SUMO-mediated regulation of DNA damage repair and responses

Trends in Biochemical Sciences

Volumn 40, Issue 4, 2015, Pages 233-242

  Sarangi, Prabha ^a,b   Zhao, Xiaolan ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b Weill Cornell Graduate School of Biomedical Sciences   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SUMO PROTEIN; SUMO 1 PROTEIN;

CHROMATIN ASSEMBLY AND DISASSEMBLY; CONFORMATIONAL TRANSITION; DNA DAMAGE; DNA METABOLISM; DNA MODIFICATION; DNA PROTEIN COMPLEX; DNA REPAIR; DNA REPLICATION; MOLECULAR MODEL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DNA BINDING; PROTEIN DNA INTERACTION; PROTEIN FUNCTION; REVIEW; SUMOYLATION; TRANSCRIPTION REGULATION; ANIMAL; GENETICS; HUMAN; METABOLISM; PHYSIOLOGY; PROTEIN PROCESSING;

ANIMALS; DNA REPAIR; HUMANS; PROTEIN PROCESSING, POST-TRANSLATIONAL; SUMO-1 PROTEIN; SUMOYLATION;

EID: 84925297959     PISSN: 09680004     EISSN: 13624326     Source Type: Journal    
DOI: 10.1016/j.tibs.2015.02.006     Document Type: Review

References (120)

1. Kerscher O., et al. Modification of proteins by ubiquitin and ubiquitin-like proteins. Annu. Rev. Cell Dev. Biol. 2006, 22:159-180.
2. Geiss-Friedlander R., et al. Concepts in sumoylation: a decade on. Nat. Rev. Mol. Cell Biol. 2007, 8:947-956.
3. Hay R.T. SUMO: a history of modification. Mol. Cell 2005, 18:1-12.
4. Johnson E.S. Protein modification by SUMO. Annu. Rev. Biochem. 2004, 73:355-382.
5. Cremona C.A., et al. Extensive DNA damage-induced sumoylation contributes to replication and repair and acts in addition to the Mec1 checkpoint. Mol. Cell 2012, 45:422-432.
6. Psakhye I., et al. Protein group modification and synergy in the SUMO pathway as exemplified in DNA repair. Cell 2012, 151:807-820.
7. Miller M.J., et al. Proteomic analyses identify a diverse array of nuclear processes affected by small ubiquitin-like modifier conjugation in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:16512-16517.
8. Elrouby N., et al. Proteome-wide screens for small ubiquitin-like modifier (SUMO) substrates identify Arabidopsis proteins implicated in diverse biological processes. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:17415-17420.
9. Ma L., et al. Identification of small ubiquitin-like modifier substrates with diverse functions using the Xenopus egg extract system. Mol. Cell. Proteomics 2014, 13:1659-1675.
10. Lamoliatte F., et al. Large-scale analysis of lysine SUMOylation by SUMO remnant immunoaffinity profiling. Nat. Commun. 2014, 5:5409.
11. Tammsalu T., et al. Proteome-wide identification of SUMO2 modification sites. Sci. Signal. 2014, 7:rs2.
12. Tatham M.H., et al. Comparative proteomic analysis identifies a role for SUMO in protein quality control. Sci. Signal. 2011, 4:rs4.
13. Cubenas-Potts C., et al. Identification of SUMO-2/3 modified proteins associated with mitotic chromosomes. Proteomics 2014, 15:763-772.
14. Hendriks I.A., et al. Uncovering global SUMOylation signaling networks in a site-specific manner. Nat. Struct. Mol. Biol. 2014, 21:927-936.
15. Schimmel J., et al. Uncovering SUMOylation dynamics during cell-cycle progression reveals FoxM1 as a key mitotic SUMO target protein. Mol. Cell 2014, 53:1053-1066.
16. Matic I., et al. Site-specific identification of SUMO-2 targets in cells reveals an inverted SUMOylation motif and a hydrophobic cluster SUMOylation motif. Mol. Cell 2010, 39:641-652.
17. Becker J., et al. Detecting endogenous SUMO targets in mammalian cells and tissues. Nat. Struct. Mol. Biol. 2013, 20:525-531.
18. Dou H., et al. SUMOylation and de-SUMOylation in response to DNA damage. FEBS Lett. 2011, 585:2891-2896.
19. Bergink S., et al. Principles of ubiquitin and SUMO modifications in DNA repair. Nature 2009, 458:461-467.
20. Smolka M.B., et al. Proteome-wide identification of in vivo targets of DNA damage checkpoint kinases. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:10364-10369.
21. Matsuoka S., et al. ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 2007, 316:1160-1166.
22. Chen S.H., et al. A proteome-wide analysis of kinase-substrate network in the DNA damage response. J. Biol. Chem. 2010, 285:12803-12812.
23. Kim W., et al. Systematic and quantitative assessment of the ubiquitin-modified proteome. Mol. Cell 2011, 44:325-340.
24. van Wijk S.J., et al. Shared and unique properties of ubiquitin and SUMO interaction networks in DNA repair. Genes Dev. 2011, 25:1763-1769.
25. Merbl Y., et al. Profiling of ubiquitin-like modifications reveals features of mitotic control. Cell 2013, 152:1160-1172.
26. Liu H., et al. A method for systematic mapping of protein lysine methylation identifies functions for HP1beta in DNA damage response. Mol. Cell 2013, 50:723-735.
27. Ulrich H.D. Two-way communications between ubiquitin-like modifiers and DNA. Nat. Struct. Mol. Biol. 2014, 21:317-324.
28. Jentsch S., et al. Control of nuclear activities by substrate-selective and protein-group SUMOylation. Annu. Rev. Genet. 2013, 47:167-186.
29. Jackson S.P., et al. Regulation of DNA damage responses by ubiquitin and SUMO. Mol. Cell 2013, 49:795-807.
30. Parker J.L., et al. SUMO modification of PCNA is controlled by DNA. EMBO J. 2008, 27:2422-2431.
31. Sinigalia E., et al. The human cytomegalovirus DNA polymerase processivity factor UL44 is modified by SUMO in a DNA-dependent manner. PLoS ONE 2012, 7:e49630.
32. Gibbs-Seymour I., et al. Ubiquitin-SUMO circuitry controls activated Fanconi Anemia ID complex dosage in response to DNA damage. Mol. Cell 2015, 57:150-164.
33. Sarangi P., et al. Sumoylation of the Rad1 nuclease promotes DNA repair and regulates its DNA association. Nucleic Acids Res. 2014, 42:6393-6404.
34. Hang L.E., et al. Regulation of Ku-DNA association by Yku70 C-terminal tail and SUMO modification. J. Biol. Chem. 2014, 289:10308-10317.
35. Moriyama T., et al. SUMO-modification and elimination of the active DNA demethylation enzyme TDG in cultured human cells. Biochem. Biophys. Res. Commun. 2014, 447:419-424.
36. Sacher M., et al. Control of Rad52 recombination activity by double-strand break-induced SUMO modification. Nat. Cell Biol. 2006, 8:1284-1290.
37. Hang L.E., et al. SUMOylation regulates telomere length homeostasis by targeting Cdc13. Nat. Struct. Mol. Biol. 2011, 18:920-926.
38. Azuma Y., et al. SUMO-2/3 regulates Topoisomerase II in mitosis. J. Cell Biol. 2003, 163:477-487.
39. Wang Q.E., et al. Ubiquitylation-independent sumoylation of Xeroderma pigmentosum group C protein is required for efficient nucleotide excision repair. Nucleic Acids Res. 2007, 35:5338-5350.
40. Horie K., et al. SUMO-1 conjugation to intact DNA Topoisomerase I amplifies cleavable complex formation induced by camptothecin. Oncogene 2002, 21:7913-7922.
41. Chen X.L., et al. Topoisomerase I-dependent viability loss in Saccharomyces cerevisiae mutants defective in both SUMO conjugation and DNA repair. Genetics 2007, 177:17-30.
42. Silver H.R., et al. A role for SUMO in nucleotide excision repair. DNA Repair 2011, 10:1243-1251.
43. Ohuchi T., et al. Rad52 sumoylation and its involvement in the efficient induction of homologous recombination. DNA Repair 2008, 7:879-889.
44. Altmannova V., et al. Rad52 SUMOylation affects the efficiency of the DNA repair. Nucleic Acids Res. 2010, 38:4708-4721.
45. Newman M., et al. Structure of an XPF endonuclease with and without DNA suggests a model for substrate recognition. EMBO J. 2005, 24:895-905.
46. Walker J.R., et al. Structure of the Ku heterodimer bound to DNA and its implications for double-strand break repair. Nature 2001, 412:607-614.
47. Rivera-Calzada A., et al. Structural model of full-length human Ku70-Ku80 heterodimer and its recognition of DNA and DNA-PKcs. EMBO Rep. 2007, 8:56-62.
48. Joo W., et al. Structure of the FANCI-FANCD2 complex: insights into the Fanconi anemia DNA repair pathway. Science 2011, 333:312-316.
49. Galanty Y., et al. Mammalian SUMO E3-ligases PIAS1 and PIAS4 promote responses to DNA double-strand breaks. Nature 2009, 462:935-939.
50. Morris J.R., et al. The SUMO modification pathway is involved in the BRCA1 response to genotoxic stress. Nature 2009, 462:886-890.
51. Wu S.Y., et al. Crosstalk between sumoylation and acetylation regulates p53-dependent chromatin transcription and DNA binding. EMBO J. 2009, 28:1246-1259.
52. Sarangi P., et al. Sumoylation influences DNA break repair partly by increasing the solubility of a conserved end resection protein. PLOS Genet. 2014, 11:e1004899.
53. Garg M., et al. Tpz1TPP1 SUMOylation reveals evolutionary conservation of SUMO-dependent Stn1 telomere association. EMBO Rep. 2014, 15:871-877.
54. Miyagawa K., et al. SUMOylation regulates telomere length by targeting the shelterin subunit Tpz1(Tpp1) to modulate shelterin-Stn1 interaction in fission yeast. Proc. Natl. Acad. Sci. U.S.A. 2014, 111:5950-5955.
55. Potts P.R., et al. The SMC5/6 complex maintains telomere length in ALT cancer cells through SUMOylation of telomere-binding proteins. Nat. Struct. Mol. Biol. 2007, 14:581-590.
56. Ferreira H.C., et al. The PIAS homologue Siz2 regulates perinuclear telomere position and telomerase activity in budding yeast. Nat. Cell Biol. 2011, 13:867-874.
57. Pelisch F., et al. Dynamic SUMO modification regulates mitotic chromosome assembly and cell cycle progression in Caenorhabditis elegans. Nat. Commun. 2014, 5:5485.
58. Binz S.K., et al. The phosphorylation domain of the 32-kDa subunit of replication protein A (RPA) modulates RPA-DNA interactions. Evidence for an intersubunit interaction. J. Biol. Chem. 2003, 278:35584-35591.
59. Unal E., et al. DNA damage response pathway uses histone modification to assemble a double-strand break-specific cohesin domain. Mol. Cell 2004, 16:991-1002.
60. Flott S., et al. Slx4 becomes phosphorylated after DNA damage in a Mec1/Tel1-dependent manner and is required for repair of DNA alkylation damage. Biochem. J. 2005, 391:325-333.
61. Herzberg K., et al. Phosphorylation of Rad55 on serines 2, 8, and 14 is required for efficient homologous recombination in the recovery of stalled replication forks. Mol. Cell. Biol. 2006, 26:8396-8409.
62. Chen X., et al. Cell cycle regulation of DNA double-strand break end resection by Cdk1-dependent Dna2 phosphorylation. Nat. Struct. Mol. Biol. 2011, 18:1015-1019.
63. Saugar I., et al. Temporal regulation of the Mus81-Mms4 endonuclease ensures cell survival under conditions of DNA damage. Nucleic Acids Res. 2013, 41:8943-8958.
64. Szakal B., et al. Premature Cdk1/Cdc5/Mus81 pathway activation induces aberrant replication and deleterious crossover. EMBO J. 2013, 32:1155-1167.
65. Lu C.S., et al. The RING finger protein RNF8 ubiquitinates Nbs1 to promote DNA double-strand break repair by homologous recombination. J. Biol. Chem. 2012, 287:43984-43994.
66. Tikoo S., et al. Ubiquitin-dependent recruitment of the Bloom syndrome helicase upon replication stress is required to suppress homologous recombination. EMBO J. 2013, 32:1778-1792.
67. Feng L., et al. The E3 ligase RNF8 regulates KU80 removal and NHEJ repair. Nat. Struct. Mol. Biol. 2012, 19:201-206.
68. Smogorzewska A., et al. Identification of the FANCI protein, a monoubiquitinated FANCD2 paralog required for DNA repair. Cell 2007, 129:289-301.
69. Flotho A., et al. Sumoylation: a regulatory protein modification in health and disease. Annu. Rev. Biochem. 2013, 82:357-385.
70. Bergink S., et al. Role of Cdc48/p97 as a SUMO-targeted segregase curbing Rad51-Rad52 interaction. Nat. Cell Biol. 2013, 15:526-532.
71. Shen T.H., et al. The mechanisms of PML-nuclear body formation. Mol. Cell 2006, 24:331-339.
72. Wu C.S., et al. SUMOylation of ATRIP potentiates DNA damage signaling by boosting multiple protein interactions in the ATR pathway. Genes Dev. 2014, 28:1472-1484.
73. Guervilly J.H., et al. The SLX4 complex is a SUMO E3 ligase that impacts on replication stress outcome and genome stability. Mol. Cell 2015, 57:123-137.
74. Ouyang J., et al. Noncovalent interactions with SUMO and ubiquitin orchestrate distinct functions of the SLX4 complex in genome maintenance. Mol. Cell 2015, 57:108-122.
75. Bernardi R., et al. Structure, dynamics and functions of promyelocytic leukaemia nuclear bodies. Nat. Rev. Mol. Cell. Biol. 2007, 8:1006-1016.
76. Pfander B., et al. SUMO-modified PCNA recruits Srs2 to prevent recombination during S phase. Nature 2005, 436:428-433.
77. Papouli E., et al. Crosstalk between SUMO and ubiquitin on PCNA is mediated by recruitment of the helicase Srs2p. Mol. Cell 2005, 19:123-133.
78. Xie Y., et al. The yeast Hex3.Slx8 heterodimer is a ubiquitin ligase stimulated by substrate sumoylation. J. Biol. Chem. 2007, 282:34176-34184.
79. Song J., et al. Identification of a SUMO-binding motif that recognizes SUMO-modified proteins. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:14373-14378.
80. Kolesar P., et al. Dual roles of the SUMO-interacting motif in the regulation of Srs2 sumoylation. Nucleic Acids Res. 2012, 40:7831-7843.
81. Krumova P., et al. Sumoylation inhibits alpha-synuclein aggregation and toxicity. J. Cell Biol. 2011, 194:49-60.
82. Janer A., et al. SUMOylation attenuates the aggregation propensity and cellular toxicity of the polyglutamine expanded Ataxin-7. Hum. Mol. Genet. 2010, 19:181-195.
83. Sarangi P., et al. A versatile scaffold contributes to damage survival via sumoylation and nuclease interactions. Cell Rep. 2014, 9:143-152.
84. Moldovan G.L., et al. PCNA controls establishment of sister chromatid cohesion during S phase. Mol. Cell 2006, 23:723-732.
85. Ciccia A., et al. The DNA damage response: making it safe to play with knives. Mol. Cell 2010, 40:179-204.
86. Ulrich H.D., et al. Ubiquitin signalling in DNA replication and repair. Nat. Rev. Mol. Cell Biol. 2010, 11:479-489.
87. Polo S.E., et al. Dynamics of DNA damage response proteins at DNA breaks: a focus on protein modifications. Genes Dev. 2011, 25:409-433.
88. Hardeland U., et al. Modification of the human Thymine-DNA Glycosylase by ubiquitin-like proteins facilitates enzymatic turnover. EMBO J. 2002, 21:1456-1464.
89. Vigasova D., et al. Lif1 SUMOylation and its role in non-homologous end-joining. Nucleic Acids Res. 2013, 41:5341-5353.
90. Sridharan V., et al. SUMOylation regulates Polo-like Kinase 1-interacting Checkpoint Helicase (PICH) during mitosis. J. Biol. Chem. 2015, 290:3269-3276.
91. Steinacher R., et al. Functionality of human Thymine DNA Glycosylase requires SUMO-regulated changes in protein conformation. Curr. Biol. 2005, 15:616-623.
92. Bowles M., et al. Fluorescence-based incision assay for human XPF-ERCC1 activity identifies important elements of DNA junction recognition. Nucleic Acids Res. 2012, 40:e101.
93. Luo K., et al. Sumoylation of MDC1 is important for proper DNA damage response. EMBO J. 2012, 31:3008-3019.
94. Gronholm J., et al. Structure-function analysis indicates that sumoylation modulates DNA-binding activity of STAT1. BMC Biochem. 2012, 13:20.
95. Sutinen P., et al. Nuclear mobility and activity of FOXA1 with androgen receptor are regulated by SUMOylation. Mol. Endocrinol. 2014, 28:1719-1728.
96. Rosonina E., et al. Sumoylation of transcription factor Gcn4 facilitates its Srb10-mediated clearance from promoters in yeast. Genes Dev. 2012, 26:350-355.
97. Takahashi Y., et al. SIZ1/SIZ2 control of chromosome transmission fidelity is mediated by the sumoylation of Topoisomerase II. Genetics 2006, 172:783-794.
98. Bayer P., et al. Structure determination of the small ubiquitin-related modifier SUMO-1. J. Mol. Biol. 1998, 280:275-286.
99. Eilebrecht S., et al. SUMO-1 possesses DNA binding activity. BMC Res. Notes 2010, 3:146.
100. Bekker-Jensen S., et al. The ubiquitin- and SUMO-dependent signaling response to DNA double-strand breaks. FEBS Lett. 2011, 585:2914-2919.
101. Danielsen J.R., et al. DNA damage-inducible SUMOylation of HERC2 promotes RNF8 binding via a novel SUMO-binding Zinc finger. J. Cell Biol. 2012, 197:179-187.
102. Ismail I.H., et al. CBX4-mediated SUMO modification regulates BMI1 recruitment at sites of DNA damage. Nucleic Acids Res. 2012, 40:5497-5510.
103. Guzzo C.M., et al. RNF4-dependent hybrid SUMO-ubiquitin chains are signals for RAP80 and thereby mediate the recruitment of BRCA1 to sites of DNA damage. Sci. Signal. 2012, 5:ra88.
104. Hu X., et al. Rap80 protein recruitment to DNA double-strand breaks requires binding to both small ubiquitin-like modifier (SUMO) and ubiquitin conjugates. J. Biol. Chem. 2012, 287:25510-25519.
105. Kim Y., et al. Mutations of the SLX4 gene in Fanconi anemia. Nat. Genet. 2011, 43:142-146.
106. Lachaud C., et al. Distinct functional roles for the two SLX4 ubiquitin-binding UBZ domains mutated in Fanconi anemia. J. Cell Sci. 2014, 127:2811-2817.
107. Ragland R.L., et al. RNF4 and PLK1 are required for replication fork collapse in ATR-deficient cells. Genes Dev. 2013, 27:2259-2273.
108. Chen X., et al. Rpb1 sumoylation in response to UV radiation or transcriptional impairment in yeast. PLoS ONE 2009, 4:e5267.
109. Guo Z., et al. Sequential posttranslational modifications program FEN1 degradation during cell-cycle progression. Mol. Cell 2012, 47:444-456.
110. Dou H., et al. Regulation of DNA repair through deSUMOylation and SUMOylation of Replication Protein A complex. Mol. Cell 2010, 39:333-345.
111. Yurchenko V., et al. SUMO modification of human XRCC4 regulates its localization and function in DNA double-strand break repair. Mol. Cell. Biol. 2006, 26:1786-1794.
112. Hudson J.J., et al. SUMO modification of the neuroprotective protein TDP1 facilitates chromosomal single-strand break repair. Nat. Commun. 2012, 3:733.
113. Bachant J., et al. The SUMO-1 isopeptidase Smt4 is linked to centromeric cohesion through SUMO-1 modification of DNA Topoisomerase II. Mol. Cell 2002, 9:1169-1182.
114. Takahashi Y., et al. In vivo modeling of polysumoylation uncovers targeting of Topoisomerase II to the nucleolus via optimal level of SUMO modification. Chromosoma 2008, 117:189-198.
115. Eladad S., et al. Intra-nuclear trafficking of the BLM helicase to DNA damage-induced foci is regulated by SUMO modification. Hum. Mol. Genet. 2005, 14:1351-1365.
116. Ouyang K.J., et al. SUMO modification regulates BLM and RAD51 interaction at damaged replication forks. PLoS Biol. 2009, 7:e1000252.
117. Torres-Rosell, et al. The Smc5-Smc6 complex and SUMO modification of Rad52 regulates recombinational repair at the ribosomal gene locus. Nat. Cell Biol. 2007, 9:923-931.
118. Baba D., et al. Crystal structure of Thymine DNA Glycosylase conjugated to SUMO-1. Nature 2005, 435:979-982.
119. Baba D., et al. Crystal structure of SUMO-3-modified Thymine-DNA Glycosylase. J. Mol. Biol. 2006, 359:137-147.
120. Smet-Nocca C., et al. SUMO-1 regulates the conformational dynamics of Thymine-DNA Glycosylase regulatory domain and competes with its DNA binding activity. BMC Biochem. 2011, 12:4.