J. Exp. Med., Volume 188, Number 8, October 19, 1998 1413-1419

Fractalkine and CX₃CR1 Mediate a Novel Mechanism of Leukocyte Capture, Firm Adhesion, and Activation under Physiologic Flow

By Alan M. Fong,^* Lisa A. Robinson,^§ Douglas A. Steeber, Thomas F. Tedder, Osamu Yoshie, Toshio Imai, and Dhavalkumar D. Patel^*

From the ^* Department of Medicine, the  Department of Immunology, and the ^§ Department of Pediatrics, Duke University Medical Center, Durham, North Carolina 27710; and the  Shionogi Institute for Medical Science, Settsu 566, Japan

Leukocyte migration into sites of inflammation involves multiple molecular interactions between leukocytes and vascular endothelial cells, mediating sequential leukocyte capture, rolling, and firm adhesion. In this study, we tested the role of molecular interactions between fractalkine (FKN), a transmembrane mucin-chemokine hybrid molecule expressed on activated endothelium, and its receptor (CX₃CR1) in leukocyte capture, firm adhesion, and activation under physiologic flow conditions. Immobilized FKN fusion proteins captured resting peripheral blood mononuclear cells at physiologic wall shear stresses and induced firm adhesion of resting monocytes, resting and interleukin (IL)-2-activated CD8⁺ T lymphocytes and IL-2-activated NK cells. FKN also induced cell shape change in firmly adherent monocytes and IL-2-activated lymphocytes. CX₃CR1-transfected K562 cells, but not control K562 cells, firmly adhered to FKN-expressing ECV-304 cells (ECV-FKN) and tumor necrosis factor -activated human umbilical vein endothelial cells. This firm adhesion was not inhibited by pertussis toxin, EDTA/EGTA, or antiintegrin antibodies, indicating that the firm adhesion was integrin independent. In summary, FKN mediated the rapid capture, integrin-independent firm adhesion, and activation of circulating leukocytes under flow. Thus, FKN and CX₃CR1 mediate a novel pathway for leukocyte trafficking.

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• Balabanian, K., Foussat, A., Dorfmuller, P., Durand-Gasselin, I., Capel, F., Bouchet-Delbos, L., Portier, A., Marfaing-Koka, A., Krzysiek, R., Rimaniol, A.-C., Simonneau, G., Emilie, D., Humbert, M. (2002). CX3C Chemokine Fractalkine in Pulmonary Arterial Hypertension. Am. J. Respir. Crit. Care Med. 165: 1419-1425 [Abstract] [Full Text]  
• Ludwig, A., Berkhout, T., Moores, K., Groot, P., Chapman, G. (2002). Fractalkine Is Expressed by Smooth Muscle Cells in Response to IFN-{gamma} and TNF-{alpha} and Is Modulated by Metalloproteinase Activity. J. Immunol. 168: 604-612 [Abstract] [Full Text]  
• Tanaka, R., Yoshida, A., Murakami, T., Baba, E., Lichtenfeld, J., Omori, T., Kimura, T., Tsurutani, N., Fujii, N., Wang, Z.-X., Peiper, S. C., Yamamoto, N., Tanaka, Y. (2001). Unique Monoclonal Antibody Recognizing the Third Extracellular Loop of CXCR4 Induces Lymphocyte Agglutination and Enhances Human Immunodeficiency Virus Type 1-Mediated Syncytium Formation and Productive Infection. J. Virol. 75: 11534-11543 [Abstract] [Full Text]  
• Volin, M. V., Woods, J. M., Amin, M. A., Connors, M. A., Harlow, L. A., Koch, A. E. (2001). Fractalkine: A Novel Angiogenic Chemokine in Rheumatoid Arthritis. Am. J. Pathol. 159: 1521-1530 [Abstract] [Full Text]  
• Foussat, A., Bouchet-Delbos, L., Berrebi, D., Durand-Gasselin, I., Coulomb-L'Hermine, A., Krzysiek, R., Galanaud, P., Levy, Y., Emilie, D. (2001). Deregulation of the expression of the fractalkine/fractalkine receptor complex in HIV-1-infected patients. Blood 98: 1678-1686 [Abstract] [Full Text]  
• Wayne Alexander, R. (2001). Cytokine Receptor CX3CR-1 and Fractalkine: New Factors in the Atherosclerosis Drama?. Circ. Res. 89: 376-377 [Full Text]  
• Fujimoto, K., Imaizumi, T., Yoshida, H., Takanashi, S., Okumura, K., Satoh, K. (2001). Interferon-gamma Stimulates Fractalkine Expression in Human Bronchial Epithelial Cells and Regulates Mononuclear Cell Adherence. Am. J. Respir. Cell Mol. Bio. 25: 233-238 [Abstract] [Full Text]  
• Beisser, P. S., Laurent, L., Virelizier, J.-L., Michelson, S. (2001). Human Cytomegalovirus Chemokine Receptor Gene US28 Is Transcribed in Latently Infected THP-1 Monocytes. J. Virol. 75: 5949-5957 [Abstract] [Full Text]  
• Greaves, D. R., Hakkinen, T., Lucas, A. D., Liddiard, K., Jones, E., Quinn, C. M., Senaratne, J., Green, F. R., Tyson, K., Boyle, J., Shanahan, C., Weissberg, P. L., Gordon, S., Yla-Hertualla, S. (2001). Linked Chromosome 16q13 Chemokines, Macrophage-Derived Chemokine, Fractalkine, and Thymus- and Activation-Regulated Chemokine, Are Expressed in Human Atherosclerotic Lesions. Arterioscler. Thromb. Vasc. Bio. 21: 923-929 [Abstract] [Full Text]  
• Chan, J. R., Hyduk, S. J., Cybulsky, M. I. (2001). Chemoattractants Induce a Rapid and Transient Upregulation of Monocyte {alpha}4 Integrin Affinity for Vascular Cell Adhesion Molecule 1 Which Mediates Arrest: An Early Step in the Process of Emigration. J. Exp. Med. 193: 1149-1158 [Abstract] [Full Text]  
• Cook, D. N., Chen, S.-C., Sullivan, L. M., Manfra, D. J., Wiekowski, M. T., Prosser, D. M., Vassileva, G., Lira, S. A. (2001). Generation and Analysis of Mice Lacking the Chemokine Fractalkine. Mol. Cell. Biol. 21: 3159-3165 [Abstract] [Full Text]  
• Zernecke, A., Weber, K. S. C., Erwig, L. P., Kluth, D. C., Schroppel, B., Rees, A. J., Weber, C. (2001). Combinatorial Model of Chemokine Involvement in Glomerular Monocyte Recruitment: Role of CXC Chemokine Receptor 2 in Infiltration During Nephrotoxic Nephritis. J. Immunol. 166: 5755-5762 [Abstract] [Full Text]  
• Qiu, B., Frait, K. A., Reich, F., Komuniecki, E., Chensue, S. W. (2001). Chemokine Expression Dynamics in Mycobacterial (Type-1) and Schistosomal (Type-2) Antigen-Elicited Pulmonary Granuloma Formation. Am. J. Pathol. 158: 1503-1515 [Abstract] [Full Text]  
• Moatti, D., Faure, S., Fumeron, F., Amara, M. E. W., Seknadji, P., McDermott, D. H., Debre, P., Aumont, M. C., Murphy, P. M., de Prost, D., Combadiere, C. (2001). Polymorphism in the fractalkine receptor CX3CR1 as a genetic risk factor for coronary artery disease. Blood 97: 1925-1928 [Abstract] [Full Text]  
• Cambien, B., Pomeranz, M., Schmid-Antomarchi, H., Millet, M.-A., Breittmayer, V., Rossi, B., Schmid-Alliana, A. (2001). Signal transduction pathways involved in soluble fractalkine-induced monocytic cell adhesion. Blood 97: 2031-2037 [Abstract] [Full Text]  
• Ding, Z., Xiong, K., Issekutz, T. B. (2001). Chemokines stimulate human T lymphocyte transendothelial migration to utilize VLA-4 in addition to LFA-1. J. Leukoc. Biol. 69: 458-466 [Abstract] [Full Text]  

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