Hyaluronan fragments act as an endogenous danger signal by engaging TLR2

Journal of Immunology

Volumn 177, Issue 2, 2006, Pages 1272-1281

  Scheibner, Kara A ^a   Lutz, Michael A ^b   Boodoo, Sada ^a   Fenton, Matthew J ^c,d   Powell, Jonathan D ^b   Horton, Maureen R ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^d NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; HYALURONIC ACID; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; IMMUNOLOGICAL ADJUVANT; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 1; MYELOID DIFFERENTIATION FACTOR 88; PROTEIN KINASE C ZETA; TOLL LIKE RECEPTOR 2; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CATABOLISM; CELLULAR IMMUNITY; CONTROLLED STUDY; EXTRACELLULAR MATRIX; GLYCOSAMINOGLYCAN METABOLISM; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IN VIVO STUDY; INNATE IMMUNITY; KNOCKOUT MOUSE; MOLECULAR WEIGHT; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CARBOHYDRATE INTERACTION; RECEPTOR BLOCKING; SIGNAL TRANSDUCTION; TISSUE INJURY;

EID: 33745840859     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.177.2.1272     Document Type: Article

References (56)

1. Janeway, C. A., Jr. 1989. Approaching the asymptote? Evolution and revolution in immunology. Cold Spring Harbor Symp. Quant Biol. 54(pt. 1): 1-13.
2. Fuchs, E. J., and P. Matzinger. 1996. Is cancer dangerous to the immune system? Semin. Immunol. 8: 271-280.
3. Matzinger, P. 1994. Tolerance, danger, and the extended family. Annu. Rev. Immunol. 12: 991-1045.
4. Matzinger, P. 2002. The danger model: a renewed sense of self. Science 296: 301-305.
5. Shi, Y., J. E. Evans, and K. L. Rock. 2003. Molecular identification of a danger signal that alerts the immune system to dying cells. Nature 425: 516-521.
6. Rovere-Querini, P., A. Capobianco, P. Scaffidi, B. Valentinis, F. Catalanotti, M. Giazzon, I. E. Dumitriu, S. Muller, M. Iannacone, C. Traversari, et al. 2004. HMGB1 is an endogenous immune adjuvant released by necrotic cells. EMBO Rep. 5: 825-830.
7. Laurent, T. C. 1995. Functions of hyaluronan. Ann. Rheum. Dis. 54: 429.
8. Fraser, J. R., T. C. Laurent, and U. B. Laurent. 1997. Hyaluronan: its nature, distribution, functions and turnover. J. Intern. Med. 242: 27-33.
9. Sampson, P., C. Rochester, B. Freundlich, and J. Elias. 1992. Cytokine regulation of human lung fibroblast hyaluronan (hyaluronic acid) production: evidence for cytokine-regulated hyaluronan (hyaluronic acid) degradation and human lung fibroblast-derived hyaluronidase. J. Clin. Invest. 90: 1492-1503.
10. Hodge-Dufour, J., P. W. Noble, M. R. Horton, C. Bao, M. Wysoka, M. D. Burdick, R. M. Stricter, G. Trinchieri, and E. Pure. 1997. Induction of IL-12 and chemokines by hyaluronan requires adhesion-dependent priming of resident but not elicited macrophages. J. Immunol. 159: 2492-2500.
11. Horton, M. R., C. M. McKee, C. Bao, F. Liao, J. M. Farber, J. Hodge-DuFour, E. Pure, B. L. Oliver, T. M. Wright, and P. W. Noble. 1998. Hyaluronan fragments synergize with interferon-γ to induce the C-X-C chemokines MIG and interferon-inducible protein-10 in mouse macrophages. J. Biol. Chem. 52: 35088-35094.
12. Horton, M. R., M. D. Burdick, R. M. Stricter, C. Bao, and P. W. Noble. 1998. Regulation of hyaluronan-induced chemokine gene expression by IL-10 and IFN-γ in mouse macrophages. J. Immunol. 160: 3023-3030.
13. Horton, M. R., S. Shapiro, C. Bao, C. J. Lowenstein, and P. W. Noble. 1999. Induction and regulation of macrophage metalloelastase by hyaluronan fragments in mouse macrophages. J. Immunol. 4171-4176.
14. McKee, C., M. Penno, M. Cowman, M. Burdick, R. Stricter, C. Bao, and P. Noble. 1996. Hyaluronan (HA) fragments induce chemokine gene expression in alveolar macrophages: the role of HA size and CD44. J. Clin. Invest. 98: 2403-2413.
15. Jiang, D., J. Liang, J. Fan, S. Yu, S. Chen, Y. Luo, G. D. Prestwich, M. M. Mascarenhas, H. G. Garg, D. A. Quinn, et al. 2005. Regulation of lung injury and repair by Toll-like receptors and hyaluronan. Nat. Med. 11: 1173-1179.
16. Termeer, C. C., J. Hennies, U. Voith, T. Ahrens, J. M. Weiss, P. Prehm, and J. C. Simon. 2000. Oligosaccharides of hyaluronan are potent activators of dendritic cells. J. Immunol. 165: 1863-1870.
17. Beck-Schimmer, B., B. Oertli, T. Pasch, and R. P. Wuthrich. 1998. Hyaluronan induces monocyte chemoattractant protein-1 expression in renal tubular epithelial cells. J. Am. Soc. Nephrol. 9: 2283-2290.
18. Montesano, R., S. Kumar, L. Orci, and M. S. Pepper. 1996. Synergistic effect of hyaluronan oligosaccharides and vascular endothelial growth factor on angiogenesis in vitro. Lab. Invest. 75: 249-262.
19. Mascarenhas, M. M., R. M. Day, C. D. Ochoa, W. I. Choi, L. Yu, B. Ouyang, H. G. Garg, C. A. Hales, and D. A. Quinn. 2004. Low molecular weight hyaluronan from stretched lung enhances interleukin-8 expression. Am. J. Respir. Cell Mol. Biol. 30: 51-60.
20. McKee, C. M., C. J. Lowenstein, M. R. Horton, J. Wu, C. Bao, B. Y. Chin, A. M. Choi, and P. W. Noble. 1997. Hyaluronan fragments induce nitric-oxide synthase in murine macrophages through a nuclear factor κB-dependent mechanism. J. Biol. Chem. 272: 8013-8018.
21. Yang, R., Z. Yan, F. Chen, G. K. Hansson, and R. Kiessling. 2002. Hyaluronic acid and chondroitin sulphate A rapidly promote differentiation of immature DC with upregulation of costimulatory and antigen-presenting molecules, and enhancement of NF-κB and protein kinase activity. Scand. J. Immunol. 55: 2-13.
22. Teder, P., R. W. Vandivier, D. Jiang, J. Liang, L. Cohn, E. Pure, P. M. Henson, and P. W. Noble. 2002. Resolution of lung inflammation by CD44. Science 296: 155-158.
23. Toole, B. P. 2004. Hyaluronan: from extracellular glue to pericellular cue. Nat. Rev. Cancer 4: 528-539.
24. Nettelbladt, O., and R. Hallgren. 1989. Hyaluronan (hyaluronic acid) in bronchoalveolar lavage fluid during the development of bleomycin-induced alveolitis in the rat. Am. Rev. Respir. Dis. 140: 1028-1032.
25. Nettelbladt, O., A. Scheynius, J. Bergh, A. Tengblad, and R. Hallgren. 1991. Alveolar accumulation of hyaluronan and alveolar cellular response in bleomycin-induced alveolitis. Eur. Respir. J. 4: 407-414.
26. Noble, P. W. 2002. Hyaluronan and its catabolic products in tissue injury and repair. Matrix Biol. 21: 25-29.
27. Wollheim, F. A. 1996. Predictors of joint damage in rheumatoid arthritis. Apmis. 104: 81-93.
28. Laurent, T. C., J. R. Fraser, U. B. Laurent, and A. Engstrom-Laurent. 1995. Hyaluronan in inflammatory joint disease. Acta Orthop. Scand Suppl. 266: 116-120.
29. Horton, M. R., S. Boodoo, and J. D. Powell. 2002. NF-κB activation mediates the cross-talk between extracellular matrix and interferon-γ (IFN-γ) leading to enhanced monokine induced by IFN-γ (MIG) expression in macrophages. J. Biol. Chem. 277: 43757-43762.
30. Noble, P. W., C. M. McKee, M. Cowman, and H. S. Shin. 1996. Hyaluronan fragments activate an NF-κB/IκBα autoregulatory loop in murine macrophages. J. Exp. Med. 183: 2373-2378.
31. Fieber, C., P. Baumann, R. Vallon, C. Termeer, J. C. Simon, M. Hofmann, P. Angel, P. Herrlich, and J. P. Sleeman. 2004. Hyaluronan-oligosaccharide- induced transcription of metalloproteases. J. Cell Sci. 117: 359-367.
32. Taylor, K. R., J. M. Trowbridge, J. A. Rudisill, C. C. Termeer, J. C. Simon, and R. L. Gallo. 2004. Hyaluronan fragments stimulate endothelial recognition of injury through TLR4. J. Biol. Chem. 279: 17079-17084.
33. Termeer, C., F. Benedix, J. Sleeman, C. Fieber, U. Voith, T. Ahrens, K. Miyake, M. Freudenberg, C. Galanos, and J. C. Simon. 2002. Oligosaccharides of Hyaluronan activate dendritic cells via Toll-like receptor 4. J. Exp. Med. 195: 99-111.
34. Mbawuike, I., and H. Herscowitz. 1989. MH-S, a murine alveolar macrophage cell line: morphological, cytochemical, and functional characteristics. J. Leukocyte Biol. 46: 119-127.
35. Ghatak, S., S. Misra, and B. P. Toole. 2002. Hyaluronan oligosaccharides inhibit anchorage-independent growth of tumor cells by suppressing the phosphoinositide 3-kinase/Akt cell survival pathway. J. Biol. Chem. 277: 38013-38020.
36. Takeuchi, O., and S. Akira. 2001. Toll-like receptors; their physiological role and signal transduction system. Int. Immunopharmacol. 1: 625-635.
37. Kaisho, T., and S. Akira. 2002. Toll-like receptors as adjuvant receptors. Biochim. Biophys. Acta 1589: 1-13.
38. Adachi, O., T. Kawai, K. Takeda, M. Matsumoto, H. Tsutsui, M. Sakagami, K. Nakanishi, and S. Akira. 1998. Targeted disruption of the MyD88 gene results in loss of IL-1- and IL-18-mediated function. Immunity 9: 143-150.
39. Noble, P., F. Lake, P. Henson, and D. Riches. 1993. Hyaluronate activation of CD44 induces insulin-like growth factor-1 expression by a tumor necrosis factor-α-dependent mechanism in murine macrophages. J. Clin. Invest. 91: 2368-2377.
40. Mummert, D. I., A. Takashima, L. Ellinger, and M. E. Mummert. 2003. Involvement of hyaluronan in epidermal Langerhans cell maturation and migration in vivo. J. Dermatol. Sci. 33: 91-97.
41. Banerji, S., J. Ni, S. X. Wang, S. Clasper, J. Su, R. Tammi, M. Jones, and D. G. Jackson. 1999. LYVE-1, a new homologue of the CD44 glycoprotein, is a lymph-specific receptor for hyaluronan. J. Cell Biol. 144: 789-801.
42. Fitzgerald, K. A., A. G. Bowie, B. S. Skeffington, and L. A. O'Neill. 2000. Ras, protein kinase Cζ, and IκB kinases 1 and 2 are downstream effectors of CD44 during the activation of NF-κ B by hyaluronic acid fragments in T-24 carcinoma cells. J. Immunol. 164: 2053-2063.
43. Kirschning, C. J., and R. R. Schumann. 2002. TLR2: cellular sensor for microbial and endogenous molecular patterns. Curr. Top. Microbiol. Immunol. 270: 121-144.
44. Park, J. S., D. Svetkauskaite, Q. He, J. Y. Kim, D. Strassheim, A. Ishizaka, and E. Abraham. 2004. Involvement of Toll-like receptors 2 and 4 in cellular activation by high mobility group box 1 protein. J. Biol. Chem. 279: 7370-7377.
45. Vabulas, R. M., P. Ahmad-Nejad, C. da Costa, T. Miethke, C. J. Kirschning, H. Hacker, and H. Wagner. 2001. Endocytosed HSP60s use Toll-like receptor 2 (TLR2) and TLR4 to activate the Toll/interleukin-1 receptor signaling pathway in innate immune cells. J. Biol. Chem. 276: 31332-31339.
46. Okamura, Y., M. Watari, E. S. Jerud, D. W. Young, S. T. Ishizaka, J. Rose, J. C. Chow, and J. F. Strauss, 3rd. 2001. The extra domain A of fibronectin activates Toll-like receptor 4. J. Biol. Chem. 276: 10229-10233.
47. Johnson, G. B., G. J. Brunn, Y. Kodaira, and J. L. Platt. 2002. Receptor-mediated monitoring of tissue well-being via detection of soluble heparan sulfate by Toll-like receptor 4. J. Immunol. 168: 5233-5239.
48. Guillot, L., V. Balloy, F. X. McCormack, D. T. Golenbock, M. Chignard, and M. Si-Tahar. 2002. Cutting edge: the immunostimulatory activity of the lung surfactant protein-A involves Toll-like receptor 4. J. Immunol. 168: 5989-5992.
49. Biragyn, A., P. A. Ruffini, C. A. Leifer, E. Klyushnenkova, A. Shakhov, O. Chertov, A. K. Shirakawa, J. M. Farber, D. M. Segal, J. J. Oppenheim, and L. W. Kwak. 2002. Toll-like receptor 4-dependent activation of dendritic cells by β-defensin 2. Science 298: 1025-1029.
50. Hirschfeld, M., Y. Ma, J. H. Weis, S. N. Vogel, and J. J. Weis. 2000. Cutting edge: repurification of lipopolysaccharide eliminates signaling through both human and murine Toll-like receptor 2. J. Immunol. 165: 618-622.
51. Tsan, M. F., and B. Gao. 2004. Endogenous ligands of Toll-like receptors. J. Leukocyte Biol. 76: 514-519.
52. Hallgren, R., A. Eklund, B. Engstrom-Laurent, and B. Schmekel. 1985. Hyaluronate in bronchoalveolar lavage fluid: a new marker in sarcoidosis reflecting pulmonary disease. Br. Med. J. 290: 1778-1781.
53. Milman, N., M. S. Kristensen, K. Bentsen, G. Grode, and J. Frederiksen. 1995. Hyaluronan and procollagen type III aminoterminal peptide in serum and bronchoalveolar lavage fluid in patients with pulmonary sarcoidosis. Sarcoidosis 12: 38-41.
54. Ruse, G. C., S. Ahlstedt, S. Larsson, I. Enander, I. Jones, P. Larsson, and B. Andersson. 1995. Bronchial inflammation in chronic bronchitis assessed by measurement of cell products in bronchial lavage fluid. Thorax 50: 360-365.
55. 2 levels in rheumatoid arthritis: a multicenter clinical trial. Clin. Exp. Rheumatol. 19: 377-383.
56. Cantor, J. O., J. M. Cerreta, S. Keller, and G. M. Turino. 1995. Modulation of airspace enlargement in elastase-induced emphysema by intratracheal instillment of hyaluronidase and hyaluronic acid. Exp. Lung Res. 21: 423-436.