Single-molecule imaging reveals the mechanism of Exo1 regulation by single-stranded DNA binding proteins

Proceedings of the National Academy of Sciences of the United States of America

Volumn 113, Issue 9, 2016, Pages E1170-E1179

  Myler, Logan R ^a   Gallardo, Ignacio F ^a   Zhou, Yi ^a   Gong, Fade ^a   Yang, Soo Hyun ^a   Wold, Marc S ^b   Miller, Kyle M ^a   Paull, Tanya T ^a   Finkelstein, Ilya J ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b UNIVERSITY OF IOWA   (United States)

Author keywords

DNA curtains; DNA repair; Nuclease; Resection; Single molecule

Indexed keywords

EXONUCLEASE; EXONUCLEASE 1; FUNGAL ENZYME; POLYPEPTIDE; RPA1 PROTEIN; RPA2 PROTEIN; RPA3 PROTEIN; SINGLE STRANDED DNA BINDING PROTEIN; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; DNA LIGASE; EXO1 PROTEIN, HUMAN; EXODEOXYRIBONUCLEASE; EXODEOXYRIBONUCLEASE I;

ARTICLE; CATALYSIS; CYTOLOGY; DNA BINDING; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; ENZYME INHIBITION; ENZYME REGULATION; FLUORESCENCE IMAGING; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; YEAST; BIOCATALYSIS; METABOLISM; PHYSIOLOGY; SACCHAROMYCES CEREVISIAE;

BIOCATALYSIS; DNA DAMAGE; DNA REPAIR ENZYMES; DNA-BINDING PROTEINS; EXODEOXYRIBONUCLEASES; HUMANS; SACCHAROMYCES CEREVISIAE;

EID: 84959525609     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1516674113     Document Type: Article

References (79)

1. Mimitou EP, Symington LS (2011) DNA end resection - Unraveling the tail. DNA Repair (Amst) 10(3):344-348.
2. Goellner EM, Putnam CD, Kolodner RD (2015) Exonuclease 1-dependent and independent mismatch repair. DNA Repair (Amst) 32:24-32.
3. Tran PT, Erdeniz N, Symington LS, Liskay RM (2004) EXO1 - A multi-tasking eukaryotic nuclease. DNA Repair (Amst) 3(12):1549-1559.
4. Genschel J, Bazemore LR, Modrich P (2002) Human exonuclease I is required for 5′ and 3′ mismatch repair. J Biol Chem 277(15):13302-13311.
5. Genschel J, Modrich P (2003) Mechanism of 5′-directed excision in human mismatch repair. Mol Cell 12(5):1077-1086.
6. Szankasi P, Smith GR (1995) A role for exonuclease I from S. pombe in mutation avoidance and mismatch correction. Science 267(5201):1166-1169.
7. Shao H, Baitinger C, Soderblom EJ, Burdett V, Modrich P (2014) Hydrolytic function of Exo1 in mammalian mismatch repair. Nucleic Acids Res 42(11):7104-7112.
8. Liberti SE, Rasmussen LJ (2004) Is hEXO1 a cancer predisposing gene? Mol Cancer Res 2(8):427-432.
9. Wei K, et al. (2003) Inactivation of Exonuclease 1 in mice results in DNA mismatch repair defects, increased cancer susceptibility, and male and female sterility. Genes Dev 17(5):603-614.
10. Eid W, et al. (2010) DNA end resection by CtIP and exonuclease 1 prevents genomic instability. EMBO Rep 11(12):962-968.
11. Tomimatsu N, et al. (2012) Exo1 plays a major role in DNA end resection in humans and influences double-strand break repair and damage signaling decisions. DNA Repair (Amst) 11(4):441-448.
12. Zhou Y, Caron P, Legube G, Paull TT (2014) Quantitation of DNA double-strand break resection intermediates in human cells. Nucleic Acids Res 42(3):e19-e19.
13. Tong AHY, et al. (2004) Global mapping of the yeast genetic interaction network. Science 303(5659):808-813.
14. Wold MS (1997) Replication protein A: A heterotrimeric, single-stranded DNA-binding protein required for eukaryotic DNA metabolism. Annu Rev Biochem 66(1):61-92.
15. Chen H, Lisby M, Symington LS (2013) RPA coordinates DNA end resection and prevents formation of DNA hairpins. Mol Cell 50(4):589-600.
16. Hass CS, Lam K, Wold MS (2012) Repair-specific functions of replication protein A. J Biol Chem 287(6):3908-3918.
17. Lisby M, Barlow JH, Burgess RC, Rothstein R (2004) Choreography of the DNA damage response: Spatiotemporal relationships among checkpoint and repair proteins. Cell 118(6):699-713.
18. Cannavo E, Cejka P, Kowalczykowski SC (2013) Relationship of DNA degradation by Saccharomyces cerevisiae exonuclease 1 and its stimulation by RPA and Mre11-Rad50- Xrs2 to DNA end resection. Proc Natl Acad Sci USA 110(18):E1661-E1668.
19. Nimonkar AV, et al. (2011) BLM-DNA2-RPA-MRN and EXO1-BLM-RPA-MRN constitute two DNA end resection machineries for human DNA break repair. Genes Dev 25(4):350-362.
20. Niu H, et al. (2010) Mechanism of the ATP-dependent DNA end-resection machinery from Saccharomyces cerevisiae. Nature 467(7311):108-111.
21. Yang S-H, et al. (2013) The SOSS1 single-stranded DNA binding complex promotes DNA end resection in concert with Exo1. EMBO J 32(1):126-139.
22. Cejka P, et al. (2010) DNA end resection by Dna2-Sgs1-RPA and its stimulation by Top3-Rmi1 and Mre11-Rad50-Xrs2. Nature 467(7311):112-116.
23. Nicolette ML, et al. (2010) Mre11-Rad50-Xrs2 and Sae2 promote 5′ strand resection of DNA double-strand breaks. Nat Struct Mol Biol 17(12):1478-1485.
24. Richard DJ, et al. (2008) Single-stranded DNA-binding protein hSSB1 is critical for genomic stability. Nature 453(7195):677-681.
25. Huang J, Gong Z, Ghosal G, Chen J (2009) SOSS complexes participate in the maintenance of genomic stability. Mol Cell 35(3):384-393.
26. Ren W, et al. (2014) Structural basis of SOSS1 complex assembly and recognition of ssDNA. Cell Reports 6(6):982-991.
27. Richard DJ, et al. (2011) hSSB1 rapidly binds at the sites of DNA double-strand breaks and is required for the efficient recruitment of the MRN complex. Nucleic Acids Res 39(5):1692-1702.
28. Finkelstein IJ, Greene EC (2011) Supported lipid bilayers and DNA curtains for highthroughput single-molecule studies. Methods Mol Biol 745:447-461.
29. Finkelstein IJ, Visnapuu M-L, Greene EC (2010) Single-molecule imaging reveals mechanisms of protein disruption by a DNA translocase. Nature 468(7326):983-987.
30. Robison AD, Finkelstein IJ (2014) High-throughput single-molecule studies of protein- DNA interactions. FEBS Lett 588(19):3539-3546.
31. Nimonkar AV, Ozsoy AZ, Genschel J, Modrich P, Kowalczykowski SC (2008) Human exonuclease 1 and BLM helicase interact to resect DNA and initiate DNA repair. Proc Natl Acad Sci USA 105(44):16906-16911.
32. Orans J, et al. (2011) Structures of human exonuclease 1 DNA complexes suggest a unified mechanism for nuclease family. Cell 145(2):212-223.
33. Liao S, Guay C, Toczylowski T, Yan H (2012) Analysis of MRE11's function in the 5'->3′ processing of DNA double-strand breaks. Nucleic Acids Res 40(10):4496-4506.
34. Tran PT, Erdeniz N, Dudley S, Liskay RM (2002) Characterization of nuclease-dependent functions of Exo1p in Saccharomyces cerevisiae. DNA Repair (Amst) 1(11):895-912.
35. Tomimatsu N, et al. (2014) Phosphorylation of EXO1 by CDKs 1 and 2 regulates DNA end resection and repair pathway choice. Nat Commun 5:3561.
36. Chen X, Paudyal SC, Chin RI, You Z (2013) PCNA promotes processive DNA end resection by Exo1. Nucleic Acids Res 41(20):9325-9338.
37. Pathak S, Davidson MC, Silva GA (2007) Characterization of the functional binding properties of antibody conjugated quantum dots. Nano Lett 7(7):1839-1845.
38. Sertic S, et al. (2011) Human exonuclease 1 connects nucleotide excision repair (NER) processing with checkpoint activation in response to UV irradiation. Proc Natl Acad Sci USA 108(33):13647-13652.
39. Thompson RE, Larson DR, Webb WW (2002) Precise nanometer localization analysis for individual fluorescent probes. Biophys J 82(5):2775-2783.
40. Schmutte C, et al. (1998) Human exonuclease I interacts with the mismatch repair protein hMSH2. Cancer Res 58(20):4537-4542.
41. Schmutte C, Sadoff MM, Shim K-S, Acharya S, Fishel R (2001) The interaction of DNA mismatch repair proteins with human exonuclease I. J Biol Chem 276(35): 33011-33018.
42. Genschel J, Modrich P (2009) Functions of MutLalpha, replication protein A (RPA), and HMGB1 in 5′-directed mismatch repair. J Biol Chem 284(32):21536-21544.
43. Chen R, Wold MS (2014) Replication protein A: Single-stranded DNA's first responder: Dynamic DNA-interactions allow replication protein A to direct single-strand DNA intermediates into different pathways for synthesis or repair. BioEssays 36(12): 1156-1161.
44. Modesti M (2011) Fluorescent labeling of proteins. Methods Mol Biol 783:101-120.
45. Brosey CA, et al. (2013) A new structural framework for integrating replication protein A into DNA processing machinery. Nucleic Acids Res 41(4):2313-2327.
46. Kim C, Snyder RO, Wold MS (1992) Binding properties of replication protein A from human and yeast cells. Mol Cell Biol 12(7):3050-3059.
47. Wyka IM, Dhar K, Binz SK, Wold MS (2003) Replication protein A interactions with DNA: Differential binding of the core domains and analysis of the DNA interaction surface. Biochemistry 42(44):12909-12918.
48. Haring SJ, Mason AC, Binz SK, Wold MS (2008) Cellular functions of human RPA1. Multiple roles of domains in replication, repair, and checkpoints. J Biol Chem 283(27): 19095-19111.
49. Binz SK, Wold MS (2008) Regulatory functions of the N-terminal domain of the 70-kDa subunit of replication protein A (RPA). J Biol Chem 283(31):21559-21570.
50. Glanzer JG, et al. (2013) A small molecule directly inhibits the p53 transactivation domain from binding to replication protein A. Nucleic Acids Res 41(3):2047-2059.
51. Iacovoni JS, et al. (2010) High-resolution profiling of gammaH2AX around DNA double strand breaks in the mammalian genome. EMBO J 29(8):1446-1457.
52. Miller KM, et al. (2010) Human HDAC1 and HDAC2 function in the DNA-damage response to promote DNA nonhomologous end-joining. Nat Struct Mol Biol 17(9): 1144-1151.
53. Zhou Y, Paull TT (2015) Direct measurement of single-stranded DNA intermediates in mammalian cells by quantitative polymerase chain reaction. Anal Biochem 479: 48-50.
54. Fiorentini P, Huang KN, Tishkoff DX, Kolodner RD, Symington LS (1997) Exonuclease I of Saccharomyces cerevisiae functions in mitotic recombination in vivo and in vitro. Mol Cell Biol 17(5):2764-2773.
55. Wilson DM, 3rd, et al. (1998) Hex1: A new human Rad2 nuclease family member with homology to yeast exonuclease 1. Nucleic Acids Res 26(16):3762-3768.
56. Gibb B, et al. (2014) Concentration-dependent exchange of replication protein A on single-stranded DNA revealed by single-molecule imaging. PLoS One 9(2):e87922.
57. Nguyen B, et al. (2014) Diffusion of human replication protein A along singlestranded DNA. J Mol Biol 426(19):3246-3261.
58. Tsutakawa SE, et al. (2011) Human flap endonuclease structures, DNA double-base flipping, and a unified understanding of the FEN1 superfamily. Cell 145(2):198-211.
59. Liu Y, Kao H-I, Bambara RA (2004) Flap endonuclease 1: A central component of DNA metabolism. Annu Rev Biochem 73(1):589-615.
60. Ray S, Bandaria JN, Qureshi MH, Yildiz A, Balci H (2014) G-quadruplex formation in telomeres enhances POT1/TPP1 protection against RPA binding. Proc Natl Acad Sci USA 111(8):2990-2995.
61. Rossi ML, et al. (2008) Pif1 helicase directs eukaryotic Okazaki fragments toward the two-nuclease cleavage pathway for primer removal. J Biol Chem 283(41):27483-27493.
62. Bae S-H, Bae K-H, Kim J-A, Seo Y-S (2001) RPA governs endonuclease switching during processing of Okazaki fragments in eukaryotes. Nature 412(6845):456-461.
63. Unciuleac MC, Shuman S (2010) Double strand break unwinding and resection by the mycobacterial helicase-nuclease AdnAB in the presence of single strand DNA-binding protein (SSB). J Biol Chem 285(45):34319-34329.
64. Roberts JA, White MF (2005) DNA end-directed and processive nuclease activities of the archaeal XPF enzyme. Nucleic Acids Res 33(20):6662-6670.
65. Gradia S, et al. (1999) hMSH2-hMSH6 forms a hydrolysis-independent sliding clamp on mismatched DNA. Mol Cell 3(2):255-261.
66. Bowen N, et al. (2013) Reconstitution of long and short patch mismatch repair reactions using Saccharomyces cerevisiae proteins. Proc Natl Acad Sci USA 110(46): 18472-18477.
67. Adkins NL, Niu H, Sung P, Peterson CL (2013) Nucleosome dynamics regulates DNA processing. Nat Struct Mol Biol 20(7):836-842.
68. Couch FB, et al. (2013) ATR phosphorylates SMARCAL1 to prevent replication fork collapse. Genes Dev 27(14):1610-1623.
69. Driscoll R, Cimprich KA (2009) HARPing on about the DNA damage response during replication. Genes Dev 23(20):2359-2365.
70. Peterson SE, et al. (2013) Activation of DSB processing requires phosphorylation of CtIP by ATR. Mol Cell 49(4):657-667.
71. Shiotani B, et al. (2013) Two distinct modes of ATR activation orchestrated by Rad17 and Nbs1. Cell Reports 3(5):1651-1662.
72. Lee JY, Finkelstein IJ, Crozat E, Sherratt DJ, Greene EC (2012) Single-molecule imaging of DNA curtains reveals mechanisms of KOPS sequence targeting by the DNA translocase FtsK. Proc Natl Acad Sci USA 109(17):6531-6536.
73. Efron B, Tibshirani RJ (1993) An Introduction to the Bootstrap (Chapman and Hall/ CRC, New York).
74. Beckett D, Kovaleva E, Schatz PJ (1999) A minimal peptide substrate in biotin holoenzyme synthetase-catalyzed biotinylation. Protein Sci 8(4):921-929.
75. Horn R (1987) Statistical methods for model discrimination. Applications to gating kinetics and permeation of the acetylcholine receptor channel. Biophys J 51(2):255-263.
76. Shee C, et al. (2013) Engineered proteins detect spontaneous DNA breakage in human and bacterial cells. eLife 2:e01222.
77. Gong F, et al. (2015) Screen identifies bromodomain protein ZMYND8 in chromatin recognition of transcription-associated DNA damage that promotes homologous recombination. Genes Dev 29(2):197-211.
78. Leung JW, et al. (2014) Nucleosome acidic patch promotes RNF168- and RING1B/BMI1- dependent H2AX and H2A ubiquitination and DNA damage signaling. PLoS Genet 10(3):e1004178.
79. Aymard F, et al. (2014) Transcriptionally active chromatin recruits homologous recombination at DNA double-strand breaks. Nat Struct Mol Biol 21(4): 366-374.