Antimicrobial peptides in the pathogenesis of psoriasis

Journal of Dermatology

Volumn 39, Issue 3, 2012, Pages 225-230

  Morizane, Shin ^a   Gallo, Richard L ^b,c  

^a OKAYAMA UNIVERSITY   (Japan)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

Author keywords

antimicrobial peptides; cathelicidin; LL 37; psoriasis; Toll like receptor

Indexed keywords

BETA DEFENSIN; BETA DEFENSIN 1; BETA DEFENSIN 2; BETA DEFENSIN 3; BETA DEFENSIN 4; CALCIPOTRIOL; CALGRANULIN A; CALGRANULIN B; CATHELICIDIN; CATHELICIDIN ANTIMICROBIAL PEPTIDE LL 37; COLECALCIFEROL; GAMMA INTERFERON; INTERLEUKIN 12; INTERLEUKIN 17; INTERLEUKIN 22; INTERLEUKIN 23; POLYPEPTIDE ANTIBIOTIC AGENT; PROTEIN S 100; PSORIASIN; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; CELL REGENERATION; HUMAN; IMMUNE RESPONSE; NONHUMAN; PATHOGENESIS; PROTEIN EXPRESSION; PSORIASIS; PSORIASIS VULGARIS; TH1 CELL; TH17 CELL; ULTRAVIOLET B RADIATION;

ANIMALS; CATHELICIDINS; CHOLECALCIFEROL; DEFENSINS; HUMANS; PSORIASIS; S100 PROTEINS;

EID: 84857536801     PISSN: 03852407     EISSN: 13468138     Source Type: Journal    
DOI: 10.1111/j.1346-8138.2011.01483.x     Document Type: Article

References (80)

1. Nestle FO, Kaplan DH, Barker J,. Psoriasis. N Engl J Med 2009; 361: 496-509.
2. Weinstein GD, McCullough JL, Ross PA,. Cell kinetic basis for pathophysiology of psoriasis. J Invest Dermatol 1985; 85: 579-583. (Pubitemid 16204237)
3. Lebwohl M,. Psoriasis. Lancet 2003; 361: 1197-1204. (Pubitemid 36398393)
4. Wrone-Smith T, Nickoloff BJ,. Dermal injection of immunocytes induces psoriasis. J Clin Invest 1996; 98: 1878-1887. (Pubitemid 26359206)
5. Griffiths CE, Voorhees JJ,. Cyclosporine A in the treatment of psoriasis: a clinical and mechanistic perspective. J Invest Dermatol 1990; 95: 53S-55S.
6. Griffiths CE, Powles AV, Leonard JN, Fry L, Baker BS, Valdimarsson H,. Clearance of psoriasis with low dose cyclosporin. Br Med J (Clin Res Ed) 1986; 293: 731-732. (Pubitemid 16025288)
7. Ellis CN, Gorsulowsky DC, Hamilton TA, et al. Cyclosporine improves psoriasis in a double-blind study. JAMA 1986; 256: 3110-3116. (Pubitemid 17045825)
8. Teunissen MB, Koomen CW, de Waal Malefyt R, Wierenga EA, Bos JD,. Interleukin-17 and interferon-gamma synergize in the enhancement of proinflammatory cytokine production by human keratinocytes. J Invest Dermatol 1998; 111: 645-649. (Pubitemid 28452327)
9. Lee E, Trepicchio WL, Oestreicher JL, et al. Increased expression of interleukin 23 p19 and p40 in lesional skin of patients with psoriasis vulgaris. J Exp Med 2004; 199: 125-130. (Pubitemid 38076484)
10. Chan JR, Blumenschein W, Murphy E, et al. IL-23 stimulates epidermal hyperplasia via TNF and IL-20R2-dependent mechanisms with implications for psoriasis pathogenesis. J Exp Med 2006; 203: 2577-2587. (Pubitemid 44833335)
11. Piskin G, Sylva-Steenland RM, Bos JD, Teunissen MB,. In vitro and in situ expression of IL-23 by keratinocytes in healthy skin and psoriasis lesions: enhanced expression in psoriatic skin. J Immunol 2006; 176: 1908-1915. (Pubitemid 43134336)
12. Toichi E, Torres G, McCormick TS, et al. An anti-IL-12p40 antibody down-regulates type 1 cytokines, chemokines, and IL-12/IL-23 in psoriasis. J Immunol 2006; 177: 4917-4926. (Pubitemid 44469828)
13. Krueger GG, Langley RG, Leonardi C, et al. A human interleukin-12/23 monoclonal antibody for the treatment of psoriasis. N Engl J Med 2007; 356: 580-592. (Pubitemid 46220818)
14. Wilson NJ, Boniface K, Chan JR, et al. Development, cytokine profile and function of human interleukin 17-producing helper T cells. Nat Immunol 2007; 8: 950-957. (Pubitemid 47300009)
15. Zheng Y, Danilenko DM, Valdez P, et al. Interleukin-22, a T(H)17 cytokine, mediates IL-23-induced dermal inflammation and acanthosis. Nature 2007; 445: 648-651. (Pubitemid 46232884)
16. Ma HL, Liang S, Li J, et al. IL-22 is required for Th17 cell-mediated pathology in a mouse model of psoriasis-like skin inflammation. J Clin Invest 2008; 118: 597-607. (Pubitemid 351206549)
17. Peric M, Koglin S, Kim SM, et al. IL-17A enhances vitamin D3-induced expression of cathelicidin antimicrobial peptide in human keratinocytes. J Immunol 2008; 181: 8504-8512.
18. van Beelen AJ, Teunissen MB, Kapsenberg ML, de Jong EC,. Interleukin-17 in inflammatory skin disorders. Curr Opin Allergy Clin Immunol 2007; 7: 374-381. (Pubitemid 47415279)
19. Tesmer LA, Lundy SK, Sarkar S, Fox DA,. Th17 cells in human disease. Immunol Rev 2008; 223: 87-113. (Pubitemid 351986173)
20. Albanesi C, De Pita O, Girolomoni G,. Resident skin cells in psoriasis: a special look at the pathogenetic functions of keratinocytes. Clin Dermatol 2007; 25: 581-588. (Pubitemid 350087605)
21. Lai Y, Gallo RL,. AMPed up immunity: how antimicrobial peptides have multiple roles in immune defense. Trends Immunol 2009; 30: 131-141.
22. Buchau AS, Gallo RL,. Innate immunity and antimicrobial defense systems in psoriasis. Clin Dermatol 2007; 25: 616-624. (Pubitemid 350087608)
23. Harder J, Schroder JM,. Psoriatic scales: a promising source for the isolation of human skin-derived antimicrobial proteins. J Leukoc Biol 2005; 77: 476-486. (Pubitemid 40489523)
24. Harder J, Bartels J, Christophers E, Schroder JM,. Isolation and characterization of human beta-defensin-3, a novel human inducible peptide antibiotic. J Biol Chem 2001; 276: 5707-5713.
25. Harder J, Bartels J, Christophers E, Schroder JM,. A peptide antibiotic from human skin. Nature 1997; 387: 861.
26. Hollox EJ, Huffmeier U, Zeeuwen PL, et al. Psoriasis is associated with increased beta-defensin genomic copy number. Nat Genet 2008; 40: 23-25.
27. Nomura I, Goleva E, Howell MD, 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. (Pubitemid 37093553)
28. Liang SC, Tan XY, Luxenberg DP, et al. Interleukin (IL)-22 and IL-17 are coexpressed by Th17 cells and cooperatively enhance expression of antimicrobial peptides. J Exp Med 2006; 203: 2271-2279. (Pubitemid 44498362)
29. Ong PY, Ohtake T, Brandt C, et al. Endogenous antimicrobial peptides and skin infections in atopic dermatitis. N Engl J Med 2002; 347: 1151-1160.
30. Eckert RL, Broome AM, Ruse M, Robinson N, Ryan D, Lee K,. S100 proteins in the epidermis. J Invest Dermatol 2004; 123: 23-33. (Pubitemid 38833459)
31. Madsen P, Rasmussen HH, Leffers H, et al. Molecular cloning, occurrence, and expression of a novel partially secreted protein "psoriasin" that is highly up-regulated in psoriatic skin. J Invest Dermatol 1991; 97: 701-712.
32. Glaser R, Meyer-Hoffert U, Harder J, et al. The antimicrobial protein psoriasin (S100A7) is upregulated in atopic dermatitis and after experimental skin barrier disruption. J Invest Dermatol 2009; 129: 641-649.
33. Peric M, Koglin S, Dombrowski Y, et al. Vitamin D analogs differentially control antimicrobial peptide/"alarmin" expression in psoriasis. PLoS One 2009; 4: e6340.
34. Glaser R, Harder J, Lange H, Bartels J, Christophers E, Schroder JM,. Antimicrobial psoriasin (S100A7) protects human skin from Escherichia coli infection. Nat Immunol 2005; 6: 57-64. (Pubitemid 40136696)
35. Jinquan T, Vorum H, Larsen CG, et al. Psoriasin: a novel chemotactic protein. J Invest Dermatol 1996; 107: 5-10.
36. Mendez-Samperio P,. The human cathelicidin hCAP18/LL-37: a multifunctional peptide involved in mycobacterial infections. Peptides 2010; 31: 1791-1798.
37. Braff MH, Hawkins MA, Di Nardo A, et al. Structure-function relationships among human cathelicidin peptides: dissociation of antimicrobial properties from host immunostimulatory activities. J Immunol 2005; 174: 4271-4278. (Pubitemid 40396008)
38. Yamasaki K, Di Nardo A, Bardan A, et al. Increased serine protease activity and cathelicidin promotes skin inflammation in rosacea. Nat Med 2007; 13: 975-980. (Pubitemid 47222043)
39. Mookherjee N, Brown KL, Bowdish DM, et al. Modulation of the TLR-mediated inflammatory response by the endogenous human host defense peptide LL-37. J Immunol 2006; 176: 2455-2464. (Pubitemid 43201696)
40. Mookherjee N, Wilson HL, Doria S, et al. Bovine and human cathelicidin cationic host defense peptides similarly suppress transcriptional responses to bacterial lipopolysaccharide. J Leukoc Biol 2006; 80: 1563-1574. (Pubitemid 44904995)
41. 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: 3915-3922.
42. De Y, Chen Q, Schmidt AP, et al. 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 2000; 192: 1069-1074.
43. Koczulla R, von Degenfeld G, Kupatt C, et al. An angiogenic role for the human peptide antibiotic LL-37/hCAP-18. J Clin Invest 2003; 111: 1665-1672. (Pubitemid 38057748)
44. Tokumaru S, Sayama K, Shirakata Y, et al. Induction of keratinocyte migration via transactivation of the epidermal growth factor receptor by the antimicrobial peptide LL-37. J Immunol 2005; 175: 4662-4668. (Pubitemid 41362007)
45. Yamasaki K, Schauber J, Coda A, et al. Kallikrein-mediated proteolysis regulates the antimicrobial effects of cathelicidins in skin. FASEB J 2006; 20: 2068-2080. (Pubitemid 44953906)
46. Frohm M, Agerberth B, Ahangari G, et al. The expression of the gene coding for the antibacterial peptide LL-37 is induced in human keratinocytes during inflammatory disorders. J Biol Chem 1997; 272: 15258-15263. (Pubitemid 27255544)
47. Morizane S, Yamasaki K, Muhleisen B, et al. Cathelicidin antimicrobial peptide LL-37 in psoriasis enables keratinocyte reactivity against TLR9 ligands. J Invest Dermatol 2012; 132: 135-143.
48. Lande R, Gregorio J, Facchinetti V, et al. Plasmacytoid dendritic cells sense self-DNA coupled with antimicrobial peptide. Nature 2007; 449: 564-569. (Pubitemid 47525141)
49. Hemmi H, Takeuchi O, Kawai T, et al. A Toll-like receptor recognizes bacterial DNA. Nature 2000; 408: 740-745. (Pubitemid 32015992)
50. Lebre MC, van der Aar AM, van Baarsen L, et al. Human keratinocytes express functional Toll-like receptor 3, 4, 5, and 9. J Invest Dermatol 2007; 127: 331-341. (Pubitemid 46106911)
51. Miller LS, Sorensen OE, Liu PT, et al. TGF-alpha regulates TLR expression and function on epidermal keratinocytes. J Immunol 2005; 174: 6137-6143. (Pubitemid 40663803)
52. Downs AM, Dunnill MG,. Exacerbation of psoriasis by interferon-alpha therapy for hepatitis C. Clin Exp Dermatol 2000; 25: 351-352. (Pubitemid 30670597)
53. Fah J, Pavlovic J, Burg G,. Expression of MxA protein in inflammatory dermatoses. J Histochem Cytochem 1995; 43: 47-52.
54. Funk J, Langeland T, Schrumpf E, Hanssen LE,. Psoriasis induced by interferon-alpha. Br J Dermatol 1991; 125: 463-465.
55. Hida S, Ogasawara K, Sato K, et al. CD8(+) T cell-mediated skin disease in mice lacking IRF-2, the transcriptional attenuator of interferon-alpha/beta signaling. Immunity 2000; 13: 643-655.
56. Ketikoglou I, Karatapanis S, Elefsiniotis I, Kafiri G, Moulakakis A,. Extensive psoriasis induced by pegylated interferon alpha-2b treatment for chronic hepatitis B. Eur J Dermatol 2005; 15: 107-109. (Pubitemid 40434638)
57. Kowalzick L,. Psoriasis flare caused by recombinant interferon beta injections. J Am Acad Dermatol 1997; 36: 501. (Pubitemid 27131991)
58. Ladoyanni E, Nambi R,. Psoriasis exacerbated by interferon-alpha in a patient with chronic myeloid leukemia. J Drugs Dermatol 2005; 4: 221-222.
59. Lopez-Lerma I, Iranzo P, Herrero C,. New-onset psoriasis in a patient treated with interferon beta-1a. Br J Dermatol 2009; 160: 716-717.
60. Pauluzzi P, Kokelj F, Perkan V, Pozzato G, Moretti M,. Psoriasis exacerbation induced by interferon-alpha. Report of two cases. Acta Derm Venereol 1993; 73: 395. (Pubitemid 23310808)
61. Schmid P, Itin P, Cox D, McMaster GK, Horisberger MA,. The type I interferon system is locally activated in psoriatic lesions. J Interferon Res 1994; 14: 229-234.
62. Suomela S, Cao L, Bowcock A, Saarialho-Kere U,. Interferon alpha-inducible protein 27 (IFI27) is upregulated in psoriatic skin and certain epithelial cancers. J Invest Dermatol 2004; 122: 717-721. (Pubitemid 38471341)
63. van der Fits L, van der Wel LI, Laman JD, Prens EP, Verschuren MC,. In psoriasis lesional skin the type I interferon signaling pathway is activated, whereas interferon-alpha sensitivity is unaltered. J Invest Dermatol 2004; 122: 51-60. (Pubitemid 38114638)
64. Webster GF, Knobler RL, Lublin FD, Kramer EM, Hochman LR,. Cutaneous ulcerations and pustular psoriasis flare caused by recombinant interferon beta injections in patients with multiple sclerosis. J Am Acad Dermatol 1996; 34: 365-367. (Pubitemid 26059484)
65. Banchereau J, Pascual V, Palucka AK,. Autoimmunity through cytokine-induced dendritic cell activation. Immunity 2004; 20: 539-550. (Pubitemid 38638124)
66. Nestle FO, Conrad C, Tun-Kyi A, et al. Plasmacytoid predendritic cells initiate psoriasis through interferon-alpha production. J Exp Med 2005; 202: 135-143. (Pubitemid 41002916)
67. Ganguly D, Chamilos G, Lande R, et al. Self-RNA-antimicrobial peptide complexes activate human dendritic cells through TLR7 and TLR8. J Exp Med 2009; 206: 1983-1994.
68. Hansel A, Gunther C, Ingwersen J, et al. Human slan (6-sulfo LacNAc) dendritic cells are inflammatory dermal dendritic cells in psoriasis and drive strong TH17/TH1 T-cell responses. J Allergy Clin Immunol 2011; 127: 787-794.
69. Chamorro CI, Weber G, Gronberg A, Pivarcsi A, Stahle M,. The human antimicrobial peptide LL-37 suppresses apoptosis in keratinocytes. J Invest Dermatol 2009; 129: 937-944.
70. Kanda N, Ishikawa T, Kamata M, Tada Y, Watanabe S,. Increased serum leucine, leucine-37 levels in psoriasis: positive and negative feedback loops of leucine, leucine-37 and pro- or anti-inflammatory cytokines. Hum Immunol 2010; 71: 1161-1171.
71. Holick MF,. Vitamin D and bone health. J Nutr 1996; 126: 1159S-1164S. (Pubitemid 26105652)
72. Dombrowski Y, Peric M, Koglin S, Ruzicka T, Schauber J,. Control of cutaneous antimicrobial peptides by vitamin D3. Arch Dermatol Res 2010; 302: 401-408.
73. Schauber J, Dorschner RA, Coda AB, et al. Injury enhances TLR2 function and antimicrobial peptide expression through a vitamin D-dependent mechanism. J Clin Invest 2007; 117: 803-811. (Pubitemid 46348539)
74. Miller J, Gallo RL,. Vitamin D and innate immunity. Dermatol Ther 2010; 23: 13-22.
75. Fogh K, Kragballe K,. Recent developments in vitamin D analogs. Curr Pharm Des 2000; 6: 961-972. (Pubitemid 30409392)
76. Gorman S, Kuritzky LA, Judge MA, et al. Topically applied 1,25-dihydroxyvitamin D3 enhances the suppressive activity of CD4+CD25+ cells in the draining lymph nodes. J Immunol 2007; 179: 6273-6283.
77. Wang TT, Nestel FP, Bourdeau V, et al. Cutting edge: 1,25- dihydroxyvitamin D3 is a direct inducer of antimicrobial peptide gene expression. J Immunol 2004; 173: 2909-2912. (Pubitemid 39141992)
78. Dombrowski Y, Peric M, Koglin S, et al. Cytosolic DNA triggers inflammasome activation in keratinocytes in psoriatic lesions. Sci Transl Med 2011; 3: 82ra38.
79. Gambichler T, Kobus S, Kobus A, et al. Expression of antimicrobial peptides and proteins in etanercept-treated psoriasis patients. Regul Pept 2011; 167: 163-166.
80. Vahavihu K, Ala-Houhala M, Peric M, et al. Narrowband ultraviolet B treatment improves vitamin D balance and alters antimicrobial peptide expression in skin lesions of psoriasis and atopic dermatitis. Br J Dermatol 2010; 163: 321-328.