Influenza virus-induced dendritic cell maturation is associated with the induction of strong T cell immunity to a coadministered, normally nonimmunogenic protein

Journal of Experimental Medicine

Volumn 198, Issue 1, 2003, Pages 133-144

  Brimnes, Marie K ^a   Bonifaz, Laura ^b   Steinman, Ralph M ^b   Moran, Thomas M ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b ROCKEFELLER UNIVERSITY   (United States)

Author keywords

Airway; Dendritic cell; Endotoxin free ovalbumin; Influenza virus; Maturation

Indexed keywords

B7 ANTIGEN; CD4 ANTIGEN; CD8 ANTIGEN; CD86 ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 2; INTERLEUKIN 4; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; OVALBUMIN; T LYMPHOCYTE RECEPTOR;

ANIMAL CELL; ARTICLE; CELL MATURATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; IMMUNOREACTIVITY; IMMUNOREGULATION; INFLUENZA VIRUS; INTERFERON PRODUCTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE; VIRUS CELL INTERACTION;

ANIMALS; ANTIBODY FORMATION; ANTIGEN PRESENTATION; ANTIGENS, CD11C; ANTIGENS, VIRAL; DENDRITIC CELLS; FEMALE; IMMUNE TOLERANCE; LYMPH NODES; MICE; MICE, INBRED C57BL; ORTHOMYXOVIRIDAE INFECTIONS; OVALBUMIN; T-LYMPHOCYTES;

EID: 0038152841     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.20030266     Document Type: Article

References (41)

1. Holt, P.G., M.A. Schon-Hegrad, J. Oliver, B.J. Holt, and P.G. McMenamin. 1990. A contiguous network of dendritic antigen-presenting cells within the respiratory epithelium. Int. Arch. Allergy Appl. Immunol. 91:155-159.
2. Nelson, D.J., C. McMenamin, A.S. McWilliam, M. Brenan, and P.G. Holt. 1994. Development of the airway intraepithelial dendritic cell network in the rat from class II major histocompatibility (Ia)-negative precursors: differential regulation of Ia expression at different levels of the respiratory tract. J. Exp. Med. 179:203-212.
3. 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.
4. Gong, J.L., K.M. McCarthy, J. Telford, T. Tamatani, M. Miyasaka, and E.E. Schneeberger. 1.992. Intraepithelial airway dendritic cells: a distinct subset of pulmonary dendritic cells obtained by microdissection. J. Exp. Med. 175:797-807.
5. Havenith, C.E., P.P. van Miert, A.J. Breedijk, R.H. Beelen, and E.C. Hoefsmit. 1993. Migration of dendritic cells into the draining lymph nodes of the lung after intratracheal instillation. Am. J. Respir. Cell Mol. Biol. 9:484-488.
6. 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.
7. Xia, W., C.E. Pinto, and R.L. Kradin. 1995. The antigen-presenting activities of Ia+ dendritic cells shift dynamically from lung to lymph node after an airway challenge with soluble antigen. J. Exp. Med. 181:1275-1283.
8. 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.
9. Akbari, O., G.J. Freeman, E.H. Meyer, E.A. Greenfield, T.T. Chang, A.H. Sharpe, G. Berry, R.H. DeKruyff, and D.T. Umetsu. 2002. Antigen-specific regulatory T cells develop via the ICOS-ICOS-ligand pathway and inhibit allergen-induced airway hyperreactivity. Nat. Med. 8:1024-1032.
10. Steinman, R.M., and M.C. Nussenzweig. 2002. Avoiding horror autotoxicus: the importance of dendritic cells in peripheral T cell tolerance. Proc. Natl. Acad. Sci. USA. 99:351-358.
11. Schuler, G., and R.M. Steinman. 1985. Murine epidermal Langerhans cells mature into potent immunostimulatory dendritic cells in vitro. J. Exp. Med. 161:526-546.
12. Inaba, K., G. Schuler, M.D. Witmer, J. Valinksy, B. Atassi, and R.M. Steinman. 1986. Immunologic properties of purified epidermal Langerhans cells. Distinct requirements for stimulation of unprimed and sensitized T lymphocytes. J. Exp. Med. 164:605-613.
13. Romani, N., S. Koide, M. Crowley, M. Witmer-Pack, A.M. Livingstone, C.G. Fathman, K. Inaba, and R.M. Steinman. 1989. Presentation of exogenous protein antigens by dendritic cells to T cell clones. Intact protein is presented best by immature, epidermal Langerhans cells. J. Exp. Med. 169: 1169-1178.
14. Huang, Q., D. Liu, P. Majewski, L.C. Schulte, J.M. Korn, R.A. Young, E.S. Lander, and N. Hacohen. 2001. The plasticity of dendritic cell responses to pathogens and their components. Science. 294:870-875.
15. Cella, M., M. Salio, Y. Sakakibara, H. Langen, I. Julkunen, and A. Lanzavecchia. 1999. Maturation, activation, and protection of dendritic cells induced by double-stranded RNA. J. Exp. Med. 189:821-829.
16. Lopez, C.B., A. Garcia-Sastre, B.R.G. Williams, and T.M. Moran. 2003. The type 1 IFN induction pathway, but not released IFN, participates in the maturation of dendritic cells induced by negative strand RNA viruses. J. Infect. Dis. 187: 1126-1136.
17. 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.
18. Yamamoto, N., S. Suzuki, Y. Suzuki, A. Shirai, M. Nakazawa, M. Suzuki, T. Takamasu, Y. Nagashima, M. Minami, and Y. Ishigatsubo. 2001. Immune response induced by airway sensitization after influenza A virus infection depends on timing of antigen exposure in mice. J. Virol. 75:499-505.
19. 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.
20. Sakamoto, M., S. Ida, and T. Takishima. 1984. Effect of influenza virus infection on allergic sensitization to aerosolized ovalbumin in mice. J. Immunol. 132:2614-2617.
21. Suzuki, S., Y. Suzuki, N. Yamamoto, Y. Matsumoto, A. Shirai, and T. Okubo. 1998. Influenza A virus infection increases IgE production and airway responsiveness in aerosolized antigen-exposed mice. J. Allergy Clin. Immunol. 102: 732-740.
22. Schwarze, J., E. Hamelmann, K.L. Bradley, K. Takeda, and E.W. Gelfand. 1997. Respiratory syncytial virus infection results in airway hyperresponsiveness and enhanced airway sensitization to allergen. J. Clin. Invest. 100:226-233.
23. Leibovitz, E., J. Freihorst, P.A. Piedra, and P.L. Ogra. 1988. Modulation of systemic and mucosal immune responses to inhaled ragweed antigen in experimentally induced infection with respiratory syncytial virus implication in virally induced allergy. Int. Arch. Allergy Appl. Immunol. 86:112-116.
24. Dakhama, A., A.M. Bramley, N.G. Chan, K.O. McKay, K.K. Schellenberg, and R.G. Hegele. 1999. Effect of respiratory syncytial virus on subsequent allergic sensitization to ovalbumin in guinea-pigs. Eur. Respir. J. 13:976-982.
25. O'Donnell, D.R., and P.J. Openshaw. 1998. Anaphylactic sensitization to aeroantigen during respiratory virus infection. Clin. Exp. Allergy. 28:1501-1508.
26. 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.
27. Akbari, O., R.H. DeKruyff, and D.T. Umetsu. 2001. Pulmonary dendritic cells producing IL-10 mediate tolerance induced by respiratory exposure to antigen. Nat. Immunol. 2: 725-731.
28. Lopez, C.B., A. Fernandez-Sesma, S.M. Czelusniak, J.L. Schulman, and T.M. Moran. 2000. A mouse model for immunization with ex vivo virus-infected dendritic cells. Cell. Immunol. 206:107-115.
29. Bonifaz, L., D. Bonnyay, K. Mahnke, M. Rivera, M.C. Nussenzweig, and R.M. Steinman. 2002. Efficient targeting of protein antigen to the dendritic cell receptor DEC-205 in the steady state leads to antigen presentation on major histocompatibility complex class I products and peripheral CD8+ T cell tolerance. J. Exp. Med. 196:1627-1638.
30. Lopez, C.B., A. Fernandez-Sesma, J.L. Schulman, and T.M. Moran. 2001. Myeloid dendritic cells stimulate both th1 and th2 immune responses depending on the nature of the antigen. J. Interferon Cytokine Res. 21:763-773.
31. Hawiger, D., K. Inaba, Y. Dorsett, M. Guo, K. Mahnke, M. Rivera, J.V. Ravetch, R.M. Steinman, and M.C. Nussenzweig. 2001. Dendritic cells induce peripheral T cell unresponsiveness under steady state conditions in vivo. J. Exp. Med. 194:769-779.
32. Crowley, M., K. Inaba, and R.M. Steinman. 1990. Dendritic cells are the principal cells in mouse spleen bearing immunogenic fragments of foreign proteins. J. Exp. Med. 172:383-386.
33. Liu, K., T. Iyoda, M. Saternus, Y. Kimura, K. Inaba, and R.M. Steinman. 2002. Immune tolerance after delivery of dying cells to dendritic cells in situ. J. Exp. Med. 196:1091-1097.
34. Kamath, A.T., J. Pooley, M.A. O'Keeffe, D. Vremec, Y. Zhan, A.M. Lew, A. D'Amico, L. Wu, D.F. Tough, and K. Shortman. 2000. The development, maturation, and turnover rate of mouse spleen dendritic cell populations. J. Immunol. 165:6762-6770.
35. Iyoda, T., S. Shimoyama, K. Liu, Y. Omatsu, Y. Akiyama, Y. Maeda, K. Takahara, R.M. Steinman, and K. Inaba. 2002. The CD8+ dendritic cell subset selectively endocytoses dying cells in culture and in vivo. J. Exp. Med. 195:1289-1302.
36. Tsitoura, D.C., R.H. DeKruyff, J.R., Lamb, and D.T. Umetsu. 1999. Intranasal exposure to protein antigen induces immunological tolerance mediated by functionally disabled CD4+ T cells. J. Immunol. 163:2592-2600.
37. De Smedt, T., B. Pajak, E. Muraille, L. Lespagnard, E. Heinen, P. De Baetselier, J. Urbain, O. Leo, and M. Moser. 1996. Regulation of dendritic cell numbers and maturation by lipopolysaccharide in vivo. J. Exp. Med. 184:1413-1424.
38. Sparwasser, T., E.S. Koch, R.M. Vabulas, K. Heeg, G.B. Lipford, J.W. Ellwart, and H. Wagner. 1998. Bacterial DNA and immunostimulatory CpG oligonucleotides trigger maturation and activation of murine dendritic cells. Eur. J. Immunol. 28:2045-2054.
39. Fujii, S., K. Shimizu, C. Smith, L. Bonifaz, and R.M. Steinman. 2003. Activation of natural killer T cells by α-galactosylceramide rapidly induces the full maturation of dendritic cells in vivo and thereby acts as an adjuvant for combined CD4 and CD8 T cell immunity to a co-administered protein. J. Exp. Med. In press.
40. Metlay, J.P., M.D. Witmer-Pack, R. Agger, M.T. Crowley, D. Lawless, and R.M. Steinman. 1990. The distinct leukocyte integrins of mouse spleen dendritic cells as identified with new hamster monoclonal antibodies. J. Exp. Med. 171: 1753-1771.
41. Crowley, M.T., K. Inaba, M.D. Witmer-Pack, S. Gezelter, and R.M. Steinman. 1990. Use of the fluorescence activated cell sorter to enrich dendritic cells from mouse spleen. J. Immunol. Methods. 133:55-66.