Animal models for Ebola and Marburg virus infections

Frontiers in Microbiology

Volumn 4, Issue SEP, 2013, Pages

  Nakayama, Eri ^a   Saijo, Masayuki ^a  

^a NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

Author keywords

Animal models; Ebola virus; Filovirus; Marburg virus; Viral hemorrhagic fever

Indexed keywords

ADENOVIRUS VECTOR; ANTIVIRUS AGENT; AVI 6002 PMO PLUS; AVI 6003 PMO PLUS; DNA VACCINE; DROTRECOGIN; EBOLA VACCINE; FGI 103; FGI 106; HEAT SHOCK PROTEIN 90 INHIBITOR; INTERFERON; MARBURG VIRUS VACCINE; MORPHOLINO OLIGONUCLEOTIDE; NSC 62914; PARAINFLUENZA VACCINE; PMOPLUS; RECOMBINANT NEMATODE ANTICOAGULANT PROTEIN C2; STAT1 PROTEIN; UNCLASSIFIED DRUG; VIRUS LIKE PARTICLE VACCINE; VIRUS PROTEIN; VIRUS VACCINE; VP24 PROTEIN;

DISEASE MODEL; EBOLA HEMORRHAGIC FEVER; EBOLA VIRUS; GUINEA PIG MODEL; HAMSTER MODEL; HUMAN; IN VITRO STUDY; MARBURG HEMORRHAGIC FEVER; MARBURG VIRUS; MOUSE MODEL; NONHUMAN; NUCLEOTIDE SEQUENCE; PARAINFLUENZA VIRUS; REPLICON; REVIEW; RNA INTERFERENCE; THROMBOCYTOPENIA; VENEZUELAN EQUINE ENCEPHALOMYELITIS ALPHAVIRUS; VESICULAR STOMATITIS VIRUS; VIREMIA; VIRION;

ANIMALIA; CAVIA; CRICETINAE; EBOLA VIRUS; FILOVIRIDAE; LAKE VICTORIA MARBURGVIRUS; MACACA; MARBURGVIRUS; PRIMATES; RODENTIA;

EID: 84885405310     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2013.00267     Document Type: Review

References (152)

1. Abbink, P., Lemckert, A. A., Ewald, B. A., Lynch, D. M., Denholtz, M., Smits, S., et al. (2007). Comparative seroprevalence and immunogenicity of six rare serotype recombinant adenovirus vaccine vectors from subgroups B and D. J. Virol. 81, 4654-4663. doi:10.1128/JVI.02696-06.
2. Alves, D. A., Glynn, A. R., Steele, K. E., Lackemeyer, M. G., Garza, N. L., Buck, J. G., et al. (2010). Aerosol exposure to the angola strain of marburg virus causes lethal viral hemorrhagic Fever in cynomolgus macaques. Vet. Pathol. 47, 831-851. doi:10.1177/0300985810378597.
3. Aman, M. J., Kinch, M. S., Warfield, K., Warren, T., Yunus, A., Enterlein, S., et al. (2009). Development of a broad-spectrum antiviral with activity against Ebola virus. Antiviral Res. 83, 245-251. doi:10.1016/j.antiviral.2009.06.001.
4. Arai, A., Hirano, H., Ueta, Y., Hamada, T., Mita, T., and Shirahata, A. (2000). Detection of mononuclear cells as the source of the increased tissue factor mRNA in the liver from lipopolysaccharide-treated rats. Thromb. Res. 97, 153-162. doi:10.1016/S0049-3848(99)00147-4.
5. Baize, S., Leroy, E. M., Georges, A. J., Georges-Courbot, M. C., Capron, M., Bedjabaga, I., et al. (2002). Inflammatory responses in Ebola virus-infected patients. Clin. Exp. Immunol. 128, 163-168. doi:10.1046/j.1365-2249.2002.01800.x.
6. Baize, S., Leroy, E. M., Georges-Courbot, M. C., Capron, M., Lansoud-Soukate, J., Debre, P., et al. (1999). Defective humoral responses and extensive intravascular apoptosis are associated with fatal outcome in Ebola virus-infected patients. Nat. Med. 5, 423-426. doi:10.1038/7422.
7. Baskerville, A., Bowen, E. T., Platt, G. S., McArdell, L. B., and Simpson, D. I. (1978). The pathology of experimental Ebola virus infection in monkeys. J. Pathol. 125, 131-138. doi:10.1002/path.1711250303.
8. Baskerville, A., Fisher-Hoch, S. P., Neild, G. H., and Dowsett, A. B. (1985). Ultrastructural pathology of experimental Ebola haemorrhagic fever virus infection. J. Pathol. 147, 199-209. doi:10.1002/path.1711470308.
9. Basler, C. F., Wang, X., Muhlberger, E., Volchkov, V., Paragas, J., Klenk, H. D., et al. (2000). The Ebola virus VP35 protein functions as a type I IFN antagonist. Proc. Natl. Acad. Sci. U.S.A. 97, 12289-12294. doi:10.1073/pnas.220398297.
10. Bente, D., Gren, J., Strong, J. E., and Feldmann, H. (2009). Disease modeling for Ebola and Marburg viruses. Dis. Model. Mech. 2, 12-17. doi:10.1242/dmm.000471.
11. Bowen, E. T., Lloyd, G., Harris, W. J., Platt, G. S., Baskerville, A., and Vella, E. E. (1977). Viral haemorrhagic fever in southern Sudan and northern Zaire. Preliminary studies on the aetiological agent. Lancet 1, 571-573. doi:10.1016/S0140-6736(77)92001-3.
12. Bowen, E. T., Platt, G. S., Lloyd, G., Raymond, R. T., and Simpson, D. I. (1980). A comparative study of strains of Ebola virus isolated from southern Sudan and northern Zaire in 1976. J. Med. Virol. 6, 129-138. doi:10.1002/jmv.1890060205.
13. Bowen, E. T., Platt, G. S., Simpson, D. I., McArdell, L. B., and Raymond, R. T. (1978). Ebola haemorrhagic fever:experimental infection of monkeys. Trans. R. Soc. Trop. Med. Hyg. 72, 188-191. doi:10.1016/0035-9203(78)90058-5.
14. Bradfute, S. B., Braun, D. R., Shamblin, J. D., Geisbert, J. B., Paragas, J., Garrison, A., et al. (2007). Lymphocyte death in a mouse model of Ebola virus infection. J. Infect. Dis. 196(Suppl. 2), S296-S304. doi:10.1086/520602.
15. Bradfute, S. B., Warfield, K. L., and Bray, M. (2012). Mouse models for filovirus infections. Viruses 4, 1477-1508. doi:10.3390/v4091477.
16. Bray, M. (2001). The role of the Type I interferon response in the resistance of mice to filovirus infection. J. Gen. Virol. 82, 1365-1373.
17. Bray, M., Davis, K., Geisbert, T., Schmaljohn, C., and Huggins, J. (1999). A mouse model for evaluation of prophylaxis and therapy of Ebola hemorrhagic fever. J. Infect. Dis. 179(Suppl. 1), S248-S258. doi:10.1086/514292.
18. Bray, M., Hatfill, S., Hensley, L., and Huggins, J. W. (2001). Haematological, biochemical and coagulation changes in mice, guinea-pigs and monkeys infected with a mouse-adapted variant of Ebola Zaire virus. J. Comp. Pathol. 125, 243-253. doi:10.1053/jcpa.2001.0503.
19. Bukreyev, A., Marzi, A., Feldmann, F., Zhang, L., Yang, L., Ward, J. M., et al. (2009). Chimeric human parainfluenza virus bearing the Ebola virus glycoprotein as the sole surface protein is immunogenic and highly protective against Ebola virus challenge. Virology 383, 348-361. doi:10.1016/j.virol.2008.09.030.
20. Bukreyev, A., Rollin, P. E., Tate, M. K., Yang, L., Zaki, S. R., Shieh, W. J., et al. (2007). Successful topical respiratory tract immunization of primates against Ebola virus. J. Virol. 81, 6379-6388. doi:10.1128/JVI.00105-07.
21. Bukreyev, A., Yang, L., Zaki, S. R., Shieh, W. J., Rollin, P. E., Murphy, B. R., et al. (2006). A single intranasal inoculation with a paramyxovirus-vectored vaccine protects guinea pigs against a lethal-dose Ebola virus challenge. J. Virol. 80, 2267-2279. doi:10.1128/JVI.80.5.2267-2279.2006.
22. Bukreyev, A. A., Dinapoli, J. M., Yang, L., Murphy, B. R., and Collins, P. L. (2010). Mucosal parainfluenza virus-vectored vaccine against Ebola virus replicates in the respiratory tract of vector-immune monkeys and is immunogenic. Virology 399, 290-298. doi:10.1016/j.virol.2010.01.015.
23. Bwaka, M. A., Bonnet, M. J., Calain, P., Colebunders, R., De Roo, A., Guimard, Y., et al. (1999). Ebola hemorrhagic fever in Kikwit, Democratic Republic of the Congo:clinical observations in 103 patients. J. Infect. Dis. 179(Suppl. 1), S1-S7. doi:10.1086/514308.
24. Chupurnov, A. A., Chernukhin, I. V., Ternovoi, V. A., Kudoiarova, N. M., Makhova, N. M., Azaev, M., et al. (1995). Attempts to develop a vaccine against Ebola fever. Vopr. Virusol. 40, 257-260.
25. Connolly, B. M., Steele, K. E., Davis, K. J., Geisbert, T. W., Kell, W. M., Jaax, N. K., et al. (1999). Pathogenesis of experimental Ebola virus infection in guinea pigs. J. Infect. Dis. 179(Suppl. 1), S203-S217. doi:10.1086/514305.
26. Cote, M., Misasi, J., Ren, T., Bruchez, A., Lee, K., Filone, C. M., et al. (2011). Small molecule inhibitors reveal Niemann-Pick C1 is essential for Ebola virus infection. Nature 477, 344-348. doi:10.1038/nature10380.
27. Daddario-Dicaprio, K. M., Geisbert, T. W., Geisbert, J. B., Stroher, U., Hensley, L. E., Grolla, A., et al. (2006a). Cross-protection against Marburg virus strains by using a live, attenuated recombinant vaccine. J. Virol. 80, 9659-9666. doi:10.1128/JVI.00959-06.
28. Daddario-Dicaprio, K. M., Geisbert, T. W., Stroher, U., Geisbert, J. B., Grolla, A., Fritz, E. A., et al. (2006b). Postexposure protection against Marburg haemorrhagic fever with recombinant vesicular stomatitis virus vectors in non-human primates:an efficacy assessment. Lancet 367, 1399-1404. doi:10.1016/S0140-6736(06)68546-2.
29. Dalgard, D. W., Hardy, R. J., Pearson, S. L., Pucak, G. J., Quander, R. V., Zack, P. M., et al. (1992). Combined simian hemorrhagic fever and Ebola virus infection in cynomolgus monkeys. Lab. Anim. Sci. 42, 152-157.
30. Davis, K. J., Anderson, A. O., Geisbert, T. W., Steele, K. E., Geisbert, J. B., Vogel, P., et al. (1997). Pathology of experimental Ebola virus infection in African green monkeys. Involvement of fibroblastic reticular cells. Arch. Pathol. Lab. Med. 121, 805-819.
31. Dietrich, M., Schumacher, H. H., Peters, D., and Knobloch, J. (1978). "Human pathology of Ebola (Maridi) virus infection in the Sudan," in Ebola Virus Haemorrhagic Fever, ed S. R. Pattyn (New York, NY:Elsevier, North-Holland Biomedical Press), 37-41.
32. Ebihara, H., Rockx, B., Marzi, A., Feldmann, F., Haddock, E., Brining, D., et al. (2011). Host response dynamics following lethal infection of rhesus macaques with Zaire ebolavirus. J. Infect. Dis. 204(Suppl. 3), S991-999. doi:10.1093/infdis/jir336.
33. Ebihara, H., Takada, A., Kobasa, D., Jones, S., Neumann, G., Theriault, S., et al. (2006). Molecular determinants of Ebola virus virulence in mice. PLoS Pathog. 2:e73. doi:10.1371/journal.ppat.0020073.
34. Ebihara, H., Zivcec, M., Gardner, D., Falzarano, D., Lacasse, R., Rosenke, R., et al. (2013). A syrian golden hamster model recapitulating ebola hemorrhagic fever. J. Infect. Dis. 207, 306-318. doi:10.1093/infdis/jis626.
35. Ellis, D. S., Bowen, E. T., Simpson, D. I., and Stamford, S. (1978). Ebola virus:a comparison, at ultrastructural level, of the behaviour of the Sudan and Zaire strains in monkeys. Br. J. Exp. Pathol. 59, 584-593.
36. Falzarano, D., Geisbert, T. W., and Feldmann, H. (2011). Progress in filovirus vaccine development:evaluating the potential for clinical use. Expert Rev. Vaccines 10, 63-77. doi:10.1586/erv.10.152.
37. Feldmann, H., Jones, S. M., Daddario-Dicaprio, K. M., Geisbert, J. B., Stroher, U., Grolla, A., et al. (2007). Effective post-exposure treatment of Ebola infection. PLoS Pathog. 3:e2. doi:10.1371/journal.ppat.0030002.
38. Fisher-Hoch, S. P., Brammer, T. L., Trappier, S. G., Hutwagner, L. C., Farrar, B. B., Ruo, S. L., et al. (1992). Pathogenic potential of filoviruses:role of geographic origin of primate host and virus strain. J. Infect. Dis. 166, 753-763. doi:10.1093/infdis/166.4.753.
39. Fisher-Hoch, S. P., Platt, G. S., Neild, G. H., Southee, T., Baskerville, A., Raymond, R. T., et al. (1985). Pathophysiology of shock and hemorrhage in a fulminating viral infection (Ebola). J. Infect. Dis. 152, 887-894. doi:10.1093/infdis/152.5.887.
40. Fowler, T., Bamberg, S., Moller, P., Klenk, H. D., Meyer, T. F., Becker, S., et al. (2005). Inhibition of Marburg virus protein expression and viral release by RNA interference. J. Gen. Virol. 86, 1181-1188. doi:10.1099/vir.0.80622-0.
41. Friedrich, B. M., Trefry, J. C., Biggins, J. E., Hensley, L. E., Honko, A. N., Smith, D. R., et al. (2012). Potential vaccines and post-exposure treatments for filovirus infections. Viruses 4, 1619-1650. doi:10.3390/v4091619.
42. Geisbert, T. W., Bailey, M., Geisbert, J. B., Asiedu, C., Roederer, M., Grazia-Pau, M., et al. (2010a). Vector choice determines immunogenicity and potency of genetic vaccines against Angola Marburg virus in nonhuman primates. J. Virol. 84, 10386-10394. doi:10.1128/JVI.00594-10.
43. Geisbert, T. W., Bausch, D. G., and Feldmann, H. (2010b). Prospects for immunisation against Marburg and Ebola viruses. Rev. Med. Virol. 20, 344-357.
44. Geisbert, T. W., Hensley, L. E., Geisbert, J. B., Leung, A., Johnson, J. C., Grolla, A., et al. (2010c). Postexposure treatment of Marburg virus infection. Emerging Infect. Dis. 16, 1119-1122. doi:10.3201/eid1607.100159.
45. Geisbert, T. W., Lee, A. C., Robbins, M., Geisbert, J. B., Honko, A. N., Sood, V., et al. (2010d). Postexposure protection of non-human primates against a lethal Ebola virus challenge with RNA interference:a proof-of-concept study. Lancet 375, 1896-1905. doi:10.1016/S0140-6736(10)60357-1.
46. Geisbert, T. W., Bailey, M., Hensley, L., Asiedu, C., Geisbert, J., Stanley, D., et al. (2011). Recombinant adenovirus serotype 26 (Ad26) and Ad35 vaccine vectors bypass immunity to Ad5 and protect nonhuman primates against ebolavirus challenge. J. Virol. 85, 4222-4233. doi:10.1128/JVI.02407-10.
47. Geisbert, T. W., Daddario-Dicaprio, K. M., Geisbert, J. B., Young, H. A., Formenty, P., Fritz, E. A., et al. (2007). Marburg virus Angola infection of rhesus macaques:pathogenesis and treatment with recombinant nematode anticoagulant protein c2. J. Infect. Dis. 196(Suppl. 2), S372-S381. doi:10.1086/520608.
48. Geisbert, T. W., Daddario-Dicaprio, K. M., Williams, K. J., Geisbert, J. B., Leung, A., Feldmann, F., et al. (2008). Recombinant vesicular stomatitis virus vector mediates postexposure protection against Sudan Ebola hemorrhagic fever in nonhuman primates. J. Virol. 82, 5664-5668. doi:10.1128/JVI.00456-08.
49. Geisbert, T. W., Geisbert, J. B., Leung, A., Daddario-Dicaprio, K. M., Hensley, L. E., Grolla, A., et al. (2009). Single-injection vaccine protects nonhuman primates against infection with marburg virus and three species of ebola virus. J. Virol. 83, 7296-7304. doi:10.1128/JVI.00561-09.
50. Geisbert, T. W., Hensley, L. E., Gibb, T. R., Steele, K. E., Jaax, N. K., and Jahrling, P. B. (2000). Apoptosis induced in vitro and in vivo during infection by Ebola and Marburg viruses. Lab. Invest. 80, 171-186. doi:10.1038/labinvest.3780021.
51. Geisbert, T. W., Hensley, L. E., Jahrling, P. B., Larsen, T., Geisbert, J. B., Paragas, J., et al. (2003a). Treatment of Ebola virus infection with a recombinant inhibitor of factor VIIa/tissue factor:a study in rhesus monkeys. Lancet 362, 1953-1958. doi:10.1016/S0140-6736(03)15012-X.
52. Geisbert, T. W., Hensley, L. E., Larsen, T., Young, H. A., Reed, D. S., Geisbert, J. B., et al. (2003b). Pathogenesis of Ebola hemorrhagic fever in cynomolgus macaques:evidence that dendritic cells are early and sustained targets of infection. Am. J. Pathol. 163, 2347-2370.
53. Geisbert, T. W., Jahrling, P. B., Larsen, T., Davis, K. J., and Hensley, L. E. (2003c). Filovirus Pathogenesis in Nonhuman Primates. Wymondham, Norfolk:Taylor and Francis.
54. Geisbert, T. W., Young, H. A., Jahrling, P. B., Davis, K. J., Kagan, E., and Hensley, L. E. (2003d). Mechanisms underlying coagulation abnormalities in ebola hemorrhagic fever:overexpression of tissue factor in primate monocytes/macrophages is a key event. J. Infect. Dis. 188, 1618-1629. doi:10.1086/379724.
55. Geisbert, T. W., Young, H. A., Jahrling, P. B., Davis, K. J., Larsen, T., Kagan, E., et al. (2003e). 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. 163, 2371-2382.
56. Geisbert, T. W., Hensley, L. E., Kagan, E., Yu, E. Z., Geisbert, J. B., Daddario-Dicaprio, K., et al. (2006). Postexposure protection of guinea pigs against a lethal ebola virus challenge is conferred by RNA interference. J. Infect. Dis. 193, 1650-1657. doi:10.1086/504267.
57. Geisbert, T. W., Pushko, P., Anderson, K., Smith, J., Davis, K. J., and Jahrling, P. B. (2002). Evaluation in nonhuman primates of vaccines against Ebola virus. Emerging Infect. Dis. 8, 503-507. doi:10.3201/eid0805.010284.
58. Gibb, T. R., Norwood, D. A. Jr., Woollen, N., and Henchal, E. A. (2001). Development and evaluation of a fluorogenic 5' nuclease assay to detect and differentiate between Ebola virus subtypes Zaire and Sudan. J. Clin. Microbiol. 39, 4125-4130. doi:10.1128/JCM.39.11.4125-4130.2001.
59. Gonchar, N. I., Pshenichnov, V. A., Pokhodiaev, V. A., Lopatov, K. L., and Firsova, I. V. (1991). The sensitivity of different experimental animals to the Marburg virus. Vopr. Virusol. 36, 435-437.
60. Gupta, M., Greer, P., Mahanty, S., Shieh, W. J., Zaki, S. R., Ahmed, R., et al. (2005). CD8-mediated protection against Ebola virus infection is perforin dependent. J. Immunol. 174, 4198-4202.
61. Halfmann, P., Ebihara, H., Marzi, A., Hatta, Y., Watanabe, S., Suresh, M., et al. (2009). Replication-deficient ebolavirus as a vaccine candidate. J. Virol. 83, 3810-3815. doi:10.1128/JVI.00074-09.
62. Halfmann, P., Neumann, G., and Kawaoka, Y. (2011). The Ebolavirus VP24 protein blocks phosphorylation of p38 mitogen-activated protein kinase. J. Infect. Dis. 204(Suppl. 3), S953-S956. doi:10.1093/infdis/jir325.
63. Hall, W. C., Geisbert, T. W., Huggins, J. W., and Jahrling, P. B. (1996). Experimental infection of guinea pigs with Venezuelan hemorrhagic fever virus (Guanarito):a model of human disease. Am. J. Trop. Med. Hyg. 55, 81-88.
64. Hass, R., and Maass, G. (1971). "Experimental infection of monkeys with the marburg virus," in Marburg Virus Disease, eds G. A. Martini and R. Siegert (New York, NY:Springer, Berlin Heidelberg), 136-143.
65. Hensley, L. E., Alves, D. A., Geisbert, J. B., Fritz, E. A., Reed, C., Larsen, T., et al. (2011). Pathogenesis of Marburg hemorrhagic fever in cynomolgus macaques. J. Infect. Dis. 204(Suppl. 3), S1021-S1031. doi:10.1093/infdis/jir339.
66. Hensley, L. E., Stevens, E. L., Yan, S. B., Geisbert, J. B., Macias, W. L., Larsen, T., et al. (2007). Recombinant human activated protein C for the postexposure treatment of Ebola hemorrhagic fever. J. Infect. Dis. 196(Suppl. 2), S390-S399. doi:10.1086/520598.
67. Hevey, M., Negley, D., Pushko, P., Smith, J., and Schmaljohn, A. (1998). Marburg virus vaccines based upon alphavirus replicons protect guinea pigs and nonhuman primates. Virology 251, 28-37. doi:10.1006/viro.1998.9367.
68. Ignat'ev, G. M., Agafonov, A. P., Strel'tsova, M. A., Kuz'min, V. A., Mainagasheva, G. I., Spirin, G. V., et al. (1991). A comparative study of the immunological indices in guinea pigs administered an inactivated Marburg virus. Vopr. Virusol. 36, 421-423.
69. Ignatiev, G. M., Dadaeva, A. A., Luchko, S. V., and Chepurnov, A. A. (2000). Immune and pathophysiological processes in baboons experimentally infected with Ebola virus adapted to guinea pigs. Immunol. Lett. 71, 131-140. doi:10.1016/S0165-2478(99)00169-8.
70. Ignatyev, G. M., Agafonov, A. P., Streltsova, M. A., and Kashentseva, E. A. (1996). Inactivated Marburg virus elicits a nonprotective immune response in Rhesus monkeys. J. Biotechnol. 44, 111-118. doi:10.1016/0168-1656(95)00104-2.
71. Isaacson, M., Sureau, P., Courteille, G., and Pattyn, S. R. (1978). "Clinical aspets of Ebola virus disease at the Ngaliema hospital, Kinshasa, Zaire, 1976," in Ebola Virus Haemorrhagic Fever, ed S. R. Pattyn (New York, NY:Elsevier, North-Holland Biomedical Press), 15-20.
72. Jaax, N., Jahrling, P., Geisbert, T., Geisbert, J., Steele, K., McKee, K., et al. (1995). Transmission of Ebola virus (Zaire strain) to uninfected control monkeys in a biocontainment laboratory. Lancet 346, 1669-1671. doi:10.1016/S0140-6736(95)92841-3.
73. Jaax, N. K., Davis, K. J., Geisbert, T. J., Vogel, P., Jaax, G. P., Topper, M., et al. (1996). Lethal experimental infection of rhesus monkeys with Ebola-Zaire (Mayinga) virus by the oral and conjunctival route of exposure. Arch. Pathol. Lab. Med. 120, 140-155.
74. Jahrling, P. B., Geisbert, T. W., Dalgard, D. W., Johnson, E. D., Ksiazek, T. G., Hall, W. C., et al. (1990). Preliminary report:isolation of Ebola virus from monkeys imported to USA. Lancet 335, 502-505. doi:10.1016/0140-6736(90)90737-P.
75. Jahrling, P. B., Geisbert, T. W., Jaax, N. K., Hanes, M. A., Ksiazek, T. G., and Peters, C. J. (1996). Experimental infection of cynomolgus macaques with Ebola-Reston filoviruses from the 1989-1990 U.S. epizootic. Arch. Virol. Suppl. 11, 115-134. doi:10.1007/978-3-7091-7482-1_11.
76. Jahrling, P. B., Smith, S., Hesse, R. A., and Rhoderick, J. B. (1982). Pathogenesis of Lassa virus infection in guinea pigs. Infect. Immun. 37, 771-778.
77. Johnson, E., Jaax, N., White, J., and Jahrling, P. (1995). Lethal experimental infections of rhesus monkeys by aerosolized Ebola virus. Int. J. Exp. Pathol. 76, 227-236.
78. Johnson, E. D., Johnson, B. K., Silverstein, D., Tukei, P., Geisbert, T. W., Sanchez, A. N., et al. (1996). Characterization of a new Marburg virus isolated from a 1987 fatal case in Kenya. Arch. Virol. Suppl. 11, 101-114. doi:10.1007/978-3-7091-7482-1_10.
79. Jones, S. M., Feldmann, H., Stroher, U., Geisbert, J. B., Fernando, L., Grolla, A., et al. (2005). Live attenuated recombinant vaccine protects nonhuman primates against Ebola and Marburg viruses. Nat. Med. 11, 786-790. doi:10.1038/nm1258.
80. Kenyon, R. H., Condie, R. M., Jahrling, P. B., and Peters, C. J. (1990). Protection of guinea pigs against experimental Argentine hemorrhagic fever by purified human IgG:importance of elimination of infected cells. Microb. Pathog. 9, 219-226. doi:10.1016/0882-4010(90)90010-N.
81. Konduru, K., Bradfute, S. B., Jacques, J., Manangeeswaran, M., Nakamura, S., Morshed, S., et al. (2011). Ebola virus glycoprotein Fc fusion protein confers protection against lethal challenge in vaccinated mice. Vaccine 29, 2968-2977. doi:10.1016/j.vaccine.2011.01.113.
82. Korb, G., and Slenczka, W. (1971). "Histologic findings in livers and spleens of guinea pigs after inoculation by the marburg virus," in Marburg Virus Disease, eds G. A. Martini and R. Siegert (New York, NY:Springer, Berlin Heidelberg), 123-128.
83. Ksiazek, T. G., Rollin, P. E., Williams, A. J., Bressler, D. S., Martin, M. L., Swanepoel, R., et al. (1999). Clinical virology of Ebola hemorrhagic fever (EHF):virus, virus antigen, and IgG and IgM antibody findings among EHF patients in Kikwit, Democratic Republic of the Congo, 1995. J. Infect. Dis. 179(Suppl. 1), S177-S187. doi:10.1086/514321.
84. Kuhn, J. H. (2008). Filoviruses:A Compendium of 40 Years of Epidemiological, Clinical, and Laboratory Studies. New York, NY:Springer Wien.
85. Kuhn, J. H., Bao, Y., Bavari, S., Becker, S., Bradfute, S., Brister, J. R., et al. (2013). Virus nomenclature below the species level:a standardized nomenclature for natural variants of viruses assigned to the family Filoviridae. Arch. Virol. 158, 301-311. doi:10.1007/s00705-012-1454-0.
86. Kuhn, J. H., Dodd, L. E., Wahl-Jensen, V., Radoshitzky, S. R., Bavari, S., and Jahrling, P. B. (2011). Evaluation of perceived threat differences posed by filovirus variants. Biosecur. Bioterror. 9, 361-371. doi:10.1089/bsp.2011.0051.
87. Leroy, E. M., Epelboin, A., Mondonge, V., Pourrut, X., Gonzalez, J. P., Muyembe-Tamfum, J. J., et al. (2009). Human Ebola outbreak resulting from direct exposure to fruit bats in Luebo, Democratic Republic of Congo, 2007. Vector Borne Zoonotic Dis. 9, 723-728. doi:10.1089/vbz.2008.0167.
88. Leroy, E. M., Rouquet, P., Formenty, P., Souquiere, S., Kilbourne, A., Froment, J. M., et al. (2004). Multiple Ebola virus transmission events and rapid decline of central African wildlife. Science 303, 387-390. doi:10.1126/science.1092528.
89. Luchko, S. V., Dadaeva, A. A., Ustinova, E. N., Sizikova, L. P., Riabchikova, E. I., and Sandakhchiev, L. S. (1995). Experimental study of Ebola hemorrhagic fever in baboon models. Biull. Eksp. Biol. Med. 120, 302-304. doi:10.1007/BF02445023.
90. Martin, J. E., Sullivan, N. J., Enama, M. E., Gordon, I. J., Roederer, M., Koup, R. A., et al. (2006). A DNA vaccine for Ebola virus is safe and immunogenic in a phase I clinical trial. Clin. Vaccine Immunol. 13, 1267-1277. doi:10.1128/CVI.00162-06.
91. Martini, G. A. (1971). "Marburg virus disease. Clinical symptome," in Marburg Virus Disease, eds G. A. Martini and R. Siegert (New York, NY:Springer, Berlin Heidelberg), 1-9.
92. Mast, T. C., Kierstead, L., Gupta, S. B., Nikas, A. A., Kallas, E. G., Novitsky, V., et al. (2010). International epidemiology of human pre-existing adenovirus (Ad) type-5, type-6, type-26 and type-36 neutralizing antibodies:correlates of high Ad5 titers and implications for potential HIV vaccine trials. Vaccine 28, 950-957. doi:10.1016/j.vaccine.2009.10.145.
93. Mateo, M., Carbonnelle, C., Reynard, O., Kolesnikova, L., Nemirov, K., Page, A., et al. (2011). VP24 is a molecular determinant of Ebola virus virulence in guinea pigs. J. Infect. Dis. 204(Suppl. 3), S1011-S1020. doi:10.1093/infdis/jir338.
94. Mateo, M., Reid, S. P., Leung, L. W., Basler, C. F., and Volchkov, V. E. (2010). Ebolavirus VP24 binding to karyopherins is required for inhibition of interferon signaling. J. Virol. 84, 1169-1175. doi:10.1128/JVI.01372-09.
95. Michelow, I. C., Lear, C., Scully, C., Prugar, L. I., Longley, C. B., Yantosca, L. M., et al. (2011). High-dose mannose-binding lectin therapy for Ebola virus infection. J. Infect. Dis. 203, 175-179. doi:10.1093/infdis/jiq025.
96. Mikhailov, V. V., Borisevich, I. V., Chernikova, N. K., Potryvaeva, N. V., and Krasnianskii, V. P. (1994). The evaluation in hamadryas baboons of the possibility for the specific prevention of Ebola fever. Vopr. Virusol. 39, 82-84.
97. Miranda, M. E., Ksiazek, T. G., Retuya, T. J., Khan, A. S., Sanchez, A., Fulhorst, C. F., et al. (1999). Epidemiology of Ebola (subtype Reston) virus in the Philippines, 1996. J. Infect. Dis. 179(Suppl. 1), S115-S119. doi:10.1086/514314.
98. Miranda, M. E., Yoshikawa, Y., Manalo, D. L., Calaor, A. B., Miranda, N. L., Cho, F., et al. (2002). Chronological and spatial analysis of the 1996 Ebola Reston virus outbreak in a monkey breeding facility in the Philippines. Exp. Anim. 51, 173-179. doi:10.1538/expanim.51.173.
99. Murphy, F. A., Simpson, D. I., Whitfield, S. G., Zlotnik, I., and Carter, G. B. (1971). Marburg virus infection in monkeys. Ultrastructural studies. Lab. Invest. 24, 279-291.
100. Ndambi, R., Akamituna, P., Bonnet, M. J., Tukadila, A. M., Muyembe-Tamfum, J. J., and Colebunders, R. (1999). Epidemiologic and clinical aspects of the Ebola virus epidemic in Mosango, Democratic Republic of the Congo, 1995. J. Infect. Dis. 179(Suppl. 1), S8-S10. doi:10.1086/514297.
101. Negredo, A., Palacios, G., Vazquez-Moron, S., Gonzalez, F., Dopazo, H., Molero, F., et al. (2011). Discovery of an ebolavirus-like filovirus in europe. PLoS Pathog. 7:e1002304. doi:10.1371/journal.ppat.1002304.
102. Phoolcharoen, W., Bhoo, S. H., Lai, H., Ma, J., Arntzen, C. J., Chen, Q., et al. (2011). Expression of an immunogenic Ebola immune complex in Nicotiana benthamiana. Plant Biotechnol. J. 9, 807-816. doi:10.1111/j.1467-7652.2011.00593.x.
103. Piedra, P. A., Poveda, G. A., Ramsey, B., McCoy, K., and Hiatt, P. W. (1998). Incidence and prevalence of neutralizing antibodies to the common adenoviruses in children with cystic fibrosis:implication for gene therapy with adenovirus vectors. Pediatrics 101, 1013-1019. doi:10.1542/peds.101.6.1013.
104. Piot, P., Sureau, P., Breman, G., Heymann, D., Kintoki, V., Masamba, M., et al. (1978). "Clinical aspects of Ebola virus infection in Tambuku area, Zaire, 1976," in Ebola Virus Haemorrhagic Fever, ed S. R. Pattyn (New York, NY:Elsevier, North-Holland Biomedical Press), 7-14.
105. Pokhodiaev, V. A., Gonchar, N. I., and Pshenichnov, V. A. (1991). An experimental study of the contact transmission of the Marburg virus. Vopr. Virusol. 36, 506-508.
106. Pushko, P., Bray, M., Ludwig, G. V., Parker, M., Schmaljohn, A., Sanchez, A., et al. (2001). Recombinant RNA replicons derived from attenuated Venezuelan equine encephalitis virus protect guinea pigs and mice from Ebola hemorrhagic fever virus. Vaccine 19, 142-153. doi:10.1016/S0264-410X(00)00113-4.
107. Qiu, X., Fernando, L., Alimonti, J. B., Melito, P. L., Feldmann, F., Dick, D., et al. (2009). Mucosal immunization of cynomolgus macaques with the VSVDeltaG/ZEBOVGP vaccine stimulates strong ebola GP-specific immune responses. PLoS ONE 4:e5547. doi:10.1371/journal.pone.0005547.
108. Ramanan, P., Edwards, M. R., Shabman, R. S., Leung, D. W., Endlich-Frazier, A. C., Borek, D. M., et al. (2012). Structural basis for Marburg virus VP35-mediated immune evasion mechanisms. Proc. Natl. Acad. Sci. U.S.A. 109, 20661-20666. doi:10.1073/pnas.1213559109.
109. Ramanan, P., Shabman, R. S., Brown, C. S., Amarasinghe, G. K., Basler, C. F., and Leung, D. W. (2011). Filoviral immune evasion mechanisms. Viruses 3, 1634-1649. doi:10.3390/v3091634.
110. Reid, S. P., Valmas, C., Martinez, O., Sanchez, F. M., and Basler, C. F. (2007). Ebola virus VP24 proteins inhibit the interaction of NPI-1 subfamily karyopherin alpha proteins with activated STAT1. J. Virol. 81, 13469-13477. doi:10.1128/JVI.01097-07.
111. Riemenschneider, J., Garrison, A., Geisbert, J., Jahrling, P., Hevey, M., Negley, D., et al. (2003). Comparison of individual and combination DNA vaccines for B. anthracis, Ebola virus, Marburg virus and Venezuelan equine encephalitis virus. Vaccine 21, 4071-4080. doi:10.1016/S0264-410X(03)00362-1.
112. Robin, Y., Bres, P., and Camain, R. (1971). "Passage of marburg virus in guinea pigs," in Marburg Virus Disease, eds G. A. Martini and R. Siegert (New York, NY:Springer, Berlin Heidelberg), 117-122.
113. Ryabchikova, E., Kolesnikova, L., Smolina, M., Tkachev, V., Pereboeva, L., Baranova, S., et al. (1996). Ebola virus infection in guinea pigs:presumable role of granulomatous inflammation in pathogenesis. Arch. Virol. 141, 909-921. doi:10.1007/BF01718165.
114. Ryabchikova, E., Smolina, M. A. G., and Rassadkin, J. (2003). Ebola virus infection in the guinea pig. Wymondham, Norfolk:Taylor and Francis.
115. Ryabchikova, E. I., Kolesnikova, L. V., and Luchko, S. V. (1999). An analysis of features of pathogenesis in two animal models of Ebola virus infection. J. Infect. Dis. 179(Suppl. 1), S199-S202. doi:10.1086/514293.
116. Sanchez, A., Geisbert, T. W., and Felsmann, H. (2007). Marburg and Ebola Viruses. Philadelphia, PA:Lippincott Williams and Wilkins.
117. Sanchez, A., Lukwiya, M., Bausch, D., Mahanty, S., Sanchez, A. J., Wagoner, K. D., et al. (2004). Analysis of human peripheral blood samples from fatal and nonfatal cases of Ebola (Sudan) hemorrhagic fever:cellular responses, virus load, and nitric oxide levels. J. Virol. 78, 10370-10377. doi:10.1128/JVI.78.19.10370-10377.2004.
118. Schulick, A. H., Vassalli, G., Dunn, P. F., Dong, G., Rade, J. J., Zamarron, C., et al. (1997). Established immunity precludes adenovirus-mediated gene transfer in rat carotid arteries. Potential for immunosuppression and vector engineering to overcome barriers of immunity. J. Clin. Invest. 99, 209-219. doi:10.1172/JCI119149.
119. Simpson, D. I. (1969). Marburg agent disease:in monkeys. Trans. R. Soc. Trop. Med. Hyg. 63, 303-309. doi:10.1016/0035-9203(69)90002-9.
120. Simpson, D. I., Zlotnik, I., and Rutter, D. A. (1968). Vervet monkey disease. Experiment infection of guinea pigs and monkeys with the causative agent. Br. J. Exp. Pathol. 49, 458-464.
121. Smith, D. H., Francis, F., and Simpson, D. I. H. (1978). "African haemorrhagic fever in the Southern Sudan, 1976:the clinical manifestations," in Ebola Virus Haemorrhagic Fever, ed S. R. Pattyn (New York, NY:Elsevier, North-Holland Biomedical Press), 21-26.
122. Smith, D. R., McCarthy, S., Chrovian, A., Olinger, G., Stossel, A., Geisbert, T. W., et al. (2010). Inhibition of heat-shock protein 90 reduces Ebola virus replication. Antiviral Res. 87, 187-194. doi:10.1016/j.antiviral.2010.04.015.
123. Spiridonov, V. A., Bazhutin, N. B., Belanov, E. F., Voitenko, A. V., Zolin, V. V., Krivenchuk, N. A., et al. (1992). Changes in the blood serum aminotransferase activity in the experimental infection of Cercopithecus aethiops monkeys with the Marburg virus. Vopr. Virusol. 37, 156-157.
124. Subbotina, E., Dadaeva, A., Kachko, A., and Chepurnov, A. (2010). Genetic factors of Ebola virus virulence in guinea pigs. Virus Res. 153, 121-133. doi:10.1016/j.virusres.2010.07.015.
125. Sullivan, N. J., Geisbert, T. W., Geisbert, J. B., Xu, L., Yang, Z. Y., Roederer, M., et al. (2003). Accelerated vaccination for Ebola virus haemorrhagic fever in non-human primates. Nature 424, 681-684. doi:10.1038/nature01876.
126. Sullivan, N. J., Sanchez, A., Rollin, P. E., Yang, Z. Y., and Nabel, G. J. (2000). Development of a preventive vaccine for Ebola virus infection in primates. Nature 408, 605-609. doi:10.1038/35046108.
127. Sun, Y., Carrion, R. Jr., Ye, L., Wen, Z., Ro, Y. T., et al. (2009). Protection against lethal challenge by Ebola virus-like particles produced in insect cells. Virology 383, 12-21. doi:10.1016/j.virol.2008.09.020.
128. Swenson, D. L., Wang, D., Luo, M., Warfield, K. L., Woraratanadharm, J., Holman, D. H., et al. (2008a). Vaccine to confer to nonhuman primates complete protection against multistrain Ebola and Marburg virus infections. Clin. Vaccine Immunol. 15, 460-467. doi:10.1128/CVI.00431-07.
129. Swenson, D. L., Warfield, K. L., Larsen, T., Alves, D. A., Coberley, S. S., and Bavari, S. (2008b). Monovalent virus-like particle vaccine protects guinea pigs and nonhuman primates against infection with multiple Marburg viruses. Expert Rev. Vaccines 7, 417-429.
130. Swenson, D. L., Warfield, K. L., Warren, T. K., Lovejoy, C., Hassinger, J. N., Ruthel, G., et al. (2009). Chemical modifications of antisense morpholino oligomers enhance their efficacy against Ebola virus infection. Antimicrob. Agents Chemother. 53, 2089-2099. doi:10.1128/AAC.00936-08.
131. Towner, J. S., Rollin, P. E., Bausch, D. G., Sanchez, A., Crary, S. M., Vincent, M., et al. (2004). Rapid diagnosis of Ebola hemorrhagic fever by reverse transcription-PCR in an outbreak setting and assessment of patient viral load as a predictor of outcome. J. Virol. 78, 4330-4341. doi:10.1128/JVI.78.8.4330-4341.2004.
132. Tsuda, Y., Caposio, P., Parkins, C. J., Botto, S., Messaoudi, I., Cicin-Sain, L., et al. (2011a). A replicating cytomegalovirus-based vaccine encoding a single Ebola virus nucleoprotein CTL epitope confers protection against Ebola virus. PLoS Negl. Trop. Dis. 5:e1275. doi:10.1371/journal.pntd.0001275.
133. Tsuda, Y., Safronetz, D., Brown, K., Lacasse, R., Marzi, A., Ebihara, H., et al. (2011b). Protective efficacy of a bivalent recombinant vesicular stomatitis virus vaccine in the Syrian hamster model of lethal Ebola virus infection. J. Infect. Dis. 204(Suppl. 3), S1090-S1097. doi:10.1093/infdis/jir379.
134. Tuffs, A. (2009). Experimental vaccine may have saved Hamburg scientist from Ebola fever. BMJ 338:b1223. doi:10.1136/bmj.b1223.
135. van der Groen, G., Jacob, W., and Pattyn, S. R. (1979). Ebola virus virulence for newborn mice. J. Med. Virol. 4, 239-240. doi:10.1002/jmv.1890040309.
136. Vanderzanden, L., Bray, M., Fuller, D., Roberts, T., Custer, D., Spik, K., et al. (1998). DNA vaccines expressing either the GP or NP genes of Ebola virus protect mice from lethal challenge. Virology 246, 134-144. doi:10.1006/viro.1998.9176.
137. Vogels, R., Zuijdgeest, D., van Rijnsoever, R., Hartkoorn, E., Damen, I., de Bethune, M. P., et al. (2003). Replication-deficient human adenovirus type 35 vectors for gene transfer and vaccination:efficient human cell infection and bypass of preexisting adenovirus immunity. J. Virol. 77, 8263-8271. doi:10.1128/JVI.77.15.8263-8271.2003.
138. Volchkov, V. E., Chepurnov, A. A., Volchkova, V. A., Ternovoj, V. A., and Klenk, H. D. (2000). Molecular characterization of guinea pig-adapted variants of Ebola virus. Virology 277, 147-155. doi:10.1006/viro.2000.0572.
139. Wahl-Jensen, V., Bollinger, L., Safronetz, D., de Kok-Mercado, F., Scott, D. P., and Ebihara, H. (2012). Use of the Syrian hamster as a new model of ebola virus disease and other viral hemorrhagic fevers. Viruses 4, 3754-3784. doi:10.3390/v4123754.
140. Wang, D., Hevey, M., Juompan, L. Y., Trubey, C. M., Raja, N. U., Deitz, S. B., et al. (2006a). Complex adenovirus-vectored vaccine protects guinea pigs from three strains of Marburg virus challenges. Virology 353, 324-332. doi:10.1016/j.virol.2006.05.033.
141. Wang, D., Raja, N. U., Trubey, C. M., Juompan, L. Y., Luo, M., Woraratanadharm, J., et al. (2006b). Development of a cAdVax-based bivalent ebola virus vaccine that induces immune responses against both the Sudan and Zaire species of Ebola virus. J. Virol. 80, 2738-2746. doi:10.1128/JVI.80.6.2738-2746.2006.
142. Warfield, K. L., Bosio, C. M., Welcher, B. C., Deal, E. M., Mohamadzadeh, M., Schmaljohn, A., et al. (2003). Ebola virus-like particles protect from lethal Ebola virus infection. Proc. Natl. Acad. Sci. U.S.A. 100, 15889-15894. doi:10.1073/pnas.2237038100.
143. Warfield, K. L., Bradfute, S. B., Wells, J., Lofts, L., Cooper, M. T., Alves, D. A., et al. (2009). Development and characterization of a mouse model for Marburg hemorrhagic fever. J. Virol. 83, 6404-6415. doi:10.1128/JVI.00126-09.
144. Warfield, K. L., Posten, N. A., Swenson, D. L., Olinger, G. G., Esposito, D., Gillette, W. K., et al. (2007a). Filovirus-like particles produced in insect cells:immunogenicity and protection in rodents. J. Infect. Dis. 196(Suppl. 2), S421-429.
145. Warfield, K. L., Swenson, D. L., Olinger, G. G., Kalina, W. V., Aman, M. J., and Bavari, S. (2007b). Ebola virus-like particle-based vaccine protects nonhuman primates against lethal Ebola virus challenge. J. Infect. Dis. 196(Suppl. 2), S430-S437.
146. Warfield, K. L., Swenson, D. L., Olinger, G. G., Nichols, D. K., Pratt, W. D., Blouch, R., et al. (2006). Gene-specific countermeasures against Ebola virus based on antisense phosphorodiamidate morpholino oligomers. PLoS Pathog. 2:e1. doi:10.1371/journal.ppat.0020001.
147. Warren, T. K., Warfield, K. L., Wells, J., Swenson, D. L., Donner, K. S., van Tongeren, S. A., et al. (2010). Advanced antisense therapies for postexposure protection against lethal filovirus infections. Nat. Med. 16, 991-994. doi:10.1038/nm.2202.
148. Xu, L., Sanchez, A., Yang, Z., Zaki, S. R., Nabel, E. G., Nichol, S. T., et al. (1998). Immunization for Ebola virus infection. Nat. Med. 4, 37-42. doi:10.1038/nm0198-037.
149. Zaki, S. R., and Goldsmith, C. S. (1999). Pathologic features of filovirus infections in humans. Curr. Top. Microbiol. Immunol. 235, 97-116. doi:10.1007/978-3-642-59949-1_7.
150. Zhang, A. P., Bornholdt, Z. A., Liu, T., Abelson, D. M., Lee, D. E., Li, S., et al. (2012). The ebola virus interferon antagonist VP24 directly binds STAT1 and has a novel, pyramidal fold. PLoS Pathog. 8:e1002550. doi:10.1371/journal.ppat.1002550.
151. Zivcec, M., Safronetz, D., Haddock, E., Feldmann, H., and Ebihara, H. (2011). Validation of assays to monitor immune responses in the Syrian golden hamster (Mesocricetus auratus). J. Immunol. Methods 368, 24-35. doi:10.1016/j.jim.2011.02.004.
152. Zlotnik, I. (1971). "Marburg disease" The pathology of experimentally infected hamsters," in Marburg Virus Disease, eds G. A. Martini and R. Siegert (New York, NY:Springer, Berlin Heidelberg), 129-135.