Journal of Dermatological Science
Volume 65, Issue 1 , Pages 4-11 , January 2012

Chemokine receptors in the pathogenesis and therapy of psoriasis

  • Tomotaka Mabuchi

      Affiliations

    • Department of Dermatology, Medical College of Wisconsin, WI, USA
    • Department of Dermatology, Tokai University School of Medicine, Kanagawa, Japan
    • Corresponding Author InformationCorresponding author at: Department of Dermatology, Tokai University School of Medicine, 143, Shimokasuya, Isehara, Kanagawa 259-1193, Japan. Tel.: +81 463 93 1121; fax: +81 463 93 9387.
  • ,
  • Timothy W. Chang

      Affiliations

    • Department of Dermatology, Medical College of Wisconsin, WI, USA
  • ,
  • Suzanne Quinter

      Affiliations

    • Department of Dermatology, Medical College of Wisconsin, WI, USA
  • ,
  • Sam T. Hwang

      Affiliations

    • Department of Dermatology, Medical College of Wisconsin, WI, USA

Received 6 October 2011 ,Revised 10 November 2011 ,Accepted 14 November 2011.

References 

  1. Christophers E. Psoriasis – epidemiology and clinical spectrum. Clin Exp Dermatol. 2001;26:314–320
  2. Kawada A, Tezuka T, Nakamizo Y, Kimura H, Nakagawa H, Ohkido M, et al. A survey of psoriasis patients in Japan from 1982 to 2001. J Dermatol Sci. 2003;31:59–64
  3. Mueller W, Herrmann B. Cyclosporin A for psoriasis. N Engl J Med. 1979;301:555
  4. 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
  5. Clark RA, Chong B, Mirchandani N, Brinster NK, Yamanaka K, Dowgiert RK, et al. The vast majority of CLA+ T cells are resident in normal skin. J Immunol. 2006;176:4431–4439
  6. Suarez-Farinas M, Fuentes-Duculan J, Lowes MA, Krueger JG. Resolved psoriasis lesions retain expression of a subset of disease-related genes. J Invest Dermatol. 2011;131:391–400
  7. Homey B, Alenius H, Muller A, Soto H, Bowman EP, Yuan W, et al. CCL27–CCR10 interactions regulate T cell-mediated skin inflammation. Nat Med. 2002;8:157–165
  8. Lonsdorf AS, Hwang ST, Enk AH. Chemokine receptors in T-cell-mediated diseases of the skin. J Invest Dermatol. 2009;129:2552–2566
  9. Charo IF, Ransohoff RM. The many roles of chemokines and chemokine receptors in inflammation. N Engl J Med. 2006;354:610–621
  10. Bromley SK, Mempel TR, Luster AD. Orchestrating the orchestrators: chemokines in control of T cell traffic. Nat Immunol. 2008;9:970–980
  11. Liu P, Cheng H, Roberts TM, Zhao JJ. Targeting the phosphoinositide 3-kinase pathway in cancer. Nat Rev Drug Discov. 2009;8:627–644
  12. Chang L, Karin M. Mammalian MAP kinase signalling cascades. Nature. 2001;410:37–40
  13. Harrington LE, Hatton RD, Mangan PR, Turner H, Murphy TL, Murphy KM, et al. Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat Immunol. 2005;6:1123–1132
  14. Park H, Li Z, Yang XO, Chang SH, Nurieva R, Wang YH, et al. A distinct lineage of CD4T cells regulates tissue inflammation by producing interleukin 17. Nat Immunol. 2005;6:1133–1141
  15. Miossec P, Korn T, Kuchroo VK. Interleukin-17 and type 17 helper T cells. N Engl J Med. 2009;361:888–898
  16. Fitch E, Harper E, Skorcheva I, Kurtz SE, Blauvelt A. Pathophysiology of psoriasis: recent advances on IL-23 and Th17 cytokines. Curr Rheumatol Rep. 2007;9:461–467
  17. Oppmann B, Lesley R, Blom B, Timans JC, Xu Y, Hunte B, et al. Novel p19 protein engages IL-12p40 to form a cytokine, IL-23, with biological activities similar as well as distinct from IL-12. Immunity. 2000;13:715–725
  18. Leonardi CL, Kimball AB, Papp KA, Yeilding N, Guzzo C, Wang Y, et al. Efficacy and safety of ustekinumab, a human interleukin-12/23 monoclonal antibody, in patients with psoriasis: 76-week results from a randomised, double-blind, placebo-controlled trial (PHOENIX 1). Lancet. 2008;371:1665–1674
  19. Johnson-Huang LM, Suarez-Farinas M, Sullivan-Whalen M, Gilleaudeau P, Krueger JG, Lowes MA. Effective narrow-band UVB radiation therapy suppresses the IL-23/IL-17 axis in normalized psoriasis plaques. J Invest Dermatol. 2010;130:2654–2663
  20. Genovese MC, Van den Bosch F, Roberson SA, Bojin S, Biagini IM, Ryan P, et al. LY2439821, a humanized anti-interleukin-17 monoclonal antibody, in the treatment of patients with rheumatoid arthritis: a phase I randomized, double-blind, placebo-controlled, proof-of-concept study. Arthritis Rheum. 2010;62:929–939
  21. Hueber W, Patel DD, Dryja T, Wright AM, Koroleva I, Bruin G, et al. Effects of AIN457, a fully human antibody to interleukin-17A, on psoriasis, rheumatoid arthritis, and uveitis. Sci Transl Med. 2010;2:52ra72
  22. Chan JR, Blumenschein W, Murphy E, Diveu C, Wiekowski M, Abbondanzo S, 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
  23. Zheng Y, Danilenko DM, Valdez P, Kasman I, Eastham-Anderson J, Wu J, et al. Interleukin-22, a T(H)17 cytokine, mediates IL-23-induced dermal inflammation and acanthosis. Nature. 2007;445:648–651
  24. Hedrick MN, Lonsdorf AS, Shirakawa AK, Lee CR, Liao F, Singh SP, et al. CCR6 is required for IL-23-induced psoriasis-like inflammation in mice. J Clin Invest. 2009;119:2317–2329
  25. Lim HW, Lee J, Hillsamer P, Kim CH. Human Th17 cells share major trafficking receptors with both polarized effector T cells and FOXP3+ regulatory T cells. J Immunol. 2008;180:122–129
  26. Liao F, Alderson R, Su J, Ullrich SJ, Kreider BL, Farber JM. STRL22 is a receptor for the CC chemokine MIP-3a. Biochem Biophys Res Commun. 1997;236:212–217
  27. Greaves DR, Wang W, Dairaghi DJ, Dieu MC, de Saint-Vis B, Franz-Bacon K, et al. CCR6, a CC chemokine receptor that interacts with macrophage inflammatory protein 3a and is highly expressed human dendritic cells. J Exp Med. 1997;186:837–844
  28. Power CA, Church DJ, Meyer A, Alouani S, Proudfoot AE, Clark-Lewis I, et al. Cloning and characterization of a specific receptor for the novel CC chemokine MIP-3α from lung dendritic cells. J Exp Med. 1997;186:825–835
  29. Homey B, Dieu-Nosjean M, Wiesenborn A, Massacrier C, Pin J, Oldham E, et al. Up-regulation of macrophage inflammatory protein-3a/CCL20 and CC chemokine receptor 6 in psoriasis. J Immunol. 2000;164:6621–6632
  30. Fitzhugh DJ, Naik S, Caughman SW, Hwang ST. Cutting edge: CC chemokine receptor-6 (CCR6) is essential for arrest of a subset of memory T cells on activated dermal microvascular endothelial cells under physiologic flow conditions in vitro. J Immunol. 2000;165:6677–6681
  31. Nograles KE, Davidovici B, Krueger JG. New insights in the immunologic basis of psoriasis. Semin Cutan Med Surg. 2010;29:3–9
  32. Hedrick MN, Lonsdorf AS, Hwang ST, Farber JM. CCR6 as a possible therapeutic target in psoriasis. Expert Opin Ther Targets. 2010;14:911–922
  33. Schutyser E, Struyf S, Van Damme J. The CC chemokine CCL20 and its receptor CCR6. Cytokine Growth Factor Rev. 2003;14:409–426
  34. Yang D, Chertox O, Bykovskaia SN, Chen Q, Buffo MJ, Shogan J, et al. β-Defensins: linking innate and adaptive immunity through dendritic and T cell CCR6. Science. 1999;286:525–528
  35. Grinlinton FM, Skinner MA, Birchall NM, Tan PL. γδ+ T cells from patients with psoriatic and rheumatoid arthritis respond to streptococcal antigen. J Rheumatol. 1993;20:982–987
  36. de Boer OJ, Verhagen CE, Visser A, Bos JD, Das PK. Cellular interactions and adhesion molecules in psoriatic skin. Acta Derm Venereol Suppl (Stockh). 1994;186:15–18
  37. Seung NR, Park EJ, Kim CW, Kim KH, Kim KJ, Cho HJ, et al. Comparison of expression of heat-shock protein 60, Toll-like receptors 2 and 4, and T-cell receptor γδ in plaque and guttate psoriasis. J Cutan Pathol. 2007;34:903–911
  38. Laggner U, Di Meglio P, Perera GK, Hundhausen C, Lacy KE, Ali N, et al. Identification of a novel proinflammatory human skin-homing Vγ9Vδ2T cell subset with a potential role in psoriasis. J Immunol. 2011;187:2783–2793
  39. Sutton CE, Lalor SJ, Sweeney CM, Brereton CF, Lavelle EC, Mills KH. Interleukin-1 and IL-23 induce innate IL-17 production from γδ T cells, amplifying Th17 responses and autoimmunity. Immunity. 2009;31:331–341
  40. Gray EE, Suzuki K, Cyster JG. Cutting edge: identification of a motile IL-17-producing γδ T cell population in the dermis. J Immunol. 2011;186:6091–6095
  41. Girardi M, Lewis J, Glusac E, Filler RB, Geng L, Hayday AC, et al. Resident skin-specific γδ T cells provide local, nonredundant regulation of cutaneous inflammation. J Exp Med. 2002;195:855–867
  42. Girardi M. Immunosurveillance and immunoregulation by γδ T cells. J Invest Dermatol. 2006;126:25–31
  43. Mabuchi T, Takekoshi T, Hwang ST. Epidermal CCR6+ γδ T cells are major producers of IL-22 and IL-17 in a murine model of psoriasiform dermatitis. J Immunol. 2011;187:5026–5031
  44. Nestle FO, Di Meglio P, Qin JZ, Nickoloff BJ. Skin immune sentinels in health and disease. Nat Rev Immunol. 2009;9:679–691
  45. Dieu-Nosjean MC, Massacrier C, Vanbervliet B, Fridman WH, Caux C. IL-10 induces CCR6 expression during Langerhans cell development while IL-4 and IFN-γ suppress it. J Immunol. 2001;167:5594–5602
  46. Dieu-Nosjean MC, Massacrier C, Homey B, Vanbervliet B, Pin JJ, Vicari A, et al. Macrophage inflammatory protein 3α is expressed at inflamed epithelial surfaces and is the most potent chemokine known in attracting Langerhans cell precursors. J Exp Med. 2000;192:705–718
  47. Komine M, Karakawa M, Takekoshi T, Sakurai N, Minatani Y, Mitsui H, et al. Early inflammatory changes in the “perilesional skin” of psoriatic plaques: is there interaction between dendritic cells and keratinocytes?. J Invest Dermatol. 2007;127:1915–1922
  48. Lowes MA, Chamian F, Abello MV, Fuentes-Duculan J, Lin SL, Nussbaum R, et al. Increase in TNF-α and inducible nitric oxide synthase-expressing dendritic cells in psoriasis and reduction with efalizumab (anti-CD11a). Proc Natl Acad Sci U S A. 2005;102:19057–19062
  49. Lee E, Trepicchio WL, Oestreicher JL, Pittman D, Wang F, Chamian F, 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
  50. Wang F, Lee E, Lowes MA, Haider AS, Fuentes-Duculan J, Abello MV, et al. Prominent production of IL-20 by CD68+/CD11c+ myeloid-derived cells in psoriasis: gene regulation and cellular effects. J Invest Dermatol. 2006;126:1590–1599
  51. Vestergaard C, Just H, Baumgartner Nielsen J, Thestrup-Pedersen K, Deleuran M. Expression of CCR2 on monocytes and macrophages in chronically inflamed skin in atopic dermatitis and psoriasis. Acta Derm Venereol. 2004;84:353–358
  52. de Groot M, Teunissen MB, Ortonne JP, Lambert JR, Naeyaert JM, Picavet DI, et al. Expression of the chemokine receptor CCR5 in psoriasis and results of a randomized placebo controlled trial with a CCR5 inhibitor. Arch Dermatol Res. 2007;299:305–313
  53. Goebeler M, Toksoy A, Spandau U, Engelhardt E, Brocker EB, Gillitzer R. The C-X-C chemokine Mig is highly expressed in the papillae of psoriatic lesions. J Pathol. 1998;184:89–95
  54. Rottman JB, Smith TL, Ganley KG, Kikuchi T, Krueger JG. Potential role of the chemokine receptors CXCR3, CCR4, and the integrin αEβ7 in the pathogenesis of psoriasis vulgaris. Lab Invest. 2001;81:335–347
  55. Wen H, Hogaboam CM, Lukacs NW, Cook DN, Lira SA, Kunkel SL. The chemokine receptor CCR6 is an important component of the innate immune response. Eur J Immunol. 2007;37:2487–2498
  56. Jansen PA, Rodijk-Olthuis D, Hollox EJ, Kamsteeg M, Tjabringa GS, de Jongh GJ, et al. β-Defensin-2 protein is a serum biomarker for disease activity in psoriasis and reaches biologically relevant concentrations in lesional skin. PLoS One. 2009;4:e4725
  57. Hollox EJ, Huffmeier U, Zeeuwen PL, Palla R, Lascorz J, Rodijk-Olthuis D, et al. Psoriasis is associated with increased β-defensin genomic copy number. Nat Genet. 2008;40:23–25
  58. Chen SC, de Groot M, Kinsley D, Laverty M, McClanahan T, Arreaza M, et al. Expression of chemokine receptor CXCR3 by lymphocytes and plasmacytoid dendritic cells in human psoriatic lesions. Arch Dermatol Res. 2010;302:113–123
  59. Homey B, Meller S. Chemokines and other mediators as therapeutic targets in psoriasis vulgaris. Clin Dermatol. 2008;26:539–545
  60. Wells TN, Power CA, Shaw JP, Proudfoot AE. Chemokine blockers – therapeutics in the making?. Trends Pharmacol Sci. 2006;27:41–47
  61. Schroder JM, Christophers E. Identification of C5adesarg and an anionic neutrophil-activating peptide (ANAP) in psoriatic scales. J Invest Dermatol. 1986;87:53–58
  62. Fukuoka M, Ogino Y, Sato H, Ohta T, Komoriya K, Nishioka K, et al. RANTES expression in psoriatic skin, and regulation of RANTES and IL-8 production in cultured epidermal keratinocytes by active vitamin D3 (tacalcitol). AAD Rev. 1998;138:63–70
  63. Raychaudhuri SP, Jiang WY, Farber EM, Schall TJ, Ruff MR, Pert CB. Upregulation of RANTES in psoriatic keratinocytes: a possible pathogenic mechanism for psoriasis. Acta Derm Venereol. 1999;79:9–11
  64. Hirota K, Yoshitomi H, Hashimoto M, Maeda S, Teradaira S, Sugimoto N, et al. Preferential recruitment of CCR6-expressing Th17 cells to inflamed joints via CCL20 in rheumatoid arthritis and its animal model. J Exp Med. 2007;204:2803–2812
  65. Carlsson J, Coleman RG, Setola V, Irwin JJ, Fan H, Schlessinger A, et al. Ligand discovery from a dopamine D(3) receptor homology model and crystal structure. Nat Chem Biol. 2011;7:769–778
  66. Veldkamp CT, Ziarek JJ, Peterson FC, Chen Y, Volkman BF. Targeting SDF-1/CXCL12 with a ligand that prevents activation of CXCR4 through structure-based drug design. J Am Chem Soc. 2010;132:7242–7243
  67. Yamaoka K, Tanaka Y. Jak inhibitor; possibility and mechanism as a new disease modifying anti-rheumatic drug. Nihon Rinsho Meneki Gakkai Kaishi. 2009;32:85–91
  68. Cohen S, Fleischmann R. Kinase inhibitors: a new approach to rheumatoid arthritis treatment. Curr Opin Rheumatol. 2010;22:330–335
  69. Kawamura M, McVicar DW, Johnston JA, Blake TB, Chen YQ, Lal BK, et al. Molecular cloning of L-JAK, a Janus family protein-tyrosine kinase expressed in natural killer cells and activated leukocytes. Proc Natl Acad Sci U S A. 1994;91:6374–6378
  70. Harada D, Takada C, Nosaka Y, Takashima Y, Kobayashi K, Takaba K, et al. Effect of orally administered KF66490, a phosphodiesterase 4 inhibitor, on dermatitis in mouse models. Int Immunopharmacol. 2009;9:55–62
  71. Spina D. PDE4 inhibitors: current status. Br J Pharmacol. 2008;155:308–315
  72. Nazarian R, Weinberg JM. AN-2728, a PDE4 inhibitor for the potential topical treatment of psoriasis and atopic dermatitis. Curr Opin Investig Drugs. 2009;10:1236–1242
  73. Baumer W, Hoppmann J, Rundfeldt C, Kietzmann M. Highly selective phosphodiesterase 4 inhibitors for the treatment of allergic skin diseases and psoriasis. Inflamm Allergy Drug Targets. 2007;6:17–26
  74. Bolli MH, Abele S, Binkert C, Bravo R, Buchmann S, Bur D, et al. 2-Imino-thiazolidin-4-one derivatives as potent, orally active S1P1 receptor agonists. J Med Chem. 2010;53:4198–4211
  75. Giustizieri ML, Mascia F, Frezzolini A, De Pita O, Chinni LM, Giannetti A, et al. Keratinocytes from patients with atopic dermatitis and psoriasis show a distinct chemokine production profile in response to T cell-derived cytokines. J Allergy Clin Immun. 2001;107:871–877
  76. Uchida T, Suto H, Ra C, Ogawa H, Kobata K, Okumura K. Preferential expression of T(h)2-type chemokine and its receptor in atopic dermatitis. Int Immunol. 2002;14:1431–1438
  77. Teraki Y, Miyake A, Takebayashi R, Shiohara T. Homing receptor and chemokine receptor on intraepidermal T cells in psoriasis vulgaris. Clin Exp Dermatol. 2004;29:658–663
  78. Morita E, Kameyoshi Y, Hiragun T, Mihara S, Yamamoto S. The C-C chemokines, RANTES and eotaxin, in atopic dermatitis. Allergy. 2001;56:194–195
  79. Kakinuma T, Saeki H, Tsunemi Y, Fujita H, Asano N, Mitsui H, et al. Increased serum cutaneous T cell-attracting chemokine (CCL27) levels in patients with atopic dermatitis and psoriasis vulgaris. J Allergy Clin Immunol. 2003;111:592–597
  80. Campanati A, Goteri G, Simonetti O, Ganzetti G, Giuliodori K, Stramazzotti D, et al. CTACK/CCL27 expression in psoriatic skin and its modification after administration of etanercept. Br J Dermatol. 2007;157:1155–1160
  81. Schulz BS, Michel G, Wagner S, Suss R, Beetz A, Peter RU, et al. Increased expression of epidermal IL-8 receptor in psoriasis. Down-regulation by FK-506 in vitro. J Immunol. 1993;151:4399–4406
  82. Kulke R, Bornscheuer E, Schluter C, Bartels J, Rowert J, Sticherling M, et al. The CXC receptor 2 is overexpressed in psoriatic epidermis. J Invest Dermatol. 1998;110:90–94
  83. Gillitzer R, Ritter U, Spandau U, Goebeler M, Brocker EB. Differential expression of GRO-α and IL-8 mRNA in psoriasis: a model for neutrophil migration and accumulation in vivo. J Invest Dermatol. 1996;107:778–782
  84. Yamashita T, Akamatsu H, Tomitaka A, Ogawa Y, Sugawara N, Matsunaga K. IP-10 in atopic dermatitis. Allergy. 2003;58:261
  85. Oh ST, Schramme A, Tilgen W, Gutwein P, Reichrath J. Overexpression of CXCL16 in lesional psoriatic skin. Dermatoendocrinology. 2009;1:114–118
  86. Fraticelli P, Sironi M, Bianchi G, D’Ambrosio D, Albanesi C, Stoppacciaro A, et al. Fractalkine (CX3CL1) as an amplification circuit of polarized Th1 responses. J Clin Invest. 2001;107:1173–1181

PII: S0923-1811(11)00323-9

doi: 10.1016/j.jdermsci.2011.11.007

Journal of Dermatological Science
Volume 65, Issue 1 , Pages 4-11 , January 2012