DNA-dependent SUMO modification of PARP-1

DNA Repair

Volumn 12, Issue 9, 2013, Pages 761-773

  Zilio, Nicola ^a,d   Williamson, Chris T ^a,e   Eustermann, Sebastian ^b   Shah, Rajvee ^a   West, Stephen C ^a   Neuhaus, David ^b   Ulrich, Helle D ^a,c  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^b MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^c INSTITUTE OF MOLECULAR BIOLOGY   (Armenia)

^d SCRIPPS RESEARCH INSTITUTE   (United States)

^e INSTITUTE OF CANCER RESEARCH   (United Kingdom)

Author keywords

DNA binding; DNA repair; PARP 1; Posttranslational modification; SUMO; Transcription

Indexed keywords

DNA; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1;

ARTICLE; CATALYSIS; CHROMATIN; CONTROLLED STUDY; DNA BINDING; DNA DAMAGE; DNA STRUCTURE; NONHUMAN; PRIORITY JOURNAL; STRUCTURE ANALYSIS; SUMOYLATION;

DNA BINDING; DNA REPAIR; PARP-1; POSTTRANSLATIONAL MODIFICATION; SUMO; TRANSCRIPTION;

BASE SEQUENCE; CATALYTIC DOMAIN; CHROMATIN; DNA; DNA BREAKS; DNA-BINDING PROTEINS; ENZYME ACTIVATION; HEK293 CELLS; HUMANS; INVERTED REPEAT SEQUENCES; NUCLEIC ACID CONFORMATION; PLASMIDS; POLY(ADP-RIBOSE) POLYMERASES; PROTEIN BINDING; SUMO-1 PROTEIN; SUMOYLATION; UBIQUITIN-CONJUGATING ENZYMES;

EID: 84880961949     PISSN: 15687864     EISSN: 15687856     Source Type: Journal    
DOI: 10.1016/j.dnarep.2013.07.001     Document Type: Article

References (50)

1. Walsh C.T., Garneau-Tsodikova S., Gatto G.J. Protein posttranslational modifications: the chemistry of proteome diversifications. Angew. Chem. Int. Ed. Engl. 2005, 44:7342-7372.
2. Geiss-Friedlander R., Melchior F. Concepts in sumoylation: a decade on. Nat. Rev. Mol. Cell Biol. 2007, 8:947-956.
3. Kerscher O. SUMO junction-what's your function? New insights through SUMO-interacting motifs. EMBO Rep. 2007, 8:550-555.
4. Zilio N., Ulrich H.D. Functions of SUMO in the maintenance of genome stability. SUMO Regulation of Cellular Processes 2009, 77-96. Springer, Netherlands. V.G. Wilson (Ed.).
5. Matunis M.J., Zhang X.D., Ellis N.A. SUMO: the glue that binds. Dev. Cell 2006, 11:596-597.
6. Baba D., Maita N., Jee J.G., Uchimura Y., Saitoh H., Sugasawa K., Hanaoka F., Tochio H., Hiroaki H., Shirakawa M. Crystal structure of thymine DNA glycosylase conjugated to SUMO-1. Nature 2005, 435:979-982.
7. Hardeland U., Steinacher R., Jiricny J., Schar P. Modification of the human thymine-DNA glycosylase by ubiquitin-like proteins facilitates enzymatic turnover. EMBO J. 2002, 21:1456-1464.
8. Steinacher R., Schar P. Functionality of human thymine DNA glycosylase requires SUMO-regulated changes in protein conformation. Curr. Biol. 2005, 15:616-623.
9. Altmannova V., Eckert-Boulet N., Arneric M., Kolesar P., Chaloupkova R., Damborsky J., Sung P., Zhao X., Lisby M., Krejci L. Rad52 SUMOylation affects the efficiency of the DNA repair. Nucleic Acids Res. 2010, 38:4708-4721.
10. Parker J.L., Bucceri A., Davies A.A., Heidrich K., Windecker H., Ulrich H.D. SUMO modification of PCNA is controlled by DNA. EMBO J. 2008, 27:2422-2431.
11. Gareau J.R., Lima C.D. The SUMO pathway: emerging mechanisms that shape specificity, conjugation and recognition. Nat. Rev. Mol. Cell Biol. 2010, 11:861-871.
12. Ame J.C., Spenlehauer C., de Murcia G. The PARP superfamily. Bioessays 2004, 26:882-893.
13. Altmeyer M., Messner S., Hassa P.O., Fey M., Hottiger M.O. Molecular mechanism of poly(ADP-ribosyl)ation by PARP1 and identification of lysine residues as ADP-ribose acceptor sites. Nucleic Acids Res. 2009, 37:3723-3738.
14. Schreiber V., Dantzer F., Ame J.C., de Murcia G. Poly(ADP-ribose): novel functions for an old molecule. Nat. Rev. Mol. Cell Biol. 2006, 7:517-528.
15. Woodhouse B.C., Dianov G.L. Poly ADP-ribose polymerase-1: an international molecule of mystery. DNA Repair 2008, 7:1077-1086.
16. Ikejima M., Noguchi S., Yamashita R., Ogura T., Sugimura T., Gill D.M., Miwa M. 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. 1990, 265:21907-21913.
17. Langelier M.F., Planck J.L., Roy S., Pascal J.M. Crystal structures of poly(ADP-ribose) polymerase-1 (PARP-1) zinc fingers bound to DNA: structural and functional insights into DNA-dependent PARP-1 activity. J. Biol. Chem. 2011, 286:10690-10701.
18. Eustermann S., Videler H., Yang J.C., Cole P.T., Gruszka D., Veprintsev D., Neuhaus D. The DNA-binding domain of human PARP-1 interacts with DNA single-strand breaks as a monomer through its second zinc finger. J. Mol. Biol. 2011, 407:149-170.
19. Gradwohl G., Menissier de Murcia J.M., Molinete M., Simonin F., Koken M., Hoeijmakers J.H., de Murcia G. The second zinc-finger domain of poly(ADP-ribose) polymerase determines specificity for single-stranded breaks in DNA. Proc. Natl Acad. Sci. U.S.A. 1990, 87:2990-2994.
20. Langelier M.F., Planck J.L., Roy S., Pascal J.M. Structural basis for DNA damage-dependent poly(ADP-ribosyl)ation by human PARP-1. Science 2012, 336:728-732.
21. Menissier-de Murcia J., Molinete M., Gradwohl G., Simonin F., de Murcia G. Zinc-binding domain of poly(ADP-ribose)polymerase participates in the recognition of single strand breaks on DNA. J. Mol. Biol. 1989, 210:229-233.
22. Langelier M.F., Ruhl D.D., Planck J.L., Kraus W.L., Pascal J.M. The Zn3 domain of human poly(ADP-ribose) polymerase-1 (PARP-1) functions in both DNA-dependent poly(ADP-ribose) synthesis activity and chromatin compaction. J. Biol. Chem. 2010, 285:18877-18887.
23. Langelier M.F., Servent K.M., Rogers E.E., Pascal J.M. A third zinc-binding domain of human poly(ADP-ribose) polymerase-1 coordinates DNA-dependent enzyme activation. J. Biol. Chem. 2008, 283:4105-4114.
24. Tao Z., Gao P., Hoffman D.W., Liu H.W. Domain C of human poly(ADP-ribose) polymerase-1 is important for enzyme activity and contains a novel zinc-ribbon motif. Biochemistry 2008, 47:5804-5813.
25. Kraus W.L. Transcriptional control by PARP-1: chromatin modulation, enhancer-binding, coregulation, and insulation. Curr. Opin. Cell Biol. 2008, 20:294-302.
26. Realini C.A., Althaus F.R. Histone shuttling by poly(ADP-ribosylation). J. Biol. Chem. 1992, 267:18858-18865.
27. Panzeter P.L., Zweifel B., Malanga M., Waser S.H., Richard M., Althaus F.R. Targeting of histone tails by poly(ADP-ribose). J. Biol. Chem. 1993, 268:17662-17664.
28. Ahel D., Horejsi Z., Wiechens N., Polo S.E., Garcia-Wilson E., Ahel I., Flynn H., Skehel M., West S.C., Jackson S.P., Owen-Hughes T., Boulton S.J. Poly(ADP-ribose)-dependent regulation of DNA repair by the chromatin remodeling enzyme ALC1. Science 2009, 325:1240-1243.
29. Gottschalk A.J., Timinszky G., Kong S.E., Jin J., Cai Y., Swanson S.K., Washburn M.P., Florens L., Ladurner A.G., Conaway J.W., Conaway R.C. Poly(ADP-ribosyl)ation directs recruitment and activation of an ATP-dependent chromatin remodeler. Proc. Natl Acad. Sci. U.S.A. 2009, 106:13770-13774.
30. Timinszky G., Till S., Hassa P.O., Hothorn M., Kustatscher G., Nijmeijer B., Colombelli J., Altmeyer M., Stelzer E.H., Scheffzek K., Hottiger M.O., Ladurner A.G. A macrodomain-containing histone rearranges chromatin upon sensing PARP1 activation. Nat. Struct. Mol. Biol. 2009, 16:923-929.
31. Pavri R., Lewis B., Kim T.K., Dilworth F.J., Erdjument-Bromage H., Tempst P., de Murcia G., Evans R., Chambon P., Reinberg D. PARP-1 determines specificity in a retinoid signaling pathway via direct modulation of mediator. Mol. Cell 2005, 18:83-96.
32. Messner S., Schuermann D., Altmeyer M., Kassner I., Schmidt D., Schar P., Muller S., Hottiger M.O. Sumoylation of poly(ADP-ribose) polymerase 1 inhibits its acetylation and restrains transcriptional coactivator function. FASEB J. 2009, 23:3978-3989.
33. Martin N., Schwamborn K., Schreiber V., Werner A., Guillier C., Zhang X.D., Bischof O., Seeler J.S., Dejean A. PARP-1 transcriptional activity is regulated by sumoylation upon heat shock. EMBO J. 2009, 28:3534-3548.
34. Ryu H., Al-Ani G., Deckert K., Kirkpatrick D., Gygi S.P., Dasso M., Azuma Y. PIASy mediates SUMO-2/3 conjugation of poly(ADP-ribose) polymerase 1 (PARP1) on mitotic chromosomes. J. Biol. Chem. 2010, 285:14415-14423.
35. Blomster H.A., Hietakangas V., Wu J., Kouvonen P., Hautaniemi S., Sistonen L. Novel proteomics strategy brings insight into the prevalence of SUMO-2 target sites. Mol. Cell. Proteomics 2009, 8:1382-1390.
36. Dantzer F., Ame J.C., Schreiber V., Nakamura J., Menissier-de Murcia J., de Murcia G. Poly(ADP-ribose) polymerase-1 activation during DNA damage and repair. Methods Enzymol. 2006, 409:493-510.
37. Werner A., Moutty M.C., Möller U., Melchior F. Performing in vitro sumoylation reactions using recombinant enzymes. Methods Mol. Biol. 2009, 497:187-199.
38. Yunus A.A., Lima C.D. Purification of SUMO conjugating enzymes and kinetic analysis of substrate conjugation methods. Mol. Biol. 2009, 497:167-186.
39. Muller S., Berger M., Lehembre F., Seeler J.S., Haupt Y., Dejean A. c-Jun and p53 activity is modulated by SUMO-1 modification. J. Biol. Chem. 2000, 275:13321-13329.
40. Weisshaar S.R., Keusekotten K., Krause A., Horst C., Springer H.M., Gottsche K., Dohmen R.J., Praefcke G.J. Arsenic trioxide stimulates SUMO-2/3 modification leading to RNF4-dependent proteolytic targeting of PML. FEBS Lett. 2008, 582:3174-3178.
41. Lowary P.T., Widom J. New DNA sequence rules for high affinity binding to histone octamer and sequence-directed nucleosome positioning. J. Mol. Biol. 1998, 276:19-42.
42. Gradwohl G., Mazen A., de Murcia G. Poly(ADP-ribose) polymerase forms loops with DNA. Biochem. Biophys. Res. Commun. 1987, 148:913-919.
43. Lonskaya I., Potaman V.N., Shlyakhtenko L.S., Oussatcheva E.A., Lyubchenko Y.L., Soldatenkov V.A. Regulation of poly(ADP-ribose) polymerase-1 by DNA structure-specific binding. J. Biol. Chem. 2005, 280:17076-17083.
44. Sastry S.S., Buki K.G., Kun E. Binding of adenosine diphosphoribosyltransferase to the termini and internal regions of linear DNAs. Biochemistry 1989, 28:5670-5680.
45. Petesch S.J., Lis J.T. Activator-induced spread of poly(ADP-ribose) polymerase promotes nucleosome loss at Hsp70. Mol. Cell 2012, 45:64-74.
46. Macauley M.S., Errington W.J., Scharpf M., Mackereth C.D., Blaszczak A.G., Graves B.J., McIntosh L.P. Beads-on-a-string, characterization of ETS-1 sumoylated within its flexible N-terminal sequence. J. Biol. Chem. 2006, 281:4164-4172.
47. Macauley M.S., Errington W.J., Okon M., Scharpf M., Mackereth C.D., Schulman B.A., McIntosh L.P. Structural and dynamic independence of isopeptide-linked RanGAP1 and SUMO-1. J. Biol. Chem. 2004, 279:49131-49137.
48. Knipscheer P., Flotho A., Klug H., Olsen J.V., van Dijk W.J., Fish A., Johnson E.S., Mann M., Sixma T.K., Pichler A. Ubc9 sumoylation regulates SUMO target discrimination. Mol. Cell 2008, 31:371-382.
49. Pichler A., Knipscheer P., Oberhofer E., van Dijk W.J., Korner R., Olsen J.V., Jentsch S., Melchior F., Sixma T.K. SUMO modification of the ubiquitin-conjugating enzyme E2-25K. Nat. Struct. Mol. Biol. 2005, 12:264-269.
50. Bernier-Villamor V., Sampson D.A., Matunis M.J., Lima C.D. Structural basis for E2-mediated SUMO conjugation revealed by a complex between ubiquitin-conjugating enzyme Ubc9 and RanGAP1. Cell 2002, 108:345-356.