Senataxin associates with replication forks to protect fork integrity across RNA-polymerase-II-transcribed genes

Cell

Volumn 151, Issue 4, 2012, Pages 835-846

  Alzu, Amaya ^a   Bermejo, Rodrigo ^a,d   Begnis, Martina ^a,e   Lucca, Chiara ^a   Piccini, Daniele ^a   Carotenuto, Walter ^a   Saponaro, Marco ^a,e   Brambati, Alessandra ^a,b   Cocito, Andrea ^a   Foiani, Marco ^a,c   Liberi, Giordano ^a,b  

^a FIRC INSTITUTE OF MOLECULAR ONCOLOGY   (Italy)

^b CNR   (Italy)

^c UNIVERSITY OF MILAN   (Italy)

^d Instituto de Biología Funcional y Genómica and Departamento de Microbiología y Genética   (Spain)

^e IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

HELICASE; RNA HELICASE; RNA POLYMERASE II;

AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; ATAXIA; CONTROLLED STUDY; DEGENERATIVE DISEASE; DNA RNA HYBRIDIZATION; DNA STRUCTURE; GENE; GENE FUNCTION; GENE REPLICATION; GENETIC ASSOCIATION; GENETIC DISORDER; GENETIC TRANSCRIPTION; NONHUMAN; PRIORITY JOURNAL; RNA PROCESSING; SENATAXIN GENE;

EID: 84869026790     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2012.09.041     Document Type: Article

References (85)

1. A. Aguilera mRNA processing and genomic instability Nat. Struct. Mol. Biol. 12 2005 737 738 (Pubitemid 43086246)
2. J.T. Arigo, D.E. Eyler, K.L. Carroll, and J.L. Corden Termination of cryptic unstable transcripts is directed by yeast RNA-binding proteins Nrd1 and Nab3 Mol. Cell 23 2006 841 851 (Pubitemid 44344519)
3. A. Azvolinsky, S. Dunaway, J.Z. Torres, J.B. Bessler, and V.A. Zakian The S. cerevisiae Rrm3p DNA helicase moves with the replication fork and affects replication of all yeast chromosomes Genes Dev. 20 2006 3104 3116 (Pubitemid 44790626)
4. A. Azvolinsky, P.G. Giresi, J.D. Lieb, and V.A. Zakian Highly transcribed RNA polymerase II genes are impediments to replication fork progression in Saccharomyces cerevisiae Mol. Cell 34 2009 722 734
5. J. Bartkova, N. Rezaei, M. Liontos, P. Karakaidos, D. Kletsas, N. Issaeva, L.V. Vassiliou, E. Kolettas, K. Niforou, and V.C. Zoumpourlis Oncogene-induced senescence is part of the tumorigenesis barrier imposed by DNA damage checkpoints Nature 444 2006 633 637 (Pubitemid 44864442)
6. R. Bermejo, T. Capra, V. Gonzalez-Huici, D. Fachinetti, A. Cocito, G. Natoli, Y. Katou, H. Mori, K. Kurokawa, K. Shirahige, and M. Foiani Genome-organizing factors Top2 and Hmo1 prevent chromosome fragility at sites of S phase transcription Cell 138 2009 870 884
7. R. Bermejo, T. Capra, R. Jossen, A. Colosio, C. Frattini, W. Carotenuto, A. Cocito, Y. Doksani, H. Klein, and B. Gómez-González The replication checkpoint protects fork stability by releasing transcribed genes from nuclear pores Cell 146 2011 233 246
8. R. Bermejo, M.S. Lai, and M. Foiani Preventing replication stress to maintain genome stability: resolving conflicts between replication and transcription Mol. Cell 45 2012 710 718
9. G. Blobel Gene gating: a hypothesis Proc. Natl. Acad. Sci. USA 82 1985 8527 8529 (Pubitemid 16105094)
10. H. Boubakri, A.L. de Septenville, E. Viguera, and B. Michel The helicases DinG, Rep and UvrD cooperate to promote replication across transcription units in vivo EMBO J. 29 2010 145 157
11. D. Branzei, and M. Foiani Maintaining genome stability at the replication fork Nat. Rev. Mol. Cell Biol. 11 2010 208 219
12. B.J. Brewer, and W.L. Fangman A replication fork barrier at the 3′ end of yeast ribosomal RNA genes Cell 55 1988 637 643
13. Y.Z. Chen, C.L. Bennett, H.M. Huynh, I.P. Blair, I. Puls, J. Irobi, I. Dierick, A. Abel, M.L. Kennerson, and B.A. Rabin DNA/RNA helicase gene mutations in a form of juvenile amyotrophic lateral sclerosis (ALS4) Am. J. Hum. Genet. 74 2004 1128 1135 (Pubitemid 38669312)
14. I. Chiolo, W. Carotenuto, G. Maffioletti, J.H. Petrini, M. Foiani, and G. Liberi Srs2 and Sgs1 DNA helicases associate with Mre11 in different subcomplexes following checkpoint activation and CDK1-mediated Srs2 phosphorylation Mol. Cell. Biol. 25 2005 5738 5751 (Pubitemid 40853606)
15. B.W. Clelland, and M.C. Schultz Genome stability control by checkpoint regulation of tRNA gene transcription Transcription 1 2010 115 125
16. J.A. Cobb, L. Bjergbaek, K. Shimada, C. Frei, and S.M. Gasser DNA polymerase stabilization at stalled replication forks requires Mec1 and the RecQ helicase Sgs1 EMBO J. 22 2003 4325 4336 (Pubitemid 37021759)
17. S.R. Collins, K.M. Miller, N.L. Maas, A. Roguev, J. Fillingham, C.S. Chu, M. Schuldiner, M. Gebbia, J. Recht, and M. Shales Functional dissection of protein complexes involved in yeast chromosome biology using a genetic interaction map Nature 446 2007 806 810 (Pubitemid 46582025)
18. N.K. Conrad, S.M. Wilson, E.J. Steinmetz, M. Patturajan, D.A. Brow, M.S. Swanson, and J.L. Corden A yeast heterogeneous nuclear ribonucleoprotein complex associated with RNA polymerase II Genetics 154 2000 557 571 (Pubitemid 30096580)
19. T.J. Creamer, M.M. Darby, N. Jamonnak, P. Schaughency, H. Hao, S.J. Wheelan, and J.L. Corden Transcriptome-wide binding sites for components of the Saccharomyces cerevisiae non-poly(A) termination pathway: Nrd1, Nab3, and Sen1 PLoS Genet. 7 2011 e1002329
20. D.J. DeMarini, M. Winey, D. Ursic, F. Webb, and M.R. Culbertson SEN1, a positive effector of tRNA-splicing endonuclease in Saccharomyces cerevisiae Mol. Cell. Biol. 12 1992 2154 2164
21. A.M. Deshpande, and C.S. Newlon DNA replication fork pause sites dependent on transcription Science 272 1996 1030 1033 (Pubitemid 26259324)
22. R. Di Micco, M. Fumagalli, A. Cicalese, S. Piccinin, P. Gasparini, C. Luise, C. Schurra, M. Garre', P.G. Nuciforo, and A. Bensimon Oncogene-induced senescence is a DNA damage response triggered by DNA hyper-replication Nature 444 2006 638 642 (Pubitemid 44864443)
23. M.S. Domínguez-Sánchez, S. Barroso, B. Gómez- González, R. Luna, and A. Aguilera Genome instability and transcription elongation impairment in human cells depleted of THO/TREX PLoS Genet. 7 2011 e1002386
24. M. Drolet Growth inhibition mediated by excess negative supercoiling: the interplay between transcription elongation, R-loop formation and DNA topology Mol. Microbiol. 59 2006 723 730
25. W. Gan, Z. Guan, J. Liu, T. Gui, K. Shen, J.L. Manley, and X. Li R-loop-mediated genomic instability is caused by impairment of replication fork progression Genes Dev. 25 2011 2041 2056
26. S. Gangloff, C. Soustelle, and F. Fabre Homologous recombination is responsible for cell death in the absence of the Sgs1 and Srs2 helicases Nat. Genet. 25 2000 192 194 (Pubitemid 30394991)
27. B. Gómez-González, M. García-Rubio, R. Bermejo, H. Gaillard, K. Shirahige, A. Marín, M. Foiani, and A. Aguilera Genome-wide function of THO/TREX in active genes prevents R-loop-dependent replication obstacles EMBO J. 30 2011 3106 3119
28. P. Gottipati, T.N. Cassel, L. Savolainen, and T. Helleday Transcription-associated recombination is dependent on replication in Mammalian cells Mol. Cell. Biol. 28 2008 154 164
29. M. Hampsey, B.N. Singh, A. Ansari, J.P. Lainé, and S. Krishnamurthy Control of eukaryotic gene expression: gene loops and transcriptional memory Adv. Enzyme Regul. 51 2011 118 125
30. A. Helmrich, M. Ballarino, and L. Tora Collisions between replication and transcription complexes cause common fragile site instability at the longest human genes Mol. Cell 44 2011 966 977
31. Z. Hu, A. Zhang, G. Storz, S. Gottesman, and S.H. Leppla An antibody-based microarray assay for small RNA detection Nucleic Acids Res. 34 2006 e52
32. P. Huertas, and A. Aguilera Cotranscriptionally formed DNA:RNA hybrids mediate transcription elongation impairment and transcription-associated recombination Mol. Cell 12 2003 711 721 (Pubitemid 37222491)
33. A.S. Ivessa, B.A. Lenzmeier, J.B. Bessler, L.K. Goudsouzian, S.L. Schnakenberg, and V.A. Zakian The Saccharomyces cerevisiae helicase Rrm3p facilitates replication past nonhistone protein-DNA complexes Mol. Cell 12 2003 1525 1536 (Pubitemid 38037020)
34. N. Jamonnak, T.J. Creamer, M.M. Darby, P. Schaughency, S.J. Wheelan, and J.L. Corden Yeast Nrd1, Nab3, and Sen1 transcriptome-wide binding maps suggest multiple roles in post-transcriptional RNA processing RNA 17 2011 2011 2025
35. Y. Katou, Y. Kanoh, M. Bando, H. Noguchi, H. Tanaka, T. Ashikari, K. Sugimoto, and K. Shirahige S-phase checkpoint proteins Tof1 and Mrc1 form a stable replication-pausing complex Nature 424 2003 1078 1083 (Pubitemid 37064311)
36. A. Kerrest, R.P. Anand, R. Sundararajan, R. Bermejo, G. Liberi, B. Dujon, C.H. Freudenreich, and G.F. Richard SRS2 and SGS1 prevent chromosomal breaks and stabilize triplet repeats by restraining recombination Nat. Struct. Mol. Biol. 16 2009 159 167
37. H.D. Kim, J. Choe, and Y.S. Seo The sen1(+) gene of Schizosaccharomyces pombe, a homologue of budding yeast SEN1, encodes an RNA and DNA helicase Biochemistry 38 1999 14697 14710
38. T. Kogoma Stable DNA replication: interplay between DNA replication, homologous recombination, and transcription Microbiol. Mol. Biol. Rev. 61 1997 212 238 (Pubitemid 27283801)
39. A. Köhler, and E. Hurt Exporting RNA from the nucleus to the cytoplasm Nat. Rev. Mol. Cell Biol. 8 2007 761 773 (Pubitemid 47462133)
40. D.A. Koster, A. Crut, S. Shuman, M.A. Bjornsti, and N.H. Dekker Cellular strategies for regulating DNA supercoiling: a single-molecule perspective Cell 142 2010 519 530
41. A. Lengronne, J. McIntyre, Y. Katou, Y. Kanoh, K.P. Hopfner, K. Shirahige, and F. Uhlmann Establishment of sister chromatid cohesion at the S. cerevisiae replication fork Mol. Cell 23 2006 787 799 (Pubitemid 44344523)
42. X. Li, and J.L. Manley Inactivation of the SR protein splicing factor ASF/SF2 results in genomic instability Cell 122 2005 365 378 (Pubitemid 41127139)
43. G. Liberi, G. Maffioletti, C. Lucca, I. Chiolo, A. Baryshnikova, C. Cotta-Ramusino, M. Lopes, A. Pellicioli, J.E. Haber, and M. Foiani Rad51-dependent DNA structures accumulate at damaged replication forks in sgs1 mutants defective in the yeast ortholog of BLM RecQ helicase Genes Dev. 19 2005 339 350 (Pubitemid 40189297)
44. G. Liberi, C. Cotta-Ramusino, M. Lopes, J. Sogo, C. Conti, A. Bensimon, and M. Foiani Methods to study replication fork collapse in budding yeast Methods Enzymol. 409 2006 442 462
45. L.F. Liu, and J.C. Wang Supercoiling of the DNA template during transcription Proc. Natl. Acad. Sci. USA 84 1987 7024 7027
46. E.V. Mirkin, and S.M. Mirkin Replication fork stalling at natural impediments Microbiol. Mol. Biol. Rev. 71 2007 13 35 (Pubitemid 46456682)
47. H.E. Mischo, B. Gómez-González, P. Grzechnik, A.G. Rondón, W. Wei, L. Steinmetz, A. Aguilera, and N.J. Proudfoot Yeast Sen1 helicase protects the genome from transcription-associated instability Mol. Cell 41 2011 21 32
48. M.C. Moreira, S. Klur, M. Watanabe, A.H. Németh, I. Le Ber, J.C. Moniz, C. Tranchant, P. Aubourg, M. Tazir, and L. Schöls Senataxin, the ortholog of a yeast RNA helicase, is mutant in ataxia-ocular apraxia 2 Nat. Genet. 36 2004 225 227 (Pubitemid 38282744)
49. M. Nonet, C. Scafe, J. Sexton, and R. Young Eucaryotic RNA polymerase conditional mutant that rapidly ceases mRNA synthesis Mol. Cell. Biol. 7 1987 1602 1611 (Pubitemid 17059154)
50. E. Nudler RNA polymerase backtracking in gene regulation and genome instability Cell 149 2012 1438 1445
51. L. Olavarrieta, M.L. Martínez-Robles, P. Hernández, D.B. Krimer, and J.B. Schvartzman Knotting dynamics during DNA replication Mol. Microbiol. 46 2002 699 707 (Pubitemid 35365605)
52. B.D. Page, and M. Snyder CIK1: a developmentally regulated spindle pole body-associated protein important for microtubule functions in Saccharomyces cerevisiae Genes Dev. 6 1992 1414 1429
53. V. Pagès, and R.P. Fuchs Uncoupling of leading- and lagging-strand DNA replication during lesion bypass in vivo Science 300 2003 1300 1303 (Pubitemid 36618243)
54. E. Papouli, S. Chen, A.A. Davies, D. Huttner, L. Krejci, P. Sung, and H.D. Ulrich Crosstalk between SUMO and ubiquitin on PCNA is mediated by recruitment of the helicase Srs2p Mol. Cell 19 2005 123 133 (Pubitemid 40884663)
55. R.D. Paulsen, D.V. Soni, R. Wollman, A.T. Hahn, M.C. Yee, A. Guan, J.A. Hesley, S.C. Miller, E.F. Cromwell, and D.E. Solow-Cordero A genome-wide siRNA screen reveals diverse cellular processes and pathways that mediate genome stability Mol. Cell 35 2009 228 239
56. R.T. Pomerantz, and M. O'Donnell The replisome uses mRNA as a primer after colliding with RNA polymerase Nature 456 2008 762 766
57. L. Postow, C. Ullsperger, R.W. Keller, C. Bustamante, A.V. Vologodskii, and N.R. Cozzarelli Positive torsional strain causes the formation of a four-way junction at replication forks J. Biol. Chem. 276 2001 2790 2796
58. T.P. Rasmussen, and M.R. Culbertson The putative nucleic acid helicase Sen1p is required for formation and stability of termini and for maximal rates of synthesis and levels of accumulation of small nucleolar RNAs in Saccharomyces cerevisiae Mol. Cell. Biol. 18 1998 6885 6896 (Pubitemid 28533010)
59. E.P. Rocha The organization of the bacterial genome Annu. Rev. Genet. 42 2008 211 233
60. A.G. Rondón, H.E. Mischo, J. Kawauchi, and N.J. Proudfoot Fail-safe transcriptional termination for protein-coding genes in S. cerevisiae Mol. Cell 36 2009 88 98
61. C.J. Rudolph, P. Dhillon, T. Moore, and R.G. Lloyd Avoiding and resolving conflicts between DNA replication and transcription DNA Repair (Amst.) 6 2007 981 993 (Pubitemid 46880478)
62. N. Sabouri, K.R. McDonald, C.J. Webb, I.M. Cristea, and V.A. Zakian DNA replication through hard-to-replicate sites, including both highly transcribed RNA Pol II and Pol III genes, requires the S. pombe Pfh1 helicase Genes Dev. 26 2012 581 593
63. K. Shirahige, T. Iwasaki, M.B. Rashid, N. Ogasawara, and H. Yoshikawa Location and characterization of autonomously replicating sequences from chromosome VI of Saccharomyces cerevisiae Mol. Cell. Biol. 13 1993 5043 5056 (Pubitemid 23220408)
64. K. Skourti-Stathaki, N.J. Proudfoot, and N. Gromak Human senataxin resolves RNA/DNA hybrids formed at transcriptional pause sites to promote Xrn2-dependent termination Mol. Cell 42 2011 794 805
65. F. Spencer, S.L. Gerring, C. Connelly, and P. Hieter Mitotic chromosome transmission fidelity mutants in Saccharomyces cerevisiae Genetics 124 1990 237 249 (Pubitemid 20066094)
66. R. Steinacher, F. Osman, J.Z. Dalgaard, A. Lorenz, and M.C. Whitby The DNA helicase Pfh1 promotes fork merging at replication termination sites to ensure genome stability Genes Dev. 26 2012 594 602
67. E.J. Steinmetz, N.K. Conrad, D.A. Brow, and J.L. Corden RNA-binding protein Nrd1 directs poly(A)-independent 3′-end formation of RNA polymerase II transcripts Nature 413 2001 327 331 (Pubitemid 32905855)
68. P.C. Stirling, Y.A. Chan, S.W. Minaker, M.J. Aristizabal, I. Barrett, P. Sipahimalani, M.S. Kobor, and P. Hieter R-loop-mediated genome instability in mRNA cleavage and polyadenylation mutants Genes Dev. 26 2012 163 175
69. A. Suraweera, O.J. Becherel, P. Chen, N. Rundle, R. Woods, J. Nakamura, M. Gatei, C. Criscuolo, A. Filla, and L. Chessa Senataxin, defective in ataxia oculomotor apraxia type 2, is involved in the defense against oxidative DNA damage J. Cell Biol. 177 2007 969 979 (Pubitemid 46955702)
70. A. Suraweera, Y. Lim, R. Woods, G.W. Birrell, T. Nasim, O.J. Becherel, and M.F. Lavin Functional role for senataxin, defective in ataxia oculomotor apraxia type 2, in transcriptional regulation Hum. Mol. Genet. 18 2009 3384 3396
71. M. Thiebaut, E. Kisseleva-Romanova, M. Rougemaille, J. Boulay, and D. Libri Transcription termination and nuclear degradation of cryptic unstable transcripts: a role for the nrd1-nab3 pathway in genome surveillance Mol. Cell 23 2006 853 864 (Pubitemid 44344521)
72. S. Tuduri, L. Crabbé, C. Conti, H. Tourrière, H. Holtgreve-Grez, A. Jauch, V. Pantesco, J. De Vos, A. Thomas, and C. Theillet Topoisomerase I suppresses genomic instability by preventing interference between replication and transcription Nat. Cell Biol. 11 2009 1315 1324
73. D. Ursic, K.L. Himmel, K.A. Gurley, F. Webb, and M.R. Culbertson The yeast SEN1 gene is required for the processing of diverse RNA classes Nucleic Acids Res. 25 1997 4778 4785 (Pubitemid 27517212)
74. L. Vasiljeva, and S. Buratowski Nrd1 interacts with the nuclear exosome for 3′ processing of RNA polymerase II transcripts Mol. Cell 21 2006 239 248 (Pubitemid 43099939)
75. F.J. Vizeacoumar, N. van Dyk, F. S Vizeacoumar, V. Cheung, J. Li, Y. Sydorskyy, N. Case, Z. Li, A. Datti, and C. Nislow Integrating high-throughput genetic interaction mapping and high-content screening to explore yeast spindle morphogenesis J. Cell Biol. 188 2010 69 81
76. L. Wahba, J.D. Amon, D. Koshland, and M. Vuica-Ross RNase H and multiple RNA biogenesis factors cooperate to prevent RNA:DNA hybrids from generating genome instability Mol. Cell 44 2011 978 988
77. J.C. Wang Cellular roles of DNA topoisomerases: a molecular perspective Nat. Rev. Mol. Cell Biol. 3 2002 430 440 (Pubitemid 34685700)
78. T.A. Weinert, and L.H. Hartwell The RAD9 gene controls the cell cycle response to DNA damage in Saccharomyces cerevisiae Science 241 1988 317 322
79. W. Wlotzka, G. Kudla, S. Granneman, and D. Tollervey The nuclear RNA polymerase II surveillance system targets polymerase III transcripts EMBO J. 30 2011 1790 1803
80. H. Xu, C. Boone, and H.L. Klein Mrc1 is required for sister chromatid cohesion to aid in recombination repair of spontaneous damage Mol. Cell. Biol. 24 2004 7082 7090 (Pubitemid 39014435)
81. Y.B. Yurov, S.G. Vorsanova, and I.Y. Iourov The DNA replication stress hypothesis of Alzheimer's disease ScientificWorldJournal 11 2011 2602 2612
82. Lucca, C., Vanoli, F., Cotta-Ramusino, C., Pellicioli, A., Liberi, G., Haber, J., and Foiani, M. (2004). Checkpoint-mediated control of replisome-fork association and signalling in response to replication pausing. Oncogene 23, 1206-1213. (Pubitemid 38297174)
83. Storici, F., and Resnick, M.A. (2006). The delitto perfetto approach to in vivo site-directed mutagenesis and chromosome rearrangements with synthetic oligonucleotides in yeast. Methods Enzymol. 409, 329-345.
84. Visintin, C., Tomson, B.N., Rahal, R., Paulson, J., Cohen, M., Taunton, J., Amon, A., and Visintin, R. (2008). APC/C-Cdh1-mediated degradation of the Polo kinase Cdc5 promotes the return of Cdc14 into the nucleolus. Genes Dev. 22, 79-90.
85. Wach, A., Brachat, A., Pöhlmann, R., and Philippsen, P. (1994). New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. Yeast 10, 1793-1808.