Leishmaniasis, contact hypersensitivity and graft-versus-host disease: Understanding the role of dendritic cell subsets in balancing skin immunity and tolerance

Experimental Dermatology

Volumn 19, Issue 8, 2010, Pages 760-771

  Kautz Neu, Kordula ^a   Meyer, Ralf G ^a   Clausen, Björn E ^b   von Stebut, Esther ^a  

^a UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

^b ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTIVE IMMUNITY; ANTIGEN PRESENTING CELL; ARTICLE; CELL DIFFERENTIATION; CELL INTERACTION; CELL MIGRATION; CONTACT ALLERGY; DENDRITIC CELL; EFFECTOR CELL; GRAFT VERSUS HOST REACTION; HUMAN; IMMUNOLOGICAL TOLERANCE; LANGERHANS CELL; LEISHMANIA MAJOR; NONHUMAN; REGULATORY T LYMPHOCYTE; SKIN LEISHMANIASIS; ULTRAVIOLET RADIATION;

ANIMALS; CELL DIFFERENTIATION; DENDRITIC CELLS; DERMATITIS, CONTACT; DISEASE MODELS, ANIMAL; GRAFT VS HOST DISEASE; HUMANS; IMMUNE SYSTEM; IMMUNE TOLERANCE; LANGERHANS CELLS; LEISHMANIASIS; MICE; SKIN; T-LYMPHOCYTES;

EID: 77954837192     PISSN: 09066705     EISSN: 16000625     Source Type: Journal    
DOI: 10.1111/j.1600-0625.2010.01116.x     Document Type: Article

References (116)

1. Katz S I, Tamaki K, Sachs D H. Epidermal Langerhans cells are derived from cells originating in bone marrow. Nature 1979, 282:324-326.
2. Frelinger J G, Hood L, Hill S, Frelinger J A. Mouse epidermal Ia molecules have a bone marrow origin. Nature 1979, 282:321-323.
3. Banchereau J, Steinman R M. Dendritic cells and the control of immunity. Nature 1998, 392:245-252.
4. Shortman K, Liu Y J. Mouse and human dendritic cell subtypes. Nat Rev Immunol 2002, 2:151-161.
5. Shortman K, Naik S H. Steady-state and inflammatory dendritic-cell development. Nat Rev Immunol 2007, 7:19-30.
6. Henri S, Vremec D, Kamath A. The dendritic cell populations of mouse lymph nodes. J Immunol 2001, 167:741-748.
7. Boonstra A, Asselin-Paturel C, Gilliet M. Flexibility of mouse classical and plasmacytoid-derived dendritic cells in directing T helper type 1 and 2 cell development: dependency on antigen dose and differential toll-like receptor ligation. J Exp Med 2003, 197:101-109.
8. Takeda K, Akira S. TLR signaling pathways. Semin Immunol 2004, 16:3-9.
9. Geijtenbeek T B, van Vliet S J, Engering A, 't Hart B A, van Kooyk Y. Self- and nonself-recognition by C-type lectins on dendritic cells. Annu Rev Immunol 2004, 22:33-54.
10. Asselin-Paturel C, Boonstra A, Dalod M. Mouse type I IFN-producing cells are immature APCs with plasmacytoid morphology. Nat Immunol 2001, 2:1144-1150.
11. Wu L, Dakic A. Development of dendritic cell system. Cell Mol Immunol 2004, 1:112-118.
12. Schuler G, Steinman R M. Murine epidermal Langerhans cells mature into potent immunostimulatory dendritic cells in vitro. J Exp Med 1985, 161:526-546.
13. Romani N, Holzmann S, Tripp C H, Koch F, Stoitzner P. Langerhans cells - dendritic cells of the epidermis. APMIS 2003, 111:725-740.
14. Valladeau J, Clair-Moninot V, Dezutter-Dambuyant C. Identification of mouse langerin/CD207 in Langerhans cells and some dendritic cells of lymphoid tissues. J Immunol 2002, 168:782-792.
15. Takahara K, Omatsu Y, Yashima Y. Identification and expression of mouse Langerin (CD207) in dendritic cells. Int Immunol 2002, 14:433-444.
16. Kissenpfennig A, Henri S, Dubois B. Dynamics and function of Langerhans cells in vivo: dermal dendritic cells colonize lymph node areas distinct from slower migrating Langerhans cells. Immunity 2005, 22:643-654.
17. Douillard P, Stoitzner P, Tripp C H. Mouse lymphoid tissue contains distinct subsets of langerin/CD207 dendritic cells, only one of which represents epidermal-derived Langerhans cells. J Invest Dermatol 2005, 125:983-994.
18. Ginhoux F, Collin M P, Bogunovic M. Blood-derived dermal langerin+ dendritic cells survey the skin in the steady state. J Exp Med 2007, 204:3133-3146.
19. Bursch L S, Wang L, Igyarto B. Identification of a novel population of Langerin+ dendritic cells. J Exp Med 2007, 204:3147-3156.
20. 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.
21. Henri S, Poulin L F, Tamoutounour S. CD207+ CD103+ dermal dendritic cells cross-present keratinocyte-derived antigens irrespective of the presence of Langerhans cells. J Exp Med 2010, 207:189-206.
22. Kaplan D H, Kissenpfennig A, Clausen B E. Insights into Langerhans cell function from Langerhans cell ablation models. Eur J Immunol 2008, 38:2369-2376.
23. Nagao K, Ginhoux F, Leitner W W. Murine epidermal Langerhans cells and langerin-expressing dermal dendritic cells are unrelated and exhibit distinct functions. Proc Natl Acad Sci U S A 2009, 106:3312-3317.
24. Ritter U, Meissner A, Scheidig C, Korner H. CD8 alpha- and Langerin-negative dendritic cells, but not Langerhans cells, act as principal antigen-presenting cells in leishmaniasis. Eur J Immunol 2004, 34:1542-1550.
25. Misslitz A C, Bonhagen K, Harbecke D, Lippuner C, Kamradt T, Aebischer T. Two waves of antigen-containing dendritic cells in vivo in experimental Leishmania major infection. Eur J Immunol 2004, 34:715-725.
26. Itano A A, McSorley S J, Reinhardt R L. Distinct dendritic cell populations sequentially present antigen to CD4 T cells and stimulate different aspects of cell-mediated immunity. Immunity 2003, 19:47-57.
27. Allan R S, Waithman J, Bedoui S. Migratory dendritic cells transfer antigen to a lymph node-resident dendritic cell population for efficient CTL priming. Immunity 2006, 25:153-162.
28. He Y, Zhang J, Donahue C, Falo L D. Skin-derived dendritic cells induce potent CD8(+) T cell immunity in recombinant lentivector-mediated genetic immunization. Immunity 2006, 24:643-656.
29. Cunningham A L, Carbone F, Geijtenbeek T B. Langerhans cells and viral immunity. Eur J Immunol 2008, 38:2377-2385.
30. Martin P, Ruiz S R, del Hoyo G M. Dramatic increase in lymph node dendritic cell number during infection by the mouse mammary tumor virus occurs by a CD62L-dependent blood-borne DC recruitment. Blood 2002, 99:1282-1288.
31. 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.
32. Leon B, Ardavin C. Monocyte migration to inflamed skin and lymph nodes is differentially controlled by L-selectin and PSGL-1. Blood 2008, 111:3126-3130.
33. Leon B, Ardavin C. Monocyte-derived dendritic cells in innate and adaptive immunity. Immunol Cell Biol 2008, 86:320-324.
34. Leon B, Lopez-Bravo M, Ardavin C. Monocyte-derived dendritic cells formed at the infection site control the induction of protective T helper 1 responses against Leishmania. Immunity 2007, 26:519-531.
35. Haniffa M, Ginhoux F, Wang X N. Differential rates of replacement of human dermal dendritic cells and macrophages during hematopoietic stem cell transplantation. J Exp Med 2009, 206:371-385.
36. O'Kane C J, Moffat K G. Selective cell ablation and genetic surgery. Curr Opin Genet Dev 1992, 2:602-607.
37. Saito M, Iwawaki T, Taya C. Diphtheria toxin receptor-mediated conditional and targeted cell ablation in transgenic mice. Nat Biotechnol 2001, 19:746-750.
38. Naglich J G, Metherall J E, Russell D W, Eidels L. Expression cloning of a diphtheria toxin receptor: identity with a heparin-binding EGF-like growth factor precursor. Cell 1992, 69:1051-1061.
39. Collier R J. Understanding the mode of action of diphtheria toxin: a perspective on progress during the 20th century. Toxicon 2001, 39:1793-1803.
40. Honjo T, Nishizuka Y, Kato I, Hayaishi O. Adenosine diphosphate ribosylation of aminoacyl transferase II and inhibition of protein synthesis by diphtheria toxin. J Biol Chem 1971, 246:4251-4260.
41. Buch T, Heppner F L, Tertilt C. A Cre-inducible diphtheria toxin receptor mediates cell lineage ablation after toxin administration. Nat Methods 2005, 2:419-426.
42. Breitman M L, Clapoff S, Rossant J. Genetic ablation: targeted expression of a toxin gene causes microphthalmia in transgenic mice. Science 1987, 238:1563-1565.
43. Palmiter R D, Behringer R R, Quaife C J, Maxwell F, Maxwell I H, Brinster R L. Cell lineage ablation in transgenic mice by cell-specific expression of a toxin gene. Cell 1987, 50:435-443.
44. Jung S, Unutmaz D, Wong P. In vivo depletion of CD11c(+) dendritic cells abrogates priming of CD8(+) T cells by exogenous cell-associated antigens. Immunity 2002, 17:211-220.
45. Bennett C L, Clausen B E. DC ablation in mice: promises, pitfalls, and challenges. Trends Immunol 2007, 28:525-531.
46. Probst H C, Tschannen K, Odermatt B, Schwendener R, Zinkernagel R M, Van Den B M. Histological analysis of CD11c-DTR/GFP mice after in vivo depletion of dendritic cells. Clin Exp Immunol 2005, 141:398-404.
47. Bennett C L, van Rijn E, Jung S. Inducible ablation of mouse Langerhans cells diminishes but fails to abrogate contact hypersensitivity. J Cell Biol 2005, 169:569-576.
48. 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.
49. Merad M, Manz M G, Karsunky H. Langerhans cells renew in the skin throughout life under steady-state conditions. Nat Immunol 2002, 3:1135-1141.
50. Peters N C, Egen J G, Secundino N. In vivo imaging reveals an essential role for neutrophils in leishmaniasis transmitted by sand flies. Science 2008, 321:970-974.
51. van Zandbergen G, Klinger M, Mueller A. Cutting edge: neutrophil granulocyte serves as a vector for Leishmania entry into macrophages. J Immunol 2004, 173:6521-6525.
52. Ng L G, Hsu A, Mandell M A. Migratory dermal dendritic cells act as rapid sensors of protozoan parasites. PLoS Pathog 2008, 4:e1000222.
53. McConville M J, de Souza D, Saunders E, Likic V A, Naderer T. Living in a phagolysosome; metabolism of Leishmania amastigotes. Trends Parasitol 2007, 23:368-375.
54. Scott P, Artis D, Uzonna J, Zaph C. The development of effector and memory T cells in cutaneous leishmaniasis: the implications for vaccine development. Immunol Rev 2004, 201:318-338.
55. Sacks D, Noben-Trauth N. The immunology of susceptibility and resistance to Leishmania major in mice. Nat Rev Immunol 2002, 2:845-858.
56. Reiner S L, Locksley R M. The regulation of immunity to Leishmania major. Annu Rev Immunol 1995, 13:151-177.
57. De Trez C, Magez S, Akira S, Ryffel B, Carlier Y, Muraille E. iNOS-producing inflammatory dendritic cells constitute the major infected cell type during the chronic Leishmania major infection phase of C57BL/6 resistant mice. PLoS Pathog 2009, 5:e1000494.
58. Belkaid Y, Mendez S, Lira R, Kadambi N, Milon G, Sacks D. A natural model of Leishmania major infection reveals a prolonged " silent" phase of parasite amplification in the skin before the onset of lesion formation and immunity. J Immunol 2000, 165:969-977.
59. Woelbing F, Kostka S L, Moelle K. Uptake of Leishmania major by dendritic cells is mediated by Fcgamma receptors and facilitates acquisition of protective immunity. J Exp Med 2006, 203:177-188.
60. Belkaid Y, Von Stebut E, Mendez S. CD8+ T cells are required for primary immunity in C57BL/6 mice following low-dose, intradermal challenge with Leishmania major. J Immunol 2002, 168:3992-4000.
61. Moll H. The role of dendritic cells at the early stages of Leishmania infection. Adv Exp Med Biol 2000, 479:163-173.
62. Moll H, Fuchs H, Blank C, Rollinghoff M. Langerhans cells transport Leishmania major from the infected skin to the draining lymph node for presentation to antigen-specific T cells. Eur J Immunol 1993, 23:1595-1601.
63. Von Stebut E, Belkaid Y, Nguyen B V, Cushing M, Sacks D L, Udey M C. Leishmania major-infected murine langerhans cell-like dendritic cells from susceptible mice release IL-12 after infection and vaccinate against experimental cutaneous Leishmaniasis. Eur J Immunol 2000, 30:3498-3506.
64. Bottrel R L, Dutra W O, Martins F A. Flow cytometric determination of cellular sources and frequencies of key cytokine-producing lymphocytes directed against recombinant LACK and soluble Leishmania antigen in human cutaneous leishmaniasis. Infect Immun 2001, 69:3232-3239.
65. Bourreau E, Gardon J, Pradinaud R. Th2 responses predominate during the early phases of infection in patients with localized cutaneous leishmaniasis and precede the development of Th1 responses. Infect Immun 2003, 71:2244-2246.
66. Kolde G, Luger T, Sorg C, Sunderkotter C. Successful treatment of cutaneous leishmaniasis using systemic interferon-gamma. Dermatology 1996, 192:56-60.
67. Geiger B, Wenzel J, Hantschke M, Haase I, Stander S, Von Stebut E. Resolving lesions in human cutaneous leishmaniasis predominantly harbour chemokine receptor CXCR3-positive T helper 1/T cytotoxic type 1 cells. Br J Dermatol 2009
68. Modlin R L. Th1-Th2 paradigm: insights from leprosy. J Invest Dermatol 1994, 102:828-832.
69. Dubsky P, Ueno H, Piqueras B, Connolly J, Banchereau J, Palucka A K. Human dendritic cell subsets for vaccination. J Clin Immunol 2005, 25:551-572.
70. Von Stebut E, Belkaid Y, Jakob T, Sacks D L, Udey M C. Uptake of Leishmania major amastigotes results in activation and interleukin 12 release from murine skin-derived dendritic cells: implications for the initiation of anti-Leishmania immunity. J Exp Med 1998, 188:1547-1552.
71. Baldwin T, Henri S, Curtis J. Dendritic cell populations in Leishmania major-infected skin and draining lymph nodes. Infect Immun 2004, 72:1991-2001.
72. Ritter U, Osterloh A. A new view on cutaneous dendritic cell subsets in experimental leishmaniasis. Med Microbiol Immunol (Berl) 2007, 196:51-59.
73. Iezzi G, Frohlich A, Ernst B. Lymph node resident rather than skin-derived dendritic cells initiate specific T cell responses after Leishmania major infection. J Immunol 2006, 177:1250-1256.
74. Liu Y J. IPC: professional type 1 interferon-producing cells and plasmacytoid dendritic cell precursors. Annu Rev Immunol 2005, 23:275-306.
75. McKenna K, Beignon A S, Bhardwaj N. Plasmacytoid dendritic cells: linking innate and adaptive immunity. J Virol 2005, 79:17-27.
76. Remer K A, Apetrei C, Schwarz T, Linden C, Moll H. Vaccination with plasmacytoid dendritic cells induces protection against infection with Leishmania major in mice. Eur J Immunol 2007, 37:2463-2473.
77. Saint-Mezard P, Berard F, Dubois B, Kaiserlian D, Nicolas J F. The role of CD4+ and CD8+ T cells in contact hypersensitivity and allergic contact dermatitis. Eur J Dermatol 2004, 14:131-138.
78. Martin S F, Jakob T. From innate to adaptive immune responses in contact hypersensitivity. Curr Opin Allergy Clin Immunol 2008, 8:289-293.
79. Bennett C L, Noordegraaf M, Martina C A, Clausen B E. Langerhans cells are required for efficient presentation of topically applied hapten to T cells. J Immunol 2007, 179:6830-6835.
80. Fukunaga A, Khaskhely N M, Sreevidya C S, Byrne S N, Ullrich S E. Dermal dendritic cells, and not Langerhans cells, play an essential role in inducing an immune response. J Immunol 2008, 180:3057-3064.
81. Noordegraaf M, Flacher V, Stoitzner P, Clausen B E. Functional redundancy of Langerhans cells and Langerin+ dermal dendritic cells in contact hypersensitivity. 2010, in press
82. Clausen B E, Kel J M. Langerhans cells: critical regulators of skin immunity? Immunol Cell Biol. 2010, 88(4):351-60. May
83. 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.
84. Bedoui S, Whitney P G, Waithman J. Cross-presentation of viral and self antigens by skin-derived CD103+ dendritic cells. Nat Immunol 2009, 10:488-495.
85. Toews G B, Bergstresser P R, Streilein J W. Epidermal Langerhans cell density determines whether contact hypersensitivity or unresponsiveness follows skin painting with DNFB. J Immunol 1980, 124:445-453.
86. Elmets C A, Bergstresser P R, Tigelaar R E, Wood P J, Streilein J W. Analysis of the mechanism of unresponsiveness produced by haptens painted on skin exposed to low dose ultraviolet radiation. J Exp Med 1983, 158:781-794.
87. Schwarz A, Maeda A, Wild M K. Ultraviolet radiation-induced regulatory T cells not only inhibit the induction but can suppress the effector phase of contact hypersensitivity. J Immunol 2004, 172:1036-1043.
88. Schwarz T. 25 years of UV-induced immunosuppression mediated by T cells-from disregarded T suppressor cells to highly respected regulatory T cells. Photochem Photobiol 2008, 84:10-18.
89. Schwarz A, Maeda A, Kernebeck K, van Steeg H, Beissert S, Schwarz T. Prevention of UV radiation-induced immunosuppression by IL-12 is dependent on DNA repair. J Exp Med 2005, 201:173-179.
90. Loser K, Mehling A, Loeser S. Epidermal RANKL controls regulatory T-cell numbers via activation of dendritic cells. Nat Med 2006, 12:1372-1379.
91. Wong B R, Josien R, Lee S Y. TRANCE (tumor necrosis factor [TNF]-related activation-induced cytokine), a new TNF family member predominantly expressed in T cells, is a dendritic cell-specific survival factor. J Exp Med 1997, 186:2075-2080.
92. Schwarz A, Noordegraaf M, Maeda A, Torii K, Clausen B E, Schwarz T. Langerhans Cells Are Required for UVR-Induced Immunosuppression. J Invest Dermatol 2010, 130(5):1419-1427. May
93. Wang L, Jameson S C, Hogquist K A. Epidermal Langerhans cells are not required for UV-induced immunosuppression. J Immunol 2009, 183:5548-5553.
94. Aberer W, Schuler G, Stingl G, Honigsmann H, Wolff K. Ultraviolet light depletes surface markers of Langerhans cells. J Invest Dermatol 1981, 76:202-210.
95. Kolgen W, van Steeg H, van der Horst G T. Association of transcription-coupled repair but not global genome repair with ultraviolet-B-induced Langerhans cell depletion and local immunosuppression. J Invest Dermatol 2003, 121:751-756.
96. Appelbaum F R. Haematopoietic cell transplantation as immunotherapy. Nature 2001, 411:385-389.
97. Kolb H J. Graft-versus-leukemia effects of transplantation and donor lymphocytes. Blood 2008, 112:4371-4383.
98. Korngold R, Sprent J. Lethal graft-versus-host disease after bone marrow transplantation across minor histocompatibility barriers in mice. Prevention by removing mature T cells from marrow. J Exp Med 1978, 148:1687-1698.
99. Ferrara J L, Yanik G. Acute graft versus host disease: pathophysiology, risk factors, and prevention strategies. Clin Adv Hematol Oncol 2005, 3:415-419. 428
100. Sun Y, Tawara I, Toubai T, Reddy P. Pathophysiology of acute graft-versus-host disease: recent advances. Transl Res 2007, 150:197-214.
101. Hill G R, Crawford J M, Cooke K R, Brinson Y S, Pan L, Ferrara J L. Total body irradiation and acute graft-versus-host disease: the role of gastrointestinal damage and inflammatory cytokines. Blood 1997, 90:3204-3213.
102. Shlomchik W D, Couzens M S, Tang C B. Prevention of graft versus host disease by inactivation of host antigen-presenting cells. Science 1999, 285:412-415.
103. Ruggeri L, Capanni M, Urbani E. Effectiveness of donor natural killer cell alloreactivity in mismatched hematopoietic transplants. Science 2002, 295:2097-2100.
104. Matte C C, Liu J, Cormier J. Donor APCs are required for maximal GVHD but not for GVL. Nat Med 2004, 10:987-992.
105. Beilhack A, Schulz S, Baker J. Prevention of acute graft-versus-host disease by blocking T-cell entry to secondary lymphoid organs. Blood 2008, 111:2919-2928.
106. Auffermann-Gretzinger S, Lossos I S, Vayntrub T A. Rapid establishment of dendritic cell chimerism in allogeneic hematopoietic cell transplant recipients. Blood 2002, 99:1442-1448.
107. Perreault C, Pelletier M, Belanger R. Persistence of host Langerhans cells following allogeneic bone marrow transplantation: possible relationship with acute graft-versus-host disease. Br J Haematol 1985, 60:253-260.
108. Suitters A J, Lampert I A. The loss of Ia+ Langerhans' cells during graft-versus-host disease in rats. Transplantation 1983, 36:540-546.
109. Merad M, Hoffmann P, Ranheim E. Depletion of host Langerhans cells before transplantation of donor alloreactive T cells prevents skin graft-versus-host disease. Nat Med 2004, 10:510-517.
110. Collin M P, Hart D N, Jackson G H. The fate of human Langerhans cells in hematopoietic stem cell transplantation. J Exp Med 2006, 203:27-33.
111. Meyer R G, Britten C M, Wehler D. Prophylactic transfer of CD8-depleted donor lymphocytes after T-cell-depleted reduced-intensity transplantation. Blood 2007, 109:374-382.
112. Obhrai J S, Oberbarnscheidt M, Zhang N. Langerhans cells are not required for efficient skin graft rejection. J Invest Dermatol 2008, 128:1950-1955.
113. Nakano H, Yanagita M, Gunn M D. CD11c(+)B220(+)Gr-1(+) cells in mouse lymph nodes and spleen display characteristics of plasmacytoid dendritic cells. J Exp Med 2001, 194:1171-1178.
114. Brewig N, Kissenpfennig A, Malissen B. Priming of CD8+ and CD4+ T cells in experimental leishmaniasis is initiated by different dendritic cell subtypes. J Immunol 2009, 182:774-783.
115. Lopez-Bravo M, Ardavin C. In vivo induction of immune responses to pathogens by conventional dendritic cells. Immunity 2008, 29:343-351.
116. Zaba L C, Krueger J G, Lowes M A. Resident and " inflammatory" dendritic cells in human skin. J Invest Dermatol 2009, 129:302-308.