J. Exp. Med., Volume 188, Number 1, July 1, 1998 157-167

The Coordinated Action of CC Chemokines in the Lung Orchestrates Allergic Inflammation and Airway Hyperresponsiveness

By Jose-Angel Gonzalo,^* Clare M. Lloyd,^* Danyi Wen,^* Juan P. Albar, Timothy N.C. Wells,^§ Amanda Proudfoot,^§ C. Martinez-A, Martin Dorf, Torbjörn Bjerke,^¶ Anthony J. Coyle,^* and Jose-Carlos Gutierrez-Ramos^*

From ^* Millennium Pharmaceuticals, Inc., Cambridge, Massachusetts 02139; the  Centro Nacional Biotecnologia Consejo Superior Investigaciones Cientificas, Madrid, 28049 Spain; the ^§ Glaxo Institute for Molecular Biology, Geneva, CH1228 Switzerland; the  Harvard Medical School, Boston, Massachusetts 02115; and ^¶ Astra Draco AB, S-22100 Lund, Sweden

The complex pathophysiology of lung allergic inflammation and bronchial hyperresponsiveness (BHR) that characterize asthma is achieved by the regulated accumulation and activation of different leukocyte subsets in the lung. The development and maintenance of these processes correlate with the coordinated production of chemokines. Here, we have assessed the role that different chemokines play in lung allergic inflammation and BHR by blocking their activities in vivo. Our results show that blockage of each one of these chemokines reduces both lung leukocyte infiltration and BHR in a substantially different way. Thus, eotaxin neutralization reduces specifically BHR and lung eosinophilia transiently after each antigen exposure. Monocyte chemoattractant protein (MCP)-5 neutralization abolishes BHR not by affecting the accumulation of inflammatory leukocytes in the airways, but rather by altering the trafficking of the eosinophils and other leukocytes through the lung interstitium. Neutralization of RANTES (regulated upon activation, normal T cell expressed and secreted) receptor(s) with a receptor antagonist decreases significantly lymphocyte and eosinophil infiltration as well as mRNA expression of eotaxin and RANTES. In contrast, neutralization of one of the ligands for RANTES receptors, macrophage-inflammatory protein 1, reduces only slightly lung eosinophilia and BHR. Finally, MCP-1 neutralization diminishes drastically BHR and inflammation, and this correlates with a pronounced decrease in monocyte- and lymphocyte-derived inflammatory mediators. These results suggest that different chemokines activate different cellular and molecular pathways that in a coordinated fashion contribute to the complex pathophysiology of asthma, and that their individual blockage results in intervention at different levels of these processes.

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• Ensminger, S. M., Spriewald, B. M., Sorensen, H. V., Witzke, O., Flashman, E. G., Bushell, A., Morris, P. J., Rose, M. L., Rahemtulla, A., Wood, K. J. (2001). Critical Role for IL-4 in the Development of Transplant Arteriosclerosis in the Absence of CD40-CD154 Costimulation. J. Immunol. 167: 532-541 [Abstract] [Full Text]  
• Fillion, I., Ouellet, N., Simard, M., Bergeron, Y., Sato, S., Bergeron, M. G. (2001). Role of Chemokines and Formyl Peptides in Pneumococcal Pneumonia-Induced Monocyte/Macrophage Recruitment. J. Immunol. 166: 7353-7361 [Abstract] [Full Text]  
• Hardy, R. D., Jafri, H. S., Olsen, K., Wordemann, M., Hatfield, J., Rogers, B. B., Patel, P., Duffy, L., Cassell, G., McCracken, G. H., Ramilo, O. (2001). Elevated Cytokine and Chemokine Levels and Prolonged Pulmonary Airflow Resistance in a Murine Mycoplasma pneumoniae Pneumonia Model: a Microbiologic, Histologic, Immunologic, and Respiratory Plethysmographic Profile. Infect. Immun. 69: 3869-3876 [Abstract] [Full Text]  
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• Kim, Y., Sung, S.-s. J., Kuziel, W. A., Feldman, S., Fu, S. M., Rose, C. E. Jr (2001). Enhanced Airway Th2 Response After Allergen Challenge in Mice Deficient in CC Chemokine Receptor-2 (CCR2). J. Immunol. 166: 5183-5192 [Abstract] [Full Text]  
• Teixeira, M. M., Talvani, A., Tafuri, W. L., Lukacs, N. W., Hellewell, P. G. (2001). Eosinophil recruitment into sites of delayed-type hypersensitivity reactions in mice. J. Leukoc. Biol. 69: 353-360 [Abstract] [Full Text]  

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