Attenuated NYCBH vaccinia virus deleted for the E3L gene confers partial protection against lethal monkeypox virus disease in cynomolgus macaques

Vaccine

Volumn 29, Issue 52, 2011, Pages 9684-9690

  Denzler, Karen L ^a   Babas, Tahar ^b   Rippeon, Amy ^b   Huynh, Trung ^a   Fukushima, Nobuko ^a   Rhodes, Lowrey ^b   Silvera, Peter M ^b   Jacobs, Bertram L ^a  

^a ARIZONA STATE UNIVERSITY   (United States)

^b SOUTHERN RESEARCH INSTITUTE   (United States)

Author keywords

E3L; Monkeypox virus; Smallpox; Vaccinia virus

Indexed keywords

ALPHA2 INTERFERON; INTERFERON REGULATORY FACTOR 3; NEUTRALIZING ANTIBODY; PROTEIN KINASE R; STRESS ACTIVATED PROTEIN KINASE; SYNAPTOPHYSIN; VACCINIA VACCINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; E3L GENE; FEMALE; GENE DELETION; GENE INDUCTION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; MACACA; MONKEYPOX VIRUS; MORTALITY; NONHUMAN; POXVIRUS INFECTION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SCAR FORMATION; SIGNAL TRANSDUCTION; SINGLE DRUG DOSE; SKIN DEFECT; UNITED STATES; VACCINATION; VACCINIA VIRUS; VIRUS ATTENUATION; VIRUS GENE; VIRUS LOAD;

ANIMALS; FEMALE; GENE DELETION; MACACA FASCICULARIS; MALE; MONKEYPOX; MONKEYPOX VIRUS; NEW YORK CITY; PRIMATE DISEASES; RNA-BINDING PROTEINS; SKIN DISEASES; SMALLPOX VACCINE; SURVIVAL ANALYSIS; UNITED STATES; VACCINES, ATTENUATED; VACCINIA VIRUS; VIRAL PROTEINS; VIREMIA; VIRULENCE FACTORS;

EID: 82555187127     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2011.09.135     Document Type: Article

References (43)

1. Jacobs B.L., Langland J.O., Kibler K.V., Denzler K.L., White S.D., Holechek S.A., et al. Vaccinia virus vaccines: past, present and future. Antiviral Res 2009, 84(October (1)):1-13.
2. Rosenthal S.R., Merchlinsky M., Kleppinger C., Goldenthal K.L. Developing new smallpox vaccines. Emerg Infect Dis 2001, 7(November-December (6)):920-926.
3. Greenberg R.N., Kennedy J.S. ACAM2000: a newly licensed cell culture-based live vaccinia smallpox vaccine. Expert Opin Investig Drugs 2008, 17(April (4)):555-564.
4. Jentarra G.M., Heck M.C., Youn J.W., Kibler K., Langland J.O., Baskin C.R., et al. Vaccinia viruses with mutations in the E3L gene as potential replication-competent, attenuated vaccines: scarification vaccination. Vaccine 2008, 26(June (23)):2860-2872.
5. Chang H.W., Jacobs B.L. Identification of a conserved motif that is necessary for binding of the vaccinia virus E3L gene products to double-stranded RNA. Virology 1993, 194(June (2)):537-547.
6. Kim Y.G., Lowenhaupt K., Oh D.B., Kim K.K., Rich A. Evidence that vaccinia virulence factor E3L binds to Z-DNA in vivo: implications for development of a therapy for poxvirus infection. Proc Natl Acad Sci U S A 2004, 101(February (6)):1514-1518.
7. Langland J.O., Kash J.C., Carter V., Thomas M.J., Katze M.G., Jacobs B.L. Suppression of proinflammatory signal transduction and gene expression by the dual nucleic acid binding domains of the vaccinia virus E3L proteins. J Virol 2006, 80(October (20)):10083-10095.
8. Langland J.O., Jacobs B.L. Inhibition of PKR by vaccinia virus: role of the N- and C-terminal domains of E3L. Virology 2004, 324(July (2)):419-429.
9. Perdiguero B., Esteban M. The interferon system and vaccinia virus evasion mechanisms. J Interferon Cytokine Res 2009, 29(September (9)):581-598.
10. Xiang Y., Condit R.C., Vijaysri S., Jacobs B., Williams B.R., Silverman R.H. Blockade of interferon induction and action by the E3L double-stranded RNA binding proteins of vaccinia virus. J Virol 2002, 76(May (10)):251-259.
11. Valentine R., Smith G.L. Inhibition of the RNA polymerase III-mediated dsDNA-sensing pathway of innate immunity by vaccinia virus protein E3. J Gen Virol 2010, 91(September (Pt 9)):2221-2229.
12. Marq J.B., Hausmann S., Luban J., Kolakofsky D., Garcin D. The double-stranded RNA binding domain of the vaccinia virus E3L protein inhibits both RNA- and DNA-induced activation of interferon beta. J Biol Chem 2009, 284(September (38)):25471-25478.
13. Kim Y.G., Muralinath M., Brandt T., Pearcy M., Hauns K., Lowenhaupt K., et al. A role for Z-DNA binding in vaccinia virus pathogenesis. Proc Natl Acad Sci U S A 2003, 100(June (12)):6974-6979.
14. Brandt T.A., Jacobs B.L. Both carboxy- and amino-terminal domains of the vaccinia virus interferon resistance gene, E3L, are required for pathogenesis in a mouse model. J Virol 2001, 75(January (2)):850-856.
15. Snoy P.J. Establishing efficacy of human products using animals: the US food and drug administration's animal rule. Vet Pathol 2010, 47(September (5)):774-778.
16. Denzler KL, Rice AD, MacNeill AL, Fukushima N, Lindsey SF, Wallace G, et al. The NYCBH vaccinia virus deleted for the innate immune evasion gene, E3L, protects rabbits against lethal challenge by rabbitpox virus. doi:10.1016/j.vaccine.2011.07.140.
17. Denzler K.L., Schriewer J., Parker S., Werner C., Hartzler H., Hembrador E., et al. The attenuated NYCBH vaccinia virus deleted for the immune evasion gene, E3L, completely protects mice against heterologous challenge with ectromelia virus. Vaccine 2011, 10.1016/j.vaccine.2011.09.108.
18. Fenner F., Henderson D.A., Arita I., Jezek Z., Ladnyi I.D. Smallpox and its eradication 1988, World Health Organization, Geneva, Switzerland. 1st ed.
19. Arita I., Jezek Z., Khodakevich L., Ruti K. Human monkeypox: a newly emerged orthopoxvirus zoonosis in the tropical rain forests of Africa. Am J Trop Med Hyg 1985, 34(July (4)):781-789.
20. Jezek Z., Grab B., Szczeniowski M., Paluku K.M., Mutombo M. Clinico-epidemiological features of monkeypox patients with an animal or human source of infection. Bull World Health Organ 1988, 66(4):459-464.
21. Jezek Z., Fenner F. Human monkeypox. Monographs in virology 1988, Karger, Basel, p. 1-140.
22. Stephenson J. Monkeypox outbreak a reminder of emerging infections vulnerabilities. JAMA 2003, 290(July (1)):23-24.
23. Reed K.D., Melski J.W., Graham M.B., Regnery R.L., Sotir M.J., Wegner M.V., et al. The detection of monkeypox in humans in the Western Hemisphere. N Engl J Med 2004, 350(January (4)):342-350.
24. Kulesh D.A., Baker R.O., Loveless B.M., Norwood D., Zwiers S.H., Mucker E., et al. Smallpox and pan-orthopox virus detection by real-time 3'-minor groove binder TaqMan assays on the roche LightCycler and the Cepheid smart Cycler platforms. J Clin Microbiol 2004, 42(February (2)):601-609.
25. Li Z., Rubin S.A., Taffs R.E., Merchlinsky M., Ye Z., Carbone K.M. Mouse neurotoxicity test for vaccinia-based smallpox vaccines. Vaccine 2004, 22(March (11-12)):1486-1493.
26. Downie A.W., McCarthy K. The antibody response in man following infection with viruses of the pox group. III. Antibody response in smallpox. J Hyg (Lond) 1958, 56(December (4)):479-487.
27. Mack T.M., Noble J., Thomas D.B. A prospective study of serum antibody and protection against smallpox. Am J Trop Med Hyg 1972, 21(March (2)):214-218.
28. Chaudhri G., Panchanathan V., Bluethmann H., Karupiah G. Obligatory requirement for antibody in recovery from a primary poxvirus infection. J Virol 2006, 80(July (13)):6339-6344.
29. Gordon S.N., Cecchinato V., Andresen V., Heraud J.M., Hryniewicz A., Parks R.W., et al. Smallpox vaccine safety is dependent on T cells and not B cells. J Infect Dis 2011, 203(April (8)):1043-1053.
30. Guerra S., Lopez-Fernandez L.A., Pascual-Montano A., Najera J.L., Zaballos A., Esteban M. Host response to the attenuated poxvirus vector NYVAC: upregulation of apoptotic genes and NF-kappaB-responsive genes in infected HeLa cells. J Virol 2006, 80(January (2)):985-998.
31. Najera J.L., Gomez C.E., Domingo-Gil E., Gherardi M.M., Esteban M. Cellular and biochemical differences between two attenuated poxvirus vaccine candidates (MVA and NYVAC) and role of the C7L gene. J Virol 2006, 80(June (12)):6033-6047.
32. Ludwig H., Suezer Y., Waibler Z., Kalinke U., Schnierle B.S., Sutter G. Double-stranded RNA-binding protein E3 controls translation of viral intermediate RNA, marking an essential step in the life cycle of modified vaccinia virus Ankara. J Gen Virol 2006, 87(May (Pt 5)):1145-1155.
33. Sancho M.C., Schleich S., Griffiths G., Krijnse-Locker J. The block in assembly of modified vaccinia virus Ankara in HeLa cells reveals new insights into vaccinia virus morphogenesis. J Virol 2002, 76(August (16)):8318-8334.
34. Kibler K.V., Gomez C.E., Perdiguero B., Wong S., Huynh T., Holechek S., et al. Improved NYVAC-based vaccine vectors. PLoS One 2011, in press.
35. Delaloye J., Roger T., Steiner-Tardivel Q.G., Le Roy D., Knaup Reymond M., Akira S., et al. Innate immune sensing of modified vaccinia virus Ankara (MVA) is mediated by TLR2-TLR6, MDA-5 and the NALP3 inflammasome. PLoS Pathog 2009, 5(June (6)):e1000480.
36. Mooij P., Balla-Jhagjhoorsingh S.S., Beenhakker N., van Haaften P., Baak I., Nieuwenhuis I.G., et al. Comparison of human and rhesus macaque T-cell responses elicited by boosting with NYVAC encoding human immunodeficiency virus type 1 clade C immunogens. J Virol 2009, 83(June (11)):5881-5889.
37. Mooij P., Balla-Jhagjhoorsingh S.S., Koopman G., Beenhakker N., van Haaften P., Baak I., et al. Differential CD4+ versus CD8+ T-cell responses elicited by different poxvirus-based human immunodeficiency virus type 1 vaccine candidates provide comparable efficacies in primates. J Virol 2008, 82(March (6)):2975-2988.
38. Hel Z., Nacsa J., Tsai W.P., Thornton A., Giuliani L., Tartaglia J., et al. Equivalent immunogenicity of the highly attenuated poxvirus-based ALVAC-SIV and NYVAC-SIV vaccine candidates in SIVmac251-infected macaques. Virology 2002, 304(December (1)):125-134.
39. Earl P.L., Americo J.L., Wyatt L.S., Eller L.A., Whitbeck J.C., Cohen G.H., et al. Immunogenicity of a highly attenuated MVA smallpox vaccine and protection against monkeypox. Nature 2004, 428(March (6979)):182-185.
40. Nigam P., Earl P.L., Americo J.L., Sharma S., Wyatt L.S., Edghill-Spano Y., et al. DNA/MVA HIV-1/AIDS vaccine elicits long-lived vaccinia virus-specific immunity and confers protection against a lethal monkeypox challenge. Virology 2007, 366(September (1)):73-83.
41. Earl P.L., Americo J.L., Wyatt L.S., Espenshade O., Bassler J., Gong K., et al. Rapid protection in a monkeypox model by a single injection of a replication-deficient vaccinia virus. Proc Natl Acad Sci U S A 2008, 105(August (31)):10889-10894.
42. Stittelaar K.J., van Amerongen G., Kondova I., Kuiken T., van Lavieren R.F., Pistoor F.H., et al. Modified vaccinia virus Ankara protects macaques against respiratory challenge with monkeypox virus. J Virol 2005, 79(June (12)):7845-7851.
43. Osborne J.D., Da Silva M., Frace A.M., Sammons S.A., Olsen-Rasmussen M., Upton C., et al. Genomic differences of vaccinia virus clones from Dryvax smallpox vaccine: the Dryvax-like ACAM2000 and the mouse neurovirulent Clone-3. Vaccine 2007, 25(December (52)):8807-8832.