Cathelicidin antimicrobial peptides inhibit hyaluronan-induced cytokine release and modulate chronic allergic dermatitis

Journal of Immunology

Volumn 181, Issue 6, 2008, Pages 3915-3922

  Morioka, Yasuhide ^a,b   Yamasaki, Kenshi ^a   Leung, Donald ^c   Gallo, Richard L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SHIONOGI AND CO LTD   (Japan)

^c NATIONAL JEWISH MEDICAL AND RESEARCH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1 FLUORO 2,4 DINITROBENZENE; CATHELICIDIN; CYCLIC AMP; EPIDERMAL GROWTH FACTOR RECEPTOR; G PROTEIN COUPLED RECEPTOR; HERMES ANTIGEN; HYALURONIC ACID; INTERLEUKIN 8; MACROPHAGE ACTIVATING LIPOPEPTIDE 2; MACROPHAGE INFLAMMATORY PROTEIN 2; PROTEIN INHIBITOR; ANTIMICROBIAL CATIONIC PEPTIDE; AUTACOID; CATHELICIDIN ANTIMICROBIAL PEPTIDE; CYTOKINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BINDING ASSAY; CELL INFILTRATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOKINE RELEASE; DISEASE MODEL; DRUG INHIBITION; DRUG POTENCY; DRUG PROTEIN BINDING; DRUG TARGETING; IMMUNOMODULATION; MALE; MEMBRANE BINDING; MOUSE; NONHUMAN; OTITIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SKIN ALLERGY; SKIN INFLAMMATION; WILD TYPE; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; CELL ADHESION; CELL CULTURE; CELL LINE; CHRONIC DISEASE; DRUG ANTAGONISM; GENETICS; HUMAN; IMMUNOLOGY; MACROPHAGE; METABOLISM; MOUSE MUTANT; PATHOLOGY; PHYSIOLOGY; SECRETION; TUMOR CELL LINE;

ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; CELL ADHESION; CELL LINE; CELL LINE, TUMOR; CELLS, CULTURED; CHRONIC DISEASE; CYTOKINES; DERMATITIS, ALLERGIC CONTACT; HUMANS; HYALURONIC ACID; INFLAMMATION MEDIATORS; MACROPHAGES; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT;

EID: 56149103147     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.181.6.3915     Document Type: Article

References (54)

1. Zasloff, M. 2002. Antimicrobial peptides of multicellular organisms. Nature 415: 389-395.
2. Braff, M. H., A. Bardan, V. Nizet, and R. L. Gallo. 2005. Cutaneous defense mechanisms by antimicrobial peptides. J. Invest. Dermatol. 125: 9-13. (Pubitemid 40981418)
3. Zanetti, M. 2005. The role of cathelicidins in the innate host defenses of mammals. Curr. Issues Mol. Biol. 7: 179-196. (Pubitemid 41051685)
4. Howell, M. D., J. F. Jones, K. O. Kisich, J. E. Streib, R. L. Gallo, and D. Y. Leung. 2004. Selective killing of vaccinia virus by LL-37: implications for eczema vaccinatum. J. Immunol. 172: 1763-1767.
5. Chromek, M., Z. Slamova, P. Bergman, L. Kovacs, L. Podracka, I. Ehren, T. Hokfelt, G. H. Gudmundsson, R. L. Gallo, B. Agerberth, and A. Brauner. 2006. The antimicrobial peptide cathelicidin protects the urinary tract against invasive bacterial infection. Nat. Med. 12: 636-641. (Pubitemid 43865231)
6. Nizet, V., T. Ohtake, X. Lauth, J. Trowbridge, J. Rudisill, R. A. Dorschner, V. Pestonjamasp, J. Piraino, K. Huttner, and R. L. Gallo. 2001. Innate antimicrobial peptide protects the skin from invasive bacterial infection. Nature 414: 454-457. (Pubitemid 34173727)
7. Ong, P. Y., T. Ohtake, C. Brandt, I. Strickland, M. Boguniewicz, T. Ganz, R. L. Gallo, and D. Y. Leung. 2002. Endogenous antimicrobial peptides and skin infections in atopic dermatitis. N. Engl. J. Med. 347: 1151-1160.
8. Carretero, M., M. J. Escamez, M. Garcia, B. Duarte, A. Holguin, L. Retamosa, J. L. Jorcano, M. D. Rio, and F. Larcher. 2008. In vitro and in vivo wound healing-promoting activities of human cathelicidin LL-37. J. Invest. Dermatol. 128: 223-236. (Pubitemid 350249392)
9. Yamasaki, K., A. Di Nardo, A. Bardan, M. Murakami, T. Ohtake, A. Coda, R. A. Dorschner, C. Bonnart, P. Descargues, A. Hovnanian, et al. 2007. Increased serine protease activity and cathelicidin promotes skin inflammation in rosacea. Nat. Med. 13: 975-980. (Pubitemid 47222043)
10. Dorschner, R. A., V. K. Pestonjamasp, S. Tamakuwala, T. Ohtake, J. Rudisill, V. Nizet, B. Agerberth, G. H. Gudmundsson, and R. L. Gallo. 2001. Cutaneous injury induces the release of cathelicidin anti-microbial peptides active against group A Streptococcus. J. Invest. Dermatol. 117: 91-97.
11. Braff, M. H., M. A. Hawkins, A. Di Nardo, B. Lopez-Garcia, M. D. Howell, C. Wong, K. Lin, J. E. Streib, R. Dorschner, D. Y. Leung, and R. L. Gallo. 2005. Structure-function relationships among human cathelicidin peptides: dissociation of antimicrobial properties from host immunostimulatory activities. J. Immunol. 174: 4271-4278.
12. Kurosaka, K., Q. Chen, F. Yarovinsky, J. J. Oppenheim, and D. Yang. 2005. Mouse cathelin-related antimicrobial peptide chemoattracts leukocytes using formyl peptide receptor-like 1/mouse formyl peptide receptor-like 2 as the receptor and acts as an immune adjuvant. J. Immunol. 174: 6257-6265. (Pubitemid 40663818)
13. Lande, R., J. Gregorio, V. Facchinetti, B. Chatterjee, Y. H. Wang, B. Homey, W. Cao, Y. H. Wang, B. Su, F. O. Nestle, et al. 2007. Plasmacytoid dendritic cells sense self-DNA coupled with antimicrobial peptide. Nature 449: 564-569. (Pubitemid 47525141)
14. Howell, M. D., R. L. Gallo, M. Boguniewicz, J. F. Jones, C. Wong, J. E. Streib, and D. Y. Leung. 2006. Cytokine milieu of atopic dermatitis skin subverts the innate immune response to vaccinia virus. Immunity 24: 341-348.
15. Howell, M. D., A. Wollenberg, R. L. Gallo, M. Flaig, J. E. Streib, C. Wong, T. Pavicic, M. Boguniewicz, and D. Y. Leung. 2006. Cathelicidin deficiency predisposes to eczema herpeticum. J. Allergy Clin. Immunol. 117: 836-841.
16. Di Nardo, A., M. H. Braff, K. R. Taylor, C. Na, R. D. Granstein, J. E. McInturff, S. Krutzik, R. L. Modlin, and R. L. Gallo. 2007. Cathelicidin antimicrobial peptides block dendritic cell TLR4 activation and allergic contact sensitization. J. Immunol. 178: 1829-1834. (Pubitemid 46154655)
17. 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. (Pubitemid 43093664)
18. 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. (Pubitemid 34074500)
19. Stern, R., A. A. Asari, and K. N. Sugahara. 2006. Hyaluronan fragments: an information-rich system. Eur. J. Cell Biol. 85: 699-715.
20. Jiang, D., J. Liang, and P. W. Noble. 2007. Hyaluronan in tissue injury and repair. Annu. Rev. Cell Dev. Biol. 23: 435-461.
21. 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.
22. Taylor, K. R., K. Yamasaki, K. A. Radek, A. Di Nardo, H. Goodarzi, D. Golenbock, B. Beutler, and R. L. Gallo. 2007. Recognition of hyaluronan released in sterile injury involves a unique receptor complex dependent on Tolllike receptor 4, CD44, and MD-2. J. Biol. Chem. 282: 18265-18275.
23. Nagai, H., Y. Ueda, T. Ochi, Y. Hirano, H. Tanaka, N. Inagaki, and K. Kawada. 2000. Different role of IL-4 in the onset of hapten-induced contact hypersensitivity in BALB/c and C57BL/6 mice. Br. J. Pharmacol. 129: 299-306. (Pubitemid 30072650)
24. Zmolik, J. M., and M. E. Mummert. 2005. Pep-1 as a novel probe for the in situ detection of hyaluronan. J. Histochem. Cytochem. 53: 745-751. (Pubitemid 40726954)
25. Gee, K., M. Kozlowski, and A. Kumar. 2003. Tumor necrosis factor-α induces functionally active hyaluronan-adhesive CD44 by activating sialidase through p38 mitogen-activated protein kinase in lipopolysaccharide-stimulated human monocytic cells. J. Biol. Chem. 278: 37275-37287. (Pubitemid 37175244)
26. Mummert, M. E., M. Mohamadzadeh, D. I. Mummert, N. Mizumoto, and A. Takashima. 2000. Development of a peptide inhibitor of hyaluronan-mediated leukocyte trafficking. J. Exp. Med. 192: 769-779.
27. Mookherjee, N., L. M. Rehaume, and R. E. Hancock. 2007. Cathelicidins and functional analogues as antisepsis molecules. Expert Opin. Ther. Targets 11: 993-1004. (Pubitemid 47240677)
28. Miyake, K., C. B. Underhill, J. Lesley, and P. W. Kincade. 1990. Hyaluronate can function as a cell adhesion molecule and CD44 participates in hyaluronate recognition. J. Exp. Med. 172: 69-75. (Pubitemid 20217247)
29. Matsuoka, T., M. Hirata, H. Tanaka, Y. Takahashi, T. Murata, K. Kabashima, Y. Sugimoto, T. Kobayashi, F. Ushikubi, Y. Aze, et al. 2000. Prostaglandin D2 as a mediator of allergic asthma. Science 287: 2013-2017.
30. Herrick, C. A., L. Xu, A. N. McKenzie, R. E. Tigelaar, and K. Bottomly. 2003. IL-13 is necessary, not simply sufficient, for epicutaneously induced Th2 responses to soluble protein antigen. J. Immunol. 170: 2488-2495.
31. Mookherjee, N., K. L. Brown, D. M. Bowdish, S. Doria, R. Falsafi, K. Hokamp, F. M. Roche, R. Mu, G. H. Doho, J. Pistolic, et al. 2006. Modulation of the TLR-mediated inflammatory response by the endogenous human host defense peptide LL-37. J. Immunol. 176: 2455-2464. (Pubitemid 43201696)
32. Kandler, K., R. Shaykhiev, P. Kleemann, F. Klescz, M. Lohoff, C. Vogelmeier, and R. Bals. 2006. The anti-microbial peptide LL-37 inhibits the activation of dendritic cells by TLR ligands. Int. Immunol. 18: 1729-1736. (Pubitemid 44884035)
33. Rosenfeld, Y., N. Papo, and Y. Shai. 2006. Endotoxin (lipopolysaccharide) neutralization by innate immunity host-defense peptides: peptide properties and plausible modes of action. J. Biol. Chem. 281: 1636-1643. (Pubitemid 43752480)
34. Baranska-Rybak, W., A. Sonesson, R. Nowicki, and A. Schmidtchen. 2006. Glycosaminoglycans inhibit the antibacterial activity of LL-37 in biological fluids. J. Antimicrob. Chemother. 57: 260-265. (Pubitemid 43160167)
35. Liu, D., and M. S. Sy. 1997. Phorbol myristate acetate stimulates the dimerization of CD44 involving a cysteine in the transmembrane domain. J. Immunol. 159: 2702-2711.
36. Suzuki, M., H. Kobayashi, M. Fujie, T. Nishida, M. Takigawa, N. Kanayama, and T. Terao. 2002. Kunitz-type protease inhibitor bikunin disrupts phorbol esterinduced oligomerization of CD44 variant isoforms containing epitope v9 and subsequently suppresses expression of urokinase-type plasminogen activator in human chondrosarcoma cells. J. Biol. Chem. 277: 8022-8032. (Pubitemid 34968254)
37. 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.
38. McKee, C. M., M. B. Penno, M. Cowman, M. D. Burdick, R. M. Strieter, C. Bao, and P. W. 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.
39. McKee, C. M., C. J. Lowenstein, M. R. Horton, J. Wu, C. Bao, B. Y. Chin, A. M. K. 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.
40. 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. 162: 4171-4176.
41. Noble, P. W., F. R. Lake, P. M. Henson, and D. W. 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.
42. Hodge-Dufour, J., P. W. Noble, M. R. Horton, C. Bao, M. Wysoka, M. D. Burdick, R. M. Strieter, 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. (Pubitemid 127681045)
43. 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. 273: 35088-35094.
44. Katoh, S., Z. Zheng, K. Oritani, T. Shimozato, and P. W. Kincade. 1995. Glycosylation of CD44 negatively regulates its recognition of hyaluronan. J. Exp. Med. 182: 419-429.
45. 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. (Pubitemid 29234556)
46. Blundell, C. D., A. Almond, D. J. Mahoney, P. L. DeAngelis, I. D. Campbell, and A. J. Day. 2005. Towards a structure for a TSG-6.hyaluronan complex by modeling and NMR spectroscopy: insights into other members of the link module superfamily. J. Biol. Chem. 280: 18189-18201.
47. Blundell, C. D., D. J. Mahoney, A. Almond, P. L. DeAngelis, J. D. Kahmann, P. Teriete, A. R. Pickford, I. D. Campbell, and A. J. Day. 2003. The link module from ovulation- and inflammation-associated protein TSG-6 changes conformation on hyaluronan binding. J. Biol. Chem. 278: 49261-49270.
48. Man, M. Q., Y. Hatano, S. H. Lee, M. Man, S. Chang, K. R. Feingold, D. Y. Leung, W. Holleran, Y. Uchida, and P. M. Elias. 2008. Characterization of a hapten-induced, murine model with multiple features of atopic dermatitis: structural, immunologic, and biochemical changes following single versus multiple oxazolone challenges. J. Invest. Dermatol. 128: 79-86.
49. Camp, R. L., A. Scheynius, C. Johansson, and E. Pure. 1993. CD44 is necessary for optimal contact allergic responses but is not required for normal leukocyte extravasation. J. Exp. Med. 178: 497-507.
50. Gonda, A., I. Gal, S. Szanto, B. Sarraj, T. T. Glant, J. Hunyadi, and K. Mikecz. 2005. CD44, but not l-selectin, is critically involved in leucocyte migration into the skin in a murine model of allergic dermatitis. Exp. Dermatol. 14: 700-708. (Pubitemid 41150366)
51. 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. (Pubitemid 37315901)
52. Inagaki, N., N. Shiraishi, K. Igeta, T. Itoh, T. Chikumoto, M. Nagao, J. F. Kim, and H. Nagai. 2006. Inhibition of scratching behavior associated with allergic dermatitis in mice by tacrolimus, but not by dexamethasone. Eur. J. Pharmacol. 546: 189-196. (Pubitemid 44331846)
53. Bender, B. G., R. Ballard, B. Canono, J. R. Murphy, and D. Y. Leung. 2008. Disease severity, scratching, and sleep quality in patients with atopic dermatitis. J. Am. Acad. Dermatol. 58: 415-420. (Pubitemid 351226301)
54. De, Y., Q. Chen, A. P. Schmidt, G. M. Anderson, J. M. Wang, J. Wooters, J. J. Oppenheim, and O. Chertov. 2000. LL-37, the neutrophil granule- and epithelial cell-derived cathelicidin, utilizes formyl peptide receptor-like 1 (FPRL1) as a receptor to chemoattract human peripheral blood neutrophils, monocytes, and T cells. J. Exp. Med. 192: 1069-1074.