ATM induces MacroD2 nuclear export upon DNA damage

Nucleic Acids Research

Volumn 45, Issue 1, 2017, Pages 244-254

  Golia, Barbara ^a   Moeller, Giuliana Katharina ^a   Jankevicius, Gytis ^a,b   Schmidt, Andreas ^a   Hegele, Anna ^a   Preißer, Julia ^a   Tran, Mai Ly ^a   Imhof, Axel ^a   Timinszky, Gyula ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; HYDROLASE; PROTEIN MACROD2; UNCLASSIFIED DRUG; ADENOSINE DIPHOSPHATE; ATM PROTEIN, HUMAN; DNA LIGASE; MACROD2 PROTEIN, HUMAN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE;

ADENOSINE DIPHOSPHATE RIBOSYLATION; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL NUCLEUS; CONTROLLED STUDY; DNA DAMAGE; ENZYME ACTIVITY; HUMAN; HUMAN CELL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; PROTEOMICS; SIGNAL TRANSDUCTION; GENETICS; HELA CELL LINE; METABOLISM; NUCLEOCYTOPLASMIC TRANSPORT; OSTEOBLAST; PHOSPHORYLATION; PHYSIOLOGICAL FEEDBACK; PROTEIN PROCESSING; TUMOR CELL LINE;

ACTIVE TRANSPORT, CELL NUCLEUS; ADENOSINE DIPHOSPHATE; AMINO ACID MOTIFS; ATAXIA TELANGIECTASIA MUTATED PROTEINS; CELL LINE, TUMOR; CELL NUCLEUS; DNA DAMAGE; DNA REPAIR ENZYMES; FEEDBACK, PHYSIOLOGICAL; HELA CELLS; HUMANS; HYDROLASES; OSTEOBLASTS; PHOSPHORYLATION; POLY(ADP-RIBOSE) POLYMERASES; PROTEIN PROCESSING, POST-TRANSLATIONAL; SIGNAL TRANSDUCTION;

EID: 85016153208     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkw904     Document Type: Article

References (40)

1. Caldecott, K.W. (2014) Protein ADP-ribosylation and the cellular response to DNA strand breaks. DNA Repair, 19, 108-113.
2. Golia, B., Singh, H.R. and Timinszky, G. (2015) Poly-ADP-ribosylation signaling during DNA damage repair. Front. Biosci., 20, 440-457.
3. Ryu, K.W., Kim, D.S. and Kraus, W.L. (2015) New facets in the regulation of gene expression by ADP-ribosylation and poly(ADP-ribose) polymerases. Chem. Rev., 115, 2453-2481.
4. Hottiger, M.O., Hassa, P.O., Luscher, B., Schuler, H. and Koch-Nolte, F. (2010) Toward a unified nomenclature for mammalian ADP-ribosyltransferases. Trends Biochem. Sci., 35, 208-219.
5. Butepage, M., Eckei, L., Verheugd, P. and Luscher, B. (2015) Intracellular Mono-ADP-Ribosylation in signaling and disease. Cells, 4, 569-595.
6. Tanny, J.C., Dowd, G.J., Huang, J., Hilz, H. and Moazed, D. (1999) An enzymatic activity in the yeast Sir2 protein that is essential for gene silencing. Cell, 99, 735-745.
7. Haigis, M.C., Mostoslavsky, R., Haigis, K.M., Fahie, K., Christodoulou, D.C., Murphy, A.J., Valenzuela, D.M., Yancopoulos, G.D., Karow, M., Blander, G. et al. (2006) SIRT4 inhibits glutamate dehydrogenase and opposes the effects of calorie restriction in pancreatic beta cells. Cell, 126, 941-954.
8. Liszt, G., Ford, E., Kurtev, M. and Guarente, L. (2005) Mouse Sir2 homolog SIRT6 is a nuclear ADP-ribosyltransferase. J. Biol. Chem., 280, 21313-21320.
9. Kassner, I., Andersson, A., Fey, M., Tomas, M., Ferrando-May, E. and Hottiger, M.O. (2013) SET7/9-dependent methylation of ARTD1 at K508 stimulates poly-ADP-ribose formation after oxidative stress. Open Biol., 3, 120173.
10. Mao, Z., Hine, C., Tian, X., Van Meter, M., Au, M., Vaidya, A., Seluanov, A. and Gorbunova, V. (2011) SIRT6 promotes DNA repair under stress by activating PARP1. Science, 332, 1443-1446.
11. Wright, R.H., Castellano, G., Bonet, J., Le Dily, F., Font-Mateu, J., Ballare, C., Nacht, A.S., Soronellas, D., Oliva, B. and Beato, M. (2012) CDK2-dependent activation of PARP-1 is required for hormonal gene regulation in breast cancer cells. Genes Dev., 26, 1972-1983.
12. 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. et al. (2007) ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science, 316, 1160-1166.
13. Gagne, J.P., Moreel, X., Gagne, P., Labelle, Y., Droit, A., Chevalier-Pare, M., Bourassa, S., McDonald, D., Hendzel, M.J., Prigent, C. et al. (2009) Proteomic investigation of phosphorylation sites in poly(ADP-ribose) polymerase-1 and poly(ADP-ribose) glycohydrolase. J. Proteome Res., 8, 1014-1029.
14. Bensimon, A., Schmidt, A., Ziv, Y., Elkon, R., Wang, S.Y., Chen, D.J., Aebersold, R. and Shiloh, Y. (2010) ATM-dependent and -independent dynamics of the nuclear phosphoproteome after DNA damage. Sci. Signal., 3, rs3.
15. Shiloh, Y. and Ziv, Y. (2013) The ATM protein kinase: regulating the cellular response to genotoxic stress, and more. Nat. Rev. Mol. Cell Biol., 14, 197-210.
16. Haince, J.F., Kozlov, S., Dawson, V.L., Dawson, T.M., Hendzel, M.J., Lavin, M.F. and Poirier, G.G. (2007) Ataxia telangiectasia mutated (ATM) signaling network is modulated by a novel poly(ADP-ribose)-dependent pathway in the early response to DNA-damaging agents. J. Biol. Chem., 282, 16441-16453.
17. Jankevicius, G., Hassler, M., Golia, B., Rybin, V., Zacharias, M., Timinszky, G. and Ladurner, A.G. (2013) A family of macrodomain proteins reverses cellular mono-ADP-ribosylation. Nat. Struct. Mol. Biol., 20, 508-514.
18. Rosenthal, F., Feijs, K.L., Frugier, E., Bonalli, M., Forst, A.H., Imhof, R., Winkler, H.C., Fischer, D., Caflisch, A., Hassa, P.O. et al. (2013) Macrodomain-containing proteins are new mono-ADP-ribosylhydrolases. Nat. Struct. Mol. Biol., 20, 502-507.
19. Sharifi, R., Morra, R., Appel, C.D., Tallis, M., Chioza, B., Jankevicius, G., Simpson, M.A., Matic, I., Ozkan, E., Golia, B. et al. (2013) Deficiency of terminal ADP-ribose protein glycohydrolase TARG1/C6orf130 in neurodegenerative disease. EMBO J., 32, 1225-1237.
20. Neuvonen, M. and Ahola, T. (2009) Differential activities of cellular and viral macro domain proteins in binding of ADP-ribose metabolites. J. Mol. Biol., 385, 212-225.
21. Mohseni, M., Cidado, J., Croessmann, S., Cravero, K., Cimino-Mathews, A., Wong, H.Y., Scharpf, R., Zabransky, D.J., Abukhdeir, A.M., Garay, J.P. et al. (2014) MACROD2 overexpression mediates estrogen independent growth and tamoxifen resistance in breast cancers. Proc. Natl. Acad. Sci. U.S.A., 111, 17606-17611.
22. Linnebacher, M., Ostwald, C., Koczan, D., Salem, T., Schneider, B., Krohn, M., Ernst, M. and Prall, F. (2013) Single nucleotide polymorphism array analysis of microsatellite-stable, diploid/near-diploid colorectal carcinomas without the CpG island methylator phenotype. Oncol. Lett., 5, 173-178.
23. van den Broek, E., Dijkstra, M.J., Krijgsman, O., Sie, D., Haan, J.C., Traets, J.J., van de Wiel, M.A., Nagtegaal, I.D., Punt, C.J., Carvalho, B. et al. (2015) High prevalence and clinical relevance of genes affected by chromosomal breaks in colorectal cancer. PLoS One, 10, e0138141.
24. Briffa, R., Um, I., Faratian, D., Zhou, Y., Turnbull, A.K., Langdon, S.P. and Harrison, D.J. (2015) Multi-Scale genomic, transcriptomic and proteomic analysis of colorectal cancer cell lines to identify novel biomarkers. PLoS One, 10, e0144708.
25. Anney, R., Klei, L., Pinto, D., Regan, R., Conroy, J., Magalhaes, T.R., Correia, C., Abrahams, B.S., Sykes, N., Pagnamenta, A.T. et al. (2010) A genome-wide scan for common alleles affecting risk for autism. Hum. Mol. Genet., 19, 4072-4082.
26. Tsang, K.M., Croen, L.A., Torres, A.R., Kharrazi, M., Delorenze, G.N., Windham, G.C., Yoshida, C.K., Zerbo, O. and Weiss, L.A. (2013) A genome-wide survey of transgenerational genetic effects in autism. PloS One, 8, e76978.
27. Jones, R.M., Cadby, G., Blangero, J., Abraham, L.J., Whitehouse, A.J. and Moses, E.K. (2014) MACROD2 gene associated with autistic-like traits in a general population sample. Psychiatric Gen., 24, 241-248.
28. Hanai, S., Kanai, M., Ohashi, S., Okamoto, K., Yamada, M., Takahashi, H. and Miwa, M. (2004) Loss of poly(ADP-ribose) glycohydrolase causes progressive neurodegeneration in drosophila melanogaster. Proc. Natl. Acad. Sci. U.S.A., 101, 82-86.
29. Timinszky, G., Till, S., Hassa, P.O., Hothorn, M., Kustatscher, G., Nijmeijer, B., Colombelli, J., Altmeyer, M., Stelzer, E.H., Scheffzek, K. et al. (2009) A macrodomain-containing histone rearranges chromatin upon sensing PARP1 activation. Nat. Struct. Mol. Biol., 16, 923-929.
30. Kamentsky, L., Jones, T.R., Fraser, A., Bray, M.A., Logan, D.J., Madden, K.L., Ljosa, V., Rueden, C., Eliceiri, K.W. and Carpenter, A.E. (2011) Improved structure, function and compatibility for Cell Profiler: modular high-throughput image analysis software. Bioinformatics (Oxford, England), 27, 1179-1180.
31. Jensen, S.S. and Larsen, M.R. (2007) Evaluation of the impact of some experimental procedures on different phosphopeptide enrichment techniques. Rapid Commu. Mass Spectrom.: RCM, 21, 3635-3645.
32. Vizcaíno, J.A., Deutsch, E.W., Wang, R., Csordas, A., Reisinger, F., Ríos, D., Dianes, J.A., Sun, Z., Farrah, T., Bandeira, N. et al. (2014) Proteome Xchange provides globally coordinated proteomics data submission and dissemination. Nat. Biotechnol., 32, 223-226.
33. Rost, B., Yachdav, G. and Liu, J. (2004) The Predict Protein server. Nucleic Acids Res., 32, W321-W326.
34. Hasmann, M. and Schemainda, I. (2003) FK866, a highly specific noncompetitive inhibitor of nicotinamide phosphoribosyl transferase, represents a novel mechanism for induction of tumor cell apoptosis. Cancer Res., 63, 7436-7442.
35. Cambronne, X.A., Stewart, M.L., Kim, D., Jones-Brunette, A.M., Morgan, R.K., Farrens, D.L., Cohen, M.S. and Goodman, R.H. (2016) Biosensor reveals multiple sources for mitochondrial NAD(+). Science (New York, N.Y.), 352, 1474-1477.
36. Furgason, J.M. and Bahassi el, M. (2013) Targeting DNA repair mechanisms in cancer. Pharmacol. Ther., 137, 298-308.
37. Kim, S.T., Lim, D.S., Canman, C.E. and Kastan, M.B. (1999) Substrate specificities and identification of putative substrates of ATM kinase family members. J. Biol. Chem., 274, 37538-37543.
38. Wu, Z.H., Shi, Y., Tibbetts, R.S. and Miyamoto, S. (2006) Molecular linkage between the kinase ATM and NF-kappaB signaling in response to genotoxic stimuli. Science (New York, N.Y.), 311, 1141-1146.
39. Su, C.H., Zhao, R., Velazquez-Torres, G., Chen, J., Gully, C., Yeung, S.C. and Lee, M.H. (2010) Nuclear export regulation of COP1 by 14-3-3sigma in response to DNA damage. Mol. Cancer, 9, 243.
40. Haince, J.F., McDonald, D., Rodrigue, A., Dery, U., Masson, J.Y., Hendzel, M.J. and Poirier, G.G. (2008) PARP1-dependent kinetics of recruitment of MRE11 and NBS1 proteins to multiple DNA damage sites. J. Biol. Chem., 283, 1197-1208.