Proteome-wide Identification of Poly(ADP-ribose) Binding Proteins and Poly(ADP-ribose)-associated Protein Complexes

Overview

Journal Nucleic Acids Res

Publisher Oxford University Press

Specialty Biochemistry

Date 2008 Nov 5

PMID 18981049

Citations 221

Authors

Jean-Philippe Gagne

Maxim Isabelle

Ken Sin Lo

Sylvie Bourassa

Michael J Hendzel

Valina L Dawson

Ted M Dawson

Guy G Poirier

Affiliations

Soon will be listed here.

Abstract

Poly(ADP-ribose) (pADPr) is a polymer assembled from the enzymatic polymerization of the ADP-ribosyl moiety of NAD by poly(ADP-ribose) polymerases (PARPs). The dynamic turnover of pADPr within the cell is essential for a number of cellular processes including progression through the cell cycle, DNA repair and the maintenance of genomic integrity, and apoptosis. In spite of the considerable advances in the knowledge of the physiological conditions modulated by poly(ADP-ribosyl)ation reactions, and notwithstanding the fact that pADPr can play a role of mediator in a wide spectrum of biological processes, few pADPr binding proteins have been identified so far. In this study, refined in silico prediction of pADPr binding proteins and large-scale mass spectrometry-based proteome analysis of pADPr binding proteins were used to establish a comprehensive repertoire of pADPr-associated proteins. Visualization and modeling of these pADPr-associated proteins in networks not only reflect the widespread involvement of poly(ADP-ribosyl)ation in several pathways but also identify protein targets that could shed new light on the regulatory functions of pADPr in normal physiological conditions as well as after exposure to genotoxic stimuli.

Citing Articles

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References

Aguiar R, Takeyama K, He C, Kreinbrink K, Shipp M . B-aggressive lymphoma family proteins have unique domains that modulate transcription and exhibit poly(ADP-ribose) polymerase activity. J Biol Chem. 2005; 280(40):33756-65. DOI: 10.1074/jbc.M505408200. View

Ahel I, Ahel D, Matsusaka T, Clark A, Pines J, Boulton S . Poly(ADP-ribose)-binding zinc finger motifs in DNA repair/checkpoint proteins. Nature. 2008; 451(7174):81-5. DOI: 10.1038/nature06420. View

Andrabi S, Kim N, Yu S, Wang H, Koh D, Sasaki M . Poly(ADP-ribose) (PAR) polymer is a death signal. Proc Natl Acad Sci U S A. 2006; 103(48):18308-13. PMC: 1838747. DOI: 10.1073/pnas.0606526103. View

Zahradka P, Ebisuzaki K . Poly(ADP-ribose) polymerase is a zinc metalloenzyme. Eur J Biochem. 1984; 142(3):503-9. DOI: 10.1111/j.1432-1033.1984.tb08314.x. View

Keller A, Nesvizhskii A, Kolker E, Aebersold R . Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal Chem. 2002; 74(20):5383-92. DOI: 10.1021/ac025747h. View

Haince J, McDonald D, Rodrigue A, Dery U, Masson J, Hendzel M . PARP1-dependent kinetics of recruitment of MRE11 and NBS1 proteins to multiple DNA damage sites. J Biol Chem. 2007; 283(2):1197-208. DOI: 10.1074/jbc.M706734200. View

Forsburg S . The MCM helicase: linking checkpoints to the replication fork. Biochem Soc Trans. 2008; 36(Pt 1):114-9. DOI: 10.1042/BST0360114. View

Ruscetti T, Lehnert B, Halbrook J, Le Trong H, Hoekstra M, Chen D . Stimulation of the DNA-dependent protein kinase by poly(ADP-ribose) polymerase. J Biol Chem. 1998; 273(23):14461-7. DOI: 10.1074/jbc.273.23.14461. View

Simbulan-Rosenthal C, Rosenthal D, Boulares A, Hickey R, Malkas L, Coll J . Regulation of the expression or recruitment of components of the DNA synthesome by poly(ADP-ribose) polymerase. Biochemistry. 1998; 37(26):9363-70. DOI: 10.1021/bi9731089. View

10.

Faraone-Mennella M . Chromatin architecture and functions: the role(s) of poly(ADP-RIBOSE) polymerase and poly(ADPribosyl)ation of nuclear proteins. Biochem Cell Biol. 2005; 83(3):396-404. DOI: 10.1139/o05-042. View

11.

Ko B, Turck C, Lee K, Yang Y, Chung S . Purification, identification, and characterization of an osmotic response element binding protein. Biochem Biophys Res Commun. 2000; 270(1):52-61. DOI: 10.1006/bbrc.2000.2376. View

12.

Yeh T, Sbodio J, Tsun Z, Luo B, Chi N . Insulin-stimulated exocytosis of GLUT4 is enhanced by IRAP and its partner tankyrase. Biochem J. 2006; 402(2):279-90. PMC: 1798437. DOI: 10.1042/BJ20060793. View

13.

Fahrer J, Kranaster R, Altmeyer M, Marx A, Burkle A . Quantitative analysis of the binding affinity of poly(ADP-ribose) to specific binding proteins as a function of chain length. Nucleic Acids Res. 2007; 35(21):e143. PMC: 2175335. DOI: 10.1093/nar/gkm944. View

14.

Gagne J, Hunter J, Labrecque B, Chabot B, Poirier G . A proteomic approach to the identification of heterogeneous nuclear ribonucleoproteins as a new family of poly(ADP-ribose)-binding proteins. Biochem J. 2003; 371(Pt 2):331-40. PMC: 1223283. DOI: 10.1042/BJ20021675. View

15.

Combet C, Blanchet C, Geourjon C, Deleage G . NPS@: network protein sequence analysis. Trends Biochem Sci. 2000; 25(3):147-50. DOI: 10.1016/s0968-0004(99)01540-6. View

16.

Monaco L, Kolthur-Seetharam U, Loury R, Menissier-de Murcia J, de Murcia G, Sassone-Corsi P . Inhibition of Aurora-B kinase activity by poly(ADP-ribosyl)ation in response to DNA damage. Proc Natl Acad Sci U S A. 2005; 102(40):14244-8. PMC: 1242315. DOI: 10.1073/pnas.0506252102. View

17.

Brochu G, Duchaine C, Thibeault L, Lagueux J, Shah G, Poirier G . Mode of action of poly(ADP-ribose) glycohydrolase. Biochim Biophys Acta. 1994; 1219(2):342-50. DOI: 10.1016/0167-4781(94)90058-2. View

18.

Shannon P, Markiel A, Ozier O, Baliga N, Wang J, Ramage D . Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 2003; 13(11):2498-504. PMC: 403769. DOI: 10.1101/gr.1239303. View

19.

Shah G, Poirier D, Duchaine C, Brochu G, Desnoyers S, Lagueux J . Methods for biochemical study of poly(ADP-ribose) metabolism in vitro and in vivo. Anal Biochem. 1995; 227(1):1-13. DOI: 10.1006/abio.1995.1245. View

20.

Petroski M, Deshaies R . Function and regulation of cullin-RING ubiquitin ligases. Nat Rev Mol Cell Biol. 2005; 6(1):9-20. DOI: 10.1038/nrm1547. View