Delayed Time-to-Treatment of an Antisense Morpholino Oligomer Is Effective against Lethal Marburg Virus Infection in Cynomolgus Macaques

PLoS Neglected Tropical Diseases

Volumn 10, Issue 2, 2016, Pages

  Warren, Travis K ^a   Whitehouse, Chris A ^a   Wells, Jay ^a   Welch, Lisa ^a   Charleston, Jay S ^b   Heald, Alison ^b   Nichols, Donald K ^a   Mattix, Marc E ^a,c   Palacios, Gustavo ^a   Kugleman, Jeffrey R ^a   Iversen, Patrick L ^b   Bavari, Sina ^a  

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

^b AVI BIOPHARMA INC   (United States)

^c WIL RESEARCH LABORATORIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE AMINOTRANSFERASE; ALKALINE PHOSPHATASE; ASPARTATE AMINOTRANSFERASE; AVI 7288; EOTAXIN; GAMMA GLUTAMYLTRANSFERASE; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERLEUKIN 6; MACROPHAGE DERIVED CHEMOKINE; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MONOCYTE CHEMOTACTIC PROTEIN 1; MORPHOLINO OLIGONUCLEOTIDE; THYMUS AND ACTIVATION REGULATED CHEMOKINE; UNCLASSIFIED DRUG; VIRUS ANTIGEN; VIRUS RNA; AVI-7288; COMPLEMENTARY RNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BILIRUBIN BLOOD LEVEL; CONTROLLED STUDY; FEMALE; HISTOPATHOLOGY; IMMUNE RESPONSE; IMMUNOHISTOCHEMISTRY; LIMIT OF QUANTITATION; MACACA FASCICULARIS; MALE; MARBURG HEMORRHAGIC FEVER; NONHUMAN; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS; THERAPY DELAY; UREA NITROGEN BLOOD LEVEL; VIRAL PLAQUE ASSAY; VIRUS LOAD; ANIMAL; DISEASE MODEL; GENE THERAPY; GENETICS; HUMAN; MARBURG VIRUS DISEASE; MARBURGVIRUS; METABOLISM; PHYSIOLOGY; TIME TO TREATMENT; VIROLOGY;

ANIMALS; DISEASE MODELS, ANIMAL; FEMALE; GENETIC THERAPY; HUMANS; MACACA FASCICULARIS; MALE; MARBURG VIRUS DISEASE; MARBURGVIRUS; MORPHOLINOS; RNA, ANTISENSE; TIME-TO-TREATMENT;

EID: 84959293746     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0004456     Document Type: Article

References (32)

1. Brauburger K, Hume AJ, Muhlberger E, Olejnik J, (2012) Forty-five years of Marburg virus research. Viruses4: 1878–1927. doi: 10.3390/v410187823202446
2. Mehedi M, Groseth A, Feldmann H, Ebihara H, (2011) Clinical aspects of Marburg hemorrhagic fever. Future Virol6: 1091–1106. 22046196
3. van Paassen J, Bauer MP, Arbous MS, Visser LG, Schmidt-Chanasit J, et al. (2012) Acute liver failure, multiorgan failure, cerebral oedema, and activation of proangiogenic and antiangiogenic factors in a case of Marburg haemorrhagic fever. Lancet Infect Dis12: 635–642. doi: 10.1016/S1473-3099(12)70018-X22394985
4. Daddario-DiCaprio KM, Geisbert TW, Stroher U, Geisbert JB, Grolla A, et al. (2006) Postexposure protection against Marburg haemorrhagic fever with recombinant vesicular stomatitis virus vectors in non-human primates: an efficacy assessment. Lancet367: 1399–1404. 16650649
5. Geisbert TW, Daddario-DiCaprio KM, Geisbert JB, Young HA, Formenty P, et al. (2007) Marburg virus Angola infection of rhesus macaques: pathogenesis and treatment with recombinant nematode anticoagulant protein c2. J Infect Dis196Suppl 2: S372–381. 17940973
6. Ursic-Bedoya R, Mire CE, Robbins M, Geisbert JB, Judge A, et al. (2014) Protection against lethal marburg virus infection mediated by lipid encapsulated small interfering RNA. J Infect Dis209: 562–570. doi: 10.1093/infdis/jit46523990568
7. Thi EP, Mire CE, Ursic-Bedoya R, Geisbert JB, Lee AC, et al. (2014) Marburg virus infection in nonhuman primates: Therapeutic treatment by lipid-encapsulated siRNA. Sci Transl Med6: 250ra116. doi: 10.1126/scitranslmed.300970625143366
8. Dolnik O, Kolesnikova L, Welsch S, Strecker T, Schudt G, et al. (2014) Interaction with Tsg101 is necessary for the efficient transport and release of nucleocapsids in marburg virus-infected cells. PLoS Pathog10: e1004463. doi: 10.1371/journal.ppat.100446325330247
9. DiCarlo A, Biedenkopf N, Hartlieb B, Klussmeier A, Becker S, (2011) Phosphorylation of Marburg virus NP region II modulates viral RNA synthesis. J Infect Dis204Suppl 3: S927–933. doi: 10.1093/infdis/jir31921987771
10. Lebleu B, Moulton HM, Abes R, Ivanova GD, Abes S, et al. (2008) Cell penetrating peptide conjugates of steric block oligonucleotides. Adv Drug Deliv Rev60: 517–529. 18037527
11. Hudziak RM, Barofsky E, Barofsky DF, Weller DL, Huang SB, et al. (1996) Resistance of morpholino phosphorodiamidate oligomers to enzymatic degradation. Antisense Nucleic Acid Drug Dev6: 267–272. 9012862
12. Youngblood DS, Hatlevig SA, Hassinger JN, Iversen PL, Moulton HM, (2007) Stability of cell-penetrating peptide-morpholino oligomer conjugates in human serum and in cells. Bioconjug Chem18: 50–60. 17226957
13. Enterlein S, Warfield KL, Swenson DL, Stein DA, Smith JL, et al. (2006) VP35 knockdown inhibits Ebola virus amplification and protects against lethal infection in mice. Antimicrobial Agents and Chemotherapy50: 984–993. 16495261
14. Swenson DL, Warfield KL, Warren TK, Lovejoy C, Hassinger JN, et al. (2009) Chemical modifications of antisense morpholino oligomers enhance their efficacy against Ebola virus infection. Antimicrobial Agents and Chemotherapy53: 2089–2099. doi: 10.1128/AAC.00936-0819223614
15. Yuan J, Stein DA, Lim T, Qiu D, Coughlin S, et al. (2006) Inhibition of coxsackievirus B3 in cell cultures and in mice by peptide-conjugated morpholino oligomers targeting the internal ribosome entry site. Journal of Virology80: 11510–11519. 16987987
16. Gabriel G, Nordmann A, Stein DA, Iversen PL, Klenk HD, (2008) Morpholino oligomers targeting the PB1 and NP genes enhance the survival of mice infected with highly pathogenic influenza A H7N7 virus. Journal of General Virology89: 939–948. doi: 10.1099/vir.0.83449-018343835
17. Lupfer C, Stein DA, Mourich DV, Tepper SE, Iversen PL, et al. (2008) Inhibition of influenza A H3N8 virus infections in mice by morpholino oligomers. Arch Virol153: 929–937. doi: 10.1007/s00705-008-0067-018369525
18. Paessler S, Rijnbrand R, Stein DA, Ni H, Yun NE, et al. (2008) Inhibition of alphavirus infection in cell culture and in mice with antisense morpholino oligomers. Virology376: 357–370. doi: 10.1016/j.virol.2008.03.03218468653
19. Stein DA, Skilling DE, Iversen PL, Smith AW, (2001) Inhibition of Vesivirus infections in mammalian tissue culture with antisense morpholino oligomers. Antisense Nucleic Acid Drug Dev11: 317–325. 11763348
20. Kinney RM, Huang CY, Rose BC, Kroeker AD, Dreher TW, et al. (2005) Inhibition of dengue virus serotypes 1 to 4 in vero cell cultures with morpholino oligomers. Journal of Virology79: 5116–5128. 15795296
21. Neuman BW, Stein DA, Kroeker AD, Churchill MJ, Kim AM, et al. (2005) Inhibition, escape, and attenuated growth of severe acute respiratory syndrome coronavirus treated with antisense morpholino oligomers. Journal of Virology79: 9665–9676. 16014928
22. Warren TK, Warfield KL, Wells J, Swenson DL, Donner KS, et al. (2010) Advanced antisense therapies for postexposure protection against lethal filovirus infections. Nature Medicine16: 991–994. doi: 10.1038/nm.220220729866
23. Iversen PL, Warren TK, Wells JB, Garza NL, Mourich DV, et al. (2012) Discovery and early development of AVI-7537 and AVI-7288 for the treatment of Ebola virus and Marburg virus infections. Viruses4: 2806–2830. doi: 10.3390/v411280623202506
24. United States National Research Council (2011) Guide for the care and use of laboratory animals.
25. Warren TK, Trefry JC, Marko ST, Chance TB, Wells JB, et al. (2014) Euthanasia assessment in ebola virus infected nonhuman primates. Viruses6: 4666–4682. doi: 10.3390/v611466625421892
26. Smith DH, Johnson BK, Isaacson M, Swanapoel R, Johnson KM, et al. (1982) Marburg-virus disease in Kenya. Lancet1: 816–820. 6122054
27. Warren TK, Shurtleff AC, Bavari S, (2012) Advanced morpholino oligomers: a novel approach to antiviral therapy. Antiviral Res94: 80–88. doi: 10.1016/j.antiviral.2012.02.00422353544
28. Hensley LE, Alves DA, Geisbert JB, Fritz EA, Reed C, et al. (2011) Pathogenesis of Marburg hemorrhagic fever in cynomolgus macaques. J Infect Dis204Suppl 3: S1021–1031. doi: 10.1093/infdis/jir33921987738
29. Kuhn JH, (2008) Filoviruses—A Compendium of 40 Years of Epidemiological, Clinical, and Laboratory Studies. New York and Vienna: SpringerWien.
30. Martini GA, Schmidt HA, (1968) [Spermatogenic transmission of the "Marburg virus". (Causes of "Marburg simian disease")]. Klin Wochenschr46: 398–400. 4971902
31. Rogstad KE, Tunbridge A, (2015) Ebola virus as a sexually transmitted infection. Curr Opin Infect Dis28: 83–85. doi: 10.1097/QCO.000000000000013525501666
32. Heald AE, Charleston JS, Iversen PL, Warren TK, Saoud JB, et al. (2015) AVI-7288 for Marburg Virus in Nonhuman Primates and Humans. N Engl J Med373: 339–348. doi: 10.1056/NEJMoa141034526200980