A Systems Approach Reveals MAVS Signaling in Myeloid Cells as Critical for Resistance to Ebola Virus in Murine Models of Infection

Cell Reports

Volumn 18, Issue 3, 2017, Pages 816-829

  Dutta, Mukta ^a   Robertson, Shelly J ^b   Okumura, Atsushi ^a,b,c   Scott, Dana P ^b   Chang, Jean ^a   Weiss, Jeffrey M ^a   Sturdevant, Gail L ^b   Feldmann, Friederike ^b   Haddock, Elaine ^b   Chiramel, Abhilash I ^b   Ponia, Sanket S ^b   Dougherty, Jonathan D ^b   Katze, Michael G ^a   Rasmussen, Angela L ^a,c   Best, Sonja M ^b  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

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

^c Department of Medicine   (United States)

Author keywords

conditional; Ebola virus; interferon; knockout; macrophages; MAVS; mouse adapted; RLR

Indexed keywords

ALPHA INTERFERON; MEMBRANE RECEPTOR; MITOCHONDRIAL ANTIVIRAL SIGNALING PROTEIN; MITOCHONDRIAL PROTEIN; RETINOIC ACID INDUCIBLE PROTEIN I; RIG I LIKE RECEPTOR; UNCLASSIFIED DRUG; INTERFERON; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW CELL; CELL DEATH; CONTROLLED STUDY; DISEASE CONTROL; EBOLAVIRUS; GENE DELETION; HOST RESISTANCE; INFLAMMATION; LIVER; MACROPHAGE; MALE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SPLEEN; VIRUS REPLICATION; VIRUS RESISTANCE; VIRUS TRANSCRIPTION; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CYTOLOGY; DISEASE MODEL; EBOLA HEMORRHAGIC FEVER; GENETICS; HUMAN; IMMUNOLOGY; KAPLAN MEIER METHOD; KNOCKOUT MOUSE; METABOLISM; MORTALITY; PATHOLOGY; PHYSIOLOGY; VIROLOGY;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; DEAD BOX PROTEIN 58; DISEASE MODELS, ANIMAL; EBOLAVIRUS; HEMORRHAGIC FEVER, EBOLA; HUMANS; INTERFERON TYPE I; KAPLAN-MEIER ESTIMATE; LIVER; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYELOID CELLS; SIGNAL TRANSDUCTION; SPLEEN; VIRUS REPLICATION;

EID: 85009810416     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2016.12.069     Document Type: Article

References (37)

1. Albariño, C.G., Wiggleton Guerrero, L., Lo, M.K., Nichol, S.T., Towner, J.S., Development of a reverse genetics system to generate a recombinant Ebola virus Makona expressing a green fluorescent protein. Virology 484 (2015), 259–264.
2. Bradfute, S.B., Braun, D.R., Shamblin, J.D., Geisbert, J.B., Paragas, J., Garrison, A., Hensley, L.E., Geisbert, T.W., Lymphocyte death in a mouse model of Ebola virus infection. J. Infect. Dis. 196:Suppl 2 (2007), S296–S304.
3. Bradfute, S.B., Warfield, K.L., Bray, M., Mouse models for filovirus infections. Viruses 4 (2012), 1477–1508.
4. Bray, M., The role of the Type I interferon response in the resistance of mice to filovirus infection. J. Gen. Virol. 82 (2001), 1365–1373.
5. Chakrabarti, A., Banerjee, S., Franchi, L., Loo, Y.M., Gale, M. Jr., Núñez, G., Silverman, R.H., RNase L activates the NLRP3 inflammasome during viral infections. Cell Host Microbe 17 (2015), 466–477.
6. Dixit, E., Boulant, S., Zhang, Y., Lee, A.S., Odendall, C., Shum, B., Hacohen, N., Chen, Z.J., Whelan, S.P., Fransen, M., et al. Peroxisomes are signaling platforms for antiviral innate immunity. Cell 141 (2010), 668–681.
7. Ebihara, H., Takada, A., Kobasa, D., Jones, S., Neumann, G., Theriault, S., Bray, M., Feldmann, H., Kawaoka, Y., Molecular determinants of Ebola virus virulence in mice. PLoS Pathog., 2, 2006, e73.
8. Feldmann, H., Geisbert, T.W., Ebola haemorrhagic fever. Lancet 377 (2011), 849–862.
9. Feng, Z., Cerveny, M., Yan, Z., He, B., The VP35 protein of Ebola virus inhibits the antiviral effect mediated by double-stranded RNA-dependent protein kinase PKR. J Virol. 81 (2007), 182–192.
10. Geisbert, T.W., Hensley, L.E., Larsen, T., Young, H.A., Reed, D.S., Geisbert, J.B., Scott, D.P., Kagan, E., Jahrling, P.B., Davis, K.J., Pathogenesis of Ebola hemorrhagic fever in cynomolgus macaques: evidence that dendritic cells are early and sustained targets of infection. Am. J. Pathol. 163 (2003), 2347–2370.
11. Gibb, T.R., Bray, M., Geisbert, T.W., Steele, K.E., Kell, W.M., Davis, K.J., Jaax, N.K., Pathogenesis of experimental Ebola Zaire virus infection in BALB/c mice. J. Comp. Pathol. 125 (2001), 233–242.
12. Gitlin, L., Benoit, L., Song, C., Cella, M., Gilfillan, S., Holtzman, M.J., Colonna, M., Melanoma differentiation-associated gene 5 (MDA5) is involved in the innate immune response to Paramyxoviridae infection in vivo. PLoS Pathog., 6, 2010, e1000734.
13. Hartman, A.L., Bird, B.H., Towner, J.S., Antoniadou, Z.A., Zaki, S.R., Nichol, S.T., Inhibition of IRF-3 activation by VP35 is critical for the high level of virulence of ebola virus. J. Virol. 82 (2008), 2699–2704.
14. Heng, T.S., Painter, M.W., Immunological Genome Project Consortium. The Immunological Genome Project: networks of gene expression in immune cells. Nat. Immunol. 9 (2008), 1091–1094.
15. Hoogeboom, R., Tolar, P., Molecular mechanisms of B cell antigen gathering and endocytosis. Curr. Top. Microbiol. Immunol. 393 (2016), 45–63.
16. Kumagai, Y., Takeuchi, O., Kato, H., Kumar, H., Matsui, K., Morii, E., Aozasa, K., Kawai, T., Akira, S., Alveolar macrophages are the primary interferon-alpha producer in pulmonary infection with RNA viruses. Immunity 27 (2007), 240–252.
17. Kumar, S., Ingle, H., Mishra, S., Mahla, R.S., Kumar, A., Kawai, T., Akira, S., Takaoka, A., Raut, A.A., Kumar, H., IPS-1 differentially induces TRAIL, BCL2, BIRC3 and PRKCE in type I interferons-dependent and -independent anticancer activity. Cell Death Dis., 6, 2015, e1758.
18. Lazear, H.M., Pinto, A.K., Ramos, H.J., Vick, S.C., Shrestha, B., Suthar, M.S., Gale, M. Jr., Diamond, M.S., Pattern recognition receptor MDA5 modulates CD8+ T cell-dependent clearance of West Nile virus from the central nervous system. J. Virol. 87 (2013), 11401–11415.
19. Leung, L.W., Martinez, O., Reynard, O., Volchkov, V.E., Basler, C.F., Ebola virus failure to stimulate plasmacytoid dendritic cell interferon responses correlates with impaired cellular entry. J. Infect. Dis. 204:Suppl 3 (2011), S973–S977.
20. Leung, L.W., Park, M.S., Martinez, O., Valmas, C., López, C.B., Basler, C.F., Ebolavirus VP35 suppresses IFN production from conventional but not plasmacytoid dendritic cells. Immunol. Cell Biol. 89 (2011), 792–802.
21. Loo, Y.M., Gale, M. Jr., Immune signaling by RIG-I-like receptors. Immunity 34 (2011), 680–692.
22. MacMicking, J.D., Interferon-inducible effector mechanisms in cell-autonomous immunity. Nat. Rev. Immunol. 12 (2012), 367–382.
23. Malakhova, O.A., Zhang, D.E., ISG15 inhibits Nedd4 ubiquitin E3 activity and enhances the innate antiviral response. J Biol Chem. 283 (2008), 8783–8787.
24. Messaoudi, I., Amarasinghe, G.K., Basler, C.F., Filovirus pathogenesis and immune evasion: insights from Ebola virus and Marburg virus. Nat. Rev. Microbiol. 13 (2015), 663–676.
25. Okumura, A., Pitha, P.M., Harty, R.N., ISG15 inhibits Ebola VP40 VLP budding in an L-domain-dependent manner by blocking Nedd4 ligase activity. Proc Natl Acad Sci USA. 105 (2008), 3974–3979.
26. Olagnier, D., Scholte, F.E., Chiang, C., Albulescu, I.C., Nichols, C., He, Z., Lin, R., Snijder, E.J., van Hemert, M.J., Hiscott, J., Inhibition of dengue and chikungunya virus infections by RIG-I-mediated type I interferon-independent stimulation of the innate antiviral response. J. Virol. 88 (2014), 4180–4194.
27. Prins, K.C., Delpeut, S., Leung, D.W., Reynard, O., Volchkova, V.A., Reid, S.P., Ramanan, P., Cárdenas, W.B., Amarasinghe, G.K., Volchkov, V.E., Basler, C.F., Mutations abrogating VP35 interaction with double-stranded RNA render Ebola virus avirulent in guinea pigs. J. Virol. 84 (2010), 3004–3015.
28. Rasmussen, A.L., Okumura, A., Ferris, M.T., Green, R., Feldmann, F., Kelly, S.M., Scott, D.P., Safronetz, D., Haddock, E., LaCasse, R., et al. Host genetic diversity enables Ebola hemorrhagic fever pathogenesis and resistance. Science 346 (2014), 987–991.
29. Raymond, J., Bradfute, S., Bray, M., Filovirus infection of STAT-1 knockout mice. J. Infect. Dis. 204:Suppl 3 (2011), S986–S990.
30. Reid, S.P., Valmas, C., Martinez, O., Sanchez, F.M., Basler, C.F., Ebola virus VP24 proteins inhibit the interaction of NPI-1 subfamily karyopherin alpha proteins with activated STAT1. J. Virol. 81 (2007), 13469–13477.
31. Rhein, B.A., Powers, L.S., Rogers, K., Anantpadma, M., Singh, B.K., Sakurai, Y., Bair, T., Miller-Hunt, C., Sinn, P., Davey, R.A., et al. Interferon-γ Inhibits Ebola Virus Infection. PLoS Pathog., 11, 2015, e1005263.
32. Ruibal, P., Oestereich, L., Lüdtke, A., Becker-Ziaja, B., Wozniak, D.M., Kerber, R., Korva, M., Cabez-Cabrerizo, M., Bore, J.A., Koundouno, F.R., et al. Unique human immune signature of Ebola virus disease in Guinea. Nature 533 (2016), 100–104.
33. Subramanian, N., Natarajan, K., Clatworthy, M.R., Wang, Z., Germain, R.N., The adaptor MAVS promotes NLRP3 mitochondrial localization and inflammasome activation. Cell 153 (2013), 348–361.
34. Sun, Q., Sun, L., Liu, H.H., Chen, X., Seth, R.B., Forman, J., Chen, Z.J., The specific and essential role of MAVS in antiviral innate immune responses. Immunity 24 (2006), 633–642.
35. Suthar, M.S., Brassil, M.M., Blahnik, G., McMillan, A., Ramos, H.J., Proll, S.C., Belisle, S.E., Katze, M.G., Gale, M. Jr., A systems biology approach reveals that tissue tropism to West Nile virus is regulated by antiviral genes and innate immune cellular processes. PLoS Pathog., 9, 2013, e1003168.
36. Swiecki, M., Colonna, M., The multifaceted biology of plasmacytoid dendritic cells. Nat. Rev. Immunol. 15 (2015), 471–485.
37. Wauquier, N., Becquart, P., Padilla, C., Baize, S., Leroy, E.M., Human fatal zaire ebola virus infection is associated with an aberrant innate immunity and with massive lymphocyte apoptosis. PLoS Negl. Trop. Dis., 4, 2010, e837.