The toll-like receptor 4 antagonist eritoran protects mice from lethal filovirus challenge

mBio

Volumn 8, Issue 2, 2017, Pages

  Younan, Patrick ^a,b   Ramanathan, Palaniappan ^a,b   Graber, Jessica ^b   Gusovsky, Fabian ^c   Bukreyeva, Alexander ^a,b  

^a University of Texas Medical Branch School of Medicine   (United States)

^b UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

^c EISAI INC   (United States)

Author keywords

Cytokine storm; Ebola virus; Marburg virus; Toll like receptor 4; Viral hemorrhagic fever

Indexed keywords

COLONY STIMULATING FACTOR 1; CXCL2 CHEMOKINE; CXCL9 CHEMOKINE; ERITORAN; FREE RADICAL; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GRANULOCYTE COLONY STIMULATING FACTOR; HYDROGEN PEROXIDE; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 4; INTERLEUKIN 6; INTERLEUKIN 7; INTERLEUKIN 9; LEUKEMIA INHIBITORY FACTOR; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; NITRIC OXIDE; PEROXY RADICAL; PEROXYNITRITE ANION; PLACEBO; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; CYTOKINE; DISACCHARIDE; IMMUNOLOGIC FACTOR; SUGAR PHOSPHATE; TLR4 PROTEIN, MOUSE; TOLL LIKE RECEPTOR 4;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL SURVIVAL; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RESPONSE; CYTOKINE STORM; DISEASE SEVERITY; EBOLA HEMORRHAGIC FEVER; FLOW CYTOMETRY; GRANULOCYTOSIS; HEMATOPOIETIC STEM CELL; LETHALITY; LYMPHOCYTOPENIA; MARBURG HEMORRHAGIC FEVER; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SURVIVAL; T LYMPHOCYTE SUBPOPULATION; VIREMIA; ANIMAL; ANTAGONISTS AND INHIBITORS; BLOOD; DISEASE MODEL; SURVIVAL ANALYSIS; TREATMENT OUTCOME;

ANIMALS; CYTOKINES; DISACCHARIDES; DISEASE MODELS, ANIMAL; HEMORRHAGIC FEVER, EBOLA; IMMUNOLOGIC FACTORS; MARBURG VIRUS DISEASE; MICE; SUGAR PHOSPHATES; SURVIVAL ANALYSIS; TOLL-LIKE RECEPTOR 4; TREATMENT OUTCOME;

EID: 85019080255     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00226-17     Document Type: Article

References (37)

1. CDC. 2016. Outbreaks chronology: Ebola virus disease. CDC, Atlanta, GA. https://www.cdc.gov/vhf/ebola/outbreaks/history/chronology.html.
2. CDC. 2016. Outbreak of Ebola in Guinea, Liberia, and Sierra Leone. CDC, Atlanta, GA. https://www.cdc.gov/vhf/ebola/outbreaks/2014-west-africa/ index.html.
3. Kilgore PE, Grabenstein JD, Salim AM, Rybak M. 2015. Treatment of Ebola virus disease. Pharmacotherapy 35:43-53. https://doi.org/10.1002/phar.1545.
4. Bray M, Mahanty S. 2003. Ebola hemorrhagic fever and septic shock. J Infect Dis 188:1613-1617. https://doi.org/10.1086/379727.
5. Hellman J. 2015. Addressing the complications of Ebola and other viral hemorrhagic fever infections: using insights from bacterial and fungal sepsis. PLo S Pathog 11:e1005088. https://doi.org/10.1371/journal.ppat.1005088.
6. Falasca L, Agrati C, Petrosillo N, Di Caro A, Capobianchi MR, Ippolito G, Piacentini M. 2015. Molecular mechanisms of Ebola virus pathogenesis: focus on cell death. Cell Death Differ 22:1250-1259. https://doi.org/10.1038/cdd.2015.67.
7. Feldmann H, Geisbert TW. 2011. Ebola haemorrhagic fever. Lancet 377: 849-862. https://doi.org/10.1016/S0140-6736(10)60667-8.
8. Marcinkiewicz J, Bryniarski K, Nazimek K. 2014. Ebola haemorrhagic fever virus: pathogenesis, immune responses, potential prevention. Folia Med Cracov 54:39-48.
9. Low DE. 2013. Toxic shock syndrome: major advances in pathogenesis, but not treatment. Crit Care Clin 29:651-675. https://doi.org/10.1016/j.ccc.2013.03.012.
10. Beutler B, Rietschel ET. 2003. Innate immune sensing and its roots: the story of endotoxin. Nat Rev Immunol 3:169-176. https://doi.org/10.1038/nri1004.
11. Hoshino K, Takeuchi O, Kawai T, Sanjo H, Ogawa T, Takeda Y, Takeda K, Akira S. 1999. Cutting edge: Toll-like receptor 4 (TLR4)-deficient mice are hyporesponsive to lipopolysaccharide: evidence for TLR4 as the Lps gene product. J Immunol 162:3749-3752.
12. Imai Y, Kuba K, Neely GG, Yaghubian-Malhami R, Perkmann T, van Loo G, Ermolaeva M, Veldhuizen R, Leung YH, Wang H, Liu H, Sun Y, Pasparakis M, Kopf M, Mech C, Bavari S, Peiris JS, Slutsky AS, Akira S, Hultqvist M, Holmdahl R, Nicholls J, Jiang C, Binder CJ, Penninger JM. 2008. Identification of oxidative stress and Toll-like receptor 4 signaling as a key pathway of acute lung injury. Cell 133:235-249. https://doi.org/10.1016/ j.cell.2008.02.043.
13. Shirey KA, Lai W, Scott AJ, Lipsky M, Mistry P, Pletneva LM, Karp CL, Mc Alees J, Gioannini TL, Weiss J, Chen WH, Ernst RK, Rossignol DP, Gusovsky F, Blanco JC, Vogel SN. 2013. The TLR4 antagonist eritoran protects mice from lethal influenza infection. Nature 497:498-502. https://doi.org/10.1038/nature12118.
14. Kim HM, Park BS, Kim JI, Kim SE, Lee J, Oh SC, Enkhbayar P, Matsushima N, Lee H, Yoo OJ, Lee JO. 2007. Crystal structure of the TLR4-MD-2 complex with bound endotoxin antagonist eritoran. Cell 130:906-917. https://doi.org/10.1016/j.cell.2007.08.002.
15. 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 84:27-33. https://doi.org/10.1128/JVI.01462-09.
16. Escudero-Pérez B, Volchkova VA, Dolnik O, Lawrence P, Volchkov VE. 2014. Shed GP of Ebola virus triggers immune activation and increased vascular permeability. PLo S Pathog 10:e1004509. https://doi.org/10.1371/journal.ppat.1004509.
17. Bray M, Davis K, Geisbert T, Schmaljohn C, Huggins J. 1999. A mouse model for evaluation of prophylaxis and therapy of Ebola hemorrhagic fever. J Infect Dis 179(Suppl 1):S248-S258. https://doi.org/10.1086/ 514292.
18. Mohamadzadeh M, Chen L, Schmaljohn AL. 2007. How Ebola and Marburg viruses battle the immune system. Nat Rev Immunol 7:556-567. https://doi.org/10.1038/nri2098.
19. Lukacs NW, Hogaboam C, Campbell E, Kunkel SL. 1999. Chemokines: function, regulation and alteration of inflammatory responses. Chem Immunol 72:102-120.
20. Metcalfe SM. 2011. LIF in the regulation of T-cell fate and as a potential therapeutic. Genes Immun 12:157-168. https://doi.org/10.1038/gene.2011.9.
21. Hensley LE, Young HA, Jahrling PB, Geisbert TW. 2002. Proinflammatory response during Ebola virus infection of primate models: possible involvement of the tumor necrosis factor receptor superfamily. Immunol Lett 80:169-179. https://doi.org/10.1016/S0165-2478(01)00327-3.
22. Surbatovic M, Popovic N, Vojvodic D, Milosevic I, Acimovic G, Stojicic M, Veljovic M, Jevdjic J, Djordjevic D, Radakovic S. 2015. Cytokine profile in severe Gram-positive and Gram-negative abdominal sepsis. Sci Rep 5:11355. https://doi.org/10.1038/srep11355.
23. Baize S, Leroy EM, Georges AJ, Georges-Courbot MC, Capron M, Bedjabaga I, Lansoud-Soukate J, Mavoungou E. 2002. Inflammatory responses in Ebola virus-infected patients. Clin Exp Immunol 128:163-168. https://doi.org/10.1046/j.1365-2249.2002.01800.x.
24. Vaure C, Liu Y. 2014. A comparative review of toll-like receptor 4 expression and functionality in different animal species. Front Immunol 5:316. https://doi.org/10.3389/fimmu.2014.00316.
25. Roger T, Froidevaux C, Le Roy D, Reymond MK, Chanson AL, Mauri D, Burns K, Riederer BM, Akira S, Calandra T. 2009. Protection from lethal gramnegative bacterial sepsis by targeting Toll-like receptor 4. Proc Natl Acad Sci U S A 106:2348-2352. https://doi.org/10.1073/pnas.0808146106.
26. Alves-Filho JC, Spiller F, Cunha FQ. 2010. Neutrophil paralysis in sepsis. Shock 34(Suppl 1):15-21. https://doi.org/10.1097/SHK.0b013e31 81e7e61b.
27. Blüml S, Kirchberger S, Bochkov VN, Krönke G, Stuhlmeier K, Majdic O, Zlabinger GJ, Knapp W, Binder BR, Stöckl J, Leitinger N. 2005. Oxidized phospholipids negatively regulate dendritic cell maturation induced by TLRs and CD40. J Immunol 175:501-508. https://doi.org/10.4049/ jimmunol.175.1.501.
28. Bochkov VN, Kadl A, Huber J, Gruber F, Binder BR, Leitinger N. 2002. Protective role of phospholipid oxidation products in endotoxininduced tissue damage. Nature 419:77-81. https://doi.org/10.1038/ nature01023.
29. Bretscher P, Egger J, Shamshiev A, Trötzmüller M, Köfeler H, Carreira EM, Kopf M, Freigang S. 2015. Phospholipid oxidation generates potent anti-inflammatory lipid mediators that mimic structurally related proresolving eicosanoids by activating Nrf2. EMBO Mol Med 7:593-607. https://doi.org/10.15252/emmm.201404702.
30. Bwaka MA, Bonnet MJ, Calain P, Colebunders R, De Roo A, Guimard Y, Katwiki KR, Kibadi K, Kipasa MA, Kuvula KJ, Mapanda BB, Massamba M, Mupapa KD, Muyembe-Tamfum JJ, Ndaberey E, Peters CJ, Rollin PE, Van den Enden E. 1999. Ebola hemorrhagic fever in Kikwit, Democratic Republic of the Congo: clinical observations in 103 patients. J Infect Dis 179(Suppl 1):S1-S7. https://doi.org/10.1086/514308.
31. Griffiths A, Hayhurst A, Davey R, Shtanko O, Carrion R, Jr, Patterson JL. 2013. Ebola virus infection, chapter 24, p 435-449. In Singh SK, Ruzek D (ed), Viral hemorrhagic fevers. CRC Press, Boca Raton, FL.
32. Sullivan NJ, Sanchez A, Rollin PE, Yang ZY, Nabel GJ. 2000. Development of a preventive vaccine for Ebola virus infection in primates. Nature 408:605-609. https://doi.org/10.1038/35046108.
33. Reed DS, Lackemeyer MG, Garza NL, Sullivan LJ, Nichols DK. 2011. Aerosol exposure to Zaire ebolavirus in three nonhuman primate species: differences in disease course and clinical pathology. Microbes Infect 13:930-936. https://doi.org/10.1016/j.micinf.2011.05.002.
34. Qiu X, Audet J, Wong G, Pillet S, Bello A, Cabral T, Strong JE, Plummer F, Corbett CR, Alimonti JB, Kobinger GP. 2012. Successful treatment of Ebola virus-infected cynomolgus macaques with monoclonal antibodies. Sci Transl Med 4:138ra81. https://doi.org/10.1126/scitranslmed.3003876.
35. Aziz M, Jacob A, Yang WL, Matsuda A, Wang P. 2013. Current trends in inflammatory and immunomodulatory mediators in sepsis. J Leukoc Biol 93:329-342. https://doi.org/10.1189/jlb.0912437.
36. Ferguson NR, Galley HF, Webster NR. 1999. T helper cell subset ratios in patients with severe sepsis. Intensive Care Med 25:106-109. https://doi.org/10.1007/s001340050795.
37. Warfield KL, Alves DA, Bradfute SB, Reed DK, Van Tongeren S, Kalina WV, Olinger GG, Bavari S. 2007. Development of a model for marburgvirus based on severe-combined immunodeficiency mice. Virol J 4:108. https://doi.org/10.1186/1743-422X-4-108.