A δdinB mutation that sensitizes Escherichia coli to the lethal effects of UV- and X-radiation

Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis

Volumn 763-764, Issue , 2014, Pages 19-27

  Lee, Mei Chong W ^a,c   Franco, Magdalena ^a,d   Vargas, Doris M ^a,e   Hudman, Deborah A ^b   White, Steven J ^a   Fowler, Robert G ^a   Sargentini, Neil J ^b  

^a SAN JOSE STATE UNIVERSITY   (United States)

^b A T STILL UNIVERSITY   (United States)

^c University of California Santa Cruz   (United States)

^d STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e MAYO GRADUATE SCHOOL   (United States)

Author keywords

Checkpoint; DinB; Escherichia coli; TLS; UmuDC; UV radiation sensitivity

Indexed keywords

DNA POLYMERASE; UMUDC POLYMERASE; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATASE; DINB PROTEIN, E COLI; DNA BINDING PROTEIN; DNA DIRECTED DNA POLYMERASE; DNA HELICASE; ESCHERICHIA COLI PROTEIN; UMUC PROTEIN, E COLI; UMUD PROTEIN, E COLI; UVRA PROTEIN, E COLI; UVRB PROTEIN, E COLI;

ARTICLE; BACTERIAL STRAIN; CELL PROTECTION; CELL SURVIVAL; COMPARATIVE STUDY; CONTROLLED STUDY; DINB GENE; DNA DAMAGE; DNA DAMAGE CHECKPOINT; DNA SEQUENCE; ESCHERICHIA COLI; EXCISION REPAIR; GAIN OF FUNCTION MUTATION; GENE; GENE INTERACTION; GENE MUTATION; GROWTH CURVE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RADIATION MUTAGENESIS; RADIOSENSITIVITY; RADIOSENSITIZATION; SENSITIVITY ANALYSIS; ULTRAVIOLET RADIATION; UMUDC GENE; X RAY; ALLELE; GENETICS; METABOLISM; MICROBIAL VIABILITY; MUTATION; RADIATION RESPONSE;

ADENOSINE TRIPHOSPHATASES; ALLELES; DNA HELICASES; DNA-BINDING PROTEINS; DNA-DIRECTED DNA POLYMERASE; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MICROBIAL VIABILITY; MUTATION; ULTRAVIOLET RAYS; X-RAYS;

EID: 84897054813     PISSN: 00275107     EISSN: 09218262     Source Type: Journal    
DOI: 10.1016/j.mrfmmm.2014.03.003     Document Type: Article

References (43)

1. Tang M., Shen X., Frank E.G., O'Donnell M., Woodgate R., Goodman M.F. UmuD'(2)C is an error-prone DNA polymerase, Escherichia coli polV. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:8919-8924.
2. Wagner J., Gruz P., Kim S.R., Yamada M., Matsui K., Fuchs R.P., Nohmi T. The dinB gene encodes a novel E. coli DNA polymerase, DNA pol IV, involved in mutagenesis. Mol. Cell 1999, 4:281-286.
3. Courcelle C.T., Belle J.J., Courcelle J. Nucleotide excision repair or polymerase V-mediated lesion bypass can act to restore UV-arrested replication forks in Escherichia coli. J. Bacteriol. 2005, 187:6953-6961.
4. Steinborn G. Uvm mutants of Escherichia coli K12 deficient in UV mutagenesis: I. Isolation of uvm mutants and their phenotypical characterization in DNA repair and mutagenesis. Mol. Gen. Genet. 1978, 165:87-93.
5. Opperman T., Murli S., Smith B.T., Walker G.C. A model for a umuDC-dependent prokaryotic DNA damage checkpoint. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:9218-9223.
6. Bhamre S., Gadea B.B., Koyama C.A., White S.J., Fowler R.G. An aerobic recA-, umuC-dependent pathway of spontaneous base-pair substitution mutagenesis in Escherichia coli. Mutat. Res. 2001, 473:229-247.
7. Curti E., McDonald J.P., Mead S., Woodgate R. DNA polymerase switching: effects on spontaneous mutagenesis in Escherichia coli. Mol. Microbiol. 2009, 71:315-331.
8. Kato T., Shinoura Y. Isolation and characterization of mutants of Escherichia coli deficient in induction of mutations by ultraviolet light. Mol. Gen. Genet. 1977, 156:121-131.
9. Sargentini N.J., Smith K.C. umuC-dependent and umuC-independent gamma- and UV-radiation mutagenesis in Escherichia coli. Mutat. Res. 1984, 128:1-9.
10. Sargentini N.J., Smith K.C. Ionizing and ultraviolet radiation-induced reversion of sequenced frameshift mutations in Escherichia coli: a new role for umuDC suggested by delayed photoreactivation. Mutat. Res. 1987, 179:55-63.
11. Bjedov I., Dasgupta C.N., Slade D., Le Blastier S., Selva M., Matic I. Involvement of Escherichia coli DNA polymerase IV in tolerance of cytotoxic alkylating DNA lesions in vivo. Genetics 2007, 176:1431-1440.
12. Jarosz D.F., Godoy V.G., Delaney J.C., Essigmann J.M., Walker G.C. A single amino acid governs enhanced activity of DinB DNA polymerases on damaged templates. Nature 2006, 439:225-228.
13. Lovett S.T. Replication arrest-stimulated recombination: dependence on the RecA paralog, RadA/Sms and translesion polymerase, DinB. DNA Repair (Amst.) 2006, 5:1421-1427.
14. Bull H.J., Lombardo M.J., Rosenberg S.M. Stationary-phase mutation in the bacterial chromosome: recombination protein and DNA polymerase IV dependence. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:8334-8341.
15. Tompkins J.D., Nelson J.L., Hazel J.C., Leugers S.L., Stumpf J.D., Foster P.L. Error-prone polymerase, DNA polymerase IV, is responsible for transient hypermutation during adaptive mutation in Escherichia coli. J. Bacteriol. 2003, 185:3469-3472.
16. Godoy V.G., Jarosz D.F., Walker F.L., Simmons L.A., Walker G.C. Y-family DNA polymerases respond to DNA damage-independent inhibition of replication fork progression. EMBO J. 2006, 25:868-879.
17. Indiani C., Langston L.D., Yurieva O., Goodman M.F., O'Donnell M. Translesion DNA polymerases remodel the replisome and alter the speed of the replicative helicase. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:6031-6038.
18. Uchida K., Furukohri A., Shinozaki Y., Mori T., Ogawara D., Kanaya S., Nohmi T., Maki H., Akiyama M. Overproduction of Escherichia coli DNA polymerase DinB (Pol IV) inhibits replication fork progression and is lethal. Mol. Microbiol. 2008, 70:608-622.
19. Strauss B.S., Roberts R., Francis L., Pouryazdanparast P. Role of the dinB gene product in spontaneous mutation in Escherichia coli with an impaired replicative polymerase. J. Bacteriol. 2000, 182:6742-6750.
20. Kuban W., Jonczyk P., Gawel D., Malanowska K., Schaaper R.M., Fijalkowska I.J. Role of Escherichia coli DNA polymerase IV in in vivo replication fidelity. J. Bacteriol. 2004, 186:4802-4807.
21. Wolff E., Kim M., Hu K., Yang H., Miller J.H. Polymerases leave fingerprints: analysis of the mutational spectrum in Escherichia coli rpoB to assess the role of polymerase IV in spontaneous mutation. J. Bacteriol. 2004, 186:2900-2905.
22. Wrzesinski M., Nowosielska A., Nieminuszczy J., Grzesiuk E. Effect of SOS-induced Pol II, Pol IV, and Pol V DNA polymerases on UV-induced mutagenesis and MFD repair in Escherichia coli cells. Acta Biochim. Pol. 2005, 52:139-147.
23. Miller J.H. A Short Course in Bacterial Genetics 1992, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
24. Randles R.H. On tests applied to residuals. J. Am. Stat. Assoc. 1984, 79:349-354.
25. Buffone G.J., Darlington G.J. Isolation of DNA from biological specimens without extraction with phenol. Clin. Chem. 1985, 31:164-165.
26. Miller S.A., Dykes D.D., Polesky H.F. A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res. 1988, 16:1215.
27. Friedberg E.C., Walker G.C., Siede W., Wood R.D., Schultz R.A., Ellenberger T. DNA Repair and Mutagenesis 2006, ASM Press, Washington, DC. 2nd ed.
28. Reuven N.B., Arad G., Maor-Shoshani A., Livneh Z. The mutagenesis protein UmuC is a DNA polymerase activated by UmuD', RecA, and SSB and is specialized for translesion replication. J. Biol. Chem. 1999, 274:31763-31766.
29. 2C is an error-prone DNA polymerase, Escherichia coli pol V. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:8919-8924.
30. Sutton M.D., Walker G.C. umuDC-mediated cold sensitivity is a manifestation of functions of the UmuD2C complex involved in a DNA damage checkpoint control. J. Bacteriol. 2001, 183:1215-1224.
31. Kim S.R., Maenhaut-Michel G., Yamada M., Yamamoto Y., Matsui K., Sofuni T., Nohmi T., Ohmori H. Multiple pathways for SOS-induced mutagenesis in Escherichia coli: an overexpression of dinB/dinP results in strongly enhancing mutagenesis in the absence of any exogenous treatment to damage DNA. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:13792-13797.
32. McKenzie G.J., Magner D.B., Lee P.L., Rosenberg S.M. The dinB operon and spontaneous mutation in Escherichia coli. J. Bacteriol. 2003, 185:3972-3977.
33. Baba T., Ara T., Hasegawa M., Takai Y., Okumura Y., Baba M., Datsenko K.A., Tomita M., Wanner B.L., Mori H. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol. Syst. Biol. 2006, 2. 2006 0008.
34. Woodgate R. Construction of a umuDC operon substitution mutation in Escherichia coli. Mutat. Res. 1992, 281:221-225.
35. Godoy V.G., Jarosz D.F., Simon S.M., Abyzov A., Ilyin V., Walker G.C. UmuD and RecA directly modulate the mutagenic potential of the Y family DNA polymerase DinB. Mol. Cell 2007, 28:1058-1070.
36. Burckhardt S.E., Woodgate R., Scheuermann R.H., Echols H. UmuD mutagenesis protein of Escherichia coli: overproduction, purification, and cleavage by RecA. Proc. Natl. Acad. Sci. U. S. A. 1988, 85:1811-1815.
37. Jiang Q., Karata K., Woodgate R., Cox M.M., Goodman M.F. The active form of DNA polymerase V is UmuD'(2)C-RecA-ATP. Nature 2009, 460:359-363.
38. Cafarelli T.M., Rands T.J., Benson R.W., Rudnicki P.A., Lin I., Godoy V.G. A single residue unique to DinB-like proteins limits formation of the polymerase IV multiprotein complex in Escherichia coli. J. Bacteriol. 2013, 195:1179-1193.
39. Streisinger G., Okada Y., Emrich J., Newton J., Tsugita A., Terzaghi E., Inouye M. Frameshift mutations and the genetic code: this paper is dedicated to Professor Theodosius Dobzhansky on the occasion of his 66th birthday. Cold Spring Harb. Symp. Quant. Biol. 1966, 31:77-84.
40. Taylor L.A., Rose R.E. A correction in the nucleotide sequence of the Tn903 kanamycin resistance determinant in pUC4K. Nucleic Acids Res. 1988, 16:358.
41. Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. Basic local alignment search tool. J. Mol. Biol. 1990, 215:403-410.
42. Blattner F.R., Plunkett G., 3rd C.A., Bloch N.T., Perna V., Burland M., Riley J., Collado-Vides J.D., Glasner C.K., Rode G.F., Mayhew J., Gregor N.W., Davis H.A., Kirkpatrick M.A., Goeden D.J., Rose B., Mau Y., Shao The complete genome sequence of Escherichia coli K-12. Science 1997, 277:1453-1462.
43. Berlyn M.K. Linkage map of Escherichia coli K-12, edition 10: the traditional map. Microbiol. Mol. Biol. Rev. 1998, 62:814-984.