Advertisement

Biochemistry (Moscow)

, Volume 83, Issue 4, pp 411–422 | Cite as

Protein–Protein Interactions in DNA Base Excision Repair

  • N. A. Moor
  • O. I. Lavrik
Review
First Online:
Received:
Revised:

Abstract

The system of base excision repair (BER) ensures correction of the most abundant DNA damages in mammalian cells and plays an important role in maintaining genome stability. Enzymes and protein factors participate in the multistage BER in a coordinated fashion, which ensures repair efficiency. The suggested coordination mechanisms are based on formation of protein complexes stabilized via either direct or indirect DNA-mediated interactions. The results of investigation of direct interactions of the proteins participating in BER with each other and with other proteins are outlined in this review. The known protein partners and sites responsible for their interaction are presented for the main participants as well as quantitative characteristics of their affinity. Information on the mechanisms of regulation of protein–protein interactions mediated by DNA intermediates and posttranslational modification is presented. It can be suggested based on all available data that the multiprotein complexes are formed on chromatin independent of the DNA damage with the help of key regulators of the BER process – scaffold protein XRCC1 and poly(ADP-ribose) polymerase 1. The composition of multiprotein complexes changes dynamically depending on the DNA damage and the stage of BER process.

Keywords

base excision repair protein–protein interactions DNA repair 

Abbreviations

AP site

apurinic/apyrimidinic site

APE1

AP endonuclease 1

APTX

aprataxin

BER

base excision repair

DNALigI/DNALigIIIα

DNA ligase I/IIIα

dRp

deoxyribose phosphate

FAM

5(6)-carboxyfluorescein

FEN1

flap endonuclease 1

FRET

Förster resonance energy transfer

HR

homologous recombination

MMR

mismatch repair

NER

nucleotide excision repair

NHEJ

nonhomologous end joining

PAR

poly(ADP-ribose)

PARP1/PARP2

poly(ADP-ribose) polymerase 1/2

PNKP

polynucleotide kinase/phosphatase

Polβ/Polδ/Polε

DNA polymerase β/δ/ε

PTM

posttranslational modification

TDP1

tyrosyl-DNA phosphodiesterase 1

TMR

5(6)-carboxytetramethylrhodamine

XRD

X-ray diffraction analysis

This is a preview of subscription content, log in to check access.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Mavragani, I. V., Nikitaki, Z., Souli, M. P., Aziz, A., Nowsheen, S., Aziz, K., Rogakou, E., and Georgakilas, A. G. (2017) Complex DNA damage: a route to radiation-induced genomic instability and carcinogenesis, Cancers (Basel), 9, 91.CrossRefGoogle Scholar
  2. 2.
    Talhaoui, I., Matkarimov, B. T., Tchenio, T., Zharkov, D. O., and Saparbaev, M. K. (2017) Aberrant base excision repair pathway of oxidatively damaged DNA: implications for degenerative diseases, Free Radic. Biol. Med., 107, 266–277.CrossRefPubMedGoogle Scholar
  3. 3.
    Poletto, M., Legrand, A. J., and Dianov, G. L. (2017) DNA base excision repair: the Achilles’ heel of tumor cells and their microenvironment? Curr. Pharm. Des., doi: 10.2174/1381612823666170710123602.Google Scholar
  4. 4.
    Whitaker, A. M., Schaich, M. A., Smith, M. R., Flynn, T. S., and Freudenthal, B. D. (2017) Base excision repair of oxidative DNA damage: from mechanism to disease, Front. Biosci. (Landmark Ed.), 22, 1493–1522.CrossRefGoogle Scholar
  5. 5.
    Abbotts, R., and Wilson III, D. M. (2017) Coordination of DNA single strand break repair, Free Radic. Biol. Med., 107, 228–244.CrossRefPubMedGoogle Scholar
  6. 6.
    Berti, P. J., and McCann, J. A. B. (2006) Toward a detailed understanding of base excision repair enzymes: transition state and mechanistic analyses of N-glycoside hydrolysis and N-glycoside transfer, Chem. Rev., 106, 506–555.CrossRefPubMedGoogle Scholar
  7. 7.
    Liu, Y., Beard, W. A., Shock, D. D., Prasad, R., Hou, E. W., and Wilson, S. H. (2005) DNA polymerase beta and flap endonuclease 1 enzymatic specificities sustain DNA synthesis for long patch base excision repair, J. Biol. Chem., 280, 3665–3674.CrossRefPubMedGoogle Scholar
  8. 8.
    Lebedeva, N. A., Rechkunova, N. I., Dezhurov, S. V., Khodyreva, S. N., Favre, A., Blanco, L., and Lavrik, O. I. (2005) Comparison of functional properties of mammalian DNA polymerase lambda and DNA polymerase beta in reactions of DNA synthesis related to DNA repair, Biochim. Biophys. Acta, 1751, 150–158.CrossRefPubMedGoogle Scholar
  9. 9.
    Caldecott, K. W. (2014) DNA single-strand break repair, Exp. Cell. Res., 329, 2–8.CrossRefPubMedGoogle Scholar
  10. 10.
    Amé, J. C., Rolli, V., Schreiber, V., Niedergang, C., Apiou, F., Decker, P., Muller, S., Höger, T., Ménissier-de Murcia, J., and de Murcia, G. (1999) PARP-2, a novel mammalian DNA damage-dependent poly(ADP-ribose) polymerase, J. Biol. Chem., 274, 17860–17868.CrossRefPubMedGoogle Scholar
  11. 11.
    De Murcia, J. M., Niedergang, C., Trucco, C., Ricoul, M., Dutrillaux, B., Mark, M., Oliver, F. J., Masson, M., Dierich, A., LeMeur, M., Walztinger, C., Chambon, P., and de Murcia, G. (1997) Requirement of poly(ADP-ribose) polymerase in recovery from DNA damage in mice and in cells, Proc. Natl. Acad. Sci. USA, 94, 7303–7307.CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Ménissier-de Murcia, J., Ricoul, M., Tartier, L., Niedergang, C., Huber, A., Dantzer, F., Schreiber, V., Amé, J. C., Dierich, A., Le Meur, M., Sabatier, L., Chambon, P., and de Murcia, G. (2003) Functional interaction between PARP1 and PARP2 in chromosome stability and embryonic development in mouse, EMBO J., 22, 2255–2263.CrossRefGoogle Scholar
  13. 13.
    Pascal, J. M., and Ellenberger, T. (2015) The rise and fall of poly(ADP-ribose): an enzymatic perspective, DNA Repair (Amst.), 32, 10–16.CrossRefGoogle Scholar
  14. 14.
    Ray Chaudhuri, A., and Nussenzweig, A. (2017) The mul-tifaceted roles of PARP1 in DNA repair and chromatin remodeling, Nat. Rev. Mol. Cell Biol., 18, 610–621.CrossRefPubMedGoogle Scholar
  15. 15.
    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. (Moscow), 45, 586–600.CrossRefGoogle Scholar
  16. 16.
    Kim, Y.-J., and Wilson III, D. M. (2012) Overview of base excision repair biochemistry, Curr. Mol. Pharmacol., 5, 3–13.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Dutta, A., Yang, C., Sengupta, S., Mitra, S., and Hegde, M. L. (2015) New paradigms in the repair of oxidative damage in human genome: mechanisms ensuring repair of mutagenic base lesions during replication and involvement of accessory proteins, Cell. Mol. Life Sci., 72, 1679–1698.CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Esadze, A., Rodriguez, G., Cravens, S. L., and Stivers, J. T. (2017) AP-endonuclease 1 accelerates turnover of human 8-oxoguanine DNA glycosylase by preventing retrograde binding to the abasic-site product, Biochemistry, 56, 1974–1986.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Kubota, Y., Nash, R. A., Klungland, A., Schär, P., Barnes, D. E., and Lindahl, T. (1996) Reconstitution of DNA base excision-repair with purified human proteins: interaction between DNA polymerase β and the XRCC1 protein, EMBO J., 15, 6662–6670.PubMedPubMedCentralGoogle Scholar
  20. 20.
    Marintchev, A., Robertson, A., Dimitriadis, E. K., Prasad, R., Wilson, S. H., and Mullen, G. P. (2000) Domain specific interaction in the XRCC1-DNA polymerase β complex, Nucleic Acids Res., 28, 2049–2059.CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Marintchev, A., Gryk, M. R., and Mullen, G. P. (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.CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    London, R. E. (2015) The structural basis of XRCC1-mediated DNA repair, DNA Repair (Amst.), 30, 90–103.CrossRefGoogle Scholar
  23. 23.
    Fan, J., Otterlei, M., Wong, H. K., Tomkinson, A. E., and Wilson III, D. M. (2004) XRCC1 co-localizes and physically interacts with PCNA, Nucleic Acids Res., 32, 2193–2201.CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Akbari, M., Solvang-Garten, K., Hanssen-Bauer, A., Lieske, N. V., Pettersen, H. S., Pettersen, G. K., Wilson III, D. M., Krokan, H. E., and Otterlei, M. (2010) Direct interaction between XRCC1 and UNG2 facilitates rapid repair of uracil in DNA by XRCC1 complexes, DNA Repair (Amst.), 9, 785–795.CrossRefGoogle Scholar
  25. 25.
    Campalans, A., Marsin, S., Nakabeppu, Y., O’Connor, T. R., Boiteux, S., and Radicella, J. P. (2005) XRCC1 interactions with multiple DNA glycosylases: a model for its recruitment to base excision repair, DNA Repair (Amst.), 4, 826–835.CrossRefGoogle Scholar
  26. 26.
    Wiederhold, L., Leppard, J. B., Kedar, P., Karimi-Busheri, F., Rasouli-Nia, A., Weinfeld, M., Tomkinson, A. E., Izumi, T., Prasad, R., Wilson, S. H., Mitra, S., and Hazra, T. K. (2004) AP endonuclease-independent DNA base excision repair in human cells, Mol. Cell, 15, 209–220.CrossRefPubMedGoogle Scholar
  27. 27.
    Das, A., Wiederhold, L., Leppard, J. B., Kedar, P., Prasad, R., Wang, H., Boldogh, I., Karimi-Busheri, F., Weinfeld, M., Tomkinson, A. E., Wilson, S. H., Mitra, S., and Hazra, T. K. (2006) NEIL2-initiated, APE-independent repair of oxidized bases in DNA: evidence for a repair complex in human cells, DNA Repair (Amst.), 5, 1439–1448.CrossRefPubMedCentralGoogle Scholar
  28. 28.
    Marsin, S., Vidal, A. E., Sossou, M., Ménissier-de Murcia, J., Le Page, F., Boiteux, S., de Murcia, G., and Radicella, J. P. (2003) Role of XRCC1 in the coordination and stimulation of oxidative DNA damage repair initiated by the DNA glycosylase hOGG1, J. Biol. Chem., 278, 44068–44074.CrossRefPubMedGoogle Scholar
  29. 29.
    Hanssen-Bauer, A., Solvang-Garten, K., Gilljam, K. M., Torseth, K., Wilson III, D. M., Akbari, M., and Otterlei, M. (2012) The region of XRCC1 which harbors the three most common nonsynonymous polymorphic variants, is essential for the scaffolding function of XRCC1, DNA Repair (Amst.), 11, 357–366.CrossRefGoogle Scholar
  30. 30.
    Masson, M., Niedergang, C., Schreiber, V., Muller, S., Ménissier-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.CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Schreiber, V., Amé, J. C., Dolle, 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.CrossRefPubMedGoogle Scholar
  32. 32.
    Loizou, J. I., El-Khamisy, S. F., Zlatanou, A., Moore, D. J., Chan, D. W., Qin, J., Sarno, S., Meggio, F., Pinna, L. A., and Caldecott, K. W. (2004) The protein kinase CK2 facilitates repair of chromosomal DNA single-strand breaks, Cell, 117, 17–28.CrossRefPubMedGoogle Scholar
  33. 33.
    Lu, M., Mani, R. S., Karimi-Busheri, F., Fanta, M., Wang, H., Litchfeld, D. W., and Weinfeld, M. (2010) Independent mechanisms of stimulation of polynucleotide kinase/phosphatase by phosphorylated and non-phosphorylated XRCC1, Nucleic Acids Res., 38, 510–521.CrossRefPubMedGoogle Scholar
  34. 34.
    Luo, H., Chan, D. W., Yang, T., Rodriguez, M., Chen, B. P., Leng, M., Mu, J. J., Chen, D., Songyang, Z., Wang, Y., and Qin, J. (2004) A new XRCC1-containing complex and its role in cellular survival of methyl methanesulfonate treatment, Mol. Cell. Biol., 24, 8356–8365.CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    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.CrossRefPubMedGoogle Scholar
  36. 36.
    Nash, R. A., Caldecott, K. W., Barnes, D. E., and Lindahl, T. (1997) XRCC1 protein interacts with one of two distinct forms of DNA ligase III, Biochemistry, 36, 5207–5211.CrossRefPubMedGoogle Scholar
  37. 37.
    Cuneo, M. J., Gabel, S. A., Krahn, J. M., Ricker, M. A., and London, R. E. (2011) The structural basis for partitioning of the XRCC1/DNA ligase III-α BRCT-mediated dimer complexes, Nucleic Acids Res., 39, 7816–7827.CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Plo, I., Liao, Z. Y., Barceló, J. M., Kohlhagen, G., Caldecott, K. W., Weinfeld, M., and Pommier, Y. (2003) Association of XRCC1 and tyrosyl DNA phosphodiesterase (Tdp1) for the repair of topoisomerase I-mediated DNA lesions, DNA Repair (Amst.), 2, 1087–1100.CrossRefGoogle Scholar
  39. 39.
    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.CrossRefPubMedGoogle Scholar
  40. 40.
    Ali, A. A. E., Timinszky, G., Arribas-Bosacoma, R., Kozlowski, M., Hassa, P. O., Hassler, M., Ladurner, A. G., Pearl, L. H., and Oliver, A. W. (2012) The zinc-finger domains of PARP1 cooperate to recognize DNA strand breaks, Nat. Struct. Mol. Biol., 19, 685–692.CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Leppard, J. B., Dong, Z., Mackey, Z. B., and Tomkinson, A. E. (2003) Physical and functional interaction between DNA ligase IIIα and poly(ADP-ribose) polymerase 1 in DNA single-strand break repair, Mol. Cell. Biol., 23, 5919–5927.CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Das, B. B., Huang, S. Y., Murai, J., Rehman, I., Amé, J. C., Sengupta, S., Das, S. K., Majumdar, P., Zhang, H., Biard, D., Majumder, H. K., Schreiber, V., and Pommier, Y. (2014) PARP1-TDP1 coupling for the repair of topoisomerase I-induced DNA damage, Nucleic Acids Res., 42, 4435–4449.CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    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.CrossRefPubMedGoogle Scholar
  44. 44.
    Bennett, R. A., Wilson III, D. M., 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. USA, 94, 7166–7169.CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Whitehouse, C. J., Taylor, R. M., Thistlethwaite, A., Zhang, H., Karimi-Busheri, F., Lasko, D. D., Weinfeld, M., and Caldecott, K. W. (2001) XRCC1 stimulates human polynucleotide kinase activity at damaged DNA termini and accelerates DNA single-strand break repair, Cell, 104, 107–117.CrossRefPubMedGoogle Scholar
  46. 46.
    El-Khamisy, S. F., Saifi, G. M., Weinfeld, M., Johansson, F., Helleday, T., Lupski, J. R., and Caldecott, K. W. (2005) Defective DNA single-strand break repair in spinocerebellar ataxia with axonalneuropathy-1, Nature, 434, 108–113.CrossRefPubMedGoogle Scholar
  47. 47.
    Chiang, S. C., Carroll, J., and El-Khamisy, S. F. (2010) TDP1 serine 81 promotes interaction with DNA ligase IIIα and facilitates cell survival following DNA damage, Cell Cycle, 9, 588–595.CrossRefPubMedGoogle Scholar
  48. 48.
    Luncsford, P. J., Manvilla, B. A., Patterson, D. N., Malik, S. S., Jin, J., Hwang, B. J., Gunther, R., Kalvakolanu, S., Lipinski, L. J., Yuan, W., Lu, W., Drohat, A. C., Lu, A. L., and Toth, E. A. (2013) Coordination of MYH DNA glycosylase and APE1 endonuclease activities via physical interactions, DNA Repair (Amst.), 12, 1043–1052.CrossRefGoogle Scholar
  49. 49.
    Hegde, P. M., Dutta, A., Sengupta, S., Mitra, J., Adhikari, S., Tomkinson, A. E., Li, G. M., Boldogh, I., Hazra, T. K., Mitra, S., and Hegde, M. L. (2015) The C-terminal domain (CTD) of human DNA glycosylase NEIL1 is required for forming BERosome repair complex with DNA replication proteins at the replicating genome: dominant negative function of the CTD, J. Biol. Chem., 290, 20919–20933.CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    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.CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Langelier, M. F., Planck, J. L., Roy, S., and Pascal, J. M. (2012) Structural basis for DNA damage-dependent poly(ADP-ribosyl)ation by human PARP-1, Science, 336, 728–732.CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Cotner-Gohara, E., Kim, I. K., Tomkinson, A. E., and Ellenberger, T. (2008) Two DNA-binding and nick recognition modules in human DNA ligase III, J. Biol. Chem., 283, 10764–10772.CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Gerloff, D. L., Woods, N. T., Farago, A. A., and Monteiro, A. N. (2012) BRCT domains: a little more than kin, and less than kind, FEBS Lett., 586, 2711–2716.CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Eustermann, S., Wu, W. F., Langelier, M. F., Yang, J. C., Easton, L. E., Riccio, A. A., Pascal, J. M., and Neuhaus, D. (2015) Structural basis of detection and signaling of DNA single-strand breaks by human PARP-1, Mol. Cell, 60, 742–754.CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Gagné, J. P., Ethier, C., Defoy, D., Bourassa, S., Langelier, M. F., Riccio, A. A., Pascal, J. M., Moon, K. M., Foster, L. J., Ning, Z., Figeys, D., Droit, A., and Poirier, G. G. (2015) Quantitative site-specific ADP-ribosylation profiling of DNA-dependent PARPs, DNA Repair (Amst.), 30, 68–79.CrossRefGoogle Scholar
  56. 56.
    Gagné, J. P., Isabelle, M., Lo, K. S., Bourassa, S., Hendzel, M. J., Dawson, V. L., Dawson, T. M., and Poirier, G. G. (2008) Proteome-wide identification of poly(ADP-ribose) binding proteins and poly(ADP-ribose)-associated protein complexes, Nucleic Acids Res., 36, 6959–6976.CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Teloni, F., and Altmeyer, M. (2016) Readers of poly(ADP-ribose): designed to be fit for purpose, Nucleic Acids Res., 44, 993–1006.CrossRefPubMedGoogle Scholar
  58. 58.
    Bock, F. J., and Chang, P. (2016) New directions in poly(ADP-ribose) polymerase biology, FEBS J., 28, 4017–4031.CrossRefGoogle Scholar
  59. 59.
    Hanzlikova, H., Gittens, W., Krejcikova, K., Zeng, Z., and Caldecott, K. W. (2017) Overlapping roles for PARP1 and PARP2 in the recruitment of endogenous XRCC1 and PNKP into oxidized chromatin, Nucleic Acids Res., 45, 2546–2557.PubMedGoogle Scholar
  60. 60.
    Abdou, I., Poirier, G. G., Hendzel, M. J., and Weinfeld, M. (2015) DNA ligase III acts as a DNA strand break sensor in the cellular orchestration of DNA strand break repair, Nucleic Acids Res., 43, 875–892.CrossRefPubMedGoogle Scholar
  61. 61.
    Moor, N. A., Vasil’eva, I. A., Anarbaev, R. O., Antson, A. A., and Lavrik, O. I. (2015) Quantitative characterization of protein–protein complexes involved in base excision DNA repair, Nucleic Acids Res., 43, 6009–6022.CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Mani, R. S., Fanta, M., Karimi-Busheri, F., Silver, E., Virgen, C. A., Caldecott, K. W., Cass, C. E., and Weinfeld, M. (2007) XRCC1 stimulates polynucleotide kinase by enhancing its damage discrimination and displacement from DNA repair intermediates, J. Biol. Chem., 282, 28004–28013.CrossRefPubMedGoogle Scholar
  63. 63.
    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.CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Fang, Q., Inanc, B., Schamus, S., Wang, X. H., Wei, L., Brown, A. R., Svilar, D., Sugrue, K. F., Goellner, E. M., Zeng, X., Yates, N. A., Lan, L., Vens, C., and Sobol, R. W. (2014) HSP90 regulates DNA repair via the interaction between XRCC1 and DNA polymerase β, Nat. Commun., 5, 5513.CrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    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. USA, 101, 13738–13743.CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    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.CrossRefPubMedGoogle Scholar
  67. 67.
    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. USA, 107, 22090–22095.CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Sukhanova, M. V., Abrakhi, S., Joshi, V., Pastre, D., Kutuzov, M. M., Anarbaev, R. O., Curmi, P. A., Hamon, L., and Lavrik, O. I. (2016) Single molecule detection of PARP1 and PARP2 interaction with DNA strand breaks and their poly(ADP-ribosyl)ation using high-resolution AFM imaging, Nucleic Acids Res., 44, e60.CrossRefPubMedGoogle Scholar
  69. 69.
    Alemasova, E. E., and Lavrik, O. I. (2017) At the interface of three nucleic acids: the role of RNA-binding proteins and poly(ADP-ribose) in DNA repair, Acta Naturae, 9, 4–16.PubMedPubMedCentralGoogle Scholar
  70. 70.
    Altmeyer, M., Neelsen, K. J., Teloni, F., Pozdnyakova, I., Pellegrino, S., Grøfte, M., Rask, M. B., Streicher, W., Jungmichel, S., Nielsen, M. L., and Lukas, J. (2015) Liquid demixing of intrinsically disordered proteins is seeded by poly(ADP-ribose), Nat. Commun., 6, 8088.CrossRefPubMedPubMedCentralGoogle Scholar
  71. 71.
    Sorokin, A. V., Selyutina, A. A., Skabkin, M. A., Guryanov, S. G., Nazimov, I. V., Richard, C., Th’ng, J., Yau, J., Sorensen, P. H., Ovchinnikov, L. P., and Evdokimova, V. (2005) Proteasome-mediated cleavage of the Y-box-binding protein 1 is linked to DNA-damage stress response, EMBO J., 24, 3602–3612.CrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    Alemasova, E. E., Pestryakov, P. E., Sukhanova, M. V., Kretov, D. A., Moor, N. A., Curmi, P. A., Ovchinnikov, L. P., and Lavrik, O. I. (2015) Poly(ADP-ribosyl)ation as a new posttranslational modification of YB-1, Biochimie, 119, 36–44.CrossRefPubMedGoogle Scholar
  73. 73.
    Alemasova, E. E., Moor, N. A., Naumenko, K. N., Kutuzov, M. M., Sukhanova, M. V., Pestryakov, P. E., and Lavrik, O. I. (2016) Y-box-binding protein 1 as a non-canonical factor of base excision repair, Biochim. Biophys. Acta, 1864, 1631–1640.CrossRefPubMedGoogle Scholar
  74. 74.
    Sengupta, S., Mantha, A. K., Mitra, S., and Bhakat, K. K. (2011) Human AP endonuclease (APE1/ref-1) and its acetylation regulate YB-1-p300 recruitment and RNA polymerase II loading in the drug-induced activation of multidrug resistance gene MDR1, Oncogene, 30, 4482–4493.CrossRefGoogle Scholar
  75. 75.
    Poletto, M., Lirussi, L., Wilson III, D. M., and Tell, G. (2014) Nucleophosmin modulates stability, activity, and nucleolar accumulation of base excision repair proteins, Mol. Biol. Cell, 25, 1641–1652.PubMedGoogle Scholar
  76. 76.
    Tell, G., Fantini, D., and Quadrifoglio, F. (2010) Understanding different functions of mammalian AP endonuclease (APE1) as a promising tool for cancer treatment, Cell. Mol. Life Sci., 67, 3589–3608.CrossRefPubMedGoogle Scholar
  77. 77.
    Dyrkheeva, N. S., Lebedeva, N. A., and Lavrik, O. I. (2016) AP endonuclease 1 as a key enzyme in repair of apurinic/apyrimidinic sites, Biochemistry (Moscow), 81, 951–967.CrossRefGoogle Scholar
  78. 78.
    Paquet, N., Adams, M. N., Leong, V., Ashton, N. W., Touma, C., Gamsjaeger, R., Cubeddu, L., Beard, S., Burgess, J. T., Bolderson, E., O’Byrne, K. J., and Richard, D. J. (2015) hSSB1 (NABP2/OBFC2B) is required for the repair of 8-oxo-guanine by the hOGG1-mediated base excision repair pathway, Nucleic Acids Res., 43, 8817–8829.CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Kaur, S., Coulombe, Y., Ramdzan, Z. M., Leduy, L., Masson, J. Y., and Nepveu, A. (2016) Special AT-rich sequence-binding protein 1 (SATB1) functions as an accessory factor in base excision repair, J. Biol. Chem., 291, 22769–22780.CrossRefPubMedPubMedCentralGoogle Scholar
  80. 80.
    Maher, R. L., Marsden, C. G., Averill, A. M., Wallace, S. S., Sweasy, J. B., and Pederson, D. S. (2017) Human cells contain a factor that facilitates the DNA glycosylase-mediated excision of oxidized bases from occluded sites in nucleosomes, DNA Repair (Amst.), 57, 91–97.CrossRefGoogle Scholar
  81. 81.
    Limpose, K. L., Corbett, A. H., and Doetsch, P. W. (2017) BERing the burden of damage: pathway crosstalk and posttranslational modification of base excision repair proteins regulate DNA damage management, DNA Repair (Amst.), 56, 51–64.CrossRefGoogle Scholar
  82. 82.
    Prasad, R., Liu, Y., Deterding, L. J., Poltoratsky, V. P., Kedar, P. S., Horton, J. K., Kanno, S., Asagoshi, K., Hou, E. W., Khodyreva, S. N., Lavrik, O. I., Tomer, K. B., Yasui, A., and Wilson, S. H. (2007) HMGB1 is a cofactor in mammalian base excision repair, Mol. Cell, 27, 829–841.CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    Liu, Y., Prasad, R., and Wilson, S. H. (2010) HMGB1: roles in base excision repair and related function, Biochim. Biophys. Acta, 1799, 119–130.CrossRefPubMedPubMedCentralGoogle Scholar
  84. 84.
    Balliano, A., Hao, F., Njeri, C., Balakrishnan, L., and Hayes, J. J. (2017) HMGB1 stimulates activity of polymerase β on nucleosome substrates, Biochemistry, 56, 647–656.CrossRefPubMedPubMedCentralGoogle Scholar
  85. 85.
    Menoni, H., Di Mascio, P., Cadet, J., Dimitrov, S., and Angelov, D. (2017) Chromatin associated mechanisms in base excision repair–nucleosome remodeling and DNA transcription, two key players, Free Radic. Biol. Med., 107, 159–169.CrossRefPubMedGoogle Scholar
  86. 86.
    Almeida, K. H., and Sobol, R. W. (2007) A unified view of base excision repair: lesion-dependent protein complexes regulated by post-translational modification, DNA Repair (Amst.), 6, 695–711.CrossRefGoogle Scholar
  87. 87.
    Roychoudhury, S., Nath, S., Song, H., Hegde, M. L., Bellot, L. J., Mantha, A. K., Sengupta, S., Ray, S., Natarajan, A., and Bhakat, K. K. (2017) Human apurinic/apyrimidinic endonuclease (APE1) is acetylated at DNA damage sites in chromatin, and acetylation modulates its DNA repair activity, Mol. Cell. Biol., 37, e00401-16.PubMedGoogle Scholar
  88. 88.
    Weiser, B. P., Stivers, J. T., and Cole, P. A. (2017) Investigation of N-terminal phosphoregulation of uracil DNA glycosylase using protein semisynthesis, Biophys. J., 113, 393–401.CrossRefPubMedGoogle Scholar
  89. 89.
    Horton, J. K., Seddon, H. J., Zhao, M. L., Gassman, N. R., Janoshazi, A. K., Stefanick, D. F., and Wilson, S. H. (2017) Role of the oxidized form of XRCC1 in protection against extreme oxidative stress, Free Radic. Biol. Med., 107, 292–300.CrossRefPubMedGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2018

Authors and Affiliations

  1. 1.Institute of Chemical Biology and Fundamental MedicineSiberian Branch of the Russian Academy of SciencesNovosibirskRussia
  2. 2.Novosibirsk State UniversityNovosibirskRussia

Personalised recommendations

Cite article

Buy options