Ebola virus-like particles stimulate Type i interferons and proinflammatory cytokine expression through the toll-like receptor and interferon signaling pathways

Journal of Interferon and Cytokine Research

Volumn 34, Issue 2, 2014, Pages 79-89

  Ayithan, Natarajan ^a   Bradfute, Steven B ^b   Anthony, Scott M ^b   Stuthman, Kelly S ^b   Dye, John M ^b   Bavari, Sina ^b   Bray, Mike ^c   Ozato, Keiko ^a  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b UNITED STATES ARMY MEDICAL RESEARCH INSTITUTE OF INFECTIOUS DISEASES   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; CELLS, CULTURED; CYTOKINES; DENDRITIC CELLS; EBOLAVIRUS; HEMORRHAGIC FEVER, EBOLA; HUMANS; IMMUNITY, INNATE; INFLAMMATION MEDIATORS; INTERFERON TYPE I; MACROPHAGES; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; MYELOID DIFFERENTIATION FACTOR 88; POLY I-C; PRIMATES; RATS; RECEPTOR, INTERFERON ALPHA-BETA; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTORS; VACCINES, VIRUS-LIKE PARTICLE; VIRION;

EID: 84893955319     PISSN: 10799907     EISSN: 15577465     Source Type: Journal    
DOI: 10.1089/jir.2013.0035     Document Type: Article

References (56)

1. Ascenzi P, Bocedi A, Heptonstall J, Capobianchi MR, Di Caro A, Mastrangelo E, Bolognesi M, Ippolito G. 2008. Ebolavirus and Marburgvirus: insight the Filoviridae family. Mol Aspects Med 29(3):151-185.
2. Asselin-Paturel C, Trinchieri G. 2005. Production of type I interferons: plasmacytoid dendritic cells and beyond. J Exp Med 202(4):461-465. (Pubitemid 41186943)
3. Ayithan N, Bradfute SB, Stuthman KS, Anthony SM, Bavari S, Bray M, Ozato K. 2013. VLP post-Ebola infection protects mice via type I IFN signaling mediated negative regulation of inflammatory genes at early time point. (Manuscript to be submitted).
4. Bagchi A, Herrup EA, Warren HS, Trigilio J, Shin HS, Valentine C, Hellman J. 2007. MyD88-dependent and MyD88-independent pathways in synergy, priming, and tolerance between TLR agonists. J Immunol 178(2):1164-1171. (Pubitemid 46095190)
5. Barchet W, Cella M, Odermatt B, Asselin-Paturel C, Colonna M, Kalinke U. 2002. Virus-induced interferon alpha production by a dendritic cell subset in the absence of feedback signaling in vivo. J Exp Med 195(4):507-516. (Pubitemid 34461303)
6. Bavari S, Bosio CM, Wiegand E, Ruthel G, Will AB, Geisbert TW, Hevey M, Schmaljohn C, Schmaljohn A, Aman MJ. 2002. Lipid raft microdomains: a gateway compartmentalized trafficking of Ebola and Marburg Viruses. J Exp Med 195(5):593-602. (Pubitemid 34461504)
7. Beutler BA. 2009. TLRs and innate immunity. Blood 113(7):1399-1407.
8. Bode C, Zhao G, Steinhagen F, Kinjo T, Klinman DM. 2011. CpG DNA as a vaccine adjuvant. Expert Rev Vaccines 10(4):499-511.
9. Bosio CM, Aman MJ, Grogan C, Hogan R, Ruthel G, Negley D, Mohamadzadeh M, Bavari S, Schmaljohn A. 2003. Ebola and Marburg viruses replicate in monocyte-derived dendritic cells without inducing the production of cytokines and full maturation. J Infect Dis 188(11):1630-1638. (Pubitemid 38010672)
10. Bradfute SB, Anthony SM, Stuthman KS, Ayithan N, Tailor P, Bray M, Ozato K, Bavari S. 2013. Mechanisms of immunity in post-infection vaccination against Ebola virus infection. (Manuscript to be submitted).
11. Bray M, Geisbert TW. 2005. Ebola virus: the role of macrophages and dendritic cells in the pathogenesis of Ebola hemorrhagic fever. Int J Biochem Cell Biol 37(8):1560-1566. (Pubitemid 40719635)
12. Bray M, Murphy FA. 2007. Filovirus research: knowledge expands to meet a growing threat. J Infect Dis 196 Suppl 2:S438-S443. (Pubitemid 351417292)
13. Brierley MM, Fish EN. 2002. Review: IFN-alpha/beta receptor interactions to biologic outcomes: understanding the circuitry. J Interferon Cytokine Res 22(8):835-845. (Pubitemid 35217514)
14. Caskey M, Lefebvre F, Filali-Mouhim A, Cameron MJ, Goulet JP, Haddad EK, Breton G, Trumpfheller C, Pollak S, Shimeliovich I, Duque-Alarcon A, Pan L, Nelkenbaum A, Salazar AM, Schlesinger SJ, Steinman RM, Sekaly RP. 2011. Synthetic double-stranded RNA induces innate immune responses similar to a live viral vaccine in humans. J Exp Med 208(12):2357-2366.
15. Chang TH, Kubota T, Matsuoka M, Jones S, Bradfute SB, Bray M, Ozato K. 2009. Ebola Zaire virus blocks type I interferon production by exploiting the host SUMO modification machinery. PLoS Pathog 5(6):e1000493.
16. Darnell JE, Jr., Kerr IM, Stark GR. 1994. Jak-STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins. Science 264(5164):1415-1421. (Pubitemid 24217131)
17. Dunne A, O'Neill LA. 2005. Adaptor usage and Toll-like receptor signaling specificity. FEBS Lett 579(15):3330-3335. (Pubitemid 40804682)
18. Feldmann H, Jones S, Klenk HD, Schnittler HJ. 2003. Ebola virus: from discovery to vaccine. Nat Rev Immunol 3(8):677-685. (Pubitemid 37328670)
19. Honda K, Yanai H, Negishi H, Asagiri M, Sato M, Mizutani T, Shimada N, Ohba Y, Takaoka A, Yoshida N, Taniguchi T. 2005. IRF-7 is the master regulator of type-I interferondependent immune responses. Nature 434(7034):772-777. (Pubitemid 44739521)
20. Hu X, Chakravarty SD, Ivashkiv LB. 2008. Regulation of interferon and Toll-like receptor signaling during macrophage activation by opposing feedforward and feedback inhibition mechanisms. Immunol Rev 226:41-56.
21. Jahrling PB, Geisbert TW, Geisbert JB, Swearengen JR, Bray M, Jaax NK, Huggins JW, LeDuc JW, Peters CJ. 1999. Evaluation of immune globulin and recombinant interferon-alpha2b for treatment of experimental Ebola virus infections. J Infect Dis 179 Suppl 1:S224-S234. (Pubitemid 29091406)
22. Johnson RF, Bell P, Harty RN. 2006. Effect of Ebola virus proteins GP, NP and VP35 on VP40 VLP morphology. Virol J 3:31.
23. Kabelitz D, Medzhitov R. 2007. Innate immunity-cross-talk with adaptive immunity through pattern recognition receptors and cytokines. Curr Opin Immunol 19(1):1-3. (Pubitemid 46091738)
24. Kaletsky RL, Francica JR, Agrawal-Gamse C, Bates P. 2009. Tetherin-mediated restriction of filovirus budding is antagonized by the Ebola glycoprotein. Proc Natl Acad Sci USA 106(8):2886-2891.
25. Kawai T, Adachi O, Ogawa T, Takeda K, Akira S. 1999. Unresponsiveness of MyD88-deficient mice to endotoxin. Immunity 11(1):115-122. (Pubitemid 29359962)
26. Kawai T, Akira S. 2010. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat Immunol 11(5):373-384.
27. Kawai T, Akira S. 2011. Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity 34(5):637-650.
28. Kumar H, Kawai T, Akira S. 2011. Pathogen recognition by the innate immune system. Int Rev Immunol 30(1):16-34.
29. Kwissa M, Kasturi SP, Pulendran B. 2007. The science of adjuvants. Expert Rev Vaccines 6(5):673-684. (Pubitemid 47607845)
30. Longhi MP, Trumpfheller C, Idoyaga J, Caskey M, Matos I, Kluger C, Salazar AM, Colonna M, Steinman RM. 2009. Dendritic cells require a systemic type I interferon response to mature and induce CD4+ Th1 immunity with poly IC as adjuvant. J Exp Med 206(7):1589-1602.
31. Mahanty S, Gupta M, Paragas J, Bray M, Ahmed R, Rollin PE. 2003. Protection from lethal infection is determined by innate immune responses in a mouse model of Ebola virus infection. Virology 312(2):415-424. (Pubitemid 36966080)
32. Martinez O, Valmas C, Basler CF. 2007. Ebola virus-like particleinduced activation of NF-kappaB and Erk signaling in human dendritic cells requires the glycoprotein mucin domain. Virology 364(2):342-354. (Pubitemid 46873712)
33. Napolitani G, Rinaldi A, Bertoni F, Sallusto F, Lanzavecchia A. 2005. Selected Toll-like receptor agonist combinations synergistically trigger a T helper type 1-polarizing program in dendritic cells. Nat Immunol 6(8):769-776. (Pubitemid 43090462)
34. Noda T, Sagara H, Suzuki E, Takada A, Kida H, Kawaoka Y. 2002. Ebola virus VP40 drives the formation of virus-like filamentous particles along with GP. J Virol 76(10):4855-4865. (Pubitemid 34441691)
35. O'Neill LA, Bowie AG. 2007. The family of five: TIR-domaincontaining adaptors in Toll-like receptor signalling. Nat Rev Immunol 7(5):353-364. (Pubitemid 46674493)
36. Okumura A, Pitha PM, Yoshimura A, Harty RN. 2010. Interaction between Ebola virus glycoprotein and host toll-like receptor 4 leads to induction of proinflammatory cytokines and SOCS1. J Virol 84(1):27-33.
37. Paladino P, Cummings DT, Noyce RS, Mossman KL. 2006. The IFN-independent response to virus particle entry provides a first line of antiviral defense that is independent of TLRs and retinoic acid-inducible gene I. J Immunol 177(11):8008-8016. (Pubitemid 44846318)
38. Phoolcharoen W, Dye JM, Kilbourne J, Piensook K, Pratt WD, Arntzen CJ, Chen Q, Mason HS, Herbst-KralovetzMM. 2011. A nonreplicating subunit vaccine protects mice against lethal Ebola virus challenge. Proc Natl Acad Sci USA 108(51):20695-20700.
39. Platanias LC. 2005. Mechanisms of type-I-and type-II-interferon-mediated signalling. Nat Rev Immunol 5(5):375-386.
40. Raymond J, Bradfute S, Bray M. 2011. Filovirus infection of STAT-1 knockout mice. J Infect Dis 204 (Suppl 3):S986-S990.
41. Samuel CE. 2001. Antiviral actions of interferons. Clin Microbiol Rev 14(4):778-809 (Pubitemid 32979631)
42. Schindler C, Levy DE, Decker T. 2007. JAK-STAT signaling: from interferons to cytokines. J Biol Chem 282(28):20059-20063. (Pubitemid 47099977)
43. Schoggins JW, Wilson SJ, Panis M, Murphy MY, Jones CT, Bieniasz P, Rice CM. 2011. A diverse range of gene products are effectors of the type I interferon antiviral response. Nature 472(7344):481-485.
44. Steinman RM, Banchereau J. 2007. Taking dendritic cells into medicine. Nature 449(7161):419-426. (Pubitemid 47509552)
45. Swiecki M, Colonna M. 2010. Unraveling the functions of plasmacytoid dendritic cells during viral infections, autoimmunity, and tolerance. Immunol Rev 234(1):142-162.
46. Tailor P, Tamura T, Kong HJ, Kubota T, Kubota M, Borghi P, Gabriele L, Ozato K. 2007. The feedback phase of type I interferon induction in dendritic cells requires interferon regulatory factor 8. Immunity 27(2):228-239. (Pubitemid 47284921)
47. Tamura T, Tailor P, Yamaoka K, Kong HJ, Tsujimura H, O'Shea JJ, Singh H, Ozato K. 2005. IFN regulatory factor-4 and-8 govern dendritic cell subset development and their functional diversity. J Immunol 174(5):2573-2581. (Pubitemid 40279670)
48. Warfield KL, Aman MJ. 2011. Advances in virus-like particle vaccines for filoviruses. J Infect Dis 204 Suppl 3:S1053-S1059.
49. Warfield KL, Bosio CM, Welcher BC, Deal EM, Mohamadzadeh M, Schmaljohn A, Aman MJ, Bavari S. 2003. Ebola virus-like particles protect from lethal Ebola virus infection. Proc Natl Acad Sci USA 100(26):15889-15894. (Pubitemid 38021085)
50. Warfield KL, Olinger G, Deal EM, Swenson DL, Bailey M, Negley DL, Hart MK, Bavari S. 2005. Induction of humoral and CD8+ T cell responses are required for protection against lethal Ebola virus infection. J Immunol 175(2):1184-1191. (Pubitemid 41095006)
51. Warfield KL, Swenson DL, Olinger GG, Kalina WV, Aman MJ, Bavari S. 2007. Ebola virus-like particle-based vaccine protects nonhuman primates against lethal Ebola virus challenge. J Infect Dis 196 Suppl 2:S430-S437. (Pubitemid 351417291)
52. Warger T, Osterloh P, Rechtsteiner G, Fassbender M, Heib V, Schmid B, Schmitt E, Schild H, Radsak MP. 2006. Synergistic activation of dendritic cells by combined Toll-like receptor ligation induces superior CTL responses in vivo. Blood 108(2):544-550. (Pubitemid 44061354)
53. Weighardt H, Jusek G, Mages J, Lang R, Hoebe K, Beutler B, Holzmann B. 2004. Identification of a TLR4-and TRIF-dependent activation program of dendritic cells. Eur J Immunol 34(2):558-564. (Pubitemid 39255965)
54. Yamamoto M, Sato S, Hemmi H, Hoshino K, Kaisho T, Sanjo H, Takeuchi O, Sugiyama M, Okabe M, Takeda K, Akira S. 2003.Role of adaptor TRIF in the MyD88-independent toll-like receptor signaling pathway. Science 301(5633):640-643. (Pubitemid 36927946)
55. Yamayoshi S, Kawaoka Y. 2007. Mapping of a region of Ebola virus VP40 that is important in the production of virus-like particles. J Infect Dis 196 Suppl 2:S291-S295. (Pubitemid 351417274)
56. Zhu X, Nishimura F, Sasaki K, Fujita M, Dusak JE, Eguchi J, Fellows-Mayle W, Storkus WJ, Walker PR, Salazar AM, Okada H. 2007. Toll like receptor-3 ligand poly-ICLC promotes the efficacy of peripheral vaccinations with tumor antigen-derived peptide epitopes in murine CNS tumor models. J Transl Med 5:10.