MGL2+ dermal dendritic cells are sufficient to initiate contact hypersensitivity in vivo

PLoS ONE

Volumn 4, Issue 5, 2009, Pages

  Kumamoto, Yosuke ^a,b   Denda Nagai, Kaori ^a   Aida, Satoshi ^a   Higashi, Nobuaki ^a   Irimura, Tatsuro ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; CD45 ANTIGEN; CD8ALPHA ANTIGEN; FLUORESCEIN ISOTHIOCYANATE; GLYCOPROTEIN P 15095; LECTIN; MACROPHAGE GALACTOSE C TYPE LECTIN 2; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; UNCLASSIFIED DRUG; ASIALOGLYCOPROTEIN; CD8 ANTIGEN; CELL SURFACE RECEPTOR; DEC 205 RECEPTOR; DEC-205 RECEPTOR; LEUKOCYTE ANTIGEN; MEMBRANE PROTEIN; MGL1 PROTEIN, MOUSE; MGL2 PROTEIN, MOUSE;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTATION; ARTICLE; CELL FUNCTION; CELL SPECIFICITY; CONTACT ALLERGY; CONTROLLED STUDY; DENDRITIC CELL; EAR DISEASE; EDEMA; FEMALE; IMMUNE RESPONSE; IMMUNE SYSTEM; IMMUNOPATHOGENESIS; IN VIVO STUDY; LANGERHANS CELL; LYMPH NODE; MALE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; SKIN CELL; SKIN SENSITIZATION; VENULE; ANIMAL; BAGG ALBINO MOUSE; CELL MOTION; CONTACT DERMATITIS; FLOW CYTOMETRY; IMMUNOLOGY; METABOLISM; PHYSIOLOGY; SKIN;

MAMMALIA; MUS;

ANIMALS; ANTIGENS, CD; ANTIGENS, CD11B; ANTIGENS, CD11C; ANTIGENS, CD8; ASIALOGLYCOPROTEINS; CELL MOVEMENT; DERMATITIS, CONTACT; FLOW CYTOMETRY; LANGERHANS CELLS; LECTINS, C-TYPE; MEMBRANE PROTEINS; MICE; MICE, INBRED BALB C; RECEPTORS, CELL SURFACE; SKIN;

EID: 66149111441     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0005619     Document Type: Article

References (55)

1. Stoitzner P, Holzmann S, McLellan AD, Ivarsson L, Stossel H, 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: 266-274.
2. Kissenpfennig A, Ait-Yahia S, Clair-Moninot V, Stossel H, Badell E, et al. (2005) Disruption of the langerin/CD207 gene abolishes Birbeck granules without a marked loss of Langerhans cell function. Mol Cell Biol 25: 88-99.
3. Valladeau J, Clair-Moninot V, Dezutter-Dambuyant C, Pin JJ, Kissenpfennig A, et al. (2002) Identification of mouse langerin/CD207 in Langerhans cells and some dendritic cells of lymphoid tissues. J Immunol 168: 782-792.
4. 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: 2587-2596.
5. Randolph GJ, Angeli V, Swartz MA (2005) Dendritic-cell trafficking to lymph nodes through lymphatic vessels. Nat Rev Immunol 5: 617-628.
6. Itano AA, Jenkins MK (2003) Antigen presentation to naive CD4 T cells in the lymph node. Nat Immunol 4: 733-739.
7. Anjuere F, Martin P, Ferrero I, Fraga ML, del Hoyo GM, et al. (1999) Definition of dendritic cell subpopulations present in the spleen, Peyer's patches, lymph nodes, and skin of the mouse. Blood 93: 590-598.
8. Asselin-Paturel C, Brizard G, Pin JJ, Briere F, Trinchieri G (2003) Mouse strain differences in plasmacytoid dendritic cell frequency and function revealed by a novel monoclonal antibody. J Immunol 171: 6466-6477.
9. Ruedl C, Koebel P, Bachmann M, Hess M, Karjalainen K (2000) Anatomical origin of dendritic cells determines their life span in peripheral lymph nodes. J Immunol 165: 4910-4916.
10. Henri S, Vremec D, Kamath A, Waithman J, Williams S, et al. (2001) The dendritic cell populations of mouse lymph nodes. J Immunol 167: 741-748.
11. Itano AA, McSorley SJ, Reinhardt RL, Ehst BD, Ingulli E, et al. (2003) Distinct dendritic cell populations sequentially present antigen to CD4 T cells and stimulate different aspects of cell-mediated immunity. Immunity 19: 47-57.
12. Kissenpfennig A, Henri S, Dubois B, Laplace-Builhe C, Perrin P, et al. (2005) Dynamics and function of Langerhans cells in vivo: dermal dendritic cells colonize lymph node areas distinct from slower migrating Langerhans cells. Immunity 22: 643-654.
13. Vremec D, Shortman K (1997) Dendritic cell subtypes in mouse lymphoid organs: cross-correlation of surface markers, changes with incubation, and differences among thymus, spleen, and lymph nodes. J Immunol 159: 565-573.
14. Kamath AT, Henri S, Battye F, Tough DF, Shortman K (2002) Developmental kinetics and lifespan of dendritic cells in mouse lymphoid organs. Blood 100: 1734-1741.
15. Macatonia SE, Knight SC, Edwards AJ, Griffiths S, Fryer P (1987) Localization of antigen on lymph node dendritic cells after exposure to the contact sensitizer fluorescein isothiocyanate. Functional and morphological studies. J Exp Med 166: 1654-1667.
16. Kripke ML, Munn CG, Jeevan A, Tang JM, Bucana C (1990) Evidence that cutaneous antigen-presenting cells migrate to regional lymph nodes during contact sensitization. J Immunol 145: 2833-2838.
17. Bennett CL, van Rijn E, Jung S, Inaba K, Steinman RM, et al. (2005) Inducible ablation of mouse Langerhans cells diminishes but fails to abrogate contact hypersensitivity. J Cell Biol 169: 569-576.
18. Kaplan DH, Jenison MC, Saeland S, Shlomchik WD, Shlomchik MJ (2005) Epidermal langerhans cell-deficient mice develop enhanced contact hypersensitivity. Immunity 23: 611-620.
19. Bursch LS, Wang L, Igyarto B, Kissenpfennig A, Malissen B, et al. (2007) Identification of a novel population of Langerin+ dendritic cells. J Exp Med.
20. Ginhoux F, Collin MP, Bogunovic M, Abel M, Leboeuf M, et al. (2007) Blood-derived dermal langerin+ dendritic cells survey the skin in the steady state. J Exp Med.
21. Poulin LF, Henri S, de Bovis B, Devilard E, Kissenpfennig A, et al. (2007) The dermis contains langerin+ dendritic cells that develop and function independently of epidermal Langerhans cells. J Exp Med.
22. Allan RS, Waithman J, Bedoui S, Jones CM, Villadangos JA, et al. (2006) Migratory Dendritic Cells Transfer Antigen to a Lymph Node-Resident Dendritic Cell Population for Efficient CTL Priming. Immunity 25: 153-162.
23. Mizuochi S, Akimoto Y, Imai Y, Hirano H, Irimura T (1997) Unique tissue distribution of a mouse macrophage C-type lectin. Glycobiology 7: 137-146.
24. Denda-Nagai K, Kubota N, Tsuiji M, Kamata M, Irimura T (2002) Macrophage C-type lectin on bone marrow-derived immature dendritic cells is involved in the internalization of glycosylated antigens. Glycobiology 12: 443-450.
25. Sato K, Imai Y, Irimura T (1998) Contribution of dermal macrophage trafficking in the sensitization phase of contact hypersensitivity. J Immunol 161: 6835-6844.
26. Tsuiji M, Fujimori M, Ohashi Y, Higashi N, Onami TM, et al. (2002) Molecular cloning and characterization of a novel mouse macrophage C-type lectin, mMGL2, which has a distinct carbohydrate specificity from mMGL1. J Biol Chem 277: 28892-28901.
27. Onami TM, Lin MY, Page DM, Reynolds SA, Katayama CD, et al. (2002) Generation of mice deficient for macrophage galactose- and N-acetylgalactosamine-specific lectin: limited role in lymphoid and erythroid homeostasis and evidence for multiple lectins. Mol Cell Biol 22: 5173-5181.
28. Dupasquier M, Stoitzner P, Wan H, Cerqueira D, van Oudenaren A, et al. (2006) The dermal microenvironment induces the expression of the alternative activation marker CD301/mMGL in mononuclear phagocytes, independent of IL-4/IL-13 signaling. J Leukoc Biol 80: 838-849.
29. Kimura T, Imai Y, Irimura T (1995) Calcium-dependent conformation of a mouse macrophage calcium-type lectin. Carbohydrate binding activity is stabilized by an antibody specific for a calcium-dependent epitope. J Biol Chem 270: 16056-16062.
30. Sato K, Imai Y, Higashi N, Kumamoto Y, Onami TM, et al. (2005) Lack of antigen-specific tissue remodeling in mice deficient in the macrophage galactose-type calcium-type lectin 1/CD301a. Blood 106: 207-215.
31. Gray DH, Chidgey AP, Boyd RL (2002) Analysis of thymic stromal cell populations using flow cytometry. J Immunol Methods 260: 15-28.
32. Bogunovic M, Ginhoux F, Wagers A, Loubeau M, Isola LM, et al. (2006) Identification of a radio-resistant and cycling dermal dendritic cell population in mice and men. J Exp Med 203: 2627-2638.
33. Sato K, Imai Y, Higashi N, Kumamoto Y, Mukaida N, et al. (2005) Redistributions of macrophages expressing the macrophage galactose-type Ctype lectin (MGL) during antigen-induced chronic granulation tissue formation. Int Immunol 17: 559-568.
34. Nakano H, Yanagita M, Gunn MD (2001) CD11c(+)B220(+)Gr-1(+) cells in mouse lymph nodes and spleen display characteristics of plasmacytoid dendritic cells. J Exp Med 194: 1171-1178.
35. Ohl L, Mohaupt M, Czeloth N, Hintzen G, Kiafard Z, et al. (2004) CCR7 governs skin dendritic cell migration under inflammatory and steady-state conditions. Immunity 21: 279-288.
36. Leon B, Ardavin C (2008) Monocyte migration to inflamed skin and lymph nodes is differentially controlled by L-selectin and PSGL-1. Blood 111: 3126-3130.
37. Randolph GJ, Beaulieu S, Lebecque S, Steinman RM, Muller WA (1998) Differentiation of monocytes into dendritic cells in a model of transendothelial trafficking. Science 282: 480-483.
38. Randolph GJ, Jakubzick C, Qu C (2008) Antigen presentation by monocytes and monocyte-derived cells. Curr Opin Immunol 20: 52-60.
39. Qu C, Edwards EW, Tacke F, Angeli V, Llodra J, et al. (2004) Role of CCR8 and other chemokine pathways in the migration of monocyte-derived dendritic cells to lymph nodes. J Exp Med 200: 1231-1241.
40. Tacke F, Randolph GJ (2006) Migratory fate and differentiation of blood monocyte subsets. Immunobiology 211: 609-618.
41. Katakai T, Hara T, Lee JH, Gonda H, Sugai M, et al. (2004) A novel reticular stromal structure in lymph node cortex: an immuno-platform for interactions among dendritic cells, T cells and B cells. Int Immunol 16: 1133-1142.
42. Bajenoff M, Granjeaud S, Guerder S (2003) The strategy of T cell antigen-presenting cell encounter in antigen-draining lymph nodes revealed by imaging of initial T cell activation. J Exp Med 198: 715-724.
43. Valladeau J, Ravel O, Dezutter-Dambuyant C, Moore K, Kleijmeer M, 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.
44. Douillard P, Stoitzner P, Tripp CH, Clair-Moninot V, Ait-Yahia S, 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: 983-994.
45. Kabashima K, Shiraishi N, Sugita K, Mori T, Onoue A, et al. (2007) CXCL12-CXCR4 engagement is required for migration of cutaneous dendritic cells. Am J Pathol 171: 1249-1257.
46. Raes G, Brys L, Dahal BK, Brandt J, Grooten J, et al. (2005) Macrophage galactose-type C-type lectins as novel markers for alternatively activated macrophages elicited by parasitic infections and allergic airway inflammation. J Leukoc Biol 77: 321-327.
47. Kimber I, Dearman RJ, Cumberbatch M, Huby RJ (1998) Langerhans cells and chemical allergy. Curr Opin Immunol 10: 614-619.
48. Shelley WB, Juhlin L (1976) Langerhans cells form a reticuloepithelial trap for external contact antigens. Nature 261: 46-47.
49. Silberberg-Sinakin I, Thorbecke GJ, Baer RL, Rosenthal SA, Berezowsky V (1976) Antigen-bearing langerhans cells in skin, dermal lymphatics and in lymph nodes. Cell Immunol 25: 137-151.
50. Toews GB, Bergstresser PR, Streilein JW (1980) Epidermal Langerhans cell density determines whether contact hypersensitivity or unresponsiveness follows skin painting with DNFB. J Immunol 124: 445-453.
51. Tang A, Amagai M, Granger LG, Stanley JR, Udey MC (1993) Adhesion of epidermal Langerhans cells to keratinocytes mediated by E-cadherin. Nature 361: 82-85.
52. Witmer-Pack MD, Swiggard WJ, Mirza A, Inaba K, Steinman RM (1995) Tissue distribution of the DEC-205 protein that is detected by the monoclonal antibody NLDC-145. II. Expression in situ in lymphoid and nonlymphoid tissues. Cell Immunol 163: 157-162.
53. Lindquist RL, Shakhar G, Dudziak D, Wardemann H, Eisenreich T, et al. (2004) Visualizing dendritic cell networks in vivo. Nat Immunol 5: 1243-1250.
54. Ingulli E, Ulman DR, Lucido MM, Jenkins MK (2002) In situ analysis reveals physical interactions between CD11b+ dendritic cells and antigen-specific CD4 T cells after subcutaneous injection of antigen. J Immunol 169: 2247-2252.
55. Bajenoff M, Breart B, Huang AY, Qi H, Cazareth J, et al. (2006) Natural killer cell behavior in lymph nodes revealed by static and real-time imaging. J Exp Med 203: 619-631.