Brief Definitive Report

Requirement of the Chemokine Receptor CXCR3 for Acute Allograft Rejection

Correspondence to: Wayne W. Hancock, Millennium Pharmaceuticals, Inc., 75 Sidney St., Cambridge, MA 02139. Tel:617-551-3637 Fax:617-679-7071

Chemokines provide signals for activation and recruitment of effector cells into sites of inflammation, acting via specific G protein–coupled receptors. However, in vitro data demonstrating the presence of multiple ligands for a given chemokine receptor, and often multiple receptors for a given chemokine, have led to concerns of biologic redundancy. Here we show that acute cardiac allograft rejection is accompanied by progressive intragraft production of the chemokines interferon (IFN)-–inducible protein of 10 kD (IP-10), monokine induced by IFN- (Mig), and IFN-inducible T cell chemoattractant (I-TAC), and by infiltration of activated T cells bearing the corresponding chemokine receptor, CXCR3. We used three in vivo models to demonstrate a role for CXCR3 in the development of transplant rejection. First, CXCR3-deficient (CXCR3^-/-) mice showed profound resistance to development of acute allograft rejection. Second, CXCR3^-/- allograft recipients treated with a brief, subtherapeutic course of cyclosporin A maintained their allografts permanently and without evidence of chronic rejection. Third, CXCR^+/+ mice treated with an anti-CXCR3 monoclonal antibody showed prolongation of allograft survival, even if begun after the onset of rejection. Taken in conjunction with our findings of CXCR3 expression in rejecting human cardiac allografts, we conclude that CXCR3 plays a key role in T cell activation, recruitment, and allograft destruction.

Key Words: receptors, chemokine, transplantation, rejection, CXC chemokine receptor 3

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• Lee, I., Wang, L., Wells, A. D., Ye, Q., Han, R., Dorf, M. E., Kuziel, W. A., Rollins, B. J., Chen, L., Hancock, W. W. (2003). Blocking the Monocyte Chemoattractant Protein-1/CCR2 Chemokine Pathway Induces Permanent Survival of Islet Allografts through a Programmed Death-1 Ligand-1-Dependent Mechanism. J. Immunol. 171: 6929-6935 [Abstract] [Full Text]  
• Belperio, J. A., Keane, M. P., Burdick, M. D., Lynch, J. P. III, Zisman, D. A., Xue, Y. Y., Li, K., Ardehali, A., Ross, D. J., Strieter, R. M. (2003). Role of CXCL9/CXCR3 Chemokine Biology during Pathogenesis of Acute Lung Allograft Rejection. J. Immunol. 171: 4844-4852 [Abstract] [Full Text]  
• Sundrud, M. S., Grill, S. M., Ni, D., Nagata, K., Alkan, S. S., Subramaniam, A., Unutmaz, D. (2003). Genetic Reprogramming of Primary Human T Cells Reveals Functional Plasticity in Th Cell Differentiation. J. Immunol. 171: 3542-3549 [Abstract] [Full Text]  
• Valbuena, G., Bradford, W., Walker, D. H. (2003). Expression Analysis of the T-Cell-Targeting Chemokines CXCL9 and CXCL10 in Mice and Humans with Endothelial Infections Caused by Rickettsiae of the Spotted Fever Group. Am. J. Pathol. 163: 1357-1369 [Abstract] [Full Text]  
• Rabin, R. L., Alston, M. A., Sircus, J. C., Knollmann-Ritschel, B., Moratz, C., Ngo, D., Farber, J. M. (2003). CXCR3 Is Induced Early on the Pathway of CD4+ T Cell Differentiation and Bridges Central and Peripheral Functions. J. Immunol. 171: 2812-2824 [Abstract] [Full Text]  
• Johnston, B., Kim, C. H., Soler, D., Emoto, M., Butcher, E. C. (2003). Differential Chemokine Responses and Homing Patterns of Murine TCR{alpha}{beta} NKT Cell Subsets. J. Immunol. 171: 2960-2969 [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]  
• Zhang, Q.-W., Kish, D. D., Fairchild, R. L. (2003). Absence of Allograft ICAM-1 Attenuates Alloantigen-Specific T Cell Priming, But Not Primed T Cell Trafficking into the Graft, to Mediate Acute Rejection. J. Immunol. 170: 5530-5537 [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]  
• Streblow, D. N., Kreklywich, C., Yin, Q., De La Melena, V. T., Corless, C. L., Smith, P. A., Brakebill, C., Cook, J. W., Vink, C., Bruggeman, C. A., Nelson, J. A., Orloff, S. L. (2003). Cytomegalovirus-Mediated Upregulation of Chemokine Expression Correlates with the Acceleration of Chronic Rejection in Rat Heart Transplants. J. Virol. 77: 2182-2194 [Abstract] [Full Text]  
• Gao, P., Zhou, X.-Y., Yashiro-Ohtani, Y., Yang, Y.-F., Sugimoto, N., Ono, S., Nakanishi, T., Obika, S., Imanishi, T., Egawa, T., Nagasawa, T., Fujiwara, H., Hamaoka, T. (2003). The unique target specificity of a nonpeptide chemokine receptor antagonist: selective blockade of two Th1 chemokine receptors CCR5 and CXCR3. J. Leukoc. Biol. 73: 273-280 [Abstract] [Full Text]  
• Jiankuo, M., Xingbing, W., Baojun, H., Xiongwin, W., Zhuoya, L., Ping, X., Yong, X., Anting, L., Chunsong, H., Feili, G., Jinquan, T. (2003). Peptide Nucleic Acid Antisense Prolongs Skin Allograft Survival by Means of Blockade of CXCR3 Expression Directing T Cells into Graft. J. Immunol. 170: 1556-1565 [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]  
• Ozkaynak, E., Wang, L., Goodearl, A., McDonald, K., Qin, S., O'Keefe, T., Duong, T., Smith, T., Gutierrez-Ramos, J.-C., Rottman, J. B., Coyle, A. J., Hancock, W. W. (2002). Programmed Death-1 Targeting Can Promote Allograft Survival. J. Immunol. 169: 6546-6553 [Abstract] [Full Text]  
• Yun, J. J., Fischbein, M. P., Whiting, D., Irie, Y., Fishbein, M. C., Burdick, M. D., Belperio, J., Strieter, R. M., Laks, H., Berliner, J. A., Ardehali, A. (2002). The Role of MIG/CXCL9 in Cardiac Allograft Vasculopathy. Am. J. Pathol. 161: 1307-1313 [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]  
• Abdi, R., Smith, R. N., Makhlouf, L., Najafian, N., Luster, A. D., Auchincloss, H. Jr., Sayegh, M. H. (2002). The Role of CC Chemokine Receptor 5 (CCR5) in Islet Allograft Rejection. Diabetes 51: 2489-2495 [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]  
• 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]  
• Yoneyama, H., Narumi, S., Zhang, Y., Murai, M., Baggiolini, M., Lanzavecchia, A., Ichida, T., Asakura, H., Matsushima, K. (2002). Pivotal Role of Dendritic Cell-derived CXCL10 in the Retention of T Helper Cell 1 Lymphocytes in Secondary Lymph Nodes. JEM 195: 1257-1266 [Abstract] [Full Text]  
• Afrouzian, M., Ramassar, V., Urmson, J., Zhu, L.-F., Halloran, P. F. (2002). Transcription Factor IRF-1 in Kidney Transplants Mediates Resistance to Graft Necrosis during Rejection. J. Am. Soc. Nephrol. 13: 1199-1209 [Abstract] [Full Text]  

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