Large-scale preparation and characterization of poly(ADP-ribose) and defined length polymers

Analytical Biochemistry

Volumn 428, Issue 2, 2012, Pages 126-136

  Tan, Edwin S ^a   Krukenberg, Kristin A ^a   Mitchison, Timothy J ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

ADP ribose; ADPr; pADPr; PAR; PARG; PARP; Poly(ADP ribose); Poly(ADP ribose) glycohydrolase; Poly(ADP ribose) polymerase; Polymer

Indexed keywords

BINDING ENERGY; CHROMATOGRAPHIC ANALYSIS; CHROMATOGRAPHY; IONS; POLYMERS;

ADP-RIBOSE; ADPR; GLYCOHYDROLASE; PADPR; PARG; PARP; POLY POLYMERASE;

PROTEINS;

NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; POLY(ADENOSINE DIPHOSPHATE RIBOSE); POLY(ADP RIBOSE) GLYCOHYDROLASE; POLYMER; TANKYRASE; TANKYRASE 1; UNCLASSIFIED DRUG;

ANION EXCHANGE CHROMATOGRAPHY; ARTICLE; CALIBRATION; CHEMICAL ANALYSIS; CHROMATOGRAPHY; ENZYME ACTIVITY; ENZYME SYNTHESIS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; PARTICLE SIZE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN METABOLISM; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PURIFICATION; STRUCTURE ACTIVITY RELATION;

EID: 84864408302     PISSN: 00032697     EISSN: 10960309     Source Type: Journal    
DOI: 10.1016/j.ab.2012.06.015     Document Type: Article

References (63)

1. A. Hakme, H.K. Wong, F. Dantzer, and V. Schreiber The expanding field of poly(ADP-ribosyl)ation reactions EMBO Rep. 9 2008 1094 1100
2. M. Altmeyer, S. Messner, P.O. Hassa, M. Fey, and M.O. Hottiger Molecular mechanism of poly(ADP-ribosyl)ation by PARP1 and identification of lysine residues as ADP-ribose acceptor sites Nucleic Acids Res. 37 2009 3723 3738
3. Z. Tao, P. Gao, and H.W. Liu Identification of the ADP-ribosylation sites in the PARP-1 automodification domain: analysis and implications J. Am. Chem. Soc. 131 2009 14258 14260
4. J. Diefenbach, and A. Burkle Introduction to poly(ADP-ribose) metabolism Cell. Mol. Life Sci. 62 2005 721 730 (Pubitemid 40655622)
5. P.O. Hassa, and M.O. Hottiger The diverse biological roles of mammalian PARPS, a small but powerful family of poly-ADP-ribose polymerases Front. Biosci. 13 2008 3046 3082 (Pubitemid 351589219)
6. V. Schreiber, F. Dantzer, J.C. Ame, and G. de Murcia Poly(ADP-ribose): novel functions for an old molecule Nat. Rev. Mol. Cell Biol. 7 2006 517 528 (Pubitemid 44036457)
7. H. Kleine, E. Poreba, K. Lesniewicz, P.O. Hassa, M.O. Hottiger, D.W. Litchfield, B.H. Shilton, and B. Luscher Substrate-assisted catalysis by PARP10 limits its activity to mono-ADP-ribosylation Mol. Cell 32 2008 57 69
8. M.O. Hottiger, P.O. Hassa, B. Luscher, H. Schuler, and F. Koch-Nolte Toward a unified nomenclature for mammalian ADP-ribosyltransferases Trends Biochem. Sci. 35 2010 208 219
9. J.T. Heeres, and P.J. Hergenrother Poly(ADP-ribose) makes a date with death Curr. Opin. Chem. Biol. 11 2007 644 653 (Pubitemid 350180567)
10. P. Chang, M. Coughlin, and T.J. Mitchison Tankyrase-1 polymerization of poly(ADP-ribose) is required for spindle structure and function Nat. Cell Biol. 7 2005 1133 1139
11. P. Chang, M. Coughlin, and T.J. Mitchison Interaction between poly(ADP-ribose) and NuMA contributes to mitotic spindle pole assembly Mol. Biol. Cell 20 2009 4575 4585
12. P. Chang, M.K. Jacobson, and T.J. Mitchison Poly(ADP-ribose) is required for spindle assembly and structure Nature 432 2004 645 649 (Pubitemid 39626273)
13. S.M. Huang, Y.M. Mishina, S. Liu, A. Cheung, F. Stegmeier, G.A. Michaud, O. Charlat, E. Wiellette, Y. Zhang, S. Wiessner, M. Hild, X. Shi, C.J. Wilson, C. Mickanin, V. Myer, A. Fazal, R. Tomlinson, F. Serluca, W. Shao, H. Cheng, M. Shultz, C. Rau, M. Schirle, J. Schlegl, S. Ghidelli, S. Fawell, C. Lu, D. Curtis, M.W. Kirschner, C. Lengauer, P.M. Finan, J.A. Tallarico, T. Bouwmeester, J.A. Porter, A. Bauer, and F. Cong Tankyrase inhibition stabilizes axin and antagonizes Wnt signalling Nature 461 2009 614 620
14. + into a nuclear signal Genes Dev. 19 2005 1951 1967
15. N. Levaot, O. Voytyuk, I. Dimitriou, F. Sircoulomb, A. Chandrakumar, M. Deckert, P.M. Krzyzanowski, A. Scotter, S. Gu, S. Janmohamed, F. Cong, P.D. Simoncic, Y. Ueki, J. La Rose, and R. Rottapel Loss of tankyrase-mediated destruction of 3BP2 is the underlying pathogenic mechanism of cherubism Cell 147 2011 1324 1339
16. M. Malanga, and F.R. Althaus The role of poly(ADP-ribose) in the DNA damage signaling network Biochem. Cell Biol. 83 2005 354 364 (Pubitemid 41297203)
17. S. Smith, I. Giriat, A. Schmitt, and T. de Lange Tankyrase, a poly(ADP-ribose) polymerase at human telomeres Science 282 1998 1484 1487 (Pubitemid 28538609)
18. J.C. Ame, C. Spenlehauer, and G. de Murcia The PARP superfamily Bioessays 26 2004 882 893 (Pubitemid 39128102)
19. + FEBS J. 272 2005 4576 4589 (Pubitemid 41372054)
20. S. Smith The world according to PARP Trends Biochem. Sci. 26 2001 174 179 (Pubitemid 32197577)
21. R.J. Aubin, A. Frechette, G. de Murcia, P. Mandel, A. Lord, G. Grondin, and G.G. Poirier Correlation between endogenous nucleosomal hyper(ADP-ribosyl) ation of histone H1 and the induction of chromatin relaxation EMBO J. 2 1983 1685 1693
22. D. Ahel, Z. Horejsi, N. Wiechens, S.E. Polo, E. Garcia-Wilson, I. Ahel, H. Flynn, M. Skehel, S.C. West, S.P. Jackson, T. Owen-Hughes, and S.J. Boulton Poly(ADP-ribose)-dependent regulation of DNA repair by the chromatin remodeling enzyme ALC1 Science 325 2009 1240 1243
23. P. Caiafa, T. Guastafierro, and M. Zampieri Epigenetics: poly(ADP-ribosyl)ation of PARP-1 regulates genomic methylation patterns FASEB J. 23 2009 672 678
24. S. Eustermann, C. Brockmann, P.V. Mehrotra, J.C. Yang, D. Loakes, S.C. West, I. Ahel, and D. Neuhaus Solution structures of the two PBZ domains from human APLF and their interaction with poly(ADP-ribose) Nat. Struct. Mol. Biol. 17 2010 241 243
25. S. Guettler, J. Larose, E. Petsalaki, G. Gish, A. Scotter, T. Pawson, R. Rottapel, and F. Sicheri Structural basis and sequence rules for substrate recognition by tankyrase explain the basis for cherubism disease Cell 147 2011 1340 1354
26. G. Timinszky, S. Till, P.O. Hassa, M. Hothorn, G. Kustatscher, B. Nijmeijer, J. Colombelli, M. Altmeyer, E.H. Stelzer, K. Scheffzek, M.O. Hottiger, and A.G. Ladurner A macrodomain-containing histone rearranges chromatin upon sensing PARP1 activation Nat. Struct. Mol. Biol. 16 2009 923 929
27. Y. Zhang, S. Liu, C. Mickanin, Y. Feng, O. Charlat, G.A. Michaud, M. Schirle, X. Shi, M. Hild, A. Bauer, V.E. Myer, P.M. Finan, J.A. Porter, S.M. Huang, and F. Cong RNF146 is a poly(ADP-ribose)-directed E3 ligase that regulates axin degradation and Wnt signalling Nat. Cell Biol. 13 2011 623 629
28. S.A. Andrabi, N.S. Kim, S.W. Yu, H. Wang, D.W. Koh, M. Sasaki, J.A. Klaus, T. Otsuka, Z. Zhang, R.C. Koehler, P.D. Hurn, G.G. Poirier, V.L. Dawson, and T.M. Dawson Poly(ADP-ribose) (PAR) polymer is a death signal Proc. Natl. Acad. Sci. USA 103 2006 18308 18313 (Pubitemid 44871654)
29. K.K. David, S.A. Andrabi, T.M. Dawson, and V.L. Dawson Parthanatos, a messenger of death Front. Biosci. 14 2009 1116 1128
30. Y. Wang, N.S. Kim, J.F. Haince, H.C. Kang, K.K. David, S.A. Andrabi, G.G. Poirier, V.L. Dawson, and T.M. Dawson Poly(ADP-ribose) (PAR) binding to apoptosis-inducing factor is critical for PAR polymerase-1-dependent cell death (parthanatos) Sci. Signal. 4 2011 ra20
31. S.W. Yu, S.A. Andrabi, H. Wang, N.S. Kim, G.G. Poirier, T.M. Dawson, and V.L. Dawson Apoptosis-inducing factor mediates poly(ADP-ribose) (PAR) polymer-induced cell death Proc. Natl. Acad. Sci. USA 103 2006 18314 18319 (Pubitemid 44871655)
32. S.W. Yu, Y. Wang, D.S. Frydenlund, O.P. Ottersen, V.L. Dawson, and T.M. Dawson Outer mitochondrial membrane localization of apoptosis-inducing factor: mechanistic implications for release ASN Neuro 1 2009 275 281
33. Z. Wang, G.A. Michaud, Z. Cheng, Y. Zhang, T.R. Hinds, E. Fan, F. Cong, and W. Xu Recognition of the iso-ADP-ribose moiety in poly(ADP-ribose) by WWE domains suggests a general mechanism for poly(ADP-ribosyl)ation-dependent ubiquitination Genes Dev. 26 2012 235 240
34. I. Ahel, D. Ahel, T. Matsusaka, A.J. Clark, J. Pines, S.J. Boulton, and S.C. West Poly(ADP-ribose)-binding zinc finger motifs in DNA repair/checkpoint proteins Nature 451 2008 81 85
35. T. Minaga, and E. Kun Probable helical conformation of poly(ADP-ribose): the effect of cations on spectral properties J. Biol. Chem. 258 1983 5726 5730
36. T. Minaga, and E. Kun Spectral analysis of the conformation of polyadenosine diphosphoribose: evidence indicating secondary structure J. Biol. Chem. 258 1983 725 730
37. 15N-poly(ADP- ribose) J. Am. Chem. Soc. 131 2009 14571 14578
38. G. de Murcia, J. Jongstra-Bilen, M.E. Ittel, P. Mandel, and E. Delain Poly(ADP-ribose) polymerase auto-modification and interaction with DNA: electron microscopic visualization EMBO J. 2 1983 543 548
39. K. Hayashi, M. Tanaka, T. Shimada, M. Miwa, and T. Sugimura Size and shape of poly(ADP-ribose): examination by gel filtration, gel electrophoresis, and electron microscopy Biochem. Biophys. Res. Commun. 112 1983 102 107
40. J. Fahrer, R. Kranaster, M. Altmeyer, A. Marx, and A. Burkle Quantitative analysis of the binding affinity of poly(ADP-ribose) to specific binding proteins as a function of chain length Nucleic Acids Res. 35 2007 e143
41. C.C. Kiehlbauch, N. Aboul-Ela, E.L. Jacobson, D.P. Ringer, and M.K. Jacobson High resolution fractionation and characterization of ADP-ribose polymers Anal. Biochem. 208 1993 26 34 (Pubitemid 23086996)
42. M.F. Langelier, K.M. Servent, E.E. Rogers, and J.M. Pascal A third zinc-binding domain of human poly(ADP-ribose) polymerase-1 coordinates DNA-dependent enzyme activation J. Biol. Chem. 283 2008 4105 4114
43. F. Dantzer, J.C. Ame, V. Schreiber, J. Nakamura, J. Menissier-de Murcia, and G. de Murcia Poly(ADP-ribose) polymerase-1 activation during DNA damage and repair Methods Enzymol. 409 2006 493 510
44. P.L. Panzeter, B. Zweifel, and F.R. Althaus Fast protein liquid chromatographic purification of poly(ADP-ribose) polymerase and separation of ADP-ribose polymers J. Chromatogr. A 678 1994 35 40 (Pubitemid 24269911)
45. K. Wielckens, R. Bredehorst, P. Adamietz, and H. Hilz Protein-bound polymeric and monomeric ADP-ribose residues in hepatic tissues: comparative analyses using a new procedure for the quantification of poly(ADP-ribose) Eur. J. Biochem. 117 1981 69 74
46. D. Di Pierro, B. Tavazzi, C.F. Perno, M. Bartolini, E. Balestra, R. Calio, B. Giardina, and G. Lazzarino An ion-pairing high-performance liquid chromatographic method for the direct simultaneous determination of nucleotides, deoxynucleotides, nicotinic coenzymes, oxypurines, nucleosides, and bases in perchloric acid cell extracts Anal. Biochem. 231 1995 407 412
47. J.F. Rippmann, K. Damm, and A. Schnapp Functional characterization of the poly(ADP-ribose) polymerase activity of tankyrase 1, a potential regulator of telomere length J. Mol. Biol. 323 2002 217 224 (Pubitemid 35283687)
48. F. Simonin, L. Hofferer, P.L. Panzeter, S. Muller, G. de Murcia, and F.R. Althaus The carboxyl-terminal domain of human poly(ADP-ribose) polymerase: overproduction in Escherichia coli, large scale purification, and characterization J. Biol. Chem. 268 1993 13454 13461 (Pubitemid 23307771)
49. W. Lin, J.C. Ame, N. Aboul-Ela, E.L. Jacobson, and M.K. Jacobson Isolation and characterization of the cDNA encoding bovine poly(ADP-ribose) glycohydrolase J. Biol. Chem. 272 1997 11895 11901 (Pubitemid 27202761)
50. H. Naegeli, and F.R. Althaus Regulation of poly(ADP-ribose) polymerase: histone-specific adaptations of reaction products J. Biol. Chem. 266 1991 10596 10601 (Pubitemid 21906843)
51. R. Alvarez-Gonzalez, and M.K. Jacobson Quantification of poly(ADP-ribose) in vitro: determination of the ADP-ribose chain length and branching pattern Methods Mol. Biol. 780 2011 35 46
52. D. D'Amours, S. Desnoyers, I. D'Silva, and G.G. Poirier Poly(ADP-ribosyl)ation reactions in the regulation of nuclear functions Biochem. J. 342 1999 249 268 (Pubitemid 29425344)
53. A.M. Ferro, and B.M. Olivera Poly(ADP-ribosylation) in vitro: reaction parameters and enzyme mechanism J. Biol. Chem. 257 1982 7808 7813
54. M. Rouleau, A. Patel, M.J. Hendzel, S.H. Kaufmann, and G.G. Poirier PARP inhibition: PARP1 and beyond Nat. Rev. Cancer 10 2010 293 301
55. S.N. Gagnon, and S. Desnoyers Single amino acid substitution enhances bacterial expression of PARP-4D214A Mol. Cell. Biochem. 243 2003 15 22 (Pubitemid 36240547)
56. M. Ikejima, S. Noguchi, R. Yamashita, T. Ogura, T. Sugimura, D.M. Gill, and M. Miwa 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. 265 1990 21907 21913 (Pubitemid 120014241)
57. H. Giner, F. Simonin, G. de Murcia, and J. Menissier-de Murcia Overproduction and large-scale purification of the human poly(ADP-ribose) polymerase using a baculovirus expression system Gene 114 1992 279 283
58. K.E. Finch, C.E. Knezevic, A.C. Nottbohm, K.C. Partlow, and P.J. Hergenrother Selective small molecule inhibition of poly(ADP-ribose) glycohydrolase (PARG) ACS Chem. Biol. 7 2012 563 570
59. J.F. Haince, G.G. Poirier, and J.B. Kirkland Nonisotopic methods for determination of poly(ADP-ribose) levels and detection of poly(ADP-ribose) polymerase Curr. Protoc. Cell Biol. 2003 18.7.1 18.7.26
60. E.B. Affar, P.J. Duriez, R.G. Shah, E. Winstall, M. Germain, C. Boucher, S. Bourassa, J.B. Kirkland, and G.G. Poirier Immunological determination and size characterization of poly(ADP-ribose) synthesized in vitro and in vivo Biochim. Biophys. Acta 1428 1999 137 146 (Pubitemid 29352261)
61. R. Alvarez-Gonzalez, and M.K. Jacobson Characterization of polymers of adenosine diphosphate ribose generated in vitro and in vivo Biochemistry 26 1987 3218 3224 (Pubitemid 17087859)
62. M. Malanga, S. Bachmann, P.L. Panzeter, B. Zweifel, and F.R. Althaus Poly(ADP-ribose) quantification at the femtomole level in mammalian cells Anal. Biochem. 228 1995 245 251
63. P.L. Panzeter, and F.R. Althaus High resolution size analysis of ADP-ribose polymers using modified DNA sequencing gels Nucleic Acids Res. 18 1990 2194 (Pubitemid 20171569)