Pathogenesis of Ebola Hemorrhagic Fever in Primate Models: Evidence that Hemorrhage Is Not a Direct Effect of Virus-Induced Cytolysis of Endothelial Cells

American Journal of Pathology

Volumn 163, Issue 6, 2003, Pages 2371-2382

  Geisbert, Thomas W ^a,d   Young, Howard A ^b   Jahrling, Peter B ^a   Davis, Kelly J ^a   Larsen, Tom ^a   Kagan, Elliott ^c   Hensley, Lisa E ^a  

^a US Army Medical Institute for Infectious Diseases   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

^c UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

ALBUMIN;

ALBUMIN BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLEEDING; CELL ACTIVATION; CONTROLLED STUDY; CYTOLYSIS; ENDOTHELIUM CELL; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; MALE; MONKEY; NONHUMAN; PATHOGENESIS; PRIMATE; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; UMBILICAL VEIN; VASCULAR ENDOTHELIUM; VIRUS HEMORRHAGIC FEVER; VIRUS REPLICATION;

EID: 0345445900     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0002-9440(10)63592-4     Document Type: Article

References (38)

1. Huggins-JW: Prospects for treatment of viral hemorrhagic fevers with ribavirin, a broad-spectrum antiviral drug. Rev Infect Dis Suppl 1989, 4:S750-S761
2. Jahrling PB, Geisbert J, Swearengen JR, Jaax GP, Lewis T, Huggins JW, Schmidt JJ, LeDuc JW, Peters CJ: Passive immunization of Ebola virus-infected cynomolgus monkeys with immunoglobulin from hyperimmune horses. Arch Virol Suppl 1996, 11:135-140
3. Jahrling PB, Geisbert TW, Geisbert JB, Swearengen JR, Bray M, Jaax NK, Huggins JW, LeDuc JW, Peters CJ: Evaluation of immune globulin and recombinant interferon-α2b for treatment of experimental Ebola virus infections. J Infect Dis Suppl 1999, 179:S224-S234
4. Yang Z, Delgado R, Xu L, Todd RF, Nabel EG, Sanchez A, Nabel GJ: Distinct cellular interactions of secreted and transmembrane Ebola virus glycoproteins. Science 1998, 279:1034-1037
5. Yang Z, Duckers HJ, Sullivan NJ, Sanchez A, Nabel EG, Nabel GJ: Identification of the Ebola virus glycoprotein as the main viral determinant of vascular cell cytotoxicity and injury. Nat Med 2000, 6:886-889
6. Moncada S, Palmer RMJ, Higgs EA: Relationship between prostacyclin and nitric oxide in the thrombotic process. Thromb Res Suppl 1990, XI:3-13
7. Mantovani A, Bussolino F, Dejana E: Cytokine regulation of endothelial cell function. EMBO J 1992, 6:2591-2599
8. Harcourt BH, Sanchez A, Offermann MK: Ebola virus inhibits induction of genes by double-stranded RNA in endothelial cells. Virology 1998, 252:179-188
9. Dietrich M, Schumacher HH, Peters D, Knobloch J: Human pathology of Ebola (Maridi) virus infection in the Sudan. Ebola Virus Haemorrhagic Fever. Edited by SR Pattyn. New York, Elsevier/North-Holland Biomedical Press, 1978, pp 37-42
10. Murphy FA: Pathology of Ebola virus infection. Ebola Virus Haemorrhagic Fever. Edited by SR Pattyn. New York, Elsevier/North-Holland Biomedical Press, 1978, pp 43-60
11. Zaki SR, Goldsmith CS: Pathologic features of filovirus infections in humans. Curr Top Microbiol Immunol 1999, 235:97-116
12. Baskerville A, Fisher-Hoch SP, Neild GH, Dowsett AB: Ultrastructural pathology of experimental Ebola haemorrhagic fever virus infection. J Pathol 1985, 147:199-209
13. Geisbert TW, Jahrling PB, Hanes MA, Zack PM: Association of Ebola related Reston virus particles and antigen with tissue lesions of monkeys imported to the United States. J Comp Pathol 1992, 106:137-152
14. Jaax NK, Davis KJ, Geisbert TW, Vogel P, Jaax GP, Topper M, Jahrling PB: Lethal experimental infection of rhesus monkeys with Ebola-Zaire (Mayinga) virus by the oral and conjunctival route of exposure. Arch Pathol Lab Med 1996, 120:140-155
15. Davis KJ, Anderson AO, Geisbert TW, Steele KE, Geisbert JB, Vogel P, Connolly BM, Huggins JW, Jahrling PB, Jaax NK: Pathology of experimental Ebola virus infection in African green monkeys. Arch Pathol Lab Med 1997, 121:805-819
16. Ryabchikova EI, Kolesnikova LV, Netesov SV: Animal pathology of filoviral infections. Curr Top Microbiol Immunol 1999, 235:145-173
17. Geisbert TW, Hensley LE, Larsen T, Young HA, Reed DS, Geisbert JB, Scott DP, Kagan E, Jahrling PB, Davis KJ: 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
18. Prophet EB, Mills B, Arrington JB, Sobin LH (Eds): Laboratory Methods in Histotechnology. Washington DC, Armed Forces Institute of Pathology, 1992, pp 25-59
19. Jahrling PB: Filoviruses and arenaviruses. Manual of Clinical Microbiology. Edited by PR Murray, EJ Baron, M Pfaller, FC Tenover, RH Yolken. Washington DC, ASM Press, 1999, pp 1125-1136
20. Geisbert TW, Jahrling PB: Differentiation of filoviruses by electron microscopy. Virus Res 1995, 39:129-150
21. Baize S, Leroy EM, Georges-Courbot M-C, Capron M, Lansoud-Soukate J, Debre P, Fisher-Hoch SP, McCormick JB, Georges AJ: Defective humoral responses and extensive intravascular apoptosis are associated with fatal outcome in Ebola virus-infected patients. Nat Med 1999, 5:423-426
22. Villinger F, Rollin PE, Brar SS, Chikkala NF, Winter J, Sundstrom JB, Zaki SR, Swanepoel R, Ansari AA, Peters CJ: Markedly elevated levels of interferon (IFN)-α, IFN-γ, interleukin (IL)-2, IL-10, and tumor necrosis factor-α associated with fatal Ebola virus infection. J Infect Dis 1999, 179(Suppl 1):S188-S191
23. Hensley LE, Young HA, Jahrling PB, Geisbert TW: Proinflammatory response during Ebola virus infection of primate models: possible involvement of the tumor necrosis factor receptor superfamily. Immunol Lett 2002, 80:169-179
24. Dvorak HF, Brown LF, Detmar M, Dvorak AM: Vascular permeability factor/vascular endothelial growth factor, microvascular hyperpermeability, and angiogenesis. Am J Pathol 1995, 146:1029-1039
25. Kevil CG, Payne DK, Mire E, Alexander JS: Vascular permeability factor/vascular endothelial cell growth factor-mediated permeability occurs through disorganization of endothelial junctional proteins. J Biol Chem 1998, 273:15099-15103
26. Walker DH: Pathology and pathogenesis of the vasculotropic rickettsioses. Biology of Rickettsial Diseases. Edited by DH Walker. Boca Raton, CRC Press, 1988, pp 115-138
27. Eremeeva ME, Silverman DJ: Rickettsia rickettsii infection of the EA. hy 926 endothelial cell line: morphological response to infection and evidence for oxidative injury. Microbiology 1998, 144:2037-2048
28. Wong KT, Shieh WJ, Kumar S, Norain K, Abdullah W, Guarner J, Goldsmith CS, Chua KB, Lam SK, Tan CT, Goh KJ, Chong HT, Jusoh R, Rollin PE, Ksiazek TG, Zaki SR: Nipah virus infection: pathology and pathogenesis of an emerging paramyxoviral zoonosis. Am J Pathol 2002, 161:2153-2167
29. Worrall NK, Chang K, LeJeune WS, Misko TP, Sullivan PM, Ferguson Jr TB, Williamson JR: TNF-alpha causes reversible in vivo systemic vascular barrier dysfunction via NO-dependent and -independent mechanisms. Am J Physiol 1997, 273:H2565-H2574
30. Feldmann H, Bugany H, Mahner F, Klenk HD, Drenckhahn D, Schnittler H-J: Filovirus-induced endothelial leakage triggered by infected monocytes/macrophages. J Virol 1996, 70:2208-2214
31. Grimley PM, Kang YH, Silverman RH, Davis G, Hoofnagle JH: Blood lymphocyte inclusions associated with alpha interferon. Lab Invest 1983, 48:30A-31A
32. Teruyama K, Abe M, Nakano T, Iwasaka-Yagi C, Takahashi S, Yamada S, Sato Y: Role of transcription factor Ets-1 in the apoptosis of human vascular endothelial cells. J Cell Physiol 2001, 188:243-252
33. Cao Y, Prescott SM: Many actions of cyclooxygenase-2 in cellular dynamics and in cancer. J Cell Physiol 2002, 190:279-286
34. Avirutnan P, Malasit P, Seliger B, Bhakdi S, Husmann M: Dengue virus infection of human endothelial cells leads to chemokine production, complement activation, and apoptosis. J Immunol 1998, 161: 6338-6346
35. Vallee I, Tait SW, Powell PP: African swine fever virus infection of porcine aortic endothelial cells leads to inhibition of inflammatory responses, activation of the thrombotic state, and apoptosis. J Virol 2001, 75:10372-10382
36. Lukashevich IS, Maryankova R, Vladyko AS, Nashkevich N, Koleda S, Djavani M, Horejsh D, Voitenok NN, Salvato MS: Lassa and Mopeia virus replication in human monocytes/macrophages and in endothelial cells: different effects on IL-8 and TNF-alpha gene expression. J Med Virol 1999, 59:552-560
37. 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
38. Simmons G, Reeves JD, Grogan CC, Vandenberghe LH, Baribaud F, Whitbeck JC, Burke E, Buchmeier MJ, Soilleux EJ, Riley JL, Doms RW, Bates P, Pohlmann S: DC-SIGN and DC-SIGNR bind Ebola glycoproteins and enhance infection of macrophages and endothelial cells. Virology 2003, 305:115-123