PARP-3 associates with polycomb group bodies and with components of the DNA damage repair machinery

Journal of Cellular Biochemistry

Volumn 100, Issue 2, 2007, Pages 385-401

  Rouleau, M ^a   McDonald, D ^b   Gagne P ^a   Ouellet, M E ^a   Droit, A ^a   Hunter, J M ^a   Dutertre, S ^c   Prigent, C ^c   Hendzel, M J ^b   Poirier, G G ^a  

^a UNIVERSITÉ LAVAL   (Canada)

^b UNIVERSITY OF ALBERTA   (Canada)

^c UNIVERSITÉ DE RENNES 1   (France)

Author keywords

DNA repair; Immunoprecipitation; Ku70 Ku80; PARP; Poly(ADP ribose); Polycomb group; Proteomics; Splice variants

Indexed keywords

ANTIGEN; DNA; DNA DEPENDENT PROTEIN KINASE; DNA LIGASE III; DNA LIGASE IV; ENZYME ANTIBODY; FLAG PEPTIDE; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; ISOENZYME; KU ANTIGEN; KU80 ANTIGEN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; NUCLEAR PROTEIN; OCTAPEPTIDE; POLY(ADENOSINE DIPHOSPHATE RIBOSE); POLYADENOSINE DIPHOSPHATE RIBOSE POLYMERASE 2; POLYADENOSINE DIPHOSPHATE RIBOSE POLYMERASE 3; POLYADENOSINE DIPHOSPHATE RIBOSE POLYMERASE 3 ANTIBODY; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; ENZYME ACTIVITY; ENZYME LOCALIZATION; ENZYME MECHANISM; GENE SILENCING; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYCOMB GROUP BODY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEOMICS; SEQUENCE ANALYSIS; STRUCTURE ACTIVITY RELATION; TRANSCRIPTION REGULATION;

AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, NUCLEAR; BASE SEQUENCE; CELL CYCLE PROTEINS; CELL LINE; CERCOPITHECUS AETHIOPS; DNA; DNA DAMAGE; DNA REPAIR; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; ISOENZYMES; MASS SPECTROMETRY; MOLECULAR SEQUENCE DATA; POLY(ADP-RIBOSE) POLYMERASES; PROTEIN BINDING; REPRESSOR PROTEINS;

EID: 33846453969     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.21051     Document Type: Article

References (55)

1. Alvarez-Gonzalez R, Althaus FR. 1989. Poly(ADP-ribose) catabolism in mammalian cells exposed to DNA-damaging agents. Mutat Res 218:67-74.
2. Amé JC, Rolli V, Schreiber V, Niedergang C, Apiou P, Decker P, Muller S, Hoger T, Ménissier-de Murcia J, de Murcia G. 1999. PARP-2: A novel mammalian DNA damage dependent poly(ADP-ribose) polymerase. J Biol Chem 274:17860-17868.
3. Amé JC, Spenlehauer C, de Murcia G. 2004. The PARP superfamily. Bioessays 26:882-893.
4. Atchison L, Ghias A, Wilkinson F, Bonini N, Atchison ML. 2003. Transcription factor YY1 functions as a PcG protein in vivo. EMBO J 6:1347-1358.
5. Audebert M, Salles B, Calsou P. 2004. Involvement of PARP-1 and XRCC1/DNA ligase III in an alternative route for DNA double-strand breaks rejoining. J Biol Chem 279:55117-55126.
6. Augustin A, Spenlehauer C, Dumond H, Ménissier-de Murcia J, Piel M, Schmit AC, Apiou F, Vonesh JL, Kock M, Bornens M, de Murcia G. 2003. PARP-3 localizes preferentially to the daughter centriole and interferes with the G1/S cell cycle progression. J Cell Sci 116:1551-1562.
7. Boulikas T. 1990. Poly(ADP-ribosylated) histones in chromatin replication. J Biol Chem 265:14638-14647.
8. Chang YL, Peng YH, Pan IC, Sun DS, King B, Huang DH. 2001. Essential role of Drosophila Hdac1 in homeotic gene silencing. Proc Natl Acad Sci 98:9730-9735.
9. Chang P, Jacobson MK, Mitchison TJ. 2004. Poly(ADP-ribose) is required for spindle assembly and structure. Nature 432:645-649.
10. Chi NW, Lodish HF. 2000. Tankyrase is a Golgi-associated mitogen-activated protein kinase substrate that interacts with IRAP in GLUT4 vesicles. J Biol Chem 275:38437-38444.
11. Cook BD, Dynek JN, Chang W, Shostak G, Smith S. 2002. Role for the related poly(ADP-ribose) polymerases tankyrases 1 and 2 at human telomeres. Mol Cell Biol 22:332-342.
12. D'Amours D, Desnoyers S, D'Silva I, Poirier GG. 1999. Poly(ADP-ribosyl)ation reactions in the regulation of nuclear functions. Biochemical J 342:249-268.
13. Dantzer F, Giraud-Panis MJ, Jaco I, Amé JC, Schultz I, Blasco M, Koering CE, Gilson E, Ménissier-de Murcia J, de Murcia G, Schreiber V. 2004. Functional interaction between poly(ADP-ribose) polymerase 2 (PARP-2) and TRF2: PARP activity negatively regulates TRF2. Mol Cell Biol 24:1595-1607.
14. Dynek JN, Smith S. 2004. Resolution of sister telomere association is required for progression through mitosis. Science 304:97-100.
15. Eng J, McCormack A, Yates JR III. 1994. An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database. J Am Soc Mass Spectrom 5:976-989.
16. Galande S, 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.
17. Hassa PO, Buerki C, Lombardi C, Imhof R, Hottiger MO. 2003. Transcriptional coactivation of nuclear factor-kappaB-dependent gene expression by p300 is regulated by poly(ADP)-ribose polymerase-1. J Biol Chem 278:45145-45153.
18. Huber A, Bai P, Ménissier-de Murcia J, de Murcia G. 2004. PARP-1, PARP-2 and ATM in the DNA damage response: Functional synergy in mouse development. DNA Repair 3:1103-1108.
19. Johansson M. 1999. A human poly(ADP-ribose) polymerase gene family (ADPRTL): cDNA cloning of two novel poly(ADP-ribose) polymerase homologues. Genomics 57:442-445.
20. Ju BG, Solum D, Song EJ, Lee KJ, Rose DW, Glass CK, Rosenfeld MG. 2004. Activating the PARP-1 sensor component of the groucho/TLE1 corepressor complex mediates a CaMKinase IIdelta-dependent neurogenic gene activation pathway. Cell 119:815-829.
21. Keller A, Nesvizhskii AI, Kolker E, Aebersold R. 2002. Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal Chem 74:5383-5392.
22. Kersey PJ, Duarte J, Williams A, Karavidopoulou Y, Birney E, Apweiler R. 2004. The International Protein Index: An integrated database for proteomics experiments. Proteomics 4:1985-1988.
23. Kickhoefer VA, Siva AC, Kedersha NL, Inman EM, Ruland C, Streuli M, Rome LH. 1999. The 193-kD vault protein, VPARP, is a novel poly(ADP-ribose) polymerase. J Cell Biol 146:917-928.
24. +-dependent modulation of chromatin structure and transcription by nucleosome binding properties of PARP-1. Cell 119:803-814.
25. Kozak M. 1989. The scanning model for translation: An update. J Cell Biol 108:229-241.
26. Kozak M. 1995. Adherence to the first-AUG rule when a second AUG codon follows closely upon the first. Proc Natl Acad Sci USA 92:2662-2666.
27. Leppard JB, Dong Z, Mackey ZB, Tomkinson AE. 2003. Physical and functional interaction between DNA ligase IIIalpha and poly(ADP-ribose) polymerase 1 in DNA single-strand break repair. Mol Cell Biol 23:5919-5927.
28. Levine SS, King IFG, Kingston RE. 2004. Division of labor in Polycomb group repression. Trends Biochem Sci 29:478-485.
29. Li B, Navarro S, Kasahara N, Comai L. 2004. Identification and biochemical characterization of a Werners's syndrome protein complex with Ku70/80 and poly(ADP-ribose) polymerase-1. J Biol Chem 279:13659-13667.
30. Maeda Y, Hunter TC, Loudy DE, Dave V, Schreiber V, Whitsett JA. 2006. PARP-2 interacts with TTF-1 and regulates expression of surfactant protein-B. J Biol Chem 281:9600-9606.
31. Matsui T, Segall J, Weil PA, Roeder RG. 1980. Multiple factors required for accurate initiation of transcription by purified RNA polymerase II. J Biol Chem 255:11992-11996.
32. Meder VS, Boeglin M, de Murcia G, Schreiber V. 2005. PARP-1 and PARP-2 interact with nucleophosmin/B23 and accumulate in transcriptionally active nucleoli. J Cell Biol 118:211-222.
33. Ménissier-de Murcia J, Ricoul M, Tartier L, Niedergang C, Huber A, Dantzer F, Schreiber V, Amé JC, Dierich A, LeMeur M, Sabatier L, Chambon P, de Murcia G. 2003. Functional interaction between PARP-1 and PARP-2 in chromosome stability and embryonic development in mouse. EMBO J 22:2255-2263.
34. Nesvizhskii AI, Keller A, Kolker E, Aebersold R. 2003. A statistical model for identifying proteins by tandem mass spectrometry. Anal Chem 75:4646-4658.
35. Oei SL, SM Y. 2001. Transcription factor Yin Yang 1 stimulates poly(ADP-ribosyl)ation and DNA repair. Biochem Biophys Res Comm 284:450-454.
36. Oei SL, Griesenbeck J, Schweiger M, Ziegler M. 1998. Regulation of RNA polymerase II-dependent transcription by poly(ADP-ribosyl)ation of transcription factors. J Biol Chem 273:31644-31647.
37. Ogata N, Ueda K, Kawaichi M, Hayaishi O. 1981. Poly(ADP-ribose) synthase, a main acceptor of poly (ADP-ribose) in isolated nuclei. J Biol Chem 256:4135-4137.
38. Olfert ED, Cross BM, McWilliam AA, editors. 1993. Guide to the care and use of experimental animals. Ottawa: Canadian Council on Animal Care, 195 p.
39. Otto H, Reche P, Bazan F, Dittmar K, Haag F, Koch-Nolte F. 2005. In silico characterization of the family of PARP-like poly(ADP-ribosyl)transferases (pARTs). BMC Genomics 6:139.
40. Ou YY, Mack GJ, Zhang M, Rattner JB. 2002. CEP110 and ninein are located in a specific domain of the centrosome associated with centrosome maturation. J Cell Sci 115:1825-1835.
41. Rouleau M, Aubin RA, Poirier GG. 2004. Poly(ADP-ribosyl)ated chromatin domains: Access granted. J Cell Sci 117:815-825.
42. Ruscetti T, Lehnert BE, Halbrook J, Trong HL, Hoekstra MF, Chen DJ, Peterson SR. 1998. Stimulation of the DNA-dependent protein kinase by poly(ADP-ribose) polymerase. J Biol Chem 273:14461-14467.
43. Saurin AJ, Shiels C, Williamson J, Satijn DPE, Otte AP, Sheer D, Freemont PS. 1998. The human Polycomb group complex associates with pericentromeric heterochromatin to form a novel nuclear domain. J Cell Biol 142:887-898.
44. Sbodio JI, Lodish HF, Chi NW. 2002. Tankyrase-2 oligomerizes with tankyrase-1 and binds to both TRF1 (telomere-repeat-binding factor 1) and IRAP (insulin-responsive aminopeptidase). Biochem J 361:451-459.
45. Schreiber V, Amé JC, Dollé P, Schultz I, Rinaldi B, Fraulob V, Ménissier-de Murcia J, 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.
46. Shall S, de Murcia G. 2000. Poly(ADP-ribose) polymerase-1: What have we learned from the deficient mouse model? Mutation Res 460:1-15.
47. Smith S, 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.
48. Sucharov CC, Helmke SM, Langer SJ, Perryman MB, Bristow M, Leinwand L. 2004. The Ku protein complex interacts with YY1, is up-regulated in human heart failure and represses α myosin heavy-chain gene expression. Mol Cell Biol 24:8705-8715.
49. Tulin A, Spradling A. 2003. Chromatin loosening by poly(ADP-ribose) polymerase (PARP-1) at Drosophila puff loci. Science 299:560-562.
50. Urbanek P, Paces J, Kralova J, Dvorak M, Paces V. 2002. Cloning and expression of PARP-3 (Adprt3) and U3-55k, two genes closely linked on mouse chromosome 9. Folia Biol (Praha) 48:182-191.
51. Veuger SJ, Curtin NJ, Smith GCM, Durkacz BW. 2004. Effects of novel inhibitors of poly(ADP-ribose) polymerase-1 and the DNA-dependent protein kinase on enzyme activities and DNA repair. Oncogene 23:7322-7329.
52. Von Haller PD, Yi E, Donohoe S, Vaughn K, Keller A, Nesvizhskii AI, Eng J, Li XJ, Goodlett DR, Aebersold R, Watts JD. 2003. The application of new software tools to quantitative protein profiling via isotope-coded affinity tag (ICAT) and tandem mass spectrometry: II. evaluation of tandem mass spectrometry methodologies for large-scale protein analysis, and the application of statistical tools for data analysis and interpretation. Mol Cell Proteomics 2:428-442.
53. Woodard RL, Lee KJ, Huang J, Dynan WS. 2001. Distinct roles for Ku protein in transcriptional reinitiation and DNA repair. J Biol Chem 276:15423-15433.
54. Yu M, Schreek S, Cerni C, Schamberger C, Lesniewicz K, Poreba E, Vervoorts J, Walsemann G, Grotzinger J, Kremmer E, Mehraein Y, Mertsching J, Kraft R, Austen M, Luscher-Firzlaff J, Luscher B. 2005. PARP-10, a novel Myc-interacting protein with poly(ADP-ribose) polymerase activity, inhibits transformation. Oncogene 24:1982-1993.
55. Ziegler M, Oei SL. 2001. A cellular survival switch: Poly(ADP-ribosyl) ation stimulates DNA repair and silences transcription. BioEssays 23:543-548.