Serine ADP-ribosylation reversal by the hydrolase ARH3

eLife

Volumn 6, Issue , 2017, Pages

  Fontana, Pietro ^a   Bonfiglio, Juan José ^b   Palazzo, Luca ^a   Bartlett, Edward ^a   Matic, Ivan ^b   Ahel, Ivan ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b MAX PLANCK INSTITUTE FOR BIOLOGY OF AGEING   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSE; AMINO ACID; ARGININE; CELL EXTRACT; GLYCOSIDASE; HISTONE; HYDROLASE; POLYCLONAL ANTIBODY; SERINE PROTEINASE; ADPRHL2 PROTEIN, HUMAN; CARRIER PROTEIN; HPF1 PROTEIN, HUMAN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; NUCLEAR PROTEIN; PARP1 PROTEIN, HUMAN; PARP2 PROTEIN, HUMAN; PROTEOME; SERINE;

ADENOSINE DIPHOSPHATE RIBOSYLATION; ARTICLE; DNA DAMAGE; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME SPECIFICITY; GENETIC COMPLEMENTATION; HYDROLYSIS; ISOTOPE LABELING; MASS SPECTROMETRY; NONHUMAN; PLASMID; PROTEIN EXPRESSION; PROTEIN PROCESSING; PROTEIN PURIFICATION; SCREENING; WESTERN BLOTTING; HUMAN; METABOLISM; PROTEOMICS; TUMOR CELL LINE;

ADP-RIBOSYLATION; CARRIER PROTEINS; CELL LINE, TUMOR; GLYCOSIDE HYDROLASES; HISTONES; HUMANS; NUCLEAR PROTEINS; POLY (ADP-RIBOSE) POLYMERASE-1; POLY(ADP-RIBOSE) POLYMERASES; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOME; PROTEOMICS; SERINE;

EID: 85029210945     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.28533     Document Type: Article

References (59)

1. Adriouch S, Bannas P, Schwarz N, Fliegert R, Guse AH, Seman M, Haag F, Koch-Nolte F. ADP-ribosylation at R125 gates the P2X7 ion channel by presenting a covalent ligand to its nucleotide binding site. The FASEB Journal. 2008;22:861-869. doi: 10.1096/fj.07-9294com.
2. Ahel D, Horejsí Z, Wiechens N, Polo SE, Garcia-Wilson E, Ahel I, Flynn H, Skehel M, West SC, Jackson SP, Owen-Hughes T, Boulton SJ. Poly(ADP-ribose)-dependent regulation of DNA repair by the chromatin remodeling enzyme ALC1. Science.2009;325:1240-1243. doi: 10.1126/science.1177321.
3. Barkauskaite E, Brassington A, Tan ES, Warwicker J, Dunstan MS, Banos B, Lafite P, Ahel M, Mitchison TJ, Ahel I, Leys D. Visualization of poly(ADP-ribose) bound to PARG reveals inherent balance between exo-and endo-glycohydrolase activities. Nature Communications. 2013;4:2164 doi: 10.1038/ncomms3164.
4. Barkauskaite E, Jankevicius G, Ahel I. Structures and mechanisms of enzymes employed in the synthesis and degradation of PARP-Dependent protein ADP-Ribosylation. Molecular Cell. 2015;58:935-946. doi: 10.1016/j.molcel.2015.05.007.
5. Bilan V, Leutert M, Nanni P, Panse C, Hottiger MO. Combining higher-energy collision dissociation and electron-transfer/higher-energy collision dissociation fragmentation in a product-dependent manner confidently assigns proteomewide ADP-ribose acceptor sites. Analytical Chemistry. 2017;89:1523-1530. doi: 10.1021/acs.analchem.6b03365.
6. Bonfiglio JJ, Fontana P, Zhang Q, Colby T, Gibbs-Seymour I, Atanassov I, Bartlett E, Zaja R, Ahel I, Matic I. Serine ADP-Ribosylation depends on HPF1. Molecular Cell.2017a;65:932-940. doi: 10.1016/j.molcel.2017.01.003.
7. Bonfiglio JJ, Colby T, Matic I. Mass spectrometry for serine ADP-ribosylation? Think o-glycosylation! Nucleic Acids Research. 2017b:6259-6264. doi: 10.1093/nar/gkx446.
8. Bütepage M, Eckei L, Verheugd P, Lüscher B. Intracellular Mono-ADP-Ribosylation in signaling and disease. Cells. 2015;4:569-595. doi: 10.3390/cells4040569.
9. Cox J, Mann M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nature Biotechnology. 2008;26:1367-1372. doi: 10.1038/nbt.1511.
10. D’Amours D, Desnoyers S, D'Silva I, Poirier GG. Poly(ADP-ribosyl)ation reactions in the regulation of nuclear functions. Biochemical Journal. 1999;342 (Pt 2):249-268. doi: 10.1042/bj3420249.
11. Daniels CM, Ong SE, Leung AK. The Promise of Proteomics for the study of ADP-Ribosylation. Molecular Cell. 2015;58:911-924. doi: 10.1016/j.molcel.2015.06.012.
12. Dunstan MS, Barkauskaite E, Lafite P, Knezevic CE, Brassington A, Ahel M, Hergenrother PJ, Leys D, Ahel I. Structure and mechanism of a canonical poly(ADP-ribose) glycohydrolase. Nature Communications. 2012;3:878 doi: 10.1038/ncomms1889.
13. Feijs KL, Forst AH, Verheugd P, Lüscher B. Macrodomain-containing proteins: regulating new intracellular functions of mono(ADP-ribosyl)ation. Nature Reviews Molecular Cell Biology. 2013;14:542-451. doi: 10.1038/nrm3623.
14. Gagné JP, Ethier C, Defoy D, Bourassa S, Langelier MF, Riccio AA, Pascal JM, Moon KM, Foster LJ, Ning Z, Figeys D, Droit A, Poirier GG. Quantitative site-specific ADP-ribosylation profiling of DNA-dependent PARPs. DNA Repair. 2015;30:68-79. doi: 10.1016/j.dnarep.2015.02.004.
15. Geiger T, Wisniewski JR, Cox J, Zanivan S, Kruger M, Ishihama Y, Mann M. Use of stable isotope labeling by amino acids in cell culture as a spike-in standard in quantitative proteomics. Nature Protocols. 2011;6:147-157. doi: 10.1038/nprot.2010.192.
16. Gibbs-Seymour I, Fontana P, Rack JG, Ahel I. HPF1/C4orf27 is a PARP-1-Interacting protein that regulates PARP-1 ADP-Ribosylation activity. Molecular Cell.2016;62:432-442. doi: 10.1016/j.molcel.2016.03.008.
17. Gibson BA, Kraus WL. New insights into the molecular and cellular functions of poly(ADP-ribose) and PARPs. Nature Reviews Molecular Cell Biology. 2012;13:411-424. doi: 10.1038/nrm3376.
18. Gibson BA, Zhang Y, Jiang H, Hussey KM, Shrimp JH, Lin H, Schwede F, Yu Y, Kraus WL. Chemical genetic discovery of PARP targets reveals a role for PARP-1 in transcription elongation. Science. 2016;353:45-50. doi: 10.1126/science.aaf7865.
19. Glowacki G, Braren R, Firner K, Nissen M, Kühl M, Reche P, Bazan F, Cetkovic-Cvrlje M, Leiter E, Haag F, Koch-Nolte F. The family of toxin-related ecto-ADP-ribosyltransferases in humans and the mouse. Protein Science. 2002;11:1657-1670. doi: 10.1110/ps.0200602.
20. Gupte R, Liu Z, Kraus WL. PARPs and ADP-ribosylation: recent advances linking molecular functions to biological outcomes. Genes & Development. 2017;31:101-126. doi: 10.1101/gad.291518.116.
21. Hakmé A, Wong HK, Dantzer F, Schreiber V. The expanding field of poly(ADP-ribosyl)ation reactions. 'Protein Modifications: Beyond the Usual Suspects' Review Series. EMBO Reports. 2008;9:1094-1100. doi: 10.1038/embor.2008.191.
22. Hanai S, Kanai M, Ohashi S, Okamoto K, Yamada M, Takahashi H, Miwa M. Loss of poly(ADP-ribose) glycohydrolase causes progressive neurodegeneration in Drosophila Melanogaster. PNAS. 2004;101:82-86. doi: 10.1073/pnas.2237114100.
23. Hassa PO, Haenni SS, Elser M, Hottiger MO. Nuclear ADP-ribosylation reactions in mammalian cells: where are we today and where are we going? Microbiology and Molecular Biology Reviews. 2006;70:789-829. doi: 10.1128/MMBR.00040-05.
24. Hatakeyama K, Nemoto Y, Ueda K, Hayaishi O. Purification and characterization of poly(ADP-ribose) glycohydrolase. Different modes of action on large and small poly(ADP-ribose) The Journal of Biological Chemistry. 1986;261:14902-14911.
25. Hottiger MO. Nuclear ADP-Ribosylation and its role in chromatin plasticity, cell differentiation, and Epigenetics. Annual Review of Biochemistry. 2015;84:227-263. doi: 10.1146/annurev-biochem-060614-034506.
26. Jankevicius G, Hassler M, Golia B, Rybin V, Zacharias M, Timinszky G, Ladurner AG. A family of macrodomain proteins reverses cellular mono-ADP-ribosylation. Nature Structural & Molecular Biology. 2013;20:508-514. doi: 10.1038/nsmb.2523.
27. Jankevicius G, Ariza A, Ahel M, Ahel I. The Toxin-Antitoxin System DarTG catalyzes reversible ADP-Ribosylation of DNA. Molecular Cell. 2016;64:1109-1116. doi: 10.1016/j.molcel.2016.11.014.
28. Kernstock S, Koch-Nolte F, Mueller-Dieckmann J, Weiss MS, Mueller-Dieckmann C. Cloning, expression, purification, crystallization and preliminary X-ray diffraction analysis of human ARH3, the first eukaryotic protein-ADP-ribosylhydrolase. Acta Crystallographica Section F Structural Biology and Crystallization Communications.2006;62:224-227. doi: 10.1107/S1744309106003435.
29. Kleine H, Poreba E, Lesniewicz K, Hassa PO, Hottiger MO, Litchfield DW, Shilton BH, Lüscher B. Substrate-assisted catalysis by PARP10 limits its activity to mono-ADP-ribosylation. Molecular Cell. 2008;32:57-69. doi: 10.1016/j.molcel.2008.08.009.
30. Lambrecht MJ, Brichacek M, Barkauskaite E, Ariza A, Ahel I, Hergenrother PJ. Synthesis of dimeric ADP-ribose and its structure with human poly(ADP-ribose) glycohydrolase. Journal of the American Chemical Society. 2015;137:3558-3564. doi: 10.1021/ja512528p.
31. Langelier MF, Planck JL, Servent KM, Pascal JM. Purification of human PARP-1 and PARP-1 domains from Escherichia coli for structural and biochemical analysis. Methods in Molecular Biology. 2011;780:209-226. doi: 10.1007/978-1-61779-270-0_13.
32. Langelier MF, Planck JL, Roy S, Pascal JM. Structural basis for DNA damage-dependent poly(ADP-ribosyl)ation by human PARP-1. Science. 2012;336:728-732. doi: 10.1126/science.1216338.
33. Leidecker O, Bonfiglio JJ, Colby T, Zhang Q, Atanassov I, Zaja R, Palazzo L, Stockum A, Ahel I, Matic I. Serine is a new target residue for endogenous ADP-ribosylation on histones. Nature Chemical Biology. 2016;12:998-1000. doi: 10.1038/nchembio.2180.
34. Lin W, Amé JC, Aboul-Ela N, Jacobson EL, Jacobson MK. Isolation and characterization of the cDNA encoding bovine poly(ADP-ribose) glycohydrolase. Journal of Biological Chemistry. 1997;272:11895-11901. doi: 10.1074/jbc.272.18.11895.
35. Martello R, Leutert M, Jungmichel S, Bilan V, Larsen SC, Young C, Hottiger MO, Nielsen ML. Proteome-wide identification of the endogenous ADP-ribosylome of mammalian cells and tissue. Nature Communications. 2016;7:12917 doi: 10.1038/ncomms12917.
36. Mashimo M, Kato J, Moss J. ADP-ribosyl-acceptor hydrolase 3 regulates poly (ADP-ribose) degradation and cell death during oxidative stress. PNAS. 2013;110:18964-18969. doi: 10.1073/pnas.1312783110.
37. Mashimo M, Kato J, Moss J. Structure and function of the ARH family of ADP-ribosyl-acceptor hydrolases. DNA Repair. 2014;23:88-94. doi: 10.1016/j.dnarep.2014.03.005.
38. Mortusewicz O, Amé JC, Schreiber V, Leonhardt H. Feedback-regulated poly(ADP-ribosyl)ation by PARP-1 is required for rapid response to DNA damage in living cells. Nucleic Acids Research. 2007;35:7665-7675. doi: 10.1093/nar/gkm933.
39. Mueller-Dieckmann C, Scheuermann T, Wursthorn K, Schröder J, Haag F, Schulz GE, Koch-Nolte F. Expression, purification, crystallization and preliminary X-ray analysis of rat ecto-ADP-ribosyltransferase 2 (ART2.2) Acta Crystallographica Section D Biological Crystallography. 2002;58:1211-1213. doi: 10.1107/S090744490200700X.
40. Mueller-Dieckmann C, Kernstock S, Lisurek M, von Kries JP, Haag F, Weiss MS, Koch-Nolte F. The structure of human ADP-ribosylhydrolase 3 (ARH3) provides insights into the reversibility of protein ADP-ribosylation. PNAS. 2006;103:15026-15031. doi: 10.1073/pnas.0606762103.
41. Niere M, Mashimo M, Agledal L, Dölle C, Kasamatsu A, Kato J, Moss J, Ziegler M. ADP-ribosylhydrolase 3 (ARH3), not poly(ADP-ribose) glycohydrolase (PARG) isoforms, is responsible for degradation of mitochondrial matrix-associated poly(ADP-ribose) Journal of Biological Chemistry. 2012;287:16088-16102. doi: 10.1074/jbc.M112.349183.
42. Oka S, Kato J, Moss J. Identification and characterization of a mammalian 39-kDa poly(ADP-ribose) glycohydrolase. Journal of Biological Chemistry. 2006;281:705-713. doi: 10.1074/jbc.M510290200.
43. Ong SE, Blagoev B, Kratchmarova I, Kristensen DB, Steen H, Pandey A, Mann M. Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Molecular & Cellular Proteomics. 2002;1:376-386. doi: 10.1074/mcp.M200025-MCP200.
44. Ono T, Kasamatsu A, Oka S, Moss J. The 39-kDa poly(ADP-ribose) glycohydrolase ARH3 hydrolyzes O-acetyl-ADP-ribose, a product of the Sir2 family of acetyl-histone deacetylases. PNAS. 2006;103:16687-16691. doi: 10.1073/pnas.0607911103.
45. Palazzo L, Thomas B, Jemth AS, Colby T, Leidecker O, Feijs KL, Zaja R, Loseva O, Puigvert JC, Matic I, Helleday T, Ahel I. Processing of protein ADP-ribosylation by nudix hydrolases. Biochemical Journal. 2015;468:293-301. doi: 10.1042/BJ20141554.
46. Palazzo L, Daniels CM, Nettleship JE, Rahman N, McPherson RL, Ong SE, Kato K, Nureki O, Leung AK, Ahel I. ENPP1 processes protein ADP-ribosylation in vitro. The FEBS Journal. 2016;283:3371-3388. doi: 10.1111/febs.13811.
47. Palazzo L, Mikoč A, Ahel I. ADP-ribosylation: new facets of an ancient modification. The FEBS Journal. 2017;23:febs.14078 doi: 10.1111/febs.14078.
48. Perina D, Mikoč A, Ahel J, Ćetković H, Žaja R, Ahel I. Distribution of protein poly(ADP-ribosyl)ation systems across all domains of life. DNA Repair. 2014;23:4-16. doi: 10.1016/j.dnarep.2014.05.003.
49. Rack JG, Morra R, Barkauskaite E, Kraehenbuehl R, Ariza A, Qu Y, Ortmayer M, Leidecker O, Cameron DR, Matic I, Peleg AY, Leys D, Traven A, Ahel I. Identification of a class of protein ADP-Ribosylating sirtuins in microbial pathogens. Molecular Cell. 2015;59:309-320. doi: 10.1016/j.molcel.2015.06.013.
50. Rack JG, Perina D, Ahel I. Macrodomains: Structure, function, evolution, and Catalytic Activities. Annual Review of Biochemistry. 2016;85:431-454. doi: 10.1146/annurev-biochem-060815-014935.
51. Rappsilber J, Ishihama Y, Mann M. Stop and go extraction tips for matrix-assisted laser desorption/ionization, Nanoelectrospray, and LC/MS sample pretreatment in proteomics. Analytical Chemistry. 2003;75:663-670. doi: 10.1021/ac026117i.
52. Rosenthal F, Feijs KL, Frugier E, Bonalli M, Forst AH, Imhof R, Winkler HC, Fischer D, Caflisch A, Hassa PO, Lüscher B, Hottiger MO. Macrodomain-containing proteins are new mono-ADP-ribosylhydrolases. Nature Structural & Molecular Biology.2013;20:502-507. doi: 10.1038/nsmb.2521.
53. Rouleau M, Patel A, Hendzel MJ, Kaufmann SH, Poirier GG. PARP inhibition: PARP1 and beyond. Nature Reviews Cancer. 2010;10:293-301. doi: 10.1038/nrc2812.
54. Schreiber V, Dantzer F, Ame JC, de Murcia G. Poly(ADP-ribose): novel functions for an old molecule. Nature Reviews Molecular Cell Biology. 2006;7:517-528. doi: 10.1038/nrm1963.
55. Sharifi R, Morra R, Appel CD, Tallis M, Chioza B, Jankevicius G, Simpson MA, Matic I, Ozkan E, Golia B, Schellenberg MJ, Weston R, Williams JG, Rossi MN, Galehdari H, Krahn J, Wan A, Trembath RC, Crosby AH, Ahel D, Hay R, Ladurner AG, Timinszky G, Williams RS, Ahel I. Deficiency of terminal ADP-ribose protein glycohydrolase TARG1/C6orf130 in neurodegenerative disease. The EMBO Journal.2013;32:1225-1237. doi: 10.1038/emboj.2013.51.
56. Slade D, Dunstan MS, Barkauskaite E, Weston R, Lafite P, Dixon N, Ahel M, Leys D, Ahel I. The structure and catalytic mechanism of a poly(ADP-ribose) glycohydrolase. Nature. 2011;477:616-620. doi: 10.1038/nature10404.
57. Tallis M, Morra R, Barkauskaite E, Ahel I. Poly(ADP-ribosyl)ation in regulation of chromatin structure and the DNA damage response. Chromosoma. 2014;123:79-90. doi: 10.1007/s00412-013-0442-9.
58. Timinszky G, Till S, Hassa PO, Hothorn M, Kustatscher G, Nijmeijer B, Colombelli J, Altmeyer M, Stelzer EH, Scheffzek K, Hottiger MO, Ladurner AG. A macrodomain-containing histone rearranges chromatin upon sensing PARP1 activation. Nature Structural & Molecular Biology. 2009;16:923-929. doi: 10.1038/nsmb.1664.
59. Vyas S, Matic I, Uchima L, Rood J, Zaja R, Hay RT, Ahel I, Chang P. Family-wide analysis of poly(ADP-ribose) polymerase activity. Nature Communications. 2014;5:4426 doi: 10.1038/ncomms5426.