MBD4 and TDG: Multifaceted DNA glycosylases with ever expanding biological roles

Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis

Volumn 743-744, Issue , 2013, Pages 12-25

  Sjolund, Ashley B ^a   Senejani, Alireza G ^a   Sweasy, Joann B ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Base excision repair; DNA glycosylase; DNA methylation; Polymorphisms

Indexed keywords

BINDING PROTEIN; METHYL CPG BINDING PROTEIN 4; PROTEIN MLH1; THYMINE DNA GLYCOSYLASE; UNCLASSIFIED DRUG;

ALTERNATIVE RNA SPLICING; AMINO ACID SUBSTITUTION; APOPTOSIS; CELL CYCLE S PHASE; DEMETHYLATION; DNA DAMAGE; DNA METHYLATION; EMBRYO DEVELOPMENT; ENZYME METABOLISM; ENZYME SUBSTRATE; GENE EXPRESSION REGULATION; GENE STRUCTURE; GENETIC VARIABILITY; HUMAN; METHYL CPG BINDING PROTEIN 4 GENE; MUTATIONAL ANALYSIS; MUTATOR GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; SOMATIC MUTATION; STRUCTURE ANALYSIS; SUMOYLATION; THYMINE DNA GLYCOSYLASE GENE; TRANSCRIPTION REGULATION;

ANIMALS; DNA DAMAGE; DNA REPAIR; ENDODEOXYRIBONUCLEASES; HUMANS; MUTATION; THYMINE; THYMINE DNA GLYCOSYLASE;

EID: 84877927182     PISSN: 00275107     EISSN: 09218262     Source Type: Journal    
DOI: 10.1016/j.mrfmmm.2012.11.001     Document Type: Review

References (115)

1. Barnes D.E., Lindahl T. Repair and genetic consequences of endogenous DNA base damage in mammalian cells. Annu. Rev. Genet. 2004, 38:445-476.
2. De Bont R., van Larebeke N. Endogenous DNA damage in humans: a review of quantitative data. Mutagenesis 2004, 19:169-185.
3. Duncan B.K., Miller J.H. Mutagenic deamination of cytosine residues in DNA. Nature 1980, 287:560-561.
4. Cooper D.N., Youssoufian H. The CpG dinucleotide and human genetic disease. Hum. Genet. 1988, 78:151-155.
5. Kleihues P., Schã{currency sign}uble B., Zur Hausen A., Estã̈ve J., Ohgaki H. Tumors associated with p53 germline mutations: a synopsis of 91 families. Am. J. Pathol. 1997, 150:1-13.
6. Starcevic D., Dalal S., Sweasy J.B. Is there a link between DNA polymerase beta and cancer?. Cell Cycle 2004, 3:998-1001.
7. Kahn A.B., Ryan M.C., Liu H., Zeeberg B.R., Jamison D.C., Weinstein J.N. SpliceMiner: a high-throughput database implementation of the NCBI Evidence Viewer for microarray splice variant analysis. BMC Bioinformatics 2007, 8:75.
8. M.R. Meng HX, MBD4 (methyl-CpG binding domain protein 4), Atlas Genet. Cytogenet. Oncol. Haematol., July 2011.
9. Hendrich B., Tweedie S. The methyl-CpG binding domain and the evolving role of DNA methylation in animals. Trends Genet. 2003, 19:269-277.
10. Hendrich B., Bird A. Identification and characterization of a family of mammalian methyl-CpG binding proteins. Mol. Cell. Biol. 1998, 18:6538-6547.
11. Wakefield R.I.D., Smith B.O., Nan X., Free A., Soteriou A., Uhrin D., Bird A.P., Barlow P.N. The solution structure of the domain from MeCP2 that binds to methylated DNA. J. Mol. Biol. 1999, 291:1055-1065.
12. Manvilla B.A., Maiti A., Begley M.C., Toth E.A., Drohat A.C. Crystal structure of human methyl-binding domain IV glycosylase bound to abasic DNA. J. Mol. Biol. 2012, 420:164-175.
13. Wu P., Qiu C., Sohail A., Zhang X., Bhagwat A.S., Cheng X. Mismatch repair in methylated DNA. Structure and activity of the mismatch-specific thymine glycosylase domain of methyl-CpG-binding protein MBD4. J. Biol. Chem. 2003, 278:5285-5291.
14. Zhang W., Liu Z., Crombet L., Amaya M.F., Liu Y., Zhang X., Kuang W., Ma P., Niu L., Qi C. Crystal structure of the mismatch-specific thymine glycosylase domain of human methyl-CpG-binding protein MBD4. Biochem. Biophys. Res. Commun. 2011, 412:425-428.
15. Morera S., Grin I., Vigouroux A., Couve S., Henriot V., Saparbaev M., Ishchenko A.A. Biochemical and structural characterization of the glycosylase domain of MBD4 bound to thymine and 5-hydroxymethyuracil-containing DNA. Nucleic Acids Res. 2012, 40:9917-9926.
16. Hendrich B., Hardeland U., Ng H.H., Jiricny J., Bird A. The thymine glycosylase MBD4 can bind to the product of deamination at methylated CpG sites. Nature 1999, 401:301-304.
17. Petronzelli F., Riccio A., Markham G.D., Seeholzer S.H., Genuardi M., Karbowski M., Yeung A.T., Matsumoto Y., Bellacosa A. Investigation of the substrate spectrum of the human mismatch-specific DNA N-glycosylase MED1 (MBD4): fundamental role of the catalytic domain. J. Cell. Physiol. 2000, 185:473-480.
18. Petronzelli F., Riccio A., Markham G.D., Seeholzer S.H., Stoerker J., Genuardi M., Yeung A.T., Matsumoto Y., Bellacosa A. Biphasic kinetics of the human DNA repair protein MED1 (MBD4), a mismatch-specific DNA N-glycosylase. J. Biol. Chem. 2000, 275:32422-32429.
19. Cortellino S., Turner D., Masciullo V., Schepis F., Albino D., Daniel R., Skalka A.M., Meropol N.J., Alberti C., Larue L., Bellacosa A. The base excision repair enzyme MED1 mediates DNA damage response to antitumor drugs and is associated with mismatch repair system integrity. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:15071-15076.
20. Henderson J.P., Byun J., Takeshita J., Heinecke J.W. Phagocytes produce 5-chlorouracil and 5-bromouracil, two mutagenic products of myeloperoxidase, in human inflammatory tissue. J. Biol. Chem. 2003, 278:23522-23528.
21. Valinluck V., Liu P., Kang J.I., Burdzy A., Sowers L.C. 5-halogenated pyrimidine lesions within a CpG sequence context mimic 5-methylcytosine by enhancing the binding of the methyl-CpG-binding domain of methyl-CpG-binding protein 2 (MeCP2). Nucleic Acids Res. 2005, 33:3057-3064.
22. Turner D.P., Cortellino S., Schupp J.E., Caretti E., Loh T., Kinsella T.J., Bellacosa A. The DNA N-glycosylase MED1 exhibits preference for halogenated pyrimidines and is involved in the cytotoxicity of 5-iododeoxyuridine. Cancer Res. 2006, 66:7686-7693.
23. Aziz M.A., Schupp J.E., Kinsella T.J. Modulation of the activity of methyl binding domain protein 4 (MBD4/MED1) while processing iododeoxyuridine generated DNA mispairs. Cancer Biol. Ther. 2009, 8:1156-1163.
24. Hashimoto H., Liu Y., Upadhyay A.K., Chang Y., Howerton S.B., Vertino P.M., Zhang X., Cheng X. Recognition and potential mechanisms for replication and erasure of cytosine hydroxymethylation. Nucleic Acids Res. 2012, 40:4841-4889.
25. Hashimoto H., Zhang X., Cheng X. Excision of thymine and 5-hydroxymethyluracil by the MBD4 DNA glycosylase domain: structural basis and implications for active DNA demethylation. Nucleic Acids Res. 2012, 40:10203-10214.
26. Cortellino S., Xu J., Sannai M., Moore R., Caretti E., Cigliano A., Le Coz M., Devarajan K., Wessels A., Soprano D., Abramowitz L.K., Bartolomei M.S., Rambow F., Bassi M.R., Bruno T., Fanciulli M., Renner C., Klein-Szanto A.J., Matsumoto Y., Kobi D., Davidson I., Alberti C., Larue L., Bellacosa A. Thymine DNA glycosylase is essential for active DNA demethylation by linked deamination-base excision repair. Cell 2011, 146:67-79.
27. Rai K., Huggins I.J., James S.R., Karpf A.R., Jones D.A., Cairns B.R. DNA demethylation in zebrafish involves the coupling of a deaminase, a glycosylase, and gadd45. Cell 2008, 135:1201-1212.
28. Zhu B., Zheng Y., Angliker H., Schwarz S., Thiry S., Siegmann M., Jost J.P. 5-Methylcytosine DNA glycosylase activity is also present in the human MBD4 (G/T mismatch glycosylase) and in a related avian sequence. Nucleic Acids Res. 2000, 28:4157-4165.
29. Millar C.B., Guy J., Sansom O.J., Selfridge J., MacDougall E., Hendrich B., Keightley P.D., Bishop S.M., Clarke A.R., Bird A. Enhanced CpG mutability and tumorigenesis in MBD4-deficient mice. Science 2002, 297:403-405.
30. Wong E., Yang K., Kuraguchi M., Werling U., Avdievich E., Fan K., Fazzari M., Jin B., Brown A.M., Lipkin M., Edelmann W. Mbd4 inactivation increases Cright-arrowT transition mutations and promotes gastrointestinal tumor formation. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:14937-14942.
31. Riccio A., Aaltonen L.A., Godwin A.K., Loukola A., Percesepe A., Salovaara R., Masciullo V., Genuardi M., Paravatou-Petsotas M., Bassi D.E., Ruggeri B.A., Klein-Szanto A.J., Testa J.R., Neri G., Bellacosa A. The DNA repair gene MBD4 (MED1) is mutated in human carcinomas with microsatellite instability. Nat. Genet. 1999, 23:266-268.
32. Miquel C., Jacob S., Grandjouan S., Aime A., Viguier J., Sabourin J.C., Sarasin A., Duval A., Praz F. Frequent alteration of DNA damage signalling and repair pathways in human colorectal cancers with microsatellite instability. Oncogene 2007, 26:5919-5926.
33. Bader S., Walker M., Hendrich B., Bird A., Bird C., Hooper M., Wyllie A. Somatic frameshift mutations in the MBD4 gene of sporadic colon cancers with mismatch repair deficiency. Oncogene 1999, 18:8044-8047.
34. Yamada T., Koyama T., Ohwada S., Tago K., Sakamoto I., Yoshimura S., Hamada K., Takeyoshi I., Morishita Y. Frameshift mutations in the MBD4/MED1 gene in primary gastric cancer with high-frequency microsatellite instability. Cancer Lett. 2002, 181:115-120.
35. Bader S., Walker M., Harrison D. Most microsatellite unstable sporadic colorectal carcinomas carry MBD4 mutations. Br. J. Cancer 2000, 83:1646-1649.
36. Giannini G., Ristori E., Cerignoli F., Rinaldi C., Zani M., Viel A., Ottini L., Crescenzi M., Martinotti S., Bignami M., Frati L., Screpanti I., Gulino A. Human MRE11 is inactivated in mismatch repair-deficient cancers. EMBO Rep. 2002, 3:248-254.
37. Bader S.A., Walker M., Harrison D.J. A human cancer-associated truncation of MBD4 causes dominant negative impairment of DNA repair in colon cancer cells. Br. J. Cancer 2007, 96:660-666.
38. Hardeland U., Kunz C., Focke F., Szadkowski M., Schar P. Cell cycle regulation as a mechanism for functional separation of the apparently redundant uracil DNA glycosylases TDG and UNG2. Nucleic Acids Res. 2007, 35:3859-3867.
39. Bellacosa A., Cicchillitti L., Schepis F., Riccio A., Yeung A.T., Matsumoto Y., Golemis E.A., Genuardi M., Neri G. MED1, a novel human methyl-CpG-binding endonuclease, interacts with DNA mismatch repair protein MLH1. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:3969-3974.
40. Kunkel T.A., Erie D.A. DNA mismatch repair. Annu. Rev. Biochem. 2005, 74:681-710.
41. Schroering A.G., Edelbrock M.A., Richards T.J., Williams K.J. The cell cycle and DNA mismatch repair. Exp. Cell Res. 2007, 313:292-304.
42. Prolla T.A., Baker S.M., Harris A.C., Tsao J.L., Yao X., Bronner C.E., Zheng B., Gordon M., Reneker J., Arnheim N., Shibata D., Bradley A., Liskay R.M. Tumour susceptibility and spontaneous mutation in mice deficient in Mlh1, Pms1 and Pms2 DNA mismatch repair. Nat. Genet. 1998, 18:276-279.
43. Sansom O.J., Bishop S.M., Bird A., Clarke A.R. MBD4 deficiency does not increase mutation or accelerate tumorigenesis in mice lacking MMR. Oncogene 2004, 23:5693-5696.
44. Branch P., Hampson R., Karran P. DNA mismatch binding defects, DNA damage tolerance, and mutator phenotypes in human colorectal carcinoma cell lines. Cancer Res. 1995, 55:2304-2309.
45. Sansom O.J., Zabkiewicz J., Bishop S.M., Guy J., Bird A., Clarke A.R. MBD4 deficiency reduces the apoptotic response to DNA-damaging agents in the murine small intestine. Oncogene 2003, 22:7130-7136.
46. Screaton R.A., Kiessling S., Sansom O.J., Millar C.B., Maddison K., Bird A., Clarke A.R., Frisch S.M. Fas-associated death domain protein interacts with methyl-CpG binding domain protein 4: a potential link between genome surveillance and apoptosis. PNAS 2003, 100:5211-5216.
47. Ruzov A., Shorning B., Mortusewicz O., Dunican D.S., Leonhardt H., Meehan R.R. MBD4 and MLH1 are required for apoptotic induction in xDNMT1-depleted embryos. Development 2009, 136:2277-2286.
48. Doerfler W. DNA methylation and gene activity. Annu. Rev. Biochem. 1983, 52:93-124.
49. Law J.A., Jacobsen S.E. Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat. Rev. Genet. 2010, 11:204-220.
50. Ishibashi T., So K., Cupples C.G., Ausio J. MBD4-mediated glycosylase activity on a chromatin template is enhanced by acetylation. Mol. Cell. Biol. 2008, 28:4734-4744.
51. Boland M.J., Christman J.K. Characterization of Dnmt3b:thymine-DNA glycosylase interaction and stimulation of thymine glycosylase-mediated repair by DNA methyltransferase(s) and RNA. J. Mol. Biol. 2008, 379:492-504.
52. Chen T., Tsujimoto N., Li E. The PWWP domain of Dnmt3a and Dnmt3b is required for directing DNA methylation to the major satellite repeats at pericentric heterochromatin. Mol. Cell. Biol. 2004, 24:9048-9058.
53. Bhutani N., Burns D.M., Blau H.M. DNA demethylation dynamics. Cell 2011, 146:866-872.
54. Metivier R., Gallais R., Tiffoche C., Le Peron C., Jurkowska R.Z., Carmouche R.P., Ibberson D., Barath P., Demay F., Reid G., Benes V., Jeltsch A., Gannon F., Salbert G. Cyclical DNA methylation of a transcriptionally active promoter. Nature 2008, 452:45-50.
55. Bogdanovic O., Veenstra G.J. DNA methylation and methyl-CpG binding proteins: developmental requirements and function. Chromosoma 2009, 118:549-565.
56. Kondo E., Gu Z., Horii A., Fukushige S. The thymine DNA glycosylase MBD4 represses transcription and is associated with methylated p16(INK4a) and hMLH1 genes. Mol. Cell. Biol. 2005, 25:4388-4396.
57. Kavli B., Andersen S., Otterlei M., Liabakk N.B., Imai K., Fischer A., Durandy A., Krokan H.E., Slupphaug G. B cells from hyper-IgM patients carrying UNG mutations lack ability to remove uracil from ssDNA and have elevated genomic uracil. J. Exp. Med. 2005, 201:2011-2021.
58. Donigan K.A., Hile S.E., Eckert K.A., Sweasy J.B. The human gastric cancer-associated DNA polymerase beta variant D160N is a mutator that induces cellular transformation. DNA Repair (Amst.) 2012, 11:381-390.
59. Nemec A.A., Donigan K.A., Murphy D.L., Jaeger J., Sweasy J.B. Colon cancer-associated DNA polymerase beta variant induces genomic instability and cellular transformation. J. Biol. Chem. 2012, 287:23840-23849.
60. Bravard A., Vacher M., Moritz E., Vaslin L., Hall J., Epe B., Radicella J.P. Oxidation status of human OGG1-S326C polymorphic variant determines cellular DNA repair capacity. Cancer Res. 2009, 69:3642-3649.
61. Pinto M., Wu Y., Suriano G., Mensink R.G., Duval A., Oliveira C., Carvalho B., Hamelin R., Seruca R., Hofstra R.M. MBD4 mutations are rare in gastric carcinomas with microsatellite instability. Cancer Genet. Cytogenet. 2003, 145:103-107.
62. Owen R.M., Baker R.D., Bader S., Dunlop M.G., Nicholl I.D. The identification of a novel alternatively spliced form of the MBD4 DNA glycosylase. Oncol. Rep. 2007, 17:111-116.
63. Neddermann P., Gallinari P., Lettieri T., Schmid D., Truong O., Hsuan J.J., Wiebauer K., Jiricny J. Cloning and expression of human G/T mismatch-specific thymine-DNA glycosylase. J. Biol. Chem. 1996, 271:12767-12774.
64. Cortazar D., Kunz C., Saito Y., Steinacher R., Schar P. The enigmatic thymine DNA glycosylase. DNA Repair (Amst.) 2007, 6:489-504.
65. Schmutte C., Baffa R., Veronese L.M., Murakumo Y., Fishel R. Human thymine-DNA glycosylase maps at chromosome 12q22-q24.1: a region of high loss of heterozygosity in gastric cancer. Cancer Res. 1997, 57:3010-3015.
66. Krzesniak M., Butkiewicz D., Samojedny A., Chorazy M., Rusin M. Polymorphisms in TDG and MGMT genes - epidemiological and functional study in lung cancer patients from Poland. Ann. Hum. Genet. 2004, 68:300-312.
67. Yatsuoka T., Furukawa T., Abe T., Yokoyama T., Sunamura M., Kobari M., Matsuno S., Horii A. Genomic analysis of the thymine-DNA glycosylase (TDG) gene on 12q22-q24.1 in human pancreatic ductal adenocarcinoma. Int. J. Pancreatol. 1999, 25:97-102.
68. Missero C., Pirro M.T., Simeone S., Pischetola M., Di Lauro R. The DNA glycosylase T:G mismatch-specific thymine DNA glycosylase represses thyroid transcription factor-1-activated transcription. J. Biol. Chem. 2001, 276:33569-33575.
69. Tini M., Benecke A., Um S.J., Torchia J., Evans R.M., Chambon P. Association of CBP/p300 acetylase and thymine DNA glycosylase links DNA repair and transcription. Mol. Cell 2002, 9:265-277.
70. Chen D., Lucey M.J., Phoenix F., Lopez-Garcia J., Hart S.M., Losson R., Buluwela L., Coombes R.C., Chambon P., Schar P., Ali S. T:G mismatch-specific thymine-DNA glycosylase potentiates transcription of estrogen-regulated genes through direct interaction with estrogen receptor alpha. J. Biol. Chem. 2003, 278:38586-38592.
71. Li Y.Q., Zhou P.Z., Zheng X.D., Walsh C.P., Xu G.L. Association of Dnmt3a and thymine DNA glycosylase links DNA methylation with base-excision repair. Nucleic Acids Res. 2007, 35:390-400.
72. C. Smet-Nocca, J.-M. Wieruszeski, V. Chaar, A. Leroy, A. Benecke, The thymine-DNA glycosylase regulatory domain: residual structure and DNA binding biochemistry, 2008 47 6519-6530.
73. Hardeland U., Steinacher R., Jiricny J., Schar P. Modification of the human thymine-DNA glycosylase by ubiquitin-like proteins facilitates enzymatic turnover. EMBO J. 2002, 21:1456-1464.
74. Mohan R.D., Litchfield D.W., Torchia J., Tini M. Opposing regulatory roles of phosphorylation and acetylation in DNA mispair processing by thymine DNA glycosylase. Nucleic Acids Res. 2010, 38:1135-1148.
75. Barrett T.E., Scharer O.D., Savva R., Brown T., Jiricny J., Verdine G.L., Pearl L.H. Crystal structure of a thwarted mismatch glycosylase DNA repair complex. EMBO J. 1999, 18:6599-6609.
76. Hardeland U., Bentele M., Jiricny J., Schar P. The versatile thymine DNA-glycosylase: a comparative characterization of the human, Drosophila and fission yeast orthologs. Nucleic Acids Res. 2003, 31:2261-2271.
77. Maiti A., Morgan M.T., Drohat A.C. Role of two strictly conserved residues in nucleotide flipping and N-glycosylic bond cleavage by human thymine DNA glycosylase. J. Biol. Chem. 2009, 284:36680-36688.
78. Hay R.T. SUMO: a history of modification. Mol. Cell 2005, 18:1-12.
79. Baba D., Maita N., Jee J.-G., Uchimura Y., Saitoh H., Sugasawa K., Hanaoka F., Tochio H., Hiroaki H., Shirakawa M. Crystal structure of thymine DNA glycosylase conjugated to SUMO-1. Nature 2005, 435:979-982.
80. Baba D., Maita N., Jee J.-G., Uchimura Y., Saitoh H., Sugasawa K., Hanaoka F., Tochio H., Hiroaki H., Shirakawa M. Crystal Structure of SUMO-3-modified thymine-DNA glycosylase. J. Mol. Biol. 2006, 359:137-147.
81. Maiti A., Morgan M.T., Pozharski E., Drohat A.C. Crystal structure of human thymine DNA glycosylase bound to DNA elucidates sequence-specific mismatch recognition. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:8890-8895.
82. Maiti A., Drohat A.C. Dependence of substrate binding and catalysis on pH, ionic strength, and temperature for thymine DNA glycosylase: insights into recognition and processing of G.T mispairs. DNA Repair (Amst.) 2011, 10:545-553.
83. Hardeland U., Bentele M., Jiricny J., Schãr P. The versatile thymine DNA-glycosylase: a comparative characterization of the human, Drosophila and fission yeast orthologs. Nucleic Acids Res. 2003, 31:2261-2271.
84. Morgan M.T., Bennett M.T., Drohat A.C. Excision of 5-halogenated uracils by human thymine DNA glycosylase. Robust activity for DNA contexts other than CpG. J. Biol. Chem. 2007, 282:27578-27586.
85. Saparbaev M., Laval J. 3,N4-ethenocytosine, a highly mutagenic adduct, is a primary substrate for Escherichia coli double-stranded uracil-DNA glycosylase and human mismatch-specific thymine-DNA glycosylase. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:8508-8513.
86. He Y.F., Li B.Z., Li Z., Liu P., Wang Y., Tang Q., Ding J., Jia Y., Chen Z., Li L., Sun Y., Li X., Dai Q., Song C.X., Zhang K., He C., Xu G.L. Tet-mediated formation of 5-carboxylcytosine and its excision by TDG in mammalian DNA. Science 2011, 333:1303-1307.
87. Maiti A., Drohat A.C. Thymine DNA glycosylase can rapidly excise 5-formylcytosine and 5-carboxylcytosine: potential implications for active demethylation of CpG sites. J. Biol. Chem. 2011, 286:35334-35338.
88. Morgan M.T., Maiti A., Fitzgerald M.E., Drohat A.C. Stoichiometry and affinity for thymine DNA glycosylase binding to specific and nonspecific DNA. Nucleic Acids Res. 2011, 39:2319-2329.
89. Maiti A., Noon M.S., Mackerell A.D., Pozharski E., Drohat A.C. Lesion processing by a repair enzyme is severely curtailed by residues needed to prevent aberrant activity on undamaged DNA. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:8091-8096.
90. Waters T.R., Gallinari P., Jiricny J., Swann P.F. Human thymine DNA glycosylase binds to apurinic sites in DNA but is displaced by human apurinic endonuclease 1. J. Biol. Chem. 1999, 274:67-74.
91. Fitzgerald M.E., Drohat A.C. Coordinating the initial steps of base excision repair. J. Biol. Chem. 2008, 283:32680-32690.
92. Mohan R.D., Rao A., Gagliardi J., Tini M. SUMO-1-dependent allosteric regulation of thymine DNA glycosylase alters subnuclear localization and CBP/p300 recruitment. Mol. Cell. Biol. 2007, 27:229-243.
93. Fischer J.A., Muller-Weeks S., Caradonna S. Proteolytic degradation of the nuclear isoform of uracil-DNA glycosylase occurs during the S phase of the cell cycle. DNA Repair (Amst.) 2004, 3:505-513.
94. Niederreither K., Harbers M., Chambon P., Dolle P. Expression of T:G mismatch-specific thymidine-DNA glycosylase and DNA methyl transferase genes during development and tumorigenesis. Oncogene 1998, 17:1577-1585.
95. Cortazar D., Kunz C., Selfridge J., Lettieri T., Saito Y., MacDougall E., Wirz A., Schuermann D., Jacobs A.L., Siegrist F., Steinacher R., Jiricny J., Bird A., Schar P. Embryonic lethal phenotype reveals a function of TDG in maintaining epigenetic stability. Nature 2011, 470:419-423.
96. Kunz C., Focke F., Saito Y., Schuermann D., Lettieri T., Selfridge J., Schar P. Base excision by thymine DNA glycosylase mediates DNA-directed cytotoxicity of 5-fluorouracil. PLoS Biol. 2009, 7:e91.
97. Longley D.B., Harkin D.P., Johnston P.G. 5-fluorouracil: mechanisms of action and clinical strategies. Nat. Rev. Cancer 2003, 3:330-338.
98. Neddermann P., Jiricny J. The purification of a mismatch-specific thymine-DNA glycosylase from HeLa cells. J. Biol. Chem. 1993, 268:21218-21224.
99. Um S., Harbers M., Benecke A., Pierrat B., Losson R., Chambon P. Retinoic acid receptors interact physically and functionally with the T:G mismatch-specific thymine-DNA glycosylase. J. Biol. Chem. 1998, 273:20728-20736.
100. Lucey M.J., Chen D., Lopez-Garcia J., Hart S.M., Phoenix F., Al-Jehani R., Alao J.P., White R., Kindle K.B., Losson R.g., Chambon P., Parker M.G., Schã{currency sign}r P., Heery D.M., Buluwela L., Ali S. T:G mismatch-specific thymine-DNA glycosylase (TDG) as a coregulator of transcription interacts with SRC1 family members through a novel tyrosine repeat motif. Nucleic Acids Res. 2005, 33:6393-6404.
101. Chevray P.M., Nathans D. Protein interaction cloning in yeast: identification of mammalian proteins that react with the leucine zipper of Jun. Proc. Natl. Acad. Sci. U.S.A. 1992, 89:5789-5793.
102. Bastien J., Rochette-Egly C. Nuclear retinoid receptors and the transcription of retinoid-target genes. Gene 2004, 328:1-16.
103. Nilsson S., ã{currency sign}kelã{currency sign} S.M., Treuter E., Tujague M., Thomsen J., Andersson G.r., Enmark E., Pettersson K., Warner M., Gustafsson J.-ã.k. Mechanisms of estrogen action. Physiol. Rev. 2001, 81:1535-1565.
104. Chiang S., Burch T., Van Domselaar G., Dick K., Radziwon A., Brusnyk C., Edwards M., Piper J., Cutts T., Cao J., Li X., He R. The interaction between thymine DNA glycosylase and nuclear receptor coactivator 3 is required for the transcriptional activation of nuclear hormone receptors. Mol. Cell. Biochem. 2010, 333:221-232.
105. Goodman R.H., Smolik S. CBP/p300 in cell growth, transformation, and development. Genes Dev. 2000, 14:1553-1577.
106. Negorev D., Maul G.G. Cellular proteins localized at and interacting within ND10/PML nuclear bodies/PODs suggest functions of a nuclear depot. Oncogene 2001, 20:7234-7242.
107. Konopatskaya O., Poole A.W. Protein kinase C alpha: disease regulator and therapeutic target. Trends Pharmacol. Sci. 2010, 31:8-14.
108. Metivier R., Penot G., Hubner M.R., Reid G., Brand H., Kos M., Gannon F. Estrogen receptor-alpha directs ordered, cyclical, and combinatorial recruitment of cofactors on a natural target promoter. Cell 2003, 115:751-763.
109. Jakowlew S.B., Breathnach R., Jeltsch J.M., Masiakowski P., Chambon P. Sequence of the pS2 mRNA induced by estrogen in the human breast cancer cell line MCF-7. Nucleic Acids Res. 1984, 12:2861-2878.
110. Sherry S.T., Ward M.H., Kholodov M., Baker J., Phan L., Smigielski E.M., Sirotkin K. dbSNP: the NCBI database of genetic variation. Nucleic Acids Res. 2001, 29:308-311.
111. Broderick P., Bagratuni T., Vijayakrishnan J., Lubbe S., Chandler I., Houlston R.S. Evaluation of NTHL1, NEIL1, NEIL2, MPG, TDG, UNG and SMUG1 genes in familial colorectal cancer predisposition. BMC Cancer 2006, 6:243.
112. Vasovcak P., Krepelova A., Menigatti M., Puchmajerova A., Skapa P., Augustinakova A., Amann G., Wernstedt A., Jiricny J., Marra G., Wimmer K. Unique mutational profile associated with a loss of TDG expression in the rectal cancer of a patient with a constitutional PMS2 deficiency. DNA Repair (Amst.) 2012.
113. Lang T., Dalal S., Chikova A., DiMaio D., Sweasy J.B. The E295K DNA polymerase beta gastric cancer-associated variant interferes with base excision repair and induces cellular transformation. Mol. Cell. Biol. 2007, 27:5587-5596.
114. Sweasy J.B., Lang T., Starcevic D., Sun K.W., Lai C.C., Dimaio D., Dalal S. Expression of DNA polymerase {beta} cancer-associated variants in mouse cells results in cellular transformation. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:14350-14355.
115. Consortium T.G.P. A map of human genome variation from population-scale sequencing. Nature 2011, 467:1061-1073.