Targeting leukocyte recruitment in the treatment of psoriasis

Clinics in Dermatology

Volumn 26, Issue 5, 2008, Pages 527-538

  Li, Yi Yang Yvonne ^a   Zollner, Thomas M ^a   Schön, Michael P ^b,c,d  

^a BAYER AG   (Germany)

^b Deutsche Forschungsgemeinschaft   (Germany)

^c UNIVERSITY OF WÜRZBURG   (Germany)

^d UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ABT 874; ABX IL8; ADALIMUMAB; ALEFACEPT; BIMOSIAMOSE; BMS 587101; CUTANEOUS LYMPHOCYTE ASSOCIATED ANTIGEN; EFALIZUMAB; ETANERCEPT; FINGOLIMOD; FUCOSYLTRANSFERASE; GAMMA INTERFERON; INFLIXIMAB; INTERCELLULAR ADHESION MOLECULE 1; NATALIZUMAB; SULFOTRANSFERASE INHIBITOR; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

CD4 CD8 RATIO; CELL MIGRATION; CLINICAL TRIAL; DENDRITIC CELL; DRUG BINDING; DRUG EFFICACY; DRUG INHIBITION; DRUG MECHANISM; DRUG SAFETY; HUMAN; LEUKOCYTE; MAST CELL; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; PSORIASIS; REVIEW; T LYMPHOCYTE ACTIVATION;

CELL ADHESION; CELL ADHESION MOLECULES; CELL MOVEMENT; HUMANS; LEUKOCYTES; PSORIASIS; SKIN; T-LYMPHOCYTES;

EID: 49849087670     PISSN: 0738081X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.clindermatol.2007.11.002     Document Type: Review

References (125)

1. Lebwohl M., Tyring S.K., Hamilton T.K., et al. A novel targeted T-cell modulator, efalizumab, for plaque psoriasis. N Engl J Med 349 (2003) 2004-2013
2. Smith C.H., and Barker J.N. Cell trafficking and role of adhesion molecules in psoriasis. Clin Dermatol 13 (1995) 151-160
3. Barker J.N. Adhesion molecules in cutaneous inflammation. Ciba Found Symp 189 (1995) 91-101
4. Mora J.R., and von U.H. T-cell homing specificity and plasticity: new concepts and future challenges. Trends Immunol 27 (2006) 235-243
5. Ghoreschi K., and Röcken M. Immune deviation strategies in the therapy of psoriasis. Curr Drug Targets Inflamm Allergy 3 (2004) 193-198
6. Zollner T.M., Asadullah K., and Schön M.P. Targeting leukocyte trafficking to inflamed skin-still an attractive therapeutic approach?. Exp Dermatol 16 (2007) 1-12
7. Schön M.P., and Ludwig R.J. Lymphocyte trafficking to inflamed skin-molecular mechanisms and implications for therapeutic target molecules. Expert Opin Ther Targets 9 (2005) 225-243
8. Mueller W., and Herrmann B. Cyclosporin A for psoriasis. N Engl J Med 301 (1979) 555
9. Bowcock A.M., and Krueger J.G. Getting under the skin: the immunogenetics of psoriasis. Nat Rev Immunol 5 (2005) 699-711
10. Kerstan A., and Schön M.P. Commentary 2. Exp Dermatol 15 (2006) 929
11. Schröder J.M., Reich K., Kabashima K., et al. Who is really in control of skin immunity under physiological circumstances-lymphocytes dendritic cells or keratinocytes?. Exp Dermatol 15 (2006) 913-929
12. Nickoloff B.J., Schröder J.M., von den D.P., et al. Is psoriasis a T-cell disease?. Exp Dermatol 9 (2000) 359-375
13. Schön M.P., and Boehncke W.H. Psoriasis. N Engl J Med 352 (2005) 1899-1912
14. Asadullah K., Volk H.D., and Sterry W. Novel immunotherapies for psoriasis. Trends Immunol 23 (2002) 47-53
15. + T cells. Nat Med 3 (1997) 183-188
16. Breban M., Hammer R.E., Richardson J.A., and Taurog J.D. Transfer of the inflammatory disease of HLA-B27 transgenic rats by bone marrow engraftment. J Exp Med 178 (1993) 1607-1616
17. + T cell-associated pathophysiology critically depends on CD18 gene dose effects in a murine model of psoriasis. J Immunol 171 (2003) 5697-5706
18. Christophers E. Psoriasis-epidemiology and clinical spectrum. Clin Exp Dermatol 26 (2001) 314-320
19. Tomfohrde J., Silverman A., Barnes R., et al. Gene for familial psoriasis susceptibility mapped to the distal end of human chromosome 17q. Science 264 (1994) 1141-1145
20. Gardembas-Pain M., Ifrah N., Foussard C., et al. Psoriasis after allogeneic bone marrow transplantation. Arch Dermatol 126 (1990) 1523
21. Eedy D.J., Burrows D., Bridges J.M., and Jones F.G. Clearance of severe psoriasis after allogenic bone marrow transplantation. BMJ 300 (1990) 908
22. Ellis C.N., and Krueger G.G. Treatment of chronic plaque psoriasis by selective targeting of memory effector T lymphocytes. N Engl J Med 345 (2001) 248-255
23. Zollner T.M., and Asadullah K. Selectin and selectin ligand binding: a bittersweet attraction. J Clin Invest 112 (2003) 980-983
24. Schön M.P., Zollner T.M., and Boehncke W.H. The molecular basis of lymphocyte recruitment to the skin: clues for pathogenesis and selective therapies of inflammatory disorders. J Invest Dermatol 121 (2003) 951-962
25. Homey B. Chemokines and chemokine receptors as targets in the therapy of psoriasis. Curr Drug Targets Inflamm Allergy 3 (2004) 169-174
26. Lebwohl M., Tyring S.K., Hamilton T.K., et al. A novel targeted T-cell modulator, efalizumab, for plaque psoriasis. N Engl J Med 349 (2003) 2004-2013
27. Ludwig R.J., Zollner T.M., Santoso S., et al. Junctional adhesion molecules (JAM)-B and -C contribute to leukocyte extravasation to the skin and mediate cutaneous inflammation. J Invest Dermatol 125 (2005) 969-976
28. Uchimura K., and Rosen S.D. Sulfated L-selectin ligands as a therapeutic target in chronic inflammation. Trends Immunol 27 (2006) 559-565
29. Issekutz A.C., and Issekutz T.B. The role of E-selectin, P-selectin, and very late activation antigen-4 in T lymphocyte migration to dermal inflammation. J Immunol 168 (2002) 1934-1939
30. Bhushan M., Bleiker T.O., Ballsdon A.E., et al. Anti-E-selectin is ineffective in the treatment of psoriasis: a randomized trial. Br J Dermatol 146 (2002) 824-831
31. Hardtke M., Friedrich M., Philipp S., et al. Anti-L-selectin therapy is not effective in psoriasis: a randomized trial. (abstr). Arch Dermatol Res 296 (2005) 427
32. Friedrich M., Bock D., Philipp S., et al. Pan-selectin antagonism improves psoriasis manifestation in mice and man. Arch Dermatol Res 297 (2006) 345-351
33. Schön M.P., Krahn T., Schön M., et al. Efomycine M, a new specific inhibitor of selectin, impairs leukocyte adhesion and alleviates cutaneous inflammation. Nat Med 8 (2002) 366-372
34. von Bonin A., Buchmann B., Bader B., et al. Efomycine M: an inhibitor of selectins?. Nat Med 12 (2006) 873-874
35. Wienrich B.G., Krahn T., Schön M., et al. Structure-function relation of efomycines, a family of small-molecule inhibitors of selectin functions. J Invest Dermatol 126 (2006) 882-889
36. Schön M.P., Drewniok C., and Boehncke W.H. Targeting selectin functions in the therapy of psoriasis. Curr Drug Targets Inflamm Allergy 3 (2004) 163-168
37. Rosen S.D. Ligands for L-selectin: homing, inflammation, and beyond. Annu Rev Immunol 22 (2004) 129-156
38. Picker L.J. Regulation of tissue-selective T-lymphocyte homing receptors during the virgin to memory/effector cell transition in human secondary lymphoid tissues. Am Rev Respir Dis 148 (1993) S47-S54
39. Schön M.P., and Ludwig R.J. Lymphocyte trafficking to inflamed skin-molecular mechanisms and implications for therapeutic target molecules. Expert Opin Ther Targets 9 (2005) 225-243
40. Homeister J.W., Thall A.D., Petryniak B., et al. The alpha(1,3)fucosyltransferases FucT-IV and FucT-VII exert collaborative control over selectin-dependent leukocyte recruitment and lymphocyte homing. Immunity 15 (2001) 115-126
41. Schottelius A.J., Hamann A., and Asadullah K. Role of fucosyltransferases in leukocyte trafficking: major impact for cutaneous immunity. Trends Immunol 24 (2003) 101-104
42. Weninger W., Ulfman L.H., Cheng G., et al. Specialized contributions by alpha(1,3)-fucosyltransferase-IV and FucT-VII during leukocyte rolling in dermal microvessels. Immunity 12 (2000) 665-676
43. Smithson G., Rogers C.E., Smith P.L., et al. Fuc-TVII is required for T helper 1 and T cytotoxic 1 lymphocyte selectin ligand expression and recruitment in inflammation, and together with Fuc-TIV regulates naive T cell trafficking to lymph nodes. J Exp Med 194 (2001) 601-614
44. Hemmerich S., and Rosen S.D. Carbohydrate sulfotransferases in lymphocyte homing. Glycobiology 10 (2000) 849-856
45. Uchimura K., Gauguet J.M., Singer M.S., et al. A major class of L-selectin ligands is eliminated in mice deficient in two sulfotransferases expressed in high endothelial venules. Nat Immunol 6 (2005) 1105-1113
46. Weninger W., Ulfman L.H., Cheng G., et al. Specialized contributions by alpha(1,3)-fucosyltransferase-IV and FucT-VII during leukocyte rolling in dermal microvessels. Immunity 12 (2000) 665-676
47. Rosen S.D., Tsay D., Singer M.S., Hemmerich S., and Abraham W.M. Therapeutic targeting of endothelial ligands for L-selectin (PNAd) in a sheep model of asthma. Am J Pathol 166 (2005) 935-944
48. Yang J., Rosen S.D., Bendele P., and Hemmerich S. Induction of PNAd and N-acetylglucosamine 6-O-sulfotransferases 1 and 2 in mouse collagen-induced arthritis. BMC Immunol 7 (2006) 12
49. Pablos J.L., Santiago B., Tsay D., et al. A HEV-restricted sulfotransferase is expressed in rheumatoid arthritis synovium and is induced by lymphotoxin-alpha/beta and TNF-alpha in cultured endothelial cells. BMC Immunol 6 (2005) 6
50. Leonardi C.L. Current concepts and review of efalizumab in the treatment of psoriasis. Dermatol Clin 22 (2004) 427-435
51. Leonardi C.L. Efalizumab in the treatment of psoriasis. Dermatol Ther 17 (2004) 393-400
52. + T cells into lesional skin. Clin Immunol 113 (2004) 38-46
53. Li Y.Y., Perez H.D., and Zollner T.M. Fatalities in natalizumab treatment-a "no go" for leukocyte recirculation approaches?. Expert Opin Ther Targets 10 (2006) 489-499
54. +) regulatory T cells. Trends Immunol 27 (2006) 541-544
55. +CD25 high regulatory T cells in psoriasis: mechanism underlying unrestrained pathogenic effector T cell proliferation. J Immunol 174 (2005) 164-173
56. + regulatory T cells in Psoriasis. Dermatology 213 (2006) 111-117
57. Verhagen J., Akdis M., Traidl-Hoffmann C., et al. Absence of T-regulatory cell expression and function in atopic dermatitis skin. J Allergy Clin Immunol 117 (2006) 176-183
58. Siegmund K., Feuerer M., Siewert C., et al. Migration matters: regulatory T-cell compartmentalization determines suppressive activity in vivo. Blood 106 (2005) 3097-3104
59. + regulatory T cells bear functional skin-homing receptors. J Immunol 177 (2006) 4488-4494
60. Wei S., Kryczek I., and Zou W. Regulatory T-cell compartmentalization and trafficking. Blood 108 (2006) 426-431
61. + T cells. J Immunol 172 (2004) 890-898
62. +CD25high regulatory T cells in psoriasis: mechanism underlying unrestrained pathogenic effector T cell proliferation. J Immunol 174 (2005) 164-173
63. + T cell responses. J Exp Med 196 (2002) 1585-1592
64. Adorini L. Immunomodulatory effects of vitamin D receptor ligands in autoimmune diseases. Int Immunopharmacol 2 (2002) 1017-1028
65. Belghith M., Bluestone J.A., Barriot S., Megret J., Bach J.F., and Chatenoud L. TGF-beta-dependent mechanisms mediate restoration of self-tolerance induced by antibodies to CD3 in overt autoimmune diabetes. Nat Med 9 (2003) 1202-1208
66. Kagen M.H., McCormick T.S., and Cooper K.D. Regulatory T cells in psoriasis. Ernst Schering Res Found Workshop (2006) 193-209
67. Boehncke W.H., Wortmann S., Kaufmann R., Mielke V., and Sterry W. A subset of macrophages located along the basement membrane ("lining cells") is a characteristic histopathological feature of psoriasis. Am J Dermatopathol 17 (1995) 139-144
68. Schön M.P. Cutaneous lymphocyte localization in the pathogenesis of psoriasis. Ernst Schering Res Found Workshop (2004) 27-51
69. Thepen T., van Vuuren A.J., Kiekens R.C., Damen C.A., Vooijs W.C., and Van De Winkel J.G. Resolution of cutaneous inflammation after local elimination of macrophages. Nat Biotechnol 18 (2000) 48-51
70. Wang H., Peters T., Kess D., Sindrilaru A., Oreshkova T., Van Rooijen N., et al. Activated macrophages are essential in a murine model for T cell-mediated chronic psoriasiform skin inflammation. J Clin Invest 116 (2006) 2105-2114
71. Stratis A., Pasparakis M., Rupec R.A., Markur D., Hartmann K., Scharffetter-Kochanek K., et al. Pathogenic role for skin macrophages in a mouse model of keratinocyte-induced psoriasis-like skin inflammation. J Clin Invest 116 (2006) 2094-2104
72. Gillitzer R., Wolff K., Tong D., et al. MCP-1 mRNA expression in basal keratinocytes of psoriatic lesions. J Invest Dermatol 101 (1993) 127-131
73. Vestergaard C., Just H., Baumgartner N.J., Thestrup-Pedersen K., and Deleuran M. Expression of CCR2 on monocytes and macrophages in chronically inflamed skin in atopic dermatitis and psoriasis. Acta Derm Venereol 84 (2004) 353-358
74. van de Kerkhof P.C., and Lammers A.M. Intraepidermal accumulation of polymorphonuclear leukocytes in chronic stable plaque psoriasis. Dermatologica 174 (1987) 224-227
75. van de Kerkhof P.C., and Chang A. Migration of polymorphonuclear leukocytes in psoriasis. Skin Pharmacol 2 (1989) 138-154
76. Kragballe K., Desjarlais L., and Voorhees J.J. Leukotrienes B4, C4 and D4 stimulate DNA synthesis in cultured human epidermal keratinocytes. Br J Dermatol 113 (1985) 43-52
77. Thelen M., Peveri P., Kernen P., von T.V., Walz A., and Baggiolini M. Mechanism of neutrophil activation by NAF, a novel monocyte-derived peptide agonist. FASEB J 2 (1988) 2702-2706
78. O'Flaherty J.T., Rossi A.G., Redman J.F., and Jacobson D.P. Tumor necrosis factor-alpha regulates expression of receptors for formyl-methionyl-leucyl-phenylalanine, leukotriene B4, and platelet-activating factor. Dissociation from priming in human polymorphonuclear neutrophils. J Immunol 147 (1991) 3842-3847
79. Ludolph-Hauser D., Schubert C., and Wiedow O. Structural changes of human epidermis induced by human leukocyte-derived proteases. Exp Dermatol 8 (1999) 46-52
80. Glinski W., Barszcz D., Janczura E., Zarebska Z., and Jablonska S. Neutral proteinases and other neutrophil enzymes in psoriasis, and their relation to disease activity. Br J Dermatol 111 (1984) 147-154
81. Glinski W., and Jablonska S. Neutrophils in psoriasis. J Invest Dermatol 82 (1984) 386-387
82. Kuijpers A.L., Zeeuwen P.L., de Jongh G.J., van de Kerkhof P.C., Alkemade H.A., and Schalkwijk J. Skin-derived antileukoproteinase (SKALP) is decreased in pustular forms of psoriasis. A clue to the pathogenesis of pustule formation?. Arch Dermatol Res 288 (1996) 641-647
83. Barszcz D., Zarebska Z., Glinska-Ferenz M., Jablonska S., Tigalonowa M., and Glinski W. Alpha 1-proteinase inhibitor in psoriasis: reduced activity in symptom-free patients and during flare. Arch Dermatol Res 280 (1988) 198-206
84. Schön M., Denzer D., Kubitza R.C., Ruzicka T., and Schön M.P. Critical role of neutrophils for the generation of psoriasiform skin lesions in flaky skin mice. J Invest Dermatol 114 (2000) 976-983
85. Romani N., Holzmann S., Tripp C.H., Koch F., and Stoitzner P. Langerhans cells-dendritic cells of the epidermis. APMIS 111 (2003) 725-740
86. Wollenberg A., Wagner M., Gunther S., et al. Plasmacytoid dendritic cells: a new cutaneous dendritic cell subset with distinct role in inflammatory skin diseases. J Invest Dermatol 119 (2002) 1096-1102
87. Nestle F.O., Conrad C., Tun-Kyi A., et al. Plasmacytoid predendritic cells initiate psoriasis through interferon-alpha production. J Exp Med 202 (2005) 135-143
88. Jiang W.Y., Chattedee A.D., Raychaudhuri S.P., Raychaudhuri S.K., and Farber E.M. Mast cell density and IL-8 expression in nonlesional and lesional psoriatic skin. Int J Dermatol 40 (2001) 699-703
89. Toruniowa B., and Jablonska S. Mast cells in the initial stages of psoriasis. Arch Dermatol Res 280 (1988) 189-193
90. Galli S.J., Nakae S., and Tsai M. Mast cells in the development of adaptive immune responses. Nat Immunol 6 (2005) 135-142
91. Tam S.Y., Tsai M., Snouwaert J.N., et al. RabGEF1 is a negative regulator of mast cell activation and skin inflammation. Nat Immunol 5 (2004) 844-852
92. Nielsen H.J., Kristensen J.K., Hansen U., Nielsen H.I., Skov P.S., and Petersen L.M. Clinical effect of ranitidine in psoriasis. An open prospective study. Ugeskr Laeger 159 (1997) 598-600
93. Nielsen H.J. Histamine-2 receptor antagonists as immunomodulators: new therapeutic views?. Ann Med 28 (1996) 107-113
94. Nielsen H.J., and Hammer J.H. Possible role of histamine in pathogenesis of autoimmune diseases: implications for immunotherapy with histamine-2 receptor antagonists. Med Hypotheses 39 (1992) 349-355
95. Mrowietz U. Concepts of the mechanisms of action of cyclosporin in psoriasis. A review with guidelines on therapy. Hautarzt 44 (1993) 353-360
96. Boyman O., Hefti H.P., Conrad C., Nickoloff B.J., Suter M., and Nestle F.O. Spontaneous development of psoriasis in a new animal model shows an essential role for resident T cells and tumor necrosis factor-alpha. J Exp Med 199 (2004) 731-736
97. Kunkel E.J., and Butcher E.C. Chemokines and the tissue-specific migration of lymphocytes. Immunity 16 (2002) 1-4
98. Springer T.A. Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm. Cell 76 (1994) 301-314
99. Butcher E.C., and Picker L.J. Lymphocyte homing and homeostasis. Science 272 (1996) 60-66
100. Bhushan M., Bleiker T.O., Ballsdon A.E., et al. Anti-E-selectin is ineffective in the treatment of psoriasis: a randomized trial. Br J Dermatol 146 (2002) 824-831
101. Hardtke S., Ohl L., and Förster R. Balanced expression of CXCR5 and CCR7 on follicular T helper cells determines their transient positioning to lymph node follicles and is essential for efficient B-cell help. Blood 106 (2005) 1924-1931
102. Homey B., Alenius H., Müller A., et al. CCL27-CCR10 interactions regulate T cell-mediated skin inflammation. Nat Med 8 (2002) 157-165
103. Schön M.P., and Ruzicka T. Psoriasis: the plot thickens. Nat Immunol 2 (2001) 91
104. Luscinskas F.W., Ma S., Nusrat A., Parkos C.A., and Shaw S.K. Leukocyte transendothelial migration: a junctional affair. Semin Immunol 14 (2002) 105-113
105. Dejana E. The transcellular railway: insights into leukocyte diapedesis. Nat Cell Biol 8 (2006) 105-107
106. Millan J., Hewlett L., Glyn M., Toomre D., Clark P., and Ridley A.J. Lymphocyte transcellular migration occurs through recruitment of endothelial ICAM-1 to caveola- and F-actin-rich domains. Nat Cell Biol 8 (2006) 113-123
107. Nieminen M., Henttinen T., Merinen M., Marttila-Ichihara F., Eriksson J.E., and Jalkanen S. Vimentin function in lymphocyte adhesion and transcellular migration. Nat Cell Biol 8 (2006) 156-162
108. Muller W.A., Weigl S.A., Deng X., and Phillips D.M. PECAM-1 is required for transendothelial migration of leukocytes. J Exp Med 178 (1993) 449-460
109. Vaporciyan A.A., DeLisser H.M., Yan H.C., et al. Involvement of platelet-endothelial cell adhesion molecule-1 in neutrophil recruitment in vivo. Science 262 (1993) 1580-1582
110. Gotsch U., Borges E., Bosse R., et al. VE-cadherin antibody accelerates neutrophil recruitment in vivo. J Cell Sci 110 (1997) 583-588
111. Corada M., Liao F., Lindgren M., et al. Monoclonal antibodies directed to different regions of vascular endothelial cadherin extracellular domain affect adhesion and clustering of the protein and modulate endothelial permeability. Blood 97 (2001) 1679-1684
112. Del Maschio A., De Luigi A., Martin-Padura I., et al. Leukocyte recruitment in the cerebrospinal fluid of mice with experimental meningitis is inhibited by an antibody to junctional adhesion molecule (JAM). J Exp Med 190 (1999) 1351-1356
113. Lechner F., Sahrbacher U., Suter T., et al. Antibodies to the junctional adhesion molecule cause disruption of endothelial cells and do not prevent leukocyte influx into the meninges after viral or bacterial infection. J Infect Dis 18 (2000) 978-982
114. Irjala H., Johansson E.L., Grenman R., Alanen K., Salmi M., and Jalkanen S. Mannose receptor is a novel ligand for L-selectin and mediates lymphocyte binding to lymphatic endothelium. J Exp Med 194 (2001) 1033-1042
115. Salmi M., Koskinen K., Henttinen T., Elima K., and Jalkanen S. CLEVER-1 mediates lymphocyte transmigration through vascular and lymphatic endothelium. Blood 104 (2004) 3849-3857
116. Matloubian M., Lo C.G., Cinamon G., et al. Lymphocyte egress from thymus and peripheral lymphoid organs is dependent on S1P receptor 1. Nature 427 (2004) 355-360
117. Pinschewer D.D., Ochsenbein A.F., Odermatt B., Brinkmann V., Hengartner H., and Zinkernagel R.M. FTY720 immunosuppression impairs effector T cell peripheral homing without affecting induction, expansion, and memory. J Immunol 164 (2000) 5761-5770
118. + T cells. J Immunol 170 (2003) 3662-3670
119. Kovarik J.M., Schmouder R.L., Barilla D., et al. FTY720 and cyclosporine: evaluation for a pharmacokinetic interaction. Ann Pharmacother 38 (2004) 1153-1158
120. Albanesi C., Scarponi C., Giustizieri M.L., and Girolomoni G. Keratinocytes in inflammatory skin diseases. Curr Drug Targets Inflamm Allergy 4 (2005) 329-334
121. Boniface K., Lecron J.C., Bernard F.X., et al. Keratinocytes as targets for interleukin-10-related cytokines: a putative role in the pathogenesis of psoriasis. Eur Cytokine Netw 16 (2005) 309-319
122. Boniface K., Bernard F.X., Garcia M., Gurney A.L., Lecron J.C., and Morel F. IL-22 inhibits epidermal differentiation and induces proinflammatory gene expression and migration of human keratinocytes. J Immunol 174 (2005) 3695-3702
123. Zenz R., and Wagner E.F. Jun signalling in the epidermis: From developmental defects to psoriasis and skin tumors. Int J Biochem Cell Biol 38 (2006) 1043-1049
124. Zenz R., Eferl R., Kenner L., et al. Psoriasis-like skin disease and arthritis caused by inducible epidermal deletion of Jun proteins. Nature 437 (2005) 369-375
125. + regulatory T cells. J Immunol 177 (2006) 840-851