SUMO-targeted ubiquitin ligase RNF4 plays a critical role in preventing chromosome loss

Genes to Cells

Volumn 19, Issue 10, 2014, Pages 743-754

  Hirota, Kouji ^a,b   Tsuda, Masataka ^a   Murai, Junko ^a   Takagi, Tokiyo ^b   Keka, Islam Shamima ^a   Narita, Takeo ^a   Fujita, Mari ^a   Sasanuma, Hiroyuki ^a   Kobayashi, Junya ^c   Takeda, Shunichi ^a  

^a KYOTO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b TOKYO METROPOLITAN UNIVERSITY   (Japan)

^c KYOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

SUMO PROTEIN; UBIQUITIN PROTEIN LIGASE;

ANAPHASE; ANIMAL; CELL LINE; CELL PROLIFERATION; CELL SURVIVAL; CHICKEN; CHROMOSOME ABERRATION; CHROMOSOME SEGREGATION; DNA DAMAGE; DNA REPLICATION; GENETICS; M PHASE CELL CYCLE CHECKPOINT; METABOLISM; MUTATION;

ANAPHASE; ANIMALS; CELL LINE; CELL PROLIFERATION; CELL SURVIVAL; CHICKENS; CHROMOSOME ABERRATIONS; CHROMOSOME SEGREGATION; DNA DAMAGE; DNA REPLICATION; M PHASE CELL CYCLE CHECKPOINTS; MUTATION; SMALL UBIQUITIN-RELATED MODIFIER PROTEINS; UBIQUITIN-PROTEIN LIGASES;

EID: 84908249676     PISSN: 13569597     EISSN: 13652443     Source Type: Journal    
DOI: 10.1111/gtc.12173     Document Type: Article

References (46)

1. Adachi, N., Suzuki, H., Iiizumi, S. & Koyama, H. (2003) Hypersensitivity of nonhomologous DNA end-joining mutants to VP-16 and ICRF-193: implications for the repair of topoisomerase II-mediated DNA damage. J. Biol. Chem. 278, 35897-35902.
2. Azuma, Y., Arnaoutov, A. & Dasso, M. (2003) SUMO-2/3 regulates topoisomerase II in mitosis. J. Cell Biol. 163, 477-487.
3. Bachant, J., Alcasabas, A., Blat, Y., Kleckner, N. & Elledge, S.J. (2002) The SUMO-1 isopeptidase Smt4 is linked to centromeric cohesion through SUMO-1 modification of DNA topoisomerase II. Mol. Cell 9, 1169-1182.
4. Bakkenist, C.J. & Kastan, M.B. (2003) DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 421, 499-506.
5. Brunet, S. & Vernos, I. (2001) Chromosome motors on the move. From motion to spindle checkpoint activity. EMBO Rep. 2, 669-673.
6. Buerstedde, J.M. & Takeda, S. (1991) Increased ratio of targeted to random integration after transfection of chicken B cell lines. Cell 67, 179-188.
7. Canman, C.E., Lim, D.S., Cimprich, K.A., Taya, Y., Tamai, K., Sakaguchi, K., Appella, E., Kastan, M.B. & Siliciano, J.D. (1998) Activation of the ATM kinase by ionizing radiation and phosphorylation of p53. Science 281, 1677-1679.
8. Downes, C.S., Mullinger, A.M. & Johnson, R.T. (1991) Inhibitors of DNA topoisomerase II prevent chromatid separation in mammalian cells but do not prevent exit from mitosis. Proc. Natl Acad. Sci. USA 88, 8895-8899.
9. Era, S., Abe, T., Arakawa, H., Kobayashi, S., Szakal, B., Yoshikawa, Y., Motegi, A., Takeda, S. & Branzei, D. (2012) The SUMO protease SENP1 is required for cohesion maintenance and mitotic arrest following spindle poison treatment. Biochem. Biophys. Res. Commun. 426, 310-316.
10. Field, J.J., Kanakkanthara, A. & Miller, J.H. (2014) Microtubule-targeting agents are clinically successful due to both mitotic and interphase impairment of microtubule function. Bioorg. Med. Chem. DOI: 10.1016/j.bmc.2014.02.035.
11. Fujita, M., Sasanuma, H., Yamamoto, K.N., Harada, H., Kurosawa, A., Adachi, N., Omura, M., Hiraoka, M., Takeda, S. & Hirota, K. (2013) Interference in DNA replication can cause mitotic chromosomal breakage unassociated with double-strand breaks. PLoS One 8, e60043.
12. Galanty, Y., Belotserkovskaya, R., Coates, J. & Jackson, S.P. (2012) RNF4, a SUMO-targeted ubiquitin E3 ligase, promotes DNA double-strand break repair. Genes Dev. 26, 1179-1195.
13. Hirota, K., Sonoda, E., Kawamoto, T., Motegi, A., Masutani, C., Hanaoka, F., Szuts, D., Iwai, S., Sale, J.E., Lehmann, A. & Takeda, S. (2010) Simultaneous disruption of two DNA polymerases, Poleta and Polzeta, in Avian DT40 cells unmasks the role of Poleta in cellular response to various DNA lesions. PLoS Genet. 6, e1001151.
14. Ikegami, S., Taguchi, T., Ohashi, M., Oguro, M., Nagano, H. & Mano, Y. (1978) Aphidicolin prevents mitotic cell division by interfering with the activity of DNA polymerase-alpha. Nature 275, 458-460.
15. Ji, K., Kogame, T., Choi, K., Wang, X., Lee, J., Taniguchi, Y. & Takeda, S. (2009) A novel approach using DNA-repair-deficient chicken DT40 cell lines for screening and characterizing the genotoxicity of environmental contaminants. Environ. Health Perspect. 117, 1737-1744.
16. Jungmichel, S., Clapperton, J.A., Lloyd, J. et al. (2012) The molecular basis of ATM-dependent dimerization of the Mdc1 DNA damage checkpoint mediator. Nucleic Acids Res. 40, 3913-3928.
17. Kikuchi, K., Abdel-Aziz, H.I., Taniguchi, Y., Yamazoe, M., Takeda, S. & Hirota, K. (2009) Bloom DNA helicase facilitates homologous recombination between diverged homologous sequences. J. Biol. Chem. 284, 26360-26367.
18. Klein, H.L. (2001) Spontaneous chromosome loss in Saccharomyces cerevisiae is suppressed by DNA damage checkpoint functions. Genetics 159, 1501-1509.
19. Koc, A., Wheeler, L.J., Mathews, C.K. & Merrill, G.F. (2004) Hydroxyurea arrests DNA replication by a mechanism that preserves basal dNTP pools. J. Biol. Chem. 279, 223-230.
20. Kohzaki, M., Nishihara, K., Hirota, K., Sonoda, E., Yoshimura, M., Ekino, S., Butler, J.E., Watanabe, M., Halazonetis, T.D. & Takeda, S. (2010) DNA polymerases nu and theta are required for efficient immunoglobulin V gene diversification in chicken. J. Cell Biol. 189, 1117-1127.
21. Larsen, A.K., Skladanowski, A. & Bojanowski, K. (1996) The roles of DNA topoisomerase II during the cell cycle. Prog. Cell Cycle Res. 2, 229-239.
22. Lou, Z., Minter-Dykhouse, K., Wu, X. & Chen, J. (2003) MDC1 is coupled to activated CHK2 in mammalian DNA damage response pathways. Nature 421, 957-961.
23. Luke, A.M., Chastain, P.D., Pachkowski, B.F., Afonin, V., Takeda, S., Kaufman, D.G., Swenberg, J.A. & Nakamura, J. (2010) Accumulation of true single strand breaks and AP sites in base excision repair deficient cells. Mutat. Res. 694, 65-71.
24. Maede, Y., Shimizu, H., Fukushima, T., Kogame, T., Nakamura, T., Miki, T., Takeda, S., Pommier, Y. & Murai, J. (2014) Differential and common DNA repair pathways for topoisomerase I- and II-targeted drugs in a genetic DT40 repair cell screen panel. Mol. Cancer Ther. 13, 214-220.
25. Murai, J., Huang, S.Y., Das, B.B., Renaud, A., Zhang, Y., Doroshow, J.H., Ji, J., Takeda, S. & Pommier, Y. (2012) Trapping of PARP1 and PARP2 by Clinical PARP Inhibitors. Cancer Res. 72, 5588-5599.
26. Nagai, S., Davoodi, N. & Gasser, S.M. (2011) Nuclear organization in genome stability: SUMO connections. Cell Res. 21, 474-485.
27. Nasmyth, K. (2001) Disseminating the genome: joining, resolving, and separating sister chromatids during mitosis and meiosis. Annu. Rev. Genet. 35, 673-745.
28. Navadgi-Patil, V.M. & Burgers, P.M. (2009) A tale of two tails: activation of DNA damage checkpoint kinase Mec1/ATR by the 9-1-1 clamp and by Dpb11/TopBP1. DNA Repair 8, 996-1003.
29. Nicklas, R.B. (1997) How cells get the right chromosomes. Science 275, 632-637.
30. Paulovich, A.G., Toczyski, D.P. & Hartwell, L.H. (1997) When checkpoints fail. Cell 88, 315-321.
31. Pommier, Y. (2006) Topoisomerase I inhibitors: camptothecins and beyond. Nat. Rev. Cancer 6, 789-802.
32. Prudden, J., Pebernard, S., Raffa, G., Slavin, D.A., Perry, J.J., Tainer, J.A., McGowan, C.H. & Boddy, M.N. (2007) SUMO-targeted ubiquitin ligases in genome stability. EMBO J. 26, 4089-4101.
33. Qing, Y., Yamazoe, M., Hirota, K., Dejsuphong, D., Sakai, W., Yamamoto, K.N., Bishop, D.K., Wu, X. & Takeda, S. (2011) The epistatic relationship between BRCA2 and the other RAD51 mediators in homologous recombination. PLoS Genet. 7, e1002148.
34. Sarkaria, J.N., Tibbetts, R.S., Busby, E.C., Kennedy, A.P., Hill, D.E. & Abraham, R.T. (1998) Inhibition of phosphoinositide 3-kinase related kinases by the radiosensitizing agent wortmannin. Cancer Res. 58, 4375-4382.
35. Segurado, M. & Tercero, J.A. (2009) The S-phase checkpoint: targeting the replication fork. Biol. Cell 101, 617-627.
36. Shigechi, T., Tomida, J., Sato, K., Kobayashi, M., Eykelenboom, J.K., Pessina, F., Zhang, Y., Uchida, E., Ishiai, M., Lowndes, N.F., Yamamoto, K., Kurumizaka, H., Maehara, Y. & Takata, M. (2012) ATR-ATRIP kinase complex triggers activation of the Fanconi anemia DNA repair pathway. Cancer Res. 72, 1149-1156.
37. Sonoda, E., Sasaki, M.S., Buerstedde, J.M., Bezzubova, O., Shinohara, A., Ogawa, H., Takata, M., Yamaguchi-Iwai, Y. & Takeda, S. (1998) Rad51-deficient vertebrate cells accumulate chromosomal breaks prior to cell death. EMBO J. 17, 598-608.
38. Sun, H., Leverson, J.D. & Hunter, T. (2007) Conserved function of RNF4 family proteins in eukaryotes: targeting a ubiquitin ligase to SUMOylated proteins. EMBO J. 26, 4102-4112.
39. Takao, N., Kato, H., Mori, R., Morrison, C., Sonada, E., Sun, X., Shimizu, H., Yoshioka, K., Takeda, S. & Yamamoto, K. (1999) Disruption of ATM in p53-null cells causes multiple functional abnormalities in cellular response to ionizing radiation. Oncogene 18, 7002-7009.
40. Thompson, S.L., Bakhoum, S.F. & Compton, D.A. (2010) Mechanisms of chromosomal instability. Curr. Biol. 20, R285-R295.
41. Tomida, J., Itaya, A., Shigechi, T. et al. (2013) A novel interplay between the Fanconi anemia core complex and ATR-ATRIP kinase during DNA cross-link repair. Nucleic Acids Res. 41, 6930-6941.
42. Uemura, T., Ohkura, H., Adachi, Y., Morino, K., Shiozaki, K. & Yanagida, M. (1987) DNA topoisomerase II is required for condensation and separation of mitotic chromosomes in S. pombe. Cell 50, 917-925.
43. Uhlmann, F. (2003) Chromosome cohesion and separa-tion: from men and molecules. Curr. Biol. 13, R104-R114.
44. Cotterill S. (ed) (1999) Eukaryotic DNA replication - A Practical Approach. Oxford, UK Oxford University Press.
45. Yamamoto, K.N., Hirota, K., Kono, K., Takeda, S., Sakamuru, S., Xia, M., Huang, R., Austin, C.P., Witt, K.L. & Tice, R.R. (2011) Characterization of environmental chemicals with potential for DNA damage using isogenic DNA repair-deficient chicken DT40 cell lines. Environ. Mol. Mutagen. 52, 547-561.
46. Yin, Y., Seifert, A., Chua, J.S., Maure, J.F., Golebiowski, F. & Hay, R.T. (2012) SUMO-targeted ubiquitin E3 ligase RNF4 is required for the response of human cells to DNA damage. Genes Dev. 26, 1196-1208.