Virus-like particles activate type I interferon pathways to facilitate post-exposure protection against Ebola virus infection

PLoS ONE

Volumn 10, Issue 2, 2015, Pages

  Ayithan, Natarajan ^a,d   Bradfute, Steven B ^b,e   Anthony, Scott M ^b   Stuthman, Kelly S ^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)

^d MEDICAL COLLEGE OF WISCONSIN   (United States)

^e UNIVERSITY OF NEW MEXICO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERFERON; INTERFERON CONSENSUS SEQUENCE BINDING PROTEIN; VIRUS LIKE PARTICLE VACCINE; ALPHA BETA INTERFERON RECEPTOR; IFNAR1 PROTEIN, MOUSE; INTERFERON REGULATORY FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DENDRITIC CELL; EBOLA HEMORRHAGIC FEVER; EBOLA VIRUS; INFLAMMATION; LIVER; MACROPHAGE; MOUSE; NEGATIVE FEEDBACK; NONHUMAN; POST EXPOSURE PROPHYLAXIS; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SPLEEN; VIRUS LIKE AGENT; VIRUS REPLICATION; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; GENETICS; HEMORRHAGIC FEVER, EBOLA; IMMUNOLOGY; METABOLISM;

EBOLA VIRUS; MUS;

ANIMALS; DENDRITIC CELLS; HEMORRHAGIC FEVER, EBOLA; INTERFERON REGULATORY FACTORS; INTERFERON TYPE I; MACROPHAGES; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; POST-EXPOSURE PROPHYLAXIS; RECEPTOR, INTERFERON ALPHA-BETA; SIGNAL TRANSDUCTION; VACCINES, VIRUS-LIKE PARTICLE;

EID: 84923913677     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0118345     Document Type: Article

References (58)

1. Geisbert TW, Young HA, Jahrling PB, Davis KJ, Larsen T, Kagan E, et al. Pathogenesis of Ebola hemorrhagic fever in primate models: evidence that hemorrhage is not a direct effect of virus-induced cytolysis of endothelial cells. Am J Pathol. 2003; 163: 2371-2382. PMID: 14633609
2. Kuhn JH. Filoviruses. A compendium of 40 years of epidemiological, clinical, and laboratory studies. Arch Virol Suppl. 2008; 20: 13-360. PMID: 18637412
3. Bradfute SB, Warfield KL, Bray M. Mouse models for filovirus infections. Viruses. 2012; 4: 1477-1508. doi: 10.3390/v4091477 PMID: 23170168
4. Bray M, Davis K, Geisbert T, Schmaljohn C, Huggins J. A mouse model for evaluation of prophylaxis and therapy of Ebola hemorrhagic fever. J Infect Dis. 1999; 179 Suppl 1: S248-258. PMID: 9988191
5. Gupta M, Mahanty S, Ahmed R, Rollin PE. Monocyte-derived human macrophages and peripheral blood mononuclear cells infected with ebola virus secrete MIP-1alpha and TNF-alpha and inhibit poly-IC-induced IFN-alpha in vitro. Virology. 2001; 284: 20-25. PMID: 11352664
6. Mohamadzadeh M, Chen L, Schmaljohn AL. How Ebola and Marburg viruses battle the immune system. Nat Rev Immunol. 2007; 7: 556-567. PMID: 17589545
7. Basler CF, Amarasinghe GK. Evasion of interferon responses by Ebola and Marburg viruses. J Interferon Cytokine Res. 2009; 29: 511-520. doi: 10.1089/jir.2009.0076 PMID: 19694547
8. Basler CF, Wang X, Muhlberger E, Volchkov V, Paragas J, Klenk HD, et al. The Ebola virus VP35 protein functions as a type I IFN antagonist. Proc Natl Acad Sci USA. 2000; 97: 12289-12294. PMID: 11027311
9. Ebihara H, Takada A, Kobasa D, Jones S, Neumann G, Theriault S, et al. Molecular determinants of Ebola virus virulence in mice. PLoS Pathog. 2006; 2: e73. PMID: 16848640
10. Chang TH, Kubota T, Matsuoka M, Jones S, Bradfute SB, Bray M, et al. Ebola Zaire virus blocks type I interferon production by exploiting the host SUMO modification machinery. PLoS Pathog. 2009; 5: e1000493. doi: 10.1371/journal.ppat.1000493 PMID: 19557165
11. Hartman AL, Ling L, Nichol ST, Hibberd ML. Whole-genome expression profiling reveals that inhibition of host innate immune response pathways by Ebola virus can be reversed by a single amino acid change in the VP35 protein. J Virol. 2008; 82: 5348-5358. doi: 10.1128/JVI.00215-08 PMID: 18353943
12. Hartman AL, Bird BH, Towner JS, Antoniadou ZA, Zaki SR, Nichol ST. Inhibition of IRF-3 activation by VP35 is critical for the high level of virulence of ebola virus. J Virol. 2008; 82: 2699-2704. doi: 10.1128/ JVI.02344-07 PMID: 18199658
13. Raymond J, Bradfute S, Bray M. Filovirus infection of STAT-1 knockout mice. J Infect Dis. 2011; 204 Suppl 3: S986-990. doi: 10.1093/infdis/jir335 PMID: 21987780
14. Lever MS, Piercy TJ, Steward JA, Eastaugh L, Smither SJ, Taylor C, et al. Lethality and pathogenesis of airborne infection with filoviruses in A129 alpha/beta -/- interferon receptor-deficient mice. J Med Microbiol. 2012; 61: 8-15. doi: 10.1099/jmm.0.036210-0 PMID: 21852521
15. Bray M. The role of the Type I interferon response in the resistance of mice to filovirus infection. J Gen Virol. 2001; 82: 1365-1373. PMID: 11369881
16. Wauquier N, Becquart P, Padilla C, Baize S, Leroy EM. Human fatal zaire ebola virus infection is associated with an aberrant innate immunity and with massive lymphocyte apoptosis. PLoS Negl Trop Dis. 2010; 4: e837. doi: 10.1371/journal.pntd.0000837 PMID: 20957152
17. Hutchinson KL, Rollin PE. Cytokine and chemokine expression in humans infected with Sudan Ebola virus. J Infect Dis. 2007; 196 Suppl 2: S357-363. PMID: 17940971
18. Mahanty S, Gupta M, Paragas J, Bray M, Ahmed R, Rollin PE. Protection from lethal infection is determined by innate immune responses in a mouse model of Ebola virus infection. Virology. 2003; 312: 415-424. PMID: 12919746
19. Smith LM, Hensley LE, Geisbert TW, Johnson J, Stossel A, Honko A, et al. Interferon-beta therapy prolongs survival in rhesus macaque models of Ebola and Marburg hemorrhagic fever. J Infect Dis. 2013; 208: 310-318. doi: 10.1093/infdis/jis921 PMID: 23255566
20. Jahrling PB, Geisbert TW, Geisbert JB, Swearengen JR, Bray M, Jaax NK, et al. Evaluation of immune globulin and recombinant interferon-alpha2b for treatment of experimental Ebola virus infections. J Infect Dis. 1999; 179 Suppl 1: S224-234. PMID: 9988188
21. Qiu X, Wong G, Fernando L, Audet J, Bello A, Strong J, et al. mAbs and Ad-Vectored IFN-alpha Therapy Rescue Ebola-Infected Nonhuman Primates When Administered After the Detection of Viremia and Symptoms. Sci Transl Med. 2013; 5: 207ra143. doi: 10.1126/scitranslmed.3006605 PMID: 24132638
22. Hoenen T, Groseth A, Feldmann H. Current ebola vaccines. Expert Opin Biol Ther. 2012; 12: 859-872. doi: 10.1517/14712598.2012.685152 PMID: 22559078
23. Fausther-Bovendo H, Mulangu S, Sullivan NJ. Ebolavirus vaccines for humans and apes. Curr Opin Virol. 2012; 2: 324-329. doi: 10.1016/j.coviro.2012.04.003 PMID: 22560007
24. Feldmann H, Jones SM, Daddario-DiCaprio KM, Geisbert JB, Stroher U, Grolla A, et al. Effective postexposure treatment of Ebola infection. PLoS Pathog. 2007; 3: e2. PMID: 17238284
25. Kushnir N, Streatfield SJ, Yusibov V. Virus-like particles as a highly efficient vaccine platform: diversity of targets and production systems and advances in clinical development. Vaccine. 2012; 31: 58-83. doi: 10.1016/j.vaccine.2012.10.083 PMID: 23142589
26. Yang C, Ye L, Compans RW. Protection against filovirus infection: virus-like particle vaccines. Expert Rev Vaccines. 2008; 7: 333-344. doi: 10.1586/14760584.7.3.333 PMID: 18393603
27. Noda T, Sagara H, Suzuki E, Takada A, Kida H, Kawaoka Y. Ebola virus VP40 drives the formation of virus-like filamentous particles along with GP. J Virol. 2002; 76: 4855-4865. PMID: 11967302
28. Johnson RF, Bell P, Harty RN. Effect of Ebola virus proteins GP, NP and VP35 on VP40 VLP morphology. Virol J. 2006; 3: 31. PMID: 16719918
29. Martinez O, Valmas C, Basler CF. Ebola virus-like particle-induced activation of NF-kappaB and Erk signaling in human dendritic cells requires the glycoprotein mucin domain. Virology. 2007; 364: 342-354. PMID: 17434557
30. Bradfute SB, Anthony SM, Stuthman KS, Ayithan N, Tailor P, Bray M, et al. Mechanisms of immunity in post-infection vaccination against Ebola virus infection. PloS One. 2015; In press. doi: 10.1371/journal. pone.0117162 PMID: 25636061
31. Warfield KL, Olinger G, Deal EM, Swenson DL, Bailey M, Negley DL, et al. Induction of humoral and CD8+ T cell responses are required for protection against lethal Ebola virus infection. J Immunol. 2005; 175: 1184-1191. PMID: 16002721
32. Bradfute SB, Bavari S. Correlates of immunity to filovirus infection. Viruses. 2011; 3: 982-1000. doi: 10.3390/v3070982 PMID: 21994766
33. Ayithan N, Bradfute SB, Anthony SM, Stuthman KS, Dye JM, Bavari S, et al. Ebola virus-like particles stimulate type I interferons and proinflammatory cytokine expression through the toll-like receptor and interferon signaling pathways. J Interferon Cytokine Res. 2014; 34: 79-89. doi: 10.1089/jir.2013.0035 PMID: 24102579
34. Olejnik J, Ryabchikova E, Corley RB, Muhlberger E. Intracellular events and cell fate in filovirus infection. Viruses. 2011; 3: 1501-1531. doi: 10.3390/v3081501 PMID: 21927676
35. O'Brien LM, Stokes MG, Lonsdale SG, Maslowski DR, Smither SJ, Lever MS, et al. Vaccination with recombinant adenoviruses expressing Ebola virus glycoprotein elicits protection in the interferon alpha/ beta receptor knock-out mouse. Virology. 2014; 452-453: 324-333. doi: 10.1016/j.virol.2014.01.012 PMID: 24606709
36. Kawai T, Akira S. TLR signaling. Semin Immunol. 2007; 19: 24-32. PMID: 17275323
37. Bafica A, Feng CG, Santiago HC, Aliberti J, Cheever A. The IFN-inducible GTPase LRG47 (Irgm1) negatively regulates TLR4-triggered proinflammatory cytokine production and prevents endotoxemia. J Immunol. 2007; 179: 5514-5522. PMID: 17911638
38. Malakhova OA, KimKI, Luo JK, ZouW, Kumar KG, Fuchs SY, et al. UBP43 is a novel regulator of interferon signaling independent of its ISG15 isopeptidase activity. EMBO J. 2006; 25: 2358-2367. PMID: 16710296
39. Shi M, Deng W, Bi E, Mao K, Ji Y, Lin G, et al. TRIM30 alpha negatively regulates TLR-mediated NFkappa B activation by targeting TAB2 and TAB3 for degradation. Nat Immunol. 2008; 9: 369-377. doi: 10.1038/ni1577 PMID: 18345001
40. Ozato K, Shin DM, Chang TH, Morse HC. TRIM family proteins and their emerging roles in innate immunity. Nat Rev Immunol. 2008; 8: 849-860. doi: 10.1038/nri2413 PMID: 18836477
41. Yoshimi R, Chang TH, Wang H, Atsumi T, Morse HC, Ozato K. Gene disruption study reveals a nonredundant role for TRIM21/Ro52 in NF-kappaB-dependent cytokine expression in fibroblasts. J Immunol. 2009; 182: 7527-7538. doi: 10.4049/jimmunol.0804121 PMID: 19494276
42. Hu Y, Mao K, Zeng Y, Chen S, Tao Z, Yang C, et al. Tripartite-motif protein 30 negatively regulates NLRP3 inflammasome activation by modulating reactive oxygen species production. J Immunol. 2010; 185: 7699-7705. doi: 10.4049/jimmunol.1001099 PMID: 21048113
43. Bray M, Murphy FA. Filovirus research: knowledge expands to meet a growing threat. J Infect Dis. 2007; 196 Suppl 2: S438-443. PMID: 17940981
44. Billiau A. Anti-inflammatory property of type I interferons. Antiviral Res. 2006; 71: 108-116. PMID: 16626815
45. Guarda G, Braun M, Staehli F, Tardivel A, Mattmann C, Forster I, et al. Type I interferon inhibits interleu-kin-1 production and inflammasome activation. Immunity. 2011; 34: 213-223. doi: 10.1016/j.immuni. 2011.02.006 PMID: 21349431
46. Pinto AK, Ramos HJ, Wu X, Aggarwal S, Shrestha B, Gorman M, et al. Deficient IFN signaling by myeloid cells leads to MAVS-dependent virus-induced sepsis. PLoS Pathog. 2014; 10: e1004086. doi: 10. 1371/journal.ppat.1004086 PMID: 24743949
47. Tamura T, Yanai H, Savitsky D, Taniguchi T. The IRF family transcription factors in immunity and oncogenesis. Annu Rev Immunol. 2008; 26: 535-584. doi: 10.1146/annurev.immunol.26.021607.090400 PMID: 18303999
48. Chang TH, Xu S, Tailor P, Kanno T, Ozato K. The small ubiquitin-like modifier-deconjugating enzyme sentrin-specific peptidase 1 switches IFN regulatory factor 8 from a repressor to an activator during macrophage activation. J Immunol. 2012; 189: 3548-3556. PMID: 22942423
49. Kurotaki D, Osato N, Nishiyama A, Yamamoto M, Ban T, Sato H, et al. Essential role of the IRF8-KLF4 transcription factor cascade in murine monocyte differentiation. Blood. 2013; 121: 1839-1849. doi: 10. 1182/blood-2012-06-437863 PMID: 23319570
50. Alter-Koltunoff M, Goren S, Nousbeck J, Feng CG, Sher A, Ozato K, et al. Innate immunity to intraphagosomal pathogens is mediated by interferon regulatory factor 8 (IRF-8) that stimulates the expression of macrophage-specific Nramp1 through antagonizing repression by c-Myc. J Biol Chem. 2008; 283: 2724-2733. PMID: 18045875
51. Tailor P, Tamura T, Kong HJ, Kubota T, KubotaM, Borghi P, et al. The feedback phase of type I interferon induction in dendritic cells requires interferon regulatory factor 8. Immunity. 2007; 27: 228-239. PMID: 17702615
52. Hambleton S, Salem S, Bustamante J, Bigley V, Boisson-Dupuis S, Azevedo J, et al. IRF8 Mutations and Human Dendritic-Cell Immunodeficiency. N Engl J Med. 2011; 365: 127-138. doi: 10.1056/ NEJMoa1100066 PMID: 21524210
53. Huang IC, Bailey CC, Weyer JL, Radoshitzky SR, Becker MM. Distinct patterns of IFITM-mediated restriction of filoviruses, SARS coronavirus, and influenza A virus. PLoS Pathog. 2011; 7: e1001258. doi: 10.1371/journal.ppat.1001258 PMID: 21253575
54. Geiss GK, Salvatore M, Tumpey TM, Carter VS, Wang X. Cellular transcriptional profiling in influenza A virus-infected lung epithelial cells: the role of the nonstructural NS1 protein in the evasion of the host innate defense and its potential contribution to pandemic influenza. Proc Natl Acad Sci USA. 2002; 99: 10736-10741. PMID: 12149435
55. Thakar J, Schmid S, Duke JL, Garcia-Sastre A, Kleinstein SH. Overcoming NS1-Mediated Immune Antagonism Involves Both Interferon-Dependent and Independent Mechanisms. J Interferon Cytokine Res. 2013; 33: 700-708. doi: 10.1089/jir.2012.0113 PMID: 23772952
56. Yoshimura A, Mori H, Ohishi M, Aki D, Hanada T. Negative regulation of cytokine signaling influences inflammation. Curr Opin Immunol. 2003; 15: 704-708. PMID: 14630206
57. Liew FY, Xu D, Brint EK, O'Neill LA. Negative regulation of toll-like receptor-mediated immune responses. Nat Rev Immunol. 2005; 5: 446-458. PMID: 15928677
58. Yoshimura A, Naka T, Kubo M. SOCS proteins, cytokine signalling and immune regulation. Nat Rev Immunol. 2007; 7: 454-465. PMID: 17525754