Activation of Protein Kinase Tel1 through Recognition of Protein-Bound DNA Ends

REFERENCES

• Akamatsu, Y., et al. 2008. Molecular characterization of the role of the Schizosaccharomyces pombe nip1+/ctp1+ gene in DNA double-strand break repair in association with the Mre11-Rad50-Nbs1 complex. Mol. Cell. Biol. 28:3639–3651.
   PubMed Web of Science ®Google Scholar
• Avemann, K., R. Knippers, T. Koller, and J. M. Sogo. 1988. Camptothecin, a specific inhibitor of type I DNA topoisomerase, induces DNA breakage at replication forks. Mol. Cell. Biol. 8:3026–3034.
   PubMed Web of Science ®Google Scholar
• Bakkenist, C. J., and M. B. Kastan. 2003. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 421:499–506.
   PubMed Web of Science ®Google Scholar
• Barker, S., M. Weinfeld, and D. Murray. 2005. DNA-protein crosslinks: their induction, repair, and biological consequences. Mutat. Res. 589:111–135.
   PubMed Web of Science ®Google Scholar
• Barker, S., M. Weinfeld, J. Zheng, L. Li, and D. Murray. 2005. Identification of mammalian proteins cross-linked to DNA by ionizing radiation. J. Biol. Chem. 280:33826–33838.
   PubMed Web of Science ®Google Scholar
• Berkovich, E., R. J. Monnat, Jr., and M. B. Kastan. 2007. Roles of ATM and NBS1 in chromatin structure modulation and DNA double-strand break repair. Nat. Cell Biol. 9:683–690.
   PubMed Web of Science ®Google Scholar
• Bressan, D. A., H. A. Olivares, B. E. Nelms, and J. H. Petrini. 1998. Alteration of N-terminal phosphoesterase signature motifs inactivates Saccharomyces cerevisiae Mre11. Genetics 150:591–600.
   PubMed Web of Science ®Google Scholar
• Chen, L., K. Trujillo, W. Ramos, P. Sung, and A. E. Tomkinson. 2001. Promotion of Dnl4-catalyzed DNA end-joining by the Rad50/Mre11/Xrs2 and Hdf1/Hdf2 complexes. Mol. Cell 8:1105–1115.
   PubMedGoogle Scholar
• Clerici, M., D. Mantiero, G. Lucchini, and M. P. Longhese. 2006. The Saccharomyces cerevisiae Sae2 protein negatively regulates DNA damage checkpoint signalling. EMBO Rep. 7:212–218.
   PubMed Web of Science ®Google Scholar
• Connelly, J. C., E. S. de Leau, and D. R. Leach. 2003. Nucleolytic processing of a protein-bound DNA end by the E. coli SbcCD (MR) complex. DNA Repair (Amst.) 2:795–807.
   PubMedGoogle Scholar
• Daley, J. M., P. L. Palmbos, D. Wu, and T. E. Wilson. 2005. Nonhomologous end joining in yeast. Annu. Rev. Genet. 39:431–451.
   PubMedGoogle Scholar
• Deng, C., J. A. Brown, D. You, and J. M. Brown. 2005. Multiple endonucleases function to repair covalent topoisomerase I complexes in Saccharomyces cerevisiae. Genetics 170:591–600.
   PubMed Web of Science ®Google Scholar
• Dinkelmann, M., et al. 2009. Multiple functions of MRN in end-joining pathways during isotype class switching. Nat. Struct. Mol. Biol. 16:808–813.
   PubMed Web of Science ®Google Scholar
• Dupré, A., L. Boyer-Chatenet, and J. Gautier. 2006. Two-step activation of ATM by DNA and the Mre11-Rad50-Nbs1 complex. Nat. Struct. Mol. Biol. 13:451–457.
   PubMed Web of Science ®Google Scholar
• Emili, A. 1998. MEC1-dependent phosphorylation of Rad9p in response to DNA damage. Mol. Cell 2:183–189.
   PubMed Web of Science ®Google Scholar
• Falck, J., J. Coates, and S. P. Jackson. 2005. Conserved modes of recruitment of ATM, ATR and DNA-PKcs to sites of DNA damage. Nature 434:605–611.
   PubMed Web of Science ®Google Scholar
• Furuya, K., M. Poitelea, L. Guo, T. Caspari, and A. M. Carr. 2004. Chk1 activation requires Rad9 S/TQ-site phosphorylation to promote association with C-terminal BRCT domains of Rad4TOPBP1. Genes Dev. 18:1154–1164.
   PubMed Web of Science ®Google Scholar
• Gravel, S., J. R. Chapman, C. Magill, and S. P. Jackson. 2008. DNA helicases Sgs1 and BLM promote DNA double-strand break resection. Genes Dev. 22:2767–2772.
   PubMed Web of Science ®Google Scholar
• Guzder, S. N., et al. 2004. Requirement of yeast Rad1-Rad10 nuclease for the removal of 3′-blocked termini from DNA strand breaks induced by reactive oxygen species. Genes Dev. 18:2283–2291.
   PubMedGoogle Scholar
• Haber, J. E. 1998. The many interfaces of Mre11. Cell 95:583–586.
   PubMed Web of Science ®Google Scholar
• Haber, J. E. 2000. Partners and pathways: repairing a double-strand break. Trends Genet. 16:259–264.
   PubMed Web of Science ®Google Scholar
• Harper, J. W., and S. J. Elledge. 2007. The DNA damage response: ten years after. Mol. Cell 28:739–745.
   PubMed Web of Science ®Google Scholar
• Hartsuiker, E., et al. 2009. Ctp1CtIP and Rad32Mre11 nuclease activity are required for Rec12Spo11 removal, but Rec12Spo11 removal is dispensable for other MRN-dependent meiotic functions. Mol. Cell. Biol. 29:1671–1681.
   PubMed Web of Science ®Google Scholar
• Hartsuiker, E., M. J. Neale, and A. M. Carr. 2009. Distinct requirements for the Rad32Mre11 nuclease and Ctp1CtIP in the removal of covalently bound topoisomerase I and II from DNA. Mol. Cell 33:117–123.
   PubMed Web of Science ®Google Scholar
• Heitman, J. 1992. How the EcoRI endonuclease recognizes and cleaves DNA. Bioessays 14:445–454.
   PubMedGoogle Scholar
• Hirano, Y., K. Fukunaga, and K. Sugimoto. 2009. Rif1 and Rif2 inhibit localization of Tel1 to DNA ends. Mol. Cell 33:312–322.
   PubMed Web of Science ®Google Scholar
• Hsiang, Y. H., M. G. Lihou, and L. F. Liu. 1989. Arrest of replication forks by drug-stabilized topoisomerase I-DNA cleavable complexes as a mechanism of cell killing by camptothecin. Cancer Res. 49:5077–5082.
   PubMed Web of Science ®Google Scholar
• Keeney, S. 2001. Mechanism and control of meiotic recombination initiation. Curr. Top. Dev. Biol. 52:1–53.
   PubMed Web of Science ®Google Scholar
• Keeney, S., C. N. Giroux, and N. Kleckner. 1997. Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell 88:375–384.
   PubMed Web of Science ®Google Scholar
• Krogh, B. O., and L. S. Symington. 2004. Recombination proteins in yeast. Annu. Rev. Genet. 38:233–271.
   PubMed Web of Science ®Google Scholar
• Lee, J. H., and T. T. Paull. 2005. ATM activation by DNA double-strand breaks through the Mre11-Rad50-Nbs1 complex. Science 308:551–554.
   PubMed Web of Science ®Google Scholar
• Lee, J. H., and T. T. Paull. 2004. Direct activation of the ATM protein kinase by the Mre11/Rad50/Nbs1 complex. Science 304:93–96.
   PubMed Web of Science ®Google Scholar
• Lengsfeld, B. M., A. J. Rattray, V. Bhaskara, R. Ghirlando, and T. T. Paull. 2007. Sae2 is an endonuclease that processes hairpin DNA cooperatively with the Mre11/Rad50/Xrs2 complex. Mol. Cell 28:638–651.
   PubMed Web of Science ®Google Scholar
• Lewis, L. K., J. M. Kirchner, and M. A. Resnick. 1998. Requirement for end-joining and checkpoint functions, but not RAD52-mediated recombination, after EcoRI endonuclease cleavage of Saccharomyces cerevisiae DNA. Mol. Cell. Biol. 18:1891–1902.
   PubMed Web of Science ®Google Scholar
• Li, T. K., and L. F. Liu. 2001. Tumor cell death induced by topoisomerase-targeting drugs. Annu. Rev. Pharmacol. Toxicol. 41:53–77.
   PubMed Web of Science ®Google Scholar
• Lieber, M. R., Y. Ma, U. Pannicke, and K. Schwarz. 2004. The mechanism of vertebrate nonhomologous DNA end joining and its role in V(D)J recombination. DNA Repair (Amst.) 3:817–826.
   PubMed Web of Science ®Google Scholar
• Limbo, O., et al. 2007. Ctp1 is a cell-cycle-regulated protein that functions with Mre11 complex to control double-strand break repair by homologous recombination. Mol. Cell 28:134–146.
   PubMed Web of Science ®Google Scholar
• Limbo, O., M. E. Porter-Goff, N. Rhind, and P. Russell. 2011. Mre11 nuclease activity and Ctp1 regulate Chk1 activation by Rad3ATR and Tel1ATM checkpoint kinases at double-strand breaks. Mol. Cell. Biol. 31:573–583.
   PubMed Web of Science ®Google Scholar
• Lisby, M., J. H. Barlow, R. C. Burgess, and R. Rothstein. 2004. Choreography of the DNA damage response: spatiotemporal relationships among checkpoint and repair proteins. Cell 118:699–713.
   PubMed Web of Science ®Google Scholar
• Liu, C., J. J. Pouliot, and H. A. Nash. 2002. Repair of topoisomerase I covalent complexes in the absence of the tyrosyl-DNA phosphodiesterase Tdp1. Proc. Natl. Acad. Sci. U. S. A. 99:14970–14975.
   PubMed Web of Science ®Google Scholar
• Lloyd, J., et al. 2009. A supramodular FHA/BRCT-repeat architecture mediates Nbs1 adaptor function in response to DNA damage. Cell 139:100–111.
   PubMed Web of Science ®Google Scholar
• Masumoto, H., D. Hawke, R. Kobayashi, and A. Verreault. 2005. A role for cell-cycle-regulated histone H3 lysine 56 acetylation in the DNA damage response. Nature 436:294–298.
   PubMed Web of Science ®Google Scholar
• Milman, N., E. Higuchi, and G. R. Smith. 2009. Meiotic DNA double-strand break repair requires two nucleases, MRN and Ctp1, to produce a single size class of Rec12 (Spo11)-oligonucleotide complexes. Mol. Cell. Biol. 29:5998–6005.
   PubMedGoogle Scholar
• Mimitou, E. P., and L. S. Symington. 2008. Sae2, Exo1 and Sgs1 collaborate in DNA double-strand break processing. Nature 455:770–774.
   PubMed Web of Science ®Google Scholar
• Naiki, T., T. Wakayama, D. Nakada, K. Matsumoto, and K. Sugimoto. 2004. Association of Rad9 with double-strand breaks through a Mec1-dependent mechanism. Mol. Cell. Biol. 24:3277–3285.
   PubMedGoogle Scholar
• Nakada, D., K. Matsumoto, and K. Sugimoto. 2003. ATM-related Tel1 associates with double-strand breaks through an Xrs2-dependent mechanism. Genes Dev. 17:1957–1962.
   PubMed Web of Science ®Google Scholar
• Nakada, D., T. Shimomura, K. Matsumoto, and K. Sugimoto. 2003. The ATM-related Tel1 protein of Saccharomyces cerevisiae controls a checkpoint response following phleomycin treatment. Nucleic Acids Res. 31:1715–1724.
   PubMedGoogle Scholar
• Nakamura, K., et al. 2010. Collaborative action of Brca1 and CtIP in elimination of covalent modifications from double-strand breaks to facilitate subsequent break repair. PLoS Genet. 6:e1000828.
   PubMed Web of Science ®Google Scholar
• Neale, M. J., J. Pan, and S. Keeney. 2005. Endonucleolytic processing of covalent protein-linked DNA double-strand breaks. Nature 436:1053–1057.
   PubMed Web of Science ®Google Scholar
• Nicolette, M. L., et al. 2010. Mre11-Rad50-Xrs2 and Sae2 promote 5′ strand resection of DNA double-strand breaks. Nat. Struct. Mol. Biol. 17:1478–1485.
   PubMed Web of Science ®Google Scholar
• Niu, H., et al. 2010. Mechanism of the ATP-dependent DNA end-resection machinery from Saccharomyces cerevisiae. Nature 467:108–111.
   PubMed Web of Science ®Google Scholar
• Osley, M. A., T. Tsukuda, and J. A. Nickoloff. 2007. ATP-dependent chromatin remodeling factors and DNA damage repair. Mutat. Res. 618:65–80.
   PubMed Web of Science ®Google Scholar
• Pellicioli, A., and M. Foiani. 2005. Signal transduction: how rad53 kinase is activated. Curr. Biol. 15:R769–R771.
   PubMedGoogle Scholar
• Pommier, Y. 2006. Topoisomerase I inhibitors: camptothecins and beyond. Nat. Rev. Cancer 6:789–802.
   PubMed Web of Science ®Google Scholar
• Pouliot, J. J., C. A. Robertson, and H. A. Nash. 2001. Pathways for repair of topoisomerase I covalent complexes in Saccharomyces cerevisiae. Genes Cells 6:677–687.
   PubMed Web of Science ®Google Scholar
• Pouliot, J. J., K. C. Yao, C. A. Robertson, and H. A. Nash. 1999. Yeast gene for a Tyr-DNA phosphodiesterase that repairs topoisomerase I complexes. Science 286:552–555.
   PubMed Web of Science ®Google Scholar
• Puddu, F., et al. 2008. Phosphorylation of the budding yeast 9-1-1 complex is required for Dpb11 function in the full activation of the UV-induced DNA damage checkpoint. Mol. Cell. Biol. 28:4782–4793.
   PubMed Web of Science ®Google Scholar
• Rass, E., et al. 2009. Role of Mre11 in chromosomal nonhomologous end joining in mammalian cells. Nat. Struct. Mol. Biol. 16:819–824.
   PubMed Web of Science ®Google Scholar
• Rothenberg, M., J. Kohli, and K. Ludin. 2009. Ctp1 and the MRN-complex are required for endonucleolytic Rec12 removal with release of a single class of oligonucleotides in fission yeast. PLoS Genet. 5:e1000722.
   PubMed Web of Science ®Google Scholar
• Sartori, A. A., et al. 2007. Human CtIP promotes DNA end resection. Nature 450:509–514.
   PubMed Web of Science ®Google Scholar
• Seidel, J. J., C. M. Anderson, and E. H. Blackburn. 2008. A novel Tel1/ATM N-terminal motif, TAN, is essential for telomere length maintenance and a DNA damage response. Mol. Cell. Biol. 28:5736–5746.
   PubMed Web of Science ®Google Scholar
• Shiotani, B., and L. Zou. 2009. Single-stranded DNA orchestrates an ATM-to-ATR switch at DNA breaks. Mol. Cell 33:547–558.
   PubMed Web of Science ®Google Scholar
• Shroff, R., et al. 2004. Distribution and dynamics of chromatin modification induced by a defined DNA double-strand break. Curr. Biol. 14:1703–1711.
   PubMed Web of Science ®Google Scholar
• Sleigh, M. J. 1976. The mechanism of DNA breakage by phleomycin in vitro. Nucleic Acids Res. 3:891–901.
   PubMedGoogle Scholar
• Stracker, T. H., C. T. Carson, and M. D. Weitzman. 2002. Adenovirus oncoproteins inactivate the Mre11-Rad50-NBS1 DNA repair complex. Nature 418:348–352.
   PubMed Web of Science ®Google Scholar
• Strumberg, D., et al. 2000. Conversion of topoisomerase I cleavage complexes on the leading strand of ribosomal DNA into 5′-phosphorylated DNA double-strand breaks by replication runoff. Mol. Cell. Biol. 20:3977–3987.
   PubMed Web of Science ®Google Scholar
• Sugimoto, K., Y. Sakamoto, O. Takahashi, and K. Matsumoto. 1995. HYS2, an essential gene required for DNA replication in Saccharomyces cerevisiae. Nucleic Acids Res. 23:3493–3500.
   PubMedGoogle Scholar
• Sweeney, F. D., et al. 2005. Saccharomyces cerevisiae Rad9 acts as a Mec1 adaptor to allow Rad53 activation. Curr. Biol. 15:1364–1375.
   PubMed Web of Science ®Google Scholar
• Trujillo, K. M., and P. Sung. 2001. DNA structure-specific nuclease activities in the Saccharomyces cerevisiae Rad50*Mre11 complex. J. Biol. Chem. 276:35458–35464.
   PubMed Web of Science ®Google Scholar
• Tsao, Y. P., A. Russo, G. Nyamuswa, R. Silber, and L. F. Liu. 1993. Interaction between replication forks and topoisomerase I-DNA cleavable complexes: studies in a cell-free SV40 DNA replication system. Cancer Res. 53:5908–5914.
   PubMed Web of Science ®Google Scholar
• Usui, T., H. Ogawa, and J. H. Petrini. 2001. A DNA damage response pathway controlled by Tel1 and the Mre11 complex. Mol. Cell 7:1255–1266.
   PubMed Web of Science ®Google Scholar
• van Attikum, H., and S. M. Gasser. 2005. ATP-dependent chromatin remodeling and DNA double-strand break repair. Cell Cycle 4:1011–1014.
   PubMed Web of Science ®Google Scholar
• Vance, J. R., and T. E. Wilson. 2002. Yeast Tdp1 and Rad1-Rad10 function as redundant pathways for repairing Top1 replicative damage. Proc. Natl. Acad. Sci. U. S. A. 99:13669–13674.
   PubMed Web of Science ®Google Scholar
• Vialard, J. E., C. S. Gilbert, C. M. Green, and N. F. Lowndes. 1998. The budding yeast Rad9 checkpoint protein is subjected to Mec1/Tel1-dependent hyperphosphorylation and interacts with Rad53 after DNA damage. EMBO J. 17:5679–5688.
   PubMed Web of Science ®Google Scholar
• Wang, J. C. 2002. Cellular roles of DNA topoisomerases: a molecular perspective. Nat. Rev. Mol. Cell Biol. 3:430–440.
   PubMed Web of Science ®Google Scholar
• Wang, J. C. 1996. DNA topoisomerases. Annu. Rev. Biochem. 65:635–692.
   PubMed Web of Science ®Google Scholar
• Williams, R. S., et al. 2009. Nbs1 flexibly tethers Ctp1 and Mre11-Rad50 to coordinate DNA double-strand break processing and repair. Cell 139:87–99.
   PubMed Web of Science ®Google Scholar
• Xie, A., A. Kwok, and R. Scully. 2009. Role of mammalian Mre11 in classical and alternative nonhomologous end joining. Nat. Struct. Mol. Biol. 16:814–818.
   PubMed Web of Science ®Google Scholar
• You, Z., J. M. Bailis, S. A. Johnson, S. M. Dilworth, and T. Hunter. 2007. Rapid activation of ATM on DNA flanking double-strand breaks. Nat. Cell Biol. 9:1311–1318.
   PubMed Web of Science ®Google Scholar
• You, Z., C. Chahwan, J. Bailis, T. Hunter, and P. Russell. 2005. ATM activation and its recruitment to damaged DNA require binding to the C terminus of Nbs1. Mol. Cell. Biol. 25:5363–5379.
   PubMed Web of Science ®Google Scholar
• You, Z., et al. 2009. CtIP links DNA double-strand break sensing to resection. Mol. Cell 36:954–969.
   PubMed Web of Science ®Google Scholar
• Zhou, B.-B. S., and S. J. Elledge. 2000. The DNA damage response: putting checkpoints in perspective. Nature 408:433–439.
   PubMed Web of Science ®Google Scholar
• Zhu, Z., W. H. Chung, E. Y. Shim, S. E. Lee, and G. Ira. 2008. Sgs1 helicase and two nucleases Dna2 and Exo1 resect DNA double-strand break ends. Cell 134:981–994.
   PubMed Web of Science ®Google Scholar