Thymine DNA glycosylase is a positive regulator of Wnt signaling in colorectal cancer

Journal of Biological Chemistry

Volumn 289, Issue 13, 2014, Pages 8881-8890

  Xu, Xuehe ^a,b,c   Yu, Tianxin ^a,c   Shi, Jiandang ^a,c   Chen, Xi ^a,c   Zhang, Wen ^a,c   Lin, Ting ^a,b,c   Liu, Zhihong ^b   Wang, Yadong ^b   Zeng, Zheng ^c   Wang, Chi ^c   Li, Mingsong ^a   Liu, Chunming ^a,c  

^a UNIVERSITY OF KENTUCKY   (United States)

^b SOUTHERN MEDICAL UNIVERSITY   (China)

^c UNIVERSITY OF KENTUCKY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIAGNOSIS; DISEASES; HISTOLOGY; TISSUE;

CATENIN DEGRADATION; COLORECTAL CANCER; COLORECTAL CANCERS (CRC); CREB BINDING PROTEINS; DNA GLYCOSYLASE; NORMAL TISSUE; TUMOR TISSUES; WNT SIGNALING;

DNA;

HISTONE ACETYLTRANSFERASE PCAF; SHORT HAIRPIN RNA; SUMO PROTEIN; THYMINE DNA GLYCOSYLASE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR TCF4; UNCLASSIFIED DRUG; BASIC HELIX LOOP HELIX LEUCINE ZIPPER TRANSCRIPTION FACTOR; BONE SIALOPROTEIN (35-62), HUMAN; PEPTIDE FRAGMENT; SIALOGLYCOPROTEIN; TCF4 PROTEIN, HUMAN; WNT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; CANCER GROWTH; CANCER INHIBITION; CELL PROLIFERATION; CLINICAL ARTICLE; COLORECTAL CANCER; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME INDUCTION; ENZYME LOCALIZATION; ENZYME REGULATION; GENE SILENCING; GENE TARGETING; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SUMOYLATION; TDG GENE; WNT SIGNALING PATHWAY; AMINO ACID SEQUENCE; CHEMISTRY; COLORECTAL TUMOR; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY; PROTEIN TRANSPORT; TUMOR CELL LINE; UPREGULATION;

AMINO ACID SEQUENCE; BASIC HELIX-LOOP-HELIX LEUCINE ZIPPER TRANSCRIPTION FACTORS; CELL LINE, TUMOR; CELL PROLIFERATION; COLORECTAL NEOPLASMS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; PEPTIDE FRAGMENTS; PROTEIN TRANSPORT; SIALOGLYCOPROTEINS; SUMOYLATION; THYMINE DNA GLYCOSYLASE; TRANSCRIPTION FACTORS; UP-REGULATION; WNT PROTEINS; WNT SIGNALING PATHWAY;

EID: 84897384365     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.538835     Document Type: Article

References (45)

1. Siegel, R., Naishadham, D., and Jemal, A. (2013) Cancer Statistics, 2013. CA Cancer J. Clin. 63, 11-30
2. Giles, R. H., van Es, J. H., and Clevers, H. (2003) Caught up in a Wnt storm. Wnt signaling in cancer. Biochim. Biophys. Acta 1653, 1-24 (Pubitemid 36627817)
3. Liu, C., Li, Y., Semenov, M., Han, C., Baeg, G. H., Tan, Y., Zhang, Z., Lin, X., and He, X. (2002) Control of β-catenin phosphorylation/degradation by a dual-kinase mechanism. Cell 108, 837-847 (Pubitemid 34327534)
4. Hart, M., Concordet, J. P., Lassot, I., Albert, I., del los Santos, R., Durand, H., Perret, C., Rubinfeld, B., Margottin, F., Benarous, R., and Polakis, P. (1999) The F-box protein β-TrCP associates with phosphorylated β-catenin and regulates its activity in the cell. Curr. Biol. 9, 207-210 (Pubitemid 29120385)
5. Amit, S., Hatzubai, A., Birman, Y., Andersen, J. S., Ben-Shushan, E., Mann, M., Ben-Neriah, Y., and Alkalay, I. (2002) Axin-mediated CKI phosphorylation of β-catenin at Ser-45. A molecular switch for the Wnt pathway. Genes Dev. 16, 1066-1076 (Pubitemid 34507196)
6. Smalley, M. J., Sara, E., Paterson, H., Naylor, S., Cook, D., Jayatilake, H., Fryer, L. G., Hutchinson, L., Fry, M. J., and Dale, T. C. (1999) Interaction of axin and Dvl-2 proteins regulates Dvl-2-stimulated TCF-dependent transcription. EMBO J. 18, 2823-2835 (Pubitemid 29233954)
7. Brunner, E., Peter, O., Schweizer, L., and Basler, K. (1997) Pangolin encodes a Lef-1 homologue that acts downstream of Armadillo to transduce the Wingless signal in Drosophila. Nature 385, 829-833 (Pubitemid 27106074)
8. van de Wetering, M., Cavallo, R., Dooijes, D., van Beest, M., van Es, J., Loureiro, J., Ypma, A., Hursh, D., Jones, T., Bejsovec, A., Peifer, M., Mortin, M., and Clevers, H. (1997) Armadillo coactivates transcription driven by the product of the Drosophila segment polarity gene dTCF. Cell 88, 789-799 (Pubitemid 27164267)
9. Wolf, D., Rodova, M., Miska, E. A., Calvet, J. P., and Kouzarides, T. (2002) Acetylation of β-catenin by CREB-binding protein (CBP). J. Biol. Chem. 277, 25562-25567 (Pubitemid 34951872)
10. Barker, N., van Es, J. H., Kuipers, J., Kujala, P., van den Born, M., Cozijnsen, M., Haegebarth, A., Korving, J., Begthel, H., Peters, P. J., and Clevers, H. (2007) Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 449, 1003-1007 (Pubitemid 350014593)
11. Aravind, L., and Koonin, E. V. (2000) The α/β fold uracil DNA glycosylases. A common origin with diverse fates. Genome Biol. 1, research0007.1-0007.8
12. Neddermann, P., and Jiricny, J. (1993) The purification of a mismatch-specific thymine-DNA glycosylase from HeLa cells. J. Biol. Chem. 268, 21218-21224 (Pubitemid 23292310)
13. Wiebauer, K., and Jiricny, J. (1989) In vitro correction of G.T mispairs to G.C pairs in nuclear extracts from human cells. Nature 339, 234-236 (Pubitemid 19126398)
14. Cortázar, D., Kunz, C., Saito, Y., Steinacher, R., and Schär, P. (2007) The enigmatic thymine DNA glycosylase. DNA Repair 6, 489-504
15. 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., and Bellacosa, A. (2011) Thymine DNA glycosylase is essential for active DNA demethylation by linked deamination-base excision repair. Cell 146, 67-79
16. Gong, Z., and Zhu, J. K. (2011) Active DNA demethylation by oxidation and repair. Cell Res. 21, 1649-1651
17. Wu, S. C., and Zhang, Y. (2010) Active DNA demethylation. Many roads lead to Rome. Nat. Rev. Mol. Cell Biol. 11, 607-620
18. Missero, C., Pirro, M. T., Simeone, S., Pischetola, M., and Di Lauro, R. (2001) The DNA glycosylase T:G mismatch-specific thymine DNA glycosylase represses thyroid transcription factor-1-activated transcription. J. Biol. Chem. 276, 33569-33575
19. Chen, D., Lucey, M. J., Phoenix, F., Lopez-Garcia, J., Hart, S. M., Losson, R., Buluwela, L., Coombes, R. C., Chambon, P., Schär, P., and Ali, S. (2003) T:G mismatch-specific thymine-DNA glycosylase potentiates transcription of estrogen-regulated genes through direct interaction with estrogen receptor α. J. Biol. Chem. 278, 38586-38592 (Pubitemid 37221755)
20. Um, S., Harbers, M., Benecke, A., Pierrat, B., Losson, R., and Chambon, P. (1998) Retinoic acid receptors interact physically and functionally with the T:G mismatch-specific thymine-DNA glycosylase. J. Biol. Chem. 273, 20728-20736 (Pubitemid 28385348)
21. Tini, M., Benecke, A., Um, S. J., Torchia, J., Evans, R. M., and Chambon, P. (2002) Association of CBP/p300 acetylase and thymine DNA glycosylase links DNA repair and transcription. Mol. Cell 9, 265-277 (Pubitemid 34195553)
22. Kim, E. J., and Um, S. J. (2008) Thymine-DNA glycosylase interacts with and functions as a coactivator of p53 family proteins. Biochem. Biophys. Res. Commun. 377, 838-842
23. Sun, W., and Yang, J. (2010) Functional mechanisms for human tumor suppressors. J. Cancer 1, 136-140
24. da Costa, N. M., Hautefeuille, A., Cros, M. P., Melendez, M. E., Waters, T., Swann, P., Hainaut, P., and Pinto, L. F. (2012) Transcriptional regulation of thymine DNA glycosylase (TDG) by the tumor suppressor protein p53. Cell Cycle 11, 4570-4578
25. Vasovcak, P., Krepelova, A., Menigatti, M., Puchmajerova, A., Skapa, P., Augustinakova, A., Amann, G., Wernstedt, A., Jiricny, J., Marra, G., and Wimmer, K. (2012) Unique mutational profile associated with a loss of TDG expression in the rectal cancer of a patient with a constitutional PMS2 deficiency. DNA Repair 11, 616-623
26. Sjolund, A. B., Senejani, A. G., and Sweasy, J. B. (2012) MBD4 and TDG. Multifaceted DNA glycosylases with ever expanding biological roles. Mutat. Res. 743-744, 12-25
27. Bhakat, K. K., Hazra, T. K., and Mitra, S. (2004) Acetylation of the human DNA glycosylase NEIL2 and inhibition of its activity. Nucleic Acids Res. 32, 3033-3039 (Pubitemid 39022994)
28. Evans, P. M., Zhang, W., Chen, X., Yang, J., Bhakat, K. K., and Liu, C. (2007) Krüppel-like factor 4 is acetylated by p300 and regulates gene transcription via modulation of histone acetylation. J. Biol. Chem. 282, 33994 -34002
29. Zhang, W., Chen, X., Kato, Y., Evans, P. M., Yuan, S., Yang, J., Rychahou, P. G., Yang, V. W., He, X., Evers, B. M., and Liu, C. (2006) Novel cross talk of Krüppel-like factor 4 and β-catenin regulates normal intestinal homeostasis and tumor repression. Mol. Cell Biol. 26, 2055-2064 (Pubitemid 43346910)
30. Evans, P. M., and Liu, C. (2005) SiteFind. A software tool for introducing a restriction site as a marker for successful site-directed mutagenesis. BMC Mol. Biol. 6, 22
31. Yang, J., Zhang, W., Evans, P. M., Chen, X., He, X., and Liu, C. (2006) Adenomatous polyposis coli (APC) differentially regulates β-catenin phosphorylation and ubiquitination in colon cancer cells. J. Biol. Chem. 281, 17751-17757 (Pubitemid 44035574)
32. Yu, T., Chen, X., Zhang, W., Colon, D., Shi, J., Napier, D., Rychahou, P., Lu, W., Lee, E. Y., Weiss, H. L., Evers, B. M., and Liu, C. (2012) Regulation of the potential marker for intestinal cells, Bmi1, by β-catenin and the zinc finger protein KLF4. Implications for colon cancer. J. Biol. Chem. 287, 3760-3768
33. Zhang, W., Yang, J., Liu, Y., Chen, X., Yu, T., Jia, J., and Liu, C. (2009) PR55 α, a regulatory subunit of PP2A, specifically regulates PP2A-mediated β-catenin dephosphorylation. J. Biol. Chem. 284, 22649-22656
34. Cancer Genome Atlas Network (2012) Comprehensive molecular characterization of human colon and rectal cancer. Nature 487, 330-337
35. Smith, J. J., Deane, N. G., Wu, F., Merchant, N. B., Zhang, B., Jiang, A., Lu, P., Johnson, J. C., Schmidt, C., Bailey, C. E., Eschrich, S., Kis, C., Levy, S., Washington, M. K., Heslin, M. J., Coffey, R. J., Yeatman, T. J., Shyr, Y., and Beauchamp, R. D. (2010) Experimentally derived metastasis gene expression profile predicts recurrence and death in patients with colon cancer. Gastroenterology 138, 958-968
36. Ji, J., Liu, R., Tong, T., Song, Y., Jin, S., Wu, M., and Zhan, Q. (2007) Gadd45a regulates β-catenin distribution and maintains cell-cell adhesion/ contact. Oncogene 26, 6396-6405 (Pubitemid 47494222)
37. Smet-Nocca, C., Wieruszeski, J. M., Chaar, V., Leroy, A., and Benecke, A. (2008) The thymine-DNA glycosylase regulatory domain. Residual structure and DNA binding. Biochemistry 47, 6519-6530 (Pubitemid 351874279)
38. Waters, T. R., Gallinari, P., Jiricny, J., and Swann, P. F. (1999) Human thymine DNA glycosylase binds to apurinic sites in DNA but is displaced by human apurinic endonuclease 1. J. Biol. Chem. 274, 67-74 (Pubitemid 29035031)
39. Wang, F., Marshall, C. B., and Ikura, M. (2013) Transcriptional/ epigenetic regulator CBP/p300 in tumorigenesis. Structural and functional versatility in target recognition. Cell. Mol. Life Sci. 70, 3989-4008
40. Hardeland, U., Bentele, M., Jiricny, J., and Schär, P. (2000) Separating substrate recognition from base hydrolysis in human thymine DNA glycosylase by mutational analysis. J. Biol. Chem. 275, 33449-33456
41. Smet-Nocca, C., Wieruszeski, J. M., Léger, H., Eilebrecht, S., and Benecke, A. (2011) SUMO-1 regulates the conformational dynamics of thymine- DNA glycosylase regulatory domain and competes with its DNA binding activity. BMC Biochem. 12, 4
42. Hardeland, U., Steinacher, R., Jiricny, J., and Schär, P. (2002) Modification of the human thymine-DNA glycosylase by ubiquitin-like proteins facilitates enzymatic turnover. EMBO J. 21, 1456-1464 (Pubitemid 34246524)
43. Mohan, R. D., Rao, A., Gagliardi, J., and Tini, M. (2007) SUMO-1-dependent allosteric regulation of thymine DNA glycosylase alters subnuclear localization and CBP/p300 recruitment. Mol. Cell Biol. 27, 229-243 (Pubitemid 46013247)
44. Greenblatt, M. S., Bennett, W. P., Hollstein, M., and Harris, C. C. (1994) Mutations in the p53 tumor suppressor gene. Clues to cancer etiology and molecular pathogenesis. Cancer Res. 54, 4855-4878 (Pubitemid 24289415)
45. Cortázar, 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., and Schär, P. (2011) Embryonic lethal phenotype reveals a function of TDG in maintaining epigenetic stability. Nature 470, 419-423