Roles of residues Arg-61 and Gln-38 of human DNA polymerase η in bypass of deoxyguanosine and 7,8-dihydro-8-oxo-2'-deoxyguanosine

Journal of Biological Chemistry

Volumn 290, Issue 26, 2015, Pages 15921-15933

  Su, Yan ^a   Patra, Amritraj ^a   Harp, Joel M ^a   Egli, Martin ^a   Guengerich, F Peter ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATALYST ACTIVITY; CHAINS; DNA; GEL PERMEATION CHROMATOGRAPHY; MOLECULES;

GEL-FILTRATION CHROMATOGRAPHY; HUMAN DNA POLYMERASE; MONOMERIC FORMS; MUTANT PROTEINS; POSITIVE CHARGES; SITE DIRECTED MUTAGENESIS; TERNARY COMPLEX; TRANSFER REACTION;

BIOMOLECULES;

7,8 DIHYDRO 8 OXO 2' DEOXYGUANOSINE; AMINO ACID DERIVATIVE; ARGININE 61; DEOXYGUANOSINE; DNA DIRECTED DNA POLYMERASE ETA; UNCLASSIFIED DRUG; 8-OXO-7-HYDRODEOXYGUANOSINE; DNA; DNA DIRECTED DNA POLYMERASE;

AMINO ACID SUBSTITUTION; AMINO ACID TRANSPORT; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME CONFORMATION; ENZYME MECHANISM; HYDROGEN BOND; HYDROPHOBICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; STATIC ELECTRICITY; STEADY STATE; ANALOGS AND DERIVATIVES; CHEMISTRY; DNA REPLICATION; ENZYME SPECIFICITY; GENETICS; HUMAN; METABOLISM; PROTEIN MOTIF; SITE DIRECTED MUTAGENESIS; X RAY CRYSTALLOGRAPHY;

AMINO ACID MOTIFS; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; DEOXYGUANOSINE; DNA; DNA REPLICATION; DNA-DIRECTED DNA POLYMERASE; HUMANS; MUTAGENESIS, SITE-DIRECTED; SUBSTRATE SPECIFICITY;

EID: 84941299739     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.653691     Document Type: Article

References (57)

1. Guengerich, F. P. (2006) Interactions of carcinogen-bound DNA with individual DNA polymerases. Chem. Rev. 106, 420-452
2. Ohmori, H., Friedberg, E. C., Fuchs, R. P. P., Goodman, M. F., Hanaoka, F., Hinkle, D., Kunkel, T. A., Lawrence, C. W., Livneh, Z., Nohmi, T., Prakash, L., Prakash, S., Todo, T., Walker, G. C., Wang, Z., and Woodgate, R. (2001) The Y-family of DNA polymerases. Mol. Cell 8, 7-8
3. Yang, W., and Woodgate, R. (2007) What a difference a decade makes: insights into translesion DNA synthesis. Proc. Natl. Acad. Sci. U. S. A. 104, 15591-15598
4. Sale, J. E., Lehmann, A. R., and Woodgate, R. (2012) Y-family DNA polymerases and their role in tolerance of cellularDNAdamage. Nat. Rev. Mol. Cell Biol. 13, 141-152
5. Yang, W. (2014) An overview of Y-family DNA polymerases and a case study of human DNA polymerase η. Biochemistry 53, 2793-2803
6. Reha-Krantz, L. J. (2010) DNA polymerase proofreading: multiple roles maintain genome stability. Biochim. Biophys. Acta 1804, 1049-1063
7. Inui, H., Oh, K. S., Nadem, C., Ueda, T., Khan, S. G., Metin, A., Gozukara, E., Emmert, S., Slor, H., Busch, D. B., Baker, C. C., Di Giovanna, J. J., Tamura, D., Seitz, C. S., Gratchev, A., Wu, W. H., Chung, K. Y., Chung, H. J., Azizi, E., Woodgate, R., Schneider, T. D., and Kraemer, K. H. (2008) Xeroderma pigmentosum-variant patients from America, Europe, and Asia. J. Invest. Dermatol. 128, 2055-2068
8. Masutani, C., Kusumoto, R., Yamada, A., Dohmae, N., Yokoi, M., Yuasa, M., Araki, M., Iwai, S., Takio, K., and Hanaoka, F. (1999) The XPV (xeroderma pigmentosum variant) gene encodes human DNA polymerase η. Nature 399, 700-704
9. Johnson, R. E., Kondratick, C. M., Prakash, S., and Prakash, L. (1999) hRAD30 mutations in the variant form of xeroderma pigmentosum. Science 285, 263-265
10. Zhao, Y., Biertümpfel, C., Gregory, M. T., Hua, Y. J., Hanaoka, F., and Yang, W. (2012) Structural basis of human DNA polymerase η-mediated chemoresistance to cisplatin. Proc. Natl. Acad. Sci. U. S. A. 109, 7269-7274
11. Gregory, M. T., Park, G. Y., Johnstone, T. C., Lee, Y. S., Yang, W., and Lippard, S. J. (2014) Structural and mechanistic studies of polymerase η bypass of phenanthriplatin DNA damage. Proc. Natl. Acad. Sci. U. S. A. 111, 9133-9138
12. Vaisman, A., Masutani, C., Hanaoka, F., and Chaney, S. G. (2000) Efficient translesion replication past oxaliplatin and cisplatin GpG adducts by human DNA polymerase η. Biochemistry 39, 4575-4580
13. Masutani, C., Kusumoto, R., Iwai, S., and Hanaoka, F. (2000) Mechanisms of accurate translesion synthesis by human DNA polymerase η. EMBO J. 19, 3100-3109
14. Bassett, E., King, N. M., Bryant, M. F., Hector, S., Pendyala, L., Chaney, S. G., and Cordeiro-Stone, M. (2004) The role of DNA polymerase η in translesion synthesis past platinum-DNA adducts in human fibroblasts. Cancer Res. 64, 6469-6475
15. Albertella, M. R., Green, C. M., Lehmann, A. R., and O'Connor, M. J. (2005) A role for polymerase η in the cellular tolerance to cisplatin-induced damage. Cancer Res. 65, 9799-9806
16. Chen, Y. W., Cleaver, J. E., Hanaoka, F., Chang, C. F., and Chou, K. M. (2006) A novel role of DNA polymerase η in modulating cellular sensitivity to chemotherapeutic agents. Mol. Cancer Res. 4, 257-265
17. Hicks, J. K., Chute, C. L., Paulsen, M. T., Ragland, R. L., Howlett, N. G., Guéranger, Q., Glover, T. W., and Canman, C. E. (2010) Differential roles for DNA polymerases eta, zeta, and REV1 in lesion bypass of intrastrand versus interstrand DNA cross-links. Mol. Cell Biol. 30, 1217-1230
18. Kawamoto, T., Araki, K., Sonoda, E., Yamashita, Y. M., Harada, K., Kikuchi, K., Masutani, C., Hanaoka, F., Nozaki, K., Hashimoto, N., and Takeda, S. (2005) Dual roles for DNA polymerase η in homologous DNA recombination and translesion DNA synthesis. Mol. Cell 20, 793-799
19. McIlwraith, M. J., Vaisman, A., Liu, Y., Fanning, E., Woodgate, R., and West, S. C. (2005) Human DNA polymerase η promotes DNA synthesis from strand invasion intermediates of homologous recombination. Mol. Cell 20, 783-792
20. Bugreev, D. V., Hanaoka, F., and Mazin, A. V. (2007) Rad54 dissociates homologous recombination intermediates by branch migration. Nat. Struct. Mol. Biol. 14, 746-753
21. Zhao, Y., Gregory, M. T., Biertümpfel, C., Hua, Y. J., Hanaoka, F., and Yang, W. (2013) Mechanism of somatic hypermutation at the WA motif by human DNA polymerase η. Proc. Natl. Acad. Sci. U. S. A. 110, 8146-8151
22. Zeng, X., Winter, D. B., Kasmer, C., Kraemer, K. H., Lehmann, A. R., and Gearhart, P. J. (2001) DNA polymerase η is an A-T mutator in somatic hypermutation of immunoglobulin variable genes. Nat. Immunol. 2, 537-541
23. Delbos, F., De Smet, A., Faili, A., Aoufouchi, S., Weill, J. C., and Reynaud, C. A. (2005) Contribution of DNA polymerase η to immunoglobulin gene hypermutation in the mouse. J. Exp. Med. 201, 1191-1196
24. Pavlov, Y. I., Rogozin, I. B., Galkin, A. P., Aksenova, A. Y., Hanaoka, F., Rada, C., and Kunkel, T. A. (2002) Correlation of somatic hypermutation specificity and A-T base pair substitution errors by DNA polymerase η during copying of a mouse immunoglobulin kappa light chain transgene. Proc. Natl. Acad. Sci. U. S. A. 99, 9954-9959
25. Rogozin, I. B., and Pavlov, Y. I. (2003) Theoretical analysis of mutation hotspots and their DNA sequence context specificity. Mutat. Res. 544, 65-85
26. Wilson, T. M., Vaisman, A., Martomo, S. A., Sullivan, P., Lan, L., Hanaoka, F., Yasui, A., Woodgate, R., and Gearhart, P. J. (2005) MSH2-MSH6 stimulatesDNApolymerase η, suggesting a role for A:T mutations in antibody genes. J. Exp. Med. 201, 637-645
27. Delbos, F., Aoufouchi, S., Faili, A., Weill, J. C., and Reynaud, C. A. (2007) DNA polymerase η is the sole contributor of A/T modifications during immunoglobulin gene hypermutation in the mouse. J. Exp. Med. 204, 17-23
28. Silverstein, T. D., Jain, R., Johnson, R. E., Prakash, L., Prakash, S., and Aggarwal, A. K. (2010) Structural basis for error-free replication of oxidatively damaged DNA by yeast DNA polymerase η. Structure 18, 1463-1470
29. Haracska, L., Yu, S. L., Johnson, R. E., Prakash, L., and Prakash, S. (2000) Efficient and accurate replication in the presence of 7, 8-dihydro-8-oxoguanine by DNA polymerase η. Nat. Genet. 25, 458-461
30. 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-2η-deoxyguanosine bypass by human DNA polymerase η. J. Biol. Chem. 289, 16867-16882
31. Van Loon, B., Markkanen, E., and Hübscher, U. (2010) Oxygen as a friend and enemy: how to combat the mutational potential of 8-oxo-guanine. DNA Repair 9, 604-616
32. Maga, G., Villani, G., Crespan, E., Wimmer, U., Ferrari, E., Bertocci, B., and Hübscher, U. (2007) 8-Oxo-guanine bypass by human DNA polymerases in the presence of auxiliary proteins. Nature 447, 606-608
33. Zahn, K. E., Wallace, S. S., and Doublié, S. (2011) DNA polymerases provide a canon of strategies for translesion synthesis past oxidatively generated lesions. Curr. Opin. Struct. Biol. 21, 358-369
34. Nakamura, T., Zhao, Y., Yamagata, Y., Hua, Y. J., and Yang, W. (2012) Watching DNA polymerase η make a phosphodiester bond. Nature 487, 196-201
35. 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 η. Nature 465, 1044-1048
36. Silverstein, T. D., Johnson, R. E., Jain, R., Prakash, L., Prakash, S., and Aggarwal, A. K. (2010) Structural basis for the suppression of skin cancers by DNA polymerase η. Nature 465, 1039-1043
37. Patra, A., Zhang, Q., Lei, L., Su, Y., Egli, M., and Guengerich, F. P. (2015) Structural and kinetic analysis of nucleoside triphosphate incorporation opposite an abasic site by human translesion DNA polymerase η. J. Biol. Chem. 290, 8028-8038
38. Ummat, A., Silverstein, T. D., Jain, R., Buku, A., Johnson, R. E., Prakash, L., Prakash, S., and Aggarwal, A. K. (2012) Human DNA polymerase η is pre-aligned for dNTP binding and catalysis. J. Mol. Biol. 415, 627-634
39. Schorr, S., Schneider, S., Lammens, K., Hopfner, K. P., and Carell, T. (2010) Mechanism of replication blocking and bypass of Y-family polymerase η by bulky acetylaminofluorene DNA adducts. Proc. Natl. Acad. Sci. U. S. A. 107, 20720-20725
40. Sassa, A., Beard, W. A., Shock, D. D., and Wilson, S. H. (2013) Steady-state, pre-steady-state, and single-turnover kinetic measurement for DNA glycosylase activity. J. Vis. Exp. 10.3791/50695
41. Otwinowski, Z., and Minor, W. (1997) Processing of x-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326
42. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674
43. 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., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221
44. Langer, G. G., Hazledine, S., Wiegels, T., Carolan, C., and Lamzin, V. S. (2013) Visual automated macromolecular model building. Acta Crystallogr. D Biol. Crystallogr. 69, 635-641
45. Murshudov, G. N., Skubák, P., Lebedev, A. A., Pannu, N. S., Steiner, R. A., Nicholls, R. A., Winn, M. D., Long, F., and Vagin, A. A. (2011) REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr. D Biol. Crystallogr. 67, 355-367
46. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501
47. 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
48. 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
49. Egli, M., and Sarkhel, S. (2007) Lone pair-aromatic interactions: to stabilize or not to stabilize. Acc. Chem. Res. 40, 197-205
50. Eoff, R. L., Irimia, A., Angel, K. C., Egli, M., and Guengerich, F. P. (2007) Hydrogen bonding of 7, 8-dihydro-8-oxodeoxyguanosine with a charged residue in the little finger domain determines miscoding events in Sulfolobus solfataricus DNA polymerase Dpo4. J. Biol. Chem. 282, 19831-19843
51. Suarez, S. C., Beardslee, R. A., Toffton, S. M., and McCulloch, S. D. (2013) Biochemical analysis of active site mutations of human polymerase η. Mutat. Res. 745, 46-54
52. Wouters, J. (1998) Cation-π (Na+-Trp) interactions in the crystal structure of tetragonal lysozyme. Protein Sci. 7, 2472-2475
53. Tereshko, V., Wilds, C. J., Minasov, G., Prakash, T. P., Maier, M. A., Howard, A., Wawrzak, Z., Manoharan, M., and Egli, M. (2001) Detection of alkali metal ions in DNA crystals using state-of-the-art x-ray diffraction experiments. Nucleic Acids Res. 29, 1208-1215
54. Lin, H. K., Chase, S. F., Laue, T. M., Jen-Jacobson, L., and Trakselis, M. A. (2012) Differential temperature-dependent multimeric assemblies of replication and repair polymerases on DNA increase processivity. Biochemistry 51, 7367-7382
55. Tang, K. H., Niebuhr, M., Aulabaugh, A., and Tsai, M. D. (2008) Solution structures of 2:1 and 1:1 DNA polymerase-DNA complexes probed by ultracentrifugation and small-angle x-ray scattering. Nucleic Acids Res. 36, 849-860
56. Tang, K. H., and Tsai, M. D. (2008) Structure and function of 2:1 DNA polymerase. DNA complexes. J. Cell Physiol. 216, 315-320
57. Kent, T., Chandramouly, G., McDevitt, S. M., Ozdemir, A. Y., and Pomerantz, R. T. (2015) Mechanism of microhomology-mediated end-joining promoted by human DNA polymerase. Nat. Struct. Mol. Biol. 22, 230-237