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J. Biol. Chem., Vol. 281, Issue 6, 3157-3164, February 10, 2006
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Tumor Necrosis Factor-
-converting Enzyme (TACE/ADAM-17) Mediates the Ectodomain Cleavage of Intercellular Adhesion Molecule-1 (ICAM-1)*
11
2
From the
Department of Physiology and Biophysics, University of Louisville, Louisville, Kentucky 40292 and the Department of Oncology and Addenbrooke's Hospital, Cambridge Institute for Medical Research, Cambridge CB2 2XY, United Kingdom
Ectodomain shedding has emerged as an important regulatory step in the function of transmembrane proteins. Intercellular adhesion molecule-1 (ICAM-1), an adhesion receptor that mediates inflammatory and immune responses, undergoes shedding in the presence of inflammatory mediators and phorbol 12-myristate 13-acetate (PMA). The shedding of ICAM-1 in ICAM-1-transfected 293 cells upon PMA stimulation and in endothelial cells upon tumor necrosis factor-
stimulation was blocked by metalloproteinase inhibitors, whereas serine protease inhibitors were ineffective. p-Aminophenylmercuric acetate, a mercuric compound that is known to activate matrix metalloproteinases, up-regulated ICAM-1 shedding. TIMP-3 (but not TIMP-1 or -2) effectively blocked cleavage. This profile suggests the involvement of the ADAM family of proteases in the cleavage of ICAM-1. The introduction of enzymatically active tumor necrosis factor--converting enzyme (TACE) into ICAM-1-expressing cells up-regulated cleavage. Small interfering RNA directed against TACE blocked ICAM-1 cleavage. ICAM-1 transfected into TACE–– fibroblasts did not show increased shedding over constitutive levels in the presence of PMA, whereas cleavage did occur in ICAM-1-transfected TACE++ cells. These results indicate that ICAM-1 shedding is mediated by TACE. Blocking the shedding of ICAM-1 altered the cell adhesive function, as ICAM-1-mediated cell adhesion was up-regulated in the presence of TACE small interfering RNA and TIMP-3, but not TIMP-1. However, cleavage was found to occur at multiple sites within the stalk domain of ICAM-1, and numerous point mutations within the region did not affect cleavage, indicating that TACE-mediated cleavage of ICAM-1 may not be sequence-specific.
Received for publication, October 3, 2005 , and in revised form, December 1, 2005.
* This work was supported by National Institutes of Health Grant HL43721, an American Heart Association Established Investigator Award, and Jewish Hospital Foundation Grant 999497 (to S. E. D.); an American Heart Association Ohio Valley Affiliate postdoctoral fellowship award (to N. L. T. and S. D. S.); the Wellcome Trust (to G. M.); and the Medical Research Council (to W. R. E. and G. M.). 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 Both authors contributed equally to this work.
2 To whom correspondence should be addressed: Dept. of Physiology and Biophysics, Health Sciences Center A-1115, University of Louisville, 500 S. Preston St., Louisville, KY 40292. Tel.: 502-852-3194; Fax: 502-852-6239; E-mail: sedsou01{at}gwise.louisville.edu.
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