Downregulation of Key Early Events in the Mobilization of Antigen-bearing Dendritic Cells by Leukocyte Immunoglobulin-like Receptor B4 in a Mouse Model of Allergic Pulmonary Inflammation

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Fanning, Laura B ^a,b   Buckley, Carolyn C ^a,b   Xing, Wei ^a,b   Breslow, Rebecca G ^a,b   Katz, Howard R ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; CHEMOKINE RECEPTOR; CHEMOKINE RECEPTOR CCL21; CHEMOKINE RECEPTOR CCR7; INTERLEUKIN 4; INTERLEUKIN 5; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR B4; OVALBUMIN; SECONDARY LYMPHOID TISSUE CHEMOKINE; UNCLASSIFIED DRUG;

ALLERGIC PNEUMONITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; CD4+ T LYMPHOCYTE; CELL MIGRATION; CELL MOTILITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; DISEASE ACTIVITY; DISEASE ASSOCIATION; DOWN REGULATION; FEMALE; FLOW CYTOMETRY; IMMUNOHISTOLOGY; LYMPH NODE; MOLECULAR DYNAMICS; MOLECULAR PATHOLOGY; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; SENSITIVITY ANALYSIS; TH2 CELL; UPREGULATION;

ANIMALS; ANTIGEN PRESENTATION; CHEMOKINE CCL21; DENDRITIC CELLS; DISEASE MODELS, ANIMAL; DOWN-REGULATION; FEMALE; INTERLEUKIN-4; INTERLEUKIN-5; LIPOPOLYSACCHARIDES; LUNG; LYMPHOID TISSUE; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; OVALBUMIN; PNEUMONIA; RECEPTORS, CCR7; RECEPTORS, IMMUNOLOGIC; TH2 CELLS;

EID: 84874198037     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0057007     Document Type: Article

References (52)

1. Banchereau J, Briere F, Caux C, Davoust J, Lebecque S, et al. (2000) Immunobiology of dendritic cells. Annu Rev Immunol 18: 767-811.
2. Itano AA, Jenkins MK, (2003) Antigen presentation to naive CD4 T cells in the lymph node. Nat Immunol 4: 733-739.
3. Medoff BD, Thomas SY, Luster AD, (2008) T cell trafficking in allergic asthma: the ins and outs. Annu Rev Immunol 26: 205-232.
4. Martin-Fontecha A, Lanzavecchia A, Sallusto F, (2009) Dendritic cell migration to peripheral lymph nodes. Handb Exp Pharmacol pp. 31-49.
5. van Rijt LS, Prins JB, Leenen PJ, Thielemans K, de Vries VC, et al. (2002) Allergen-induced accumulation of airway dendritic cells is supported by an increase in CD31hiLy-6Cneg bone marrow precursors in a mouse model of asthma. Blood 100: 3663-3671.
6. Vermaelen K, Pauwels R, (2003) Accelerated airway dendritic cell maturation, trafficking, and elimination in a mouse model of asthma. Am J Respir Cell Mol Biol 29: 405-409.
7. Huh JC, Strickland DH, Jahnsen FL, Turner DJ, Thomas JA, et al. (2003) Bidirectional interactions between antigen-bearing respiratory tract dendritic cells (DCs) and T cells precede the late phase reaction in experimental asthma: DC activation occurs in the airway mucosa but not in the lung parenchyma. J Exp Med 198: 19-30.
8. Strickland DH, Stumbles PA, Zosky GR, Subrata LS, Thomas JA, et al. (2006) Reversal of airway hyperresponsiveness by induction of airway mucosal CD4+CD25+ regulatory T cells. J Exp Med 203: 2649-2660.
9. Jahnsen FL, Moloney ED, Hogan T, Upham JW, Burke CM, et al. (2001) Rapid dendritic cell recruitment to the bronchial mucosa of patients with atopic asthma in response to local allergen challenge. Thorax 56: 823-826.
10. Lambrecht BN, Salomon B, Klatzmann D, Pauwels RA, (1998) Dendritic cells are required for the development of chronic eosinophilic airway inflammation in response to inhaled antigen in sensitized mice. J Immunol 160: 4090-4097.
11. van Rijt LS, Jung S, Kleinjan A, Vos N, Willart M, et al. (2005) In vivo depletion of lung CD11c+ dendritic cells during allergen challenge abrogates the characteristic features of asthma. J Exp Med 6: 981-991.
12. Koya T, Kodama T, Takeda K, Miyahara N, Yang ES, et al. (2006) Importance of myeloid dendritic cells in persistent airway disease after repeated allergen exposure. Am J Respir Crit Care Med 173: 42-55.
13. Zhou JS, Friend DS, Feldweg AF, Daheshia M, Li L, et al. (2003) Prevention of lipopolysaccharide-induced microangiopathy by gp49B1: Evidence for an important role for gp49B1 expression on neutrophils. J Exp Med 198: 1243-1251.
14. Zhou JS, Friend DS, Lee DM, Li L, Austen KF, et al. (2005) gp49B1 deficiency is associated with increases in cytokine and chemokine production and severity of proliferative synovitis induced by anti-type II collagen mAbs. Eur J Immunol 35: 1530-1538.
15. Zhou JS, Xing W, Friend DS, Austen KF, Katz HR, (2007) Mast cell deficiency in KitW-sh mice does not impair antibody-mediated arthritis. J Exp Med 204: 2797-2802.
16. Breslow RG, Rao JJ, Xing W, Hong DI, Barrett NA, et al. (2010) Inhibition of Th2 adaptive immune responses and pulmonary inflammation by leukocyte Ig-like receptor B4 on dendritic cells. J Immunol 184: 1003-1013.
17. Eisenbarth SC, Piggott DA, Huleatt JW, Visintin I, Herrick CA, et al. (2002) Lipopolysaccharide-enhanced, Toll-like receptor 4-dependent T helper cell type 2 responses to inhaled antigen. J Exp Med pp. 1645-1651.
18. Alexis NE, Lay JC, Almond M, Peden DB, (2004) Inhalation of low-dose endotoxin favors local T(H)2 response and primes airway phagocytes in vivo. J Allergy Clin Immunol 114: 1325-1331.
19. Schaumann F, Muller M, Braun A, Luettig B, Peden DB, et al. (2008) Endotoxin augments myeloid dendritic cell influx into the airways in patients with allergic asthma. Am J Respir Crit Care Med 177: 1307-1313.
20. von Garnier C, Wikstrom ME, Zosky G, Turner DJ, Sly PD, et al. (2007) Allergic airways disease develops after an increase in allergen capture and processing in the airway mucosa. J Immunol 179: 5748-5759.
21. Gunn MD, Kyuwa S, Tam C, Kakiuchi T, Matsuzawa A, et al. (1999) Mice lacking expression of secondary lymphoid organ chemokine have defects in lymphocyte homing and dendritic cell localization. J Exp Med 189: 451-460.
22. Saeki H, Moore AM, Brown MJ, Hwang ST, (1999) Cutting edge: secondary lymphoid-tissue chemokine (SLC) and CC chemokine receptor 7 (CCR7) participate in the emigration pathway of mature dendritic cells from the skin to regional lymph nodes. J Immunol 162: 2472-2475.
23. Itakura M, Tokuda A, Kimura H, Nagai S, Yoneyama H, et al. (2001) Blockade of secondary lymphoid tissue chemokine exacerbates Propionibacterium acnes-induced acute lung inflammation. J Immunol 166: 2071-2079.
24. Jang MH, Sougawa N, Tanaka T, Hirata T, Hiroi T, et al. (2006) CCR7 is critically important for migration of dendritic cells in intestinal lamina propria to mesenteric lymph nodes. J Immunol 176: 803-810.
25. Britschgi MR, Favre S, Luther SA, (2010) CCL21 is sufficient to mediate DC migration, maturation and function in the absence of CCL19. Eur J Immunol 40: 1266-1271.
26. Vigl B, Aebischer D, Nitschke M, Iolyeva M, Rothlin T, et al. (2011) Tissue inflammation modulates gene expression of lymphatic endothelial cells and dendritic cell migration in a stimulus-dependent manner. Blood 118: 205-215.
27. Tal O, Lim HY, Gurevich I, Milo I, Shipony Z, et al. (2011) DC mobilization from the skin requires docking to immobilized CCL21 on lymphatic endothelium and intralymphatic crawling. J Exp Med 208: 2141-2153.
28. Sugaya M, Fang L, Cardones AR, Kakinuma T, Jaber SH, et al. (2006) Oncostatin M enhances CCL21 expression by microvascular endothelial cells and increases the efficiency of dendritic cell trafficking to lymph nodes. J Immunol 177: 7665-7672.
29. Forster R, Schubel A, Breitfeld D, Kremmer E, Renner-Muller I, et al. (1999) CCR7 coordinates the primary immune response by establishing functional microenvironments in secondary lymphoid organs. Cell 99: 23-33.
30. Martín-Fontecha A, Sebastiani S, Hopken UE, Uguccioni M, Lipp M, et al. (2003) Regulation of dendritic cell migration to the draining lymph node: impact on T lymphocyte traffic and priming. J Exp Med 198: 615-621.
31. 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.
32. Hintzen G, Ohl L, del Rio ML, Rodriguez-Barbosa JI, Pabst O, et al. (2006) Induction of tolerance to innocuous inhaled antigen relies on a CCR7-dependent dendritic cell-mediated antigen transport to the bronchial lymph node. J Immunol 177: 7346-7354.
33. Sozzani S, Allavena P, D'Amico G, Luini W, Bianchi G, et al. (1998) Differential regulation of chemokine receptors during dendritic cell maturation: a model for their trafficking properties. J Immunol 161: 1083-1086.
34. Dieu MC, Vanbervliet B, Vicari A, Bridon JM, Oldham E, et al. (1998) Selective recruitment of immature and mature dendritic cells by distinct chemokines expressed in different anatomic sites. J Exp Med 188: 373-386.
35. Ritter U, Wiede F, Mielenz D, Kiafard Z, Zwirner J, et al. (2004) Analysis of the CCR7 expression on murine bone marrow-derived and spleen dendritic cells. J Leukoc Biol 76: 472-476.
36. Besnard AG, Togbe D, Guillou N, Erard F, Quesniaux V, et al. (2011) IL-33-activated dendritic cells are critical for allergic airway inflammation. Eur J Immunol 41: 1675-1686.
37. Banerji S, Ni J, Wang SX, Clasper S, Su J, et al. (1999) LYVE-1, a new homologue of the CD44 glycoprotein, is a lymph-specific receptor for hyaluronan. J Cell Biol 144: 789-801.
38. Kriehuber E, Breiteneder-Geleff S, Groeger M, Soleiman A, Schoppmann SF, et al. (2001) Isolation and characterization of dermal lymphatic and blood endothelial cells reveal stable and functionally specialized cell lineages. J Exp Med 194: 797-808.
39. Baluk P, Tammela T, Ator E, Lyubynska N, Achen MG, et al. (2005) Pathogenesis of persistent lymphatic vessel hyperplasia in chronic airway inflammation. J Clin Invest 115: 247-257.
40. Schacht V, Ramirez MI, Hong YK, Hirakawa S, Feng D, et al. (2003) T1α/podoplanin deficiency disrupts normal lymphatic vasculature formation and causes lymphedema. EMBO J 22: 3546-3556.
41. Pflicke H, Sixt M, (2009) Preformed portals facilitate dendritic cell entry into afferent lymphatic vessels. J Exp Med 206: 2925-2935.
42. Lo JC, Chin RK, Lee Y, Kang HS, Wang Y, et al. (2003) Differential regulation of CCL21 in lymphoid/nonlymphoid tissues for effectively attracting T cells to peripheral tissues. J Clin Invest 112: 1495-1505.
43. Benedict CA, De Trez C, Schneider K, Ha S, Patterson G, et al. (2006) Specific remodeling of splenic architecture by cytomegalovirus. PLoS Pathog 2: e16.
44. Tomei AA, Siegert S, Britschgi MR, Luther SA, Swartz MA, (2009) Fluid flow regulates stromal cell organization and CCL21 expression in a tissue-engineered lymph node microenvironment. J Immunol 183: 4273-4283.
45. Miteva DO, Rutkowski JM, Dixon JB, Kilarski W, Shields JD, et al. (2010) Transmural flow modulates cell and fluid transport functions of lymphatic endothelium. Circ Res 106: 920-931.
46. Daheshia M, Friend DS, Grusby MJ, Austen KF, Katz HR, (2001) Increased severity of local and systemic anaphylactic reactions in gp49B1-deficient mice. J Exp Med 194: 227-233.
47. Feldweg AF, Friend DS, Zhou JS, Kanaoka Y, Daheshia M, et al. (2003) gp49B1 suppresses stem cell factor-induced mast cell activation-secretion and attendant inflammation in vivo. Eur J Immunol 33: 2262-2268.
48. Besnard AG, Togbe D, Guillou N, Erard F, Quesniaux V, et al. (2011) IL-33-activated dendritic cells are critical for allergic airway inflammation. Eur J Immunol 41: 1675-1686.
49. Ogata M, Zhang Y, Wang Y, Itakura M, Zhang YY, et al. (1999) Chemotactic response toward chemokines and its regulation by transforming growth factor-beta1 of murine bone marrow hematopoietic progenitor cell-derived different subset of dendritic cells. Blood 93: 3225-3232.
50. Morandi F, Ferretti E, Bocca P, Prigione I, Raffaghello L, et al. (2010) A novel mechanism of soluble HLA-G mediated immune modulation: downregulation of T cell chemokine receptor expression and impairment of chemotaxis. PLoS ONE 5: e11763.
51. Morandi F, Ferretti E, Castriconi R, Dondero A, Petretto A, et al. (2011) Soluble HLA-G dampens CD94/NKG2A expression and function and differentially modulates chemotaxis and cytokine/chemokine secretion in CD56bright and CD56dim NK cells. Blood 118: 5840-5850.
52. Chang CC, Liu Z, Vlad G, Qin H, Qiao X, et al. (2009) Ig-like transcript 3 regulates expression of proinflammatory cytokines and migration of activated T cells. J Immunol 182: 5208-5216.