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Originally published In Press as doi:10.1074/jbc.C100466200 on September 24, 2001

J. Biol. Chem., Vol. 276, Issue 45, 42462-42467, November 9, 2001
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ATM Phosphorylates Histone H2AX in Response to DNA Double-strand Breaks*

Sandeep Burma, Benjamin P. Chen, Michael Murphy, Akihiro KurimasaDagger , and David J. Chen§

From the Life Sciences Division, Lawrence Berkeley National Laboratory, Berkeley, California 94720

A very early step in the response of mammalian cells to DNA double-strand breaks is the phosphorylation of histone H2AX at serine 139 at the sites of DNA damage. Although the phosphatidylinositol 3-kinases, DNA-PK (DNA-dependent protein kinase), ATM (ataxia telangiectasia mutated), and ATR (ATM and Rad3-related), have all been implicated in H2AX phosphorylation, the specific kinase involved has not yet been identified. To definitively identify the specific kinase(s) that phosphorylates H2AX in vivo, we have utilized DNA-PKcs-/- and Atm-/- cell lines and mouse embryonic fibroblasts. We find that H2AX phosphorylation and nuclear focus formation are normal in DNA-PKcs-/- cells and severely compromised in Atm-/- cells. We also find that ATM can phosphorylate H2AX in vitro and that ectopic expression of ATM in Atm-/- fibroblasts restores H2AX phosphorylation in vivo. The minimal H2AX phosphorylation in Atm-/- fibroblasts can be abolished by low concentrations of wortmannin suggesting that DNA-PK, rather than ATR, is responsible for low levels of H2AX phosphorylation in the absence of ATM. Our results clearly establish ATM as the major kinase involved in the phosphorylation of H2AX and suggest that ATM is one of the earliest kinases to be activated in the cellular response to double-strand breaks.

* This work was funded in part by the United States Department of Energy and by National Institutes of Health Grant CA50519 (to D. J. C.).The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

Dagger Present address: Life Sciences Division, Tottori University, Tottori 683-8503, Japan.

§ To whom correspondence should be addressed: Life Sciences Division, Lawrence Berkeley National Laboratory, 1 Cyclotron Rd., Berkeley, CA 94720. Tel.: 510-495-2861; Fax: 510-486-6816; E-mail: djchen@lbl.gov.

Copyright © 2001 by The American Society for Biochemistry and Molecular Biology, Inc.


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