Hyaluronan digestion controls DC migration from the skin

Journal of Clinical Investigation

Volumn 124, Issue 3, 2014, Pages 1309-1319

  Muto, Jun ^a   Morioka, Yasuhide ^a   Yamasaki, Kenshi ^a   Kim, Margaret ^a   Garcia, Andrea ^b,c   Carlin, Aaron F ^a   Varki, Ajit ^a,b   Gallo, Richard L ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b University of California San Diego   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYALURONIC ACID; HYALURONIDASE; HYALURONIDASE 1; MACROPHAGE INFLAMMATORY PROTEIN 2; TOLL LIKE RECEPTOR 4; UNCLASSIFIED DRUG;

AGAR GEL ELECTROPHORESIS; ALLERGIC REACTION; ANIMAL CELL; ARTICLE; CELL FUNCTION; CELL MATURATION; CELL MIGRATION; CONTACT ALLERGY; CONTROLLED STUDY; ENZYME DEGRADATION; ENZYME MODIFICATION; EXTRACELLULAR MATRIX; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN EXPRESSION; SKIN CELL; SKIN SENSITIZATION; TRANSIENT EXPRESSION;

ANIMALS; CELL MOVEMENT; DENDRITIC CELLS; DERMATITIS, CONTACT; FEMALE; GENE EXPRESSION; HUMANS; HYALURONIC ACID; HYALURONOGLUCOSAMINIDASE; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; SKIN; TOLL-LIKE RECEPTOR 4;

EID: 84896788927     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI67947     Document Type: Article

References (52)

1. Kawai T, Akira S. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat Immunol. 2010;11(5):373-384.
2. Chen GY, Nunez G. Sterile inflammation: sensing and reacting to damage. Nat Rev Immunol. 2010; 10(12):826-837.
3. Scaffidi P, Misteli T, Bianchi ME. Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature. 2002;418(6894):191-195.
4. Quintana FJ, Cohen IR. Heat shock proteins as endogenous adjuvants in sterile and septic inflammation. J Immunol. 2005;175(5):2777-2782.
5. Bours MJ, Swennen EL, Di Virgilio F, Cronstein BN, Dagnelie PC. Adenosine 5'-triphosphate and adenosine as endogenous signaling molecules in immunity and inflammation. Pharmacol Ther. 2006; 112(2):358-404.
6. Kono H, Chen CJ, Ontiveros F, Rock KL. Uric acid promotes an acute inflammatory response to sterile cell death in mice. J Clin Invest. 2010; 120(6):1939-1949.
7. Imaeda AB, et al. Acetaminophen-induced hepatotoxicity in mice is dependent on Tlr9 and the Nalp3 inflammasome. J Clin Invest. 2009;119(2):305-314.
8. Burckstummer T, et al. An orthogonal proteomic-genomic screen identifies AIM2 as a cytoplasmic DNA sensor for the inflammasome. Nat Immunol. 2009;10(3):266-272.
9. Cavassani KA, et al. TLR3 is an endogenous sensor of tissue necrosis during acute inflammatory events. J Exp Med. 2008;205(11):2609-2621.
10. Kariko K, Ni H, Capodici J, Lamphier M, Weissman D. mRNA is an endogenous ligand for Toll-like receptor 3. J Biol Chem. 2004;279(13):12542-12550
11. Johnson GB, Brunn GJ, Kodaira Y, Platt JL. Receptor-mediated monitoring of tissue well-being via detection of soluble heparan sulfate by Toll-like receptor 4. J Immunol. 2002;168(10):5233-5239
12. Babelova A, et al. Biglycan, a danger signal that activates the NLRP3 inflammasome via toll-like and P2X receptors. J Biol Chem. 2009;284(36):24035- 24048.
13. Schaefer L, et al. The matrix component biglycan is proinflammatory and signals through Toll-like receptors 4 and 2 in macrophages. J Clin Invest. 2005; 115(8):2223-2233.
14. Kim S, et al. Carcinoma-produced factors activate myeloid cells through TLR2 to stimulate metastasis. Nature. 2009;457(7225):102-106.
15. Jiang D, et al. Regulation of lung injury and repair by Toll-like receptors and hyaluronan. Nat Med. 2005; 11(11):1173-1179.
16. Taylor KR, Trowbridge JM, Rudisill JA, Termeer CC, Simon JC, Gallo RL. Hyaluronan fragments stimulate endothelial recognition of injury through TLR4. J Biol Chem. 2004;279(17):17079-17084.
17. Tammi R, Ripellino JA, Margolis RU, Tammi M. Localization of epidermal hyaluronic acid using the hyaluronate binding region of cartilage proteoglycan as a specific probe. J Invest Dermatol. 1988;90(3):412-414.
18. Weissmann B, Meyer K, Sampson P, Linker A. Isolation of oligosaccharides enzymatically produced from hyaluronic acid. J Biol Chem. 1954; 208(1):417-429.
19. Slevin M, et al. Hyaluronan-mediated angiogenesis in vascular disease: uncovering RHAMM and CD44 receptor signaling pathways. Matrix Biol. 2007; 26(1):58-68.
20. Toole BP. Hyaluronan: from extracellular glue to pericellular cue. Nat Rev Cancer. 2004;4(7):528-539.
21. Jackson DG. Immunological functions of hyaluronan and its receptors in the lymphatics. Immunol Rev. 2009;230(1):216-231.
22. Termeer C, Sleeman JP, Simon JC. Hyaluronan - magic glue for the regulation of the immune response? Trends Immunol. 2003;24(3):112-114.
23. Jiang D, Liang J, Noble P. Hyaluronan in tissue injury and repair. Annu Rev Cell Dev Biol. 2007; 23:435-496.
24. Taylor KR, et al. Recognition of hyaluronan released in sterile injury involves a unique receptor complex dependent on Toll-like receptor 4, CD44, and MD-2. J Biol Chem. 2007;282(25):18265-18275.
25. Termeer CC, et al. Oligosaccharides of hyaluronan are potent activators of dendritic cells. J Immunol. 2000;165(4):1863-1870.
26. Termeer C, et al. Oligosaccharides of Hyaluronan activate dendritic cells via toll-like receptor 4. J Exp Med. 2002;195(1):99-111
27. Tesar BM, Jiang D, Liang J, Palmer SM, Noble PW, Goldstein DR. The role of hyaluronan degradation products as innate alloimmune agonists. Am J Transplant. 2006;6(11):2622-2635.
28. Vasioukhin V, Degenstein L, Wise B, Fuchs E. The magical touch: genome targeting in epidermal stem cells induced by tamoxifen application to mouse skin. Proc Natl Acad Sci U S A. 1999;96(15):8551-8556.
29. Hathcock KS, Laszlo G, Pucillo C, Linsley P, Hodes RJ. Comparative analysis of B7-1 and B7-2 costimulatory ligands: expression and function. J Exp Med. 1994;180(2):631-640.
30. Bursch LS, et al. Identification of a novel population of Langerin+ dendritic cells. J Exp Med. 2007; 204(13):3147-3156.
31. Wang L, Bursch LS, Kissenpfennig A, Malissen B, Jameson SC, Hogquist KA. Langerin expressing cells promote skin immune responses under defined conditions. J Immunol. 2008;180(7):4722-4727.
32. Jameson J, et al. A role for skin gammadelta T cells in wound repair. Science. 2002;296(5568):747-749.
33. Scheibner KA, Lutz MA, Boodoo S, Fenton MJ, Powell JD, Horton MR. Hyaluronan fragments act as an endogenous danger signal by engaging TLR2. J Immunol. 2006;177(2):1272-1281.
34. Csoka AB, Frost GI, Stern R. The six hyaluronidaselike genes in the human and mouse genomes. Matrix Biol. 2001;20(8):499-508.
35. Reitinger S, Mullegger J, Greiderer B, Nielsen JE, Lepperdinger G. Designed human serum hyaluronidase 1 variant, HYAL1δL, exhibits activity up to pH 5.9. J Biol Chem. 2009;284(29):19173-19177.
36. Csoka AB, Frost GI, Wong T, Stern R. Purification and microsequencing of hyaluronidase isozymes from human urine. FEBS Lett. 1997;417(3):307-310.
37. Natowicz MR, et al. Clinical and biochemical manifestations of hyaluronidase deficiency. N Engl J Med. 1996;335(14):1029-1033.
38. Black CA. Delayed type hypersensitivity: current theories with an historic perspective. Dermatol Online J. 1999;5(1):7.
39. Noordegraaf M, Flacher V, Stoitzner P, Clausen BE. Functional redundancy of Langerhans cells and Langerin+ dermal dendritic cells in contact hypersensitivity. J Invest Dermatol. 2010;130(12):2752-2759.
40. Mummert ME. Immunologic roles of hyaluronan. Immunol Res. 2005;31(3):189-206.
41. Alter G, et al. IL-10 induces aberrant deletion of dendritic cells by natural killer cells in the context of HIV infection. J Clin Invest. 2010;120(6):1905-1913.
42. Yang R, Yan Z, Chen F, Hansson GK, Kiessling R. Hyaluronic acid and chondroitin sulphate A rapidly promote differentiation of immature DC with upregulation of costimulatory and antigen-presenting molecules, and enhancement of NF-kappaB and protein kinase activity. Scand J Immunol. 2002;55(1):2-13.
43. Rescigno M, Granucci F, Citterio S, Foti M, Ricciardi-Castagnoli P. Coordinated events during bacteria-induced DC maturation. Immunol Today. 1999; 20(5):200-203.
44. Zmolik JM, Mummert ME. Pep-1 as a novel probe for the in situ detection of hyaluronan. J Histochem Cytochem. 2005;53(6):745-751.
45. Bitter T, Muir HM. A modified uronic acid carbazole reaction. Anal Biochem. 1962;4:330-334.
46. Lee HG, Cowman MK. An agarose gel electrophoretic method for analysis of hyaluronan molecular weight distribution. Anal Biochem. 1994; 219(2):278-287.
47. Di Nardo A, et al. Cathelicidin antimicrobial peptides block dendritic cell TLR4 activation and allergic contact sensitization. J Immunol. 2007; 178(3):1829-1834.
48. Martin SF, et al. Toll-like receptor and IL-12 signaling control susceptibility to contact hypersensitivity. J Exp Med. 2008;205(9):2151-2162.
49. Jin H, et al. IL-21R is essential for epicutaneous sensitization and allergic skin inflammation in humans and mice. J Clin Invest. 2009; 119(1):47-60.
50. Jameson JM, Cauvi G, Witherden DA, Havran WL. A keratinocyte-responsive gamma delta TCR is necessary for dendritic epidermal T cell activation by damaged keratinocytes and maintenance in the epidermis. J Immunol. 2004;172(6):3573-3579.
51. Bobr A, Olvera-Gomez I, Igyarto BZ, Haley KM, Hogquist KA, Kaplan DH. Acute ablation of Langerhans cells enhances skin immune responses. J Immunol. 2010;185(8):4724-4728.
52. Morioka Y, Yamasaki K, Leung D, Gallo RL. Cathelicidin antimicrobial peptides inhibit hyaluronan-induced cytokine release and modulate chronic allergic dermatitis. J Immunol. 2008;181(6):3915-3922.