Structural and kinetic analysis of nucleoside triphosphate incorporation opposite an abasic site by human translesion DNA polymerase

Journal of Biological Chemistry

Volumn 290, Issue 13, 2015, Pages 8028-8038

  Patra, Amritaj ^a   Zhang, Qianqian ^a   Lei, Li ^a   Su, Yan ^a   Egli, Martin ^a,b   Guengerich, F Peter ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Dept of Biochemistry 868A Robinson Research Bldg ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY;

DNA POLYMERASE; H-BONDING; KINETIC ANALYSIS; TRANSLESION; TRIPHOSPHATE;

BIOLOGY;

DEOXYADENOSINE TRIPHOSPHATE; DEOXYGUANOSINE TRIPHOSPHATE; DNA DIRECTED DNA POLYMERASE ETA; NUCLEOSIDE TRIPHOSPHATE; PYRIMIDINE; 2'-DEOXYADENOSINE TRIPHOSPHATE; APURINIC ACID; DEOXYADENOSINE PHOSPHATE; DNA DIRECTED DNA POLYMERASE; PROTEIN BINDING;

ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; DNA DAMAGE; ENZYME KINETICS; ENZYME STRUCTURE; HYDROGEN BOND; PRIORITY JOURNAL; STEADY STATE; CHEMICAL STRUCTURE; CHEMISTRY; ENZYME ACTIVE SITE; HUMAN; KINETICS; TANDEM MASS SPECTROMETRY; X RAY CRYSTALLOGRAPHY;

APURINIC ACID; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; DEOXYADENINE NUCLEOTIDES; DNA-DIRECTED DNA POLYMERASE; HUMANS; HYDROGEN BONDING; KINETICS; MODELS, MOLECULAR; PROTEIN BINDING; TANDEM MASS SPECTROMETRY;

EID: 84925813561     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.637561     Document Type: Article

References (39)

1. Friedberg, E. C., Walker, G. C., Siede, W., Wood, R. D., Schultz, R. A., and Ellenberger, T. (2006) DNA Repair and Mutagenesis, 2nd Ed., American Society for Microbiology, Washington, D. C.
2. Strauss, B. S. (2002) The "A" rule revisited: polymerases as determinants of mutational specificity. DNA Repair 1, 125-135
3. Boiteux, S., and Laval, J. (1982) Coding properties of poly(deoxycytidylic acid) templatescontaininguracilorapyrimidinicsites:invitromodulationofmutagenesis by deoxyribonucleic acid repair enzymes. Biochemistry 21, 6746-6751
4. Sagher, D., and Strauss, B. (1983) Insertion of nucleotides opposite apurinic/apyrimidinic sites in deoxyribonucleic acid during in vitro synthesis: uniqueness of adenine nucleotides. Biochemistry 22, 4518-4526
5. Schaaper, R. M., Glickman, B. W., and Loeb, L. A. (1982) Mutagenesis resulting from depurination is an SOS process. Mutat. Res. 106, 1-9
6. Efrati, E., Tocco, G., Eritja, R., Wilson, S. H., and Goodman, M. F. (1997) Abasic translesion synthesis byDNApolymeraseβ violates the "A-rule." Novel types of nucleotide incorporation by human DNA polymerase β at an abasic lesion in different sequence contexts. J. Biol. Chem. 272, 2559-2569
7. Fiala, K. A., Hypes, C. D., and Suo, Z. (2007) Mechanism of abasic lesion bypass catalyzed by a Y-family DNA polymerase. J. Biol. Chem. 282, 8188-8198
8. Sagher, D., and Strauss, B. (1985) Abasic sites from cytosine as termination signals for DNA synthesis. Nucleic Acids Res. 13, 4285-4298
9. Obeid, S., Blatter, N., Kranaster, R., Schnur, A., Diederichs, K., Welte, W., and Marx, A. (2010) Replication through an abasic DNA lesion: structural basis for adenine selectivity. EMBO J. 29, 1738-1747
10. Zahn, K. E., Belrhali, H., Wallace, S. S., and Doublié, S. (2007) Caught bending the A-rule: crystal structures of translesion DNA synthesis with a non-natural nucleotide. Biochemistry 46, 10551-10561
11. Ling, H., Boudsocq, F., Woodgate, R., and Yang, W. (2004) Snapshots of replication through an abasic lesion; structural basis for base substitutions and frameshifts. Mol. Cell 13, 751-762
12. Beard, W. A., Shock, D. D., Batra, V. K., Pedersen, L. C., and Wilson, S. H. (2009) DNA polymerase β substrate specificity: side chain modulation of the "A-rule". Biol. Chem. 284, 31680-31689
13. Nair, D. T., Johnson, R. E., Prakash, L., Prakash, S., and Aggarwal, A. K. (2011) DNA synthesis across an abasic lesion by yeast REV1 DNA polymerase. J. Mol. Biol. 406, 18-28
14. Nair, D. T., Johnson, R. E., Prakash, L., Prakash, S., and Aggarwal, A. K. (2009) DNA synthesis across an abasic lesion by human DNA polymerase ≤. Structure 17, 530-537
15. Freisinger, E., Grollman, A. P., Miller, H., and Kisker, C. (2004) Lesion (in)tolerance reveals insights into DNA replication fidelity. EMBO J. 23, 1494-1505
16. Hogg, M., Wallace, S. S., and Doublié, S. (2004) Crystallographic snapshots of a replicativeDNApolymerase encountering an abasic site. EMBO J. 23, 1483-1493
17. Haracska, L., Washington, M. T., Prakash, S., and Prakash, L. (2001) Inefficient bypass of an abasic site by DNA polymerase η. Inefficient bypass of an abasic site by DNA polymerase η. J. Biol. Chem. 276, 6861-6866
18. Choi, J.-Y., Lim, S., Kim, E. J., Jo, A., and Guengerich, F. P. (2010) Translesion synthesis across abasic lesions by human B-family and Y-family DNA polymerases α, δ, η, ≤, κ, and REV1. J. Mol. Biol. 404, 34-44
19. Zhao, B., Xie, Z., Shen, H., and Wang, Z. (2004) Role of DNA polymerase η in the bypass of abasic sites in yeast cells. Nucleic Acids Res. 32, 3984-3994
20. Gibbs, P. E., McDonald, J., Woodgate, R., and Lawrence, C. W. (2005) The relative roles in vivo of Saccharomyces cerevisiae pol η, pol ζ, Rev1 protein and pol32 in the bypass and mutation induction of an abasic site, T-T (6-4) photoadduct and T-T cis-syn cyclobutane dimer. Genetics 169, 575-582
21. Kokoska, R. J., McCulloch, S. D., and Kunkel, T. A. (2003) The efficiency and specificity of apurinic/apyrimidinic site bypass by human DNA polymerase η and Sulfolobus solfataricus Dpo4. J. Biol. Chem. 278, 50537-50545
22. Biertümpfel, C., Zhao, Y., Kondo, Y., Ramón-Maiques, S., Gregory, M., Lee, J. Y., Masutani, C., Lehmann, A. R., Hanaoka, F., and Yang, W. (2010) Structure and mechanism of human DNA polymerase & et al. Nature 465, 1044-1048
23. Patra, A., Nagy, L. D., Zhang, Q., Su, Y., Müller, L., Guengerich, F. P., and Egli, M. (2014) Kinetics, structure, and mechanism of 8-oxo-7,8-dihydro- 2′-deoxyguanosine bypass by human DNA polymerase η. J. Biol. Chem. 289, 16867-16882
24. Boosalis, M. S., Petruska, J., and Goodman, M. F. (1987) DNA polymerase insertion fidelity. Gel assay for site-specific kinetics. J. Biol. Chem. 262, 14689-14696
25. O'Flaherty, D. K., and Guengerich, F. P. (2014) Steady-state kinetic analysis of DNA polymerase single-nucleotide incorporation products. Curr. Protoc. Nucleic Acid Chem. 59, 7.21.1-7.21.13
26. Zang, H., Goodenough, A. K., Choi, J. Y., Irimia, A., Loukachevitch, L. V., Kozekov, I. D., Angel, K. C., Rizzo, C. J., Egli, M., and Guengerich, F. P. (2005) DNA adduct bypass polymerization by Sulfolobus solfataricus DNA polymerase Dpo4: analysis and crystal structures of multiple base pair substitution and frameshift products with the adduct 1,N2-ethenoguanine. J. Biol. Chem. 280, 29750-29764
27. Christov, P. P., Angel, K. C., Guengerich, F. P., and Rizzo, C. J. (2009) Replication past the N5-methyl-formamidopyrimidine lesion of deoxyguanosine by DNA polymerases and an improved procedure for sequence analysis of in vitro bypass products by mass spectrometry. Chem. Res. Toxicol. 22, 1086-1095
28. Jancarik, J., and Kim, S.-H. (1991) Sparse matrix sampling: a screening method for crystallization of proteins. J. Appl. Crystallogr. 24, 409-411
29. Otwinowski, Z., and Minor, W. (1997) Processing of x-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326
30. Vagin, A., and Teplyakov, A. (1997) MOLREP: an automated program for molecular replacement. J. Appl. Crystallogr. 30, 1022-1025
31. Collaborative Computational Project No. 4 (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50, 760-763
32. Adams, P. D., Afonine, P. V., Bunkóczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W., Mc- Coy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., et al. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221
33. Emsley, P., and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132
34. Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., and Ferrin, T. E. (2004) UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612
35. Yuan, F., Zhang, Y., Rajpal, D. K., Wu, X., Guo, D., Wang, M., Taylor, J. S., and Wang, Z. (2000) Specificity of DNA lesion bypass by the yeast DNA polymerase η. J. Biol. Chem. 275, 8233-8239
36. Zang, H., Irimia, A., Choi, J.-Y., Angel, K. C., Loukachevitch, L. V., Egli, M., and Guengerich, F. P. (2006) Efficient and high fidelity incorporation of dCTP opposite 7,8-dihydro-8-oxodeoxyguanosine by Sulfolobus solfataricus DNA polymerase Dpo4. J. Biol. Chem. 281, 2358-2372
37. Furge, L. L., and Guengerich, F. P. (1999) Explanation of pre-steady-state kinetics and decreased burst amplitude of HIV-1 reverse transcriptase at sites of modified DNA bases with an additional, nonproductive enzyme- DNA-nucleotide complex. Biochemistry 38, 4818-4825
38. Jucker, F. M., and Pardi, A. (1995) GNRA tetraloops make a U-turn. RNA 1, 219-222
39. Correll, C. C., Freeborn, B., Moore, P. B., and Steitz, T. A. (1997) Metals, motifs, and recognition in the crystal structure of a 5S rRNA domain. Cell 91, 705-712