The DinB•RecA complex of Escherichia coli mediates an efficient and high-fidelity response to ubiquitous alkylation lesions

Environmental and Molecular Mutagenesis

Volumn 55, Issue 2, 2014, Pages 92-102

  Cafarelli, Tiziana M ^a   Rands, Thomas J ^a   Godoy, Veronica G ^a  

^a NORTHEASTERN UNIVERSITY   (United States)

Author keywords

DNA replication; Enzyme kinetics; Escherichia coli; Mutagenesis; Nucleotide; Protein complexes

Indexed keywords

DNA REPLICATION; ENZYME KINETICS; ESCHERICHIA COLI; MUTAGENESIS; NUCLEOTIDE; PROTEIN COMPLEXES;

ADENINE; ALKYLATION; DEOXYADENINE NUCLEOTIDES; DEOXYCYTOSINE NUCLEOTIDES; DEOXYGUANINE NUCLEOTIDES; DNA ADDUCTS; DNA REPLICATION; DNA, BACTERIAL; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; KINETICS; MUTAGENESIS; REC A RECOMBINASES; THYMINE NUCLEOTIDES;

EID: 84893723927     PISSN: 08936692     EISSN: 10982280     Source Type: Journal    
DOI: 10.1002/em.21826     Document Type: Article

References (41)

1. Andersson DI, Koskiniemi S, Hughes D. 2010. Biological roles of translesion synthesis DNA polymerases in eubacteria. Mol Microbiol 77:540-548.
2. Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K. 2001. Current protocols in Molecular Biology. New York: Wiley.
3. Benson RW, Norton MD, Lin I, Du Comb WS, Godoy VG. 2011. An active site aromatic triad in Escherichia coli DNA Pol IV coordinates cell survival and mutagenesis in different DNA damaging agents. PLoS One 6:e19944.
4. Beranek DT. 1990. Distribution of methyl and ethyl adducts following alkylation with monofunctional alkylating agents. Mutat Res 231:11-30.
5. Bjedov I, Dasgupta CN, Slade D, Le Blastier S, Selva M, Matic I. 2007. Involvement of Escherichia coli DNA polymerase IV in tolerance of cytotoxic alkylating DNA lesions in vivo. Genetics 176:1431-1440.
6. Bjedov I, Lecointre G, Tenaillon O, Vaury C, Radman M, Taddei F, Denamur E, Matic I. 2003. Polymorphism of genes encoding SOS polymerases in natural populations of Escherichia coli. DNA Repair (Amst) 2:417-426.
7. Buckstein MH, He J, Rubin H. 2008. Characterization of nucleotide pools as a function of physiological state in Escherichia coli. J Bacteriol. 190:718-726.
8. Cafarelli TM, Rands TJ, Benson RW, Rudnicki PA, Lin I, Godoy VG. 2013. A single residue unique to DinB-like proteins limits formation of the Pol IV multi-protein complex in Escherichia coli. J Bacteriol. 195:1179-1193.
9. De Bont R, van Larebeke N. 2004. Endogenous DNA damage in humans: a review of quantitative data. Mutagenesis 19:169-185.
10. Friedberg EC, Fischhaber PL, Kisker C. 2001. Error-prone DNA polymerases: novel structures and the benefits of infidelity. Cell 107:9-12.
11. Friedberg EC, Walker GC, Siede W, Wood RD, Schultz RA, Ellenberger T. 2006. DNA Repair and Mutagenesis, 2nd ed. Washington, DC: ASM Press. xxix, 1118 p., [1111] p. of plates p.
12. Godoy VG, Jarosz DF, Simon SM, Abyzov A, Ilyin V, Walker GC. 2007. UmuD and RecA directly modulate the mutagenic potential of the Y family DNA polymerase DinB. Mol Cell 28:1058-1070.
13. Guo C, Kosarek-Stancel JN, Tang TS, Friedberg EC. 2009. Y-family DNA polymerases in mammalian cells. Cell Mol Life Sci 66:2363-2381.
14. Hori M, Yonekura S, Nohmi T, Gruz P, Sugiyama H, Yonei S, Zhang-Akiyama QM. 2010. Error-Prone Translesion DNA Synthesis by Escherichia coli DNA Polymerase IV (DinB) on Templates Containing 1, 2-dihydro-2-oxoadenine. J Nucleic Acids 2010:807579.
15. Indiani C, Patel M, Goodman MF, O'Donnell ME. 2013. RecA acts as a switch to regulate polymerase occupancy in a moving replication fork. Proc Natl Acad Sci USA 110:5410-5415.
16. Jarosz DF, Beuning PJ, Cohen SE, Walker GC. 2007. Y-family DNA polymerases in Escherichia coli. Trends Microbiol 15:70-77.
17. Jarosz DF, Cohen SE, Delaney JC, Essigmann JM, Walker GC. 2009. A DinB variant reveals diverse physiological consequences of incomplete TLS extension by a Y-family DNA polymerase. Proc Natl Acad Sci USA 106:21137-21142.
18. Jarosz DF, Godoy VG, Delaney JC, Essigmann JM, Walker GC. 2006. A single amino acid governs enhanced activity of DinB DNA polymerases on damaged templates. Nature 439:225-228.
19. Jiang Q, Karata K, Woodgate R, Cox MM, Goodman MF. 2009. The active form of DNA polymerase V is UmuD'(2)C-RecA-ATP. Nature 460:359-363.
20. Johnson RE, Yu SL, Prakash S, Prakash L. 2007. A role for yeast and human translesion synthesis DNA polymerases in promoting replication through 3-methyl adenine. Mol Cell Biol 27:7198-7205.
21. Karata K, Vaisman A, Goodman MF, Woodgate R. 2012. Simple and efficient purification of Escherichia coli DNA polymerase V: cofactor requirements for optimal activity and processivity in vitro. DNA Repair (Amst) 11:431-440.
22. Kim SR, Matsui K, Yamada M, Gruz P, 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.
23. Kitagawa M, Ara T, Arifuzzaman M, Ioka-Nakamichi T, Inamoto E, Toyonaga H, Mori H. 2005. Complete set of ORF clones of Escherichia coli ASKA library (a complete set of E. coli K-12 ORF archive): unique resources for biological research. DNA Res 12:291-299.
24. Kondo N, Takahashi A, Ono K, Ohnishi T. 2010. DNA damage induced by alkylating agents and repair pathways. J Nucleic Acids 2010:543531.
25. Larson K, Sahm J, Shenkar R, Strauss B. 1985. Methylation-induced blocks to in vitro DNA replication. Mutat Res 150:77-84.
26. Minko IG, Yamanaka K, Kozekov ID, Kozekova A, Indiani C, O'Donnell ME, Jiang Q, Goodman MF, Rizzo CJ, Lloyd RS. 2008. Replication bypass of the acrolein-mediated deoxyguanine DNA-peptide cross-links by DNA polymerases of the DinB family. Chem Res Toxicol 21:1983-1990.
27. Ohmori H, Friedberg EC, Fuchs RP, Goodman MF, Hanaoka F, Hinkle D, Kunkel TA, Lawrence CW, Livneh Z, Nohmi T, Prakash L, Prakash S, Todo T, Walker GC, Wang Z, Woodgate R. 2001. The Y-family of DNA polymerases. Mol Cell 8:7-8.
28. Pages V, Mazon G, Naiman K, Philippin G, Fuchs RP. 2012. Monitoring bypass of single replication-blocking lesions by damage avoidance in the Escherichia coli chromosome. Nucleic Acids Res 40:9036-9043.
29. Plosky BS, Frank EG, Berry DA, Vennall GP, McDonald JP, Woodgate R. 2008. Eukaryotic Y-family polymerases bypass a 3-methyl-2'-deoxyadenosine analog in vitro and methyl methanesulfonate-induced DNA damage in vivo. Nucleic Acids Res 36:2152-2162.
30. Sale JE, Lehmann AR, Woodgate R. 2012. Y-family DNA polymerases and their role in tolerance of cellular DNA damage. Nat Rev Mol Cell Biol 13:141-152.
31. Schlacher K, Leslie K, Wyman C, Woodgate R, Cox MM, Goodman MF. 2005. DNA polymerase V and RecA protein, a minimal mutasome. Mol Cell 17:561-572.
32. Sedgwick B. 1997. Nitrosated peptides and polyamines as endogenous mutagens in O6-alkylguanine-DNA alkyltransferase deficient cells. Carcinogenesis 18:1561-1567.
33. Sharma A, Kottur J, Narayanan N, Nair DT. 2013. A strategically located serine residue is critical for the mutator activity of DNA polymerase IV from Escherichia coli. Nucleic Acids Res 41:5104-5114.
34. Studier FW. 2005. Protein production by auto-induction in high density shaking cultures. Protein Expr Purif 41:207-234.
35. Sutton MD, Smith BT, Godoy VG, Walker GC. 2000. The SOS response: recent insights into umuDC-dependent mutagenesis and DNA damage tolerance. Annu Rev Genet 34:479-497.
36. Taverna P, Sedgwick B. 1996. Generation of an endogenous DNA-methylating agent by nitrosation in Escherichia coli. J Bacteriol 178:5105-5111.
37. Tudek B, Boiteux S, Laval J. 1992. Biological properties of imidazole ring-opened N7-methylguanine in M13mp18 phage DNA. Nucleic Acids Res 20:3079-3084.
38. Wagner J, Gruz P, Kim SR, Yamada M, Matsui K, Fuchs RP, Nohmi T. 1999. The dinB gene encodes a novel E. coli DNA polymerase, DNA pol IV, involved in mutagenesis. Mol Cell 4:281-286.
39. Walsh JM, Parasuram R, Rajput PR, Rozners E, Ondrechen MJ, Beuning PJ. 2012. Effects of non-catalytic, distal amino acid residues on activity of E. coli DinB (DNA polymerase IV). Environ Mol Mutagen 53:766-776.
40. Waters LS, Minesinger BK, Wiltrout ME, D'Souza S, Woodruff RV, Walker GC. 2009. Eukaryotic translesion polymerases and their roles and regulation in DNA damage tolerance. Microbiol Mol Biol Rev 73:134-154.
41. Yang W. 2003. Damage repair DNA polymerases Y. Curr Opin Struct Biol 13:23-30.