SUMOylation of ATRIP potentiates DNA damage signaling by boosting multiple protein interactions in the ATR pathway

Genes and Development

Volumn 28, Issue 13, 2014, Pages 1472-1484

  Wu, Ching Shyi ^a   Ouyang, Jian ^a   Mori, Eiichiro ^b   Nguyen, Hai Dang ^a   Maréchal, Alexandre ^a   Hallet, Alexander ^a   Chen, David J ^b   Zou, Lee ^a,c  

^a HARVARD MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

ATR; ATRIP; Checkpoint; SUMOylation

Indexed keywords

ATR PROTEIN; CHECKPOINT KINASE RAD3; DNA; MRE11 PROTEIN; NIBRIN; PROTEIN; RAD50 PROTEIN; RPA70 PROTEIN; SUMO 2 PROTEIN; SUMO 3 PROTEIN; TOPBP1 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; DNA DAMAGE; GENE ACTIVATION; HUMAN; HUMAN CELL; IN VITRO STUDY; MUTANT; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; SUMOYLATION;

ATR; ATRIP; CHECKPOINT; SUMOYLATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ATAXIA TELANGIECTASIA MUTATED PROTEINS; DNA DAMAGE; DNA-BINDING PROTEINS; ENZYME ACTIVATION; HEK293 CELLS; HELA CELLS; HUMANS; PROTEIN BINDING; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; SUMOYLATION; UBIQUITIN-CONJUGATING ENZYMES;

EID: 84903778881     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.238535.114     Document Type: Article

References (64)

1. Ball HL, Myers JS, Cortez D. 2005. ATRIP binding to replication protein A-single-stranded DNA promotes ATR-ATRIP localization but is dispensable for Chk1 phosphorylation. Mol Biol Cell 16: 2372-2381.
2. Bekker-Jensen S, Mailand N. 2010. Assembly and function of DNA double-strand break repair foci in mammalian cells. DNA Repair (Amst) 9: 1219-1228.
3. Chou DM, Elledge SJ. 2006. Tipin and Timeless form a mutually protective complex required for genotoxic stress resistance and checkpoint function. Proc Natl Acad Sci 103: 18143-18147.
4. Chupreta S, Holmstrom S, Subramanian L, Iniguez-Lluhi JA. 2005. A small conserved surface in SUMO is the critical structural determinant of its transcriptional inhibitory properties. Mol Cell Biol 25: 4272-4282.
5. Ciccia A, Elledge SJ. 2010. The DNA damage response: making it safe to play with knives. Mol Cell 40: 179-204.
6. Cimprich KA, Cortez D. 2008. ATR: an essential regulator of genome integrity. Nat Rev Mol Cell Biol 9: 616-627.
7. Cortez D, Guntuku S, Qin J, Elledge SJ. 2001. ATR and ATRIP: partners in checkpoint signaling. Science 294: 1713-1716.
8. Costanzo V, Shechter D, Lupardus PJ, Cimprich KA, Gottesman M, Gautier J. 2003. An ATR-and Cdc7-dependent DNA damage checkpoint that inhibits initiation of DNA replication. Mol Cell 11: 203-213.
9. Cotta-Ramusino C, McDonald ER 3rd, Hurov K, Sowa ME, Harper JW, Elledge SJ. 2011. A DNA damage response screen identifies RHINO, a 9-1-1 and TopBP1 interacting protein required for ATR signaling. Science 332: 1313-1317.
10. Cremona CA, Sarangi P, Yang Y, Hang LE, Rahman S, Zhao X. 2012. Extensive DNA damage-induced sumoylation contributes to replication and repair and acts in addition to the mec1 checkpoint. Mol Cell 45: 422-432.
11. Delacroix S, Wagner JM, Kobayashi M, Yamamoto K, Karnitz LM. 2007. The Rad9-Hus1-Rad1 (9-1-1) clamp activates checkpoint signaling via TopBP1. Genes Dev 21: 1472-1477.
12. Dou H, Huang C, Singh M, Carpenter PB, Yeh ET. 2010. Regulation of DNA repair through deSUMOylation and SUMOylation of replication protein A complex. Mol Cell 39: 333-345.
13. Duursma AM, Driscoll R, Elias JE, Cimprich KA. 2013. A role for the MRN complex in ATR activation via TOPBP1 recruitment. Mol Cell 50: 116-122.
14. Ellison V, Stillman B. 2003. Biochemical characterization of DNA damage checkpoint complexes: clamp loader and clamp complexes with specificity for 59 recessed DNA. PLoS Biol 1: E33.
15. Flynn RL, Zou L. 2011. ATR: a master conductor of cellular responses to DNA replication stress. Trends Biochem Sci 36: 133-140.
16. Galanty Y, Belotserkovskaya R, Coates J, Polo S, Miller KM, Jackson SP. 2009. Mammalian SUMO E3-ligases PIAS1 and PIAS4 promote responses to DNA double-strand breaks. Nature 462: 935-939.
17. Galanty Y, Belotserkovskaya R, Coates J, Jackson SP. 2012. RNF4, a SUMO-targeted ubiquitin E3 ligase, promotes DNA double-strand break repair. Genes Dev 26: 1179-1195.
18. Gareau JR, Lima CD. 2010. The SUMO pathway: emerging mechanisms that shape specificity, conjugation and recognition. Nat Rev Mol Cell Biol 11: 861-871.
19. Golebiowski F, Matic I, Tatham MH, Cole C, Yin Y, Nakamura A, Cox J, Barton GJ, Mann M, Hay RT. 2009. System-wide changes to SUMO modifications in response to heat shock. Sci Signal 2: ra24.
20. Guzzo CM, Berndsen CE, Zhu J, Gupta V, Datta A, Greenberg RA, Wolberger C, Matunis MJ. 2012. RNF4-dependent hybrid SUMO-ubiquitin chains are signals for RAP80 and thereby mediate the recruitment of BRCA1 to sites of DNA damage. Sci Signal 5: ra88.
21. Hu X, Paul A, Wang B. 2012. Rap80 protein recruitment to DNA double-strand breaks requires binding to both small ubiquitinlike modifier (SUMO) and ubiquitin conjugates. J Biol Chem 287: 25510-25519.
22. Huen MS, Sy SM, Chen J. 2010. BRCA1 and its toolbox for the maintenance of genome integrity. Nat Rev Mol Cell Biol 11: 138-148.
23. Hurov KE, Cotta-Ramusino C, Elledge SJ. 2010. A genetic screen identifies the triple T complex required for DNA damage signaling and ATM and ATR stability. Genes Dev 24: 1939-1950.
24. Jackson SP, Durocher D. 2013. Regulation of DNA damage responses by ubiquitin and SUMO. Mol Cell 49: 795-807.
25. Jazayeri A, Falck J, Lukas C, Bartek J, Smith GC, Lukas J, Jackson SP. 2006. ATM-and cell cycle-dependent regulation of ATR in response to DNA double-strand breaks. Nat Cell Biol 8: 37-45.
26. Kondo S, Perrimon N. 2011. A genome-wide RNAi screen identifies core components of the G(2)-M DNA damage checkpoint. Sci Signal 4: rs1.
27. Kumagai A, Dunphy WG. 2003. Repeated phosphopeptide motifs in Claspin mediate the regulated binding of Chk1. Nat Cell Biol 5: 161-165.
28. Kumagai A, Kim SM, Dunphy WG. 2004. Claspin and the activated form of ATR-ATRIP collaborate in the activation of Chk1. J Biol Chem 279: 49599-49608.
29. Kumagai A, Lee J, Yoo HY, Dunphy WG. 2006. TopBP1 activates the ATR-ATRIP complex. Cell 124: 943-955.
30. Lee J, Dunphy WG. 2010. Rad17 plays a central role in establishment of the interaction between TopBP1 and the Rad9-Hus1-Rad1 complex at stalled replication forks. Mol Biol Cell 21: 926-935.
31. Lee J, Dunphy WG. 2013. The Mre11-Rad50-Nbs1 (MRN) complex has a specific role in the activation of Chk1 in response to stalled replication forks. Mol Biol Cell 24: 1343-1353.
32. Liu S, Shiotani B, Lahiri M, Marechal A, Tse A, Leung CC, Glover JN, Yang XH, Zou L. 2011. ATR autophosphorylation as a molecular switch for checkpoint activation. Mol Cell 43: 192-202.
33. Liu S, Ho CK, Ouyang J, Zou L. 2013. Nek1 kinase associates with ATR-ATRIP and primes ATR for efficient DNA damage signaling. Proc Natl Acad Sci 110: 2175-2180.
34. Lukas J, Lukas C, Bartek J. 2011. More than just a focus: the chromatin response to DNA damage and its role in genome integrity maintenance. Nat Cell Biol 13: 1161-1169.
35. Luo K, Zhang H, Wang L, Yuan J, Lou Z. 2012. Sumoylation of MDC1 is important for proper DNA damage response. EMBO J 31: 3008-3019.
36. Marechal A, Zou L. 2013. DNA damage sensing by the ATM and ATR kinases. Cold Spring Harb Perspect Biol 5: a012716.
37. Marechal A, Li JM, Ji XY, Wu CS, Yazinski SA, Nguyen HD, Liu S, Jimenez AE, Jin J, Zou L. 2014. PRP19 transforms into a sensor of RPA-ssDNA after DNA damage and drives ATR activation via a ubiquitin-mediated circuitry. Mol Cell 53: 235-246.
38. Mordes DA, Glick GG, Zhao R, Cortez D. 2008. TopBP1 activates ATR through ATRIP and a PIKK regulatory domain. Genes Dev 22: 1478-1489.
39. Morris JR. 2010. SUMO in the mammalian response to DNA damage. Biochem Soc Trans 38: 92-97.
40. Morris JR, Boutell C, Keppler M, Densham R, Weekes D, Alamshah A, Butler L, Galanty Y, Pangon L, Kiuchi T, et al. 2009. The SUMO modification pathway is involved in the BRCA1 response to genotoxic stress. Nature 462: 886-890.
41. Myers JS, Cortez D. 2006. Rapid activation of ATR by ionizing radiation requires ATM and Mre11. J Biol Chem 281: 9346-9350.
42. Namiki Y, Zou L. 2006. ATRIP associates with replication protein A-coated ssDNA through multiple interactions. Proc Natl Acad Sci 103: 580-585.
43. Oakley GG, Tillison K, Opiyo SA, Glanzer JG, Horn JM, Patrick SM. 2009. Physical interaction between replication protein A (RPA) and MRN: involvement of RPA2 phosphorylation and the N-terminus of RPA1. Biochemistry 48: 7473-7481.
44. Olson E, Nievera CJ, Lee AY, Chen L, Wu X. 2007a. The Mre11-Rad50-Nbs1 complex acts both upstream and downstream of ataxia telangiectasia mutated and Rad3-related protein (ATR) to regulate the S-phase checkpoint following UV treatment. J Biol Chem 282: 22939-22952.
45. Olson E, Nievera CJ, Liu E, Lee AY, Chen L, Wu X. 2007b. The Mre11 complex mediates the S-phase checkpoint through an interaction with replication protein A. Mol Cell Biol 27: 6053-6067.
46. Ouyang J, Shi Y, Valin A, Xuan Y, Gill G. 2009a. Direct binding of CoREST1 to SUMO-2/3 contributes to gene-specific repression by the LSD1/CoREST1/HDAC complex. Mol Cell 34: 145-154.
47. Ouyang KJ, Woo LL, Zhu J, Huo D, Matunis MJ, Ellis NA. 2009b. SUMO modification regulates BLM and RAD51 interaction at damaged replication forks. PLoS Biol 7: e1000252.
48. Psakhye I, Jentsch S. 2012. Protein group modification and synergy in the SUMO pathway as exemplified in DNA repair. Cell 151: 807-820.
49. Ren J, Gao X, Jin C, Zhu M, Wang X, Shaw A, Wen L, Yao X, Xue Y. 2009. Systematic study of protein sumoylation: development of a site-specific predictor of SUMOsp 2.0. Proteomics 9: 3409-3412.
50. Shiloh Y, Ziv Y. 2013. The ATM protein kinase: regulating the cellular response to genotoxic stress, and more. Nat Rev Mol Cell Biol 14: 197-210.
51. Shiotani B, Nguyen HD, Hakansson P, Marechal A, Tse A, Tahara H, Zou L. 2013. Two distinct modes of ATR activation orchestrated by Rad17 and Nbs1. Cell Rep 3: 1651-1662.
52. Smith KD, Fu MA, Brown EJ. 2009. Tim-Tipin dysfunction creates an indispensible reliance on the ATR-Chk1 pathway for continued DNA synthesis. J Cell Biol 187: 15-23.
53. Stiff T, Reis C, Alderton GK, Woodbine L, O'Driscoll M, Jeggo PA. 2005. Nbs1 is required for ATR-dependent phosphorylation events. EMBO J 24: 199-208.
54. Takai H, Wang RC, Takai KK, Yang H, de Lange T. 2007. Tel2 regulates the stability of PI3K-related protein kinases. Cell 131: 1248-1259.
55. Takai H, Xie Y, de Lange T, Pavletich NP. 2010. Tel2 structure and function in the Hsp90-dependent maturation of mTOR and ATR complexes. Genes Dev 24: 2019-2030.
56. Unsal-Kacmaz K, Mullen TE, Kaufmann WK, Sancar A. 2005. Coupling of human circadian and cell cycles by the timeless protein. Mol Cell Biol 25: 3109-3116.
57. Unsal-Kacmaz K, Chastain PD, Qu PP, Minoo P, Cordeiro-Stone M, Sancar A, Kaufmann WK. 2007. The human Tim/Tipin complex coordinates an Intra-S checkpoint response to UV that slows replication fork displacement. Mol Cell Biol 27: 3131-3142.
58. Wang X, Zou L, Lu T, Bao S, Hurov KE, Hittelman WN, Elledge SJ, Li L. 2006. Rad17 phosphorylation is required for claspin recruitment and Chk1 activation in response to replication stress. Mol Cell 23: 331-341.
59. Yan S, Michael WM. 2009. TopBP1 and DNA polymerase-a directly recruit the 9-1-1 complex to stalled DNA replication forks. J Cell Biol 184: 793-804.
60. Yin Y, Seifert A, Chua JS, Maure JF, Golebiowski F, Hay RT. 2012. SUMO-targeted ubiquitin E3 ligase RNF4 is required for the response of human cells to DNA damage. Genes Dev 26: 1196-1208.
61. Yoo HY, Kumagai A, Shevchenko A, Dunphy WG. 2009. The Mre11-Rad50-Nbs1 complex mediates activation of TopBP1 by ATM. Mol Biol Cell 20: 2351-2360.
62. Zou L, Elledge SJ. 2003. Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 300: 1542-1548.
63. Zou L, Cortez D, Elledge SJ. 2002. Regulation of ATR substrate selection by Rad17-dependent loading of Rad9 complexes onto chromatin. Genes Dev 16: 198-208.
64. Zou L, Liu D, Elledge SJ. 2003. Replication protein A-mediated recruitment and activation of Rad17 complexes. Proc Natl Acad Sci 100: 13827-13832.