Replisome assembly and the direct restart of stalled replication forks

Failure to reactivate either stalled or collapsed replication forks is a source of genomic instability in both prokaryotes and eukaryotes. In prokaryotes, dedicated fork repair systems that involve both recombination and replication proteins have been identified genetically and characterized biochemically. Replication conflicts are solved through several pathways, some of which require recombination and some of which operate directly at the stalled fork. Some recent biochemical observations support models of direct fork repair in which the removal of the blocking template lesion is not always required for replication restart.

[1]  K J Marians,et al.  The Escherichia coli preprimosome and DNA B helicase can form replication forks that move at the same rate. , 1987, The Journal of biological chemistry.

[2]  S. Sandler.  Multiple genetic pathways for restarting DNA replication forks in Escherichia coli K-12. , 2000, Genetics.

[3]  J. Lebowitz,et al.  The Escherichia coli dnaB replication protein is a DNA helicase. , 1986, The Journal of biological chemistry.

[4]  Roger Woodgate,et al.  Roles of E. coli DNA polymerases IV and V in lesion-targeted and untargeted SOS mutagenesis , 2000, Nature.

[5]  S. Sandler,et al.  dnaC mutations suppress defects in DNA replication‐ and recombination‐associated functions in priB and priC double mutants in Escherichia coli K‐12 , 1999, Molecular microbiology.

[6]  S. W. Matson,et al.  Bound Lac repressor protein differentially inhibits the unwinding reactions catalyzed by DNA helicases. , 1992, Nucleic acids research.

[7]  T. Kunkel,et al.  Mutagenic replication in human cell extracts of DNA containing site-specific N-2-acetylaminofluorene adducts. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[8]  A. Kornberg,et al.  Replication deficiencies in priA mutants of Escherichia coli lacking the primosomal replication n' protein. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[9]  S. Lovett,et al.  DNA repeat rearrangements mediated by DnaK-dependent replication fork repair. , 2006, Molecular cell.

[10]  K. Marians.  PriA-directed replication fork restart in Escherichia coli. , 2000, Trends in biochemical sciences.

[11]  R. G. Lloyd,et al.  Modulation of recombination and DNA repair by the RecG and PriA helicases of Escherichia coli K-12 , 1996, Journal of bacteriology.

[12]  J. Liu,et al.  PriA-directed Assembly of a Primosome on D Loop DNA* , 1999, The Journal of Biological Chemistry.

[13]  D. Denhardt,et al.  The rep mutation. IV. Slower movement of replication forks in Escherichia coli rep strains. , 1975, Journal of molecular biology.

[14]  R. G. Lloyd,et al.  Recombinational repair and restart of damaged replication forks , 2002, Nature Reviews Molecular Cell Biology.

[15]  B. Michel,et al.  Replication fork collapse at replication terminator sequences , 2002, The EMBO journal.

[16]  K. Marians,et al.  Identification of a domain of Escherichia coli primase required for functional interaction with the DnaB helicase at the replication fork. , 1994, The Journal of biological chemistry.

[17]  T. Okazaki,et al.  Mechanism of DNA chain growth. I. Possible discontinuity and unusual secondary structure of newly synthesized chains. , 1968, Proceedings of the National Academy of Sciences of the United States of America.

[18]  S. Kowalczykowski,et al.  Biochemistry of homologous recombination in Escherichia coli. , 1994, Microbiological reviews.

[19]  C. Wilde,et al.  Exchanges between DNA strands in ultraviolet-irradiated Escherichia coli. , 1971, Journal of molecular biology.

[20]  S. Sandler,et al.  Differential suppression of priA2::kan phenotypes in Escherichia coli K-12 by mutations in priA, lexA, and dnaC. , 1996, Genetics.

[21]  S. Sandler,et al.  Replication fork assembly at recombination intermediates is required for bacterial growth. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[22]  R. Heller,et al.  Unwinding of the Nascent Lagging Strand by Rep and PriA Enables the Direct Restart of Stalled Replication Forks*[boxs] , 2005, Journal of Biological Chemistry.

[23]  K. Kreuzer.  Interplay between DNA replication and recombination in prokaryotes. , 2005, Annual review of microbiology.

[24]  K. Zavitz,et al.  Inactivation of the Escherichia coli priA DNA replication protein induces the SOS response , 1991, Journal of bacteriology.

[25]  J. Griffith,et al.  Analysis of DNA replication forks encountering a pyrimidine dimer in the template to the leading strand. , 1999, Journal of molecular biology.

[26]  T. Baker,et al.  Helicase action of dnaB protein during replication from the Escherichia coli chromosomal origin in vitro. , 1987, The Journal of biological chemistry.

[27]  T. Okazaki,et al.  Mechanism of DNA chain growth XVI. Analyses of RNA-linked DNA pieces in Escherichia coli with polynucleotide kinase. , 1975, Journal of molecular biology.

[28]  W. Xiao,et al.  DNA postreplication repair and mutagenesis in Saccharomyces cerevisiae. , 2001, Mutation research.

[29]  R. Heller,et al.  The disposition of nascent strands at stalled replication forks dictates the pathway of replisome loading during restart. , 2005, Molecular cell.

[30]  B. Michel,et al.  A fork‐clearing role for UvrD , 2005, Molecular microbiology.

[31]  K. Smith,et al.  recA-dependent DNA repair in UV-irradiated Escherichia coli. , 1987, Journal of photochemistry and photobiology. B, Biology.

[32]  K. Smith.  DNA synthesis in sensitive and resistant mutants of Escherichia coli B after ultraviolet irradiation. , 1969, Mutation research.

[33]  V. Iyer,et al.  Usefulness of benzoylated naphthoylated DEAE-cellulose to distinguish and fractionate double-stranded DNA bearing different extents of single-stranded regions. , 1971, Biochimica et biophysica acta.

[34]  H. Masai,et al.  Stabilization of a Stalled Replication Fork by Concerted Actions of Two Helicases* , 2006, Journal of Biological Chemistry.

[35]  B. Michel,et al.  Requirement for RecFOR‐mediated recombination in priA mutant , 2004, Molecular microbiology.

[36]  Grant W. Brown,et al.  Suppression of genomic instability by SLX5 and SLX8 in Saccharomyces cerevisiae. , 2006, DNA repair.

[37]  A. Carr,et al.  Gross Chromosomal Rearrangements and Elevated Recombination at an Inducible Site-Specific Replication Fork Barrier , 2005, Cell.

[38]  K. Marians,et al.  PriA mediates DNA replication pathway choice at recombination intermediates. , 2003, Molecular cell.

[39]  C. Lawrence,et al.  Metabolic suppressors of trimethoprim and ultraviolet light sensitivities of Saccharomyces cerevisiae rad6 mutants , 1979, Journal of bacteriology.

[40]  R. G. Lloyd,et al.  Reverse branch migration of holliday junctions by RecG protein: A new mechanism for resolution of intermediates in recombination and DNA repair , 1993, Cell.

[41]  D. Leach,et al.  Control of crossing over. , 2000, Molecular cell.

[42]  Efterpi Papouli,et al.  Crosstalk between SUMO and ubiquitin on PCNA is mediated by recruitment of the helicase Srs2p. , 2005, Molecular cell.

[43]  T. C. Wang,et al.  Discontinuous DNA replication in a lig-7 strain of Escherichia coli is not the result of mismatch repair, nucleotide-excision repair, or the base-excision repair of DNA uracil. , 1989, Biochemical and biophysical research communications.

[44]  S. Sandler,et al.  A dnaT Mutant With Phenotypes Similar to Those of a priA2::kan Mutant in Escherichia coli K-12 Sequence data from this article have been deposited with the EMBL/GenBank Data Libraries under accession nos. AY331182 and AY331181. , 2004, Genetics.

[45]  J. Vos,et al.  Differential replication of a single, UV-induced lesion in the leading or lagging strand by a human cell extract: fork uncoupling or gap formation. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[46]  M. O’Donnell,et al.  Replisome Assembly Reveals the Basis for Asymmetric Function in Leading and Lagging Strand Replication , 1996, Cell.

[47]  R. G. Lloyd,et al.  Rep and PriA helicase activities prevent RecA from provoking unnecessary recombination during replication fork repair. , 2006, Genes & development.

[48]  Myron F. Goodman,et al.  The importance of repairing stalled replication forks , 2000, Nature.

[49]  R. G. Lloyd,et al.  The DNA replication protein PriA and the recombination protein RecG bind D-loops. , 1997, Journal of molecular biology.

[50]  G. Cadwell,et al.  The DNA replication priming protein, PriA, is required for homologous recombination and double-strand break repair , 1996, Journal of bacteriology.

[51]  T. Kunkel,et al.  Frequency and Fidelity of Translesion Synthesis of Site-specific N-2-Acetylaminofluorene Adducts during DNA Replication in a Human Cell Extract (*) , 1995, The Journal of Biological Chemistry.

[52]  M. O’Donnell,et al.  Functional Uncoupling of Twin Polymerases , 2004, Journal of Biological Chemistry.

[53]  S. Sandler,et al.  A novel dnaC mutation that suppresses priB rep mutant phenotypes in Escherichia coli K‐12 , 2006, Molecular microbiology.

[54]  J. Hurwitz,et al.  Conversion of phiX174 viral DNA to double-stranded form by purified Escherichia coli proteins. , 1974, Proceedings of the National Academy of Sciences of the United States of America.

[55]  J. Liu,et al.  The ordered assembly of the phiX174-type primosome. III. PriB facilitates complex formation between PriA and DnaT. , 1996, The Journal of biological chemistry.

[56]  Tzu-chien V. Wang.  Discontinuous or semi‐discontinuous DNA replication in Escherichia coli? , 2005, BioEssays : news and reviews in molecular, cellular and developmental biology.

[57]  C. McHenry,et al.  Coupling of a Replicative Polymerase and Helicase: A τ–DnaB Interaction Mediates Rapid Replication Fork Movement , 1996, Cell.

[58]  D. Kohda,et al.  Crystal structure of a biologically functional form of PriB from Escherichia coli reveals a potential single-stranded DNA-binding site. , 2005, Biochemical and biophysical research communications.

[59]  J. Courcelle,et al.  Recovery of DNA Replication in UV-IrradiatedEscherichia coli Requires both Excision Repair and RecF Protein Function , 1999, Journal of bacteriology.

[60]  M. O’Donnell,et al.  Replisome assembly at oriC, the replication origin of E. coli, reveals an explanation for initiation sites outside an origin. , 1999, Molecular cell.

[61]  S. Sandler,et al.  Role of PriA in Replication Fork Reactivation inEscherichia coli , 2000, Journal of bacteriology.

[62]  F. Fabre,et al.  UvrD helicase, unlike Rep helicase, dismantles RecA nucleoprotein filaments in Escherichia coli , 2005, The EMBO journal.

[63]  K. Marians,et al.  The ordered assembly of the phiX174-type primosome. I. Isolation and identification of intermediate protein-DNA complexes. , 1996, The Journal of biological chemistry.

[64]  R. Meneghini,et al.  Gaps in DNA synthesized by ultraviolet light-irradiated WI38 human cells. , 1976, Biochimica et biophysica acta.

[65]  P. Nurse,et al.  Two Modes of PriA Binding to DNA* , 1999, The Journal of Biological Chemistry.

[66]  R. Fuchs,et al.  Uncoupling of Leading- and Lagging-Strand DNA Replication During Lesion Bypass in Vivo , 2003, Science.

[67]  R. Schekman,et al.  Ten proteins required for conversion of phiX174 single-stranded DNA to duplex form in vitro. Resolution and reconstitution. , 1975, The Journal of biological chemistry.

[68]  R. G. Lloyd,et al.  Genome stability and the processing of damaged replication forks by RecG. , 2002, Trends in genetics : TIG.

[69]  S. Sandler,et al.  Effects of mutations involving cell division, recombination, and chromosome dimer resolution on a priA2∷kan mutant , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[70]  R. G. Lloyd,et al.  PriA supports two distinct pathways for replication restart in UV‐irradiated Escherichia coli cells , 2003, Molecular microbiology.

[71]  Z. Livneh,et al.  Error-free recombinational repair predominates over mutagenic translesion replication in E. coli. , 2002, Molecular cell.

[72]  L. Prakash.  Characterization of postreplication repair in Saccharomyces cerevisiae and effects of rad6, rad18, rev3 and rad52 mutations , 2004, Molecular and General Genetics MGG.

[73]  R. Heller,et al.  Replication fork reactivation downstream of a blocked nascent leading strand , 2006, Nature.

[74]  M. O’Donnell,et al.  Functional Uncoupling of Twin Polymerases MECHANISM OF POLYMERASE DISSOCIATION FROM A LAGGING-STRAND BLOCK* , 2004 .

[75]  H. Maki,et al.  Fate of DNA replication fork encountering a single DNA lesion during oriC plasmid DNA replication in vitro , 2003, Genes to cells : devoted to molecular & cellular mechanisms.

[76]  R. Kolodner,et al.  Multiple pathways cooperate in the suppression of genome instability in Saccharomyces cerevisiae , 2001, Nature.

[77]  A. Lehmann.  Postreplication repair of DNA in ultraviolet-irradiated mammalian cells. , 1972, Journal of molecular biology.

[78]  P. Howard-Flanders,et al.  Discontinuities in the DNA synthesized in an excision-defective strain of Escherichia coli following ultraviolet irradiation. , 1968, Journal of molecular biology.

[79]  B. Michel,et al.  Multiple pathways process stalled replication forks. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[80]  Arthur Kornberg,et al.  The dnaA protein complex with the E. coli chromosomal replication origin (oriC) and other DNA sites , 1984, Cell.

[81]  M. Cox.  The nonmutagenic repair of broken replication forks via recombination. , 2002, Mutation research.

[82]  A. Ganesan.  Persistence of pyrimidine dimers during post-replication repair in ultraviolet light-irradiated Escherichia coli K12. , 1974, Journal of molecular biology.

[83]  K. Marians,et al.  The Ordered Assembly of the φX174-type Primosome , 1996, The Journal of Biological Chemistry.

[84]  H. Nakai,et al.  Escherichia coli PriA helicase: fork binding orients the helicase to unwind the lagging strand side of arrested replication forks. , 2001, Journal of molecular biology.

[85]  J. Courcelle,et al.  RecA-dependent recovery of arrested DNA replication forks. , 2003, Annual review of genetics.

[86]  S. W. Matson,et al.  DNA helicases: Enzymes with essential roles in all aspects of DNA metabolism , 1994, BioEssays : news and reviews in molecular, cellular and developmental biology.

[87]  P. McGlynn,et al.  PriA helicase and SSB interact physically and functionally. , 2004, Nucleic acids research.

[88]  Hisao Masai,et al.  A Critical Role of the 3′ Terminus of Nascent DNA Chains in Recognition of Stalled Replication Forks* , 2003, Journal of Biological Chemistry.

[89]  A. Kuzminov.  Recombinational Repair of DNA Damage inEscherichia coli and Bacteriophage λ , 1999, Microbiology and Molecular Biology Reviews.

[90]  K. Arai,et al.  Escherichia coli PriA protein is essential for inducible and constitutive stable DNA replication. , 1994, The EMBO journal.

[91]  R. G. Lloyd,et al.  Modulation of RNA Polymerase by (p)ppGpp Reveals a RecG-Dependent Mechanism for Replication Fork Progression , 2000, Cell.

[92]  S. Sandler,et al.  PriA mutations that affect PriA–PriC function during replication restart , 2001, Molecular microbiology.

[93]  J. Gowrishankar,et al.  A dnaC Mutation in Escherichia coli That Affects Copy Number of ColE1-Like Plasmids and the PriA-PriB (but Not Rep-PriC)Pathway of Chromosomal Replication Restart , 2004, Genetics.

[94]  H. Nakai,et al.  Duplex opening by primosome protein PriA for replisome assembly on a recombination intermediate. , 1999, Journal of molecular biology.

[95]  R. G. Lloyd,et al.  Direct rescue of stalled DNA replication forks via the combined action of PriA and RecG helicase activities. , 2002, Molecular cell.

[96]  M. Hall,et al.  Helicase motifs: the engine that powers DNA unwinding , 1999, Molecular microbiology.

[97]  T. Baker,et al.  Extensive unwinding of the plasmid template during staged enzymatic initiation of DNA replication from the origin of the Escherichia coli chromosome , 1986, Cell.

[98]  J. Hurwitz,et al.  Interaction of Escherichia coli dnaB and dnaC(D) gene products in vitro. , 1975, Proceedings of the National Academy of Sciences of the United States of America.

[99]  S. Sandler.  Requirements for Replication Restart Proteins During Constitutive Stable DNA Replication in Escherichia coli K-12 , 2005, Genetics.

[100]  J. Courcelle,et al.  RuvAB and RecG are not essential for the recovery of DNA synthesis following UV-induced DNA damage in Escherichia coli. , 2004, Genetics.

[101]  A. Kornberg,et al.  Replication initiated at the origin (oriC) of the E. coli chromosome reconstituted with purified enzymes , 1984, Cell.

[102]  M. Lopes,et al.  Multiple mechanisms control chromosome integrity after replication fork uncoupling and restart at irreparable UV lesions. , 2006, Molecular cell.

[103]  J. Holton,et al.  Crystal structure of PriB, a component of the Escherichia coli replication restart primosome. , 2004, Structure.