Control of pathogenic effector T-cell activities in situ by PD-L1 expression on respiratory inflammatory dendritic cells during respiratory syncytial virus infection

Mucosal Immunology

Volumn 8, Issue 4, 2015, Pages 746-759

  Yao, S ^a   Jiang, L ^a   Moser, E K ^b   Jewett, L B ^a   Wright, J ^b   Du, J ^a   Zhou, B ^a   Davis, S D ^a   Krupp, N L ^a   Braciale, T J ^b   Sun, J ^a  

^a INDIANA UNIVERSITY   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERFERON; INTERFERON REGULATORY FACTOR 1; INTERLEUKIN 10; PROGRAMMED DEATH 1 LIGAND 1; PROGRAMMED DEATH 1 RECEPTOR; STAT1 PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVITY; CELL INFILTRATION; CLINICAL ARTICLE; CONTROLLED STUDY; DENDRITIC CELL; DISEASE COURSE; EFFECTOR CELL; HUMAN; HUMAN CELL; IMMUNE RESPONSE; MOUSE; NONHUMAN; PNEUMONIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REGULATORY T LYMPHOCYTE; RESPIRATORY SYNCYTIAL VIRUS INFECTION; SIGNAL TRANSDUCTION; VIRUS PATHOGENESIS; ANIMAL; ANTAGONISTS AND INHIBITORS; DISEASE MODEL; GENE EXPRESSION; GENETICS; HOST PATHOGEN INTERACTION; HUMAN RESPIRATORY SYNCYTIAL VIRUS; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; PATHOLOGY; T LYMPHOCYTE SUBPOPULATION;

ANIMALS; ANTIGENS, CD274; DENDRITIC CELLS; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; GENE EXPRESSION; HOST-PATHOGEN INTERACTIONS; HUMANS; INTERFERON REGULATORY FACTOR-1; INTERFERONS; LYMPHOCYTE ACTIVATION; MICE; PROGRAMMED CELL DEATH 1 RECEPTOR; RESPIRATORY SYNCYTIAL VIRUS INFECTIONS; RESPIRATORY SYNCYTIAL VIRUSES; STAT1 TRANSCRIPTION FACTOR; T-LYMPHOCYTE SUBSETS;

EID: 84932628981     PISSN: 19330219     EISSN: 19353456     Source Type: Journal    
DOI: 10.1038/mi.2014.106     Document Type: Article

References (55)

1. Smyth R.L. & Openshaw P.J. Bronchiolitis. Lancet 368, 312-322 (2006
2. Falsey A.R., Hennessey P.A., Formica M.A., Cox C. & Walsh E.E. Respiratory syncytial virus infection in elderly and high-risk adults. N. Engl. J. Med. 352, 1749-1759 (2005
3. Graham B.S., Johnson T.R. & Peebles R.S. Immune-mediated disease pathogenesis in respiratory syncytial virus infection. Immunopharmacology 48, 237-247 (2000
4. Peebles R.S. Jr & raham B.S. Pathogenesis of respiratory syncytial virus infection in the murine model. Proc. Am. Thorac. Soc. 2, 110-115 (2005
5. Bennett B.L., et al. Immunopathogenesis of respiratory syncytial virus bronchiolitis. J. Infect. Dis. 195, 1532-1540 (2007
6. Miyairi I. & DeVincenzo J.P. Human genetic factors and respiratory syncytial virus disease severity. Clin. Microbiol. Rev. 21, 686-703 (2008
7. Oshansky C.M., Zhang W., Moore E. & Tripp R.A. The host response and molecular pathogenesis associated with respiratory syncytial virus infection. Future Microbiol. 4, 279-297 (2009
8. Malley R., et al. Reduction of respiratory syncytial virus (RSV) in tracheal aspirates in intubated infants by use of humanized monoclonal antibody to RSV F protein. J. Infect. Dis. 178, 1555-1561 (1998
9. Collins P.L. & Graham B.S. Viral and host factors in human respiratory syncytial virus pathogenesis. J. Virol. 82, 2040-2055 (2008
10. Ruckwardt T.J., Bonaparte K.L., Nason M.C. & Graham B.S. 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 (2009
11. Fulton R.B., Meyerholz D.K. & Varga S.M. Foxp3+ CD4regulatory Tcells limit pulmonary immunopathology by modulating the CD8 T cell response during respiratory syncytial virus infection. J. Immunol. 185, 2382-2392 (2010
12. Lee D.C., et al. CD25+ natural regulatory Tcells are critical in limiting innate and adaptive immunity and resolving disease following respiratory syncytial virus infection. J. Virol. 84, 8790-8798 (2010
13. Loebbermann J., et al. Regulatory T cells expressing granzyme B play a critical role in controlling lung inflammation during acute viral infection. Mucosal Immunol. 5, 161-172 (2012
14. Loebbermann J., et al. IL-10 regulates viral lung immunopathology during acute respiratory syncytial virus infection in mice. PLoS One 7, e32371 (2012
15. Weiss K.A., Christiaansen A.F., Fulton R.B., Meyerholz D.K. & Varga S.M. Multiple CD4+ T cell subsets produce immunomodulatory IL-10 during respiratory syncytial virus infection. J. Immunol. 187, 3145-3154 (2011
16. Sun J., et al. Autocrine regulation of pulmonary inflammation by effector T-cell derived IL-10 during infection with respiratory syncytial virus. PLoS Pathog. 7, e1002173 (2011
17. Gentile D.A., et al. Cytokine gene polymorphisms moderate illness severity in infants with respiratory syncytial virus infection. Hum. Immunol. 64, 338-344 (2003
18. Hoebee B., et al. Influence of promoter variants of interleukin-10, interleukin-9, and tumor necrosis factor-alpha genes on respiratory syncytial virus bronchiolitis. J. Infect. Dis. 189, 239-247 (2004
19. Francisco L.M., Sage P.T. & Sharpe A.H. The PD-1 pathway in tolerance and autoimmunity. Immunol. Rev. 236, 219-242 (2010
20. Barber D.L., et al. Restoring function in exhausted CD8 T cells during chronic viral infection. Nature 439, 682-687 (2006
21. Virgin H.W., Wherry E.J. & Ahmed R. Redefining chronic viral infection. Cell 138, 30-50 (2009
22. Wherry E.J. T cell exhaustion. Nat. Immunol. 12, 492-499 (2011
23. Brown K.E., Freeman G.J., Wherry E.J. & Sharpe A.H. Role of PD-1 in regulating acute infections. Curr. Opin. Immunol. 22, 397-401 (2010
24. Erickson J.J., et al. Viral acute lower respiratory infections impair CD8+ T cells through PD-1. J. Clin. Invest. 122, 2967-2982 (2012
25. McNally B., Ye F., Willette M. & Flano E. Local blockade of epithelial PDL- 1 in the airways enhances T cell function and viral clearance during influenza virus infection. J. Virol. 87, 12916-12924 (2013
26. Rutigliano J.A., et al. Highly pathological influenza A virus infection is associated with augmented expression of PD-1 by functionally compromised virus-specific CD8+ T cells. J. Virol. 88, 1636-1651 (2014
27. Telcian A.G., et al. RSV-induced bronchial epithelial cell PD-L1 expression inhibits CD8+ Tcell nonspecific antiviral activity. J. Infect. Dis. 203, 85-94 (2011
28. Goldberg M.V., et al. Role of PD-1 and its ligand, B7-H1, in early fate decisions of CD8 T cells. Blood 110, 186-192 (2007
29. Crowe C.R., et al. Critical role of IL-17RA in immunopathology of influenza infection. J. Immunol. 183, 5301-5310 (2009
30. Polack F.P., et al. A role for immune complexes in enhanced respiratory syncytial virus disease. J. Exp. Med. 196, 859-865 (2002
31. Delgado M.F., et al. Lack of antibody affinity maturation due to poor Toll-like receptor stimulation leads to enhanced respiratory syncytial virus disease. Nat. Med. 15, 34-41 (2009
32. Crotty S. Follicular helper CD4 T cells (TFH). Annu. Rev. Immunol. 29, 621-663 (2011
33. Lambrecht B.N. & Hammad H. Lung dendritic cells in respiratory viral infection and asthma: from protection to immunopathology. Annu. Rev. Immunol. 30, 243-270 (2012
34. Hespel C. & Moser M. Role of inflammatory dendritic cells in innate and adaptive immunity. Eur. J. Immunol. 42, 2535-2543 (2012
35. Hufford M.M., Kim T.S., Sun J. & Braciale T.J. Antiviral CD8+ T cell effector activities in situ are regulated by target cell type. J. Exp. Med. 208, 167-180 (2011
36. Yamazaki T., et al. Expression of programmed death 1 ligands by murine T cells and APC. J. Immunol. 169, 5538-5545 (2002
37. Schreiner B., et al. Interferon-beta enhances monocyte and dendritic cell expression of B7-H1 (PD-L1), a strong inhibitor of autologous T-cell activation: relevance for the immune modulatory effect in multiple sclerosis. J. Neuroimmunol. 155, 172-182 (2004
38. Au-Yeung N., Mandhana R. & Horvath C.M. Transcriptional regulation by STAT1 and STAT2 in the interferon JAK-STAT pathway. JAKSTAT 2, e23931 (2013
39. Lee S.J., et al. Interferon regulatory factor-1 is prerequisite to the constitutive expression and IFN-gamma-induced upregulation of B7- H1 (CD274). FEBS Lett. 580, 755-762 (2006
40. Matsuyama T., et al. Targeted disruption of IRF-1 or IRF-2 results in abnormal type I IFN gene induction and aberrant lymphocyte development. Cell 75, 83-97 (1993
41. Shin H., et al. A role for the transcriptional repressor Blimp-1 in CD8(+) T cell exhaustion during chronic viral infection. Immunity 31, 309-320 (2009
42. Utzschneider D.T., et al. T cells maintain an exhausted phenotype after antigen withdrawal and population reexpansion. Nat. Immunol. 14, 603-610 (2013
43. Wilson J., et al. Genetic variation at the IL10 gene locus is associated with severity of respiratory syncytial virus bronchiolitis. J. Infect. Dis. 191, 1705-1709 (2005
44. Singh A.K., Stock P. & Akbari O. Role of PD-L1 and PD-L2 in allergic diseases and asthma. Allergy 66, 155-162 (2011
45. Lukacs N.W., et al. Differential immune responses and pulmonary pathophysiology are induced by two different strains of respiratory syncytial virus. Am. J. Pathol. 169, 977-986 (2006
46. Stokes K.L., et al. Differential pathogenesis of respiratory syncytial virus clinical isolates in BALB/c mice. J. Virol. 85, 5782-5793 (2011
47. Ostler T., Davidson W. & Ehl S. Virus clearance and immunopathology by CD8(+) Tcells during infectionwith respiratory syncytial virus are mediated by IFN-gamma. Eur. J. Immunol. 32, 2117-2123 (2002
48. Rutigliano J.A. & Graham B.S. Prolonged production of TNF-alpha exacerbates illness during respiratory syncytial virus infection. J. Immunol. 173, 3408-3417 (2004
49. Braciale T.J., Sun J. & Kim T.S. Regulating the adaptive immune response to respiratory virus infection. Nat. Rev. Immunol. 12, 295-305 (2012
50. Valitutti S., Muller S., Dessing M. & Lanzavecchia A. Different responses are elicited in cytotoxic T lymphocytes by different levels of T cell receptor occupancy. J. Exp. Med. 183, 1917-1921 (1996
51. Moore M.L., et al. A chimeric A2 strain of 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 (2009
52. Sun J., Dodd H., Moser E.K., Sharma R. & Braciale T.J. CD4+ T cell help and innate-derived IL-27 induceBlimp-1-dependent IL-10 production by antiviral CTLs. Nat. Immunol. 12, 327-334 (2011
53. Sun J., Madan R., Karp C.L. & Braciale T.J. Effector T cells control lung inflammation during acute influenza virus infection by producing IL-10. Nat. Med. 15, 277-284 (2009
54. Sun J. & Pearce E.J. Suppression of early IL-4 production underlies the failure of CD4 T cells activated by TLR-stimulated dendritic cells to differentiate into Th2 cells. J. Immunol. 178, 1635-1644 (2007
55. Sun J., Krawczyk C.J. & Pearce E.J. Suppression of Th2 cell development by Notch ligands Delta1 and Delta4. J. Immunol. 180, 1655-1661 (2008