Resident and "inflammatory" dendritic cells in human skin

Journal of Investigative Dermatology

Volumn 129, Issue 2, 2009, Pages 302-308

  Zaba, Lisa C ^a   Krueger, James G ^a   Lowes, Michelle A ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON; CD14 ANTIGEN; IMMUNOGLOBULIN A; MONOCLONAL ANTIBODY; T6 ANTIGEN;

ANTIGEN PRESENTING CELL; ATOPIC DERMATITIS; CELL MIGRATION; CELL POPULATION; DENDRITIC CELL; HUMAN; LANGERHANS CELL; MACROPHAGE; PRIORITY JOURNAL; PSORIASIS; REVIEW; SKIN INFLAMMATION; STEADY STATE; T LYMPHOCYTE ACTIVATION;

DENDRITIC CELLS; DERMATITIS; HUMANS; SKIN;

EID: 58549114666     PISSN: 0022202X     EISSN: 15231747     Source Type: Journal    
DOI: 10.1038/jid.2008.225     Document Type: Review

References (85)

1. Allan RS, Waithman J, Bedoui S, Jones CM, Villadangos JA, Zhan Y et al. (2006) Migratory dendritic cells transfer antigen to a lymph node-resident dendritic cell population for efficient CTL priming. Immunity 25:153-62
2. Angel CE, George E, Brooks AE, Ostrovsky LL, Brown TL, Dunbar PR (2006) Cutting edge: CD1a+ antigen-presenting cells in human dermis respond rapidly to CCR7 ligands. J Immunol 176:5730-4
3. Angel CE, Lala A, Chen CJ, Edgar SG, Ostrovsky LL, Dunbar PR (2007) CD14+ antigen-presenting cells in human dermis are less mature than their CD1a+ counterparts. Int Immunol 19:1271-9
4. Barral DC, Brenner MB (2007) CD1 antigen presentation: how it works. Nat Rev Immunol 7:929-41
5. Bennett CL, van Rijn E, Jung S, Inaba K, Steinman RM, Kapsenberg ML et al. (2005) Inducible ablation of mouse Langerhans cells diminishes but fails to abrogate contact hypersensitivity. J Cell Biol 169:569-76
6. Bogunovic M, Ginhoux F, Wagers A, Loubeau M, Isola LM, Lubrano L et al. (2006) Identification of a radio-resistant and cycling dermal dendritic cell population in mice and men. J Exp Med 203:2627-38
7. Braathen LR, Thorsby E (1980) Studies on human epidermal Langerhans cells. I. Allo-activating and antigen-presenting capacity. Scand J Immunol 11:401-8
8. Bursch LS, Wang L, Igyarto B, Kissenpfennig A, Malissen B, Kaplan DH et al. (2007) Identification of a novel population of Langerin+ dendritic cells. J Exp Med 204:3147-56
9. Butler M, Morel AS, Jordan WJ, Eren E, Hue S, Shrimpton RE et al. (2007) Altered expression and endocytic function of CD205 in human dendritic cells, and detection of a CD205-DCL-1 fusion protein upon dendritic cell maturation. Immunology 120:362-71
10. Corcoran L, Ferrero I, Vremec D, Lucas K, Waithman J, O'Keeffe M et al. (2003) The lymphoid past of mouse plasmacytoid cells and thymic dendritic cells. J Immunol 170:4926-32
11. Cumberbatch M, Singh M, Dearman RJ, Young HS, Kimber I, Griffiths CE (2006) Impaired Langerhans cell migration in psoriasis. J Exp Med 203:953-60
12. Douillard P, Stoitzner P, Tripp CH, Clair-Moninot V, Ait-Yahia S, McLellan AD et al. (2005) Mouse lymphoid tissue contains distinct subsets of langerin/CD207 dendritic cells, only one of which represents epidermal-derived Langerhans cells. J Invest Dermatol 125:983-94
13. Dubois B, Massacrier C, Vanbervliet B, Fayette J, Briere F, Banchereau J et al. (1998) Critical role of IL-12 in dendritic cell-induced differentiation of naive B lymphocytes. J Immunol 161:2223-31
14. Dzionek A, Fuchs A, Schmidt P, Cremer S, Zysk M, Miltenyi S et al. (2000) BDCA-2, BDCA-3, and BDCA-4: three markers for distinct subsets of dendritic cells in human peripheral blood. J Immunol 165:6037-46
15. Ebner S, Ehammer Z, Holzmann S, Schwingshackl P, Forstner M, Stoitzner P et al. (2004) Expression of C-type lectin receptors by subsets of dendritic cells in human skin. Int Immunol 16:877-87
16. Engel D, Dobrindt U, Tittel A, Peters P, Maurer J, Gutgemann I et al. (2006) Tumor necrosis factor alpha- and inducible nitric oxide synthase-producing dendritic cells are rapidly recruited to the bladder in urinary tract infection but are dispensable for bacterial clearance. Infect Immun 74:6100-7
17. Figdor CG, van Kooyk Y, Adema GJ (2002) C-type lectin receptors on dendritic cells and Langerhans cells. Nat Rev Immunol 2:77-84
18. Ginhoux F, Collin MP, Bogunovic M, Abel M, Leboeuf M, Helft J et al. (2007) Blood-derived dermal langerin+ dendritic cells survey the skin in the steady state. J Exp Med 204:3133-46
19. Ginhoux F, Tacke F, Angeli V, Bogunovic M, Loubeau M, Dai XM et al. (2006) Langerhans cells arise from monocytes in vivo. Nat Immunol 7:265-73
20. Guo M, Gong S, Maric S, Misulovin Z, Pack M, Mahnke K et al. (2000) A monoclonal antibody to the DEC-205 endocytosis receptor on human dendritic cells. Hum Immunol 61:729-38
21. Guttman-Yassky E, Lowes MA, Fuentes-Duculan J, Whynot J, Novitskaya I, Cardinale I et al. (2007) Major differences in inflammatory dendritic cells and their products distinguish atopic dermatitis from psoriasis. J Allergy Clin Immunol 119:1210-7
22. Haider AS, Lowes MA, Suarez-Farinas M, Zaba LC, Cardinale I, Khatcherian A et al. (2008) 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 180:1913-20
23. Headington JT (1986) The dermal dendrocyte. Adv Dermatol 1:159-71
24. Iparraguirre A, Tobias JW, Hensley SE, Masek KS, Cavanagh LL, Rendl M et al. (2008) Two distinct activation states of plasmacytoid dendritic cells induced by influenza virus and CpG 1826 oligonucleotide. J Leukoc Biol 83:610-20
25. Ito T, Amakawa R, Inaba M, Hori T, Ota M, Nakamura K et al. (2004) Plasmacytoid dendritic cells regulate Th cell responses through OX40 ligand and type I IFNs. J Immunol 172:4253-9
26. Kadowaki N, Antonenko S, Lau JY, Liu YJ (2000) Natural interferon alpha/ beta-producing cells link innate and adaptive immunity. J Exp Med 192:219-26
27. Kaplan DH, Jenison MC, Saeland S, Shlomchik WD, Shlomchik MJ (2005) Epidermal langerhans cell-deficient mice develop enhanced contact hypersensitivity. Immunity 23:611-20
28. Kissenpfennig A, Ait-Yahia S, Clair-Moninot V, Stössel H, Badell E, Bordat Y et al. (2005a) Disruption of the langerin/CD207 gene abolishes Birbeck granules without a marked loss of Langerhans cell function. Mol Cell Biol 25:88-99
29. Kissenpfennig A, Henri S, Dubois B, Laplace-Builhe C, Perrin P, Romani N et al. (2005b) Dynamics and function of Langerhans cells in vivo: dermal dendritic cells colonize lymph node areas distinct from slower migrating Langerhans cells. Immunity 22:643-54
30. Lande R, Gregorio J, Facchinetti V, Chatterjee B, Wang YH, Homey B et al. (2007) Plasmacytoid dendritic cells sense self-DNA coupled with antimicrobial peptide. Nature 449:564-9
31. Langerhans P (1868) Uber die Nerven der menschlichen Haut. Virchows Arch, 325-37
32. Larregina AT, Falo LD Jr (2005) Changing paradigms in cutaneous immunology: adapting with dendritic cells. J Invest Dermatol 124:1-12
33. Larregina AT, Morelli AE, Spencer LA, Logar AJ, Watkins SC, Thomson AW et al. (2001) Dermal-resident CD14+ cells differentiate into Langerhans cells. Nat Immunol 2:1151-8
34. Lenz A, Heine M, Schuler G, Romani N (1993) Human and murine dermis contain dendritic cells. Isolation by means of a novel method and phenotypical and functional characterization. J Clin Invest 92:2587-96
35. Liu YJ (2005) IPC: professional type 1 interferon-producing cells and plasmacytoid dendritic cell precursors. Annu Rev Immunol 23:275-306
36. Lowes MA, Chamian F, Abello MV, Fuentes-Duculan J, Lin SL, Nussbaum R et al. (2005a) Increase in TNF-alpha and inducible nitric oxide synthase-expressing dendritic cells in psoriasis and reduction with efalizumab (anti-CD11a). Proc Natl Acad Sci USA 102:19057-62
37. Lowes MA, Turton JA, Krueger JG, Barnetson RS (2005b) Psoriasis vulgaris flare during efalizumab therapy does not preclude future use: a case series. BMC Dermatol 5:9
38. MacDonald KP, Munster DJ, Clark GJ, Dzionek A, Schmitz J, Hart DN (2002) Characterization of human blood dendritic cell subsets. Blood 100:4512-20
39. Massberg S, Schaerli P, Knezevic-Maramica I, Kollnberger M, Tubo N, Moseman EA et al. (2007) Immunosurveillance by hematopoietic progenitor cells trafficking through blood, lymph, and peripheral tissues. Cell 131:994-1008
40. Mc Dermott R, Ziylan U, Spehner D, Bausinger H, Lipsker D, Mommaas M et al. (2002) Birbeck granules are subdomains of endosomal recycling compartment in human epidermal Langerhans cells, which form where Langerin accumulates. Mol Biol Cell 13:317-35
41. McLellan AD, Heiser A, Hart DN (1999) Induction of dendritic cell costimulator molecule expression is suppressed by T cells in the absence of antigen-specific signalling: role of cluster formation, CD40 and HLA-class II for dendritic cell activation. Immunology 98:171-80
42. Merad M, Hoffmann P, Ranheim E, Slaymaker S, Manz MG, Lira SA et al. (2004) Depletion of host Langerhans cells before transplantation of donor alloreactive T cells prevents skin graft-versus-host disease. Nat Med 10:510-7
43. Merad M, Manz MG, Karsunky H, Wagers A, Peters W, Charo I et al. (2002) Langerhans cells renew in the skin throughout life under steady-state conditions. Nat Immunol 3:1135-41
44. Meunier L, Gonzalez-Ramos A, Cooper KD (1993) 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 151:4067-80
45. Mommaas M, Mulder A, Vermeer BJ, Koning F (1994) Functional human epidermal Langerhans cells that lack Birbeck granules. J Invest Dermatol 103:807-10
46. Morelli AE, Rubin JP, Erdos G, Tkacheva OA, Mathers AR, Zahorchak AF et al. (2005) CD4+ T cell responses elicited by different subsets of human skin migratory dendritic cells. J Immunol 175:7905-15
47. Naik SH, Sathe P, Park HY, Metcalf D, Proietto AI, Dakic A et al. (2007) Development of plasmacytoid and conventional dendritic cell subtypes from single precursor cells derived in vitro and in vivo. Nat Immunol 8:1217-26
48. Nestle FO, Conrad C, Tun-Kyi A, Homey B, Gombert M, Boyman O et al. (2005) Plasmacytoid predendritic cells initiate psoriasis through interferon-alpha production. J Exp Med 202:135-43
49. Nestle FO, Filgueira L, Nickoloff BJ, Burg G (1998) Human dermal dendritic cells process and present soluble protein antigens. J Invest Dermatol 110:762-6
50. Nestle FO, Gilliet M (2005) Defining upstream elements of psoriasis pathogenesis: an emerging role for interferon alpha. J Invest Dermatol 125:xiv-v
51. Nestle FO, Nickoloff BJ (2005) From classical mouse models of psoriasis to a spontaneous xenograft model featuring use of AGR mice. Ernst Schering Res Found Workshop 50:203-12
52. Nestle FO, Turka LA, Nickoloff BJ (1994) Characterization of dermal dendritic cells in psoriasis. Autostimulation of T lymphocytes and induction of Th1 type cytokines. J Clin Invest 94:202-9
53. Nestle FO, Zheng XG, Thompson CB, Turka LA, Nickoloff BJ (1993) Characterization of dermal dendritic cells obtained from normal human skin reveals phenotypic and functionally distinctive subsets. J Immunol 151:6535-45
54. Novak N, Bieber T (2005) The role of dendritic cell subtypes in the pathophysiology of atopic dermatitis. J Am Acad Dermatol 53:S171-6
55. Onai N, Obata-Onai A, Schmid MA, Ohteki T, Jarrossay D, Manz MG (2007) Identification of clonogenic common Flt3+M-CSFR+ plasmacytoid and conventional dendritic cell progenitors in mouse bone marrow. Nat Immunol 8:1207-16
56. Piccioli D, Tavarini S, Borgogni E, Steri V, Nuti S, Sammicheli C et al. (2007) Functional specialization of human circulating CD16 and CD1c myeloid dendritic-cell subsets. Blood 109:5371-9
57. Pope M, Betjes MG, Hirmand H, Hoffman L, Steinman RM (1995) Both dendritic cells and memory T lymphocytes emigrate from organ cultures of human skin and form distinctive dendritic-T-cell conjugates. J Invest Dermatol 104:11-7
58. Poulin LF, Henri S, de Bovis B, Devilard E, Kissenpfennig A, Malissen B (2007) The dermis contains langerin+ dendritic cells that develop and function independently of epidermal Langerhans cells. J Exp Med 204:3119-31
59. Randolph GJ, Sanchez-Schmitz G, Liebman RM, Schakel K (2002) The CD16(+) (FcgammaRIII(+)) subset of human monocytes preferentially becomes migratory dendritic cells in a model tissue setting. J Exp Med 196:517-27
60. Ritter U, Meissner A, Scheidig C, Körner H (2004) CD8 alpha- and Langerin-negative dendritic cells, but not Langerhans cells, act as principal antigen-presenting cells in leishmaniasis. Eur J Immunol 34:1542-50
61. Rothenfusser S, Tuma E, Endres S, Hartmann G (2002) Plasmacytoid dendritic cells: the key to CpG. Hum Immunol 63:1111-9
62. Serbina NV, Salazar-Mather TP, Biron CA, Kuziel WA, Pamer EG (2003) TNF/ iNOS-producing dendritic cells mediate innate immune defense against bacterial infection. Immunity 19:59-70
63. Shortman K, Naik SH (2007) Steady-state and inflammatory dendritic-cell development. Nat Rev Immunol 7:19-30
64. Stary G, Bangert C, Tauber M, Strohal R, Kopp T, Stingl G (2007) Tumoricidal activity of TLR7/8-activated inflammatory dendritic cells. J Exp Med 204:1441-51
65. Steinman RM, Banchereau J (2007) Taking dendritic cells into medicine. Nature 449:419-26
66. Steinman RM, Cohn ZA (1973) Identification of a novel cell type in peripheral lymphoid organs of mice. I. Morphology, quantitation, tissue distribution. J Exp Med 137:1142-62
67. Steinman RM, Nussenzweig MC (2002) Avoiding horror autotoxicus: the importance of dendritic cells in peripheral T cell tolerance. Proc Natl Acad Sci USA 99:351-8
68. Stoitzner P, Holzmann S, McLellan AD, Ivarsson L, Stössel H, Kapp M et al. (2003) Visualization and characterization of migratory Langerhans cells in murine skin and lymph nodes by antibodies against Langerin/CD207. J Invest Dermatol 120:266-74
69. Stoitzner P, Tripp CH, Douillard P, Saeland S, Romani N (2005) Migratory Langerhans cells in mouse lymph nodes in steady state and inflammation. J Invest Dermatol 125:116-25
70. Stössel H, Koch F, Kämpgen E, Stöger P, Lenz A, Heufler C et al. (1990) Disappearance of certain acidic organelles (endosomes and Langerhans cell granules) accompanies loss of antigen processing capacity upon culture of epidermal Langerhans cells. J Exp Med 172:1471-82
71. Strid J, Roberts SJ, Filler RB, Lewis JM, Kwong BY, Schpero W et al. (2008) Acute upregulation of an NKG2D ligand promotes rapid reorganization of a local immune compartment with pleiotropic effects on carcinogenesis. Nat Immunol 9:146-54
72. Svensson M, Kaye PM (2006) Stromal-cell regulation of dendritic-cell differentiation and function. Trends Immunol 27:580-7
73. Tacke F, Randolph GJ (2006) Migratory fate and differentiation of blood monocyte subsets. Immunobiology 211:609-18
74. Tezuka H, Abe Y, Iwata M, Takeuchi H, Ishikawa H, Matsushita M et al. (2007) Regulation of IgA production by naturally occurring TNF/iNOS-producing dendritic cells. Nature 448:929-33
75. Theofilopoulos AN, Baccala R, Beutler B, Kono DH (2005) Type I interferons (alpha/beta) in immunity and autoimmunity. Annu Rev Immunol 23:307-36
76. Thomas JA, Biggerstaff M, Sloane JP, Easton DF (1984) Immunological and histochemical analysis of regional variations of epidermal Langerhans cells in normal human skin. Histochem J 16:507-19
77. Töröcsik D, Bardos H, Nagy L, Adany R (2005) Identification of factor XIII-A as a marker of alternative macrophage activation. Cell Mol Life Sci 62:2132-9
78. Valladeau J, Ravel O, Dezutter-Dambuyant C, Moore K, Kleijmeer M, Liu Y et al. (2000) Langerin, a novel C-type lectin specific to Langerhans cells, is an endocytic receptor that induces the formation of Birbeck granules. Immunity 12:71-81
79. Valladeau J, Saeland S (2005) Cutaneous dendritic cells. Semin Immunol 17:273-83
80. Wollenberg A, Kraft S, Hanau D, Bieber T (1996) 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 106:446-53
81. Wollenberg A, Mommaas M, Oppel T, Schottdorf EM, Gunther S, Moderer M (2002) Expression and function of the mannose receptor CD206 on epidermal dendritic cells in inflammatory skin diseases. J Invest Dermatol 118:327-34
82. Zaba LC, Cardinale I, Gilleaudeau P, Sullivan-Whalen M, Suarez Farinas M, Fuentes-Duculan J et al. (2007a) Amelioration of epidermal hyperplasia by TNF inhibition is associated with reduced Th17 responses. J Exp Med 204:3183-94
83. Zaba LC, Fuentes-Duculan J, Steinman RM, Krueger JG, Lowes MA (2007b) Normal human dermis contains distinct populations of CD11c+BDCA-1+ dendritic cells and CD163+FXIIIA+ macrophages. J Clin Invest 117:2517-25
84. Zaba LC, Fuentes-Duculan J, Eungdamrong NJ, Abello MV, Novitskaya I, Pierson K et al. (2008) Psoriasis is characterized by accumulation of immunostimulatory and Th1/Th17 cell polarizing myeloid dendritic cells. J Invest Dermatol advance online publication, 17 July 2008; doi: 10.1038/jid.2008.194
85. Zhao X, Deak E, Soderberg K, Linehan M, Spezzano D, Zhu J et al. (2003) Vaginal submucosal dendritic cells, but not Langerhans cells, induce protective Th1 responses to herpes simplex virus-2. J Exp Med 197:153-62