Clearance of influenza virus from the lung depends on migratory langerin+CD11b- but not plasmacytoid dendritic cells

Journal of Experimental Medicine

Volumn 205, Issue 7, 2008, Pages 1621-1634

  GeurtsvanKessel, Corine H ^a   Willart, Monique A M ^b   Van Rijt, Leonie S ^a   Muskens, Femke ^a   Kool, Mirjam ^a   Baas, Chantal ^a   Thielemans, Kris ^c   Bennett, Clare ^d   Clausen, Björn E ^d   Hoogsteden, Henk C ^a   Osterhaus, Albert D M E ^a   Rimmelzwaan, Guns F ^a   Lambrecht, Bart N ^a,b  

^a ERASMUS UNIVERSITY ROTTERDAM   (Netherlands)

^b GHENT UNIVERSITY HOSPITAL   (Belgium)

^c FREE UNIVERSITY OF BRUSSELS   (Belgium)

^d UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; CD8ALPHA ANTIGEN; DIPHTHERIA TOXIN; LANGERIN; VIRUS ANTIBODY; VIRUS NUCLEOPROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY PRODUCTION; ANTIGEN PRESENTATION; ANTIVIRAL ACTIVITY; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL FUNCTION; CELL MIGRATION; CELL PROLIFERATION; CELL SPECIFICITY; CONTROLLED STUDY; DENDRITIC CELL; EMBRYO; INFLUENZA VIRUS; LUNG CLEARANCE; LUNG INTERSTITIUM; MACROPHAGE; MALE; MEDIASTINUM LYMPH NODE; MOUSE; NONHUMAN; PRIORITY JOURNAL; TRACHEA;

ANIMALS; ANTIBODIES, VIRAL; ANTIBODY FORMATION; ANTIGEN PRESENTATION; ANTIGENS, CD11B; ANTIGENS, CD11C; ANTIGENS, CD8; ANTIGENS, SURFACE; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL MOVEMENT; DENDRITIC CELLS; DOGS; FEMALE; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LECTINS, C-TYPE; LUNG; LYMPH NODES; MALE; MANNOSE-BINDING LECTINS; MICE; MICE, INBRED BALB C; MICE, TRANSGENIC; NUCLEOCAPSID PROTEINS; ORTHOMYXOVIRIDAE; ORTHOMYXOVIRIDAE INFECTIONS; PLASMA CELLS; TRACHEA;

EID: 46949109891     PISSN: 00221007     EISSN: 00221007     Source Type: Journal    
DOI: 10.1084/jem.20071365     Document Type: Article

References (63)

1. + T cells. J. Exp. Med. 174:875-880.
2. Legge, K.L., and T.J. Braciale. 2005. Lymph node dendritic cells control CD8+ T cell responses through regulated FasL expression. Immunity. 23:649-659.
3. Pichlmair, A., O. Schulz, C.P. Tan, T.I. Naslund, P. Liljestrom, F. Weber, and C. Reis e Sousa. 2006. RIG-I-mediated antiviral responses to single-stranded RNA bearing 5'-phosphates. Science. 314:997-1001.
4. Tecle, T., MR. White, and K.L. Hartshorn. 2005. Innate immunity to influenza A virus infection. Current Respir. Med. Rev. 1:127-145.
5. Kumagai, Y., O. Takeuchi, H. Kato, H. Kumar, K. Matsui, E. Morii, K. Aozasa, T. Kawai, and S. Akira. 2007. Alveolar macrophages are the primary interferon-alpha producer in pulmonary infection with RNA viruses. Immunity. 27:240-252.
6. Banchereau, J., and R.M. Steinman. 1998. Dendritic cells and the control of immunity. Nature. 392:245-252.
7. McWilliam, A.S., D.J. Nelson, J.A. Thomas, and P.G. Holt. 1994. Rapid dendritic cell recruitment is a hallmark of the acute inflammatory response at mucosal surfaces. J. Exp. Med. 179:1331-1336.
8. Legge, K.L., and T.J. Braciale. 2003. Accelerated migration of respiratory dendritic cells to the regional lymph nodes is limited to the early phase of pulmonary infection. Immunity. 18:265-277.
9. Lambrecht, B.N., J.B. Prins, and H.C. Hoogsteden. 2001. Lung dendritic cells and host immunity to infection. Eur. Respir. J. 18:692-704.
10. Vermaelen, K., and R. Pauwels. 2005. Pulmonary dendritic cells. Am. J. Respir. Crit. Care Med. 172:530-551.
11. von Garnier, C, L. Filgueira, M. Wikstrom, M. Smith, J.A. Thomas, D.H. Strickland, P.G. Holt, and P.A. Stumbles. 2005. Anatomical location determines the distribution and function of dendritic cells and other APCs in the respiratory tract. J. Immunol. 175:1609-1618.
12. de Heer, H.J., H. Hammad, M. Kool, and B.N. Lambrecht. 2005. Dendritic cell subsets and immune regulation in the lung. Semin. Immunol. 17:295-303.
13. Sung, S.S., S.M. Fu, C.E. Rose Jr., F. Gaskin, ST. Ju, and S.R. Beaty. 2006. A major lung CD103 (alphaE)-beta7 integrin-positive epithelial dendritic cell population expressing Langerin and tight junction proteins. J. Immunol. 176:2161-2172.
14. Wikstrom, M.E., and P.A. Stumbles. 2007. Mouse respiratory tract dendritic cell subsets and the immunological fate of inhaled antigens. Immunol. Cell Biol. 85:182-188.
15. del Rio, M.-L., J.-I. Rodriguez-Barbosa, E. Kremmer, and R. Forster. 2007. CD103- and CD103+ bronchial lymph node dendritic cells are specialized in presenting and cross-presenting innocuous antigen to CD4+ and CD8+ T cells. J. Immunol. 178:6861-6866.
16. Shortman, K., and S.H. Naik. 2007. Steady-state and inflammatory dendritic-cell development. Nat. Rev. Immunol. 7:19-30.
17. Sertl, K., T. Takemura, E. Tschachler, V.J. Ferrans, M.A. Kaliner, and E.M. Shevach. 1986. Dendritic cells with antigen-presenting capability reside in airway epithelium, lung parenchyma, and visceral pleura. J. Exp. Med. 163:436-451.
18. 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.
19. + dendritic cells during allergen challenge abrogates the characteristic features of asthma. J. Exp. Med. 201:981-991.
20. neg hematopoietic precursors. Blood. 100:3663-3671.
21. Lambrecht, B.N. 2006. Alveolar macrophage in the driver's seat. Immunity. 24:366-368.
22. Asselin-Paturel, C., G. Brizard, J.J. Pin, F. Briere, and G. Trinchieri. 2003. Mouse strain differences in plasmacytoid dendritic cell frequency and function revealed by a novel monoclonal antibody. J. Immunol. 171:6466-6477.
23. Blasius, A.L., E. Giurisato, M. Cella, R.D. Schreiber, A.S. Shaw, and M. Colonna. 2006. Bone marrow stromal cell antigen 2 is a specific marker of type I IFN-producing cells in the naive mouse, but a promiscuous cell surface antigen following IFN stimulation. J. Immunol. 177:3260-3265.
24. 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.
25. Smit, J.J., B.D. Rudd, and N.W. Lukacs. 2006. Plasmacytoid dendritic cells inhibit pulmonary immunopathology and promote clearance of respiratory syncytial virus. J. Exp. Med. 203:1153-1159.
26. Wang, H., N. Peters, and J. Schwarze. 2006. Plasmacytoid dendritic cells limit viral replication, pulmonary inflammation, and airway hyperresponsiveness in respiratory syncytial virus infection. J. Immunol. 177:6263-6270.
27. Hamilton-Easton, A., and M. Eichelberger. 1995. Virus-specif c antigen presentation by different subsets of cells from lung and mediastinal lymph node tissues of influenza virus-infected mice. J. Virol. 69:6359-6366.
28. Yamamoto, N., S. Suzuki, A. Shirai, M. Suzuki, M. Nakazawa, Y. Nagashima, and T. Okubo. 2000. Dendritic cells are associated with augmentation of antigen sensitization by influenza A virus infection in mice. Eur. J. Immunol. 30:316-326.
29. 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.
30. Belz, G.T., C.M. Smith, L. Kleinert, P. Reading, A. Brooks, K. Shortman, F.R. Carbone, and W.R. Heath. 2004. Distinct migrating and nonmigrating dendritic cell populations are involved in MHC class Irestricted antigen presentation after lung infection with virus. Proc. Natl. Acad. Sci. USA. 101:8670-8675.
31. Belz, G.T., L. Zhang, M.D. Lay, F. Kupresanin, and M.P. Davenport. 2007. Killer T cells regulate antigen presentation for early expansion of memory, but not naive, CD8+ T cell. Proc. Natl. Acad. Sci. USA. 104:6341-6346.
32. Belz, G.T., S. Bedoui, F. Kupresanin, F.R. Carbone, and W.R. Heath. 2007. Minimal activation of memory CD8+ T cell by tissue-derived dendritic cells favors the stimulation of naive CD8+ T cells. Nat. Immunol. 8:1060-1066.
33. + cytolytic T cell responses. J. Exp. Med. 182: 1663-1671.
34. Fonteneau, J.F., M. Gilliet, M. Larsson, I. Dasilva, C. Munz, Y.J. Liu, and N. Bhardwaj. 2003. Activation of influenza virus-specif c CD4+ and CD8+ T cells: a new role for plasmacytoid dendritic cells in adaptive immunity. Blood. 101:3520-3526.
35. Dhodapkar, M.V., R.M. Steinman, M. Sapp, H. Desai, C. Fossella, J. Krasovsky, S.M. Donahoe, P.R. Dunbar, V. Cerundolo, D.F. Nixon, and N. Bhardwaj. 1999. Rapid generation of broad T-cell immunity in humans after a single injection of mature dendritic cells. J. Clin. Invest. 104:173-180.
36. Bennett, C.L., E. van Rijn, S. Jung, K. Inaba, R.M. Steinman, M.L. Kapsenberg, and B.E. Clausen. 2005. Inducible ablation of mouse Langerhans cells diminishes but fails to abrogate contact hypersensitivity. J. Cell Biol. 169:569-576.
37. 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.
38. Vermaelen, K., and R. Pauwels. 2004. Accurate and simple discrimination of mouse pulmonary dendritic cell and macrophage populations by f ow cytometry: methodology and new insights. Cytometry A. 61:170-177.
39. van Rijt, L.S., H. Kuipers, N. Vos, D. Hijdra, H.C. Hoogsteden, and B.N. Lambrecht. 2004. A rapid flow cytometric method for determining the cellular composition of bronchoalveolar lavage fluid cells in mouse models of asthma. J. Immunol. Methods. 288:111-121.
40. Topham, D.J., M.R. Castrucci, F.S. Wingo, G.T. Belz, and P.C. Doherty. 2001. The role of antigen in the localization of naive, acutely activated, and memory CD8(+) T cells to the lung during influenza pneumonia. J. Immunol. 167:6983-6990.
41. Thomas, P.G., S.A. Brown, W. Yue, J. So, R.J. Webby, and P.C. Doherty. 2006. An unexpected antibody response to an engineered influenza virus modifies CD8+ T cell responses. Proc. Natl. Acad. Sci. USA. 103:2764-2769.
42. Kreijtz, J.H., R. Bodewes, G. van Amerongen, T. Kuiken, R.A. Fouchier, A.D. Osterhaus, and G.F. Rimmelzwaan. 2007. Primary influenza A virus infection induces cross-protective immunity against a lethal infection with a heterosubtypic virus strain in mice. Vaccine. 25: 612-620.
43. +, T cells by plasmacytoid dendritic cells. J. Exp. Med. 204:1923-1933.
44. Asselin-Paturel, C., A. Boonstra, M. Dalod, I. Durand, N. Yessaad, C. Dezutter-Dambuyant, A. Vicari, A. O'Garra, C. Biron, F. Briere, and G. Trinchieri. 2001. Mouse type I IFN-producing cells are immature APCs with plasmacytoid morphology. Nat. Immunol. 2:1144-1150.
45. Naik, S.H., D. Metcalf, A. van Nieuwenhuijze, I. Wicks, L. Wu, M. O'Keeffe, and K. Shortman. 2006. Intrasplenic steady-state dendritic cell precursors that are distinct from monocytes. Nat. Immunol. 7:663-671.
46. Blusse van Oud Alblas, A., B. van der Linden-Schrever, and R. van Furth. 1981. Origin and kinetics of pulmonary macrophages during an inflammatory reaction induced by intravenous administration of heat-killed bacillus Calmette-Guerin. J. Exp. Med. 154:235-252.
47. Dudziak, D., A.O. Kamphorst, G.F. Heidkamp, V.R. Buchholz, C. Trumpfheller, S. Yamazaki, C. Cheong, K. Liu, H.W. Lee, C.G. Park, et al. 2007. Differential antigen processing by dendritic cell subsets in vivo. Science. 315:107-111.
48. Allan, R.S., J. Waithman, S. Bedoui, C.M. Jones, J.A. Villadangos, Y. Zhan, A.M. Lew, K. Shortman, W.R. Heath, and F.R. Carbone. 2006. Migratory dendritic cells transfer antigen to a lymph node-resident dendritic cell population for eficient CTL priming. Immunity. 25: 153-162.
49. Schnorrer, P., G.M. Behrens, N.S. Wilson, J.L. Pooley, C.M. Smith, D. El-Sukkari, G. Davey, F. Kupresanin, M. Li, E. Maraskovsky, et al. 2006. The dominant role of CD8+ dendritic cells in cross-presentation is not dictated by antigen capture. Proc. Natl. Acad. Sci. USA. 103:10729-10734.
50. 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.
51. Beaty, S.R., C.E. Rose Jr., and S.S. Sung. 2007. Diverse and potent chemokine production by lung CD11bhi dendritic cells in homeostasis and in allergic lung inflammation. J. Immunol. 178:1882-1895.
52. Serbina, N.V., T.P. Salazar-Mather, C.A. Biron, W.A. Kuziel, and E.G. Pamer. 2003. TNF/iNOS-producing dendritic cells mediate innate immune defense against bacterial infection. Immunity. 19:59-70.
53. Rimmelzwaan, G.F., M.M. Baars, P. de Lijster, R.A. Fouchier, and A.D. Osterhaus. 1999. Inhibition of influenza virus replication by nitric oxide. J. Virol. 73:8880-8883.
54. Diebold, S.S., M. Montoya, H. Unger, L. Alexopoulou, P. Roy, L.E. Haswell, A. Al-Shamkhani, R. Flavell, P. Borrow, and C.R. Sousa. 2003. Viral infection switches non-plasmacytoid dendritic cells into high interferon producers. Nature. 424:324-328.
55. Stoecklinger, A., I. Grieshuber, S. Scheiblhofer, R. Weiss, U. Ritter, A. Kissenpfennig, B. Malissen, N. Romani, F. Koch, F. Ferreira, et al. 2007. Epidermal langerhans cells are dispensable for humoral and cell-mediated immunity elicited by gene gun immunization. J. Immunol. 179:886-893.
56. Kissenpfennig, A., S. Henri, B. Dubois, C. Laplace-Builhe, P. Perrin, N. Romani, C.H. Tripp, P. Douillard, L. Leserman, D. Kaiserlian, 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.
57. Cella, M., F. Facchetti, A. Lanzavecchia, and M. Colonna. 2000. Plasmacytoid dendritic cells activated by influenza virus and CD40L drive a potent TH1 polarization. Nat. Immunol. 1:305-310.
58. Soumelis, V., and Y.J. Liu. 2006. From plasmacytoid to dendritic cell: morphological and functional switches during plasmacytoid pre-dendritic cell differentiation. Eur. J. Immunol. 36:2286-2292.
59. Jego, G., A.K. Palucka, J.P. Blanck, C. Chalouni, V. Pascual, and J. Banchereau. 2003. Plasmacytoid dendritic cells induce plasma cell differentiation through type I interferon and interleukin 6. Immunity. 19: 225-234.
60. Rimmelzwaan, G.F., M. Baars, E.C. Claas, and A.D. Osterhaus. 1998. Comparison of RNA hybridization, hemagglutination assay, titration of infectious virus and immunofluorescence as methods for monitoring influenza virus replication in vitro. J. Virol. Methods. 74:57-66.
61. 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.
62. Haanen, J.B., M.C. Wolkers, A.M. Kruisbeek, and T.N. Schumacher. 1999. Selective expansion of cross-reactive CD8 positive memory T cells by viral variants. J. Exp. Med. 190:1319-1328.
63. Masurel, N., P. Ophof, and P. de Jong. 1981. Antibody response to immunization with influenza A/USSR/77 (H1N1) virus in young individuals primed or unprimed for A/New Jersey/76 (H1N1) virus. J. Hyg. (Lond.). 87:201-209.