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Original Article

¹ Department of Dermatology, University of Freiburg, Freiburg D-79104, Germany
² Institute for Genetics, Forschungszentrum Karlsruhe, Karlsruhe D-76021, Germany
³ Max-Planck Institute for Immunobiology, Freiburg D-79011, Germany
⁴ Division of Infectious Genetics, Department of Microbiology and Immunology, The Institute of Medical Science, University of Tokyo, Tokyo 108-8639, Japan
⁵ Department for Biophysical Chemistry, Biocenter Basel, Basel CH-4056, Switzerland

Address correspondence to C. Termeer, Dept. of Dermatology, University of Freiburg, Hauptstr. 7, D-79104 Freiburg, Germany. Phone: 49-761-270-6831; Fax: 49-761-270-6829; E-mail: Termeer{at}haut.ukl.uni-freiburg.de

Low molecular weight fragmentation products of the polysaccharide of Hyaluronic acid (sHA) produced during inflammation have been shown to be potent activators of immunocompetent cells such as dendritic cells (DCs) and macrophages. Here we report that sHA induces maturation of DCs via the Toll-like receptor (TLR)-4, a receptor complex associated with innate immunity and host defense against bacterial infection. Bone marrow–derived DCs from C3H/HeJ and C57BL/10ScCr mice carrying mutant TLR-4 alleles were nonresponsive to sHA-induced phenotypic and functional maturation. Conversely, DCs from TLR-2–deficient mice were still susceptible to sHA. In accordance, addition of an anti–TLR-4 mAb to human monocyte–derived DCs blocked sHA-induced tumor necrosis factor production. Western blot analysis revealed that sHA treatment resulted in distinct phosphorylation of p38/p42/44 MAP-kinases and nuclear translocation of nuclear factor (NF)-B, all components of the TLR-4 signaling pathway. Blockade of this pathway by specific inhibitors completely abrogated the sHA-induced DC maturation. Finally, intravenous injection of sHA-induced DC emigration from the skin and their phenotypic and functional maturation in the spleen, again depending on the expression of TLR-4. In conclusion, this is the first report that polysaccharide degradation products of the extracellular matrix produced during inflammation might serve as an endogenous ligand for the TLR-4 complex on DCs.

Key Words: extracellular matrix • glycosaminoglycans • dendritic cells • Hyaluronan • toll-like receptors

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• Tedgui, A., Mallat, Z. (2006). Cytokines in Atherosclerosis: Pathogenic and Regulatory Pathways. Physiol. Rev. 86: 515-581 [Abstract] [Full Text]  
• Sugahara, K. N., Hirata, T., Hayasaka, H., Stern, R., Murai, T., Miyasaka, M. (2006). Tumor Cells Enhance Their Own CD44 Cleavage and Motility by Generating Hyaluronan Fragments. J. Biol. Chem. 281: 5861-5868 [Abstract] [Full Text]  
• Cohn, E. F., Nathan, C., Radzioch, D., Yu, H., Xiang, Z., Ding, A. (2006). Abrupt Expression of TLR4 in TLR4-Deficient Macrophages Imposes a Selective Disadvantage: Genetic Evidence for TLR4-Dependent Responses to Endogenous, Nonmicrobial Stimuli. J. Immunol. 176: 1185-1194 [Abstract] [Full Text]  
• Taylor, K. R., Gallo, R. L. (2006). Glycosaminoglycans and their proteoglycans: host-associated molecular patterns for initiation and modulation of inflammation. FASEB J. 20: 9-22 [Abstract] [Full Text]  
• Ma, Y., Temkin, V., Liu, H., Pope, R. M. (2005). NF-{kappa}B Protects Macrophages from Lipopolysaccharide-induced Cell Death: THE ROLE OF CASPASE 8 AND RECEPTOR-INTERACTING PROTEIN. J. Biol. Chem. 280: 41827-41834 [Abstract] [Full Text]  
• Frevert, C. W., Sannes, P. L. (2005). Matrix proteoglycans as effector molecules for epithelial cell function. ERR 14: 137-144 [Abstract] [Full Text]  
• Tsung, A., Hoffman, R. A., Izuishi, K., Critchlow, N. D., Nakao, A., Chan, M. H., Lotze, M. T., Geller, D. A., Billiar, T. R. (2005). Hepatic Ischemia/Reperfusion Injury Involves Functional TLR4 Signaling in Nonparenchymal Cells. J. Immunol. 175: 7661-7668 [Abstract] [Full Text]  
• Tzircotis, G., Thorne, R. F., Isacke, C. M. (2005). Chemotaxis towards hyaluronan is dependent on CD44 expression and modulated by cell type variation in CD44-hyaluronan binding. J. Cell Sci. 118: 5119-5128 [Abstract] [Full Text]  
• Radstake, T R D J, van Lieshout, A W T, van Riel, P L C M, van den Berg, W B, Adema, G J (2005). Dendritic cells, Fc{gamma} receptors, and Toll-like receptors: potential allies in the battle against rheumatoid arthritis. Ann Rheum Dis 64: 1532-1538 [Abstract] [Full Text]  
• Yang, X., Coriolan, D., Murthy, V., Schultz, K., Golenbock, D. T., Beasley, D. (2005). Proinflammatory phenotype of vascular smooth muscle cells: role of efficient Toll-like receptor 4 signaling. Am. J. Physiol. Heart Circ. Physiol. 289: H1069-H1076 [Abstract] [Full Text]  
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• Geisler, F., Algul, H., Riemann, M., Schmid, R. M. (2005). Questioning Current Concepts in Acute Pancreatitis: Endotoxin Contamination of Porcine Pancreatic Elastase Is Responsible for Experimental Pancreatitis-Associated Distant Organ Failure. J. Immunol. 174: 6431-6439 [Abstract] [Full Text]  
• Jameson, J. M., Cauvi, G., Sharp, L. L., Witherden, D. A., Havran, W. L. (2005). {gamma}{delta} T cell-induced hyaluronan production by epithelial cells regulates inflammation. JEM 201: 1269-1279 [Abstract] [Full Text]  
• Morris, G. E., Whyte, M. K. B., Martin, G. F., Jose, P. J., Dower, S. K., Sabroe, I. (2005). Agonists of Toll-like Receptors 2 and 4 Activate Airway Smooth Muscle via Mononuclear Leukocytes. Am. J. Respir. Crit. Care Med. 171: 814-822 [Abstract] [Full Text]  
• Tsung, A., Sahai, R., Tanaka, H., Nakao, A., Fink, M. P., Lotze, M. T., Yang, H., Li, J., Tracey, K. J., Geller, D. A., Billiar, T. R. (2005). The nuclear factor HMGB1 mediates hepatic injury after murine liver ischemia-reperfusion. JEM 201: 1135-1143 [Abstract] [Full Text]  
• Stephen, T. L., Niemeyer, M., Tzianabos, A. O., Kroenke, M., Kasper, D. L., Kalka-Moll, W. M. (2005). Effect of B7-2 and CD40 Signals from Activated Antigen-Presenting Cells on the Ability of Zwitterionic Polysaccharides To Induce T-Cell Stimulation. Infect. Immun. 73: 2184-2189 [Abstract] [Full Text]  
• De Nardo, D., Masendycz, P., Ho, S., Cross, M., Fleetwood, A. J., Reynolds, E. C., Hamilton, J. A., Scholz, G. M. (2005). A Central Role for the Hsp90{middle dot}Cdc37 Molecular Chaperone Module in Interleukin-1 Receptor-associated-kinase-dependent Signaling by Toll-like Receptors. J. Biol. Chem. 280: 9813-9822 [Abstract] [Full Text]  
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