On the mechanism of gene amplification induced under stress in Escherichia coli

PLoS Genetics

Volumn 2, Issue 4, 2006, Pages 385-398

  Slack, Andrew ^a,b   Thornton, P C ^a   Magner, Daniel B ^a   Rosenberg, Susan M ^a   Hastings, P J ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b CENTER FOR CELL AND GENE THERAPY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA DIRECTED DNA POLYMERASE ALPHA; DNA DIRECTED DNA POLYMERASE BETA; DOUBLE STRANDED DNA; FLAP ENDONUCLEASE; DNA; ESCHERICHIA COLI PROTEIN;

ARTICLE; DNA REPAIR; DNA STRAND BREAKAGE; ESCHERICHIA COLI; EXCISION REPAIR; GENE AMPLIFICATION; GENE DUPLICATION; GENE REARRANGEMENT; GENE SEQUENCE; GENE SWITCHING; HOMOLOGOUS RECOMBINATION; NONHUMAN; SEQUENCE HOMOLOGY; STRESS; BACTERIAL GENE; CHEMISTRY; DNA DAMAGE; GENETIC RECOMBINATION; GENETICS; GENOMICS; METABOLISM; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE SEQUENCE;

ESCHERICHIA COLI;

BASE SEQUENCE; DNA; DNA DAMAGE; DNA REPAIR; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE AMPLIFICATION; GENES, BACTERIAL; GENOMICS; MOLECULAR SEQUENCE DATA; MUTATION; RECOMBINATION, GENETIC; SEQUENCE HOMOLOGY, NUCLEIC ACID;

EID: 33646490411     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.0020048     Document Type: Article

References (84)

1. Lengauer C, Kinzler KW, Vogelstein B (1998) Genetic instabilities in human cancers. Nature 396: 643-649.
2. Savelyeva L, Schwab M (2001) Amplification of oncogenes revisited: From expression profiling to clinical application. Cancer Lett 167: 115-123.
3. Sebat J, Lakshmi B, Troge J, Alexander J, Young J, et al. (2004) Large-scale copy number polymorphism in the human genome. Science 305: 525-528.
4. Iafrate AJ, Feuk L, Rivera MN, Listewnik ML, Donahoe PK, et al. (2004) Detection of large-scale variation in the human genome. Nat Genet 36: 949-951.
5. Gonzalez E, Kulkarni H, Bolivar H, Mangano A, Sanchez R, et al. (2005) The influence of CCL3L1 gene-containing segmental duplications on HIV-1/AIDS susceptibility. Science 307: 1434-1440.
6. Hastings PJ, Rosenberg SM (2002) In pursuit of a molecular mechanism for adaptive gene amplification. DNA Repair 1: 111-123.
7. McClintock B (1951) Chromosome organization and genic expression. Cold Spring Harb Symp Quant Biol 16: 13-47.
8. Smith KA, Stark MB, Gorman PA, Stark GR (1992) Fusions near telomeres occur very early in the amplification of CAD genes in Syrian hamster cells. Proc Natl Acad Sci U S A 89: 5427-5431.
9. Ma C, Martin S, Trask B, Hamlin JL (1993) Sister chromatid fusion initiates amplification of the dihydrofolate reductase gene in Chinese hamster cells. Genes Dev 7: 605-620.
10. Coquelle A, Pipiras E, Toledo F, Buttin G, Debatisse M (1997) Expression of fragile sites triggers intrachromosomal mammalian gene amplification and sets boundaries to early amplicons. Cell 89: 215-225.
11. Pipiras E, Coquelle A, Bieth A, Debatisse M (1998) Interstitial deletions and intrachromosomal amplification initiated from a double-strand break targeted to a mammalian chromosome. EMBO J 17: 325-333.
12. Ciullo M, Debily MA, Rozier L, Autiero M, Billault A, et al. (2002) Initiation of the breakage-fusion-bridge mechanism through common fragile site activation in human breast cancer cells: The model of PIP gene duplication from a break at FRA7I. Hum Mol Genet 11: 2887-2894.
13. Windle BE, Wahl GM (1992) Molecular dissection of mammalian gene amplification: new mechanistic insights revealed by analyses of very early events. Mutat Res 276: 199-224.
14. Vogt N, Lefevre SH, Apiou F, Dutrillaux AM, Cor A, et al. (2004) Molecular structure of double-minute chromosomes bearing amplified copies of the epidermal growth factor receptor gene in gliomas. Proc Natl Acad Sci U S A 101: 11368-11373.
15. Debatisse M, Coquelle A, Toledo F, Buttin G (1998) Gene amplification mechanisms: the role of fragile sites. Recent Results Cancer Res 154: 216-226.
16. Tlsty TD, Albertini AM, Miller JH (1984) Gene amplification in the lac region of E. coli. Cell 37: 217-224.
17. Horiuchi T, Tomizawa J-I, Novick A (1962) Isolation and properties of bacteria capable of high rates of β-galactosidase synthesis. Biochim Biophys Acta 55: 152-163.
18. Horiuchi T, Horiuchi S, Novick A (1963) The genetic basis of hypersynthesis of β-galactosidase. Genetics 48: 157.
19. Whoriskey SK, Nghiem V-H, Leong P-M, Masson J-M, Miller JH (1987) Genetic rearrangement and gene amplification in Escherichia coli: DNA sequences at the junctures of amplified gene fusions. Genes Dev 1: 227-237.
20. Edlund T, Normark S (1981) Recombination between short DNA homologies causes tandem duplication. Nature 292: 269-271.
21. Tlsty TD, Margolin BH, Lum K (1989) Differences in the rates of gene amplification in nontumorigenic and tumorigenic cell lines as measured by Luria-Delbrück fluctuation analysis. Proc Natl Acad Sci U S A 86: 9441-9445.
22. Rath H, Tlsty T, Schimke RT (1984) Rapid emergence of methotrexate resistance in cultured mouse cells. Cancer Res 44: 3303-3306.
23. Assaraf YG, Molina A, Schimke RT (1989) Sequential amplification of dihydrofolate reductase and multidrug resistance genes in Chinese hamster ovary cells selected for stepwise resistance to the lipid-soluble antifolate trimetrexate. J Biol Chem 264: 18326-18334.
24. Hastings PJ, Bull HJ, Klump JR, Rosenberg SM (2000) Adaptive amplification: an inducible chromosomal instability mechanism. Cell 103: 723-731.
25. Lombardo MJ, Aponyi I, Rosenberg SM (2004) General stress response regulator RpoS in adaptive mutation and amplification in Escherichia coli. Genetics 166: 669-680.
26. Wilson CR, Morgan AE (1985) Chromosomal-DNA amplification in Bacillus subtilis. J Bacteriol 163: 445-453.
27. Yasui K, Mihara S, Zhao C, Okamoto H, Saito-Ohara F, et al. (2004) Alteration in copy numbers of genes as a mechanism for acquired drug resistance. Cancer Res 64: 1403-1410.
28. Strauss BS (1992) The origin of point mutations in human tumor cells. Cancer Res 52: 249-253.
29. Shaffer LG, Lupski JR (2000) Molecular mechanisms for constitutional chromosomal rearrangements in humans. Annu Rev Genet 34: 297-329.
30. van de Lagemaat LN, Gagnier L, Medstrand P, Mager DL (2005) Genomic deletions and precise removal of transposable elements mediated by short identical DNA segments in primates. Genome Res 15: 1243-1249.
31. Ma J, Bennetzen JL (2004) Rapid recent growth and divergence of rice nuclear genomes. Proc Natl Acad Sci U S A 101: 12404-12410.
32. Hastings PJ, Slack A, Petrosino JF, Rosenberg SM (2004) Adaptive amplification and point mutation are independent mechanisms: Evidence for various stress-inducible mutation mechanisms. PLoS Biol 2: e399. DOI: 10.1371/journal.pbio.0020399.
33. Cairns J, Foster PL (1991) Adaptive reversion of a frameshift mutation in Escherichia coli. Genetics 128: 695-701.
34. McKenzie GJ, Lombardo MJ, Rosenberg SM (1998) Recombination-dependent mutation in Escherichia coli occurs in stationary phase. Genetics 149: 1563-1565.
35. McKenzie GJ, Harris RS, Lee PL, Rosenberg SM (2000) The SOS response regulates adaptive mutation. Proc Natl Acad Sci U S A 97: 6646-6651.
36. Hendrickson H, Slechta ES, Bergthorsson U, Andersson DI, Roth JR (2002) Amplification-mutagenesis: Evidence that "directed" adaptive mutation and general hypermutability result from growth with a selected gene amplification. Proc Natl Acad Sci U S A 99: 2164-2169.
37. Ponder RG, Fonville NC, Rosenberg SM (2005) A switch from high-fidelity to error-prone DNA double-strand break repair underlies stress-induced mutation. Mol Cell 19: 791-804.
38. Kofoid E, Bergthorsson U, Slechta ES, Roth JR (2003) Formation of an F′ plasmid by recombination between imperfectly repeated chromosomal Rep sequences: a closer look at an old friend (F9(128) pro lac). J Bacteriol 185: 660-663.
39. Bzymek M, Lovett ST (2001) Instability of repetitive DNA sequences: The role of replication in multiple mechanisms. Proc Natl Acad Sci U S A 98: 8319-8325.
40. Foster PL, Trimarchi JM (1994) Adaptive reversion of a frameshift mutation in Escherichia coli by simple base deletions in homopolymeric runs. Science 265: 407-409.
41. Rosenberg SM, Longerich S, Gee P, Harris RS (1994) Adaptive mutation by deletions in small mononucleotide repeats. Science 265: 405-407.
42. Powell SC, Wartell RM (2001) Different characteristics distinguish early versus late arising adaptive mutations in Escherichia coli FC40. Mutat Res 473: 219-228.
43. Harris RS, Longerich S, Rosenberg SM (1994) Recombination in adaptive mutation. Science 264: 258-260.
44. Foster PL, Trimarchi JM, Maurer RA (1996) Two enzymes, both of which process recombination intermediates, have opposite effects on adaptive mutation in Escherichia coli. Genetics 142: 25-37.
45. Harris RS, Ross KJ, Rosenberg SM (1996) Opposing roles of the Holliday junction processing systems of Escherichia coli in recombination-dependent adaptive mutation. Genetics 142: 681-691.
46. Bachellier S, Gilson E, Hofnung M, Hill CW (1996) Repeated sequences. In: Curtiss R III, Ingraham JL, Lin ECC, Low KB, Magasanik B, et al., editors. Escherichia coli and Salmonella: Cellular and molecular biology. Washington (D.C.): ASM Press. pp. 2012-2040.
47. Bzymek M, Saveson CJ, Feschenko VV, Lovett ST (1999) Slipped misalignment mechanisms of deletion formation: In vivo susceptibility to nucleases. J Bacteriol 181: 477-482.
48. McKenzie GJ, Lee PL, Lombardo M-J, Hastings PJ, Rosenberg SM (2001) SOS mutator DNA polymerase IV functions in adaptive mutation and not adaptive amplification. Mol Cell 7: 571-579.
49. Bates H, Randall SK, Rayssiguier C, Bridges BA, Goodman MF, et al. (1989) Spontaneous and UV-induced mutations in Escherichia coli K-12 strains with altered or absent DNA polymerase I. J Bacteriol 171: 2480-2484.
50. Glickman BW (1975) The role of DNA polymerase I in excision-repair. Basic Life Sci 5A: 213-218.
51. Nagata Y, Mashimo K, Kawata M, Yamamoto K (2002) The roles of Klenow processing and flap processing activities of DNA polymerase I in chromosome instability in Escherichia coli K12 strains. Genetics 160: 13-23.
52. De Lucia P, Cairns J (1969) Isolation of an E. coli strain with a mutation affecting DNA polymerease. Nature 224: 1164-1166.
53. Friedberg EC, Walker GC, Siede W (1995) DNA repair and mutagenesis. Washington (D. C.): ASM Press. 698 p.
54. Foster PL, Gudmundsson G, Trimarchi JM, Cai H, Goodman MF (1995) Proofreading-defective DNA polymerase II increases adaptive mutation in Escherichia coli. Proc Natl Acad Sci U S A 92: 7951-7955.
55. Sancar A (1996) DNA excision repair. Annu Rev Biochem 65: 43-81.
56. Moolenaar GF, van Rossum-Fikkert S, van Kesteren M, Goosen N (2002) Cho, a second endonuclease involved in Escherichia coli nucleotide excision repair. Proc Natl Acad Sci U S A 99: 1467-1472.
57. Miesel L, Roth JR (1996) Evidence that functions of the "RecF pathway" contribute to RecBCD-dependent transductional recombination. J Bacteriol 178: 3146-3155.
58. Razavy H, Szigety SK, Rosenberg SM (1996) Evidence for both 3′ and 5′ single-strand DNA ends in intermediates in Chi-stimulated recombination in vivo. Genetics 142: 333-339.
59. Lupski JR, Weinstock GM (1992) Short, interspersed repetitive DNA sequences in prokaryotic genomes. J Bacteriol 174: 4525-4529.
60. Jankovic M, Kostic T, Savic DJ (1990) DNA sequence analysis of spontaneous histidine mutations in a polA1 strain of Escherichia coli K12 suggests a specific role of the GTGG sequence. Mol Gen Genet 223: 481-486.
61. Kornreich R, Bishop DF, Desnick RJ (1990) Alpha-galactosidase A gene rearrangements causing Fabry disease. Identification of short direct repeats at breakpoints in an Alu-rich gene. J Biol Chem 265: 9319-9326.
62. Hiasa H, Sakai H, Komano T, Godson GN (1990) Structural features of the priming signal recognized by primase: Mutational analysis of the phage G4 origin of complementary DNA strand synthesis. Nucleic Acids Res 18: 4825-4831.
63. Albertini AM, Hofer M, Calos MP, Miller JH (1982) On the formation of spontaneous deletions: The importance of short sequence homologies in the generation of large deletions. Cell 29: 319-328.
64. Kumagai M, Ikeda H (1991) Molecular analysis of the recombination junctions of lambda bio transducing phages. Mol Gen Genet 230: 60-64.
65. Lovett ST, Feshenko VV (1996) Stabilization of diverged tandem repeats by mismatch repair: Evidence for deletion formation via a misaligned replication intermediate. Proc Natl Acad Sci U S A 93: 7120-7124.
66. Morel P, Reverdy C, Michel B, Ehrlich SD, Cassuto E (1998) The role of SOS and flap processing in microsatellite instability in Escherichia coli. Proc Natl Acad Sci U S A 95: 10003-10008.
67. Tishkoff DX, Filosi N, Gaida GM, Kolodner RD (1997) A novel mutation avoidance mechanism dependent on S. cerevisiae RAD27 is distinct from DNA mismatch repair. Cell 88: 253-263.
68. Ruggiero BL, Topal MD (2004) Triplet repeat expansion generated by DNA slippage is suppressed by human flap endonuclease 1. J Biol Chem 279: 23088-23097.
69. Kucherlapati M, Yang K, Kuraguchi M, Zhao J, Lia M, et al. (2002) Haploinsufficiency of Flap endonuclease (Fen1) leads to rapid tumor progression. Proc Natl Acad Sci U S A 99: 9924-9929.
70. Messer W, Weigel C (1996) Initiation of chromosome replication. In: Curtiss R III, Ingraham JL, Lin ECC, Low KB, Magasanik B, et al., editors. Escherichia coli and Salmonella: Cellular and molecular biology. Washington (D.C.): ASM Press. pp. 1579-1601.
71. Yuan J, Narayanan L, Rockwell S, Glazer PM (2000) Diminished DNA repair and elevated mutagenesis in mammalian cells exposed to hypoxia and low pH. Cancer Res 60: 4372-4376.
72. Friedberg EC, Walker GC, Siede W, Wood RD, Schultz RA, et al. (2005) DNA repair and mutagenesis. 2nd edition. Washington (D. C.): ASM Press. 1118 p.
73. Slechta ES, Bunny KL, Kugelberg E, Kofoid E, Andersson DI, et al. (2003) Adaptive mutation: General mutagenesis is not a programmed response to stress but results from rare coamplification of dinB with lac. Proc Natl Acad Sci U S A 100: 12847-12852.
74. Harris RS, Feng G, Ross KJ, Sidhu R, Thulin C, et al. (1997) Mismatch repair protein MutL becomes limiting during stationary-phase mutation. Genes Dev 11: 2426-2437.
75. Harris RS, Ross KJ, Lombardo MJ, Rosenberg SM (1998) Mismatch repair in Escherichia coli cells lacking single-strand exonucleases ExoI, ExoVII, and RecJ. J Bacteriol 180: 989-993.
76. Escarceller M, Hicks J, Gudmundson G, Trump C, Tonat D, et al. (1994) Involvement of Escherichia coli DNA polymerase II in response to oxidative damage and adaptive mutation. J Bacteriol 176: 6221-6228.
77. Cunningham RP, Saporito SM, Spitzer SG, Weiss B (1986) Endonuclease IV (nfo) mutant of Escherichia coli. J Bacteriol 168: 1120-1127.
78. Phillips GJ, Prasher DC, Kushner SR (1988) Physical and biochemical characterization of cloned sbcB and xonA mutations from Escherichia coli K-12. J Bacteriol 170: 2089-2094.
79. Wolkow CA, DeBoy RT, Craig NL (1996) Conjugating plasmids are preferred targets for Tn7. Genes Dev 10: 2147-2157.
80. Datsenko KA, Wanner BL (2000) One-step gene inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97: 6640-6645.
81. Kovach ME, Elzer PH, Hill DS, Robertson GT, Farris MA, et al. (1995) Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166: 175-176.
82. Vosberg HP, Hoffmann-Berling H (1971) DNA synthesis in nucleotide-permeable Escherichia coli cells. I. Preparation and properties of ethertreated cells. J Mol Biol 58: 739-753.
83. Singer M, Baker TA, Schnitzler G, Deischel SM, Goel M, et al. (1989) A collection of strains containing genetically linked alternating antibiotic resistance elements for genetic mapping of Escherichia coli. Microbiol Rev 53: 1-24.
84. Glickman BW, van Sluis CA, Heijneker HL, Rorsch A (1973) A mutant of Escherichia coli K12 deficient in the 5′-3′ exonucleolytic activity of DNA polymerase I. I. General characterization. Mol Gen Genet 124: 69-82.