Immune functions of the skin

Clinics in Dermatology

Volumn 29, Issue 4, 2011, Pages 360-376

  Bangert, Christine ^a   Brunner, Patrick M ^a   Stingl, Georg ^a  

^a Universitatsklinik fur Dermatologie   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

BETA DEFENSIN; BETA DEFENSIN 1; BETA DEFENSIN 2; BETA DEFENSIN 3; CASPASE RECRUITMENT DOMAIN PROTEIN 15; CASPASE RECRUITMENT DOMAIN PROTEIN 4; CATHELICIDIN ANTIMICROBIAL PEPTIDE LL 37; GAMMA INTERFERON; INFLAMMASOME; INTERLEUKIN 12; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; PATTERN RECOGNITION RECEPTOR; POLYPEPTIDE ANTIBIOTIC AGENT; RIBONUCLEASE; RIBONUCLEASE 7; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 2; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; ANTIGEN PRESENTING CELL; ARTICLE; B LYMPHOCYTE; CELL FUNCTION; CELL HETEROGENEITY; CELLULAR IMMUNITY; EOSINOPHIL; HUMAN; IMMUNE RESPONSE; IMMUNOSTIMULATION; INFECTION PREVENTION; INFLAMMATORY CELL; INNATE IMMUNITY; KERATINOCYTE; LANGERHANS CELL; LYMPHOCYTE FUNCTION; MAST CELL; NATURAL KILLER CELL; NONHUMAN; PHAGOCYTE; PLASMACYTOID DENDRITIC CELL; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATORY T LYMPHOCYTE; SKIN FUNCTION; SKIN PERMEABILITY; SKIN STRUCTURE; T LYMPHOCYTE; T LYMPHOCYTE SUBPOPULATION;

ADAPTIVE IMMUNITY; ANIMALS; B-LYMPHOCYTES; DENDRITIC CELLS; EOSINOPHILS; HUMANS; IMMUNITY, INNATE; KERATINOCYTES; KILLER CELLS, NATURAL; MAST CELLS; MICE; PHAGOCYTES; SKIN; T-LYMPHOCYTES;

EID: 79958804395     PISSN: 0738081X     EISSN: 18791131     Source Type: Journal    
DOI: 10.1016/j.clindermatol.2011.01.006     Document Type: Article

References (208)

1. Elias P.M. Stratum corneum defensive functions: an integrated view. J Invest Dermatol 2005, 125:183-200.
2. Gasque P. Complement: a unique innate immune sensor for danger signals. Mol Immunol 2004, 41:1089-1098.
3. Braff M.H., Bardan A., Nizet V., Gallo R.L. Cutaneous defense mechanisms by antimicrobial peptides. J Invest Dermatol 2005, 125:9-13.
4. Schroder J.M., Harder J. Antimicrobial skin peptides and proteins. Cell Mol Life Sci 2006, 63:469-486.
5. Schauber J., Gallo R.L. Antimicrobial peptides and the skin immune defense system. J Allergy Clin Immunol 2008, 122:261-266.
6. Harder J., Bartels J., Christophers E., Schröder J.M. A peptide antibiotic from human skin. Nature 1997, 387:861.
7. 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.
8. Yang R.B., Mark M.R., Gurney A.L., Godowski P.J. Signaling events induced by lipopolysaccharide-activated toll-like receptor 2. J Immunol 1999, 163:639-643.
9. Nizet V., Ohtake T., Lauth X., et al. Innate antimicrobial peptide protects the skin from invasive bacterial infection. Nature 2001, 414:454-457.
10. Ong P.Y., Ohtake T., Brandt C., et al. Endogenous antimicrobial peptides and skin infections in atopic dermatitis. N Engl J Med 2002, 347:1151-1160.
11. López-García B., Lee P.H., Yamasaki K., Gallo R.L. Anti-fungal activity of cathelicidins and their potential role in Candida albicans skin infection. J Invest Dermatol 2005, 125:108-115.
12. Howell M.D., Wollenberg A., Gallo R.L., et al. Cathelicidin deficiency predisposes to eczema herpeticum. J Allergy Clin Immunol 2006, 117:836-841.
13. Howell M.D., Gallo R.L., Boguniewicz M., et al. Cytokine milieu of atopic dermatitis skin subverts the innate immune response to vaccinia virus. Immunity 2006, 24:341-348.
14. De Y., Chen Q., Schmidt A.P., 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.
15. Liu P.T., Stenger S., Li H., et al. Toll-like receptor triggering of a vitamin D-mediated human antimicrobial response. Science 2006, 311:1770-1773.
16. Schauber J., Dorschner R.A., Coda A.B., et al. Injury enhances TLR2 function and antimicrobial peptide expression through a vitamin D-dependent mechanism. J Clin Invest 2007, 117:803-811.
17. Lande R., Gregorio J., Facchinetti V., et al. Plasmacytoid dendritic cells sense self-DNA coupled with antimicrobial peptide. Nature 2007, 449:564-569.
18. 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.
19. 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.
20. Michalek M., Gelhaus C., Hecht O., et al. The human antimicrobial protein psoriasin acts by permeabilization of bacterial membranes. Dev Comp Immunol 2009, 33:740-746.
21. Gläser R., Harder J., Lange H., Bartels J., Christophers E., Schröder J.M. Antimicrobial psoriasin (S100A7) protects human skin from Escherichia coli infection. Nat Immunol 2005, 6:57-64.
22. Abtin A., Eckhart L., Mildner M., Gruber F., Schröder J.M., Tschachler E. Flagellin is the principal inducer of the antimicrobial peptide S100A7c (psoriasin) in human epidermal keratinocytes exposed to Escherichia coli. FASEB J 2008, 22:2168-2176.
23. Jinquan T., Vorum H., Larsen C.G., et al. Psoriasin: a novel chemotactic protein. J Invest Dermatol 1996, 107:5-10.
24. Schittek B., Hipfel R., Sauer B., et al. Dermcidin: a novel human antibiotic peptide secreted by sweat glands. Nat Immunol 2001, 2:1133-1137.
25. Senyürek I., Paulmann M., Sinnberg T., et al. Dermcidin-derived peptides show a different mode of action than the cathelicidin LL-37 against Staphylococcus aureus. Antimicrob Agents Chemother 2009, 53:2499-2509.
26. Harder J., Schroder J.M. RNase 7, a novel innate immune defense antimicrobial protein of healthy human skin. J Biol Chem 2002, 277:46779-46784.
27. Zanger P., Holzer J., Schleucher R., et al. Constitutive expression of the antimicrobial peptide RNase 7 is associated with Staphylococcus aureus infection of the skin. J Infect Dis 2009, 200:1907-1915.
28. Bickers D.R., Athar M. Oxidative stress in the pathogenesis of skin disease. J Invest Dermatol 2006, 126:2565-2575.
29. Medzhitov R., Preston-Hurlburt P., Janeway C.A. A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature 1997, 388:394-397.
30. Lemaitre B., Nicolas E., Michaut L., Reichhart J.M., Hoffmann J.A. The dorsoventral regulatory gene cassette spatzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell 1996, 86:973-983.
31. Poltorak A., He X., Smirnova I., et al. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 1998, 282:2085-2088.
32. Alexopoulou L., Holt A.C., Medzhitov R., Flavell R.A. Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 2001, 413:732-738.
33. Diebold S.S., Kaisho T., Hemmi H., Akira S., Reis e Sousa C. Innate antiviral responses by means of TLR7-mediated recognition of single-stranded RNA. Science 2004, 303:1529-1531.
34. Hemmi H., Takeuchi O., Kawai T., et al. A Toll-like receptor that recognizes bacterial DNA. Nature 2000, 408:740-745.
35. Hayashi F., Smith K.D., Ozinsky A., et al. The innate immune response to bacterial flagellin is mediated by Toll- like receptor 5. Nature 2001, 410:1099-1103.
36. Brightbill H.D., Libraty D.H., Krutzik S.R., et al. Host defense mechanisms triggered by microbial lipoproteins through toll-like receptors. Science 1999, 285:732-736.
37. Aliprantis A.O., Yang R.B., Mark M.R., et al. Cell activation and apoptosis by bacterial lipoproteins through Toll-like receptor-2. Science 1999, 285:736-739.
38. Medzhitov R., Janeway C.A. Innate immunity: impact on the adaptive immune response. Curr Opin Immunol 1997, 9:4-9.
39. Yang R.B., Mark M.R., Gray A., et al. Toll-like receptor-2 mediates lipopolysaccharide-induced cellular signalling. Nature 1998, 395:284-288.
40. Takeuchi O., Hoshino K., Kawai T., et al. Differential roles of TLR2 and TLR4 in recognition of gram-negative and gram-positive bacterial cell wall components. Immunity 1999, 11:443-451.
41. Hirschfeld M., Kirschning C.J., Schwandner R., et al. Cutting edge: inflammatory signaling by borrelia burgdorferi lipoproteins is mediated by toll-like receptor 2. J Immunol 1999, 163:2382-2386.
42. Hou L., Sasaki H., Stashenko P. Toll-like receptor 4-deficient mice have reduced bone destruction following mixed anaerobic infection. Infect Immun 2000, 68:4681-4687.
43. Gately M.K., Desai B.B., Wolitzky A.G., et al. Regulation of human lymphocyte proliferation by a heterodimeric cytokine, IL-12 (cytotoxic lymphocyte maturation factor). J Immunol 1991, 147:874-882.
44. Thoma-Uszynski S., Kiertscher S.M., Ochoa M.T., et al. Activation of Toll-like receptor 2 on human denritic cells triggers induction of IL-12 but not IL-10. J Immunol 2000, 165:3804-3810.
45. Verreck F.A., de Boer T., Langenberg D.M., et al. Human IL-23-producing type 1 macrophages promote but IL-10-producing type 2 macrophages subvert immunity to (myco)bacteria. Proc Natl Acad Sci U S A 2004, 101:4560-4565.
46. Roses R.E., Xu S., Xu M., Koldovsky U., Koski G., Czerniecki B.J. Differential production of IL-23 and IL-12 by myeloid-derived dendritic cells in response to TLR agonists. J Immunol 2008, 181:5120-5127.
47. Blander J.M., Medzhitov R. Regulation of phagosome maturation by signals from toll-like receptors. Science 2004, 304:1014-1018.
48. Doyle S.E., O'Connell R.M., Miranda G.A., et al. Toll-like receptors induce a phagocytic gene program through p38. J Exp Med 2004, 199:81-90.
49. Hertz C.J., Kiertscher S.M., Godowski P.J., et al. Microbial lipopeptides stimulate dendritic cell maturation via TLR2. J Immunol 2000, 166:2444-2450.
50. Krutzik S.R., Tan B., Li H., et al. TLR activation triggers the rapid differentiation of monocytes into macrophages and dendritic cells. Nat Med 2005, 11:653-660.
51. Doyle S., Vaidya S., O'Connell R., et al. IRF3 mediates a TLR3/TLR4-specific antiviral gene program. Immunity 2002, 17:251-263.
52. Kawai T., Takeuchi O., Fujita T., et al. Lipopolysaccharide stimulates the MyD88-independent pathway and results in activation of IFN-regulatory factor 3 and the expression of a subset of lipopolysaccharide-inducible genes. J Immunol 2001, 167:5887-5894.
53. Kawai T., Sato S., Ishii K.J., et al. Interferon-alpha induction through Toll-like receptors involves a direct interaction of IRF7 with MyD88 and TRAF6. Nat Immunol 2004, 5:1061-1068.
54. Kim J., Ochoa M.T., Krutzik S.R., et al. Activation of toll-like receptor 2 in acne triggers inflammatory cytokine responses. J Immunol 2002, 169:1535-1541.
55. Strober W., Murray P.J., Kitani A., Watanabe T. Signalling pathways and molecular interactions of NOD1 and NOD2. Nat Rev Immunol 2006, 6:9-20.
56. Fritz J.H., Ferrero R.L., Philpott D.J., Girardin S.E. Nod-like proteins in immunity, inflammation and disease. Nat Immunol 2006, 7:1250-1257.
57. Hruz P., Zinkernagel A.S., Jenikova G., et al. NOD2 contributes to cutaneous defense against Staphylococcus aureus through alpha-toxin-dependent innate immune activation. Proc Natl Acad Sci U S A 2009, 106:12873-12878.
58. Delbridge L.M., O'Riordan M.X. Innate recognition of intracellular bacteria. Curr Opin Immunol 2007, 19:10-16.
59. Martinon F., Mayor A., Tschopp J. The inflammasomes: guardians of the body. Annu Rev Immunol 2009, 27:229-265.
60. Lachmann H.J., Kone-Paut I., Kuemmerle-Deschner J.B., et al. Use of canakinumab in the cryopyrin-associated periodic syndrome. N Engl J Med 2009, 360:2416-2425.
61. Klesney-Tait J., Turnbull I.R., Colonna M. The TREM receptor family and signal integration. Nat Immunol 2006, 7:1266-1273.
62. Crocker P.R. Siglecs in innate immunity. Curr Opin Pharmacol 2005, 5:431-437.
63. Robinson M.J., Sancho D., Slack E.C., LeibundGut-Landmann S., Reis e Sousa C. Myeloid C-type lectins in innate immunity. Nat Immunol 2006, 7:1258-1265.
64. Mosser D.M., Edwards J.P. Exploring the full spectrum of macrophage activation. Nat Rev Immunol 2008, 8:958-969.
65. Gordon S. Alternative activation of macrophages. Nat Rev Immunol 2003, 3:23-35.
66. van Kooten C., Banchereau J. CD40-CD40 ligand. J Leukoc Biol 2000, 67:2-17.
67. Stone K.D., Prussin C., Metcalfe D.D. IgE, mast cells, basophils, and eosinophils. J Allergy Clin Immunol 2010, 125(2 suppl 2):S73-80.
68. Raulet D.H. Interplay of natural killer cells and their receptors with the adaptive immune response. Nat Immunol 2004, 5:996-1002.
69. Bauer S., Groh V., Wu J., et al. Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA. Science 1999, 285:727-729.
70. Groh V., Rhinehart R., Secrist H., Bauer S., Grabstein K.H., Spies T. Broad tumor-associated expression and recognition by tumor-derived gamma delta T cells of MICA and MICB. Proc Natl Acad Sci U S A 1999, 96:6879-6884.
71. Kupper T.S., Groves R.W. The interleukin-1 axis and cutaneous inflammation. J Invest Dermatol 1995, 105(1 suppl):62S-66S.
72. Blauvelt A., Asada H., Klaus-Kovtun V., Altman D.J., Lucey D.R., Katz S.I. Interleukin-15 mRNA is expressed by human keratinocytes Langerhans cells, and blood-derived dendritic cells and is downregulated by ultraviolet B radiation. J Invest Dermatol 1996, 106:1047-1052.
73. Stoll S., Müller G., Kurimoto M., et al. Production of IL-18 (IFN-gamma-inducing factor) messenger RNA and functional protein by murine keratinocytes. J Immunol 1997, 159:298-302.
74. Enk A.H., Katz S.I. Identification and induction of keratinocyte-derived IL-10. J Immunol 1992, 149:92-95.
75. Lebre M.C., Antons J.C., Kalinski P., et al. Double-stranded RNA-exposed human keratinocytes promote Th1 responses by inducing a Type-1 polarized phenotype in dendritic cells: role of keratinocyte-derived tumor necrosis factor alpha, type I interferons, and interleukin-18. J Invest Dermatol 2003, 120:990-997.
76. Soumelis V., Reche P.A., Kanzler H., et al. Human epithelial cells trigger dendritic cell mediated allergic inflammation by producing TSLP. Nat Immunol 2002, 3:673-680.
77. Harrington L.E., Mangan P.R., Weaver C.T. Expanding the effector CD4 T-cell repertoire: the Th17 lineage. Curr Opin Immunol 2006, 18:349-356.
78. Miller L.S., Sørensen O.E., Liu P.T., et al. TGF-alpha regulates TLR expression and function on epidermal keratinocytes. J Immunol 2005, 174:6137-6143.
79. Köllisch G., Kalali B.N., Voelcker V., et al. Various members of the Toll-like receptor family contribute to the innate immune response of human epidermal keratinocytes. Immunology 2005, 114:531-541.
80. Lebre M.C., van der Aar A.M., van Baarsen L., et al. Human keratinocytes express functional Toll-like receptor 3, 4, 5, and 9. J Invest Dermatol 2007, 127:331-341.
81. Nestle F.O., Di Meglio P., Qin J.Z., Nickoloff B.J. Skin immune sentinels in health and disease. Nat Rev Immunol 2009, 9:679-691.
82. Reiss Y., Proudfoot A.E., Power C.A., Campbell J.J., Butcher E.C. CC chemokine receptor (CCR)4 and the CCR10 ligand cutaneous T cell-attracting chemokine (CTACK) in lymphocyte trafficking to inflamed skin. J Exp Med 2001, 194:1541-1547.
83. Charbonnier A.S., Kohrgruber N., Kriehuber E., Stingl G., Rot A., Maurer D. Macrophage inflammatory protein 3alpha is involved in the constitutive trafficking of epidermal langerhans cells. J Exp Med 1999, 190:1755-1768.
84. Hedrick M.N., Lonsdorf A.S., Shirakawa A.K., et al. CCR6 is required for IL-23-induced psoriasis-like inflammation in mice. J Clin Invest 2009, 119:2317-2329.
85. Harper E.G., Guo C., Rizzo H., et al. Th17 cytokines stimulate CCL20 expression in keratinocytes in vitro and in vivo: implications for psoriasis pathogenesis. J Invest Dermatol 2009, 129:2175-2183.
86. Köck A., Schwarz T., Kirnbauer R., et al. Human keratinocytes are a source for tumor necrosis factor alpha: evidence for synthesis and release upon stimulation with endotoxin or ultraviolet light. J Exp Med 1990, 172:1609-1614.
87. Watts C. Capture and processing of exogenous antigens for presentation on MHC molecules. Annu Rev Immunol 1997, 15:821-850.
88. Fogg D.K., Sibon C., Miled C., et al. A clonogenic bone marrow progenitor specific for macrophages and dendritic cells. Science 2006, 311:83-87.
89. Naik S.H., Sathe P., Park H.Y., et al. Development of plasmacytoid and conventional dendritic cell subtypes from single precursor cells derived in vitro and in vivo. Nat Immunol 2007, 8:1217-1226.
90. Liu K., Waskow C., Liu X., Yao K., Hoh J., Nussenzweig M. Origin of dendritic cells in peripheral lymphoid organs of mice. Nat Immunol 2007, 8:578-583.
91. Massberg S., Schaerli P., Knezevic-Maramica I., et al. Immunosurveillance by hematopoietic progenitor cells trafficking through blood, lymph, and peripheral tissues. Cell 2007, 131:994-1008.
92. Onai N., Obata-Onai A., Schmid M.A., Ohteki T., Jarrossay D., Manz M.G. Identification of clonogenic common Flt3+M-CSFR+ plasmacytoid and conventional dendritic cell progenitors in mouse bone marrow. Nat Immunol 2007, 8:1207-1216.
93. Geissmann F., Jung S., Littman D.R. Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity 2003, 19:71-82.
94. Stumbles P.A., Strickland D.H., Pimm C.L., et al. Regulation of dendritic cell recruitment into resting and inflamed airway epithelium: use of alternative chemokine receptors as a function of inducing stimulus. J Immunol 2001, 167:228-234.
95. Merad M., Manz M.G., Karsunky H., et al. Langerhans cells renew in the skin throughout life under steady-state conditions. Nat Immunol 2002, 3:1135-1141.
96. Merad M., Hoffmann P., Ranheim E., et al. Depletion of host Langerhans cells before transplantation of donor alloreactive T cells prevents skin graft-versus-host disease. Nat Med 2004, 10:510-517.
97. Cerio R., Griffiths C.E., Cooper K.D., Nickoloff B.J., Headington J.T. Characterization of factor XIIIa positive dermal dendritic cells in normal and inflamed skin. Br J Dermatol 1989, 121:421-431.
98. Bursch L.S., Wang L., Igyarto B., et al. Identification of a novel population of Langerin+ dendritic cells. J Exp Med 2007, 204:3147-3156.
99. Ginhoux F., Collin M.P., Bogunovic M., et al. Blood-derived dermal langerin+ dendritic cells survey the skin in the steady state. J Exp Med 2007, 204:3133-3146.
100. Poulin L.F., Henri S., de Bovis B., Devilard E., Kissenpfennig A., Malissen B. The dermis contains langerin+ dendritic cells that develop and function independently of epidermal Langerhans cells. J Exp Med 2007, 204:3119-3131.
101. Romani N., Clausen B.E., Stoitzner P. Langerhans cells and more: langerin-expressing dendritic cell subsets in the skin. Immunol Rev 2010, 234:120-141.
102. Langerhans P. Über die Nerven der menschlichen Haut. Virchows Arch 1868, 44:325-337.
103. Stingl G., Wolff-Schreiner E.C., Pichler W.J., Gschnait F., Knapp W., Wolff K. Epidermal Langerhans cells bear Fc and C3 receptors. Nature 1977, 268:245-246.
104. Rowden G., Lewis M.G., Sullivan A.K. Ia antigen expression on human epidermal Langerhans cells. Nature 1977, 268:247-248.
105. Klareskog L., Tjernlund U., Forsum U., Peterson P.A. Epidermal Langerhans cells express Ia antigens. Nature 1977, 268:248-250.
106. Kissenpfennig A., Aït-Yahia S., Clair-Moninot V., et al. Disruption of the langerin/CD207 gene abolishes Birbeck granules without a marked loss of Langerhans cell function. Mol Cell Biol 2005, 25:88-99.
107. Schuster C., Vaculik C., Fiala C., et al. HLA-DR+ leukocytes acquire CD1 antigens in embryonic and fetal human skin and contain functional antigen-presenting cells. J Exp Med 2009, 206:169-181.
108. Tang A., Amagai M., Granger L.G., Stanley J.R., Udey M.C. Adhesion of epidermal Langerhans cells to keratinocytes mediated by E-cadherin. Nature 1993, 361:82-85.
109. Konrad K., Honigsmann H. Electron microscopic demonstration of a mitotic Langerhans cell in the normal human epidermis. Arch Dermatol Forsch 1973, 246:70-76.
110. Larregina A.T., Morelli A.E., Spencer L.A., et al. Dermal-resident CD14+ cells differentiate into Langerhans cells. Nat Immunol 2001, 2:1151-1158.
111. Stingl G., Tamaki K., Katz S.I. Origin and function of epidermal Langerhans cells. Immunol Rev 1980, 53:149-174.
112. Inaba K., Schuler G., Witmer M.D., Valinksy J., Atassi B., Steinman R.M. Immunologic properties of purified epidermal Langerhans cells. Distinct requirements for stimulation of unprimed and sensitized T lymphocytes. J Exp Med 1986, 164:605-613.
113. Hauser C., Katz S.I. Activation and expansion of hapten- and protein-specific T helper cells from nonsensitized mice. Proc Natl Acad Sci U S A 1988, 85:5625-5628.
114. Romani N., Koide S., Crowley M., et al. Presentation of exogenous protein antigens by dendritic cells to T cell clones. Intact protein is presented best by immature, epidermal Langerhans cells. J Exp Med 1989, 169:1169-1178.
115. Stoitzner P., Tripp C.H., Eberhart A., et al. Langerhans cells cross-present antigen derived from skin. Proc Natl Acad Sci U S A 2006, 103:7783-7788.
116. Stoitzner P., Green L.K., Jung J.Y., et al. Tumor immunotherapy by epicutaneous immunization requires langerhans cells. J Immunol 2008, 180:1991-1998.
117. Kubo A., Nagao K., Yokouchi M., Sasaki H., Amagai M. External antigen uptake by Langerhans cells with reorganization of epidermal tight junction barriers. J Exp Med 2009, 206:2937-2946.
118. Larsen C.P., Steinman R.M., Witmer-Pack M., Hankins D.F., Morris P.J., Austyn J.M. Migration and maturation of Langerhans cells in skin transplants and explants. J Exp Med 1990, 172:1483-1493.
119. Schuler G., Steinman R.M. Murine epidermal Langerhans cells mature into potent immunostimulatory dendritic cells in vitro. J Exp Med 1985, 161:526-546.
120. Kriehuber E., Breiteneder-Geleff S., Groeger M., et al. Isolation and characterization of dermal lymphatic and blood endothelial cells reveal stable and functionally specialized cell lineages. J Exp Med 2001, 194:797-808.
121. Ohl L., Mohaupt M., Czeloth N., et al. CCR7 governs skin dendritic cell migration under inflammatory and steady-state conditions. Immunity 2004, 21:279-288.
122. Eberhard Y., Ortiz S., Ruiz Lascano A., Kuznitzky R., Serra H.M. Up-regulation of the chemokine CCL21 in the skin of subjects exposed to irritants. BMC Immunol 2004, 5:7.
123. Meunier L., Gonzalez-Ramos A., Cooper K.D. Heterogeneous populations of class II MHC+ cells in human dermal cell suspensions. Identification of a small subset responsible for potent dermal antigen-presenting cell activity with features analogous to Langerhans cells. J Immunol 1993, 151:4067-4080.
124. Nestle F.O., Zheng X.G., Thompson C.B., Turka L.A., Nickoloff B.J. Characterization of dermal dendritic cells obtained from normal human skin reveals phenotypic and functionally distinctive subsets. J Immunol 1993, 151:6535-6545.
125. Zaba L.C., Krueger J.G., Lowes M.A. Resident and "inflammatory" dendritic cells in human skin. J Invest Dermatol 2009, 129:302-308.
126. Ochoa M.T., Loncaric A., Krutzik S.R., Becker T.C. Modlin RL. "Dermal dendritic cells" comprise two distinct populations: CD1+ dendritic cells and CD209+ macrophages. J Invest Dermatol 2008, 128:2225-2231.
127. Zaba L.C., Fuentes-Duculan J., Steinman R.M., Krueger J.G., Lowes M.A. Normal human dermis contains distinct populations of CD11c+BDCA-1+ dendritic cells and CD163+FXIIIA+ macrophages. J Clin Invest 2007, 117:2517-2525.
128. Jongbloed S.L., Kassianos A.J., McDonald K.J., et al. Human CD141+ (BDCA-3)+ dendritic cells (DCs) represent a unique myeloid DC subset that cross-presents necrotic cell antigens. J Exp Med 2010, 207:1247-1260.
129. Bogunovic M., Ginhoux F., Wagers A., et al. Identification of a radio-resistant and cycling dermal dendritic cell population in mice and men. J Exp Med 2006, 203:2627-2638.
130. Angel C.E., George E., Brooks A.E., Ostrovsky L.L., Brown T.L., Dunbar P.R. Cutting edge: CD1a+ antigen-presenting cells in human dermis respond rapidly to CCR7 ligands. J Immunol 2006, 176:5730-5734.
131. Randolph G.J., Sanchez-Schmitz G., Liebman R.M., Schäkel K. The CD16(+) (FcgammaRIII(+)) subset of human monocytes preferentially becomes migratory dendritic cells in a model tissue setting. J Exp Med 2002, 196:517-527.
132. Piccioli D., Tavarini S., Borgogni E., et al. Functional specialization of human circulating CD16 and CD1c myeloid dendritic-cell subsets. Blood 2007, 109:5371-5379.
133. Lowes M.A., Chamian F., Abello M.V., et al. Increase in TNF-alpha 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.
134. Guttman-Yassky E., Lowes M.A., Fuentes-Duculan J., et al. Major differences in inflammatory dendritic cells and their products distinguish atopic dermatitis from psoriasis. J Allergy Clin Immunol 2007, 119:1210-1217.
135. Stary G., Bangert C., Tauber M., Strohal R., Kopp T., Stingl G. Tumoricidal activity of TLR7/8-activated inflammatory dendritic cells. J Exp Med 2007, 204:1441-1451.
136. Zaba L.C., Fuentes-Duculan J., Eungdamrong N.J., et al. Psoriasis is characterized by accumulation of immunostimulatory and Th1/Th17 cell-polarizing myeloid dendritic cells. J Invest Dermatol 2009, 129:79-88.
137. Zaba L.C., Cardinale I., Gilleaudeau P., et al. Amelioration of epidermal hyperplasia by TNF inhibition is associated with reduced Th17 responses. J Exp Med 2007, 204:3183-3194.
138. Serbina N.V., Salazar-Mather T.P., Biron C.A., Kuziel W.A., Pamer E.G. TNF/iNOS-producing dendritic cells mediate innate immune defense against bacterial infection. Immunity 2003, 19:59-70.
139. Tezuka H., Abe Y., Iwata M., et al. Regulation of IgA production by naturally occurring TNF/iNOS-producing dendritic cells. Nature 2007, 448:929-933.
140. Palamara F., Meindl S., Holcmann M., Lührs P., Stingl G., Sibilia M. Identification and characterization of pDC-like cells in normal mouse skin and melanomas treated with imiquimod. J Immunol 2004, 173:3051-3061.
141. Haider A.S., Lowes M.A., Suárez-Fariñas M. Identification of cellular pathways of "type 1," Th17 T cells, and TNF- and inducible nitric oxide synthase-producing dendritic cells in autoimmune inflammation through pharmacogenomic study of cyclosporine A in psoriasis. J Immunol 2008, 180:1913-1920.
142. Schäkel K., von Kietzell M., Hänsel A., et al. Human 6-sulfo LacNAc-expressing dendritic cells are principal producers of early interleukin-12 and are controlled by erythrocytes. Immunity 2006, 24:767-777.
143. Wollenberg A., Kraft S., Hanau D., Bieber T. Immunomorphological and ultrastructural characterization of Langerhans cells and a novel, inflammatory dendritic epidermal cell (IDEC) population in lesional skin of atopic eczema. J Invest Dermatol 1996, 106:446-453.
144. Wollenberg A., Mommaas M., Oppel T., Schottdorf E.M., Günther S., Moderer M. Expression and function of the mannose receptor CD206 on epidermal dendritic cells in inflammatory skin diseases. J Invest Dermatol 2002, 118:327-334.
145. Schuller E., Teichmann B., Haberstok J., Moderer M., Bieber T., Wollenberg A. In situ expression of the costimulatory molecules CD80 and CD86 on langerhans cells and inflammatory dendritic epidermal cells (IDEC) in atopic dermatitis. Arch Dermatol Res 2001, 293:448-454.
146. Novak N., Valenta R., Bohle B., et al. FcepsilonRI engagement of Langerhans cell-like dendritic cells and inflammatory dendritic epidermal cell-like dendritic cells induces chemotactic signals and different T-cell phenotypes in vitro. J Allergy Clin Immunol 2004, 113:949-957.
147. Lande R., Gilliet M. Plasmacytoid dendritic cells: key players in the initiation and regulation of immune responses. Ann N Y Acad Sci 2010, 1183:89-103.
148. Siegal F.P., Kadowaki N., Shodell M., et al. The nature of the principal type 1 interferon-producing cells in human blood. Science 1999, 284:1835-1837.
149. Kohrgruber N., Halanek N., Gröger M., et al. Survival, maturation, and function of CD11c- and CD11c+ peripheral blood dendritic cells are differentially regulated by cytokines. J Immunol 1999, 163:3250-3259.
150. Gerlini G., Mariotti G., Bianchi B., Pimpinelli N. Massive recruitment of type I interferon producing plasmacytoid dendritic cells in varicella skin lesions. J Invest Dermatol 2006, 126:507-509.
151. Farkas L., Beiske K., Lund-Johansen F., Brandtzaeg P., Jahnsen F.L. Plasmacytoid dendritic cells (natural interferon- alpha/beta-producing cells) accumulate in cutaneous lupus erythematosus lesions. Am J Pathol 2001, 159:237-243.
152. Wollenberg A., Wagner M., Günther S., et al. Plasmacytoid dendritic cells: a new cutaneous dendritic cell subset with distinct role in inflammatory skin diseases. J Invest Dermatol 2002, 119:1096-1102.
153. Bangert C., Friedl J., Stary G., Stingl G., Kopp T. Immunopathologic features of allergic contact dermatitis in humans: participation of plasmacytoid dendritic cells in the pathogenesis of the disease?. J Invest Dermatol 2003, 121:1409-1418.
154. Vanbervliet B., Bendriss-Vermare N., Massacrier C., et al. The inducible CXCR3 ligands control plasmacytoid dendritic cell responsiveness to the constitutive chemokine stromal cell-derived factor 1 (SDF-1)/CXCL12. J Exp Med 2003, 198:823-830.
155. Kohrgruber N., Gröger M., Meraner P., et al. Plasmacytoid dendritic cell recruitment by immobilized CXCR3 ligands. J Immunol 2004, 173:6592-6602.
156. Vermi W., Riboldi E., Wittamer V., et al. Role of ChemR23 in directing the migration of myeloid and plasmacytoid dendritic cells to lymphoid organs and inflamed skin. J Exp Med 2005, 201:509-515.
157. Albanesi C., Scarponi C., Pallotta S., et al. Chemerin expression marks early psoriatic skin lesions and correlates with plasmacytoid dendritic cell recruitment. J Exp Med 2009, 206:249-258.
158. Kadowaki N., Antonenko S., Lau J.Y., Liu Y.J. Natural interferon alpha/beta-producing cells link innate and adaptive immunity. J Exp Med 2000, 192:219-226.
159. Rissoan M.C., Soumelis V., Kadowaki N., et al. Reciprocal control of T helper cell and dendritic cell differentiation. Science 1999, 283:1183-1186.
160. Blanco P., Palucka A.K., Gill M., Pascual V., Banchereau J. Induction of dendritic cell differentiation by IFN-alpha in systemic lupus erythematosus. Science 2001, 294:1540-1543.
161. Jego G., Palucka A.K., Blanck J.P., Chalouni C., Pascual V., Banchereau J. Plasmacytoid dendritic cells induce plasma cell differentiation through type I interferon and interleukin 6. Immunity 2003, 19:225-234.
162. von Boehmer H. Selection of the T-cell repertoire: receptor-controlled checkpoints in T-cell development. Adv Immunol 2004, 84:201-238.
163. Ellmeier W., Sawada S., Littman D.R. The regulation of CD4 and CD8 coreceptor gene expression during T cell development. Annu Rev Immunol 1999, 17:523-554.
164. Takahama Y. Journey through the thymus: stromal guides for T-cell development and selection. Nat Rev Immunol 2006, 6:127-135.
165. Sprent J., Surh C.D. T cell memory. Annu Rev Immunol 2002, 20:551-579.
166. Sallusto F., Geginat J., Lanzavecchia A. Central memory and effector memory T cell subsets: function, generation, and maintenance. Annu Rev Immunol 2004, 22:745-763.
167. Edele F., Molenaar R., Gütle D., et al. Cutting edge: instructive role of peripheral tissue cells in the imprinting of T cell homing receptor patterns. J Immunol 2008, 181:3745-3749.
168. Campbell D.J., Butcher E.C. Rapid acquisition of tissue-specific homing phenotypes by CD4(+) T cells activated in cutaneous or mucosal lymphoid tissues. J Exp Med 2002, 195:135-141.
169. Sallusto F., Mackay C.R. Chemoattractants and their receptors in homeostasis and inflammation. Curr Opin Immunol 2004, 16:724-731.
170. Morales J., Homey B., Vicari A.P., et al. CTACK, a skin-associated chemokine that preferentially attracts skin-homing memory T cells. Proc Natl Acad Sci U S A 1999, 96:14470-14475.
171. Clark R.A., Chong B., Mirchandani N., et al. The vast majority of CLA+ T cells are resident in normal skin. J Immunol 2006, 176:4431-4439.
172. Modlin R.L., Hofman F.M., Taylor C.R., Rea T.H. T lymphocyte subsets in the skin lesions of patients with leprosy. J Am Acad Dermatol 1983, 8:182-189.
173. Wang X.H., Ohmen J.D., Uyemura K., Rea T.H., Kronenberg M., Modlin R.L. Selection of T lymphocytes bearing limited T-cell receptor beta chains in the response to a human pathogen. Proc Natl Acad Sci U S A 1993, 90:188-192.
174. Diluvio L., Vollmer S., Besgen P., et al. beta-chain rearrangements in streptococcal angina and skin lesions of patients with psoriasis vulgaris. J Immunol 2006, 176:7104-7111.
175. Wood G.S., Tung R.M., Haeffner A.C., et al. Detection of clonal T-cell receptor gamma gene rearrangements in early mycosis fungoides/Sezary syndrome by polymerase chain reaction and denaturing gradient gel electrophoresis (PCR/DGGE). J Invest Dermatol 1994, 103:34-41.
176. Winter D., Fiebiger E., Meraner P., et al. Definition of TCR epitopes for CTL-mediated attack of cutaneous T cell lymphoma. J Immunol 2003, 171:2714-2724.
177. Zhu J., Koelle D.M., Cao J., et al. Virus-specific CD8+ T cells accumulate near sensory nerve endings in genital skin during subclinical HSV-2 reactivation. J Exp Med 2007, 204:595-603.
178. Teraki Y., Shiohara T. IFN-gamma-producing effector CD8+ T cells and IL-10-producing regulatory CD4+ T cells in fixed drug eruption. J Allergy Clin Immunol 2003, 112:609-615.
179. Szabo S.J., Sullivan B.M., Stemmann C., Satoskar A.R., Sleckman B.P., Glimcher L.H. Distinct effects of T-bet in TH1 lineage commitment and IFN-gamma production in CD4 and CD8 T cells. Science 2002, 295:338-342.
180. Gately M.K., Renzetti L.M., Magram J., et al. The interleukin-12/interleukin-12-receptor system: role in normal and pathologic immune responses. Annu Rev Immunol 1998, 16:495-521.
181. Mosmann T.R., Cherwinski H., Bond M.W., Giedlin M.A., Coffman R.L. Two types of murine helper T cell clone. I. Definition according to profiles of lymphokine activities and secreted proteins. J Immunol 1986, 136:2348-2357.
182. Abbas A.K., Murphy K.M., Sher A. Functional diversity of helper T lymphocytes. Nature 1996, 383:787-793.
183. Zheng W., Flavell R.A. The transcription factor GATA-3 is necessary and sufficient for Th2 cytokine gene expression in CD4 T cells. Cell 1997, 89:587-596.
184. Lee G.R., Fields P.E., Flavell R.A. Regulation of IL-4 gene expression by distal regulatory elements and GATA-3 at the chromatin level. Immunity 2001, 14:447-459.
185. Korn T., Bettelli E., Oukka M., Kuchroo V.K. IL-17 and Th17 cells. Annu Rev Immunol 2009, 27:485-517.
186. Ivanov I.I., McKenzie B.S., Zhou L., et al. The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell 2006, 126:1121-1133.
187. Kleinewietfeld M., Puentes F., Borsellino G., Battistini L., Rötzschke O., Falk K. CCR6 expression defines regulatory effector/memory-like cells within the CD25(+)CD4+ T-cell subset. Blood 2005, 105:2877-2886.
188. Wilson N.J., Boniface K., Chan J.R., et al. Development, cytokine profile and function of human interleukin 17-producing helper T cells. Nat Immunol 2007, 8:950-957.
189. Manel N., Unutmaz D., Littman D.R. The differentiation of human T(H)-17 cells requires transforming growth factor-beta and induction of the nuclear receptor RORgammat. Nat Immunol 2008, 9:641-649.
190. Kleinschek M.A., Boniface K., Sadekova S., et al. Circulating and gut-resident human Th17 cells express CD161 and promote intestinal inflammation. J Exp Med 2009, 206:525-534.
191. Zou W., Restifo N.P. T(H)17 cells in tumour immunity and immunotherapy. Nat Rev Immunol 2010, 10:248-256.
192. He D., Wu L., Kim H.K., Li H., Elmets C.A., Xu H. CD8+ IL-17-producing T cells are important in effector functions for the elicitation of contact hypersensitivity responses. J Immunol 2006, 177:6852-6858.
193. Boniface K., Bernard F.X., Garcia M., Gurney A.L., Lecron J.C., Morel F. IL-22 inhibits epidermal differentiation and induces proinflammatory gene expression and migration of human keratinocytes. J Immunol 2005, 174:3695-3702.
194. Duhen T., Geiger R., Jarrossay D., Lanzavecchia A., Sallusto F. Production of interleukin 22 but not interleukin 17 by a subset of human skin-homing memory T cells. Nat Immunol 2009, 10:857-863.
195. Eyerich S., Eyerich K., Pennino D., et al. Th22 cells represent a distinct human T cell subset involved in epidermal immunity and remodeling. J Clin Invest 2009, 119:3573-3585.
196. Shevach E.M., DiPaolo R.A., Andersson J., Zhao D.M., Stephens G.L., Thornton A.M. The lifestyle of naturally occurring CD4+ CD25+ Foxp3+ regulatory T cells. Immunol Rev 2006, 212:60-73.
197. Shevach E.M. Mechanisms of foxp3+ T regulatory cell-mediated suppression. Immunity 2009, 30:636-645.
198. Stary G., Klein I., Brüggen M.C., Kohlhofer S., et al. Host defense mechanisms in secondary syphilitic lesions: a role for IFN-gamma-/IL-17-producing CD8+ T cells?. Am J Pathol 2010, 177:2421-2432.
199. Hertl M., Eming R., Veldman C. T cell control in autoimmune bullous skin disorders. J Clin Invest 2006, 116:1159-1166.
200. Landsteiner K., Chase M.W. Studies on the sensitization of animals with simple chemical compounds: Vii. Skin sensitization by intraperitoneal injections. J Exp Med 1940, 71:237-245.
201. Beutner E.H., Jordon R.E. Demonstration of skin antibodies in sera of pemphigus vulgaris patients by indirect immunofluorescent staining. Proc Soc Exp Biol Med 1964, 117:505-510.
202. Streilein J.W. Skin-associated lymphoid tissues (SALT): origins and functions. J Invest Dermatol 1983, 80(suppl):12s-16s.
203. Stoitzner P., Pfaller K., Stössel H., Romani N. A close-up view of migrating Langerhans cells in the skin. J Invest Dermatol 2002, 118:117-125.
204. Kaplan D.H., Jenison M.C., Saeland S., Shlomchik W.D., Shlomchik M.J. Epidermal langerhans cell-deficient mice develop enhanced contact hypersensitivity. Immunity 2005, 23:611-620.
205. Bennett C.L., van Rijn E., Jung S., et al. Inducible ablation of mouse Langerhans cells diminishes but fails to abrogate contact hypersensitivity. J Cell Biol 2005, 169:569-576.
206. Kong Y.Y., Yoshida H., Sarosi I., et al. OPGL is a key regulator of osteoclastogenesis, lymphocyte development and lymph-node organogenesis. Nature 1999, 397:315-323.
207. Loser K., Mehling A., Loeser S., et al. Epidermal RANKL controls regulatory T-cell numbers via activation of dendritic cells. Nat Med 2006, 12:1372-1379.
208. Loser K., Beissert S. Regulation of cutaneous immunity by the environment: an important role for UV irradiation and vitamin D. Int Immunopharmacol 2009, 9:587-589.