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PMID: 7923355 Published · ppublish English Journal Article Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

DNA replication triggered by double-stranded breaks in E. coli: dependence on homologous recombination functions.

Cell ·Vol. 78 ·No. 6 ·1994-09-23 ·Pages 1051-61

Asai T, Bates DB, Kogoma T

Abstract

Homologous recombination-dependent DNA replication (RDR) of a lambda cos site-carrying plasmid is demonstrated in E. coli cells when the cells express lambda terminase that introduces a double-stranded break into the cos site. RDR occurs in normal wild-type cells if the plasmid also contains the recombination hotspot chi. Chi is dispensable when cells are induced for the SOS response or contain a recD mutation. recBC sbcA mutant cells are also capable of RDR induction. A recN mutation greatly reduces RDR in normal cells, but not in SOS-induced cells. RDR proceeds by the theta mode or rolling circle mode of DNA synthesis, yielding covalently closed circular plasmid monomers or linear plasmid multimers, respectively. Previously described inducible stable DNA replication is considered to be a special type of RDR that starts exclusively from specific sites (oriMs) on the chromosome.

Related Genes
MeSH Terms
Bacterial Proteins/genetics Base Sequence DNA Damage DNA Repair/genetics DNA Replication DNA Restriction Enzymes Endodeoxyribonucleases/genetics Escherichia coli/genetics Escherichia coli Proteins Exodeoxyribonuclease V Exodeoxyribonucleases/genetics Models, Genetic Molecular Sequence Data Mutation Plasmids/biosynthesis,genetics Recombination, Genetic SOS Response, Genetics Sequence Homology, Nucleic Acid
Chemicals
Bacterial Proteins Escherichia coli Proteins Endodeoxyribonucleases Exodeoxyribonucleases terminase Exodeoxyribonuclease V exodeoxyribonuclease V, E coli DNA Restriction Enzymes RecN protein, Bacteria
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Asai T
Department of Cell Biology, University of New Mexico School of Medicine, Albuquerque 87131.
Bates D B
Kogoma T
References (61)
61 references, click to expand
  1. Genetic analysis of the RecE pathway of genetic recombination in Escherichia coli K-12.
    J Bacteriol. 1981 Jan;145(1):521-32 PMID: 6257642
  2. Exonuclease VIII of Escherichia coli. II. Mechanism of action.
    J Biol Chem. 1983 Sep 10;258(17):10418-24 PMID: 6309804
  3. In vitro insertional mutagenesis with a selectable DNA fragment.
    Gene. 1984 Sep;29(3):303-13 PMID: 6237955
  4. Repair of DNA double-strand breaks in Escherichia coli K12 requires a functional recN product.
    Mol Gen Genet. 1984;195(1-2):267-74 PMID: 6092851
  5. The maturation of coliphage lambda DNA in the absence of its packaging.
    Gene. 1984 Oct;30(1-3):183-94 PMID: 6096213
  6. A new class of Escherichia coli recBC mutants: implications for the role of RecBC enzyme in homologous recombination.
    Proc Natl Acad Sci U S A. 1984 Dec;81(24):7850-4 PMID: 6393130
  7. Chi-dependent DNA strand cleavage by RecBC enzyme.
    Cell. 1985 May;41(1):145-51 PMID: 3888404
  8. RecBC enzyme nicking at Chi sites during DNA unwinding: location and orientation-dependence of the cutting.
    Cell. 1985 May;41(1):153-63 PMID: 3888405
  9. Rec-mediated recombinational activity of two adjacent Chi elements in bacteriophage lambda.
    Genet Res. 1985 Feb;45(1):1-8 PMID: 3158572
  10. Synthesis of linear plasmid multimers in Escherichia coli K-12.
    J Bacteriol. 1986 Jul;167(1):327-35 PMID: 3522548
  11. recD: the gene for an essential third subunit of exonuclease V.
    Proc Natl Acad Sci U S A. 1986 Aug;83(15):5558-62 PMID: 3526335
  12. Quantitation of the involvement of the recA, recB, recC, recF, recJ, recN, lexA, radA, radB, uvrD, and umuC genes in the repair of X-ray-induced DNA double-strand breaks in Escherichia coli.
    Radiat Res. 1986 Jul;107(1):58-72 PMID: 3526390
  13. DNA synthesis dependent on genetic recombination: characterization of a reaction catalyzed by purified bacteriophage T4 proteins.
    Cell. 1986 Dec 5;47(5):793-806 PMID: 3022939
  14. Synthesis of linear multimers of OriC and pBR322 derivatives in Escherichia coli K-12: role of recombination and replication functions.
    J Bacteriol. 1987 Jul;169(7):3131-7 PMID: 3298213
  15. Homologous recombination in procaryotes.
    Microbiol Rev. 1988 Mar;52(1):1-28 PMID: 3280962
  16. PsiB polypeptide prevents activation of RecA protein in Escherichia coli.
    Mol Gen Genet. 1988 Nov;214(3):389-95 PMID: 3063944
  17. The genetic dependence of recombination in recD mutants of Escherichia coli.
    Genetics. 1988 Sep;120(1):37-45 PMID: 3065139
  18. Lethal effect of lambda DNA terminase in recombination deficient Escherichia coli.
    Mol Gen Genet. 1988 Jul;213(1):42-9 PMID: 3065611
  19. Double-strand breaks at an initiation site for meiotic gene conversion.
    Nature. 1989 Mar 2;338(6210):87-90 PMID: 2645528
  20. DNA double-chain breaks in recombination of phage lambda and of yeast.
    Annu Rev Genet. 1988;22:169-97 PMID: 2977087
  21. Identification and purification of a single-stranded-DNA-specific exonuclease encoded by the recJ gene of Escherichia coli.
    Proc Natl Acad Sci U S A. 1989 Apr;86(8):2627-31 PMID: 2649886
  22. A collection of strains containing genetically linked alternating antibiotic resistance elements for genetic mapping of Escherichia coli.
    Microbiol Rev. 1989 Mar;53(1):1-24 PMID: 2540407
  23. Plasmid-mediated lethality and plasmid multimer formation in an Escherichia coli recBC sbcBC mutant. Involvement of RecF recombination pathway genes.
    J Mol Biol. 1989 Oct 20;209(4):623-34 PMID: 2685325
  24. Biochemistry of homologous recombination in Escherichia coli.
    Microbiol Rev. 1994 Sep;58(3):401-65 PMID: 7968921
  25. Biochemical and physical characterization of exonuclease V from Escherichia coli. Comparison of the catalytic activities of the RecBC and RecBCD enzymes.
    J Biol Chem. 1990 Feb 25;265(6):3447-54 PMID: 2154479
  26. Bacteriophage lambda DNA: the beginning of the end.
    J Bacteriol. 1990 Jun;172(6):2819-24 PMID: 2140565
  27. Further tests of a recombination model in which chi removes the RecD subunit from the RecBCD enzyme of Escherichia coli.
    Genetics. 1990 Nov;126(3):519-33 PMID: 2249753
  28. Conjugational recombination in E. coli: myths and mechanisms.
    Cell. 1991 Jan 11;64(1):19-27 PMID: 1986865
  29. Extensive 3'-overhanging, single-stranded DNA associated with the meiosis-specific double-strand breaks at the ARG4 recombination initiation site.
    Cell. 1991 Mar 22;64(6):1155-61 PMID: 2004421
  30. Homologous pairing in vitro stimulated by the recombination hotspot, Chi.
    Cell. 1991 Jul 26;66(2):361-71 PMID: 1855256
  31. Escherichia coli RecBCD enzyme: inducible overproduction and reconstitution of the ATP-dependent deoxyribonuclease from purified subunits.
    Gene. 1991 Jun 15;102(1):1-6 PMID: 1864499
  32. rec genes and homologous recombination proteins in Escherichia coli.
    Biochimie. 1991 Apr;73(4):523-32 PMID: 1911953
  33. Inhibition of the recBCD-dependent activation of Chi recombinational hot spots in SOS-induced cells of Escherichia coli.
    J Bacteriol. 1992 Feb;174(4):1172-8 PMID: 1310498
  34. DMC1: a meiosis-specific yeast homolog of E. coli recA required for recombination, synaptonemal complex formation, and cell cycle progression.
    Cell. 1992 May 1;69(3):439-56 PMID: 1581960
  35. Rad51 protein involved in repair and recombination in S. cerevisiae is a RecA-like protein.
    Cell. 1992 May 1;69(3):457-70 PMID: 1581961
  36. RecBCD enzyme is altered upon cutting DNA at a chi recombination hotspot.
    Proc Natl Acad Sci U S A. 1992 Jun 15;89(12):5226-30 PMID: 1535156
  37. Reconstitution of the activities of the RecBCD holoenzyme of Escherichia coli from the purified subunits.
    J Biol Chem. 1992 Jul 5;267(19):13564-72 PMID: 1618858
  38. Evidence that recBC-dependent degradation of duplex DNA in Escherichia coli recD mutants involves DNA unwinding.
    J Bacteriol. 1992 Aug;174(16):5424-9 PMID: 1322885
  39. Prokaryotic DNA replication.
    Annu Rev Biochem. 1992;61:673-719 PMID: 1497322
  40. DNA damage-inducible origins of DNA replication in Escherichia coli.
    EMBO J. 1992 Nov;11(11):4219-25 PMID: 1396602
  41. Mechanisms for gene conversion and homologous recombination: the double-strand break repair model and the successive half crossing-over model.
    Adv Biophys. 1992;28:81-133 PMID: 1442245
  42. Chi sequence protects against RecBCD degradation of DNA in vivo.
    Proc Natl Acad Sci U S A. 1992 Dec 15;89(24):12073-7 PMID: 1465442
  43. The recombination hotspot chi is a regulatory sequence that acts by attenuating the nuclease activity of the E. coli RecBCD enzyme.
    Cell. 1993 Apr 9;73(1):87-96 PMID: 8384931
  44. RecQ DNA helicase of Escherichia coli. Characterization of the helix-unwinding activity with emphasis on the effect of single-stranded DNA-binding protein.
    J Mol Biol. 1993 Apr 20;230(4):1145-50 PMID: 8387604
  45. Homologous recombination-dependent initiation of DNA replication from DNA damage-inducible origins in Escherichia coli.
    EMBO J. 1993 Aug;12(8):3287-95 PMID: 8344265
  46. Relating biochemistry to biology: how the recombinational repair function of RecA protein is manifested in its molecular properties.
    Bioessays. 1993 Sep;15(9):617-23 PMID: 8240315
  47. Genetic and molecular analyses of the C-terminal region of the recE gene from the Rac prophage of Escherichia coli K-12 reveal the recT gene.
    J Bacteriol. 1993 Dec;175(23):7673-82 PMID: 8244937
  48. Meiosis-induced double-strand break sites determined by yeast chromatin structure.
    Science. 1994 Jan 28;263(5146):515-8 PMID: 8290959
  49. DNA double-strand break repair: genetic determinants of flanking crossing-over.
    Proc Natl Acad Sci U S A. 1994 Feb 1;91(3):1173-7 PMID: 8302849
  50. DNA damage-inducible replication of the Escherichia coli chromosome is initiated at separable sites within the minimal oriC.
    J Mol Biol. 1994 Feb 4;235(5):1459-69 PMID: 8107086
  51. D-loops and R-loops: alternative mechanisms for the initiation of chromosome replication in Escherichia coli.
    J Bacteriol. 1994 Apr;176(7):1807-12 PMID: 8144445
  52. Reversible inactivation of the Escherichia coli RecBCD enzyme by the recombination hotspot chi in vitro: evidence for functional inactivation or loss of the RecD subunit.
    Proc Natl Acad Sci U S A. 1994 Apr 12;91(8):2980-4 PMID: 8159691
  53. Homologous pairing and strand exchange promoted by the Escherichia coli RecT protein.
    Proc Natl Acad Sci U S A. 1994 Apr 12;91(8):3205-9 PMID: 8159725
  54. Chi sites in combination with RecA protein increase the survival of linear DNA in Escherichia coli by inactivating exoV activity of RecBCD nuclease.
    EMBO J. 1994 Jun 15;13(12):2764-76 PMID: 8026461
  55. A new high-capacity cosmid vector and its use.
    Gene. 1980 Nov;11(3-4):271-82 PMID: 6260574
  56. Effect of suppressors of SOS-mediated filamentation on sfiA operon expression in Escherichia coli.
    J Bacteriol. 1983 Jan;153(1):169-75 PMID: 6336731
  57. Recombination of bacteriophage lambda in recD mutants of Escherichia coli.
    Genome. 1989;31(1):53-67 PMID: 2556327
  58. Characteristics of some multiply recombination-deficient strains of Escherichia coli.
    J Bacteriol. 1969 Oct;100(1):231-9 PMID: 4898990
  59. Pedigrees of some mutant strains of Escherichia coli K-12.
    Bacteriol Rev. 1972 Dec;36(4):525-57 PMID: 4568763
  60. Repair of DNA double-strand breaks in Escherichia coli, which requires recA function and the presence of a duplicate genome.
    J Mol Biol. 1977 Oct 15;116(1):81-98 PMID: 338918
  61. Orientation-dependent recombination hotspot activity in bacteriophage lambda.
    J Mol Biol. 1979 Jul 15;131(4):681-95 PMID: 159958
Article Info
Journal
Cell
Abbr.
Cell
ISSN
0092-8674
Published
1994-09-23
Pages
1051-61
Language
English
Region
United States
NLM ID
0413066
PMCID
PMC2988837
Subset
IM
Grants
NIGMS NIH HHS · R01 GM022092-22 · United States
NIGMS NIH HHS · GM22092 · United States
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