The replication fork's five degrees of freedom, their failure and genome rearrangements

Current Opinion in Cell Biology

Volumn 21, Issue 6, 2009, Pages 778-784

  Weinert, T ^a   Kaochar, S ^a   Jones, H ^a   Paek, A ^a   Clark, AJ ^a  

^a The University of Arizona   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA POLYMERASE; HISTONE H3;

CARCINOGENICITY; CELL BUDDING; CHROMOSOME REARRANGEMENT; DNA REPAIR; DNA REPLICATION; DNA SEQUENCE; DNA TEMPLATE; DOUBLE STRANDED DNA BREAK; GENE REARRANGEMENT; GENE SWITCHING; GENOMIC INSTABILITY; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; REVIEW; SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY; YEAST;

ANIMALS; CELL CYCLE PROTEINS; CHROMOSOMES; DNA BREAKS, DOUBLE-STRANDED; DNA REPLICATION; GENE REARRANGEMENT; GENOME; GENOMIC INSTABILITY; HUMANS;

EID: 70549097977     PISSN: 09550674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ceb.2009.10.004     Document Type: Review

References (56)

1. Kolodner R.D., Putnam C.D., and Myung K. Maintenance of genome stability in Saccharomyces cerevisiae. Science 297 5581 (2002) 552-557
2. Sharp A.J., Hansen S., Selzer R.R., Cheng Z., Regan R., Hurst J.A., Stewart H., Price S.M., Blair E., Hennekam R.C., et al. Discovery of previously unidentified genomic disorders from the duplication architecture of the human genome. Nat Genet 38 9 (2006) 1038-1042
3. Lee J.A., Carvalho C.M., and Lupski J.R. A DNA replication mechanism for generating nonrecurrent rearrangements associated with genomic disorders. Cell 131 7 (2007) 1235-1247. An oft-cited study of the structure of genome rearrangements in a human disorder. The authors invoke a template-switch model, in which DNA polymerase must 'hop' 3 or 4 times between sequences up to 0.5 MB apart to sequences of little homology, to make sense of the rearrangement structures.
4. Mefford H.C., and Eichler E.E. Duplication hotspots, rare genomic disorders, and common disease. Curr Opin Genet Dev 19 3 (2009) 196-204
5. Narayanan V., Mieczkowski P.A., Kim H., Petes T.D., and Lobachev K.S. The pattern of gene amplification is determined by the chromosomal location of hairpin-capped breaks. Cell 125 7 (2006) 1283-1296
6. Aguilera A., and Gomez-Gonzalez B. Genome instability: a mechanistic view of its causes and consequences. Nat Rev Genet 9 3 (2008) 204-217
7. Ivessa A.S., Lenzmeier B.A., Bessler J.B., Goudsouzian L.K., Schnakenberg S.L., and Zakian V.A. The Saccharomyces cerevisiae helicase Rrm3p facilitates replication past nonhistone protein-DNA complexes. Mol Cell 12 6 (2003) 1525-1536. A classic study showing that in budding yeast, the replication apparatus may stall about once every 10 kb (if the Rrm3 DNA helicase is defective).
8. Cordeiro-Stone M., Makhov A.M., Zaritskaya L.S., and Griffith J.D. Analysis of DNA replication forks encountering a pyrimidine dimer in the template to the leading strand. J Mol Biol 289 5 (1999) 1207-1218. A key study, using SV40 replication in vitro, defined plasmid templates with damage, and EM to study structures, that DNA replication can be uncoupled.
9. Pages V., and Fuchs R.P. Uncoupling of leading- and lagging-strand DNA replication during lesion bypass in vivo. Science 300 5623 (2003) 1300-1303. A beautiful study using multiple technical tricks and mutants to show that, in bacteria, a lesion that blocks the leading strand (and lagging strand-data not shown) causes uncoupling of DNA synthesis, with absolutely no detectable delay in replication.
10. Friedel A.M., Pike B.L., and Gasser S.M. ATR/Mec1: coordinating fork stability and repair. Curr Opin Cell Biol 21 2 (2009) 237-244
11. Heller R.C., and Marians K.J. Replisome assembly and the direct restart of stalled replication forks. Nat Rev Mol Cell Biol 7 12 (2006) 932-943
12. Atkinson J., and McGlynn P. Replication fork reversal and the maintenance of genome stability. Nucleic Acids Res 37 11 (2009) 3475-3492. An absolutely marvelous review that describes fully the issues of replication fork biology, complete with diagrams of strands going this way and that make sense and are easy to follow.
13. Cobb J.A., Bjergbaek L., Shimada K., Frei C., and Gasser S.M. DNA polymerase stabilization at stalled replication forks requires Mec1 and the RecQ helicase Sgs1. EMBO J 22 16 (2003) 4325-4336. The study often credited, among others, with defining what a collapsed fork does; DNA polymerases dissociate (regulated by Mec1) and Mcm helicases (regulated by Rad53). They performed ChIP experiments on synchronized cells after HU-depletion, generating stalled forks in specific regions of the genome.
14. Haber J.E., Lopes M., Cotta-Ramusino C., Pellicioli A., Liberi G., Foiani M., MaffiolettiG, Lucca C., Baryskhnikova A., and Chiolo I. Rad51-dependent DNA structures accumulate at damaged replication forks in sgs1 mutants defective in the yeast ortholog of BLM RecQ helicase. Genes Dev 19 3 (2005) 339-350
15. Lopes M., Cotta-Ramusino C., Liberi G., and Foiani M. Branch migrating sister chromatid junctions form at replication origins through Rad51/Rad52-independent mechanisms. Mol Cell 12 6 (2003) 1499-1510
16. Zou H., and Rothstein R. Holliday junctions accumulate in replication mutants via a RecA homolog-independent mechanism. Cell 90 1 (1997) 87-96
17. Friedman K.L., and Brewer B.J. Analysis of replication intermediates by two-dimensional agarose gel electrophoresis. Methods Enzymol 262 (1995) 613-627
18. Sogo J.M., Lopes M., and Foiani M. Fork reversal and ssDNA accumulation at stalled replication forks owing to checkpoint defects. Science 297 5581 (2002) 599-602. A landmark study using EM to study the stalled DNA structures from yeast cells.
19. Katou Y., Kanoh Y., Bando M., Noguchi H., Tanaka H., Ashikari T., Sugimoto K., and Shirahige K. S-phase checkpoint proteins Tof1 and Mrc1 form a stable replication-pausing complex. Nature 424 6952 (2003) 1078-1083
20. Possoz C., Filipe S.R., Grainge I., and Sherratt D.J. Tracking of controlled Escherichia coli replication fork stalling and restart at repressor-bound DNA in vivo. EMBO J 25 11 (2006) 2596-2604
21. Bidnenko V., Ehrlich S.D., and Michel B. Replication fork collapse at replication terminator sequences. EMBO J 21 14 (2002) 3898-3907
22. Calzada A., Hodgson B., Kanemaki M., Bueno A., and Labib K. Molecular anatomy and regulation of a stable replisome at a paused eukaryotic DNA replication fork. Genes Dev 19 16 (2005) 1905-1919
23. Lambert S., Watson A., Sheedy D.M., Martin B., and Carr A.M. Gross chromosomal rearrangements and elevated recombination at an inducible site-specific replication fork barrier. Cell 121 5 (2005) 689-702. This study describes a RFB system in fission yeast that may yield deep insight into replication fork biology. In this study, the RTS system was maniupulated to cause profound stalls of forks, leading to genome rearrangements.
24. Lopes M., Cotta-Ramusino C., Pellicioli A., Liberi G., Plevani P., Muzi-Falconi M., Newlon C.S., and Foiani M. The DNA replication checkpoint response stabilizes stalled replication forks. Nature 412 6846 (2001) 557-561
25. Tercero J.A., and Diffley J.F. Regulation of DNA replication fork progression through damaged DNA by the Mec1/Rad53 checkpoint. Nature 412 6846 (2001) 553-557
26. Long D.T., and Kreuzer K.N. Regression supports two mechanisms of fork processing in phage T4. Proc Natl Acad Sci U S A 105 19 (2008) 6852-6857. A remarkable system described in this review. The 'origin fork' may indeed be a very informative model for understanding fork behavior in more genetically complex eukaryotic systems. In particular, the authors find a specific 2-D gel structure that appears to be an intact regressed fork.
27. Branzei D., Vanoli F., and Foiani M. SUMOylation regulates Rad18-mediated template switch. Nature 456 7224 (2008) 915-920. One of what will be many studies struggling to understand post-replication repair and their links to specific DNA structures.
28. Lopes M., Foiani M., and Sogo J.M. Multiple mechanisms control chromosome integrity after replication fork uncoupling and restart at irreparable UV lesions. Mol Cell 21 1 (2006) 15-27
29. •], this EM study of DNA structures suggests how specific proteins are linked to specific DNA structures; Rad53 allows regressed fork formation, and Exo1 acts on regressed forks.
30. •]).
31. Blastyák A., Pintér L., Unk I., Prakash L., Prakash S., and Haracska L. Yeast Rad5 protein required for postreplication repair has a DNA helicase activity specific for replication fork regression. Mol Cell 28 1 (2007) 167-175
32. Kerrest A., Anand R.P., Sundararajan R., Bermejo R., Liberi G., Dujon B., Freudenreich C.H., and Richard G.F. SRS2 and SGS1 prevent chromosomal breaks and stabilize triplet repeats by restraining recombination. Nat Struct Mol Biol 16 2 (2009) 159-167
33. Indiani C., Langston L.D., Yurieva O., Goodman M.F., and O'Donnell M. Translesion DNA polymerases remodel the replisome and alter the speed of the replicative helicase. Proc Natl Acad Sci U S A 106 15 (2009) 6031-6038
34. Lovett S.T. Encoded errors: mutations and rearrangements mediated by misalignment at repetitive DNA sequences. Mol Microbiol 52 5 (2004) 1243-1253
35. Smith C.E., Llorente B., and Symington L.S. Template switching during break-induced replication. Nature 447 7140 (2007) 102-105. Study shows how DNA polymerase must switch between allelic sequences on two homologs as it carries out replication, starting from a DSB (A BIR event).
36. Schmidt K.H., Wu J., and Kolodner R.D. Control of translocations between highly diverged genes by Sgs1, the Saccharomyces cerevisiae homolog of the Bloom's syndrome protein. Mol Cell Biol 26 14 (2006) 5406-5420
37. Rattray A.J., Shafer B.K., Neelam B., and Strathern J.N. A mechanism of palindromic gene amplification in Saccharomyces cerevisiae. Genes Dev 19 11 (2005) 1390-1399. A genomic instability system induced by a DSB that generates palindromes by the single-strand DNA 'looping' back and pairing with small regions of homology. The mechanism was deduced from sequencing the rearrangements formed.
38. Weitao T., Budd M., Hoopes L.L., and Campbell J.L. Dna2 helicase/nuclease causes replicative fork stalling and double-strand breaks in the ribosomal DNA of Saccharomyces cerevisiae. J Biol Chem 278 25 (2003) 22513-22522
39. Seigneur M., Bidnenko V., Ehrlich S.D., and Michel B. RuvAB acts at arrested replication forks. Cell 95 3 (1998) 419-430
40. Putnam C.D., Pennaneach V., and Kolodner R.D. Saccharomyces cerevisiae as a model system to define the chromosomal instability phenotype. Mol Cell Biol 25 16 (2005) 7226-7238
41. Payen C., Koszul R., Dujon B., and Fischer G. Segmental duplications arise from Pol32-dependent repair of broken forks through two alternative replication-based mechanisms. PLoS Genet 4 9 (2008) pe1000175. A study of segmental duplication in budding yeast. The system is described briefly in this review. It is a lovely study.
42. Elliott B., and Jasin M. Double-strand breaks and translocations in cancer. Cell Mol Life Sci 59 2 (2002) 373-385
43. Elliott B., Richardson C., and Jasin M. Chromosomal translocation mechanisms at intronic alu elements in mammalian cells. Mol Cell 17 6 (2005) 885-894
44. Nikiforova M.N., Stringer J.R., Blough R., Medvedovic M., Fagin J.A., and Nikiforov Y.E. Proximity of chromosomal loci that participate in radiation-induced rearrangements in human cells. Science 290 5489 (2000) 138-141
45. Lichten M., and Haber J.E. Position effects in ectopic and allelic mitotic recombination in Saccharomyces cerevisiae. Genetics 123 2 (1989) 261-268
46. Burgess S.M., and Kleckner N. Collisions between yeast chromosomal loci in vivo are governed by three layers of organization. Genes Dev 13 14 (1999) 1871-1883
47. Bi X., and Liu L.F. DNA rearrangement mediated by inverted repeats. Proc Natl Acad Sci U S A 93 2 (1996) 819-823
48. Kitamura E., Blow J.J., and Tanaka T.U. Live-cell imaging reveals replication of individual replicons in eukaryotic replication factories. Cell 125 7 (2006) 1297-1308
49. Admire A., Shanks L., Danzl N., Wang M., Weier U., Stevens W., Hunt E., and Weinert T. Cycles of chromosome instability are associated with a fragile site and are increased by defects in DNA replication and checkpoint controls in yeast. Genes Dev 20 2 (2006) 159-173
50. Lemoine F.J., Degtyareva N.P., Lobachev K., and Petes T.D. Chromosomal translocations in yeast induced by low levels of DNA polymerase a model for chromosome fragile sites. Cell 120 5 (2005) 587-598
51. Mimitou E.P., and Symington L.S. Sae2, Exo1 and Sgs1 collaborate in DNA double-strand break processing. Nature 455 7214 (2008) 770-774. A soon to be classic study of how a DSB is degraded first by Sae2-directed mechanism, and then Exo1 and Sgs1.
52. Pannunzio N.R., Manthey G.M., and Bailis A.M. RAD59 is required for efficient repair of simultaneous double-strand breaks resulting in translocations in Saccharomyces cerevisiae. DNA Repair (Amst) 7 5 (2008) 788-800. A study of genome instability described in this review. The genetic data suggest to us that genome rearrangements that are spontaneous occur by a different mechanism (fork-mediated?) compared to DSB-mediated events. The author focuses on the role of Rad59 in mediating fusion between short sequences of homology.
53. Putnam C.D., Hayes T.K., and Kolodner R.D. Specific pathways prevent duplication-mediated genome rearrangements. Nature 460 7258 (2009) 984-989. A study of genome rearrangements using paralogous sequences, defining the events and the genetic requirements. The results from this study were compared to the genetic requirements for rearrangements involving singlecopy sequences; they are different.
54. Halazonetis T.D., Gorgoulis V.G., and Bartek J. An oncogene-induced DNA damage model for cancer development. Science 319 5868 (2008) 1352-1355
55. Bartkova J., Rezaei N., Liontos M., Karakaidos P., Kletsas D., Issaeva N., Vassiliou L.V., Kolettas E., Niforou K., Zoumpourlis V.C., et al. Oncogene-induced senescence is part of the tumorigenesis barrier imposed by DNA damage checkpoints. Nature 444 7119 (2006) 633-637
56. Gorgoulis V.G., Vassiliou L.V., Karakaidos P., Zacharatos P., Kotsinas A., Liloglou T., Venere M., Ditullio Jr. R.A., Kastrinakis N.G., and Levy B. Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions. Nature 434 7035 (2005) 907-913