Site-specific phosphorylation dynamics of the nuclear proteome during the DNA damage response

Molecular and Cellular Proteomics

Volumn 9, Issue 6, 2010, Pages 1314-1323

  Bennetzen, Martin V ^a   Larsen, Dorthe Helena ^a,b   Bunkenborg, Jakob ^a   Bartek, Jiri ^a,c   Lukas, Jiri ^b   Andersen, Jens S ^a  

^a UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^b DANISH CANCER SOCIETY RESEARCH CENTER   (Denmark)

^c PALACKÝ UNIVERSITY   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; PROTEOME;

ARTICLE; CONSENSUS SEQUENCE; CONTROLLED STUDY; DEPHOSPHORYLATION; DNA DAMAGE; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IONIZING RADIATION; MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEOMICS;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; CELL LINE; CELL NUCLEUS; CHROMATOGRAPHY; CLUSTER ANALYSIS; CONSENSUS SEQUENCE; DNA DAMAGE; HUMANS; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; PHOSPHORYLATION; PROTEIN KINASES; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOME; REPRODUCIBILITY OF RESULTS; SIGNAL TRANSDUCTION; TIME FACTORS;

EID: 77953148666     PISSN: 15359476     EISSN: None     Source Type: Journal    
DOI: 10.1074/mcp.M900616-MCP200     Document Type: Article

References (44)

1. Löbrich, M., and Jeggo, P. A. (2007) The impact of a negligent G2/M checkpoint on genomic instability and cancer induction. Nat. Rev. Cancer 7, 861-869 (Pubitemid 350006255)
2. Bartek, J., and Lukas, J. (2007) DNA damage checkpoints: from initiation to recovery or adaptation. Curr. Opin. Cell Biol. 19, 238-245 (Pubitemid 46386406)
3. Zhou, B. B., and Elledge, S. J. (2000) The DNA damage response: putting checkpoints in perspective. Nature 408, 433-439
4. Lavin, M. F. (2008) Ataxia-telangiectasia: from a rare disorder to a paradigm for cell signalling and cancer. Nat. Rev. Mol. Cell Biol. 9, 759-769
5. Jackson, S. P., and Bartek, J. (2009) The DNA-damage response in human biology and disease. Nature 461, 1071-1078
6. Bakkenist, C. J., and Kastan, M. B. (2003) DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 421, 499-506
7. Matsuoka, S., Ballif, B. A., Smogorzewska, A., McDonald, E. R., 3rd, Hurov, K. E., Luo, J., Bakalarski, C. E., Zhao, Z., Solimini, N., Lerenthal, Y., Shiloh, Y., Gygi, S. P., and Elledge, S. J. (2007) ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 316, 1160-1166 (Pubitemid 46877472)
8. Olsen, J. V., Blagoev, B., Gnad, F., Macek, B., Kumar, C., Mortensen, P., and Mann, M. (2006) Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 127, 635-648 (Pubitemid 44647421)
9. Ong, S. E., Blagoev, B., Kratchmarova, I., Kristensen, D. B., Steen, H., Pandey, A., and Mann, M. (2002) Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol. Cell. Proteomics 1, 376-386
10. Alpert, A. J. (2008) Electrostatic repulsion hydrophilic interaction chromatography for isocratic separation of charged solutes and selective isolation of phosphopeptides. Anal. Chem. 80, 62-76
11. Larsen, M. R., Thingholm, T. E., Jensen, O. N., Roepstorff, P., and Jørgensen, T. J. (2005) Highly selective enrichment of phosphorylated peptides from peptide mixtures using titanium dioxide microcolumns. Mol. Cell. Proteomics 4, 873-886 (Pubitemid 41309146)
12. Rappsilber, J., Ishihama, Y., and Mann, M. (2003) Stop and go extraction tips for matrix-assisted laser desorption/ionization, nanoelectrospray, and LC/MS sample pretreatment in proteomics. Anal. Chem. 75, 663-670 (Pubitemid 36176744)
13. Hu, Q., Noll, R. J., Li, H., Makarov, A., Hardman, M., and Graham Cooks, R. (2005) The Orbitrap: a new mass spectrometer. J. Mass Spectrom. 40, 430-443
14. Schroeder, M. J., Shabanowitz, J., Schwartz, J. C., Hunt, D. F., and Coon, J. J. (2004) A neutral loss activation method for improved phosphopeptide sequence analysis by quadrupole ion trap mass spectrometry. Anal. Chem. 76, 3590-3598 (Pubitemid 38868819)
15. Olsen, J. V., de Godoy, L. M., Li, G., Macek, B., Mortensen, P., Pesch, R., Makarov, A., Lange, O., Horning, S., and Mann, M. (2005) Parts per million mass accuracy on an Orbitrap mass spectrometer via lock mass injection into a C-trap. Mol. Cell. Proteomics 4, 2010-2021 (Pubitemid 41830195)
16. Cox, J., and Mann, M. (2008) MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26, 1367-1372
17. Olsen, J. V., and Mann, M. (2004) Improved peptide identification in proteomics by two consecutive stages of mass spectrometric fragmentation. Proc. Natl. Acad. Sci. U.S.A. 101, 13417-13422
18. Elkon, R., Vesterman, R., Amit, N., Ulitsky, I., Zohar, I., Weisz, M., Mass, G., Orlev, N., Sternberg, G., Blekhman, R., Assa, J., Shiloh, Y., and Shamir, R. (2008) SPIKE - a database, visualization and analysis tool of cellular signaling pathways. BMC Bioinformatics 9, 110 (Pubitemid 351356765)
19. Saeed, A. I., Sharov, V., White, J., Li, J., Liang, W., Bhagabati, N., Braisted, J., Klapa, M., Currier, T., Thiagarajan, M., Sturn, A., Snuffin, M., Rezantsev, A., Popov, D., Ryltsov, A., Kostukovich, E., Borisovsky, I., Liu, Z., Vinsavich, A., Trush, V., and Quackenbush, J. (2003) TM4: a free, open-source system for microarray data management and analysis. BioTechniques 34, 374-378 (Pubitemid 36184095)
20. Schwartz, D., and Gygi, S. P. (2005) An iterative statistical approach to the identification of protein phosphorylation motifs from large-scale data sets. Nat. Biotechnol. 23, 1391-1398 (Pubitemid 41679391)
21. Linding, R., Jensen, L. J., Pasculescu, A., Olhovsky, M., Colwill, K., Bork, P., Yaffe, M. B., and Pawson, T. (2008) NetworKIN: a resource for exploring cellular phosphorylation networks. Nucleic Acids Res. 36, D695-D699 (Pubitemid 351149809)
22. Gnad, F., Ren, S., Cox, J., Olsen, J. V., Macek, B., Oroshi, M., and Mann, M. (2007) PHOSIDA (phosphorylation site database): management, structural and evolutionary investigation, and prediction of phosphosites. Genome Biol. 8, R250 (Pubitemid 351917499)
23. Ashburner, M., Ball, C. A., Blake, J. A., Botstein, D., Butler, H., Cherry, J. M., Davis, A. P., Dolinski, K., Dwight, S. S., Eppig, J. T., Harris, M. A., Hill, D. P., Issel-Tarver, L., Kasarskis, A., Lewis, S., Matese, J. C., Richardson, J. E., Ringwald, M., Rubin, G. M., and Sherlock, G. (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat. Genet. 25, 25-29
24. Shannon, P., Markiel, A., Ozier, O., Baliga, N. S., Wang, J. T., Ramage, D., Amin, N., Schwikowski, B., and Ideker, T. (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13, 2498-2504 (Pubitemid 37428274)
25. Maere, S., Heymans, K., and Kuiper, M. (2005) BiNGO: a Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics 21, 3448-3449 (Pubitemid 41222459)
26. Dennis, G., Jr., Sherman, B. T., Hosack, D. A., Yang, J., Gao, W., Lane, H. C., and Lempicki, R. A. (2003) DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol. 4, P3
27. Groth, A., Lukas, J., Nigg, E. A., Silljé, H. H., Wernstedt, C., Bartek, J., and Hansen, K. (2003) Human Tousled like kinases are targeted by an ATM-and Chk1-dependent DNA damage checkpoint. EMBO J. 22, 1676-1687 (Pubitemid 36417415)
28. Sunavala-Dossabhoy, G., Balakrishnan, S. K., Sen, S., Nuthalapaty, S., and De Benedetti, A. (2005) The radioresistance kinase TLK1B protects the cells by promoting repair of double strand breaks. BMC Mol. Biol. 6, 19 (Pubitemid 41418991)
29. Dephoure, N., Zhou, C., Villén, J., Beausoleil, S. A., Bakalarski, C. E., Elledge, S. J., and Gygi, S. P. (2008) A quantitative atlas of mitotic phosphorylation. Proc. Natl. Acad. Sci. U.S.A. 105, 10762-10767
30. Jilani, A., Ramotar, D., Slack, C., Ong, C., Yang, X. M., Scherer, S. W., and Lasko, D. D. (1999) Molecular cloning of the human gene, PNKP, encoding a polynucleotide kinase 3′-phosphatase and evidence for its role in repair of DNA strand breaks caused by oxidative damage. J. Biol. Chem. 274, 24176-24186 (Pubitemid 129528465)
31. Chen, W., Yazicioglu, M., and Cobb, M. H. (2004) Characterization of OSR1, a member of the mammalian Ste20p/germinal center kinase subfamily. J. Biol. Chem. 279, 11129-11136 (Pubitemid 38401606)
32. Feng, Q., Wang, H., Ng, H. H., Erdjument-Bromage, H., Tempst, P., Struhl, K., and Zhang, Y. (2002) Methylation of H3-lysine 79 is mediated by a new family of HMTases without a SET domain. Curr. Biol. 12, 1052-1058 (Pubitemid 34703339)
33. Huyen, Y., Zgheib, O., Ditullio, R. A., Jr., Gorgoulis, V. G., Zacharatos, P., Petty, T. J., Sheston, E. A., Mellert, H. S., Stavridi, E. S., and Halazonetis, T. D. (2004) Methylated lysine 79 of histone H3 targets 53BP1 to DNA double-strand breaks. Nature 432, 406-411 (Pubitemid 39551676)
34. Wysocki, R., Javaheri, A., Allard, S., Sha, F., Côté, J., and Kron, S. J. (2005) Role of Dot1-dependent histone H3 methylation in G1 and S phase DNA damage checkpoint functions of Rad9. Mol. Cell. Biol. 25, 8430-8443 (Pubitemid 41369165)
35. Dumenco, L. L., Allay, E., Norton, K., and Gerson, S. L. (1993) The prevention of thymic lymphomas in transgenic mice by human O6-alkylguanine- DNA alkyltransferase. Science 259, 219-222 (Pubitemid 23041797)
36. Bokar, J. A., Shambaugh, M. E., Polayes, D., Matera, A. G., and Rottman, F. M. (1997) Purification and cDNA cloning of the AdoMet-binding sub-unit of the human mRNA (N6-adenosine)-methyltransferase. RNA 3, 1233-1247 (Pubitemid 27495096)
37. Kim, J. D., Kang, K., and Kim, J. (2009) YY1's role in DNA methylation of Peg3 and Xist. Nucleic Acids Res. 37, 5656-5664
38. Gordon, S., Akopyan, G., Garban, H., and Bonavida, B. (2006) Transcription factor YY1: structure, function, and therapeutic implications in cancer biology. Oncogene 25, 1125-1142 (Pubitemid 43297928)
39. Milne, T. A., Briggs, S. D., Brock, H. W., Martin, M. E., Gibbs, D., Allis, C. D., and Hess, J. L. (2002) MLL targets SET domain methyltransferase activity to Hox gene promoters. Mol. Cell 10, 1107-1117 (Pubitemid 35453828)
40. van Attikum, H., and Gasser, S. M. (2009) Crosstalk between histone modifications during the DNA damage response. Trends Cell Biol. 19, 207-217
41. Lustig, A. J. (1998) Mechanisms of silencing in Saccharomyces cerevisiae. Curr. Opin. Genet. Dev. 8, 233-239
42. Bae, N. S., and Baumann, P. (2007) A RAP1/TRF2 complex inhibits non-homologous end-joining at human telomeric DNA ends. Mol. Cell 26, 323-334
43. Yudkovsky, N., Logie, C., Hahn, S., and Peterson, C. L. (1999) Recruitment of the SWI/SNF chromatin remodeling complex by transcriptional activators. Genes Dev. 13, 2369-2374 (Pubitemid 29453608)
44. Doyon, Y., and Côté, J. (2004) The highly conserved and multifunctional NuA4 HAT complex. Curr. Opin. Genet. Dev. 14, 147-154 (Pubitemid 38520142)