The THO complex component Thp2 counteracts telomeric R-loops and telomere shortening

EMBO Journal

Volumn 32, Issue 21, 2013, Pages 2861-2871

  Pfeiffer, Verena ^a   Crittin, Jérôme ^a   Grolimund, Larissa ^a   Lingner, Joachim ^a  

^a EPFL   (Switzerland)

Author keywords

DNA replication stress; R loops; telomere instability; TERRA; THO

Indexed keywords

EXONUCLEASE; LONG UNTRANSLATED RNA; PROTEIN; PROTEIN THO; PROTEIN THP2; RIBONUCLEASE H; RNA; TELOMERE BINDING PROTEIN; TELOMERIC REPEAT CONTAINING RNA; UNCLASSIFIED DRUG;

ARTICLE; CELL STRESS; CHROMOSOME; CONTROLLED STUDY; DNA DAMAGE CHECKPOINT; DNA REPLICATION; DNA RNA HYBRIDIZATION; GENE DELETION; GENE OVEREXPRESSION; GENETIC ANALYSIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN SUBUNIT; TELOMERE HOMEOSTASIS; TELOMERE SHORTENING;

DNA, FUNGAL; DNA-BINDING PROTEINS; NUCLEAR PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TELOMERE; TELOMERE SHORTENING; TRANSCRIPTION FACTORS;

EID: 84887053583     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2013.217     Document Type: Article

References (46)

1. Askree SH, Yehuda T, Smolikov S, Gurevich R, Hawk J, Coker C, Krauskopf A, Kupiec M, McEachern MJ (2004) A genome-wide screen for Saccharomyces cerevisiae deletion mutants that affect telomere length. Proc Natl Acad Sci USA 101: 8658-8663 (Pubitemid 38745827)
2. Azvolinsky A, Dunaway S, Torres JZ, Bessler JB, Zakian VA (2006) The S. cerevisiae Rrm3p DNA helicase moves with the replication fork and affects replication of all yeast chromosomes. Genes Dev 20: 3104-3116 (Pubitemid 44790626)
3. Azzalin CM, Reichenbach P, Khoriauli L, Giulotto E, Lingner J (2007) Telomeric repeat containing RNA and RNA surveillance factors at mammalian chromosome ends. Science 318: 798-801 (Pubitemid 351411771)
4. Bermejo R, Lai MS, Foiani M (2012) Preventing replication stress to maintain genome stability: resolving conflicts between replication and transcription. Mol Cell 45: 710-718
5. Boguslawski SJ, Smith DE, Michalak MA, Mickelson KE, Yehle CO, Patterson WL, Carrico RJ (1986) Characterization of monoclonal antibody to DNA.RNA and its application to immunodetection of hybrids. J Immunol Methods 89: 123-130 (Pubitemid 16079589)
6. Casteel DE, Zhuang S, Zeng Y, Perrino FW, Boss GR, Goulian M, Pilz RB (2009) A DNA polymerase-{alpha}{middle dot}primase cofactor with homology to replication protein A-32regulates DNA replication in mammalian cells. J Biol Chem 284: 5807-5818
7. Chawla R, Redon S, Raftopoulou C, Wischnewski H, Gagos S, Azzalin CM (2011) Human UPF1 interacts with TPP1 and telomerase and sustains telomere leading-strand replication. EMBO J 30: 4047-4058
8. Crabbe L, Verdun RE, Haggblom CI, Karlseder J (2004) Defective telomere lagging strand synthesis in cells lacking WRN helicase activity. Science 306: 1951-1953 (Pubitemid 39627862)
9. Crouch RJ, Arudchandran A, Cerritelli SM (2001) RNase H1 of Saccharomyces cerevisiae: methods and nomenclature. Methods Enzymol 341: 395-413 (Pubitemid 32928540)
10. El Hage A, French SL, Beyer AL, Tollervey D (2010) Loss of Topoisomerase I leads to R-loop-mediated transcriptional blocks during ribosomal RNA synthesis. Genes Dev 24: 1546-1558
11. Forstemann K, Hoss M, Lingner J (2000) Telomerase-dependent repeat divergence at the 30 ends of yeast telomeres. Nucleic Acids Res 28: 2690-2694 (Pubitemid 30488012)
12. Ginno PA, Lott PL, Christensen HC, Korf I, Chedin F (2012) R-loop formation is a distinctive characteristic of unmethylated human CpG island promoters. Mol Cell 45: 814-825
13. Gomez-Gonzalez 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
14. Gomez-Gonzalez B, Garcia-Rubio M, Bermejo R, Gaillard H, Shirahige K, Marin A, Foiani M, Aguilera A (2011) Genomewide function of THO/TREX in active genes prevents R-loopdependent replication obstacles. EMBO J 30: 3106-3119
15. Grossi S, Puglisi A, Dmitriev PV, Lopes M, Shore D (2004) Pol12, the B subunit of DNA polymerase alpha, functions in both telomere capping and length regulation. Genes Dev 18: 992-1006 (Pubitemid 38620240)
16. Gu P, Min JN, Wang Y, Huang C, Peng T, Chai W, Chang S (2012) CTC1 deletion results in defective telomere replication, leading to catastrophic telomere loss and stem cell exhaustion. EMBO J 31: 2309-2321
17. Hu Z, Zhang A, Storz G, Gottesman S, Leppla SH (2006) An antibody-based microarray assay for small RNA detection. Nucleic Acids Res 34: e52
18. Huang C, Dai X, Chai W (2012) Human Stn1 protects telomere integrity by promoting efficient lagging-strand synthesis at telomeres and mediating C-strand fill-in. Cell Res 22: 1681-1695
19. Huertas P, Aguilera A (2003) Cotranscriptionally formed DNA:RNA hybrids mediate transcription elongation impairment and transcription-associated recombination. Mol Cell 12: 711-721 (Pubitemid 37222491)
20. Iglesias N, Redon S, Pfeiffer V, Dees M, Lingner J, Luke B (2011) Subtelomeric repetitive elements determine TERRA regulation by Rap1/Rif and Rap1/Sir complexes in yeast. EMBO Rep 12: 587-593
21. Ito H, Fukuda Y, Murata K, Kimura A (1983) Transformation of intact yeast cells treated with alkali cations. J Bacteriol 153: 163-168 (Pubitemid 13119852)
22. Ivessa AS, Zhou JQ, Schulz VP, Monson EK, Zakian VA (2002) Saccharomyces Rrm3p, a 50 to 30 DNA helicase that promotes replication fork progression through telomeric and subtelomeric DNA. Genes Dev 16: 1383-1396 (Pubitemid 34615091)
23. Longtine MS, McKenzie 3rd A, Demarini DJ, Shah NG, Wach A, Brachat A, Philippsen P, Pringle JR (1998) Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14: 953-961 (Pubitemid 28328001)
24. Luke B, Panza A, Redon S, Iglesias N, Li Z, Lingner J (2008) The Rat1p 50 to 30 exonuclease degrades telomeric repeat-containing RNA and promotes telomere elongation in Saccharomyces cerevisiae. Mol Cell 32: 465-477
25. Makovets S, Herskowitz I, Blackburn EH (2004) Anatomy and dynamics of DNA replication fork movement in yeast telomeric regions. Mol Cell Biol 24: 4019-4031 (Pubitemid 38496178)
26. Miller KM, Rog O, Cooper JP (2006) Semi-conservative DNA replication through telomeres requires Taz1. Nature 440: 824-828
27. Mischo HE, Gomez-Gonzalez B, Grzechnik P, Rondon 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
28. Paeschke K, Capra JA, Zakian VA (2011) DNA replication through G-quadruplex motifs is promoted by the Saccharomyces cerevisiae Pif1 DNA helicase. Cell 145: 678-691
29. Paschini M, Toro TB, Lubin JW, Braunstein-Ballew B, Morris DK, Lundblad V (2012) A naturally thermolabile activity compromises genetic analysis of telomere function in Saccharomyces cerevisiae. Genetics 191: 79-93
30. Pfeiffer V, Lingner J (2012) TERRA promotes telomere shortening through exonuclease 1-mediated resection of chromosome ends. PLoS Genet 8: e1002747
31. Qi H, Zakian VA (2000) The Saccharomyces telomere-binding protein Cdc13p interacts with both the catalytic subunit of DNA polymerase alpha and the telomerase-associated Est1 protein. Genes Dev 14: 1777-1788 (Pubitemid 30602996)
32. Redon S, Reichenbach P, Lingner J (2010) The non-coding RNA TERRA is a natural ligand and direct inhibitor of human telomerase. Nucleic Acids Res 38: 5797-5806
33. Rondon AG, Jimeno S, Aguilera A (2010) The interface between transcription and mRNP export: from THO to THSC/TREX-2. Biochim Biophys Acta 1799: 533-538
34. Rougemaille M, Dieppois G, Kisseleva-Romanova E, Gudipati RK, Lemoine S, Blugeon C, Boulay J, Jensen TH, Stutz F, Devaux F, Libri D (2008) THO/Sub2p functions to coordinate 30-end processing with gene-nuclear pore association. Cell 135: 308-321
35. Schoeftner S, Blasco MA (2008) Developmentally regulated transcription of mammalian telomeres by DNA-dependent RNA polymerase II. Nat Cell Biol 10: 228-236 (Pubitemid 351194053)
36. Sfeir A, De Lange T (2012) Removal of shelterin reveals the telomere end-protection problem. Science 336: 593-597
37. Sfeir A, Kosiyatrakul ST, Hockemeyer D, MacRae SL, Karlseder J, Schildkraut CL, De Lange T (2009) Mammalian telomeres resemble fragile sites and require TRF1 for efficient replication. Cell 138: 90-103
38. Skourti-Stathaki K, Proudfoot NJ, Gromak N (2011) Human senataxin resolves RNA/DNA hybrids formed at transcriptional pause sites to promote Xrn2-dependent termination. Mol Cell 42: 794-805
39. Stewart JA, Wang F, Chaiken MF, Kasbek C, Chastain 2nd PD, Wright WE, Price CM (2012) Human CST promotes telomere duplex replication and general replication restart after fork stalling. EMBO J 31: 3537-3549
40. 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
41. Szekvolgyi L, Rakosy Z, Balint BL, Kokai E, Imre L, Vereb G, Bacso Z, Goda K, Varga S, Balazs M, Dombradi V, Nagy L, Szabo G (2007) Ribonucleoprotein-masked nicks at 50-kbp intervals in the eukaryotic genomic DNA. Proc Natl Acad Sci USA 104: 14964-14969 (Pubitemid 47619576)
42. Teixeira MT, Arneric M, Sperisen P, Lingner J (2004) Telomere length homeostasis is achieved via a switch between telomeraseextendible and-nonextendible states. Cell 117: 323-335 (Pubitemid 38534539)
43. Vannier JB, Pavicic-Kaltenbrunner V, Petalcorin MI, Ding H, Boulton SJ (2012) RTEL1 dismantles T loops and counteracts telomeric G4-DNA to maintain telomere integrity. Cell 149: 795-806
44. 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
45. Wu P, Takai H, De Lange T (2012) Telomeric 30 overhangs derive from resection by Exo1 and Apollo and Fill-In by POT1b-associated CST. Cell 150: 39-52
46. Zenklusen D, Vinciguerra P, Wyss JC, Stutz F (2002) Stable mRNP formation and export require cotranscriptional recruitment of the mRNA export factors Yra1p and Sub2p by Hpr1p. Mol Cell Biol 22: 8241-8253 (Pubitemid 35304057)