Human β-defensin-3 increases the expression of interleukin-37 through CCR6 in human keratinocytes

Journal of Dermatological Science

Volumn 77, Issue 1, 2015, Pages 46-53

  Smithrithee, Rithee ^a   Niyonsaba, François ^a   Kiatsurayanon, Chanisa ^a   Ushio, Hiroko ^a   Ikeda, Shigaku ^a   Okumura, Ko ^a   Ogawa, Hideoki ^a  

^a JUNTENDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Caspase; CCR6; Human defensin; Interleukin 37; Keratinocyte

Indexed keywords

BETA DEFENSIN 3; CASPASE 4; CELL PROTEIN; CHEMOKINE RECEPTOR CCR6; EPIDERMAL GROWTH FACTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA CONVERTING ENZYME; INTERLEUKIN 37; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; SMAD3 PROTEIN; SMALL INTERFERING RNA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; BETA DEFENSIN; BETA-DEFENSIN 3, HUMAN; CASP4 PROTEIN, HUMAN; CCR6 PROTEIN, HUMAN; IL37 PROTEIN, HUMAN; INITIATOR CASPASE; INTERLEUKIN 1; SMAD3 PROTEIN, HUMAN;

ARTICLE; COLORIMETRY; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; ENZYME ACTIVITY; GENE; HUMAN; HUMAN CELL; IL 37 GENE; KERATINOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; UPREGULATION; WESTERN BLOTTING; AUTOIMMUNE DISEASE; CELL CULTURE; CYTOLOGY; GENE EXPRESSION REGULATION; IMMUNOLOGY; IMMUNOSUPPRESSIVE TREATMENT; INFLAMMATION; INNATE IMMUNITY; METABOLISM; PHOSPHORYLATION; PSORIASIS;

AUTOIMMUNE DISEASES; BETA-DEFENSINS; CASPASE 1; CASPASES, INITIATOR; CELLS, CULTURED; GENE EXPRESSION REGULATION; HUMANS; IMMUNITY, INNATE; IMMUNOSUPPRESSION; INFLAMMATION; INTERLEUKIN-1; KERATINOCYTES; MAP KINASE SIGNALING SYSTEM; NF-KAPPA B; PHOSPHORYLATION; PSORIASIS; RECEPTORS, CCR6; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SMAD3 PROTEIN;

EID: 84926145101     PISSN: 09231811     EISSN: 1873569X     Source Type: Journal    
DOI: 10.1016/j.jdermsci.2014.12.001     Document Type: Article

References (50)

1. Niyonsaba F., Nagaoka I., Ogawa H., Okumura K. Multifunctional antimicrobial proteins and peptides: natural activators of immune systems. Curr Pharm Des 2009, 15:2393-2413.
2. Niyonsaba F., Nagaoka I., Ogawa H. Human defensins and cathelicidins in the skin: beyond direct antimicrobial properties. Crit Rev Immunol 2006, 26:545-576.
3. Selsted M.E., Tang Y.Q., Morris W.L., McGuire P.A., Novotny M.J., Smith W., et al. Purification, primary structures, and antibacterial activities of beta-defensins, a new family of antimicrobial peptides from bovine neutrophils. J Biol Chem 1993, 268:6641-6648.
4. Ganz T., Selsted M.E., Szklarek D., Harwig S.S., Daher K., Bainton D.F., et al. Defensins. Natural peptide antibiotics of human neutrophils. J Clin Invest 1985, 76:1427-1435.
5. Ghosh D., Porter E., Shen B., Lee S.K., Wilk D., Drazba J., et al. Paneth cell trypsin is the processing enzyme for human defensin-5. Nat Immunol 2002, 3:583-590.
6. Ganz T. Defensins: antimicrobial peptides of innate immunity. Nat Rev Immunol 2003, 3:710-720.
7. Ali R.S., Falconer A., Ikram M., Bissett C.E., Cerio R., Quinn A.G. Expression of the peptide antibiotics human beta defensin-1 and human beta defensin-2 in normal human skin. J Invest Dermatol 2001, 117:106-111.
8. Fulton C., Anderson G.M., Zasloff M., Bull R., Quinn A.G. Expression of natural peptide antibiotics in human skin. Lancet 1997, 350:1750-1751.
9. Harder J., Bartels J., Christophers E., Schroder J.M. A peptide antibiotic from human skin. Nature 1997, 387:861.
10. Liu A.Y., Destoumieux D., Wong A.V., Park C.H., Valore E.V., Liu L., et al. Human beta-defensin-2 production in keratinocytes is regulated by interleukin-1, bacteria, and the state of differentiation. J Invest Dermatol 2002, 118:275-281.
11. Harder J., Bartels J., Christophers E., Schroder J.M. Isolation and characterization of human beta-defensin-3, a novel human inducible peptide antibiotic. J Biol Chem 2001, 276:5707-5713.
12. Garcia J.R., Krause A., Schulz S., Rodriguez-Jimenez F.J., Kluver E., Adermann K., et al. Human beta-defensin 4: a novel inducible peptide with a specific salt-sensitive spectrum of antimicrobial activity. FASEB J 2001, 15:1819-1821.
13. Harder J., Meyer-Hoffert U., Wehkamp K., Schwichtenberg L., Schroder J.M. Differential gene induction of human beta-defensins (hBD-1, -2 -3, and -4) in keratinocytes is inhibited by retinoic acid. J Invest Dermatol 2004, 123:522-529.
14. Niyonsaba F., Ushio H., Nagaoka I., Okumura K., Ogawa H. The human beta-defensins (-1, -2, -3 -4) and cathelicidin LL-37 induce IL-18 secretion through p38 and ERK MAPK activation in primary human keratinocytes. J Immunol 2005, 175:1776-1784.
15. Niyonsaba F., Ushio H., Nakano N., Ng W., Sayama K., Hashimoto K., et al. Antimicrobial peptides human beta-defensins stimulate epidermal keratinocyte migration, proliferation and production of proinflammatory cytokines and chemokines. J Invest Dermatol 2007, 127:594-604.
16. Sorensen O.E., Cowland J.B., Theilgaard-Monch K., Liu L., Ganz T., Borregaard N. Wound healing and expression of antimicrobial peptides/polypeptides in human keratinocytes, a consequence of common growth factors. J Immunol 2003, 170:5583-5589.
17. Nomura I., Goleva E., Howell M.D., Hamid Q.A., Ong P.Y., Hall C.F., et al. Cytokine milieu of atopic dermatitis, as compared to psoriasis, skin prevents induction of innate immune response genes. J Immunol 2003, 171:3262-3269.
18. Ong P.Y., Ohtake T., Brandt C., Strickland I., Boguniewicz M., Ganz T., et al. Endogenous antimicrobial peptides and skin infections in atopic dermatitis. N Engl J Med 2002, 347:1151-1160.
19. Kiatsurayanon C., Niyonsaba F., Smithrithee R., Akiyama T., Ushio H., Hara M., et al. Host defense (antimicrobial) peptide, human beta-defensin-3, improves the function of the epithelial tight-junction barrier in human keratinocytes. J Invest Dermatol 2014, 134:2163-2173.
20. Nold M.F., Nold-Petry C.A., Zepp J.A., Palmer B.E., Bufler P., Dinarello C.A. IL-37 is a fundamental inhibitor of innate immunity. Nat Immunol 2010, 11:1014-1022.
21. Dinarello C.A., Bufler P. Interleukin-37. Semin Immunol 2013, 25:466-468.
22. Kumar S., McDonnell P.C., Lehr R., Tierney L., Tzimas M.N., Griswold D.E., et al. Identification and initial characterization of four novel members of the interleukin-1 family. J Biol Chem 2000, 275:10308-10314.
23. Sharma S., Kulk N., Nold M.F., Graf R., Kim S.H., Reinhardt D., et al. The IL-1 family member 7b translocates to the nucleus and down-regulates proinflammatory cytokines. J Immunol 2008, 180:5477-5482.
24. Kumar S., Hanning C.R., Brigham-Burke M.R., Rieman D.J., Lehr R., Khandekar S., et al. Interleukin-1F7B (IL-1H4/IL-1F7) is processed by caspase-1 and mature IL-1F7B binds to the IL-18 receptor but does not induce IFN-gamma production. Cytokine 2002, 18:61-71.
25. Bufler P., Gamboni-Robertson F., Azam T., Kim S.H., Dinarello C.A. Interleukin-1 homologues IL-1F7b and IL-18 contain functional mRNA instability elements within the coding region responsive to lipopolysaccharide. Biochem J 2004, 381:503-510.
26. Fujita H., Inoue Y., Seto K., Komitsu N., Aihara M. Interleukin-37 is elevated in subjects with atopic dermatitis. J Dermatol Sci 2013, 69:173-175.
27. Muhr P., Zeitvogel J., Heitland I., Werfel T., Wittmann M. Expression of interleukin (IL)-1 family members upon stimulation with IL-17 differs in keratinocytes derived from patients with psoriasis and healthy donors. Br J Dermatol 2011, 165:189-193.
28. Akdis M., Burgler S., Crameri R., Eiwegger T., Fujita H., Gomez E., et al. Interleukins, from 1 to 37, and interferon-gamma: receptors, functions, and roles in diseases. J Allergy Clin Immunol 2011, 127:701-721. e701-70.
29. Pan G., Risser P., Mao W., Baldwin D.T., Zhong A.W., Filvaroff E., et al. IL-1H, an interleukin 1-related protein that binds IL-18 receptor/IL-1Rrp. Cytokine 2001, 13:1-7.
30. Boraschi D., Lucchesi D., Hainzl S., Leitner M., Maier E., Mangelberger D., et al. IL-37: a new anti-inflammatory cytokine of the IL-1 family. Eur Cytokine Netw 2011, 22:127-147.
31. Garlanda C., Dinarello C.A., Mantovani A. The interleukin-1 family: back to the future. Immunity 2013, 39:1003-1018.
32. Teng X., Hu Z., Wei X., Wang Z., Guan T., Liu N., et al. IL-37 ameliorates the inflammatory process in psoriasis by suppressing proinflammatory cytokine production. J Immunol 2014, 192:1815-1823.
33. Shi J., Aono S., Lu W., Ouellette A.J., Hu X., Ji Y., et al. A novel role for defensins in intestinal homeostasis: regulation of IL-1beta secretion. J Immunol 2007, 179:1245-1253.
34. Bulau A.M., Nold M.F., Li S., Nold-Petry C.A., Fink M., Mansell A., et al. Role of caspase-1 in nuclear translocation of IL-37, release of the cytokine, and IL-37 inhibition of innate immune responses. Proc Natl Acad Sci U S A 2014, 111:2650-2655.
35. Jinnin M., Ihn H., Tamaki K. Characterization of SIS3, a novel specific inhibitor of Smad3, and its effect on transforming growth factor-beta1-induced extracellular matrix expression. Mol Pharmacol 2006, 69:597-607.
36. Nagaoka I., Niyonsaba F., Tsutsumi-Ishii Y., Tamura H., Hirata M. Evaluation of the effect of human beta-defensins on neutrophil apoptosis. Int Immunol 2008, 20:543-553.
37. Chang L., Karin M. Mammalian MAP kinase signalling cascades. Nature 2001, 410:37-40.
38. Zhou R., O'Hara S.P., Chen X.M. MicroRNA regulation of innate immune responses in epithelial cells. Cell Mol Immunol 2011, 8:371-379.
39. Pistolic J., Cosseau C., Li Y., Yu J.J., Filewod N.C., Gellatly S., et al. Host defence peptide LL-37 induces IL-6 expression in human bronchial epithelial cells by activation of the NF-kappaB signaling pathway. J Innate Immun 2009, 1:254-267.
40. Sorensen O.E., Thapa D.R., Rosenthal A., Liu L., Roberts A.A., Ganz T. Differential regulation of beta-defensin expression in human skin by microbial stimuli. J Immunol 2005, 174:4870-4879.
41. Proud D., Sanders S.P., Wiehler S. Human rhinovirus infection induces airway epithelial cell production of human beta-defensin 2 both in vitro and in vivo. J Immunol 2004, 172:4637-4645.
42. Kanda N., Kamata M., Tada Y., Ishikawa T., Sato S., Watanabe S. Human beta-defensin-2 enhances IFN-gamma and IL-10 production and suppresses IL-17 production in T cells. J Leukoc Biol 2011, 89:935-944.
43. Singh D., Vaughan R., Kao C.C. LL-37 Peptide enhancement of signal transduction by toll-like receptor 3 is regulated by pH: identification of a peptide antagonist of LL-37. J Biol Chem 2014, 289:27614-27624.
44. Piccini A., Carta S., Tassi S., Lasiglie D., Fossati G., Rubartelli A. ATP is released by monocytes stimulated with pathogen-sensing receptor ligands and induces IL-1beta and IL-18 secretion in an autocrine way. Proc Natl Acad Sci U S A 2008, 105:8067-8072.
45. Ferry X., Brehin S., Kamel R., Landry Y. G protein-dependent activation of mast cell by peptides and basic secretagogues. Peptides 2002, 23:1507-1515.
46. Niyonsaba F., Suzuki A., Ushio H., Nagaoka I., Ogawa H., Okumura K. The human antimicrobial peptide dermcidin activates normal human keratinocytes. Br J Dermatol 2009, 160:243-249.
47. Yu J., Mookherjee N., Wee K., Bowdish D.M., Pistolic J., Li Y., et al. Host defense peptide LL-37, in synergy with inflammatory mediator IL-1beta, augments immune responses by multiple pathways. J Immunol 2007, 179:7684-7691.
48. He L., Liang Z., Zhao F., Peng L., Chen Z. Modulation of IL-37 expression by triptolide and triptonide in THP-1 cells. Cell Mol Immunol 2014, 10.1038/cmi.2014.92.
49. Wang X.C., Jobin C., Allen J.B., Roberts W.L., Jaffe G.J. Suppression of NF-kappaB-dependent proinflammatory gene expression in human RPE cells by a proteasome inhibitor. Invest Ophthalmol Vis Sci 1999, 40:477-486.
50. Zhi L., Ang A.D., Zhang H., Moore P.K., Bhatia M. Hydrogen sulfide induces the synthesis of proinflammatory cytokines in human monocyte cell line U937 via the ERK-NF-kappaB pathway. J Leukoc Biol 2007, 81:1322-1332.