Identification of candidate substrates for poly(ADP-ribose) polymerase-2 (PARP2) in the absence of DNA damage using high-density protein microarrays

FEBS Journal

Volumn 278, Issue 19, 2011, Pages 3676-3687

  Troiani, Sonia ^a   Lupi, Rosita ^a   Perego, Rita ^a   Re Depaolini, Stefania ^a   Thieffine, Sandrine ^a   Bosotti, Roberta ^a   Rusconi, Luisa ^a  

^a NERVIANO MEDICAL SCIENCES   (Italy)

Author keywords

ADP ribosylation; biotinylated NAD; DNA damage; PARP2; protein microarray

Indexed keywords

FK 506 BINDING PROTEIN; FK 506 BINDING PROTEIN 3; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 2; PROTEIN SH3; RECOMBINANT ENZYME; RNA HELICASE; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 4; UNCLASSIFIED DRUG;

ADENOSINE DIPHOSPHATE RIBOSYLATION; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DNA DAMAGE; DNA STRAND BREAKAGE; ENZYME ACTIVATION; ENZYME ASSAY; ENZYME SUBSTRATE COMPLEX; FUNCTIONAL PROTEOMICS; HIGH DENSITY PROTEIN MICROARRAY; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROCESS DEVELOPMENT; PROTEIN FUNCTION; PROTEIN MICROARRAY; SCORING SYSTEM; SENSITIVITY AND SPECIFICITY; TRANSLATION INITIATION; TRANSLATION REGULATION;

ADENOSINE DIPHOSPHATE; CELL CYCLE PROTEINS; DNA DAMAGE; HUMANS; NERVE TISSUE PROTEINS; NUCLEAR PROTEINS; POLY(ADP-RIBOSE) POLYMERASES; PROTEIN ARRAY ANALYSIS; TACROLIMUS BINDING PROTEINS;

EID: 80052961045     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2011.08286.x     Document Type: Article

References (60)

1. Altmeyer M, Messner S, Hassa PO, Fey M, &, Hottiger MO, (2009) Molecular mechanism of poly(ADP-ribosyl)ation by PARP1 and identification of lysine residues as ADP-ribose acceptor sites. Nucleic Acids Res 37, 3723-3738.
2. Corda D, &, Di Girolamo M, (2003) Functional aspects of protein mono-ADPribosylation. EMBO J 22, 1953-1958.
3. Di Girolamo M, Dani N, Stilla A, &, Corda D, (2005) Physiological relevance of the endogenous mono(ADP-ribosyl)ation of cellular proteins. FEBS J 272, 4565-4575. (Pubitemid 41366982)
4. Schreiber V, Dantzer F, Amé J-C, &, de Murcia G, (2006) Poly(ADP-ribose): novel functions for an old molecule. Nat Rev Mol Cell Biol 7, 517-528. (Pubitemid 44036457)
5. Amé J-C, Spenlehauer C, &, de Murcia G, (2004) The PARP superfamily. Bioessays 26, 882-893. (Pubitemid 39128102)
6. Otto H, Reche PA, Bazan F, Dittmar K, Haag F, &, Koch-Nolte F, (2005) In silico characterization of the family of PARP-like poly(ADP-ribosyl) transferases (pARTs). BMC Genomics 6, 139-161.
7. Kleine H, Poreba E, Lesniewicz K, Hassa PO, Hottiger MO, Litchfield DW, Shilton BH, &, Lüscher B, (2008) Substrate-assisted catalysis by PARP10 limits its activity to mono-ADP-ribosylation. Mol Cell 32, 57-69.
8. Hottiger MO, Hassa PO, Lüscher B, Schüler H, &, Koch-Nolte F, (2010) Toward a unified nomenclature for mammalian ADP-ribosyltransferases. Trends Biochem Sci 35, 208-219.
9. Boehler C, Gauthier LR, Mortusewicz O, Biard DS, Saliou J-M, Bresson A, Sanglier-Cianferani S, Smith S, Schreiber V, Boussin F, et al. (2011) Poly(ADP-ribose) polymerase 3 (PARP3), a newcomer in cellular response to DNA damage and mitotic progression. Proc Natl Acad Sci USA 108, 2783-2788.
10. Rulten SL, Fisher AE, Robert I, Zuma MC, Rouleau M, Ju L, Poirier G, Reina-San-Martin B, &, Caldecott KW, (2011) PARP-3 and APLF function together to accelerate nonhomologous end-joining. Mol Cell 41, 33-45.
11. Dantzer F, de La Rubia G, Ménissier-De Murcia J, Hostomsky Z, de Murcia G, &, Schreiber V, (2000) Base excision repair is impaired in mammalian cells lacking Poly(ADP-ribose) polymerase-1. Biochemistry 39, 7559-7569. (Pubitemid 30422075)
12. Schreiber V, Amé JC, Dollé P, Schultz I, Rinaldi B, Fraulob V, Ménissier-de Murcia J, &, 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. (Pubitemid 34967289)
13. Kickhoefer VA, Silva AC, Kedersha NL, Inman EM, Ruland C, Streuli M, &, Rome LH, (1999) The 193-kD vault protein, VPARP, is a novel poly(ADP-ribose) polymerase. J Cell Biol 146, 917-928. (Pubitemid 29430436)
14. Aravind L, (2001) The WWE domain: a common interaction module in protein ubiquitination and ADP ribosylation. Trends Biochem Sci 26, 273-275. (Pubitemid 32436369)
15. Yélamos J, Schreiber V, &, Dantzer F, (2008) Toward specific functions of poly(ADP-ribose) polymerase-2. Trends Mol Med 14, 169-178.
16. Isabelle M, Moreel X, Gagné J-P, Rouleau M, Ethier C, Gagné P, Hendzel MJ, &, Poirier GG, (2010) Investigation of PARP-1, PARP-2 and PARG interactomes by affinity-purification mass spectrometry. Proteome Sci 8, 22.
17. Dantzer F, Mark M, Quenet D, Scerthan H, Huber A, Liebe B, Monaco L, Chiche Portiche A, Sassone-Corsi P, de Murcia G, et al. (2006) Poly(ADP-ribose) polymerase-2 contributes to the fidelity of male meiosis I and spermiogenesis. Proc Natl Acad Sci USA 103, 14854-14859. (Pubitemid 44527818)
18. Bai P, Houten SM, Huber A, Schreiber V, Watanabe M, Kiss B, de Murcia G, Auwerx J, &, Ménissier-de Murcia J, (2007) Peroxisome proliferator-activated receptor (PPAR)-2 controls adipocyte differentiation and adipose tissue function through the regulation of the activity of the Retinoid X Receptor/PPARγ heterodimer. J Biol Chem 282, 37738-37746.
19. Yélamos J, Monreal Y, Saenz L, Aguado E, Schreiber V, Mota R, Fuente R, Minguela A, Parrilla P, de Murcia J, et al. (2006) PARP-2 deficiency affects the survival of CDC4+CD8+ double- positive thymocytes. EMBO J 25, 4350-4360. (Pubitemid 44435232)
20. 2+, histones H1 and H3, and ATP. Biochemistry 43, 210-216. (Pubitemid 38055957)
21. Kalousek F, Darigo MD, &, Rosenberg LE, (1980) Isolation and characterization of propionyl-CoA carboxylase from normal human liver. Evidence for a protomeric tetramer of non identical subunits. J Biol Chem 255, 60-65. (Pubitemid 10146029)
22. Gravel RA, Lam KF, Mahuran D, &, Kronis A, (1980) Purification of human liver propionyl-CoA carboxylase by carbon tetrachloride extraction and monomeric avidin affinity chromatography. Arch Biochem Biophys 201, 669-673.
23. Aguiar RCT, Takeyama K, He C, Kreinbrink K, &, Shipp MA, (2005) B-aggressive lymphoma family proteins have unique domains that modulate transcription and exhibit poly(ADP-ribose) polymerase activity. J Biol Chem 280, 33756-33765. (Pubitemid 41443094)
24. Kraus WL, (2009) New functions for an ancient domain. Nat Struct Mol Biol 16, 904-907.
25. Ahel I, Ahel D, Matsusaka T, Clark AJ, Pines J, Boulton SJ, &, West SC, (2008) Poly(ADP-ribose)-binding zinc finger motifs in DNA repair/checkpoint proteins. Nature 451, 81-85.
26. Gagné J-P, Isabelle M, Sin Lo K, Bourassa S, Hendzel MJ, Dawson VL, Dawson TM, &, Poirier GG, (2008) Proteome-wide identification of poly(ADP-ribose) binding proteins and poy(ADP-ribose)-associated protein complexes. Nucleic Acids Res 36, 6959-6976.
27. Krishnakumar R, &, Kraus WL, (2010) The PARP side of the nucleus: molecular actions, physiological outcomes, and clinical targets. Mol Cell 39, 8-24.
28. Hunter S, Apweiler R, Attwood TK, Bairoch A, Bateman A, Binns D, Bork P, Das U, Daugherty L, Duquenne L, et al. (2009) InterPro: the integrative protein signature database. Nucleic Acids Res 37: D211-D215.
29. Rulten SL, Cortes-Ledesma F, Guo L, Iles NJ, &, Caldecott KW, (2008) APLF (C2orf13) is a novel component of poly(ADP-ribose) signaling in mammalian cells. Mol Cell Biol 28, 4620-4628. (Pubitemid 351977759)
30. Kanno S, Kuzuoka H, Sasao S, Hong Z, Lan L, Nakajima S, &, Yasui A, (2007) A novel human AP endonuclease with conserved zinc-finger-like motifs involved in DNA strand break responses. EMBO J 26, 2094-2103. (Pubitemid 46625798)
31. Meder VS, Boeglin M, de Murcia G, &, Schreiber V, (2005) PARP-1 and PARP-2 interact with nucleophosmin/B23 and accumulate in transcriptionally active nucleoli. J Cell Sci 118, 211-222. (Pubitemid 40277117)
32. Saxena A, Wong LH, Kalitsis P, Earle E, Shaffer LG, &, Choo KH, (2002) Poly(ADP-ribose) polymerase 2 localizes to mammalian active centromeres and interacts with PARP-1, Cenpa, Cenpb and Bub3, but not Cenpc. Hum Mol Genet 11, 2319-2329.
33. Thomas PD, Campbell MJ, Kejariwal A, Mi H, Karlak B, Daverman R, Diemer K, Muruganujan A, &, Narechania A, (2003) PANTHER: a library of protein families and subfamilies indexed by function. Genome Res 13, 2129-2141. (Pubitemid 37161770)
34. Anderson NL, &, Anderson NG, (2002) The human plasma proteome: history, character, and diagnostic prospects. Mol Cell Proteomics 1, 845-867.
35. Tao Z, Gao P, &, Liu H-w, (2009) Studies of expression of human poly(ADP-ribose) polymerase-1 in Saccharomyces cerevisiae and identification of PARP-1 substrates by yeast proteome microarray screening. Biochemistry 48, 11745-11754.
36. Hanus J, Kalinowska-Herok M, &, Widlak P, (2008) The major apoptotic endonuclease DFF40/CAD is a deoxyribose-specific and double-strand-specific enzyme. Apoptosis 13, 377-382.
37. Höck J, Weinmann L, Ender C, Rüdel S, Kremmer E, Raabe M, Urlaub H, &, Meister G, (2007) Proteomic and functional analysis of Argonaute-containing mRNA-protein complexes in human cells. EMBO Rep 8, 1052-1060. (Pubitemid 350042341)
38. Galat A, Lane WS, Standaert RF, &, Schreiber SL, (1992) A rapamycin-selective 25-kDa immunophilin. Biochemistry 31, 2427-2434.
39. Yang WM, Yao YL, &, Seto E, (2001) The FK506-binding protein 25 functionally associates with histone deacetylases and with transcription factor YY1. EMBO J 20, 4814-4825. (Pubitemid 32848633)
40. Ahn J, Murphy M, Kratowicz S, Wang A, Levine AJ, &, George DL, (1999) Down-regulation of the stathmin/Op18 and FKBP25 genes following p53 induction. Oncogene 18, 5954-5958. (Pubitemid 29520452)
41. Ochocka AM, Kampanis P, Nicol S, Allende-Vega N, Cox M, Marcar L, Milne D, Fuller-Pace F, &, Meek D, (2009) FKBP25, a novel regulator of the p53 pathway, induces the degradation of MDM2 and activation of p53. FEBS Lett 583, 621-626.
42. Dephoure N, Zhou C, Villen J, Beausoleil SA, Bakalarski CE, Elledge SJ, &, Gygi SP, (2008) A quantitative atlas of mitotic phosphorylation. Proc Natl Acad Sci USA 105, 10762-10767.
43. Choudhary C, Kumar C, Gnad F, Nielsen ML, Rehman M, Walther T, Olsen JV, &, Mann M, (2009) Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 325, 834-840.
44. Jiang H, Kim JH, Frizzell KM, Kraus WL, &, Lin H, (2010) Clickable NAD analogues for labelling substrate proteins of poly(ADP-ribose) polymerases. J Am Chem Soc 132, 9363-9372.
45. Suzuki H, Kawai J, Taga C, Yaoi T, Hara A, Hirose K, Hayashizaki Y, &, Watanabe S, (1996) Stac, a novel neuron-specific protein with cysteine-rich and SH3 domains. Biochem Biophys Res Commun 229, 902-909. (Pubitemid 27035815)
46. Satoh J, Nanri Y, &, Yamamura T, (2006) Rapid identification of 14-3-3-binding proteins by protein microarray analysis. J Neurosci Methods 152, 278-288. (Pubitemid 43343500)
47. Mitra S, Mazumder Indra D, Bhattacharya N, Singh RK, Basu PS, Mondal RK, Roy A, Zabarovsky ER, Roychoudhury S, &, Panda CK, (2010) RBSP3 is frequently altered in premalignant cervical lesions: clinical and prognostic significance. Genes Chromosom Cancer 49, 155-170.
48. Kofler J, Otsuka T, Zhang Z, Nopppens R, Grafe MR, Koh DW, Dawson VL, Ménissiewr de Murcia J, Hurn PD, &, Traystman RJ, (2006) Differential effect of PARP-2 deletion on brain injury after focal and global cerebral ischemia. J Cereb Blood Flow Metab 26, 135-141. (Pubitemid 41818077)
49. Moroni F, Formentini L, Gerace E, Camaioni E, Pellegrini-Giampietro DE, Chiarugi A, &, Pellicciari R, (2009) Selective PARP-2 inhibitors increase apoptosis in hippocampal slices but protect cortical cells in models of post-ischaemic brain damage. Br J Pharmacol 157, 854-862.
50. Schnack C, Hengerer B, &, Gillardon F, (2008) Identification of novel substrates for Cdk5 and new targets for Cdk5 inhibitors using high-density protein microarrays. Proteomics 8, 1980-1986. (Pubitemid 351775778)
51. Zhu J, Liao G, Shan L, Zhang J, Chen M-R, Hayward GS, Hayward SD, Desai P, &, Zhu H, (2009) Protein array identification of substrates of the Epstein-Barr virus protein kinase BGLF4. J Virol 83, 5219-5231.
52. Foster MW, Forrester MT, &, Stamler JS, (2009) A protein microarray-based analysis of S-nitrosylation. Proc Natl Acad Sci USA 106, 18948-18953.
53. Gupta R, Kus B, Fladd C, Wasmuth J, Tonikian R, Sidhu S, Krogan NJ, Parkinson J, &, Rotin D, (2007) Ubiquitination screen using protein microarrays for comprehensive identification of Rsp5 substrates in yeast. Mol Syst Biol 3, 116.
54. Lu J-y, Lin Y-y, Qian J, Tao S-c, Zhu J, Pickart C, &, Zhu H, (2008) Functional dissection of a HECT ubiquitin E3 ligase. Mol Cell Proteomics 7, 35-45. (Pubitemid 351248232)
55. Persaud A, Alberts P, Amsen EM, Xiong X, Wasmuth J, Saadon Z, Fladd C, Parkinson J, &, Rotin D, (2009) Comparison of substrate specificity of the ubiquitin ligases Nedd4 and Nedd4-2 using proteome arrrays. Mol Syst Biol 5, 333.
56. Fenner BJ, Scannell M, &, Prehn JHM, (2010) Expanding the substantial interactome of NEMO using protein microarrays. PLoS ONE 5, e8799.
57. del Rincõn SV, Rogers J, Widschwendter M, Sun D, Sieburg HB, &, Spruck C, (2010) Development and validation of a method for profiling post-translational modification activities using protein microarrays. PLoS ONE 5, e11332.
58. Montagnoli A, Bosotti R, Villa F, Rialland M, Brotherton D, Mercurio C, Berthelsen J, &, Santocanale C, (2002) Drf1, a novel regulatory subunit for human Cdc7 kinase. EMBO J 21, 3171-3181. (Pubitemid 34670400)
59. Studier FW, (2005) Protein production by auto-induction in high density shaking cultures. Protein Expr Purif 41, 207-234.
60. Rosa JL, Pérez JX, Ventura F, Tauler A, Gil J, Shimoyama M, Pilkis SJ, &, Bartrons R, (1995) Role of the N-terminal region in covalent modification of 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase: comparison of phosphorylation and ADP-ribosylation. Biochem J 309, 119-125.