The role of cytokines and chemokines in filovirus infection

Viruses

Volumn 7, Issue 10, 2015, Pages 5489-5507

  Bixler, Sandra L ^a   Goff, Arthur J ^a  

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

Author keywords

Chemokine; Cytokine; Ebola; Filovirus; Immunopathology; Marburg

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON; CHEMOKINE; CXCL1 CHEMOKINE; CYTOKINE; EOTAXIN; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; GROWTH FACTOR; INTERLEUKIN 8; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MONOCYTE CHEMOTACTIC PROTEIN 1; PATTERN RECOGNITION RECEPTOR; RANTES; TUMOR NECROSIS FACTOR ALPHA;

ANTIGEN PRESENTATION; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; EBOLA HEMORRHAGIC FEVER; FILOVIRUS INFECTION; HUMAN; IMMUNE RESPONSE; IMMUNOMODULATION; MARBURG HEMORRHAGIC FEVER; NONHUMAN; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; UPREGULATION; VIRUS IMMUNITY; VIRUS TRANSMISSION; VIRUS VIRULENCE; ANIMAL; FILOVIRIDAE; IMMUNOLOGY; PATHOLOGY;

ANIMALS; CYTOKINES; FILOVIRIDAE; FILOVIRIDAE INFECTIONS; HUMANS;

EID: 84945335362     PISSN: None     EISSN: 19994915     Source Type: Journal    
DOI: 10.3390/v7102892     Document Type: Review

References (135)

1. Kuhn, J.H.; Becker, S.; Ebihara, H.; Geisbert, T.W.; Johnson, K.M.; Kawaoka, Y.; Lipkin, W.I.; Negredo, A.I.; Netesov, S.V.; Nichol, S.T. et al. Proposal for a revised taxonomy of the family Filoviridae: Classification, names of taxa and viruses, and virus abbreviations. Arch. Virol. 2010, 155, 2083–2103. [PubMed]
2. Siegert, R.; Shu, H.L.; Slenczka, W.; Peters, D.; Muller, G. On the etiology of an unknown human infection originating from monkeys. Dtsch. Med. Wochenschr. 1967, 92, 2341–2343.[CrossRef] [PubMed]
3. Martini, G.A.; Siegert, R. Marburg Virus Disease; Springer: New York, NY, USA, 1971.
4. Johnson, K.M.; Lange, J.V.; Webb, P.A.; Murphy, F.A. Isolation and partial characterisation of a new virus causing acute haemorrhagic fever in Zaire. Lancet 1977, 1, 569–571.[CrossRef]
5. Report of a WHO/International Study Team. Ebola haemorrhagic fever in Sudan, 1976. Bull. World Health Organ. 1978, 56, 247–270.
6. Burke, J.; Declerq, R. Ebola Haemorrhagic Fever in Zaire, 1976: Report of an International Commission. Bull. World Health Organ. 1978, 56, 271–293.
7. Feldmann, H.; Geisbert, T.W. Ebola haemorrhagic fever. Lancet 2011, 377, 849–862.[CrossRef]
8. Paessler, S.; Walker, D.H. Pathogenesis of the viral hemorrhagic fevers. Annu. Rev. Pathol. 2013, 8, 411–440.[CrossRef] [PubMed]
9. Le Guenno, B.; Formenty, P.; Wyers, M.; Gounon, P.; Walker, F.; Boesch, C. Isolation and partial characterisation of a new strain of Ebola virus. Lancet 1995, 345, 1271–1274.[CrossRef]
10. Centers for Disease Control. Update: Filovirus infection in animal handlers. Morb. Mortal. Wkly. Rep. 1990, 39, 221–221.
11. Sanchez, A.; Khan, A.S.; Zaki, S.R.; Nabel, G.J.; Ksiazek, T.G.; Peters, C.J. Filoviridae: Marburg and Ebola Viruses. In Fields Virology; Knipe, D.M., Howley, P.M., Griffin, D.E., Martin, M.A., Lamb, R.A., Roizman, B., Eds.; Lippincott, Williams & Wilkins: Philadelphia, PA, USA, 2001; Volume 1, pp. 1279–1304.
12. Centers for Disease Control. Ebola virus infection in imported primates—Virginia, 1989. Morb. Mortal. Wkly. Rep. 1989, 38, 831–832.
13. Jahrling, P.B.; Geisbert, T.W.; Dalgard, D.W.; Johnson, E.D.; Ksiazek, T.G.; Hall, W.C.; Peters, C.J. Preliminary report: Isolation of Ebola virus from monkeys imported to USA. Lancet 1990, 335, 502–505.[CrossRef]
14. Ebola Current Situation. Available online: http://apps.who.int/ebola/ (accessed on 16 June 2015).
15. Ebola Outbreak in West Africa. 2014. Available online: http://www.cdc.gov/vhf/ebola/outbreaks/ 2014-west-africa/ (accessed on 16 June 2015).
16. Towner, J.S.; Amman, B.R.; Sealy, T.K.; Carroll, S.A.; Comer, J.A.; Kemp, A.; Swanepoel, R.; Paddock, C.D.; Balinandi, S.; Khristova, M.L. et al. Isolation of genetically diverse Marburg viruses from Egyptian fruit bats. PLoS Pathog. 2009, 5, e1000536.[CrossRef] [PubMed]
17. Amman, B.R.; Carroll, S.A.; Reed, Z.D.; Sealy, T.K.; Balinandi, S.; Swanepoel, R.; Kemp, A.; Erickson, B.R.; Comer, J.A.; Campbell, S. et al. Seasonal pulses of Marburg virus circulation in juvenile Rousettus Aegyptiacus bats coincide with periods of increased risk of human infection. PLoS Pathog. 2012, 8, e1002877.[CrossRef] [PubMed]
18. Leroy, E.M.; Kumulungui, B.; Pourrut, X.; Rouquet, P.; Hassanin, A.; Yaba, P.; Delicat, A.; Paweska, J.T.; Gonzalez, J.P.; Swanepoel, R. Fruit bats as reservoirs of Ebola virus. Nature 2005, 438, 575–576.[CrossRef] [PubMed]
19. Barrette, R.W.; Metwally, S.A.; Rowland, J.M.; Xu, L.; Zaki, S.R.; Nichol, S.T.; Rollin, P.E.; Towner, J.S.; Shieh, W.J.; Batten, B. et al. Discovery of swine as a host for the Reston ebolavirus. Science 2009, 325, 204–206.[CrossRef] [PubMed]
20. Groseth, A.; Feldmann, H.; Strong, J.E. The ecology of Ebola virus. Trends Microbiol. 2007, 15, 408–416.[CrossRef] [PubMed]
21. Bente, D.; Gren, J.; Strong, J.E.; Feldmann, H. Disease modeling for Ebola and Marburg viruses. Dis. Model. Mech. 2009, 2, 12–17.[CrossRef] [PubMed]
22. 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.[CrossRef] [PubMed]
23. 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. 1998, 178, 651–661.[CrossRef] [PubMed]
24. Warfield, K.L.; Alves, D.A.; Bradfute, S.B.; Reed, D.K.; vanTongeren, S.; Kalina, W.V.; Olinger, G.G.; Bavari, S. Development of a model for marburgvirus based on severe-combined immunodeficiency mice. Virol. J. 2007, 4.[CrossRef] [PubMed]
25. Warfield, K.L.; Bradfute, S.B.; Wells, J.; Lofts, L.; Cooper, M.T.; Alves, D.A.; Reed, D.K.; vanTongeren, S.A.; Mech, C.A.; Bavari, S. Development and characterization of a mouse model for Marburg hemorrhagic fever. J. Virol. 2009, 83, 6404–6415.[CrossRef] [PubMed]
26. Ebihara, H.; Zivcec, M.; Gardner, D.; Falzarano, D.; LaCasse, R.; Rosenke, R.; Long, D.; Haddock, E.; Fischer, E.; Kawaoka, Y. et al. A Syrian golden hamster model recapitulating Ebola hemorrhagic fever. J. Infect. Dis. 2013, 207, 306–318.[CrossRef] [PubMed]
27. Ryabchikova, E.; Kolesnikova, L.; Smolina, M.; Tkachev, V.; Pereboeva, L.; Baranova, S.; Grazhdantseva, A.; Rassadkin, Y. Ebola virus infection in guinea pigs: Presumable role of granulomatous inflammation in pathogenesis. Arch. Virol. 1996, 141, 909–921.[CrossRef] [PubMed]
28. Simpson, D.I.; Zlotnik, I.; Rutter, D.A. Vervet monkey disease. Experiment infection of guinea pigs and monkeys with the causative agent. Br. J. Exp. Pathol. 1968, 49, 458–464. [PubMed]
29. Connolly, B.M.; Steele, K.E.; Davis, K.J.; Geisbert, T.W.; Kell, W.M.; Jaax, N.K.; Jahrling, P.B. Pathogenesis of experimental Ebola virus infection in guinea pigs. J. Infect. Dis. 1999, 179, S203–S217.[CrossRef] [PubMed]
30. Leroy, E.M.; Epelboin, A.; Mondonge, V.; Pourrut, X.; Gonzalez, J.P.; Muyembe-Tamfum, J.J.; Formenty, P. Human Ebola outbreak resulting from direct exposure to fruit bats in Luebo, Democratic Republic of Congo, 2007. Vector Borne Zoonotic Dis. 2009, 9, 723–728.[CrossRef] [PubMed]
31. Leroy, E.M.; Rouquet, P.; Formenty, P.; Souquiere, S.; Kilbourne, A.; Froment, J.M.; Bermejo, M.; Smit, S.; Karesh, W.; Swanepoel, R. et al. Multiple Ebola virus transmission events and rapid decline of central African wildlife. Science 2004, 303, 387–390.[CrossRef] [PubMed]
32. Pourrut, X.; Kumulungui, B.; Wittmann, T.; Moussavou, G.; Delicat, A.; Yaba, P.; Nkoghe, D.; Gonzalez, J.P.; Leroy, E.M. The natural history of Ebola virus in Africa. Microbes Infect./Inst. Pasteur 2005, 7, 1005–1014.[CrossRef]
33. Roels, T.H.; Bloom, A.S.; Buffington, J.; Muhungu, G.L.; Mac Kenzie, W.R.; Khan, A.S.; Ndambi, R.; Noah, D.L.; Rolka, H.R.; Peters, C.J. et al. Ebola hemorrhagic fever, Kikwit, Democratic Republic of the Congo, 1995: Risk factors for patients without a reported exposure. J. Infect. Dis. 1999, 179, S92–S97.[CrossRef] [PubMed]
34. Dowell, S.F.; Mukunu, R.; Ksiazek, T.G.; Khan, A.S.; Rollin, P.E.; Peters, C.J. Transmission of Ebola hemorrhagic fever: A study of risk factors in family members, Kikwit, Democratic Republic of the Congo, 1995. Commission de Lutte contre les Epidemies a Kikwit. J. Infect. Dis. 1999, 179, S87–S91.[CrossRef] [PubMed]
35. Martines, R.B.; Ng, D.L.; Greer, P.W.; Rollin, P.E.; Zaki, S.R. Tissue and cellular tropism, pathology and pathogenesis of Ebola and Marburg viruses. J. Pathol. 2015, 235, 153–174.[CrossRef] [PubMed]
36. Brauburger, K.; Hume, A.J.; Muhlberger, E.; Olejnik, J. Forty-five years of Marburg virus research. Viruses 2012, 4, 1878–1927.[CrossRef] [PubMed]
37. Kortepeter, M.G.; Bausch, D.G.; Bray, M. Basic clinical and laboratory features of filoviral hemorrhagic fever. J. Infect. Dis. 2011, 204, S810–S816.[CrossRef] [PubMed]
38. Ligon, B.L. Outbreak of Marburg hemorrhagic fever in Angola: A review of the history of the disease and its biological aspects. Semin. Pediatr. Infect. Dis. 2005, 16, 219–224.[CrossRef] [PubMed]
39. Dixon, M.G.; Schafer, I.J.; Centers for Disease Control and Prevention. Ebola viral disease outbreak—West Africa, 2014. Morb. Mortal. Wkly. Rep. 2014, 63, 548–551.
40. Zaki, S.R.; Goldsmith, C.S. Pathologic features of filovirus infections in humans. Curr. Top. Microbiol. Immunol. 1999, 235, 97–116. [PubMed]
41. 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. 2010, 4, e837.[CrossRef] [PubMed]
42. Baize, S.; Leroy, E.M.; Georges, A.J.; Georges-Courbot, M.C.; Capron, M.; Bedjabaga, I.; Lansoud-Soukate, J.; Mavoungou, E. Inflammatory responses in Ebola virus-infected patients. Clin. Exp. Immunol. 2002, 128, 163–168.[CrossRef] [PubMed]
43. Fernando, L.; Qiu, X.; Melito, P.L.; Williams, K.J.; Feldmann, F.; Feldmann, H.; Jones, S.M.; Alimonti, J.B. Immune Response to Marburg Virus Angola Infection in Nonhuman Primates. J. Infect. Dis. 2015, 212, S234–S241.[CrossRef] [PubMed]
44. Tisoncik, J.R.; Korth, M.J.; Simmons, C.P.; Farrar, J.; Martin, T.R.; Katze, M.G. Into the eye of the cytokine storm. Microbiol. Mol. Biol. Rev. 2012, 76, 16–32.[CrossRef] [PubMed]
45. Misasi, J.; Sullivan, N.J. Camouflage and misdirection: The full-on assault of Ebola virus disease. Cell 2014, 159, 477–486.[CrossRef] [PubMed]
46. 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. 2003, 163, 2347–2370.[CrossRef]
47. Alves, D.A.; Glynn, A.R.; Steele, K.E.; Lackemeyer, M.G.; Garza, N.L.; Buck, J.G.; Mech, C.; Reed, D.S. Aerosol exposure to the angola strain of Marburg virus causes lethal viral hemorrhagic Fever in cynomolgus macaques. Vet. Pathol. 2010, 47, 831–851.[CrossRef] [PubMed]
48. Fritz, E.A.; Geisbert, J.B.; Geisbert, T.W.; Hensley, L.E.; Reed, D.S. Cellular immune response to Marburg virus infection in cynomolgus macaques. Viral Immunol. 2008, 21, 355–363.[CrossRef] [PubMed]
49. Hensley, L.E.; Alves, D.A.; Geisbert, J.B.; Fritz, E.A.; Reed, C.; Larsen, T.; Geisbert, T.W. Pathogenesis of Marburg hemorrhagic fever in cynomolgus macaques. J. Infect. Dis. 2011, 204, S1021–S1031.[CrossRef] [PubMed]
50. Geisbert, T.W.; Jaax, N.K. Marburg hemorrhagic fever: Report of a case studied by immunohistochemistry and electron microscopy. Ultrastruct. Pathol. 1998, 22, 3–17.[CrossRef] [PubMed]
51. Schnittler, H.J.; Feldmann, H. Viral hemorrhagic fever—A vascular disease? Thromb. Haemost. 2003, 89, 967–972. [PubMed]
52. Schnittler, H.J.; Feldmann, H. Marburg and Ebola hemorrhagic fevers: Does the primary course of infection depend on the accessibility of organ-specific macrophages? Clin. Infect. Dis. 1998, 27, 404–406.[CrossRef] [PubMed]
53. Geisbert, T.W.; Daddario-DiCaprio, K.M.; Geisbert, J.B.; Young, H.A.; Formenty, P.; Fritz, E.A.; Larsen, T.; Hensley, L.E. Marburg virus Angola infection of rhesus macaques: Pathogenesis and treatment with recombinant nematode anticoagulant protein c 2. J. Infect. Dis. 2007, 196, S372–S381.[CrossRef] [PubMed]
54. Geisbert, T.W.; Hensley, L.E.; Gibb, T.R.; Steele, K.E.; Jaax, N.K.; Jahrling, P.B. Apoptosis induced in vitro and in vivo during infection by Ebola and Marburg viruses. Lab. Investig. 2000, 80, 171–186.[CrossRef] [PubMed]
55. Ryabchikova, E.; Strelets, L.; Kolesnikova, L.; Pyankov, O.; Sergeev, A. Respiratory Marburg virus infection in guinea pigs. Arch. Virol. 1996, 141, 2177–2190.[CrossRef] [PubMed]
56. Wool-Lewis, R.J.; Bates, P. Characterization of Ebola virus entry by using pseudotyped viruses: Identification of receptor-deficient cell lines. J. Virol. 1998, 72, 3155–3160. [PubMed]
57. Escudero-Perez, B.; Volchkova, V.A.; Dolnik, O.; Lawrence, P.; Volchkov, V.E. Shed GP of Ebola virus triggers immune activation and increased vascular permeability. PLoS Pathog. 2014, 10, e1004509.[CrossRef] [PubMed]
58. Bosio, C.M.; Aman, M.J.; Grogan, C.; Hogan, R.; Ruthel, G.; Negley, D.; Mohamadzadeh, M.; Bavari, S.; Schmaljohn, A. Ebola and Marburg viruses replicate in monocyte-derived dendritic cells without inducing the production of cytokines and full maturation. J. Infect. Dis. 2003, 188, 1630–1638.[CrossRef] [PubMed]
59. Mahanty, S.; Hutchinson, K.; Agarwal, S.; McRae, M.; Rollin, P.E.; Pulendran, B. Cutting edge: Impairment of dendritic cells and adaptive immunity by Ebola and Lassa viruses. J. Immunol. 2003, 170, 2797–2801.[CrossRef] [PubMed]
60. Lubaki, N.M.; Ilinykh, P.; Pietzsch, C.; Tigabu, B.; Freiberg, A.N.; Koup, R.A.; Bukreyev, A. The lack of maturation of Ebola virus-infected dendritic cells results from the cooperative effect of at least two viral domains. J. Virol. 2013, 87, 7471–7485.[CrossRef] [PubMed]
61. Gupta, M.; Spiropoulou, C.; Rollin, P.E. Ebola virus infection of human PBMCs causes massive death of macrophages, CD4 and CD8 T cell sub-populations in vitro. Virology 2007, 364, 45–54.[CrossRef] [PubMed]
62. Baize, S.; Leroy, E.M.; Georges-Courbot, M.C.; Capron, M.; Lansoud-Soukate, J.; Debre, P.; Fisher-Hoch, S.P.; McCormick, J.B.; Georges, A.J. Defective humoral responses and extensive intravascular apoptosis are associated with fatal outcome in Ebola virus-infected patients. Nat. Med. 1999, 5, 423–426.[CrossRef] [PubMed]
63. Reed, D.S.; Hensley, L.E.; Geisbert, J.B.; Jahrling, P.B.; Geisbert, T.W. Depletion of peripheral blood T lymphocytes and NK cells during the course of Ebola hemorrhagic Fever in cynomolgus macaques. Viral Immunol. 2004, 17, 390–400.[CrossRef] [PubMed]
64. 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. 2007, 196, S296–S304.[CrossRef] [PubMed]
65. Leroy, E.M.; Baize, S.; Volchkov, V.E.; Fisher-Hoch, S.P.; Georges-Courbot, M.C.; Lansoud-Soukate, J.; Capron, M.; Debre, P.; McCormick, J.B.; Georges, A.J. Human asymptomatic Ebola infection and strong inflammatory response. Lancet 2000, 355, 2210–2215.[CrossRef]
66. Hevey, M.; Negley, D.; Pushko, P.; Smith, J.; Schmaljohn, A. Marburg virus vaccines based upon alphavirus replicons protect guinea pigs and nonhuman primates. Virology 1998, 251, 28–37.[CrossRef] [PubMed]
67. Ignatyev, G.M. Immune response to filovirus infections. Curr. Top. Microbiol. Immunol. 1999, 235, 205–217. [PubMed]
68. Perry, A.K.; Chen, G.; Zheng, D.; Tang, H.; Cheng, G. The host type I interferon response to viral and bacterial infections. Cell Res. 2005, 15, 407–422.[CrossRef] [PubMed]
69. Iwasaki, A.; Medzhitov, R. Toll-like receptor control of the adaptive immune responses. Nat. Immunol. 2004, 5, 987–995.[CrossRef] [PubMed]
70. Theofilopoulos, A.N.; Baccala, R.; Beutler, B.; Kono, D.H. Type I interferons (_/_) in immunity and autoimmunity. Annu. Rev. Immunol. 2005, 23, 307–336.[CrossRef] [PubMed]
71. Prins, K.C.; Cardenas, W.B.; Basler, C.F. Ebola virus protein VP35 impairs the function of interferon regulatory factor-activating kinases IKKepsilon and TBK-1. J. Virol. 2009, 83, 3069–3077.[CrossRef] [PubMed]
72. Basler, C.F.; Mikulasova, A.; Martinez-Sobrido, L.; Paragas, J.; Muhlberger, E.; Bray, M.; Klenk, H.D.; Palese, P.; Garcia-Sastre, A. The Ebola virus VP35 protein inhibits activation of interferon regulatory factor 3. J. Virol. 2003, 77, 7945–7956.[CrossRef] [PubMed]
73. Basler, C.F.; Wang, X.; Muhlberger, E.; Volchkov, V.; Paragas, J.; Klenk, H.D.; Garcia-Sastre, A.; Palese, P. The Ebola virus VP35 protein functions as a type I IFN antagonist. Proc. Natl. Acad. Sci. USA 2000, 97, 12289–12294.[CrossRef] [PubMed]
74. Chang, T.H.; Kubota, T.; Matsuoka, M.; Jones, S.; Bradfute, S.B.; Bray, M.; Ozato, K. Ebola Zaire virus blocks type I interferon production by exploiting the host SUMO modification machinery. PLoS Pathog. 2009, 5, e1000493.[CrossRef] [PubMed]
75. Zhang, A.P.; Bornholdt, Z.A.; Liu, T.; Abelson, D.M.; Lee, D.E.; Li, S.; Woods, V.L.,; Saphire, E.O. The ebola virus interferon antagonist VP24 directly binds STAT1 and has a novel, pyramidal fold. PLoS Pathog. 2012, 8, e1002550.[CrossRef] [PubMed]
76. Reid, S.P.; Leung, L.W.; Hartman, A.L.; Martinez, O.; Shaw, M.L.; Carbonnelle, C.; Volchkov, V.E.; Nichol, S.T.; Basler, C.F. Ebola virus VP24 binds karyopherin alpha1 and blocks STAT1 nuclear accumulation. J. Virol. 2006, 80, 5156–5167.[CrossRef] [PubMed]
77. Ramanan, P.; Shabman, R.S.; Brown, C.S.; Amarasinghe, G.K.; Basler, C.F.; Leung, D.W. Filoviral immune evasion mechanisms. Viruses 2011, 3, 1634–1649.[CrossRef] [PubMed]
78. Hartman, A.L.; Towner, J.S.; Nichol, S.T. A C-terminal basic amino acid motif of Zaire ebolavirus VP35 is essential for type I interferon antagonism and displays high identity with the RNA-binding domain of another interferon antagonist, the NS1 protein of influenza A virus. Virology 2004, 328, 177–184.[CrossRef] [PubMed]
79. Valmas, C.; Grosch, M.N.; Schumann, M.; Olejnik, J.; Martinez, O.; Best, S.M.; Krahling, V.; Basler, C.F.; Muhlberger, E. Marburg virus evades interferon responses by a mechanism distinct from ebola virus. PLoS Pathog. 2010, 6, e1000721.[CrossRef] [PubMed]
80. Kash, J.C.; Muhlberger, E.; Carter, V.; Grosch, M.; Perwitasari, O.; Proll, S.C.; Thomas, M.J.; Weber, F.; Klenk, H.D.; Katze, M.G. Global suppression of the host antiviral response by Ebola- and Marburgviruses: Increased antagonism of the type I interferon response is associated with enhanced virulence. J. Virol. 2006, 80, 3009–3020.[CrossRef] [PubMed]
81. Lofts, L.L.; Wells, J.B.; Bavari, S.; Warfield, K.L. Key genomic changes necessary for an in vivo lethal mouse Marburgvirus variant selection process. J. Virol. 2011, 85, 3905–3917.[CrossRef] [PubMed]
82. Valmas, C.; Basler, C.F. Marburg virus VP40 antagonizes interferon signaling in a species-specific manner. J. Virol. 2011, 85, 4309–4317.[CrossRef] [PubMed]
83. Neil, S.J.; Sandrin, V.; Sundquist, W.I.; Bieniasz, P.D. An interferon-alpha-induced tethering mechanism inhibits HIV-1 and Ebola virus particle release but is counteracted by the HIV-1 Vpu protein. Cell Host Microbe 2007, 2, 193–203.[CrossRef] [PubMed]
84. Neil, S.J.; Zang, T.; Bieniasz, P.D. Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 2008, 451, 425–430.[CrossRef] [PubMed]
85. Van Damme, N.; Goff, D.; Katsura, C.; Jorgenson, R.L.; Mitchell, R.; Johnson, M.C.; Stephens, E.B.; Guatelli, J. The interferon-induced protein BST-2 restricts HIV-1 release and is downregulated from the cell surface by the viral Vpu protein. Cell Host Microbe 2008, 3, 245–252.[CrossRef] [PubMed]
86. Kuhl, A.; Banning, C.; Marzi, A.; Votteler, J.; Steffen, I.; Bertram, S.; Glowacka, I.; Konrad, A.; Sturzl, M.; Guo, J.T. et al. The Ebola virus glycoprotein and HIV-1 Vpu employ different strategies to counteract the antiviral factor tetherin. J. Infect. Dis. 2011, 204, S850–S860.[CrossRef] [PubMed]
87. Hutchinson, K.L.; Rollin, P.E. Cytokine and chemokine expression in humans infected with Sudan Ebola virus. J. Infect. Dis. 2007, 196 (Suppl. S2), S357–S363.[CrossRef] [PubMed]
88. Jahrling, P.B.; Geisbert, T.W.; Geisbert, J.B.; Swearengen, J.R.; Bray, M.; Jaax, N.K.; Huggins, J.W.; LeDuc, J.W.; Peters, C.J. Evaluation of immune globulin and recombinant interferon-alpha2b for treatment of experimental Ebola virus infections. J. Infect. Dis. 1999, 179, S224–S234.[CrossRef] [PubMed]
89. Smith, L.M.; Hensley, L.E.; Geisbert, T.W.; Johnson, J.; Stossel, A.; Honko, A.; Yen, J.Y.; Geisbert, J.; Paragas, J.; Fritz, E. et al. Interferon-beta therapy prolongs survival in rhesus macaque models of Ebola and Marburg hemorrhagic fever. J. Infect. Dis. 2013, 208, 310–318.[CrossRef] [PubMed]
90. Bradfute, S.B.; Anthony, S.M.; Stuthman, K.S.; Ayithan, N.; Tailor, P.; Shaia, C.I.; Bray, M.; Ozato, K.; Bavari, S. Mechanisms of immunity in post-exposure vaccination against Ebola virus infection. PLoS ONE 2015, 10, e0118434.[CrossRef] [PubMed]
91. Ayithan, N.; Bradfute, S.B.; Anthony, S.M.; Stuthman, K.S.; Bavari, S.; Bray, M.; Ozato, K. Virus-like particles activate type I interferon pathways to facilitate post-exposure protection against Ebola virus infection. PLoS ONE 2015, 10, e0118345.[CrossRef] [PubMed]
92. Villinger, F.; Rollin, P.E.; Brar, S.S.; Chikkala, N.F.; Winter, J.; Sundstrom, J.B.; Zaki, S.R.; Swanepoel, R.; Ansari, A.A.; Peters, C.J. Markedly elevated levels of interferon (IFN)-, IFN-_, interleukin (IL)-2, IL-10, and tumor necrosis factor-alpha associated with fatal Ebola virus infection. J. Infect. Dis. 1999, 179, S188–S191.[CrossRef] [PubMed]
93. Gupta, M.; MacNeil, A.; Reed, Z.D.; Rollin, P.E.; Spiropoulou, C.F. Serology and cytokine profiles in patients infected with the newly discovered Bundibugyo ebolavirus. Virology 2012, 423, 119–124.[CrossRef] [PubMed]
94. Gupta, M.; Goldsmith, C.S.; Metcalfe, M.G.; Spiropoulou, C.F.; Rollin, P.E. Reduced virus replication, proinflammatory cytokine production, and delayed macrophage cell death in human PBMCs infected with the newly discovered Bundibugyo ebolavirus relative to Zaire ebolavirus. Virology 2010, 402, 203–208.[CrossRef] [PubMed]
95. Hensley, L.E.; Young, H.A.; Jahrling, P.B.; Geisbert, T.W. Proinflammatory response during Ebola virus infection of primate models: Possible involvement of the tumor necrosis factor receptor superfamily. Immunol. Lett. 2002, 80, 169–179.[CrossRef]
96. Schroder, K.; Hertzog, P.J.; Ravasi, T.; Hume, D.A. Interferon-gamma: An overview of signals, mechanisms and functions. J. Leukoc. Biol. 2004, 75, 163–189.[CrossRef] [PubMed]
97. Bach, E.A.; Aguet, M.; Schreiber, R.D. The IFN gamma receptor: A paradigm for cytokine receptor signaling. Annu. Rev. Immunol. 1997, 15, 563–591.[CrossRef] [PubMed]
98. Boehm, U.; Klamp, T.; Groot, M.; Howard, J.C. Cellular responses to interferon-gamma. Annu. Rev. Immunol. 1997, 15, 749–795.[CrossRef] [PubMed]
99. Decker, T.; Stockinger, S.; Karaghiosoff, M.; Muller, M.; Kovarik, P. IFNs and STATs in innate immunity to microorganisms. J. Clin. Investig. 2002, 109, 1271–1277.[CrossRef] [PubMed]
100. Ebihara, H.; Rockx, B.; Marzi, A.; Feldmann, F.; Haddock, E.; Brining, D.; LaCasse, R.A.; Gardner, D.; Feldmann, H. Host response dynamics following lethal infection of rhesus macaques with Zaire ebolavirus. J. Infect. Dis. 2011, 204, S991–S999.[CrossRef] [PubMed]
101. Badovinac, V.P.; Harty, J.T. Programming, demarcating, and manipulating CD8+ T-cell memory. Immunol. Rev. 2006, 211, 67–80.[CrossRef] [PubMed]
102. Warfield, K.L.; Bosio, C.M.; Welcher, B.C.; Deal, E.M.; Mohamadzadeh, M.; Schmaljohn, A.; Aman, M.J.; Bavari, S. Ebola virus-like particles protect from lethal Ebola virus infection. Proc. Natl. Acad. Sci. USA 2003, 100, 15889–15894.[CrossRef] [PubMed]
103. Warfield, K.L.; Olinger, G.; Deal, E.M.; Swenson, D.L.; Bailey, M.; Negley, D.L.; Hart, M.K.; Bavari, S. Induction of humoral and CD8+ T cell responses are required for protection against lethal Ebola virus infection. J. Immunol. 2005, 175, 1184–1191.[CrossRef] [PubMed]
104. McElroy, A.K.; Akondy, R.S.; Davis, C.W.; Ellebedy, A.H.; Mehta, A.K.; Kraft, C.S.; Lyon, G.M.; Ribner, B.S.; Varkey, J.; Sidney, J. et al. Human Ebola virus infection results in substantial immune activation. Proc. Natl. Acad. Sci. USA 2015, 112, 4719–4724.[CrossRef] [PubMed]
105. Zlotnik, A.; Yoshie, O. Chemokines: A new classification system and their role in immunity. Immunity 2000, 12, 121–127.[CrossRef]
106. Viola, A.; Luster, A.D. Chemokines and their receptors: Drug targets in immunity and inflammation. Annu. Rev. Pharmacol. Toxicol. 2008, 48, 171–197.[CrossRef] [PubMed]
107. Connor, J.H.; Yen, J.; Caballero, I.S.; Garamszegi, S.; Malhotra, S.; Lin, K.; Hensley, L.; Goff, A.J. Transcriptional Profiling of the Immune Response to Marburg Virus Infection. J. Virol. 2015, 89, 9865–9874.[CrossRef] [PubMed]
108. Lin, K.L.; Twenhafel, N.A.; Connor, J.H.; Cashman, K.A.; Shamblin, J.D.; Donnelly, G.C.; Esham, H.L.; Wlazlowski, C.B.; Johnson, J.C.; Honko, A.N. et al. Temporal Characterization of Marburg Virus Angola Infection following Aerosol Challenge in Rhesus Macaques. J. Virol. 2015, 89, 9875–9885.[CrossRef] [PubMed]
109. Zampieri, C.A.; Sullivan, N.J.; Nabel, G.J. Immunopathology of highly virulent pathogens: Insights from Ebola virus. Nat. Immunol. 2007, 8, 1159–1164.[CrossRef] [PubMed]
110. Khabar, K.S.; Al-Zoghaibi, F.; Al-Ahdal, M.N.; Murayama, T.; Dhalla, M.; Mukaida, N.; Taha, M.; Al-Sedairy, S.T.; Siddiqui, Y.; Kessie, G. et al. The _ chemokine, interleukin 8, inhibits the antiviral action of interferon alpha. J. Exp. Med. 1997, 186, 1077–1085.[CrossRef]
111. Bradley, J.R. TNF-mediated inflammatory disease. J. Pathol. 2008, 214, 149–160.[CrossRef] [PubMed]
112. Ignatyev, G.M.; Agafonov, A.P.; Streltsova, M.A.; Kashentseva, E.A. Inactivated Marburg virus elicits a nonprotective immune response in Rhesus monkeys. J. Biotechnol. 1996, 44, 111–118.[CrossRef]
113. Ignatyev, G.; Steinkasserer, A.; Streltsova, M.; Atrasheuskaya, A.; Agafonov, A.; Lubitz, W. Experimental study on the possibility of treatment of some hemorrhagic fevers. J. Biotechnol. 2000, 83, 67–76.[CrossRef]
114. Bray, M.; Mahanty, S. Ebola hemorrhagic fever and septic shock. J. Infect. Dis. 2003, 188, 1613–1617.[CrossRef] [PubMed]
115. Feldmann, H.; Bugany, H.; Mahner, F.; Klenk, H.D.; Drenckhahn, D.; Schnittler, H.J. Filovirus-induced endothelial leakage triggered by infected monocytes/macrophages. J. Virol. 1996, 70, 2208–2214. [PubMed]
116. Bockeler, M.; Stroher, U.; Seebach, J.; Afanasieva, T.; Suttorp, N.; Feldmann, H.; Schnittler, H.J. Breakdown of paraendothelial barrier function during Marburg virus infection is associated with early tyrosine phosphorylation of platelet endothelial cell adhesion molecule- 1. J. Infect. Dis. 2007, 196, S337–S346.[CrossRef] [PubMed]
117. Stroher, U.; West, E.; Bugany, H.; Klenk, H.D.; Schnittler, H.J.; Feldmann, H. Infection and activation of monocytes by Marburg and Ebola viruses. J. Virol. 2001, 75, 11025–11033.[CrossRef] [PubMed]
118. Ignat’ev, G.M.; Strel’tsova, M.A.; Kashentseva, E.A.; Patrushev, N.A. Effects of tumor necrosis factor antiserum of the course of Marburg hemorrhagic fever. Vestn. Ross. Akad. Med. Nauk 1998, 3, 35–38. [PubMed]
119. Mizel, S.B.; Farrar, J.J. Revised nomenclature for antigen-nonspecific T cell proliferation and helper factors. J. Immunol. 1979, 123, 2928–2929.[CrossRef]
120. Commins, S.P.; Borish, L.; Steinke, J.W. Immunologic messenger molecules: Cytokines, interferons, and chemokines. J. Allergy Clin. Immunol. 2010, 125, S53–S72.[CrossRef] [PubMed]
121. Leroy, E.M.; Baize, S.; Debre, P.; Lansoud-Soukate, J.; Mavoungou, E. Early immune responses accompanying human asymptomatic Ebola infections. Clin. Exp. Immunol. 2001, 124, 453–460.[CrossRef] [PubMed]
122. Dinarello, C.A. Interleukin-18, a proinflammatory cytokine. Eur. Cytokine Netw. 2000, 11, 483–486. [PubMed]
123. Panchal, R.G.; Mourich, D.V.; Bradfute, S.; Hauck, L.L.; Warfield, K.L.; Iversen, P.L.; Bavari, S. Induced IL-10 splice altering approach to antiviral drug discovery. Nucl. Acid Ther. 2014, 24, 179–185.[CrossRef] [PubMed]
124. Ferrara, N.; Davis-Smyth, T. The biology of vascular endothelial growth factor. Endocr. Rev. 1997, 18, 4–25.[CrossRef] [PubMed]
125. Otrock, Z.K.; Mahfouz, R.A.; Makarem, J.A.; Shamseddine, A.I. Understanding the biology of angiogenesis: Review of the most important molecular mechanisms. Blood Cells Mol. Dis. 2007, 39, 212–220.[CrossRef] [PubMed]
126. Kindrachuk, J.; Wahl-Jensen, V.; Safronetz, D.; Trost, B.; Hoenen, T.; Arsenault, R.; Feldmann, F.; Traynor, D.; Postnikova, E.; Kusalik, A. et al. Ebola virus modulates transforming growth factor beta signaling and cellular markers of mesenchyme-like transition in hepatocytes. J. Virol. 2014, 88, 9877–9892.[CrossRef] [PubMed]
127. McElroy, A.K.; Erickson, B.R.; Flietstra, T.D.; Rollin, P.E.; Nichol, S.T.; Towner, J.S.; Spiropoulou, C.F. Ebola hemorrhagic Fever: Novel biomarker correlates of clinical outcome. J. Infect. Dis. 2014, 210, 558–566.[CrossRef] [PubMed]
128. Hamilton, J.A. Colony-stimulating factors in inflammation and autoimmunity. Nat. Rev. Immunol. 2008, 8, 533–544.[CrossRef] [PubMed]
129. Martinez, O.; Johnson, J.C.; Honko, A.; Yen, B.; Shabman, R.S.; Hensley, L.E.; Olinger, G.G.; Basler, C.F. Ebola virus exploits a monocyte differentiation program to promote its entry. J. Virol. 2013, 87, 3801–3814.[CrossRef] [PubMed]
130. Eisenstein, E.M.; Williams, C.B. The T(reg)/Th17 cell balance: A new paradigm for autoimmunity. Pediatr. Res. 2009, 65, 26R–31R.[CrossRef] [PubMed]
131. Michelow, I.C.; Lear, C.; Scully, C.; Prugar, L.I.; Longley, C.B.; Yantosca, L.M.; Ji, X.; Karpel, M.; Brudner, M.; Takahashi, K. et al. High-dose mannose-binding lectin therapy for Ebola virus infection. J. Infect. Dis. 2011, 203, 175–179.[CrossRef] [PubMed]
132. Sobarzo, A.; Groseth, A.; Dolnik, O.; Becker, S.; Lutwama, J.J.; Perelman, E.; Yavelsky, V.; Muhammad, M.; Kuehne, A.I.; Marks, R.S. et al. Profile and persistence of the virus-specific neutralizing humoral immune response in human survivors of Sudan ebolavirus (Gulu). J. Infect. Dis. 2013, 208, 299–309.[CrossRef] [PubMed]
133. Xu, L.; Sanchez, A.; Yang, Z.; Zaki, S.R.; Nabel, E.G.; Nichol, S.T.; Nabel, G.J. Immunization for Ebola virus infection. Nat. Med. 1998, 4, 37–42.[CrossRef] [PubMed]
134. McElroy, A.K.; Erickson, B.R.; Flietstra, T.D.; Rollin, P.E.; Nichol, S.T.; Towner, J.S.; Spiropoulou, C.F. Biomarker correlates of survival in pediatric patients with Ebola virus disease. Emerg. Infect. Dis. 2014, 20, 1683–1690.[CrossRef] [PubMed]
135. Schall, T.J.; Bacon, K.; Toy, K.J.; Goeddel, D.V. Selective attraction of monocytes and T lymphocytes of the memory phenotype by cytokine RANTES. Nature 1990, 347, 669–671.[CrossRef] [PubMed]