Modified vaccinia virus ankara encoding influenza virus hemagglutinin induces heterosubtypic immunity in macaques

Journal of Virology

Volumn 88, Issue 22, 2014, Pages 13418-13428

  Florek, Nicholas W ^a,b   Weinfurter, Jason T ^a,b   Jegaskanda, Sinthujan ^c   Brewoo, Joseph N ^d   Powell, Tim D ^d   Young, Ginger R ^d   Das, Subash C ^d   Hatta, Masato ^a   Broman, Karl W ^e   Hungnes, Olav ^f   Dudman, Susanne G ^f   Kawaoka, Yoshihiro ^a   Kent, Stephen J ^c   Stinchcomb, Dan T ^d   Osorio, Jorge E ^a,d   Friedrich, Thomas C ^a,b  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF WISCONSIN   (United States)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d Takeda Vaccines Inc   (United States)

^e UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^f NORWEGIAN INSTITUTE OF PUBLIC HEALTH   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

INFLUENZA VIRUS HEMAGGLUTININ; MODIFIED VACCINIA VIRUS ANKARA VACCINE; UNCLASSIFIED DRUG; VIRUS ANTIBODY; VIRUS ANTIGEN; VIRUS NUCLEOPROTEIN; VIRUS VACCINE; DRUG CARRIER; INFLUENZA VACCINE; RECOMBINANT VACCINE;

2009 H1N1 INFLUENZA; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ANTIBODY RESPONSE; ANTIGEN EXPRESSION; ARTICLE; BLOOD LEVEL; CELLULAR IMMUNITY; CONTROLLED STUDY; CROSS REACTION; IMMUNE RESPONSE; IMMUNOGENICITY; INFECTION PREVENTION; INFLUENZA VIRUS A H5N1; LYMPHOCYTE ACTIVATION; LYMPHOCYTE FUNCTION; MACACA; MALE; MOLECULAR DYNAMICS; NONHUMAN; PROTEIN DETERMINATION; PROTEIN FUNCTION; VACCINATION; VACCINIA VIRUS; VACCINIA VIRUS ANKARA; VIRUS ISOLATION; VIRUS REPLICATION; VIRUS SHEDDING; ANIMAL; BLOOD; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; DISEASE MODEL; GENE VECTOR; GENETICS; HUMAN; IMMUNOLOGY; INFLUENZA A VIRUS (H1N1); INFLUENZA A VIRUS (H5N1); MACACA FASCICULARIS; ORTHOMYXOVIRIDAE INFECTIONS; PRIMATE DISEASES; PROCEDURES;

ANIMALS; ANTIBODIES, VIRAL; ANTIBODY-DEPENDENT CELL CYTOTOXICITY; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CROSS REACTIONS; DISEASE MODELS, ANIMAL; DRUG CARRIERS; GENETIC VECTORS; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HUMANS; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA A VIRUS, H5N1 SUBTYPE; INFLUENZA VACCINES; MACACA FASCICULARIS; MALE; ORTHOMYXOVIRIDAE INFECTIONS; PRIMATE DISEASES; VACCINATION; VACCINES, SYNTHETIC; VACCINIA VIRUS;

EID: 84908388845     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01219-14     Document Type: Article

References (50)

1. Ekiert DC, Bhabha G, Elsliger M-A, Friesen RHE, Jongeneelen M, Throsby M, Goudsmit J, Wilson IA. 2009. Antibody recognition of a highly conserved influenza virus epitope. Science 324:246-251. http://dx.doi.org/10.1126/science.1171491.
2. Ekiert DC, Friesen RHE, Bhabha G, Kwaks T, Jongeneelen M, Yu W, Ophorst C, Cox F, Korse HJWM, Brandenburg B, Vogels R, Brakenhoff JPJ, Kompier R, Koldijk MH, Cornelissen LAHM, Poon LLM, Peiris M, Koudstaal W, Wilson IA, Goudsmit J. 2011. A highly conserved neutralizing epitope on group 2 influenza A viruses. Science 333:843-850. http://dx.doi.org/10.1126/science.1204839.
3. Corti D, Voss J, Gamblin SJ, Codoni G, Macagno A, Jarrossay D, Vachieri SG, Pinna D, Minola A, Vanzetta F, Silacci C, Fernandez-Rodriguez BM, Agatic G, Bianchi S, Giacchetto-Sasselli I, Calder L, Sallusto F, Collins P, Haire LF, Temperton N, Langedijk JPM, Skehel JJ, Lanzavecchia A. 2011. A neutralizing antibody selected from plasma cells that binds to group 1 and group 2 influenza A hemagglutinins. Science 333:850-856. http://dx.doi.org/10.1126/science.1205669.
4. Corti D, Suguitan AL, Pinna D, Silacci C, Fernandez-Rodriguez BM, Vanzetta F, Santos C, Luke CJ, Torres-Velez FJ, Temperton NJ, Weiss RA, Sallusto F, Subbarao K, Lanzavecchia A. 2010. Heterosubtypic neutralizing antibodies are produced by individuals immunized with a seasonal influenza vaccine. J. Clin. Investig. 120:1663-1673. http://dx.doi.org/10.1172/JCI41902.
5. Li G-M, Chiu C, Wrammert J, McCausland M, Andrews SF, Zheng N-Y, Lee J-H, Huang M, Qu X, Edupuganti S, Mulligan M, Das SR, Yewdell JW, Mehta AK, Wilson PC, Ahmed R. 2012. Pandemic H1N1 influenza vaccine induces a recall response in humans that favors broadly cross-reactive memory B cells. Proc. Natl. Acad. Sci. U. S. A. 109:9047-9052. http://dx.doi.org/10.1073/pnas.1118979109.
6. Cohen J. 2009. Public health. A race against time to vaccinate against novel H1N1 virus. Science 325:1328-1329. http://dx.doi.org/10.1126/science.325_1328.
7. Osterholm MT, Kelley NS, Sommer A, Belongia EA. 2011. Efficacy and effectiveness of influenza vaccines: a systematic review and meta-analysis. LancetInfect. Dis. 12:36-44.http://dx.doi.org/10.1016/S1473-3099(11)70295-X.
8. Basha S, Hazenfeld S, Brady RC, Subbramanian RA. 2011. Comparison of antibody and T-cell responses elicited by licensed inactivated-and liveattenuated influenza vaccines against H3N2 hemagglutinin. Hum. Immunol. 72:463-469. http://dx.doi.org/10.1016/j.humimm.2011.03.001.
9. Subbramanian RA, Basha S, Shata MT, Brady RC, Bernstein DI. 2010. Pandemic and seasonal H1N1 influenza hemagglutinin-specific T cell responses elicited by seasonal influenza vaccination. Vaccine 28:8258-8267. http://dx.doi.org/10.1016/j.vaccine.2010.10.077.
10. Verheust C, Goossens M, Pauwels K, Breyer D. 2012. Biosafety aspects of modified vaccinia virus Ankara (MVA)-based vectors used for gene therapy or vaccination. Vaccine 30:2623-2632. http://dx.doi.org/10.1016/j.vaccine.2012.02.016.
11. Rimmelzwaan GF, Sutter G. 2009. Candidate influenza vaccines based on recombinant modified vaccinia virus Ankara. Expert Rev. Vaccines 8:447-454. http://dx.doi.org/10.1586/erv.09.4.
12. Volz A, Sutter G. 2013. Protective efficacy of modified vaccinia virus Ankara in preclinical studies. Vaccine 31:4235-4240. http://dx.doi.org/10.1016/j.vaccine.2013.03.016.
13. Berthoud TK, Hamill M, Lillie PJ, Hwenda L, Collins KA, Ewer KJ, Milicic A, Poyntz HC, Lambe T, Fletcher HA, Hill AV, Gilbert SC. 2011. Potent CD8+ T-cell immunogenicity in humans of a novel heterosubtypic influenza A vaccine, MVA-NP+M1. Clin. Infect. Dis. 52:1-7. http://dx.doi.org/10.1093/cid/ciq015.
14. Kreijtz JH, Suezer Y, van Amerongen G, de Mutsert G, Schnierle BS, Wood JM, Kuiken T, Fouchier RA, Lower J, Osterhaus AD, Sutter G, Rimmelzwaan GF. 2007. Recombinant modified vaccinia virus Ankarabased vaccine induces protective immunity in mice against infection with influenza virus H5N1. J. Infect. Dis. 195:1598-1606. http://dx.doi.org/10.1086/517614.
15. Lillie PJ, Berthoud TK, Powell TJ, Lambe T, Mullarkey C, Spencer AJ, Hamill M, Peng Y, Blais M-E, Duncan CJA, Sheehy SH, Havelock T, Faust SN, Williams RL, Gilbert A, Oxford J, Dong T, Hill AVS, Gilbert SC. 2012. Preliminary assessment of the efficacy of a T-cell-based influenza vaccine,MVA-NP+M1, in humans. Clin. Infect. Dis. 55:19-25. http://dx.doi.org/10.1093/cid/cis327.
16. Hessel A, Schwendinger M, Holzer GW, Orlinger KK, Coulibaly S, Savidis-Dacho H, Zips M-L, Crowe BA, Kreil TR, Ehrlich HJ, Barrett PN, Falkner FG. 2011. Vectors based on modified vaccinia Ankara expressing influenza H5N1 hemagglutinin induce substantial cross-clade protective immunity. PLoS One 6:e16247. http://dx.doi.org/10.1371/journal.pone.0016247.
17. Sutter G, Wyatt LS, Foley PL, Bennink JR, Moss B. 1994. A recombinant vector derived from the host range-restricted and highly attenuated MVA strain of vaccinia virus stimulates protective immunity in mice to influenza virus. Vaccine 12:1032-1040. http://dx.doi.org/10.1016/0264-410X(94)90341-7.
18. Breathnach CC, Clark HJ, Clark RC, Olsen CW, Townsend HGG, Lunn DP. 2006. Immunization with recombinant modified vaccinia Ankara (rMVA) constructs encoding the HA or NP gene protects ponies from equine influenza virus challenge. Vaccine 24:1180-1190. http://dx.doi.org/10.1016/j.vaccine.2005.08.091.
19. Bender BS, Rowe CA, Taylor SF, Wyatt LS, Moss B, Small PA. 1996. Oral immunization with a replication-deficient recombinant vaccinia virus protects mice against influenza. J. Virol. 70:6418-6424.
20. Kreijtz JH, Suezer Y, de Mutsert G, van den Brand JM, van Amerongen G, Schnierle BS, Kuiken T, Fouchier RA, Lower J, Osterhaus AD, Sutter G, Rimmelzwaan GF. 2009. Recombinant modified vaccinia virus Ankara expressing the hemagglutinin gene confers protection against homologous and heterologous H5N1 influenza virus infections in macaques. J. Infect. Dis. 199:405-413. http://dx.doi.org/10.1086/595984.
21. Lee LY, Ha Do LA, Simmons C, de Jong MD, Chau NV, Schumacher R, Peng YC, McMichael AJ, Farrar JJ, Smith GL, Townsend AR, Askonas BA, Rowland-Jones S, Dong T. 2008. Memory T cells established by seasonal human influenza A infection cross-react with avian influenza A (H5N1) in healthy individuals. J. Clin. Investig. 118:3478-3490. http://dx.doi.org/10.1172/JCI32460.
22. Brewoo JN, Powell TD, Jones JC, Gundlach NA, Young GR, Chu H, Das SC, Partidos CD, Stinchcomb DT, Osorio JE. 2013. Crossprotective immunity against multiple influenza virus subtypes by a novel modified vaccinia Ankara (MVA) vectored vaccine in mice. Vaccine 31: 1848-1855. http://dx.doi.org/10.1016/j.vaccine.2013.01.038.
23. National Research Council. 1996. Guide for the care and use of laboratory animals. National Academy Press, Washington, DC.
24. Weatherall D. 2006. The use of non-human primates in research: a working group report. Medical Research Council, London, United Kingdom.
25. Christman MC, Kedwaii A, Xu J, Donis RO, Lu G. 2011. Pandemic (H1N1) 2009 virus revisited: an evolutionary retrospective. Infect. Genet. Evol. 11:803-811. http://dx.doi.org/10.1016/j.meegid.2011.02.021.
26. Watanabe T, Imai M, Watanabe S, Shinya K, Hatta M, Li C, Neumann G, Ozawa M, Hanson A, Zhong G, Fukuyama S, Kawakami E, Simmons HA, Schenkman D, Brunner K, Capuano SV, Weinfurter JT, Kilander A, Dudman SG, Suresh M, Hungnes O, Friedrich TC, Kawaoka Y. 2012. Characterization in vitro and in vivo of pandemic (H1N1) 2009 influenza viruses isolated from patients. J. Virol. 86:9361-9368. http://dx.doi.org/10.1128/JVI.01214-12.
27. Rimmelzwaan GF, Kuiken T, van Amerongen G, Bestebroer TM, Fouchier RA, Osterhaus AD. 2001. Pathogenesis of influenza A (H5N1) virus infection in a primate model. J. Virol. 75:6687-6691. http://dx.doi.org/10.1128/JVI.75.14.6687-6691.2001.
28. Weinfurter JT, Brunner K, Capuano III, Li SVC, Broman KW, Kawaoka Y, Friedrich TC. 2011. Cross-reactive T cells are involved in rapid clearance of 2009 pandemic H1N1 influenza virus in nonhuman primates. PLoS Pathog. 7:e1002381. http://dx.doi.org/10.1371/journal.ppat.1002381.
29. Moncla LH, Ross TM, Dinis JM, Weinfurter JT, Mortimer TD, Schultz-Darken N, Brunner K, Capuano SV, Boettcher C, Post J, Johnson M, Bloom CE, Weiler AM, Friedrich TC. 2013. A novel nonhuman primate model for influenza transmission. PLoS One 8:e78750. http://dx.doi.org/10.1371/journal.pone.0078750.
30. Jegaskanda S, Weinfurter JT, Friedrich TC, Kent SJ. 2013. Antibodydependent cellular cytotoxicity (ADCC) is associated with control of pandemic H1N1 influenza virus infection of macaques. J. Virol. 87:5512-5522. http://dx.doi.org/10.1128/JVI.03030-12.
31. Pica N, Hai R, Krammer F, Wang TT, Maamary J, Eggink D, Tan GS, Krause JC, Moran T, Stein CR, Banach D, Wrammert J, Belshe RB, Garcia-Sastre A, Palese P. 2012. Hemagglutinin stalk antibodies elicited by the 2009 pandemic influenza virus as a mechanism for the extinction of seasonal H1N1 viruses. Proc. Natl. Acad. Sci. U. S. A. 109:2573-2578. http://dx.doi.org/10.1073/pnas.1200039109.
32. Rykkvin R, Kilander A, Dudman SG, Hungnes O. 2013. Within-patient emergence of the influenza A(H1N1)pdm09 HA1 222G variant and clear association with severe disease, Norway. Euro Surveill. 18:20369.
33. Uraki R, Kiso M, Shinya K, Goto H, Takano R, Iwatsuki-Horimoto K, Takahashi K, Daniels RS, Hungnes O, Watanabe T, Kawaoka Y. 2013. Virulence determinants of pandemic A(H1N1)2009 influenza virus in a mouse model. J. Virol. 87:2226-2233. http://dx.doi.org/10.1128/JVI.01565-12.
34. Kilander A, Rykkvin R, Dudman SG, Hungnes O. 2010. Observed association between the HA1 mutation D222G in the 2009 pandemic influenza A(H1N1) virus and severe clinical outcome, Norway 2009-2010. Euro Surveill. 15:19498.
35. Watanabe T, Shinya K, Watanabe S, Imai M, Hatta M, Li C, Wolter BF, Neumann G, Hanson A, Ozawa M, Yamada S, Imai H, Sakabe S, Takano R, Iwatsuki-Horimoto K, Kiso M, Ito M, Fukuyama S, Kawakami E, Gorai T, Simmons HA, Schenkman D, Brunner K, Capuano SV, Weinfurter JT, Nishio W, Maniwa Y, Igarashi T, Makino A, Travanty EA, Wang J, Kilander A, Dudman SG, Suresh M, Mason RJ, Hungnes O, Friedrich TC, Kawaoka Y. 2011. Avian-type receptorbinding ability can increase influenza virus pathogenicity in macaques. J. Virol. 85:13195-13203. http://dx.doi.org/10.1128/JVI.00859-11.
36. Hashimoto G, Wright PF, Karzon DT. 1983. Antibody-dependent cellmediated cytotoxicity against influenza virus-infected cells. J. Infect. Dis. 148:785-794. http://dx.doi.org/10.1093/infdis/148.5.785.
37. Sui J, Hwang WC, Perez S, Wei G, Aird D, Chen LM, Santelli E, Stec B, Cadwell G, Ali M, Wan H, Murakami A, Yammanuru A, Han T, Cox NJ, Bankston LA, Donis RO, Liddington RC, Marasco WA. 2009. Structural and functional bases for broad-spectrum neutralization of avian and human influenza A viruses. Nat. Struct. Mol. Biol. 16:265-273. http://dx.doi.org/10.1038/nsmb.1566.
38. Bai T, Zhou J, Shu Y. 2013. Serologic study for influenza A (H7N9) among high-risk groups in China. N. Engl. J. Med. 368:2339-2340. http://dx.doi.org/10.1056/NEJMc1305865.
39. Zhou J, Wang D, Gao R, Zhao B, Song J, Qi X, Zhang Y, Shi Y, Yang L, Zhu W, Bai T, Qin K, Lan Y, Zou S, Guo J, Dong J, Dong L, Zhang Y, Wei H, Li X, Lu J, Liu L, Zhao X, Li X, Huang W, Wen L, Bo H, Xin L, Chen Y, Xu C, Pei Y, Yang Y, Zhang X, Wang S, Feng Z, Han J, Yang W, Gao GF, Wu G, Li D, Wang Y, Shu Y. 2013. Biological features of novel avian influenza A (H7N9) virus. Nature 499:500-503. http://dx.doi.org/10.1038/nature12379.
40. Boni MF, Chau NVV, Dong N, Todd S, Nhat NTD, de Bruin E, van Beek J, Hien NT, Simmons CP, Farrar J, Koopmans M. 2013. Population-level antibody estimates to novel influenza A/H7N9. J. Infect. Dis. 208:554-558. http://dx.doi.org/10.1093/infdis/jit224.
41. Pica N, Palese P. 2013. Toward a universal influenza virus vaccine: prospects and challenges. Annu. Rev. Med. 64:189-202. http://dx.doi.org/10.1146/annurev-med-120611-145115.
42. Hessel A, Savidis-Dacho H, Coulibaly S, Portsmouth D, Kreil TR, Crowe BA, Schwendinger MG, Pilz A, Barrett PN, Falkner FG, Schäfer B. 2014. MVA vectors expressing conserved influenza proteins protect mice against lethal challenge with H5N1, H9N2 and H7N1 viruses. PLoS One 9:e88340. http://dx.doi.org/10.1371/journal.pone.0088340.
43. Amara RR, Villinger F, Staprans SI, Altman JD, Montefiori DC, Kozyr NL, Xu Y, Wyatt LS, Earl PL, Herndon JG, McClure HM, Moss B, Robinson HL. 2002. Different patterns of immune responses but similar control of a simian-human immunodeficiency virus 89.6P mucosal challenge by modified vaccinia virus Ankara(MVA)andDNA/MVAvaccines. J. Virol. 76:7625-7631. http://dx.doi.org/10.1128/JVI.76.15.7625-7631.2002.
44. Shiver JW, Fu TM, Chen L, Casimiro DR, Davies ME, Evans RK, Zhang ZQ, Simon AJ, Trigona WL, Dubey SA, Huang L, Harris VA, Long RS, Liang X, Handt L, Schleif WA, Zhu L, Freed DC, Persaud NV, Guan L, Punt KS, Tang A, Chen M, Wilson KA, Collins KB, Heidecker GJ, Fernandez VR, Perry HC, Joyce JG, Grimm KM, Cook JC, Keller PM, Kresock DS, Mach H, Troutman RD, Isopi LA, Williams DM, Xu Z, Bohannon KE, Volkin DB, Montefiori DC, Miura A, Krivulka GR, Lifton MA, Kuroda MJ, Schmitz JE, Letvin NL, Caulfield MJ, Bett AJ, Youil R, Kaslow DC, Emini EA. 2002. Replication-incompetent adenoviral vaccine vector elicits effective anti-immunodeficiency-virus immunity. Nature 415:331-335. http://dx.doi.org/10.1038/415331a.
45. Antrobus RD, Lillie PJ, Berthoud TK, Spencer AJ, McLaren JE, Ladell K, Lambe T, Milicic A, Price DA, Hill AVS, Gilbert SC. 2012. A T cell-inducing influenza vaccine for the elderly: safety and immunogenicity of MVA-NP+M1 in adults aged over 50 years. PLoS One 7:e48322. http://dx.doi.org/10.1371/journal.pone.0048322.
46. DiLillo DJ, Tan GS, Palese P, Ravetch JV. 2014. Broadly neutralizing hemagglutinin stalk-specific antibodies require FcγR interactions for protection against influenza virus in vivo. Nat. Med. 20:143-151. http://dx.doi.org/10.1038/nm.3443.
47. Nobusawa E, Aoyama T, Kato H, Suzuki Y, Tateno Y, Nakajima K. 1991. Comparison of complete amino acid sequences and receptor-binding properties among 13 serotypes of hemagglutinins of influenza A viruses. Virology 182:475-485. http://dx.doi.org/10.1016/0042-6822(91)90588-3.
48. Laddy DJ, Yan J, Khan AS, Andersen H, Cohn A, Greenhouse J, Lewis M, Manischewitz J, King LR, Golding H, Draghia-Akli R, Weiner DB. 2009. Electroporation of syntheticDNAantigens offers protection in nonhuman primates challenged with highly pathogenic avian influenza virus. J. Virol. 83:4624-4630. http://dx.doi.org/10.1128/JVI.02335-08.
49. Jegaskanda S, Amarasena TH, Laurie KL, Tan H-X, Butler J, Parsons MS, Alcantara S, Petravic J, Davenport MP, Hurt AC, Reading PC, Kent SJ. 2013. Standard trivalent influenza virus protein vaccination does not prime antibody-dependent cellular cytotoxicity in macaques. J. Virol. 87: 13706-13718. http://dx.doi.org/10.1128/JVI.01666-13.
50. Hovden AO, Cox RJ, Haaheim LR. 2005. Whole influenza virus vaccine is more immunogenic than split influenza virus vaccine and induces primarily an IgG2a response in BALB/c mice. Scand. J. Immunol. 62:36-44. http://dx.doi.org/10.1111/j.1365-3083.2005.01633.x.