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Molecular and Cellular Biology, September 2002, p. 6521-6532, Vol. 22, No. 18
0270-7306/02/$04.00+0     DOI: 10.1128/MCB.22.18.6521-6532.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.

Chk2 Is a Tumor Suppressor That Regulates Apoptosis in both an Ataxia Telangiectasia Mutated (ATM)-Dependent and an ATM-Independent Manner

Atsushi Hirao,1,2 Alison Cheung,1 Gordon Duncan,1 Pierre-Marie Girard,3 Andrew J. Elia,1 Andrew Wakeham,1 Hitoshi Okada,1 Talin Sarkissian,1 Jorge A. Wong,1 Takashi Sakai,1 Elisa de Stanchina,4 Robert G. Bristow,5 Toshio Suda,2 Scott W. Lowe,4 Penny A. Jeggo,3 Stephen J. Elledge,6 and Tak W. Mak1*

Departments of Medical Biophysics and Immunology, Ontario Cancer Institute, University of Toronto, Toronto, Ontario M5G 2C1,1 Department of Radiation Oncology and Department of Medical Biophysics, Ontario Cancer Institute, University of Toronto, Toronto, Ontario M5G 2M9, Canada,5 Genome Damage and Stability Centre, University of Sussex, Falmer, Sussex BN1 9RR, United Kingdom,3 Cold Spring Harbor Laboratory, Cold Spring Harbor, New York 11724,4 Verna and Marrs McLean Department of Biochemistry and Molecular Biology and Department of Molecular and Human Genetics, Howard Hughes Medical Institute, Baylor College of Medicine, Houston, Texas 77030,6 The Sakaguchi Laboratory of Developmental Biology, School of Medicine, Keio University, Tokyo 160-8582, Japan2

Received 5 March 2002/ Accepted 18 June 2002

In response to ionizing radiation (IR), the tumor suppressor p53 is stabilized and promotes either cell cycle arrest or apoptosis. Chk2 activated by IR contributes to this stabilization, possibly by direct phosphorylation. Like p53, Chk2 is mutated in patients with Li-Fraumeni syndrome. Since the ataxia telangiectasia mutated (ATM) gene is required for IR-induced activation of Chk2, it has been assumed that ATM and Chk2 act in a linear pathway leading to p53 activation. To clarify the role of Chk2 in tumorigenesis, we generated gene-targeted Chk2-deficient mice. Unlike ATM-/- and p53-/- mice, Chk2-/- mice do not spontaneously develop tumors, although Chk2 does suppress 7,12-dimethylbenzanthracene-induced skin tumors. Tissues from Chk2-/- mice, including those from the thymus, central nervous system, fibroblasts, epidermis, and hair follicles, show significant defects in IR-induced apoptosis or impaired G1/S arrest. Quantitative comparison of the G1/S checkpoint, apoptosis, and expression of p53 proteins in Chk2-/- versus ATM-/- thymocytes suggested that Chk2 can regulate p53-dependent apoptosis in an ATM-independent manner. IR-induced apoptosis was restored in Chk2-/- thymocytes by reintroduction of the wild-type Chk2 gene but not by a Chk2 gene in which the sites phosphorylated by ATM and ataxia telangiectasia and rad3+ related (ATR) were mutated to alanine. ATR may thus selectively contribute to p53-mediated apoptosis. These data indicate that distinct pathways regulate the activation of p53 leading to cell cycle arrest or apoptosis.

* Corresponding author. Mailing address: Ontario Cancer Institute, University of Toronto, 620 University Ave., Suite 706, Toronto, Ontario M5G 2C1, Canada. Phone: (416) 204-2236. Fax: (416) 204-5300. E-mail: tmak{at}uhnres.utoronto.ca.

Molecular and Cellular Biology, September 2002, p. 6521-6532, Vol. 22, No. 18
0022-538X/02/$04.00+0     DOI: 10.1128/MCB.22.18.6521-6532.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.



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