Poly(ADP-ribose) polymerase 1 regulates both the exonuclease and helicase activities of the Werner syndrome protein

Nucleic Acids Research

Volumn 32, Issue 13, 2004, Pages 4003-4014

  von Kobbe, Cayetano ^b,c   Harrigan, Jeanine A ^b   Schreiber, Valérie ^a   Stiegler, Patrick ^a   Piotrowski, Jason ^b   Dawut, Lale ^b   Bohr, Vilhelm A ^b  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b NATIONAL INSTITUTE ON AGING   (United States)

^c Centro Nacional de Investigaciones Oncológicas   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; BRCA1 PROTEIN; DNA; EXONUCLEASE; HELICASE; ISOENZYME; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 2; NUCLEAR PROTEIN; UNCLASSIFIED DRUG; WERNER SYNDROME PROTEIN; POLY(ADP RIBOSE) POLYMERASE 2, MOUSE; POLY(ADP-RIBOSE) POLYMERASE-2, MOUSE; RECQ HELICASE; WRN PROTEIN, HUMAN;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; AMINO TERMINAL SEQUENCE; ARTICLE; BIOCHEMISTRY; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CONTROLLED STUDY; DNA BINDING; DNA METABOLISM; DNA RECOMBINATION; DNA REPAIR; DNA REPLICATION; DNA STRAND BREAKAGE; DNA TRANSCRIPTION; ENZYME ACTIVITY; ENZYME INACTIVATION; ENZYME INHIBITION; ENZYME REGULATION; ENZYME SPECIFICITY; GENE MUTATION; GENETIC DISORDER; GENETIC STABILITY; MODULATION; PREMATURE AGING; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INTERACTION; WERNER SYNDROME; BINDING SITE; BIOLOGICAL MODEL; CHEMISTRY; HELA CELL; HUMAN; METABOLISM; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE;

BINDING SITES; DNA; DNA HELICASES; EXONUCLEASES; HELA CELLS; HUMANS; MODELS, BIOLOGICAL; POLY(ADP-RIBOSE) POLYMERASES; PROTEIN STRUCTURE, TERTIARY; RECQ HELICASES;

EID: 3843101621     PISSN: 03051048     EISSN: None     Source Type: Journal    
DOI: 10.1093/nar/gkh721     Document Type: Article

References (47)

1. Hickson,I.D. (2003) RecQ helicases: caretakers of the genome. Nat. Rev. Cancer, 3, 169-178.
2. Harrigan,J.A. and Bohr,V.A. (2003) Human diseases deficient in RecQ helicases. Biochimie, 85, 1185-1193.
3. Opresko,P.L., Cheng,W.H., von Kobbe,C., Harrigan,J.A. and Bohr,V.A. (2003) Werner syndrome and the function of the Werner protein; what they can teach us about the molecular aging process. Carcinogenesis, 24, 791-802.
4. Shen,J.C., Gray,M.D., Oshima,J., Kamath-Loeb,A.S., Fry,M. and Loeb,L.A. (1998) Werner syndrome protein. I. dna helicase and dna exonuclease reside on the same polypeptide. J. Biol. Chem,, 273, 34139-34144.
5. von Kobbe,C. and Bohr,V.A. (2002) A nucleolar targeting sequence in the Werner syndrome protein resides within residues 949-1092. J. Cell Sci., 115, 3901-3907.
6. von Kobbe,C., Thoma,N.H., Czyzewski,B.K., Pavletich,N.P. and Bohr,V.A. (2003) Werner syndrome protein contains three structure-specific DNA binding domains. J. Biol. Chem., 278, 52997-53006.
7. Brosh,R.M.,Jr, von Kobbe,C., Sommers,J.A., Karmakar,P., Opresko,P.L., Piotrowski,J., Dianova,I., Dianov,G.L. and Bohr,V.A. (2001) Werner syndrome protein interacts with human flap endonuclease 1 and stimulates its cleavage activity. EMBO J., 20, 5791-5801.
8. von Kobbe,C., Karmakar,P., Dawut,L., Opresko,P., Zeng,X., Brosh,R.M.,Jr, Hickson,I.D. and Bohr,V.A. (2002) Colocalization, physical, and functional interaction between Werner and Bloom syndrome proteins. J. Biol. Chem., 277, 22035-22044.
9. Opresko,P.L., von Kobbe,C., Laine,J.P., Harrigan,J., Hickson,I.D. and Bohr,V.A. (2002) Telomere-binding protein TRF2 binds to and stimulates the Werner and Bloom syndrome helicases. J. Biol. Chem., 277, 41110-41119.
10. Harrigan,J.A., Opresko,P.L., von Kobbe,C., Kedar,P.S., Prasad,R., Wilson,S.H. and Bohr,V.A. (2003) The Werner syndrome protein stimulates DNA polymerase beta strand displacement synthesis via its helicase activity. J. Biol. Chem., 278, 22686-22695.
11. von Kobbe,C., Harrigan,J.A., May,A., Opresko,P.L., Dawut,L., Cheng,W.H. and Bohr,V.A. (2003) Central role for the Werner syndrome protein/poly(ADP-ribose) polymerase 1 complex in the poly(ADP-ribosyl)ation pathway after DNA damage. Mol. Cell. Biol., 23, 8601-8613.
12. 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.
13. Smith,S. (2001) The world according to PARP. Trends Biochem. Sci., 26, 174-179.
14. Dantzer,F., De La,R.G., Menissier-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.
15. Masson,M., Niedergang,C., Schreiber,V., Muller,S., Menissier-de Murcia,J. 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.
16. 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.
17. 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., 23, 5919-5927.
18. Shieh,W.M., Ame,J.C., Wilson,M.V., Wang,Z.Q., Koh,D.W., Jacobson,M.K. and Jacobson,E.L. (1998) Poly(ADP-ribose) polymerase null mouse cells synthesize ADP-ribose polymers. J. Biol. Chem., 273, 30069-30072.
19. Ame,J.C., Rolli,V., Schreiber,V., Niedergang,C., Apiou,F., Decker,P., Muller,S., Hoger,T., Menissier-de Murcia,J. and de Murcia,G. (1999) PARP-2, A novel mammalian DNA damage-dependent poly(ADP-ribose) polymerase. J. Biol. Chem., 274, 17860-17868.
20. Tong,W.M., Hande,M.P., Lansdorp,P.M. and Wang,Z.Q. (2001) DNA strand break-sensing molecule poly(ADP-Ribose) polymerase cooperates with p53 in telomere function, chromosome stability, and tumor suppression. Mol. Cell. Biol., 21, 4046-4054.
21. Menissier,d.M., Ricoul,M., Tartier,L., Niedergang,C., Huber,A., Dantzer,F., Schreiber,V., Ame,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.
22. Ame,J.C., Schreiber,V., Fraulob,V., Dolle,P., de Murcia,G. and Niedergang,C.P. (2001) A bidirectional promoter connects the poly(ADP-ribose) polymerase 2 (PARP-2) gene to the gene for RNase P RNA. Structure and expression of the mouse PARP-2 gene: J. Biol. Chem., 276, 11092-11099.
23. Schreiber,V., Ame,J.C., Dolle,P., Schultz,I., Rinaldi,B., Fraulob,V., Menissier-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.
24. Orren,D.K., Brosh,R.M.,Jr, Nehlin,J.O., Machwe,A., Gray,M.D. and Bohr,V.A. (1999) Enzymatic and DNA binding properties of purified WRN protein: high affinity binding to single-stranded DNA but not to DNA damage induced by 4NQO. Nucleic Acids Res., 27, 3557-3566.
25. Machwe,A., Ganunis,R., Bohr,V.A. and Orren,D.K. (2000) Selective blockage of the 3′→5′ exonuclease activity of WRN protein by certain oxidative modifications and bulky lesions in DNA. Nucleic Acids Res., 28, 2762-2770.
26. Giner,H., Simonin,F., de Murcia,G. and Menissier-de Murcia,J. (1992) Overproduction and large-scale purification of the human poly(ADP-ribose) polymerase using a baculovirus expression system. Gene, 114, 279-283.
27. Karmakar,P., Snowden,C.M., Ramsden,D.A. and Bohr,V.A. (2002) Ku heterodimer binds to both ends of the Werner protein and functional interaction occurs at the Werner N-terminus. Nucleic Acids Res., 30, 3583-3591.
28. Karmakar,P., Piotrowski,J., Brosh,R.M.,Jr, Sommers,J.A., Miller,S.P., Cheng,W.H., Snowden,C.M., Ramsden,D.A. and Bohr,V.A. (2002) Werner protein is a target of DNA-dependent protein kinase in vivo and in vitro, and its catalytic activities are regulated by phosphorylation. J. Biol. Chem., 277, 18291-18302.
29. Huang,S., Li,B., Gray,M.D., Oshima,J., Mian,I.S. and Campisi,J. (1998) The premature ageing syndrome protein, WRN, is a 3′→5′ exonuclease. Nature Genet., 20, 114-116.
30. Adelfalk,C., Kontou,M., Hirsch-Kauffmann,M. and Schweiger,M. (2003) Physical and functional interaction of the Werner syndrome protein with poly-ADP ribosyl transferase. FEBS Lett., 554, 55-58.
31. Li,B., Navarro,S., Kasahara,N. and Comai,L. (2004) Identification and biochemical characterization of a Werner's syndrome protein complex with Ku70/80 and poly(ADP-ribose) polymerase-1. J. Biol. Chem., 279, 13659-13667.
32. Ludwig,A., Behnke,B., Holtlund,J. and Hilz,H. (1988) Immunoquantitation and size determination of intrinsic poly(ADP-ribose) polymerase from acid precipitates. An analysis of the in vivo status in mammalian species and in lower eukaryotes. J. Biol. Chem., 263, 6993-6999.
33. Yamanaka,H., Penning,C.A., Willis,E.H., Wasson,D.B. and Carson,D.A. (1988) Characterization of human poly(ADP-ribose) polymerase with autoantibodies. J. Biol. Chem., 263, 3879-3883.
34. Moser,M.J., Kamath-Loeb,A.S., Jacob,J.E., Bennett,S.E., Oshima,J. and Monnat Jr,R.J. (2000) WRN helicase expression in Werner syndrome cell lines. Nucleic Acids Res., 28, 648-654.
35. Brosh,J., Karmakar,P., Sommers,J.A., Yang,Q., Wang,X.W., Spillare,E.A., Harris,C.C. and Bohr,V.A. (2001) p53 modulates the exonuclease activity of Werner syndrome protein. J.Biol.Chem., 276, 35093-35102.
36. Cooper,M.P., Machwe,A., Orren,D.K., Brosh,R.M., Ramsden,D. and Bohr,V.A. (2000) Ku complex interacts with and stimulates the Werner protein. Genes Dev., 14, 907-912.
37. Yannone,S.M., Roy,S., Chan,D.W., Murphy,M.B., Huang,S., Campisi,J. and Chen,D.J. (2001) Werner syndrome protein is regulated and phosphorylated by dna- dependent protein kinase. J. Biol. Chem., 276, 38242-38248.
38. Ruscetti,T., Lehnert,B.E., Halbrook,J., Le Trong,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.
39. Ariumi,Y., Masutani,M., Copeland,T.D., Mimori,T., Sugimura,T., Shimotohno,K., Ueda,K., Hatanaka,M. and Noda,M. (1999) Suppression of the poly(ADP-ribose) polymerase activity by DNA-dependent protein kinase in vitro. Oncogene, 18, 4616-4625.
40. Lindahl,T., Satoh,M.S., Poirier,G.G. and Klungland,A. (1995) Post-translational modification of poly(ADP-ribose) polymerase induced by DNA strand breaks. Trends Biochem. Sci., 20, 405-411.
41. 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.
42. 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.
43. Szekely,A.M., Chen,Y.H., Zhang,C., Oshima,J. and Weissman,S.M. (2000) Werner protein recruits DNA polymerase delta to the nucleolus. Proc. Natl Acad. Sci. USA, 97, 11365-11370.
44. Kamath-Loeb,A.S., Johansson,E., Burgers,P.M. and Loeb,L.A. (2000) Functional interaction between the Werner Syndrome protein and DNA polymerase delta. Proc. Natl Acad. Sci. USA, 97, 4603-4608.
45. Muiras,M.L. (2003) Mammalian longevity under the protection of PARP-1's multi-facets. Ageing Res. Rev., 2, 129-148.
46. Lebel,M., Lavoie,J., Gaudreault,I., Bronsard,M. and Drouin,R. (2003) Genetic cooperation between the Werner syndrome protein and poly(ADP-ribose) polymerase-1 in preventing chromatid breaks, complex chromosomal rearrangements, and cancer in mice. Am. J. Pathol., 162, 1559-1569.
47. de Murcia,G. and Menissier,d.M. (1994) Poly(ADP-ribose) polymerase: a molecular nick-sensor. Trends Biochem. Sci., 19, 172-176.