ATM activation and its recruitment to damaged DNA require binding to the C terminus of Nbs1

Molecular and Cellular Biology

Volumn 25, Issue 13, 2005, Pages 5363-5379

  You, Zhongsheng ^a   Chahwan, Charly ^b   Bailis, Julie ^a   Hunter, Tony ^a   Russell, Paul ^a,b  

^a SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; DNA; MRE11 PROTEIN; NIBRIN; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 KINASE RELATED KINASE; RAD50 PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; DNA BINDING; DNA DAMAGE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; PROTEIN DOMAIN; PROTEIN MOTIF; XENOPUS;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; CELL CYCLE PROTEINS; CELL EXTRACTS; CHROMOSOMAL PROTEINS, NON-HISTONE; CONSERVED SEQUENCE; DNA DAMAGE; DNA-BINDING PROTEINS; FEMALE; FUNGAL PROTEINS; HUMANS; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; OOCYTES; PHOSPHORYLATION; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; PROTEIN-SERINE-THREONINE KINASES; SCHIZOSACCHAROMYCES POMBE PROTEINS; TUMOR SUPPRESSOR PROTEINS; TWO-HYBRID SYSTEM TECHNIQUES; XENOPUS; XENOPUS PROTEINS;

SACCHAROMYCETALES; SCHIZOSACCHAROMYCES POMBE;

EID: 20744436198     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.25.13.5363-5379.2005     Document Type: Article

References (76)

1. Abraham, R. T. 2001. Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes Dev. 15:2177-2196.
2. Andrade, M. A., C. Petosa, S. I. O'Donoghue, C. W. Muller, and P. Bork. 2001. Comparison of ARM and HEAT protein repeats. J. Mol. Biol. 309:1-18.
3. Bahler, J., J. Q. Wu, M. S. Longtine, N. G. Shah, A. McKenzie III, A. B. Steever, A. Wach, P. Philippsen, and J. R. Pringle. 1998. Heterologous modules for efficient and versatile PCR-based gene targeting in Schizosaccharomyces pombe. Yeast 14:943-951.
4. Bakkenist, C. J., and M. B. Kastan. 2003. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 421:499-506.
5. Bakkenist, C. J., and M. B. Kastan. 2004. Initiating cellular stress responses. Cell 118:9-17.
6. Bayliss, R., T. Littlewood, and M. Stewart. 2000. Structural basis for the interaction between FxFG nucleoporin repeats and importin-beta in nuclear trafficking. Cell 102:99-108.
7. Blow, J. J., and R. A. Laskey. 1986. Initiation of DNA replication in nuclei and purified DNA by a cell-free extract of Xenopus eggs. Cell 47:577-587.
8. Carney, J. P., R. S. Maser, H. Olivares, E. M. Davis, M. Le Beau, J. R. Yates III, L. Hays, W. F. Morgan, and J. H. Petrini. 1998. The hMre11/hRad50 protein complex and Nijmegen breakage syndrome: linkage of double-strand break repair to the cellular DNA damage response. Cell 93:477-486.
9. Carson, C. T., R. A. Schwartz, T. H. Stracker, C. E. Lilley, D. V. Lee, and M. D. Weitzman. 2003. The Mre11 complex is required for ATM activation and the G2/M checkpoint. EMBO J. 22:6610-6620.
10. Cerosaletti, K., and P. Concannon. 2004. Independent roles for nibrin and Mre11/Rad50 in the activation and function of Atm. J. Biol. Chem. 279:38813-38819.
11. Chahwan, C., T. M. Nakamura, S. Sivakumar, P. Russell, and N. Rhind. 2003. The fission yeast Rad32 (Mre11)-Rad50-Nbs1 complex is required for the S-phase DNA damage checkpoint. Mol. Cell. Biol. 23:6564-6573.
12. Chen, S., P. Paul, and B. D. Price. 2003. ATM's leucine-rich domain and adjacent sequences are essential for ATM to regulate the DNA damage response. Oncogene 22:6332-6339.
13. Chunk, Y. M., and G. Blobel. 1999. Structure of the nuclear transport complex karyopherin-beta2-Ran × GppNHp. Nature 399:230-237.
14. Cingolani, G., C. Petosa, K. Weis, and C. W. Muller. 1999. Structure of importin-beta bound to the IBB domain of importin-alpha. Nature 399:221-229.
15. Connelly, J. C., and D. R. Leach. 2002. Tethering on the brink: the evolutionarily conserved Mre11-Rad50 complex. Trends Biochem. Sci. 27:410-418.
16. Costanzo, V., T. Paull, M. Gottesman, and J. Gautier. 2004. Mre11 assembles linear DNA fragments into DNA damage signaling complexes. PLoS Biol. 2:600-609.
17. Costanzo, V., K. Robertson, C. Y. Ying, E. Kim, E. Avvedimento, M. Gottesman, D. Grieco, and J. Gautier. 2000. Reconstitution of an ATM-dependent checkpoint that inhibits chromosomal DNA replication following DNA damage. Mol. Cell 6:649-659.
18. D'Amours, D., and S. P. Jackson. 2002. The Mre11 complex: at the crossroads of DNA repair and checkpoint signaling. Nat. Rev. Mol. Cell Biol. 3:317-327.
19. Delia, D., M. Piane, G. Buscemi, C. Savio, S. Palmeri, P. Lulli, L. Carlessi, E. Fontanella, and L. Chessa. 2004. MRE11 mutations and impaired ATM-dependent responses in an Italian family with ataxia-telangiectasia-like disorder. Hum. Mol. Genet. 13:2155-2163.
20. Demuth, I., P. O. Frappart, G. Hildebrand, A. Melchers, S. Lobitz, L. Stockl, R. Varon, Z. Herceg, K. Sperling, Z. Q. Wang, and M. Digweed. 2004. An inducible null mutant murine model of Nijmegen breakage syndrome proves the essential function of NBS1 in chromosomal stability and cell viability. Hum. Mol. Genet. 13:2385-2397.
21. Desai-Mehta, A., K. M. Cerosaletti, and P. Concannon. 2001. Distinct functional domains of nibrin mediate Mre11 binding, focus formation, and nuclear localization. Mol. Cell. Biol. 21:2184-2191.
22. Du, L. L., T. M. Nakamura, B. A. Moser, and P. Russell. 2003. Retention but not recruitment of Crb2 at double-strand breaks requires Rad1 and Rad3 complexes. Mol. Cell. Biol. 23:6150-6158.
23. 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.
24. Farah, J. A., E. Hartsuiker, K. Mizuno, K. Ohta, and G. R. Smith. 2002. A 160-bp palindrome is a Rad50. Rad32-dependent mitotic recombination hotspot in Schizosaccharomyces pombe. Genetics 161:461-468.
25. Fernandez-Capetillo, O., A. Lee, M. Nussenzweig, and A. Nussenzweig. 2004. H2AX: the histone guardian of the genome. DNA Repair (Amsterdam) 3:959-967.
26. Gell, D., and S. P. Jackson. 1999. Mapping of protein-protein interactions within the DNA-dependent protein kinase complex. Nucleic Acids Res. 27:3494-3502.
27. Gottesfeld, J., and L. S. Bloomer. 1982. Assembly of transcriptionally active 5S RNA gene chromatin in vitro. Cell 28:781-791.
28. Groves, M. R., N. Hanlon, P. Turowski, B. A. Hemmings, and D. Barford. 1999. The structure of the protein phosphatase 2A PR65/A subunit reveals the conformation of its 15 tandemly repeated HEAT motifs. Cell 96:99-110.
29. Guo, Z., and W. G. Dunphy. 2000. Response of Xenopus Cds1 in cell-free extracts to DNA templates with double-stranded ends. Mol. Biol. Cell 11:1535-1546.
30. Haber, J. E. 1998. The many interfaces of Mre11. Cell 95:583-586.
31. Heckman, D. S., D. M. Geiser, B. R. Eidell, R. L. Stauffer, N. L. Kardos, and S. B. Hedges. 2001. Molecular evidence for the early colonization of land by fungi and plants. Science 293:1129-1133.
32. Hodson, J. A., J. M. Bailis, and S. L. Forsburg. 2003. Efficient labeling of fission yeast Schizosaccharomyces pombe with thymidine and BUdR. Nucleic Acids Res. 31:e134.
33. Hopfner, K. P., A. Karcher, D. Shin, C. Fairley, J. A. Tainer, and J. P. Carney. 2000. Mre11 and Rad50 from Pyrococcus furiosus: cloning and biochemical characterization reveal an evolutionarily conserved multiprotein machine. J. Bacteriol. 182:6036-6041.
34. Hopfner, K. P., A. Karcher, D. S. Shin, L. Craig, L. M. Arthur, J. P. Carney, and J. A. Tainer. 2000. Structural biology of Rad50 ATPase: ATP-driven conformational control in DNA double-strand break repair and the ABC-ATPase superfamily. Cell 101:789-800.
35. Hopfner, K. P., and J. A. Tainer. 2003. Rad50/SMC proteins and ABC transporters: unifying concepts from high-resolution structures. Curr. Opin. Struct. Biol. 13:249-255.
36. Horejsi, Z., J. Falck, C. J. Bakkenist, M. B. Kastan, J. Lukas, and J. Bartek. 2004. Distinct functional domains of Nbs1 modulate the timing and magnitude of ATM activation after low doses of ionizing radiation. Oncogene 23:3122-3127.
37. Kastan, M. B., and J. Bartek. 2004. Cell-cycle checkpoints and cancer. Nature 432:316-323.
38. Kitagawa, R., C. J. Bakkenist, P. J. McKinnon, and M. B. Kastan. 2004. Phosphorylation of SMC1 is a critical downstream event in the ATM-NBS1-BRCA1 pathway. Genes Dev. 18:1423-1438.
39. Kobayashi, J., H. Tauchi, S. Sakamoto, A. Nakamura, K. Morishima, S. Matsuura, T. Kobayashi, K. Tamai, K. Tanimoto, and K. Komatsu. 2002. NBS1 localizes to gamma-H2AX foci through interaction with the FHA/BRCT domain. Curr. Biol. 12:1846-1851.
40. Laskey, R. A., and W. C. Earnshaw. 1980. Nucleosome assembly. Nature 286:763-767.
41. Lavin, M. F., and Y. Shiloh. 1997. The genetic defect in ataxia-telangiectasia. Annu. Rev. Immunol. 15:177-202.
42. 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.
43. Lindsay, H. D., D. J. Griffiths, R. J. Edwards, P. U. Christensen, J. M. Murray, F. Osman, N. Walworth, and A. M. Carr. 1998. S-phase-spedfic activation of Cds1 kinase defines a subpathway of the checkpoint response in Schizosaccharomyces pombe. Genes Dev. 12:382-395.
44. 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.
45. 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.
46. Maser, R. S., R. Zinkel, and J. H. Petrini. 2001. An alternative mode of translation permits production of a variant NBS1 protein from the common Nijmegen breakage syndrome allele. Nat. Genet. 27:417-421.
47. +. Genetics 152:1501-1512.
48. Mochan, T. A., M. Venere, R. A. DiTullio, Jr., and T. D. Halazonetis. 2003. 53BP1 and NFBD1/MDC1-Nbs1 function in parallel interacting pathways activating ataxia-telangiectasia mutated (ATM) in response to DNA damage. Cancer Res. 63:8586-8591.
49. Morgan, S. E., C. Lovly, T. K. Pandita, Y. Shiloh, and M. B. Kastan. 1997. Fragments of ATM which have dominant-negative or complementing activity. Mol. Cell. Biol. 17:2020-2029.
50. 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.
51. Nakamura, T. M., L. L. Du, C. Redon, and P. Russell. 2004. Histone H2A phosphorylation controls Crb2 recruitment at DNA breaks, maintains checkpoint arrest, and influences DNA repair in fission yeast. Mol. Cell. Biol. 24:6215-6230.
52. Nakamura, T. M., B. A. Moser, and P. Russell. 2002. Telomere binding of checkpoint sensor and DNA repair proteins contributes to maintenance of functional fission yeast telomeres. Genetics 161:1437-1452.
53. Navas, T. A., Z. Zhou, and S. J. Elledge. 1995. DNA polymerase epsilon links the DNA replication machinery to the S phase checkpoint. Cell 80:29-39.
54. Newport, J. 1987. Nuclear reconstitution in vitro: stages of assembly around protein-free DNA. Cell 48:205-217.
55. Nyherg, K. A., R. J. Michelson, C. W. Putnam, and T. A. Weinert. 2002. Toward maintaining the genome: DNA damage and replication checkpoints. Annu. Rev. Genet. 36:617-656.
56. O'Driscoll, M., V. L. Ruiz-Perez, C. G. Woods, P. A. Jeggo, and J. A. Goodship. 2003. A splicing mutation affecting expression of ataxia- telangiectasia and Rad3-related protein (ATR) results in Seckel syndrome. Nat. Genet. 33:497-501.
57. Perry, J., and N. Kleckner. 2003. The ATRs, ATMs, and TORs are giant HEAT repeat proteins. Cell 112:151-155.
58. Petrini, J. H., and T. H. Stracker. 2003. The cellular response to DNA double-strand breaks: defining the sensors and mediators. Trends Cell Biol. 13:458-462.
59. Rawls, J. M., and J. W. Fristrom. 1975. A complex genetic locus that controls of the first three steps of pyrimidine biosynthesis in Drosophila. Nature 255:738-740.
60. Redon, C., D. Pilch, E. Rogakuii, O. Sedelnikova, K. Newrock, and W. Bonner. 2002. Histone H2A variants H2AX and H2AZ. Curr. Opin. Genet. Dev. 12:162-169.
61. Ritchie, K. B., and T. D. Petes. 2000. The Mre11p/Rad50p/Xrs2p complex and the Tel1p function in a single pathway for telomere maintenance in yeast. Genetics 155:475-479.
62. Rouse, J., and S. P. Jackson. 2002. Interfaces between the detection, signaling, and repair of DNA damage. Science 297:547-551.
63. Rout, M. P., and S. R. Wente. 1994. Pores for thought: nuclear pore complex proteins. Trends Cell Biol. 4:357-365.
64. Sanders, S. L., M. Portoso, J. Mata, J. Bahler, R. C. Allshire, and T. Kouzarides. 2004. Methylation of histone H4 lysine 20 controls recruitment of Crb2 to sites of DNA damage. Cell 119:603-614.
65. Shechter, D., V. Costanzo, and J. Gautier. 2004. ATR and ATM regulate the timing of DNA replication origin firing. Nat. Cell Biol. 6:648-655.
66. Shiloh, Y. 1997. Ataxia-telangiectasia and the Nijmegen breakage syndrome: related disorders but genes apart. Annu. Rev. Genet. 31:635-662.
67. Shiloh, Y. 2003. ATM and related protein kinases: safeguarding genome integrity. Nat. Rev. Cancer 3:155-168.
68. Sigler, P. B., Z. Xu, H. S. Rye, S. G. Burston, W. A. Fenton, and A. L. Horwich. 1998. Structure and function in GroEL-mediated protein folding. Annu. Rev. Biochem. 67:581-608.
69. Smith, G. C., and S. P. Jackson. 1999. The DNA-dependent protein kinase. Genes Dev. 13:916-934.
70. Tauchi, H., J. Kobayashi, K. Morishima, S. Matsuura, A. Nakamura, T. Shiraishi, E. Ito, D. Masnada, D. Delia, and K. Komatsu. 2001. The fork-head-associated domain of NBS1 is essential for nuclear foci formation after irradiation but not essential for hRAD50-hMRE11-NBS1 complex DNA repair activity. J. Biol. Chem. 276:12-15.
71. Tsukamoto, Y., C. Mitsuoka, M. Terasawa, H. Ogawa, and T. Ogawa. 2005. Xrs2p regulates mre11p translocation to the nucleus and plays a role in telomere elongation and meiotic recombination. Mol. Biol. Cell 16:597-608.
72. + gene involved in DNA repair and telomere maintenance. Mol. Cell. Biol. 23:6553-6563.
73. Uziel, T., Y. Lerenthal, L. Moyal, Y. Andegeko, L. Mittelman, and Y. Shiloh. 2003. Requirement of the MRN complex for ATM activation by DNA damage. EMBO J. 22:5612-5621.
74. Wakayama, T., T. Kondo, S. Ando, K. Matsumoto, and K. Sugimoto. 2001. Pie1, a protein interacting with Mec1, controls cell growth and checkpoint responses in Saccharomyces cerevisiae. Mol. Cell. Biol. 21:755-764.
75. You, Z., K. Harvey, L. Kong, and J. Newport. 2002. Xic1 degradation in Xenopus egg extracts is coupled to initiation of DNA replication. Genes Dev. 16:1182-1194.
76. Zhang, Z., W. Hu, L. Cano, T. D. Lee, D. J. Chen, and Y. Chen. 2004. Solution structure of the C-terminal domain of Ku80 suggests important sites for protein-protein interactions. Structure (Cambridge) 12:495-502.