HERC2-USP20 axis regulates DNA damage checkpoint through Claspin

Nucleic Acids Research

Volumn 42, Issue 21, 2014, Pages 13110-13121

  Yuan, Jian ^a   Luo, Kuntian ^a   Deng, Min ^b   Li, Yunhui ^a   Yin, Ping ^b   Gao, Bowen ^b   Fang, Yuan ^b   Wu, Puqiang ^b   Liu, Tongzheng ^a,b   Lou, Zhenkun ^b  

^a TONGJI UNIVERSITY SCHOOL OF MEDICINE   (China)

^b MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; ATR PROTEIN, HUMAN; CLSPN PROTEIN, HUMAN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; HERC2 PROTEIN, HUMAN; PROTEINASE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TUMOR SUPPRESSOR PROTEIN; UBIQUITIN THIOLESTERASE; USP20 PROTEIN, HUMAN; USP20 PROTEIN, MOUSE;

ANIMAL; CELL CULTURE; CELL CYCLE CHECKPOINT; CELL LINE; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; GENETICS; HEK293 CELL LINE; HUMAN; METABOLISM; MOUSE; NUDE MOUSE; PHOSPHORYLATION; PHYSIOLOGY;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; ATAXIA TELANGIECTASIA MUTATED PROTEINS; CELL CYCLE CHECKPOINTS; CELL LINE; CELLS, CULTURED; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; ENDOPEPTIDASES; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HEK293 CELLS; HUMANS; MICE; MICE, NUDE; PHOSPHORYLATION; TUMOR SUPPRESSOR PROTEINS; UBIQUITIN THIOLESTERASE;

EID: 84941109316     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku1034     Document Type: Article

References (48)

1. Ciccia, A. And Elledge, S. J. (2010) The DNA damage response: making it safe to play with knives. Mol. Cell, 40, 179-204.
2. Jackson, S. P. And Bartek, J. (2009) The DNA-damage response in human biology and disease. Nature, 461, 1071-1078.
3. Lukas, J., Lukas, C. And Bartek, J. (2011) More than just a focus: The chromatin response to DNA damage and its role in genome integrity maintenance. Nat. Cell. Biol., 13, 1161-1169.
4. Huen, M. S. And Chen, J. (2010) Assembly of checkpoint and repair machineries at DNA damage sites. Trends Biochem. Sci., 35, 101-108.
5. Downs, J. A., Nussenzweig, M. C. And Nussenzweig, A. (2007) Chromatin dynamics and the preservation of genetic information. Nature, 447, 951-958.
6. Bassermann, F. And Pagano, M. (2010) Dissecting the role of ubiquitylation in the DNA damage response checkpoint in G2. Cell Death Diff., 17, 78-85.
7. Kastan, M. B. And Bartek, J. (2004) Cell-cycle checkpoints and cancer. Nature, 432, 316-323.
8. Matsuoka, S., Ballif, B. A., Smogorzewska, A., McDonald, E. R. 3rd, Hurov, K. E., Luo, J., Bakalarski, C. E., Zhao, Z., Solimini, N., Lerenthal, Y. et al. (2007) ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science, 316, 1160-1166.
9. Stokes, M. P., Rush, J., Macneill, J., Ren, J. M., Sprott, K., Nardone, J., Yang, V., Beausoleil, S. A., Gygi, S. P., Livingstone, M. et al. (2007) Profiling of UV-induced ATM/ATR signaling pathways. Proc. Natl. Acad. Sci. U. S. A., 104, 19855-19860.
10. Shiloh, Y. And Ziv, Y. (2013) The ATM protein kinase: regulating the cellular response to genotoxic stress, and more. Nat. Rev. Mol. Cell Biol., 14, 197-210.
11. Zeman, M. K. And Cimprich, K. A. (2014) Causes and consequences of replication stress. Nat. Cell. Biol., 16, 2-9.
12. Flynn, R. L. And Zou, L. (2011) ATR: A master conductor of cellular responses to DNA replication stress. Trends Biochem. Sci., 36, 133-140.
13. Cortez, D., Guntuku, S., Qin, J. And Elledge, S. J. (2001) ATR and ATRIP: partners in checkpoint signaling. Science, 294, 1713-1716.
14. Byun, T. S., Pacek, M., Yee, M. C., Walter, J. C. And Cimprich, K. A. (2005) Functional uncoupling of MCM helicase and DNA polymerase activities activates the ATR-dependent checkpoint. Genes Dev., 19, 1040-1052.
15. Costanzo, V., Shechter, D., Lupardus, P. J., Cimprich, K. A., Gottesman, M. And Gautier, J. (2003) An ATR-and Cdc7-dependent DNA damage checkpoint that inhibits initiation of DNA replication. Mol. Cell, 11, 203-213.
16. Zou, L. And Elledge, S. J. (2003) Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science, 300, 1542-1548.
17. Bao, S., Lu, T., Wang, X., Zheng, H., Wang, L. E., Wei, Q., Hittelman, W. N. And Li, L. (2004) Disruption of the Rad9/Rad1/Hus1 (9-1-1) complex leads to checkpoint signaling and replication defects. Oncogene, 23, 5586-5593.
18. Ellison, V. And Stillman, B. (2003) Biochemical characterization of DNA damage checkpoint complexes: clamp loader and clamp complexes with specificity for 5-recessed DNA. PLoS Biol., 1, E33.
19. Zou, L., Cortez, D. And Elledge, S. J. (2002) Regulation of ATR substrate selection by Rad17-dependent loading of Rad9 complexes onto chromatin. Genes Dev., 16, 198-208.
20. Kumagai, A., Lee, J., Yoo, H. Y. And Dunphy, W. G. (2006) TopBP1 activates the ATR-ATRIP complex. Cell, 124, 943-955.
21. Mordes, D. A., Glick, G. G., Zhao, R. And Cortez, D. (2008) TopBP1 activates ATR through ATRIP and a PIKK regulatory domain. Genes Dev., 22, 1478-1489.
22. Navadgi-Patil, V. M. And Burgers, P. M. (2009) The unstructured C-terminal tail of the 9-1-1 clamp subunit Ddc1 activates Mec1/ATR via two distinct mechanisms. Mol. Cell, 36, 743-753.
23. Delacroix, S., Wagner, J. M., Kobayashi, M., Yamamoto, K. And Karnitz, L. M. (2007) The Rad9-Hus1-Rad1 (9-1-1) clamp activates checkpoint signaling via TopBP1. Genes Dev., 21, 1472-1477.
24. Lee, J. And Dunphy, W. G. (2010) Rad17 plays a central role in establishment of the interaction between TopBP1 and the Rad9-Hus1-Rad1 complex at stalled replication forks. Mol. Biol. Cell, 21, 926-935.
25. Liu, S., Shiotani, B., Lahiri, M., Marechal, A., Tse, A., Leung, C. C., Glover, J. N., Yang, X. H. And Zou, L. (2011) ATR autophosphorylation as a molecular switch for checkpoint activation. Mol. Cell, 43, 192-202.
26. Wang, J., Gong, Z. And Chen, J. (2011) MDC1 collaborates with TopBP1 in DNA replication checkpoint control. J. Cell Biol., 193, 267-273.
27. Liu, S., Bekker-Jensen, S., Mailand, N., Lukas, C., Bartek, J. And Lukas, J. (2006) Claspin operates downstream of TopBP1 to direct ATR signaling towards Chk1 activation. Mol. Cell. Biol., 26, 6056-6064.
28. Wang, X., Zou, L., Lu, T., Bao, S., Hurov, K. E., Hittelman, W. N., Elledge, S. J. And Li, L. (2006) Rad17 phosphorylation is required for claspin recruitment and Chk1 activation in response to replication stress. Mol. Cell, 23, 331-341.
29. Kumagai, A. And Dunphy, W. G. (2003) Repeated phosphopeptide motifs in Claspin mediate the regulated binding of Chk1. Nat. Cell. Biol., 5, 161-165.
30. Chini, C. C., Wood, J. And Chen, J. (2006) Chk1 is required to maintain claspin stability. Oncogene, 25, 4165-4171.
31. Jackson, S. P. And Durocher, D. (2013) Regulation of DNA damage responses by ubiquitin and SUMO. Mol. Cell, 49, 795-807.
32. Jacq, X., Kemp, M., Martin, N. M. And Jackson, S. P. (2013) Deubiquitylating enzymes and DNA damage response pathways. Cell Biochem. Biophys., 67, 25-43.
33. Messick, T. E. And Greenberg, R. A. (2009) The ubiquitin landscape at DNA double-strand breaks. J. Cell Biol., 187, 319-326.
34. Bekker-Jensen, S. And Mailand, N. (2011) The ubiquitin-and SUMO-dependent signaling response to DNA double-strand breaks. FEBS Lett., 585, 2914-2919.
35. Shim, H., Dolde, C., Lewis, B. C., Wu, C. S., Dang, G., Jungmann, R. A., Dalla-Favera, R. And Dang, C. V. (1997) c-Myc transactivation of LDH-A: implications for tumor metabolism and growth. Proc. Natl. Acad. Sci. U. S. A., 94, 6658-6663.
36. Wilkinson, K. D. (1997) Regulation of ubiquitin-dependent processes by deubiquitinating enzymes. FASEB J., 11, 1245-1256.
37. Bassermann, F., Frescas, D., Guardavaccaro, D., Busino, L., Peschiaroli, A. And Pagano, M. (2008) The Cdc14B-Cdh1-Plk1 axis controls the G2 DNA-damage-response checkpoint. Cell, 134, 256-267.
38. Peschiaroli, A., Dorrello, N. V., Guardavaccaro, D., Venere, M., Halazonetis, T., Sherman, N. E. And Pagano, M. (2006) SCFbetaTrCP-mediated degradation of Claspin regulates recovery from the DNA replication checkpoint response. Mol. Cell, 23, 319-329.
39. Mailand, N., Bekker-Jensen, S., Bartek, J. And Lukas, J. (2006) Destruction of Claspin by SCFbetaTrCP restrains Chk1 activation and facilitates recovery from genotoxic stress. Mol. Cell, 23, 307-318.
40. Bekker-Jensen, S., Rendtlew Danielsen, J., Fugger, K., Gromova, I., Nerstedt, A., Lukas, C., Bartek, J., Lukas, J. And Mailand, N. (2010) HERC2 coordinates ubiquitin-dependent assembly of DNA repair factors on damaged chromosomes. Nat. Cell. Biol., 12, 80-86; supp. 81-12.
41. Wu, W., Sato, K., Koike, A., Nishikawa, H., Koizumi, H., Venkitaraman, A. R. And Ohta, T. (2010) HERC2 is an E3 ligase that targets BRCA1 for degradation. Cancer Res., 70, 6384-6392.
42. Kang, T. H., Reardon, J. T. And Sancar, A. (2011) Regulation of nucleotide excision repair activity by transcriptional and post-transcriptional control of the XPA protein. Nucleic Acids Res., 39, 3176-3187.
43. Curcio-Morelli, C., Zavacki, A. M., Christofollete, M., Gereben, B., de Freitas, B. C., Harney, J. W., Li, Z., Wu, G. And Bianco, A. C. (2003) Deubiquitination of type 2 iodothyronine deiodinase by von Hippel-Lindau protein-interacting deubiquitinating enzymes regulates thyroid hormone activation. J. Clin. Investig., 112, 189-196.
44. Li, Z., Wang, D., Messing, E. M. And Wu, G. (2005) VHL protein-interacting deubiquitinating enzyme 2 deubiquitinates and stabilizes HIF-1alpha. EMBO Rep., 6, 373-378.
45. Yasunaga, J., Lin, F. C., Lu, X. And Jeang, K. T. (2011) Ubiquitin-specific peptidase 20 targets TRAF6 and human T cell leukemia virus type 1 tax to negatively regulate NF-kappaB signaling. J. Virol., 85, 6212-6219.
46. Berthouze, M., Venkataramanan, V., Li, Y. And Shenoy, S. K. (2009) The deubiquitinases USP33 and USP20 coordinate beta2 adrenergic receptor recycling and resensitization. EMBO J., 28, 1684-1696.
47. Shanmugam, I., Abbas, M., Ayoub, F., Mirabal, S., Bsaili, M., Caulder, E. K., Weinstock, D. M., Tomkinson, A. E., Hromas, R. And Shaheen, M. (2014) Ubiquitin-specific peptidase 20 regulates Rad17 stability, checkpoint kinase 1 phosphorylation and DNA repair by homologous recombination. J. Biol. Chem., 289, 22739-22748.
48. Danielsen, J. R., Povlsen, L. K., Villumsen, B. H., Streicher, W., Nilsson, J., Wikstrom, M., Bekker-Jensen, S. And Mailand, N. (2012) DNA damage-inducible SUMOylation of HERC2 promotes RNF8 binding via a novel SUMO-binding Zinc finger. J. Cell Biol., 197, 179-187.