K. Hashimoto, Prediction of unidentified human genes on the basis of sequence similarity to novel cDNAs from cynomolgus monkey brain, Genome Biol. 3 (2002) RESEARCH0006.
105. Welford R.W., Kirkpatrick J.M., McNeill L.A., Puri M., Oldham N.J., and Schofield C.J. Incorporation of oxygen into the succinate co-product of iron(II) and 2-oxoglutarate dependent oxygenases from bacteria, plants and humans. FEBS Lett. 579 (2005) 5170-5174
106. Cupples C.G., and Miller J.H. A set of lacZ mutations in Escherichia coli that allow rapid detection of each of the six base substitutions. Proc. Natl. Acad. Sci. USA 86 (1989) 5345-5349
107. Sandve G.K., and Drablos F. Generalised composite motif discovery. In: Khosla R. (Ed). Knowledge-Based Intelligent Information and Engineering Systems (2005) pp. 763-769