Drosophila Claspin is required for the G2 arrest that is induced by DNA replication stress but not by DNA double-strand breaks

DNA Repair

Volumn 11, Issue 9, 2012, Pages 741-752

  Lee, Eun Mi ^a   Trinh, Tram Thi Bich ^a   Shim, Hee Jin ^a   Park, Suk Young ^a   Nguyen, Trang Thi Thu ^a   Kim, Min Joo ^a   Song, Young Han ^a  

^a Hallym University   (South Korea)

Author keywords

Claspin; Drosophila; G2 arrest; Hydroxyurea; Ionizing radiation; Replication checkpoint

Indexed keywords

ATR PROTEIN; CHECKPOINT KINASE 1; CLASPIN; DOUBLE STRANDED DNA; HYDROXYUREA; PROTEIN KINASE; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL CYCLE ARREST; CELL CYCLE G2 PHASE; CONTROLLED STUDY; DNA DAMAGE; DNA REPLICATION; DNA REPLICATION STRESS; DOUBLE STRANDED DNA BREAK; DROSOPHILA; EMBRYO; EMBRYO DEVELOPMENT; IONIZING RADIATION; LARVA; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; STRESS;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CELL CYCLE PROTEINS; DNA; DNA BREAKS, DOUBLE-STRANDED; DNA REPLICATION; DROSOPHILA; DROSOPHILA PROTEINS; G2 PHASE CELL CYCLE CHECKPOINTS; GAMMA RAYS; HYDROXYUREA; PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; STRESS, PHYSIOLOGICAL;

EID: 84865098829     PISSN: 15687864     EISSN: 15687856     Source Type: Journal    
DOI: 10.1016/j.dnarep.2012.06.007     Document Type: Article

References (40)

1. Nyberg K.A., Michelson R.J., Putnam C.W., Weinert T.A. Toward maintaining the genome: DNA damage and replication checkpoints. Annu. Rev. Genet. 2002, 36:617-656.
2. Cortez D., Guntuku S., Qin J., Elledge S.J. ATR and ATRIP: partners in checkpoint signaling. Science 2001, 294:1713-1716.
3. Liu S., Bekker-Jensen S., Mailand N., Lukas C., Bartek J., Lukas J. Claspin operates downstream of TopBP1 to direct ATR signaling towards Chk1 activation. Mol. Cell. Biol. 2006, 26:6056-6064.
4. Kumagai A., Dunphy W.G., Claspin a novel protein required for the activation of Chk1 during a DNA replication checkpoint response in Xenopus egg extracts. Mol. Cell 2000, 6:839-849.
5. Chini C.C., Chen J. Repeated phosphopeptide motifs in human Claspin are phosphorylated by Chk1 and mediate Claspin function. J. Biol. Chem. 2006, 281:33276-33282.
6. Kumagai A., Dunphy W.G. Repeated phosphopeptide motifs in Claspin mediate the regulated binding of Chk1. Nat. Cell Biol. 2003, 5:161-165.
7. Chini C.C., Chen J. Human claspin is required for replication checkpoint control. J. Biol. Chem. 2003, 278:30057-30062.
8. Petermann E., Helleday T., Caldecott K.W. Claspin promotes normal replication fork rates in human cells. Mol. Biol. Cell 2008, 19:2373-2378.
9. Yoo H.Y., Kumagai A., Shevchenko A., Dunphy W.G. Adaptation of a DNA replication checkpoint response depends upon inactivation of Claspin by the Polo-like kinase. Cell 2004, 117:575-588.
10. Mamely I., van Vugt M.A., Smits V.A., Semple J.I., Lemmens B., Perrakis A., Medema R.H., Freire R. Polo-like kinase-1 controls proteasome-dependent degradation of Claspin during checkpoint recovery. Curr. Biol. 2006, 16:1950-1955.
11. Mailand N., Bekker-Jensen S., Bartek J., Lukas J. Destruction of Claspin by SCFbetaTrCP restrains Chk1 activation and facilitates recovery from genotoxic stress. Mol. Cell 2006, 23:307-318.
12. Peschiaroli A., Dorrello N.V., Guardavaccaro D., Venere M., Halazonetis T., Sherman N.E., Pagano M. SCFbetaTrCP-mediated degradation of Claspin regulates recovery from the DNA replication checkpoint response. Mol. Cell 2006, 23:319-329.
13. Song Y.H. Drosophila melanogaster: a model for the study of DNA damage checkpoint response. Mol. Cells 2005, 19:167-179.
14. Smolik S., Jones K. Drosophila dCBP is involved in establishing the DNA replication checkpoint. Mol. Cell. Biol. 2007, 27:135-146.
15. de Vries H.I., Uyetake L., Lemstra W., Brunsting J.F., Su T.T., Kampinga H.H., Sibon O.C. Grp/DChk1 is required for G2-M checkpoint activation in Drosophila S2 cells, whereas Dmnk/DChk2 is dispensable. J. Cell Sci. 2005, 118:1833-1842.
16. Kondo S., Perrimon N. A genome-wide RNAi screen identifies core components of the G-M DNA damage checkpoint. Sci. Signal. 2011, 4:rs1.
17. Brodsky M.H., Sekelsky J.J., Tsang G., Hawley R.S.G.M. Rubin, mus304 encodes a novel DNA damage checkpoint protein required during Drosophila development. Genes Dev. 2000, 14:666-678.
18. Sibon O.C., Laurencon A., Hawley R., Theurkauf W.E. The Drosophila ATM homologue Mei-41 has an essential checkpoint function at the midblastula transition. Curr. Biol. 1999, 9:302-312.
19. Sibon O.C., Stevenson V.A., Theurkauf W.E. DNA-replication checkpoint control at the Drosophila midblastula transition. Nature 1997, 388:93-97.
20. Takada S., Kelkar A., Theurkauf W.E. Drosophila checkpoint kinase 2 couples centrosome function and spindle assembly to genomic integrity. Cell 2003, 113:87-99.
21. Song Y.H., Mirey G., Betson M., Haber D.A., Settleman J. The Drosophila ATM ortholog, dATM, mediates the response to ionizing radiation and to spontaneous DNA damage during development. Curr. Biol. 2004, 14:1354-1359.
22. LaRocque J.R., Jaklevic B., Su T.T., Sekelsky J. Drosophila ATR in double-strand break repair. Genetics 2007, 175:1023-1033.
23. Rothwell W.F., Sullivan W. Fluorescent analysis of Drosophila embryos. Drosophila Protocols 2000, 141-157. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. W. Sullivan, M. Ashburner, R.S. Hawley (Eds.).
24. Krause S.A., Loupart M.L., Vass S., Schoenfelder S., Harrison S., Heck M.M. Loss of cell cycle checkpoint control in Drosophila Rfc4 mutants. Mol. Cell. Biol. 2001, 21:5156-5168.
25. Park S.Y., Song Y.H. Genetic screen for genes involved in Chk2 signaling in Drosophila. Mol. Cells 2008, 26:350-355.
26. Banga S.S., Shenkar R., Boyd J.B. Hypersensitivity of Drosophila mei-41 mutants to hydroxyurea is associated with reduced mitotic chromosome stability. Mutat. Res. 1986, 163:157-165.
27. Purdy A., Uyetake L., Cordeiro M.G., Su T.T. Regulation of mitosis in response to damaged or incompletely replicated DNA require different levels of Grapes (Drosophila Chk1). J. Cell Sci. 2005, 118:3305-3315.
28. Sullivan W., Fogarty P., Theurkauf W. Mutations affecting the cytoskeletal organization of syncytial Drosophila embryos. Development 1993, 118:1245-1254.
29. Baker B.S., Carpenter A.T., Ripoll P. The utilization during mitotic cell division of loci controlling meiotic recombination and disjunction in Drosophila melanogaster. Genetics 1978, 90:531-578.
30. Chini C.C., Chen J. Claspin, a regulator of Chk1 in DNA replication stress pathway. DNA Repair (Amst.) 2004, 3:1033-1037.
31. Brodsky M.H., Weinert B.T., Tsang G., Rong Y.S., McGinnis N.M., Golic K.G., Rio D.C., Rubin G.M. Drosophila melanogaster MNK/Chk2 and p53 regulate multiple DNA repair and apoptotic pathways following DNA damage. Mol. Cell. Biol. 2004, 24:1219-1231.
32. Kim S.M., Kumagai A., Lee J., Dunphy W.G. Phosphorylation of Chk1 by ATM- and Rad3-related (ATR) in Xenopus egg extracts requires binding of ATRIP to ATR but not the stable DNA-binding or coiled-coil domains of ATRIP. J. Biol. Chem. 2005, 280:38355-38364.
33. Yan S., Lindsay H.D., Michael W.M. Direct requirement for Xmus101 in ATR-mediated phosphorylation of Claspin bound Chk1 during checkpoint signaling. J. Cell Biol. 2006, 173:181-186.
34. Ball H.L., Cortez D. ATRIP oligomerization is required for ATR-dependent checkpoint signaling. J. Biol. Chem. 2005, 280:31390-31396.
35. Yoo H.Y., Jeong S.Y., Dunphy W.G. Site-specific phosphorylation of a checkpoint mediator protein controls its responses to different DNA structures. Genes Dev. 2006, 20:772-783.
36. Clarke C.A., Clarke P.R. DNA-dependent phosphorylation of Chk1 and Claspin in a human cell-free system. Biochem. J. 2005, 388:705-712.
37. Smits V.A., Warmerdam D.O., Martin Y., Freire R. Mechanisms of ATR-mediated checkpoint signalling. Front. Biosci. 2010, 15:840-853.
38. Lo T., Pellegrini L., Venkitaraman A.R., Blundell T.L. Sequence fingerprints in BRCA2 and RAD51: implications for DNA repair and cancer. DNA Repair (Amst.) 2003, 2:1015-1028.
39. Meng Z., Capalbo L., Glover D.M., Dunphy W.G. Role for casein kinase 1 in the phosphorylation of Claspin on critical residues necessary for the activation of Chk1. Mol. Biol. Cell 2011, 22:2834-2847.
40. Lin S.Y., Li K., Stewart G.S., Elledge S.J. Human Claspin works with BRCA1 to both positively and negatively regulate cell proliferation. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:6484-6489.