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Molecular and Cellular Biology, March 2000, p. 2198-2208, Vol. 20, No. 6
0270-7306/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

Activation of Apoptosis Signal-Regulating Kinase 1 (ASK1) by Tumor Necrosis Factor Receptor-Associated Factor 2 Requires Prior Dissociation of the ASK1 Inhibitor Thioredoxindagger

Hong Liu,1 Hideki Nishitoh,2 Hidenori Ichijo,2 and John M. Kyriakis1,*

The Diabetes Research Laboratory, Medical Services, Massachusetts General Hospital and The Department of Medicine, Harvard Medical School, Charlestown, Massachusetts 02129,1 and The Department of Biomaterials Science, Faculty of Dentistry, Tokyo Medical and Dental University, Tokyo, Japan2

Received 17 September 1999/Returned for modification 24 November 1999/Accepted 20 December 1999

The stress-activated protein kinases (SAPKs, also called c-Jun NH2-terminal kinases) and the p38s, two mitogen-activated protein kinase (MAPK) subgroups activated by cytokines of the tumor necrosis factor (TNF) family, are pivotal to the de novo gene expression elicited as part of the inflammatory response. Apoptosis signal-regulating kinase 1 (ASK1) is a MAPK kinase kinase (MAP3K) that activates both the SAPKs and p38s in vivo. Here we show that TNF receptor (TNFR) associated factor 2 (TRAF2), an adapter protein that couples TNFRs to the SAPKs and p38s, can activate ASK1 in vivo and can interact in vivo with the amino- and carboxyl-terminal noncatalytic domains of the ASK1 polypeptide. Expression of the amino-terminal noncatalytic domain of ASK1 can inhibit TNF and TRAF2 activation of SAPK. TNF can stimulate the production of reactive oxygen species (ROS), and the redox-sensing enzyme thioredoxin (Trx) is an endogenous inhibitor of ASK1. We also show that expression of TRAF2 fosters the production of ROS in transfected cells. We demonstrate that Trx significantly inhibits TRAF2 activation of SAPK and blocks the ASK1-TRAF2 interaction in a reaction reversed by oxidants. Finally, the mechanism of ASK1 activation involves, in part, homo-oligomerization. We show that expression of ASK1 with TRAF2 enhances in vivo ASK1 homo-oligomerization in a manner dependent, in part, upon the TRAF2 RING effector domain and the generation of ROS. Thus, activation of ASK1 by TNF requires the ROS-mediated dissociation of Trx possibly followed by the binding of TRAF2 and consequent ASK1 homo-oligomerization.

* Corresponding author. Mailing address: Diabetes Research Laboratory, Massachusetts General Hospital East, 149 13th St., Charlestown, MA 02129. Phone: (617) 726-9451. Fax: (617) 726-9452. E-mail: kyriakis{at}helix.mgh.harvard.edu.

dagger This paper is dedicated to the memory of Eleanor Troccoli.

Molecular and Cellular Biology, March 2000, p. 2198-2208, Vol. 20, No. 6
0270-7306/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.


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