J. Exp. Med., Volume 188, Number 2, July 20, 1998 373-386

Selective Recruitment of Immature and Mature Dendritic Cells by Distinct Chemokines Expressed in Different Anatomic Sites

By Marie-Caroline Dieu,^* Béatrice Vanbervliet,^* Alain Vicari,^* Jean-Michel Bridon,^* Elisabeth Oldham, Smina Aït-Yahia,^* Francine Brière,^* Albert Zlotnik, Serge Lebecque,^* and Christophe Caux^*

From the ^* Schering-Plough, Laboratory for Immunological Research, 69571, Dardilly, France; and  DNAX, Research Institute, Palo Alto, California 94304

DCs (dendritic cells) function as sentinels of the immune system. They traffic from the blood to the tissues where, while immature, they capture antigens. They then leave the tissues and move to the draining lymphoid organs where, converted into mature DC, they prime naive T cells. This suggestive link between DC traffic pattern and functions led us to investigate the chemokine responsiveness of DCs during their development and maturation. DCs were differentiated either from CD34⁺ hematopoietic progenitor cells (HPCs) cultured with granulocyte/macrophage colony-stimulating factor (GM-CSF) plus tumor necrosis factor (TNF)- or from monocytes cultured with GM-CSF plus interleukin 4. Immature DCs derived from CD34⁺ HPCs migrate most vigorously in response to macrophage inflammatory protein (MIP)-3, but also to MIP-1 and RANTES (regulated on activation, normal T cell expressed and secreted). Upon maturation, induced by either TNF-, lipopolysaccharide, or CD40L, DCs lose their response to these three chemokines when they acquire a sustained responsiveness to a single other chemokine, MIP-3. CC chemokine receptor (CCR)6 and CCR7 are the only known receptors for MIP-3 and MIP-3, respectively. The observation that CCR6 mRNA expression decreases progressively as DCs mature, whereas CCR7 mRNA expression is sharply upregulated, provides a likely explanation for the changes in chemokine responsiveness. Similarly, MIP-3 responsiveness and CCR7 expression are induced upon maturation of monocyte- derived DCs. Furthermore, the chemotactic response to MIP-3 is also acquired by CD11c⁺ DCs isolated from blood after spontaneous maturation. Finally, detection by in situ hybridization of MIP-3 mRNA only within inflamed epithelial crypts of tonsils, and of MIP-3 mRNA specifically in T cell-rich areas, suggests a role for MIP-3/CCR6 in recruitment of immature DCs at site of injury and for MIP-3/CCR7 in accumulation of antigen-loaded mature DCs in T cell-rich areas.

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• Hausmann, M., Bataille, F., Spoettl, T., Schreiter, K., Falk, W., Schoelmerich, J., Herfarth, H., Rogler, G. (2005). Physiological Role of Macrophage Inflammatory Protein-3{alpha} Induction during Maturation of Intestinal Macrophages. J. Immunol. 175: 1389-1398 [Abstract] [Full Text]  
• Osterholzer, J. J., Ames, T., Polak, T., Sonstein, J., Moore, B. B., Chensue, S. W., Toews, G. B., Curtis, J. L. (2005). CCR2 and CCR6, but Not Endothelial Selectins, Mediate the Accumulation of Immature Dendritic Cells within the Lungs of Mice in Response to Particulate Antigen. J. Immunol. 175: 874-883 [Abstract] [Full Text]  
• Cremel, M., Berlier, W., Hamzeh, H., Cognasse, F., Lawrence, P., Genin, C., Bernengo, J.-C., Lambert, C., Dieu-Nosjean, M.-C., Delezay, O. (2005). Characterization of CCL20 secretion by human epithelial vaginal cells: involvement in Langerhans cell precursor attraction. J. Leukoc. Biol. 78: 158-166 [Abstract] [Full Text]  
• Gurney, K. B., Elliott, J., Nassanian, H., Song, C., Soilleux, E., McGowan, I., Anton, P. A., Lee, B. (2005). Binding and Transfer of Human Immunodeficiency Virus by DC-SIGN+ Cells in Human Rectal Mucosa. J. Virol. 79: 5762-5773 [Abstract] [Full Text]  
• McDonald, K. G., McDonough, J. S., Newberry, R. D. (2005). Adaptive Immune Responses Are Dispensable for Isolated Lymphoid Follicle Formation: Antigen-Naive, Lymphotoxin-Sufficient B Lymphocytes Drive the Formation of Mature Isolated Lymphoid Follicles. J. Immunol. 174: 5720-5728 [Abstract] [Full Text]  
• Paoletti, S., Petkovic, V., Sebastiani, S., Danelon, M. G., Uguccioni, M., Gerber, B. O. (2005). A rich chemokine environment strongly enhances leukocyte migration and activities. Blood 105: 3405-3412 [Abstract] [Full Text]  
• Riol-Blanco, L., Sanchez-Sanchez, N., Torres, A., Tejedor, A., Narumiya, S., Corbi, A. L., Sanchez-Mateos, P., Rodriguez-Fernandez, J. L. (2005). The Chemokine Receptor CCR7 Activates in Dendritic Cells Two Signaling Modules That Independently Regulate Chemotaxis and Migratory Speed. J. Immunol. 174: 4070-4080 [Abstract] [Full Text]  
• Kleinewietfeld, M., Puentes, F., Borsellino, G., Battistini, L., Rotzschke, O., Falk, K. (2005). CCR6 expression defines regulatory effector/memory-like cells within the CD25+CD4+ T-cell subset. Blood 105: 2877-2886 [Abstract] [Full Text]  
• Mori, T., Kim, J., Yamano, T., Takeuchi, H., Huang, S., Umetani, N., Koyanagi, K., Hoon, D. S.B. (2005). Epigenetic Up-regulation of C-C Chemokine Receptor 7 and C-X-C Chemokine Receptor 4 Expression in Melanoma Cells. Cancer Res. 65: 1800-1807 [Abstract] [Full Text]  
• Schimanski, C. C., Schwald, S., Simiantonaki, N., Jayasinghe, C., Gonner, U., Wilsberg, V., Junginger, T., Berger, M. R., Galle, P. R., Moehler, M. (2005). Effect of Chemokine Receptors CXCR4 and CCR7 on the Metastatic Behavior of Human Colorectal Cancer. Clin. Cancer Res. 11: 1743-1750 [Abstract] [Full Text]  
• Radstake, T R D J, van der Voort, R, ten Brummelhuis, M, de Waal Malefijt, M, Looman, M, Figdor, C G, van den Berg, W B, Barrera, P, Adema, G J (2005). Increased expression of CCL18, CCL19, and CCL17 by dendritic cells from patients with rheumatoid arthritis, and regulation by Fc gamma receptors. Ann Rheum Dis 64: 359-367 [Abstract] [Full Text]  
• de Noronha, S., Hardy, S., Sinclair, J., Blundell, M. P., Strid, J., Schulz, O., Zwirner, J., Jones, G. E., Katz, D. R., Kinnon, C., Thrasher, A. J. (2005). Impaired dendritic-cell homing in vivo in the absence of Wiskott-Aldrich syndrome protein. Blood 105: 1590-1597 [Abstract] [Full Text]  
• Yang, C. C., Ogawa, H., Dwinell, M. B., McCole, D. F., Eckmann, L., Kagnoff, M. F. (2005). Chemokine receptor CCR6 transduces signals that activate p130Cas and alter cAMP-stimulated ion transport in human intestinal epithelial cells. Am. J. Physiol. Cell Physiol. 288: C321-C328 [Abstract] [Full Text]  
• Munz, C., Dao, T., Ferlazzo, G., de Cos, M. A., Goodman, K., Young, J. W. (2005). Mature myeloid dendritic cell subsets have distinct roles for activation and viability of circulating human natural killer cells. Blood 105: 266-273 [Abstract] [Full Text]  
• Jinushi, M., Takehara, T., Tatsumi, T., Kanto, T., Miyagi, T., Suzuki, T., Kanazawa, Y., Hiramatsu, N., Hayashi, N. (2004). Negative Regulation of NK Cell Activities by Inhibitory Receptor CD94/NKG2A Leads to Altered NK Cell-Induced Modulation of Dendritic Cell Functions in Chronic Hepatitis C Virus Infection. J. Immunol. 173: 6072-6081 [Abstract] [Full Text]  
• Treilleux, I., Blay, J.-Y., Bendriss-Vermare, N., Ray-Coquard, I., Bachelot, T., Guastalla, J.-P., Bremond, A., Goddard, S., Pin, J.-J., Barthelemy-Dubois, C., Lebecque, S. (2004). Dendritic Cell Infiltration and Prognosis of Early Stage Breast Cancer. Clin. Cancer Res. 10: 7466-7474 [Abstract] [Full Text]  

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