The spliceosome-associated protein Nrl1 suppresses homologous recombination-dependent R-loop formation in fission yeast

Nucleic Acids Research

Volumn 44, Issue 4, 2015, Pages 1703-1717

  Aronica, Lucia ^a,b   Kasparek, Torben ^c   Ruchman, David ^a   Marquez, Yamile ^d   Cipak, Lubos ^e   Cipakova, Ingrid ^e   Anrather, Dorothea ^a   Mikolaskova, Barbora ^e   Radtke, Maximilian ^a   Sarkar, Sovan ^c   Pai, Chen Chun ^c   Blaikley, Elizabeth ^c   Walker, Carol ^c   Shen, Kuo Fang ^f   Schroeder, Renee ^a   Barta, Andrea ^d   Forsburg, Susan L ^f   Humphrey, Timothy C ^c  

^a MAX F PERUTZ LABORATORIES   (Austria)

^b STANFORD UNIVERSITY   (United States)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d MEDICAL UNIVERSITY OF VIENNA   (Austria)

^e CANCER RESEARCH INSTITUTE   (Slovakia)

^f UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; DNA; MESSENGER RNA PRECURSOR; NRL1 PROTEIN; RAD51 PROTEIN; RAD52 PROTEIN; RNA; UNCLASSIFIED DRUG; NRL1 PROTEIN, S POMBE; RAD52 PROTEIN, HUMAN; RNA PRECURSOR; SCHIZOSACCHAROMYCES POMBE PROTEIN;

ARTICLE; CONTROLLED STUDY; DNA DAMAGE; DNA HYBRIDIZATION; GENE EXPRESSION; GENETIC CONSERVATION; GENETIC STABILITY; GENOMIC INSTABILITY; HOMOLOGOUS RECOMBINATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RECOMBINATION REPAIR; RNA HYBRIDIZATION; RNA SPLICING; SCHIZOSACCHAROMYCES; SPLICEOSOME; WILD TYPE; ALTERNATIVE RNA SPLICING; CHEMISTRY; DNA REPAIR; GENETICS; METABOLISM;

ALTERNATIVE SPLICING; DNA; DNA REPAIR; GENOMIC INSTABILITY; HOMOLOGOUS RECOMBINATION; RAD51 RECOMBINASE; RAD52 DNA REPAIR AND RECOMBINATION PROTEIN; RNA; RNA PRECURSORS; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; SPLICEOSOMES;

EID: 84960490650     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv1473     Document Type: Article

References (56)

1. Hanahan, D. andWeinberg, R.A. (2011) Hallmarks of cancer: the next generation. Cell, 144, 646-674.
2. Malkova, A. and Haber, J.E. (2012) Mutations arising during repair of chromosome breaks. Annu. Rev. Genet., 46, 455-473.
3. Skourti-Stathaki, K. and Proudfoot, N.J. (2014) A double-edged sword: R loops as threats to genome integrity and powerful regulators of gene expression. Genes Dev., 28, 1384-1396.
4. Aguilera, A. and Garcia-Muse, T. (2012) R loops: from transcription byproducts to threats to genome stability. Mol. Cell, 46, 115-124.
5. Hamperl, S. and Cimprich, K.A. (2014) The contribution of co-transcriptional RNA:DNA hybrid structures to DNA damage and genome instability. DNA Repair (Amst), 19, 84-94.
6. Ginno, P.A., Lim, Y.W., Lott, P.L., Korf, I. and Chedin, F. (2013) GC skew at the 5' and 3' ends of human genes links R-loop formation to epigenetic regulation and transcription termination. Genome Res., 23, 1590-1600.
7. Sun, Q., Csorba, T., Skourti-Stathaki, K., Proudfoot, N.J. and Dean, C. (2013) R-loop stabilization represses antisense transcription at the Arabidopsis FLC locus. Science, 340, 619-621.
8. Chan, Y.A., Aristizabal, M.J., Lu, P.Y., Luo, Z., Hamza, A., Kobor, M.S., Stirling, P.C. and Hieter, P. (2014) Genome-wide profiling of yeast DNA:RNA hybrid prone sites with DRIP-chip. PLoS Genet., 10, e1004288.
9. Skourti-Stathaki, K., Proudfoot, N.J. and Gromak, N. (2011) Human senataxin resolves RNA/DNA hybrids formed at transcriptional pause sites to promote Xrn2-dependent termination. Mol. Cell, 42, 794-805.
10. Chan, Y.A., Hieter, P. and Stirling, P.C. (2014) Mechanisms of genome instability induced by RNA-processing defects. Trends Genet., 30, 245-253.
11. Stirling, P.C., Chan, Y.A., Minaker, S.W., Aristizabal, M.J., Barrett, I., Sipahimalani, P., Kobor, M.S. and Hieter, P. (2012) R-loop-mediated genome instability in mRNA cleavage and polyadenylation mutants. Genes Dev., 26, 163-175.
12. Bhatia, V., Barroso, S.I., Garcia-Rubio, M.L., Tumini, E., Herrera-Moyano, E. and Aguilera, A. (2014) BRCA2 prevents R-loop accumulation and associates with TREX-2 mRNA export factor PCID2. Nature, 511, 362-365.
13. Chernikova, S.B., Razorenova, O.V., Higgins, J.P., Sishc, B.J., Nicolau, M., Dorth, J.A., Chernikova, D.A., Kwok, S., Brooks, J.D., Bailey, S.M. et al. (2012) Deficiency in mammalian histone H2B ubiquitin ligase Bre1 (Rnf20/Rnf40) leads to replication stress and chromosomal instability. Cancer Res., 72, 2111-2119.
14. Ruiz, J.F., Gomez-Gonzalez, B. and Aguilera, A. (2011) AID induces double-strand breaks at immunoglobulin switch regions and c-MYC causing chromosomal translocations in yeast THO mutants. PLoS Genet., 7, e1002009.
15. Jackson, B.R., Noerenberg, M. and Whitehouse, A. (2014) A novel mechanism inducing genome instability in Kaposi's sarcoma-associated herpesvirus infected cells. PLoS Pathog., 10, e1004098.
16. Paulsen, R.D., Soni, D.V., Wollman, R., Hahn, A.T., Yee, M.C., Guan, A., Hesley, J.A., Miller, S.C., Cromwell, E.F., Solow-Cordero, D.E. et al. (2009) A genome-wide siRNA screen reveals diverse cellular processes and pathways that mediate genome stability. Mol. Cell, 35, 228-239.
17. Lenzken, S.C., Loffreda, A. and Barabino, S.M. (2013) RNA splicing: a new player in the DNA damage response. Int. J. Cell Biol., 2013, 153634.
18. Sato, Y., Yoshizato, T., Shiraishi, Y., Maekawa, S., Okuno, Y., Kamura, T., Shimamura, T., Sato-Otsubo, A., Nagae, G., Suzuki, H. et al. (2013) Integrated molecular analysis of clear-cell renal cell carcinoma. Nat. Genet., 45, 860-867.
19. Li, X. and Manley, J.L. (2005) Inactivation of the SR protein splicing factor ASF/SF2 results in genomic instability. Cell, 122, 365-378.
20. Rajesh, C., Baker, D.K., Pierce, A.J. and Pittman, D.L. (2011) The splicing-factor related protein SFPQ/PSF interacts with RAD51D and is necessary for homology-directed repair and sister chromatid cohesion. Nucleic Acids Res., 39, 132-145.
21. Adamson, B., Smogorzewska, A., Sigoillot, F.D., King, R.W. and Elledge, S.J. (2012) A genome-wide homologous recombination screen identifies the RNA-binding protein RBMX as a component of the DNA-damage response. Nat. Cell Biol., 14, 318-328.
22. Wahba, L., Gore, S.K. and Koshland, D. (2013) The homologous recombination machinery modulates the formation of RNA-DNA hybrids and associated chromosome instability. Elife, 2, e00505.
23. Savage, K.I., Gorski, J.J., Barros, E.M., Irwin, G.W., Manti, L., Powell, A.J., Pellagatti, A., Lukashchuk, N., McCance, D.J., McCluggage, W.G. et al. (2014) Identification of a BRCA1-mRNA splicing complex required for efficient DNA repair and maintenance of genomic stability. Mol. Cell, 54, 445-459.
24. Marechal, A., Li, J.M., Ji, X.Y., Wu, C.S., Yazinski, S.A., Nguyen, H.D., Liu, S., Jimenez, A.E., Jin, J. and Zou, L. (2014) PRP19 transforms into a sensor of RPA-ssDNA after DNA damage and drives ATR activation via a ubiquitin-mediated circuitry. Mol Cell, 53, 235-246.
25. Jones, K.B., Salah, Z., Del Mare, S., Galasso, M., Gaudio, E., Nuovo, G.J., Lovat, F., LeBlanc, K., Palatini, J., Randall, R.L. et al. (2012) miRNA signatures associate with pathogenesis and progression of osteosarcoma. Cancer Res., 72, 1865-1877.
26. Chiu, C.G., Nakamura, Y., Chong, K.K., Huang, S.K., Kawas, N.P., Triche, T., Elashoff, D., Kiyohara, E., Irie, R.F., Morton, D.L. et al. (2014) Genome-wide characterization of circulating tumor cells identifies novel prognostic genomic alterations in systemic melanoma metastasis. Clin. Chem., 60, 873-885.
27. Gregan, J., Rabitsch, P.K., Rumpf, C., Novatchkova, M., Schleiffer, A. and Nasmyth, K. (2006) High-throughput knockout screen in fission yeast. Nat. Protoc., 1, 2457-2464.
28. Cipak, L., Spirek, M., Novatchkova, M., Chen, Z., Rumpf, C., Lugmayr, W., Mechtler, K., Ammerer, G., Csaszar, E. and Gregan, J. (2009) An improved strategy for tandem affinity purification-tagging of Schizosaccharomyces pombe genes. Proteomics, 9, 4825-4828.
29. Moss, J., Tinline-Purvis, H., Walker, C.A., Folkes, L.K., Stratford, M.R., Hayles, J., Hoe, K.L., Kim, D.U., Park, H.O., Kearsey, S.E. et al. (2010) Break-induced ATR and Ddb1-Cul4(Cdt)(2) ubiquitin ligase-dependent nucleotide synthesis promotes homologous recombination repair in fission yeast. Genes Dev., 24, 2705-2716.
30. Cipak, L., Gupta, S., Rajovic, I., Jin, Q.W., Anrather, D., Ammerer, G., McCollum, D. and Gregan, J. (2013) Crosstalk between casein kinase II and Ste20-related kinase Nak1. Cell Cycle, 12, 884-888.
31. Cox, J. and Mann, M. (2008) MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol., 26, 1367-1372.
32. Zhong, S., Joung, J.G., Zheng, Y., Chen, Y.R., Liu, B., Shao, Y., Xiang, J.Z., Fei, Z. and Giovannoni, J.J. (2011) High-throughput illumina strand-specific RNA sequencing library preparation. Cold Spring Harb. Protoc., 8, 940-949.
33. Loidl, J. and Lorenz, A. (2009) Analysis of Schizosaccharomyces pombe meiosis by nuclear spreading. Methods Mol. Biol., 558, 15-36.
34. Wahba, L., Amon, J.D., Koshland, D. and 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.
35. Guang, S., Bochner, A.F., Burkhart, K.B., Burton, N., Pavelec, D.M. and Kennedy, S. (2010) Small regulatory RNAs inhibit RNA polymerase II during the elongation phase of transcription. Nature, 465, 1097-1101.
36. Ben-Yehuda, S., Dix, I., Russell, C.S., McGarvey, M., Beggs, J.D. and Kupiec, M. (2000) Genetic and physical interactions between factors involved in both cell cycle progression and pre-mRNA splicing in Saccharomyces cerevisiae. Genetics, 156, 1503-1517.
37. Rigaut, G., Shevchenko, A., Rutz, B., Wilm, M., Mann, M. and Seraphin, B. (1999) A generic protein purification method for protein complex characterization and proteome exploration. Nat. Biotechnol., 17, 1030-1032.
38. Chen, W., Shulha, H.P., Ashar-Patel, A., Yan, J., Green, K.M., Query, C.C., Rhind, N., Weng, Z. and Moore, M.J. (2014) Endogenous U2.U5.U6 snRNA complexes in S. pombe are intron lariat spliceosomes. RNA, 20, 308-320.
39. Lee, N.N., Chalamcharla, V.R., Reyes-Turcu, F., Mehta, S., Zofall, M., Balachandran, V., Dhakshnamoorthy, J., Taneja, N., Yamanaka, S., Zhou, M. et al. (2013) Mtr4-like protein coordinates nuclear RNA processing for heterochromatin assembly and for telomere maintenance. Cell, 155, 1061-1074.
40. Caspari, T. and Carr, A.M. (1999) DNA structure checkpoint pathways in Schizosaccharomyces pombe. Biochimie, 81, 173-181.
41. Walworth, N.C. and Bernards, R. (1996) rad-dependent response of the chk1-encoded protein kinase at the DNA damage checkpoint. Science, 271, 353-356.
42. Latif, C., den Elzen, N.R. and O'Connell, M.J. (2004) DNA damage checkpoint maintenance through sustained Chk1 activity. J. Cell Sci., 117, 3489-3498.
43. Kim, W.J., Lee, S., Park, M.S., Jang, Y.K., Kim, J.B. and Park, S.D. (2000) Rad22 protein, a rad52 homologue in Schizosaccharomyces pombe, binds to DNA double-strand breaks. J. Biol. Chem., 275, 35607-35611.
44. Lisby, M., Mortensen, U.H. and Rothstein, R. (2003) Colocalization of multiple DNA double-strand breaks at a single Rad52 repair centre. Nat. Cell Biol., 5, 572-577.
45. van den Bosch, M., Vreeken, K., Zonneveld, J.B., Brandsma, J.A., Lombaerts, M., Murray, J.M., Lohman, P.H. and Pastink, A. (2001) Characterization of RAD52 homologs in the fission yeast Schizosaccharomyces pombe. Mutat. Res., 461, 311-323.
46. Tinline-Purvis, H., Savory, A.P., Cullen, J.K., Dave, A., Moss, J., Bridge, W.L., Marguerat, S., Bahler, J., Ragoussis, J., Mott, R. et al. (2009) Failed gene conversion leads to extensive end processing and chromosomal rearrangements in fission yeast. EMBO J., 28, 3400-3412.
47. Wold, M.S. (1997) Replication protein A: a heterotrimeric, single-stranded DNA-binding protein required for eukaryotic DNA metabolism. Annu. Rev. Biochem., 66, 61-92.
48. Sugawara, N., Wang, X. and Haber, J.E. (2003) In vivo roles of Rad52, Rad54, and Rad55 proteins in Rad51-mediated recombination. Mol. Cell, 12, 209-219.
49. Watson, A., Mata, J., Bahler, J., Carr, A. and Humphrey, T. (2004) Global gene expression responses of fission yeast to ionizing radiation. Mol. Biol. Cell, 15, 851-860.
50. Boguslawski, S.J., Smith, D.E., Michalak, M.A., Mickelson, K.E., Yehle, C.O., Patterson, W.L. and Carrico, R.J. (1986) Characterization of monoclonal antibody to DNA.RNA and its application to immunodetection of hybrids. J. Immunol. Methods, 89, 123-130.
51. El Hage, A., Webb, S., Kerr, A. and Tollervey, D. (2014) Genome-wide distribution of RNA-DNA hybrids identifies RNase H targets in tRNA genes, retrotransposons and mitochondria. PLoS Genet., 10, e1004716.
52. Steinmetz, E.J., Warren, C.L., Kuehner, J.N., Panbehi, B., Ansari, A.Z. and Brow, D.A. (2006) Genome-wide distribution of yeast RNA polymerase II and its control by Sen1 helicase. Mol. Cell, 24, 735-746.
53. Mischo, H.E., Gomez-Gonzalez, B., Grzechnik, P., Rondon, A.G., Wei, W., Steinmetz, L., Aguilera, A. and Proudfoot, N.J. (2011) Yeast Sen1 helicase protects the genome from transcription-associated instability. Mol. Cell, 41, 21-32.
54. Lazzaro, F., Novarina, D., Amara, F., Watt, D.L., Stone, J.E., Costanzo, V., Burgers, P.M., Kunkel, T.A., Plevani, P. and Muzi-Falconi, M. (2012) RNase H and postreplication repair protect cells from ribonucleotides incorporated in DNA. Mol Cell, 45, 99-110.
55. Keskin, H., Shen, Y., Huang, F., Patel, M., Yang, T., Ashley, K., Mazin, A.V. and Storici, F. (2014) Transcript-RNA-templated DNA recombination and repair. Nature, 515, 436-439.
56. Vizcaino, J.A., Deutsch, E.W., Wang, R., Csordas, A., Reisinger, F., Rios, D., Dianes, J.A., Sun, Z., Farrah, T., Bandeira, N. et al. (2014) ProteomeXchange provides globally coordinated proteomics data submission and dissemination. Nat. Biotechnol., 32, 223-226.