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PMID: 16045619 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, U.S. Gov't, P.H.S.

Polyphosphate kinase regulates error-prone replication by DNA polymerase IV in Escherichia coli.

Molecular microbiology ·Vol. 57 ·No. 3 ·2005-08-00 ·Pages 751-61

Stumpf JD, Foster PL

Abstract

The ppk gene encodes polyphosphate kinase (Ppk), an enzyme that catalyses the polymerization of inorganic phosphate into long chains of polyphosphate (polyP). An insertion mutation in ppk causes a decrease in adaptive mutation in Escherichia coli strain FC40. Adaptive mutation in FC40 mostly results from error-prone DNA polymerase IV (Pol IV), encoded by dinB; most of the antimutagenic phenotype of the ppk mutant disappears in a dinB mutant strain. In addition, the ppk mutant causes a decrease in growth-dependent mutations produced by overexpressing Pol IV. However, the amount of Pol IV protein is unchanged in the ppk mutant strain, indicating that the activity or fidelity of Pol IV is altered. Adaptive mutation is inhibited both by the absence of Ppk, which results in low amounts of polyP, and by overproduction of Ppk, which results in high amounts of polyP, suggesting that an optimal level of polyP is necessary. Taken together, these results suggest a novel mechanism involving polyP that directly or indirectly regulates DNA polymerase activity or fidelity.

MeSH Terms
Adaptation, Physiological Escherichia coli/enzymology,genetics,growth & development Escherichia coli Proteins/genetics,metabolism Gene Expression Regulation, Bacterial Mutagenesis Mutation Phosphotransferases (Phosphate Group Acceptor)/genetics,metabolism Ultraviolet Rays
Chemicals
DinB protein, E coli Escherichia coli Proteins Phosphotransferases (Phosphate Group Acceptor) polyphosphate kinase
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Stumpf Jeffrey D
Department of Biology, Indiana University, 1001 E. Third Street, Bloomington, IN 47405, USA.
Foster Patricia L
References (56)
56 references, click to expand
  1. Adaptive mutation in Escherichia coli: a role for conjugation.
    Science. 1995 Apr 21;268(5209):418-20 PMID: 7716545
  2. Population dynamics of a Lac- strain of Escherichia coli during selection for lactose utilization.
    Genetics. 1994 Oct;138(2):253-61 PMID: 7828809
  3. Inorganic polyphosphates in the acquisition of competence in Escherichia coli.
    J Biol Chem. 1995 Jun 2;270(22):12980-3 PMID: 7768888
  4. Adaptive reversion of an episomal frameshift mutation in Escherichia coli requires conjugal functions but not actual conjugation.
    Proc Natl Acad Sci U S A. 1995 Jun 6;92(12):5487-90 PMID: 7777535
  5. Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter.
    J Bacteriol. 1995 Jul;177(14):4121-30 PMID: 7608087
  6. In vivo stability of the Umu mutagenesis proteins: a major role for RecA.
    J Bacteriol. 1996 Jun;178(12):3550-6 PMID: 8655553
  7. Two enzymes, both of which process recombination intermediates, have opposite effects on adaptive mutation in Escherichia coli.
    Genetics. 1996 Jan;142(1):25-37 PMID: 8770582
  8. Opposing roles of the holliday junction processing systems of Escherichia coli in recombination-dependent adaptive mutation.
    Genetics. 1996 Mar;142(3):681-91 PMID: 8849879
  9. Nonadaptive mutations occur on the F' episome during adaptive mutation conditions in Escherichia coli.
    J Bacteriol. 1997 Mar;179(5):1550-4 PMID: 9045812
  10. Guanosine tetra- and pentaphosphate promote accumulation of inorganic polyphosphate in Escherichia coli.
    J Biol Chem. 1997 Aug 22;272(34):21240-3 PMID: 9261133
  11. Inorganic polyphosphate and the induction of rpoS expression.
    Proc Natl Acad Sci U S A. 1997 Oct 14;94(21):11210-5 PMID: 9326588
  12. Functional interaction of Escherichia coli RNA polymerase with inorganic polyphosphate.
    Genes Cells. 1997 Jul;2(7):433-41 PMID: 9366549
  13. Polyphosphate kinase is a component of the Escherichia coli RNA degradosome.
    Mol Microbiol. 1997 Oct;26(2):387-98 PMID: 9383162
  14. 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 Dec 9;94(25):13792-7 PMID: 9391106
  15. DNA polymerase II (polB) is involved in a new DNA repair pathway for DNA interstrand cross-links in Escherichia coli.
    J Bacteriol. 1999 May;181(9):2878-82 PMID: 10217781
  16. SPECIFICITY OF THE INDUCTION OF THE ENZYMES OF THE LAC OPERON IN ESCHERICHIA COLI.
    J Mol Biol. 1964 Nov;10:303-18 PMID: 14235589
  17. Determining mutation rates in bacterial populations.
    Methods. 2000 Jan;20(1):4-17 PMID: 10610800
  18. Roles of E. coli DNA polymerases IV and V in lesion-targeted and untargeted SOS mutagenesis.
    Nature. 2000 Apr 27;404(6781):1014-8 PMID: 10801133
  19. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products.
    Proc Natl Acad Sci U S A. 2000 Jun 6;97(12):6640-5 PMID: 10829079
  20. Complementation of defective translesion synthesis and UV light sensitivity in xeroderma pigmentosum variant cells by human and mouse DNA polymerase eta.
    Nucleic Acids Res. 2000 Jul 1;28(13):2473-80 PMID: 10871396
  21. Inorganic polyphosphate: a molecule of many functions.
    Annu Rev Biochem. 1999;68:89-125 PMID: 10872445
  22. Involvement of inorganic polyphosphate in expression of SOS genes.
    Biochim Biophys Acta. 2000 Sep 7;1493(1-2):73-81 PMID: 10978509
  23. The beta clamp targets DNA polymerase IV to DNA and strongly increases its processivity.
    EMBO Rep. 2000 Dec;1(6):484-8 PMID: 11263491
  24. Comparative gene expression profiles following UV exposure in wild-type and SOS-deficient Escherichia coli.
    Genetics. 2001 May;158(1):41-64 PMID: 11333217
  25. Role of inorganic polyphosphate in promoting ribosomal protein degradation by the Lon protease in E. coli.
    Science. 2001 Jul 27;293(5530):705-8 PMID: 11474114
  26. SOS mutator DNA polymerase IV functions in adaptive mutation and not adaptive amplification.
    Mol Cell. 2001 Mar;7(3):571-9 PMID: 11463382
  27. Roles of chromosomal and episomal dinB genes encoding DNA pol IV in targeted and untargeted mutagenesis in Escherichia coli.
    Mol Genet Genomics. 2001 Oct;266(2):207-15 PMID: 11683261
  28. The Escherichia coli RNA degradosome: structure, function and relationship in other ribonucleolytic multienzyme complexes.
    Biochem Soc Trans. 2002 Apr;30(2):150-5 PMID: 12035760
  29. Error-prone repair DNA polymerases in prokaryotes and eukaryotes.
    Annu Rev Biochem. 2002;71:17-50 PMID: 12045089
  30. Signal transduction and regulatory mechanisms involved in control of the sigma(S) (RpoS) subunit of RNA polymerase.
    Microbiol Mol Biol Rev. 2002 Sep;66(3):373-95, table of contents PMID: 12208995
  31. Induction of a DNA nickase in the presence of its target site stimulates adaptive mutation in Escherichia coli.
    J Bacteriol. 2002 Oct;184(20):5599-608 PMID: 12270817
  32. Adaptive mutation in Escherichia coli.
    Cold Spring Harb Symp Quant Biol. 2000;65:21-9 PMID: 12760017
  33. Error-prone DNA polymerase IV is controlled by the stress-response sigma factor, RpoS, in Escherichia coli.
    Mol Microbiol. 2003 Oct;50(2):549-61 PMID: 14617178
  34. Competitive processivity-clamp usage by DNA polymerases during DNA replication and repair.
    EMBO J. 2003 Dec 1;22(23):6408-18 PMID: 14633999
  35. Global analysis of Escherichia coli RNA degradosome function using DNA microarrays.
    Proc Natl Acad Sci U S A. 2004 Mar 2;101(9):2758-63 PMID: 14981237
  36. General stress response regulator RpoS in adaptive mutation and amplification in Escherichia coli.
    Genetics. 2004 Feb;166(2):669-80 PMID: 15020458
  37. Adaptive point mutation and adaptive amplification pathways in the Escherichia coli Lac system: stress responses producing genetic change.
    J Bacteriol. 2004 Aug;186(15):4838-43 PMID: 15262914
  38. Adaptive mutation in Escherichia coli.
    J Bacteriol. 2004 Aug;186(15):4846-52 PMID: 15262917
  39. Adaptive mutation: how growth under selection stimulates Lac(+) reversion by increasing target copy number.
    J Bacteriol. 2004 Aug;186(15):4855-60 PMID: 15262920
  40. Effects of inorganic polyphosphate on the proteolytic and DNA-binding activities of Lon in Escherichia coli.
    J Biol Chem. 2004 Aug 13;279(33):34406-10 PMID: 15187082
  41. Construction and characterization of new cloning vehicles. II. A multipurpose cloning system.
    Gene. 1977;2(2):95-113 PMID: 344137
  42. DNA-damaging agents stimulate gene expression at specific loci in Escherichia coli.
    Proc Natl Acad Sci U S A. 1980 May;77(5):2819-23 PMID: 6771759
  43. Inducibility of a gene product required for UV and chemical mutagenesis in Escherichia coli.
    Proc Natl Acad Sci U S A. 1981 Sep;78(9):5749-53 PMID: 7029544
  44. Genetic and sequence analysis of frameshift mutations induced by ICR-191.
    J Mol Biol. 1981 Nov 25;153(1):39-64 PMID: 7040679
  45. Enhanced recombination between lambda plac5 and F42lac: identification of cis- and trans-acting factors.
    Proc Natl Acad Sci U S A. 1984 Dec;81(23):7500-4 PMID: 6095300
  46. Quinolone-resistant mutations of the gyrA gene of Escherichia coli.
    Mol Gen Genet. 1988 Jan;211(1):1-7 PMID: 2830458
  47. Adaptive reversion of a frameshift mutation in Escherichia coli.
    Genetics. 1991 Aug;128(4):695-701 PMID: 1916241
  48. Uses of transposons with emphasis on Tn10.
    Methods Enzymol. 1991;204:139-80 PMID: 1658561
  49. The role of oriT in tra-dependent enhanced recombination between mini-F-lac-oriT and lambda plac5.
    Genet Res. 1992 Jun;59(3):157-65 PMID: 1511865
  50. An exopolyphosphatase of Escherichia coli. The enzyme and its ppx gene in a polyphosphate operon.
    J Biol Chem. 1993 Jan 5;268(1):633-9 PMID: 8380170
  51. Polyphosphate present in DNA preparations from filamentous fungal species of Colletotrichum inhibits restriction endonucleases and other enzymes.
    Anal Biochem. 1993 Mar;209(2):291-7 PMID: 8385889
  52. Adaptive mutation: the uses of adversity.
    Annu Rev Microbiol. 1993;47:467-504 PMID: 8257106
  53. Recombination in adaptive mutation.
    Science. 1994 Apr 8;264(5156):258-60 PMID: 8146657
  54. Adaptive mutation by deletions in small mononucleotide repeats.
    Science. 1994 Jul 15;265(5170):405-7 PMID: 8023163
  55. Adaptive reversion of a frameshift mutation in Escherichia coli by simple base deletions in homopolymeric runs.
    Science. 1994 Jul 15;265(5170):407-9 PMID: 8023164
  56. Evidence that F plasmid transfer replication underlies apparent adaptive mutation.
    Science. 1995 Apr 21;268(5209):421-3 PMID: 7716546
Article Info
Journal
Molecular microbiology
Abbr.
Mol Microbiol
ISSN
0950-382X
Published
2005-08-00
Pages
751-61
Language
English
Region
England
NLM ID
8712028
PMCID
PMC1314974
Subset
IM
Grants
NIGMS NIH HHS · R01 GM065175 · United States
NIGMS NIH HHS · GM651575 · United States
PHS HHS · T32 G07757 · United States
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