Discordance between phosphorylation and recruitment of 53BP1 in response to DNA double-strand breaks

Cell Cycle

Volumn 11, Issue 7, 2012, Pages 1432-1444

  Harding, Shane M ^a,b   Bristow, Robert G ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b PRINCESS MARGARET HOSPITAL   (Canada)

Author keywords

53BP1; ATM; DNA double strand breaks; DNA repair foci; DNA PKcs; Ionizing radiation; MRE11; RNF168

Indexed keywords

BINDING PROTEIN; DOUBLE STRANDED DNA; HISTONE H2AX; HYDROXYUREA; P53 BINDING PROTEIN 1; SERINE; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE S PHASE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; DOUBLE STRANDED DNA BREAK; ENZYME ACTIVITY; FIBROBLAST; HUMAN; HUMAN CELL; PROTEIN PHOSPHORYLATION; TUMOR CELL; UBIQUITINATION;

EID: 84860343773     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.19824     Document Type: Article

References (58)

1. Iwabuchi K, Bartel PL, Li B, Marraccino R, Fields S. Two cellular proteins that bind to wild-type but not mutant p53. Proc Natl Acad Sci USA 1994; 91:6098-102; PMID:8016121; http://dx.doi.org/10.1073/pnas.91.13.6098.
2. Schultz LB, Chehab NH, Malikzay A, Halazonetis TD. p53 binding protein 1 (53BP1) is an early participant in the cellular response to DNA double-strand breaks. J Cell Biol 2000; 151:1381-90; PMID:11134068; http://dx.doi.org/10.1083/ jcb.151.7.1381.
3. Lavin MF. The Mre11 complex and ATM: a two-way functional interaction in recognising and signaling DNA double strand breaks. DNA Repair (Amst) 2004; 3:1515-20; PMID:15380107; http://dx.doi.org/10.1016/j.dnarep.2004.07.001.
4. Bonner WM, Redon CE, Dickey JS, Nakamura AJ, Sedelnikova OA, Solier S, et al. GammaH2AX and cancer. Nat Rev Cancer 2008; 8:957-67; PMID:19005492; http://dx.doi.org/10.1038/nrc2523.
5. Redon CE, Nakamura AJ, Martin OA, Parekh PR, Weyemi US, Bonner WM. Recent developments in the use of γH2AX as a quantitative DNA double-strand break biomarker. Aging (Albany NY) 2011; 3:168-74; PMID:21325706.
6. Stiff T, O'Driscoll M, Rief N, Iwabuchi K, Löbrich M, Jeggo PA. ATM and DNA-PK function redundantly to phosphorylate H2AX after exposure to ionizing radiation. Cancer Res 2004; 64:2390-6; PMID:15059890; http://dx.doi.org/10. 1158/0008-5472.CAN-03-3207.
7. Stewart GS. Solving the RIDDLE of 53BP1 recruitment to sites of damage. Cell Cycle 2009; 8:1532-8; PMID:19372751; http://dx.doi.org/10.4161/cc.8.10. 8351.
8. Huyen Y, Zgheib O, Ditullio RA Jr, Gorgoulis VG, Zacharatos P, Petty TJ, et al. Methylated lysine 79 of histone H3 targets 53BP1 to DNA double-strand breaks. Nature 2004; 432:406-11; PMID:15525939; http://dx.doi.org/10.1038/ nature03114.
9. Botuyan MV, Lee J, Ward IM, Kim JE, Thompson JR, Chen J, et al. Structural basis for the methylation state-specific recognition of histone H4-K20 by 53BP1 and Crb2 in DNA repair. Cell 2006; 127:1361-73; PMID:17190600; http://dx.doi.org/10.1016/j.cell.2006.10.043.
10. Wang B, Matsuoka S, Carpenter PB, Elledge SJ. 53BP1, a mediator of the DNA damage checkpoint. Science 2002; 298:1435-8; PMID:12364621; http://dx.doi.org/10.1126/science.1076182.
11. Bekker-Jensen S, Lukas C, Melander F, Bartek J, Lukas J. Dynamic assembly and sustained retention of 53BP1 at the sites of DNA damage are controlled by Mdc1/NFBD1. J Cell Biol 2005; 170:201-11; PMID:16009723; http://dx.doi.org/10. 1083/jcb.200503043.
12. Adams MM, Carpenter PB. Tying the loose ends together in DNA double strand break repair with 53BP1. Cell Div 2006; 1:19; PMID:16945145; http://dx.doi.org/10.1186/1747-1028-1-19.
13. Al Rashid ST, Harding SM, Law C, Coackley C, Bristow RG. Protein-protein interactions occur between p53 phosphoforms and ATM and 53BP1 at sites of exogenous DNA damage. Radiat Res 2011; 175:588-98; PMID:21361779; http://dx.doi.org/10.1667/RR2084.1.
14. Shibata A, Barton O, Noon AT, Dahm K, Deckbar D, Goodarzi AA, et al. Role of ATM and the damage response mediator proteins 53BP1 and MDC1 in the maintenance of G(2)/M checkpoint arrest. Mol Cell Biol 2010; 30:3371-83; PMID:20421415; http://dx.doi.org/10.1128/MCB.0164409.
15. Mochan TA, Venere M, DiTullio RA Jr, Halazonetis TD. 53BP1, an activator of ATM in response to DNA damage. DNA Repair (Amst) 2004; 3:945-52; PMID:15279780; http://dx.doi.org/10.1016/j.dnarep.2004.03.017.
16. Xie A, Hartlerode A, Stucki M, Odate S, Puget N, Kwok A, et al. Distinct roles of chromatin-associated proteins MDC1 and 53BP1 in mammalian double-strand break repair. Mol Cell 2007; 28:1045-57; PMID:18158901; http://dx.doi.org/10. 1016/j.molcel.2007.12.005.
17. Iwabuchi K, Basu BP, Kysela B, Kurihara T, Shibata M, Guan D, et al. Potential role for 53BP1 in DNA end-joining repair through direct interaction with DNA. J Biol Chem 2003; 278:36487-95; PMID:12824158; http://dx.doi.org/10. 1074/jbc.M304066200.
18. Bunting SF, Callén E, Wong N, Chen HT, Polato F, Gunn A, et al. 53BP1 inhibits homologous recombination in Brca1-deficient cells by blocking resection of DNA breaks. Cell 2010; 141:243-54; PMID:20362325; http://dx.doi.org/10.1016/j.cell.2010.03.012.
19. Dimitrova N, Chen YCM, Spector DL, de Lange T. 53BP1 promotes nonhomologous end joining of telomeres by increasing chromatin mobility. Nature 2008; 456:524-8; PMID:18931659; http://dx.doi.org/10.1038/nature07433.
20. Rodier F, Muñoz DP, Teachenor R, Chu V, Le O, Bhaumik D, et al. DNA-SCARS: distinct nuclear structures that sustain damage-induced senescence growth arrest and inflammatory cytokine secretion. J Cell Sci 2011; 124:68-81; PMID:21118958; http://dx.doi.org/10.1242/jcs.071340.
21. Goodarzi AA, Jeggo P, Löbrich M. The influence of heterochromatin on DNA double strand break repair: Getting the strong, silent type to relax. DNA Repair (Amst) 2010; 9:1273-82; PMID:21036673; http://dx.doi.org/10.1016/j. dnarep.2010.09.013.
22. Jowsey P, Morrice NA, Hastie CJ, McLauchlan H, Toth R, Rouse J. Characterisation of the sites of DNA damage-induced 53BP1 phosphorylation catalysed by ATM and ATR. DNA Repair (Amst) 2007; 6:1536-44; PMID:17553757; http://dx.doi.org/10.1016/j.dnarep.2007.04.011.
23. Gorgoulis VG, Vassiliou LVF, 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; 434:907-13; PMID:15829965; http://dx.doi.org/10.1038/nature03485.
24. Bartkova J, Horejsí Z, Koed K, Krämer A, Tort F, Zieger K, et al. DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis. Nature 2005; 434:864-70; PMID:15829956; http://dx.doi.org/10. 1038/nature03482.
25. Bartkova J, Horejsí Z, Sehested M, Nesland JM, Rajpert-De Meyts E, Skakkebaek NE, et al. DNA damage response mediators MDC1 and 53BP1: constitutive activation and aberrant loss in breast and lung cancer, but not in testicular germ cell tumours. Oncogene 2007; 26:741422;PMID:17546051; http://dx.doi.org/10.1038/sj.onc.1210553.
26. Nuciforo PG, Luise C, Capra M, Pelosi G, d'Adda di Fagagna F. Complex engagement of DNA damage response pathways in human cancer and in lung tumor progression. Carcinogenesis 2007; 28:2082-8; PMID:17522062; http://dx.doi.org/ 10.1093/carcin/bgm108.
27. Harding SM, Coackley C, Bristow RG. ATM-dependent phosphorylation of 53BP1 in response to genomic stress in oxic and hypoxic cells. Radiotherapy and Oncology. Journal of the European Society for Therapeutic Radiology and Oncology 2011; 99:307-12; http://dx.doi.org/10.1016/j.radonc.2011.05.039.
28. MacPhail SH, Banáth JP, Yu Y, Chu E, Olive PL. Cell cycle-dependent expression of phosphorylated histone H2AX: reduced expression in unirradiated but not X-irradiated G1-phase cells. Radiat Res 2003; 159:759-67; PMID:12751958; http://dx.doi.org/10.1667/RR3003.
29. Fraser M, Harding SM, Zhao H, Coackley C, Durocher D, Bristow RG. MRE11 promotes AKT phosphorylation in direct response to DNA double-strand breaks. Cell Cycle 2011; 10:2218-32; PMID:21623170; http://dx.doi.org/10.4161/cc.10.13. 16305.
30. Goodarzi AA, Noon AT, Deckbar D, Ziv Y, Shiloh Y, Löbrich M, et al. ATM signaling facilitates repair of DNA double-strand breaks associated with heterochromatin. Mol Cell 2008; 31:167-77; PMID:18657500; http://dx.doi.org/10. 1016/j.molcel.2008.05.017.
31. Pospelova TV, Demidenko ZN, Bukreeva EI, Pospelov VA, Gudkov AV, Blagosklonny MV. Pseudo-DNA damage response in senescent cells. Cell Cycle 2009; 8:4112-8; PMID:19946210; http://dx.doi.org/10.4161/cc.8.24.10215.
32. Al Rashid ST, Dellaire G, Cuddihy A, Jalali F, Vaid M, Coackley C, et al. Evidence for the direct binding of phosphorylated p53 to sites of DNA breaks in vivo. Cancer Res 2005; 65:10810-21; PMID:16322227; http://dx.doi.org/10.1158/ 0008-5472.CAN-05-0729.
33. 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; 22:5612-21; PMID:14532133; http://dx.doi.org/10.1093/emboj/cdg541.
34. Lee JH, Paull TT. ATM activation by DNA double-strand breaks through the Mre11-Rad50-Nbs1 complex. Science 2005; 308:551-4; PMID:15790808; http://dx.doi.org/10.1126/science.1108297.
35. Stewart GS, Stankovic T, Byrd PJ, Wechsler T, Miller ES, Huissoon A, et al. RIDDLE immunodeficiency syndrome is linked to defects in 53BP1-mediated DNA damage signaling. Proc Natl Acad Sci USA 2007; 104:16910-5; PMID:17940005; http://dx.doi.org/10.1073/pnas.0708408104.
36. Kastan MB. DNA damage responses: mechanisms and roles in human disease: 2007 G.H.A. Clowes Memorial Award Lecture. Mol Cancer Res 2008; 6:517-24; PMID:18403632; http://dx.doi.org/10.1158/1541-7786.MCR-08-0020.
37. Harper JW, Elledge SJ. The DNA damage response: ten years after. Mol Cell 2007; 28:739-45; PMID:18082599; http://dx.doi.org/10.1016/j.molcel.2007.11.015.
38. Ward IM, Minn K, Jorda KG, Chen J. Accumulation of checkpoint protein 53BP1 at DNA breaks involves its binding to phosphorylated histone H2AX. J Biol Chem 2003; 278:19579-82; PMID:12697768; http://dx.doi.org/10.1074/jbc. C300117200.
39. Callén E, Jankovic M, Wong N, Zha S, Chen HT, Difilippantonio S, et al. Essential role for DNA-PKcs in DNA double-strand break repair and apoptosis in ATM-deficient lymphocytes. Mol Cell 2009; 34:285-97; PMID:19450527; http://dx.doi.org/10.1016/j.molcel.2009.04.025.
40. White JS, Choi S, Bakkenist CJ. Transient ATM kinase inhibition disrupts DNA damage-induced sister chromatid exchange. Sci Signal 2010; 3:44; PMID:20516478; http://dx.doi.org/10.1126/scisignal.2000758.
41. Dobbs TA, Tainer JA, Lees-Miller SP. A structural model for regulation of NHEJ by DNA-PKcs autophosphorylation. DNA Repair (Amst) 2010; 9:1307-14; PMID:21030321; http://dx.doi.org/10.1016/j.dnarep.2010.09.019.
42. Ward I, Kim JE, Minn K, Chini CC, Mer G, Chen J. The tandem BRCT domain of 53BP1 is not required for its repair function. J Biol Chem 2006; 281:38472-7; PMID:17043355; http://dx.doi.org/10.1074/jbc.M607577200.
43. Bothmer A, Robbiani DF, Di Virgilio M, Bunting SF, Klein IA, Feldhahn N, et al. Regulation of DNA end joining, resection and immunoglobulin class switch recombination by 53BP1. Mol Cell 2011; 42:319-29; PMID:21549309; http://dx.doi.org/10.1016/j.molcel.2011.03.019.
44. Stiff T, Walker SA, Cerosaletti K, Goodarzi AA, Petermann E, Concannon P, et al. ATR-dependent phosphorylation and activation of ATM in response to UV treatment or replication fork stalling. EMBO J 2006; 25:5775-82; PMID:17124492; http://dx.doi.org/10.1038/sj.emboj.7601446.
45. Petermann E, Orta ML, 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; PMID:20188668; http://dx.doi.org/10.1016/j.molcel.2010.01.021.
46. Nakamura AJ, Rao VA, Pommier Y, Bonner WM. The complexity of phosphorylated H2AX foci formation and DNA repair assembly at DNA double-strand breaks. Cell Cycle 2010; 9:389-97; PMID:20046100; http://dx.doi.org/10.4161/cc. 9.2.10475.
47. Nelson G, Buhmann M, von Zglinicki T. DNA damage foci in mitosis are devoid of 53BP1. Cell Cycle 2009; 8:3379-83; PMID:19806024; http://dx.doi.org/ 10.4161/cc.8.20.9857.
48. Tomimatsu N, Mukherjee B, Burma S. Distinct roles of ATR and DNA-PKcs in triggering DNA damage responses in ATM-deficient cells. EMBO Rep 2009; 10:629-35; PMID:19444312; http://dx.doi.org/10.1038/embor.2009.60.
49. Bouwman P, Aly A, Escandell JM, Pieterse M, Bartkova J, van der Gulden H, et al. 53BP1 loss rescues BRCA1 deficiency and is associated with triple-negative and BRCA-mutated breast cancers. Nat Struct Mol Biol 2010; 17:688-95; PMID:20453858; http://dx.doi.org/10.1038/nsmb.1831.
50. Bencokova Z, Kaufmann MR, Pires IM, Lecane PS, Giaccia AJ, Hammond EM. ATM activation and signaling under hypoxic conditions. Mol Cell Biol 2009; 29:526-37; PMID:18981219; http://dx.doi.org/10.1128/MCB.01301-08.
51. Moon SH, Nguyen TA, Darlington Y, Lu X, Donehower LA. Dephosphorylation of γH2AX by WIP1: an important homeostatic regulatory event in DNA repair and cell cycle control. Cell Cycle 2010; 9:2092-6; PMID:20495376; http://dx.doi.org/10.4161/cc.9.11.11810.
52. Kang Y, Lee JH, Hoan NN, Sohn HM, Chang IY, You HJ. Protein phosphatase 5 regulates the function of 53BP1 after neocarzinostatin-induced DNA damage. J Biol Chem 2009; 284:9845-53; PMID:19176521; http://dx.doi.org/10.1074/jbc. M809272200.
53. Shreeram S, Demidov ON, Hee WK, Yamaguchi H, Onishi N, Kek C, et al. Wip1 phosphatase modulates ATM-dependent signaling pathways. Mol Cell 2006; 23:757-64; PMID:16949371; http://dx.doi.org/10.1016/j.molcel.2006.07.010.
54. Stewart GS, Panier S, Townsend K, Al-Hakim AK, Kolas NK, Miller ES, et al. The RIDDLE syndrome protein mediates a ubiquitin-dependent signaling cascade at sites of DNA damage. Cell 2009; 136:420-34; PMID:19203578; http://dx.doi.org/10.1016/j.cell.2008.12.042.
55. Beucher A, Birraux J, Tchouandong L, Barton O, Shibata A, Conrad S, et al. ATM and Artemis promote homologous recombination of radiation-induced DNA double-strand breaks in G2. EMBO J 2009; 28:3413-27; PMID:19779458; http://dx.doi.org/10.1038/emboj.2009.276.
56. Rodier F, Coppé JP, Patil CK, Hoeijmakers WAM, Muñoz DP, Raza SR, et al. Persistent DNA damage signalling triggers senescence-associated inflammatory cytokine secretion. Nat Cell Biol 2009; 11:973-9; PMID:19597488; http://dx.doi.org/10.1038/ncb1909.
57. Debacq-Chainiaux F, Erusalimsky JD, Campisi J, Toussaint O. Protocols to detect senescence-associated beta-galactosidase (SA-betagal) activity, a biomarker of senescent cells in culture and in vivo. Nat Protoc 2009; 4:1798-806; PMID:20010931; http://dx.doi.org/10.1038/nprot.2009.191.
58. Cubillos-Rojas M, Amair-Pinedo F, Tato I, Bartrons R, Ventura F, Rosa JL. Simultaneous electrophoretic analysis of proteins of very high and low molecular mass using Tris-acetate polyacrylamide gels. Electrophoresis 2010; 31:1318-21; PMID:20309890; http://dx.doi.org/10.1002/elps.200900657.