Pol (ADP-ribosyl)ated chromatin domains: Access granted

Journal of Cell Science

Volumn 117, Issue 6, 2004, Pages 815-825

  Rouleau, Michèle ^a   Aubin, Rémy A ^b   Poirier, Guy G ^a  

^a UNIVERSITÉ LAVAL   (Canada)

^b Health Canada and World Health Organization Collaborating Center for Standardization and Evaluation of Biologicals   (Canada)

Author keywords

Chromatin; Histones; PARG; PARP; Poly(ADP ribose); Poly(ADP ribosyl)ation

Indexed keywords

HISTONE; HISTONE H1; HISTONE H2A; HISTONE H2B; HISTONE H3; HISTONE H4; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; POLY(ADENOSINE DIPHOSPHATE RIBOSE); DNA; NICOTINAMIDE ADENINE DINUCLEOTIDE; NONHISTONE PROTEIN;

ADENOSINE DIPHOSPHATE RIBOSYLATION; CHROMATIN CONDENSATION; CHROMATIN STRUCTURE; CYTOARCHITECTURE; DNA DAMAGE; DNA METABOLISM; DNA RECOMBINATION; DNA REPAIR; DNA REPLICATION; DNA TRANSCRIPTION; GENE ACTIVITY; GENE FUNCTION; GENETIC CODE; GENETIC STABILITY; GENETIC TRANSCRIPTION; HUMAN; INTERPHASE; MITOSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN PROCESSING; PROTEIN VARIANT; REVIEW; ANIMAL; APOPTOSIS; CELL NUCLEUS; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOME; CONFORMATION; METABOLISM; PHYSIOLOGY;

ANIMALS; APOPTOSIS; CELL NUCLEUS; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOMAL PROTEINS, NON-HISTONE; CHROMOSOMES; DNA; HISTONES; HUMANS; NAD; NUCLEIC ACID CONFORMATION; POLY ADENOSINE DIPHOSPHATE RIBOSE; POLY(ADP-RIBOSE) POLYMERASES; TRANSCRIPTION, GENETIC;

EID: 1642308537     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.01080     Document Type: Review

References (117)

1. Adamietz, P. and Rudolph, A. (1984). ADP-ribosylation of nuclear proteins in vivo. Identification of histone H2B as a major acceptor for mono- and poly(ADP-ribose) in dimethyl sulfate-treated hepatoma AH 7974 cells. J. Biol. Chem. 259, 6841-6846.
2. Adolph, K. W. and Song, M. K. (1985a). Variations in ADP-ribosylation of nuclear scaffold proteins during the HeLa cell cycle. Biochem. Biophys. Res. Commun. 126, 840-847.
3. Adolph, K. W. and Song, M. K. (1985b). Decrease in ADP-ribosylation of HeLa non-histone proteins from interphase to metaphase. Biochemistry 24, 345-352.
4. Affar, E. B., Germain, M. and Poirier, G. G. (2000). Role of poly(ADP-ribose) polymerase in cell death. In Poly(ADP-ribosyl)ation Reactions: From DNA Damage And Stress Signalling To Cell Death (ed. G. de Murcia and S. Shall), pp. 125-150. Oxford: Oxford University Press.
5. Allen, M. D., Buckle, A. M., Cordell, S. C., Löwe, J. and Bycroft, M. (2003). The crystal structure of AF1521 a protein from Archaeoglobus fulgidus with homology to the non-histone domain of macro H2A. J. Mol. Biol. 330, 503-511.
6. Althaus, F. R. (1992). Poly ADP-ribosylation: a histone shuttle mechanism in DNA excision repair. J. Cell Sci. 102, 663-670.
7. Alvarez-Gonzalez, R. and Jacobson, M. K. (1987). Characterization of polymers of adenosine diphosphate ribose generated in vitro and in vivo. Biochemistry 26, 3218-3224.
8. Aravind, L. (2001). The WWE domain: a common interaction module in protein ubiquitination and ADP ribosylation. Trends Biochem. Sci. 26, 273-275.
9. Arents, G. and Moudrianakis, E. N. (1995). The histone fold: a ubiquitous architectural motif utilized in DNA compaction and protein dimerization. Proc. Natl. Acad. Sci. USA 92, 11170-11174.
10. Aubin, R., Fréchette, A., de Murcia, G., Mandel, P., Lord, A. and Poirier, G. G. (1983). Correlation between endogenous nucleosomal hyper(ADP-ribosyl)ation of histone H1 and the induction of chromatin relaxation. EMBO J. 2, 1685-1693.
11. Augustin, A., Spenlehauer, C., Dumond, H., Ménissier-de Murcia, J., Piel, M., Schmit, A. C., Aplou, F., Vonesch, J. L., Kock, M., Bornens, M. et al. (2003). PARP-3 localizes preferentially to the daughter centriole and interferes with the G1/S cycle progression. J. Cell Sci. 116, 1551-1562.
12. Ausió, J., Abbott, D. W., Wang, X. and Moore, S. C. (2001). Histone variants and histone modifications: A structural perspective. Biochem. Cell Biol. 79, 693-708.
13. Benjamin, R. C. and Gill, D. M. (1980). 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, 10502-10508.
14. Bonicalzi, M. E., Vodenicharov, M., Coulombe, M., Gagné, J. P. and Poirier, G. G. (2003). Alteration of poly(ADP-ribose) glycohydrolase nucleocytoplasmic shuttling characteristics upon cleavage by apoptotic proteases. Biol. Cell. 95, 635-644.
15. Bouchard, V. J., Rouleau, M. and Poirier, G. G. (2003). PARP-1, a determinant of cell survival in response to DNA damage. Exp. Hematol. 31, 446-454.
16. Bürkle, A., Schreiber, V., Dantzer, F., Olivier, F. J., Niedergang, C., de Murcia, G. and Ménissier-de Murcia, J. (2000). Biological significance of poly(ADP-ribosyl)ation reactions: Molecular and genetic approaches. In Poly(ADP-ribosyl)ation Reactions: From DNA Damage And Stress Signalling To Cell Death (ed. G. de Murcia and S. Shall), pp. 80-124. Oxford: Oxford University Press.
17. Bustin, M. (2001). Revised nomenclature for high mobility group (HMG) chromosomal proteins. Trends Biochem. Sci. 26, 152-153.
18. Butt, T. R., deCoste, B., Jump, D. B., Nolan, N. and Smulson, M. E. (1980). Characterization of a putative poly(adenosine diphosphate ribose)-chromatin complex. Biochemistry 19, 5243-5249.
19. Candé, C., Cecconi, F., Dessen, P. and Kroemer, G. (2002). Apoptosis-inducing factor (AIF): key to the conserved caspase-independent pathways of cell death? J. Cell Sci. 115, 4727-4734.
20. Chan, S. W. and Blackburn, E. H. (2002). New ways not to make ends meet: telomerase, DNA damage proteins and heterochromatin. Oncogene 21, 553-563.
21. Chiarugi, A. (2002). Poly(ADP-ribose) polymerase: killer or conspirator? The 'suicide hypothesis' revisited. Trends Pharmacol. Sci. 23, 122-129.
22. Cook, B. D., Dynek, J. N., Chang, W., Shostak, G. and Smith, S. (2002). Role for the related poly(ADP-ribose) polymerases tankyrase 1 and 2 at human telomeres. Mol. Cell. Biol. 22, 332-342.
23. Costanzi, C. and Pehrson, J. R. (1998). Histone macroH2A1 is concentrated in the inactive X chromosome of female mammals. Nature 393, 599-601.
24. 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.
25. Davidovic, L., Vodenicharov, M., Affar, E. B. and Poirier, G. G. (2001). Importance of poly(ADP-ribose) glycohydrolase in the control of poly(ADP-ribose) metabolism. Exp. Cell Res. 268, 7-13.
26. 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.
27. D'Amours, D., Sallmann, F. R., Dixit, V. M. and Poirier, G. G. (2001). Gain-of-function of poly(ADP-ribose) poymerase-1 upon cleavage by apoptotic proteases: implication for apoptosis. J. Cell Sci. 114, 3771-3778.
28. de Capoa, A., Febbo, F. R., Giovannelli, F., Niveleau, A., Zardo, G., Marenzi, S. and Caiafa, P. (1999). Reduced levels of poly(ADP-ribosyl)ation result in chromatin compaction and hypermethylation as shown by cell-by-cell computer-assisted quantitative analysis. FASEB J. 13, 89-93.
29. de Murcia, G., Huletsky, A., Lamarre, D., Gaudreau, A., Pouyet, J., Daune, M. and Poirier, G. G. (1986). Modulation of chromatin superstructure by poly(ADP-ribose) synthesis and degradation. J. Biol. Chem. 261, 7011-7017.
30. d'Erme, M., Zardo, G., Reale, A. and Caiafa, P. (1996). Cooperative interactions of oligonucleosomal DNA with the h1e histone variant and its poly(ADP-ribosyl)ated isoform. Biochem. J. 316, 475-480.
31. Desnoyers, S., Shah, G. M., Brochu, G., Hoflack, J. C., Verreault, A. and Poirier, G. G. (1995). Biochemical properties and function of poly(ADP-ribose) glycohydrolase. Biochimie 77, 433-438.
32. 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.
33. Fakan, S., Leduc, Y., Lamarre, D., Brunet, G. and Poirier, G. G. (1988). Immunoelectron microscopical distribution of poly(ADP-ribose) polymerase in the mammalian cell nucleus. Exp. Cell Res. 179, 517-526.
34. Flohr, C., Burkle, A., Radicella, J. P. and Epe, B. (2003). Poly(ADP-ribosyl)ation accelerates DNA repair in a pathway dependent on Cockayne syndrome B protein. Nucleic Acids Res. 31, 5332-5337.
35. 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.
36. Futai, M., Mizuno, D. and Sugimura, T. (1968). Mode of action of rat liver phosphodiesterase on a polymer of phosphoribosyl adenosine monophosphate and related compounds. J Biol. Chem. 243, 6325-6329.
37. Gagné, J. P., Hunter, J., Labreque, B., Chabot, B. and Poirier, G. G. (2003). A proteomic approach to the identification of heterogeneous nuclear ribonucleoproteins as a new family of poly(ADP-ribose)-binding proteins. Biochem. J. 371, 331-340.
38. 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.
39. Gradwohl, G., Mazen, A. and de Murcia, G. (1987). Poly(ADP-ribose) polymerase form loops with DNA. Biochem. Biophys. Res. Commun. 148, 913-919.
40. Hassa, P. O. and Hottiger, M. O. (2002). The functional role of poly(ADP-ribose) polymerase 1 as novel coactivator of NF-κB in inflammatory disorders. Cell. Mol. Life Sci. 59, 1534-1553.
41. Huletsky, A., Niedergang, C., Fréchette, A., Aubin, R., Gaudreau, A. and Poirier, G. G. (1985). Sequential poly(ADP-ribosyl)ation pattern of nucleosomal histones. Eur. J. Biochem. 14, 277-285.
42. Huletsky, A., de Murcia, G., Muller, S., Hengartner, M., Lamarre, D. and Poirier, G. G. (1989). The effect of poly(ADP-ribosyl)ation on native and H1-depleted chromatin. A role of poly(ADP-ribosyl)ation on core nucleosome structure. J. Biol. Chem. 264, 8878-8886.
43. Ikejima, M., Noguchi, S., Yamashita, R., Ogura, T., Sugimura, T., Gill, D. M. and Miwa, M. (1990). The zinc fingers of human poly(ADP-ribose) polymerase are differentially required for the recognition of DNA breaks and nicks and the consequent enzyme activation. Other structures recognize intact DNA. J. Biol. Chem. 265, 21907-21913.
44. Kaufmann, S. H., Brunet, G., Talbot, B., Lamarre, D., Dumas, C., Shaper, J. and Poirier, G. G. (1991). Association of poly(ADP-ribose) polymerase with the nuclear matrix. Exp. Cell Res. 192, 524-535.
45. Kaufmann, S. H., Desnoyers, S., Ottaviano, Y., Davidson, N. E. and Poirier, G. G. (1993). Specific proteolytic cleavage of poly(ADP-ribose) polymerase: an early marker of chemotherapy-induced apoptosis. Cancer Res. 53, 3976-3985.
46. Konishi, A., Shimizu, S., Hirota, J., Takao, T., Fan, Y., Matsuoka, Y., Zhang, L., Yoneda, Y., Fujii, Y., Skoultchi, A. I. et al. (2003). Involvement of histone H1.2 in apoptosis induced by DNA double-strand breaks. Cell 114, 673-688.
47. Kraus, W. L. and Lis, J. J. (2003). PARP goes transcription. Cell 113, 677-683.
48. Krupitza, G. and Cerutti, P. (1989a). Poly(ADP-ribosylation) of histones in intact human keratinocytes. Biochemistry 28, 4054-4060.
49. Krupitza, G. and Cerutti, P. (1989b). ADP-ribosylation of ADPR-transferase and topoisomerase I in intact mouse epidermal cells JB6. Biochemistry 28, 2034-2040.
50. Lachner, M., O'Sullivan, R. J. and Jenuwein, T. (2003). An epigenetic road map for histone lysine methylation. J. Cell Sci. 116, 2117-2124.
51. Ladurner, G. (2003). Inactivating chromosomes: A macro domain that minimizes transcription. Mol. Cell 12, 1-4.
52. Lamarre, D., Talbot, B., de Murcia, G., Laplante, C., Leduc, Y., Mazen, A. and Poirier, G. G. (1988). Structural and functional analysis of poly(ADP-ribose) polymerase: an immunological study. Biochim. Biophys. Acta 950, 147-160.
53. 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. J. Biol. Chem. 276, 25541-25548.
54. Leppard, J. B., Dong, Z., Mackey, Z. B. and Tomkinson, A. E. (2003). Physical and functional interaction between DNA ligase IIIalpha and poly(ADP-Ribose) polymerase 1 in DNA single-strand break repair. Mol. Cell. Biol. 16, 5919-5927.
55. Levy-Wilson, B. (1981). ADP-ribosylation of trout testis chromosomal proteins: distribution of ADP-ribosylated proteins among DNase I-sensitive and -resistant chromatin domains. Arch. Biochem. Biophys. 208, 528-534.
56. Lindahl, T., Satoh, M. S., Poirier, G. G. and Klungland, A. (1995). Posttranslational modification of poly(ADP-ribose) polymerase induced by DNA strand breaks. Trends Biochem. Sci. 20, 405-411.
57. Lizuka, M. and Smith, M. M. (2003). Functional consequences of histone modifications. Curr. Opin. Gen. Dev. 13, 154-160.
58. Malanga, M., Atorino, L., Tramontano, F., Farina, B. and Quesada, P. (1998). Poly(ADP-ribose) binding properties of histone H1 variants. Biochim. Biophys. Acta 1399, 154-160.
59. Ménissier-de Murcia, J., Ricoul, M., Tartier, L., Niedergang, C., Huber, A., Dantzer, F., Schreiber, V., Amé, J. C., Dierich, A., LeMeur, M. et al. (2003). Functional interaction between PARP-1 and PARP-2 in chromosome stability and embryonic development in mouse. EMBO J. 22, 2255-2263.
60. Mennella, M. R., Quesada, P., Farina, B., Leone, E. and Jones, R. (1982). ADP-ribosylation of nuclear proteins in mouse testis. Biochem. J. 205, 245-248.
61. Miwa, M. and Sugimura, T. (1982). Phosphodiesterases and poly(ADP-ribose) glycohydrolase. In ADP-Ribosylation Reactions (ed. O. Hayaishi and K. Ueda), pp. 263-277. New York: Academic Press.
62. Nolan, N. L., Butt, T. R., Wong, M., Lambrianidon, A. and Smulson, M. E. (1980). Characterization of poly(ADP-ribose)-histone H1 complex formation in purified polynucleosomes and chromatin. Eur. J. Biochem. 113, 15-25.
63. Ogata, N., Ueda, K. and Hayaishi, O. (1980a). ADP-ribosylation of histone H2B. Identification of glutamic acid residue 2 as the modification site. J. Biol. Chem. 255, 7610-7615.
64. Ogata, N., Ueda, K., Kagamiyona, H. and Hayaishi, O. (1980b). ADP-ribosylation of histone H1. Identification of glutamic acid residues 2, 14, and the COOH-terminal lysine residue as modification sites. J. Biol. Chem. 255, 7616-7620.
65. Ohashi, S., Kanai, M., Hanai, S., Uchiumi, F., Maruta, H., Tanuma, S. and Miwa, M. (2003). Subcellular localization of poly(ADP-ribose) glycohydrolase in mammalian cells. Biochem. Biophys. Res. Com. 307, 915-921.
66. Oka, J., Ueda, K., Hayaishi, O., Komura, H. and Nakanishi, K. (1984). ADP-ribosyl protein lyase. Purification, properties, and identification of the product. J. Biol. Chem. 259, 986-995.
67. 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.
68. Okayama, H., Ueda, K. and Hayaishi, O. (1978a). Purification of ADP-ribosylated nuclear proteins by covalent chromatography on dihydroxyboryl polyacrylamide beads and their characterization. Proc. Natl. Acad. Sci. USA 75, 1111-1115.
69. Okayama, H. and Hayaishi, O. (1978b). ADP-ribosylation of nuclear protein A24. Biochem. Biophys. Res. Commun. 84, 755-762.
70. Panzeter, P. L., Zweifel, B., Malanga, M., Waser, S. H., Richard, M. C. and Althaus, F. R. (1993). Targeting of histone tails by poly(ADP-ribose). J. Biol. Chem. 268, 17662-17664.
71. Pedraza-Reyes, M. and Alvarez-Gonzales, R. (1990). Oligo(3′-deoxy ADP-ribosyl)ation of the nuclear matrix lamins from rat liver utilizing 3′-deoxy NAD as a substrate. FEBS Lett. 277, 88-92.
72. Pleschke, J. M., Kleczkowska, H. E., 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.
73. Poirier, G. G., de Murcia, G., Niedergang, C., Jongstra-Bilen, J. and Mandel, P. (1982a). Poly(ADP-ribosyl)ation of polynucleosomes causes relaxation of the chromatin structure. Proc. Natl. Acad. Sci. USA 79, 3423-3427.
74. Poirier, G. G., Niedergang, C., Champagne, M., Mazen, A. and Mandel, P. (1982b). Adenosine diphosphate ribosylation of chicken-erythrocyte histones H1, H5 and high-mobility-group proteins by purified calf-thymus poly(adenosinediphosphate-ribose) polymerase. Eur. J. Biochem. 127, 437-442.
75. Prasad, R., Lavrik, O. I., Kim, S. J., Kedar, P., Yang, X. P., Vande Berg, B. J. and Wilson, S. H. (2001). DNA polymerase β-mediated long patch base excision repair. J. Biol. Chem. 276, 32411-32414.
76. Rawling, J. M. and Alvarez-Gonzalez, R. (1997). TFIIF, a basal eukaryotic transcription factor, is a substrate for poly(ADP-ribosyl)ation. Biochem. J. 324, 249-253.
77. Realini, C. A. and Althaus, F. R. (1992). Histone shuttling by poly(ADP-ribosylation). J. Biol. Chem. 267, 18858-18865.
78. Redon, C., Pilch, D., Rogakou, E., Sedelnikova, O., Newrock, K. and Bonner, W. (2002). Histone H2A variants H2AX and H2AZ. Curr. Opin. Genet. Dev. 12, 162-169.
79. Riquelme, P. R., Burzio, L. O. and Koide, S. S. (1979). ADP ribosylation of rat liver lysine-rich histone in vitro. J. Biol. Chem. 254, 3018-3028.
80. Rouleau, M. and Poirier, G. G. (2004). Potential role of PARP inhibitors in cancer treatment and cell death. In DNA Repair in Cancer Therapy (ed. L. C. Panasci and M. A. Alaoui-Jamali). Totowa: Humana Press (in press).
81. Saxena, A., Saffery, R., Wong, L. H., Kalitsis, P. and Choo, K. H. A. (2002a). Centromere proteins Cenpa, Cenpb and Bub3 interact with poly(ADP-ribose) polymerase-1 protein and are poly(ADP-ribosyl)ated. J. Biol. Chem. 277, 26921-26926.
82. Saxena, A., Wong, L. H., Kalitsis, P., Earle, E., Shaffer, L. G. and Choo, K. H. A. (2002b). Poly(ADP-ribose) polymerase 2 localizes to mammalian active centromeres and interacts with PARP-1, Cenpa, Cenpb and Bub3, but not Cenpc. Hum. Mol. Genet. 11, 2319-2329.
83. Schreiber, V., Ame, 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.
84. Scovassi, A. I., Mariani, C., Negroni, M., Negri, C. and Bertazzoni, U. (1993). ADP-ribosylation of nonhistone proteins in HeLa cells: modification of DNA topoisomerase II. Exp. Cell Res. 206, 177-181.
85. 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.
86. Singh, N., Poirier, G. G. and Cerutti, P. A. (1985). Tumor promoter phorbol-12-myristate-13 acetate induces poly(ADP-ribosyl)ation in fibroblasts. EMBO J. 4, 1491-1494.
87. Slattery, E., Dignam, D. J., Matsui, T. and Roeder, R. G. (1983). Purification and analysis of a factor which suppresses nick-induced transcription by RNA polymerase II and its identity with poly(ADP-ribose) polymerase. J. Biol. Chem. 258, 5955-5959.
88. Smith, M. M. (2002). Centromeres and variant histones: what, where, when and why? Curr. Opin. Cell Biol. 14, 279-285.
89. Smith, S., Giriat, I., Schmitt, A. and de Lange, T. (1998). Tankyrase, a poly(ADP-ribose) polymerase at human telomeres. Science 282, 1484-1487.
90. Smith, S. and de Lange, T. (1999). Cell cycle dependent localization of the telomeric PARP, tankyrase, to nuclear pore complexes and centrosomes. J. Cell Sci. 112, 3649-3656.
91. Stone, P. R., Lorimer, W. S. and Kidwell, W. R. (1977). Properties of the complex between histone H1 and poly(ADP-ribose) synthesised in HeLa cell nuclei. Eur. J. Biochem. 81, 9-18.
92. Sullivan, K. F., Hechenberger, M. and Masri, K. (1994). Human CENP-A contains a histone H3 related histone fold domain that is required for targeting to the centromere. J. Cell Biol. 127, 581-592.
93. Szabo, C. and Dawson, V. (1998). Role of poly(ADP-ribose)synthetase in inflammation and ischemia-reperfusion. Trends Pharmacol. Sci. 19, 287-298.
94. Tanuma, S., Johnson, L. D. and Johnson, G. S. (1983). ADP-ribosylation of chromosomal proteins and mouse mammary tumor virus gene expression. Glucocorticoids rapidly decrease endogenous ADP-ribosylation of nonhistone high mobility group 14 and 17 proteins. J. Biol. Chem. 258, 15371-15375.
95. Tanuma, S., Yagi, T. and Johnson, G. S. (1985). Endogenous ADP ribosylation of high mobility group proteins 1 and 2 and histone H1 following DNA damage in intact cells. Arch. Biochem. Biophys. 237, 38-42.
96. Tartier, L., Spenlehauer, C., Newman, H. C., Folkard, M., Prise, D. M., Michael, B. D., Ménissier-de Murcia, J. and de Murcia, G. (2003). Local DNA damage by proton microbeam irradiation induces poly(ADP-ribose) synthesis in mammalian cells. Mutagenesis 18, 411-416.
97. Thoma, F., Losa, R. and Koller, T. (1983). Involvement of the domains of histones H1 and H5 in the structural organization of soluble chromatin. J. Mol. Biol. 167, 619-640.
98. Thomassin, H., Ménard, L., Hengartner, C. and Poirier, G. G. (1992). Poly(ADP-ribosyl)ation of chromatin in an in vitro poly(ADP-ribose) turnover system. Biochim. Biophys. Acta 1137, 171-181.
99. Tong, W. M., Cortes, U. and Wang, Z. Q. (2001). Poly(ADP-ribose) polymerase: a guardian angel protecting the genome and suppressing tumorigenesis. Biochim. Biophys. Acta 1552, 27-37.
100. Tulin, A. and Spradling, A. (2003). Chromatin loosening by poly(ADP-ribose) polymerase (PARP-1) at Drosophila puff loci. Science 299, 560-562.
101. Tulin, A., Stewart, D. and Spradling, A. C. (2002). The Drosophila heterochromatic gene encoding poly(ADP-ribose) polymerase (PARP-1) is required to modulate chromatin structure during development. Genes Dev. 16, 2108-2119.
102. Turner, B. (2002). Cellular memory and histone code. Cell 111, 285-291.
103. Ullrich, O., Diestel, A., Eyupoglu, I. Y. and Nitsch, R. (2001). Regulation of microglial expression of integrins by poly(ADP-ribose) polymerase-1. Nat. Cell Biol. 3, 1035-1042.
104. van Holde, K. (1988). Chromatin. Berlin: Springer-Verlag.
105. Virág, L. and Szabó, C. (2003). The therapeutic potential of poly(ADP-ribose) polymerase inhibitors. Pharmacol Rev. 54, 375-429.
106. Vispé, S., Yung, T. M. C., Ritchot, J., Serizawa, H. and Satoh, M. S. (2000). A cellular defense pathway regulating transcription through poly(ADP-ribosyl)ation in response to DNA damage. Proc. Natl. Acad. Sci. USA 97, 9886-9891.
107. Weinfeld, M., Chaudhry, M. A., D'Amours, D., Pelletier, J. D., Poirier, G. G., Povirk, L. F., and Lees-Miller, S. P. (1997). Interaction of DNA-dependent protein kinase and poly(ADP-ribose) polymerase with radiation-induced DNA strand breaks. Radiat. Res. 148, 22-28.
108. Wieler, S., Gagné, J. P., Vaziri, H., Poirier, G. G. and Benchimol, S. (2003). Poly(ADP-ribose) polymerase-1 is a positive regulator of the p53-mediated G1 arrest response following ionizing radiation. J. Biol. Chem. 278, 18914-18921.
109. Winstall, E., Affar, E. B., Shah, R., Bourassa, S., Scovassi, I. and Poirier, G. G. (1999). Preferential perinuclear localization of poly(ADP-ribose) glycohydrolase. Exp. Cell Res. 251, 372-378.
110. Wolffe, A. (1998). Chromatin: Structure and Function. London: Academic Press.
111. Wong, M., Kanai, Y., Miwa, M., Bustin, M. and Smulson, M. (1983). Immunological evidence for the in vivo occurrence of a crosslinked complex of poly(ADP-ribosylated) histone H1. Proc. Natl. Acad. Sci. USA 80, 205-209.
112. Wu, J. and Grunstein, M. (2000). 25 years after the nucleosome model: chromatin modifications. Trends Biochem. Sci. 25, 619-623.
113. Yu, S. W., Wang, H., Poitras, M. F., Coombs, C., Bowers, W. J., Federoff, H. J., Poirier, G. G., Dawson, T. M. and Dawson, V. L. (2002). Mediation of poly(ADP-ribose) polymerase-1 dependent cell death by apoptosis inducing factor. Science 297, 259-263.
114. Yung, T. M. C. and Satoh, M. S. (2001). Functional competition between poly(ADP-ribose) polymerase and its 24-kDa apoptotic fragment in DNA repair and transcription. J. Biol. Chem. 276, 11279-11286.
115. Zardo, G., D'Erme, M., Reale, A., Strom, R., Perilli, M. and Caiafa, P. (1997). Does poly(ADP-ribosyl)ation regulate the DNA methylation pattern? Biochemistry 36, 7937-7943.
116. Zardo, G. and Caiafa, P. (1998). The unmethylated status of CpG islands in mouse fibroblasts depends on the poly (ADP-ribosyl)ation process. J. Biol. Chem. 273, 16517-16520.
117. Zlatanova, J., Caiafa, P. and van Holde, K. (2000). Linker histone binding and displacement: versatile mechanism for transcriptional regulation. FASEB J. 14, 1697-1704.