DNA break repair: Refined rules of an already complicated game

Biochemistry and Cell Biology

Volumn 83, Issue 3, 2005, Pages 365-373

  Vidaković, Melita ^a   Poznanović, Goran ^a   Bode, Juergen ^b  

^a UNIVERSITY OF BELGRADE   (Serbia)

^b HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

Author keywords

DNA strand break repair (DSBR); Non homologous end joining (NHEJ); Nuclear architecture; Nuclear matrix; PARP 1

Indexed keywords

BIOCHEMISTRY; ENZYME IMMOBILIZATION; PROTEINS;

DNA STRAND BREAK REPAIR (DSBR); NON-HOMOLOGUS END JOINING (NHEJ); NUCLEAR ARCHITECTURE; NUCLEAR MATRIX; PARP-I;

DNA;

DEOXYRIBONUCLEOPROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; POL PROTEIN; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; PROTEIN XRCC1; UNCLASSIFIED DRUG;

APOPTOSIS; CELL NUCLEUS MATRIX; CYTOARCHITECTURE; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; DNA STRAND BREAKAGE; HUMAN; NONHUMAN; REVIEW;

ANIMALS; APOPTOSIS; CELL NUCLEUS; DNA; DNA DAMAGE; DNA LIGASES; DNA REPAIR; GAMMA RAYS; HUMANS; MODELS, BIOLOGICAL; PLASMIDS; POLY(ADP-RIBOSE) POLYMERASES; TIME FACTORS;

EID: 24744458206     PISSN: 08298211     EISSN: None     Source Type: Journal    
DOI: 10.1139/o05-044     Document Type: Review

References (57)

1. Althaus, F.R. 2005. Commentary: poly(ADP-ribose): a co-regulator of DNA methylation? Oncogene, 24: 11-12.
2. Althaus, F.R., Hofferer, L., Kleczkowska, H.E., Malanga, M., Naegeli, H., Panzeter, P.L., and Realini, C.A. 1994. Histone shuttling by poly(ADP-ribosyl)ation. Mol. Cell. Biochem. 138: 53-59.
3. Alvarez-Gonzalez, R., and Ringer, P. 1988. Nuclear matrix associated poly(ADP-ribose) metabolism in regenerating rat liver. FEBS Lett. 236: 362-366.
4. Alvarez-Gonzalez, R., Spring, H., Mueller, M., and Buerkle, A. 1999. Selective loss of poly(ADP-ribose) and the 85 kDa-fragment of poly(ADP-ribose) polymerase in nucleoli during alkylation-induced apoptosis of HeLa cells. J. Biol. Chem. 274: 32122-32126.
5. Audebert, M., Salles, B., and Calsou, P. 2004. Involvement of poly(ADP-ribose) polymerase-1 and XRCC1/DNA ligase III in an alternative route for DNA double-strand breaks rejoining. J. Biol. Chem. 279: 55117-55126.
6. Berezney, R., and Coffey, D.S. 1977. Nuclear matrix: isolation and characterization of a framework structure from rat liver nuclei. J. Cell Biol. 73: 616-637.
7. Bode, J., Kohwi, Y., Dickinson, L., Joh, T., Klehr, D., Mielke, C., and Kohwi-Shigematsu, T. 1992. Biological significance of unwinding capability of nuclear matrix-associated DNAs. Science (Wash.), 255: 195-197.
8. Bode, J., Goetze, S., Heng, H., Krawetz, S.A., and Benham, C. 2003. From DNA structure to gene expression: mediators of nuclear compartmentalization and -dynamics. Chromosome Res. 11: 435-445.
9. Boulikas, T. 1996. A unified model explaining the preferential repair of active over inactive genes and of the transcribed over the non-transcribed strand: a leading role for transcription factors and matrix. Int. J. Oncol. 8: 77-84.
10. Bradley, M.O., and Dysart, G. 1985. DNA single-strand breaks, double-strand breaks, and crosslinks in rat testicular germ cells: measurements of their formation and repair by alkaline and neutral filter elution. Cell Biol. Toxicol. 1: 181-95.
11. Buerkle, A. 2001. Poly(APD-ribosyl)ation, a DNA damage-driven protein modification and regulator of genomic instability. Cancer Lett. 163: 1-5.
12. Caldecott, K.W. 2001. Mammalian DNA single-strand break repair: an X-ra(y)ted affair. Bioessays, 23: 447-455.
13. Caldecott, K.W., Aoufouchi, S., Johnson, P., and Shall, S. 1996. XRCC1 polypeptide interacts with DNA polymerase beta and possibly poly(ADP-ribose) polymerase, and DNA ligase III is a novel molecular 'nick-sensor' in vitro. Nucleic Acids Res. 24: 4387-4394.
14. Cardenas-Corona, M.E., Jacobson, E.L., and Jacobson, M.K. 1987. Endogenous polymers of ADP-ribose are associated with the nuclear matrix. J. Biol. Chem. 262: 14863-14866.
15. Cook, P.R. 2002. Predicting three-dimensional genome structure from transcriptional activity. Nat. Genet. 32: 347-352.
16. Cremer, T., and Cremer, C. 2001. Chromosome territories, nuclear architecture and gene regulation in mammalian cells. Nat. Rev. Genet. 2: 292-301.
17. DiBiase, S.J., Curran, W.J., and Iliakis, G. 2000. DNA-PK stimulates an independently active non-homologous end-joining apparatus. Cancer Res. 60: 1245-1253.
18. Desmarais, Y., Menard, L., Lagueux, J., and Poirier, G.G. 1991. Enzymological properties of poly(ADP-ribose) polymerase: characterization of automodification sites and NADase activity. Biochim. Biophys. Acta, 1078: 179-186.
19. Desnoyers, S., Kaufmann, S.H., and Piorier, G.G. 1996. Alteration and the nucleolar localization of poly(ADP-ribose) polymerase upon treatment with transcription inhibitors. Exp. Cell Res. 227: 146-153.
20. Fernandes, D.J., and Catapano, C.V. 1995. The nuclear matrix as a site of anticancer drug action. Int. Rev. Cytol. 162A: 539-576.
21. Ferraro, A., Cervoni, L., Eufemi, M., Altieri, F., and Turano, C. 1996. Comparison of DNA-Protein interactions in nulei from avian liver and erythrocytes: a crosslinking study. J. Cell. Biochem. 62: 495-505.
22. Frouin, I., Maga, G., Denegri, M., Riva, F., Savio, M., Spadari, S., Prosperi, E., and Scovassi, A.I. 2003. Human proliferating cell nuclear antigen, Poly(ADP-ribose) polymerase-1, and p21waf1/ cip1. A dynamic exchange of partners. J. Biol. Chem. 278: 39265-39268.
23. Galande, S., and Kohwi-Shigematsu, T. 1999. Poly(ADP-ribose) polymerase and Ku autoantigen form a complex and synergistically bind to matrix attachment sequences. J. Biol. Chem. 274: 20521-20528.
24. Germain, M., Affar, E.B., D'Amours, D., Dixit, V.M., Salvesen, G.S., and Poirier, G.G. 1999. Cleavage of automodified poly(ADP-ribose) polymerase during apoptosis. Evidence for involvement of caspase-7. J. Biol. Chem. 274: 28379-28384.
25. Gerner, C., and Sauermann, G. 1999. Nuclear matrix proteins specific for subtypes of human hematopoietic cells. J. Cell. Biochem. 72: 470-482.
26. Goldman, R.D., Gruenbaum, Y., Moir, R.D., Shumaker, D.K., and Spann, T.P. 2002. Nuclear lamins: building blocks of nuclear architecture. Genes Dev. 16: 533-547.
27. Heng, H.H.Q., Goetze, S., Ye, C.J., Lu, W., Liu, G., Bremer, S., Hughes, M., Bode, J., and Krawetz, S.A. 2004. Dynamic features of scaffold/matrix attached regions (S/MARs) in anchoring chromatin loops. J. Cell Sci. 117: 999-1008.
28. Ivanović-Matić, S., Dinić, S., Vujoš evič, M., and Poznanović, G. 2000. The protein composition of the hepatocyte nuclear matrix is differentiation-stage specific. IUBMB Life, 49: 511-517.
29. Koehler, D.R., and Hanawalt, P.C. 1996. Recruitment of damaged DNA to the nuclear matrix in hamster cells following ultraviolet irradiation. Nucleic Acids Res. 24: 2877-2884.
30. Lee, J.Y., Chang, C., Song, H.K., Moon, J., Yang, J.K., Kim, H.-K., Kwon, S.-T., and Suh, S.W. 2000. Cristal structure of NAD+-dependent DNA ligase: modular architecture and functional implications. EMBO J. 19: 1119-1129.
31. Ludérus, M.E.E., Den Blaauwen, J.L., De Smit, O.J.B., Compton, D.A., and van Driel, R. 1994. Binding of matrix attachment regions to lamin Polymers involves single-stranded regions and the minor groove. Mol. Cell. Biol. 14: 6297-6305.
32. Ma, H., Siegel, A.J., and Berezney, R. 1999. Association of chromosome territories with the nuclear matrix: Disruption of human chromosome territories correlates with the release of a subset of nuclear matrix proteins. J. Cell Biol. 146: 531-541.
33. Ma, Y., Pannicke, U., Schwarz, K., and Lieber, M.R. 2002. Hairpin opening and overhang processing by an artemis/DNA-dependent protein kinase complex in nonhomologous end joining and V(D)J recombination. Cell, 108: 781-794.
34. Masson, M., Niedergang, C., Schreiber, V., Muller, S., de Murcia, J.M., 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.
35. Mauldin, S.K., Getts, R.C., Liu, W., and Stamato, T.D. 2002. DNA-PK-dependent binding of DNA ends to plasmids containing nuclear matrix attachment region DNA sequences: evidence for assembly of a repair complex. Nucleic Acids Res. 30: 4075-4087.
36. McElhinny, S.A.N., Snowden, C.M., McCarville, J., and Ramsden, D.A. 2000. Ku recruits the XRCC4-ligase IV complex to DNA ends. Mol. Cell Biol. 20: 2996-3003.
37. Nelms, B.E., Maser, R.S., MacKay, J.F., Lagally, M.G., and Petrini, J.H. 1998. In situ visualization of DNA double-strand break repair in human fibroblasts. Science (Wash.), 280: 590-592.
38. Noël, G., Giocanti, N., Fernet, M., Mégnin-Chanet, and F. Favaudon, V. 2003. Poly(ADP-ribose) polymerase (PARP-1) is not involved in DNA double-strand break recovery. BMC Cell Biol. 4: 7-10.
39. Oei, S.L., and Ziegler, M. 2000. ATP for the DNA ligation step in base excision repair is generated from poly(ADPribose). J. Biol. Chem. 275: 23234-23239.
40. Paunesku, T., Mittal, S., Protic, M., Oryhon, J., Korolev, S.V., Joachimiak, A., and Woloschjak, G.E. 2001. Proliferating cell nuclear antigen (PCNA): ringmaster of the genome. Int. J. Radiol. 77: 1007-1021.
41. Pleschke, J., Kleczkowska, H., Strohm, M., and Althaus, F.R. 2000. Poly(ADP-ribose) binds to specific domains in DNA damage checkpoint proteins. J. Biol. Chem. 275: 40974-40980.
42. Prosperi, E., and Scovassi, A.I. 2004. Dynamic interaction between PARP-1, PCNA and p21 waf1/cip1. In Poly(ADP-ribosyl)ation. Edited by A. Buerkle. Landes Bioscience, Chapter 7. ISBN 1-58706-292-5.
43. Quesada, P., d'Erme, M., Parise, G., Faraone-Mennella, M.R., Caiafa, P., and Farina, B. 1994. Nuclear matrix associated poly(ADP-ribosyl)ation system in rat testis chromatin. Exp. Cell Res. 214: 351-357.
44. Quesada, P., Atorino, L., Cardone, A., Ciarcia, G., and Farina, B. 1996. Poly(ADPribosyl)ation system in rat germinal cells at different stages of differentiation. Exp. Cell Res. 226: 183-190.
45. Quesada, P., Tramontano, F., Faraone-Mennella, M.R., and Farina, B. 2000. The analysis of the poly(ADPR) polymerase mode of action in rat testis nuclear fractions defines a specific poly(ADP-ribosyl)ation system associated with the nuclear matrix. Mol. Cell. Biochem. 205: 91-99.
46. Reale, A., De Matteis, G., Galleazzi, G., Zampieri, M., and Caiafa, P. 2005. Modulation of DNMT1 activity by ADP-ribose polymers. Oncogene, 24: 13-19.
47. Rolli, V., Ruf, A., Augustin, A., Schulz, G.E., Menissier de Murcia, J., and de Murcia, G. 2000. Poly(ADP-ribose)polymerase structure and function and poly ADP-ribosylation reactions. In From DNA damage and stress signaling to cell death. Edited by G. de Murcia and S. Shall. Oxford University Press, Inc., New York, Oxford. pp. 35-57.
48. Ruscetti, T., Lehnert, B.E., Le Trong, J.H., Hoekstra, M.F., Chen, D.J., and Peterson, S.R. 1998. Stimulation of the DNA-dependent protein kinase by Poly(ADP-Ribose) polymerase. J. Biol. Chem. 273: 14461-14467.
49. Sastry, S.S., and Kun, E. 1990. The interaction of adenosine diphosphoribosyl transferase (ADPRT) with a cruciform DNA. Biochem. Biophys. Res. Commun. 167: 842-847.
50. Schreiber, V., Ame, J.C., Dolle, P., Schultz, I., Rinaldi, B., Fraulob, V. et al. 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.
51. Slee, E.A., Adrain, C., and Martin, S.J. 2001. Executioner caspase-3, -6 and -7 perform distinct, non-redundant roles during the demolition phase of apoptosis. J. Biol. Chem. 276: 7320-7326.
52. Soldatenkov, V.A., Chasovskikh, S., Potaman, V.N., Trofimova, I., Smulson, M.E., and Dritschilo, A. 2002. Transcriptional repression by binding of poly(ADP-ribose) polymerase to promoter sequences. J. Biol. Chem. 277: 665-670.
53. Stein, G.S., Zaidi S.K., Braastad, C.D., Montecino, M., van Wijnen, A.J., Choi, J.Y. et al. 2003. Functional architecture of the nucleus: organizing the regulatory machinery for gene expression, replication and repair. Trends Cell Biol. 13: 584-592.
54. Sukhanova, M.V., Lavrik, O.I., and Khodyreva, S.N. 2004. Poly (ADP-ribose) polymerase-1: a regulator of protein-nucleic acid interactions in processes responding to genotoxic impact. Mol. Biol. 38: 706-717.
55. Tewari, M., Quan, L.T., O'Rourke, K., Desnoyers, S., Zeng, Z., Beidler, D.R. et al. 1995. Yama/CPP32 beta, a mammalian homolog of CED-3, is a CrmA-inhibitable protease that cleaves the death substrate Poly (ADP-ribose) polymerase. Cell, 81: 801-809.
56. Vidaković, M., Grdović, N., Quesada, P., Poznanović, G., and Bode, J. 2004. Poly(ADP-ribose) polymerase-1 association with the peripheral nuclear lamina in rat hepatocytes. J. Cell. Biochem. 93: 1155-1168.
57. Vidaković, M., Koester, M., Goetze, S., Winkelmann, S., Klar, M., Poznanović, G., and Bode, J. 2005. Colocalization of PARP-1 and lamin B in the nuclear architecture: a halo-FISH and confocal microscopy study. J. Cell. Biochem. In press.