E2-mediated small ubiquitin-like modifier (SUMO) modification of thymine DNA glycosylase is efficient but not selective for the enzyme-product complex

Journal of Biological Chemistry

Volumn 289, Issue 22, 2014, Pages 15810-15819

  Coey, Christopher T ^a   Fitzgerald, Megan E ^a   Maiti, Atanu ^a   Reiter, Katherine H ^b   Guzzo, Catherine M ^b   Matunis, Michael J ^b   Drohat, Alexander C ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; BIOLOGY;

DNA BINDING; DNA GLYCOSYLASE; IN-VITRO; PRODUCT RELEASE; SMALL UBIQUITIN-LIKE MODIFIERS; SUMOYLATION;

ENZYMES;

SUMO 1 PROTEIN; SUMO 2 PROTEIN; THYMINE DNA GLYCOSYLASE;

ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; ENZYME GLYCOSYLATION; ENZYME MECHANISM; HUMAN; HUMAN CELL; IN VITRO STUDY; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; PROTEIN PURIFICATION; PROTEIN TARGETING; SUMOYLATION;

BASE EXCISION REPAIR (BER); DNA METHYLATION; DNA REPAIR; ENZYME TURNOVER; POST-TRANSLATIONAL MODIFICATION (PTM); SMALL UBIQUITIN-LIKE MODIFIER (SUMO); SUMOYLATION; UBIQUITIN-CONJUGATING ENZYME (E2 ENZYME);

DNA METHYLATION; DNA REPAIR; DNA-BINDING PROTEINS; GLYCOSYLATION; GTPASE-ACTIVATING PROTEINS; HELA CELLS; HUMANS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SMALL UBIQUITIN-RELATED MODIFIER PROTEINS; SUBSTRATE SPECIFICITY; SUMO-1 PROTEIN; SUMOYLATION; THYMINE DNA GLYCOSYLASE; UBIQUITIN-CONJUGATING ENZYMES;

EID: 84901705539     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.572081     Document Type: Article

References (65)

1. Neddermann, P., and Jiricny, J. (1993) The purification of a mismatchspecific thymine-DNA glycosylase from HeLa cells. J. Biol. Chem. 268, 21218-21224
2. Neddermann, P., Gallinari, P., Lettieri, T., Schmid, D., Truong, O., Hsuan, J. J., Wiebauer, K., and Jiricny, J. (1996) Cloning and expression of human G/T mismatch-specific thymine-DNA glycosylase. J. Biol. Chem. 271, 12767-12774
3. 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
4. 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
5. Maiti, A., and Drohat, A. C. (2011) Thymine DNA glycosylase can rapidly excise 5-formylcytosine and 5-carboxylcytosine: potential implications for active demethylation of CpG sites. J. Biol. Chem. 286, 35334-35338
6. 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., and Xu, G. L. (2011) Tet-mediated formation of 5-carboxylcytosine and its excision by TDG in mammalian DNA. Science 333, 1303-1307
7. Ito, S., Shen, L., Dai, Q., Wu, S. C., Collins, L. B., Swenberg, J. A., He, C., and Zhang, Y. (2011) Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine. Science 333, 1300-1303
8. Pfaffeneder, T., Hackner, B., Truss, M., Münzel, M., Müller, M., Deiml, C. A., Hagemeier, C., and Carell, T. (2011) The discovery of 5-formylcytosine in embryonic stem cell DNA. Angew. Chem. Int. Ed. Engl. 50, 7008-7012
9. Song, C. X., Szulwach, K. E., Dai, Q., Fu, Y., Mao, S. Q., Lin, L., Street, C., Li, Y., Poidevin, M., Wu, H., Gao, J., Liu, P., Li, L., Xu, G. L., Jin, P., and He, C. (2013) Genome-wide profiling of 5-formylcytosine reveals its roles in epigenetic priming. Cell 153, 678-691
10. Shen, L., Wu, H., Diep, D., Yamaguchi, S., D'Alessio, A. C., Fung, H. L., Zhang, K., and Zhang, Y. (2013) Genome-wide analysis reveals TET- and TDG-dependent 5-methylcytosine oxidation dynamics. Cell 153, 692-706
11. Waters, T. R., and Swann, P. F. (1998) Kinetics of the action of thymine DNA glycosylase. J. Biol. Chem. 273, 20007-20014
12. 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
13. Steinacher, R., and Schär, P. (2005) Functionality of human thymine DNA glycosylase requires SUMO-regulated changes in protein conformation. Curr. Biol. 15, 616-623
14. Fitzgerald, M. E., and Drohat, A. C. (2008) Coordinating the initial steps of base excision repair: apurinic/apyrimidinic endonuclease 1 actively stimulates thymine DNA glycosylase by disrupting the product complex. J. Biol. Chem. 283, 32680-32690
15. Schärer, O. D., Nash, H. M., Jiricny, J., Laval, J., and Verdine, G. L. (1998) Specific binding of a designed pyrrolidine abasic site analog to multiple DNA glycosylases. J. Biol. Chem. 273, 8592-8597
16. 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
17. Baba, D., Maita, N., Jee, J. G., Uchimura, Y., Saitoh, H., Sugasawa, K., Hanaoka, F., Tochio, H., Hiroaki, H., and Shirakawa, M. (2005) Crystal structure of thymine DNA glycosylase conjugated to SUMO-1. Nature 435, 979-982
18. Baba, D., Maita, N., Jee, J. G., Uchimura, Y., Saitoh, H., Sugasawa, K., Hanaoka, F., Tochio, H., Hiroaki, H., and Shirakawa, M. (2006) Crystal structure of SUMO-3-modified thymine-DNA glycosylase. J. Mol. Biol. 359, 137-147
19. Schärer, O. D., Kawate, T., Gallinari, P., Jiricny, J., and Verdine, G. L. (1997) Investigation of the mechanisms of DNA binding of the human G/T glycosylase using designed inhibitors. Proc. Natl. Acad. Sci. U.S.A. 94, 4878-4883
20. Morgan, M. T., Maiti, A., Fitzgerald, M. E., and Drohat, A. C. (2011) Stoichiometry and affinity for thymine DNA glycosylase binding to specific and nonspecific DNA. Nucleic Acids Res. 39, 2319-2329
21. Maiti, A., Noon, M. S., MacKerell, A. D., Jr., Pozharski, E., and Drohat, A. C. (2012) 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. 109, 8091-8096
22. Johnson, E. S. (2004) Protein modification by SUMO. Annu. Rev. Biochem. 73, 355-382
23. Geiss-Friedlander, R., and Melchior, F. (2007) Concepts in sumoylation: a decade on. Nat. Rev. Mol. Cell Biol. 8, 947-956
24. Sjolund, A. B., Senejani, A. G., and Sweasy, J. B. (2013) MBD4 and TDG: multifaceted DNA glycosylases with ever expanding biological roles. Mutat. Res. 743, 12-25
25. Pilla, E., Möller, U., Sauer, G., Mattiroli, F., Melchior, F., and Geiss-Friedlander, R. (2012) A novel SUMO1-specific interacting motif in dipeptidyl peptidase 9 (DPP9) that is important for enzymatic regulation. J. Biol. Chem. 287, 44320-44329
26. Matunis, M. J., Coutavas, E., and Blobel, G. (1996) A novel ubiquitin-like modification modulates the partitioning of the Ran-GTPase-activating protein RanGAP1 between the cytosol and the nuclear pore complex. J. Cell Biol. 135, 1457-1470
27. Mahajan, R., Delphin, C., Guan, T., Gerace, L., and Melchior, F. (1997) A small ubiquitin-related polypeptide involved in targeting RanGAP1 to nuclear pore complex protein RanBP2. Cell 88, 97-107
28. Bergink, S., and Jentsch, S. (2009) Principles of ubiquitin andSUMOmodifications in DNA repair. Nature 458, 461-467
29. Flotho, A., and Melchior, F. (2013) Sumoylation: a regulatory protein modification in health and disease. Annu. Rev. Biochem. 82, 357-385
30. Liu, X. M., Yang, F. F., Yuan, Y. F., Zhai, R., and Huo, L. J. (2013) SUMOylation of mouse p53b by SUMO-1 promotes its pro-apoptotic function in ovarian granulosa cells. PLoS One 8, e63680
31. Müller, S., Matunis, M. J., and Dejean, A. (1998) Conjugation with the ubiquitin-related modifier SUMO-1 regulates the partitioning of PML within the nucleus. EMBO J. 17, 61-70
32. Takahashi, H., Hatakeyama, S., Saitoh, H., and Nakayama, K. I. (2005) Noncovalent SUMO-1 binding activity of thymine DNA glycosylase (TDG) is required for its SUMO-1 modification and colocalization with the promyelocytic leukemia protein. J. Biol. Chem. 280, 5611-5621
33. Zhang, H., Saitoh, H., and Matunis, M. J. (2002) Enzymes of the SUMO modification pathway localize to filaments of the nuclear pore complex. Mol. Cell. Biol. 22, 6498-6508
34. Werner, A., Moutty, M. C., Möller, U., and Melchior, F. (2009) Performing in vitro sumoylation reactions using recombinant enzymes. Methods Mol. Biol. 497, 187-199
35. Zhu, J., Zhu, S., Guzzo, C. M., Ellis, N. A., Sung, K. S., Choi, C. Y., and Matunis, M. J. (2008) Small ubiquitin-related modifier (SUMO) binding determines substrate recognition and paralog-selective SUMO modification. J. Biol. Chem. 283, 29405-29415
36. Morgan, M. T., Bennett, M. T., and Drohat, A. C. (2007) Excision of 5-halogenated uracils by human thymine DNA glycosylase: robust activity for DNA contexts other than CpG. J. Biol. Chem. 282, 27578-27586
37. Uchimura, Y., Nakamura, M., Sugasawa, K., Nakao, M., and Saitoh, H. (2004) Overproduction of eukaryotic SUMO-1- and SUMO-2-conjugated proteins in Escherichia coli. Anal. Biochem. 331, 204-206
38. Maiti, A., and Drohat, A. C. (2011) 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 10, 545-553
39. Maiti, A., Morgan, M. T., and Drohat, A. C. (2009) Role of two strictly conserved residues in nucleotide flipping and N-glycosylic bond cleavage by human thymine DNA glycosylase. J. Biol. Chem. 284, 36680-36688
40. Scheffner, M., Huibregtse, J. M., and Howley, P. M. (1994) Identification of a human ubiquitin-conjugating enzyme that mediates the E6-AP-dependent ubiquitination of p53. Proc. Natl. Acad. Sci. U.S.A. 91, 8797-8801
41. Maiti, A., Michelson, A. Z., Armwood, C. J., Lee, J. K., and Drohat, A. C. (2013) Divergent mechanisms for enzymatic excision of 5-formylcytosine and 5-carboxylcytosine from DNA. J. Am. Chem. Soc. 135, 15813-15822
42. 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
43. Gareau, J. R., and Lima, C. D. (2010) The SUMO pathway: emerging mechanisms that shape specificity, conjugation, and recognition. Nat. Rev. Mol. Cell Biol. 11, 861-871
44. Tatham, M. H., Kim, S., Yu, B., Jaffray, E., Song, J., Zheng, J., Rodriguez, M. S., Hay, R. T., and Chen, Y. (2003) Role of an N-terminal site of Ubc9 in SUMO-1, -2, and -3 binding and conjugation. Biochemistry 42, 9959-9969
45. Yunus, A. A., and Lima, C. D. (2006) Lysine activation and functional analysis of E2-mediated conjugation in the SUMO pathway. Nat. Struct. Mol. Biol. 13, 491-499
46. Zilio, N., Williamson, C. T., Eustermann, S., Shah, R., West, S. C., Neuhaus, D., and Ulrich, H. D. (2013) DNA-dependentSUMOmodification of PARP-1. DNA Repair 12, 761-773
47. Hickey, C. M., Wilson, N. R., and Hochstrasser, M. (2012) Function and regulation of SUMO proteases. Nat. Rev. Mol. Cell Biol. 13, 755-766
48. Yunus, A. A., and Lima, C. D. (2009) Purification of SUMO-conjugating enzymes and kinetic analysis of substrate conjugation. Methods Mol. Biol. 497, 167-186
49. Yunus, A. A., and Lima, C. D. (2005) Purification and activity assays for Ubc9, the ubiquitin-conjugating enzyme for the small ubiquitin-like modifier SUMO. Methods Enzymol. 398, 74-87
50. Mohideen, F., Capili, A. D., Bilimoria, P. M., Yamada, T., Bonni, A., and Lima, C. D. (2009) A molecular basis for phosphorylation-dependent SUMO conjugation by the E2 UBC9. Nat. Struct. Mol. Biol. 16, 945-952
51. Psakhye, I., and Jentsch, S. (2012) Protein group modification and synergy in the SUMO pathway as exemplified in DNA repair. Cell 151, 807-820
52. 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
53. Bernier-Villamor, V., Sampson, D. A., Matunis, M. J., and Lima, C. D. (2002) Structural basis for E2-mediated SUMO conjugation revealed by a complex between ubiquitin-conjugating enzyme Ubc9 and RanGAP1. Cell 108, 345-356
54. 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
55. Hock, A., and Vousden, K. H. (2010) Regulation of the p53 pathway by ubiquitin and related proteins. Int. J. Biochem. Cell Biol. 42, 1618-1621
56. Stindt, M. H., Carter, S., Vigneron, A. M., Ryan, K. M., and Vousden, K. H. (2011) MDM2 promotes SUMO-2/3 modification of p53 to modulate transcriptional activity. Cell Cycle 10, 3176-3188
57. 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
58. 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
59. 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., Chambon, P., Parker, M. G., Schär, P., Heery, D. M., Buluwela, L., and Ali, S. (2005) 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. 33, 6393-6404
60. Chevray, P. M., and Nathans, D. (1992) Protein interaction cloning in yeast: identification of mammalian proteins that react with the leucine zipper of Jun. Proc. Natl. Acad. Sci. U.S.A. 89, 5789-5793
61. Xu, X., Yu, T., Shi, J., Chen, X., Zhang, W., Lin, T., Liu, Z., Wang, Y., Zeng, Z., Wang, C., Li, M., and Liu, C. (2014) Thymine DNA glycosylase is a positive regulator of Wnt signaling in colorectal cancer. J. Biol. Chem. 13, 8881-8890
62. Choi, S. J., Chung, S. S., Rho, E. J., Lee, H. W., Lee, M. H., Choi, H. S., Seol, J. H., Baek, S. H., Bang, O. S., and Chung, C. H. (2006) Negative modulation of RXRα transcriptional activity by small ubiquitin-related modifier (SUMO) modification and its reversal by SUMO-specific protease SUSP1. J. Biol. Chem. 281, 30669-30677
63. Muller, S., Berger, M., Lehembre, F., Seeler, J. S., Haupt, Y., and Dejean, A. (2000) c-Jun and p53 activity is modulated by SUMO-1 modification. J. Biol. Chem. 275, 13321-13329
64. Bossis, G., Malnou, C. E., Farras, R., Andermarcher, E., Hipskind, R., Rodriguez, M., Schmidt, D., Muller, S., Jariel-Encontre, I., and Piechaczyk, M. (2005) Down-regulation of c-Fos/c-Jun AP-1 dimer activity by sumoylation. Mol. Cell. Biol. 25, 6964-6979
65. Sentis, S., Le Romancer, M., Bianchin, C., Rostan, M. C., and Corbo, L. (2005) Sumoylation of the estrogen receptor α hinge region regulates its transcriptional activity. Mol. Endocrinol. 19, 2671-2684