Instability of repetitive DNA sequences: The role of replication in multiple mechanisms

Rearrangements between tandem sequence homologies of various lengths are a major source of genomic change and can be deleterious to the organism. These rearrangements can result in either deletion or duplication of genetic material flanked by direct sequence repeats. Molecular genetic analysis of repetitive sequence instability in Escherichia coli has provided several clues to the underlying mechanisms of these rearrangements. We present evidence for three mechanisms of RecA-independent sequence rearrangements: simple replication slippage, sister-chromosome exchange-associated slippage, and single-strand annealing. We discuss the constraints of these mechanisms and contrast their properties with RecA-dependent homologous recombination. Replication plays a critical role in the two slipped misalignment mechanisms, and difficulties in replication appear to trigger rearrangements via all these mechanisms.

[1]  F. Young Biochemistry , 1955, The Indian Medical Gazette.

[2]  M. Inouye,et al.  Frameshift mutations and the genetic code. This paper is dedicated to Professor Theodosius Dobzhansky on the occasion of his 66th birthday. , 1966, Cold Spring Harbor symposia on quantitative biology.

[3]  B. Low Formation of merodiploids in matings with a class of Rec- recipient strains of Escherichia coli K12. , 1968, Proceedings of the National Academy of Sciences of the United States of America.

[4]  B. Low,et al.  Genetic Location of Certain Mutations Conferring Recombination Deficiency in Escherichia coli , 1969, Journal of bacteriology.

[5]  F Capaldo-Kimball,et al.  Involvement of Recombination Genes in Growth and Viability of Escherichia coli K-12 , 1971, Journal of bacteriology.

[6]  M. Gefter,et al.  DNA Replication , 2019, Advances in Experimental Medicine and Biology.

[7]  B. Bainbridge,et al.  Genetics , 1981, Experientia.

[8]  D. Galas An analysis of sequence repeats in the lacI gene of Escherichia coli. , 1978, Journal of molecular biology.

[9]  J. Miller,et al.  Genetic studies of the lac repressor. VII. On the molecular nature of spontaneous hotspots in the lacI gene of Escherichia coli. , 1978, Journal of molecular biology.

[10]  Tom Maniatis,et al.  The structure and evolution of the human β-globin gene family , 1980, Cell.

[11]  Timothy J. Foster,et al.  Three Tn10-associated excision events: Relationship to transposition and role of direct and inverted repeats , 1981, Cell.

[12]  A. Albertini,et al.  On the formation of spontaneous deletions: The importance of short sequence homologies in the generation of large deletions , 1982, Cell.

[13]  J. Lemontt,et al.  Molecular and Cellular Mechanisms of Mutagenesis , 1982, Springer US.

[14]  R. Bambara,et al.  Site-specific pausing of deoxyribonucleic acid synthesis catalyzed by four forms of Escherichia coli DNA polymerase III. , 1983, Biochemistry.

[15]  M. Syvanen,et al.  New class of mutations in Escherichia coli (uup) that affect precise excision of insertion elements and bacteriophage Mu growth , 1983, Journal of bacteriology.

[16]  Analysis of spontaneous deletions and gene amplification in the lac region of Escherichia coli. , 1983, Cold Spring Harbor symposia on quantitative biology.

[17]  Characterization of the Escherichia coli SSB-113 mutant single-stranded DNA-binding protein. Cloning of the gene, DNA and protein sequence analysis, high pressure liquid chromatography peptide mapping, and DNA-binding studies. , 1984, The Journal of biological chemistry.

[18]  B. Glickman,et al.  Structural intermediates of deletion mutagenesis: a role for palindromic DNA. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[19]  N. Kleckner,et al.  Mismatch repair mutations of Escherichia coli K12 enhance transposon excision. , 1985, Genetics.

[20]  G. Warren,et al.  Comparison of physical and genetic properties of palindromic DNA sequences , 1985, Journal of bacteriology.

[21]  A. Cohen,et al.  Synthesis of linear plasmid multimers in Escherichia coli K-12 , 1986, Journal of bacteriology.

[22]  W. J. Dower,et al.  High efficiency transformation of E. coli by high voltage electroporation , 1988, Nucleic Acids Res..

[23]  T. Yi,et al.  Illegitimate recombination in an Escherichia coli plasmid: modulation by DNA damage and a new bacterial gene , 1988, Journal of bacteriology.

[24]  S. Lovett,et al.  The genetic dependence of recombination in recD mutants of Escherichia coli. , 1988, Genetics.

[25]  D. Berg,et al.  Palindromy and the location of deletion endpoints in Escherichia coli. , 1989, Genetics.

[26]  S. Lovett,et al.  Genetic and physical analysis of plasmid recombination in recB recC sbcB and recB recC sbcA Escherichia coli K-12 mutants. , 1989, Genetics.

[27]  D. Berg,et al.  Context effects in the formation of deletions in Escherichia coli. , 1990, Genetics.

[28]  N. Sternberg,et al.  Repair of double-stranded DNA breaks by homologous DNA fragments during transfer of DNA into mouse L cells , 1990, Molecular and cellular biology.

[29]  E. Maryon,et al.  Characterization of recombination intermediates from DNA injected into Xenopus laevis oocytes: evidence for a nonconservative mechanism of homologous recombination , 1991, Molecular and cellular biology.

[30]  R. Sinden,et al.  Preferential DNA secondary structure mutagenesis in the lagging strand of replication in E. coli , 1991, Nature.

[31]  G. Dianov,et al.  Mechanisms of deletion formation in Escherichia coli plasmids. II. Deletions mediated by short direct repeats. , 1991, Molecular & general genetics : MGG.

[32]  T. Silhavy,et al.  Escherichia coli xonA (sbcB) mutants enhance illegitimate recombination. , 1991, Genetics.

[33]  J. Miller,et al.  Isolation and characterization of Escherichia coli mutants with altered rates of deletion formation. , 1991, Genetics.

[34]  Karen N. Allen,et al.  On the deletion of inverted repeated DNA in Escherichia coli: effects of length, thermal stability, and cruciform formation in vivo. , 1991, Genetics.

[35]  Jeffrey H. Miller,et al.  A short course in bacterial genetics , 1992 .

[36]  D. Gordenin,et al.  Transposon Tn5 excision in yeast: influence of DNA polymerases alpha, delta, and epsilon and repair genes. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[37]  R. Worton,et al.  Partial gene duplication as a cause of human disease , 1992, Human mutation.

[38]  AC Tose Cell , 1993, Cell.

[39]  S. Kowalczykowski,et al.  The recombination hotspot χ is a regulatory sequence that acts by attenuating the nuclease activity of the E. coli RecBCD enzyme , 1993, Cell.

[40]  S. Lovett,et al.  A sister-strand exchange mechanism for recA-independent deletion of repeated DNA sequences in Escherichia coli. , 1993, Genetics.

[41]  L. Liu,et al.  recA-independent and recA-dependent intramolecular plasmid recombination. Differential homology requirement and distance effect. , 1994, Journal of molecular biology.

[42]  B. Michel,et al.  Copy‐choice illegitimate DNA recombination revisited. , 1994, The EMBO journal.

[43]  P. Lestienne,et al.  Mitochondrial DNA alterations and genetic diseases: a review. , 1994, Biomedicine & pharmacotherapy = Biomedecine & pharmacotherapie.

[44]  E. Dervyn,et al.  Frequency of deletion formation decreases exponentially with distance between short direct repeats , 1994, Molecular microbiology.

[45]  L. Liu,et al.  Specific stimulation of recA-independent plasmid recombination by a DNA sequence at a distance. , 1995, Journal of molecular biology.

[46]  G. Sharples,et al.  Structural and functional similarities between the SbcCD proteins of Escherichia coli and the RAD50 and MRE11 (RAD32) recombination and repair proteins of yeast , 1995, Molecular microbiology.

[47]  R. Sinden,et al.  Differential DNA secondary structure-mediated deletion mutation in the leading and lagging strands , 1995, Journal of bacteriology.

[48]  Nihon Hassei Seibutsu Gakkai,et al.  Genes to cells , 1996 .

[49]  S. Lovett,et al.  Stabilization of diverged tandem repeats by mismatch repair: evidence for deletion formation via a misaligned replication intermediate. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[50]  S. Ehrlich,et al.  Copy-choice recombination mediated by DNA polymerase III holoenzyme from Escherichia coli. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[51]  D. Leach,et al.  The sbcC and sbcD genes of Escherichia coli encode a nuclease involved in palindrome inviability and genetic recombination , 1996, Genes to cells : devoted to molecular & cellular mechanisms.

[52]  B. Michel,et al.  Deletions at stalled replication forks occur by two different pathways , 1997, The EMBO journal.

[53]  D. Leach,et al.  Overexpression, Purification, and Characterization of the SbcCD Protein from Escherichia coli * , 1997, The Journal of Biological Chemistry.

[54]  J. Gowrishankar,et al.  Identification and characterization of ssb and uup mutants with increased frequency of precise excision of transposon Tn10 derivatives: nucleotide sequence of uup in Escherichia coli , 1997, Journal of bacteriology.

[55]  R. Kolodner,et al.  A Novel Mutation Avoidance Mechanism Dependent on S. cerevisiae RAD27 Is Distinct from DNA Mismatch Repair , 1997, Cell.

[56]  B. Michel,et al.  Isolation of a dnaE mutation which enhances RecA‐independent homologous recombination in the Escherichia coli chromosome , 1997, Molecular microbiology.

[57]  D. Leach,et al.  Repair by recombination of DNA containing a palindromic sequence , 1997, Molecular microbiology.

[58]  S. Lovett,et al.  Enhanced deletion formation by aberrant DNA replication in Escherichia coli. , 1997, Genetics.

[59]  L. Kirkham,et al.  The SbcCD nuclease of Escherichia coli is a structural maintenance of chromosomes (SMC) family protein that cleaves hairpin DNA. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[60]  S. Lovett,et al.  Slipped misalignment mechanisms of deletion formation: analysis of deletion endpoints. , 1998, Journal of molecular biology.

[61]  S. Lovett,et al.  Expansion of DNA repeats in Escherichia coli: effects of recombination and replication functions. , 1999, Journal of molecular biology.

[62]  S. Ehrlich,et al.  Replication Slippage of Different DNA Polymerases Is Inversely Related to Their Strand Displacement Efficiency* , 1999, The Journal of Biological Chemistry.

[63]  S. Lovett,et al.  Slipped Misalignment Mechanisms of Deletion Formation: In Vivo Susceptibility to Nucleases , 1999, Journal of bacteriology.

[64]  C. Millar,et al.  Palindromes as substrates for multiple pathways of recombination in Escherichia coli. , 2000, Genetics.

[65]  J. Gowrishankar,et al.  Characterization of the uup Locus and Its Role in Transposon Excisions and Tandem Repeat Deletions inEscherichia coli , 2000, Journal of bacteriology.

[66]  S. Kowalczykowski Initiation of genetic recombination and recombination-dependent replication. , 2000, Trends in biochemical sciences.

[67]  B. Michel Replication fork arrest and DNA recombination. , 2000, Trends in biochemical sciences.