FBH1 promotes DNA double-strand breakage and apoptosis in response to DNA replication stress

Journal of Cell Biology

Volumn 200, Issue 2, 2013, Pages 141-149

  Jeong, Yeon Tae ^a   Rossi, Mario ^a   Cermak, Lukas ^a,b   Saraf, Anita ^c   Florens, Laurence ^c   Washburn, Michael P ^c,d   Sung, Patrick ^e   Schildkraut, Carl ^f   Pagano, Michele ^a,b  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c STOWERS INSTITUTE FOR MEDICAL RESEARCH   (United States)

^d UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^e YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA BINDING PROTEIN; DOUBLE STRANDED DNA; FBH1 PROTEIN; HELICASE; PROTEIN; PROTEIN P53; REPLICATION FACTOR A; REPLICATION FACTOR A2; SINGLE STRANDED DNA; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; DNA DAMAGE CHECKPOINT; DNA REPLICATION; DOUBLE STRANDED DNA BREAK; ENZYME ACTIVITY; GENOMIC INSTABILITY; GENOTOXICITY; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION;

APOPTOSIS; DNA BREAKS, DOUBLE-STRANDED; DNA HELICASES; DNA REPLICATION; DNA-BINDING PROTEINS; GENOMIC INSTABILITY; HEK293 CELLS; HELA CELLS; HUMANS; HYDROXYUREA; PHOSPHORYLATION; PROTEIN STRUCTURE, TERTIARY; REPLICATION PROTEIN A; S PHASE; STRESS, PHYSIOLOGICAL; ULTRAVIOLET RAYS;

EID: 84873042958     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201209002     Document Type: Article

References (31)

1. Barber, L.J., J.L. Youds, J.D. Ward, M.J. McIlwraith, N.J. O'Neil, M.I. Petalcorin, J.S. Martin, S.J. Collis, S.B. Cantor, M. Auclair, et al. 2008. RTEL1 maintains genomic stability by suppressing homologous recombination. Cell. 135:261-271. http://dx.doi.org/10.1016/j.cell.2008.08.016
2. Binz, S.K., A.M. Sheehan, and M.S. Wold. 2004. Replication protein A phosphorylation and the cellular response to DNA damage. DNA Repair (Amst.). 3:1015-1024. http://dx.doi.org/10.1016/j.dnarep.2004.03.028
3. Busino, L., F. Bassermann, A. Maiolica, C. Lee, P.M. Nolan, S.I. Godinho, G.F. Draetta, and M. Pagano. 2007. SCFFbxl3 controls the oscillation of the circadian clock by directing the degradation of cryptochrome proteins. Science. 316:900-904. http://dx.doi.org/10.1126/science.1141194
4. Chiolo, I., M. Saponaro, A. Baryshnikova, J.H. Kim, Y.S. Seo, and G. Liberi. 2007. The human F-Box DNA helicase FBH1 faces Saccharomyces cerevisiae Srs2 and postreplication repair pathway roles. Mol. Cell. Biol. 27:7439-7450. http://dx.doi.org/10.1128/MCB.00963-07
5. Chu, W.K., and I.D. Hickson. 2009. RecQ helicases: multifunctional genome caretakers. Nat. Rev. Cancer. 9:644-654. http://dx.doi.org/10.1038/nrc2682
6. Ciccia, A., and S.J. Elledge. 2010. The DNA damage response: making it safe to play with knives. Mol. Cell. 40:179-204. http://dx.doi.org/10.1016/j.molcel.2010.09.019
7. Cleaver, J.E., L. Feeney, and I. Revet. 2011. Phosphorylated H2Ax is not an unambiguous marker for DNA double-strand breaks. Cell Cycle. 10:3223- 3224. http://dx.doi.org/10.4161/cc.10.19.17448
8. D'Angiolella, V., V. Donato, S. Vijayakumar, A. Saraf, L. Florens, M.P. Washburn, B. Dynlacht, and M. Pagano. 2010. SCF(Cyclin F) controls centrosome homeostasis and mitotic fidelity through CP110 degradation. Nature. 466:138-142. http://dx.doi.org/10.1038/nature09140
9. Eng, J., A.L. McCormack, and J.R. Yates III. 1994. An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database. J. Amer. Mass Spectrom. 5:976-989. http://dx.doi.org/10.1016/1044-0305(94)80016-2
10. Feng, W., S. DiRienzi, M. Raghuraman, and B. Brewer. 2011. Replication stressinduced chromosome breakage is correlated with replication fork progression and is preceded by single-stranded DNA formation. Genes, Genomes. Genetics. 1:327-335.
11. Florens, L., and M.P. Washburn. 2006. Proteomic analysis by multidimensional protein identification technology. Methods Mol. Biol. 328:159-175.
12. Fugger, K., M. Mistrik, J.R. Danielsen, C. Dinant, J. Falck, J. Bartek, J. Lukas, and N. Mailand. 2009. Human Fbh1 helicase contributes to genome maintenance via pro- and anti-recombinase activities. J. Cell Biol. 186: 655-663. http://dx.doi.org/10.1083/jcb.200812138
13. Kim, J., J.H. Kim, S.H. Lee, D.H. Kim, H.Y. Kang, S.H. Bae, Z.Q. Pan, and Y.S. Seo. 2002. The novel human DNA helicase hFBH1 is an F-box protein. J. Biol. Chem. 277:24530-24537. http://dx.doi.org/10.1074/jbc.M201612200
14. Kim, J.H., J. Kim, D.H. Kim, G.H. Ryu, S.H. Bae, and Y.S. Seo. 2004. SCFhFBH1 can act as helicase and E3 ubiquitin ligase. Nucleic Acids Res. 32:2287-2297. http://dx.doi.org/10.1093/nar/gkh534
15. Kohzaki, M., A. Hatanaka, E. Sonoda, M. Yamazoe, K. Kikuchi, N. Vu Trung, D. Szüts, J.E. Sale, H. Shinagawa, M. Watanabe, and S. Takeda. 2007. Cooperative roles of vertebrate Fbh1 and Blm DNA helicases in avoidance of crossovers during recombination initiated by replication fork collapse. Mol. Cell. Biol. 27:2812-2820. http://dx.doi.org/10.1128/MCB.02043-06
16. Laulier, C., A. Cheng, N. Huang, and J.M. Stark. 2010. Mammalian Fbh1 is important to restore normal mitotic progression following decatenation stress. DNA Repair (Amst.). 9:708-717. http://dx.doi.org/10.1016/j.dnarep.2010.03.011
17. Lawrence, C.L., N. Jones, and C.R. Wilkinson. 2009. Stress-induced phosphorylation of S. pombe Atf1 abrogates its interaction with F box protein Fbh1. Curr. Biol. 19:1907-1911. http://dx.doi.org/10.1016/j.cub.2009.09.044
18. MacCoss, M.J., W.H. McDonald, A. Saraf, R. Sadygov, J.M. Clark, J.J. Tasto, K.L. Gould, D. Wolters, M. Washburn, A. Weiss, et al. 2002. Shotgun identification of protein modifications from protein complexes and lens tissue. Proc. Natl. Acad. Sci. USA. 99:7900-7905. http://dx.doi.org/10.1073/pnas.122231399
19. Manthey, K.C., S. Opiyo, J.G. Glanzer, D. Dimitrova, J. Elliott, and G.G. Oakley. 2007. NBS1 mediates ATR-dependent RPA hyperphosphorylation following replication-fork stall and collapse. J. Cell Sci. 120:4221-4229. http://dx.doi.org/10.1242/jcs.004580
20. Moldovan, G.L., D. Dejsuphong, M.I. Petalcorin, K. Hofmann, S. Takeda, S.J. Boulton, and A.D. D'Andrea. 2012. Inhibition of homologous recombination by the PCNA-interacting protein PARI. Mol. Cell. 45:75-86. http://dx.doi.org/10.1016/j.molcel.2011.11.010
21. Morishita, T., F. Furukawa, C. Sakaguchi, T. Toda, A.M. Carr, H. Iwasaki, and H. Shinagawa. 2005. Role of the Schizosaccharomyces pombe F-Box DNA helicase in processing recombination intermediates. Mol. Cell. Biol. 25:8074-8083. http://dx.doi.org/10.1128/MCB.25.18.8074-8083.2005
22. Osman, F., J. Dixon, A.R. Barr, and M.C. Whitby. 2005. The F-Box DNA helicase Fbh1 prevents Rhp51-dependent recombination without mediator proteins. Mol. Cell. Biol. 25:8084-8096. http://dx.doi.org/10.1128/MCB.25.18.8084-8096.2005
23. Park, J.S., E. Choi, S.H. Lee, C. Lee, and Y.S. Seo. 1997. A DNA helicase from Schizosaccharomyces pombe stimulated by single-stranded DNA-binding protein at low ATP concentration. J. Biol. Chem. 272:18910-18919. http://dx.doi.org/10.1074/jbc.272.30.18910
24. Petermann, E., M.L. Orta, N. Issaeva, N. Schultz, and T. Helleday. 2010. Hydroxyurea-stalled replication forks become progressively inactivated and require two different RAD51-mediated pathways for restart and repair. Mol. Cell. 37:492-502. http://dx.doi.org/10.1016/j.molcel.2010.01.021
25. Raderschall, E., E.I. Golub, and T. Haaf. 1999. Nuclear foci of mammalian recombination proteins are located at single-stranded DNA regions formed after DNA damage. Proc. Natl. Acad. Sci. USA. 96:1921-1926. http://dx.doi.org/10.1073/pnas.96.5.1921
26. Saintigny, Y., F. Delacǒte, G. Vareàs, F. Petitot, S. Lambert, D. Averbeck, and B.S. Lopez. 2001. Characterization of homologous recombination induced by replication inhibition in mammalian cells. EMBO J. 20:3861- 3870. http://dx.doi.org/10.1093/emboj/20.14.3861
27. Sakaguchi, C., T. Morishita, H. Shinagawa, and T. Hishida. 2008. Essential and distinct roles of the F-box and helicase domains of Fbh1 in DNA damage repair. BMC Mol. Biol. 9:27. http://dx.doi.org/10.1186/1471-2199-9-27
28. Sirbu, B.M., F.B. Couch, J.T. Feigerle, S. Bhaskara, S.W. Hiebert, and D. Cortez. 2011. Analysis of protein dynamics at active, stalled, and collapsed replication forks. Genes Dev. 25:1320-1327. http://dx.doi.org/10.1101/gad.2053211
29. Tabb, D.L., W.H. McDonald, and J.R. Yates III. 2002. DTASelect and Contrast: tools for assembling and comparing protein identifications from shotgun proteomics. J. Proteome Res. 1:21-26. http://dx.doi.org/10.1021/pr015504q
30. Washburn, M.P., D. Wolters, and J.R. Yates III. 2001. Large-scale analysis of the yeast proteome by multidimensional protein identification technology. Nat. Biotechnol. 19:242-247. http://dx.doi.org/10.1038/85686
31. Zhang, Y., Z. Wen, M.P. Washburn, and L. Florens. 2010. Refinements to label free proteome quantitation: how to deal with peptides shared by multiple proteins. Anal. Chem. 82:2272-2281. http://dx.doi.org/10.1021/ac9023999