RAD18, WRNIP1 and ATMIN promote ATM signalling in response to replication stress

Oncogene

Volumn 35, Issue 30, 2016, Pages 4009-4019

  Kanu, N ^a,c   Zhang, T ^a,e   Burrell, R A ^a   Chakraborty, A ^a,g   Cronshaw, J ^a   Dacosta, C ^a   Gronroos E ^a   Pemberton, H N ^a   Anderton, E ^a   Gonzalez, L ^a,f   Sabbioneda, S ^b   Ulrich, H D ^a,f   Swanton, C ^a,c   Behrens, A ^a,d  

^a THE FRANCIS CRICK INSTITUTE   (United Kingdom)

^b CNR   (Italy)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d KING'S COLLEGE LONDON   (United Kingdom)

^e INSTITUTE OF MEDICAL BIOLOGY   (Singapore)

^f INSTITUTE OF MOLECULAR BIOLOGY   (Armenia)

^g ASTRAZENECA   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

APHIDICOLIN; ATM PROTEIN; ATMIN PROTEIN; BINDING PROTEIN; CYCLINE; PROTEIN; RAD18 PROTEIN; SINGLE STRANDED DNA; UNCLASSIFIED DRUG; WRN INTERACTING PROTEIN 1; ATM PROTEIN, HUMAN; ATMIN PROTEIN, HUMAN; CARRIER PROTEIN; DNA BINDING PROTEIN; RAD18 PROTEIN, HUMAN; TRANSCRIPTION FACTOR; UBIQUITIN PROTEIN LIGASE; WRNIP1 PROTEIN, HUMAN;

ARTICLE; AUTOPHOSPHORYLATION; CELL CYCLE S PHASE; CONTROLLED STUDY; DNA REPLICATION; FEMALE; GENOMIC INSTABILITY; HCT116 CELL LINE; HELA CELL LINE; HUMAN; HUMAN CELL; HYPOOSMOTIC STRESS; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SISTER CHROMATID; UBIQUITINATION; DNA DAMAGE; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION;

APHIDICOLIN; ATAXIA TELANGIECTASIA MUTATED PROTEINS; CARRIER PROTEINS; DNA DAMAGE; DNA REPLICATION; DNA-BINDING PROTEINS; GENOMIC INSTABILITY; HUMANS; PROLIFERATING CELL NUCLEAR ANTIGEN; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84979920495     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2015.427     Document Type: Article

References (48)

1. Derheimer FA, Kastan MB. Multiple roles of ATM in monitoring and maintaining DNA integrity. FEBS Lett 2010; 584: 3675-3681.
2. Lee JH, Paull TT. Activation and regulation of ATM kinase activity in response to DNA double-strand breaks. Oncogene 2007; 26: 7741-7748.
3. Lee JH, Paull TT. ATM activation by DNA double-strand breaks through the Mre11-Rad50-Nbs1 complex. Science 2005; 308: 551-554.
4. Uziel T, Lerenthal Y, Moyal L, Andegeko Y, Mittelman L, Shiloh Y. Requirement of the MRN complex for ATM activation by DNA damage. EMBO J 2003; 22: 5612-5621.
5. Bakkenist CJ, Kastan MB. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 2003; 421: 499-506.
6. Difilippantonio S, Celeste A, Fernandez-Capetillo O, Chen HT, Reina San Martin B, Van Laethem F et al. Role of Nbs1 in the activation of the Atm kinase revealed in humanized mouse models. Nat Cell Biol 2005; 7: 675-685.
7. Kanu N, Behrens A. ATMIN defines an NBS1-independent pathway of ATM signalling. EMBO J 2007; 26: 2933-2941.
8. McNees CJ, Conlan LA, Tenis N, Heierhorst J. ASCIZ regulates lesion-specific Rad51 focus formation and apoptosis after methylating DNA damage. EMBO J 2005; 24: 2447-2457.
9. Kanu N, Behrens A. ATMINistrating ATM signalling: regulation of ATM by ATMIN. Cell Cycle 2008; 7: 3483-3486.
10. Schmidt L, Wiedner M, Velimezi G, Prochazkova J, Owusu M, Bauer S et al. ATMIN is required for the ATM-mediated signaling and recruitment of 53BP1 to DNA damage sites upon replication stress. DNA Repair 2014; 24: 122-130.
11. Zeman MK, Cimprich KA. Causes and consequences of replication stress. Nat Cell Biol 2013; 16: 2-9.
12. Baumann C, Korner R, Hofmann K, Nigg EA. PICH, a centromere-associated SNF2 family ATPase, is regulated by Plk1 and required for the spindle checkpoint. Cell 2007; 128: 101-114.
13. Chan KL, Palmai-Pallag T, Ying S, Hickson ID. Replication stress induces sisterchromatid bridging at fragile site loci in mitosis. Nat Cell Biol 2009; 11: 753-760.
14. Chan KL, Hickson ID. New insights into the formation and resolution of ultra-fine anaphase bridges. Semin Cell Dev Biol 2011; 22: 906-912.
15. Harrigan JA, Belotserkovskaya R, Coates J, Dimitrova DS, Polo SE, Bradshaw CR et al. Replication stress induces 53BP1-containing OPT domains in G1 cells. J Cell Biol 2011; 193: 97-108.
16. Lukas C, Savic V, Bekker-Jensen S, Doil C, Neumann B, Pedersen RS et al. 53BP1 nuclear bodies form around DNA lesions generated by mitotic transmission of chromosomes under replication stress. Nat Cell Biol 2011; 13: 243-253.
17. Hoege C, Pfander B, Moldovan GL, Pyrowolakis G, Jentsch S. RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature 2002; 419: 135-141.
18. Ulrich HD. Regulating post-translational modifications of the eukaryotic replication clamp PCNA. DNA Repair 2009; 8: 461-469.
19. Crosetto N, Bienko M, Hibbert RG, Perica T, Ambrogio C, Kensche T et al. Human Wrnip1 is localized in replication factories in a ubiquitin-binding zinc fingerdependent manner. J Biol Chem 2008; 283: 35173-35185.
20. Kannouche PL, Wing J, Lehmann AR. Interaction of human DNA polymerase eta with monoubiquitinated PCNA: a possible mechanism for the polymerase switch in response to DNA damage. Mol Cell 2004; 14: 491-500.
21. Zhang Z, Zhang S, Lin SH, Wang X, Wu L, Lee EY et al. Structure of monoubiquitinated PCNA: implications for DNA polymerase switching and Okazaki fragment maturation. Cell Cycle 2012; 11: 2128-2136.
22. Saugar I, Parker JL, Zhao S, Ulrich HD. The genome maintenance factor Mgs1 is targeted to sites of replication stress by ubiquitylated PCNA. Nucleic Acids Res 2012; 40: 245-257.
23. Olcina MM, Foskolou IP, Anbalagan S, Senra JM, Pires IM, Jiang Y et al. Replication stress and chromatin context link ATM activation to a role in DNA replication. Mol Cell 2013; 52: 758-766.
24. Glover TW, Berger C, Coyle J, Echo B. DNA polymerase alpha inhibition by aphidicolin induces gaps and breaks at common fragile sites in human chromosomes. Hum Genet 1984; 67: 136-142.
25. Lilley CE, Chaurushiya MS, Boutell C, Landry S, Suh J, Panier S et al. A viral E3 ligase targets RNF8 and RNF168 to control histone ubiquitination and DNA damage responses. EMBO J 2010; 29: 943-955.
26. Soutoglou E, Dorn JF, Sengupta K, Jasin M, Nussenzweig A, Ried T et al. Positional stability of single double-strand breaks in mammalian cells. Nat Cell Biol 2007; 9: 675-682.
27. Payne BT, van Knippenberg IC, Bell H, Filipe SR, Sherratt DJ, McGlynn P. Replication fork blockage by transcription factor-DNA complexes in Escherichia coli. Nucleic Acids Res 2006; 34: 5194-5202.
28. Bish RA, Myers MP. Werner helicase-interacting protein 1 binds polyubiquitin via its zinc finger domain. J Biol Chem 2007; 282: 23184-23193.
29. Niimi A, Brown S, Sabbioneda S, Kannouche PL, Scott A, Yasui A et al. Regulation of proliferating cell nuclear antigen ubiquitination in mammalian cells. Proc Natl Acad Sci USA 2008; 105: 16125-16130.
30. Byun TS, Pacek M, Yee MC, Walter JC, Cimprich KA. Functional uncoupling of MCM helicase and DNA polymerase activities activates the ATR-dependent checkpoint. Genes Dev 2005; 19: 1040-1052.
31. Burrell RA, McClelland SE, Endesfelder D, Groth P, Weller MC, Shaikh N et al. Replication stress links structural and numerical cancer chromosomal instability. Nature 2013; 494: 492-496.
32. Chan KL, North PS, Hickson ID. BLM is required for faithful chromosome segregation and its localization defines a class of ultrafine anaphase bridges. EMBO J 2007; 26: 3397-3409.
33. Ammazzalorso F, Pirzio LM, Bignami M, Franchitto A, Pichierri P. ATR and ATM differently regulate WRN to prevent DSBs at stalled replication forks and promote replication fork recovery. EMBO J 2010; 29: 3156-3169.
34. Davalos AR, Kaminker P, Hansen RK, Campisi J. ATR and ATM-dependent movement of BLM helicase during replication stress ensures optimal ATM activation and 53BP1 focus formation. Cell Cycle 2004; 3: 1579-1586.
35. Trenz K, Smith E, Smith S, Costanzo V. ATM and ATR promote Mre11 dependent restart of collapsed replication forks and prevent accumulation of DNA breaks. EMBO J 2006; 25: 1764-1774.
36. Bish RA, Fregoso OI, Piccini A, Myers MP. Conjugation of complex polyubiquitin chains to WRNIP1. J Proteome Res 2008; 7: 3481-3489.
37. Gamper AM, Choi S, Matsumoto Y, Banerjee D, Tomkinson AE, Bakkenist CJ. ATM protein physically and functionally interacts with proliferating cell nuclear antigen to regulate DNA synthesis. J Biol Chem 2012; 287: 12445-12454.
38. Kawabe Y, Branzei D, Hayashi T, Suzuki H, Masuko T, Onoda F et al. A novel protein interacts with the Werner's syndrome gene product physically and functionally. J Biol Chem 2001; 276: 20364-20369.
39. Yoshimura A, Seki M, Kanamori M, Tateishi S, Tsurimoto T, Tada S et al. Physical and functional interaction between WRNIP1 and RAD18. Genes Genet Syst 2009; 84: 171-178.
40. Loizou JI, Sancho R, Kanu N, Bolland DJ, Yang F, Rada C et al. ATMIN is required for maintenance of genomic stability and suppression of B cell lymphoma. Cancer Cell 2011; 19: 587-600.
41. Blackford AN, Schwab RA, Nieminuszczy J, Deans AJ, West SC, Niedzwiedz W. The DNA translocase activity of FANCM protects stalled replication forks. Hum Mol Genet 2012; 21: 2005-2016.
42. Sirbu BM, Couch FB, Feigerle JT, Bhaskara S, Hiebert SW, Cortez D. Analysis of protein dynamics at active, stalled, and collapsed replication forks. Genes Dev 2011; 25: 1320-1327.
43. Fugger K, Mistrik M, Neelsen KJ, Yao Q, Zellweger R, Kousholt AN et al. FBH1 catalyzes regression of stalled replication forks. Cell Rep e-pub ahead of print 10 March 2015.
44. Ying S, Minocherhomji S, Chan KL, Palmai-Pallag T, Chu WK, Wass T et al. MUS81 promotes common fragile site expression. Nat Cell Biol 2013; 15: 1001-1007.
45. Bartkova J, Horejsi Z, Koed K, Kramer A, Tort F, Zieger K et al. DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis. Nature 2005; 434: 864-870.
46. Gorgoulis VG, Vassiliou LV, Karakaidos P, Zacharatos P, Kotsinas A, Liloglou T et al. Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions. Nature 2005; 434: 907-913.
47. Halazonetis TD, Gorgoulis VG, Bartek J. An oncogene-induced DNA damage model for cancer development. Science 2008; 319: 1352-1355.
48. Parker JL, Ulrich HD. In vitro PCNA modification assays. Methods Mol Biol 2012; 920: 569-589.