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J. Biol. Chem. 281 (39): 28802-28810

© 2006 by The American Society for Biochemistry and Molecular Biology, Inc.

Osmotic Stress Activates the TAK1-JNK Pathway While Blocking TAK1-mediated NF-{kappa}B Activation

TAO2 REGULATES TAK1 PATHWAYS*

Wei-Chun HuangFu{ddagger}, Emily Omori{ddagger}§, Shizuo Akira, Kunihiro Matsumoto§||, , and Jun Ninomiya-Tsuji{ddagger}1

{ddagger}Department of Environmental and Molecular Toxicology, North Carolina State University, Raleigh, North Carolina 27695, the §Department of Molecular Biology, Graduate School of Science, Nagoya University, Nagoya 464-8602, Japan, the Department of Host Defense, Research Institute for Microbial Diseases, Osaka University, Osaka 565-0871, Japan, and ||Solution Oriented Research for Science and Technology (SORST), Japan Science and Technology Agency, Kawaguchi 332-0012, Japan

Abstract: Osmotic stress activates MAPKs, including JNK and p38, which play important roles in cellular stress responses. Transforming growth factor-beta-activated kinase 1 (TAK1) is a member of the MAPK kinase kinase (MAPKKK) family and can activate JNK and p38. TAK1 can also activate I{kappa}B kinase (IKK) that leads to degradation of I{kappa}B and subsequent NF-{kappa}B activation. We found that TAK1 is essential for osmotic stress-induced activation of JNK but is not an exclusive mediator of p38 activation. Furthermore, we found that although TAK1 was highly activated upon osmotic stress, it could not induce degradation of I{kappa}B or activation of NF-{kappa}B. These results suggest that TAK1 activity is somehow modulated to function specifically in osmotic stress signaling, leading to the activation of JNK but not of IKK. To elucidate the mechanism underlying this modulation, we screened for potential TAK1-binding proteins. We found that TAO2 (thousand-and-one amino acid kinase 2) associates with TAK1 and can inhibit TAK1-mediated activation of NF-{kappa}B but not of JNK. We observed that TAO2 can interfere with the interaction between TAK1 and IKK and thus may regulate TAK1 function. TAK1 is activated by many distinct stimuli, including cytokines and stresses, and regulation by TAO2 may be important to activate specific intracellular signaling pathways that are unique to osmotic stress.


Received for publication April 14, 2006. Revision received August 4, 2006.

* This work was supported by special grants for SORST and Advanced Research on Cancer from the Ministry of Education, Culture, and Science of Japan (to K. M.) and by National Institutes of Health Grants GM068812 and AR050972 (to J. N. T.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

1 To whom correspondence should be addressed: Dept. of Environmental and Molecular Toxicology, North Carolina State University, Campus Box 7633, Raleigh, NC 27695. Tel.: 919-513-1586; Fax: 919-515-7169; E-mail: Jun_Tsuji{at}ncsu.edu.


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