Structure of UvrA nucleotide excision repair protein in complex with modified DNA

Nature Structural and Molecular Biology

Volumn 18, Issue 2, 2011, Pages 191-198

  Jaciuk, Marcin ^a   Nowak, Elzbieta ^a   Skowronek, Krzysztof ^a   Tañska, Anna ^a   Nowotny, Marcin ^a  

^a INTERNATIONAL INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

ABC EXCINUCLEASE; DIMER; DNA; OLIGONUCLEOTIDE; PROTEIN UVRA; UNCLASSIFIED DRUG;

ARTICLE; CHEMICAL MODIFICATION; CHEMICAL STRUCTURE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DNA BINDING; DNA CONFORMATION; DNA DAMAGE; DNA HELIX; DNA MODIFICATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; THERMOTOGA MARITIMA;

ADENOSINE DIPHOSPHATE; BACTERIAL PROTEINS; BASE SEQUENCE; CRYSTALLOGRAPHY, X-RAY; DNA; DNA DAMAGE; DNA REPAIR; DNA-BINDING PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; PROTEIN BINDING; PROTEIN CONFORMATION; THERMOTOGA MARITIMA;

EID: 79551624662     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.1973     Document Type: Article

References (53)

1. Truglio, J.J., Croteau, D.L., Van Houten, B. & Kisker, C. Prokaryotic nucleotide excision repair: the UvrABC system. Chem. Rev. 106, 233-252 (2006).
2. Boyce, R.P. & Howard-Flanders, P. Release of ultraviolet light-induced thymine dimers from DNA in E. coli K-12. Proc. Natl. Acad. Sci. USA 51, 293-300 (1964).
3. Howard-Flanders, P., Boyce, R.P. & Theriot, L. Three loci in Escherichia coli K-12 that control the excision of pyrimidine dimers and certain other mutagen products from DNA. Genetics 53, 1119-1136 (1966).
4. Sancar, A. & Reardon, J.T. Nucleotide excision repair in E. coli and man. Adv. Protein Chem. 69, 43-71 (2004).
5. Lehmann, A.R. DNA repair-defcient diseases, xeroderma pigmentosum, Cockayne syndrome and trichothiodystrophy. Biochimie 85, 1101-1111 (2003).
6. Cleaver, J.E., Lam, E.T. & Revet, I. Disorders of nucleotide excision repair: the genetic and molecular basis of heterogeneity. Nat. Rev. Genet. 10, 756-768 (2009).
7. Sancar, A. & Rupp, W.D. 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 (1983).
8. Machius, M., Henry, L., Palnitkar, M. & Deisenhofer, J. Crystal structure of the DNA nucleotide excision repair enzyme UvrB from Thermus thermophilus. Proc. Natl. Acad. Sci. USA 96, 11717-11722 (1999).
9. Nakagawa, N. et al. Crystal structure of Thermus thermophilus HB8 UvrB protein, a key enzyme of nucleotide excision repair. J. Biochem. 126, 986-990 (1999).
10. Theis, K., Chen, P.J., Skorvaga, M., Van Houten, B. & Kisker, C. Crystal structure of UvrB, a DNA helicase adapted for nucleotide excision repair. EMBO J. 18, 6899-6907 (1999).
11. Truglio, J.J. et al. Structural basis for DNA recognition and processing by UvrB. Nat. Struct. Mol. Biol. 13, 360-364 (2006).
12. Aravind, L., Walker, D.R. & Koonin, E.V. Conserved domains in DNA repair proteins and evolution of repair systems. Nucleic Acids Res. 27, 1223-1242 (1999).
13. Truglio, J.J. et al. Structural insights into the frst incision reaction during nucleotide excision repair. EMBO J. 24, 885-894 (2005).
14. Karakas, E. et al. 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 (2007).
15. Hopfner, K.P. & Tainer, J.A. Rad50/SMC proteins and ABC transporters: unifying concepts from high-resolution structures. Curr. Opin. Struct. Biol. 13, 249-255 (2003).
16. Linton, K.J. Structure and function of ABC transporters. Physiology (Bethesda) 22, 122-130 (2007).
17. Lamers, M.H. et al. The crystal structure of DNA mismatch repair protein MutS binding to a G x T mismatch. Nature 407, 711-717 (2000).
18. Obmolova, G., Ban, C., Hsieh, P. & Yang, W. Crystal structures of mismatch repair protein MutS and its complex with a substrate DNA. Nature 407, 703-710 (2000).
19. Pakotiprapha, D. et al. Crystal structure of Bacillus stearothermophilus UvrA provides insight into ATP-modulated dimerization, UvrB interaction, and DNA binding. Mol. Cell 29, 122-133 (2008).
20. Timmins, J. et al. Structural and mutational analyses of Deinococcus radiodurans UvrA2 provide insight into DNA binding and damage recognition by UvrAs. Structure 17, 547-558 (2009).
21. Pakotiprapha, D., Liu, Y., Verdine, G.L. & Jeruzalmi, D. A structural model for the damage-sensing complex in bacterial nucleotide excision repair. J. Biol. Chem. 284, 12837-12844 (2009).
22. Oh, E.Y., Claassen, L., Thiagalingam, S., Mazur, S. & Grossman, L. ATPase activity of the UvrA and UvrAB protein complexes of the Escherichia coli UvrABC endonuclease. Nucleic Acids Res. 17, 4145-4159 (1989).
23. Thiagalingam, S. & Grossman, L. The multiple roles for ATP in the Escherichia coli UvrABC endonuclease-catalyzed incision reaction. J. Biol. Chem. 268, 18382-18389 (1993).
24. DellaVecchia, M.J. et al. Analyzing the handoff of DNA from UvrA to UvrB utilizing DNA-protein photoaffnity labeling. J. Biol. Chem. 279, 45245-45256 (2004).
25. Waters, T.R., Eryilmaz, J., Geddes, S. & Barrett, T.E. Damage detection by the UvrABC pathway: crystal structure of UvrB bound to fuorescein-adducted DNA. FEBS Lett. 580, 6423-6427 (2006).
26. Van Houten, B. & Snowden, A. Mechanism of action of the Escherichia coli UvrABC nuclease: clues to the damage recognition problem. Bioessays 15, 51-59 (1993).
27. Moolenaar, G.F. et al. The effect of the DNA fanking the lesion on formation of the UvrB-DNA preincision complex. Mechanism for the UvrA-mediated loading of UvrB onto a DNA damaged site. J. Biol. Chem. 275, 8038-8043 (2000).
28. Croteau, D.L., DellaVecchia, M.J., Perera, L. & Van Houten, B. Cooperative damage recognition by UvrA and UvrB: identifcation of UvrA residues that mediate DNA binding. DNA Repair (Amst.) 7, 392-404 (2008).
29. Bellon, S.F., Coleman, J.H. & Lippard, S.J. DNA unwinding produced by site-specifc intrastrand cross-links of the antitumor drug cis- diamminedichloroplatinum(II). Biochemistry 30, 8026-8035 (1991).
30. 13C NMR spectroscopy. Biochemistry 37, 5426-5438 (1998).
31. Suri, A.K., Mao, B., Amin, S., Geacintov, N.E. & Patel, D.J. Solution conformation of the (+)-trans-anti-benzo[g]chrysene-dA adduct opposite dT in a DNA duplex. J. Mol. Biol. 292, 289-307 (1999). (Pubitemid 29435767)
32. Kabsch, W., Sander, C. & Trifonov, E.N. The ten helical twist angles of B-DNA. Nucleic Acids Res. 10, 1097-1104 (1982).
33. Park, H. et al. Crystal structure of a DNA decamer containing a cis-syn thymine dimer. Proc. Natl. Acad. Sci. USA 99, 15965-15970 (2002).
34. Wiesehahn, G. & Hearst, J.E. DNA unwinding induced by photoaddition of psoralen derivatives and determination of dark-binding equilibrium constants by gel electrophoresis. Proc. Natl. Acad. Sci. USA 75, 2703-2707 (1978).
35. Isaacs, R.J. & Spielmann, H.P. A model for initial DNA lesion recognition by NER and MMR based on local conformational fexibility. DNA Repair (Amst.) 3, 455-464 (2004).
36. Oh, E.Y. & Grossman, L. The effect of Escherichia coli Uvr protein binding on the topology of supercoiled DNA. Nucleic Acids Res. 14, 8557-8571 (1986).
37. Mazur, S.J. & Grossman, L. Dimerization of Escherichia coli UvrA and its binding to undamaged and ultraviolet light damaged DNA. Biochemistry 30, 4432-4443 (1991).
38. Van Houten, B., Gamper, H., Hearst, J.E. & Sancar, A. Analysis of sequential steps of nucleotide excision repair in Escherichia coli using synthetic substrates containing single psoralen adducts. J. Biol. Chem. 263, 16553-16560 (1988).
39. Wagner, K., Moolenaar, G., Van Noort, J. & Goosen, N. Single-molecule analysis reveals two separate DNA-binding domains in the Escherichia coli UvrA dimer. Nucleic Acids Res. 37, 1962-1972 (2009).
40. Croteau, D.L. et al. The C-terminal zinc fnger of UvrA does not bind DNA directly but regulates damage-specifc DNA binding. J. Biol. Chem. 281, 26370-26381 (2006).
41. Min, J.H. & Pavletich, N.P. Recognition of DNA damage by the Rad4 nucleotide excision repair protein. Nature 449, 570-575 (2007).
42. Scrima, A. et al. Structural basis of UV DNA-damage recognition by the DDB1-DDB2 complex. Cell 135, 1213-1223 (2008).
43. Otwinowski, Z. & Minor, W. Processing of X-ray diffraction data collected in oscillation mode. in Methods Enzymol. 276, 307-326 (1997).
44. Long, F., Vagin, A.A., Young, P. & Murshudov, G.N. BALBES: a molecular-replacement pipeline. Acta Crystallogr. D Biol. Crystallogr. 64, 125-132 (2008).
45. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (2004).
46. Afonine, P.V., Grosse-Kunstleve, R.W. & Adams, P.D. The Phenix refnement framework. CCP4 Newsl. 42, 8 (2005).
47. Chen, V.B. et al. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. 66, 12-21 (2010).
48. Baker, N.A., Sept, D., Joseph, S., Holst, M.J. & McCammon, J.A. Electrostatics of nanosystems: application to microtubules and the ribosome. Proc. Natl. Acad. Sci. USA 98, 10037-10041 (2001).
49. Pettersen, E.F. et al. UCSF Chimera- a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612 (2004).
50. Lavery, R., Moakher, M., Maddocks, J.H., Petkeviciute, D. & Zakrzewska, K. Conformational analysis of nucleic acids revisited: Curves+. Nucleic Acids Res. 37, 5917-5929 (2009).
51. Henkel, R.D., VandeBerg, J.L. & Walsh, R.A. A microassay for ATPase. Anal. Biochem. 169, 312-318 (1988).
52. Conlan, L.H. & Dupureur, C.M. Dissecting the metal ion dependence of DNA binding by PvuII endonuclease. Biochemistry 41, 1335-1342 (2002).
53. Jiang, G.H., Skorvaga, M., Croteau, D.L., Van Houten, B. & States, J.C. Robust incision of Benoz[a]pyrene-7,8-dihyrodiol-9,10-epoxide-DNA adducts by a recombinant thermoresistant interspecies combination UvrABC endonuclease system. Biochemistry 45, 7834-7843 (2006).