Quantitative characterization of protein-protein complexes involved in base excision DNA repair

Nucleic Acids Research

Volumn 43, Issue 12, 2015, Pages 6009-6022

  Moor, Nina A ^a   Vasil'eva, Inna A ^a   Anarbaev, Rashid O ^a   Antson, Alfred A ^b   Lavrik, Olga I ^a,c  

^a INSTITUTE OF CHEMICAL BIOLOGY AND FUNDAMENTAL MEDICINE   (Russian Federation)

^b UNIVERSITY OF YORK   (United Kingdom)

^c NOVOSIBIRSK STATE UNIVERSITY   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

DNA (APURINIC OR APYRIMIDINIC SITE) LYASE; DNA DIRECTED DNA POLYMERASE BETA; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; PHOSPHODIESTERASE; TYROSYL DNA PHOSPHODIESTERASE; UNCLASSIFIED DRUG; XRCC1 PROTEIN; APEX1 PROTEIN, HUMAN; DNA; DNA BINDING PROTEIN; DNA LIGASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PARP1 PROTEIN, HUMAN; TDP1 PROTEIN, HUMAN; X-RAY REPAIR CROSS COMPLEMENTING PROTEIN 1;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; BINDING SITE; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DNA BINDING; DNA CLEAVAGE; DNA DAMAGE; DNA SYNTHESIS; ENERGY TRANSFER; ENZYME ACTIVITY; EXCISION REPAIR; FLUORESCENCE; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; ANIMAL; DNA REPAIR; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMAN; LIGHT; METABOLISM; RADIATION SCATTERING; RAT;

ANIMALS; DNA; DNA POLYMERASE BETA; DNA REPAIR; DNA REPAIR ENZYMES; DNA-(APURINIC OR APYRIMIDINIC SITE) LYASE; DNA-BINDING PROTEINS; FLUORESCENCE; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMANS; LIGHT; PHOSPHORIC DIESTER HYDROLASES; POLY(ADP-RIBOSE) POLYMERASES; RATS; SCATTERING, RADIATION;

EID: 84942163162     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv569     Document Type: Article

References (118)

1. Kim, Y.-J. and Wilson, D.M. III (2012) Overview of base excision repair biochemistry. Curr. Mol. Pharmacol., 5, 3-13.
2. Prasad, R., Beard, W.A., Batra, V.K., Liu, Y., Shock, D.D. and Wilson, S.H. (2011) A review of recent experiments on step-to-step 'hand-off' of the DNA intermediates in mammalian base excision repair pathways. Mol. Biol. (Mosk.), 45, 586-600.
3. Caldecott, K.W. (2008) Single-strand break repair and genetic disease. Nat. Rev. Genet., 9, 619-631.
4. Beernink, P.T., Hwang, M., Ramirez, M., Murphy, M.B., Doyle, S.A. and Thelen, M.P. (2005) Specificity of protein interactions mediated by BRCT domains of the XRCC1 DNA repair protein. J. Biol. Chem., 280, 30206-30213.
5. Hanssen-Bauer, A., Solvang-Garten, K., Gilljam, K.M., Torseth, K., Wilson, DM. III, Akbari, M. and Otterlei, M. (2012) The region of XRCC1 which harbours the three most common nonsynonymous polymorphic variants, is essential for the scaffolding function of XRCC1. DNA Repair (Amst.), 11, 357-366.
6. D'Amours, D, Desnoyers, S., D'Silva, I. and Poirier, G.G. (1999) Poly(ADP-ribosyl)ation reactions in the regulation of nuclear functions. Biochem. J., 342, 249-268.
7. Dantzer, F., de La Rubia, G, Ménissier-De Murcia, J., Hostomsky, Z., de Murcia, G and Schreiber, V (2000) Base excision repair is impaired in mammalian cells lacking poly(ADP-ribose) polymerase-1. Biochemistry, 39, 7559-7569.
8. Schreiber, V, Amé, J.C, Dollé, P, Schultz, I., Rinaldi, B., Fraulob, V., Ménissier-de Murcia, J. and de Murcia, G (2002) Poly(ADP-ribose) polymerase-2 (PARP-2) is required for efficient base excision DNA repair in association with PARP-1 and XRCC1. J. Biol. Chem., 277, 23028-23036.
9. Lavrik, O.I., Prasad, R., Sobol, R.W., Horton, J.K., Ackerman, E.J. and Wilson, S.H. (2001) Photoaffinity labeling of mouse fibroblast enzymes by a base excision repair intermediate. Evidence for the role of poly(ADP-ribose) polymerase-1 in DNA repair. J. Biol. Chem., 276, 25541-25548.
10. Sukhanova, M.V., Khodyreva, S.N, Lebedeva, NA, Prasad, R., Wilson, S.H. and Lavrik, O.I. (2005) Human base excision repair enzymes apurinic/apyrimidinic endonuclease1 (APE1), DNA polymerase β and poly(ADP-ribose) polymerase 1: interplay between strand-displacement DNA synthesis and proofreading exonuclease activity. Nucleic Acids Res., 33, 1222-1229.
11. Kutuzov, M.M., Khodyreva, S.N, Amé, J.C, Ilina, E.S., Sukhanova, M.V., Schreiber, V and Lavrik, O.I. (2013) Interaction of PARP-2 with DNA structures mimicking DNA repair intermediates and consequences on activity of base excision repair proteins. Biochimie, 95, 1208-1215.
12. Pommier, Y, Barcelo, J.M., Rao, VA., Sordet, O., Jobson, G, Thibaut, L., Miao, Z.H., Seiler, J.A., Zhang, H, Marchand, C. et al (2006) Repair of topoisomerase I-mediated DNA damage. Prog. Nucleic Acid Res Mol Biol, 81, 179-229.
13. Lebedeva, NA, Rechkunova, NI, Ishchenko, A.A., Saparbaev, M. and Lavrik, O.I. (2013) The mechanism of human tyrosyl-DNA phosphodiesterase 1 in the cleavage of AP site and its synthetic analogs. DNA Repair (Amst.), 12, 1037-1042.
14. Strauss, PR, Beard, W.A., Patterson, TA. and Wilson, S.H. (1997) Substrate binding by human apurinic/apyrimidinic endonuclease indicates a Briggs-Haldane mechanism. J. Biol. Chem., 272, 1302-1307.
15. Kumar, A., Widen, S.G., Williams, K.R., Kedar, P, Karpel, R.L. and Wilson, S.H. (1990) Studies of the domain structure of mammalian DNA polymerase β. Identification of a discrete template binding domain. J. Biol. Chem., 265, 2124-2131.
16. Interthal, H, Pouliot, J.J. and Champoux, J.J. (2001) The tyrosyl-DNA phosphodiesterase Tdp1 is a member of the phospholipase D superfamily. Proc. Natl Acad. Sci. U.S.A., 98, 12009-12014.
17. Belousova, E.A., Vasil'eva, I.A., Moor, NA., Zatsepin, TS., Oretskaya, TS. and Lavrik, O.I. (2013) Clustered DNA lesions containing 5-formyluracil and AP site: repair via the BER system. PLoS One, 8, e68576.
18. Sukhanova, M.V., Khodyreva, SN. and Lavrik, O.I. (2004) Poly(ADP-ribose) polymerase-1 inhibits strand-displacement synthesis of DNA catalyzed by DNA polymerase β. Biochemistry (Mosc.), 69, 558-568.
19. Haugland, R.P (2005) The Handbook - a Guide to Fluorescent Probes and Labeling Technologies, 10th edn. Molecular Probes, Eugene, OR.
20. Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem., 72, 248-254.
21. Blouin, S., Craggs, TD., Lafontaine, D.A. and Penedo, J.C. (2009) Functional studies of DNA-protein interactions using FRET techniques. In: Moss, T and Leblanc, B (eds). Methods in Molecular Biology, DNA-Protein Interactions. Humana Press, NY, Vol. 543, pp. 475-502.
22. Prinz, H. (2010) Hill coefficients, dose-response curves and allosteric mechanisms. J. Biol. Chem., 3, 37-44.
23. Hieb, A.R., D'Arcy, S., Kramer, M.A., White, A.E. and Luger, K. (2012) Fluorescence strategies for high-throughput quantification of protein interactions. Nucleic Acids Res., 40, e33.
24. Lalonde, S., Ehrhardt, D.W., Loqué, D., Chen, J., Rhee, S.Y and Frommer, W.B. (2008) Molecular and cellular approaches for the detection of protein-protein interactions: latest techniques and current limitations. Plant J., 53, 610-635.
25. Wojtuszewski, K., Harvey, J.J., Han, M.K. and Knutson, J.R. (2007) Fluorescence detection of proximity. In: Schuck, P and Atassi, MZ (eds). Protein interactions; biophysical approaches for the study of complex reversible systems. Springer, NY, pp. 367-396.
26. Liu, Y, Prasad, R., Beard, W.A., Kedar, P.S., Hou, E.W., Shock, D.D. and Wilson, S.H. (2007) Coordination of steps in single-nucleotide base excision repair mediated by apurinic/apyrimidinic endonuclease 1 and DNA polymerase β. J. Biol. Chem., 282, 13532-13541.
27. Shall, S. and de Murcia, G. (2000) Poly(ADP-ribose) polymerase-1: what have we learned from the deficient mouse model? Mutat. Res., 460, 1-15.
28. Nazarkina, Z.K., Khodyreva, S.N, Marsin, S., Lavrik, O.I. and Radicella, J.P (2007) XRCC1 interactions with base excision repair DNA intermediates. DNA Repair (Amst.), 6, 54-64.
29. Mani, R.S., Karimi-Busheri, F, Fanta, M., Caldecott, K.W., Cass, C.E. and Weinfeld, M. (2004) Biophysical characterization of human XRCC1 and its binding to damaged and undamaged DNA. Biochemistry, 43, 16505-16514.
30. Khodyreva, S.N., Prasad, R., Ilina, E.S., Sukhanova, M.V, Kutuzov, M.M., Liu, Y, Hou, E.W., Wilson, S.H. and Lavrik, O.I. (2010) Apurinic/apyrimidinic (AP) site recognition by the 5'-dRP/AP lyase in poly(ADP-ribose) polymerase-1 (PARP-1). Proc Natl Acad. Sci. U.S.A., 107, 22090-22095.
31. Some, D (2013) Light-scattering-based analysis of biomolecular interactions. Biophys. Rev., 5, 147-158.
32. Hanssen-Bauer, A., Solvang-Garten, K., Sundheim, O., Pena-Diaz, J., Andersen, S., Slupphaug, G., Krokan, H.E., Wilson, DM. III, Akbari, M. and Otterlei, M. (2011) XRCC1 coordinates disparate responses and multiprotein repair complexes depending on the nature and context of the DNA damage. Environ. Mol. Mutagen., 52, 623-635.
33. Cistulli, C, Lavrik, O.I., Prasad, R., Hou, E. and Wilson, S.H. (2004) AP endonuclease and poly(ADP-ribose) polymerase-1 interact with the same base excision repair intermediate. DNA Repair (Amst.), 3, 581-591.
34. Prasad, R., Williams, J.G., Hou, E.W. and Wilson, S.H. (2012) Pol β associated complex and base excision repair factors in mouse fibroblasts. Nucleic Acids Res., 40, 11571-11582.
35. Das, B.B., Huang, S.Y, Murai, J., Rehman, I., Amé, J.C, Sengupta, S., Das, S.K., Majumdar, P, Zhang, H., Biard, D. et al. (2014) PARP1-TDP1 coupling for the repair of topoisomerase I-induced DNA damage. Nucleic Acids Res., 42, 4435-4449.
36. Das, B.B., Antony, S., Gupta, S., Dexheimer, T.S., Redon, C.E., Garfield, S., Shiloh, Y and Pommier, Y (2009) Optimal function of the DNA repair enzyme TDP1 requires its phosphorylation by ATM and/or DNA-PK. EMBO J., 28, 3667-3680.
37. Chiang, S.C., Carroll, J. and El-Khamisy, S.F (2010) TDP1 serine 81 promotes interaction with DNA ligase IIIa and facilitates cell survival following DNA damage. Cell Cycle, 9, 588-595.
38. Dexheimer, T.S., Antony, S., Marchand, C. and Pommier, Y (2008) Tyrosyl-DNA phosphodiesterase as a target for anticancer therapy. Anticancer Agents Med. Chem., 8, 381-389.
39. Bennett, R.A., Wilson, D.M. III, Wong, D and Demple, B. (1997) Interaction of human apurinic endonuclease and DNA polymerase β in the base excision repair pathway. Proc. Natl Acad. Sci. U.S.A., 94, 7166-7169.
40. Dimitriadis, E.K., Prasad, R., Vaske, M.K., Chen, L., Tomkinson, A.E., Lewis, M.S. and Wilson, S.H. (1998) Thermodynamics of human DNA ligase I trimerization and association with DNA polymerase β. J. Biol. Chem., 273, 20540-20550.
41. Wilson, DM. III and Barsky, D. (2001) The major human abasic endonuclease: formation, consequences and repair of a basic lesions in DNA. Mutat. Res., 485, 283-307.
42. Wilson, S.H., Beard, W.A., Shock, D.D, Batra, VK, Cavanaugh, NA., Prasad, R., Hou, E.W., Liu, Y, Asagoshi, K., Horton, J.K. et al. (2010) Base excision repair and design of small molecule inhibitors of human DNA polymerase β. Cell Mol. Life Sci., 67, 3633-3647.
43. Pleschke, J.M., Kleczkowska, H.E., Strohm, M. and Althaus, FR. (2000) Poly(ADP-ribose) binds to specific domains in DNA damage checkpoint proteins. J. Biol. Chem., 275, 40974-40980.
44. Masson, M., Niedergang, C, Schreiber, V., Muller, S., Menissier-de Murcia, J. and de Murcia, G (1998) XRCC1 is specifically associated with poly(ADP-ribose) polymerase and negatively regulates its activity following DNA damage. Mol. Cell Biol, 18, 3563-3571.
45. Leppard, J.B., Dong, Z., Mackey, Z.B. and Tomkinson, A.E. (2003) Physical and functional interaction between DNA ligase IIIa and poly(ADP-ribose) polymerase 1 in DNA single-strand break repair. Mol. Cell Biol., 23, 5919-5927.
46. El-Khamisy, S.F, Masutani, M., Suzuki, H. and Caldecott, K.W (2003) A requirement for PARP-1 for the assembly or stability of XRCC1 nuclear foci at sites of oxidative DNA damage. Nucleic Acids Res., 31, 5526-5533.
47. Okano, S., Lan, L., Caldecott, K.W., Mori, T and Yasui, A. (2003) Spatial and temporal cellular responses to single-strand breaks in human cells. Mol. Cell Biol, 23, 3974-3981.
48. Kim, I.K., Stegeman, R.A., Brosey, C.A. and Ellenberger, T (2015) A quantitative assay reveals ligand specificity of the DNA scaffold repair protein XRCC1 and efficient disassembly of complexes of XRCC1 and the poly(ADP-ribose) polymerase 1 by poly(ADP-ribose) glycohydrolase. J. Biol. Chem., 290, 3775-3783.
49. Cuneo, M.J. and London, R.E. (2010) Oxidation state of the XRCC1 N-terminal domain regulates DNA polymerase β binding affinity. Proc. Natl Acad. Sci. U.S.A., 107, 6805-6810.
50. Marintchev, A., Robertson, A., Dimitriadis, E.K., Prasad, R., Wilson, S.H. and Mullen, GP (2000) Domain specific interaction in the XRCC1-DNA polymerase β complex. Nucleic Acids Res., 28, 2049-2059.
51. Marintchev, A., Gryk, M.R. and Mullen, GP (2003) Site-directed mutagenesis analysis of the structural interaction of the single-strand-break repair protein, X-ray cross-complementing group 1, with DNA polymerase β. Nucleic Acids Res, 31, 580-588.
52. Luo, H., Chan, D.W., Yang, T, Rodriguez, M., Chen, B.P, Leng, M., Mu, J.J., Chen, D, Songyang, Z., Wang, Y et al. (2004) A new XRCC1-containing complex and its role in cellular survival of methyl methanesulfonate treatment. Mol. Cell Biol, 24, 8356-8365.
53. Lu, M., Mani, R.S., Karimi-Busheri, F, Fanta, M., Wang, H., Litchfeld, DW. and Weinfeld, M. (2010) Independent mechanisms of stimulation of polynucleotide kinase/phosphatase by phosphorylated and non-phosphorylatedXRCC1. Nucleic Acids Res., 38, 510-521.
54. Dianova, I.I., Sleeth, K.M., Allinson, S.L., Parsons, J.L., Breslin, C, Caldecott, K.W. and Dianov, GL. (2004) XRCC1-DNA polymerase β interaction is required for efficient base excision repair. Nucleic Acids Res., 32, 2550-2555.
55. Wong, H.-K. and Wilson, D.M. III (2005) XRCC1 and DNA polymerase β interaction contributes to cellular alkylating-agent resistance and single-strand break repair. J. Cell Biochem., 95, 794-804.
56. Horton, J.K., Stefanick, DF, Gassman, NR., Williams, J.G, Gabel, S.A., Cuneo, M.J., Prasad, R., Kedar, PS., Derose, E.F, Hou, E.W. et al. (2013) Preventing oxidation of cellular XRCC1 affects PARP-mediated DNA damage responses. DNA Repair (Amst.), 12, 774-785.
57. Lan, L., Nakajima, S., Oohata, Y, Takao, M., Okano, S., Masutani, M., Wilson, S.H. and Yasui, A. (2004) In situ analysis of repair processes for oxidative DNA damage in mammalian cells. Proc. Natl Acad. Sci. U.S.A., 101, 13738-13743.
58. Fang, Q., Inanc, B., Schamus, S., Wang, X.H., Wei, L., Brown, A.R., Svilar, D, Sugrue, K.F, Goellner, E.M, Zeng, X. et al. (2014) HSP90 regulates DNA repair via the interaction between XRCC1 and DNA polymerase β. Nat. Commun., 5, 5513.
59. Caldecott, K.W., Tucker, J.D, Stanker, L.H. and Thompson, L.H. (1995) Characterization of the XRCC1-DNA ligase III complex in vitro and its absence from mutant hamster cells. Nucleic Acids Res., 23, 4836-4843.
60. Kim, Y.-J. and Wilson, D.M. III (2012) Overview of base excision repair biochemistry. Curr. Mol. Pharmacol., 5, 3-13.
61. Prasad, R., Beard, W.A., Batra, V.K., Liu, Y., Shock, D.D. and Wilson, S.H. (2011) A review of recent experiments on step-to-step 'hand-off' of the DNA intermediates in mammalian base excision repair pathways. Mol. Biol. (Mosk.), 45, 586-600.
62. Caldecott, K.W. (2008) Single-strand break repair and genetic disease. Nat. Rev. Genet., 9, 619-631.
63. Beernink, P.T., Hwang, M., Ramirez, M., Murphy, M.B., Doyle, S.A. and Thelen, M.P. (2005) Specificity of protein interactions mediated by BRCT domains of the XRCC1 DNA repair protein. J. Biol. Chem., 280, 30206-30213.
64. Hanssen-Bauer, A., Solvang-Garten, K., Gilljam, K.M., Torseth, K., Wilson, DM. III, Akbari, M. and Otterlei, M. (2012) The region of XRCC1 which harbours the three most common nonsynonymous polymorphic variants, is essential for the scaffolding function of XRCC1. DNA Repair (Amst.), 11, 357-366.
65. D'Amours, D, Desnoyers, S., D'Silva, I. and Poirier, G.G. (1999) Poly(ADP-ribosyl)ation reactions in the regulation of nuclear functions. Biochem. J., 342, 249-268.
66. Dantzer, F., de La Rubia, G, Ménissier-De Murcia, J., Hostomsky, Z., de Murcia, G and Schreiber, V (2000) Base excision repair is impaired in mammalian cells lacking poly(ADP-ribose) polymerase-1. Biochemistry, 39, 7559-7569.
67. Schreiber, V, Amé, J.C, Dollé, P, Schultz, I., Rinaldi, B., Fraulob, V., Ménissier-de Murcia, J. and de Murcia, G (2002) Poly(ADP-ribose) polymerase-2 (PARP-2) is required for efficient base excision DNA repair in association with PARP-1 and XRCC1. J. Biol. Chem., 277, 23028-23036.
68. Lavrik, O.I., Prasad, R., Sobol, R.W., Horton, J.K., Ackerman, E.J. and Wilson, S.H. (2001) Photoaffinity labeling of mouse fibroblast enzymes by a base excision repair intermediate. Evidence for the role of poly(ADP-ribose) polymerase-1 in DNA repair. J. Biol. Chem., 276, 25541-25548.
69. Sukhanova, M.V., Khodyreva, S.N, Lebedeva, NA, Prasad, R., Wilson, S.H. and Lavrik, O.I. (2005) Human base excision repair enzymes apurinic/apyrimidinic endonuclease1 (APE1), DNA polymerase β and poly(ADP-ribose) polymerase 1: interplay between strand-displacement DNA synthesis and proofreading exonuclease activity. Nucleic Acids Res., 33, 1222-1229.
70. Kutuzov, M.M., Khodyreva, S.N, Amé, J.C, Ilina, E.S., Sukhanova, M.V., Schreiber, V and Lavrik, O.I. (2013) Interaction of PARP-2 with DNA structures mimicking DNA repair intermediates and consequences on activity of base excision repair proteins. Biochimie, 95, 1208-1215.
71. Pommier, Y, Barcelo, J.M., Rao, VA., Sordet, O., Jobson, G, Thibaut, L., Miao, Z.H., Seiler, J.A., Zhang, H, Marchand, C. et al (2006) Repair of topoisomerase I-mediated DNA damage. Prog. Nucleic Acid Res Mol Biol, 81, 179-229.
72. Lebedeva, NA, Rechkunova, NI, Ishchenko, A.A., Saparbaev, M. and Lavrik, O.I. (2013) The mechanism of human tyrosyl-DNA phosphodiesterase 1 in the cleavage of AP site and its synthetic analogs. DNA Repair (Amst.), 12, 1037-1042.
73. Strauss, PR, Beard, W.A., Patterson, TA. and Wilson, S.H. (1997) Substrate binding by human apurinic/apyrimidinic endonuclease indicates a Briggs-Haldane mechanism. J. Biol. Chem., 272, 1302-1307.
74. Kumar, A., Widen, S.G., Williams, K.R., Kedar, P, Karpel, R.L. and Wilson, S.H. (1990) Studies of the domain structure of mammalian DNA polymerase β. Identification of a discrete template binding domain. J. Biol. Chem., 265, 2124-2131.
75. Interthal, H, Pouliot, J.J. and Champoux, J.J. (2001) The tyrosyl-DNA phosphodiesterase Tdp1 is a member of the phospholipase D superfamily. Proc. Natl Acad. Sci. U.S.A., 98, 12009-12014.
76. Belousova, E.A., Vasil'eva, I.A., Moor, NA., Zatsepin, TS., Oretskaya, TS. and Lavrik, O.I. (2013) Clustered DNA lesions containing 5-formyluracil and AP site: repair via the BER system. PLoS One, 8, e68576.
77. Sukhanova, M.V., Khodyreva, SN. and Lavrik, O.I. (2004) Poly(ADP-ribose) polymerase-1 inhibits strand-displacement synthesis of DNA catalyzed by DNA polymerase β. Biochemistry (Mosc.), 69, 558-568.
78. Haugland, R.P (2005) The Handbook - a Guide to Fluorescent Probes and Labeling Technologies, 10th edn. Molecular Probes, Eugene, OR.
79. Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem., 72, 248-254.
80. Blouin, S., Craggs, TD., Lafontaine, D.A. and Penedo, J.C. (2009) Functional studies of DNA-protein interactions using FRET techniques. In: Moss, T and Leblanc, B (eds). Methods in Molecular Biology, DNA-Protein Interactions. Humana Press, NY, Vol. 543, pp. 475-502.
81. Prinz, H. (2010) Hill coefficients, dose-response curves and allosteric mechanisms. J. Biol. Chem., 3, 37-44.
82. Hieb, A.R., D'Arcy, S., Kramer, M.A., White, A.E. and Luger, K. (2012) Fluorescence strategies for high-throughput quantification of protein interactions. Nucleic Acids Res., 40, e33.
83. Lalonde, S., Ehrhardt, D.W., Loqué, D., Chen, J., Rhee, S.Y and Frommer, W.B. (2008) Molecular and cellular approaches for the detection of protein-protein interactions: latest techniques and current limitations. Plant J., 53, 610-635.
84. Wojtuszewski, K., Harvey, J.J., Han, M.K. and Knutson, J.R. (2007) Fluorescence detection of proximity. In: Schuck, P and Atassi, MZ (eds). Protein interactions; biophysical approaches for the study of complex reversible systems. Springer, NY, pp. 367-396.
85. Liu, Y, Prasad, R., Beard, W.A., Kedar, P.S., Hou, E.W., Shock, D.D. and Wilson, S.H. (2007) Coordination of steps in single-nucleotide base excision repair mediated by apurinic/apyrimidinic endonuclease 1 and DNA polymerase β. J. Biol. Chem., 282, 13532-13541.
86. Shall, S. and de Murcia, G. (2000) Poly(ADP-ribose) polymerase-1: what have we learned from the deficient mouse model? Mutat. Res., 460, 1-15.
87. Nazarkina, Z.K., Khodyreva, S.N, Marsin, S., Lavrik, O.I. and Radicella, J.P (2007) XRCC1 interactions with base excision repair DNA intermediates. DNA Repair (Amst.), 6, 54-64.
88. Mani, R.S., Karimi-Busheri, F, Fanta, M., Caldecott, K.W., Cass, C.E. and Weinfeld, M. (2004) Biophysical characterization of human XRCC1 and its binding to damaged and undamaged DNA. Biochemistry, 43, 16505-16514.
89. Khodyreva, S.N., Prasad, R., Ilina, E.S., Sukhanova, M.V, Kutuzov, M.M., Liu, Y, Hou, E.W., Wilson, S.H. and Lavrik, O.I. (2010) Apurinic/apyrimidinic (AP) site recognition by the 5'-dRP/AP lyase in poly(ADP-ribose) polymerase-1 (PARP-1). Proc Natl Acad. Sci. U.S.A., 107, 22090-22095.
90. Some, D (2013) Light-scattering-based analysis of biomolecular interactions. Biophys. Rev., 5, 147-158.
91. Hanssen-Bauer, A., Solvang-Garten, K., Sundheim, O., Pena-Diaz, J., Andersen, S., Slupphaug, G., Krokan, H.E., Wilson, DM. III, Akbari, M. and Otterlei, M. (2011) XRCC1 coordinates disparate responses and multiprotein repair complexes depending on the nature and context of the DNA damage. Environ. Mol. Mutagen., 52, 623-635.
92. Cistulli, C, Lavrik, O.I., Prasad, R., Hou, E. and Wilson, S.H. (2004) AP endonuclease and poly(ADP-ribose) polymerase-1 interact with the same base excision repair intermediate. DNA Repair (Amst.), 3, 581-591.
93. Prasad, R., Williams, J.G., Hou, E.W. and Wilson, S.H. (2012) Pol β associated complex and base excision repair factors in mouse fibroblasts. Nucleic Acids Res., 40, 11571-11582.
94. Das, B.B., Huang, S.Y, Murai, J., Rehman, I., Amé, J.C, Sengupta, S., Das, S.K., Majumdar, P, Zhang, H., Biard, D. et al. (2014) PARP1-TDP1 coupling for the repair of topoisomerase I-induced DNA damage. Nucleic Acids Res., 42, 4435-4449.
95. Das, B.B., Antony, S., Gupta, S., Dexheimer, T.S., Redon, C.E., Garfield, S., Shiloh, Y and Pommier, Y (2009) Optimal function of the DNA repair enzyme TDP1 requires its phosphorylation by ATM and/or DNA-PK. EMBO J., 28, 3667-3680.
96. Chiang, S.C., Carroll, J. and El-Khamisy, S.F (2010) TDP1 serine 81 promotes interaction with DNA ligase IIIa and facilitates cell survival following DNA damage. Cell Cycle, 9, 588-595.
97. Dexheimer, T.S., Antony, S., Marchand, C. and Pommier, Y (2008) Tyrosyl-DNA phosphodiesterase as a target for anticancer therapy. Anticancer Agents Med. Chem., 8, 381-389.
98. Bennett, R.A., Wilson, D.M. III, Wong, D and Demple, B. (1997) Interaction of human apurinic endonuclease and DNA polymerase β in the base excision repair pathway. Proc. Natl Acad. Sci. U.S.A., 94, 7166-7169.
99. Dimitriadis, E.K., Prasad, R., Vaske, M.K., Chen, L., Tomkinson, A.E., Lewis, M.S. and Wilson, S.H. (1998) Thermodynamics of human DNA ligase I trimerization and association with DNA polymerase β. J. Biol. Chem., 273, 20540-20550.
100. Wilson, DM. III and Barsky, D. (2001) The major human abasic endonuclease: formation, consequences and repair of a basic lesions in DNA. Mutat. Res., 485, 283-307.
101. Wilson, S.H., Beard, W.A., Shock, D.D, Batra, VK, Cavanaugh, NA., Prasad, R., Hou, E.W., Liu, Y, Asagoshi, K., Horton, J.K. et al. (2010) Base excision repair and design of small molecule inhibitors of human DNA polymerase β. Cell Mol. Life Sci., 67, 3633-3647.
102. Pleschke, J.M., Kleczkowska, H.E., Strohm, M. and Althaus, FR. (2000) Poly(ADP-ribose) binds to specific domains in DNA damage checkpoint proteins. J. Biol. Chem., 275, 40974-40980.
103. Masson, M., Niedergang, C, Schreiber, V., Muller, S., Menissier-de Murcia, J. and de Murcia, G (1998) XRCC1 is specifically associated with poly(ADP-ribose) polymerase and negatively regulates its activity following DNA damage. Mol. Cell Biol, 18, 3563-3571.
104. Leppard, J.B., Dong, Z., Mackey, Z.B. and Tomkinson, A.E. (2003) Physical and functional interaction between DNA ligase IIIa and poly(ADP-ribose) polymerase 1 in DNA single-strand break repair. Mol. Cell Biol., 23, 5919-5927.
105. El-Khamisy, S.F, Masutani, M., Suzuki, H. and Caldecott, K.W (2003) A requirement for PARP-1 for the assembly or stability of XRCC1 nuclear foci at sites of oxidative DNA damage. Nucleic Acids Res., 31, 5526-5533.
106. Okano, S., Lan, L., Caldecott, K.W., Mori, T and Yasui, A. (2003) Spatial and temporal cellular responses to single-strand breaks in human cells. Mol. Cell Biol, 23, 3974-3981.
107. Kim, I.K., Stegeman, R.A., Brosey, C.A. and Ellenberger, T (2015) A quantitative assay reveals ligand specificity of the DNA scaffold repair protein XRCC1 and efficient disassembly of complexes of XRCC1 and the poly(ADP-ribose) polymerase 1 by poly(ADP-ribose) glycohydrolase. J. Biol. Chem., 290, 3775-3783.
108. Cuneo, M.J. and London, R.E. (2010) Oxidation state of the XRCC1 N-terminal domain regulates DNA polymerase β binding affinity. Proc. Natl Acad. Sci. U.S.A., 107, 6805-6810.
109. Marintchev, A., Robertson, A., Dimitriadis, E.K., Prasad, R., Wilson, S.H. and Mullen, GP (2000) Domain specific interaction in the XRCC1-DNA polymerase β complex. Nucleic Acids Res., 28, 2049-2059.
110. Marintchev, A., Gryk, M.R. and Mullen, GP (2003) Site-directed mutagenesis analysis of the structural interaction of the single-strand-break repair protein, X-ray cross-complementing group 1, with DNA polymerase β. Nucleic Acids Res, 31, 580-588.
111. Luo, H., Chan, D.W., Yang, T, Rodriguez, M., Chen, B.P, Leng, M., Mu, J.J., Chen, D, Songyang, Z., Wang, Y et al. (2004) A new XRCC1-containing complex and its role in cellular survival of methyl methanesulfonate treatment. Mol. Cell Biol, 24, 8356-8365.
112. Lu, M., Mani, R.S., Karimi-Busheri, F, Fanta, M., Wang, H., Litchfeld, DW. and Weinfeld, M. (2010) Independent mechanisms of stimulation of polynucleotide kinase/phosphatase by phosphorylated and non-phosphorylatedXRCC1. Nucleic Acids Res., 38, 510-521.
113. Dianova, I.I., Sleeth, K.M., Allinson, S.L., Parsons, J.L., Breslin, C, Caldecott, K.W. and Dianov, GL. (2004) XRCC1-DNA polymerase β interaction is required for efficient base excision repair. Nucleic Acids Res., 32, 2550-2555.
114. Wong, H.-K. and Wilson, D.M. III (2005) XRCC1 and DNA polymerase β interaction contributes to cellular alkylating-agent resistance and single-strand break repair. J. Cell Biochem., 95, 794-804.
115. Horton, J.K., Stefanick, DF, Gassman, NR., Williams, J.G, Gabel, S.A., Cuneo, M.J., Prasad, R., Kedar, PS., Derose, E.F, Hou, E.W. et al. (2013) Preventing oxidation of cellular XRCC1 affects PARP-mediated DNA damage responses. DNA Repair (Amst.), 12, 774-785.
116. Lan, L., Nakajima, S., Oohata, Y, Takao, M., Okano, S., Masutani, M., Wilson, S.H. and Yasui, A. (2004) In situ analysis of repair processes for oxidative DNA damage in mammalian cells. Proc. Natl Acad. Sci. U.S.A., 101, 13738-13743.
117. Fang, Q., Inanc, B., Schamus, S., Wang, X.H., Wei, L., Brown, A.R., Svilar, D, Sugrue, K.F, Goellner, E.M, Zeng, X. et al. (2014) HSP90 regulates DNA repair via the interaction between XRCC1 and DNA polymerase β. Nat. Commun., 5, 5513.
118. Caldecott, K.W., Tucker, J.D, Stanker, L.H. and Thompson, L.H. (1995) Characterization of the XRCC1-DNA ligase III complex in vitro and its absence from mutant hamster cells. Nucleic Acids Res., 23, 4836-4843.