Respiratory syncytial virus infection induces a subset of types I and III interferons in human dendritic cells

Virology

Volumn 504, Issue , 2017, Pages 63-72

  Hillyer, Philippa ^a   Mane, Viraj P ^a   Chen, Aaron ^a   dos Santos, Maria B ^a   Schramm, Lynnsie M ^a   Shepard, Rachel E ^a   Luongo, Cindy ^b   Le Nouën, Cyril ^b   Huang, Lei ^a   Yan, Lihan ^a   Buchholz, Ursula J ^b   Jubin, Ronald G ^c   Collins, Peter L ^b   Rabin, Ronald L ^a  

^a CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^c PBL Interferon Source   (United States)

Author keywords

Bronchial epithelial cell; Dendritic cell; Innate immunity; Interferon; Interferon stimulated gene; Interferon subtype; Respiratory syncytial virus

Indexed keywords

ALPHA1 INTERFERON; ALPHA14 INTERFERON; ALPHA2 INTERFERON; ALPHA21 INTERFERON; ALPHA8 INTERFERON; BETA INTERFERON; GAMMA INTERFERON; INTERFERON; INTERFERON TYPE III; UNCLASSIFIED DRUG; ALPHA INTERFERON; CYTOKINE;

ARTICLE; BRONCHUS EPITHELIUM; CONTROLLED STUDY; DENDRITIC CELL; DISEASE SEVERITY; EPITHELIUM CELL; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN RESPIRATORY SYNCYTIAL VIRUS; PROTEIN EXPRESSION; RESPIRATORY SYNCYTIAL VIRUS INFECTION; VIRUS STRAIN; ADULT; BRONCHUS; CELL CULTURE; CYTOLOGY; IMMUNOLOGY; INFLAMMATION; LUNG; METABOLISM; PATHOLOGY; RESPIRATORY MUCOSA; SECRETION (PROCESS); VIROLOGY;

ADULT; BRONCHI; CELLS, CULTURED; CYTOKINES; DENDRITIC CELLS; EPITHELIAL CELLS; HUMANS; INFLAMMATION; INTERFERON-ALPHA; INTERFERON-BETA; LUNG; RESPIRATORY MUCOSA; RESPIRATORY SYNCYTIAL VIRUS INFECTIONS; RESPIRATORY SYNCYTIAL VIRUS, HUMAN;

EID: 85010850351     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2017.01.017     Document Type: Article

References (49)

1. Barik, S., Respiratory syncytial virus mechanisms to interfere with type 1 interferons. Curr. Top. Microbiol. Immunol. 372 (2013), 173–191.
2. Bartz, H., Turkel, O., Hoffjan, S., Rothoeft, T., Gonschorek, A., Schauer, U., Respiratory syncytial virus decreases the capacity of myeloid dendritic cells to induce interferon-gamma in naive T cells. Immunology 109 (2003), 49–57.
3. Benjamini, Y., Hochberg, Y., Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B (Methodol.), 1995, 289–300.
4. Bolen, C.R., Ding, S., Robek, M.D., Kleinstein, S.H., Dynamic expression profiling of type I and type III interferon-stimulated hepatocytes reveals a stable hierarchy of gene expression. Hepatology 59 (2014), 1262–1272.
5. Chanock, R., Roizman, B., Myers, R., Recovery from infants with respiratory illness of a virus related to chimpanzee coryza agent (CCA). I. Isolation, properties and characterization. Am. J. Hyg. 66 (1957), 281–290.
6. Chi, B., Dickensheets, H.L., Spann, K.M., Alston, M.A., Luongo, C., Dumoutier, L., Huang, J., Renauld, J.C., Kotenko, S.V., Roederer, M., Beeler, J.A., Donnelly, R.P., Collins, P.L., Rabin, R.L., Alpha and lambda interferon together mediate suppression of CD4 T cells induced by respiratory syncytial virus. J. Virol. 80 (2006), 5032–5040.
7. de Graaff, P.M., de Jong, E.C., van Capel, T.M., van Dijk, M.E., Roholl, P.J., Boes, J., Luytjes, W., Kimpen, J.L., van Bleek, G.M., Respiratory syncytial virus infection of monocyte-derived dendritic cells decreases their capacity to activate CD4 T cells. J. Immunol. 175 (2005), 5904–5911.
8. Dickensheets, H.L., Venkataraman, C., Schindler, U., Donnelly, R.P., Interferons inhibit activation of STAT6 by interleukin 4 in human monocytes by inducing SOCS-1 gene expression. Proc. Natl. Acad. Sci. USA 96 (1999), 10800–10805.
9. Durbin, J.E., Johnson, T.R., Durbin, R.K., Mertz, S.E., Morotti, R.A., Peebles, R.S., Graham, B.S., The role of IFN in respiratory syncytial virus pathogenesis. J. Immunol. 168 (2002), 2944–2952.
10. Essayan, D.M., Krishnaswamy, G., Oriente, A., Lichtenstein, L.M., Huang, S.K., Differential regulation of antigen-induced IL-4 and IL-13 generation from T lymphocytes by IFN-alpha. J. Allergy Clin. Immunol. 103 (1999), 451–457.
11. Fukuyama, S., Nakano, T., Matsumoto, T., Oliver, B.G., Burgess, J.K., Moriwaki, A., Tanaka, K., Kubo, M., Hoshino, T., Tanaka, H., McKenzie, A.N., Matsumoto, K., Aizawa, H., Nakanishi, Y., Yoshimura, A., Black, J.L., Inoue, H., Pulmonary suppressor of cytokine signaling-1 induced by IL-13 regulates allergic asthma phenotype. Am. J. Respir. Crit. Care Med. 179 (2009), 992–998.
12. Genin, P., Vaccaro, A., Civas, A., The role of differential expression of human interferon—a genes in antiviral immunity. Cytokine Growth Factor Rev. 20 (2009), 283–295.
13. Gill, M.A., Bajwa, G., George, T.A., Dong, C.C., Dougherty, I.I., Jiang, N., Gan, V.N., Gruchalla, R.S., Counterregulation between the Fcepsilon RI pathway and antiviral responses in human plasmacytoid dendritic cells. J. Immunol. 184 (2010), 5999–6006.
14. Guerrero-Plata, A., Casola, A., Suarez, G., Yu, X., Spetch, L., Peeples, M.E., Garofalo, R.P., Differential response of dendritic cells to human metapneumovirus and respiratory syncytial virus. Am. J. Respir. Cell Mol. Biol. 34 (2006), 320–329.
15. Hebenstreit, D., Luft, P., Schmiedlechner, A., Duschl, A., Horejs-Hoeck, J., SOCS-1 and SOCS-3 inhibit IL-4 and IL-13 induced activation of Eotaxin-3/CCL26 gene expression in HEK293 cells. Mol. Immunol. 42 (2005), 295–303.
16. Hebenstreit, D., Luft, P., Schmiedlechner, A., Regl, G., Frischauf, A.M., Aberger, F., Duschl, A., Horejs-Hoeck, J., IL-4 and IL-13 induce SOCS-1 gene expression in A549 cells by three functional STAT6-binding motifs located upstream of the transcription initiation site. J. Immunol. 171 (2003), 5901–5907.
17. Herlocher, M.L., Ewasyshyn, M., Sambhara, S., Gharaee-Kermani, M., Cho, D., Lai, J., Klein, M., Maassab, H.F., Immunological properties of plaque purified strains of live attenuated respiratory syncytial virus (RSV) for human vaccine. Vaccine 17 (1999), 172–181.
18. Hillyer, P., Mane, V.P., Schramm, L.M., Puig, M., Verthelyi, D., Chen, A., Zhao, Z., Navarro, M.B., Kirschman, K.D., Bykadi, S., Jubin, R.G., Rabin, R.L., Expression profiles of human interferon-alpha and interferon-lambda subtypes are ligand- and cell-dependent. Immunol. Cell Biol. 90 (2012), 774–783.
19. Hillyer, P., Raviv, N., Gold, D.M., Dougherty, D., Liu, J., Johnson, T.R., Graham, B.S., Rabin, R.L., Subtypes of type I IFN differentially enhance cytokine expression by suboptimally stimulated CD4 T cells. Eur. J. Immunol., 2013.
20. Holt, P.G., Pulmonary dendritic cells in local immunity to inert and pathogenic antigens in the respiratory tract. Proc. Am. Thorac. Soc. 2 (2005), 116–120.
21. Hotard, A.L., Lee, S., Currier, M.G., Crowe, J.E. Jr., Sakamoto, K., Newcomb, D.C., Peebles, R.S. Jr., Plemper, R.K., Moore, M.L., Identification of residues in the human respiratory syncytial virus fusion protein that modulate fusion activity and pathogenesis. J. Virol. 89 (2015), 512–522.
22. Huber, J.P., Ramos, H.J., Gill, M.A., Farrar, J.D., Cutting edge: Type I IFN reverses human Th2 commitment and stability by suppressing GATA3. J. Immunol. 185 (2010), 813–817.
23. Jilg, N., Lin, W., Hong, J., Schaefer, E.A., Wolski, D., Meixong, J., Goto, K., Brisac, C., Chusri, P., Fusco, D.N., Chevaliez, S., Luther, J., Kumthip, K., Urban, T.J., Peng, L.F., Lauer, G.M., Chung, R.T., Kinetic differences in the induction of interferon stimulated genes by interferon-alpha and interleukin 28B are altered by infection with hepatitis C virus. Hepatology 59 (2014), 1250–1261.
24. Johnson, J.E., Gonzales, R.A., Olson, S.J., Wright, P.F., Graham, B.S., The histopathology of fatal untreated human respiratory syncytial virus infection. Mod. Pathol. 20 (2007), 108–119.
25. Lavoie, T.B., Kalie, E., Crisafulli-Cabatu, S., Abramovich, R., DiGioia, G., Moolchan, K., Pestka, S., Schreiber, G., Binding and activity of all human alpha interferon subtypes. Cytokine 56 (2011), 282–289.
26. Lazear, H.M., Nice, T.J., Diamond, M.S., Interferon-lambda: immune functions at barrier surfaces and beyond. Immunity 43 (2015), 15–28.
27. Le Nouen, C., Munir, S., Losq, S., Winter, C.C., McCarty, T., Stephany, D.A., Holmes, K.L., Bukreyev, A., Rabin, R.L., Collins, P.L., Buchholz, U.J., Infection and maturation of monocyte-derived human dendritic cells by human respiratory syncytial virus, human metapneumovirus, and human parainfluenza virus type 3. Virology 385 (2009), 169–182.
28. Lewis, F.A., Rae, M.L., Lehmann, N.I., Ferris, A.A., A syncytial virus associated with epidemic disease of the lower respiratory tract in infants and young children. Med. J. Aust., 2, 1961, 932.
29. Lotz, M.T., Moore, M.L., Peebles, R.S. Jr., Respiratory syncytial virus and reactive airway disease. Curr. Top. Microbiol. Immunol. 372 (2013), 105–118.
30. Lukacs, N.W., Moore, M.L., Rudd, B.D., Berlin, A.A., Collins, R.D., Olson, S.J., Ho, S.B., Peebles, R.S. Jr., Differential immune responses and pulmonary pathophysiology are induced by two different strains of respiratory syncytial virus. Am. J. Pathol. 169 (2006), 977–986.
31. Mane, V.P., Heuer, M.A., Hillyer, P., Navarro, M.B., Rabin, R.L., Systematic method for determining an ideal housekeeping gene for real-time PCR analysis. J. Biomol. Tech. 19 (2008), 342–347.
32. Melero, J.A., Moore, M.L., Influence of respiratory syncytial virus strain differences on pathogenesis and immunity. Curr. Top. Microbiol. Immunol. 372 (2013), 59–82.
33. Moore, M.L., Chi, M.H., Luongo, C., Lukacs, N.W., Polosukhin, V.V., Huckabee, M.M., Newcomb, D.C., Buchholz, U.J., Crowe, J.E. Jr., Goleniewska, K., Williams, J.V., Collins, P.L., Peebles, R.S. Jr., 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 (2009), 4185–4194.
34. Mordstein, M., Neugebauer, E., Ditt, V., Jessen, B., Rieger, T., Falcone, V., Sorgeloos, F., Ehl, S., Mayer, D., Kochs, G., Schwemmle, M., Gunther, S., Drosten, C., Michiels, T., Staeheli, P., Lambda interferon renders epithelial cells of the respiratory and gastrointestinal tracts resistant to viral infections. J. Virol. 84 (2010), 5670–5677.
35. Munir, S., Le Nouen, C., Luongo, C., Buchholz, U.J., Collins, P.L., Bukreyev, A., Nonstructural proteins 1 and 2 of respiratory syncytial virus suppress maturation of human dendritic cells. J. Virol. 82 (2008), 8780–8796.
36. Novatt, H., Theisen, T.C., Massie, T., Simonyan, V., Voskanian-Kordi, A., Renn, L.A., Rabin, R.L., Distinct patterns of expression of transcription factors in response to Interferon beta and Interferon lambda-1. J. Interferon Cytokine Res. 36 (2016), 589–598.
37. O'Brien, T.R., Prokunina-Olsson, L., Donnelly, R.P., IFN-lambda4: the paradoxical new member of the interferon lambda family. J. Interferon Cytokine Res. 34 (2014), 829–838.
38. Okabayashi, T., Kojima, T., Masaki, T., Yokota, S., Imaizumi, T., Tsutsumi, H., Himi, T., Fujii, N., Sawada, N., Type-III interferon, not type-I, is the predominant interferon induced by respiratory viruses in nasal epithelial cells. Virus Res. 160 (2011), 360–366.
39. Schandene, L., Del Prete, G.F., Cogan, E., Stordeur, P., Crusiaux, A., Kennes, B., Romagnani, S., Goldman, M., Recombinant interferon-alpha selectively inhibits the production of interleukin-5 by human CD4+ T cells. J. Clin. Invest. 97 (1996), 309–315.
40. Schoggins, J.W., Wilson, S.J., Panis, M., Murphy, M.Y., Jones, C.T., Bieniasz, P., Rice, C.M., A diverse range of gene products are effectors of the type I interferon antiviral response. Nature 472 (2011), 481–485.
41. Schreiber, G., Piehler, J., The molecular basis for functional plasticity in type I interferon signaling. Trends Immunol. 36 (2015), 139–149.
42. Selvaggi, C., Pierangeli, A., Fabiani, M., Spano, L., Nicolai, A., Papoff, P., Moretti, C., Midulla, F., Antonelli, G., Scagnolari, C., Interferon lambda 1-3 expression in infants hospitalized for RSV or HRV associated bronchiolitis. J. Infect. 68 (2014), 467–477.
43. Sommereyns, C., Paul, S., Staeheli, P., Michiels, T., IFN-lambda (IFN-lambda) is expressed in a tissue-dependent fashion and primarily acts on epithelial cells in vivo. PLoS Pathog., 4, 2008, e1000017.
44. Spann, K.M., Tran, K.C., Chi, B., Rabin, R.L., Collins, P.L., Suppression of the induction of alpha, beta, and lambda interferons by the NS1 and NS2 proteins of human respiratory syncytial virus in human epithelial cells and macrophages [corrected]. J. Virol. 78 (2004), 4363–4369.
45. Stokes, K.L., Chi, M.H., Sakamoto, K., Newcomb, D.C., Currier, M.G., Huckabee, M.M., Lee, S., Goleniewska, K., Pretto, C., Williams, J.V., Hotard, A., Sherrill, T.P., Peebles, R.S. Jr., Moore, M.L., Differential pathogenesis of respiratory syncytial virus clinical isolates in BALB/c mice. J. Virol. 85 (2011), 5782–5793.
46. Teach, S.J., Gill, M.A., Togias, A., Sorkness, C.A., Arbes, S.J. Jr., Calatroni, A., Wildfire, J.J., Gergen, P.J., Cohen, R.T., Pongracic, J.A., Kercsmar, C.M., Khurana Hershey, G.K., Gruchalla, R.S., Liu, A.H., Zoratti, E.M., Kattan, M., Grindle, K.A., Gern, J.E., Busse, W.W., Szefler, S.J., Preseasonal treatment with either omalizumab or an inhaled corticosteroid boost to prevent fall asthma exacerbations. J. Allergy Clin. Immunol. 136 (2015), 1476–1485.
47. Voigt, E.A., Yin, J., Kinetic differences and synergistic antiviral effects between type I and type III interferon signaling indicate pathway independence. J. Interferon Cytokine Res., 2015.
48. Witte, K., Gruetz, G., Volk, H.D., Looman, A.C., Asadullah, K., Sterry, W., Sabat, R., Wolk, K., Despite IFN-lambda receptor expression, blood immune cells, but not keratinocytes or melanocytes, have an impaired response to type III interferons: implications for therapeutic applications of these cytokines. Genes Immun. 10 (2009), 702–714.
49. Zaritsky, L.A., Bedsaul, J.R., Zoon, K.C., Virus multiplicity of infection affects type I interferon subtype induction profiles and interferon-stimulated genes. J. Virol. 89 (2015), 11534–11548.