Codon-optimized filovirus DNA vaccines delivered by intramuscular electroporation protect cynomolgus macaques from lethal Ebola and Marburg virus challenges

Human Vaccines and Immunotherapeutics

Volumn 11, Issue 8, 2015, Pages 1991-2004

  Grant Klein, Rebecca J ^a   Altamura, Louis A ^a   Badger, Catherine V ^a   Bounds, Callie E ^a   Van Deusen, Nicole M ^a   Kwilas, Steven A ^a   Vu, Hong A ^b   Warfield, Kelly L ^b   Hooper, Jay W ^a   Hannaman, Drew ^c   Dupuy, Lesley C ^a   Schmaljohn, Connie S ^a  

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

^b Integrated BioTherapeutics Inc   (United States)

^c Ichor Medical Systems Inc   (United States)

Author keywords

Codon optimized; DNA vaccine; Ebola virus; Electroporation; Filovirus; Marburg virus

Indexed keywords

ASPARTATE AMINOTRANSFERASE; DNA VACCINE; GAMMA INTERFERON; IMMUNOGLOBULIN G; CODON; GLYCOPROTEIN; NEUTRALIZING ANTIBODY; VIRUS ANTIBODY;

ADULT; ANIMAL EXPERIMENT; ANTIBODY RESPONSE; ANTIBODY TITER; ARTICLE; BLOOD SAMPLING; CONTROLLED STUDY; EBOLAVIRUS; ELECTROPORATION; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME LINKED IMMUNOSPOT ASSAY; FEMALE; FILOVIRUS INFECTION; IMMUNE RESPONSE; LUCIFERASE ASSAY; MALE; MARBURGVIRUS; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; VACCINATION; VIREMIA; ANIMAL; BLOOD; CODON; DISEASE MODEL; FILOVIRIDAE; GENETICS; HEMORRHAGIC FEVER, EBOLA; IMMUNOLOGY; INTRAMUSCULAR DRUG ADMINISTRATION; MACACA FASCICULARIS; MARBURG VIRUS DISEASE; MONONUCLEAR CELL; PLASMID; PRECLINICAL STUDY; RANDOMIZED CONTROLLED TRIAL; SECRETION (PROCESS); SERODIAGNOSIS; SURVIVAL ANALYSIS; TREATMENT OUTCOME;

ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; CODON; DISEASE MODELS, ANIMAL; DRUG EVALUATION, PRECLINICAL; ELECTROPORATION; ENZYME-LINKED IMMUNOSORBENT ASSAY; ENZYME-LINKED IMMUNOSPOT ASSAY; FEMALE; FILOVIRIDAE; GLYCOPROTEINS; HEMORRHAGIC FEVER, EBOLA; IMMUNOGLOBULIN G; INJECTIONS, INTRAMUSCULAR; INTERFERON-GAMMA; LEUKOCYTES, MONONUCLEAR; MACACA FASCICULARIS; MALE; MARBURG VIRUS DISEASE; NEUTRALIZATION TESTS; PLASMIDS; SURVIVAL ANALYSIS; TREATMENT OUTCOME; VACCINES, DNA;

EID: 84944458438     PISSN: 21645515     EISSN: 2164554X     Source Type: Journal    
DOI: 10.1080/21645515.2015.1039757     Document Type: Article

References (49)

1. Kuhn JH, Becker S, Ebihara H, Geisbert TW, Johnson KM, Kawaoka Y, Lipkin WI, Negredo AI, Netesov SV, Nichol ST, et al. Proposal for a revised taxonomy of the family Filoviridae: classification, names of taxa and viruses, and virus abbreviations. Arch Virol 2010; 155:2083-103; PMID:21046175; http://dx. doi. org/ 10. 1007/s00705-010-0814-x
2. Kuhn JH. Filoviruses. A compendium of 40 years of epidemiological, clinical, and laboratory studies. Arch Virol Suppl 2008; 20:13-360; PMID:18637412; http://dx. doi. org/10. 1007/978-3-211-69495-4_1
3. Towner JS, Amman BR, Sealy TK, Carroll SA, Comer JA, Kemp A, Swanepoel R, Paddock CD, Balinandi S, Khristova ML, et al. Isolation of genetically diverse Marburg viruses from Egyptian fruit bats. PLoS Path 2009; 5:e1000536; PMID:19649327; http://dx. doi. org/10. 1371/journal. ppat. 1000536
4. Leroy EM, Kumulungui B, Pourrut X, Rouquet P, Hassanin A, Yaba P, Délicat A, Paweska JT, Gonzalez JP, Swanepoel R. Fruit bats as reservoirs of Ebola virus. Nature 2005; 438:575-6; PMID:16319873; http://dx. doi. org/10. 1038/438575a
5. Feldmann H, Klenk HD, Sanchez A. Molecular biology and evolution of filoviruses. Arch Virol Suppl 1993; 7:81-100; PMID:8219816; http://dx. doi. org/ 10. 1007/978-3-7091-9300-6_8
6. Sanchez A, Kiley MP, Holloway BP, Auperin DD. Sequence analysis of the Ebola virus genome: organization, genetic elements, and comparison with the genome of Marburg virus. Virus Res 1993; 29:215-40; PMID:8237108; http://dx. doi. org/10. 1016/0168- 1702(93)90063-S
7. Sanchez A, Trappier SG, Mahy BW, Peters CJ, Nichol ST. The virion glycoproteins of Ebola viruses are encoded in two reading frames and are expressed through transcriptional editing. Proc Natl Acad Sci U S A 1996; 93:3602-7; PMID:8622982; http://dx. doi. org/10. 1073/pnas. 93. 8. 3602
8. Volchkov VE, Becker S, Volchkova VA, Ternovoj VA, Kotov AN, Netesov SV, Klenk HD. GP mRNA of Ebola virus is edited by the Ebola virus polymerase and by T7 and vaccinia virus polymerases. Virology 1995; 214:421-30; PMID:8553543; http://dx. doi. org/ 10. 1006/viro. 1995. 0052
9. Volchkov VE, Feldmann H, Volchkova VA, Klenk HD. Processing of the Ebola virus glycoprotein by the proprotein convertase furin. Proc Natl Acad Sci U S A 1998; 95:5762-7; PMID:9576958; http://dx. doi. org/ 10. 1073/pnas. 95. 10. 5762
10. Jones SM, Stroher U, Fernando L, Qiu X, Alimonti J, Melito P, Bray M, Klenk HD, Feldmann H. Assessment of a vesicular stomatitis virus-based vaccine by use of the mouse model of Ebola virus hemorrhagic fever. J Infect Dis 2007; 196 Suppl 2:S404-12; PMID:17940977; http://dx. doi. org/10. 1086/520591
11. Bukreyev A, Yang L, Zaki SR, Shieh WJ, Rollin PE, Murphy BR, Collins PL, Sanchez A. A single intranasal inoculation with a paramyxovirus-vectored vaccine protects guinea pigs against a lethaldose Ebola virus challenge. J Virol 2006; 80:2267- 79; PMID:16474134; http://dx. doi. org/10. 1128/ JVI. 80. 5. 2267-2279. 2006
12. Swenson DL, Wang D, Luo M, Warfield KL, Woraratanadharm J, Holman DH, Dong JY, Pratt WD. Vaccine to confer to nonhuman primates complete protection against multistrain Ebola and Marburg virus infections. Clin Vaccine Immunol 2008; 15:460-7; PMID:18216185; http://dx. doi. org/ 10. 1128/CVI. 00431-07
13. Sullivan NJ, Sanchez A, Rollin PE, Yang ZY, Nabel GJ. Development of a preventive vaccine for Ebola virus infection in primates. Nature 2000; 408: 605-9; PMID:11117750; http://dx. doi. org/10. 1038/ 35046108
14. Sullivan NJ, Geisbert TW, Geisbert JB, Xu L, Yang ZY, Roederer M, Koup RA, Jahrling PB, Nabel GJ. Accelerated vaccination for Ebola virus haemorrhagic fever in non-human primates. Nature 2003; 424:681-4; PMID:12904795; http://dx. doi. org/ 10. 1038/nature01876
15. 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; PMID:9813200; http://dx. doi. org/10. 1006/viro. 1998. 9367
16. Warfield KL, Posten NA, Swenson DL, Olinger GG, Esposito D, Gillette WK, Hopkins RF, Costantino J, Panchal RG, Hartley JL, et al. Filovirus-like particles produced in insect cells: immunogenicity and protection in rodents. J Infect Dis 2007; 196 Suppl 2:S421-9; http://dx. doi. org/10. 1086/520612
17. Parren PW, Geisbert TW, Maruyama T, Jahrling PB, Burton DR. Pre- and postexposure prophylaxis of Ebola virus infection in an animal model by passive transfer of a neutralizing human antibody. J Virol 2002; 76:6408-12; PMID:12021376; http://dx. doi. org/10. 1128/JVI. 76. 12. 6408-6412. 2002
18. Dye JM, Herbert AS, Kuehne AI, Barth JF, Muhammad MA, Zak SE, Ortiz RA, Prugar LI, Pratt WD. Postexposure antibody prophylaxis protects nonhuman primates from filovirus disease. Proc Natl Acad Sci U S A 2012; 109:5034-9; PMID:22411795; http://dx. doi. org/10. 1073/pnas. 1200409109
19. Qiu X, Audet J, Wong G, Pillet S, Bello A, Cabral T, Strong JE, Plummer F, Corbett CR, Alimonti JB, et al. Successful treatment of ebola virusinfected cynomolgus macaques with monoclonal antibodies. Sci Transl Med 2012; 4:138ra81; PMID:22700957; http://dx. doi. org/10. 1126/ scitranslmed. 3003876
20. Marzi A, Engelmann F, Feldmann F, Haberthur K, Shupert WL, Brining D, Scott DP, Geisbert TW, Kawaoka Y, Katze MG, et al. Antibodies are necessary for rVSV/ZEBOV-GP-mediated protection against lethal Ebola virus challenge in nonhuman primates. Proc Natl Acad Sci U S A 2013; 110:1893-8; PMID:23319647; http://dx. doi. org/ 10. 1073/pnas. 1209591110
21. Sullivan NJ, Hensley L, Asiedu C, Geisbert TW, Stanley D, Johnson J, Honko A, Olinger G, Bailey M, Geisbert JB, et al. CD8+ cellular immunity mediates rAd5 vaccine protection against Ebola virus infection of nonhuman primates. Nat Med 2011; 17:1128-31; PMID:21857654; http://dx. doi. org/10. 1038/nm. 2447
22. Riemenschneider J, Garrison A, Geisbert J, Jahrling P, Hevey M, Negley D, Schmaljohn A, Lee J, Hart MK, Vanderzanden L, et al. Comparison of individual and combination DNA vaccines for B. anthracis, Ebola virus, Marburg virus and Venezuelan equine encephalitis virus. Vaccine 2003; 21:4071-80; PMID:12922144; http://dx. doi. org/10. 1016/S0264-410X(03)00362-1
23. Mellquist-Riemenschneider JL, Garrison AR, Geisbert JB, Saikh KU, Heidebrink KD, Jahrling PB, et al. Comparison of the protective efficacy of DNA and baculovirus-derived protein vaccines for EBOLA virus in guinea pigs. Virus Res 2003; 92:187-93; PMID:12686428; http://dx. doi. org/10. 1016/S0168- 1702(02)00338-6
24. Grant-Klein RJ, Van Deusen NM, Badger CV, Hannaman D, Dupuy LC, Schmaljohn CS. A multiagent filovirus DNA vaccine delivered by intramuscular electroporation completely protects mice from ebola and Marburg virus challenge. Hum Vacc Immunother 2012; 8:1703-6; PMID:22922764; http://dx. doi. org/ 10. 4161/hv. 21873
25. Nakayama E, Saijo M. Animal models for Ebola and Marburg virus infections. Front Microbiol 2013; 4:267; PMID:24046765; http://dx. doi. org/10. 3389/ fmicb. 2013. 00267
26. Hevey M, Negley D, VanderZanden L, Tammariello RF, Geisbert J, Schmaljohn C, Smith JF, Jahrling PB, Schmaljohn AL. Marburg virus vaccines: comparing classical and new approaches. Vaccine 2001; 20:586- 93; PMID:11672925; http://dx. doi. org/10. 1016/ S0264-410X(01)00353-X
27. Schmaljohn CS, Spik KW, Hooper JW. DNA vaccines for HFRS: laboratory and clinical studies. Virus Res 2014; 187:91-6; PMID:24370868; http://dx. doi. org/ 10. 1016/j. virusres. 2013. 12. 020
28. Dupuy LC, Richards MJ, Ellefsen B, Chau L, Luxembourg A, Hannaman D, Livingston BD, Schmaljohn CS. A DNA vaccine for venezuelan equine encephalitis virus delivered by intramuscular electroporation elicits high levels of neutralizing antibodies in multiple animal models and provides protective immunity to mice and nonhuman primates. Clin Vaccine Immunol 2011; 18:707-16; PMID:21450977; http://dx. doi. org/ 10. 1128/CVI. 00030-11
29. Spik KW, Badger C, Mathiessen I, Tjelle T, Hooper JW, Schmaljohn C. Mixing of M segment DNA vaccines to Hantaan virus and Puumala virus reduces their immunogenicity in hamsters. Vaccine 2008; 26:5177-81; PMID:18482782; http://dx. doi. org/10. 1016/j. vaccine. 2008. 03. 097
30. Hooper JW, Moon JE, Paolino KM, Newcomer R, McLain DE, Josleyn M, Hannaman D, Schmaljohn C. A Phase 1 clinical trial of Hantaan virus and Puumala virus M-segment DNA vaccines for haemorrhagic fever with renal syndrome delivered by intramuscular electroporation. Clin Microbiol Infect 2014; 20 Suppl 5:110- 7; PMID:24447183; http://dx. doi. org/10. 1111/1469- 0691. 12553
31. Boudreau EF, Josleyn M, Ullman D, Fisher D, Dalrymple L, Sellers-Myers K, Loudon P, Rusnak J, Rivard R, Schmaljohn C, et al. A Phase 1 clinical trial of Hantaan virus and Puumala virus M-segment DNA vaccines for hemorrhagic fever with renal syndrome. Vaccine 2012; 30:1951-8; PMID:22248821; http://dx. doi. org/10. 1016/j. vaccine. 2012. 01. 024
32. Hooper JW, Josleyn M, Ballantyne J, Brocato R. A novel Sin Nombre virus DNA vaccine and its inclusion in a candidate pan-hantavirus vaccine against hantavirus pulmonary syndrome (HPS) and hemorrhagic fever with renal syndrome (HFRS). Vaccine 2013; 31:4314- 21; PMID:23892100; http://dx. doi. org/10. 1016/j. vaccine. 2013. 07. 025
33. Brocato RL, Josleyn MJ, Wahl-Jensen V, Schmaljohn CS, Hooper JW. Construction and nonclinical testing of a Puumala virus synthetic M gene-based DNA vaccine. Clin Vaccine Immunol 2013; 20:218-26; PMID:23239797; http://dx. doi. org/ 10. 1128/CVI. 00546-12
34. Kwilas S, Kishimori JM, Josleyn M, Jerke K, Ballantyne J, Royals M, Hooper JW. A Hantavirus Pulmonary Syndrome (HPS) DNA Vaccine Delivered Using a Spring-powered Jet Injector Elicits a Potent Neutralizing Antibody Response in Rabbits and Nonhuman Primates. Curr Gene Ther 2014; 14:200-10; PMID:24867065; http://dx. doi. org/ 10. 2174/1566523214666140522122633
35. Dupuy LC, Richards MJ, Reed DS, Schmaljohn CS. Immunogenicity and protective efficacy of a DNA vaccine against Venezuelan equine encephalitis virus aerosol challenge in nonhuman primates. Vaccine 2010; 28:7345-50; PMID:20851089; http://dx. doi. org/ 10. 1016/j. vaccine. 2010. 09. 005
36. Hood CL, Abraham J, Boyington JC, Leung K, Kwong PD, Nabel GJ. Biochemical and structural characterization of cathepsin L-processed Ebola virus glycoprotein: implications for viral entry and immunogenicity. J Virol 2010; 84:2972-82; PMID:20053739; http://dx. doi. org/10. 1128/JVI. 02151-09
37. Shedlock DJ, Bailey MA, Popernack PM, Cunningham JM, Burton DR, Sullivan NJ. Antibody-mediated neutralization of Ebola virus can occur by two distinct mechanisms. Virology 2010; 401:228-35; PMID:20304456; http://dx. doi. org/10. 1016/j. virol. 2010. 02. 029
38. Wilson JA, Hevey M, Bakken R, Guest S, Bray M, Schmaljohn AL, Hart MK. Epitopes involved in antibody- mediated protection from Ebola virus. Science 2000; 287:1664-6; PMID:10698744; http://dx. doi. org/10. 1126/science. 287. 5458. 1664
39. Baize S, Pannetier D, Oestereich L, Rieger T, Koivogui L, Magassouba N, Soropogui B, Sow MS, Keïta S, De Clerck H, et al. Emergence of Zaire Ebola Virus Disease in Guinea - Preliminary Report. N Engl J Med 2014; 371(15):1418-25; PMID:24738640
40. Mohan GS, Li W, Ye L, Compans RW, Yang C. Antigenic subversion: a novel mechanism of host immune evasion by Ebola virus. PLoS Path 2012; 8:e1003065; PMID:23271969; http://dx. doi. org/10. 1371/journal. ppat. 1003065
41. Oswald WB, Geisbert TW, Davis KJ, Geisbert JB, Sullivan NJ, Jahrling PB, Parren PW, Burton DR. Neutralizing antibody fails to impact the course of Ebola virus infection in monkeys. PLoS Path 2007; 3:e9; PMID:17238286; http://dx. doi. org/10. 1371/journal. ppat. 0030009
42. Marzi A, Yoshida R, Miyamoto H, Ishijima M, Suzuki Y, Higuchi M, Matsuyama Y, Igarashi M, Nakayama E, Kuroda M, et al. Protective efficacy of neutralizing monoclonal antibodies in a nonhuman primate model of Ebola hemorrhagic fever. PloS One 2012; 7:e36192; PMID:22558378; http://dx. doi. org/10. 1371/journal. pone. 0036192
43. Olinger GG, Jr., Pettitt J, Kim D, Working C, Bohorov O, Bratcher B, Hiatt E, Hume SD, Johnson AK, Morton J, et al. Delayed treatment of Ebola virus infection with plant-derived monoclonal antibodies provides protection in rhesus macaques. Pro Nat Acad Sci U S A 2012; 109:18030-5; PMID:23071322; http://dx. doi. org/10. 1073/pnas. 1213709109
44. Emond RT, Evans B, Bowen ET, Lloyd G. A case of Ebola virus infection. Br Med J 1977; 2:541-4; PMID:890413; http://dx. doi. org/10. 1136/bmj. 2. 6086. 541
45. Mupapa K, Massamba M, Kibadi K, Kuvula K, Bwaka A, Kipasa M, Colebunders R, Muyembe-Tamfum JJ. Treatment of Ebola hemorrhagic fever with blood transfusions from convalescent patients. International Scientific and Technical Committee. J Infect Dis 1999; 179 Suppl 1:S18-23; PMID:9988160; http://dx. doi. org/10. 1086/514298
46. Qiu X, Wong G, Audet J, Bello A, Fernando L, Alimonti JB, Fausther-Bovendo H, Wei H, Aviles J, Hiatt E, et al. Reversion of advanced Ebola virus disease in nonhuman primates with ZMapp. Nature 2014; 514 (7520):47-53; PMID:25171469
47. Daddario-DiCaprio KM, Geisbert TW, Geisbert JB, Stroher U, Hensley LE, Grolla A, Fritz EA, Feldmann F, Feldmann H, Jones SM. Cross-protection against Marburg virus strains by using a live, attenuated recombinant vaccine. J Virol 2006; 80:9659-66; PMID:16973570; http://dx. doi. org/ 10. 1128/JVI. 00959-06
48. Lee JE, Fusco ML, Hessell AJ, Oswald WB, Burton DR, Saphire EO. Structure of the Ebola virus glycoprotein bound to an antibody from a human survivor. Nature 2008; 454:177-82; PMID:18615077; http:// dx. doi. org/10. 1038/nature07082
49. Ogino M, Ebihara H, Lee BH, Araki K, Lundkvist A, Kawaoka Y, Yoshimatsu K, Arikawa J. Use of vesicular stomatitis virus pseudotypes bearing hantaan or seoul virus envelope proteins in a rapid and safe neutralization test. Clin Diag Lab Immunol 2003; 10:154-60; PMID:12522053