Preparation of site-specific T = mCG cis-syn cyclobutane dimer-containing template and its error-free bypass by yeast and human polymerase η

Journal of Biological Chemistry

Volumn 287, Issue 11, 2012, Pages 8021-8028

  Song, Qian ^a   Sherrer, Shanen M ^b   Suo, Zucai ^b   Taylor, John Stephen ^a  

^a WASHINGTON UNIVERSITY   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE; CYCLOBUTANE PYRIMIDINE DIMERS; CYCLOBUTANES; DNA DAMAGES; IN-VITRO; OLIGODEOXYNUCLEOTIDES; P53 GENE; SITE-SPECIFIC; SOLVENT POLARITY; TAUTOMERIC FORMS;

ALKYLATION; BUTANE; GENES; SOLVENTS; YEAST;

POLYMERS;

5 METHYLCYTOSINE; CYTOSINE; DNA DIRECTED DNA POLYMERASE ETA; OLIGODEOXYNUCLEOTIDE; PYRIMIDINE DIMER; THYMINE; WATER;

3' UNTRANSLATED REGION; ARTICLE; BASAL CELL CARCINOMA; CONTROLLED STUDY; DNA METHYLATION; DNA SYNTHESIS; DNA TEMPLATE; ENZYME ACTIVE SITE; ERROR; HUMAN; MUTATIONAL ANALYSIS; NONHUMAN; P53 GENE; PRIORITY JOURNAL; SQUAMOUS CELL CARCINOMA; TUMOR GENE; YEAST;

CATALYTIC DOMAIN; CPG ISLANDS; DNA; DNA DAMAGE; DNA METHYLATION; DNA-DIRECTED DNA POLYMERASE; HUMANS; PYRIMIDINE DIMERS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84858009757     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.333591     Document Type: Article

References (50)

1. Brash, D. E., Rudolph, J. A., Simon, J. A., Lin, A., McKenna, G. J., Baden, H. P., Halperin, A. J., and Pontén, J. (1991) A role for sunlight in skin cancer: UV-induced p53 mutations in squamous cell carcinoma. Proc. Natl. Acad. Sci. U.S.A. 88, 10124-10128 (Pubitemid 21915787)
2. Ziegler, A., Leffell, D. J., Kunala, S., Sharma, H. W., Gailani, M., Simon, J. A., Halperin, A. J., Baden, H. P., Shapiro, P. E., and Bale, A. E. (1993) Mutation hotspots due to sunlight in the p53 gene of non-melanoma skin cancers. Proc. Natl. Acad. Sci. U.S.A. 90, 4216-4220 (Pubitemid 23134197)
3. You, Y. H., Li, C., and Pfeifer, G. P. (1999) Involvement of 5-methylcytosine in sunlight-induced mutagenesis. J. Mol. Biol. 293, 493-503 (Pubitemid 29512051)
4. You, Y. H., Szabó, P. E., and Pfeifer, G. P. (2000) Cyclobutane pyrimidine dimers form preferentially at the major p53 mutational hotspot in UVB-induced mouse skin tumors. Carcinogenesis 21, 2113-2117
5. Setlow, R. B., Carrier, W. L., and Bollum, F. J. (1965) Pyrimidine dimers in UV-irradiated poly dI:dC. Proc. Natl. Acad. Sci. U.S.A. 53, 1111-1118
6. Liu, F. T., and Yang, N. C. (1978) Photochemistry of cytosine derivatives. 1. Photochemistry of thymidylyl-(3′ → 5′)-deoxycytidine. Biochemistry 17, 4865-4876
7. Fix, D., and Bockrath, R. (1981) Thermal resistance to photoreactivation of specific mutations potentiated in E. coli B/r ung by ultraviolet light. Mol. Gen. Genet. 182, 7-11
8. Lemaire, D. G., and Ruzsicska, B. P. (1993) Kinetic analysis of the deamination reactions of cyclobutane dimers of thymidylyl-3′,5′- 2′-deoxycytidine and 2′-deoxycytidylyl-3′,5′-thymidine. Biochemistry 32, 2525-2533 (Pubitemid 23090638)
9. Barak, Y., Cohen-Fix, O., and Livneh, Z. (1995) Deamination of cytosine-containing pyrimidine photodimers in UV-irradiated DNA. Significance for UV light mutagenesis. J. Biol. Chem. 270, 24174-24179
10. Peng, W., and Shaw, B. R. (1996) Accelerated deamination of cytosine residues in UV-induced cyclobutane pyrimidine dimers leads to CC→TT transitions. Biochemistry 35, 10172-10181 (Pubitemid 26269935)
11. Tu, Y., Dammann, R., and Pfeifer, G. P. (1998) Sequence- and time-dependent deamination of cytosine bases in UVB-induced cyclobutane pyrimidine dimers in vivo. J. Mol. Biol. 284, 297-311 (Pubitemid 28542455)
12. Nouspikel, T. (2009) DNA repair in mammalian cells: nucleotide excision repair: variations on versatility. Cell. Mol. Life Sci. 66, 994-1009
13. Tornaletti, S. (2009) DNA repair in mammalian cells: transcription- coupled DNA repair: directing your effort where it's most needed. Cell. Mol. Life Sci. 66, 1010-1020
14. Lagerwerf, S., Vrouwe, M. G., Overmeer, R. M., Fousteri, M. I., and Mullenders, L. H. (2011) DNA damage response and transcription. DNA Repair 10, 743-750
15. Waters, L. S., Minesinger, B. K., Wiltrout, M. E., D'Souza, S., Woodruff, R. V., and Walker, G. C. (2009) Eukaryotic translesion polymerases and their roles and regulation in DNA damage tolerance. Microbiol. Mol. Biol.
16. n tract bending and its biological implications. Proc. Natl. Acad. Sci. U.S.A. 88, 9072-9076
17. Jing, Y., Kao, J. F., and Taylor, J. S. (1998) Thermodynamic and base pairing studies of matched and mismatched DNA dodecamer duplexes containing cis-syn, (6-4), and Dewar photoproducts of TT. Nucleic Acids Res. 26, 3845-3853 (Pubitemid 28367994)
18. Park, H., Zhang, K., Ren, Y., Nadji, S., Sinha, N., Taylor, J. S., and Kang, C. (2002) Crystal structure of a DNA decamer containing a cis-syn thymine dimer. Proc. Natl. Acad. Sci. U.S.A. 99, 15965-15970 (Pubitemid 35462732)
19. Huang, J. C., Hsu, D. S., Kazantsev, A., and Sancar, A. (1994) Substrate spectrum of human excinuclease: repair of abasic sites, methylated bases, mismatches, and bulky adducts. Proc. Natl. Acad. Sci. U.S.A. 91, 12213-12217 (Pubitemid 24368635)
20. Johnson, R. E., Prakash, S., and Prakash, L. (1999) Efficient bypass of a thymine-thymine dimer by yeast DNA polymerase, pol η. Science 283, 1001-1004
21. 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 ≲τα ∀. Nature 399, 700-704 (Pubitemid 29289067)
22. Prakash, S., Johnson, R. E., and Prakash, L. (2005) Eukaryotic translesion synthesis DNA polymerases: specificity of structure and function. Annu. Rev. Biochem. 74, 317-353 (Pubitemid 40995510)
23. Sun, L., Zhang, K., Zhou, L., Hohler, P., Kool, E. T., Yuan, F., Wang, Z., and Taylor, J. S. (2003) Yeast pol ≲τα∀ holds a cis-syn thymine dimer loosely in the active site during elongation opposite the 3′-T of the dimer, but tightly opposite the 5′-T. Biochemistry 42, 9431-9437 (Pubitemid 36959251)
24. Hwang, H., and Taylor, J. S. (2005) Evidence for Watson-Crick and not Hoogsteen or wobble base pairing in the selection of nucleotides for insertion opposite pyrimidines and a thymine dimer by yeast DNA pol ≲τα ∀. Biochemistry 44, 4850-4860 (Pubitemid 40396763)
25. 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
26. Jiang, N., and Taylor, J. S. (1993) In vivo evidence that UV-induced C→T mutations at dipyrimidine sites could result from the replicative bypass of cis-syn cyclobutane dimers or their deamination products. Biochemistry 32, 472-481 (Pubitemid 23034883)
27. Danilo, V. I., Les, A., and Alderfer, J. L. (2001) A theoretical study of the cis-syn pyrimidine dimers in the gas phase and water cluster and a tautomer bypass mechanism for the origin of UV-induced mutations. J. Biomol. Struct. Dyn. 19, 179-191 (Pubitemid 32844647)
28. Brown, D. M., and Hewlins, M. J. (1968) Dihydrocytosine and related compounds. J. Chem. Soc. C 2050-2055
29. Dupuy-Mamelle, N., and Pullman, B. (1967) No. 61.-Recherches theoriques sur la structure electronique des purine et pyrimidines bilogiques. IV. Les pyrimidines saturees sur la liaison 5-6. J. Chim. Phys. Phys. Chim. Biol. 64, 708-712
30. Danilov, V. I., Stewart, J. J. P., Les, A., and Alderfer, J. L. (2000) A theoretical study of pyrimidine photohydrates and a proposed mechanism for the mutagenic effect of ultraviolet light. Chem. Phys. Lett. 328, 75-82
31. Yu, S. L., Johnson, R. E., Prakash, S., and Prakash, L. (2001) Requirement of DNA polymerase η for error-free bypass of UV-induced CC and TC photoproducts. Mol. Cell. Biol. 21, 185-188
32. Yoon, J. H., Prakash, L., and Prakash, S. (2009) Highly error-free role of DNA polymerase η in the replicative bypass of UV-induced pyrimidine dimers in mouse and human cells. Proc. Natl. Acad. Sci. U.S.A. 106, 18219-18224
33. Vu, B., Cannistraro, V. J., Sun, L., and Taylor, J. S. (2006) DNA synthesis past a 5-methyl-C-containing cis-syn cyclobutane pyrimidine dimer by yeast pol ≲τα∀ is highly non-mutagenic. Biochemistry 45, 9327-9335 (Pubitemid 44156396)
34. Cannistraro, V. J., and Taylor, J. S. (2009) Acceleration of 5-methylcytosine deamination in cyclobutane dimers by G and its implications for UV-induced C-to-T mutation hotspots. J. Mol. Biol. 392, 1145-1157
35. Frederico, L. A., Kunkel, T. A., and Shaw, B. R. (1990) A sensitive genetic assay for the detection of cytosine deamination: determination of rate Rev. 73, 134-154 constants and the activation energy. Biochemistry 29, 2532-2537 (Pubitemid 20100849)
36. Shen, J. C., Rideout, W. M., 3rd, and Jones, P. A. (1994) The rate of hydrolytic deamination of 5-methylcytosine in double-stranded DNA. Nucleic Acids Res. 22, 972-976
37. Horsfall, M. J., Borden, A., and Lawrence, C. W. (1997) Mutagenic properties of the T-C cyclobutane dimer. J. Bacteriol. 179, 2835-2839 (Pubitemid 27194427)
38. Cannistraro, V. J., and Taylor, J. S. (2004) DNA-thumb interactions and processivity of T7 DNA polymerase in comparison to yeast polymerase ≲τα∀. J. Biol. Chem. 279, 18288-18295 (Pubitemid 38623243)
39. Sherrer, S. M., Fiala, K. A., Fowler, J. D., Newmister, S. A., Pryor, J. M., and Suo, Z. (2011) Quantitative analysis of the efficiency and mutagenic spectra of abasic lesion bypass catalyzed by human Y-family DNA polymerases. Nucleic Acids Res. 39, 609-622
40. Wang, Y., Taylor, J. S., and Gross, M. L. (1999) Nuclease P1 digestion combined with tandem mass spectrometry for the structure determination of DNA photoproducts. Chem. Res. Toxicol. 12, 1077-1082
41. Swan, M. K., Johnson, R. E., Prakash, L., Prakash, S., and Aggarwal, A. K. (2009) Structural basis of high fidelity DNA synthesis by yeast DNA polymerase η. Nat. Struct. Mol. Biol. 16, 979-986
42. Washington, M. T., Johnson, R. E., Prakash, S., and Prakash, L. (2000) Accuracy of thymine-thymine dimer bypass by Saccharomyces cerevisiae DNA polymerase ≲τα∀. Proc. Natl. Acad. Sci. U.S.A. 97, 3094-3099 (Pubitemid 30183261)
43. Washington, M. T., Johnson, R. E., Prakash, L., and Prakash, S. (2001) Accuracy of lesion bypass by yeast and human DNA polymerase ≲τα ∀. Proc. Natl. Acad. Sci. U.S.A. 98, 8355-8360 (Pubitemid 32678035)
44. Brown, J. A., Zhang, L., Sherrer, S. M., Taylor, J. S., Burgers, P. M., and Suo, Z. (2010) Pre-steady-state kinetic analysis of truncated and full-length Saccharomyces cerevisiae DNA polymerase eta. J. Nucleic Acids doi: 10.4061/2010/871939
45. Johnson, R. E., Washington, M. T., Prakash, S., and Prakash, L. (2000) Fidelity of human DNA polymerase ≲τα∀. J. Biol. Chem. 275, 7447-7450 (Pubitemid 30159635)
46. Smith, C. A., Baeten, J., and Taylor, J. S. (1998) The ability of a variety of polymerases to synthesize past site-specific cis-syn, trans-syn-II, (6-4), and Dewar photoproducts of thymidylyl-(3′ → 5′)-thymidine. J. Biol. Chem. 273, 21933-21940 (Pubitemid 28405372)
47. Sun, L., Wang, M., Kool, E. T., and Taylor, J. S. (2000) Pyrene nucleotide as a mechanistic probe: evidence for a transient abasic site-like intermediate in the bypass of dipyrimidine photoproducts by T7 DNA polymerase. Biochemistry 39, 14603-14610
48. Taylor, J. S. (2002) New structural and mechanistic insight into the A rule and the instructional and non-instructional behavior of DNA photoproducts and other lesions. Mutat. Res. 510, 55-70
49. Cannistraro, V. J., and Taylor, J. S. (2010) Methyl CpG-binding protein 2 (MeCP2) enhances photodimer formation at methyl-CpG sites but suppresses dimer deamination. Nucleic Acids Res. 38, 6943-6955
50. Song, Q., Cannistraro, V. J., and Taylor, J. S. (2011) Rotational position of a 5-methylcytosine-containing cyclobutane pyrimidine dimer in a nucleosome greatly affects its deamination rate. J. Biol. Chem. 286, 6329-6335