Dynamic relocation of poly(ADP-ribose) glycohydrolase isoforms during radiation-induced DNA damage

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1763, Issue 2, 2006, Pages 226-237

  Haince, Jean François ^a   Ouellet, Marie Eve ^a   McDonald, Darin ^b   Hendzel, Michael J ^b   Poirier, Guy G ^a  

^a LAVAL UNIVERSITY   (Canada)

^b UNIVERSITY OF ALBERTA   (Canada)

Author keywords

DNA damage; FRAP; Nucleocytoplasmic shuttling; Poly(ADP ribose); Poly(ADP ribose) glycohydrolase; Subcellular localization

Indexed keywords

GLYCOSIDASE; HYBRID PROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR; POLY(ADENOSINE DIPHOSPHATE RIBOSE);

ARTICLE; BLEACHING; CONTROLLED STUDY; CYTOPLASM; DNA DAMAGE; DNA REPAIR; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; RADIATION;

BLOTTING, WESTERN; CELL LINE, TUMOR; CELL NUCLEUS; CYTOPLASM; DIFFUSION; DNA; DNA DAMAGE; ELECTROPHORESIS, POLYACRYLAMIDE GEL; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; GLYCOSIDE HYDROLASES; HUMANS; ISOENZYMES; KINETICS; MICROSCOPY, FLUORESCENCE; NEUROBLASTOMA; POLY ADENOSINE DIPHOSPHATE RIBOSE; RADIATION, IONIZING; SUBCELLULAR FRACTIONS;

EID: 33644984966     PISSN: 01674889     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2005.11.015     Document Type: Article

References (56)

1. V.J. Bouchard, M. Rouleau, and G.G. Poirier PARP-1, a determinant of cell survival in response to DNA damage Exp. Hematol. 31 2003 446 454
2. A. Ivana Scovassi, and M. Diederich Modulation of poly(ADP-ribosylation) in apoptotic cells Biochem. Pharmacol. 68 2004 1041 1047
3. S.W. Yu, H. Wang, T.M. Dawson, and V.L. Dawson Poly(ADP-ribose) polymerase-1 and apoptosis inducing factor in neurotoxicity Neurobiol. Dis. 14 2003 303 317
4. M.Y. Kim, S. Mauro, N. Gevry, J.T. Lis, and W.L. Kraus NAD+-dependent modulation of chromatin structure and transcription by nucleosome binding properties of PARP-1 Cell 119 2004 803 814
5. V. Pirrotta The ways of PARP Cell 119 2004 735 736
6. M.L. Meyer-Ficca, R.G. Meyer, E.L. Jacobson, and M.K. Jacobson Poly(ADP-ribose) polymerases: managing genome stability Int. J. Biochem. Cell Biol. 37 2005 920 926
7. D. D'Amours, S. Desnoyers, I. D'Silva, and G.G. Poirier Poly(ADP-ribosyl)ation reactions in the regulation of nuclear functions Biochem. J. 342 1999 249 268
8. J.C. Ame, V. Rolli, V. Schreiber, C. Niedergang, F. Apiou, P. Decker, S. Muller, T. Hoger, and J. Menissier-de Murcia G. de Murcia, PARP-2, A novel mammalian DNA damage-dependent poly(ADP-ribose) polymerase J. Biol. Chem. 274 1999 17860 17868
9. V. Schreiber, J.C. Ame, P. Dolle, I. Schultz, B. Rinaldi, V. Fraulob, J. Menissier-de Murcia, and G. de Murcia 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 2002 23028 23036
10. J.C. Ame, C. Spenlehauer, and G. de Murcia The PARP superfamily Bioessays 26 2004 882 893
11. M.E. Bonicalzi, J.F. Haince, A. Droit, and G.G. Poirier Regulation of poly(ADP-ribose) metabolism by poly(ADP-ribose) glycohydrolase: where and when? Cell Mol. Life Sci. 62 2005 739 750
12. W. Lin, J.C. Ame, N. Aboul-Ela, E.L. Jacobson, and M.K. Jacobson Isolation and characterization of the cDNA encoding bovine poly(ADP-ribose) glycohydrolase J. Biol. Chem. 272 1997 11895 11901
13. J.C. Ame, F. Apiou, E.L. Jacobson, and M.K. Jacobson Assignment of the poly(ADP-ribose) glycohydrolase gene (PARG) to human chromosome 10q11.23 and mouse chromosome 14B by in situ hybridization Cytogenet. Cell Genet. 85 1999 269 270
14. E. Winstall, E.B. Affar, R. Shah, S. Bourassa, A.I. Scovassi, and G.G. Poirier Poly(ADP-ribose) glycohydrolase is present and active in mammalian cells as a 110-kDa protein Exp. Cell Res. 246 1999 395 398
15. S. Panda, G.G. Poirier, and S.A. Kay tej defines a role for poly(ADP-ribosyl)ation in establishing period length of the Arabidopsis circadian oscillator Dev. Cell 3 2002 51 61
16. T. Shimokawa, M. Masutani, S. Nagasawa, T. Nozaki, N. Ikota, Y. Aoki, H. Nakagama, and T. Sugimura Isolation and cloning of rat poly(ADP-ribose) glycohydrolase: presence of a potential nuclear export signal conserved in mammalian orthologs J. Biochem. (Tokyo) 126 1999 748 755
17. R.G. Meyer, M.L. Meyer-Ficca, E.L. Jacobson, and M.K. Jacobson Human poly(ADP-ribose) glycohydrolase (PARG) gene and the common promoter sequence it shares with inner mitochondrial membrane translocase 23 (TIM23) Gene 314 2003 181 190
18. M.L. Meyer-Ficca, R.G. Meyer, D.L. Coyle, E.L. Jacobson, and M.K. Jacobson Human poly(ADP-ribose) glycohydrolase is expressed in alternative splice variants yielding isoforms that localize to different cell compartments Exp. Cell Res. 297 2004 521 532
19. C.N. Patel, D.W. Koh, M.K. Jacobson, and M.A. Oliveira Identification of three critical acidic residues of poly(ADP-ribose) glycohydrolase involved in catalysis: determining the PARG catalytic domain Biochem. J. 388 2005 493 500
20. D.W. Koh, A.M. Lawler, M.F. Poitras, M. Sasaki, S. Wattler, M.C. Nehls, T. Stoger, G.G. Poirier, V.L. Dawson, and T.M. Dawson Failure to degrade poly(ADP-ribose) causes increased sensitivity to cytotoxicity and early embryonic lethality Proc. Natl. Acad. Sci. U. S. A. 101 2004 17699 17704
21. E.B. Affar, M. Germain, E. Winstall, M. Vodenicharov, R.G. Shah, G.S. Salvesen, and G.G. Poirier Caspase-3-mediated processing of poly(ADP-ribose) glycohydrolase during apoptosis J. Biol. Chem. 276 2001 2935 2942
22. S. Ohashi, M. Kanai, S. Hanai, F. Uchiumi, H. Maruta, S. Tanuma, and M. Miwa Subcellular localization of poly(ADP-ribose) glycohydrolase in mammalian cells Biochem. Biophys. Res. Commun. 307 2003 915 921
23. M.E. Bonicalzi, M. Vodenicharov, M. Coulombe, J.P. Gagne, and G.G. Poirier Alteration of poly(ADP-ribose) glycohydrolase nucleocytoplasmic shuttling characteristics upon cleavage by apoptotic proteases Biol. Cell 95 2003 635 644
24. J.C. Ame, E.L. Jacobson, and M.K. Jacobson Molecular heterogeneity and regulation of poly(ADP-ribose) glycohydrolase Mol. Cell. Biochem. 193 1999 75 81
25. J.P. Gagné, M.-E. Bonicalzi, P. Gagné, M.-E. Ouellet, M.J. Hendzel, and G.G. Poirier Poly(ADP-ribose) glycohydrolase is a component of the FMRP-associated messenger ribonucleoparticles Biochem. J. 392 2005 499 509
26. A.M. Ferro, and N.J. Oppenheimer Structure of a poly (adenosine diphosphoribose) monomer: 2′-(5″-hosphoribosyl)-5′-adenosine monophosphate Proc. Natl. Acad. Sci. U. S. A. 75 1978 809 813
27. R.C. Benjamin, and D.M. Gill Poly(ADP-ribose) synthesis in vitro programmed by damaged DNA. A comparison of DNA molecules containing different types of strand breaks J. Biol. Chem. 255 1980 10502 10508
28. K. Wielckens, E. George, T. Pless, and H. Hilz Stimulation of poly(ADP-ribosyl)ation during Ehrlich ascites tumor cell "starvation" and suppression of concomitant DNA fragmentation by benzamide J. Biol. Chem. 258 1983 4098 4104
29. A. Kreimeyer, K. Wielckens, P. Adamietz, and H. Hilz DNA repair-associated ADP-ribosylation in vivo. Modification of histone H1 differs from that of the principal acceptor proteins J. Biol. Chem. 259 1984 890 896
30. R. Alvarez-Gonzalez, and F.R. Althaus Poly(ADP-ribose) catabolism in mammalian cells exposed to DNA-damaging agents Mutat. Res. 218 1989 67 74
31. F. Simonin, O. Poch, M. Delarue, and G. de Murcia Identification of potential active-site residues in the human poly(ADP-ribose) polymerase J. Biol. Chem. 268 1993 8529 8535
32. L. Tartier, C. Spenlehauer, H.C. Newman, M. Folkard, K.M. Prise, B.D. Michael, J. Menissier-de Murcia, and G. de Murcia Local DNA damage by proton microbeam irradiation induces poly(ADP-ribose) synthesis in mammalian cells Mutagenesis 18 2003 411 416
33. F.R. Althaus, and C. Richter ADP-ribosylation of proteins. Enzymology and biological significance Mol. Biol. Biochem. Biophys. 37 1987 1 237
34. Y.H. Kang, M.J. Yi, M.J. Kim, M.T. Park, S. Bae, C.M. Kang, C.K. Cho, I.C. Park, M.J. Park, C.H. Rhee, S.I. Hong, H.Y. Chung, Y.S. Lee, and S.J. Lee Caspase-independent cell death by arsenic trioxide in human cervical cancer cells: reactive oxygen species-mediated poly(ADP-ribose) polymerase-1 activation signals apoptosis-inducing factor release from mitochondria Cancer Res. 64 2004 8960 8967
35. S. Hanai, M. Kanai, S. Ohashi, K. Okamoto, M. Yamada, H. Takahashi, and M. Miwa Loss of poly(ADP-ribose) glycohydrolase causes progressive neurodegeneration in Drosophila melanogaster Proc. Natl. Acad. Sci. U. S. A. 101 2004 82 86
36. U. Cortes, W.M. Tong, D.L. Coyle, M.L. Meyer-Ficca, R.G. Meyer, V. Petrilli, Z. Herceg, E.L. Jacobson, M.K. Jacobson, and Z.Q. Wang Depletion of the 110-kilodalton isoform of poly(ADP-ribose) glycohydrolase increases sensitivity to genotoxic and endotoxic stress in mice Mol. Cell. Biol. 24 2004 7163 7178
37. N.S. Patel, U. Cortes, R. Di Poala, E. Mazzon, H. Mota-Filipe, S. Cuzzocrea, Z.Q. Wang, and C. Thiemermann Mice lacking the 110-kD isoform of poly(ADP-Ribose) glycohydrolase are protected against renal ischemia/reperfusion injury J. Am. Soc. Nephrol. 16 2005 712 719
38. D. Koh, V. Dawson, and T. Dawson The road to survival goes through PARG Cell Cycle 4 2005 397 399
39. M. Masutani, H. Nakagama, and T. Sugimura Poly(ADP-ribose) and carcinogenesis Genes Chromosomes Cancer 38 2003 339 348
40. W. Ying, M.B. Sevigny, Y. Chen, and R.A. Swanson Poly(ADP-ribose) glycohydrolase mediates oxidative and excitotoxic neuronal death Proc. Natl. Acad. Sci. U. S. A. 98 2001 12227 12232
41. H. Chen, D.D. Hughes, T.A. Chan, J.W. Sedat, and D.A. Agard IVE (Image Visualization Environment): a software platform for all three-dimensional microscopy applications J. Struct. Biol. 116 1996 56 60
42. G. Carrero, D. McDonald, E. Crawford, G. de Vries, and M.J. Hendzel Using FRAP and mathematical modeling to determine the in vivo kinetics of nuclear proteins Methods 29 2003 14 28
43. G. Carrero, E. Crawford, J. Th'ng, G. de Vries, and M.J. Hendzel Quantification of protein-protein and protein-DNA interactions in vivo, using fluorescence recovery after photobleaching Methods Enzymol. 375 2004 415 442
44. G. Brochu, G.M. Shah, and G.G. Poirier Purification of poly(ADP-ribose) glycohydrolase and detection of its isoforms by a zymogram following one- or two-dimensional electrophoresis Anal. Biochem. 218 1994 265 272
45. N.W. Chi, and H.F. Lodish Tankyrase is a Golgi-associated mitogen-activated protein kinase substrate that interacts with IRAP in GLUT4 vesicles J. Biol. Chem. 275 2000 38437 38444
46. J.M. Graham, and D. Rickwood Subcellular Fractionation: A Practical Approach 1997 IRL Press Oxford, NY
47. G.G. Jonsson, L. Menard, E.L. Jacobson, G.G. Poirier, and M.K. Jacobson Effect of hyperthermia on poly(adenosine diphosphate-ribose) glycohydrolase Cancer Res. 48 1988 4240 4243
48. E. Winstall, E.B. Affar, R. Shah, S. Bourassa, I.A. Scovassi, and G.G. Poirier Preferential perinuclear localization of poly(ADP-ribose) glycohydrolase Exp. Cell Res. 251 1999 372 378
49. H. Hilz, K. Wielckens, P. Adamietz, R. Bredehorst, and A. Kreymeier Functional aspects of mono- and poly(ADP-ribosyl)ation: subcellular distribution and ADP-ribosyl turnover under conditions of repair and 'starvation' Princess Takamatsu Symp. 13 1983 155 163
50. H. Maruta, N. Matsumura, and S. Tanuma Role of (ADP-ribose)n catabolism in DNA repair Biochem. Biophys. Res. Commun. 236 1997 265 269
51. V.S. Meder, M. Boeglin, G. de Murcia, and V. Schreiber PARP-1 and PARP-2 interact with nucleophosmin/B23 and accumulate in transcriptionally active nucleoli J. Cell Sci. 118 2005 211 222
52. J.S. Andersen, C.E. Lyon, A.H. Fox, A.K. Leung, Y.W. Lam, H. Steen, M. Mann, and A.I. Lamond Directed proteomic analysis of the human nucleolus Curr. Biol. 12 2002 1 11
53. N. Leitinger, and J. Wesierska-Gadek ADP-ribosylation of nucleolar proteins in HeLa tumor cells J. Cell. Biochem. 52 1993 153 158
54. S. Desnoyers, S.H. Kaufmann, and G.G. Poirier Alteration of the nucleolar localization of poly(ADP-ribose) polymerase upon treatment with transcription inhibitors Exp. Cell Res. 227 1996 146 153
55. S. Beneke, J. Diefenbach, and A. Burkle Poly(ADP-ribosyl)ation inhibitors: promising drug candidates for a wide variety of pathophysiologic conditions Int. J. Cancer 111 2004 813 818
56. S.W. Yu, H. Wang, M.F. Poitras, C. Coombs, W.J. Bowers, H.J. Federoff, G.G. Poirier, T.M. Dawson, and V.L. Dawson Mediation of poly(ADP-ribose) polymerase-1-dependent cell death by apoptosis-inducing factor Science 297 2002 259 263