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[Cancer Research 64, 2390-2396, April 1, 2004]
© 2004 American Association for Cancer Research

Regular Articles

ATM and DNA-PK Function Redundantly to Phosphorylate H2AX after Exposure to Ionizing Radiation

Tom Stiff1, Mark O’Driscoll1, Nicole Rief2, Kuniyoshi Iwabuchi3, Markus Löbrich2 and Penny A. Jeggo1

1 Genome Damage and Stability Centre, University of Sussex, East Sussex, United Kingdom; 2 Fachrichtung Biophysik, Universität des Saarlandes, Homburg/Saar, Germany; and 3 Department of Biochemistry, Kanazawa Medical University, Ishikawa, Japan

H2AX phosphorylation is an early step in the response to DNA damage. It is widely accepted that ATM (ataxia telangiectasia mutated protein) phosphorylates H2AX in response to DNA double-strand breaks (DSBs). Whether DNA-dependent protein kinase (DNA-PK) plays any role in this response is unclear. Here, we show that H2AX phosphorylation after exposure to ionizing radiation (IR) occurs to similar extents in human fibroblasts and in mouse embryo fibroblasts lacking either DNA-PK or ATM but is ablated in ATM-deficient cells treated with LY294002, a drug that specifically inhibits DNA-PK. Additionally, we show that inactivation of both DNA-PK and ATM is required to ablate IR-induced H2AX phosphorylation in chicken cells. We confirm that H2AX phosphorylation induced by DSBs in nonreplicating cells is ATR (ataxia telangiectasia and Rad3-related protein) independent. Taken together, we conclude that under most normal growth conditions, IR-induced H2AX phosphorylation can be carried out by ATM and DNA-PK in a redundant, overlapping manner. In contrast, DNA-PK cannot phosphorylate other proteins involved in the checkpoint response, including chromatin-associated Rad17. However, by phosphorylating H2AX, DNA-PK can contribute to the presence of the damage response proteins MDC1 and 53BP1 at the site of the DSB.




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X. Liu, Y. Guo, Y. Li, Y. Jiang, S. Chubb, A. Azuma, P. Huang, A. Matsuda, W. Hittelman, and W. Plunkett
Molecular Basis for G2 Arrest Induced by 2'-C-Cyano-2'-Deoxy-1-{beta}-D-Arabino-Pentofuranosylcytosine and Consequences of Checkpoint Abrogation
Cancer Res., August 1, 2005; 65(15): 6874 - 6881.
[Abstract] [Full Text] [PDF]

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 J. Cell Sci.Home page
M. A. Bellani, P. J. Romanienko, D. A. Cairatti, and R. D. Camerini-Otero
SPO11 is required for sex-body formation, and Spo11 heterozygosity rescues the prophase arrest of Atm-/- spermatocytes
J. Cell Sci., August 1, 2005; 118(15): 3233 - 3245.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
Y. Zhang, C. U.K. Lim, E. S. Williams, J. Zhou, Q. Zhang, M. H. Fox, S. M. Bailey, and H. L. Liber
NBS1 Knockdown by Small Interfering RNA Increases Ionizing Radiation Mutagenesis and Telomere Association in Human Cells
Cancer Res., July 1, 2005; 65(13): 5544 - 5553.
[Abstract] [Full Text] [PDF]

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 Hum Mol GenetHome page
L. Erker, R. Schubert, H. Yakushiji, C. Barlow, D. Larson, J. B. Mitchell, and A. Wynshaw-Boris
Cancer chemoprevention by the antioxidant tempol acts partially via the p53 tumor suppressor
Hum. Mol. Genet., June 15, 2005; 14(12): 1699 - 1708.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
S. Dhanalakshmi, C. Agarwal, R. P. Singh, and R. Agarwal
Silibinin Up-regulates DNA-Protein Kinase-dependent p53 Activation to Enhance UVB-induced Apoptosis in Mouse Epithelial JB6 Cells
J. Biol. Chem., May 27, 2005; 280(21): 20375 - 20383.
[Abstract] [Full Text] [PDF]

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 FASEB J.Home page
R. Dip and H. Naegeli
More than just strand breaks: the recognition of structural DNA discontinuities by DNA-dependent protein kinase catalytic subunit
FASEB J, May 1, 2005; 19(7): 704 - 715.
[Abstract] [Full Text] [PDF]

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 MutagenesisHome page
E. Bilsland and J. A. Downs
Tails of histones in DNA double-strand break repair
Mutagenesis, May 1, 2005; 20(3): 153 - 163.
[Abstract] [Full Text] [PDF]

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 Mol. Biol. CellHome page
J. D. Friesner, B. Liu, K. Culligan, and A. B. Britt
Ionizing Radiation-dependent {gamma}-H2AX Focus Formation Requires Ataxia Telangiectasia Mutated and Ataxia Telangiectasia Mutated and Rad3-related
Mol. Biol. Cell, May 1, 2005; 16(5): 2566 - 2576.
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 Mol. Biol. CellHome page
D. G. Pankratz and S. L. Forsburg
Meiotic S-Phase Damage Activates Recombination without Checkpoint Arrest
Mol. Biol. Cell, April 1, 2005; 16(4): 1651 - 1660.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
J. Li and D. F. Stern
Regulation of CHK2 by DNA-dependent Protein Kinase
J. Biol. Chem., March 25, 2005; 280(12): 12041 - 12050.
[Abstract] [Full Text] [PDF]

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 Nucleic Acids ResHome page
E. E. Bosco and E. S. Knudsen
Differential role of RB in response to UV and IR damage
Nucleic Acids Res., March 14, 2005; 33(5): 1581 - 1592.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
J. Drouet, C. Delteil, J. Lefrancois, P. Concannon, B. Salles, and P. Calsou
DNA-dependent Protein Kinase and XRCC4-DNA Ligase IV Mobilization in the Cell in Response to DNA Double Strand Breaks
J. Biol. Chem., February 25, 2005; 280(8): 7060 - 7069.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
S. Rooney, F. W. Alt, J. Sekiguchi, and J. P. Manis
Artemis-independent functions of DNA-dependent protein kinase in Ig heavy chain class switch recombination and development
PNAS, February 15, 2005; 102(7): 2471 - 2475.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
J. G. Viniegra, N. Martinez, P. Modirassari, J. H. Losa, C. P. Cobo, V. J. S.-A. Lobo, C. I. A. Luquero, L. Alvarez-Vallina, S. Ramon y Cajal, J. M. Rojas, et al.
Full Activation of PKB/Akt in Response to Insulin or Ionizing Radiation Is Mediated through ATM
J. Biol. Chem., February 11, 2005; 280(6): 4029 - 4036.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
I. H. Ismail, S. Nystrom, J. Nygren, and O. Hammarsten
Activation of Ataxia Telangiectasia Mutated by DNA Strand Break-inducing Agents Correlates Closely with the Number of DNA Double Strand Breaks
J. Biol. Chem., February 11, 2005; 280(6): 4649 - 4655.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
B. Kysela, M. Chovanec, and P. A. Jeggo
Phosphorylation of linker histones by DNA-dependent protein kinase is required for DNA ligase IV-dependent ligation in the presence of histone H1
PNAS, February 8, 2005; 102(6): 1877 - 1882.
[Abstract] [Full Text] [PDF]

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 Hum Mol GenetHome page
M. Fernet, M. Gribaa, M. A.M. Salih, M. Z. Seidahmed, J. Hall, and M. Koenig
Identification and functional consequences of a novel MRE11 mutation affecting 10 Saudi Arabian patients with the ataxia telangiectasia-like disorder
Hum. Mol. Genet., January 15, 2005; 14(2): 307 - 318.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
C. Bavoux, A. M. Leopoldino, V. Bergoglio, J. O-Wang, T. Ogi, A. Bieth, J.-G. Judde, S. D. J. Pena, M.-F. Poupon, T. Helleday, et al.
Up-Regulation of the Error-Prone DNA Polymerase {kappa} Promotes Pleiotropic Genetic Alterations and Tumorigenesis
Cancer Res., January 1, 2005; 65(1): 325 - 330.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
E. U. Kurz, P. Douglas, and S. P. Lees-Miller
Doxorubicin Activates ATM-dependent Phosphorylation of Multiple Downstream Targets in Part through the Generation of Reactive Oxygen Species
J. Biol. Chem., December 17, 2004; 279(51): 53272 - 53281.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
I. Hickson, Y. Zhao, C. J. Richardson, S. J. Green, N. M. B. Martin, A. I. Orr, P. M. Reaper, S. P. Jackson, N. J. Curtin, and G. C. M. Smith
Identification and Characterization of a Novel and Specific Inhibitor of the Ataxia-Telangiectasia Mutated Kinase ATM
Cancer Res., December 15, 2004; 64(24): 9152 - 9159.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
S. J. Collis, J. M. Schwaninger, A. J. Ntambi, T. W. Keller, W. G. Nelson, L. E. Dillehay, and T. L. DeWeese
Evasion of Early Cellular Response Mechanisms following Low Level Radiation-induced DNA Damage
J. Biol. Chem., November 26, 2004; 279(48): 49624 - 49632.
[Abstract] [Full Text] [PDF]

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 JEMHome page
B. Reina-San-Martin, H. T. Chen, A. Nussenzweig, and M. C. Nussenzweig
ATM Is Required for Efficient Recombination between Immunoglobulin Switch Regions
J. Exp. Med., November 1, 2004; 200(9): 1103 - 1110.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
R. Daniel, J. Ramcharan, E. Rogakou, K. D. Taganov, J. G. Greger, W. Bonner, A. Nussenzweig, R. A. Katz, and A. M. Skalka
Histone H2AX Is Phosphorylated at Sites of Retroviral DNA Integration but Is Dispensable for Postintegration Repair
J. Biol. Chem., October 29, 2004; 279(44): 45810 - 45814.
[Abstract] [Full Text] [PDF]


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