Hypermutagenesis in mutA cells is mediated by mistranslational corruption of polymerase, and is accompanied by replication fork collapse

Molecular Microbiology

Volumn 62, Issue 6, 2006, Pages 1752-1763

  Al Mamun, Abu Amar M ^a   Gautam, Satyendra ^a   Humayun, M Zafri ^a  

^a RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; DNA DIRECTED DNA POLYMERASE GAMMA; DNA POLYMERASE; GLUTAMIC ACID; TRANSFER RNA;

ALLELE; ARTICLE; BACTERIOPHAGE T4; CONTROLLED STUDY; DNA REPLICATION; ENVIRONMENTAL FACTOR; ENZYME MODIFICATION; ESCHERICHIA COLI; GENE EXPRESSION; HOMOLOGOUS RECOMBINATION; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROPHAGE; PROTEIN METABOLISM; RECA GENE; REPLICATION FORK; RNA TRANSLATION; SIGNAL TRANSDUCTION;

BACTERIOPHAGE T4; BASE SEQUENCE; DNA MUTATIONAL ANALYSIS; DNA POLYMERASE III; DNA REPLICATION; DNA, BACTERIAL; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; MUTAGENESIS; NUCLEIC ACID CONFORMATION; PLASMIDS; PROTEIN BIOSYNTHESIS; REC A RECOMBINASES; SEQUENCE ANALYSIS, DNA; SOS RESPONSE (GENETICS);

EID: 33751370456     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2006.05490.x     Document Type: Article

References (50)

1. Al Mamun, A.A., Marians, K.J., and Humayun, M.Z. (2002) DNA polymerase III from Escherichia coli cells expressing mutA mistranslator tRNA is error-prone. J Biol Chem 277: 46319-46327.
2. Balashov, S., and Humayun, M.Z. (2002) Mistranslation induced by streptomycin provokes a RecABC/RuvABC-dependent mutator phenotype in Escherichia coli cells. J Mol Biol 315: 513-527.
3. Balashov, S., and Humayun, M.Z. (2003) Escherichia coli cells bearing a ribosomal ambiguity mutation in rpsD have a mutator phenotype that correlates with increased mistranslation. J Bacteriol 185: 5015-5018.
4. Balashov, S., and Humayun, M.Z. (2004) Specificity of spontaneous mutations induced in mutA mutator cells. Mutat Res 548: 9-18.
5. Benzer, S., and Champe, S.P. (1961) Ambivalent rII mutants of phage T4. Proc Natl Acad Sci USA 47: 1025-1038.
6. Berger, H., and Yanofsky, C. (1967) Suppressor selection for amino acid replacements expected on the basis of the genetic code. Science 156: 394-397.
7. Boles, B.R., Thoendel, M., and Singh, P.K. (2004) Self-generated diversity produces 'insurance effects' in biofilm communities. Proc Natl Acad Sci USA 101: 16630-16635.
8. Bouadloun, F., Donner, D., and Kurland, C.G. (1983) Codon-specific missense errors in vivo. EMBO J 2: 1351-1356.
9. Conkling, M.A., and Drake, J.W. (1984) Isolation and characterization of conditional alleles of bacteriophage T4 genes uvsX and uvsY. Genetics 107: 505-523.
10. Cupples, C.G., and Miller, J.H. (1989) A set of lacZ mutations in Escherichia coli that allow rapid detection of each of the six base substitutions. Proc Natl Acad Sci USA 86: 5345-5349.
11. Datsenko, K.A., and Wanner, B.L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97: 6640-6645.
12. Degnen, G.E., and Cox, E.C. (1974) Conditional mutator gene in Escherichia coli: isolation, mapping, and effector studies. J Bacteriol 117: 477-487.
13. Dorazi, R., Lingutla, J.J., and Humayun, M.Z. (2002) Expression of mutant alanine tRNAs increases spontaneous mutagenesis in Escherichia coli. Mol Microbiol 44: 131-142.
14. Echols, H., Lu, C., and Burgers, P.M. (1983) Mutator strains of Escherichia coli, mutD and dnaQ, with defective exo-nucleolytic editing by DNA polymerase III holoenzyme. Proc Natl Acad Sci USA 80: 2189-2192.
15. Fersht, A.R., Knill-Jones, J.W., and Tsui, W.C. (1982) Kinetic basis of spontaneous mutation. Misinsertion frequencies, proofreading specificities and cost of proofreading by DNA polymerases of Escherichia coli. J Mol Biol 156: 37-51.
16. Foster, P.L. (2005) Stress responses and genetic variation in bacteria. Mutat Res 569: 3-11.
17. Hendrickson, H., Slechta, E.S., Bergthorsson, U., Andersson, D.I., and Roth, J.R. (2002) Amplification-mutagenesis: evidence that 'directed' adaptive mutation and general hypermutability result from growth with a selected gene amplification. Proc Natl Acad Sci USA 99: 2164-2169.
18. Hersh, M.N., Ponder, R.G., Hastings, P.J., and Rosenberg, S.M. (2004) Adaptive mutation and amplification in Escherichia coli: two pathways of genome adaptation under stress. Res Microbiol 155: 352-359.
19. Hill, C.W. (1975) Informational suppression of missense mutations. Cell 6: 419-427.
20. Humayun, M.Z. (1998) SOS and Mayday: multiple inducible mutagenic pathways in Escherichia coli. Mol Microbiol 30: 905-910.
21. Jeruzalmi, D., O'Donnell, M., and Kuriyan, J. (2001) Crystal structure of the processivity clamp loader gamma (gamma) complex of E. coli DNA polymerase III. Cell 106: 429-441.
22. Jones, M.E., Thomas, S.M., and Rogers, A. (1994) Luria-Delbruck fluctuation experiments: design and analysis. Genetics 136: 1209-1216.
23. Livny, J., and Friedman, D.I. (2004) Characterizing spontaneous induction of Stx encoding phages using a selectable reporter system. Mol Microbiol 51: 1691-1704.
24. Loftfield, R.B. (1963) The frequency of errors in protein biosynthesis. Biochem J 89: 82-92.
25. Lovett, S.T. (2006) Replication arrest-stimulated recombination: dependence on the RecA paralog, RadA/Sms and translesion polymerase, DinB. DNA Repair (Amst) doi: 10.1016/j.dnarep.2006.008.
26. Maki, H., Mo, J.Y., and Sekiguchi, M. (1991) A strong mutator effect caused by an amino acid change in the alpha subunit of DNA polymerase III of Escherichia coli. J Biol Chem 266: 5055-5061.
27. Michaels, M.L., Cruz, C., and Miller, J.H. (1990) mutA and mutC: two mutator loci in Escherichia coli that stimulate transversions. Proc Natl Acad Sci USA 87: 9211-9215.
28. Miller, J.H. (1992) A Short Course in Bacterial Genetics: A Laboratory Manual and Handbook for Escherichia coli and Related Bacteria. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
29. Murphy, H.S., and Humayun, M.Z. (1997) Escherichia coli cells expressing a mutant glyV (glycine tRNA) gene have a UVM-constitutive phenotype: implications for mechanisms underlying the mutA or mutC mutator effect. J Bacteriol 179: 7507-7514.
30. Ninio, J. (1991) Transient mutators: a semiquantitative analysis of the influence of translation and transcription errors on mutation rates. Genetics 129: 957-962.
31. Parker, J. (1989) Errors and alternatives in reading the universal genetic code. Microbiol Rev 53: 273-298.
32. Pham, P.T., Olson, M.W., McHenry, C.S., and Schaaper, R.M. (1998) The base substitution and frameshift fidelity of Escherichia coli DNA polymerase III holoenzyme in vitro. J Biol Chem 273: 23575-23584.
33. Pham, P.T., Zhao, W., and Schaaper, R.M. (2006) Mutator mutants of Escherichia coli carrying a defect in the DNA polymerase III tau subunit. Mol Microbiol 59: 1149-1161.
34. Podbielski, A., Spellerberg, B., Woischnik, M., Pohl, B., and Lutticken, R. (1996) Novel series of plasmid vectors for gene inactivation and expression analysis in group A streptococci (GAS). Gene 177: 137-147.
35. Ponder, R.G., Fonville, N.C., and Rosenberg, S.M. (2005) A switch from high-fidelity to error-prone DNA double-strand break repair underlies stress-induced mutation. Mol Cell 19: 791-804.
36. Pritchard, A.E., Dallmann, H.G., Glover, B.P., and McHenry, C.S. (2000) A novel assembly mechanism for the DNA polymerase III holoenzyme DnaX complex: association of deltadelta' with DnaX(4) forms DnaX(3)deltadelta'. EMBO J 19: 6536-6545.
37. Ren, L., Al Mamun, A.A., and Humayun, M.Z. (1999) The mutA mistranslator tRNA-induced mutator phenotype requires recA and recB genes, but not the derepression of lexA-regulated functions. Mol Microbiol 32: 607-615.
38. Ren, L., Al Mamun, A.A., and Humayun, M.Z. (2000) Requirement for homologous recombination functions for expression of the mutA mistranslator tRNA-induced mutator phenotype in Escherichia coli. J Bacteriol 182: 1427-1431.
39. Ripley, L.S., and Drake, J.W. (1972) A genetic assay for transversion mutations in bacteriophage T4. Mol Gen Genet 118: 1-10.
40. Santos, M.E., and Drake, J.W. (1994) Rates of spontaneous mutation in bacteriophage T4 are independent of host fidelity determinants. Genetics 138: 553-564.
41. Saveson, C.J., and Lovett, S.T. (1997) Enhanced deletion formation by aberrant DNA replication in Escherichia coli. Genetics 146: 457-470.
42. Schaaper, R.M., and Radman, M. (1989) The extreme mutator effect of Escherichia coli mutD5 results from saturation of mismatch repair by excessive DNA replication errors. EMBO J 8: 3511-3516.
43. Slater, S.C., Lifsics, M.R., O'Donnell, M., and Maurer, R. (1994) holE, the gene coding for the theta subunit of DNA polymerase III of Escherichia coli: characterization of a holE mutant and comparison with a dnaQ (epsilon-subunit) mutant. J Bacteriol 176: 815-821.
44. Slupska, M.M., Baikalov, C., Lloyd, R., and Miller, J.H. (1996) Mutator tRNAs are encoded by the Escherichia coli mutator genes mutA and mutC: a novel pathway for mutagenesis. Proc Natl Acad Sci USA 93: 4380-4385.
45. Slupska, M.M., King, A.G., Lu, L.I., Lin, R.H., Mao, E.F., Lackey, C.A., et al. (1998) Examination of the role of DNA polymerase proofreading in the mutator effect of miscoding tRNAs. J Bacteriol 180: 5712-5717.
46. Sorensen, M.A. (2001) Charging levels of four tRNA species in Escherichia coli Rel(+) and Rel(-) strains during amino acid starvation: a simple model for the effect of ppGpp on translational accuracy. J Mol Biol 307: 785-798.
47. Sugaya, Y., Ihara, K., Masuda, Y., Ohtsubo, E., and Maki, H. (2002) Hyper-processive and slower DNA chain elongation catalysed by DNA polymerase III holoenzyme purified from the dnaE173 mutator mutant of Escherichia coli. Genes Cells 7: 385-399.
48. Taft-Benz, S.A., and Schaaper, R.M. (1999) The C-terminal domain of dnaQ contains the polymerase binding site. J Bacteriol 181: 2963-2965.
49. Wang, F.J., and Ripley, L.S. (1998) The spectrum of acridine resistant mutants of bacteriophage T4 reveals cryptic effects of the tsL141 DNA polymerase allele on spontaneous mutagenesis. Genetics 148: 1655-1665.
50. Zhao, J., Leung, H.E., and Winkler, M.E. (2001) The miaA mutator phenotype of Escherichia coli K-12 requires recombination functions. J Bacteriol 183: 1796-1800.