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J. Biol. Chem., Vol. 276, Issue 41, 37993-38001, October 12, 2001
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From the Fractalkine (CX3CL1) is an unusual
member of the chemokine family that is synthesized with its chemokine
domain at the end of a mucin-rich, transmembrane stalk. This
membrane-bound localization allows fractalkine to function as an
adhesion molecule for cells bearing its receptor, CX3CR1. In addition,
fractalkine can be proteolytically released from the cell surface,
generating a soluble molecule that functions as a chemoattractant
similar to the other members of the chemokine family. In this study, we
have examined the mechanisms that regulate the conversion between these
two functionally distinct forms of fractalkine. We demonstrate that under normal conditions fractalkine is synthesized as an intracellular precursor that is rapidly transported to the cell surface where it
becomes a target for metalloproteinase-dependent cleavage
that causes the release of a fragment containing the majority of the fractalkine extracellular domain. We show that the cleavage of fractalkine can be markedly enhanced by stimulating cells with phorbol
12-myristate 13-acetate (PMA), and we identify tumor necrosis factor-
Tumor Necrosis Factor-
-converting Enzyme (ADAM17) Mediates the
Cleavage and Shedding of Fractalkine (CX3CL1)*
§,§,
,, and§§
Department of Pathology, University of
Washington, Harborview Medical Center, Seattle, Washington 98104, ¶ Memorial Sloan-Kettering Cancer Center,
New York, New York 10021, School of Biological Sciences,
University of East Anglia, Norwich NR4 7TJ, United Kingdom,
** Sir William Dunn School of Pathology, University of
Oxford, Oxford OX1 3RE, United Kingdom, and
Pacific Northwest Research Institute,
Seattle, Washington 98122
converting enzyme (TACE; ADAM17) as the protease responsible for this PMA-induced fractalkine release. In addition, we provide data
showing that TACE-mediated fractalkine cleavage occurs at a site
distinct from the dibasic juxtamembrane motif that had been suggested
previously based on protein sequence homologies. The identification of
TACE as a major protease responsible for the conversion of fractalkine
from a membrane-bound adhesion molecule to a soluble chemoattractant
will provide new information for understanding the physiological
function of this chemokine.
*
This work was supported by National Institutes of Health
Grants HL18645 (to E. W. R) and DK59778 (to P. J. D.), the Paul G. Allen Foundation for Medical Research (to K. J. G), the American Heart Association (to P. J. G), and the British Heart Foundation (to
D. R. G).The costs of publication of this
article were defrayed in part by the
payment of page charges. The article
must therefore be hereby marked
"advertisement" in
accordance with 18 U.S.C. Section
1734 solely to indicate this fact.
Copyright © 2001 by The American Society for Biochemistry and Molecular Biology, Inc.
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D. V. Bax, A. J. Messent, J. Tart, M. van Hoang, J. Kott, R. A. Maciewicz, and M. J. Humphries Integrin {alpha}5{beta}1 and ADAM-17 Interact in Vitro and Co-localize in Migrating HeLa Cells J. Biol. Chem., May 21, 2004; 279(21): 22377 - 22386. [Abstract] [Full Text] [PDF]
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S. Abel, C. Hundhausen, R. Mentlein, A. Schulte, T. A. Berkhout, N. Broadway, D. Hartmann, R. Sedlacek, S. Dietrich, B. Muetze, et al. The Transmembrane CXC-Chemokine Ligand 16 Is Induced by IFN-{gamma} and TNF-{alpha} and Shed by the Activity of the Disintegrin-Like Metalloproteinase ADAM10 J. Immunol., May 15, 2004; 172(10): 6362 - 6372. [Abstract] [Full Text] [PDF]
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M. Daoudi, E. Lavergne, A. Garin, N. Tarantino, P. Debre, F. Pincet, C. Combadiere, and P. Deterre Enhanced Adhesive Capacities of the Naturally Occurring Ile249-Met280 Variant of the Chemokine Receptor CX3CR1 J. Biol. Chem., May 7, 2004; 279(19): 19649 - 19657. [Abstract] [Full Text] [PDF]
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P. J. Gough, K. J. Garton, P. T. Wille, M. Rychlewski, P. J. Dempsey, and E. W. Raines A Disintegrin and Metalloproteinase 10-Mediated Cleavage and Shedding Regulates the Cell Surface Expression of CXC Chemokine Ligand 16 J. Immunol., March 15, 2004; 172(6): 3678 - 3685. [Abstract] [Full Text] [PDF]
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K.-P. Xu, Y. Ding, J. Ling, Z. Dong, and F.-S. X. Yu Wound-Induced HB-EGF Ectodomain Shedding and EGFR Activation in Corneal Epithelial Cells Invest. Ophthalmol. Vis. Sci., March 1, 2004; 45(3): 813 - 820. [Abstract] [Full Text] [PDF]
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A. C. Cruz, B. T. Frank, S. T. Edwards, P. F. Dazin, J. J. Peschon, and K. C. Fang Tumor Necrosis Factor-{alpha}-converting Enzyme Controls Surface Expression of c-Kit and Survival of Embryonic Stem Cell-derived Mast Cells J. Biol. Chem., February 13, 2004; 279(7): 5612 - 5620. [Abstract] [Full Text] [PDF]
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T. Shimaoka, T. Nakayama, N. Fukumoto, N. Kume, S. Takahashi, J. Yamaguchi, M. Minami, K. Hayashida, T. Kita, J. Ohsumi, et al. Cell surface-anchored SR-PSOX/CXC chemokine ligand 16 mediates firm adhesion of CXC chemokine receptor 6-expressing cells J. Leukoc. Biol., February 1, 2004; 75(2): 267 - 274. [Abstract] [Full Text] [PDF]
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B. Chandrasekar, S. Bysani, and S. Mummidi CXCL16 Signals via Gi, Phosphatidylinositol 3-Kinase, Akt, I{kappa}B Kinase, and Nuclear Factor-{kappa}B and Induces Cell-Cell Adhesion and Aortic Smooth Muscle Cell Proliferation J. Biol. Chem., January 30, 2004; 279(5): 3188 - 3196. [Abstract] [Full Text] [PDF]
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S. Vitale, A. Schmid-Alliana, V. Breuil, M. Pomeranz, M.-A. Millet, B. Rossi, and H. Schmid-Antomarchi Soluble Fractalkine Prevents Monocyte Chemoattractant Protein-1-Induced Monocyte Migration via Inhibition of Stress-Activated Protein Kinase 2/p38 and Matrix Metalloproteinase Activities J. Immunol., January 1, 2004; 172(1): 585 - 592. [Abstract] [Full Text] [PDF]
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H. Umehara, E. T. Bloom, T. Okazaki, Y. Nagano, O. Yoshie, and T. Imai Fractalkine in Vascular Biology: From Basic Research to Clinical Disease Arterioscler. Thromb. Vasc. Biol., January 1, 2004; 24(1): 34 - 40. [Abstract] [Full Text] [PDF]
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J. Barlic, J. M. Sechler, and P. M. Murphy IL-15 and IL-2 oppositely regulate expression of the chemokine receptor CX3CR1 Blood, November 15, 2003; 102(10): 3494 - 3503. [Abstract] [Full Text] [PDF]
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 S. P. Umland, C. G. Garlisi, H. Shah, Y. Wan, J. Zou, K. E. Devito, W.-M. Huang, E. L. Gustafson, and R. Ralston Human ADAM33 Messenger RNA Expression Profile and Post-Transcriptional Regulation Am. J. Respir. Cell Mol. Biol., November 1, 2003; 29(5): 571 - 582. [Abstract] [Full Text]
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F F Mohammed, D S Smookler, and R Khokha Metalloproteinases, inflammation, and rheumatoid arthritis Ann Rheum Dis, November 1, 2003; 62(90002): ii43 - 47. [Abstract] [Full Text] [PDF]
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D. Hahn, A. Pischitzis, S. Roesmann, M. K. Hansen, B. Leuenberger, U. Luginbuehl, and E. E. Sterchi Phorbol 12-Myristate 13-Acetate-induced Ectodomain Shedding and Phosphorylation of the Human Meprin{beta} Metalloprotease J. Biol. Chem., October 31, 2003; 278(44): 42829 - 42839. [Abstract] [Full Text] [PDF]
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V. Matthews, B. Schuster, S. Schutze, I. Bussmeyer, A. Ludwig, C. Hundhausen, T. Sadowski, P. Saftig, D. Hartmann, K.-J. Kallen, et al. Cellular Cholesterol Depletion Triggers Shedding of the Human Interleukin-6 Receptor by ADAM10 and ADAM17 (TACE) J. Biol. Chem., October 3, 2003; 278(40): 38829 - 38839. [Abstract] [Full Text] [PDF]
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K. J. Garton, P. J. Gough, J. Philalay, P. T. Wille, C. P. Blobel, R. H. Whitehead, P. J. Dempsey, and E. W. Raines Stimulated Shedding of Vascular Cell Adhesion Molecule 1 (VCAM-1) Is Mediated by Tumor Necrosis Factor-{alpha}-converting Enzyme (ADAM 17) J. Biol. Chem., September 26, 2003; 278(39): 37459 - 37464. [Abstract] [Full Text] [PDF]
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B. Walcheck, S. R. Alexander, C. A. St. Hill, and E. Matala ADAM-17-independent shedding of L-selectin J. Leukoc. Biol., September 1, 2003; 74(3): 389 - 394. [Abstract] [Full Text] [PDF]
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C. Contin, V. Pitard, T. Itai, S. Nagata, J.-F. Moreau, and J. Dechanet-Merville Membrane-anchored CD40 Is Processed by the Tumor Necrosis Factor-{alpha}-converting Enzyme: IMPLICATIONS FOR CD40 SIGNALING J. Biol. Chem., August 29, 2003; 278(35): 32801 - 32809. [Abstract] [Full Text] [PDF]
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C. Hundhausen, D. Misztela, T. A. Berkhout, N. Broadway, P. Saftig, K. Reiss, D. Hartmann, F. Fahrenholz, R. Postina, V. Matthews, et al. The disintegrin-like metalloproteinase ADAM10 is involved in constitutive cleavage of CX3CL1 (fractalkine) and regulates CX3CL1-mediated cell-cell adhesion Blood, August 15, 2003; 102(4): 1186 - 1195. [Abstract] [Full Text] [PDF]
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A. Borroto, S. Ruiz-Paz, T. V. de la Torre, M. Borrell-Pages, A. Merlos-Suarez, A. Pandiella, C. P. Blobel, J. Baselga, and J. Arribas Impaired Trafficking and Activation of Tumor Necrosis Factor-{alpha}-converting Enzyme in Cell Mutants Defective in Protein Ectodomain Shedding J. Biol. Chem., July 3, 2003; 278(28): 25933 - 25939. [Abstract] [Full Text] [PDF]
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M. D. Silverman, D. O. Zamora, Y. Pan, P. V. Texeira, S.-H. Baek, S. R. Planck, and J. T. Rosenbaum Constitutive and Inflammatory Mediator-Regulated Fractalkine Expression in Human Ocular Tissues and Cultured Cells Invest. Ophthalmol. Vis. Sci., April 1, 2003; 44(4): 1608 - 1615. [Abstract] [Full Text] [PDF]
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A. Thathiah, C. P. Blobel, and D. D. Carson Tumor Necrosis Factor-alpha Converting Enzyme/ADAM 17 Mediates MUC1 Shedding J. Biol. Chem., January 24, 2003; 278(5): 3386 - 3394. [Abstract] [Full Text] [PDF]
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 D. F. Seals and S. A. Courtneidge The ADAMs family of metalloproteases: multidomain proteins with multiple functions Genes & Dev., January 1, 2003; 17(1): 7 - 30. [Full Text] [PDF]
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T Seifert, B C Kieseier, S Ropele, S Strasser-Fuchs, F Quehenberger, F Fazekas, and H-P Hartung TACE mRNA expression in peripheral mononuclear cells precedes new lesions on MRI in multiple sclerosis Multiple Sclerosis, December 1, 2002; 8(6): 447 - 451. [Abstract] [PDF]
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K. A. Hintz, A. J. Rassias, K. Wardwell, M. L. Moss, P. M. Morganelli, P. A. Pioli, A. L. Givan, P. K. Wallace, M. P. Yeager, and P. M. Guyre Endotoxin induces rapid metalloproteinase-mediated shedding followed by up-regulation of the monocyte hemoglobin scavenger receptor CD163 J. Leukoc. Biol., October 1, 2002; 72(4): 711 - 717. [Abstract] [Full Text] [PDF]
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M. Nishimura, H. Umehara, T. Nakayama, O. Yoneda, K. Hieshima, M. Kakizaki, N. Dohmae, O. Yoshie, and T. Imai Dual Functions of Fractalkine/CX3C Ligand 1 in Trafficking of Perforin+/Granzyme B+ Cytotoxic Effector Lymphocytes That Are Defined by CX3CR1 Expression J. Immunol., June 15, 2002; 168(12): 6173 - 6180. [Abstract] [Full Text] [PDF]
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 T. J. Williams Stalking the Chemokine Am. J. Respir. Crit. Care Med., May 15, 2002; 165(10): 1350 - 1351. [Full Text] [PDF]
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K. Balabanian, A. Foussat, P. Dorfmuller, I. Durand-Gasselin, F. Capel, L. Bouchet-Delbos, A. Portier, A. Marfaing-Koka, R. Krzysiek, A.-C. Rimaniol, et al. CX3C Chemokine Fractalkine in Pulmonary Arterial Hypertension Am. J. Respir. Crit. Care Med., May 15, 2002; 165(10): 1419 - 1425. [Abstract] [Full Text] [PDF]
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A. Ludwig, T. Berkhout, K. Moores, P. Groot, and G. Chapman Fractalkine Is Expressed by Smooth Muscle Cells in Response to IFN-{gamma} and TNF-{alpha} and Is Modulated by Metalloproteinase Activity J. Immunol., January 15, 2002; 168(2): 604 - 612. [Abstract] [Full Text] [PDF]
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C.-L. Tsou, C. A. Haskell, and I. F. Charo Tumor Necrosis Factor-alpha -converting Enzyme Mediates the Inducible Cleavage of Fractalkine J. Biol. Chem., November 21, 2001; 276(48): 44622 - 44626. [Abstract] [Full Text] [PDF]
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