Dynamics of the UvrABC nucleotide excision repair proteins analyzed by fluorescence resonance energy transfer

Biochemistry

Volumn 46, Issue 31, 2007, Pages 9080-9088

  Malta, Erik ^a   Moolenaar, Geri F ^a   Goosen, Nora ^a  

^a LEIDEN UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL NUCLEOTIDE; FLUORESCENCE RESONANCE ENERGY TRANSFER (FRET);

BINDING ENERGY; DIMERIZATION; DISSOCIATION; FLUORESCENCE; RESONANCE;

PROTEINS;

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; BACTERIAL PROTEIN; DIMER; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; NUCLEOTIDE EXCISION REPAIR PROTEIN UVRA; NUCLEOTIDE EXCISION REPAIR PROTEIN UVRB; NUCLEOTIDE EXCISION REPAIR PROTEIN UVRC; OLIGOMER; PROTEIN SUBUNIT; UNCLASSIFIED DRUG; YELLOW FLUORESCENT PROTEIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; CONTROLLED STUDY; DIMERIZATION; DISSOCIATION; DNA DAMAGE; ENZYME ACTIVE SITE; ESCHERICHIA COLI; EXCISION REPAIR; FLUORESCENCE RESONANCE ENERGY TRANSFER; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY;

ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; BACTERIAL PROTEINS; BASE SEQUENCE; DIMERIZATION; DNA; DNA DAMAGE; DNA HELICASES; DNA REPAIR; DNA-BINDING PROTEINS; ENDODEOXYRIBONUCLEASES; ESCHERICHIA COLI PROTEINS; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENE DELETION; GREEN FLUORESCENT PROTEINS; LUMINESCENT PROTEINS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; RECOMBINANT FUSION PROTEINS; ULTRAVIOLET RAYS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 34547797856     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi7002235     Document Type: Article

References (33)

1. Goosen, N., and Moolenaar, G. F. (2001) Role of ATP hydrolysis by UvrA and UvrB during nucleotide excision repair, Res. Microbiol. 152, 401-409.
2. 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.
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. Theis, K., Chen, P. J., Skorvaga, M., Van Houten, B., and Kisker, C. Crystal structure of UvrB, a DNA helicase adapted for nucleotide excision repair, EMBO J. 18, 6899-6907.
5. Machius, M., Henry, L., Palnitkar, M., and Deisenhofer, J. (1999) Crystal structure of the DNA nucleotide excision repair protein UvrB from Thermus thermophilus, Proc. Natl. Acad. Sci. U.S.A. 96, 11717-11722.
6. Nakagawa, N., Sugahara, M., Masui, R., Kato, F., Fukuyama, K., and Kuramitsu, S. (1999) Crystal structure of Thermus thermophilus HB8 UvrB protein, a key enzyme of nucleotide excision repair, J. Biochem. 126, 986-990.
7. Sohi, M., Alexandrovich, A., Moolenaar, G. F., Visse, R., Goosen, N., Vernede, X., Fontecilla-Camps, J. C., Champness, J., and Sanderson, M. R. (2000) Crystal structure of Escherichia coli UvrB C-terminal domain and a model for UvrB-UvrC interaction, FEBS Lett. 465, 161-164.
8. Alexandrovich, A., Sanderson, M. R., Moolenaar, G. F., Goosen, N., and Lane, A. N. (1999) NMR assignments and secondary structure of the UvrC binding domain of UvrB, FEBS Lett. 451, 181-185.
9. Truglio, J. J., Croteau, D. L., Skorvaga, M., DellaVecchia, M. J., Theis, K., Mandavilli, B. S., Van Houten, B., and Kisker, C. (2004) Interactions between UvrA and UvrB: The role of UvrB's domain 2 in nucleotide excision repair, EMBO J. 23, 2498-2509.
10. 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.
11. 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. U.S.A. 86, 5237-5241.
12. Oh, E. Y., Claassen, L., Thiagalingam, S., Mazur, S., and Grossman, L. (1989) ATPase activity of the UvrA and UvrAB protein complexes of the Escherichia coli UvrABC endonuclease, Nucleic Acids Res. 17, 4145-4159.
13. Hildebrand, E. L., and Grossman, L. (1999) Oligomerization of the UvrB nucleotide excision repair protein of Escherichia coli, J. Biol. Chem. 274, 27885-27890.
14. Verhoeven, E. E. A., Wyman, C., Moolenaar, G. F., and Goosen, N. (2002) The presence of two UvrB subunits in the UvrAB complex ensures damage detection in both DNA strands, EMBO J. 21, 4196-4205.
15. Moolenaar, G. F., Schut, M., and Goosen, N. (2005) Binding of the UvrB dimer to non-damaged and damaged DNA: Residues Y92 and Y93 influence the stability of both subunits, DNA Repair 4, 699-713.
16. Verhoeven, E. E. A., van Kesteren, M., Moolenaar, G. F., Visse, R., and Goosen, N. (2000) Catalytic sites for 3′- and 5′-incision of E. coli nucleotide excision repair are both located in UvrC, J. Biol. Chem. 275, 5120-5123.
17. 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.
18. Moolenaar, G. F., Franken, K. L., Dijkstra, D. M., Thomas-Oates, J. E., Visse, R., van de Putte, P., and Goosen, N. (1995) The C-terminal region of the UvrB protein of Escherichia coli contains an important determinant for UvrC binding to the preincision complex but not the catalytic site for 3′-incision, J. Biol. Chem. 270, 30508-30515.
19. Moolenaar, G. F., Franken, K. L., van de Putte, P., and Goosen, N. (1997) Function of the homologous regions of the Escherichia coli DNA excision repair proteins UvrB and UvrC in stabilization of the UvrBC-DNA complex and in 3′-incision, Mutat. Res. 385, 195-203.
20. Zimmermann, T., Rietdorf, J., Girod, A., Georget, V., and Pepperkok, R. (2002) Spectral imaging and linear un-mixing enables improved FRET efficiency with a novel GFP2-YFP FRET pair, FEBS Lett. 531, 245-249.
21. Malta, E., Moolenaar, G. F., and Goosen, N. (2006) Base flipping in nucleotide excision repair, J. Biol. Chem. 281, 2184-2194.
22. Moolenaar, G. F., Visse, R., Ortiz-Buysse, M., Goosen, N., and van de Putte, P. (1994) Helicase motifs V and VI of the Escherichia coli UvrB protein of the UvrABC endonuclease are essential for the formation of the preincision complex, J. Mol. Biol. 240, 294-307.
23. Moolenaar, G. F., Höglund, L., and Goosen, N. (2001) Clue to damage recognition by UvrB: Residues in the β-hairpin structure prevent binding to non-damaged DNA, EMBO J. 20, 6140-6149.
24. Visse, R., de Ruijter, M., Moolenaar, G. F., and van de Putte, P. (1992) Analysis of UvrABC endonuclease reaction intermediates on cisplatin-damaged DNA using mobility shift gel electrophoresis, J. Biol. Chem. 267, 6736-6742.
25. Verhoeven, E. E. A., van Kesteren, M., Turner, J. J., van der Marel, G. A., van Boom, J. H., Moolenaar, G. F., and Goosen, N. (2002) The C-terminal region of E. coli UvrC contributes to the flexibility of the UvrABC nucleotide excision repair system, Nucleic Acids Res. 30, 2492-2500.
26. Douki, T., Court, M., Sauvaigo, S., Odin, F., and Cadet, J. (2000) Formation of the main UV-induced thymine dimeric lesions within isolated and cellular DNA as measured by high performance liquid chromatography-tandem mass spectrometry, J. Biol. Chem. 275, 11678-11685.
27. Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989) in Molecular Cloning: A Laboratory Manual, Cold Spring Harbor Laboratory Press, Plainview, NY.
28. Verhoeven, E. E. A., van Kesteren, M., Turner, J. J., van der Marel, G. A., van Boom, J. H., Moolenaar, G. F., and Goosen, N. (2002) The C-terminal region of Escherichia coli UvrC contributes to the flexibility of the UvrABC nucleotide excision repair system, Nucleic Acids Res. 30, 2492-2500.
29. Seeley, T. W., and Grossman, L. (1989) Mutations in the Escherichia coli UvrB ATPase motif compromise excision repair capacity, Proc. Natl. Acad. Sci. U.S.A. 86, 6577-6581.
30. 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.
31. Moolenaar, G. F., Herron, M. F., Monaco, V., van der Marel, G. A., van Boom, J. H., Visse, R., and Goosen, N. (2000) The role of ATP binding and hydrolysis by UvrB during nucleotide excision repair, J. Biol. Chem. 265, 8044-8050.
32. Ameer-Beg, S. M., Edme, N., Peter, M., Barber, P. R., Ng, T., and Vojnovic, B. (2003) Imaging protein-protein interactions by multiphoton FLIM, Proc. SPIE 5139, 180-189.
33. Visse, R., de Ruijter, M., Moolenaar, G. F., and van de Putte, P. (1991) Analysis of UvrABC endonuclease intermediates on cisplatin-damaged DNA using mobility shift gtel electrophoresis. J. Biol. Chem. 267, 6736-6742.