J. Exp. Med., Volume 187, Number 12, June 15, 1998 2009-2021

Interferon-inducible T Cell Alpha Chemoattractant (I-TAC): A Novel Non-ELR CXC Chemokine with Potent Activity on Activated T Cells through Selective High Affinity Binding to CXCR3

By Katherine E. Cole,^* Christine A. Strick,^* Timothy J. Paradis, Kevin T. Ogborne,^* Marcel Loetscher,^§ Ronald P. Gladue, Wen Lin,^* James G. Boyd,^* Bernhard Moser,^§ Douglas E. Wood,^* Barbara G. Sahagan,^* and Kuldeep Neote^*

From the ^* Department of Molecular Sciences and the  Department of Immunology, Central Research Division, Pfizer Inc., Groton, Connecticut 06340; and the ^§ Theodor Kocher Institute, University of Bern, CH-300-ern-9, Switzerland

Chemokines are essential mediators of normal leukocyte trafficking as well as of leukocyte recruitment during inflammation. We describe here a novel non-ELR CXC chemokine identified through sequence analysis of cDNAs derived from cytokine-activated primary human astrocytes. This novel chemokine, referred to as I-TAC (interferon-inducible T cell alpha chemoattractant), is regulated by interferon (IFN) and has potent chemoattractant activity for interleukin (IL)-2-activated T cells, but not for freshly isolated unstimulated T cells, neutrophils, or monocytes. I-TAC interacts selectively with CXCR3, which is the receptor for two other IFN-inducible chemokines, the IFN--inducible 10-kD protein (IP-10) and IFN-- induced human monokine (HuMig), but with a significantly higher affinity. In addition, higher potency and efficacy of I-TAC over IP-10 and HuMig is demonstrated by transient mobilization of intracellular calcium as well as chemotactic migration in both activated T cells and transfected cell lines expressing CXCR3. Stimulation of astrocytes with IFN- and IL-1 together results in an ~400,000-fold increase in I-TAC mRNA expression, whereas stimulating monocytes with either of the cytokines alone or in combination results in only a 100-fold increase in the level of I-TAC transcript. Moderate expression is also observed in pancreas, lung, thymus, and spleen. The high level of expression in IFN- and IL-1-stimulated astrocytes suggests that I-TAC could be a major chemoattractant for effector T cells involved in the pathophysiology of neuroinflammatory disorders, although I-TAC may also play a role in the migration of activated T cells during IFN-dominated immune responses.

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• Thomas, S. Y., Hou, R., Boyson, J. E., Means, T. K., Hess, C., Olson, D. P., Strominger, J. L., Brenner, M. B., Gumperz, J. E., Wilson, S. B., Luster, A. D. (2003). CD1d-Restricted NKT Cells Express a Chemokine Receptor Profile Indicative of Th1-Type Inflammatory Homing Cells. J. Immunol. 171: 2571-2580 [Abstract] [Full Text]  
• Singh, U. P., Singh, S., Taub, D. D., Lillard, J. W. Jr. (2003). Inhibition of IFN-{gamma}-Inducible Protein-10 Abrogates Colitis in IL-10-/- Mice. J. Immunol. 171: 1401-1406 [Abstract] [Full Text]  
• Xie, J. H., Nomura, N., Lu, M., Chen, S.-L., Koch, G. E., Weng, Y., Rosa, R., Di Salvo, J., Mudgett, J., Peterson, L. B., Wicker, L. S., DeMartino, J. A. (2003). Antibody-mediated blockade of the CXCR3 chemokine receptor results in diminished recruitment of T helper 1 cells into sites of inflammation. J. Leukoc. Biol. 73: 771-780 [Abstract] [Full Text]  
• Nau, G. J., Schlesinger, A., Richmond, J. F. L., Young, R. A. (2003). Cumulative Toll-Like Receptor Activation in Human Macrophages Treated with Whole Bacteria. J. Immunol. 170: 5203-5209 [Abstract] [Full Text]  
• Campanella, G. S. V., Lee, E. M. J., Sun, J., Luster, A. D. (2003). CXCR3 and Heparin Binding Sites of the Chemokine IP-10 (CXCL10). J. Biol. Chem. 278: 17066-17074 [Abstract] [Full Text]  
• Hill, N. J., Van Gunst, K., Sarvetnick, N. (2003). Th1 and Th2 Pancreatic Inflammation Differentially Affects Homing of Islet-Reactive CD4 Cells in Nonobese Diabetic Mice. J. Immunol. 170: 1649-1658 [Abstract] [Full Text]  
• Clark-Lewis, I., Mattioli, I., Gong, J.-H., Loetscher, P. (2003). Structure-Function Relationship between the Human Chemokine Receptor CXCR3 and Its Ligands. J. Biol. Chem. 278: 289-295 [Abstract] [Full Text]  
• Strieter, R. M., Belperio, J. A., Keane, M. P. (2002). CXC Chemokines in Angiogenesis Related to Pulmonary Fibrosis. Chest 122: 298S-301S [Abstract] [Full Text]  
• D'Ambrosio, D., Albanesi, C., Lang, R., Girolomoni, G., Sinigaglia, F., Laudanna, C. (2002). Quantitative Differences in Chemokine Receptor Engagement Generate Diversity in Integrin-Dependent Lymphocyte Adhesion. J. Immunol. 169: 2303-2312 [Abstract] [Full Text]  
• Salomon, I., Netzer, N., Wildbaum, G., Schif-Zuck, S., Maor, G., Karin, N. (2002). Targeting the Function of IFN-{gamma}-Inducible Protein 10 Suppresses Ongoing Adjuvant Arthritis. J. Immunol. 169: 2685-2693 [Abstract] [Full Text]  
• Inston, N. G., Cockwell, P. (2002). The evolving role of chemokines and their receptors in acute allograft rejection. Nephrol Dial Transplant 17: 1374-1379 [Full Text]  
• Hauser, A. E., Debes, G. F., Arce, S., Cassese, G., Hamann, A., Radbruch, A., Manz, R. A. (2002). Chemotactic Responsiveness Toward Ligands for CXCR3 and CXCR4 Is Regulated on Plasma Blasts During the Time Course of a Memory Immune Response. J. Immunol. 169: 1277-1282 [Abstract] [Full Text]  
• Park, M. K., Amichay, D., Love, P., Wick, E., Liao, F., Grinberg, A., Rabin, R. L., Zhang, H. H., Gebeyehu, S., Wright, T. M., Iwasaki, A., Weng, Y., DeMartino, J. A., Elkins, K. L., Farber, J. M. (2002). The CXC Chemokine Murine Monokine Induced by IFN-{gamma} (CXC Chemokine Ligand 9) Is Made by APCs, Targets Lymphocytes Including Activated B Cells, and Supports Antibody Responses to a Bacterial Pathogen In Vivo. J. Immunol. 169: 1433-1443 [Abstract] [Full Text]  
• Boztug, K., Carson, M. J., Pham-Mitchell, N., Asensio, V. C., DeMartino, J., Campbell, I. L. (2002). Leukocyte Infiltration, But Not Neurodegeneration, in the CNS of Transgenic Mice with Astrocyte Production of the CXC Chemokine Ligand 10. J. Immunol. 169: 1505-1515 [Abstract] [Full Text]  
• Zhao, D. X.-M., Hu, Y., Miller, G. G., Luster, A. D., Mitchell, R. N., Libby, P. (2002). Differential Expression of the IFN-{gamma}-Inducible CXCR3-Binding Chemokines, IFN-Inducible Protein 10, Monokine Induced by IFN, and IFN-Inducible T Cell {alpha} Chemoattractant in Human Cardiac Allografts: Association with Cardiac Allograft Vasculopathy and Acute Rejection. J. Immunol. 169: 1556-1560 [Abstract] [Full Text]  
• Fleischer, J., Grage-Griebenow, E., Kasper, B., Heine, H., Ernst, M., Brandt, E., Flad, H.-D., Petersen, F. (2002). Platelet Factor 4 Inhibits Proliferation and Cytokine Release of Activated Human T Cells. J. Immunol. 169: 770-777 [Abstract] [Full Text]  
• Belperio, J. A., Keane, M. P., Burdick, M. D., Lynch, J. P. III, Xue, Y. Y., Li, K., Ross, D. J., Strieter, R. M. (2002). Critical Role for CXCR3 Chemokine Biology in the Pathogenesis of Bronchiolitis Obliterans Syndrome. J. Immunol. 169: 1037-1049 [Abstract] [Full Text]  
• Ludwig, A., Schiemann, F., Mentlein, R., Lindner, B., Brandt, E. (2002). Dipeptidyl peptidase IV (CD26) on T cells cleaves the CXC chemokine CXCL11 (I-TAC) and abolishes the stimulating but not the desensitizing potential of the chemokine. J. Leukoc. Biol. 72: 183-191 [Abstract] [Full Text]  
• Olson, T. S., Ley, K. (2002). Chemokines and chemokine receptors in leukocyte trafficking. Am. J. Physiol. Regul. Integr. Comp. Physiol. 283: R7-R28 [Abstract] [Full Text]  
• Hodge, D. L., Schill, W. B., Wang, J. M., Blanca, I., Reynolds, D. A., Ortaldo, J. R., Young, H. A. (2002). IL-2 and IL-12 Alter NK Cell Responsiveness to IFN-{gamma}-Inducible Protein 10 by Down-Regulating CXCR3 Expression. J. Immunol. 168: 6090-6098 [Abstract] [Full Text]  
• Mohan, K., Ding, Z., Hanly, J., Issekutz, T. B. (2002). IFN-{gamma}-Inducible T Cell {alpha} Chemoattractant Is a Potent Stimulator of Normal Human Blood T Lymphocyte Transendothelial Migration: Differential Regulation by IFN-{gamma} and TNF-{alpha}. J. Immunol. 168: 6420-6428 [Abstract] [Full Text]  
• Wildbaum, G., Netzer, N., Karin, N. (2002). Plasmid DNA Encoding IFN-{gamma}-Inducible Protein 10 Redirects Antigen-Specific T Cell Polarization and Suppresses Experimental Autoimmune Encephalomyelitis. J. Immunol. 168: 5885-5892 [Abstract] [Full Text]  
• Cockwell, P., Calderwood, J. W., Brooks, C. J., Chakravorty, S. J., Savage, C. O. S. (2002). Chemoattraction of T cells expressing CCR5, CXCR3 and CX3CR1 by proximal tubular epithelial cell chemokines. Nephrol Dial Transplant 17: 734-744 [Abstract] [Full Text]  
• Shiraha, H., Glading, A., Chou, J., Jia, Z., Wells, A. (2002). Activation of m-Calpain (Calpain II) by Epidermal Growth Factor Is Limited by Protein Kinase A Phosphorylation of m-Calpain. Mol. Cell. Biol. 22: 2716-2727 [Abstract] [Full Text]  
• Padovan, E., Spagnoli, G. C., Ferrantini, M., Heberer, M. (2002). IFN-{alpha}2a induces IP-10/CXCL10 and MIG/CXCL9 production in monocyte-derived dendritic cells and enhances their capacity to attract and stimulate CD8+ effector T cells. J. Leukoc. Biol. 71: 669-676 [Abstract] [Full Text]  
• Dufour, J. H., Dziejman, M., Liu, M. T., Leung, J. H., Lane, T. E., Luster, A. D. (2002). IFN-{gamma}-Inducible Protein 10 (IP-10; CXCL10)-Deficient Mice Reveal a Role for IP-10 in Effector T Cell Generation and Trafficking. J. Immunol. 168: 3195-3204 [Abstract] [Full Text]  
• Yoshie, O., Fujisawa, R., Nakayama, T., Harasawa, H., Tago, H., Izawa, D., Hieshima, K., Tatsumi, Y., Matsushima, K., Hasegawa, H., Kanamaru, A., Kamihira, S., Yamada, Y. (2002). Frequent expression of CCR4 in adult T-cell leukemia and human T-cell leukemia virus type 1-transformed T cells. Blood 99: 1505-1511 [Abstract] [Full Text]  
• Kai, K., Nasu, K., Nakamura, S., Fukuda, J., Nishida, M., Miyakawa, I. (2002). Expression of interferon-{gamma}-inducible protein-10 in human endometrial stromal cells. Mol Hum Reprod 8: 176-180 [Abstract] [Full Text]  
• Sauty, A., Colvin, R. A., Wagner, L., Rochat, S., Spertini, F., Luster, A. D. (2001). CXCR3 Internalization Following T Cell-Endothelial Cell Contact: Preferential Role of IFN-Inducible T Cell {alpha} Chemoattractant (CXCL11). J. Immunol. 167: 7084-7093 [Abstract] [Full Text]  
• Proost, P., Schutyser, E., Menten, P., Struyf, S., Wuyts, A., Opdenakker, G., Detheux, M., Parmentier, M., Durinx, C., Lambeir, A.-M., Neyts, J., Liekens, S., Maudgal, P. C., Billiau, A., Van Damme, J. (2001). Amino-terminal truncation of CXCR3 agonists impairs receptor signaling and lymphocyte chemotaxis, while preserving antiangiogenic properties. Blood 98: 3554-3561 [Abstract] [Full Text]  

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