Single-molecule analysis reveals human UV-damaged DNA-binding protein (UV-DDB) dimerizes on DNA via multiple kinetic intermediates

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

Volumn 111, Issue 18, 2014, Pages

  Ghodke, Harshad ^a,b   Wang, Hong ^c   Hsieh, Ching L ^a,b   Woldemeskel, Selamawit ^a   Watkins, Simon C ^a   Rapić Otrin, Vesna ^a,b   Van Houten, Bennett ^a,b  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

^c NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

DNA damage recognition; DNA tightrope; Human nucleotide excision repair; Single molecule tracking

Indexed keywords

DIMER; DNA BINDING PROTEIN; QUANTUM DOT;

ARTICLE; DNA DAMAGE; DNA DETERMINATION; EXCISION REPAIR; FLUORESCENCE MICROSCOPY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; ULTRAVIOLET RADIATION;

DNA DAMAGE RECOGNITION; DNA TIGHTROPE; HUMAN NUCLEOTIDE EXCISION REPAIR; SINGLE-MOLECULE TRACKING;

AMINO ACID SUBSTITUTION; DNA; DNA DAMAGE; DNA-BINDING PROTEINS; HUMANS; KINETICS; MICROSCOPY, FLUORESCENCE; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; NUCLEIC ACID CONFORMATION; OSMOLAR CONCENTRATION; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; PYRIMIDINE DIMERS; QUANTUM DOTS; ULTRAVIOLET RAYS; XERODERMA PIGMENTOSUM;

EID: 84899825410     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1323856111     Document Type: Article

References (60)

1. Sugasawa K (2011) Multiple DNA damage recognition factors involved in mammalian nucleotide excision repair. Biochemistry (Mosc) 76(1):16-23
2. Lange SS, Takata K, Wood RD (2011) DNA polymerases and cancer. Nat Rev Cancer 11(2):96-110
3. Hanawalt PC, Spivak G ( 2008) Transcription-coupled DNA repair: Two decades of progress and surprises. Nat Rev Mol Cell Biol 9(12):958-970
4. Pfeifer GP, You YH, Besaratinia A (2005) Mutations induced by ultraviolet light. Mutat Res 571(1- 2):19-31.
5. Tang JY Hwang BJ Ford JM Hanawalt PC Chu G, 2000, Xeroderma pigmentosum p48 gene enhances global genomic repair and suppresses UV-induced mutagenesis, Mol Cell,5,4, 737-744.
6. Aboussekhra A, et al. (1995) Mammalian DNA nucleotide excision repair reconstituted with purified protein components. Cell 80(6):859-868
7. Gillet LC, Schä rer OD (2006) Molecular mechanisms of mammalian global genome nucleotide excision repair. Chem Rev 106(2):253-276
8. Wakasugi M, et al. (2001) Damaged DNA-binding protein DDB stimulates the excision of cyclobutane pyrimidine dimers in vitro i n concert with XPA and replication protein A. J Biol Chem 276(18):15434-15440
9. Wood RD (1996) DNA repair in eukaryotes. Annu Rev Biochem 65:135-167
10. DiGiovanna JJ, Kraemer KH (2012) Shining a light on xeroderma pigmentosum. J Invest Dermatol 132(3 Pt 2):785-796
11. Nichols AF, Ong P, Linn S (1996) Mutations specific to the xeroderma pigmentosum group E Ddb- phenotype. J Biol Chem 271(40):24317-24320
12. Rapi-c-Otrin V, et al. (2003) True XP group E patients have a defective UV-damaged DNA binding protein compl ex and mutations in DDB2 which reveal the functional domains of its p48 product. Hum Mol Genet 12(13):1507-1522
13. Iwai S, et al. (1999) Benzimidazolium triflate-activated synthesis of (6-4) photoproductcontaining oligonucleotides and its application. Nucleic Acids Res 27(11):2299-2303
14. Wittschieben BO, Iwai S, Wood RD (2005) DDB1-DDB2 (xeroderma pigmentosum group E) protein complex recognizes a cyclobutane pyrimidine dimer, mismatches, apurinic/apyrimidinic sites, and compound lesions in DNA. J Biol Chem 280(48): 39982-39989
15. Reardon JT, et al. (1993) Comparative analysis of binding of human damaged DNAbinding protein (XPE) and Escherichia coli damage recognition protein (UvrA) to the major ultraviolet photoproducts: T[c,s]T, T[t,s]T, T[6-4]T, and T[Dewar]T. J Biol Chem 268(28):21301-21308
16. Groisman R, et al. (2003) The ubiquitin ligase activity in the DDB2 and CSA complexes is differentially regulated by the COP9 signalosome in response to DNA damage. Cell 113(3):357-367
17. Luijsterburg MS, et al. (2007) Dynamic in vivo interaction of DDB2 E3 ubiquitin ligase with UV-damaged DNA is independent of damage-recognition protein XPC. J Cell Sci 120(Pt 15):2706-2716
18. Fisch er ES, et al. (2011) The molecular basis of CRL4DDB2/CSA ubiquitin ligase architecture, targeting, and activation. Cell 147(5):1024-1039
19. Kapetanaki MG, et al. (2006) The DDB1-CUL4ADDB2 ubiquitin ligase is deficient in xeroderma pigmentosum group E and targets histone H2A at UV-damaged DNA sites. Proc Natl Acad Sci USA 103(8):2588-2593
20. Guerrero-Santoro J, et al. (2008) The cullin 4B-based UV-damaged DNA-binding protein ligase binds to UV-damaged chromatin and ubiquitinates histone H2A. Cancer Res 68(13):5014-5022
21. Sugasawa K, et al. (2005) UV-induced ubiquitylation of XPC protein mediated by UVDDB- ubiquitin ligase complex. Cell 121(3):387-400
22. Lan L, et al. (2012) Monoubiquitinated histone H2A destabilizes photolesioncontaining nucleosomes with concomitant release of UV-damaged DNA-binding protein E3 ligase. J Biol Chem 287(15):12036-12049
23. Wang H, et al. (2006) Histone H3 and H4 ubiquitylation by the CUL4-DDB-ROC1 ubiquitin ligase facilitates cellular response to DNA damage. Mol Cell 22(3):383-394
24. Takedachi A, Saijo M, Tanaka K (2010) DDB2 complex-mediated ubiquitylation around DNA damage is oppositely regulated by XPC and Ku and contributes to the recruitment of XPA. Mol Cell Biol 30(11):2708-2723
25. Rapi-c-Otrin V, McLenigan MP, Bisi DC, Gonzalez M, Levine AS (2002) Sequential binding of UV DNA damage binding factor and degradation of the p48 subunit as early events after UV irradiation. Nucleic Acids Res 30(11):2588-2598.
26. Yeh JI et al. (2012) Damaged DNA induced UV-damaged DNA-binding protein (UVDDB) dimerization and its roles in chromatinized DNA repair, Proc Natl Acad Sci USA, 109, 41, E2737-E2746.
27. Hughes CD, et al. (2013) Real-time single-molecule imaging reveals a direct interaction between UvrC and UvrB on DNA tightropes. Nucleic Acids Res 41(9): 4901-4912
28. Kad NM, Wang H, Kennedy GG, Warshaw DM, Van Houten B (2010) Collaborative dynamic DNA scanning by nucleotide excision repair proteins investigated by singlemolecule imaging of quantum-dot-labeled proteins. Mol Cell 37(5):702-713
29. Dunn AR, Kad NM, Nelson SR, Warshaw DM, Wallace SS (2011) Single Qdot-labeled glycosylase molecules use a wedge amino acid to probe for lesions while scanning along DNA. Nucleic Acids Res 39(17):7487-7498
30. Lin J, et al . (2014) TRF1 and TRF2 use different mechanisms to find telomeric DNA but share a novel mechanism to search for protein partners at telomeres. Nucleic Acids Res 42(4):2493-2504
31. Savir Y, Tlusty T (2007) Conformational proofreading: The impact of conformational changes on the specificity of molecular recognition. PLoS ONE 2(5):e468
32. Kad NM, Van Houten B (2012) Dynamics of lesion processing by bacterial nucleotide excision repair proteins. Prog Mol Biol Transl Sci 110:1-24
33. Gorman J, Greene EC (2008) Visualizing one-dimensional diffusion of proteins along DNA. Nat Struct Mol Biol 15(8):768-774
34. von Hippel PH, Berg OG (1989) Facilitated target location in biological systems. J Biol Chem 264(2):675-678
35. Wang F, et al. (2013) The promoter-search mechanism of Escherichia coli RNA polymerase is dominated by three-dimensional diffusion. Nat Struct Mol Biol 20(2): 174-181
36. Resch-Genger U, Grabolle M, Cavaliere-Jaricot S, Nitschke R, Nann T (2008) Quantum dots versus organic dyes as fluorescent labels. Nat Methods 5(9):763-775
37. Bruchez MP (2011) Quantum dots find their stride in single molecule tracking. Curr Opin Chem Biol 15(6):775-780
38. Tycon MA, Dial CF, Faison K, Melvin W, Fecko CJ (2012) Quantification of dye-mediated photodamage during single-molecule DNA imaging. Anal Biochem 426(1):13-21
39. Kastantin M, Schwartz DK (2013) Identifying multiple populations from single-molecule lifetime distributions. ChemPhysChem 14(2):374-380
40. Geng H, et al. (2011) In vitro studies of DNA mismatch repair proteins. Anal Biochem 413(2):179-184
41. Alekseev S, et al. (2008) Cellular concentrations of DDB2 regulate dynamic binding of DDB1 at UV-induced DNA damage. Mol Cell Biol 28(24):7402-7413
42. El-M ahdy MA, et al. (2006) Cullin 4A-mediated proteolysis of DDB2 protein at DNA damage sites regulates in vivo lesion recognition by XPC. J Biol Chem 281(19): 13404-13411
43. Wang QE, et al. ( 2005) Cellular ubiquitination and proteasomal functions positively modulate mammalian nucleotide excision repair. Mol Carcinog 42(1):53-64
44. Scrima A, et al. (2008) Structural basis of UV DNA-damage recognition by the DDB1- DDB2 complex. Cell 135(7):1213-1223
45. Eyal E, Yang LW, Bahar I (2006) Anisotropic network model: Systematic evaluation and a new web interface. Bioinformatics 22(21):2619-2627
46. Hoskins AA, et al. (2011) Ordered and dynamic assembly of single spliceosomes. Science 331(6022):1289-1295
47. Hopfield JJ (1974) Kinetic proofreading: A new mechanism for reducing errors in biosynthetic processes requiring high specificity. Proc Natl Acad Sci USA 71(10): 4135-4139
48. Fried man LJ, Mumm JP, Gelles J (2013) RNA polymerase approaches its promoter without long-range sliding along DNA. Proc Natl Acad Sci USA 110(24):9740-9745
49. Duan MR, Smerdon MJ (2010) UV dam age in DNA promotes nucleosome unwrapping. J Biol Chem 285(34):26295-26303
50. Pines A, et al. (2012) PARP1 promotes nucleotide excision repair through DDB2 stabilization and recruitment of ALC1. J Cell Biol 199(2):235-249
51. Robu M, et al. (2013) Role of poly(ADP-ribose) polymerase-1 in the removal of UVinduced DNA lesions by nucleotide excision repair. Proc Natl Acad Sci USA 110(5): 1658-1663
52. Zhao Q, et al. (2008) The p38 mitogen-activated protein kinase augments nucleotide excision repair by mediating DDB2 degradation and chromatin relaxation. J Biol Chem 283(47):32553-32561
53. Tsuge M, et al. (2013) SUMOylation of damaged DNA-binding protein DDB2. Biochem Biophys Res Commun 438(1):26-31
54. Wakasugi M, et al. (2009) Physi cal and functional interaction between DDB and XPA in nucleotide excision repair. Nucleic Acids Res 37(2):516-525
55. Otrin VR, McLenigan M, Takao M, Levine AS, Proti-c M (1997) Translocation of a UVdamaged DNA binding protein into a tight association with chromatin after treatment of mammalian cells with UV light. J Cell Sci 110(Pt 10):1159-1168
56. Naegeli H, Sugasawa K (2011) The xeroderma pigmentosum pathway: Decision tree analysis of DNA quality. DNA Repair (Amst) 10(7):673-683
57. Reardon JT, Sancar A (2004) Thermodynamic cooperativity and kinetic proofreading in DNA damage recognition and repair. Cell Cycle 3(2):141-144
58. Mathieu N, Kaczmarek N, Naegeli H (2010) Strand- and site-specific DNA lesion demarcation by the xeroderma pigmentosum group D helicase. Proc Natl Acad Sci USA 107(41):17545-17550
59. De Vlaminck I, et al. (2012) Mechanism of homology recognition in DNA recombination from dual-molecule experiments. Mol Cell 46(5):616-624
60. Sagi D, Tlusty T, Stavans J (2006) High fidelity of RecA-catalyzed recombination: A watchdog of genetic diversity. Nucleic Acids Res 34(18):5021-5031