Inefficient lymph node sensitization during respiratory viral infection promotes IL-17-mediated lung pathology

Journal of Immunology

Volumn 185, Issue 7, 2010, Pages 4137-4147

  Kallal, Lara E ^a   Hartigan, Adam J ^a   Hogaboam, Cory M ^a   Schaller, Matthew A ^a   Lukacs, Nicholas W ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CCR7; GAMMA INTERFERON; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 4; INTERLEUKIN 5; LYMPHOTOXIN; CCR7 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW; BRONCHUS; CD4+ T LYMPHOCYTE; CELL MIGRATION; CELLULAR IMMUNITY; CHIMERA; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RESPONSE; ECTOPIC PULMONARY LYMPH NODE; ECTOPIC TISSUE; EFFECTOR CELL; IMMUNE RESPONSE; LYMPH NODE; LYMPHOID TISSUE; MOUSE; MUCUS SECRETION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RESPIRATORY SYNCYTIAL VIRUS INFECTION; WILD TYPE; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CELL SEPARATION; CHORISTOMA; FLOW CYTOMETRY; GENETICS; IMMUNOLOGY; LUNG DISEASE; METABOLISM; MOUSE MUTANT; MUCUS; NEUTROPHIL CHEMOTAXIS; PATHOLOGY; RESPIRATORY SYNCYTIAL PNEUMOVIRUS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; T LYMPHOCYTE; VIROLOGY;

ANIMALS; CELL SEPARATION; CHEMOTAXIS, LEUKOCYTE; CHORISTOMA; FLOW CYTOMETRY; INTERLEUKIN-17; LUNG DISEASES; LYMPH NODES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUCUS; RECEPTORS, CCR7; RESPIRATORY SYNCYTIAL VIRUS INFECTIONS; RESPIRATORY SYNCYTIAL VIRUSES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; T-LYMPHOCYTES;

EID: 77958147027     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1000677     Document Type: Article

References (45)

1. Mebius, R. E. 2003. Organogenesis of lymphoid tissues. Nat. Rev. Immunol. 3:292-303.
2. Luther, S. A., H. L. Tang, P. L. Hyman, A. G. Farr, and J. G. Cyster. 2000. Coexpression of the chemokines ELC and SLC by T zone stromal cells and deletion of the ELC gene in the plt/plt mouse. Proc. Natl. Acad. Sci. USA 97:12694-12699.
3. Förster, R., A. Schubel, D. Breitfeld, E. Kremmer, I. Renner-Müller, E. Wolf, and M. Lipp. 1999. CCR7 coordinates the primary immune response by establishing functional microenvironments in secondary lymphoid organs. Cell 99:23-33.
4. Sallusto, F., P. Schaerli, P. Loetscher, C. Schaniel, D. Lenig, C. R. Mackay, S. Qin, and A. Lanzavecchia. 1998. Rapid and coordinated switch in chemokine receptor expression during dendritic cell maturation. Eur. J. Immunol. 28:2760-2769.
5. + T cells exhibit differential requirements for CCR7-mediated antigen transport during influenza infection. J. Immunol. 181:6984-6994.
6. Kursar, M., U. E. Höpken, M. Koch, A. Köhler, M. Lipp, S. H. Kaufmann, and H. W. Mittrücker. 2005. Differential requirements for the chemokine receptor CCR7 in T cell activation during Listeria monocytogenes infection. J. Exp. Med. 201:1447-1457.
7. Junt, T., E. Scandella, R. Förster, P. Krebs, S. Krautwald, M. Lipp, H. Hengartner, and B. Ludewig. 2004. Impact of CCR7 on priming and distribution of antiviral effector and memory CTL. J. Immunol. 173:6684-6693.
8. Lund, F. E., S. Partida-Sánchez, B. O. Lee, K. L. Kusser, L. Hartson, R. J. Hogan, D. L. Woodland, and T. D. Randall. 2002. Lymphotoxin-a-deficient mice make delayed, but effective, T and B cell responses to influenza. J. Immunol. 169:5236-5243.
9. Kocks, J. R., A. C. Davalos-Misslitz, G. Hintzen, L. Ohl, and R. Förster. 2007. Regulatory T cells interfere with the development of bronchus-associated lymphoid tissue. J. Exp. Med. 204:723-734.
10. Welliver, R. C. 2003. Review of epidemiology and clinical risk factors for severe respiratory syncytial virus (RSV) infection. J. Pediatr. 143 (5 Suppl.) S112-S117.
11. Peebles, R. S., Jr. 2004. Viral infections, atopy, and asthma: is there a causal relationship? J. Allergy Clin. Immunol. 113 (1 Suppl.) S15-S18.
12. Herlocher, M. L., M. Ewasyshyn, S. Sambhara, M. Gharaee-Kermani, D. Cho, J. Lai, M. Klein, and H. F. Maassab. 1999. Immunological properties of plaque purified strains of live attenuated respiratory syncytial virus (RSV) for human vaccine. Vaccine 17:172-181.
13. Lukacs, N. W., M. L. Moore, B. D. Rudd, A. A. Berlin, R. D. Collins, S. J. Olson, S. B. Ho, and R. S. Peebles, Jr. 2006. Differential immune responses and pulmonary pathophysiology are induced by two different strains of respiratory syncytial virus. Am. J. Pathol. 169:977-986.
14. Tekkanat, K. K., H. F. Maassab, D. S. Cho, J. J. Lai, A. John, A. Berlin, M. H. Kaplan, and N. W. Lukacs. 2001. IL-13-induced airway hyperreactivity during respiratory syncytial virus infection is STAT6 dependent. J. Immunol. 166:3542-3548.
15. Chen, Y., P. Thai, Y. H. Zhao, Y. S. Ho, M. M. DeSouza, and R. Wu. 2003. Stimulation of airway mucin gene expression by interleukin (IL)-17 through IL-6 paracrine/autocrine loop. J. Biol. Chem. 278:17036-17043.
16. Fujisawa, T., S. Velichko, P. Thai, L. Y. Hung, F. Huang, and R. Wu. 2009. Regulation of airway MUC5AC expression by IL-1beta and IL-17A; the NF-κB paradigm. J. Immunol. 183:6236-6243.
17. Lukacs, N. W., K. K. Tekkanat, A. Berlin, C. M. Hogaboam, A. Miller, H. Evanoff, P. Lincoln, and H. Maassab. 2001. Respiratory syncytial virus predisposes mice to augmented allergic airway responses via IL-13-mediated mechanisms. J. Immunol. 167:1060-1065.
18. Aloisi, F., and R. Pujol-Borrell. 2006. Lymphoid neogenesis in chronic inflammatory diseases. Nat. Rev. Immunol. 6:205-217.
19. Moyron-Quiroz, J. E., J. Rangel-Moreno, K. Kusser, L. Hartson, F. Sprague, S. Goodrich, D. L. Woodland, F. E. Lund, and T. D. Randall. 2004. Role of inducible bronchus associated lymphoid tissue (iBALT) in respiratory immunity. Nat. Med. 10:927-934.
20. Kocks, J. R., H. Adler, H. Danzer, K. Hoffmann, D. Jonigk, U. Lehmann, and R. Förster. 2009. Chemokine receptor CCR7 contributes to a rapid and efficient clearance of lytic murine gamma-herpes virus 68 from the lung, whereas bronchus-associated lymphoid tissue harbors virus during latency. J. Immunol. 182:6861-6869.
21. Halle, S., H. C. Dujardin, N. Bakocevic, H. Fleige, H. Danzer, S. Willenzon, Y. Suezer, G. Hämmerling, N. Garbi, G. Sutter, et al. 2009. Induced bronchusassociated lymphoid tissue serves as a general priming site for T cells and is maintained by dendritic cells. J. Exp. Med. 206:2593-2601.
22. Armengol, M. P., M. Juan, A. Lucas-Martín, M. T. Fernández-Figueras, D. Jaraquemada, T. Gallart, and R. Pujol-Borrell. 2001. Thyroid autoimmune disease: demonstration of thyroid antigen-specific B cells and recombinationactivating gene expression in chemokine-containing active intrathyroidal germinal centers. Am. J. Pathol. 159:861-873.
23. Young, C. L., T. C. Adamson, III, J. H. Vaughan, and R. I. Fox. 1984. Immunohistologic characterization of synovial membrane lymphocytes in rheumatoid arthritis. Arthritis Rheum. 27:32-39.
24. Salomonsson, S., M. V. Jonsson, K. Skarstein, K. A. Brokstad, P. Hjelmström, M. Wahren-Herlenius, and R. Jonsson. 2003. Cellular basis of ectopic germinal center formation and autoantibody production in the target organ of patients with Sjögren's syndrome. Arthritis Rheum. 48:3187-3201.
25. Kaiserling, E. 2001. Newly-formed lymph nodes in the submucosa in chronic inflammatory bowel disease. Lymphology 34:22-29.
26. Houtkamp, M. A., O. J. de Boer, C. M. van der Loos, A. C. van der Wal, and A. E. Becker. 2001. Adventitial infiltrates associated with advanced atherosclerotic plaques: structural organization suggests generation of local humoral immune responses. J. Pathol. 193:263-269.
27. Brusselle, G. G., T. Demoor, K. R. Bracke, C. A. Brandsma, and W. Timens. 2009. Lymphoid follicles in (very) severe COPD: beneficial or harmful? Eur. Respir. J. 34:219-230.
28. Sikkel, M. B., J. K. Quint, P. Mallia, J. A. Wedzicha, and S. L. Johnston. 2008. Respiratory syncytial virus persistence in chronic obstructive pulmonary disease. Pediatr. Infect. Dis. J. 27 (10 Suppl.) S63-S70.
29. Carragher, D. M., J. Rangel-Moreno, and T. D. Randall. 2008. Ectopic lymphoid tissues and local immunity. Semin. Immunol. 20:26-42.
30. Ware, C. F., P. D. Crowe, M. H. Grayson, M. J. Androlewicz, and J. L. Browning. 1992. Expression of surface lymphotoxin and tumor necrosis factor on activated T, B, and natural killer cells. J. Immunol. 149:3881-3888.
31. Doganci, A., T. Eigenbrod, N. Krug, G. T. De Sanctis, M. Hausding, V. J. Erpenbeck, B. Haddad, H. A. Lehr, E. Schmitt, T. Bopp, et al. 2005. The IL-6Ra chain controls lung CD4+CD25+ Treg development and function during allergic airway inflammation in vivo. [Published erratum appears in 2005 J. Clin. Invest. 115:1388.] J. Clin. Invest. 115:313-325.
32. Voo, K. S., Y. H. Wang, F. R. Santori, C. Boggiano, Y. H. Wang, K. Arima, L. Bover, S. Hanabuchi, J. Khalili, E. Marinova, et al. 2009. Identification of IL-17-producing FOXP3+ regulatory T cells in humans. Proc. Natl. Acad. Sci. USA 106:4793-4798.
33. - T cells or are self-induced to become Th17 cells in the absence of exogenous TGF-beta. J. Immunol. 178:6725-6729.
34. He, R., H. Y. Kim, J. Yoon, M. K. Oyoshi, A. MacGinnitie, S. Goya, E. J. Freyschmidt, P. Bryce, A. N. McKenzie, D. T. Umetsu, et al. 2009. Exaggerated IL-17 response to epicutaneous sensitization mediates airway inflammation in the absence of IL-4 and IL-13. J. Allergy Clin. Immunol. 124:761-770.
35. Wilson, R. H., G. S. Whitehead, H. Nakano, M. E. Free, J. K. Kolls, and D. N. Cook. 2009. Allergic sensitization through the airway primes Th17-dependent neutrophilia and airway hyperresponsiveness. Am. J. Respir. Crit. Care Med. 180:720-730.
36. Di Stefano, A., G. Caramori, I. Gnemmi, M. Contoli, C. Vicari, A. Capelli, F. Magno, S. E. D'Anna, A. Zanini, P. Brun, et al. 2009. T helper type 17-related cytokine expression is increased in the bronchial mucosa of stable chronic obstructive pulmonary disease patients. Clin. Exp. Immunol. 157:316-324.
37. Hashimoto, K., B. S. Graham, S. B. Ho, K. B. Adler, R. D. Collins, S. J. Olson, W. Zhou, T. Suzutani, P. W. Jones, K. Goleniewska, et al. 2004. Respiratory syncytial virus in allergic lung inflammation increases Muc5ac and gob-5. Am. J. Respir. Crit. Care Med. 170:306-312.
38. Crowe, C. R., K. Chen, D. A. Pociask, J. F. Alcorn, C. Krivich, R. I. Enelow, T. M. Ross, J. L. Witztum, and J. K. Kolls. 2009. Critical role of IL-17RA in immunopathology of influenza infection. J. Immunol. 183:5301-5310.
39. Moore, M. L., M. H. Chi, C. Luongo, N. W. Lukacs, V. V. Polosukhin, M. M. Huckabee, D. C. Newcomb, U. J. Buchholz, J. E. Crowe, Jr., K. Goleniewska, et al. 2009. A chimeric A2 strain respiratory syncytial virus (RSV) with the fusion protein of RSV strain Line 19 exhibits enhanced viral load, mucus, and airway dysfunction. J. Virol. 83:4185-4194.
40. Rudd, B. D., J. J. Smit, R. A. Flavell, L. Alexopoulou, M. A. Schaller, A. Gruber, A. A. Berlin, and N. W. Lukacs. 2006. Deletion of TLR3 alters the pulmonary immune environment and mucus production during respiratory syncytial virus infection. J. Immunol. 176:1937-1942.
41. Ermers, M. J., B. Hoebee, H. M. Hodemaekers, T. G. Kimman, J. L. Kimpen, and L. Bont. 2007. IL-13 genetic polymorphism identifies children with late wheezing after respiratory syncytial virus infection. J. Allergy Clin. Immunol. 119:1086-1091.
42. Puthothu, B., M. Krueger, J. Forster, and A. Heinzmann. 2006. Association between severe respiratory syncytial virus infection and IL13/IL4 haplotypes. J. Infect. Dis. 193:438-441.
43. Ruckwardt, T. J., K. L. Bonaparte, M. C. Nason, and B. S. Graham. 2009. Regulatory T cells promote early influx of CD8+ T cells in the lungs of respiratory syncytial virus-infected mice and diminish immunodominance disparities. J. Virol. 83:3019-3028.
44. Zheng, Y., A. Chaudhry, A. Kas, P. deRoos, J. M. Kim, T. T. Chu, L. Corcoran, P. Treuting, U. Klein, and A. Y. Rudensky. 2009. Regulatory T-cell suppressor program co-opts transcription factor IRF4 to control T (H) 2 responses. Nature 458:351-356.
45. + regulatory T cells control TH17 responses in a Stat3-dependent manner. Science 326:986-991.