IL-17Induced pulmonary pathogenesis during respiratory viral infection and exacerbation of allergic disease

American Journal of Pathology

Volumn 179, Issue 1, 2011, Pages 248-258

  Mukherjee, Sumanta ^a   Lindell, Dennis M ^b   Berlin, Aaron A ^a   Morris, Susan B ^a   Shanley, Thomas P ^a   Hershenson, Marc B ^a   Lukacs, Nicholas W ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b SEATTLE CHILDREN S RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALLERGEN; COCKROACH ALLERGEN; EOMESODERMIN; GAMMA INTERFERON; GRANZYME B; INTERLEUKIN 17; INTERLEUKIN 17 ANTIBODY; INTERLEUKIN 23; INTERLEUKIN 6; RECOMBINANT CYTOKINE; RECOMBINANT INTERLEUKIN 17; TRANSCRIPTION FACTOR T BET; UNCLASSIFIED DRUG; VIRUS PROTEIN; GRANZYME; MESSENGER RNA; MONOCLONAL ANTIBODY;

ALLERGIC REACTION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CD8+ T LYMPHOCYTE; CELL DAMAGE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; CYTOTOXIC T LYMPHOCYTE; DISEASE EXACERBATION; DISEASE SEVERITY; ENZYME LINKED IMMUNOSORBENT ASSAY; EPITHELIUM CELL; FEMALE; HISTOPATHOLOGY; HUMAN; IMMUNOPATHOGENESIS; INFANT; MOUSE; MUCUS SECRETION; NONHUMAN; PRIORITY JOURNAL; RESPIRATORY SYNCYTIAL VIRUS INFECTION; RESPIRATORY TRACT ALLERGY; TH2 CELL; TRACHEAL ASPIRATION PROCEDURE; UPREGULATION; VIRUS LOAD; VIRUS NEUTRALIZATION; ANIMAL; BAGG ALBINO MOUSE; DISEASE MODEL; FLOW CYTOMETRY; GENETICS; HYPERSENSITIVITY; INFLAMMATION; LUNG DISEASE; METABOLISM; MOUSE MUTANT; MUCUS; PATHOGENICITY; PATHOLOGY; PHYSIOLOGY; RESPIRATORY SYNCYTIAL PNEUMOVIRUS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VIROLOGY; WESTERN BLOTTING;

ANIMALS; ANTIBODIES, MONOCLONAL; BLOTTING, WESTERN; CD8-POSITIVE T-LYMPHOCYTES; DISEASE MODELS, ANIMAL; FEMALE; FLOW CYTOMETRY; GRANZYMES; HUMANS; HYPERSENSITIVITY; INFLAMMATION; INTERFERON-GAMMA; INTERLEUKIN-17; INTERLEUKIN-23; LUNG DISEASES; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; MUCUS; RESPIRATORY SYNCYTIAL VIRUS INFECTIONS; RESPIRATORY SYNCYTIAL VIRUSES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; T-LYMPHOCYTES, CYTOTOXIC; VIRAL LOAD; VIRAL PROTEINS;

EID: 80052508971     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2011.03.003     Document Type: Article

References (63)

1. P.J. Openshaw, G.S. Dean, and F.J. Culley Links between respiratory syncytial virus bronchiolitis and childhood asthma: clinical and research approaches Pediatr Infect Dis J 22 2 Suppl 2003 S58 S64 discussion S64S65
2. C.P. Black Systematic review of the biology and medical management of respiratory syncytial virus infection Respir Care 48 2003 209 231 discussion 231233
3. L.G. Stensballe, J.K. Devasundaram, and E.A. Simoes Respiratory syncytial virus epidemics: the ups and downs of a seasonal virus Pediatr Infect Dis J 22 2 Suppl 2003 S21 S32
4. H.S. Jafri, S. Chavez-Bueno, A. Mejias, A.M. Gomez, A.M. Rios, S.S. Nassi, M. Yusuf, P. Kapur, R.D. Hardy, J. Hatfield, B.B. Rogers, K. Krisher, and O. Ramilo Respiratory syncytial virus induces pneumonia, cytokine response, airway obstruction, and chronic inflammatory infiltrates associated with long-term airway hyperresponsiveness in mice J Infect Dis 189 2004 1856 1865
5. J. Schwarze, G. Cieslewicz, E. Hamelmann, A. Joetham, L.D. Shultz, M.C. Lamers, and E.W. Gelfand IL-5 and eosinophils are essential for the development of airway hyperresponsiveness following acute respiratory syncytial virus infection J Immunol 162 1999 2997 3004
6. K.K. Tekkanat, H. Maassab, A. Miller, A.A. Berlin, S.L. Kunkel, and N.W. Lukacs RANTES (CCL5) production during primary respiratory syncytial virus infection exacerbates airway disease Eur J Immunol 32 2002 3276 3284
7. K. Hashimoto, J.E. Durbin, W. Zhou, R.D. Collins, S.B. Ho, J.K. Kolls, P.J. Dubin, Sheller Jr, K. Goleniewska, J.F. O'Neal, S.J. Olson, D. Mitchell, B.S. Graham, and R.S. Peebles Jr Respiratory syncytial virus infection in the absence of STAT 1 results in airway dysfunction, airway mucus, and augmented IL-17 levels J Allergy Clin Immunol 116 2005 550 557
8. S.G. Hymowitz, E.H. Filvaroff, J.P. Yin, J. Lee, L. Cai, P. Risser, M. Maruoka, W. Mao, J. Foster, R.F. Kelley, G. Pan, A.L. Gurney, A.M. de Vos, and M.A. Starovasnik IL-17s adopt a cystine knot fold: structure and activity of a novel cytokine, IL-17F, and implications for receptor binding EMBO J 20 2001 5332 5341
9. M. Kawaguchi, L.F. Onuchic, X.D. Li, D.M. Essayan, J. Schroeder, H.Q. Xiao, M.C. Liu, G. Krishnaswamy, G. Germino, and S.K. Huang Identification of a novel cytokine, ML-1, and its expression in subjects with asthma J Immunol 167 2001 4430 4435
10. N. Hizawa, M. Kawaguchi, S.K. Huang, and M. Nishimura Role of interleukin-17F in chronic inflammatory and allergic lung disease Clin Exp Allergy 36 2006 1109 1114
11. W. Ouyang, J.K. Kolls, and Y. Zheng The biological functions of T helper 17 cell effector cytokines in inflammation Immunity 28 2008 454 467
12. X.O. Yang, S.H. Chang, H. Park, R. Nurieva, B. Shah, L. Acero, Y.H. Wang, K.S. Schluns, R.R. Broaddus, Z. Zhu, and C. Dong Regulation of inflammatory responses by IL-17F J Exp Med 205 2008 1063 1075
13. S. Nakae, Y. Komiyama, A. Nambu, K. Sudo, M. Iwase, I. Homma, K. Sekikawa, M. Asano, and Y. Iwakura Antigen-specific T cell sensitization is impaired in IL-17-deficient mice, causing suppression of allergic cellular and humoral responses Immunity 17 2002 375 387
14. S. Schnyder-Candrian, D. Togbe, I. Couillin, I. Mercier, F. Brombacher, V. Quesniaux, F. Fossiez, B. Ryffel, and B. Schnyder Interleukin-17 is a negative regulator of established allergic asthma J Exp Med 203 2006 2715 2725
15. K. Hashimoto, B.S. Graham, S.B. Ho, K.B. Adler, R.D. Collins, S.J. Olson, W. Zhou, T. Suzutani, P.W. Jones, K. Goleniewska, J.F. O'Neal, and R.S. Peebles Jr Respiratory syncytial virus in allergic lung inflammation increases Muc5ac and gob-5 Am J Respir Crit Care Med 170 2004 306 312
16. K.K. Tekkanat, H. Maassab, A.A. Berlin, P.M. Lincoln, H.L. Evanoff, M.H. Kaplan, and N.W. Lukacs Role of interleukin-12 and stat-4 in the regulation of airway inflammation and hyperreactivity in respiratory syncytial virus infection Am J Pathol 159 2001 631 638
17. W. Al-Ramli, D. Préfontaine, F. Chouiali, J.G. Martin, R. Olivenstein, C. Lemiere, and Q. Hamid T(H)17-associated cytokines (IL-17A and IL-17F) in severe asthma J Allergy Clin Immunol 123 2009 1185 1187
18. X.O. Yang, R. Nurieva, G.J. Martinez, H.S. Kang, Y. Chung, B.P. Pappu, B. Shah, S.H. Chang, K.S. Schluns, S.S. Watowich, X.H. Feng, A.M. Jetten, and C. Dong Molecular antagonism and plasticity of regulatory and inflammatory T cell programs Immunity 29 2008 44 56
19. E.M. Campbell, I.F. Charo, S.L. Kunkel, R.M. Strieter, L. Boring, J. Gosling, and N.W. Lukacs Monocyte chemoattractant protein-1 mediates cockroach allergen-induced bronchial hyperreactivity in normal but not CCR2-/- mice: the role of mast cells J Immunol 163 1999 2160 2167
20. E.M. Campbell, S.L. Kunkel, R.M. Strieter, and N.W. Lukacs Temporal role of chemokines in a murine model of cockroach allergen-induced airway hyperreactivity and eosinophilia J Immunol 161 1998 7047 7053
21. M.L. Moore, 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, J.V. Williams, P.L. Collins, and R.S. Peebles Jr 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 2009 4185 4194
22. M.L. Herlocher, M. Ewasyshyn, S. Sambhara, M. Gharaee-Kermani, D. Cho, J. Lai, M. Klein, and H.F. Maassab Immunological properties of plaque purified strains of live attenuated respiratory syncytial virus (RSV) for human vaccine Vaccine 17 1999 172 181
23. N.W. Lukacs, M.L. Moore, B.D. Rudd, A.A. Berlin, R.D. Collins, S.J. Olson, S.B. Ho, and R.S. Peebles Jr Differential immune responses and pulmonary pathophysiology are induced by two different strains of respiratory syncytial virus Am J Pathol 169 2006 977 986
24. B.D. Rudd, J.J. Smit, R.A. Flavell, L. Alexopoulou, M.A. Schaller, A. Gruber, A.A. Berlin, and N.W. Lukacs Deletion of TLR3 alters the pulmonary immune environment and mucus production during respiratory syncytial virus infection J Immunol 176 2006 1937 1942
25. J.J. Smit, B.D. Rudd, and N.W. Lukacs Plasmacytoid dendritic cells inhibit pulmonary immunopathology and promote clearance of respiratory syncytial virus J Exp Med 203 2006 1153 1159
26. A.L. Miller, C. Gerard, M. Schaller, A.D. Gruber, A.A. Humbles, and N.W. Lukacs Deletion of CCR1 attenuates pathophysiologic responses during respiratory syncytial virus infection J Immunol 176 2006 2562 2567
27. A.L. Miller, T.L. Bowlin, and N.W. Lukacs Respiratory syncytial virus-induced chemokine production: linking viral replication to chemokine production in vitro and in vivo J Infect Dis 189 2004 1419 1430
28. A.E. John, C.J. Gerard, M. Schaller, A.L. Miller, A.A. Berlin, A.A. Humbles, and N.W. Lukacs Respiratory syncytial virus-induced exaggeration of allergic airway disease is dependent upon CCR1-associated immune responses [Erratum appeared in Eur J Immunol 2005;35:3083] Eur J Immunol 35 2005 108 116
29. T. Ito, M. Schaller, C.M. Hogaboam, T.J. Standiford, M. Sandor, N.W. Lukacs, S.W. Chensue, and S.L. Kunkel TLR9 regulates the mycobacteria-elicited pulmonary granulomatous immune response in mice through DC-derived Notch ligand delta-like 4 J Clin Invest 119 2009 33 46
30. L.E. Kallal, A.J. Hartigan, C.M. Hogaboam, M.A. Schaller, and N.W. Lukacs Inefficient lymph node sensitization during respiratory viral infection promotes IL-17-mediated lung pathology J Immunol 185 2010 4137 4147
31. N.W. Lukacs, J.J. Smit, S. Mukherjee, S.B. Morris, G. Nunez, and D.M. Lindell Respiratory virus-induced TLR7 activation controls IL-17-associated increased mucus via IL-23 regulation J Immunol 185 2010 2231 2239
32. C.M. Hogaboam, C.S. Gallinat, D.D. Taub, R.M. Strieter, S.L. Kunkel, and N.W. Lukacs Immunomodulatory role of C10 chemokine in a murine model of allergic bronchopulmonary aspergillosis J Immunol 162 1999 6071 6079
33. N.W. Lukacs, K.K. Tekkanat, A. Berlin, C.M. Hogaboam, A. Miller, H. Evanoff, P. Lincoln, and H. Maassab Respiratory syncytial virus predisposes mice to augmented allergic airway responses via IL-13-mediated mechanisms [Erratum appeared in J Immunol 2005;175:8442] J Immunol 167 2001 1060 1065
34. K.K. Tekkanat, H.F. Maassab, D.S. Cho, J.J. Lai, A. John, A. Berlin, M.H. Kaplan, and N.W. Lukacs IL-13-induced airway hyperreactivity during respiratory syncytial virus infection is STAT6 dependent [Erratum appeared in J Immunol 2005;175:8442] J Immunol 166 2001 3542 3548
35. M. Kumar, A.K. Behera, H. Matsuse, R.F. Lockey, and S.S. Mohapatra Intranasal IFN-gamma gene transfer protects BALB/c mice against respiratory syncytial virus infection Vaccine 18 1999 558 567
36. H. Matsuse, A.K. Behera, M. Kumar, R.F. Lockey, and S.S. Mohapatra Differential cytokine mRNA expression in Dermatophagoides farinae allergen-sensitized and respiratory syncytial virus-infected mice Microbes Infect 2 2000 753 759
37. S.K. Lundy, S.A. Lira, J.J. Smit, D.N. Cook, A.A. Berlin, and N.W. Lukacs Attenuation of allergen-induced responses in CCR6-/- mice is dependent upon altered pulmonary T lymphocyte activation J Immunol 174 2005 2054 2060
38. R. Medzhitov Recognition of microorganisms and activation of the immune response Nature 449 2007 819 826
39. S.Z. Wang, and K.D. Forsyth The interaction of neutrophils with respiratory epithelial cells in viral infection Respirology 5 2000 1 10
40. C.T. Weaver, R.D. Hatton, P.R. Mangan, and L.E. Harrington IL-17 family cytokines and the expanding diversity of effector T cell lineages Annu Rev Immunol 25 2007 821 852
41. M.A. Schaller, L.E. Kallal, and N.W. Lukacs A key role for CC chemokine receptor 1 in T-cell-mediated respiratory inflammation Am J Pathol 172 2008 386 394
42. R.C. Welliver Review of epidemiology and clinical risk factors for severe respiratory syncytial virus (RSV) infection J Pediatr 143 5 Suppl 2003 S112 S117
43. F.D. Martinez Respiratory syncytial virus bronchiolitis and the pathogenesis of childhood asthma Pediatr Infect Dis J 22 2 Suppl 2003 S76 S82
44. R.A. Tripp, C. Oshansky, and R. Alvarez Cytokines and respiratory syncytial virus infection Proc Am Thorac Soc 2 2005 147 149
45. S.H. Chang, and C. Dong IL-17F: regulation, signaling and function in inflammation Cytokine 46 2009 7 11
46. D.C. Newcomb, W. Zhou, M.L. Moore, K. Goleniewska, G.K. Hershey, J.K. Kolls, and R.S. Peebles Jr A functional IL-13 receptor is expressed on polarized murine CD4+ Th17 cells and IL-13 signaling attenuates Th17 cytokine production J Immunol 182 2009 5317 5321
47. P. Ye, F.H. Rodriguez, S. Kanaly, K.L. Stocking, J. Schurr, P. Schwarzenberger, P. Oliver, W. Huang, P. Zhang, J. Zhang, J.E. Shellito, G.J. Bagby, S. Nelson, K. Charrier, J.J. Peschon, and J.K. Kolls Requirement of interleukin 17 receptor signaling for lung CXC chemokine and granulocyte colony-stimulating factor expression, neutrophil recruitment, and host defense J Exp Med 194 2001 519 527
48. F. Osorio, S. LeibundGut-Landmann, M. Lochner, K. Lahl, T. Sparwasser, G. Eberl, and C. Reis e Sousa DC activated via dectin-1 convert Treg into IL-17 producers Eur J Immunol 38 2008 3274 3281
49. A.V. Chintakuntlawar, and J. Chodosh Chemokine CXCL1/KC and its receptor CXCR2 are responsible for neutrophil chemotaxis in adenoviral keratitis J Interferon Cytokine Res 29 2009 657 666
50. S.M. Vieira, H.P. Lemos, R. Grespan, M.H. Napimoga, D. Dal-Secco, A. Freitas, T.M. Cunha, W.A. Verri Jr, D.A. Souza-Junior, M.C. Jamur, K.S. Fernandes, C. Oliver, J.S. Silva, M.M. Teixeira, and F.Q. Cunha A crucial role for TNF-alpha in mediating neutrophil influx induced by endogenously generated or exogenous chemokines, KC/CXCL1 and LIX/CXCL5 Br J Pharmacol 158 2009 779 789
51. C.R. Crowe, K. Chen, D.A. Pociask, J.F. Alcorn, C. Krivich, R.I. Enelow, T.M. Ross, J.L. Witztum, and J.K. Kolls Critical role of IL-17RA in immunopathology of influenza infection J Immunol 183 2009 5301 5310
52. S. Wiehler, and D. Proud Interleukin-17A modulates human airway epithelial responses to human rhinovirus infection Am J Physiol Lung Cell Mol Physiol 293 2007 L505 L515
53. P. Jaovisidha, M.E. Peeples, A.A. Brees, L.R. Carpenter, and J.N. Moy Respiratory syncytial virus stimulates neutrophil degranulation and chemokine release J Immunol 163 1999 2816 2820
54. R.H. Dougherty, and J.V. Fahy Acute exacerbations of asthma: epidemiology, biology and the exacerbation-prone phenotype Clin Exp Allergy 39 2009 193 202
55. P.A. Wark, S.L. Johnston, I. Moric, J.L. Simpson, M.J. Hensley, and P.G. Gibson Neutrophil degranulation and cell lysis is associated with clinical severity in virus-induced asthma Eur Respir J 19 2002 68 75
56. W. Hou, H.S. Kang, and B.S. Kim Th17 cells enhance viral persistence and inhibit T cell cytotoxicity in a model of chronic virus infection J Exp Med 206 2009 313 328
57. M. Numasaki, J. Fukushi, M. Ono, S.K. Narula, P.J. Zavodny, T. Kudo, P.D. Robbins, H. Tahara, and M.T. Lotze Interleukin-17 promotes angiogenesis and tumor growth Blood 101 2003 2620 2627
58. E.L. Pearce, A.C. Mullen, G.A. Martins, C.M. Krawczyk, A.S. Hutchins, V.P. Zediak, M. Banica, C.B. DiCioccio, D.A. Gross, C.A. Mao, H. Shen, N. Cereb, S.Y. Yang, T. Lindsten, J. Rossant, C.A. Hunter, and S.L. Reiner Control of effector CD8+ T cell function by the transcription factor eomesodermin Science 302 2003 1041 1043
59. A.M. Intlekofer, A. Banerjee, N. Takemoto, S.M. Gordon, C.S. Dejong, H. Shin, C.A. Hunter, E.J. Wherry, T. Lindsten, and S.L. Reiner Anomalous type 17 response to viral infection by CD8+ T cells lacking T-bet and eomesodermin Science 321 2008 408 411
60. M. Ramaswamy, D.J. Groskreutz, and D.C. Look Recognizing the importance of respiratory syncytial virus in chronic obstructive pulmonary disease COPD 6 2009 64 75
61. N.W. Johnston The similarities and differences of epidemic cycles of chronic obstructive pulmonary disease and asthma exacerbations Proc Am Thorac Soc 4 2007 591 596
62. A.R. Falsey Respiratory syncytial virus infection in adults Semin Respir Crit Care Med 28 2007 171 181
63. R.C. Welliver RSV and chronic asthma Lancet 346 1995 789 790