Regulation of DNA-End Resection by hnRNPU-like Proteins Promotes DNA Double-Strand Break Signaling and Repair

Molecular Cell

Volumn 45, Issue 4, 2012, Pages 505-516

  Polo, Sophie E ^a   Blackford, Andrew N ^b   Chapman, J Ross ^a   Baskcomb, Linda ^a   Gravel, Serge ^a   Rusch, Andre ^c   Thomas, Anoushka ^b   Blundred, Rachel ^b   Smith, Philippa ^a   Kzhyshkowska, Julia ^d,e   Dobner, Thomas ^c   Taylor, A Malcolm R ^b   Turnell, Andrew S ^b   Stewart, Grant S ^b   Grand, Roger J ^b   Jackson, Stephen P ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^c LEIBNIZ INSTITUTE FOR EXPERIMENTAL VIROLOGY   (Germany)

^d UNIVERSITY OF HEIDELBERG   (Germany)

^e INSTITUTE OF GENERAL PATHOLOGY AND PATHOPHYSIOLOGY   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

HELICASE; RIBONUCLEOPROTEIN;

ARTICLE; CELL SURVIVAL; DNA DAMAGE; DNA REPAIR; DOUBLE STRANDED DNA BREAK; EMBRYO; HUMAN; HUMAN CELL; PROTEIN FUNCTION; PROTEIN INTERACTION;

CARRIER PROTEINS; CELL CYCLE PROTEINS; DNA BREAKS, DOUBLE-STRANDED; DNA END-JOINING REPAIR; DNA REPAIR ENZYMES; DNA-BINDING PROTEINS; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEINS; HUMANS; NUCLEAR PROTEINS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 84863415403     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2011.12.035     Document Type: Article

References (59)

1. Barral P.M., Rusch A., Turnell A.S., Gallimore P.H., Byrd P.J., Dobner T., Grand R.J. The interaction of the hnRNP family member E1B-AP5 with p53. FEBS Lett. 2005, 579:2752-2758.
2. Bekker-Jensen S., Lukas C., Kitagawa R., Melander F., Kastan M.B., Bartek J., Lukas J. Spatial organization of the mammalian genome surveillance machinery in response to DNA strand breaks. J. Cell Biol. 2006, 173:195-206.
3. Berglund F.M., Clarke P.R. hnRNP-U is a specific DNA-dependent protein kinase substrate phosphorylated in response to DNA double-strand breaks. Biochem. Biophys. Res. Commun. 2009, 381:59-64.
4. Bernstein K.A., Rothstein R. At loose ends: resecting a double-strand break. Cell 2009, 137:807-810.
5. Blackford A.N., Bruton R.K., Dirlik O., Stewart G.S., Taylor A.M., Dobner T., Grand R.J., Turnell A.S. A role for E1B-AP5 in ATR signaling pathways during adenovirus infection. J. Virol. 2008, 82:7640-7652.
6. Britton S., Froment C., Frit P., Monsarrat B., Salles B., Calsou P. Cell nonhomologous end joining capacity controls SAF-A phosphorylation by DNA-PK in response to DNA double-strand breaks inducers. Cell Cycle 2009, 8:3717-3722.
7. Budd M.E., Campbell J.L. Interplay of Mre11 nuclease with Dna2 plus Sgs1 in Rad51-dependent recombinational repair. PLoS ONE 2009, 4:e4267.
8. Cejka P., Cannavo E., Polaczek P., Masuda-Sasa T., Pokharel S., Campbell J.L., Kowalczykowski S.C. DNA end resection by Dna2-Sgs1-RPA and its stimulation by Top3-Rmi1 and Mre11-Rad50-Xrs2. Nature 2010, 467:112-116.
9. Chapman J.R., Jackson S.P. Phospho-dependent interactions between NBS1 and MDC1 mediate chromatin retention of the MRN complex at sites of DNA damage. EMBO Rep. 2008, 9:795-801.
10. Chiolo I., Carotenuto W., Maffioletti G., Petrini J.H., Foiani M., Liberi G. Srs2 and Sgs1 DNA helicases associate with Mre11 in different subcomplexes following checkpoint activation and CDK1-mediated Srs2 phosphorylation. Mol. Cell. Biol. 2005, 25:5738-5751.
11. Cimprich K.A., Cortez D. ATR: an essential regulator of genome integrity. Nat. Rev. Mol. Cell Biol. 2008, 9:616-627.
12. Clerici M., Mantiero D., Lucchini G., Longhese M.P. The Saccharomyces cerevisiae Sae2 protein promotes resection and bridging of double strand break ends. J. Biol. Chem. 2005, 280:38631-38638.
13. Cortez D., Guntuku S., Qin J., Elledge S.J. ATR and ATRIP: partners in checkpoint signaling. Science 2001, 294:1713-1716.
14. Difilippantonio S., Nussenzweig A. The NBS1-ATM connection revisited. Cell Cycle 2007, 6:2366-2370.
15. Dupré A., Boyer-Chatenet L., Sattler R.M., Modi A.P., Lee J.H., Nicolette M.L., Kopelovich L., Jasin M., Baer R., Paull T.T., Gautier J. A forward chemical genetic screen reveals an inhibitor of the Mre11-Rad50-Nbs1 complex. Nat. Chem. Biol. 2008, 4:119-125.
16. Falck J., Coates J., Jackson S.P. Conserved modes of recruitment of ATM, ATR and DNA-PKcs to sites of DNA damage. Nature 2005, 434:605-611.
17. Friedberg E.C., Walker G.C., Siede W., Wood R.D., Schultz R.A., Ellenberger T. DNA Repair and Mutagenesis 2006, ASM Press, Washington, DC. Second Edition.
18. Gabler S., Schütt H., Groitl P., Wolf H., Shenk T., Dobner T. E1B 55-kilodalton-associated protein: a cellular protein with RNA-binding activity implicated in nucleocytoplasmic transport of adenovirus and cellular mRNAs. J. Virol. 1998, 72:7960-7971.
19. Galanty Y., Belotserkovskaya R., Coates J., Polo S., Miller K.M., Jackson S.P. Mammalian SUMO E3-ligases PIAS1 and PIAS4 promote responses to DNA double-strand breaks. Nature 2009, 462:935-939.
20. Gravel S., Chapman J.R., Magill C., Jackson S.P. DNA helicases Sgs1 and BLM promote DNA double-strand break resection. Genes Dev. 2008, 22:2767-2772.
21. Haley B., Paunesku T., Protić M., Woloschak G.E. Response of heterogeneous ribonuclear proteins (hnRNP) to ionising radiation and their involvement in DNA damage repair. Int. J. Radiat. Biol. 2009, 85:643-655.
22. Han S.P., Tang Y.H., Smith R. Functional diversity of the hnRNPs: past, present and perspectives. Biochem. J. 2010, 430:379-392.
23. Hari F.J., Spycher C., Jungmichel S., Pavic L., Stucki M. A divalent FHA/BRCT-binding mechanism couples the MRE11-RAD50-NBS1 complex to damaged chromatin. EMBO Rep. 2010, 11:387-392.
24. Harper J.W., Elledge S.J. The DNA damage response: ten years after. Mol. Cell 2007, 28:739-745.
25. Harrigan J.A., Belotserkovskaya R., Coates J., Dimitrova D.S., Polo S.E., Bradshaw C.R., Fraser P., Jackson S.P. Replication stress induces 53BP1-containing OPT domains in G1 cells. J. Cell Biol. 2011, 193:97-108.
26. Hartlerode A.J., Scully R. Mechanisms of double-strand break repair in somatic mammalian cells. Biochem. J. 2009, 423:157-168.
27. Huertas P. DNA resection in eukaryotes: deciding how to fix the break. Nat. Struct. Mol. Biol. 2010, 17:11-16.
28. Jackson S.P., Bartek J. The DNA-damage response in human biology and disease. Nature 2009, 461:1071-1078.
29. Kim J.S., Krasieva T.B., Kurumizaka H., Chen D.J., Taylor A.M., Yokomori K. Independent and sequential recruitment of NHEJ and HR factors to DNA damage sites in mammalian cells. J. Cell Biol. 2005, 170:341-347.
30. Kzhyshkowska J., Rusch A., Wolf H., Dobner T. Regulation of transcription by the heterogeneous nuclear ribonucleoprotein E1B-AP5 is mediated by complex formation with the novel bromodomain-containing protein BRD7. Biochem. J. 2003, 371:385-393.
31. Lee J.H., Paull T.T. ATM activation by DNA double-strand breaks through the Mre11-Rad50-Nbs1 complex. Science 2005, 308:551-554.
32. Lieber M.R. The mechanism of human nonhomologous DNA end joining. J. Biol. Chem. 2008, 283:1-5.
33. Limbo O., Chahwan C., Yamada Y., de Bruin R.A., Wittenberg C., Russell P. Ctp1 is a cell-cycle-regulated protein that functions with Mre11 complex to control double-strand break repair by homologous recombination. Mol. Cell 2007, 28:134-146.
34. Lloyd J., Chapman J.R., Clapperton J.A., Haire L.F., Hartsuiker E., Li J., Carr A.M., Jackson S.P., Smerdon S.J. A supramodular FHA/BRCT-repeat architecture mediates Nbs1 adaptor function in response to DNA damage. Cell 2009, 139:100-111.
35. Longhese M.P., Bonetti D., Manfrini N., Clerici M. Mechanisms and regulation of DNA end resection. EMBO J. 2010, 29:2864-2874.
36. Lukas C., Savic V., Bekker-Jensen S., Doil C., Neumann B., Pedersen R.S., Grøfte M., Chan K.L., Hickson I.D., Bartek J., Lukas J. 53BP1 nuclear bodies form around DNA lesions generated by mitotic transmission of chromosomes under replication stress. Nat. Cell Biol. 2011, 13:243-253.
37. Matsuoka S., Ballif B.A., Smogorzewska A., McDonald E.R., Hurov K.E., Luo J., Bakalarski C.E., Zhao Z., Solimini N., Lerenthal Y., et al. ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 2007, 316:1160-1166.
38. Meek K., Dang V., Lees-Miller S.P. DNA-PK: the means to justify the ends?. Adv. Immunol. 2008, 99:33-58.
39. Melander F., Bekker-Jensen S., Falck J., Bartek J., Mailand N., Lukas J. Phosphorylation of SDT repeats in the MDC1 N terminus triggers retention of NBS1 at the DNA damage-modified chromatin. J. Cell Biol. 2008, 181:213-226.
40. Mimitou E.P., Symington L.S. Sae2, Exo1 and Sgs1 collaborate in DNA double-strand break processing. Nature 2008, 455:770-774.
41. Mimitou E.P., Symington L.S. Nucleases and helicases take center stage in homologous recombination. Trends Biochem. Sci. 2009, 34:264-272.
42. Nimonkar A.V., Genschel J., Kinoshita E., Polaczek P., Campbell J.L., Wyman C., Modrich P., Kowalczykowski S.C. BLM-DNA2-RPA-MRN and EXO1-BLM-RPA-MRN constitute two DNA end resection machineries for human DNA break repair. Genes Dev. 2011, 25:350-362.
43. Niu H., Chung W.H., Zhu Z., Kwon Y., Zhao W., Chi P., Prakash R., Seong C., Liu D., Lu L., et al. Mechanism of the ATP-dependent DNA end-resection machinery from Saccharomyces cerevisiae. Nature 2010, 467:108-111.
44. Pardo B., Gómez-González B., Aguilera A. DNA repair in mammalian cells: DNA double-strand break repair: how to fix a broken relationship. Cell. Mol. Life Sci. 2009, 66:1039-1056.
45. Pierce A.J., Hu P., Han M., Ellis N., Jasin M. Ku DNA end-binding protein modulates homologous repair of double-strand breaks in mammalian cells. Genes Dev. 2001, 15:3237-3242.
46. Polo S.E., Jackson S.P. Dynamics of DNA damage response proteins at DNA breaks: a focus on protein modifications. Genes Dev. 2011, 25:409-433.
47. Raderschall E., Golub E.I., Haaf T. Nuclear foci of mammalian recombination proteins are located at single-stranded DNA regions formed after DNA damage. Proc. Natl. Acad. Sci. USA 1999, 96:1921-1926.
48. Rupnik A., Lowndes N.F., Grenon M. MRN and the race to the break. Chromosoma 2010, 119:115-135. Published online October 28, 2009. 10.1007/s00412-009-0242-4.
49. San Filippo J., Sung P., Klein H. Mechanism of eukaryotic homologous recombination. Annu. Rev. Biochem. 2008, 77:229-257.
50. Sartori A.A., Lukas C., Coates J., Mistrik M., Fu S., Bartek J., Baer R., Lukas J., Jackson S.P. Human CtIP promotes DNA end resection. Nature 2007, 450:509-514.
51. Shanbhag N.M., Rafalska-Metcalf I.U., Balane-Bolivar C., Janicki S.M., Greenberg R.A. ATM-dependent chromatin changes silence transcription in cis to DNA double-strand breaks. Cell 2010, 141:970-981.
52. Shim E.Y., Chung W.H., Nicolette M.L., Zhang Y., Davis M., Zhu Z., Paull T.T., Ira G., Lee S.E. Saccharomyces cerevisiae Mre11/Rad50/Xrs2 and Ku proteins regulate association of Exo1 and Dna2 with DNA breaks. EMBO J. 2010, 29:3370-3380.
53. Spycher C., Miller E.S., Townsend K., Pavic L., Morrice N.A., Janscak P., Stewart G.S., Stucki M. Constitutive phosphorylation of MDC1 physically links the MRE11-RAD50-NBS1 complex to damaged chromatin. J. Cell Biol. 2008, 181:227-240.
54. 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.
55. Williams R.S., Dodson G.E., Limbo O., Yamada Y., Williams J.S., Guenther G., Classen S., Glover J.N., Iwasaki H., Russell P., Tainer J.A. Nbs1 flexibly tethers Ctp1 and Mre11-Rad50 to coordinate DNA double-strand break processing and repair. Cell 2009, 139:87-99.
56. Wu L., Luo K., Lou Z., Chen J. MDC1 regulates intra-S-phase checkpoint by targeting NBS1 to DNA double-strand breaks. Proc. Natl. Acad. Sci. USA 2008, 105:11200-11205.
57. You Z., Bailis J.M. DNA damage and decisions: CtIP coordinates DNA repair and cell cycle checkpoints. Trends Cell Biol. 2010, 20:402-409.
58. Zhu Z., Chung W.H., Shim E.Y., Lee S.E., Ira G. Sgs1 helicase and two nucleases Dna2 and Exo1 resect DNA double-strand break ends. Cell 2008, 134:981-994.
59. Zou L., Elledge S.J. Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 2003, 300:1542-1548.