A proteome-wide visual screen identifies fission yeast proteins localizing to DNA double-strand breaks

DNA Repair

Volumn 12, Issue 6, 2013, Pages 433-443

  Yu, Yang ^a,b   Ren, Jing Yi ^b   Zhang, Jia Min ^b   Suo, Fang ^b   Fang, Xiao Feng ^b   Wu, Fan ^b   Du, Li Lin ^b  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

^b NATIONAL INSTITUTE OF BIOLOGICAL SCIENCES   (China)

Author keywords

DNA damage response; DNA double strand break; DNA repair; Fission yeast; ORFeome; Schizosaccharomyces pombe

Indexed keywords

DOUBLE STRANDED DNA; FUNGAL PROTEIN; HELICASE; PROTEOME;

ARTICLE; DNA DAMAGE; DNA REPAIR; DNA STRAND BREAKAGE; NONHUMAN; OPEN READING FRAME; PLASMID; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; SCHIZOSACCHAROMYCES POMBE;

CELL CYCLE PROTEINS; DNA BREAKS, DOUBLE-STRANDED; DNA HELICASES; OPEN READING FRAMES; PROTEOME; RECOMBINATIONAL DNA REPAIR; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS;

EUKARYOTA; SCHIZOSACCHAROMYCES POMBE; SCHIZOSACCHAROMYCETACEAE;

EID: 84877831999     PISSN: 15687864     EISSN: 15687856     Source Type: Journal    
DOI: 10.1016/j.dnarep.2013.04.001     Document Type: Article

References (67)

1. Hiom K. Coping with DNA double strand breaks. DNA Repair (Amst.) 2010, 9:1256-1263.
2. Kasparek T.R., Humphrey T.C. DNA double-strand break repair pathways, chromosomal rearrangements and cancer. Semin. Cell Dev. Biol. 2011, 22:886-897.
3. Langerak P., Russell P. Regulatory networks integrating cell cycle control with DNA damage checkpoints and double-strand break repair. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 2011, 366:3562-3571.
4. Lisby M., Rothstein R. Choreography of recombination proteins during the DNA damage response. DNA Repair (Amst.) 2009, 8:1068-1076.
5. Bekker-Jensen S., Mailand N. Assembly and function of DNA double-strand break repair foci in mammalian cells. DNA Repair (Amst.) 2010, 9:1219-1228.
6. Haber J.E. Transpositions and translocations induced by site-specific double-strand breaks in budding yeast. DNA Repair (Amst.) 2006, 5:998-1009.
7. Lisby M., Mortensen U.H., Rothstein R. Colocalization of multiple DNA double-strand breaks at a single Rad52 repair centre. Nat. Cell Biol. 2003, 5:572-577.
8. Friedberg E.C. Deoxyribonucleic acid repair in the yeast Saccharomyces cerevisiae. Microbiol. Rev. 1988, 52:70-102.
9. Phipps J., Nasim A., Miller D.R. Recovery, repair, and mutagenesis in Schizosaccharomyces pombe. Adv. Genet. 1985, 23:1-72.
10. Bennett C.B., Lewis L.K., Karthikeyan G., et al. Genes required for ionizing radiation resistance in yeast. Nat. Genet. 2001, 29:426-434.
11. Birrell G.W., Giaever G., Chu A.M., Davis R.W., Brown J.M. A genome-wide screen in Saccharomyces cerevisiae for genes affecting UV radiation sensitivity. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:12608-12613.
12. Deshpande G.P., Hayles J., Hoe K.-L., Kim D.-U., Park H.-O., Hartsuiker E. Screening a genome-wide S. pombe deletion library identifies novel genes and pathways involved in genome stability maintenance. DNA Repair (Amst.) 2009, 8:672-679.
13. Han T.X., Xu X.-Y., Zhang M.-J., Peng X., Du L.-L. Global fitness profiling of fission yeast deletion strains by barcode sequencing. Genome Biol. 2010, 11:R60.
14. Forsburg S.L., Rhind N. Basic methods for fission yeast. Yeast 2006, 23:173-183.
15. Li P., Li J., Li M., et al. Multiple end joining mechanisms repair a chromosomal DNA break in fission yeast. DNA Repair (Amst.) 2012, 11:120-130.
16. Matsuyama A., Arai R., Yashiroda Y., et al. ORFeome cloning and global analysis of protein localization in the fission yeast Schizosaccharomyces pombe. Nat. Biotechnol. 2006, 24:841-847.
17. Carbon S., Ireland A., Mungall C.J., Shu S., Marshall B., Lewis S. AmiGO: online access to ontology and annotation data. Bioinformatics 2009, 25:288-289.
18. Langerak P., Mejia-Ramirez E., Limbo O., Russell P. Release of Ku and MRN from DNA ends by Mre11 nuclease activity and Ctp1 is required for homologous recombination repair of double-strand breaks. PLoS Genet. 2011, 7:e1002271.
19. Matsuyama A., Shirai A., Yashiroda Y., Kamata A., Horinouchi S., Yoshida M. pDUAL, a multipurpose, multicopy vector capable of chromosomal integration in fission yeast. Yeast 2004, 21:1289-1305.
20. Wood V., Harris M.A., McDowall M.D., et al. PomBase: a comprehensive online resource for fission yeast. Nucleic Acids Res. 2012, 40:D695-D699.
21. Maundrell K. Thiamine-repressible expression vectors pREP and pRIP for fission yeast. Gene 1993, 123:127-130.
22. Du L.-L., Nakamura T.M., Moser B.A., Russell P. Retention but not recruitment of Crb2 at double-strand breaks requires Rad1 and Rad3 complexes. Mol. Cell. Biol. 2003, 23:6150-6158.
23. Riggs A.D., Suzuki H., Bourgeois S. Lac repressor-operator interaction. I. Equilibrium studies. J. Mol. Biol. 1970, 48:67-83.
24. Iacovoni J.S., Russell P., Gaits F. A new inducible protein expression system in fission yeast based on the glucose-repressed inv1 promoter. Gene 1999, 232:53-58.
25. Marguerat S., Schmidt A., Codlin S., Chen W., Aebersold R., Bähler J. Quantitative analysis of fission yeast transcriptomes and proteomes in proliferating and quiescent cells. Cell 2012, 151:671-683.
26. Tommasino M., Maundrell K. Uptake of thiamine by Schizosaccharomyces pombe and its effect as a transcriptional regulator of thiamine-sensitive genes. Curr. Genet. 1991, 20:63-66.
27. Ryan C.J., Roguev A., Patrick K., et al. Hierarchical modularity and the evolution of genetic interactomes across species. Mol. Cell. 2012, 46:691-704.
28. Edwards R.J., Bentley N.J., Carr A.M. A Rad3-Rad26 complex responds to DNA damage independently of other checkpoint proteins. Nat. Cell Biol. 1999, 1:393-398.
29. Cortez D., Guntuku S., Qin J., Elledge S.J. ATR and ATRIP: partners in checkpoint signaling. Science 2001, 294:1713-1716.
30. Furuya K., Poitelea M., Guo L., Caspari T., Carr A.M. Chk1 activation requires Rad9 S/TQ-site phosphorylation to promote association with C-terminal BRCT domains of Rad4TOPBP1. Genes Dev. 2004, 18:1154-1164.
31. Qu M., Yang B., Tao L., et al. Phosphorylation-dependent interactions between Crb2 and Chk1 are essential for DNA damage checkpoint. PLoS Genet. 2012, 8:e1002817.
32. Lopez-Girona A., Tanaka K., Chen X.B., Baber B.A., McGowan C.H., Russell P. Serine-345 is required for Rad3-dependent phosphorylation and function of checkpoint kinase Chk1 in fission yeast. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:11289-11294.
33. Lisby M., Barlow J.H., Burgess R.C., Rothstein R. Choreography of the DNA damage response: spatiotemporal relationships among checkpoint and repair proteins. Cell 2004, 118:699-713.
34. Tkach J.M., Yimit A., Lee A.Y., et al. Dissecting DNA damage response pathways by analysing protein localization and abundance changes during DNA replication stress. Nat. Cell Biol. 2012, 14:966-976.
35. Smogorzewska A., Desetty R., Saito T.T., et al. A genetic screen identifies FAN1, a Fanconi anemia-associated nuclease necessary for DNA interstrand crosslink repair. Mol. Cell. 2010, 39:36-47.
36. Adamson B., Smogorzewska A., Sigoillot F.D., King R.W., Elledge S.J. A genome-wide homologous recombination screen identifies the RNA-binding protein RBMX as a component of the DNA-damage response. Nat. Cell Biol. 2012, 14:318-328.
37. Gregan J., Rabitsch P.K., Sakem B., et al. Novel genes required for meiotic chromosome segregation are identified by a high-throughput knockout screen in fission yeast. Curr. Biol. 2005, 15:1663-1669.
38. Kennedy P.J., Vashisht A.A., Hoe K.-L., et al. A genome-wide screen of genes involved in cadmium tolerance in Schizosaccharomyces pombe. Toxicol. Sci. 2008, 106:124-139.
39. Liu N.-N., Han T.X., Du L.-L., Zhou J.-Q. A genome-wide screen for Schizosaccharomyces pombe deletion mutants that affect telomere length. Cell Res. 2010, 20:963-965.
40. Sun W., Nandi S., Osman F., et al. The FANCM ortholog Fml1 promotes recombination at stalled replication forks and limits crossing over during DNA double-strand break repair. Mol. Cell. 2008, 32:118-128.
41. Huh W.-K., Falvo J.V., Gerke L.C., et al. Global analysis of protein localization in budding yeast. Nature 2003, 425:686-691.
42. Caspari T., Murray J.M., Carr A.M. Cdc2-cyclin B kinase activity links Crb2 and Rqh1-topoisomerase III. Genes Dev. 2002, 16:1195-1208.
43. Meister P., Poidevin M., Francesconi S., Tratner I., Zarzov P., Baldacci G. Nuclear factories for signalling and repairing DNA double strand breaks in living fission yeast. Nucleic Acids Res. 2003, 31:5064-5073.
44. Nakamura T.M., Du L.-L., Redon C., Russell P. Histone H2A phosphorylation controls Crb2 recruitment at DNA breaks, maintains checkpoint arrest, and influences DNA repair in fission yeast. Mol. Cell. Biol. 2004, 24:6215-6230.
45. Morishita T., Furukawa F., Sakaguchi C., et al. Role of the Schizosaccharomyces pombe F-Box DNA helicase in processing recombination intermediates. Mol. Cell. Biol. 2005, 25:8074-8083.
46. Osman F., Dixon J., Barr A.R., Whitby M.C. The F-Box DNA helicase Fbh1 prevents Rhp51-dependent recombination without mediator proteins. Mol. Cell. Biol. 2005, 25:8084-8096.
47. Du L.-L., Nakamura T.M., Russell P. Histone modification-dependent and -independent pathways for recruitment of checkpoint protein Crb2 to double-strand breaks. Genes Dev. 2006, 20:1583-1596.
48. Akamatsu Y., Tsutsui Y., Morishita T., et al. Fission yeast Swi5/Sfr1 and Rhp55/Rhp57 differentially regulate Rhp51-dependent recombination outcomes. EMBO J. 2007, 26:1352-1362.
49. Dovey C.L., Russell P. Mms22 preserves genomic integrity during DNA replication in Schizosaccharomyces pombe. Genetics 2007, 177:47-61.
50. Pinter S.F., Aubert S.D., Zakian V.A. The Schizosaccharomyces pombe Pfh1p DNA helicase is essential for the maintenance of nuclear and mitochondrial DNA. Mol. Cell. Biol. 2008, 28:6594-6608.
51. Octobre G., Lorenz A., Loidl J., Kohli J. The Rad52 homologs Rad22 and Rti1 of Schizosaccharomyces pombe are not essential for meiotic interhomolog recombination, but are required for meiotic intrachromosomal recombination and mating-type-related DNA repair. Genetics 2008, 178:2399-2412.
52. Williams J.S., Williams R.S., Dovey C.L., Guenther G., Tainer J.A., Russell P. gammaH2A binds Brc1 to maintain genome integrity during S-phase. EMBO J. 2010, 29:1136-1148.
53. Cavero S., Limbo O., Russell P. Critical functions of Rpa3/Ssb3 in S-phase DNA damage responses in fission yeast. PLoS Genet. 2010, 6:e1001138.
54. Yasuhira S., Saito T., Maesawa C., Masuda T. Sensor and effector kinases in DNA damage checkpoint regulate capacity for homologous recombination repair of fission yeast in G2 phase. DNA Repair (Amst.) 2012, 11:666-675.
55. Moreira M.-C., Klur S., Watanabe M., et al. Senataxin, the ortholog of a yeast RNA helicase, is mutant in ataxia-ocular apraxia 2. Nat. Genet. 2004, 36:225-227.
56. Yüce-Petronczki O., West S.C. Senataxin, defective in the neurogenerative disorder AOA-2, lies at the interface of transcription and the DNA damage response. Mol. Cell. Biol. 2013, 33:406-417.
57. Alzu A., Bermejo R., Begnis M., et al. Senataxin associates with replication forks to protect fork integrity across RNA-polymerase-II-transcribed genes. Cell 2012, 151:835-846.
58. Roguev A., Bandyopadhyay S., Zofall M., et al. Conservation and rewiring of functional modules revealed by an epistasis map in fission yeast. Science 2008, 322:405-410.
59. van den Bosch M., Zonneveld J.B.M., Vreeken K., de Vries F.A.T., Lohman P.H.M., Pastink A. Differential expression and requirements for Schizosaccharomyces pombe RAD52 homologs in DNA repair and recombination. Nucleic Acids Res. 2002, 30:1316-1324.
60. Sparks J.L., Kumar R., Singh M., Wold M.S., Pandita T.K., Burgers P.M. Human exonuclease 5 is a novel sliding exonuclease required for genome stability. J. Biol. Chem. 2012, 287:42773-42783.
61. Doe C.L., Whitby M.C. The involvement of Srs2 in post-replication repair and homologous recombination in fission yeast. Nucleic Acids Res. 2004, 32:1480-1491.
62. Chen X., Cui D., Papusha A., et al. The Fun30 nucleosome remodeller promotes resection of DNA double-strand break ends. Nature 2012, 489:576-580.
63. Costelloe T., Louge R., Tomimatsu N., et al. The yeast Fun30 and human SMARCAD1 chromatin remodellers promote DNA end resection. Nature 2012, 489:581-584.
64. Kratz K., Schöpf B., Kaden S., et al. Deficiency of FANCD2-associated nuclease KIAA1018/FAN1 sensitizes cells to interstrand crosslinking agents. Cell 2010, 142:77-88.
65. MacKay C., Déclais A.-C., Lundin C., et al. Identification of KIAA1018/FAN1, a DNA repair nuclease recruited to DNA damage by monoubiquitinated FANCD2. Cell 2010, 142:65-76.
66. Liu T., Ghosal G., Yuan J., Chen J., Huang J. FAN1 acts with FANCI-FANCD2 to promote DNA interstrand cross-link repair. Science 2010, 329:693-696.
67. Bhoumik A., Takahashi S., Breitweiser W., Shiloh Y., Jones N., Ronai Z. ATM-dependent phosphorylation of ATF2 is required for the DNA damage response. Mol. Cell. 2005, 18:577-587.