Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.
Subscribe

Logo for

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.

THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Role for TAK1 in cigarette smoke-induced proinflammatory signaling and IL-8 release by human airway smooth muscle cells.
T. Pera, C. Atmaj, M. van der Vegt, A. J. Halayko, J. Zaagsma, and H. Meurs (2012)
Am J Physiol Lung Cell Mol Physiol 303, L272-L278
   Abstract »    Full Text »    PDF »
Osmotic Stress Regulates Mammalian Target of Rapamycin (mTOR) Complex 1 via c-Jun N-terminal Kinase (JNK)-mediated Raptor Protein Phosphorylation.
D. Kwak, S. Choi, H. Jeong, J.-H. Jang, Y. Lee, H. Jeon, M. N. Lee, J. Noh, K. Cho, J. S. Yoo, et al. (2012)
J. Biol. Chem. 287, 18398-18407
   Abstract »    Full Text »    PDF »
TGF-{beta}-activated Kinase 1 (TAK1) and Apoptosis Signal-regulating Kinase 1 (ASK1) Interact with the Promyogenic Receptor Cdo to Promote Myogenic Differentiation via Activation of p38MAPK Pathway.
P. Tran, S.-M. Ho, B.-G. Kim, T. A. Vuong, Y.-E. Leem, G.-U. Bae, and J.-S. Kang (2012)
J. Biol. Chem. 287, 11602-11615
   Abstract »    Full Text »    PDF »
c-Jun N-terminal kinase phosphorylates DCP1a to control formation of P bodies.
K. Rzeczkowski, K. Beuerlein, H. Muller, O. Dittrich-Breiholz, H. Schneider, D. Kettner-Buhrow, H. Holtmann, and M. Kracht (2011)
J. Cell Biol. 194, 581-596
   Abstract »    Full Text »    PDF »
Arsenic Trioxide-Dependent Activation of Thousand-and-One Amino Acid Kinase 2 and Transforming Growth Factor-{beta}-Activated Kinase 1.
J. L. McNeer, D. J. Goussetis, A. Sassano, B. Dolniak, B. Kroczynska, H. Glaser, J. K. Altman, and L. C. Platanias (2010)
Mol. Pharmacol. 77, 828-835
   Abstract »    Full Text »    PDF »
Transforming Growth Factor-{beta}-activated Kinase 1 Is an Essential Regulator of Myogenic Differentiation.
S. Bhatnagar, A. Kumar, D. Y. Makonchuk, H. Li, and A. Kumar (2010)
J. Biol. Chem. 285, 6401-6411
   Abstract »    Full Text »    PDF »
Two Mechanistically and Temporally Distinct NF-{kappa}B Activation Pathways in IL-1 Signaling.
K. Yamazaki, J. Gohda, A. Kanayama, Y. Miyamoto, H. Sakurai, M. Yamamoto, S. Akira, H. Hayashi, B. Su, and J.-i. Inoue (2009)
Science Signaling 2, ra66
   Abstract »    Full Text »    PDF »
TNF-Like Weak Inducer of Apoptosis (TWEAK) Activates Proinflammatory Signaling Pathways and Gene Expression through the Activation of TGF-{beta}-Activated Kinase 1.
M. Kumar, D. Y. Makonchuk, H. Li, A. Mittal, and A. Kumar (2009)
J. Immunol. 182, 2439-2448
   Abstract »    Full Text »    PDF »
Physiology of Cell Volume Regulation in Vertebrates.
E. K. Hoffmann, I. H. Lambert, and S. F. Pedersen (2009)
Physiol Rev 89, 193-277
   Abstract »    Full Text »    PDF »
TAK1-binding Protein 1, TAB1, Mediates Osmotic Stress-induced TAK1 Activation but Is Dispensable for TAK1-mediated Cytokine Signaling.
M. Inagaki, E. Omori, J.-Y. Kim, Y. Komatsu, G. Scott, M. K. Ray, G. Yamada, K. Matsumoto, Y. Mishina, and J. Ninomiya-Tsuji (2008)
J. Biol. Chem. 283, 33080-33086
   Abstract »    Full Text »    PDF »
TAK1 Regulates Reactive Oxygen Species and Cell Death in Keratinocytes, Which Is Essential for Skin Integrity.
E. Omori, S. Morioka, K. Matsumoto, and J. Ninomiya-Tsuji (2008)
J. Biol. Chem. 283, 26161-26168
   Abstract »    Full Text »    PDF »
Type 1 TNF Receptor Forms a Complex with and Uses Jak2 and c-Src to Selectively Engage Signaling Pathways That Regulate Transcription Factor Activity.
R. Pincheira, A. F. Castro, O. N. Ozes, P. S. Idumalla, and D. B. Donner (2008)
J. Immunol. 181, 1288-1298
   Abstract »    Full Text »    PDF »
Cellular Response to Hyperosmotic Stresses.
M. B. Burg, J. D. Ferraris, and N. I. Dmitrieva (2007)
Physiol Rev 87, 1441-1474
   Abstract »    Full Text »    PDF »

To Advertise     Find Products

Science Signaling. ISSN 1937-9145 (online), 1945-0877 (print). Pre-2008: Science's STKE. ISSN 1525-8882