Proteomic approach to identification of proteins reactive for abasic sites in DNA

Molecular and Cellular Proteomics

Volumn 5, Issue 5, 2006, Pages 858-867

  Rieger, Robert A ^a   Zaika, Elena I ^a,c   Xie, Weiping ^a   Johnson, Francis ^a   Grollman, Arthur P ^a   Iden, Charles R ^a   Zharkov, Dmitry O ^b  

^a STONY BROOK UNIVERSITY   (United States)

^b NOVOSIBIRSK STATE UNIVERSITY   (Russian Federation)

^c UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 DEHYDRO 3 DEOXYPHOSPHOHEPTONATE ALDOLASE; DNA; DNA DIRECTED DNA POLYMERASE BETA; DNA FORMAMIDOPYRIMIDINE GLYCOSYLASE; ELONGATION FACTOR TU; ESCHERICHIA COLI PROTEIN; EXINUCLEASE ABC SUBUNIT A; PROTEIN ARC1; PROTEIN DNAK; PROTEIN REQUIRED FOR YEAST VIABILITY; SACCHAROMYCES CEREVISIAE PROTEIN; SODIUM BOROHYDRIDE; TRYPTOPHANASE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; APURINIC SITE; APYRIMIDINIC SITE; ARTICLE; BACTERIAL CELL; BINDING AFFINITY; CONTROLLED STUDY; DNA REPAIR; ESCHERICHIA COLI; FUNCTIONAL PROTEOMICS; FUNGAL CELL; FUNGAL STRAIN; MASS SPECTROMETRY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN CROSS LINKING; PROTEIN PROTEIN INTERACTION; SACCHAROMYCES CEREVISIAE; SENSITIVITY ANALYSIS; SEQUENCE ANALYSIS;

CELL EXTRACTS; CROSS-LINKING REAGENTS; DNA; DNA-BINDING PROTEINS; ESCHERICHIA COLI; PROTEOMICS; SACCHAROMYCES CEREVISIAE; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; STREPTAVIDIN;

ESCHERICHIA COLI; EUKARYOTA; PROKARYOTA;

EID: 33646912434     PISSN: 15359476     EISSN: None     Source Type: Journal    
DOI: 10.1074/mcp.M500224-MCP200     Document Type: Article

References (64)

1. Friedberg, E. C., Walker, G. C., and Siede, W. (1995) DNA Repair and Mutagenesis, 2nd Ed., American Society for Microbiology (ASM) Press, Washington, D. C.
2. Lindahl, T., and Nyberg, B. (1972) Rate of depurination of native deoxyribonucleic acid. Biochemistry 11, 3610-3618
3. Nakamura, J., Walker, V. E., Upton, P. B., Chiang, S. Y., Kow, Y. W., and Swenberg, J. A. (1998) Highly sensitive apurinic/apyrimidinic site assay can detect spontaneous and chemically induced depurination under physiological conditions. Cancer Res. 58, 222-225
4. Atamna, H., Cheung, I., and Ames, B. N. (2000) A method for detecting abasic sites in living cells: age-dependent changes in base excision repair. Proc. Natl. Acad. Sci. U. S. A. 97, 686-691
5. Rivero, M. T., Vázquez-Gundín, F., Goyanes, V., Campos, A., Blasco, M., Gosálvez, J., and Fernández, J. L. (2001) High frequency of constitutive alkali-labile sites in mouse major satellite DNA, detected by DNA breakage detection-fluorescence in situ hybridization. Mutat. Res. 483, 43-50
6. Kubo, K., Ide, H., Wallace, S. S., and Kow, Y. W. (1992) A novel sensitive and specific assay for abasic sites, the most commonly produced DNA lesion. Biochemistry 31, 3703-3708
7. Burrows, C. J., and Muller, J. G. (1998) Oxidative nucleobase modifications leading to strand scission. Chem. Rev. 98, 1109-1151
8. Loeb, L. A., and Preston, B. D. (1986) Mutagenesis by apurinic/ apyrimidinic sites. Annu. Rev. Genet. 20, 201-230
9. Krokan, H. E., Nilsen, H., Skorpen, F., Ofterlei, M., and Slupphaug, G. (2000) Base excision repair of DNA in mammalian cells. FEBS Lett. 476, 73-77
10. David, S. S., and Williams, S. D. (1998) Chemistry of glycosylases and endonucleases involved in base-excision repair. Chem. Rev. 98, 1221-1261
11. McCullough, A. K., Dodson, M. L., and Lloyd, R. S. (1999) Initiation of base excision repair: glycosylase mechanisms and structures. Annu, Rev. Biochem. 68, 255-285
12. Sun, B., Latham, K. A., Dodson, M. L., and Lloyd, R. S. (1995) Studies of the catalytic mechanism of five DNA glycosylases. Probing for enzyme-DNA imino intermediates. J. Biol. Chem. 270, 19501-19508
13. Zharkov, D. O., and Grollman, A. P. (1998) MutY DNA glycosylase: base release and intermediate complex formation. Biochemistry 37, 12384-12394
14. Pourquier, P., Ueng, L.-M., Kohlhagen, G., Mazumder, A., Gupta, M., Kohn, K. W., and Pommier, Y. (1997) Effects of uracil incorporation, DNA mismatches, and abasic sites on cleavage and religation activities of mammalian topoisomerase I. J. Biol. Chem. 272, 7792-7796
15. Paz-Elizur, T., Takeshita, M., Goodman, M., O'Donnell, M., and Livneh, Z. (1996) Mechanism of translesion DNA synthesis by DNA polymerase II. Comparison to DNA polymerases I and III core. J. Biol. Chem, 271, 24662-24669
16. Paz-Elizur, T., Takeshita, M., and Livneh, Z. (1997) Mechanism of bypass synthesis through an abasic site analog by DNA polymerase I. Biochemistry 36, 1766-1773
17. Yu, S.-L., Lee, S.-K., Johnson, R. E., Prakash, L., and Prakash, S. (2003) The stalling of transcription at abasic sites is highly mutagenic. Mol Cell. Biol. 23, 382-388
18. Piersen, C. E., Prasad, R., Wilson, S. H., and Lloyd, R. S. (1996) Evidence for an imino intermediate in the DNA polymerase β deoxyribose phosphate excision reaction. J. Biol. Chem. 271, 17811-17815
19. Pinz, K. G., and Bogenhagen, D. F. (2000) Characterization of a catalytically slow AP Iyase activity in DNA polymerase γ and other family A DNA polymerases. J. Biol. Chem. 275, 12509-12514
20. Mazumder, A., Neamati, N., Pilon, A. A., Sunder, S., and Pommier, Y. (1996) Chemical trapping of ternary complexes of human immunodeficiency virus type 1 integrase, divalent metal, and DNA substrates containing an abasic site. Implications for the role of lysine 136 in DNA binding. J, Biol. Chem. 271, 27330-27338
21. Yang, A. S., Shen, J.-C., Zingg, J.-M., Mi, S., and Jones, P. A. (1995) Hhal and Hpall DNA methyltransferases bind DNA mismatches, methylate uracil and block DNA repair. Nucleic Acids Res. 23, 1380-1387
22. Bogenhagen, D. F., and Pinz, K. G. (1998) The action of DNA ligase at abasic sites in DNA. J. Biol. Chem. 273, 7888-7893
23. Nicolas, E., Beggs, J. M., Haltiwanger, B. M., and Taraschi, T. F. (1998) A new class of DNA glycosylase/apurinic/apyrimidinic Iyases that act on specific adenines in single-stranded DNA. J. Biol. Chem. 273, 17216-17220
24. Wang, Y.-X., Neamati, N., Jacob, J., Palmer, I., Stahl, S. J., Kaufman, J. D., Huang, P. L., Huang, P. L., Winslow, H. E., Pommier, Y., Wingfield, P. T., Lee-Huang, S., Bax, A., and Torchia, D. A. (1999) Solution structure of anti-HIV-1 and anti-tumor protein MAP30: structural insights into its multiple functions. Cell 99, 433-442
25. Nicolas, E., Beggs, J. M., and Taraschi, T. F. (2000) Gelonin is an unusual DNA glycosylase that removes adenine from single-stranded DNA, normal base pairs and mismatches. J. Biol. Chem. 275, 31399-31406
26. Brigotti, M., Accorsi, P., Carnicelli, D., Rizzi, S., Vara, A. G., Montanaro, L., and Sperti, S. (2001) Shiga toxin 1: damage to DNA in vitro. Toxicon 39, 341-348
27. Yacoub, A., Augeri, L., Kelley, M. R., Doetsch, P. W., and Deutsch, W. A. (1996) A Drosophila ribosomal protein contains 8-oxoguanine and abasic site DNA repair activities. EMBO J. 15, 2306-2312
28. Hegde, V., Wang, M., and Deutsch, W. A. (2004) Characterization of human ribosomal protein S3 binding to 7,8-dihydro-8-oxoguanine and abasic sites by surface plasmon resonance. DNA Repair 3, 121-126
29. Postal, E. H., Abramczyk, B. M., Levit, M. N., and Kyin, S. (2000) Catalysis of DNA cleavage and nucleoside triphosphate synthesis by NM23-H2/ NDP kinase share an active site that implies a DNA repair function. Proc. Natl. Acad. Sci. U. S. A. 97, 14194-14199
30. Shishkina, I. G., and Johnson, F. (2000) A new method for the postsynthetic generation of abasic sites in oligomeric DNA. Chem. Res. Toxicol. 13, 907-912
31. Rieger, R. A., McTigue, M. M., Kycia, J. H., Gerchman, S. E., Grollman, A. P., and Iden, C. R. (2000) Characterization of a cross-linked DNA-endonuclease Vill repair complex by electrospray ionization mass spectrometry. J. Am. Soc. Mass Spectrom. 11, 505-515
32. Gilboa, R., Zharkov, D. O., Golan, G., Fernandes, A. S., Gerchman, S.E., Matz, E., Kycia, J. H., Grollman, A. P., and Shoham, G. (2002) Structure of formamidopyrimidine-DNA glycosylase covalently complexed to DNA. J. Biol. Chem. 277,19811-19816
33. 2-terminal proline acts as a nucleophile in the glycosylase /AP-lyase reaction catalyzed by Escherichia coli formamidopyrimidine-DNA glyco-sylase (Fpg) protein. J. Biol. Chem. 272, 5335-5341
34. Aebersold, R., and Goodlett, D. R. (2001) Mass spectrometry in proteomics. Chem. Rev. 101, 269-295
35. Kinter, M., and Sherman, N. E. (2000) Protein Sequencing and Identification Using Tandem Mass Spectrometry, Wiley-Interscience, New York
36. Yates, J. R., III, Speicher, S., Griffin, P. R., and Hunkapiller, T. (1993) Peptide mass maps: a highly informative approach to protein identification. Anal. Biochem. 214, 397-408
37. Pappin, D. J. (1997) Peptide mass fingerprinting using MALDI-TOF mass spectrometry. Methods Mol. Biol. 64, 165-173
38. Marchler-Bauer, A., Panchenko, A. R., Shoemaker, B. A., Thiessen, P. A., Geer, L. Y., and Bryant, S. H. (2002) CDD: a database of conserved domain alignments with links to domain three-dimensional structure. Nucleic Acids Res. 30, 281-283
39. Parikh, S. S., Mol, C. D., Slupphaug, G., Bharati, S., Krokan, H. E., and Tainer, J. A. (1998) Base excision repair initiation revealed by crystal structures and binding kinetics of human uracil-DNA glycosylase with DNA. EMBO J. 17, 5214-5226
40. Rayment, I. (1997) Reductive alkylation of lysine residues to alter crystallization properties of proteins. Methods Enzymol. 276, 171-179
41. Cocuzza, A. J. (1989) A phosphoramidite reagent for automated solid-phase synthesis of 5′-biotinylated oligonucleotides. Tetrahedron Lett. 30, 6287-6290
42. Rehman, F. N., Audeh, M., Abrams, E. S., Hammond, P. W., Kenney, M., and Boles, T. C. (1999) Immobilization of acrylamide-modified oligonu-cleotides by co-polymerization. Nucleic Acids Res. 27, 649-655
43. Tchou, J., and Grollman, A. P. (1995) The catalytic mechanism of Fpg protein. Evidence for a Schiff base intermediate and amino terminus localization of the catalytic site. J. Biol. Chem. 270, 11671-11677
44. Prasad, R., Beard, W. A., Strauss, P. R., and Wilson, S. H. (1998) Human DNA polymerase β deoxyribose phosphate Iyase. Substrate specificity and catalytic mechanism. J. Biol. Chem. 273, 15263-15270
45. Tettelin, H., Agostoni Carbone, M. L., Albermann, K., Albers, M., Arroyo, J., Backes, U., Barreiros, T., Bertani, I., Bjourson, A. J., Bruckner, M., Bruschi, C. V., Carignani, G., Castagnoli, L., Cerdan, E., Clemente, M. L., Coblenz, A., Coglievina, M., Coissac, E., Defoor, E., Del Bino, S., Delius, H., Delneri, D., de Wergifosse, P., Dujon, B., et al. (1997) The nucleotide sequence of Saccharomyces cerevisiae chromosome VII. Nature 387, S81-S84
46. Gavin, A. C., Bosche, M., Krause, R., Grandi, P., Marzioch, M., Bauer, A., Schultz, J., Rick, J. M., Michon, A. M., Cruciat, C. M., Remor, M., Hofert, C., Schelder, M., Brajenovic, M., Ruffner, H., Merino, A., Klein, K., Hudak, M., Dickson, D., Rudi, T., Gnau, V., Bauch, A., Bastuck, S., Huhse, B., Leutwein, C., Heurtier, M. A., Copley, R. R., Edelmann, A., Querfurth, E., Rybin, V., Drewes, G., Raida, M., Bouwmeester, T., Bork, P., Seraphin, B., Kuster, B., Neubauer, G., and Superti-Furga, G. (2002) Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature 415, 141-147
47. Ho, Y., Gruhler, A., Heilbut, A., Bader, G. D., Moore, L., Adams, S. L., Millar, A., Taylor, P., Bennett, K., Boutilier, K., Yang, L., Wolting, C., Donaldson, I., Schandorff, S., Shewnarane, J., Vo, M., Taggart, J., Goudreault, M., Muskat, B., Alfarano, C., Dewar, D., Lin, Z., Michalickova, K., Willems, A. R., Sassi, H., Nielsen, P. A., Rasmussen, K. J., Andersen, J. R., Johansen, L. E., Hansen, L. H., Jespersen, H., Podtelejnikov, A., Nielsen, E., Crawford, J., Poulsen, V., Sorensen, B. D., Matthiesen, J., Hendrickson, R. C., Gleeson, F., Pawson, T., Moran, M. F., Durocher, D., Mann, M., Hogue, C. W., Figeys, D., and Tyers, M. (2002) Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry. Nature 415, 180-183
48. Nyberg, K. A., Michelson, R. J., Putnam, C. W., and Weinert, T. A. (2002) Toward maintaining the genome: DNA damage and replication check-points. Annu. Rev. Genet. 36, 617-656
49. Higuchi, K., Katayama, T., Iwai, S., Hidaka, M., Horiuchi, T., and Maki, H. (2003) Fate of DNA replication fork encountering a single DNA lesion during oriC plasmid DNA replication in vitro. Genes Cells 8, 437-449
50. Snowden, A., Kow, Y. W., and Van Houten, B. (11990) Damage repertoire of the Escherichia coli UvrABC nuclease complex includes abasic sites, base-damage analogues, and lesions containing adjacent 5′ or 3′ nicks. Biochemistry 29, 7251-7259
51. Kim, J., Chubatsu, L. S., Admon, A., Stahl, J., Fellous, R., and Linn, S. (1995) Implication of mammalian ribosomal protein S3 in the processing of DNA damage. J. Biol. Chem. 270, 13620-13629
52. Sandigursky, M., Yacoub, A., Kelley, M. R., Deutsch, W. A., and Franklin, W. A. (1997) The Drosophile ribosomal protein S3 contains a DNA deoxyribophosphodiesterase (dRpase) activity. J. Biol. Chem. 272, 17480-17484
53. Hegde, V., Kelley, M. R., Xu, Y., Mian, I. S., and Deutsch, W. A. (2001) Conversion of the bifunctional 8-oxoguanine/β-8 apurinic /apyrimidinic DNA repair activities of Drosophila ribosomal protein S3 into the human S3 monofunctional β-elimination catalyst through a single amino acid change. J. Biol, Chem. 276, 27591-27596
54. Kelley, M. R., Tritt, R., Xu, Y., New, S., Freie, B., Clapp, D. W., and Deutsch, W. A. (2001) The Drosophila S3 multifunctional DNA repair/ ribosomal protein protects Fanconi anemia cells against oxidative DNA damaging agents. Mutat. Res. 485,107-119
55. Cappelli, E., D'Osualdo, A., Bogliolo, M., Kelley, M. R., and Frosina, G. (2003) Drosophila S3 ribosomal protein accelerates repair of 8-oxoguanine performed by human and mouse cell extracts. Environ. Mol. Mutagen 42, 50-58
56. Kenny, M. K., Mendez, F., Sandigursky, M., Kureekattil, R. P., Goldman, J. D., Franklin, W. A., and Bases, R. (2001) Heat shock protein 70 binds to human apurinic/apyrimidinic endonuclease and stimulates endonuclease activity at abasic sites. J. Biol. Chem. 276, 9532-9536
57. Mendez, F., Sandigursky, M., Kureekattil, R. P., Kenny, M. K., Franklin, W. A., and Bases, R. (2003) Specific stimulation of human apurinic/ apyrimidinic endonuclease by heat shock protein 70. DNA Repair 2, 259-271
58. Boiteux, S., O'Connor, T. R., Lederer, F., Gouyette, A., and Laval, J. (1990) Homogeneous Escherichia coli FPG protein. A DNA glycosylase which excises imidazole ring-opened purines and nicks DNA at apurinic/ apyrimidinic sites. J. Biol. Chem. 265, 3916-3922
59. Jacobson, G. R., and Rosenbusch, J. P. (1976) Abundance and membrane association of elongation factor Tu in E. coli. Nature 261, 23-26
60. Ayadi, L., Coulombeau, C., and Lavery, R. (2000) The impact of abasic sites on DNA flexibility. J. Biomol. Struct. Dyn. 17, 645-653
61. Barsky, D., Foloppe, N., Ahmadia, S., Wilson, O. M., III, and MacKerell, A. D., Jr (2000) New insights into the structure of abasic DNA from molecular dynamics simulations. Nucleic Acids Res. 28, 2613-2626
62. Rhodes, D., Schwabe, J. W. R., Chapman, L., and Fairall, L. (1996) Towards an understanding of protein-DNA recognition. Philos. Trans. Biol. Sci. 351, 501-509
63. Bugreev, D. V., Baranova, S., Zakharova, 0. D., Parissi, V., Desjobert, C., Sottofattori, E., Balbi, A., Litvak, S., Tarrago-Litvak, L., and Nevinsky, G. A. (2003) Dynamic, thermodynamic, and kinetic basis for recognition and transformation of DNA by human immunodeficiency virus type 1 integrase. Biochemistry 42, 9235-9247
64. Kroeger, K. M., Hashimoto, M., Kow, Y. W., and Greenberg, M. M. (2003) Cross-linking of 2-deoxyribonolactone and its β-elimination product by base excision repair enzymes. Biochemistry 42, 2449-2455