A quantitative 14-3-3 interaction screen connects the nuclear exosome targeting complex to the DNA damage response

Genes and Development

Volumn 28, Issue 18, 2014, Pages 1977-1982

  Blasius, Melanie ^a,b,c   Wagner, Sebastian A ^d   Choudhary, Chunaram ^d   Bartek, Jiri ^d,e   Jackson, Stephen P ^a,b,f  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c DANISH CANCER SOCIETY RESEARCH CENTER   (Denmark)

^d University of Copenhagen   (Denmark)

^e PALACKÝ UNIVERSITY   (Czech Republic)

^f WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

14 3 3; DNA damage response; MAPKAPK2; Nuclear exosome; UV

Indexed keywords

ATR PROTEIN; CHECKPOINT KINASE 1; DNA; GREEN FLUORESCENT PROTEIN; HEAT SHOCK PROTEIN 27; MESSENGER RNA; MK2 KINASE; NUCLEAR RNA; PHOSPHOTRANSFERASE; PROMPT PROTEIN; PROTEIN TYROSINE PHOSPHATASE; RBM7 PROTEIN; RIBONUCLEASE A; SYNAPTOPHYSIN; UNCLASSIFIED DRUG; UNTRANSLATED RNA; EXOSOME MULTIENZYME RIBONUCLEASE COMPLEX; MAP KINASE ACTIVATED KINASE 2; MAP-KINASE-ACTIVATED KINASE 2; PROTEIN 14 3 3; PROTEIN SERINE THREONINE KINASE; SIGNAL PEPTIDE;

ARTICLE; CELL CYCLE REGULATION; CELL SURVIVAL; CELLULAR DISTRIBUTION; DNA DAMAGE; EXOSOME; FOLLOW UP; HCT116 CELL LINE; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; IN VITRO STUDY; NUCLEAR EXOSOME TARGETING; POLYADENYLATION; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN METABOLISM; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING; PROTEIN TARGETING; QUANTITATIVE ANALYSIS; RNA METABOLISM; TRANSCRIPTION ELONGATION; 14-3-3; DNA DAMAGE RESPONSE; MAPKAPK2; METABOLISM; NUCLEAR EXOSOME; PHOSPHORYLATION; PHYSIOLOGY; SIGNAL TRANSDUCTION; ULTRAVIOLET RADIATION;

14-3-3; DNA DAMAGE RESPONSE; MAPKAPK2; NUCLEAR EXOSOME; UV;

14-3-3 PROTEINS; DNA DAMAGE; EXOSOME MULTIENZYME RIBONUCLEASE COMPLEX; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MAP KINASE SIGNALING SYSTEM; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN-SERINE-THREONINE KINASES; RNA, UNTRANSLATED; ULTRAVIOLET RAYS;

EID: 84907151091     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.246272.114     Document Type: Article

References (34)

1. Beli P, Lukashchuk N, Wagner SA, Weinert BT, Olsen JV, Baskcomb L, Mann M, Jackson SP, Choudhary C. 2012. Proteomic investigations reveal a role for RNA processing factor THRAP3 in the DNA damage response. Mol Cell 46: 212-225.
2. Bhatia V, Barroso SI, García-Rubio ML, Tumini E, Herrera-Moyano E, Aguilera A. 2014. BRCA2 prevents R-loop accumulation and associates with TREX-2 mRNA export factor PCID2. Nature 511: 362-365.
3. Blasius M, Forment JV, Thakkar N, Wagner SA, Choudhary C, Jackson SP. 2011. A phospho-proteomic screen identifies substrates of the checkpoint kinase Chk1. Genome Biol 12: R78.
4. Britton S, Dernoncourt E, Delteil C, Froment C, Schiltz O, Salles B, Frit P, Calsou P. 2014. DNA damage triggers SAF-A and RNA biogenesis factors exclusion from chromatin coupled to R-loops removal. Nucleic Acids Res 42: 9047-9062.
5. Bulavin DV, Higashimoto Y, Popoff IJ, Gaarde WA, Basrur V, Potapova O, Appella E, Fornace AJ Jr. 2001. Initiation of a G2/M checkpoint after ultraviolet radiation requires p38 kinase. Nature 411: 102-107.
6. Chen L, Liu T, Walworth NC. 1999. Association of Chk1 with 14-3-3 proteins is stimulated by DNA damage. Genes Dev 13: 675-685.
7. Chlebowski A, Lubas M, Jensen TH, Dziembowski A. 2013. RNA decay machines: the exosome. Biochim Biophys Acta 1829: 552-560.
8. Dalal SN, Yaffe MB, Decaprio JA. 2004. 14-3-3 family members act coordinately to regulate mitotic progression. Cell Cycle 3: 672-677.
9. Darnell JE Jr. 2013. Reflections on the history of pre-mRNA processing and highlights of current knowledge: a unified picture. RNA 19: 443-460.
10. Dorion S, Landry J. 2002. Activation of the mitogen-activated protein kinase pathways by heat shock. Cell Stress Chaperones 7: 200-206.
11. Gaillard H, Aguilera A. 2008. A novel class of mRNA-containing cytoplasmic granules are produced in response to UV-irradiation. Mol Biol Cell 19: 4980-4992.
12. Guo TB, Boros LG, Chan KC, Hikim APS, Hudson AP, Swerdloff RS, Mitchell AP, Salameh WA. 2003. Spermatogenetic expression of RNAbinding motif protein 7, a protein that interacts with splicing factors. J Androl 24: 204-214.
13. Gustafson MP, Welcker M, Hwang HC, Clurman BE. 2005. Zcchc8 is a glycogen synthase kinase-3 substrate that interacts with RNAbinding proteins. Biochem Biophys Res Commun 338: 1359-1367.
14. Hornbeck PV, Chabra I, Kornhauser JM, Skrzypek E, Zhang B. 2004. PhosphoSite: a bioinformatics resource dedicated to physiological protein phosphorylation. Proteomics 4: 1551-1561.
15. Jackson SP, Bartek J. 2009. The DNA-damage response in human biology and disease. Nature 461: 1071-1078.
16. Jiang K, Pereira E, Maxfield M, Russell B, Goudelock DM, Sanchez Y. 2003. Regulation of Chk1 includes chromatin association and 14-3-3 binding following phosphorylation on Ser-345. J Biol Chem 278: 25207-25217.
17. Johnson C, Crowther S, Stafford MJ, Campbell DG, Toth R, MacKintosh C. 2010. Bioinformatic and experimental survey of 14-3-3-binding sites. Biochem J 427: 69-78.
18. Johnson C, Tinti M, Wood NT, Campbell DG, Toth R, Dubois F, Geraghty KM, Wong BHC, Brown LJ, Tyler J, et al. 2011. Visualization and biochemical analyses of the emerging mammalian 14-3-3-phosphoproteome. Mol Cell Proteomics 10: M110.005751.
19. Lubas M, Christensen MS, Kristiansen MS, Domanski M, Falkenby LG, Lykke-Andersen S, Andersen JS, Dziembowski A, Jensen TH. 2011. Interaction profiling identifies the human nuclear exosome targeting complex. Mol Cell 43: 624-637.
20. Mohammad DH, Yaffe MB. 2009. 14-3-3 proteins, FHA domains and BRCT domains in the DNA damage response. DNA Repair (Amst) 8: 1009-1017.
21. Morita M, Ler LW, Fabian MR, Siddiqui N, Mullin M, Henderson VC, Alain T, Fonseca BD, Karashchuk G, Bennett CF, et al. 2012. A novel 4EHP-GIGYF2 translational repressor complex is essential for mammalian development. Mol Cell Biol 32: 3585-3593.
22. Nechaev S, Adelman K. 2011. Pol II waiting in the starting gates: regulating the transition from transcription initiation into productive elongation. Biochim Biophys Acta 1809: 34-45.
23. Ong S-E, Blagoev B, Kratchmarova I, Kristensen DB, Steen H, Pandey A, 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.
24. Polo SE, Jackson SP. 2011. Dynamics of DNA damage response proteins at DNA breaks: a focus on protein modifications. Genes Dev 25: 409-433.
25. Preker P, Nielsen J, Kammler S, Lykke-Andersen S, Christensen MS, Mapendano CK, Schierup MH, Heick JTH. 2008. RNA exosome depletion reveals transcription upstream of active human promoters. Science 322: 1851-1854.
26. Preker P, Almvig K, Christensen MS, Valen E, Mapendano CK, Sandelin A, Jensen TH. 2011. Promoter upstream transcripts share characteristics with mRNAs and are produced upstream of all three major types of mammalian promoters. Nucleic Acids Res 39: 7179-7193.
27. Reinhardt HC, Yaffe BM. 2009. Kinases that control the cell cycle in response to DNA Damage: Chk1, Chk2, and MK2. Curr Opin Cell Biol 21: 245-255.
28. Reinhardt HC, Hasskamp P, Schmedding I, Morandell S, van Vugt MATM, Wang X, Linding R, Ong SE, Weaver D, Carr SA, et al. 2010. DNA damage activates a spatially distinct late cytoplasmic cell-cycle checkpoint network controlled by MK2-mediated RNA stabilization. Mol Cell 40: 34-49.
29. Reinhardt HC, Cannell IG, Morandell S, Yaffe MB. 2011. Is posttranscriptional stabilization, splicing and translation of selective mRNAs a key to the DNA damage response? Cell Cycle 10: 23-27.
30. Sette C. 2010. An emerging role for nuclear RNA-mediated responses to genotoxic stress. RNA Biol 7: 390-396.
31. Shi Y, Manley JL. 2007. A complex signaling pathway regulates SRp38 phosphorylation and pre-mRNA splicing in response to heat shock. Mol Cell 28: 79-90.
32. Smith J, Tho LM, Xu N, Gillespie DA. 2010. The ATM-Chk2 and ATR-Chk1 pathways in DNA damage signaling and cancer. Adv Cancer Res 108: 73-112.
33. Sunayama J. 2005. JNK antagonizes Akt-mediated survival signals by phosphorylating 14-3-3. J Cell Biol 170: 295-304.
34. Yaffe M, Rittinger K, Volinia S, Caron P, Aitken A. 1997. The structural basis for 14-3-3:phosphopeptide binding specificity. Cell 91: 961-971.