ATR inhibition rewires cellular signaling networks induced by replication stress

Proteomics

Volumn 16, Issue 3, 2016, Pages 402-416

  Wagner, Sebastian A ^a,b   Oehler, Hannah ^a   Voigt, Andrea ^c   Dalic, Denis ^a   Freiwald, Anja ^c   Serve, Hubert ^a,b   Beli, Petra ^c  

^a GOETHE UNIVERSITY   (Germany)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c INSTITUTE OF MOLECULAR BIOLOGY IMB   (Germany)

Author keywords

ATR kinase; Cancer; DNA replication stress; Phosphoproteomics; Quantitative MS; Systems biology

Indexed keywords

ATR PROTEIN; DNA; MINICHROMOSOME MAINTENANCE PROTEIN 6; PEPTIDES AND PROTEINS; PROTEIN PSMD4; PROTEIN RAD51AP1; PROTEIN TOPBP1; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; ATM PROTEIN; ATR PROTEIN, HUMAN; CARRIER PROTEIN; DNA BINDING PROTEIN; HYDROXYUREA; MCM6 PROTEIN, HUMAN; NUCLEAR PROTEIN; PHOSPHOPROTEIN; PROTEASOME; PSMD4 PROTEIN, HUMAN; RAD51AP1 PROTEIN, HUMAN; TOPBP1 PROTEIN, HUMAN;

ARTICLE; CELL DIVISION; DNA DAMAGE; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RNA SPLICING; RNA TRANSCRIPTION; AMINO ACID SEQUENCE; ANTAGONISTS AND INHIBITORS; CELL CYCLE; CELL SURVIVAL; DNA REPLICATION; DRUG EFFECTS; GENE REGULATORY NETWORK; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; MOLECULAR GENETICS; OSTEOBLAST; PATHOLOGY; PHOSPHORYLATION; PHYSIOLOGICAL STRESS; PROTEIN ANALYSIS; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

AMINO ACID SEQUENCE; ANTINEOPLASTIC AGENTS; ATAXIA TELANGIECTASIA MUTATED PROTEINS; CARRIER PROTEINS; CELL CYCLE; CELL LINE, TUMOR; CELL SURVIVAL; DNA; DNA REPLICATION; DNA-BINDING PROTEINS; GENE REGULATORY NETWORKS; HUMANS; HYDROXYUREA; MINICHROMOSOME MAINTENANCE COMPLEX COMPONENT 6; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; OSTEOBLASTS; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN INTERACTION MAPPING; RNA SPLICING; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; TRANSCRIPTION, GENETIC;

EID: 84958041043     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.201500172     Document Type: Article

References (68)

1. Lindahl, T., Instability and decay of the primary structure of DNA. Nature 1993, 362, 709-715.
2. Lecona, E., Fernández-Capetillo, O., Replication stress and cancer: it takes two to tango. Exp. Cell Res. 2014, 329, 26-34.
3. Pacek, M., Walter, J. C., A requirement for MCM7 and Cdc45 in chromosome unwinding during eukaryotic DNA replication. EMBO. J. 2004, 23, 3667-3676.
4. Byun, T. S., Pacek, M., Yee, M., Walter, J. C., Cimprich, K. A., Functional uncoupling of MCM helicase and DNA polymerase activities activates the ATR-dependent checkpoint. Genes Dev. 2005, 19, 1040-1052.
5. Zou, L., Elledge, S. J., Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 2003, 300, 1542-1548.
6. López-Contreras, A. J., Fernandez-Capetillo, O., The ATR barrier to replication-born DNA damage. DNA Repair 2010, 9, 1249-1255.
7. MacDougall, C. A., Byun, T. S., Van, C., Yee, M., Cimprich, K. A., The structural determinants of checkpoint activation. Genes Dev. 2007, 21, 898-903.
8. Zeman, M. K., Cimprich, K. A., Causes and consequences of replication stress. Nat. Cell Biol. 2014, 16, 2-9.
9. Mazouzi, A., Velimezi, G., Loizou, J. I., DNA replication stress: causes, resolution and disease. Exp. Cell Res. 2014, 329, 85-93.
10. Petermann, E., Helleday, T., Pathways of mammalian replication fork restart. Nat. Rev. Mol. Cell Biol. 2010, 11, 683-687.
11. Eykelenboom, J. K., Harte, E. C., Canavan, L., Pastor-Peidro, A. et al., ATR activates the S-M checkpoint during unperturbed growth to ensure sufficient replication prior to mitotic onset. Cell Rep. 2013, 5, 1095-1107.
12. Petermann, E., Orta, M. L., Issaeva, N., Schultz, N., Helleday, T., Hydroxyurea-stalled replication forks become progressively inactivated and require two different RAD51-mediated pathways for restart and repair. Mol. Cell 2010, 37, 492-502.
13. Toledo, L. I., Altmeyer, M., Rask, M.-B., Lukas, C. et al., ATR prohibits replication catastrophe by preventing global exhaustion of RPA. Cell 2013, 155, 1088-1103.
14. Hanada, K., Budzowska, M., Davies, S. L., van Drunen, E. et al., The structure-specific endonuclease Mus81 contributes to replication restart by generating double-strand DNA breaks. Nat. Struct. Mol. Biol. 2007, 14, 1096-1104.
15. Chanoux, R. A., Yin, B., Urtishak, K. A., Asare, A. et al., ATR and H2AX cooperate in maintaining genome stability under replication stress. J. Biol. Chem. 2009, 284, 5994-6003.
16. O'Driscoll, M., Jeggo, P. A., The role of the DNA damage response pathways in brain development and microcephaly: insight from human disorders. DNA Repair 2008, 7, 1039-1050.
17. Ogi, T., Walker, S., Stiff, T., Hobson, E. et al., Identification of the first ATRIP-deficient patient and novel mutations in ATR define a clinical spectrum for ATR-ATRIP Seckel syndrome. PLoS Genet. 2012, 8, e1002945.
18. Di Micco, R., Fumagalli, M., Cicalese, A., Piccinin, S. et al., Oncogene-induced senescence is a DNA damage response triggered by DNA hyper-replication. Nature 2006, 444, 638-642.
19. Bester, A. C., Roniger, M., Oren, Y. S., Im, M. M. et al., Nucleotide deficiency promotes genomic instability in early stages of cancer development. Cell 2011, 145, 435-446.
20. Jones, R. M., Mortusewicz, O., Afzal, I., Lorvellec, M. et al., Increased replication initiation and conflicts with transcription underlie Cyclin E-induced replication stress. Oncogene 2013, 32, 3744-3753.
21. Dominguez-Sola, D., Ying, C. Y., Grandori, C., Ruggiero, L. et al., Non-transcriptional control of DNA replication by c-Myc. Nature 2007, 448, 445-451.
22. Llona-Minguez, S., Höglund, A., Jacques, S. A., Koolmeister, T., Helleday, T., Chemical strategies for development of ATR inhibitors. Expert. Rev. Mol. Med. 2014, 16, e10.
23. Huntoon, C. J., Flatten, K. S., Wahner Hendrickson, A. E., Huehls, A. M. et al., ATR inhibition broadly sensitizes ovarian cancer cells to chemotherapy independent of BRCA status. Cancer Res. 2013, 73, 3683-3691.
24. Toledo, L. I., Murga, M., Fernandez-Capetillo, O., Targeting ATR and Chk1 kinases for cancer treatment: a new model for new (and old) drugs. Mol. Oncol. 2011, 5, 368-373.
25. Jossé, R., Martin, S. E., Guha, R., Ormanoglu, P. et al., ATR inhibitors VE-821 and VX-970 sensitize cancer cells to topoisomerase i inhibitors by disabling DNA replication initiation and fork elongation responses. Cancer Res. 2014, 74, 6968-6979.
26. Parikh, R. A., Appleman, L. J., Bauman, J. E., Sankunny, M. et al., Upregulation of the ATR-CHEK1 pathway in oral squamous cell carcinomas. Genes Chromosomes Cancer 2014, 53, 25-37.
27. Flynn, R. L., Cox, K. E., Jeitany, M., Wakimoto, H. et al., Alternative lengthening of telomeres renders cancer cells hypersensitive to ATR inhibitors. Science 2015, 347, 273-277.
28. Hoglund, A., Nilsson, L. M., Muralidharan, S. V., Hasvold, L. A. et al., Therapeutic implications for the induced levels of Chk1 in Myc-expressing cancer cells. Clin. Cancer Res. 2011, 17, 7067-7079.
29. Sirbu, B. M., Couch, F. B., Feigerle, J. T., Bhaskara, S. et al., Analysis of protein dynamics at active, stalled, and collapsed replication forks. Genes Dev. 2011, 25, 1320-1327.
30. Sirbu, B. M., McDonald, W. H., Dungrawala, H., Badu-Nkansah, A. et al., Identification of proteins at active, stalled, and collapsed replication forks using isolation of proteins on nascent DNA (iPOND) coupled with mass spectrometry. J. Biol. Chem. 2013, 288, 31458-31467.
31. Shiotani, B., Zou, L., ATR signaling at a glance. J. Cell Sci. 2009, 122, 301-304.
32. Couch, F. B., Bansbach, C. E., Driscoll, R., Luzwick, J. W. et al., ATR phosphorylates SMARCAL1 to prevent replication fork collapse. Genes Dev. 2013, 27, 1610-1623.
33. Choudhary, C., Mann, M., Decoding signalling networks by mass spectrometry-based proteomics. Nat. Rev. Mol. Cell Biol. 2010, 11, 427-439.
34. Sabidó, E., Selevsek, N., Aebersold, R., Mass spectrometry-based proteomics for systems biology. Curr. Opin. Biotechnol. 2012, 23, 591-597.
35. Altelaar, A. F. M., Munoz, J., Heck, A. J. R., Next-generation proteomics: towards an integrative view of proteome dynamics. Nat. Rev. Genet. 2013, 14, 35-48.
36. Beli, P., Lukashchuk, N., Wagner, S. A., Weinert, B. T. et al., Proteomic investigations reveal a role for RNA processing factor THRAP3 in the DNA damage response. Mol. Cell 2012, 46, 212-225.
37. Matsuoka, S., Ballif, B. A., Smogorzewska, A., McDonald, E. R. et al., ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 2007, 316, 1160-1166.
38. Bensimon, A., Schmidt, A., Ziv, Y., Elkon, R. et al., ATM-dependent and -independent dynamics of the nuclear phosphoproteome after DNA damage. Sci. Signal. 2010, 3, rs3.
39. Larance, M., Lamond, A. I., Multidimensional proteomics for cell biology. Nat. Rev. Mol. Cell Biol. 2015, 16, 269-280.
40. Bennetzen, M. V, Larsen, D. H., Bunkenborg, J., Bartek, J. et al., Site-specific phosphorylation dynamics of the nuclear proteome during the DNA damage response. Mol. Cell. Proteomics 2010, 9, 1314-1323.
41. Blasius, M., Forment, J. V, Thakkar, N., Wagner, S. A. et al., A phospho-proteomic screen identifies substrates of the checkpoint kinase Chk1. Genome Biol. 2011, 12, R78.
42. Reaper, P. M., Griffiths, M. R., Long, J. M., Charrier, J.-D. et al., Selective killing of ATM- or p53-deficient cancer cells through inhibition of ATR. Nat. Chem. Biol. 2011, 7, 428-430.
43. Ong, S.-E., Blagoev, B., Kratchmarova, I., Kristensen, D. B. et al., Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol. Cell. Proteomics 2002, 1, 376-386.
44. Weinert, B. T., Scholz, C., Wagner, S. A., Iesmantavicius, V. et al., Lysine succinylation is a frequently occurring modification in prokaryotes and eukaryotes and extensively overlaps with acetylation. Cell Rep. 2013, 4, 842-851.
45. Rappsilber, J., Mann, M., Ishihama, Y., Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips. Nat. Protoc. 2007, 2, 1896-1906.
46. Michalski, A., Damoc, E., Hauschild, J. P., Lange, O. et al., Mass spectrometry-based proteomics using Q Exactive, a high-performance benchtop quadrupole Orbitrap mass spectrometer. Mol. Cell Proteomics 2011, 10, M111 011015.
47. Olsen, J. V, Macek, B., Lange, O., Makarov, A. et al., Higher-energy C-trap dissociation for peptide modification analysis. Nat. Methods 2007, 4, 709-712.
48. Cox, J., Mann, M., MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 2008, 26, 1367-1372.
49. Stokes, M. P., Rush, J., MacNeill, J., Ren, J. M. et al., Profiling of UV-induced ATM/ATR signaling pathways. Proc. Natl. Acad. Sci. 2007, 104, 19855-19860.
50. Cox, J., Neuhauser, N., Michalski, A., Scheltema, R. A. et al., Andromeda: a peptide search engine integrated into the MaxQuant environment. J. Proteome Res. 2011, 10, 1794-1805.
51. Olsen, J. V, Blagoev, B., Gnad, F., Macek, B. et al., Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 2006, 127, 635-648.
52. Elias, J. E., Gygi, S. P., Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry. Nat. Methods 2007, 4, 207-214.
53. Vizcaino, J. A., Cote, R. G., Csordas, A., Dianes, J. A. et al., The PRoteomics IDEntifications (PRIDE) database and associated tools: status in 2013. Nucleic Acids Res. 2013, 41, D1063-D1069.
54. Franceschini, A., Szklarczyk, D., Frankild, S., Kuhn, M. et al., STRING v9.1: protein-protein interaction networks, with increased coverage and integration. Nucleic Acids Res. 2013, 41, D808-D815.
55. Saito, R., Smoot, M. E., Ono, K., Ruscheinski, J. et al., A travel guide to Cytoscape plugins. Nat. Methods 2012, 9, 1069-1076.
56. Gaillard, H., García-Muse, T., Aguilera, A., Replication stress and cancer. Nat. Rev. Cancer 2015, 15, 276-289.
57. Weber, A. M., Ryan, A. J., ATM and ATR as therapeutic targets in cancer. Pharmacol. Ther. 2014, 149, 124-138.
58. Reinhardt, H. C., Cannell, I. G., Morandell, S., Yaffe, M. B., Is post-transcriptional stabilization, splicing and translation of selective mRNAs a key to the DNA damage response? Cell Cycle 2011, 10, 23-27.
59. Drougat, L., Olivier-Van Stichelen, S., Mortuaire, M., Foulquier, F. et al., Characterization of O-GlcNAc cycling and proteomic identification of differentially O-GlcNAcylated proteins during G1/S transition. Biochim. Biophys. Acta 2012, 1820, 1839-1848.
60. Kovalenko, O. V, Golub, E. I., Bray-Ward, P., Ward, D. C., Radding, C. M., A novel nucleic acid-binding protein that interacts with human rad51 recombinase. Nucleic Acids Res. 1997, 25, 4946-4953.
61. Wiese, C., Dray, E., Groesser, T., San Filippo, J. et al., Promotion of homologous recombination and genomic stability by RAD51AP1 via RAD51 recombinase enhancement. Mol. Cell 2007, 28, 482-490.
62. Modesti, M., Budzowska, M., Baldeyron, C., Demmers, J. A. A. et al., RAD51AP1 is a structure-specific DNA binding protein that stimulates joint molecule formation during RAD51-mediated homologous recombination. Mol. Cell 2007, 28, 468-481.
63. Henson, S. E., Tsai, S.-C., Malone, C. S., Soghomonian, S. V et al., Pir51, a Rad51-interacting protein with high expression in aggressive lymphoma, controls mitomycin C sensitivity and prevents chromosomal breaks. Mutat. Res. 2006, 601, 113-124.
64. Parplys, A. C., Kratz, K., Speed, M. C., Leung, S. G. et al., RAD51AP1-deficiency in vertebrate cells impairs DNA replication. DNA Repair 2014, 24, 87-97.
65. Faustrup, H., Bekker-Jensen, S., Bartek, J., Lukas, J., Mailand, N., USP7 counteracts SCFbetaTrCP- but not APCCdh1-mediated proteolysis of Claspin. J. Cell Biol. 2009, 184, 13-29.
66. Alonso-de Vega, I., Martín, Y., Smits, V. A., USP7 controls Chk1 protein stability by direct deubiquitination. Cell Cycle 2014, 13, 3921-3926.
67. Wiltshire, T. D., Lovejoy, C. A., Wang, T., Xia, F. et al., Sensitivity to poly(ADP-ribose) polymerase (PARP) inhibition identifies ubiquitin-specific peptidase 11 (USP11) as a regulator of DNA double-strand break repair. J. Biol. Chem. 2010, 285, 14565-14571.
68. Nijman, S. M. B., Huang, T. T., Dirac, A. M. G., Brummelkamp, T. R. et al., The deubiquitinating enzyme USP1 regulates the Fanconi anemia pathway. Mol. Cell 2005, 17, 331-339.