Structural Basis of Detection and Signaling of DNA Single-Strand Breaks by Human PARP-1

Molecular Cell

Volumn 60, Issue 5, 2015, Pages 742-754

  Eustermann, Sebastian ^a,c   Wu, Wing Fung ^a,d   Langelier, Marie France ^b,e   Yang, Ji Chun ^a   Easton, Laura E ^a   Riccio, Amanda A ^b,e   Pascal, John M ^b,e   Neuhaus, David ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

^c UNIVERSITY OF MUNICH   (Germany)

^d UNIVERSITY OF HONG KONG   (Hong Kong)

^e UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

MONOMER; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; POLY(ADENOSINE DIPHOSPHATE RIBOSE); ZINC FINGER PROTEIN; DNA; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PARP1 PROTEIN, HUMAN;

ALLOSTERISM; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; DNA DAMAGE; DNA STRUCTURE; ENZYME ACTIVE SITE; MOLECULAR DYNAMICS; MOLECULAR RECOGNITION; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN FOLDING; SIGNAL TRANSDUCTION; SINGLE STRANDED DNA BREAK; CHEMISTRY; CONFORMATION; DNA REPAIR; HUMAN; METABOLISM; MOLECULAR MODEL; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; X RAY CRYSTALLOGRAPHY;

CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; DNA; DNA BREAKS, SINGLE-STRANDED; DNA REPAIR; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION; POLY (ADP-RIBOSE) POLYMERASE-1; POLY(ADP-RIBOSE) POLYMERASES; PROTEIN FOLDING; ZINC FINGERS;

EID: 84952875833     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2015.10.032     Document Type: Article

References (58)

1. Ali A.A., Timinszky G., Arribas-Bosacoma R., Kozlowski M., Hassa P.O., Hassler M., Ladurner A.G., Pearl L.H., Oliver A.W. The zinc-finger domains of PARP1 cooperate to recognize DNA strand breaks. Nat. Struct. Mol. Biol. 2012, 19:685-692.
2. Bax A., Grishaev A. Weak alignment NMR: a hawk-eyed view of biomolecular structure. Curr. Opin. Struct. Biol. 2005, 15:563-570.
3. Bryant H.E., Schultz N., Thomas H.D., Parker K.M., Flower D., Lopez E., Kyle S., Meuth M., Curtin N.J., Helleday T. Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase. Nature 2005, 434:913-917.
4. Bryant H.E., Petermann E., Schultz N., Jemth A.S., Loseva O., Issaeva N., Johansson F., Fernandez S., McGlynn P., Helleday T. PARP is activated at stalled forks to mediate Mre11-dependent replication restart and recombination. EMBO J. 2009, 28:2601-2615.
5. Caldecott K.W. Single-strand break repair and genetic disease. Nat. Rev. Genet. 2008, 9:619-631.
6. Caldecott K.W. Protein ADP-ribosylation and the cellular response to DNA strand breaks. DNA Repair (Amst.) 2014, 19:108-113.
7. Chao L.H., Stratton M.M., Lee I.H., Rosenberg O.S., Levitz J., Mandell D.J., Kortemme T., Groves J.T., Schulman H., Kuriyan J. A mechanism for tunable autoinhibition in the structure of a human Ca2+/calmodulin- dependent kinase II holoenzyme. Cell 2011, 146:732-745.
8. Chou D.M., Adamson B., Dephoure N.E., Tan X., Nottke A.C., Hurov K.E., Gygi S.P., Colaiácovo M.P., Elledge S.J. A chromatin localization screen reveals poly (ADP ribose)-regulated recruitment of the repressive polycomb and NuRD complexes to sites of DNA damage. Proc. Natl. Acad. Sci. USA 2010, 107:18475-18480.
9. Correll C.C., Swinger K. Common and distinctive features of GNRA tetraloops based on a GUAA tetraloop structure at 1.4 A resolution. RNA 2003, 9:355-363.
10. D'Amours D., Desnoyers S., D'Silva I., Poirier G.G. Poly(ADP-ribosyl)ation reactions in the regulation of nuclear functions. Biochem. J. 1999, 342:249-268.
11. Dawicki-McKenna J.M., Langelier M.F., DeNizio J.E., Riccio A.A., Cao C.D., Karch K.R., McCauley M., Steffen J.D., Black B.E., Pascal J.M. PARP-1 activation requires local unfolding of an autoinhibitory domain. Mol. Cell 2015, 60:755-768. this issue.
12. de Murcia G., Ménissier de Murcia J. Poly(ADP-ribose) polymerase: a molecular nick-sensor. Trends Biochem. Sci. 1994, 19:172-176.
13. de Murcia G., Schreiber V., Molinete M., Saulier B., Poch O., Masson M., Niedergang C., Ménissier de Murcia J. Structure and function of poly(ADP-ribose) polymerase. Mol. Cell. Biochem. 1994, 138:15-24.
14. Durkacz B.W., Omidiji O., Gray D.A., Shall S. (ADP-ribose)n participates in DNA excision repair. Nature 1980, 283:593-596.
15. Elia A.E., Boardman A.P., Wang D.C., Huttlin E.L., Everley R.A., Dephoure N., Zhou C., Koren I., Gygi S.P., Elledge S.J. Quantitative Proteomic Atlas of Ubiquitination and Acetylation in the DNA Damage Response. Mol. Cell 2015, 59:867-881.
16. 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.
17. Farmer H., McCabe N., Lord C.J., Tutt A.N., Johnson D.A., Richardson T.B., Santarosa M., Dillon K.J., Hickson I., Knights C., et al. Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature 2005, 434:917-921.
18. Fernández C., Wider G. TROSY in NMR studies of the structure and function of large biological macromolecules. Curr. Opin. Struct. Biol. 2003, 13:570-580.
19. Fouquerel E., Goellner E.M., Yu Z., Gagné J.P., Barbi de Moura M., Feinstein T., Wheeler D., Redpath P., Li J., Romero G., et al. ARTD1/PARP1 negatively regulates glycolysis by inhibiting hexokinase 1 independent of NAD+ depletion. Cell Rep. 2014, 8:1819-1831.
20. Göbl C., Madl T., Simon B., Sattler M. NMR approaches for structural analysis of multidomain proteins and complexes in solution. Prog. Nucl. Magn. Reson. Spectrosc. 2014, 80:26-63.
21. Guettler S., LaRose J., Petsalaki E., Gish G., Scotter A., Pawson T., Rottapel R., Sicheri F. Structural basis and sequence rules for substrate recognition by Tankyrase explain the basis for cherubism disease. Cell 2011, 147:1340-1354.
22. Helleday T. The underlying mechanism for the PARP and BRCA synthetic lethality: clearing up the misunderstandings. Mol. Oncol. 2011, 5:387-393.
23. Helsen C., Kerkhofs S., Clinckemalie L., Spans L., Laurent M., Boonen S., Vanderschueren D., Claessens F. Structural basis for nuclear hormone receptor DNA binding. Mol. Cell. Endocrinol. 2012, 348:411-417.
24. Hunter C.A., Anderson H.L. What is cooperativity?. Angew. Chem. Int. Ed. Engl. 2009, 48:7488-7499.
25. Jucker F.M., Pardi A. Solution structure of the CUUG hairpin loop: a novel RNA tetraloop motif. Biochemistry 1995, 34:14416-14427.
26. Khodyreva S.N., Prasad R., Ilina E.S., Sukhanova M.V., Kutuzov M.M., Liu Y., Hou E.W., Wilson S.H., Lavrik O.I. Apurinic/apyrimidinic (AP) site recognition by the 5'-dRP/AP lyase in poly(ADP-ribose) polymerase-1 (PARP-1). Proc. Natl. Acad. Sci. USA 2010, 107:22090-22095.
27. +-dependent modulation of chromatin structure and transcription by nucleosome binding properties of PARP-1. Cell 2004, 119:803-814.
28. Kobashigawa Y., Kumeta H., Ogura K., Inagaki F. Attachment of an NMR-invisible solubility enhancement tag using a sortase-mediated protein ligation method. J. Biomol. NMR 2009, 43:145-150.
29. Krishnakumar R., Kraus W.L. The PARP side of the nucleus: molecular actions, physiological outcomes, and clinical targets. Mol. Cell 2010, 39:8-24.
30. Lamers M.H., Perrakis A., Enzlin J.H., Winterwerp H.H.K., de Wind N., Sixma T.K. The crystal structure of DNA mismatch repair protein MutS binding to a G x T mismatch. Nature 2000, 407:711-717.
31. 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.
32. 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.
33. Lazebnik Y.A., Kaufmann S.H., Desnoyers S., Poirier G.G., Earnshaw W.C. Cleavage of poly(ADP-ribose) polymerase by a proteinase with properties like ICE. Nature 1994, 371:346-347.
34. Le Cam E., Fack F., Ménissier-de Murcia J., Cognet J.A., Barbin A., Sarantoglou V., Révet B., Delain E., de Murcia G. Conformational analysis of a 139 base-pair DNA fragment containing a single-stranded break and its interaction with human poly(ADP-ribose) polymerase. J. Mol. Biol. 1994, 235:1062-1071.
35. Lee D., Hilty C., Wider G., Wuthrich K. Effective rotational correlation times of proteins from NMR relaxation interference. J. Magn. Reson. 2006, 178:72-76.
36. Lilyestrom W., van der Woerd M.J., Clark N., Luger K. Structural and biophysical studies of human PARP-1 in complex with damaged DNA. J. Mol. Biol. 2010, 395:983-994.
37. Lord C.J., Ashworth A. Mechanisms of resistance to therapies targeting BRCA-mutant cancers. Nat. Med. 2013, 19:1381-1388.
38. Luo X., Kraus W.L. On PAR with PARP: cellular stress signaling through poly(ADP-ribose) and PARP-1. Genes Dev. 2012, 26:417-432.
39. Mackereth C.D., Madl T., Bonnal S., Simon B., Zanier K., Gasch A., Rybin V., Valcárcel J., Sattler M. Multi-domain conformational selection underlies pre-mRNA splicing regulation by U2AF. Nature 2011, 475:408-411.
40. Mansoorabadi S.O., Wu M., Tao Z., Gao P., Pingali S.V., Guo L., Liu H.W. Conformational activation of poly(ADP-ribose) polymerase-1 upon DNA binding revealed by small-angle X-ray scattering. Biochemistry 2014, 53:1779-1788.
41. Marchand J.R., Carotti A., Passeri D., Filipponi P., Liscio P., Camaioni E., Pellicciari R., Gioiello A., Macchiarulo A. Investigating the allosteric reverse signalling of PARP inhibitors with microsecond molecular dynamic simulations and fluorescence anisotropy. Biochim. Biophys. Acta 2014, 1844:1765-1772.
42. Mendes-Pereira A.M., Martin S.A., Brough R., McCarthy A., Taylor J.R., Kim J.S., Waldman T., Lord C.J., Ashworth A. Synthetic lethal targeting of PTEN mutant cells with PARP inhibitors. EMBO Mol. Med. 2009, 1:315-322.
43. Mendoza-Alvarez H., Alvarez-Gonzalez R. Poly(ADP-ribose) polymerase is a catalytic dimer and the automodification reaction is intermolecular. J. Biol. Chem. 1993, 268:22575-22580.
44. Min J.H., Pavletich N.P. Recognition of DNA damage by the Rad4 nucleotide excision repair protein. Nature 2007, 449:570-575.
45. Molinete M., Vermeulen W., Bürkle A., Ménissier-de Murcia J., Küpper J.H., Hoeijmakers J.H., de Murcia G. Overproduction of the poly(ADP-ribose) polymerase DNA-binding domain blocks alkylation-induced DNA repair synthesis in mammalian cells. EMBO J. 1993, 12:2109-2117.
46. Moreno-Herrero F., de Jager M., Dekker N.H., Kanaar R., Wyman C., Dekker C. Mesoscale conformational changes in the DNA-repair complex Rad50/Mre11/Nbs1 upon binding DNA. Nature 2005, 437:440-443.
47. Murai J., Huang S.Y., Das B.B., Renaud A., Zhang Y., Doroshow J.H., Ji J., Takeda S., Pommier Y. Trapping of PARP1 and PARP2 by Clinical PARP Inhibitors. Cancer Res. 2012, 72:5588-5599.
48. Pion E., Bombarda E., Stiegler P., Ullmann G.M., Mély Y., de Murcia G., Gérard D. Poly(ADP-ribose) polymerase-1 dimerizes at a 5' recessed DNA end in vitro: a fluorescence study. Biochemistry 2003, 42:12409-12417.
49. Pion E., Ullmann G.M., Amé J.C., Gérard D., de Murcia G., Bombarda E. DNA-induced dimerization of poly(ADP-ribose) polymerase-1 triggers its activation. Biochemistry 2005, 44:14670-14681.
50. Polo S.E., Jackson S.P. Dynamics of DNA damage response proteins at DNA breaks: a focus on protein modifications. Genes Dev. 2011, 25:409-433.
51. Sass H.J., Musco G., Stahl S.J., Wingfield P.T., Grzesiek S. An easy way to include weak alignment constraints into NMR structure calculations. J. Biomol. NMR 2001, 21:275-280.
52. Satoh M.S., Lindahl T. Role of poly(ADP-ribose) formation in DNA repair. Nature 1992, 356:356-358.
53. 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.
54. Schwieters C.D., Kuszewski J.J., Tjandra N., Clore G.M. The Xplor-NIH NMR molecular structure determination package. J. Magn. Reson. 2003, 160:65-73.
55. Shen Y., Aoyagi-Scharber M., Wang B. Trapping Poly(ADP-Ribose) Polymerase. J. Pharmacol. Exp. Ther. 2015, 353:446-457.
56. Shoemaker B.A., Portman J.J., Wolynes P.G. Speeding molecular recognition by using the folding funnel: the fly-casting mechanism. Proc. Natl. Acad. Sci. USA 2000, 97:8868-8873.
57. Sonnenblick A., de Azambuja E., Azim H.A., Piccart M. An update on PARP inhibitors--moving to the adjuvant setting. Nat. Rev. Clin. Oncol. 2015, 12:27-41.
58. Zhang Y., Wang J., Ding M., Yu Y. Site-specific characterization of the Asp- and Glu-ADP-ribosylated proteome. Nat. Methods 2013, 10:981-984.