Reversible Top1 cleavage complexes are stabilized strand-specifically at the ribosomal replication fork barrier and contribute to ribosomal DNA stability

Nucleic Acids Research

Volumn 42, Issue 8, 2014, Pages 4985-4995

  Krawczyk, Claudia ^a   Dion, Vincent ^b,c   Schär, Primo ^a   Fritsch, Olivier ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

^b FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

^c UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; DNA TOPOISOMERASE; FOB1 PROTEIN; REVERSIBLE TOP1 CLEAVAGE COMPLEX; RIBOSOME DNA; TOF2 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BIOACCUMULATION; BUDDING YEAST; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME MECHANISM; ENZYME REGULATION; ENZYME SPECIFICITY; ENZYME STABILITY; MOLECULAR STABILITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN TARGETING; RIBOSOMAL REPLICATION FORK BARRIER; RNA STRUCTURE; YEAST;

DNA BREAKS, DOUBLE-STRANDED; DNA CLEAVAGE; DNA REPLICATION; DNA TOPOISOMERASES, TYPE I; DNA, RIBOSOMAL; DNA-BINDING PROTEINS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; PROTEIN STABILITY; RECQ HELICASES; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84899876564     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku148     Document Type: Article

References (54)

1. Hill, T.M., Tecklenburg, M.L., Pelletier, A.J. and Kuempel, P.L. (1989) tus, the trans-acting gene required for termination of DNA replication in Escherichia coli, encodes a DNA-binding protein. Proc. Natl Acad. Sci. USA., 86, 1593-1597.
2. Mirkin, E.V. and Mirkin, S.M. (2007) Replication fork stalling at natural impediments. Microbiol. Mol. Biol. Rev., 71, 13-35.
3. Calzada, A., Hodgson, B., Kanemaki, M., Bueno, A. and Labib, K. (2005) Molecular anatomy and regulation of a stable replisome at a paused eukaryotic DNA replication fork. Gene Dev., 19, 1905-1919.
4. Kobayashi, T. and Horiuchi, T. (1996) A yeast gene product, Fob1 protein, required for both replication fork blocking and recombinational hotspot activities. Genes Cells., 1, 465-474.
5. Sogo, J.M., Lopes, M. and Foiani, M. (2002) Fork reversal and ssDNA accumulation at stalled replication forks owing to checkpoint defects. Science., 297, 599-602.
6. Brewer, B.J., Lockshon, D. and Fangman, W.L. (1992) The arrest of replication forks in the rDNA of yeast occurs independently of transcription. Cell., 71, 267-276.
7. Kobayashi, T. (2003) The replication fork barrier site forms a unique structure with Fob1p and inhibits the replication fork. Mol. Cell Biol., 23, 9178-9188.
8. Brewer, B.J. and Fangman, W.L. (1988) A replication fork barrier at the 3′ end of yeast ribosomal RNA genes. Cell., 55, 637-643.
9. Kobayashi, T., Horiuchi, T., Tongaonkar, P., Vu, L. and Nomura, M. (2004) SIR2 regulates recombination between different rDNA repeats, but not recombination within individual rRNA genes in yeast. Cell., 117, 441-453.
10. Kobayashi, T., Heck, D.J., Nomura, M. and Horiuchi, T. (1998) Expansion and contraction of ribosomal DNA repeats in Saccharomyces cerevisiae: requirement of replication fork blocking (Fob1) protein and the role of RNA polymerase I. Gene Dev., 12, 3821-3830.
11. Weitao, T., Budd, M., Hoopes, L. and Campbell, J. (2003) Dna2 helicase/nuclease causes replicative fork stalling and double-strand breaks in the ribosomal DNA of Saccharomyces cerevisiae. J. Biol. Chem., 278, 22513-22522.
12. Weitao, T., Budd, M. and Campbell, J.L. (2003) Evidence that yeast SGS1, DNA2, SRS2, and FOB1 interact to maintain rDNA stability. Mut. Res., 532, 157-172.
13. Burkhalter, M.D. and Sogo, J.M. (2004) rDNA enhancer affects replication initiation and mitotic recombination: Fob1 mediates nucleolytic processing independently of replication. Mol. Cell., 15, 409-421.
14. Fritsch, O., Burkhalter, M.D., Kais, S., Sogo, J.M. and Schar, P. (2010) DNA ligase 4 stabilizes the ribosomal DNA array upon fork collapse at the replication fork barrier. DNA Repair., 9, 879-888.
15. Mekhail, K., Seebacher, J., Gygi, S.P. and Moazed, D. (2008) Role for perinuclear chromosome tethering in maintenance of genome stability. Nature., 456, 667-670.
16. Chan, J.N.Y., Poon, B.P.K., Salvi, J., Olsen, J.B., Emili, A. and Mekhail, K. (2011) Perinuclear cohibin complexes maintain replicative life span via roles at distinct silent chromatin domains. Dev. Cell., 20, 867-879.
17. Huang, J., Brito, I.L., Villen, J., Gygi, S.P., Amon, A. and Moazed, D. (2006) Inhibition of homologous recombination by a cohesin-associated clamp complex recruited to the rDNA recombination enhancer. Gene Dev., 20, 2887-2901.
18. French, S.L., Sikes, M.L., Hontz, R.D., Osheim, Y.N., Lambert, T.E., Hage, El, A., Smith, M.M., Tollervey, D., Smith, J.S. and Beyer, A.L. (2011) Distinguishing the roles of Topoisomerases I and II in relief of transcription-induced torsional stress in yeast rRNA genes. Mol. Cell Biol., 31, 482-494.
19. Vogelauer, M. and Camilloni, G. (1999) Site-specific in vivo cleavages by DNA topoisomerase I in the regulatory regions of the 35S rRNA in Saccharomyces cerevisiae are transcription independent. J. Mol. Biol., 293, 19-28.
20. Brill, S.J., DiNardo, S., Voelkel-Meiman, K. and Sternglanz, R. (1987) Need for DNA topoisomerase activity as a swivel for DNA replication for transcription of ribosomal RNA. Nature., 326, 414-416.
21. Schultz, M.C., Brill, S.J., Ju, Q., Sternglanz, R. and Reeder, R.H. (1992) Topoisomerases and yeast rRNA transcription: negative supercoiling stimulates initiation and topoisomerase activity is required for elongation. Gene Dev., 6, 1332-1341.
22. Bryk, M., Banerjee, M., Murphy, M., Knudsen, K.E., Garfinkel, D.J. and Curcio, M.J. (1997) Transcriptional silencing of Ty1 elements in the RDN1 locus of yeast. Gene Dev., 11, 255-269.
23. Smith, J.S. and Boeke, J.D. (1997) An unusual form of transcriptional silencing in yeast ribosomal DNA. Gene Dev., 11, 241-254.
24. Smith, J.S., Caputo, E. and Boeke, J.D. (1999) A genetic screen for ribosomal DNA silencing defects identifies multiple DNA replication and chromatin-modulating factors. Mol. Cell Biol., 19, 3184-3197.
25. Christman, M.F., Dietrich, F.S. and Fink, G.R. (1988) Mitotic recombination in the rDNA of S. cerevisiae is suppressed by the combined action of DNA topoisomerases I and II. Cell., 55, 413-425.
26. Kim, R.A. and Wang, J.C. (1989) A subthreshold level of DNA topoisomerases leads to the excision of yeast rDNA as extrachromosomal rings. Cell., 57, 975-985.
27. Zhu, J. and Schiestl, R.H. (2004) Human topoisomerase I mediates illegitimate recombination leading to DNA insertion into the ribosomal DNA locus in Saccharomyces cerevisiae. Mol. Genet. Genom., 271, 347-358.
28. Koster, D.A., Croquette, V., Dekker, C., Shuman, S. and Dekker, N.H. (2005) Friction and torque govern the relaxation of DNA supercoils by eukaryotic topoisomerase IB. Nature., 434, 671-674.
29. Champoux, J.J. (2011) Human DNA Topoisomerase I: Structure, Enzymology and Biology. DNA Topoisomerases and Cancer. Springer New York, New York, NY, pp. 53-69.
30. Rohner, S., Gasser, S.M. and Meister, P. (2008) Modules for cloning-free chromatin tagging in Saccharomyces cerevisae. Yeast., 25, 235-239.
31. van Attikum, H., Fritsch, O., Hohn, B. and Gasser, S.M. (2004) Recruitment of the INO80 complex by H2A phosphorylation links ATP-dependent chromatin remodeling with DNA doublestrand break repair. Cell., 119, 777-788.
32. Martin, S.G., Laroche, T., Suka, N., Grunstein, M. and Gasser, S.M. (1999) Relocalization of telomeric Ku and SIR proteins in response to DNA strand breaks in yeast. Cell., 97, 621-633.
33. Takahashi, T., Burguiere-Slezak, G., Van der Kemp, P.A. and Boiteux, S. (2011) Topoisomerase 1 provokes the formation of short deletions in repeated sequences upon high transcription in Saccharomyces cerevisiae. Proc. Natl Acad. Sci. USA., 108, 692-697.
34. Dion, V., Kalck, V., Horigome, C., Towbin, B.D. and Gasser, S.M. (2012) Increased mobility of double-strand breaks requires Mec1, Rad9 and the homologous recombination machinery. Nat. Cell Biol., 14, 502-509.
35. Meister, P., Gehlen, L.R., Varela, E., Kalck, V. and Gasser, S.M. (2010) Visualizing yeast chromosomes and nuclear architecture. Meth. Enzymol., 470, 535-567.
36. Neumann, F.R., Dion, V., Gehlen, L.R., Tsai-Pflugfelder, M., Schmid, R., Taddei, A. and Gasser, S.M. (2012) Targeted INO80 enhances subnuclear chromatin movement and ectopic homologous recombination. Gene Dev., 26, 369-383.
37. Ponti, A., Schwarb, P., Gulati, A. and Baker, V. (2007) Huygens remote manager: a web interface for high-volume batch deconvolution. Imag. Microscop., 9, 57-58.
38. Huang, J. and Moazed, D. (2003) Association of the RENT complex with nontranscribed and coding regions of rDNA and a regional requirement for the replication fork block protein Fob1 in rDNA silencing. Gene Dev., 17, 2162-2176.
39. Nieduszynski, C.A., Hiraga, S.-I., Ak, P., Benham, C.J. and Donaldson, A.D. (2007) OriDB: a DNA replication origin database. Nucleic Acids Res., 35, D40-D46.
40. Torres-Rosell, J., Sunjevaric, I., De Piccoli, G., Sacher, M., Eckert-Boulet, N., Reid, R., Jentsch, S., Rothstein, R., Aragon, L. and Lisby, M. (2007) The Smc5-Smc6 complex and SUMO modification of Rad52 regulates recombinational repair at the ribosomal gene locus. Nat. Cell Biol., 9, 923-931.
41. Di Felice, F., Cioci, F. and Camilloni, G. (2005) FOB1 affects DNA topoisomerase I in vivo cleavages in the enhancer region of the Saccharomyces cerevisiae ribosomal DNA locus. Nucleic Acids Res., 33, 6327-6337.
42. Vance, J.R. and Wilson, T.E. (2002) Yeast Tdp1 and Rad1-Rad10 function as redundant pathways for repairing Top1 replicative damage. Proc. Natl Acad. Sci. USA., 99, 13669-13674.
43. Liu, C., Pouliot, J.J. and Nash, H.A. (2002) Repair of topoisomerase I covalent complexes in the absence of the tyrosyl-DNA phosphodiesterase Tdp1. Proc. Natl Acad. Sci. USA., 99, 14970-14975.
44. Park, H. and Sternglanz, R. (1999) Identification and characterization of the genes for two topoisomerase I-interacting proteins from Saccharomyces cerevisiae. Yeast., 15, 35-41.
45. Christman, M.F., Dietrich, F.S., Levin, N.A., Sadoff, B.U. and Fink, G.R. (1993) The rRNA-encoding DNA array has an altered structure in topoisomerase I mutants of Saccharomyces cerevisiae. Proc. Natl Acad. Sci. USA., 90, 7637-7641.
46. Ii, M., Ii, T. and Brill, S.J. (2007) Mus81 functions in the quality control of replication forks at the rDNA and is involved in the maintenance of rDNA repeat number in Saccharomyces cerevisiae. Mut. Res., 625, 1-19.
47. Versini, G., Comet, I., Wu, M., Hoopes, L., Schwob, E. and Pasero, P. (2003) The yeast Sgs1 helicase is differentially required for genomic and ribosomal DNA replication. EMBO J., 22, 1939-1949.
48. Defossez, P.A., Prusty, R., Kaeberlein, M., Lin, S.J., Ferrigno, P., Silver, P.A., Keil, R.L. and Guarente, L. (1999) Elimination of replication block protein Fob1 extends the life span of yeast mother cells. Mol. Cell., 3, 447-455.
49. Johzuka, K. and Horiuchi, T. (2002) Replication fork block protein, Fob1, acts as an rDNA region specific recombinator in S. cerevisiae. Genes Cells., 7, 99-113.
50. Shuman, S. and Prescott, J. (1990) Specific DNA cleavage and binding by vaccinia virus DNA topoisomerase I. J. Biol. Chem., 265, 17826-17836.
51. Edwards, K.A., Halligan, B.D., Davis, J.L., Nivera, N.L. and Liu, L.F. (1982) Recognition sites of eukaryotic DNA topoisomerase I: DNA nucleotide sequencing analysis of topo I cleavage sites on SV40 DNA. Nucleic Acids Res., 10, 2565-2576.
52. Tsang, E. and Carr, A.M. (2008) Replication fork arrest, recombination and the maintenance of ribosomal DNA stability. DNA Repair., 7, 1613-1623.
53. Ahn, J., Osman, F. and Whitby, M. (2005) Replication fork blockage by RTS1 at an ectopic site promotes recombination in fission yeast. EMBO J., 24, 2011-2023.
54. Caserta, M., Amadei, A., Di Mauro, E. and Camilloni, G. (1989) In vitro preferential topoisomerization of bent DNA. Nucleic Acids Res., 17, 8463-8474.