Functional interaction of H2AX, NBS1, and p53 in ATM-dependent DNA damage responses and tumor suppression

Molecular and Cellular Biology

Volumn 25, Issue 2, 2005, Pages 661-670

  Kang, Jian ^a   Ferguson, David ^b   Song, Hoseok ^a   Bassing, Craig ^b   Eckersdorff, Mark ^b   Alt, Frederick W ^b   Xu, Yang ^a,c  

^a SECTION OF MOLECULAR BIOLOGY   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; HISTONE H2A; PROTEIN P53;

ANIMAL TISSUE; ARTICLE; CANCER INHIBITION; DNA DAMAGE; DOWNSTREAM PROCESSING; EMBRYO; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

ANIMALS; CELL CYCLE; CELL CYCLE PROTEINS; CELLS, CULTURED; DNA DAMAGE; DNA-BINDING PROTEINS; FIBROBLASTS; GENES, TUMOR SUPPRESSOR; HISTONES; HUMANS; KARYOTYPING; LYMPHOMA; MICE; MICE, KNOCKOUT; NUCLEAR PROTEINS; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; RADIATION, IONIZING; SERINE; TRANSCRIPTION, GENETIC; TRANSLOCATION, GENETIC; TUMOR SUPPRESSOR PROTEIN P53; TUMOR SUPPRESSOR PROTEINS;

ANIMALIA; ATAXIA; ATAXIA TELANGIECTASIA;

EID: 11844259424     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.25.2.661-670.2005     Document Type: Article

References (55)

1. Ahn, J. Y., J. K. Schwarz, H. Piwnica-Worms, and C. E. Canman. 2000. Threonine 68 phosphorylation by ataxia telangiectasia mutated is required for efficient activation of Chk2 in response to ionizing radiation. Cancer Res. 60:5934-5936.
2. Bakkenist, C. J., and M. B. Kastan. 2003. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 421:499-506.
3. Barlow, C., S. Hirotsune, R. Paylor, M. Liyanage, M. Eckhaus, F. Collins, Y. Shiloh, J. N. Crawley, T. Ried, D. Tagle, and A. Wynshaw-Boris. 1996. Atm-deficient mice: a paradigm of ataxia telangiectasia. Cell 86:159-171.
4. Bassing, C. H., H. Suh, D. O. Ferguson, K. F. Chua, J. Manis, M. Eckersdorff, M. Gleason, R. Bronson, C. Lee, and F. W. Alt. 2003. Histone H2AX: a dosage-dependent suppressor of oncogenic translocations and tumors. Cell 114:359-370.
5. Boley, S. E., V. A. Wong, J. E. French, and L. Recio. 2002. p53 heterozygosity alters the mRNA expression of p53 target genes in the bone marrow in response to inhaled benzene. Toxicol. Sci. 66:209-215.
6. Burma, S., B. P. Chen, M. Murphy, A. Kurimasa, and D. J. Chen. 2001. ATM phosphorylates histone H2AX in response to DNA double-strand breaks. J. Biol. Chem. 276:42462-42467.
7. Buscemi, G., C. Savio, L. Zannini, F. Miceiche, D. Masnada, M. Nakanishi, H. Tauchi, K. Komatsu, S. Mizutani, K. Khanna, P. Chen, P. Concannon, L. Chessa, and D. Delia. 2001. Chk2 activation dependence on Nbs1 after DNA damage. Mol. Cell. Biol. 21:5214-5222.
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. 2/M checkpoint. EMBO J. 22:6610-6620.
10. Celeste, A., S. Difilippantonio, M. J. Difilippantonio, O. Fernandez-Capetillo, D. R. Pilch, O. A. Sedelnikova, M. Eckhaus, T. Ried, W. M. Bonner, and A. Nussenzweig. 2003. H2AX haploinsufficiency modifies genomic stability and tumor susceptibility. Cell 114:371-383.
11. Celeste, A., O. Fernandez-Capetillo, M. J. Kruhlak, D. R. Pilch, D. W. Staudt, A. Lee, R. F. Bonner, W. M. Bonner, and A. Nussenzweig. 2003. Histone H2AX phosphorylation is dispensable for the initial recognition of DNA breaks. Nat. Cell Biol. 5:675-679.
12. Celeste, A., S. Petersen, P. J. Romanienko, O. Fernandez-Capetillo, H. T. Chen, O. A. Sedelnikova, B. Reina-San-Martin, V. Coppola, E. Meffre, M. J. Difilippantonio, C. Redon, D. R. Pilch, A. Olaru, M. Eckhaus, R. D. Camerini-Otero, L. Tessarollo, F. Livak, K. Manova, W. M. Bonner, M. C. Nussenzweig, and A. Nussenzweig. 2002. Genomic instability in mice lacking histone H2AX. Science 296:922-927.
13. Chao, C., M. Hergenhahn, M. D. Kaeser, Z. Wu, S. Saito, R. Iggo, M. Hollstein, E. Appella, and Y. Xu. 2003. Cell type- and promoter-specific roles of Ser18 phosphorylation in regulating p53 responses. J. Biol. Chem. 8:8.
14. Chao, C., S. Saito, C. W. Anderson, E. Appella, and Y. Xu. 2000. Phosphorylation of murine p53 at ser-18 regulates the p53 responses to DNA damage. Proc. Natl. Acad. Sci. USA 97:11936-11941.
15. Chao, C., S. Saito, J. Kang, C. W. Anderson, E. Appella, and Y. Xu. 2000. p53 transcriptional activity is essential for p53-dependent apoptosis following DNA damage. EMBO J. 19:4967-4975.
16. Donehower, L. A., M. Harvey, B. L. Slagle, M. J. McArthur, C. A. Montgomery, Jr., J. S. Butel, and A. Bradley. 1992. Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours. Nature 356:215-221.
17. Dumaz, N., D. M. Milne, and D. W. Meek. 1999. Protein kinase CK1 is a p53-threonine 18 kinase which requires prior phosphorylation of serine 15. FEBS Lett. 463:312-316.
18. Elson, A., Y. Wang, C. J. Daugherty, C. C. Morton, F. Zhou, J. Campos-Torres, and P. Leder. 1996. Pleiotropic defects in ataxia-telangiectasia protein-deficient mice. Proc. Natl. Acad. Sci. USA 93:13084-13089.
19. Ferguson, D. O., J. M. Sekiguchi, S. Chang, K. M. Frank, Y. Gao, R. A. DePinho, and F. W. Alt. 2000. The nonhomologous end-joining pathway of DNA repair is required for genomic stability and the suppression of translocations. Proc. Natl. Acad. Sci. USA 97:6630-6633.
20. 2-M checkpoint activation by histone H2AX and 53BP1. Nat. Cell Biol. 4:993-997.
21. Gatei, M., D. Young, K. M. Cerosaletti, A. Desai-Mehta, K. Spring, S. Kozlov, M. F. Lavin, R. A. Gatti, P. Concannon, and K. Khanna. 2000. ATM-dependent phosphorylation of nibrin in response to radiation exposure. Nat. Genet. 25:115-119.
22. 1/S arrest. Oncogene 21:4191-4199.
23. 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.
24. Jacks, T., L. Remington, B. O. Williams, E. M. Schmitt, S. Halachmi, R. T. Bronson, and R. A. Weinberg. 1994. Tumor spectrum analysis in p53-mutant mice. Curr. Biol. 4:1-7.
25. Kang, J., R. T. Bronson, and Y. Xu. 2002. Targeted disruption of NBS1 reveals its roles in mouse development and DNA repair. EMBO J. 21:1447-1455.
26. Kastan, M. B., Q. Zhan, W. S. el-Deiry, F. Carrier, T. Jacks, W. V. Walsh, B. S. Plunkett, B. Vogelstein, and A. J. Fornace, Jr. 1992. A mammalian cell cycle checkpoint pathway utilizing p53 and GADD45 is defective in ataxiatelangiectasia. Cell 71:587-597.
27. 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.
28. Lambert, P. F., F. Kashanchi, M. F. Radonovich, R. Shiekhattar, and J. N. Brady. 1998. Phosphorylation of p53 serine 15 increases interaction with CBP. J. Biol. Chem. 273:33048-33053.
29. 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.
30. Lim, D. S., S. T. Kim, B. Xu, R. S. Maser, J. Lin, J. H. Petrini, and M. B. Kastan. 2000. ATM phosphorylates p95/nbs1 in an S-phase checkpoint pathway. Nature 404:613-617.
31. Lista, F., V. Bertness, C. J. Guidos, J. S. Danska, and I. R. Kirsch. 1997. The absolute number of trans-rearrangements between the TCRG and TCRB loci is predictive of lymphoma risk: a severe combined immune deficiency (SCID) murine model. Cancer Res. 57:4408-4413.
32. Liyanage, M., A. Coleman, S. du Manoir, T. Veldman, S. McCormack, R. B. Dickson, C. Barlow, A. Wynshaw-Boris, S. Janz, J. Wienberg, M. A. Ferguson-Smith, E. Schrock, and T. Ried. 1996. Multicolour spectral karyotyping of mouse chromosomes. Nat. Genet. 14:312-315.
33. 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.
34. 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.
35. Matsuoka, S., G. Rotman, A. Ogawa, Y. Shiloh, K. Tamai, and S. J. Elledge. 2000. Ataxia telangiectasia-mutated phosphorylates Chk2 in vivo and in vitro. Proc. Natl. Acad. Sci. USA 97:10389-10394.
36. Matsuura, S., H. Tauchi, A. Nakamura, N. Kondo, S. Sakamoto, S. Endo, D. Smeets, B. Solder, B. H. Belohradsky, V. M. Der Kaloustian, M. Oshimura, M. Isomura, Y. Nakamura, and K. Komatsu. 1998. Positional cloning of the gene for Nijmegen breakage syndrome. Nat. Genet. 19:179-181.
37. Melchionna, R., X. B. Chen, A. Blasina, and C. H. McGowan. 2000. Threonine 68 is required for radiation-induced phosphorylation and activation of Cdsl. Nat. Cell Biol. 2:762-765.
38. Mills, K. D., D. O. Ferguson, and F. W. Alt. 2003. The role of DNA breaks in genomic instability and tumorigenesis. Immunol. Rev. 194:77-95.
39. 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.
40. Rogakou, E. P., D. R. Pilch, A. H. Orr, V. S. Ivanova, and W. M. Bonner. 1998. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J. Biol. Chem. 273:5858-5868.
41. Sedelnikova, O. A., D. R. Pilch, C. Redon, and W. M. Bonner. 2003. Histone H2AX in DNA damage and repair. Cancer Biol. Ther. 2:233-235.
42. Shiloh, Y. 2003. ATM and related protein kinases: safeguarding genome integrity. Nat. Rev. Cancer 3:155-168.
43. Shiloh, Y., and M. B. Kastan. 2001. ATM: genome stability, neuronal development, and cancer cross paths. Adv. Cancer Res. 83:209-254.
44. Shiloh, Y., and G. Rotman. 1996. Ataxia-telangiectasia and the ATM gene: linking neurodegeneration, immunodeficiency, and cancer to cell cycle checkpoints. J. Clin. Immunol. 16:254-260.
45. 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.
46. van der Burgt, I., K. H. Chrzanowska, D. Smeets, and C. Weemaes. 1996. Nijmegen breakage syndrome. J. Med. Genet. 33:153-156.
47. Varon, R., C. Vissinga, M. Platzer, K. M. Cerosaletti, K. H. Chrzanowska, K. Saar, G. Beckmann, E. Seemanova, P. R. Cooper, N. J. Nowak, M. Stumm, C. M. Weemaes, R. A. Gatti, R. K. Wilson, M. Digweed, A. Rosenthal, K. Sperling, P. Concannon, and A. Reis. 1998. Nibrin, a novel DNA double-strand break repair protein, is mutated in Nijmegen breakage syndrome. Cell 93:467-476.
48. Ward, I. M., K. Minn, K. G. Jorda, and J. Chen. 2003. Accumulation of checkpoint protein 53BP1 at DNA breaks involves its binding to phosphorylated histone H2AX. J. Biol. Chem. 278:19579-19582.
49. Westphal, C. H., S. Rowan, C. Schmaltz, A. Elson, D. E. Fisher, and P. Leder. 1997. atm and p53 cooperate in apoptosis and suppression of tumorigenesis, but not in resistance to acute radiation toxicity. Nat. Genet. 16:397-401.
50. Williams, B. R., O. K. Mirzoeva, W. F. Morgan, J. Lin, W. Dunnick, and J. H. Petrini. 2002. A murine model of Nijmegen breakage syndrome. Curr. Biol. 12:648-653.
51. Wu, X., V. Ranganathan, D. S. Weisman, W. F. Heine, D. N. Ciccone, T. B. O'Neill, K. E. Crick, K. A. Pierce, W. S. Lane, G. Rathbun, D. M. Livingston, and D. T. Weaver. 2000. ATM phosphorylation of Nijmegen breakage syndrome protein is required in a DNA damage response. Nature 405:477-482.
52. Xu, Y., T. Ashley, E. E. Brainerd, R. T. Bronson, M. S. Meyn, and D. Baltimore. 1996. Targeted disruption of ATM leads to growth retardation, chromosomal fragmentation during meiosis, immune defects, and thymic lymphoma. Genes Dev. 10:2411-2422.
53. Xu, Y., and D. Baltimore. 1996. Dual roles of ATM in the cellular response to radiation and in cell growth control. Genes Dev. 10:2401-2410.
54. -/- mice. Mol. Cell. Biol. 18:4385-4390.
55. Zhao, S., Y. C. Weng, S. S. Yuan, Y. T. Lin, H. C. Hsu, S. C. Lin, E. Gerbino, M. H. Song, M. Z. Zdzienicka, R. A. Gatti, J. W. Shay, Y. Ziv, Y. Shiloh, and E. Y. Lee. 2000. Functional link between ataxia-telangiectasia and Nijmegen breakage syndrome gene products. Nature 405:473-477.