Chromatin architecture and functions: The role(s) of poly(ADP-RIBOSE) polymerase and poly(ADPribosyl)ation of nuclear proteins

Biochemistry and Cell Biology

Volumn 83, Issue 3, 2005, Pages 396-404

  Faraone Mennella, Maria Rosaria ^a  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

Author keywords

Chromatin; Epigenetic; PARP; Poly(ADP ribose)

Indexed keywords

ACETYLATION; CATALYSIS; HISTOLOGY; PATHOLOGY; PATTERN RECOGNITION;

CHROMATIN; EPIGENETIC; PARP; POLY(ADP-RIBOSE);

PROTEINS;

BRCA1 PROTEIN; CYCLIN DEPENDENT KINASE INHIBITOR 1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; NUCLEAR PROTEIN; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; PROTEIN MSH6; PROTEIN P53; UNCLASSIFIED DRUG;

APOPTOSIS; CELL DIFFERENTIATION; CELL DIVISION; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN CONDENSATION; CHROMATIN STRUCTURE; CYTOARCHITECTURE; DNA DAMAGE; DNA RECOMBINATION; DNA REPAIR; DNA REPLICATION; DNA STRAND BREAKAGE; EPIGENETICS; GENE AMPLIFICATION; GENE EXPRESSION; HUMAN; MALIGNANT TRANSFORMATION; NONHUMAN; PROTEIN PROCESSING; REVIEW;

ADENOSINE DIPHOSPHATE RIBOSE; ANIMALS; CATALYSIS; CELL DIFFERENTIATION; CELL NUCLEUS; CELL TRANSFORMATION, NEOPLASTIC; CHROMATIN; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; EPIGENESIS, GENETIC; HUMANS; MODELS, BIOLOGICAL; NUCLEAR PROTEINS; OXYGEN; POLY(ADP-RIBOSE) POLYMERASES; RECOMBINATION, GENETIC;

EID: 24744439538     PISSN: 08298211     EISSN: None     Source Type: Journal    
DOI: 10.1139/o05-042     Document Type: Review

References (86)

1. Adamietz, P., and Rudolph, A. 1984. ADP-ribosylation of nuclear proteins in vivo. J. Biol. Chem. 259: 6841-6846.
2. Akiyama, T., Takasawa, S., Nata, K., Kobayashi, S., Abe, M., Shervani, N.J. et al. 2001. Activation of Reg gene for insulin-producting β-cell regeneration: poly(ADP-ribose) polymerase binds Reg promoter and regulates the transcription by autopoly(ADP-ribosyl)ation. Proc. Natl. Acad. Sci. U.S.A. 98: 48-53.
3. Alvarez-Gonzalez, R., and Ringer, D.P. 1988. Nuclear matrix associated poly(ADP-ribose) metabolism in regenerating rat liver. FEBS Lett. 236: 362-366.
4. Amé, J.C., Spenlehauer, C., and de Murcia, G. 2004. The PARP superfamily. BioEssays, 26: 882-893.
5. Anderson, M.G., Scoggin, K.E., Simbulan-Rosenthal, C.M., and Steadman, J.A. 2000. Identification of poly(ADP-ribose) polymerase as a transcriptional coactivator of the human T-cell leukemia virus type 1 Tax protein. J. Virol. 74: 2169-2177.
6. Arnold, J., and Grune, T. 2002. PARP-mediated proteasome activation: a co-ordination of DNA repair and protein degradation? BioEssays, 24: 1060-1065.
7. Bonicalzi, M.E., Vodenicharov, M., Coulombe, M., Gagné, J.P., and Poirier, G.G. 2003. Alteration of PARG nucleocytoplasmic shuttling characteristics upon cleavage by apoptotic proteases. Biol. Cell, 95: 635-644.
8. Boulikas, T. 1995. Chromatin domains and prediction of matrix associated regions. Int. Rev. Cytol. 162A: 279-388.
9. Burkle, A. 2001. Physiology and pathophisiology of poly(ADP-ribosyl) ation. BioEssays, 23: 795-806.
10. Butler, A.J., and Ordahl, C.P. 1999. Poly(ADP-ribose) polymerase binds with transcription enhancer factor 1 to MCAT1 elements to regulate muscle-specific transcription. Mol. Cell. Biol. 19: 296-306.
11. Carmo-Fonseca, M. 2004. The contribution of nuclear compartmentalization to gene regulation. Cell, 108: 513-521.
12. Carrillo, A., Monreal, Y., Ramirez, P., Marin, L., Parrilla, P., Oliver, F.J., and Yelamos, J. 2004. Transcription regulation of TNF-{alpha}-early response genes by poly(ADP-ribose) polymerase-1 in murine heart endothelial cells. Nucleic Acids Res. 32: 757-766.
13. Chiarugi, A. 2002. PARP: killer or conspirator? The suicide hypothesis revisited. Trends Pharmacol. Sci. 23: 122-129.
14. Cohen-Armon, M., Visochek, L., Katzoff, A., Levitan, D., Susswein, A.J., Klein, R. et al. 2004. Long-term memory requires Poly-ADP-ribosylation. Science, 304: 1820-1822.
15. Cremer, T., and Cremer, C. 2001. Chromosome territories, nuclear architecture and gene regulation in mammalian cells. Nat. Rev. Gen. 2: 292-301.
16. d'Adda di Fagagna, F., Hande, M.P., Tong, W.M., Lansdorp, P.M., Wan, G.Z.Q., and Jackson, S.P. 1999. Functions of poly(ADP-ribose) polymerase in controlling telomere length and chromosomal stability. Nat. Genet. 23: 76-80
17. 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.
18. Dantzer, F., Giraud-Panis, MJ., Jaco, I., Ame, J.C., Schultz, I., Blasco, M. et al. V. 2004. Functional interaction between PARP 2 and TRF2: PARP activity negatively regulates TRF2. Mol. Cell. Biol. 24: 1595-1607.
19. de Lange, T. 1992. Human telomeres are attached to nuclear matrix. EMBO J. 11: 717-724.
20. De Lucia, F., Faraone-Mennella, M.R., Derme, M., Quesada, P., Caiafa, P., and Farina, B. 1994. Histone-induced condensation of rat testis chromatin: testis-specific Hit versus somatic H1 variants. Biochem. Biophys. Res. Commun. 198: 32-39.
21. De Murcia, G., and Shall, S. 2000. From DNA damage and stress signalling to cell death: poly(ADP-ribosyl)ation reactions. Oxford University Press, New York.
22. Ehrenhofer-Murray, A.E. 2004. Chromatin dynamics at DNA replication, transcription and repair. Eur. J. Biochem. 271: 2335-2349.
23. 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.
24. Faraone-Mennella, M.R., Quesada, P., Leone, E., Farina, B., and Jones, R. 1984. Purification of non-histone acceptor proteins for ADP-ribose from mouse testis nuclei. Biochem. J. 221: 223-231.
25. Faraone-Mennella, M.R., De Lucia, F., Palomba, L., Quesada, P., and Farina, B. 1993. Effect of ADP-ribosylation reaction on bull testis chromatin. Biochem. Mol. Biol. Int. 31: 373-380.
26. Faraone-Mennella, M.R., De Lucia, R, Gentile, N., Quesada, P., and Farina, B. 1999. In vitro poly(ADP-ribosyl)ated histones H1a and H1t modulate rat testis chromatin condensation differently J. Cell. Biochem. 76: 20-29.
27. Faraone-Mennella, M.R., Roma, G., and Farina, B. 2003. Active poly(ADP-ribose) metabolism in DNAase- and salt-resistant rat testis chromatin with high transcriptional activity/competence. J. Cell. Biochem. 89: 688-697.
28. Felsfendel, G., and Groudine, M. 2003. Controlling the double helix. Nature (London), 421: 448-453.
29. Frouin, I., Maga, G., Denegri, M., Riva, F., Savio, M., Spadari, S. et al. 2003. Human PCNA, PARP-1, and p21waff1/cip1. A dynamic exchange of partners. J. Biol. Chem. 278: 39265-39268.
30. Galande, S. 2002. Chromatin (dis)organization and cancer: BUR-binding proteins as biomarkers of cancer. Curr. Cancer Drug Targets, 2: 157-190.
31. 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.
32. Golderer, G., and Grobner, P. 1991. ADP-ribosylation of core histones and their acetylated subspecies. Biochem. J. 277: 607-610.
33. Hendzel, M.J., Lever M.A., Crawford E., and Th'ng, J.P. 2004. The C-terminal domain is the primary determinant of histone H1 binding to chromatin in vivo. J. Biol. Chem. 279: 20028-20034.
34. Henikoff, S., Furuyama, T., and Ahmad, K. 2004. Histone variants, nucleosome assembly and epigenetic inheritance. Trends Genet. 20(7): 320-326.
35. Huber, A., Bai, P., de Murcia, J.M., and de Murcia, G. 2004. PARP-1, PARP-2 and ATM in the DNA damage response: functional synergy in mouse development. DNA Repair (Amst.), 3: 1103-1108.
36. Huletsky, A., de Murcia, G., Muller, S., Hengartner, M., Menard, L., Lamarre, D., and Poirer, 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.
37. Kaminker, P.G., Kim, S.H., Taylor, R.D., Zebarjadian, Y., Funk, W.D., Morin, G.B. et al. 2001. TANK2, a new TRF1-associated PARP, causes rapid induction of cell death upon overexpression. J. Biol. Chem. 276: 35891-35899.
38. Karagiannis, T.C., and El-Osta, A. 2004. Epigenetic changes activate widespread signals in response to double strand breaks. Cancer Biol. Ther. 3: 617-623.
39. Khadake, J.R., and Rao, R.S. 1995. DNA- and chromatin-condensing properties of rat testes H1a and H1t compared to those of rat liver H1bdec; H1t is a poor condenser of chromatin. Biochemistry, 34: 15792-15801.
40. Kirsten, E., Kun, E., Mendeleyev, J., and Ordhal, C.P. 2004. Activity assays for poly(ADP-ribose) polymerase. Methods Mol. Biol. 287: 137-149.
41. Kraus, W.L., and Lis, J.T. 2003. PARP goes transcription. Cell, 113: 677-683.
42. Krupitza, G., and Cerutti, P. 1989. Poly(ADP-ribosyl)ation of histones in intact human keratinocytes. Biochemistry, 28: 4054-4060.
43. Kuimov, A.N., Kuprash, D.V., Petrov, V.N., Vdovichenko, K.K., Scanlan, M.J., Jongeneel, C.V. et al. 2001. Cloning and characterization of TNKL, a member of tankyrase gene family. Genes Immun. 2: 52-55.
44. Kun, E., Kirsten, E., Kun, E., and Ordhal, C.P. 2002. Coenzymatic activity of randomly broken or intact ds-DNAs in auto- and histone H1 trans-poly(ADP-ribosyl)ation, catalyzed by PARP. J. Biol. Chem. 277: 39066-39069.
45. 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.
46. Malanga, M., and Althaus, F.R. 2004. Poly(ADP-ribose) reactivates stalled DNA topoisomerase I and Induces DNA strand break resealing. J. Biol. Chem. 279: 5244-5248.
47. Malanga, M., Atorino, L., Tramontane, F., Farina, B., and Quesada, P. 1998. Poly(ADP-ribose) properties of histone H1 variants. Biochim. Biophys. Acta, 1399: 154-160.
48. Malik, N., and Smulson, M. 1984. A relationship between nuclear poly(adenosine diphosphate ribosylation) and acetylation post-translational modifications. 1. Nucleosome studies. Biochemistry, 23: 3721-3725.
49. Menissier de Murcia, J., Ricoul, M., Tartier, L., Niedergang, C., Huber, A. et al. 2003. Functional interaction between PARP-1 and PARP-2 in chromosome stability and embryonic development in mouse. EMBO J. 22: 2255-2263.
50. Misteli, T. 2000. Cell biology of transcription and pre-mRNA splicing: nuclear architecture meets nuclear function. J. Cell Sci. 113: 1841-1849.
51. Monz, D., Munnia, A., Comtesse, N., Fischer, U., Steudel, W.I., Feiden, W. et al. 2001. Novel tankyrase-related gene detected with meningioma-specific sera. Clin. Cancer Res. 7: 113-119.
52. Morin, V., Diaz, F., Montecino, M., Fothergill-Gilmore, L., Puchi, M., and Imschenetsky, M. 1999. Poly(ADP-ribosyl)ation protects maternally derived histones from proteolysis after fertilization. Biochem. J. 343: 95-98.
53. Nakajima, H. Nagaso, H., Kakui, N., Ishikawa, M., Hiranuma, T., and Hoshiko, S. 2004. Critical Role of the automodification of poly(ADP-ribose) polymerase-1 in nuclear factor-{kappa}B-dependent gene expression in primary cultured mouse glial cells. J. Biol. Chem. 279: 42774-42786.
54. Oei, S.L., Griesenbeck, J., Schweiger, M., and Ziegler, M. 1998. Regulation of RNA polymerase II-dependent transcription by poly(ADP-ribosyl) ation of transcription factors. J. Biol. Chem. 273: 31644-31647.
55. 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.
56. Osley, M.A. 2004. H2B ubiquitylation: the end is in sight. Biochim. Biophys. Acta, 1677: 74-78.
57. Pandita, T.K., and Dhar, S. 2000. Influence of ATM function on interactions between telomeres and nuclear matrix. Radiat. Res. 154: 133-139.
58. Plaza, S., Aumercier, M., Bailly, M., Dozier, C., and Saule, S. 1999. Involvement of poly (ADP-ribose)-polymerase in the Pax-6 gene regulation in neuroretina. Oncogene, 18: 1041-1051.
59. 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.
60. Poirier, G.G., de Murcia, G., Jongstra-Bilen, J., Niedergang, C., and Mandel, P. 1982. Poly(ADP-ribosyl)ation of polynucleosomes causes relaxation of chromatin structure. Proc. Natl. Acad. Sci. U.S.A. 79: 3423-3427.
61. Quesada, P., Tramontano, F., Raraone-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.
62. Rawling, J.M., and Alvarez-Gonzalez, R. 1997. TFIIR a basal eukaryotic transcription factor, is a substrate for poly(ADP-ribosyl)ation. Biochem. J. 324: 249-253.
63. Reale, A., Malanga, M., Zardo, G., Strom, R., Scovassi A.I., Farina, B., and Caiafa, P. 2000. In vitro induction of H1-H1 histone cross-linking by ADP-ribose polymers. Biochemistry, 39: 10413-10418.
64. Reale, A., De Matteis, G., Galleazzi, G., Zamperi, M., and Caiafa, P. 2005. Modulation of DMT1 activity by ADP-ribose polymers. Oncogene, 24: 13-18.
65. Realini, C.A., and Althaus, F.R. 1992. Histone shuttling by poly (ADP-ribosyl)ation. J. Biol. Chem. 267: 18858-18865.
66. Rouleau, M., Aubin, R.A., and Poirier, G.G. 2004. Poly(ADP-ribosyl)ated domains: access granted. J. Cell Sci. 117: 815-825.
67. Sakkers, R.J., Brunsting, J.F., Filon, A.R., Kampinga, H.H., Konings, A.W., and Mullenders, L.H. 1999. Altered association of transcriptionally active DNA with the nuclear-matrix after heat shock. Int. J. Radiat. Biol. 75: 875-883.
68. Santos, F., and Dean, W. 2004. Epigenetic reprogramming during early development in mammals. Reproduction, 127: 643-651.
69. Sawatsubashi, S., Maki, A., Ito, S., Suzuki, E., Zhao, Y., Yamagata, K. et al. 2004. Ecdysone receptor-dependent gene regulation mediates histone poly(ADP-ribosyl)ation. Biochim. Biophys. Res. Commun. 320: 268-272.
70. Saxena, A., Saffery, R., Wong, L.H., Kalitsis, P., and Choo, K.H. 2002. 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.
71. Simbulan-Rosenthal, C.M., Rosenthal, D.S., Luo, R., Li, J.H., Zhang, J., and Smulson, M.E. 2001. Inhibition of poly(ADP-ribose) polymerase activity is insufficient to induce tetraploidy. Nucleic Acids Res. 29: 841-849.
72. Smith, S. 2001. The world according to PARP. Trends Biochem. Sci. 26: 174-179.
73. Smith, S., and de Lange, T. 2000. Tankyrase promotes telomere elongation in human cells. Curr. Biol. 10: 1299-1302.
74. 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.
75. Stein, G.S., Zaidi, S.K., Corey, D.B., Montecino, M., van Wijen, A.J., Choi, J.Y., et al. 2003. Functional architecture of the nucleus: organizing the regulatory machinery for gene expression, replication, repair. Trends Cell Biol. 13: 584-592.
76. Strahl, B.D., and Allis, C.D. 2000. The language of covalent histone modifications. Nature, 403: 41-45.
77. Tramontano, F., Di Meglio, S., and Quesada, P. 2005. Co-localization of poly(ADPR)polymerase 1 (PARP-1) poly(ADPR)polymerase 2 (PARP-2) and related proteins in rat testis nuclear matrix defined by chemical cross-linking. J. Cell. Biochem. 94(1): 58-66.
78. Tulin, A., and Spradling, A. 2003. Chromatin loosening by PARP at Drosophila puff loci. Science (Wash.), 299: 560-562.
79. Virag, L., and Szabo, C. 2002. The therapeutic potential of PARP inhibitors. Pharmacol. Rev. 54: 375-429.
80. Wang, Y., Fischle, W., Cheung, W., Jacobs, S., Khorasanizadeh, S., and Allis, C.D. 2004. Beyond the double helix: writing and reading the histone code. Novartis Found. Symp. 259: 3-17.
81. Wellman, S.E. 1996. C-terminal peptides from H1 histone variants: DNA binding characteristics and solution conformation. Biopolymers, 39: 491-501.
82. Wesierska-Gadek, J., Wojciechowski, J., and Schmid, G. 2003. Phosphorylation regulates the interaction and complex formation between wt p53 protein and PARP-1. J. Cell. Biochem. 89: 1260-1284.
83. Wong, M., Kanai, Y., Miwa, M., Bustin, M., and Smulson, M. 1983. Immunological evidence for the in vivo occurrence of a croo-linked complex of poly(ADPribosyl)ated H1 histone. Proc. Natl. Acad. Sci. U.S.A. 80: 205-209.
84. Yamashita, K., Shinohara, M., and Shinohara, A. 2004. Rad6-Bre1-mediated histone H2B ubiquitylation modulates the formation of DSB during meiosis. Proc. Natl. Acad. Sci. U.S.A. 101: 11380-11385.
85. Yao, N., Hurwitz, J., and O'Donnell, M. 2000. Dynamics of beta and proliferating cell nuclear antigen sliding clamps in traversing DNA secondary structure. J. Biol. Chem. 275: 1421-1432.
86. Yung, T.M.C., Sato, S., and Satoh, M.S. 2004. Poly(ADP-ribosyl) ation as a DNA damage-induced post-translational modification regulating poly(ADP-ribose) polymerase-1-topoisomerase I interaction. J. Biol. Chem. 279: 39686-39696.