In vivo depletion of lung CD11c+ dendritic cells during allergen challenge abrogates the characteristic features of asthma

Journal of Experimental Medicine

Volumn 201, Issue 6, 2005, Pages 981-991

  Van Rijt, Leonie S ^a   Jung, Steffen ^b   KleinJan, Alex ^a   Vos, Nanda ^a   Willart, Monique ^a   Duez, Catherine ^c   Hoogsteden, Henk C ^a   Lambrecht, Bart N ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^c INSTITUT PASTEUR DE LILLE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ALLERGEN; B7 ANTIGEN; CD40 ANTIGEN; DIPHTHERIA TOXIN; GAMMA INTERFERON; GLYCOPROTEIN P 15095; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 13; INTERLEUKIN 4; INTERLEUKIN 5; OVALBUMIN;

ADOPTIVE TRANSFER; ALLERGIC ASTHMA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN PRESENTING CELL; ARTICLE; BODY PLETHYSMOGRAPHY; BRONCHUS HYPERREACTIVITY; CELL HYPERPLASIA; CONTROLLED STUDY; CYTOKINE RELEASE; DENDRITIC CELL; EOSINOPHILIA; GOBLET CELL; IN VIVO STUDY; LUNG ALVEOLUS MACROPHAGE; LUNG LAVAGE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROVOCATION TEST; RESPIRATORY TRACT INFLAMMATION; T LYMPHOCYTE; TH2 CELL; TRANSGENIC MOUSE;

ADOPTIVE TRANSFER; AEROSOLS; ALLERGENS; ANIMALS; ANTIGENS, CD11C; ASTHMA; CYTOKINES; DENDRITIC CELLS; DIPHTHERIA TOXIN; EOSINOPHILS; INFLAMMATION; LUNG; MACROPHAGES, ALVEOLAR; MICE; MICE, INBRED BALB C; MICE, TRANSGENIC; OVALBUMIN; TH2 CELLS;

EID: 17144367365     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.20042311     Document Type: Article

References (48)

1. Wills-Karp, M. 1999. Immunologic basis of antigen-induced airway hyperresponsiveness. Annu. Rev. Immunol. 17:255-281.
2. Herrick, C.A., and K. Bottomly. 2003. To respond or not to respond: T cells in allergic asthma. Nat. Rev. Immunol. 3:405-412.
3. Holt, P.G., M.A. Schon-Hegrad, and J. Oliver. 1988. MHC class II antigen-bearing dendritic cells in pulmonary tissues of the rat. Regulation of antigen presentation activity by endogenous macrophage populations. J. Exp. Med. 167:262-274.
4. Banchereau, J., and R.M. Steinman. 1998. Dendritic cells and the control of immunity. Nature. 392:245-252.
5. Brimnes, M.K., L. Bonifaz, R.M. Steinman, and T.M. Moran. 2003. Influenza virus-induced dendritic cell maturation is associated with the induction of strong T cell immunity to a coadministered, normally nonimmunogenic protein. J. Exp. Med. 198:133-144.
6. Lambrecht, B.N., R.A. Peleman, G.R. Bullock, and R.A. Pauwels. 2000. Sensitization to inhaled antigen by intratracheal instillation of dendritic cells. Clin. Exp. Allergy. 30:214-224.
7. Vermaelen, K.Y., I. Carro-Muino, B.N. Lambrecht, and R.A. Pauwels. 2001. Specific migratory dendritic cells rapidly transport antigen from the airways to the thoracic lymph nodes. J. Exp. Med. 193:51-60.
8. Lambrecht, B.N., M. De Veerman, A.J. Coyle, J.C. Gutierrez-Ramos, K. Thielemans, and R.A. Pauwels. 2000. Myeloid dendritic cells induce Th2 responses to inhaled antigen, leading to eosinophilic airway inflammation. J. Clin. Invest. 106:551-559.
9. Lambrecht, B.N., R.A. Pauwels, and B. Fazekas De St Groth. 2000. Induction of rapid T cell activation, division, and recirculation by intratracheal injection of dendritic cells in a TCR transgenic model. J. Immunol. 164:2937-2946.
10. Huh, J.C., D.H. Strickland, F.L. Jahnsen, D.J. Turner, J.A. Thomas, S. Napoli, I. Tobagus, P.A. Stumbles, P.D. Sly, and P.G. Holt. 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.
11. Vermaelen, K., and R. Pauwels. 2003. Accelerated airway dendritic cell maturation, trafficking, and elimination in a mouse model of asthma. Am. J. Respir. Cell Mol. Biol. 29:405-409.
12. Lambrecht, B.N., and H. Hammad. 2003. Taking our breath away: dendritic cells in the pathogenesis of asthma. Nat. Rev. Immunol. 3:994-1003.
13. Stampfli, M.R., R.E. Wiley, G.S. Neigh, B.U. Gajewska, X.F. Lei, D.P. Snider, Z. Xing, and M. Jordana. 1998. GM-CSF transgene expression in the airway allows aerosolized ovalbumin to induce allergic sensitization in mice. J. Clin. Invest. 102:1704-1714.
14. Eisenbarth, S.C., D.A. Piggott, J.W. Huleatt, I. Visintin, C.A. Herrick, and K. Bottomly. 2002. Lipopolysaccharide-enhanced, toll-like receptor 4-dependent T helper cell type 2 responses to inhaled antigen. J. Exp. Med. 196:1645-1651.
15. Jahnsen, F.L., E.D. Moloney, T. Hogan, J.W. Upham, C.M. Burke, and P.G. Holt. 2001. Rapid dendritic cell recruitment to the bronchial mucosa of patients with atopic asthma in response to local allergen challenge. Thorax. 56:823-826.
16. Moller, G.M., S.E. Overbeek, G.G. Van Helden-Meeuwsen, J.M. Van Haarst, E.P. Prens, P.G. Mulder, D.S. Postma, and H.C. Hoogsteden. 1996. Increased numbers of dendritic cells in the bronchial mucosa of atopic asthmatic patients: downregulation by inhaled corticosteroids. Clin. Exp. Allergy. 26:517-524.
17. van Rijt, L.S., J.B. Prins, P.J. Leenen, K. Thielemans, V.C. de Vries, H.C. Hoogsteden, and B.N. Lambrecht. 2002. Allergen-induced accumulation of airway dendritic cells is supported by an increase in CD31(hi)Ly-6C(neg) bone marrow precursors in a mouse model of asthma. Blood. 100:3663-3671.
18. Vermaelen, K.Y., D. Cataldo, K. Tournoy, T. Maes, A. Dhulst, R. Louis, J.M. Foidart, A. Noel, and R. Pauwels. 2003. Matrix metalloproteinase-9-mediated dendritic cell recruitment into the airways is a critical step in a mouse model of asthma. J. Immunol. 171:1016-1022.
19. Lambrecht, B.N., B. Salomon, D. Klatzmann, and R.A. Pauwels. 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.
20. London, C.A., M.P. Lodge, and A.K. Abbas. 2000. Functional responses and costimulator dependence of memory CD4 + T cells. J. Immunol. 164:265-272.
21. Dubey, C., M. Croft, and S.L. Swain. 1996. Naive and effector CD4 T cells differ in their requirements for T cell receptor versus costimulatory signals. J. Immunol. 157:3280-3289.
22. Gause, W.C., V. Mitro, C. Via, P. Linsley, J.F. Urban Jr., and R.J. Greenwald. 1997. Do effector and memory T helper cells also need B7 ligand costimulatory signals? J. Immunol. 159:1055-1058.
23. Jung, S., D. Unutmaz, P. Wong, G. Sano, K. De los Santos, T. Sparwasser, S. Wu, S. Vuthoori, K. Ko, F. Zavala, et al. 2002. In vivo depletion of CD11c(+) dendritic cells abrogates priming of CD8(+) T cells by exogenous cell-associated antigens. Immunity. 17:211-220.
24. Cohn, L., R.J. Homer, A. Marinov, J. Rankin, and K. Bottomly. 1997. Induction of airway mucus production By T helper 2 (Th2) cells: a critical role for interleukin 4 in cell recruitment but not mucus production. J. Exp. Med. 186:1737-1747.
25. Demangel, C., A.G. Bean, E. Martin, C.G. Feng, A.T. Kamath, and W.J. Britton. 1999. Protection against aerosol Mycobacterium tuberculosis infection using Mycobacterium bovis Bacillus Calmette Guerin-infected dendritic cells. Eur. J. Immunol. 29:1972-1979.
26. De Heer, H.J., H. Hammad, T. Soullie, D. Hijdra, N. Vos, M.A. Willart, H.C. Hoogsteden, and B.N. Lambrecht. 2004. Essential role of lung plasmacytoid dendritic cells in preventing asthmatic reactions to harmless inhaled antigen. J. Exp. Med. 200:89-98.
27. Lambrecht, B.N., I. Carro-Muino, K. Vermaelen, and R.A. Pauwels. 1999. Allergen-induced changes in bone-marrow progenitor and airway dendritic cells in sensitized rats. Am. J. Respir. Cell Mol. Biol. 20:1165-1174.
28. + T cells independent of the PD-1 receptor. J. Exp. Med. 198:31-38.
29. Hammad, H., H. Jan de Heer, T. Soullie, H.C. Hoogsteden, F. Trottein, and B.N. Lambrecht. 2003. Prostaglandin D2 inhibits airway dendritic cell migration and function in steady state conditions by selective activation of the D prostanoid receptor 1. J. Immunol. 171:3936-3940.
30. Holt, P.G., S. Haining, D.J. Nelson, and J.D. Sedgwick. 1994. Origin and steady-state turnover of class II MHC-bearing dendritic cells in the epithelium of the conducting airways. J. Immunol. 153:256-261.
31. Hu, H., G. Huston, D. Duso, N. Lepak, E. Roman, and S.L. Swain. 2001. CD4(+) T cell effectors can become memory cells with high efficiency and without further division. Nat. Immunol. 2:705-710.
32. Harbertson, J., E. Biederman, K.E. Bennett, R.M. Kondrack, and L.M. Bradley. 2002. Withdrawal of stimulation may initiate the transition of effector to memory CD4 cells. J. Immunol. 168:1095-1102.
33. Tang, C., M.D. Inman, N. van Rooijen, P. Yang, H. Shen, K. Matsumoto, and P.M. O'Byrne. 2001. Th type 1-stimulating activity of lung macrophages inhibits Th2-mediated allergic airway inflammation by an IFN-gamma-dependent mechanism. J. Immunol. 166:1471-1481.
34. Huleatt, J.W., and L. Lefrancois. 1995. Antigen-driven induction of CD11c on intestinal intraepithelial lymphocytes and CD8+ T cells in vivo. J. Immunol. 154:5684-5693.
35. Gonzalo, J.A., C.M. Lloyd, L. Kremer, E. Finger, A.C. Martinez, M.H. Siegelman, M. Cybulsky, and J.C. Gutierrez-Ramos. 1996. Eosinophil recruitment to the lung in a murine model of allergic inflammation. The role of T cells, chemokines, and adhesion receptors. J. Clin. Invest. 98:2332-2345.
36. Zhang, Y., K.H. Rogers, and D.B. Lewis. 1996. β2-microglobulin- dependent T cells are dispensable for allergen-induced T helper 2 responses. J. Exp. Med. 184:1507-1512.
37. Van Rijt, L.S., N. Vos, D. Hijdra, V.C. De Vries, H.C. Hoogsteden, and B.N. Lambrecht. 2003. Airway eosinophils accumulate in the mediastinal lymph nodes but lack antigen-presenting potential for naive T cells. J. Immunol. 171:3372-3378.
38. Schweitzer, A.N., and A.H. Sharpe. 1998. Studies using antigen-presenting cells lacking expression of both B7-1 (CD80) and B7-2 (CD86) show distinct requirements for B7 molecules during priming versus restimulation of Th2 but not Th1 cytokine production. J. Immunol. 161:2762-2771.
39. Coyle, A.J., S. Lehar, C. Lloyd, J. Tian, T. Delaney, S. Manning, T. Nguyen, T. Burwell, H. Schneider, J.A. Gonzalo, et al. 2000. The CD28-related molecule ICOS is required for effective T cell-dependent immune responses. Immunity. 13:95-105.
40. Mathur, M., K. Herrmann, Y. Qin, F. Gulmen, X. Li, R. Krimins, J. Weinstock, D. Elliott, J.A. Bluestone, and P. Padrid. 1999. CD28 interactions with either CD80 or CD86 are sufficient to induce allergic airway inflammation in mice. Am. J. Respir. Cell Mol. Biol. 21:498-509.
41. Deurloo, D.T., M.A. van Berkel, B.C. van Esch, F. Hofhuis, F.P. Nijkamp, M.A. Oosterwegel, and A.J. van Oosterhout. 2003. CD28/CTLA4 double deficient mice demonstrate crucial role for B7 co-stimulation in the induction of allergic lower airways disease. Clin. Exp. Allergy. 33:1297-1304.
42. Harris, N., R. Peach, J. Naemura, P.S. Linsley, G. Le Gros, and F. Ronchese. 1997. CD80 costimulation is essential for the induction of airway eosinophilia. J. Exp. Med. 185:177-182.
43. Keane-Myers, A., W.C. Gause, P.S. Linsley, S.J. Chen, and M. Wills-Karp. 1997. B7-CD28/CTLA-4 costimulatory pathways are required for the development of T helper cell 2-mediated allergic airway responses to inhaled antigens. J. Immunol. 158:2042-2049.
44. Hammad, H., H.H. Smits, C. Ratajczak, A. Nithiananthan, E.A. Wierenga, G.A. Stewart, A. Jacquet, A.B. Tonnel, and J. Pestel. 2003. Monocyte-derived dendritic cells exposed to Der p 1 allergen enhance the recruitment of Th2 cells: major involvement of the chemokines TARC/CCL17 and MDC/CCL22. Eur. Cytokine Netw. 14:219-228.
45. Malmstrom, V., D. Shipton, B. Singh, A. Al-Shamkhani, M.J. Puklavec, A.N. Barclay, and F. Powrie. 2001. CD134L expression on dendritic cells in the mesenteric lymph nodes drives colitis in T cell-restored SCID mice. J. Immunol. 166:6972-6981.
46. Rosmalen, J.G., F. Homo-Delarche, S. Durant, M. Kap, P.J. Leenen, and H.A. Drexhage. 2000. Islet abnormalities associated with an early influx of dendritic cells and macrophages in NOD and NODscid mice. Lab. Invest. 80:769-777.
47. Lutz, M.B., N. Kukutsch, A.L. Ogilvie, S. Rossner, F. Koch, N. Romani, and G. Schuler. 1999. An advanced culture method for generating large quantities of highly pure dendritic cells from mouse bone marrow. J. Immunol. Methods. 223:77-92.
48. Hamelmann, E., J. Schwarze, K. Takeda, A. Oshiba, G.L. Larsen, C.G. Irvin, and E.W. Gelfand. 1997. Noninvasive measurement of airway responsiveness in allergic mice using barometric plethysmography. Am. J. Respir. Crit. Care Med. 156:766-775.