Mutagenicity and genotoxicity of (5′ s)-8,5′-cyclo-2′- deoxyadenosine in escherichia coli and replication of (5′ s)-8,5′-cyclopurine-2′-deoxynucleosides in vitro by dna polymerase iv, exo-free klenow fragment, and dpo4

Chemical Research in Toxicology

Volumn 27, Issue 2, 2014, Pages 200-210

  Pednekar, Varsha ^a   Weerasooriya, Savithri ^a   Jasti, Vijay P ^a   Basu, Ashis K ^a  

^a UNIVERSITY OF CONNECTICUT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEOXYADENOSINES; DEOXYGUANOSINE; DNA POLYMERASE BETA; DNA POLYMERASE I; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MUTAGENS; NUCLEOTIDES;

EID: 84894260933     PISSN: 0893228X     EISSN: 15205010     Source Type: Journal    
DOI: 10.1021/tx4002786     Document Type: Article

References (38)

1. Jaruga, P. and Dizdaroglu, M. (2008) 8,5′-Cyclopurine-2′- deoxynucleosides in DNA: mechanisms of formation, measurement, repair and biological effects DNA Repair 7, 1413-1425
2. Huang, H., Das, R. S., Basu, A. K., and Stone, M. P. (2011) Structure of (5′ S)-8,5′-cyclo-2′-deoxyguanosine in DNA J. Am. Chem. Soc. 133, 20357-20368
3. Kuraoka, I., Bender, C., Romieu, A., Cadet, J., Wood, R. D., and Lindahl, T. (2000) Removal of oxygen free-radical-induced 5′,8-purine cyclodeoxynucleosides from DNA by the nucleotide excision-repair pathway in human cells Proc. Natl. Acad. Sci. U.S.A. 97, 3832-3837
4. Brooks, P. J., Wise, D. S., Berry, D. A., Kosmoski, J. V., Smerdon, M. J., Somers, R. L., Mackie, H., Spoonde, A. Y., Ackerman, E. J., Coleman, K., Tarone, R. E., and Robbins, J. H. (2000) The oxidative DNA lesion 8,5′-(S)-cyclo-2′-deoxyadenosine is repaired by the nucleotide excision repair pathway and blocks gene expression in mammalian cells J. Biol. Chem. 275, 22355-22362
5. Pande, P., Das, R. S., Sheppard, C., Kow, Y. W., and Basu, A. K. (2012) Repair efficiency of (5′ S)-8,5′-cyclo-2′-deoxyguanosine and (5′ S)-8,5′-cyclo-2′-deoxyadenosine depends on the complementary base DNA Repair 11, 926-931
6. Brooks, P. J. (2008) The 8,5′-cyclopurine-2′- deoxynucleosides: candidate neurodegenerative DNA lesions in xeroderma pigmentosum, and unique probes of transcription and nucleotide excision repair DNA Repair 7, 1168-1179
7. Kirkali, G., de Souza-Pinto, N. C., Jaruga, P., Bohr, V. A., and Dizdaroglu, M. (2009) Accumulation of (5′ S)-8,5′-cyclo-2′- deoxyadenosine in organs of Cockayne syndrome complementation group B gene knockout mice DNA Repair 8, 274-278
8. Jasti, V. P., Das, R. S., Hilton, B. A., Weerasooriya, S., Zou, Y., and Basu, A. K. (2011) (5′S)-8,5′-cyclo-2′-deoxyguanosine is a strong block to replication, a potent pol V-dependent mutagenic lesion, and is inefficiently repaired in Escherichia coli Biochemistry 50, 3862-3865
9. Yuan, B., Wang, J., Cao, H., Sun, R., and Wang, Y. (2011) High-throughput analysis of the mutagenic and cytotoxic properties of DNA lesions by next-generation sequencing Nucleic Acids Res. 39, 5945-5954
10. Ohmori, H., Friedberg, E. C., Fuchs, R. 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
11. 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
12. Rangarajan, S., Woodgate, R., and Goodman, M. F. (1999) A phenotype for enigmatic DNA polymerase II: a pivotal role for pol II in replication restart in UV-irradiated Escherichia coli Proc. Natl. Acad. Sci. U.S.A. 96, 9224-9229
13. Swanson, A. L., Wang, J., and Wang, Y. (2012) Accurate and efficient bypass of 8,5′-cyclopurine-2′-deoxynucleosides by human and yeast DNA polymerase eta Chem. Res. Toxicol. 25, 1682-1691
14. Wagner, J., Gruz, P., Kim, S. R., Yamada, M., Matsui, K., Fuchs, R. P., and Nohmi, T. (1999) The dinB gene encodes a novel E. coli DNA polymerase, DNA pol IV, involved in mutagenesis Mol. Cell 4, 281-286
15. Hollstein, M., Shomer, B., Greenblatt, M., Soussi, T., Hovig, E., Montesano, R., and Harris, C. C. (1996) Somatic point mutations in the p53 gene of human tumors and cell lines: updated compilation Nucleic Acids Res. 24, 141-146
16. Moriya, M. (1993) Single-stranded shuttle phagemid for mutagenesis studies in mammalian cells: 8-oxoguanine in DNA induces targeted G.C → T.A transversions in simian kidney cells Proc. Natl. Acad. Sci. U.S.A. 90, 1122-1126
17. Raychaudhury, P. and Basu, A. K. (2011) Genetic requirement for mutagenesis of the G[8,5-Me]T cross-link in Escherichia coli: DNA polymerases IV and V compete for error-prone bypass Biochemistry 50, 2330-2338
18. 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
19. Mendelman, L. V., Petruska, J., and Goodman, M. F. (1990) Base mispair extension kinetics. Comparison of DNA polymerase alpha and reverse transcriptase J. Biol. Chem. 265, 2338-2346
20. Kim, S. R., Matsui, K., Yamada, M., Gruz, P., and Nohmi, T. (2001) Roles of chromosomal and episomal dinB genes encoding DNA pol IV in targeted and untargeted mutagenesis in Escherichia coli Mol. Genet. Genomics 266, 207-215
21. Ollis, D. L., Brick, P., Hamlin, R., Xuong, N. G., and Steitz, T. A. (1985) Structure of large fragment of Escherichia coli DNA polymerase I complexed with dTMP Nature 313, 762-766
22. Benkovic, S. J. and Cameron, C. E. (1995) Kinetic analysis of nucleotide incorporation and misincorporation by Klenow fragment of Escherichia coli DNA polymerase I Methods Enzymol. 262, 257-269
23. Ling, H., Boudsocq, F., Woodgate, R., and Yang, W. (2001) Crystal structure of a Y-family DNA polymerase in action: a mechanism for error-prone and lesion-bypass replication Cell 107, 91-102
24. Fiala, K. A. and Suo, Z. (2004) Mechanism of DNA polymerization catalyzed by Sulfolobus solfataricus P2 DNA polymerase IV Biochemistry 43, 2116-2125
25. Fiala, K. A. and Suo, Z. (2004) Pre-steady-state kinetic studies of the fidelity of Sulfolobus solfataricus P2 DNA polymerase IV Biochemistry 43, 2106-2115
26. Ohashi, E., Bebenek, K., Matsuda, T., Feaver, W. J., Gerlach, V. L., Friedberg, E. C., Ohmori, H., and Kunkel, T. A. (2000) Fidelity and processivity of DNA synthesis by DNA polymerase kappa, the product of the human DINB1 gene J. Biol. Chem. 275, 39678-39684
27. Boudsocq, F., Iwai, S., Hanaoka, F., and Woodgate, R. (2001) Sulfolobus solfataricus P2 DNA polymerase IV (Dpo4): an archaeal DinB-like DNA polymerase with lesion-bypass properties akin to eukaryotic pol eta Nucleic Acids Res. 29, 4607-4616
28. Doublie, S., Tabor, S., Long, A. M., Richardson, C. C., and Ellenberger, T. (1998) Crystal structure of a bacteriophage T7 DNA replication complex at 2.2 A resolution Nature 391, 251-258
29. Steitz, T. A. (1999) DNA polymerases: structural diversity and common mechanisms J. Biol. Chem. 274, 17395-17398
30. Boudsocq, F., Kokoska, R. J., Plosky, B. S., Vaisman, A., Ling, H., Kunkel, T. A., Yang, W., and Woodgate, R. (2004) Investigating the role of the little finger domain of Y-family DNA polymerases in low fidelity synthesis and translesion replication J. Biol. Chem. 279, 32932-32940
31. Boudsocq, F., Ling, H., Yang, W., and Woodgate, R. (2002) Structure-based interpretation of missense mutations in Y-family DNA polymerases and their implications for polymerase function and lesion bypass DNA Repair 1, 343-358
32. You, C., Swanson, A. L., Dai, X., Yuan, B., Wang, J., and Wang, Y. (2013) Translesion synthesis of 8,5′-cyclopurine-2′-deoxynucleosides by DNA polymerases eta, iota, and zeta J. Biol. Chem. 288, 28548-28556
33. Lee, C. H., Chandani, S., and Loechler, E. L. (2006) Homology modeling of four Y-family, lesion-bypass DNA polymerases: the case that E. coli Pol IV and human Pol kappa are orthologs, and E. coli Pol V and human Pol eta are orthologs J. Mol. Graphics Model. 25, 87-102
34. 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 eta Nature 465, 1039-1043
35. Biertumpfel, C., Zhao, Y., Kondo, Y., Ramon-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 eta Nature 465, 1044-1048
36. Johnson, R. E., Prakash, L., and Prakash, S. (2005) Distinct mechanisms of cis-syn thymine dimer bypass by Dpo4 and DNA polymerase eta Proc. Natl. Acad. Sci. U.S.A. 102, 12359-12364
37. Tang, M., Pham, P., Shen, X., Taylor, J. S., O'Donnell, M., Woodgate, R., and Goodman, M. F. (2000) Roles of E. coli DNA polymerases IV and V in lesion-targeted and untargeted SOS mutagenesis Nature 404, 1014-1018
38. Prakash, S. and Prakash, L. (2002) Translesion DNA synthesis in eukaryotes: a one-or two-polymerase affair Genes Dev. 16, 1872-1883