Claspin Operates Downstream of TopBP1 To Direct ATR Signaling towards Chk1 Activation

REFERENCES

• Abraham, R. T. 2001. Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes Dev. 15:2177–2196.
   PubMed Web of Science ®Google Scholar
• Alcasabas, A. A., A. J. Osborn, J. Bachant, F. Hu, P. J. Werler, K. Bousset, K. Furuya, J. F. Diffley, A. M. Carr, and S. J. Elledge. 2001. Mrc1 transduces signals of DNA replication stress to activate Rad53. Nat. Cell Biol. 3:958–965.
   PubMed Web of Science ®Google Scholar
• Ball, H. L., and D. Cortez. 2005. ATRIP oligomerization is required for ATR-dependent checkpoint signaling. J. Biol. Chem. 280:31390–31396.
   PubMed Web of Science ®Google Scholar
• Ball, H. L., J. S. Myers, and D. Cortez. 2005. ATRIP binding to replication protein A-single-stranded DNA promotes ATR-ATRIP localization but is dispensable for Chk1 phosphorylation. Mol. Biol. Cell 16:2372–2381.
   PubMed Web of Science ®Google Scholar
• Bartek, J., and J. Lukas. 2003. Chk1 and Chk2 kinases in checkpoint control and cancer. Cancer Cell 3:421–429.
   PubMed Web of Science ®Google Scholar
• Bekker-Jensen, S., C. Lukas, R. Kitagawa, F. Melander, M. B. Kastan, J. Bartek, and J. Lukas. 2006. Spatial organization of the mammalian genome surveillance machinery in response to DNA strand breaks. J. Cell Biol. 173:195–206.
   PubMed Web of Science ®Google Scholar
• Bekker-Jensen, S., C. Lukas, F. Melander, J. Bartek, and J. Lukas. 2005. Dynamic assembly and sustained retention of 53BP1 at the sites of DNA damage are controlled by Mdc1/NFBD1. J. Cell Biol. 170:201–211.
   PubMed Web of Science ®Google Scholar
• Busino, L., M. Donzelli, M. Chiesa, D. Guardavaccaro, D. Ganoth, N. V. Dorrello, A. Hershko, M. Pagano, and G. F. Draetta. 2003. Degradation of Cdc25A by beta-TrCP during S phase and in response to DNA damage. Nature 426:87–91.
   PubMed Web of Science ®Google Scholar
• Chini, C. C., and J. Chen. 2004. Claspin, a regulator of Chk1 in DNA replication stress pathway. DNA Repair 3:1033–1037.
   PubMed Web of Science ®Google Scholar
• Chini, C. C., and J. Chen. 2003. Human claspin is required for replication checkpoint control. J. Biol. Chem. 278:30057–30062.
   PubMed Web of Science ®Google Scholar
• Clarke, C. A., and P. R. Clarke. 2005. DNA-dependent phosphorylation of Chk1 and Claspin in a human cell-free system. Biochem. J. 388:705–712.
   PubMed Web of Science ®Google Scholar
• de Klein, A., M. Muijtjens, R. van Os, Y. Verhoeven, B. Smit, A. M. Carr, A. R. Lehmann, and J. H. Hoeijmakers. 2000. Targeted disruption of the cell-cycle checkpoint gene ATR leads to early embryonic lethality in mice. Curr. Biol. 10:479–482.
   PubMed Web of Science ®Google Scholar
• Falck, J., J. H. Petrini, B. R. Williams, J. Lukas, and J. Bartek. 2002. The DNA damage-dependent intra-S phase checkpoint is regulated by parallel pathways. Nat. Genet. 30:290–294.
   PubMed Web of Science ®Google Scholar
• Garcia, V., K. Furuya, and A. M. Carr. 2005. Identification and functional analysis of TopBP1 and its homologs. DNA Repair 4:1227–1239.
   PubMed Web of Science ®Google Scholar
• Jazayeri, A., J. Falck, C. Lukas, J. Bartek, G. C. Smith, J. Lukas, and S. P. Jackson. 2006. ATM- and cell cycle-dependent regulation of ATR in response to DNA double-strand breaks. Nat. Cell Biol. 8:37–45.
   PubMed Web of Science ®Google Scholar
• Jeong, S. Y., A. Kumagai, J. Lee, and W. G. Dunphy. 2003. Phosphorylated claspin interacts with a phosphate-binding site in the kinase domain of Chk1 during ATR-mediated activation. J. Biol. Chem. 278:46782–46788.
   PubMedGoogle Scholar
• Jiang, K., E. Pereira, M. Maxfield, B. Russell, D. M. Goudelock, and Y. Sanchez. 2003. Regulation of Chk1 includes chromatin association and 14-3-3 binding following phosphorylation on Ser-345. J. Biol. Chem. 278:25207–25217.
   PubMed Web of Science ®Google Scholar
• Jin, J., T. Shirogane, L. Xu, G. Nalepa, J. Qin, S. J. Elledge, and J. W. Harper. 2003. SCFbeta-TRCP links Chk1 signaling to degradation of the Cdc25A protein phosphatase. Genes Dev. 17:3062–3074.
   PubMed Web of Science ®Google Scholar
• Kim, J. E., S. A. McAvoy, D. I. Smith, and J. Chen. 2005. Human TopBP1 ensures genome integrity during normal S phase. Mol. Cell. Biol. 25:10907–10915.
   PubMedGoogle Scholar
• Kumagai, A., and W. G. Dunphy. 2000. Claspin, a novel protein required for the activation of Chk1 during a DNA replication checkpoint response in Xenopus egg extracts. Mol. Cell 6:839–849.
   PubMed Web of Science ®Google Scholar
• Kumagai, A., and W. G. Dunphy. 2003. Repeated phosphopeptide motifs in Claspin mediate the regulated binding of Chk1. Nat. Cell Biol. 5:161–165.
   PubMedGoogle Scholar
• Kumagai, A., S. M. Kim, and W. G. Dunphy. 2004. Claspin and the activated form of ATR-ATRIP collaborate in the activation of Chk1. J. Biol. Chem. 279:49599–49608.
   PubMed Web of Science ®Google Scholar
• Kumagai, A., J. Lee, H. Y. Yoo, and W. G. Dunphy. 2006. TopBP1 activates the ATR-ATRIP complex. Cell 124:943–955.
   PubMed Web of Science ®Google Scholar
• Liu, K., F. T. Lin, J. M. Ruppert, and W. C. Lin. 2003. Regulation of E2F1 by BRCT domain-containing protein TopBP1. Mol. Cell. Biol. 23:3287–3304.
   PubMed Web of Science ®Google Scholar
• Liu, K., Y. Luo, F. T. Lin, and W. C. Lin. 2004. TopBP1 recruits Brg1/Brm to repress E2F1-induced apoptosis, a novel pRb-independent and E2F1-specific control for cell survival. Genes Dev. 18:673–686.
   PubMed Web of Science ®Google Scholar
• Lukas, C., J. Falck, J. Bartkova, J. Bartek, and J. Lukas. 2003. Distinct spatiotemporal dynamics of mammalian checkpoint regulators induced by DNA damage. Nat. Cell Biol. 5:255–260.
   PubMed Web of Science ®Google Scholar
• Lukas, C., F. Melander, M. Stucki, J. Falck, S. Bekker-Jensen, M. Goldberg, Y. Lerenthal, S. P. Jackson, J. Bartek, and J. Lukas. 2004. Mdc1 couples DNA double-strand break recognition by Nbs1 with its H2AX-dependent chromatin retention. EMBO J. 23:2674–2683.
   PubMed Web of Science ®Google Scholar
• Lupardus, P. J., and K. A. Cimprich. 2006. Phosphorylation of Xenopus Rad1 and Hus1 defines a readout for ATR activation that is independent of Claspin and the Rad9 carboxy terminus. Mol. Biol. Cell 17:1559–1569.
   PubMed Web of Science ®Google Scholar
• Mailand, N., J. Falck, C. Lukas, R. G. Syljuasen, M. Welcker, J. Bartek, and J. Lukas. 2000. Rapid destruction of human Cdc25A in response to DNA damage. Science 288:1425–1429.
   PubMed Web of Science ®Google Scholar
• Makiniemi, M., T. Hillukkala, J. Tuusa, K. Reini, M. Vaara, D. Huang, H. Pospiech, I. Majuri, T. Westerling, T. P. Makela, and J. E. Syvaoja. 2001. BRCT domain-containing protein TopBP1 functions in DNA replication and damage response. J. Biol. Chem. 276:30399–30406.
   PubMed Web of Science ®Google Scholar
• Parrilla-Castellar, E. R., and L. M. Karnitz. 2003. Cut5 is required for the binding of Atr and DNA polymerase alpha to genotoxin-damaged chromatin. J. Biol. Chem. 278:45507–45511.
   PubMedGoogle Scholar
• Sanchez, Y., C. Wong, R. S. Thoma, R. Richman, Z. Wu, H. Piwnica-Worms, and S. J. Elledge. 1997. Conservation of the Chk1 checkpoint pathway in mammals: linkage of DNA damage to Cdk regulation through Cdc25. Science 277:1497–1501.
   PubMed Web of Science ®Google Scholar
• Shiloh, Y. 2003. ATM and related protein kinases: safeguarding genome integrity. Nat. Rev. Cancer 3:155–168.
   PubMed Web of Science ®Google Scholar
• Smits, V. A., P. M. Reaper, and S. P. Jackson. 2006. Rapid PIKK-dependent release of Chk1 from chromatin promotes the DNA-damage checkpoint response. Curr. Biol. 16:150–159.
   PubMedGoogle Scholar
• Sorensen, C. S., R. G. Syljuasen, J. Falck, T. Schroeder, L. Ronnstrand, K. K. Khanna, B. B. Zhou, J. Bartek, and J. Lukas. 2003. Chk1 regulates the S phase checkpoint by coupling the physiological turnover and ionizing radiation-induced accelerated proteolysis of Cdc25A. Cancer Cell 3:247–258.
   PubMed Web of Science ®Google Scholar
• Sporbert, A., A. Gahl, R. Ankerhold, H. Leonhardt, and M. C. Cardoso. 2002. DNA polymerase clamp shows little turnover at established replication sites but sequential de novo assembly at adjacent origin clusters. Mol. Cell 10:1355–1365.
   PubMed Web of Science ®Google Scholar
• Stewart, G. S., B. Wang, C. R. Bignell, A. M. Taylor, and S. J. Elledge. 2003. MDC1 is a mediator of the mammalian DNA damage checkpoint. Nature 421:961–966.
   PubMed Web of Science ®Google Scholar
• Stiff, T., M. O'Driscoll, N. Rief, K. Iwabuchi, M. Lobrich, and P. A. Jeggo. 2004. ATM and DNA-PK function redundantly to phosphorylate H2AX after exposure to ionizing radiation. Cancer Res. 64:2390–2396.
   PubMed Web of Science ®Google Scholar
• Stucki, M., and S. P. Jackson. 2004. MDC1/NFBD1: a key regulator of the DNA damage response in higher eukaryotes. DNA Repair 3:953–957.
   PubMed Web of Science ®Google Scholar
• Syljuasen, R. G., C. S. Sorensen, L. T. Hansen, K. Fugger, C. Lundin, F. Johansson, T. Helleday, M. Sehested, J. Lukas, and J. Bartek. 2005. Inhibition of human Chk1 causes increased initiation of DNA replication, phosphorylation of ATR targets, and DNA breakage. Mol. Cell. Biol. 25:3553–3562.
   PubMed Web of Science ®Google Scholar
• Syljuasen, R. G., C. S. Sorensen, J. Nylandsted, C. Lukas, J. Lukas, and J. Bartek. 2004. Inhibition of Chk1 by CEP-3891 accelerates mitotic nuclear fragmentation in response to ionizing radiation. Cancer Res. 64:9035–9040.
   PubMed Web of Science ®Google Scholar
• Takai, H., K. Tominaga, N. Motoyama, Y. A. Minamishima, H. Nagahama, T. Tsukiyama, K. Ikeda, K. Nakayama, and M. Nakanishi. 2000. Aberrant cell cycle checkpoint function and early embryonic death in Chk1−/− mice. Genes Dev. 14:1439–1447.
   PubMed Web of Science ®Google Scholar
• Tanaka, K., and P. Russell. 2001. Mrc1 channels the DNA replication arrest signal to checkpoint kinase Cds1. Nat. Cell Biol. 3:966–972.
   PubMed Web of Science ®Google Scholar
• Ward, I. M., and J. Chen. 2001. Histone H2AX is phosphorylated in an ATR-dependent manner in response to replicational stress. J. Biol. Chem. 276:47759–47762.
   PubMedGoogle Scholar
• Xu, X., J. Lee, and D. F. Stern. 2004. Microcephalin is a DNA damage response protein involved in regulation of CHK1 and BRCA1. J. Biol. Chem. 279:34091–34094.
   PubMed Web of Science ®Google Scholar
• Yamane, K., M. Kawabata, and T. Tsuruo. 1997. A DNA-topoisomerase-II-binding protein with eight repeating regions similar to DNA-repair enzymes and to a cell-cycle regulator. Eur. J. Biochem. 250:794–799.
   PubMedGoogle Scholar
• Yamane, K., X. Wu, and J. Chen. 2002. A DNA damage-regulated BRCT-containing protein, TopBP1, is required for cell survival. Mol. Cell. Biol. 22:555–566.
   PubMed Web of Science ®Google Scholar
• Yan, S., H. D. Lindsay, and W. M. Michael. 2006. Direct requirement for Xmus101 in ATR-mediated phosphorylation of Claspin bound Chk1 during checkpoint signaling. J. Cell Biol. 173:181–186.
   PubMed Web of Science ®Google Scholar
• Zhao, H., and H. Piwnica-Worms. 2001. ATR-mediated checkpoint pathways regulate phosphorylation and activation of human Chk1. Mol. Cell. Biol. 21:4129–4139.
   PubMed Web of Science ®Google Scholar
• Zhou, B. B., and S. J. Elledge. 2000. The DNA damage response: putting checkpoints in perspective. Nature 408:433–439.
   PubMed Web of Science ®Google Scholar
• Zou, L., and S. J. Elledge. 2003. Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 300:1542–1548.
   PubMed Web of Science ®Google Scholar