RNA polymerase II contributes to preventing transcription-mediated replication fork stalls

EMBO Journal

Volumn 34, Issue 2, 2015, Pages 236-250

  Felipe Abrio, Irene ^a   Lafuente Barquero, Juan ^a   García Rubio, María L ^a   Aguilera, Andrés ^a  

^a UNIVERSITY OF SEVILLE   (Spain)

Author keywords

DNA damage response; DNA replication; Double strand break repair; Genome instability; RNAPII

Indexed keywords

RNA POLYMERASE II; BIOLOGICAL MARKER; RPB1 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN;

ALLELISM; ARTICLE; CHROMATIN; DOUBLE STRANDED DNA BREAK; GENE INTERACTION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RNA REPLICATION; RNA TRANSCRIPTION; TRANSCRIPTION ELONGATION; CHROMATIN IMMUNOPRECIPITATION; DNA MICROARRAY; DNA REPAIR; DNA REPLICATION; ENZYMOLOGY; GENE EXPRESSION PROFILING; GENETIC TRANSCRIPTION; GENETICS; GENOMIC INSTABILITY; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MUTATION; SACCHAROMYCES CEREVISIAE;

BIOLOGICAL MARKERS; CHROMATIN IMMUNOPRECIPITATION; DNA REPAIR; DNA REPLICATION; GENE EXPRESSION PROFILING; GENOMIC INSTABILITY; MUTATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RNA POLYMERASE II; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSCRIPTION, GENETIC;

EID: 84921314292     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.15252/embj.201488544     Document Type: Article

References (81)

1. Aguilera A, Gómez-González B (2008) Genome instability: a mechanistic view of its causes and consequences. Nat Rev Genet 9: 204-217
2. Aguilera A, García-Muse T (2012) R loops: from transcription byproducts to threats to genome stability. Mol Cell 46: 115-124
3. Aguilera A, García-Muse T (2013) Causes of genome instability. Annu Rev Genet 47: 1-32
4. Alvaro D, Lisby M, Rothstein R (2007) Genome-wide analysis of Rad52 foci reveals diverse mechanisms impacting recombination. PLoS Genet 3: e228
5. Atkinson J, Gupta MK, Rudolph CJ, Bell H, Lloyd RG, McGlynn P (2010) Localization of an accessory helicase at the replisome is critical in sustaining efficient genome duplication. Nucleic Acids Res 39: 949-957
6. Azvolinsky A, Giresi PG, Lieb JD, Zakian VA (2009) Highly transcribed RNA polymerase II genes are impediments to replication fork progression in Saccharomyces cerevisiae. Mol Cell 34: 722-734
7. Baharoglu Z, Lestini R, Duigou S, Michel B (2010) RNA polymerase mutations that facilitate replication progression in the rep uvrD recF mutant lacking two accessory replicative helicases. Mol Microbiol 77: 324-336
8. Belotserkovskii BP, Neil AJ, Saleh SS, Shin JH, Mirkin SM, Hanawalt PC (2013) Transcription blockage by homopurine DNA sequences: role of sequence composition and single-strand breaks. Nucleic Acids Res 41: 1817-1828
9. Bermejo R, Capra T, Gonzalez-Huici V, Fachinetti D, Cocito A, Natoli G, Katou Y, Mori H, Kurokawa K, Shirahige K, Foiani M (2009) Genome-organizing factors Top2 and Hmo1 prevent chromosome fragility at sites of S phase transcription. Cell 138: 870-884
10. Bermejo R, Kumar A, Foiani M (2012) Preserving the genome by regulating chromatin association with the nuclear envelope. Trends Cell Biol 22: 465-473
11. Bianco JN, Poli J, Saksouk J, Bacal J, Silva MJ, Yoshida K, Lin YL, Tourriere H, Lengronne A, Pasero P (2012) Analysis of DNA replication profiles in budding yeast and mammalian cells using DNA combing. Methods 57: 149-157
12. Boubakri H, de Septenville AL, Viguera E, Michel B (2010) The helicases DinG, Rep and UvrD cooperate to promote replication across transcription units in vivo. EMBO J 29: 145-157
13. Braberg H, Jin H, Moehle EA, Chan YA, Wang S, Shales M, Benschop JJ, Morris JH, Qiu C, Hu F, Tang LK, Fraser JS, Holstege FC, Hieter P, Guthrie C, Kaplan CD, Krogan NJ (2013) From structure to systems: high-resolution, quantitative genetic analysis of RNA polymerase II. Cell 154: 775-788
14. Branzei D, Foiani M (2010) Maintaining genome stability at the replication fork. Nat Rev Genet 11: 208-219
15. Castellano-Pozo M, García-Muse T, Aguilera A (2012) R-loops cause replication impairment and genome instability during meiosis. EMBO Rep 13: 923-929
16. Chavez S, Aguilera A (1997) The yeast HPR1 gene has a functional role in transcriptional elongation that uncovers a novel source of genome instability. Genes Dev 11: 3459-3470
17. Chen X, Ruggiero C, Li S (2007) Yeast Rpb9 plays an important role in ubiquitylation and degradation of Rpb1 in response to UV-induced DNA damage. Mol Cell Biol 27: 4617-4625
18. Desany BA, Alcasabas AA, Bachant JB, Elledge SJ (1998) Recovery from DNA replicational stress is the essential function of the S-phase checkpoint pathway. Genes Dev 12: 2956-2970
19. Domínguez-Sanchez MS, Barroso S, Gómez-González B, Luna R, Aguilera A (2011) Genome instability and transcription elongation impairment in human cells depleted of THO/TREX. PLoS Genet 7: e1002386
20. Domkin V, Thelander L, Chabes A (2002) Yeast DNA damage-inducible Rnr3 has a very low catalytic activity strongly stimulated after the formation of a cross-talking Rnr1/Rnr3 complex. J Biol Chem 277: 18574-18578
21. Drolet M, Phoenix P, Menzel R, Masse E, Liu LF, Crouch RJ (1995) Overexpression of RNase H partially complements the growth defect of an Escherichia coli delta topA mutant: R-loop formation is a major problem in the absence of DNA topoisomerase I. Proc Natl Acad Sci USA 92: 3526-3530
22. Duch A, Felipe-Abrio I, Barroso S, Yaakov G, Garcia-Rubio M, Aguilera A, de Nadal E, Posas F (2013) Coordinated control of replication and transcription by a SAPK protects genomic integrity. Nature 493: 116-119
23. Dutta D, Shatalin K, Epshtein V, Gottesman ME, Nudler E (2011) Linking RNA polymerase backtracking to genome instability in E. coli. Cell 146: 533-543
24. Gaillard H, Tous C, Botet J, González-Aguilera C, Quintero MJ, Viladevall L, García-Rubio ML, Rodríguez-Gil A, Marin A, Arino J, Revuelta JL, Chavez S, Aguilera A (2009) Genome-wide analysis of factors affecting transcription elongation and DNA repair: a new role for PAF and Ccr4-not in transcription-coupled repair. PLoS Genet 5: e1000364
25. Gaillard H, Aguilera A (2013a) Transcription coupled repair at the interface between transcription elongation and mRNP biogenesis. Biochim Biophys Acta 1829: 141-150
26. Gaillard H, Herrera-Moyano E, Aguilera A (2013b) Transcription-associated genome instability. Chem Rev 113: 8638-8661
27. Gan W, Guan Z, Liu J, Gui T, Shen K, Manley JL, Li X (2011) R-loop-mediated genomic instability is caused by impairment of replication fork progression. Genes Dev 25: 2041-2056
28. Gómez-González B, Felipe-Abrio I, Aguilera A (2009) The S-phase checkpoint is required to respond to R-loops accumulated in THO mutants. Mol Cell Biol 29: 5203-5213
29. Gómez-González B, García-Rubio M, Bermejo R, Gaillard H, Shirahige K, Marin A, Foiani M, Aguilera A (2011a) Genome-wide function of THO/TREX in active genes prevents R-loop-dependent replication obstacles. EMBO J 30: 3106-3119
30. Gómez-González B, Ruiz JF, Aguilera A (2011b) Genetic and molecular analysis of mitotic recombination in Saccharomyces cerevisiae. Methods Mol Biol 745: 151-172
31. Gonzalez-Aguilera C, Tous C, Babiano R, de la Cruz J, Luna R, Aguilera A (2011) Nab2 functions in the metabolism of RNA driven by polymerases II and III. Mol Biol Cell 22: 2729-2740
32. González-Aguilera C, Tous R, Gómez-González B, Huertas P, Luna R, Aguilera A (2008) The THP1-SAC3-SUS1-CDC31 complex works in transcription elongation-mRNA export preventing RNA-mediated genome instability. Mol Biol Cell 19: 4310-4318
33. González-Barrera S, Prado F, Verhage R, Brouwer J, Aguilera A (2002) Defective nucleotide excision repair in yeast hpr1 and tho2 mutants. Nucleic Acids Res 30: 2193-2201
34. Hemming SA, Jansma DB, Macgregor PF, Goryachev A, Friesen JD, Edwards AM (2000) RNA polymerase II subunit Rpb9 regulates transcription elongation in vivo. J Biol Chem 275: 35506-35511
35. Holmes AM, Haber JE (1999) Double-strand break repair in yeast requires both leading and lagging strand DNA polymerases. Cell 96: 415-424
36. Huertas P, Aguilera A (2003) Cotranscriptionally formed DNA:RNA hybrids mediate transcription elongation impairment and transcription-associated recombination. Mol Cell 12: 711-721
37. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4: 249-264
38. Ivessa AS, Zhou JQ, Zakian VA (2000) The Saccharomyces Pif1p DNA helicase and the highly related Rrm3p have opposite effects on replication fork progression in ribosomal DNA. Cell 100: 479-489
39. Ivessa AS, Lenzmeier BA, Bessler JB, Goudsouzian LK, Schnakenberg SL, Zakian VA (2003) The Saccharomyces cerevisiae helicase Rrm3p facilitates replication past nonhistone protein-DNA complexes. Mol Cell 12: 1525-1536
40. Kim N, Abdulovic AL, Gealy R, Lippert MJ, Jinks-Robertson S (2007) Transcription-associated mutagenesis in yeast is directly proportional to the level of gene expression and influenced by the direction of DNA replication. DNA Repair (Amst) 6: 1285-1296
41. Kim TS, Liu CL, Yassour M, Holik J, Friedman N, Buratowski S, Rando OJ (2010) RNA polymerase mapping during stress responses reveals widespread nonproductive transcription in yeast. Genome Biol 11: R75
42. Kim N, Jinks-Robertson S (2012) Transcription as a source of genome instability. Nat Rev Genet 13: 204-214
43. Labib K, De Piccoli G (2011) Surviving chromosome replication: the many roles of the S-phase checkpoint pathway. Philos Trans R Soc Lond B Biol Sci 366: 3554-3561
44. Lennon JC 3rd, Wind M, Saunders L, Hock MB, Reines D (1998) Mutations in RNA polymerase II and elongation factor SII severely reduce mRNA levels in Saccharomyces cerevisiae. Mol Cell Biol 18: 5771-5779
45. Li X, Manley JL (2005) Inactivation of the SR protein splicing factor ASF/SF2 results in genomic instability. Cell 122: 365-378
46. Li S, Ding B, Chen R, Ruggiero C, Chen X (2006) Evidence that the transcription elongation function of Rpb9 is involved in transcription-coupled DNA repair in Saccharomyces cerevisiae. Mol Cell Biol 26: 9430-9441
47. Lisby M, Rothstein R, Mortensen UH (2001) Rad52 forms DNA repair and recombination centers during S phase. Proc Natl Acad Sci USA 98: 8276-8282
48. Luna R, Jimeno S, Marin M, Huertas P, García-Rubio M, Aguilera A (2005) Interdependence between transcription and mRNP processing and export, and its impact on genetic stability. Mol Cell 18: 711-722
49. Marin A, Gallardo M, Kato Y, Shirahige K, Gutierrez G, Ohta K, Aguilera A (2003) Relationship between G+C content, ORF-length and mRNA concentration in Saccharomyces cerevisiae. Yeast 20: 703-711
50. Martin C, Okamura S, Young R (1990) Genetic exploration of interactive domains in RNA polymerase II subunits. Mol Cell Biol 10: 1908-1914
51. McGlynn P, Lloyd RG (2000) Modulation of RNA polymerase by (p)ppGpp reveals a RecG-dependent mechanism for replication fork progression. Cell 101: 35-45
52. Merrikh H, Zhang Y, Grossman AD, Wang JD (2012) Replication-transcription conflicts in bacteria. Nat Rev Microbiol 10: 449-458
53. Mischo HE, Gómez-González B, Grzechnik P, Rondón AG, Wei W, Steinmetz L, Aguilera A, Proudfoot NJ (2011) Yeast Sen1 helicase protects the genome from transcription-associated instability. Mol Cell 41: 21-32
54. Moriel-Carretero M, Aguilera A (2010) A postincision-deficient TFIIH causes replication fork breakage and uncovers alternative Rad51- or Pol32-mediated restart mechanisms. Mol Cell 37: 690-701
55. Muñoz-Galván S, Jimeno S, Rothstein R, Aguilera A (2013a) Histone H3K56 acetylation, Rad52, and non-DNA repair factors control double-strand break repair choice with the sister chromatid. PLoS Genet 9: e1003237
56. Muñoz-Galván S, Lopez-Saavedra A, Jackson SP, Huertas P, Cortes-Ledesma F, Aguilera A (2013b) Competing roles of DNA end resection and non-homologous end joining functions in the repair of replication-born double-strand breaks by sister-chromatid recombination. Nucleic Acids Res 41: 1669-1683
57. Nonet M, Scafe C, Sexton J, Young R (1987) Eucaryotic RNA polymerase conditional mutant that rapidly ceases mRNA synthesis. Mol Cell Biol 7: 1602-1611
58. Paulsen RD, Soni DV, Wollman R, Hahn AT, Yee MC, Guan A, Hesley JA, Miller SC, Cromwell EF, Solow-Cordero DE, Meyer T, Cimprich KA (2009) A genome-wide siRNA screen reveals diverse cellular processes and pathways that mediate genome stability. Mol Cell 35: 228-239
59. Powell W, Reines D (1996) Mutations in the second largest subunit of RNA polymerase II cause 6-azauracil sensitivity in yeast and increased transcriptional arrest in vitro. J Biol Chem 271: 6866-6873
60. Prado F, Aguilera A (2005) Impairment of replication fork progression mediates RNA polII transcription-associated recombination. EMBO J 24: 1267-1276
61. Rodríguez-Navarro S, Fischer T, Luo MJ, Antúnez O, Brettschneider S, Lechner J, Pérez-Ortín JE, Reed R, Hurt E (2004) Sus1, a functional component of the SAGA histone acetylase complex and the nuclear pore-associated mRNA export machinery. Cell 116: 75-86
62. Rondón AG, Gallardo M, García-Rubio M, Aguilera A (2004) Molecular evidence indicating that the yeast PAF complex is required for transcription elongation. EMBO Rep 5: 47-53
63. Rondon AG, García-Rubio M, González-Barrera S, Aguilera A (2003) Molecular evidence for a positive role of Spt4 in transcription elongation. EMBO J 22: 612-620
64. Santocanale C, Diffley JF (1998) A Mec1- and Rad53-dependent checkpoint controls late-firing origins of DNA replication. Nature 395: 615-618
65. Santos-Pereira JM, Herrero AB, Garcia-Rubio ML, Marin A, Moreno S, Aguilera A (2013) The Npl3 hnRNP prevents R-loop-mediated transcription-replication conflicts and genome instability. Genes Dev 27: 2445-2458
66. Scafe C, Martin C, Nonet M, Podos S, Okamura S, Young RA (1990) Conditional mutations occur predominantly in highly conserved residues of RNA polymerase II subunits. Mol Cell Biol 10: 1270-1275
67. Schmidt KH, Reimers JM, Wright BE (2006) The effect of promoter strength, supercoiling and secondary structure on mutation rates in Escherichia coli. Mol Microbiol 60: 1251-1261
68. Schroeder SC, Schwer B, Shuman S, Bentley D (2000) Dynamic association of capping enzymes with transcribing RNA polymerase II. Genes Dev 14: 2435-2440
69. Selth LA, Sigurdsson S, Svejstrup JQ (2010) Transcript Elongation by RNA Polymerase II. Annu Rev Biochem 79: 271-293
70. Smyth GK (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: Article 3
71. Song OK, Wang X, Waterborg JH, Sternglanz R (2003) An Nalpha-acetyltransferase responsible for acetylation of the N-terminal residues of histones H4 and H2A. J Biol Chem 278: 38190-38112
72. Stirling PC, Chan YA, Minaker SW, Aristizabal MJ, Barrett I, Sipahimalani P, Kobor MS, Hieter P (2012) R-loop-mediated genome instability in mRNA cleavage and polyadenylation mutants. Genes Dev 26: 163-175
73. Strathern J, Malagon F, Irvin J, Gotte D, Shafer B, Kireeva M, Lubkowska L, Jin DJ, Kashlev M (2013) The fidelity of transcription: RPB1 (RPO21) mutations that increase transcriptional slippage in S. cerevisiae. J Biol Chem 288: 2689-2699
74. Tardiff DF, Abruzzi KC, Rosbash M (2007) Protein characterization of Saccharomyces cerevisiae RNA polymerase II after in vivo cross-linking. Proc Natl Acad Sci USA 104: 19948-19953
75. Tous C, Aguilera A (2007) Impairment of transcription elongation by R-loops in vitro. Biochem Biophys Res Comm 360: 428-432
76. Tous C, Rondón AG, García-Rubio M, González-Aguilera C, Luna R, Aguilera A (2011) A novel assay identifies transcript elongation roles for the Nup84 complex and RNA processing factors. EMBO J 30: 1953-1964
77. Trautinger BW, Lloyd RG (2002) Modulation of DNA repair by mutations flanking the DNA channel through RNA polymerase. EMBO J 21: 6944-6953
78. Van Mullem V, Wery M, Werner M, Vandenhaute J, Thuriaux P (2002) The Rpb9 subunit of RNA polymerase II binds transcription factor TFIIE and interferes with the SAGA and elongator histone acetyltransferases. J Biol Chem 277: 10220-10225
79. Wahba L, Amon JD, Koshland D, Vuica-Ross M (2011) RNase H and multiple RNA biogenesis factors cooperate to prevent RNA:DNA hybrids from generating genome instability. Mol Cell 44: 978-988
80. Wellinger RE, Prado F, Aguilera A (2006) Replication fork progression is impaired by transcription in hyperrecombinant yeast cells lacking a functional THO complex. Mol Cell Biol 26: 3327-3334
81. Wettenhall JM, Simpson KM, Satterley K, Smyth GK (2006) affylmGUI: a graphical user interface for linear modeling of single channel microarray data. Bioinformatics 22: 897-899