Alpha/beta interferon receptor signaling amplifies early proinflammatory cytokine production in the lung during respiratory syncytial virus infection

Journal of Virology

Volumn 88, Issue 11, 2014, Pages 6128-6136

  Goritzka, Michelle ^a   Durant, Lydia R ^a   Pereira, Catherine ^a   Salek Ardakani, Samira ^a   Openshaw, Peter J M ^a   Johansson, Cecilia ^a  

^a NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA BETA INTERFERON RECEPTOR; ALPHA INTERFERON; BETA INTERFERON; CHEMOKINE; CYTOKINE; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERFERON LAMBDA; MESSENGER RNA; PROTEIN; PROTEIN MX 1; RECOMBINANT ALPHA INTERFERON; RETINOIC ACID INDUCIBLE PROTEIN I; TOLL LIKE RECEPTOR AGONIST; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIVIRAL RESISTANCE; ARTICLE; CONTROLLED STUDY; CXCL1 GENE; CXCL10 GENE; CYTOKINE PRODUCTION; DDX58 GENE; EIF2AK2 GENE; FEMALE; GAPDH GENE; GENE; GENE EXPRESSION; IFNB GENE; IFNL2 GENE; IFNL3 GENE; IL1B GENE; IL6 GENE; INNATE IMMUNITY; L GENE; MALE; MOUSE; MX1 GENE; NONHUMAN; OAS1A GENE; PNEUMONIA; PRIORITY JOURNAL; PROTEIN ANALYSIS; RESPIRATORY SYNCYTIAL PNEUMOVIRUS; RESPIRATORY SYNCYTIAL VIRUS INFECTION; RSAD2 GENE; SIGNAL TRANSDUCTION; VIRUS LOAD; WEIGHT REDUCTION;

ANIMALS; CYTOKINES; DNA PRIMERS; GENE EXPRESSION REGULATION; LUNG; MICE; MICE, KNOCKOUT; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTOR, INTERFERON ALPHA-BETA; RESPIRATORY SYNCYTIAL VIRUS INFECTIONS; SIGNAL TRANSDUCTION; STATISTICS, NONPARAMETRIC; VIRAL LOAD;

EID: 84899829425     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00333-14     Document Type: Article

References (48)

1. Randall RE, Goodbourn S. 2008. Interferons and viruses: an interplay between induction, signalling, antiviral responses and virus countermeasures. J. Gen. Virol. 89:1-47. http://dx. doi. org/10. 1099/vir. 0. 83391-0.
2. Durbin RK, Kotenko SV, Durbin JE. 2013. Interferon induction and function at the mucosal surface. Immunol. Rev. 255:25-39. http://dx. doi. org/10. 1111/imr. 12101.
3. González-Navajas JM, Lee J, David M, Raz E. 2012. Immunomodulatory functions of type I interferons. Nat. Rev. Immunol. 12:125-135. http://dx. doi. org/10. 1038/nri3133.
4. Takeuchi O, Akira S. 2009. Innate immunity to virus infection. Immunol. Rev. 227:75-86. http://dx. doi. org/10. 1111/j. 1600-065X. 2008. 00737. x.
5. Kumagai Y, Takeuchi O, Kato H, Kumar H, Matsui K, Morii E, Aozasa K, Kawai T, Akira S. 2007. Alveolar macrophages are the primary interferon-alpha producer in pulmonary infection with RNA viruses. Immunity 27:240-252. http://dx. doi. org/10. 1016/j. immuni. 2007. 07. 013.
6. Kim D, Martinez-Sobrido L, Choi C, Petroff N, García-Sastre A, Niewiesk S, Carsillo T. 2011. Induction of type I interferon secretion through recombinant Newcastle disease virus expressing measles virus hemagglutinin stimulates antibody secretion in the presence of maternal antibodies. J. Virol. 85:200-207. http://dx. doi. org/10. 1128/JVI. 01624-10.
7. Guerrero-Plata A, Casola A, Garofalo RP. 2005. Human metapneumovirus induces a profile of lung cytokines distinct from that of respiratory syncytial virus. J. Virol. 79:14992-14997. http://dx. doi. org/10. 1128/JVI. 79. 23. 14992-14997. 2005.
8. Guerrero-Plata A, Baron S, Poast JS, Adegboyega PA, Casola A, Garofalo RP. 2005. Activity and regulation of alpha interferon in respiratory syncytial virus and human metapneumovirus experimental infections. J. Virol. 79:10190-10199. http://dx. doi. org/10. 1128/JVI. 79. 16. 10190-10199. 2005.
9. Jewell NA, Vaghefi N, Mertz SE, Akter P, Peebles RS, Bakaletz LO, Durbin RK, Flaño E, Durbin JE. 2007. Differential type I interferon induction by respiratory syncytial virus and influenza A virus in vivo. J. Virol. 81:9790-9800. http://dx. doi. org/10. 1128/JVI. 00530-07.
10. Borchers AT, Chang C, Gershwin ME, Gershwin LJ. 2013. Respiratory syncytial virus-a comprehensive review. Clin. Rev. Allergy Immunol. 45:331-379. http://dx. doi. org/10. 1007/s12016-013-8368-9.
11. Janssen R, Bont L, Siezen CLE, Hodemaekers HM, Ermers MJ, Doornbos G, van t Slot R, Wijmenga C, Goeman JJ, Kimpen JLL, van Houwelingen HC, Kimman TG, Hoebee B. 2007. Genetic susceptibility to respiratory syncytial virus bronchiolitis is predominantly associated with innate immune genes. J. Infect. Dis. 196:826-834. http://dx. doi. org/10. 1086/520886.
12. Awomoyi AA, Rallabhandi P, Pollin TI, Lorenz E, Sztein MB, Boukhvalova MS, Hemming VG, Blanco JCG, Vogel SN. 2007. Association of TLR4 polymorphisms with symptomatic respiratory syncytial virus infection in high-risk infants and young children. J. Immunol. 179:3171-3177.
13. Tal G, Mandelberg A, Dalal I, Cesar K, Somekh E, Tal A, Oron A, Itskovich S, Ballin A, Houri S, Beigelman A, Lider O, Rechavi G, Amariglio N. 2004. Association between common Toll-like receptor 4 mutations and severe respiratory syncytial virus disease. J. Infect. Dis. 189:2057-2063. http://dx. doi. org/10. 1086/420830.
14. Tulic MK, Hurrelbrink RJ, Prêle CM, Laing IA, Upham JW, Le Souef P, Sly PD, Holt PG. 2007. TLR4 polymorphisms mediate impaired responses to respiratory syncytial virus and lipopolysaccharide. J. Immunol. 179:132-140.
15. de Weerd NA, Vivian JP, Nguyen TK, Mangan NE, Gould JA, Braniff S-J, Zaker-Tabrizi L, Fung KY, Forster SC, Beddoe T, Reid HH, Rossjohn J, Hertzog PJ. 2013. Structural basis of a unique interferon-β signaling axis mediated via the receptor IFNAR1. Nat. Immunol. 14:901-907. http://dx. doi. org/10. 1038/ni. 2667.
16. Johansson C, Wetzel JD, He J, Mikacenic C, Dermody TS, Kelsall BL. 2007. Type I interferons produced by hematopoietic cells protect mice against lethal infection by mammalian reovirus. J. Exp. Med. 204:1349-1358. http://dx. doi. org/10. 1084/jem. 20061587.
17. Schilte C, Couderc T, Chrétien F, Sourisseau M, Gangneux N, Guivel-Benhassine F, Kraxner A, Tschopp J, Higgs S, Michault A, Arenzana-Seisdedos F, Colonna M, Peduto L, Schwartz O, Lecuit M, Albert ML. 2010. Type I IFN controls chikungunya virus via its action on nonhematopoietic cells. J. Exp. Med. 207:429-442. http://dx. doi. org/10. 1084/jem. 20090851.
18. Seo S-U, Kwon H-J, Ko H-J, Byun Y-H, Seong BL, Uematsu S, Akira S, Kweon M-N. 2011. Type I interferon signaling regulates Ly6C(hi) monocytes and neutrophils during acute viral pneumonia in mice. PLoS Pathog. 7:e1001304. http://dx. doi. org/10. 1371/journal. ppat. 1001304.
19. Johnson TR, Mertz SE, Gitiban N, Hammond S, Legallo R, Durbin RK, Durbin JE. 2005. Role for innate IFNs in determining respiratory syncytial virus immunopathology. J. Immunol. 174:7234-7241.
20. Lee DCP, Harker JAE, Tregoning JS, Atabani SF, Johansson C, Schwarze J, Openshaw PJM. 2010. CD25+ natural regulatory T cells are critical in limiting innate and adaptive immunity and resolving disease following respiratory syncytial virus infection. J. Virol. 84:8790-8798. http://dx. doi. org/10. 1128/JVI. 00796-10.
21. Asselin-Paturel C, Boonstra A, Dalod M, Durand I, Yessaad N, Dezutter-Dambuyant C, Vicari A, O'Garra A, Biron C, Brière F, Trinchieri G. 2001. Mouse type I IFN-producing cells are immature APCs with plasmacytoid morphology. Nat. Immunol. 2:1144-1150. http://dx. doi. org/10. 1038/ni736.
22. Slater L, Bartlett NW, Haas JJ, Zhu J, Message SD, Walton RP, Sykes A, Dahdaleh S, Clarke DL, Belvisi MG, Kon OM, Fujita T, Jeffery PK, Johnston SL, Edwards MR. 2010. Co-ordinated role of TLR3, RIG-I and MDA5 in the innate response to rhinovirus in bronchial epithelium. PLoS Pathog. 6:e1001178. http://dx. doi. org/10. 1371/journal. ppat. 1001178.
23. Bartlett NW, Slater L, Glanville N, Haas JJ, Caramori G, Casolari P, Clarke DL, Message SD, Aniscenko J, Kebadze T, Zhu J, Mallia P, Mizgerd JP, Belvisi M, Papi A, Kotenko SV, Johnston SL, Edwards MR. 2012. Defining critical roles for NF-κB p65 and type I interferon in innate immunity to rhinovirus. EMBO Mol. Med. 4:1244-1260. http://dx. doi. org/10. 1002/emmm. 201201650.
24. Culley FJ, Pollott J, Openshaw PJM. 2002. Age at first viral infection determines the pattern of T cell-mediated disease during reinfection in adulthood. J. Exp. Med. 196:1381-1386. http://dx. doi. org/10. 1084/jem. 20020943.
25. Pribul PK, Harker J, Wang B, Wang H, Tregoning JS, Schwarze J, Openshaw PJM. 2008. Alveolar macrophages are a major determinant of early responses to viral lung infection but do not influence subsequent disease development. J. Virol. 82:4441-4448. http://dx. doi. org/10. 1128/JVI. 02541-07.
26. Honda K, Taniguchi T. 2006. IRFs: master regulators of signalling by Toll-like receptors and cytosolic pattern-recognition receptors. Nat. Rev. Immunol. 6:644-658. http://dx. doi. org/10. 1038/nri1900.
27. Durbin JE, Johnson TR, Durbin RK, Mertz SE, Morotti RA, Peebles RS, Graham BS. 2002. The role of IFN in respiratory syncytial virus pathogenesis. J. Immunol. 168:2944-2952.
28. McNally B, Willette M, Ye F, Partida-Sanchez S, Flaño E. 2012. Intranasal administration of dsRNA analog poly(I:C) induces interferon-α receptordependent accumulation of antigen experienced T cells in the airways. PLoS One 7:e51351. http://dx. doi. org/10. 1371/journal. pone. 0051351.
29. Jewell NA, Cline T, Mertz SE, Smirnov SV, Flaño E, Schindler C, Grieves JL, Durbin RK, Kotenko SV, Durbin JE. 2010. Lambda interferon is the predominant interferon induced by influenzaAvirus infection in vivo. J. Virol. 84:11515-11522. http://dx. doi. org/10. 1128/JVI. 01703-09.
30. Crotta S, Davidson S, Mahlakoiv T, Desmet CJ, Buckwalter MR, Albert ML, Staeheli P, Wack A. 2013. Type I and type III interferons drive redundant amplification loops to induce a transcriptional signature in influenza-infected airway epithelia. PLoS Pathog. 9:e1003773. http://dx. doi. org/10. 1371/journal. ppat. 1003773.
31. Mordstein M, Neugebauer E, Ditt V, Jessen B, Rieger T, Falcone V, Sorgeloos F, Ehl S, Mayer D, Kochs G, Schwemmle M, Günther S, Drosten C, Michiels T, Staeheli P. 2010. Lambda interferon renders epithelial cells of the respiratory and gastrointestinal tracts resistant to viral infections. J. Virol. 84:5670-5677. http://dx. doi. org/10. 1128/JVI. 00272-10.
32. Nguyen KB, Watford WT, Salomon R, Hofmann SR, Pien GC, Morinobu A, Gadina M, O'Shea JJ, Biron CA. 2002. Critical role for STAT4 activation by type 1 interferons in the interferon-gamma response to viral infection. Science 297: 2063-2066. http://dx. doi. org/10. 1126/science. 1074900.
33. Mack EA, Kallal LE, Demers DA, Biron CA. 2011. Type 1 interferon induction of natural killer cell gamma interferon production for defense during lymphocytic choriomeningitis virus infection. mBio 2(4):pii: e00169-11. http://dx. doi. org/10. 1128/mBio. 00169-11.
34. Gough DJ, Messina NL, Hii L, Gould JA, Sabapathy K, Robertson APS, Trapani JA, Levy DE, Hertzog PJ, Clarke CJP, Johnstone RW. 2010. Functional crosstalk between type I and II interferon through the regulated expression of STAT1. PLoS Biol. 8:e1000361. http://dx. doi. org/10. 1371/journal. pbio. 1000361.
35. Kelly-Scumpia KM, Scumpia PO, Delano MJ, Weinstein JS, Cuenca AG, Wynn JL, Moldawer LL. 2010. Type I interferon signaling in hematopoietic cells is required for survival in mouse polymicrobial sepsis by regulating CXCL10. J. Exp. Med. 207:319-326. http://dx. doi. org/10. 1084/jem. 20091959.
36. Gautier G, Humbert M, Deauvieau F, Scuiller M, Hiscott J, Bates EEM, Trinchieri G, Caux C, Garrone P. 2005. A type I interferon autocrineparacrine loop is involved in Toll-like receptor-induced interleukin-12p70 secretion by dendritic cells. J. Exp. Med. 201:1435-1446. http://dx. doi. org/10. 1084/jem. 20041964.
37. Rudd BD, Luker GD, Luker KE, Peebles RS, Lukacs NW. 2007. Type I interferon regulates respiratory virus infected dendritic cell maturation and cytokine production. Viral Immunol. 20:531-540. http://dx. doi. org/10. 1089/vim. 2007. 0057.
38. Pattison MJ, MacKenzie KF, Elcombe SE, Arthur JSC. 2013. IFNb autocrine feedback is required to sustain TLR induced production of MCP-1 in macrophages. FEBS Lett. 587:1496-1503. http://dx. doi. org/10. 1016/j. febslet. 2013. 03. 025.
39. Doughty L, Nguyen K, Durbin J, Biron C. 2001. A role for IFN-alpha beta in virus infection-induced sensitization to endotoxin. J. Immunol. 166:2658-2664. http://www. jimmunol. org/content/166/4/2658. long.
40. Huys L, Van Hauwermeiren F, Dejager L, Dejonckheere E, Lienenklaus S, Weiss S, Leclercq G, Libert C. 2009. Type I interferon drives tumor necrosis factor-induced lethal shock. J. Exp. Med. 206:1873-1882. http://dx. doi. org/10. 1084/jem. 20090213.
41. Majer O, Bourgeois C, Zwolanek F, Lassnig C, Kerjaschki D, Mack M, Müller M, Kuchler K. 2012. Type I interferons promote fatal immunopathology by regulating inflammatory monocytes and neutrophils during Candida infections. PLoS Pathog. 8:e1002811. http://dx. doi. org/10. 1371/journal. ppat. 1002811.
42. Pfeffer LM. 2011. The role of nuclear factor κB in the interferon response. J. Interferon Cytokine Res. 31:553-559. http://dx. doi. org/10. 1089/jir. 2011. 0028.
43. Haeberle HA, Takizawa R, Casola A, Brasier AR, Dieterich H-J, van Rooijen N, Gatalica Z, Garofalo RP. 2002. Respiratory syncytial virusinduced activation of nuclear factor-kappaB in the lung involves alveolar macrophages and toll-like receptor 4-dependent pathways. J. Infect. Dis. 186:1199-1206. http://dx. doi. org/10. 1086/344644.
44. Platanias LC. 2005. Mechanisms of type-I-and type-II-interferonmediated signalling. Nat. Rev. Immunol. 5:375-386. http://dx. doi. org/10. 1038/nri1604.
45. Kelley KW, Bluthé R-M, Dantzer R, Zhou J-H, Shen W-H, Johnson RW, Broussard SR. 2003. Cytokine-induced sickness behavior. Brain Behav. Immun. 17(Suppl 1):S112-S118. http://dx. doi. org/10. 1016/S0889-1591(02)00077-6.
46. Tregoning JS, Yamaguchi Y, Harker J, Wang B, Openshaw PJM. 2008. The role of T cells in the enhancement of respiratory syncytial virus infection severity during adult reinfection of neonatally sensitized mice. J. Virol. 82:4115-4124. http://dx. doi. org/10. 1128/JVI. 02313-07.
47. López CB, Yount JS, Hermesh T, Moran TM. 2006. Sendai virus infection induces efficient adaptive immunity independently of type I interferons. J. Virol. 80:4538-4545. http://dx. doi. org/10. 1128/JVI. 80. 9. 4538-4545. 2006.
48. Wilks J, Beilinson H, Golovkina TV. 2013. Dual role of commensal bacteria in viral infections. Immunol. Rev. 255:222-229. http://dx. doi. org/10. 1111/imr. 12097.