Isolating contributions from intersegmental transfer to DNA searching by alkyladenine DNA glycosylase

Journal of Biological Chemistry

Volumn 288, Issue 34, 2013, Pages 24550-24559

  Hedglin, Mark ^a   Zhang, Yaru ^a   O'Brien, Patrick J ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMICAL ASSAY; DNA REPAIR PATHWAYS; DNA-BINDING PROTEIN; FACILITATED DIFFUSIONS; JUMPING MECHANISMS; MONOMERIC PROTEINS; SALT CONCENTRATION; SINGLE BINDING SITES;

BINDING ENERGY; BINDING SITES; DISSOCIATION; GENES; PROTEINS;

DNA;

ALKYLADENINE DNA GLYCOSYLASE; DNA; DNA GLYCOSYLTRANSFERASE; SODIUM CHLORIDE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DISSOCIATION; GENE TRANSFER; INTERSEGMENTAL TRANSFER; NUCLEOTIDE BINDING SITE; PRIORITY JOURNAL; PROTEIN DNA BINDING;

BASE EXCISION REPAIR; DNA GLYCOSYLASE; DNA REPAIR; ENZYME KINETICS; ENZYME MECHANISMS; FACILITATED DIFFUSION; INTERSEGMENTAL TRANSFER; MUTAGENESIS MECHANISMS;

BINDING SITES; DNA; DNA GLYCOSYLASES; HUMANS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY;

EID: 84883188890     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.477018     Document Type: Article

References (42)

1. 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
2. Halford, S. E., and Marko, J. F. (2004) How do site-specific DNA-binding proteins find their targets? Nucleic Acids Res. 32, 3040-3052
3. Friedman, J. I., and Stivers, J. T. (2010) Detection of damaged DNA bases by DNA glycosylase enzymes. Biochemistry 49, 4957-4967
4. Doucleff, M., and Clore, G. M. (2008) Global jumping and domain-specific intersegment transfer between DNA cognate sites of the multidomain transcription factor Oct-1. Proc. Natl. Acad. Sci. U.S.A. 105, 13871-13876
5. Iwahara, J., and Clore, G. M. (2006) Direct observation of enhanced translocation of a homeodomain between DNA cognate sites by NMR exchange spectroscopy. J. Am. Chem. Soc. 128, 404-405
6. Lieberman, B. A., and Nordeen, S. K. (1997) DNA intersegment transfer, how steroid receptors search for a target site. J. Biol. Chem. 272, 1061-1068
7. Fried, M. G., and Crothers, D. M. (1984) Kinetics and mechanism in the reaction of gene regulatory proteins with DNA. J. Mol. Biol. 172, 263-282
8. Ruusala, T., and Crothers, D. M. (1992) Sliding and intermolecular transfer of the lac repressor: kinetic perturbation of a reaction intermediate by a distant DNA sequence. Proc. Natl. Acad. Sci. U.S.A. 89, 4903-4907
9. Kozlov, A. G., and Lohman, T. M. (2002) Kinetic mechanism of direct transfer of Escherichia coli SSB tetramers between single-stranded DNA molecules. Biochemistry 41, 11611-11627
10. Gorman, J., Wang, F., Redding, S., Plys, A. J., Fazio, T., Wind, S., Alani, E. E., and Greene, E. C. (2012) Single-molecule imaging reveals targetsearch mechanisms during DNA mismatch repair. Proc. Natl. Acad. Sci. U.S.A. 109, E3074-E3083
11. Hedglin, M., and O'Brien, P. J. (2008) Human alkyladenine DNA glycosylase employs a processive search for DNA damage. Biochemistry 47, 11434-11445
12. Hitchcock, T. M., Dong, L., Connor, E. E., Meira, L. B., Samson, L. D., Wyatt, M. D., and Cao, W. (2004) Oxanine DNA glycosylase activity from mammalian alkyladenine glycosylase. J. Biol. Chem. 279, 38177-38183
13. O'Brien, P. J., and Ellenberger, T. (2004) Dissecting the broad substrate specificity of human 3-methyladenine-DNA glycosylase. J. Biol. Chem. 279, 9750-9757
14. O'Connor, T. R. (1993) Purification and characterization of human 3-methyladenine-DNA glycosylase. Nucleic Acids Res. 21, 5561-5569
15. Engelward, B. P., Weeda, G., Wyatt, M. D., Broekhof, J. L., de Wit, J., Donker, I., Allan, J. M., Gold, B., Hoeijmakers, J. H., and Samson, L. D. (1997) Base excision repair deficient mice lacking the Aag alkyladenine DNA glycosylase. Proc. Natl. Acad. Sci. U.S.A. 94, 13087-13092
16. Lau, A. Y., Wyatt, M. D., Glassner, B. J., Samson, L. D., and Ellenberger, T. (2000) Molecular basis for discriminating between normal and damaged bases by the human alkyladenine glycosylase, AAG. Proc. Natl. Acad. Sci. U.S.A. 97, 13573-13578
17. Wolfe, A. E., and O'Brien, P. J. (2009) Kinetic mechanism for the flipping and excision of 1, N6-ethenoadenine by human alkyladenine DNA glycosylase. Biochemistry 48, 11357-11369
18. Hedglin, M., and O'Brien, P. J. (2010) Hopping enables a DNA repair glycosylase to search both strands and bypass a bound protein. ACS Chem. Biol. 5, 427-436
19. Lau, A. Y., Schärer, O. D., Samson, L., Verdine, G. L., and Ellenberger, T. (1998) Crystal structure of a human alkylbase-DNA repair enzyme complexed to DNA: mechanisms for nucleotide flipping and base excision. Cell 95, 249-258
20. Ward, J. J., Sodhi, J. S., McGuffin, L. J., Buxton, B. F., and Jones, D. T. (2004) Prediction and functional analysis of native disorder in proteins from the three kingdoms of life. J. Mol. Biol. 337, 635-645
21. Dyson, H. J., and Wright, P. E. (2005) Intrinsically unstructured proteins and their functions. Nat. Rev. Mol. Cell Biol. 6, 197-208
22. Hegde, M. L., Hazra, T. K., and Mitra, S. (2010) Functions of disordered regions in mammalian early base excision repair proteins. Cell. Mol. Life Sci. 67, 3573-3587
23. Vuzman, D., and Levy, Y. (2012) Intrinsically disordered regions as affinity tuners in protein-DNA interactions. Mol. BioSyst. 8, 47-57
24. Vuzman, D., Polonsky, M., and Levy, Y. (2010) Facilitated DNA search by multidomain transcription factors: cross talk via a flexible linker. Biophys. J. 99, 1202-1211
25. Baldwin, M. R., and O'Brien, P. J. (2010) Nonspecific DNA binding and coordination of the first two steps of base excision repair. Biochemistry 49, 7879-7891
26. Baldwin, M. R., and O'Brien, P. J. (2012) Defining the functional footprint for recognition and repair of deaminated DNA. Nucleic Acids Res. 40, 11638-11647
27. Terry, B. J., Jack, W. E., and Modrich, P. (1985) Facilitated diffusion during catalysis by EcoRI endonuclease. Nonspecific interactions in EcoRI catalysis. J. Biol. Chem. 260, 13130-13137
28. Stanford, N. P., Szczelkun, M. D., Marko, J. F., and Halford, S. E. (2000) One-and three-dimensional pathways for proteins to reach specific DNA sites. EMBO J. 19, 6546-6557
29. Jeltsch, A., Alves, J., Wolfes, H., Maass, G., and Pingoud, A. (1994) Pausing of the restriction endonuclease EcoRI during linear diffusion on DNA. Biochemistry 33, 10215-10219
30. Lyons, D. M., and O'Brien, P. J. (2009) Efficient recognition of an unpaired lesion by a DNA repair glycosylase. J. Am. Chem. Soc. 131, 17742-17743
31. Kienberger, F., Pastushenko, C., Kada, G., Gruber, H., Riener, C., Schindler, H., and Hinterdorfer, P. (2000) Static and dynamical properties of single poly(ethylene glycol) molecules investigated by force spectroscopy. Single Mol 1, 123-128
32. Krishnamurthy, V. M., Semetey, V., Bracher, P. J., Shen, N., and Whitesides, G. M. (2007) Dependence of effective molarity on linker length for an intramolecular protein-ligand system. J. Am. Chem. Soc. 129, 1312-1320
33. Tian, L., and Heyduk, T. (2009) Bivalent ligands with long nanometerscale flexible linkers. Biochemistry 48, 264-275
34. Takayama, Y., and Clore, G. M. (2011) Intra-and intermolecular translocation of the bi-domain transcription factor Oct1 characterized by liquid crystal and paramagnetic NMR. Proc. Natl. Acad. Sci. U.S.A. 108, E169-E176
35. Baldwin, M. R., and O'Brien, P. J. (2009) Human AP endonuclease 1 stimulates multiple-turnover base excision by alkyladenine DNA glycosylase. Biochemistry 48, 6022-6033
36. Vuzman, D., Azia, A., and Levy, Y. (2010) Searching DNA via a "Monkey Bar" mechanism: the significance of disordered tails. J. Mol. Biol. 396, 674-684
37. O'Brien, P. J., and Ellenberger, T. (2003) Human alkyladenine DNA glycosylase uses acid-base catalysis for selective excision of damaged purines. Biochemistry 42, 12418-12429
38. von Hippel, P. H., and Berg, O. G. (1989) Facilitated target location in biological systems. J. Biol. Chem. 264, 675-678
39. Sheinman, M., and Kafri, Y. (2009) The effects of intersegmental transfers on target location by proteins. Phys. Biol. 6, 016003
40. Gowers, D. M., Wilson, G. G., and Halford, S. E. (2005) Measurement of the contributions of 1D and 3D pathways to the translocation of a protein along DNA. Proc. Natl. Acad. Sci. U.S.A. 102, 15883-15888
41. Halford, S. E. (2001) Hopping, jumping and looping by restriction enzymes. Biochem. Soc. Trans. 29, 363-374
42. Wentzell, L. M., and Halford, S. E. (1998) DNA looping by the SfiI restriction endonuclease. J. Mol. Biol. 281, 433-444