Real-time single-molecule imaging reveals a direct interaction between UvrC and UvrB on DNA tightropes

Nucleic Acids Research

Volumn 41, Issue 9, 2013, Pages 4901-4912

  Hughes, Craig D ^a   Wang, Hong ^b,c,d   Ghodke, Harshad ^b,c   Simons, Michelle ^a   Towheed, Atif ^b,c   Peng, Ye ^b,c   Van Houten, Bennett ^b,c   Kad, Neil M ^a  

^a UNIVERSITY OF ESSEX   (United Kingdom)

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

^c UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

^d NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA BINDING PROTEIN; DOUBLE STRANDED DNA; MUTANT PROTEIN; POTASSIUM CHLORIDE; QUANTUM DOT; UNCLASSIFIED DRUG; UVRB PROTEIN; UVRC PROTEIN;

ARTICLE; ASSAY; COMPLEX FORMATION; DIFFUSION COEFFICIENT; DNA TIGHTROPE ASSAY; EXCISION REPAIR; FLUORESCENCE IMAGING; MOLECULAR IMAGING; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; STRUCTURE ACTIVITY RELATION;

DIFFUSION; DNA; DNA HELICASES; DNA-BINDING PROTEINS; ENDODEOXYRIBONUCLEASES; MICROSCOPY, ATOMIC FORCE; MICROSCOPY, FLUORESCENCE; QUANTUM DOTS;

EID: 84877300985     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt177     Document Type: Article

References (56)

1. Van Houten, B. (1990) Nucleotide excision repair in Escherichia coli. Microbiol. Rev., 54, 18-51.
2. Sancar, A. (1996) DNA excision repair. Annu. Rev. Biochem., 65, 43-81.
3. Truglio, J.J., Croteau, D.L., Van Houten, B. and Kisker, C. (2006) Prokaryotic nucleotide excision repair: the UvrABC system. Chem. Rev., 106, 233-252.
4. Van Houten, B., Croteau, D.L., DellaVecchia, M.J., Wang, H. and Kisker, C. (2005) 'Close-fitting sleeves': DNA damage recognition by the UvrABC nuclease system. Mutat. Res., 577, 92-117.
5. Peng, Y., Wang, H., Santana-Santos, L., Kisker, C. and Van Houten, B. (2011) In: Penning, T.M. (ed.), Chemical Carcinogenesis. Springer Science + Business Media, New York, pp. 267-296.
6. Kad, N.M., Wang, H., Kennedy, G.G., Warshaw, D.M. and Van Houten, B. (2010) Collaborative dynamic DNA scanning by nucleotide excision repair proteins investigated by single-molecule imaging of quantum-dot-labeled proteins. Mol. Cell, 37, 702-713.
7. Goosen, N. and Moolenaar, G.F. (2008) Repair of UV damage in bacteria. DNA Repair, 7, 353-379.
8. DellaVecchia, M.J., Croteau, D.L., Skorvaga, M., Dezhurov, S.V., Lavrik, O.I. and Van Houten, B. (2004) Analyzing the handoff of DNA from UvrA to UvrB utilizing DNA-protein photoaffinity labeling. J. Biol. Chem., 279, 45245-45256.
9. Visse, R., King, A., Moolenaar, G.F., Goosen, N. and van de Putte, P. (1994) Protein-DNA interactions and alterations in the DNA structure upon UvrB-DNA preincision complex formation during nucleotide excision repair in Escherichia coli. Biochemistry, 33, 9881-9888.
10. Orren, D.K. and Sancar, A. (1989) The (A)BC excinuclease of Escherichia coli has only the UvrB and UvrC subunits in the incision complex. Proc. Natl Acad. Sci. USA, 86, 5237-5241.
11. Orren, D.K. and Sancar, A. (1990) Formation and enzymatic properties of the UvrB.DNA complex. J. Biol. Chem., 265, 15796-15803.
12. Verhoeven, E.E., van Kesteren, M., Moolenaar, G.F., Visse, R. and Goosen, N. (2000) Catalytic sites for 3 and 5 incision of Escherichia coli nucleotide excision repair are both located in UvrC. J. Biol. Chem., 275, 5120-5123.
13. Yoakum, G.H. and Grossman, L. (1981) Identification of E. coli uvrC protein. Nature, 292, 171-173.
14. Sancar, A. and Rupp, W.D. (1983) A novel repair enzyme: UVRABC excision nuclease of Escherichia coli cuts a DNA strand on both sides of the damaged region. Cell, 33, 249-260.
15. Caron, P.R., Kushner, S.R. and Grossman, L. (1985) Involvement of helicase II (uvrD gene product) and DNA polymerase I in excision mediated by the uvrABC protein complex. Proc. Natl Acad. Sci. USA, 82, 4925-4929.
16. Husain, I., Van Houten, B., Thomas, D.C., Abdel-Monem, M. and Sancar, A. (1985) Effect of DNA polymerase I and DNA helicase II on the turnover rate of UvrABC excision nuclease. Proc. Natl Acad. Sci. USA, 82, 6774-6778.
17. Crowley, D.J. and Hanawalt, P.C. (2001) The SOS-dependent upregulation of uvrD is not required for efficient nucleotide excision repair of ultraviolet light induced DNA photoproducts in Escherichia coli. Mutat. Res., 485, 319-329.
18. Moolenaar, G.F., Bazuine, M., van Knippenberg, I.C., Visse, R. and Goosen, N. (1998) Characterization of the Escherichia coli damage-independent UvrBC endonuclease activity. J. Biol. Chem., 273, 34896-34903.
19. Lin, J.J. and Sancar, A. (1992) Active site of (A)BC excinuclease. I. Evidence for 5' incision by UvrC through a catalytic site involving Asp399, Asp438, Asp466, and His538 residues. J. Biol. Chem., 267, 17688-17692.
20. Truglio, J.J., Rhau, B., Croteau, D.L., Wang, L., Skorvaga, M., Karakas, E., DellaVecchia, M.J., Wang, H., Van Houten, B. and Kisker, C. (2005) Structural insights into the first incision reaction during nucleotide excision repair. EMBO J., 24, 885-894.
21. Karakas, E., Truglio, J.J., Croteau, D., Rhau, B., Wang, L., Van Houten, B. and Kisker, C. (2007) Structure of the C-terminal half of UvrC reveals an RNase H endonuclease domain with an Argonaute-like catalytic triad. EMBO J., 26, 613-622.
22. Wang, H., Lu, M., Tang, M.S., Van Houten, B., Ross, J.B., Weinfeld, M. and Le, X.C. (2009) DNA wrapping is required for DNA damage recognition in the Escherichia coli DNA nucleotide excision repair pathway. Proc. Natl Acad. Sci. USA, 106, 12849-12854.
23. Wang, H., DellaVecchia, M.J., Skorvaga, M., Croteau, D.L., Erie, D.A. and Van Houten, B. (2006) UvrB domain 4, an autoinhibitory gate for regulation of DNA binding and ATPase activity. J. Biol. Chem., 281, 15227-15237.
24. Theis, K., Chen, P.J., Skorvaga, M., Van Houten, B. and Kisker, C. (1999) Crystal structure of UvrB, a DNA helicase adapted for nucleotide excision repair. EMBO J., 18, 6899-6907.
25. Skorvaga, M., DellaVecchia, M.J., Croteau, D.L., Theis, K., Truglio, J.J., Mandavilli, B.S., Kisker, C. and Van Houten, B. (2004) Identification of residues within UvrB that are important for efficient DNA binding and damage processing. J. Biol. Chem., 279, 51574-51580.
26. Machius, M., Henry, L., Palnitkar, M. and Deisenhofer, J. (1999) Crystal structure of the DNA nucleotide excision repair enzyme UvrB from Thermus thermophilus. Proc. Natl Acad. Sci. USA, 96, 11717-11722.
27. Truglio, J.J., Karakas, E., Rhau, B., Wang, H., DellaVecchia, M.J., Van Houten, B. and Kisker, C. (2006) Structural basis for DNA recognition and processing by UvrB. Nat. Struct. Mol. Biol., 13, 360-364.
28. Verhoeven, E.E., Wyman, C., Moolenaar, G.F., Hoeijmakers, J.H. and Goosen, N. (2001) Architecture of nucleotide excision repair complexes: DNA is wrapped by UvrB before and after damage recognition. EMBO J., 20, 601-611.
29. Kad, N.M. and Van Houten, B. (2012) Dynamics of lesion processing by bacterial nucleotide excision repair proteins. Prog. Mol. Biol. Transl. Sci., 110, 1-24.
30. Dunn, A.R., Kad, N.M., Nelson, S.R., Warshaw, D.M. and Wallace, S.S. (2011) Single Qdot-labeled glycosylase molecules use a wedge amino acid to probe for lesions while scanning along DNA. Nucleic Acids Res., 39, 7487-7498.
31. Blainey, P.C., van Oijen, A.M., Banerjee, A., Verdine, G.L. and Xie, X.S. (2006) A base-excision DNA-repair protein finds intrahelical lesion bases by fast sliding in contact with DNA. Proc. Natl Acad. Sci. USA, 103, 5752-5757.
32. Harada, Y., Funatsu, T., Murakami, K., Nonoyama, Y., Ishihama, A. and Yanagida, T. (1999) Single-molecule imaging of RNA polymerase-DNA interactions in real time. Biophys. J., 76, 709-715.
33. Gorman, J., Plys, A.J., Visnapuu, M.L., Alani, E. and Greene, E.C. (2010) Visualizing one-dimensional diffusion of eukaryotic DNA repair factors along a chromatin lattice. Nat. Struct. Mol. Biol., 17, 932-938.
34. Finkelstein, I.J., Visnapuu, M.L. and Greene, E.C. (2010) Single-molecule imaging reveals mechanisms of protein disruption by a DNA translocase. Nature, 468, 983-987.
35. Tafvizi, A., Huang, F., Leith, J.S., Fersht, A.R., Mirny, L.A. and van Oijen, A.M. (2008) Tumor suppressor p53 slides on DNA with low friction and high stability. Biophys. J., 95, L01-L03.
36. Berg, O.G., Winter, R.B. and von Hippel, P.H. (1981) Diffusion-driven mechanisms of protein translocation on nucleic acids. 1. Models and theory. Biochemistry, 20, 6929-6948.
37. von Hippel, P.H. and Berg, O.G. (1989) Facilitated target location in biological systems. J. Biol. Chem., 264, 675-678.
38. Croteau, D.L., DellaVecchia, M.J., Wang, H., Bienstock, R.J., Melton, M.A. and Van Houten, B. (2006) The C-terminal zinc finger of UvrA does not bind DNA directly but regulates damage-specific DNA binding. J. Biol. Chem., 281, 26370-26381.
39. Wang, H., Tessmer, I., Croteau, D.L., Erie, D.A. and Van Houten, B. (2008) Functional characterization and atomic force microscopy of a DNA repair protein conjugated to a quantum dot. Nano Letts., 8, 1631-1637.
40. Hohng, S. and Ha, T. (2004) Near-complete suppression of quantum dot blinking in ambient conditions. J. Am. Chem. Soc., 126, 1324-1325.
41. Thompson, R.E., Larson, D.R. and Webb, W.W. (2002) Precise nanometer localization analysis for individual fluorescent probes. Biophys. J., 82, 2775-2783.
42. Saxton, M.J. (2001) Anomalous subdiffusion in fluorescence photobleaching recovery: a Monte Carlo study. Biophys. J., 81, 2226-2240.
43. Zou, Y., Walker, R., Bassett, H., Geacintov, N.E. and Van Houten, B. (1997) Formation of DNA repair intermediates and incision by the ATP-dependent UvrB-UvrC endonuclease. J. Biol. Chem., 272, 4820-4827.
44. Skorvaga, M., Theis, K., Mandavilli, B.S., Kisker, C. and Van Houten, B. (2002) The beta-hairpin motif of UvrB is essential for DNA binding, damage processing, and UvrC-mediated incisions. J. Biol. Chem., 277, 1553-1559.
45. Bienstock, R.J., Skorvaga, M., Mandavilli, B.S. and Van Houten, B. (2003) Structural and functional characterization of the human DNA repair helicase XPD by comparative molecular modeling and site-directed mutagenesis of the bacterial repair protein UvrB. J. Biol. Chem., 278, 5309-5316.
46. Moolenaar, G.F., Hoglund, L. and Goosen, N. (2001) Clue to damage recognition by UvrB: residues in the beta-hairpin structure prevent binding to non-damaged DNA. EMBO J., 20, 6140-6149.
47. Hsu, D.S., Kim, S.T., Sun, Q. and Sancar, A. (1995) Structure and function of the UvrB protein. J. Biol. Chem., 270, 8319-8327.
48. Zou, Y. and Van Houten, B. (1999) Strand opening by the UvrA(2)B complex allows dynamic recognition of DNA damage. EMBO J., 18, 4889-4901.
49. Singh, S., Folkers, G.E., Bonvin, A.M., Boelens, R., Wechselberger, R., Niztayev, A. and Kaptein, R. (2002) Solution structure and DNA-binding properties of the C-terminal domain of UvrC from E.coli. EMBO J., 21, 6257-6266.
50. Huisman, O., D'Ari, R. and Gottesman, S. (1984) Cell-division control in Escherichia coli: specific induction of the SOS function SfiA protein is sufficient to block septation. Proc. Natl Acad. Sci. USA, 81, 4490-4494.
51. Aravind, L., Walker, D.R. and Koonin, E.V. (1999) Conserved domains in DNA repair proteins and evolution of repair systems. Nucleic Acids Res., 27, 1223-1242.
52. Yildiz, A. and Selvin, P.R. (2005) Fluorescence imaging with one nanometer accuracy: application to molecular motors. Acc. Chem. Res., 38, 574-582.
53. Hughes, B.D. (1995) Random Walks and Random Environment. Clarendon Press, Oxford.
54. Gorman, J., Chowdhury, A., Surtees, J.A., Shimada, J., Reichman, D.R., Alani, E. and Greene, E.C. (2007) Dynamic basis for one-dimensional DNA scanning by the mismatch repair complex Msh2-Msh6. Mol. Cell, 28, 359-370.
55. Schurr, J.M. (1979) The one-dimensional diffusion coefficient of proteins absorbed on DNA. Hydrodynamic considerations. Biophys. Chem., 9, 413-414.
56. Bagchi, B., Blainey, P.C. and Xie, X.S. (2008) Diffusion constant of a nonspecifically bound protein undergoing curvilinear motion along DNA. J. Phys. Chem. B, 112, 6282-6284.